Handbook of Paleoanthropology: Vol I:Principles, Methods and Approaches Vol II:Primate Evolution and Human Origins Vol III:Phylogeny of Hominids 9783642278006

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

Historical Overview of Paleoanthropological Research Winfried Henke* Institut f€ ur Anthropologie, Johannes Gutenberg-Universita¨t Mainz, Mainz, Germany

Abstract This chapter provides a comprehensive scientific historical overview of paleoanthropology as a multifaceted biological discipline. A brief summary of pre-Darwinian theories of evolution is followed by a historical report of the paradigmatic change wrought by Darwin’s perspective on life processes, from a teleological to a teleonomic view. Focusing on the fossil discoveries in Europe and later on in Asia and Africa, and on various methodological approaches, it becomes obvious that, as opposed to other biological disciplines, paleoanthropology remained until post-World War II first and foremost a narrative discipline, with widespread contemporary preconceptions (e.g., Eurocentrism, ethnocentrism) as well as erroneous conceptualizations (e.g., typological approach, orthogenism) that set it in many ways apart from the mainstream of biological thinking. Paleoanthropology is widely believed to have maintained this “iridescent image,” wrongly, as I will hopefully show. However, there remains skepticism that current theories of human origins are free of narrative components. Since Sherwood L. Washburn provided his innovative conceptual outline for physical anthropology, a theoretical and methodological change has arisen in the understanding of human evolution, focusing on evolutionary adaptations within the order Primates. The anthropological subdiscipline of paleoanthropology profited tremendously from this new approach – albeit with some delay, maybe caused by problems with the “Modern Synthesis” (e.g., the “single species hypothesis”). Intensified exploitation of old and new sites, the improvement of excavation techniques, and complex laboratory research on hominid fossils, on the one hand, and comparative research on living primates (e.g., taxonomy, biomechanics, behavioral psychology, ethology, molecular genetics, and genomics), on the other, constituted paleoanthropology as a highly innovative subdiscipline within the evolutionary sciences seeking to explain the processes of hominization, including our evolution, by concise hypothesis testing. A profound historiographical look back, as we move forward, seems helpful for different reasons: In this way, perhaps we will become more critical about the reliability and validity of our theoretical concepts, methodological approaches, and empirical basis. The history of paleoanthropology could thus help to increase the credibility of ideas about our evolutionary origins.

*Email: [email protected] Page 1 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

Introduction Historical Research: More than Looking into a Mirror! “Does disciplinary history matter?” This question was asked by Corbey and Roebroeks (2001a, p. 1) at the eponymous congress focusing on the history of paleoanthropology and archaeology. A negative answer assumes that studying the history of these scientific fields is an unsuitable job, at best a nice leisure time activity for retired colleagues. And since Landau (1991) implies in her book on Narratives of Human Evolution that modern paleoanthropologists are still only “storytellers,” a history of paleoanthropology faces a double-sided problem: We have to ask whether there is really any need for a dubious historical approach to a biological discipline that only alleges to be doing science. The allegation that paleoanthropology is not a serious and respectable field of research is unacceptable, as I hope that the broad spectrum of genuine research presented in the diverse contributions of this handbook of paleoanthropology is proof of this, although this anthropological subdiscipline may have its discreditable aspects (White 2000; Kalb 2001; Stoczkowski 2002; Henke 2010a, b; Reader 2011; more on this later). In addition, what should one say about the history of science in general? Is disciplinary history no more than a waste of time for practitioners, as well as historians of science? Experience shows that there is no uniform answer to this question. Willoughby (2005) mentions correctly that the historical sciences are different from the so-called hard sciences in which assumptions can be tested experimentally; but even biology is no physics. Popper described evolutionary biology as a “metaphysical research program” and “a possible framework for testable scientific hypotheses” as Tattersall (2002, p. 14) mentions in his sophisticated essay “The Monkey in the Mirror.” Though the distinction between the so-called hard and soft sciences has been made for a long time, and anthropology is positioned on the soft side, we have become increasingly aware from recent epigenetic findings (Jobling et al. 2004; Sassone-Corsi and Christen 2012) that the “white coat group” has similar epistemological problems (Oeser 2004). Obviously, scientists need support € from philosophers. In his essay Uber die Unvermeidlichkeit der Geisteswissenschaften, the German philosopher Odo Marquard (1987) emphasized the compensatory function of the cultural sciences and pleaded for the “Inkompetenzkompensationskompetenz” [I confess I like this term] of his discipline (Marquard 1974). It think it’s a gross error in European curricula of the biological sciences to have marginalized a propaedeuticum logicum as merely soft skills. Let’s come back to the historical sciences and their relevance for paleoanthropology. Willoughby (2005, p. 60) summarizes: “Rather than worrying about ‘physics envy’ (Gould 1981 (sic!), p. 113), some historical sciences are beginning to learn how to live within these restrictions.” And this seems to be right for the following reasons: If paleoanthropologists and historians of science can provide good suggestions for the improvement of the discipline, why should one give up studying the history of sciences or look on this discipline as an insignificant one? Goodrum (2009, p. 349) concludes in his valuable contribution to The History of Human Origins Research: “Historians, philosophers, and sociologists of science have a great deal to contribute to a better understanding of the development of palaeoanthropology as a science and to the impact it has had on modern culture and society.” Ernst Mayr (1904–2005) – an outstanding modern Darwinist – gave a reasonable, albeit not exhaustive, classification of the various relevant historical approaches: (1) elaborated lexicographic histories, (2) chronological histories, (3) biographical histories, (4) cultural and sociological histories, and (5) problematic histories (Mayr 1982). The essential point of all these is that the historicist approach may give rise to reflection, as Bowler (1976, 1988, 1996, 1997, 2001), Wolpoff Page 2 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

and Caspari (1997), Spencer (1997), Theunissen (2001), Stoczkowski (2002), Delisle (2007), Goodrum (2009, 2013), and Gundling (2005) emphasize. Although some may doubt whether the various approaches they suggest (heuristics, source criticism, interpretation, hermeneutics, and analytics) will improve paleoanthropology, Corbey and Roebroeks (2001a) emphasize the heuristic value of historical studies. Dennell sees two further lessons from science history: awareness of the dangers of fragmentation and complacency. He considers the lack of dialogue and understanding between the anthropological disciplines as a fatal risk and warns that “There is still excessive specialisation and insufficient dialogue across the disciplines, especially where the terminology and techniques are unfamiliar” (Dennell 2001, p. 66). Concerning the aspect of complacency, he explains that “It is always much easier to see the danger in retrospect, but perhaps one of the main lessons to absorb from the history of science is the danger of too many people becoming too comfortable for too long with an idea, just because so many agree with it, and have agreed with it so often in the past” (Dennell 2001, p. 66). Stoczkowski (2002, p. 197) insists that “we must not forget that the past, remote as it may be, acts on us with a force no less powerful than that of the present. [. . .] Acknowledging that historical processes can be slow and protracted, that timelags due to the force of inertia are omnipresent, that the ideas of yesterday and the day before weigh on those of the present, does in fact offer a few practical consequences, not only on the historian but also to any scientists who seek a better mastery of their conceptual tools.” And Goodrum (2009, p. 338) touches on another relevant aspect when expressing the hope that historiographical studies “can help bridge the gap that sometimes appears to exist between the history of natural sciences and the history of the human sciences.” I am convinced that a view across the fence between natural and cultural sciences is both necessary and long overdue (see Riedl 1985, 2003; Sarasin and Sommer 2010). The above severe arguments for the improvement of science by disciplinary history are valid for every field of study or “area of intellectual endeavour that holds a common set of concerns, theories, and procedures or techniques that are intended to address a closely connected web of problems” (Shipman and Storm 2002, p. 108). The Darwin anniversary in 2009, with innumerable interdisciplinary colloquia on evolutionary biology and a flood of “Darwinia,” demonstrated that there is an ongoing dialogue which longs for “a cross-fertilization of the various theoretical approaches” as “the crucial step towards a thorough understanding the evolutionary history of our science” (Destro-Bisol and Paine 2011; further Delisle 2007; Henke 2010a, b; Henke and Herrgen 2012; Begun 2013; Goodrum 2013). A major aspect of biological anthropology is that the present is inevitably rooted in the past. For this reason, Dennell (2001, p. 65) sees the study of human origins as “a search for windows that should give us access to the past through fossil specimens, stratigraphic and climatic changes, inferences from the world around us, and the like.” Paleoanthropologists and prehistorians and archaeologists seek windows to the past but use different sets of keys. A fatal danger is, however, that we may mistake a mirror for a window and simply extrapolate our own views and prejudices about the present onto the past. The important point here is, as L.P. Hartley put it: “the past is a foreign country, they do things differently there” (Foley 1987, p. 78). For this reason, Foley maintains that “The past cannot just be invented or imagined, nor reconstructed solely from observations of the way the world is at the present.” This brings both the task and the challenge of paleoanthropological research and other evolutionary sciences to the fore: We are creating essential models (Foley 1987; Henke and Rothe 1994; McHenry 1996; Delson et al. 2000; Stoczkowski 2002; Gutmann et al. 2010; Henke 2003a, b, 2004, 2005, 2007a, b, 2009, 2010a, b, c; Henke and Hardt 2011; Henke and Herrgen 2012). This kind of approach (Figs. 1 and 2) is by no means simply narrative; it is rather contextual hypothesis testing; and even if in some cases it Page 3 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

Fig. 1 Diagrammatic relationships between inductive and deductive scientific approaches (After Galley 1978, modified, see Henke and Rothe (1994))

involves scientific speculation, the accent is still on science (White 1988; Henke and Rothe 1994; Henke 2003a). Every scientist needs to arrive at innovative solutions within a channeled imagination. Tattersall (2002, p. 3) stresses in this context: “Indeed, there is no single scientific method. Scientific methods of course there are, in abundance; and methodologies lie at the heart of the immense variety of different things that scientists do [but] there is no particular method that will give you the key to all types of scientific inquiry.” The gift of Darwin’s theory is “that there was no blueprint to be followed, only unfoldings of opportunity,” as Howells (1993, p. 14) put it. If the magnificent panoply of life today is the outcome of a real historical-genetic process without a plan, how do we explain the patterns and processes? Darwin’s theory is uncontested as the center of the whole science of biology. In Darwin’s Dangerous Idea, Dennett (1995, blurb) compares the theory of evolution to a universal acid, an imaginary “liquid that is so corrosive that it will eat through anything!” and asks “Is nothing sacred?” Every traditional concept that tries to explain our existence has to compete with Darwin’s revolutionized worldview. As a consequence of Darwin’s theory of life, even human beings can no longer be explained in a teleological way, as expressed by Dobzhansky (1973, p. 125) in his famous dictum: “Nothing in biology makes sense except in the light of evolution”. Common sense mainly considers paleoanthropology as the study of human fossils and a descriptive and broadly narrative discipline that is dominated by poorly researched and media-

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

Fig. 2 An illustration of how skeletal and contextual data from the fossil records might be used to understand five broad overlapping categories of early hominins (After White 1988, redrawn)

friendly fossils and findings that cause changing views on the process of human evolution. Particularly, popular science media convey the impression that paleoanthropology is scarcely more than storytelling, labeling every human fossil as spectacular despite the fact that, when viewed soberly, most of the fossils and findings are just as expected. And empirical studies show that the public interest mostly fades very soon or bursts like a soap bubble. But is the history of paleoanthropology in fact something more than the demonstration of “a road full of errors, freak opinions and bizarre concepts finally discarded? (Corbey and Roebroeks 2001a, p. 1)” Or, as Stoczkowski (2002, p. 2) comments: “The problems of origins of humanity and culture, constantly pondered over millennia, provides a convenient opportunity for reconstructing a naive anthropology widely accepted in western culture. This may enable us to retrace the influence exerted by this shadowy knowledge on present day scholarly thought.” Given that we are in a dilemma of subjectobject identity, we should be conscious of the baggage we carry over from “various ‘social’ factors, such as fashionable theories, paradigms, ideologies and power relations within the scientific community” (Stroczkowski 2010, p. 1). Are most anthropologists even aware of these obstacles? Apparently not. Most paleoanthropologists are largely concerned with “pure facts.” Most anthropologists today agree that paleoanthropology is, like other categories of evolutionary biology, a serious subject involving hypothesis testing and scientific modeling (Wuketits 1978; Foley 1987; White 2000; Wood and Richmond 2000; Wood and Lonergan 2008; Cartmill and

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

Fig. 3 Pathways to the past; ways of investigating hominid evolution (After Foley 1987, modified)

Smith 2011; Begun 2013). They are aware that data ascertained from fossils do not speak for themselves and that for this reason the scientific approach involves the creation and testing of hypotheses and theories (Fig. 3). It is by doubting theoretical insights that we come to questioning; and by questioning, we may perceive the truth – or what we think to be the truth (Popper 1959a, b, 1968, 1983; Foley 1987; Mahner and Bunge 2000; Vollmer 2003; Oeser 2004). Stronger theories are those that are optimally corroborated; however, even well-tested general theories may conceivably be refuted (overview in Sarasin and Sommer 2010; Toepfer 2011; Wood 2011). Paleoanthropology is not, like physics, empirical science sensu stricto; but this does not mean at all that it is a narrative subject; storytelling is frowned upon in every science, and I agree with Kroeber (1953, p. 358) who stressed that “there exists basically only one kind of fundamental science. All genuine science aims at the comprehension of reality, and it uses both theory and evidence, in combination, to achieve this comprehension.” In history varying answers have been given to the question “What is the meaning of man?” However, in post-Darwinian times, there is no consensus on how we got here (overview in Eldredge and Tattersall 1982; Tattersall 1995, 1998, 2002; Corbey and Theunissen 1995; Antweiler 2009; Bohlken and Thies 2009; Bayertz 2012). Like all other anthropological scientists, paleoanthropologists are only able to establish a reductionistic view of our conditio humana (Henke and Herrgen 2012). Heberer (1968a) used the terms “Jetztbild” and “Jeweilsbild” (meaning status quo) to intimate the changeability of our knowledge and the fact that every paleoanthropological report will be out of date very soon after it is published (Hoßfeld 1997, 2005a, b; Schwartz and Tattersall 2002, 2003, 2005). In spite of the multiple schemes in hominin taxonomy and the irritating – not only for laymen and outsiders but for undergraduate students too – various interpretations of the hominid/hominin fossil record (see, e.g., Wood 2000; Wood and Lonergan 2010), there is no doubt that biologists are in principle on the right track when evaluating human fossil finds and reconstructing human origin in evolutionary terms (Tattersall 1998, 2002; Delson et al. 2000; Levinton 2001; Grupe and Peters 2003; Cartmill and Smith 2009; Begun 2013).

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

One word concerning alternative nonbiological explanations of human origin: It is wasting time to discuss pseudoscientific theories of intelligent design proponents at eye level; I am tempted to quote Berthold Brecht: “Wie kommt die Dummheit in die Intelligenz?.” Biologists have first and foremost to keep their own house clean; however, there is a great interest on the part of historians of science to decipher the reasons and the underlying social and political structures that have recently promoted the renaissance of creationism (Graf 2007, 2010; Graf and Soran 2010; Meyer (2006) for an excellent review and critics, see Neukamm 2009).

Darwin’s Perspective on Life Processes The paradigmatic change from a traditional static view to a dynamic evolutionary concept at the beginning of the second half of the last century resulted in the recognition that humans are an integrated part of a historical process. The so-called Darwinian Revolution, triggered by Darwin’s masterpiece from 1859, long remained in a state of confusion. As Bowler (1988) demonstrates in his historiography The Non-Darwinian Revolution, Darwin’s ideas were fundamentally misunderstood. In his judgment, the impact of evolutionism on late nineteenth-century thought has been greatly overestimated by historiographers (Hull 1973; Moore 1981; Desmond and Moore 1991; Engels 1995; Bowler 1996, 1997, 2001, 2009; Hemleben 1996; Ruse 2005; Goodrum 2004, 2009, 2013; Wuketits and Ayala 2005; Engels and Glick 2008). Traditionally, it has been assumed that the Darwinian Revolution in biology provided the impetus for a new evaluation of human origins, and Bowler claims that this assumption is valid up to a point. “Because of religious concerns, Darwin and his followers knew that they would have to explain how higher human faculties had emerged in the course of mankind’s evolution from the apes” (Bowler 1988, p. 141). The complex scientific answers within the frame of ever-increasing biological facts and the “disciplinary matrix” sensu Kuhn (Chamberlain and Hartwig 1999) essentially reflected our self-image and orientation. An argument often given for the scientific necessity of paleoanthropological research is that humans have to know where they come from to decide where to go; but “How [do] we know what we think we know?” to borrow a phrase from Tattersall’s (1995) eponymous book. Today’s paleoanthropology is a subdiscipline of evolutionary biology that aims to describe, analyze, and interpret the process of human evolution, mainly through a vast set of inductive approaches and deductive hypothesis testing (Foley 1987; Henke and Rothe 1994; Wolpoff 1999; Tattersall and Schwartz 2000; Begun 2013). If we want to know more about our origins, there are three basic approaches available to reconstruct our evolutionary history (Washburn 1953; Henke and Rothe 1994, 1999a; Cartmill and Smith 2009): • First, the primatological approach: One can study the closest living relatives to understand the evolutionary context. Such work includes field and laboratory research on behavior and cognition and comparative morphological, physiological, serological, cytogenetical, molecular biological, and genetic studies (e.g., Goodall 1986; Martin 1990; Jones et al. 1992; Tomasello and Call 1997; Tomasello 1999, 2008; de Waal 2000; Dunbar et al. 2010). • Second, the paleoanthropological or human paleontological and paleogenetic approach: One can reconstruct our evolutionary history from the recovery and analysis of any relevant fossil evidence, macro- and micromorphological, histological, and biophysical (e.g., isotopes), and by paleogenetic approaches: ancient mtDNA and genomicDNA (e.g., Aiello and Dean 1990; Herrmann 1986, 1994; Henke and Rothe 1994, 1999a, 2003; Henke 2005; 2010a; Hartwig 2002; Schwartz and Tattersall 2002, 2003, 2005; Hummel 2003; Jobling et al. 2004; Burger 2007; Wagner 2007). Page 7 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

• Third, the population genetic approach: One can study the phenetic and genetic intergroup and intragroup variation of recent human populations to provide clues about geographical samples and their evolutionary histories (e.g., Jones et al. 1992; Freeman and Herron 1998; Jobling et al. 2004; Crawford 2006). • Finally, there is additional information on prehistoric human activities, mind reading, and symbolism from cultural findings, i.e., the archaeological record, and behavioral fossils (e.g., Haidle 2006; Gamble 1999; Klein 2009; Dunbar et al. 2010; Haidle and Conard 2011; Pu˚tova´ and Soukup, in press). Current paleoanthropological research asks not only what our forerunners looked like and when, where, and how they evolved, but also specifically asks, for example, why humans evolved while other primate species died out (White 1988; Tattersall and Schwartz 2000). We have to reconstruct the ecological niches of fossil humans to define the determinants that caused adaptation in human evolution, a process sometimes defined as hominization, although some anthropologists argue that this term is misleading as it sounds teleological (Delisle 2001). Hence, when using this concept, we should be aware that it describes a teleonomic process sensu Pittendrigh (1958). In paleoanthropology – as in other life sciences with a chronological perspective – the experiment is in the historical process of nature itself. We have correspondingly to interpret this process within the general principles of evolutionary theory ex post-factum, and we have to take into account all the problems that arise from the epistemological difficulty known as subject-object identity (Riedl 1975; Mahner and Bunge 2000; Vogel 2000; Vollmer 2003).

Why a Scientific Historical Approach to Paleoanthropology? The present review of the historical development of paleoanthropology as a multifaceted biological subject is intended to focus on its cultural and social background and on its many problematic timespecific aspects. This historical point of view promises to clarify the following questions: • Which paradigmatic changes in evolutionary thinking have guided the field of paleoanthropological research? • Which cultural, social, and scientific factors have decelerated or accelerated the progress of paleoanthropology? • Which outstanding scientists, and which ideas, brought about the integration of biological, geological, and archaeological research? • What underlies the successive development, respectively, from Darwinism to neo-Darwinism and from the Synthetic Theory and “Modern Synthesis” to the System Theory of Evolution as the concept and strategy of paleoanthropological research? • What were country-specific impacts on the orientation of paleoanthropological research? • What influence of political ideologies and systems (e.g., radical authoritarian nationalism, communism, colonialism) can be noted on paleoanthropological thoughts and research? • How was paleoanthropological thought on sex-specific roles in human evolution influenced by the fact that this subdiscipline was for long male dominated? • What is the impact on current paleoanthropology and its image of innovative biological techniques in these multimedia times? • Is paleoanthropology a fossil- and/or media-driven science, triggered by the discovery of and publicity about exceptional hominin fossils? • If the accusation is correct that paleoanthropologists offer mainly shallow but media-friendly “findings” (White 2000) that contribute only very little to a proper understanding of the pattern Page 8 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

and process of human evolution (following Shakespeare: “Much Ado About Nothing”), how can historic studies on paleoanthropology contribute to new educational strategies to survive antievolutionary thinking?

Paradigmatic Change in the Nineteenth Century: Step by Step Darwin’s Forerunners, Especially in France and England The biblical view of the permanence of species expressed by Linnaeus’ sentence “Species tot sunt diversae, quot diversas formas ab initio creavit infinitum ens” was the underlying dogma of Genesis and the Judeo-Christian tradition. Although animal fossils had been described long before Darwin’s theory was published, they were interpreted as witnesses of “lost worlds” within cataclysm models, and not as evidence of a real historical-genetic process (for contemporary views, see, e.g., Paley 1860; Zo¨ckler 1860, 1876; for recent literature on pre-Darwinian thinking, see, e.g., Nebelsick 1985; Corbey and Theunissen 1995; Livingstone 2008; Bayertz 2012; Schwarz 2012; Ingensiep 2013). Georges Cuvier (1769–1832), the outstanding French comparative anatomist, did pioneering research on mammalian fossils and contributed to the self-consciously new science of geology. He began to understand that fossils truly represent remains of once-living organisms and argued for the reality of extinction caused by sudden physical events, so-called catastrophes. Cuvier first opened up the geohistorical perspective that is now appreciated as his most important legacy to science (Rudwick 1997). Besides this, he adamantly rejected “transformist” explanations. Although he was doubly on the wrong track, and his remark “l’homme fossile n’existe pas” slowed the development of thinking on human evolution, Rudwick’s interpretation of the primary texts demystified Cuvier, who was one of the first to professionally plan his research. His approach had an important influence on scientists of his time. One of the outstanding opponents of catastrophism was Sir Charles Lyell (1797–1875), British geologist and popularizer of uniformitarianism. He defended one of the most basic principles of modern geology, the belief that fundamentally the same geological processes that operated in the distant past also operate today. Principles of Geology, his specific work in the field of stratigraphy, was the most influential geological work of the middle of the nineteenth century and did much to put geology on a modern footing (Bynum 1984; Wilson 1998). In spite of much progress in natural scientific thinking, the early explanatory approaches of evolutionary theorists were not able to replace traditional views. All pre-Darwinian explanations of diversity and variability are regarded as just another story of natural history, because they failed to explain the driving force of evolution. This holds true for such outstanding naturalists of the eighteenth century as Georges-Louis Leclec, Comte de Buffon (1707–1788); Erasmus Darwin (1731–1802), grandfather of Charles R. Darwin; and William Paley (1743–1805), whose Natural Theology, or Evidences of the Existence and Attributes of the Deity Collected from the Appearances of Nature was a best seller of which the 20th edition was published in 1820. Paley tried to prove that the world has been created by a designer. Charles Darwin had studied Paley’s “long argumentations” carefully, as he noted in his Autobiography, before he wrote “I think” in his First Notebook on Transmutation of Species (1837) (for concise information on the dispute between theology and natural sciences during the last four centuries, see Schwarz 2012). The evolutionary theory of Jean Baptiste de Lamarck (1744–1829) proved to be a nonvalid explanation for transformation. However, Charles Darwin (1809–1882) looked upon this Page 9 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

retrospectively as an “eminent service of arousing attention to the probability of all changes in the organic, as well as in the inorganic world, being the result of law, and not of miraculous interposition” (Darwin 1861, preface). For a revised assessment of Lamarck’s merits, see Wuketits (2009a). Lamarck’s theory triggered Darwin’s evolutionary thinking on “transmutation” of species; Darwin himself regarded his Lamarckianistic pangenesis theory in retrospect as “stillbirth” (see Wuketits 2009b, p. 626). However, it was foremost Lyell’s Principles of Geology and Thomas Malthus’ essay on the Principle of Population (which stated that the population size is limited by the food resources available) that inspired Darwin to his multifaceted approach toward deciphering the biological principles of evolution. He defined the fundamentals and described evolution as a self-organizing process by a mutation-selection mechanism without the necessity of a creator or deus ex machina. The driving force of this event, natural selection (codiscovered by Alfred Russell Wallace, 1823–1913), is the central explanation of the evolutionary process (Glaubrecht 2008a, b). Darwin’s and Wallace’s legacy, the theory of natural selection, ultimately led to a paradigmatic change, a totally new view of the development of life systems including human origins. The vintage philosophical questions “Who are we?” “Where do we come from?” and “Where are we going?” were transferred from the metaphysical and the philosophical to a biological focus. They created new and important existential questions. Kuhn (1962) saw the truly revolutionary aspect of Darwin’s theory, not as lying in its evolutionism, but in its powerful rejection of the traditional, teleological view of nature. How explosive Darwin’s evolutionary theory was, and how conscious Darwin was of this, is reflected in the fact that he hesitated to deal with the questions of human evolution. The first edition of his classical opus On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life (Darwin 1859), provides proof of this feeling of insecurity. It then took him 12 years to publish his ideas in The Descent of Man and Selection in Relation to Sex (Darwin 1871). His innovative focus on human origins set the context for many of the themes of paleoanthropology during the following century. The anthropological challenge within the dynamic evolutionary concept was how to explain ourselves without compromising our posture. Altner (1981a, p. 3) verbalizes the existential problem as follows: “Der neuzeitliche Mensch ist aus allen ihn u€bergreifenden Sinnbez€ ugen herausgefallen und auf sich selbst und sein Werden zur€ uckgeworfen.” (For more recent literature on the impact of Darwinism to contemporary and current philosophical thoughts, see Becker et al. 2009; Bohlken and Thies 2009; Engels 2009.) Evolutionary thinking was widespread during the nineteenth century as various science historians have shown. Bowler (1988, p. 5) suggests in this context “that Darwin’s theory should be seen not as the central theme in the nineteenth-century evolutionism but as a catalyst that helped to bring about the transition to an evolutionary viewpoint within an essentially non-Darwinian conceptual framework.” Nowadays we know that most late nineteenth-century evolutionism was non-Darwinian as “it succeeded in preserving and modernizing the old teleological view of things”; however, it was a revolution “in the sense that it required the rejection of certain key aspects of creationism,” as Bowler (1988, p. 5) says (see also Moore 1981; Desmond and Moore 1991). The heart of Darwin’s materialism, the theory of natural selection, had little impact until the twentieth century. For this reason, the Darwinian Revolution did not take place in the second half of the nineteenth century and remained incomplete until the synthesis with genetics in the twenties and thirties of the last century. But even after this breakthrough, there was no straightforward scientific approach in paleoanthropology until anthropologists appreciated the essential corollary of Darwin’s theory, that we are only “another unique species” (Foley 1987). Page 10 of 84

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In retrospect it becomes obvious that the earliest “evidence” for human evolution was disregarded and misinterpreted. Fossils do not speak, but the dictum in paleontology is that they give silent witness. One can only get morphological, ecological, or taxonomical information within a concise methodological approach. Apparently easy paleoanthropological questions about the space and place of human origins do not necessarily have easy answers, so it requires rigorous efforts to establish a sophisticated research design and an adequate methodology to find solutions for the key questions given earlier (see section on “Why a Scientific Historical Approach to Paleoanthropology?”). As there was no evolutionary context at the time when William Buckland (1784–1856), professor at the University of Oxford, discovered the first human fossil, the “Red Lady of Paviland” at Goat’s Hole in South Wales in 1823, he totally misinterpreted this 26-ka-old find (Sommer 2004, 2006, 2007a). Buckland considered the find as of postdiluvian age and was unwilling to attribute any great antiquity to this Upper Paleolithic fossil skeleton. “For most of the nineteenth century, no one believed or anticipated discoveries that would demonstrate a history of humans and their ancestors stretching back over more than a few thousand years,” wrote Trinkaus and Shipman (1993, p. 9). Although savants struggled with evolutionary ideas for decades, the belief persisted that the human past differed from the present only in the “primitiveness” of the ancient peoples, not in their very essence and being. Starting in the twenties of the nineteenth century, there sprang up one local natural history society after another. The Red Lady inspired the hunt for human fossils and artifacts (Sommer 2004, 2006, 2007a; Delisle 2007). Kent’s Cavern in Torquay, Devon, today recognized as one of the most important archaeological sites in the British Isles, was excavated by John MacEnery and William Pengelly (1812–1894) (Sackett 2000). They discovered an Upper Paleolithic skeleton in association with flaked stone tools. John Lubbock (1834–1913), the foremost British archaeologist at that time, refused the report on “modern savages” written by Godwin-Austin and considered the findings as “improbable” (Trinkaus and Shipman 1993). Lubbock divided the Stone Age into two distinct periods, the Paleolithic and the Neolithic, based on the presence of crudely shipped flint tools versus more subtly made tools. Goodrum (2009, p. 341) mentions Lubbock’s Prehistoric Times (1865) and Daniel Wilson’s (1816–1892) work on Prehistoric Man (1865) as landmark in “the emergence of a new discipline, prehistoric archaeology, and the use of the term ‘prehistory’ in English” (overviews in Grayson 1983; Sackett 2000; Goodrum 2009, 2013a). Phillipe-Charles Schmerling (1791–1836), a Belgian physician and anatomist, unearthed an infant skull in 1829/1830 at Engis near Lie`ge, which was diagnosed later as a Neanderthal fossil. The Engis child was the first specimen of this kind to be discovered (Schmerling 1833). During the same period, Casimir Picard (1806–1841), a physician and avid archaeologist, was excavating prehistoric stone tools in France. His passion was in taking an experimental approach to archaeology, and he attempted to make and use stone artifacts like those that were being found in excavations. Due to inadequate chronology of the artifact-bearing horizons, he was not able to calibrate some of his stone tools as Neolithic. But his experiments led him to conclusions about how the tools were manufactured. Picard developed, for the first time, both systematic excavation techniques and a stratigraphic approach. While his innovative research was without wider impact on archaeological progress, he impressed his friend Boucher de Perthes (1788–1868). This influential aristocrat, who combined his romantic views on human origins with archaeological fieldwork, argued for the existence of Pleistocene – or, as he said, pre-Celtic-humans; but his findings were at first disregarded by the scientific community. When, in 1864, some of his findings were published in The Anthropological Review, the comment of the scientific board was downright British: “We abstain at the present from offering any comment on the above” (Trinkaus and Page 11 of 84

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Shipman 1993, p. 44). Although Boucher de Perthes could not avoid the image of flamboyant enthusiast and “madman,” there was finally a change in the assessment of the hand axes as genuine tools. The careful excavation of the gravel beds of the Somme at St Acheul by the French amateur naturalist Marcel-Je´roˆme Rigollot (1786–1854) impressed a group of outstanding British colleagues, among them Charles Lyell (Fritzsche 1997), and led to the acceptance of the claim that the hand axes were associated with extinct mammal bones – but where did this leave the human fossils? (See Klein and Edgar 2002; Goodrum 2009; Wuketits 2009a.)

Neanderthal Case: “Neanderthals Without Honor” The Neanderthal man from the Kleine Feldhofer Grotte in the Neander Valley near D€ usseldorf was found by limestone workers in 1856 and described by the local teacher Johann Carl Fuhlrott (1803–1877). The fossil was the first early human specimen to be recognized as such. The discoveries from Engis (found 1829) and Gibraltar (found before 1848) were made sooner, but their nature became evident much later. Fuhlrott’s merit was that he realized the significance of the fossils, which the limestone workers took for animal bones. Luckily, the owner of the excavation site saved them at the last moment (Schmitz and Thissen 2000). Fuhlrott fought, together with the anatomist Hermann Schaaffhausen (1816–1893) who taught at the University of Bonn, for their acceptance as ancient remains from the diluvial age. Both were convinced that the morphological structure of the bones indicated a high-diluvial age. Since the discovery of the fossil bones antedated the publication of Darwin’s Origin of Species, this specimen has often been termed as first proof for human evolution. A deeper analysis of the Fuhlrott/Schaaffhausen contribution demonstrates that both protagonists of paleoanthropological research in Germany were far from an evolutionary interpretation, although they looked upon their fossils as diluvial forerunner of recent Homo sapiens (Za¨ngl-Kumpf 1990). A contemporary of Fuhlrott and Schaaffhausen was Thomas Henry Huxley (1825–1895), the famous British zoologist often referred to as “Darwin’s Bulldog” (Desmond 1997). However, Huxley was no Darwinian. Historians know the difficulties of accurate definition, and Hull (1985, 1988) gets to the heart of this problem in suggesting “that Darwinians are simply those scientists who expressed loyalty to Darwin as the founder of evolutionism, whatever their beliefs about how evolution actually works” (Bowler 1988, p. 73). Although Huxley was highly committed by Darwin’s theory, it is well known that he had essential problems with the selection theory. Further, he was strongly tempted by non-Darwinian ideas, e.g., internal factors that would produce changes independent of the environment. Not being really interested in adaptation, Huxley speculated that evolution might sometimes work in a saltatory manner (Bowler 1988; Desmond 1997). His position was that the continuity between humans and other animals does not detract from the inherent specialness of humans. Similarly, other contemporary so-called proponents of Darwinism were not at all Darwinian evolutionists. In his famous papers on Evidences as to Man’s Place in Nature, Huxley (1863) gave morphological arguments for our relationship with recent primates and pointed to the scant fossil record known in his time. In spite of contrary statements by many historians, Huxley said virtually nothing about human origins, but concentrated exclusively on demonstrating the physical resemblances of humans and apes. Concerning the Neanderthal man from Germany, Huxley conducted a sophisticated comparison with anatomically modern skulls from Australian Aborigines and other aboriginal relicts, pioneering new ways of orienting and measuring skulls for easier comparison (Desmond 1997). His conclusion was that the Neanderthal skull emerged as an exaggerated modification of the lowest of the Australian skulls. Huxley stated that the brain of the Neanderthal man was of normal size for an ancient savage, and its stout limbs suggested to him a cold adaptation to glacial Europe. However, in no sense was this specimen Page 12 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

“intermediate between man and apes.” He viewed the Neanderthals as a very “primitive race” of humans, “the most pithecoid of human crania yet discovered” (Huxley 1863, p. 205). The Huxley biographer Desmond (1997) illustrates this by reference to Huxley’s diary entries: “Where, then must we look for primeval Man? Was the oldest Homo sapiens pliocene or miocene, or yet more ‘ancient’? How much further back must we go to find the ‘fossilized bones of an ape more anthropoid, or a man more pithekoid’ (sic!)?” Desmond concludes that Huxley was preparing the world for ancient semihumans. How misleading the effects of the concept of “semihumans” were becomes evident from the popular scientific literature and illustrations (see Corbey and Theunissen 1995; Kort and Hollein 2009, herein especially Jane Goodall’s article; Ingensiep 2013). The Irish zoologist William King (1809–1886) proposed in 1864 the name Homo neanderthalensis, although his arguments for a separate species in the genus Homo were inadequate, not to say absurd. Since then, opinion has fluctuated as to whether the fossils should be considered as a separate species, H. neanderthalensis or H. sapiens neanderthalensis (a subspecies of H. sapiens). The “fate of the Neanderthals” is the trickiest controversy in paleoanthropology (e.g., Henke and Rothe 1999b; Stringer and Gamble 1993; Tattersall 1999; Krings et al. 1997; Wolpoff 1999; Henke 2003a, b, 2005; Finlayson 2004; Green et al. 2008, Green et al. 2010a, b; Condemi and Weniger 2011; Stringer 2012). The question of whether some or all of these fossils deserve a place in our direct ancestry or whether they can be viewed as a single lineage leading to and culminating in the classic Neanderthals of the last Ice Age is the longest-running taxonomic problem in paleoanthropology (Schmitz 2006; Uelsberg and Lo¨tters 2006; Harvati and Harrison 2006; Cartmill and Smith 2009). What very soon became apparent with Huxley’s Evidences was the tremendous need for an extension of the fossil record and for an improved comparative methodology to analyze and interpret the fossils of recent primates. The starting signal for the search of the so-called missing link was given.

Theoretical and Methodological Progress in Paleoanthropology Since Darwin Till Mid-twentieth Century Successive Discovery of the Paleoanthropological Background In Darwin’s time, it was already evident that the scant evidence of hominin life in the past does not allow us to neglect any clues. We need all available sources to reconstruct our evolutionary history, and to do this we rely overwhelmingly on fossils. No wonder the mantra of paleoanthropologist’s of the first hour was “We Need More Fossils!” – and this call has never faded. However, there arose a paradox: the more fossils, the more complex the phylogenetic interpretations of the material became. Begun (2004) even wondered “Is Less More?” The answer must be an improvement of the epistemological and methodological bases of paleoanthropological inquiry, to ensure the trustworthiness of the investigation of fossils. These latter are obviously mute; and for this reason, one has to formulate hypotheses about the biological and phylogenetic roles of the extinct taxa. The only reliable approach to increasing our knowledge of the lost worlds is to compare them with recent sets of well-known phenomena (Foley 1987; Henke and Rothe 1994). This scientific process started very soon after the creative flash (fulguration sensu Popper) of the pre-Darwinian interpretation of fossil specimens as documents of species of former times and of their relevance to Darwin’s evolutionary theory. It was in this context that the systematic search for phylogenetic forerunners of recent taxa began. The most dramatic part of the Darwinian paradigm focused on the question of how humans evolved from archaic primates. What did the hypothetical species transitional between apes and man look like? When, where, and how did the “missing link” Page 13 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

live? (The origin of this term is contested. Some claim it was created in 1861 by Asa Gray (Shipman and Storm 2002), while other sources say it was coined by Lyell in 1837). Like the term “semihumans,” just mentioned, this concept caused a lot of misunderstandings (Goodall 2009; Ingensiep 2013), and for this reason it should be abandoned as inadequate for modern evolutionary thinking. However, John Reader’s (2011) Missing Links, an enthralling story of fossil hunting, stuffed with eccentrics and enthusiasts, and even some frauds in the search for humanity’s origins, demonstrates the hold this expression has had on the popular scientific media since Herbert Wendt’s (1953) best seller Ich suchte Adam. Fortunately, controversial book titles don’t implicitly match with a book’s contents; reader’s advanced and ambitious storytelling is as diverting as Wendt’s publication which first aroused my interest in the subject. Darwin’s evolutionary theory of natural selection did not automatically provide an answer to the question of human ancestors, and Darwin himself was cautious enough not to give a premature answer. But he had provided a new framework in which all these questions could be answered. While the public longed for strong proof of human evolution, Darwin gathered all available arguments for more than 10 years before finally publishing his brilliant anthropological volumes The Descent of Man and Selection in Relation to Sex (1871) and The Expression of Emotions in Animals and Man (1872). Both books deal with human evolution, and particularly with sexual selection, whose enormous evolutionary impact was first understood only around 100 years later, when the sociobiological paradigm emerged (Wilson 1975; Vogel 1982; Miller 1998; Voland and Grammer 2002; Voland 2000a; 2009). During the 1860s, Darwin’s ideas were widely popularized. However, there was still much scientific skepticism since the laws of heredity worked out by Gregor Mendel (1822–1884) in 1865 remained unknown until the twentieth century. Beside Darwin’s British supporters, especially Thomas H. Huxley and Charles Lyell, it was the German geologist and paleontologist Friedrich Rolle (1827–1887) and the zoologist Carl Vogt (1817–1895) who advocated Darwin’s theory (Rolle 1863; Vogt 1863; for more details, see Bowler 1988; Junker and Hoßfeld 2002; Hoßfeld 2005a, b; Rupke 2005; Ruse 2005). Even more committed and sarcastic than the “Affenvogt” was Ernst Haeckel (1834–1919), an outstanding German biologist who sagaciously fought against the “ape complex.” He is best known for his recapitulation law (ontogeny recapitulates phylogeny), a highly controversial assumption. After reading The Origin, he became a powerful and eloquent supporter of evolution. Although Haeckel admired Darwin’s theory, he remained an orthogradualist and a Lamarckian concerning the concept of the “survival of the fittest.” Haeckel was not really supportive of natural selection as the basic principle of evolution, and his interest in fossils and paleoanthropology was small. He was convinced that due to the intertwining of phylogeny and ontogeny, ontogenetic structures were sufficient evidence for evolution (Haeckel 1898, 1902, 1905, 1922; Heberer 1965b, 1968b, 1981; Hoßfeld and Breidbach 2005; Kleeberg see www; Preuß et al. 2006; Henke und Rothe 2006; Sarasin and Sommer 2010). Despite misunderstanding many of Darwin’s ideas, Haeckel inspired the public and colleagues with his enthusiasm for evolution and animated the debate. As he was highly motivated by his antiChristian attitude, his influence in science faded, especially after he had created his monistic theories and dabbled in esoteric fields (Hoßfeld 2005b; Kleeberg see www; Richards 2005). Still, he gave paleoanthropology an essential impulse by publishing the first phylogenetic tree (Fig. 4) that included humankind. Darwin’s comment on this was “Your boldness, however, sometimes make me tremble, but as Huxley remarked, some one must be bold enough to make the beginning in drawing up tables of descent” (German translation “Ihre K€ uhnheit la¨ßt mich jedoch zuweilen erbeben, aber, wie Huxley bemerkte, irgend jemand muß eben k€ uhn genug sein und einen Anfang Page 14 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

machen, indem er Stammba¨ume entwirft”) (Darwin’s letter to Haeckel, November 12, 1868) (Schmitz 1982). As the limited fossil record only allowed a very hypothetical pedigree, there was much courage needed indeed. Haeckel postulated a forerunner species Pithecanthropus alalus – a speechless ape-man – a missing link, which he believed lived during the Pliocene in Southeast Asia or Africa. Within an orthogenetic pedigree, he posited a primitive species – which he named Homo stupidus – between this “ape-man” and the recent H. sapiens. Around 30 years later, fossils were found in the postulated Asian region by the Dutch physician Eugene Dubois (1858–1940), which roughly fitted the expectation of a Pithecanthropus (Bergner 1965). Meanwhile a focus of research was the phenomenon of the Ice Ages and the discovery of Upper Paleolithic man and Ice Age cultures (Trinkaus and Shipman 1993; Sackett 2000). Although human fossils were rare at the time of Darwin’s revolutionary discovery, there was much evidence from animal bones, mollusks, sediments, and other materials to give insight into ancient populations. Further, there were ever-increasing indications of long-term fluctuations in the earth’s climate. Geologists, like Agassiz, Geike, and Lyell as well as Br€ uckner and Penck, established a Pleistocene framework of successive glaciations (Gra¨slund 1987), and archaeologists strove to establish the antiquity of human ancestry through the association of stone tools with extinct animals. The geological research resulted in the Alpine model, a chronological system of glaciations that gave a framework for the ongoing discovery of Neanderthal fossils. As biological, anthropological, paleontological, geological, and archaeological data came together within the framework of the evolutionary theory during the second half of the nineteenth century, many scientific societies were founded, which supported all kinds of scientific research. Rudolf L.C. Virchow (1821–1902), a famous German physician and anthropologist sensu lato, best known for his guiding research in cellular pathology and comparative pathology, was a universal scientist and liberal politician who founded the German Society of Anthropology, Ethnology, and Prehistory in 1869 (Degen 1968; Andree 1976; Schipperges 1994; Goschler 2002; Saherwala 2002; Tr€ umper 2004). He included humankind in the historicization of nature and came to the conclusion that H. sapiens was “post-history” (Goschler 2002, p. 322). For that reason, he was highly skeptical about the validity of Darwinian theory as regards our own species and doubted the phylogenetic classification of the species H. neanderthalensis, as the Irish zoologist William King had dubbed the skeleton from the Kleine Feldhofer Grotte (Stringer and Gamble 1993; Trinkaus and Shipman 1993; Schmitz and Thissen 2000). Due to his “pathologist view,” he interpreted the Neanderthals’ derived features, or apomorphies, as pathological features resulting from arthritis; further, from the erroneous information that the skeletal remains were associated with polished stone tools (an indicator for the Neolithic), he concluded that the Neanderthal specimen must have lived in recent times (Schott 1979). Thus, not all human fossils known at that time were accepted as convincing evidence of our ancestry, especially given their uncertain dating. Neither Virchow nor Haeckel pushed paleoanthropological research, the former from misinterpretation of the facts and skepticism on Darwin, the latter from his conviction that ontogenetic research delivers sufficient information to demonstrate phylogenetic evolution. Virchow’s interest was much more in prehistoric anthropology and ethnology, from the point of view of the decoupling of natural and cultural evolution. The retrograde view that the assumed “missing link” does not exist was admired by the Christian church, and when Pithecanthropus erectus, the so-called Java man, was described, he thought that the bones represented a giant gibbon. However, Haeckel’s interpretation was not in accordance with the results of the discoverer. Dubois was convinced “that his famous specimens from Trinil represented a true human ancestor, while other fossils from Sangiran and Zhoukoudian in China were too derived to have been ancestral to later Page 15 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

Fig. 4 Hand-drawn sketch of the family tree of primates by Ernst Haeckel; published in Herbert Wendt: Ich suchte Adam, 2nd ed. 1954 (Grote Verlag, Hamm). The artwork is part of the estate of Gerhard Heberer, and currently in the possession of Uwe Hoßfeld (Jena). Due to a detailed recherche by David Morrison (see Morrison et al. (2013), www), it was detected that contrary to earlier claims, this is not the first primate pedigree from Haeckel; there is evidence to suppose that the sketch was designed around 1895

humans. His theories, however, were widely misunderstood at the time” (Durband 2009, p. 10). As an excellent proof that in science history really matters, it can be noted that his “somewhat bizarre” reading of the evidence was roundly chastised by anatomists of the time (e.g., Le Gros Clark 1934; Weidenreich 1946) and generally dismissed by the scientific community as a whole. Only decades later, through the efforts of Theunissen (1989) and later Shipman (2001), were Dubois’ motives for this stance made clear (Durband 2009, p. 10; see too Theunissen 1989; and Shipman 2001). Virchow’s skeptical attitude concerning Pithecanthropus as well as his critical interpretation of the Neanderthal fossil as a pathological individual lessened the biological impact of a premature “paleoanthropology” in Germany during the second half of the nineteenth century (Tr€ umper 2004). This holds true for the English and French scientific scenes as well. Although the physician Paul

Page 16 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

Pierre Broca (1824–1880), the founder of the Socie´te´ d’Anthropologie de Paris in 1859, was a pioneer of comparative anatomy and anthropology, he never accepted the Neanderthals as fossil documents. His interest was in understanding patterns of variation in order to understand the significance of anatomical differences. For this reason, he became one of the first to use statistical concepts in establishing anthropology as a scientific discipline in contrast to medical science. In 1882, his French colleagues Quatrefages and Hamy published Crania ethnica, a monograph which exemplifies the huge interest in recent cranial variation that dominated the anthropological discipline. E´douard Lartet (1801–1871) was the first to describe the primate genera Dryopithecus and Pliopithecus, but much more important was his discovery of signs of prehistoric art made by early humans (Lartet and Christy 1865–1875). The fossil ivory carving of La Madeleine, found in 1864, was presented at the world exhibition in Paris 1867 and raised tremendous interest. In the following period, neither the discoveries of human fossils from La Naulette in Belgium nor those of Pontnewydd (Wales), Rievaulx (Southern France), Sˇipka, Mladecˇ (see Teschlerˇ zech Republic) were able to convince the European scientific commuNicola 2006), and Brno (C nity of great human antiquity. Even the analysis of the Spy fossils, which had been discovered in Belgium in 1886, did not slow the rejection of evolutionary ideas. Trinkaus and Shipman (1993, p. 132) summarized: “The man of the Neander Valley remained without honour, even in his own country.” In the motherlands of evolutionary thinking, France and England, Paleolithic archaeology dominated paleoanthropological discussion as it began taking shape as an organized scientific field of research in the 1860s. Sackett (2000, p. 38) put it this way: “discovering the Paleolithic became a matter of empirically demonstrating that human remains and artifacts could be found in association with the remains of extinct animals belonging to the deep time of earth history.” Progress was for the first time possible through the geological recognition of the Pleistocene epoch, making the interpretation of fossils possible within a solid geological background. Although Cuvier and Lyell had done indispensable scientific work in understanding the past, the first assumed that the changes came about by a series of revolutions, while the second, although he had major objections to Cuvier’s theory of catastrophism, was no evolutionist either. The challenging question for the evolutionists was how to provide empirical data on the existence of “diluvial” and “antediluvial” early human populations. As these workers had to rely on the research of the paleontologists and the archaeologists, paleoanthropological science was becoming multidisciplinary even at this early stage. The evidence from the Paleolithic record was mainly from data from stream gravel terraces, rock shelters, and bone caves. As Sackett (2000, p. 42) mentions, from the 1820s until 1859, there was a series of discoveries in France (especially in the Perigord), England (Paviland bone cave near Swansea, Wales; Kent’s Cavern, near Torquay, Devonshire), and Belgium (Engis near Lie`ge). The research resulted in the assignment of Pleistocene faunas to deep geological times, but it did not support evolutionary thinking due to the many alternative explanations available. The consequent question was whether actual human remains existed in association with Pleistocene animal fossils and undoubted artifacts. The immediate question of human antiquity came up with the discussion of the fossils from the Neanderthal in Germany and Darwin’s evolutionary theory. Most of the geologists and paleontologists remained skeptical; they saw no proof of a high antiquity of humankind from evidence from the bone caves or gravel terraces. One reason for their skepticism resulted from the archaeological work of Jacques Boucher de Perthes, director of customs at Abbeville, France, whose empirical evidence was much doubted. As consequence of his having “found much too much,” as Sackett (2000, p. 45) put it, the Bible continued to dominate everyday metaphor; and ironically enough, the successful Page 17 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

archaeological research in the Near East, Egypt, and Palestine solidified the traditional view that humankind was unique and doubtless recent. In spite of many convincing facts – as retrospectively gauged – from archaeology, the social establishment of the mid-nineteenth century maintained the older view. An opportunity for change came in 1858, when Brixham Cave near Torquay on the Devon Coast was discovered, and outstanding scientists like Hugh Falconer (1808–1865), Charles Lyell, Richard Owen (1804–1892) supervised excavations there. William Pengelly (1812–1894), a local schoolteacher and geologist, was able to gather, by a new method of layer-by-layer excavation, thousands of animal bones including those of hyena, cave bear, rhinoceros, and reindeer. The impact of these fossils on the question of human antiquity would have been zero if Pengelly had not found undeniable artifacts, which he described as “knives.” These chipped stones from Brixham Cave challenged the received opinion about human antiquity in 1859. While the belief in human antiquity of the excavator and some colleagues was confirmed by the association of fossil bones and the hand axes, others like Owen did not agree and thought that the animals had not become extinct until geologically modern times. New aspects came into the stagnating discussion when the implements of the Brixham Cave were compared to the finds at Abbeville and Amiens excavated by Boucher de Perthes. The ultimate convincing facts came when the English team, digging in the Somme terraces, was able to document a hand axe in place in a fossil-bearing stratum at St Acheul. This was the turning point as Pengelly, Prestwich, and Lyell were then able to convince the British establishment of the antiquity of humankind. The French scientific community, which had contradicted Boucher de Perthes’ interpretations for many years, now no longer rejected the idea of human antiquity. Some French scientists like the zoologist Isodore Geoffrey St Hilaire (1805–1861) and E´douard Lartet had been more or less convinced about human antiquity before, but the discovery of human teeth intermixed with fossils of cave bear and hyena in a cave near Massat in southern France brought about final acceptance. Lartet published the ultimate proof in 1860. He described cut marks on fossil bones that had been made by stone tools when the bones were still fresh. This was the essential evidence of contemporaneity of humans and extinct animals, and it signaled the start of intensified geological research. The glaciological research aimed at structuring the Pleistocene epoch that helped to put the human antiquity into a chronological frame; and the amalgamation of archaeological and geological facts brought up a new era that started with Lyell’s first edition of his famous Geological Evidences for the Antiquity of Man (Lyell 1863). The coming together of diverse aspects of the cultural and natural sciences ultimately yielded an innovative conception of man and his origin (Daniel 1959, 1975; Trinkaus and Shipman 1993; Sackett 2000; Murray 2001; Sommer 2004, 2007a; Delisle 2007).

Southeast Asia as Supposed Cradle of Humankind If paleoanthropologists had to answer the question of which fossils had the most exceptional influence on human evolutionary thinking, they would, of course, include the Homo erectus fossils from Java alongside those from the Neander Valley (Theunissen 1989; Durband 2009). The assessment is very easy to understand: first, there is a hero, a young, enthusiastic physician from the Netherlands, Euge`ne Dubois, who feels inspired by Darwin’s theory and Haeckel’s preliminary draft of a link between the lesser apes and earliest human populations; he joins the army as military surgeon and embarks for Indonesia. Besides his service in the army, he is looking for the so-called missing link, P. alalus, as Haeckel had dubbed the speechless and small-brained human species (Shipman 2001; Shipman and Storm 2002). Second, this paleontological amateur is successful in discovering a fossil human tooth and then a skullcap in the gravels of the Solo River. He proposes at Page 18 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

first the name Anthropopithecus and then changes it to Pithecanthropus, the name given by Haeckel. Finally, a stroke of good fortune leads to the discovery of a human femur, which seems to belong to the Pithecanthropus fossils, and causes the species to be named erectus. Third, Dubois, the man who found the posited “missing link,” gets into more and more trouble with his critics and, due to severe personal problems, the end of his career is tragic. Since Dubois was neither an accidental discoverer nor a paranoid eccentric person, as science historians and colleagues (v. Koenigswald 1971) have sometimes characterized him, the reinvestigation of his lifework yields a less discreditable view (Theunissen 1989; Shipman 2001; Shipman and Storm 2002; Durband 2009). If one takes all aspects of this story together, it shows the main characteristics of a myth. On the one hand, his unbelievable luck and, on the other hand, his unyielding, difficult character and his stubborn nature made Dubois an interesting public figure. While some historians like Erickson (1976) look upon Dubois as an unimportant figure in paleoanthropology, others like Haddon (1910), Theunissen (1989), and Shipman (2001) see him as one of the founding fathers of paleoanthropology (Shipman and Storm 2002). Did Dubois’ essential discovery coincide with a paradigm shift in paleoanthropology? While Howell (1996, p. 4) stated that the entire field of paleoanthropology is “close to a paradigm state without yet having achieved it,” Chamberlain and Hartwig (1999, p. 42) suggest “that the validity and promotion of knowledge claims in palaeoanthropology are explicitly Kuhnian and that future epistemological progress depends on acceptance of both Kuhnian and positivist approaches to knowledge-building.” In opposition to Chamberlain and Hartwig’s opinion, Cartmill (1999, p. 46) stated that “Whatever a paradigm is, normal science consists of attempts to ‘articulate’ a paradigm by answering questions, verifying predictions, and solving sticky problems in paradigmatic terms.” He continues: “Conceptual change in science is perpetually going on at all levels, and is not ordinarily concentrated in punctuational events that can be distinguished as ‘revolutions’.” Whatever position one adopts, there are obviously good reasons to regard Dubois as a founder of paleoanthropology. According to Shipman and Storm (2002, p. 109), founders must have special qualifications, e.g.: • • • •

A pivotal discovery of fossils or artifacts Development of an innovative technique for the description and analysis of discoveries A new framing of the problems or questions of the fledgling field A broad dissemination of information or debate about the subject, which serves to make it a matter of wide concern • The provocation of a general reaction or response from potential colleagues The last point fits with the Machiavellian fact that an invention needs the attention of the scientific community to become common currency. One may ask what would have happened to Dubois’ discovery in modern times. The rules of “The Economy of Attention,” formulated by Georg Franck (1998a, b), list the following stepwise pattern: “Attention by other people is the most irresistible of drugs. To receive it outshines receiving any other kind of income. This is why glory surpasses power and why wealth is overshadowed by prominence.” While Haeckel, Broca, and other scientists focused on the comparative anatomy and embryology as proof of human evolution, Dubois was the first who implemented a new strategy. Since he realized that human evolution is a chronological process, which must have happened in preferred localities with specific ecological niches, he set out for Southeast Asia, promised by Haeckel’s Page 19 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

fictional pedigrees as a possible “cradle of mankind” where the mysterious so-called missing link should have lived. Dubois was the first to write a detailed monograph on a hominin fossil, and he applied for the first time metrical and mathematical procedures for the calculation of brain volumes and stature heights to a human fossil. A critical evaluation of his work by Shipman (2001) shows that his scientific work was innovative and erudite, contrary to reports circulated by paleoanthropologists and science historians. The contemporary reviews of his 1895 monograph by, e.g., the German anatomist Wilhelm Krause and the multitalented scientist Rudolf Virchow were scathing, just as were those of British, French, and Swiss scientists. On the other hand, it was no surprise that Haeckel’s comment was positive. The skepticism of part of the scientific community incited him to tremendous activity, and there resulted a flow of papers on Pithecanthropus. It is thanks to Dubois that the focus on human fossils increased (Shipman and Storm 2002). The marketplace for human fossils and paleoanthropological discussions was open (Sander 1976). Among the scientific activities at the turn of the penultimate century of anthropological organizations in different European countries, e.g., the Gesellschaft f€ ur Anthropologie, Ethnologie und Urgeschichte in Berlin or the Socie´te´ d’Anthropologie de Paris as well as the Royal Anthropological Society of Great Britain, interest in the diversity of recent humankind was paramount. While many activities were concentrated on the typological classification of recent populations as well as prehistorical and archaeological research, paleoanthropological problems and fossils played only a minor role. Dennell (2001, p. 52) designates the period from ca. 1870 to 1930 as the “Age of Prejudice so far as European (and North American) perceptions of non-whites is concerned.” The dominating theme was the racial prejudice of fixity and inequality of races. While this attitude did not change when the first non-European fossil caught the interest of scientists and the public in general, it introduced a new aspect of human evolution: the confrontation of Eurocentric typological views with paleoanthropological facts (Hoßfeld 2005a, b, c; Henke 2010a, b; Henke and Hardt 2011; Henke and Herrgen 2012). In the light of the Pithecanthropus fossils, the Neanderthal problem reached a new dimension. Virchow’s diagnosis implied that the Neanderthal man was diseased with rickets as a child and arthritis as an adult. To many, this explanation of the special bony features of Neanderthals sounded farfetched (Trinkaus and Shipman 1993). There was a fundamental need for appropriate comparative biological research and a reasonable taxonomic approach. With the benefit of the hindsight, one can see that in those times there was no theoretical basis for paleoanthropological research, since the anatomists as well as the archaeologists were concentrating on case studies, while zoologists, like Haeckel (1866), were focusing on other topics than merely paleoanthropology. The end of the nineteenth and the beginning of twentieth century yielded exciting discoveries of human fossils (Table 1). The obvious lack of a sophisticated theoretical basis and elaborate methodological skills in paleoanthropological research gradually led to the development of a new field of evolutionary biology. The best basis for such a development existed in France, where Pierre Marcelin Boule (1861–1942), a qualified geologist, paleontologist, and archaeologist, unified all necessary attributes to establish a program for paleoanthropology. His classical description of the Neanderthal skeletons from La Chapelle-aux-Saints (Boule 1911–1913) was a landmark in the history of human paleontology (Heberer 1955a). Contemporaneously, the German anatomist Gustav Schwalbe (1844–1916) analyzed a skull fragment from Eguisheim as well as the famous Javanese Pithecanthropus erectus (Schwalbe 1906; Fischer 1917): research that is regarded as critical to the founding of paleoanthropology as a research field of its own. Heberer (1955b, p. 298) comments on this: “An die Stelle ungen€ ugend fundierten Theoretisierens tritt jetzt in der menschlichen Page 20 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

Table 1 Timetable of the unearthing and interpretation of human fossil remains and relevant breakpoints of paleoanthropological research before 1930 Year 1830

Place and site Engis, Belgium

1848

Forbes’ Quarry, Gibraltar Kleine Feldhofer Grotte (Neanderthal, Germany)

1856

Specimens, taxon, pathbreaking finding First Neanderthal fossil, Mousterian culture Neanderthal calvarium

Aspects and comments Described much later as such Described much later as such

Calotte and postcranial skeleton, no archaeological remains

First human fossil remains which have been attributed by Fuhlrott and Schaaffhausen in 1857 as diluvial remains, detailed description by Fuhlrott in 1859 1859 London (UK) Charles Darwin publishes his “Origin Darwin’s descent theory and his of Species by Means of Natural explanatory theory of selection Selection . . .” induced a paradigmatic change 1866 La Naulette (Belgium) Mandible, W€urm I Further indication for the existence of fossil man 1868 Cro-Magnon (France) Fossil remains of several individuals, The fossils have been described by best known as “Le Villard” Vacher de Lapouge as H. spelaeus but (Cro-Magnon 1), type specimen of are fully modern Upper Paleolithic a so-called Cro-Magnon race within humans. The association of the “Crocontemporary typological Magnon” type with an (evolved) classifications of those times Aurignacian and an extinct Pleistocene fauna was essential for the acceptance of a human antiquity ˇ 1880 Sipka (Czech Fragmentary mandible of a child, The Neanderthal mandible did not Republic) Mousterian, W€urm I/II convince the critics of the evolutionary theory 1886 Spy (near Namur, Two skulls and postcranial remains The morphology of the bones Belgium) disproved any doubt on the existence of Neanderthal man in Europe 1887–1892 Taubach (Germany) Isolated teeth, Mousterian culture “Pre”-Neanderthal remains 1891–1898 Trinil (Central Java, Calotte and complete femur, partial The discovery of the Trinil fossils by Indonesia) femur, teeth Euge`ne Dubois (Pithecanthropus erectus) was essential for the discussion of the “missing link” and displaced the focus on human origins from Europe to Asia The “H. primigenius” (later on 1899–1905 Krapina (Croatia) >670 cranial remains, Riss-W€urm Interglacial, cannibalism, burnt bones, H. neanderthalensis) was excellently described and analyzed by Mousterian culture Gorjanovic´-Kramberger (1906) 1907 Mauer (near Fossil mandible, dated to the middle Schoetensack (1908) described the Heidelberg, Germany) Pleistocene, between the Cromerian Mauer jaw as a new species, H. heidelbergensis. Some regard the and Holsteinian interglacials, fossil as H. erectus or classify the ca. 500 ka specimen as archaic H. sapiens 1908 La Chapelle-aux-Saints Well-preserved Neanderthal skeleton Boule’s description of the fossil (France) with a lot of pathologies, Charentian, (1911–1913) was a milestone of Mousterian, W€urm II research of the Neanderthals and “established” them as a separate (continued) Page 21 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

Historical Overview of Paleoanthropological Research, Table 1 (continued) Year

Place and site

1908

La Quina (France)

1908/1914

Le Moustier (France)

1908–1915 Piltdown (Sussex, England)

1908–1913 Weimar-Ehringsdorf and 1914/ (Germany) 1916/1925 1909–1912 La Ferrassie (France) 1920–1921

1918 f.

Zhoukoudian (near Beijing, China)

1921

Broken Hill (newly Kabwe; near Lusaka) Zambia (formerly Rhodesia)

1924

Taung (North West Province, South Africa)

1924–1926 Kiik-Koba (Crimea, Ukraine)

Specimens, taxon, pathbreaking finding

Remains of a total of 27 hominin individuals, highly fragmentary, including an infant skull (H 18); Quina variant of the Mousterian, traces of fire Adolescent and infantile skeleton, associated with Mousterian culture and overlying Chaˆtelperronian assemblage

From “Pleistocene gravels” “unearthed” specimen, a chimera of an intentionally manipulated mandible of a juvenile orangutan and portions of the skull of an anatomically modern man Calvaria, parietal, mandible, teeth, older than the classical Neanderthal man, Mousterian culture Fossil material of two adult and several highly incomplete and poorly preserved immature individuals, crouched burials Zdansky collected in the large karst cave human teeth and Bohlin started the excavation campaign 1928–1929 followed by further excavations

Aspects and comments species of their own; long time regarded as “archetype” of the classic Neanderthals of western Europe Louis Henry-Martin described the fossil material in 1908 and in the following years as classic W€urm Neanderthal remains Described by Klaatsch and Hauser (1910) as the type specimen of the species H. mousteriensis, although the Neanderthal affinity of the specimens has never been disputed The specimen was named Eoanthropus dawsoni and caused a lot of trouble in paleoanthropology as most of the leading British paleoanthropologists regarded the fossils authentic “Pre”-Neanderthal remains

Field descriptions by Capitan and Peyrony (1909, 1911–1912) and detailed analysis by Boule (1911–1913) The successful excavation of the site shifted the focus of paleoanthropological research and the origin of mankind entirely to Asia. Black’s description of Sinanthropus pekinensis established a species very similar to P. erectus Woodward (1921) classified the The well-preserved calvarium is associated with an African MSA, dated “Rhodesian Man” as a new species to 200–125 ka H. rhodesiensis and Pycraft (1928) opted for a new genus Cyphanthropus rhodesiensis, while Mourant (1928) saw Neanderthal affinities. Actually the specimen is mostly attributed to H. heidelbergensis The skull and hemiendocast of a child The characters in Dart’s A. africanus have been described by Raymond Dart were diametrically opposed to those expected; for this reason his (1925) in a Nature article as species classification was highly criticized by nova Australopithecus africanus Woodward and Keith, the contemporary leading British paleoanthropologists Hominid remains including an adult Extension of the distribution map of male and an infant (possible burials) Neanderthal sites to eastern Europe (continued)

Page 22 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

Historical Overview of Paleoanthropological Research, Table 1 (continued) Year

Place and site

1926

Ga´novce, Slovakia

1927

Mugharet el-Zuttiyeh, near Lake Galilee, Levante (today Israel) Saccopastore near Roma (Italy)

1929

Specimens, taxon, pathbreaking finding assigned to H. neanderthalensis, Mousterian occupation level, W€urm I Cranial and postcranial remains, RissW€ urm Interglacial, Mousterian culture Frontal skull fragment with an intermediate morphology, neither modern nor Neanderthal Clavarium (Saccopastore 1), skull fragments, upper jaw, Riss-W€urm Interglacial

Aspects and comments

“Pre-Neanderthal” remains First human fossil remain from the crossroads of the Middle East Corridor “Pre”-Neanderthal remains from stage 5e (130–120 ka)

Compiled from Henke and Rothe (1994, 1999a, references given there)

Fossilforschung die exakte Empirie.” Albeit this sounds somewhat effusive, the empirical approach to the morphological and metrical analysis of the fossils allowed an independent development separate from geology and archaeology. This view characterizes, on the one hand, the poor cooperation of paleoanthropology, as a biological field of research, with the geosciences as well as with archaeology/prehistory and, on the other hand, the overestimation of the scientific importance of quantifying morphological methods (Chaoui 2004; Hoßfeld 2005b). Both of these aspects hampered any essential progress in paleoanthropology for decades, the subject remaining mainly narrative and descriptive (see Hoßfeld 2005a, b; Henke 2006a, b, 2010a, b; Blanchard 2010).

Development of Principles and Methodical Skills in Paleoanthropology Neither Haeckel nor Virchow regarded paleoanthropology as a particularly important subject, and even anthropology itself was not a discipline of great significance in their times. The reason for the late establishment of anthropology as a separate biological discipline is, as Grimm (1961, p. 1) suggested, that “der Anthropologe viel weniger als der Zoologe oder der Pra¨historiker oder der Anatom in der Lage schien, die Grenzen seines Faches zu bestimmen.” In the first half of the twentieth century, paleoanthropology remained uncentered as physicians, anatomists, biologists, archaeologists, and ethnographers from different viewpoints and with different intentions and aims all practiced anthropology (Henke 2010a, b). This becomes especially obvious if one looks from the more zoological fields of research across to archaeology. The division of so-called explanatory natural sciences (erkla¨rende Naturwissenschaften) from the comprehending humanities (verstehende Geisteswissenschaften) sensu Dilthey 1883 (Groethuysen 1990) was completed at the beginning of the twentieth century, contingent on the obvious consciousness of superiority of natural sciences (Fig. 5). The rediscovery of Gregor Mendel’s laws in 1900 by Carl Correns, Erich von TschermakSeysenegg, and Hugo de Vries gave a push to evolutionary thinking. Around 1930, protagonists of neo-Darwinism like Ronald A. Fisher, John B. S. Haldane, and Sewall Wright developed the basic principles of population genetics and induced a fruitful diversification of natural sciences. In the following period, the Russian-American geneticist and evolutionary biologist Theodosius Dobzhansky (1900–1975), the American paleontologist George Gaylord Simpson (1902–1984), the German evolutionary taxonomist Ernst Mayr (1904–2005), and finally the British biologist Julian Huxley (1887–1975) founded the Synthetic Theory of Evolution, integrating additionally quite a number of neighboring disciplines to reconstruct the phylogenetic process of our own origin Page 23 of 84

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Fig. 5 Paleoanthropology versus archaeology – identical aims but different approaches (Henke and Rothe 2006)

(Jahn et al. 1982; Jahn 2000; Junker 2004; Wuketits and Ayala 2005; Hoßfeld 2005a, b). The major principles of the “Synthesis” itself were subsequently enunciated between 1937 and 1944 in three seminal books. While Dobzhansky (1937) focused on the gene, Mayr’s (1942) vantage point was the species and Simpson’s (1944) perspective was on the higher taxa. Tattersall’s (2000a, p. 2) assertion that “the Synthesis was doomed to harden, much like a religion,” is controversial (see, e.g., Foley 2001). However, before we discuss the consequences of the “Synthesis” (for alternative terms, see Junker 2004), we shall have a closer look at paleoanthropology.

Fossils: Hypotheses, Controversies, and Approaches In the early days of paleoanthropology, the main question was quite simple: Is there a fossil record that proves the existence of our ancestors from ancient times? The protagonists of paleoanthropology soon recognized the need for a more sophisticated empirical approach. The best basis for such a development existed in France, where Pierre Marcelin Boule, just mentioned, unified in persona all necessary attributes to establish a qualified paleoanthropology. His classic study of the Neanderthal skeleton from La Chapelle-aux-Saints (Boule 1911–1913) became a landmark in the history of human paleontology (Heberer 1955a). He aimed to understand the patterns of variation and the significance of anatomical differences. For this reason, Boule invented special instruments for quantification and simple statistical concepts to analyze the variation in human skeletons (Boule 1921, 1923; Boule and Vallois 1946, 1952). Boule established a paleontology of humans, later on called paleoanthropology, as a scientific discipline; but as evolution itself was still regarded as a widely speculative myth, the debate on human evolution “rose and fell like a tide in France, Germany, England, and the United States,” as Trinkaus and Shipman (1993, p. 154) described the situation. During the late nineteenth and the early twentieth centuries, an overemphasis quantifying procedures strongly affected the anthropological research, starting with the first occupants of anthropological chairs, Jean Louis Armand de Quatrefages de Breau (1855, Paris) and Marcelin Boule (1867, Paris), as well as Johannes Ranke (1886, Munich) and Felix v. Luschan (1900, Berlin). While Ranke was deeply opposed to the idea of human evolution, with Otto Schwalbe, just Page 24 of 84

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mentioned, Theodor Mollison (M€ unchen), Felix v. Luschan (Berlin), Rudolf Martin (M€ unchen), and Otto Schlaginhaufen (Z€ urich) successively advocated measuring techniques of every conceivable kind (Keller 1995; Chaoui 2004; Junker 2004; Hoßfeld 2005b). While Schwalbe was convinced that information on evolutionary history could only be gained from neo- and paleozoology, others focused predominantly on typological classification of prehistorical populations and neglected broader paleoanthropological questions. This can only be understood by the fact that the conventional wisdom of that time was that modern “races” arose from types that were already separate in the early Pleistocene. For this reason, there was a big problem when Gorjanovic´Kramberger (1906) described the fossils from Krapina, excavated in 1899–1905, in a voluminous monograph as belonging to a “man-eating” population (Radovcˇic´ et al. 1988). As this thesis was accepted by one of the most outstanding anthropologists of the time, Alecˇ Hrˇdlicka (Prague, later on Washington), who pushed paleoanthropological research using his influential position at the Smithsonian Institution, Krapina became a big challenge to the scientific community (Henke 2006a). Notwithstanding the problem that the assumed anthropophagy/cannibalism of the Neanderthals remained controversial (see, e.g., Ullrich 1978, 1995, 2005a; Orschiedt 2008), it must be emphasized that Gorjanovic´-Kramberger (1856–1936) did excellent geological, paleontological, paleoanthropological, and archaeological research far ahead of the standards of his time (Frayer 2006; Henke 2006a). Tim White (2006, preface) lauded him in the centennial bibliography, edited by Frayer, thus: “His osteological and archaeological skills brought the valuable Krapina remains and their contexts to light. His paleoanthropological insights are embedded in a body of scholarly writings (1899–1929) foundational to modern paleoanthropology.” And Frayer (2006, p. 3) refers to the publications of Jakov Radovcˇic´ (1988) and Radovcˇic´ et al. (1988): “Gorjanovic´-Kramberger was first 1. to preserve and map a detailed stratigraphic profile of a Neandertal site, 2. to save virtually every Neandertal fossil he encountered from the four tooth germs to the 16, mostly complete patellas, 3. to number the fossils and record the levels from where they derived, 4. to save most of the faunal remains and all the stone tools, 5. to use the emerging field of radiology for documenting Neandertal morphology, 6. to conduct trace element analysis as a relative dating technique for confirming the contemporaneity of fossil mammals and humans, 7. to publish multiple, quality photographs of the hominin fossils and 8. to propose and document cannibalism in the fossil record based on burned specimens, cut marks and other bone damage.” What might he have done further? I confess that Gorjanovic´-Kramberger is my favorite as most innovative paleoanthropologist of his time (see Henke 2006a), followed by Gustav Schwalbe, anatomist at the University of Strasbourg, whose comparative morphologic research on fossils (e.g., Pithecanthropus from Java, Neanderthal calotte, Eguisheim, Br€ ux, Oreopithecus) was setting standards. Compared to the two protagonists just mentioned above, the image of Hermann Klaatsch (1863–1916; Breslau) is colorful and iridescent; his research output varies from highly elaborated to suspect. The excavator (together with Otto Hauser [see, e.g., Dro¨ßler 1988; Dro¨ßler et al. 2006]) and researcher of the fossils from Le Moustier and Combe-Capelle was, e.g., wrong about the “sleeping position” of Le Moustier 1 (see Ullrich 2005a, b; Hoffmann 2003a, b), and his papers on Combe-Capelle are – to say the least – under suspicion, since it became known by the radiocarbon Page 25 of 84

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calibration of the newly recovered skull that the icon of the Aurignacian, the earliest period of the Upper Paleolithic, is not older than late Mesolithic (Hoffmann et al. 2011; Henke 2011). These results are both irritating and suspicious, as Klaatsch “used the fossil record to support his polygenist view, and one way he could do so was to show that the Neandertals and Aurignacians (races he believed had separate origins) coexisted” (Wolpoff and Caspari 1997, p. 127; for more details, see Henke 2011). Further controversies were born when descriptions of the Upper Paleolithic skeletons from, e.g., Chancelade, Grimaldi, Combe-Capelle, and Oberkassel, and also Neanderthals such as Le Moustier, La Chapelle-aux-Saints, La Ferrassie, and La Quina were excavated and published (Henke et al. 2006). There was special interest in the mandible from Mauer that was described in 1908 by Otto Schoettensack (1850–1912) as Homo heidelbergensis (Adam 1997; Wagner and Beinhauer 1997; Hardt and Henke 2007; Wagner et al. 2007; Henke and Hardt 2011). In England, the motherland of Darwinism, there was for a long time little progress in paleoanthropology since the alleged Darwinists were obviously “no Darwinians in the modern sense” (Bowler 2001, p. 14). During the period from 1860 to 1940, a Darwinian style of explanation began to replace non-Darwinian developmental models stepwise, but a real breakthrough or turnover did not occur before World War II, largely due to the overwhelming influence of the paleontologist and geologist Arthur Smith Woodward (1864–1944) and the zoologist Sir Arthur Keith (1866–1955) as the leading authorities on human remains. Keith published An Introduction to the Study of Anthropoid Apes in 1896 (see also Keith 1911), followed by a monograph, The Antiquity of Man, which appeared in 1915. This publication on all-important fossil human remains founded his worldwide reputation and appeared in an enlarged edition in 1925. As can be seen from his textbook Concerning Man’s Origin (Keith 1927), he was at that time less convinced than he had been 10 years before that modern humans and extinct “primitive” types had lived contemporaneously. In his volume New Discoveries, Keith (1931) rejected this interpretation given the strength of the arguments for an evolutionary branching of hominins. From the viewpoint of history of science, we have to ask why the leading “anthropologist” as well as his compatriot Sir Grafton Elliot-Smith (1871–1937) retained this view for so long in the face of compelling contrary arguments from paleoanthropological discoveries in Europe, Asia, and after 1925 in South Africa too. One plausible explanation is that theories are the filters through which facts are interpreted as Popper (1959b) said. The reason why the English authorities adhered to wrong models combines the fatal misinterpretation of the Piltdown hoax with wishful thinking and cultural bias (Spencer 1990a). The background of the Piltdown forgery has been analyzed and described many times (Spencer 1990a, b). The most plausible explanation why the Eoanthropus dawsoni hoax was so successful is that it seemed to provide proof for a missing link between apes and humans, using a mix of plesioand apomorphic characters. Especially, the primitive jaw and dentition made Eoanthropus a more suitable intermediate candidate than Pithecanthropus. Even after the discovery of Australopithecus at Taung in 1924, and the excavation of the first Sinanthropus skull from Zhoukoudian (Chou-koutien) shortly thereafter, Keith (1931) hypothesized that the Piltdown type arose from the main ancestral stem of modern humanity. At that time, prominent British anthropologists such as Smith Woodward, Keith, and Elliot Smith were fixed on a European origin of humankind and absolutely in opposition to models of Asian and African origin. The expected phylogenetic sequence was that the cerebralization antedated the changes of the viscerocranium. As the plesiomorphic jaw and the apomorph brain of Eoanthropus complied with this expectation, it fitted perfectly into a scheme that was in fact Page 26 of 84

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wrong. One could comment on this “credibility of the plausible” in Plato’s (The Republic, 382d) word: “And also in the fables of which we were just now speaking, owing to our ignorance of the truth about antiquity, we liken the false to the true as far as we may” (see Stoczkowski 2002, p. 168). It took more than 40 years before Joseph S. Weiner (1915–1982), Sir Kenneth P. Oakley (1911–1985), and Sir Wilfrid Le Gros Clark (1895–1971) jointly exposed the hoax, although there was much skepticism and rumor earlier. Whoever the players were in this black mark in science, they were aware of the attractiveness and fascination of fossils, the rare resources that help to decipher our place in nature, and they obviously knew about the public appeal (Stringer and Gamble 1993; Walsh 1996; Weiner and Stringer 2003; overview in Harter (1996–1997) www; Turritin (1996–1997) www). The interpretation of the Piltdown fossil as a human precursor was partially responsible for the vehement dismissal of the first Australopithecus from South Africa. Dart’s interpretation of the Taung child as missing link between ape and man yielded a storm of controversy (Tobias 1984). As Trinkaus and Shipman (1993, p. 206) put it: “The entire scientific coterie of Britain believed in the fossils without hesitation.” This is remarkable insofar as Dart’s discovery matched the prophecy of Darwin (1871, p. 202): “It is, therefore, probable that Africa was formerly inhabited by extinct apes closely allied to the gorilla and chimpanzee: and, as these two species are now man’s nearest allies, it is somewhat more probable that our progenitors lived on the African continent than elsewhere.” To the extent that these and other indications for an extra-European “cradle of humankind” were deliberately ignored, the Piltdown case is a telling example of cut and dried opinions. Are there more self-fulfilling prophecies? It may be that Klaatsch’s “contradictions and fanciful reconstructions” (see Za¨ngl-Kumpf 1997, p. 575), and especially his polygenist view, influenced his interpretation of the Le Moustier and Combe-Capelle fossils (Henke 2011). If paleoanthropologists see what they please, small wonder that the scientific output of paleoanthropology during the first decades of the last century was very heterogeneous and confusing and more redolent of stagnation than progress. The evolutionary biology at those times was characterized by Mayr as “chaotic” (Tattersall 2000a, p. 2). But why? First, even at the beginning of the twentieth century, Darwin’s principles were widely misunderstood by anthropologists, who persisted in orthogenetic biological thinking or insisted on the theoretical split between natural sciences and humanities. Paleoanthropological theory and methodology were still in statu nascendi, judging from the literature of the time (Klaatsch 1899; Hrdlicˇka 1914; Werth 1921; Weinert 1928; Wiegers 1928; Abel 1931; Hooton 1931; Keith 1931; Le Gros Clark 1934). Second, the rediscovery of Mendel’s work in 1900 demonstrated that new hereditary variation, i.e., mutation, occurs in every generation and every trait of an organism. The founding of genetics at the beginning of the twentieth century gave tremendous support to Darwin’s theory and removed the objections to his postulates. However, the effects of genetics and population genetics were felt less in paleoanthropology than in the biology of recent populations and especially in aberrations like typological social biology, ethnogeny, and race typology. In Germany, social Darwinism and fatal concepts of hereditary and race dominated biological and medical research on living people. Paleoanthropology was of only minor interest, while the aim of anthropology was defined in the national socialist area or “the Third Reich,” “. . . der deutschen Volksgemeinschaft zu dienen” (Reche 1937; see further Zmarzlik 1969; Gould 1983; M€ uller-Hill 1988; Seidler and Rett 1988; Weingart et al. 1988; Za¨ngl-Kumpf 1992; Hoßfeld and Junker 2003; Junker 2004; Hoßfeld 2005a, b; Preuß 2009).

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Third, various approaches to explain the process of hominization later on turned out to be politically highly incorrect: e.g., Kollmann created in 1885 the term “neoteny” suggesting that humans evolved from pygmies who had simply retained juvenile features during size increase (Kollmann 1902). The basic idea was that pygmy progenitors probably arose from juvenile apes that had lost the ancestral tendency to regress. Bolk (1926) argued in a long series of papers that man evolved by retaining the juvenile features of his ancestors. His “fetalization hypothesis” influenced evolutionary thinking on human origins and formed expectations of the appearance of transitional species. Bolk’s theory was highly criticized and later on rejected by Starck (1962) because it was built on flawed arguments and a misinterpretation of Darwin’s principles. Similar questions still resound in the current so-called evo-devo discussion, e.g., the evidence overwhelmingly suggests that neoteny, the retention of juvenile characteristics, was one of the most important processes involved in the origin of H. sapiens (Minugh-Purvis and McNamara 2002). Fourth, the discovery of numerous Neanderthal skeletons (Table 1) caused new arguments in the discussion of gradualism versus continuity. Boule’s monograph evicted the Neanderthals from our family tree, although some outstanding early twentieth-century paleoanthropologists like Alecˇ Hrdlicˇka argued for gradualism, a controversy that continues to this day (overview in Wood and Lonergan 2008; Cartmill and Smith 2009; Henke and Hardt 2011; see also below). Finally, the non-European fossils from, e.g., Java, China, and South Africa, could have been a strong stimulus for a wider view of human origins (for details on the history of contemporary excavations, see, e.g., fossil catalogues by Schwartz and Tattersall 2002, 2003, 2005; encyclopedia by Delson et al. 2000; and textbooks by Cartmill and Smith 2008). However, the prejudice of the leading British scientists crushed innovative hypotheses, and the critical skepticism on non-European roots of humankind due to Eurocentric perspectives and the fatal misinterpretation of the Piltdown man resulted in a stagnation of paleoanthropological theories. Dennell (2001, p. 51) puts it this way: “. . . it is depressing to realize how much of what was written on human origins before WWII was little more than prejudice masquerading as science, it is impossible to understand the study of human origins without reference to these prejudices” (see also Stoczkowski 2002; Hoßfeld 2005b; Junker 2004; Delisle 2007; Henke 2010a, 2011).

Paleoanthropology, Ideology, and Politics: Symptomatic Events The misapplication of the Darwinian biological theory known as social Darwinism has been intensively discussed in another context (M€ uhlmann 1968; Zmarzlik 1969; Altner 1981a, b; M€ uller-Hill 1988; Weingart 1988; Hofstadter 1995; Hawkins 1997; Dickens 2000; Junker 2004; Hoßfeld 2005b). It is well known that this biological ideology was the “Janus head” of scientific Darwinism (Altner 1981b) from the beginning; however, it became highly influential and threatening after World War I, especially during the period of National Socialism in Germany. That paleoanthropology was no free zone of research stems from different reasons: first, because paleoanthropology was a subdiscipline of the highly politically involved physical anthropology (Weingart et al. 1988; Hoßfeld 2005a, b) and second, because racial thinking and racist theory were interwoven with all aspects of daily life (Bowler 1976; Stepan 1982; Bowler 1986, 1988, 1996, 1997, 2001; Proctor 1988; Weingart et al. 1988; Vogel 1983, 2000; Hoßfeld 2005a; Preuß 2009; Henke 2010b; 2011) – long before the fascistic “Third Reich” in Germany began. The following symptomatic cases are discussed to exemplify pars pro toto and exemplarily the impact of social Darwinism, ethnocentrism, and racism on paleoanthropology.

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First Case: Hermann Klaatsch’s Iridescent Image As mentioned above, Hermann Klaatsch, a German comparative anatomist, anthropologist, prehistorian, and ethnologist who headed the Institute of Anthropology and Ethnology in Breslau (today Wrocław) since 1907 till his sudden death in 1916, was one of the most prominent paleoanthropologists in his time. He started an excellent career under the renowned anatomist Karl Gegenbaur (1826–1903; Heidelberg). The young researcher was impressively noticed by the scientific community of physical anthropologists at the Anthropology Congress 1899 at Lindau, where he presented a paper “About man’s place among the mammals, especially the primates and the mode of evolution from an earlier form” (Klaatsch 1899, 1900). Advocating for the application of Darwinian principles to humans, Klaatsch received fierce criticisms from the doyens Virchow and Ranke (see Trinkaus and Shipman 1993; Wolpoff and Caspari 1997; Hoßfeld 2005a, b; Weniger and Klaatsch 2005; Henke 2006a, 2011). Evans (2010, p. 81) states that Klaatsch was the only physical anthropologist in German-speaking anthropological circles besides Gustav Schwalbe (and Hermann Schaaffhausen who died 1893) who championed Darwinism at the late 1890s. I would like to add Dragutin (Karl) Gorjanovic´-Kramberger who was trained in Germany and maintained close contacts to Schwalbe (see Henke 2006a) but was on slippery ground with his colleague from Breslau, after having refused joint research on the Krapina fossils. Trinkaus and Shipman (1993, p. 168) describe Klaatsch’s motives for a cooperation as follows: “the fossils were someone’s ticket into the brightly lit heart of anthropology, and Klaatsch lusted after them.” Klaatsch had done doubtless excellent innovative comparative research on primates and human fossils, e.g., the Neanderthal calotte (citations see Wegner and Klaatsch 2005); but, he didn’t have priority access to human fossils. It has been suggested that this deficit gave the impetus for his Australian expedition from 1903 to 1907; however, there may have been other reasons, including the “Out-of-Australia” theory of his close friend Otto Schoetensack (1850–1912) who developed the notion that the human race in fact originated in Australia (Schoetensack 1901, 1904). In this he was influenced by Thomas H. Huxley who had visited Australia earlier, looking for the origin of mankind in the fifth continent. Corinna Erckenbrecht (2010, p. 49) suggests in her biographicalethnological thesis on Hermann Klaatsch: “As Schoetensack himself was in poor health it was agreed upon that Klaatsch was to make the trip to Australia.” Her conclusions on the “Personality of Klaatsch as a Scientist and His Ethics of Collecting” are complex; on the one hand, she describes Klaatsch as “a very versatile, well educated and trained scientist who thought in major scientific and theoretical contexts on a high level.” On the other hand, she reveals: “To enforce his personal research interests he acted in a very energetic, sometimes uncompromising way without respect for the feelings and values of the Aborigines.” In contradiction to this attitude, “he publicly stood up for the rights of the indigenous people, criticized their treatment by the white Australian society” (Erckenbrecht 2010, p. 49). Though one may explain his conflicting behavior as compromisingly assertive, on the one hand, and paternalistically protective, on the other hand, as an attitude of social Darwinistic superior-inferior thinking, and typical of a colonialist mentality, it is in modern terms of political correctness simply unethical. For historiographical reasons, we must ask how this personality may have influenced Klaatsch’s paleoanthroplogical research. In 1907 Klaatsch returned to Germany and cooperated highly successfully with the Swiss art dealer and archaeologist Otto Hauser (1874–1932; Dro¨ßler 1988; Hoffmann 2003a, b; Dro¨ßler et al. 2006), excavating and analyzing the famous skeletons of Le Moustier and Combe-Capelle (Hoffmann 2003a, b; Ullrich 2005a). The French historian Benoit Massin (1996, p. 88) describes that Klaatsch, “previously an advocate of the unity of mankind,” made a dramatic about-face at the 1910 meeting. On the basis of comparative morphological study Page 29 of 84

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Fig. 6 Klaatsch’s polygenist tree, assuming different roots of the Neanderthals and the Aurignac Man (Klaatsch 1911, p. 480)

of prehistoric human races, Klaatsch argued that there were two main branches of human evolution: one Western stock from which emerged the gorilla and Neanderthal man and one Eastern stock for the orangutan and the Aurignacian race (Klaatsch 1910a: 91–99; see further Klaatsch 1911; Henke 2011). Evans (2010, p. 65) adds: “Klaatsch’s polygenist ideas won few adherents, however, and the resistance that he engendered, confirmed the monogenist consensus.” From the beginning, CombeCapelle’s high early Aurignacian age was heavily criticized, though it fitted perfectly in Klaatsch’s phylogenetic scheme (Fig. 6). As it recently turned out after the surprising rediscovery of the individual and radiocarbon dating that showed merely an early Holocene age (Hoffmann et al. 2011), there arose many unpleasant questions, e.g., the suspicion that Klaatsch and Hauser might have preferred the greater age for unscientific reasons. Though this isn’t proof, there remains a bad aftertaste; however, in dubio pro reo! As has been demonstrated by a historical analysis of the literature on Combe-Capelle (Henke 2011), the false calibration of the Upper Paleolithic icon Combe-Capelle had tremendously influenced paleoanthropological theories during the first half of the last century. This is not trivial, insofar as the “Aurignac Man” played a prominent role in the contemporary racial typologies, e.g., the Nordicism, an ideology of racial supremacy and “master race” racism (e.g., Weinert 1941). Apart from this, one might mention that both authors profited – Klaatsch earned scientific praise and Hauser additionally thousands of Reichsmarks because Combe-Capelle was thought to be the oldest anatomically modern human fossil worldwide: Honi soit qui mal y pense! Though historians will quite likely not be able to solve the problem of whether the diagnosis was a deliberate move on the part of Klaatsch, or was simply a selffulfilling prophecy, this case should be a lesson “to see what we are looking at, not to put it in a preferred scheme” (sensu W.W. Howells 1993). Furthermore, this case should make us cautious, as not every scientist knows the guidelines of good and ethical practice (see Wuketits 2010, 2012), and sociobiologists would comment laconically: Never suppose a positive cause, if there could be a negative one.

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Second Case: Political Constraints, See What “We” Want That archaeological and paleoanthropological researches were not spared by the ideology of the national socialists is documented, e.g., by the fact that the Neanderthal Museum, which had been inaugurated on May 1, 1937, was closed by order of the Reichsleiter f€ ur Vorgeschichte, Reinertz, on March 3, 1938. The arguments were that the museum, which should demonstrate “Deutsche Urgeschichte, soweit sie mit dem Neandertal in engster Beziehung steht,” did not pass the evaluation of an NS commission (Beckmann 1987). This case may be a warning that (paleo)anthropological exhibitions in museums and all kinds of popular scientific media are interpretatively filtered through ideologies and personal perceptions of the curators and authors (see, e.g., Ickerodt 2005; Sarasin and Sommer 2010). Additionally, one must be aware that this equally applies to all kinds of science and knowledge transfer (Henke 2007a, 2010a). Third Case: Franz Weidenreich, Politically Unwanted Even more inimical to the development of paleoanthropology during the Nazi era was the fact that the most outstanding German paleoanthropologist at that time, Franz Weidenreich (1873–1948), lost with effect from December 31, 1935, his venia legendi at the Johann Wolfgang Goethe University due to the persecution of the Jewish population (Hertler 2007). His emigration to the USA was an irreplaceable loss for anthropology in Germany. Exempla docent – after Hubert Markl, former president of the Max Planck Society, we should learn from good and bad experiences in our history; in the latter context, history of science plays a most significant role. The well-known biography of most famous scientists, e.g., Albert Einstein, Ernst Mayr, and Erwin Chargaff, is impressive proof that “science serves with heads.” Markl’s (1988) identical worded article “Wissenschaft dient mit Ko¨pfen” convincingly shows that the scientific community needs internationality: “Wir wissen auch, daß manche dieser Netze buchsta¨blich zum lebensrettenden Sprungtuch auf der Flucht vor Verfolgung geworden sind und immer wieder werden. Niemand hat diese Weltb€ urgerschaft des Wissenschaftlers € uberzeugender deutlich gemacht als Albert Einstein” (Markl 1988, p. 116–119). Since Franz Weidenreich was involved in research on the largest H. erectus sample from a single locality, Zhoukoudian, paleoanthropology in Germany lost a vital contact with the international scientific community. Thanks to Weidenreich (1943), brilliant documentation, casts, and descriptions survived of the “Sinanthropus” – skulls which were lost during an attempt to ship them to the USA (Shapiro 1974) – and, equally important, Weidenreich is viewed as the founder of the “multiregional theory of human evolution” (Wolpoff and Caspari 1997; Wolpoff 1999; Hertler 2007; for a popular scientific biography, see Hartkopf 2012). Weidenreich’s illustration (see Fig. 7) of the process of human evolution became known as “trellis,” a network of populations by gene exchanges. Wolpoff and Caspari (1997, p. 200) explicate the graphic as follows: “[trellis], a network with vertical lines passing through the main stages of evolution, horizontally separated into the main centers of evolution (distribution and specialization), and the diagonal connections between them reflecting the patterns of genetic exchanges,” in Weidenreich’s own explanation, “a graphic presentation of the conception of the hominid group as one species” (Weidenreich 1946, p. 30). This “trellis” or “lattice” expresses Weidenreich’s idea that evolution is transformation, in close connection with interbreeding. As the trellis metaphor caused a lot of misinterpretations (e.g., by Howells 1959, 1993) and vehement criticism from cladists and “splitters,” we will come back to this controversy later (see below).

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Fig. 7 Pedigree of the Hominidae, so-called trellis, from Weidenreich (1946, p. 30) (Redrawn by Wolpoff and Caspari 1997, p. 201)

Fourth Case: Delayed Awakening It is widely known that during the Third Reich, German physical anthropologists were strongly involved in the functioning and ideological underpinning of the Nazi regime. In an oppressive manner, e.g., Schafft’s (2004) historical analysis “From Racism to Genocide” reveals anthropology’s entanglements and unmasks blatant cases of pseudoscience. Therefore, it is not surprising that paleoanthropology was also fraught with racist ideology, though on the international level, there was groundbreaking change in evolutionary thinking (Junker 2004; Hoßfeld 2005b; Mayr 1988). The protagonist of evolutionary thinking, Ernst Mayr (1904–2005), a trained German zoologist, left his homeland in the year 1931 and did his research at the AMNH in New York and after 1953 at the Harvard University in Cambridge. He denied that the “Synthesis” (see Fig. 8) was a revolution; his conclusion was: “It was not so much the discovery of new facts that characterized the synthesis as the removal of misunderstandings. The period from 1859 to 1935 had suffered from being dominated by erroneous conceptualizations, such as essentialism (typology), a belief in an intrinsic tendency toward progress, a misunderstanding of the nature of inheritance and of mutation, a failure to understand the nature of populations and the uniqueness of individuals, and of other erroneous concepts” (Mayr 1988). When misunderstanding of evolutionary principles was commonplace, no wonder German paleoanthropologists didn’t conduct acknowledged science.

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Fig. 8 Development of the theoretical basis of the biological sciences (After Jahn 2000, modified)

Above all, it must be stressed in this context that the “misunderstandings” mentioned by Mayr in no way equate with wrong conceptions of racial and political ideologies that so horribly became virulent during the era of National Socialism in Germany; there is no excuse for racial discrimination and all kinds of racism from a false understanding of the principles of human evolution. Further, there is absolutely no doubt that a large part of anthropologists and human geneticists were involved in such racist activities, in some cases perhaps only passive, but in many demonstrable cases highly actively, in roles ranging from deskworkers (“Schreibtischta¨ter”) to racist executioners (Stocking 1988; Proctor 1988; Weingart et al. 1988; Massin 1993, 1996; Hoßfeld 2005b; Schafft 2004). From the perspectives of paleoanthropology and the history of science, it is noteworthy that during World War II, the first edition of Gerhard Heberer’s compendium “Die Evolution der Organismen” appeared (Heberer 1943). The anthropogenetical contributions of the multifaceted volumes deal, e.g., with comparative anatomy (v. Krogh 1909–1992), paleontology (Gieseler 1900–1976), ethology, and archaeology (Weinert 1887–1967). However, in the view of the scientific historians Hoßfeld and Junker (2003) and Hoßfeld (2005b), the chapter authored by Otto Reche (1879–1966) is the only one that takes the model of synthetic Darwinism into account. I’m in full agreement with the following overall assessment: “. . .[es] handelt sich € uber weite Strecken um vergleichende Untersuchungen zur Stammesgeschichte der Menschheit, wie sie bereits im 19. Jahrhundert angestellt wurden, erga¨nzt durch neuere Daten aus Serologie und Pala¨ontologie” (Hoßfeld and Junker 2003, p. 107). Of particular interest, Junker and Hoßfeld (2002, p. 242) mention that the volumes of “Evolution der Organismen” are “with few exceptions – without any reference to national socialist ideas”. The major exception is Heberer’s preface, and the authors assume “that Heberer as editor and the publisher (Gustav Fischer) have demanded ideological neutrality.” The biological impact on paleoanthropology was minor, since in practice fossil discoveries came into the literature through collaboration between the archaeologists who excavated them and the anatomists who described them. Physical anthropologists with a biological background, such as Gerhard Heberer (1901–1973), a convinced national socialist who

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was induced into the SS by Heinrich Himmler (Deichmann 1995; for biography, see Hoßfeld 1997), were rare (Massin 1993, 1996). These theoretical deficits caused consequences in paleoanthropological thinking, especially concerning Darwinian and Neo-Darwinian thoughts. And I agree with Foley’s (2001, p. 6) statement: “Archaeologists and professors of anatomy seldom made a rich cocktail of Darwinian theory.” In general the descriptive casuistic and more or less narrative approaches in paleoanthropology hold true throughout the period under discussion, and for early postwar times, in Germany as well as in other countries (Tattersall 2000a; Foley 2001; Henke 2010a, b). The period leading up to World War II had seen the emergence of the evolutionary synthesis, but not until the 1950s did innovative biological principles and methods begin to inform paleoanthropological science too (Spencer 1984; Mayr 1988; Delisle 1995; Hoßfeld 1997, 2005b; Jahn 2000; Tattersall 2000a; Foley 2001; Corbey and Roebroeks 2001b; Hoßfeld and Junker 2003; Junker 2004). What’s the message in all of this? Firstly, research is embedded in an ongoing process of paradigmatic and methodological innovation and needs permanently a critical evaluation. This can most effectively be achieved by international standards. Secondly, physical anthropologists, mainly the negligibly small group of paleoanthropologists in Nazi Germany, missed correctives from outside, or more correctly, many protagonists – like Gerhard Heberer, Wilhelm Gieseler, and Hans Weinert – felt comfortable under a National Socialistic regime in spite of the knowledge of injustice against humanity (e.g., Vogel 1983; Massin 1993, 1996; Hoßfeld 2005a, b). It should also be mentioned that most of them continued their careers in postwar times (Saller 1961; Preuß et al. 2006; Preuß 2009). Thirdly, every scientist should be aware of the ethical standards of his discipline and should follow ethical rules and the recommendations of good science practice, as personal responsibility will always remain (see Max-Planck-Gesellschaft (1984); AAPA Statement on Biological Aspects of Race (1996) – and ongoing discussion, e.g., Cartmill 1999; Brattain 2007).

Keeping Pace with Other Sciences: Toward a “New Physical Anthropology” The selected examples given here demonstrate that social and political reasons far removed from paleoanthropology are important; and in this context Dennell (2001, p. 45) reminds us “that paradigmatic shifts in palaeoanthropology occur in response to a wider world, and are not wholly dependent on internal evidence or individual personalities alone.” After World War II, the world opened up, causing drastic changes for paleoanthropology too. Ethnocentricity and old-fashioned typological methodologies of physical anthropology and evolutionary biological thinking were subjected to critical review. The reevaluation of paleoanthropology was mainly carried out by US-American anthropologists like Sherwood Washburn (1911–2000; see Howell 2003; Marks 2000) and especially Francis Clark Howell (1925–2007). His younger colleague Tim White praised him in an obituary (published by Sanders 2007, p. 1, www): “Clark’s central importance since the 1950s has been to make paleoanthropology what it is today – that is, the integration of archaeology, geology, biological anthropology, ecology, evolutionary biology, primatology and ethnography.” Besides Clark Howell, one must mention the British-born Kenyan Louis S. B. Leakey (1903–1972) (see Isaac and McCown 1976) as a further prominent innovator of the discipline. Desmond Clarke (1976, p. 541) appreciation – by his discoveries, and his brilliant personality, he gained the admiration and captured the imagination of the world – meets it exactly. In summary, paleoanthropology needs, like all sciences, a properly evaluated underlying theory and methodology (Oeser 2004; Ruse 2005) and can only flourish in open-minded cosmopolitan societies. Furthermore, every discipline needs exceptional personalities too, even if teamwork Page 34 of 84

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dominates, and I would like to add, as far as paleoanthropology is concerned, also those with charisma since human evolution is a topic of extreme public interest and with generosity, as “sites” and “nuggets” should be shared according to fair rules (e.g., see EVAN Society, www; NESPOS Organization, www; Weber this volume). These preconditions were developed in the second half of the last century; let’s have a closer look at them.

Diversification of Anthropology in the Second Half of the Twentieth Century Early Post-World War II Period The principal architects of the evolutionary synthesis mentioned previously gained more and more influence in World War II and postwar times, and their ideas shaped the field of biological anthropology including paleoanthropology (Tattersall 2000a; Foley 2001; Levinton 2001; Mayr 2001; Junker 2004; Hoßfeld 2005b; Wolpoff 2003). Although the fossil record had steadily increased, it was still a challenge to reconstruct the raw outlines of human evolution from the tiny catalog of human skeletal remains. There was tremendous progress as the hominin status (at that time taxonomically termed hominid) of the small-brained, bipedal australopithecines became accepted due to the new finds from fossils from Kromdraai Cave, excavated by Robert Broom (1866–1951) in 1938. The successful excavation of further exciting australopithecine fossils from the cave sites Sterkfontein, Makapansgat, and Swartkrans by Broom and John T. Robinson (1923–2001) after 1947 was the continuation of the success story of human paleontology in South Africa that had started with Dart’s description of the Taung child in 1924, had continued with Broom’s excavations (Broom and Scheffers 1946), and lasts to the present day (overviews in Grine 1988; Sperber 1990; Partridge et al. 2003; Tobias 2005; Berger et al. 2010; Balter 2011). The diversity of the australopithecine taxa became especially obvious from the megadont Paranthropus from Swartkrans, “Another new type of fossil ape-man,” as described by Broom (1949, 1952) and Broom and Scheffers (1946). In addition, human origins became even more complex and debatable as the “East Side Story” (sensu Coppens 1994) developed, having started with Wilhelm Kattwinkel’s and Hans Reck’s explorations in 1911, continued still with scant success by Louis and Mary Leakey in the 1930s, and came into major focus by the discovery of Zinjanthropus boisei, a hyperrobust australopithecine (Leakey 1959), and culminated in the successful Afar Research Expedition (Johanson et al. 1978) and many more recent projects.As the dating of known specimens was limited to the relative time scale “older than/younger than,” and as the techniques of absolute dating were still unknown (Oakley 1964), there was a lot of uncertainty in the calibrations. The overall picture was a stepwise adaptive evolution from primitiveness to high-order hominids/hominins with modern-shaped bodies and cultural skills. The evolutionary ladder reached from the gracile and robust australopithecines, i.e., very apelike species, to the Pithecanthropus and Sinanthropus species. These had been lumped with the European H. heidelbergensis in a single species, H. erectus. This simple gradualistic model regarded the Middle Pleistocene “Java man,” “Peking man,” and the “Mauer man” as intermediate stages between the early taxa from Africa and the later Neanderthals, a well-documented fossil human group from late Ice Age sites in Europe and western Asia. Little wonder that in this confusion, paleoanthropologists welcomed Mayr’s and Dobzhansky’s simplifying message that only one kind of hominid (new systematic: hominin) could have existed at any time and that virtually all developments in human evolution since Java man had taken place within the single, albeit variable, species H. sapiens. Tattersall (2000a, p. 3) suggests that Dobzhansky was

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

influenced “by his newly arrived New York neighbor Franz Weidenreich, nowadays hailed as the father of ‘multiregional continuity’.” Ernst Mayr took the position that at the most three successive species could be discerned within the genus Homo: H. transvaalensis (the australopithecines), H. erectus, and H. sapiens (including the Neanderthals). Few paleoanthropologists followed these pronouncements in every detail; however, schemes of hominin evolution routinely came to incorporate the synthesis’ basic assumptions, whereby evolutionary change consisted simply of the gradual modification of lineages, usually no more than one, over long spans of time. Human evolution thus became the story of a long, single-minded struggle from primitiveness to perfection which became highly criticized (more later; overview in Tattersall 2000a; see further Foley 2001; Wolpoff 2003; Wuketits, this volume). Successively there arose different problems from Mayr’s simplified model. First, the evolutionary model was in contradiction to the mosaic pattern of the erroneously ancient, heavily encephalized Piltdown man. This problem disintegrated when in 1953, Piltdown was declared a hoax by authorities at the British Natural History Museum (Spencer 1990b). Second, paleoanthropological results were severely flawed due to arbitrary taxonomic approaches (see Table 2). For this reason, there was a genuine need for the revision of the overabundance of species and genus names, which had been applied liberally more or less without a taxonomical concept to hominid fossils. The taxonomic revision of the hominid/hominin sample asked for a strict consensus regarding the underlying species concept and how to reconstruct phylogenetic relationships (Washburn 1951, 1953; Hennig 1950, 1966; Remane 1952; Eldredge and Cracraft 1980; Eldredge 1993; Waegele 2000; Gould 2002; Wiesem€ uller et al. 2003; Lieberman and Vrba 2005; Wood and Lonergan 2008; Henke and Hardt 2011; Willermet 2012). Niles Eldredge’s (1993) pressing issue “What, if anything, is a species?” is symptomatic of the need to solve principle taxonomic questions still today (however, this is not an exclusive problem of paleoanthropology; e.g., Hunt 2003). Third, the uncertainty of the temporal allocation of fossils reflected the absence of absolute dating techniques (Oakley 1964; Bishop and Miller 1972). In sum, it became more and more obvious that there was tremendous need for a new and precise strategy of physical anthropology within the frame of a revised Synthetic Theory of Evolution (Cartmill 1990a, b; Bowler 1997; Eldredge 1993; Levinton 2001; Tattersall 2000a, b; Lieberman and Vrba 2005; Willermet 2012). In the immediate postwar period, there arose a body of theory that swept away a host of conflicting notions about the nature of the evolutionary process. The elegantly simple concept stated that all evolutionary phenomena could be ascribed to a single mechanism: the gradual change of genes and gene frequencies within lineages of organisms under the guiding hand of natural selection (Cartmill 1990a, b). Though the innovative population genetic approaches in the 1920s of Ronald A. Fisher (1890–1962), John B. S. Haldane (1892–1964), and Sewall G. Wright (1889–1988) were obviously of great importance for the field of paleoanthropology too, and notwithstanding that the protagonists of the Synthetic Theory of Evolution had given special attention to this area at the time when the discipline was absorbing its theoretical underpinnings, there was need for active initiatives by (paleo-)anthropologists themselves. First, the rejection of the typological approach was required before population genetic thinking could board the New Physical Anthropology sensu Washburn in the 1950s. However, many challenges had to be overcome, and some are still waiting to the present day (Vogel 1983; Foley 1987; Martin 1990; Delisle 1995; Wolpoff 1999; Tattersall 1995, 2000a, b; Foley 2001; Levinton 2001; Gould 2002; Jobling et al. 2004; Cartmill and Smith 2009; Fuentes 2010).

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

Table 2 Hominin taxonomy: Genera and species designations of former and current taxa, temporal and geographical ranges. Except Homo sapiens, all the other taxa are extinct (Adapted from Collard (2002), modified and enlarged; see further Groves (2001); Henke (2003b); Wood and Lonergan (2008)) Genus Homo Linnaeus, 1758 [including the following genera: Anthropopithecus Dubois, 1892, Pithecanthropus Dubois, 1894; Protanthropus Haeckel, 1895; Sinanthropus Black, 1927; Cyphanthropus Pycraft, 1928; Meganthropus Weidenreich, 1945; Atlanthropus Arambourg, 1954; Telanthropus Broom and Robinson, 1949; earliest appearance in the Pliocene, worldwide distribution] Homo sapiens Linnaeus, 1758. Pleistocene to present, worldwide Homo neanderthalensis King, 1864. Pleistocene, western Asia Homo erectus (Dubois, 1892), Weidenreich 1940. Pleistocene, western Eurasia Homo heidelbergensis Schoetensack, 1908. Pleistocene, Africa and Eurasia Homo rhodesiensis (cf. heidelbergensis) Woodward 1921. Pleistocene, Africa Homo helmei Dreyer, 1935. Pleistocene, northern and East Africa Homo soloensis Dubois, 1940. Middle Pleistocene, Southeast Asia Homo modjokertensis v. Ko¨nigswald, 1950. Early Pleistocene, Indonesia Homo mauritanicus Arambourg, 1963. Middle Pleistocene, North Africa Homo habilis L.S.B. Leakey et al., 1964. Plio-Pleistocene, Africa Homo ergaster Groves and Maza´k, 1975. Pleistocene, Africa and Eurasia Homo palaeojavanicus Sartono, 1981. Middle Pleistocene. Southeast Asia Homo rudolfensis (Alexeev, 1986), Wood 1992. Plio-Pleistocene. East Africa and Malawi Homo antecessor Bermudez de Castro et al., 1997. Early Pleistocene, Western Europe Homo georgicus Gabunia et al., 2002. Early Pleistocene, Northwestern Asia Homo cepranensis Mallegni et al., 2003. Early Pleistocene, Italy Homo floresiensis Brown et al., 2004. Late Pleistocene–Early Holocene, Indonesia [“Denisova Man,” sometimes designated as “Homo denisovan” is not regarded as a species by Krause et al. (2007, 2010)] Genus Australopithecus Dart, 1925 [includes the genus Plesianthropus Broom, 1938]. Pliocene, Africa Australopithecus africanus Dart, 1925. ca. 3.0–2.5 Ma; South Africa Australopithecus afarensis s.s. Johanson et al., 1978. ca. 3.7–3.0 Ma; Ethiopia, Tanzania, Kenya Australopithecus anamensis M.G. Leakey et al., 1995. ca. 4.2–4.0 Ma; Kenya Australopithecus bahrelghazali Brunet et al., 1996. ca. 3.5–3 Ma; Tchad (North Africa) Australopithecus garhi Asfaw et al., 1999. ca. 2.5 Ma; Ethiopia Australopithecus sediba Berger et al., 2010. ca 1.78–1.95; South Africa Genus Paranthropus Broom, 1938 [includes Zinjanthropus L.S.B. Leakey 1959, Par Australopithecus Arambourg and Coppens, 1967]. Plio-Pleistocene, Africa Paranthropus robustus Broom, 1938. ca. 1.5–2.0 Ma; South Africa Paranthropus boisei L.S.B. Leakey, 1959. ca. 2.3–1.4 Ma; Tanzania, Kenya, Ethiopia, Malawi Paranthropus aethiopicus Arambourg and Coppens, 1968. ca. 2.7–2.3 Ma; Ethiopia, Kenya, Tanzania (?) Genus Ardipithecus White et al., 1995. Pliocene, East Africa Ardipithecus ramidus s.s. (White et al., 1994) White et al., 1994. ca. 4.5–4.3 Ma, Ethiopia Ardipithecus kadabba Haile-Selassi et al., 2004. ca. 5.8–5.2 Ma, Ethiopia Genus Kenyanthropus M.G. Leakey et al., 2001. Pliocene, East Africa Kenyanthropus platyops M.G. Leakey et al., 2001. ca. 3.5–3.3 Ma, Kenya Genus Orrorin Senut et al., 2001, Miocene, East Africa Orrorin tugenensis Senut et al., 2001. 6.6–5.7 Ma, Tugen Hills, Kenya Genus Sahelanthropus Brunet et al., 2002. Miocene, northern East Africa Sahelanthropus tchadensis Brunet et al., 2002. ca. 7–6 Ma, Tchad

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

Fig. 9 The strategy of physical anthropology (Redrawn from S.L. Washburn 1953, modified)

New Strategies, Concepts, and Challenges in Physical Anthropology In the early 1950s, there began an intensive discussion on the strategy of physical anthropology, i.e., the body of scientific theory and techniques with which it attacks its problems. Washburn (1951, 1953) was one of the protagonists of a new conception which was formulated in the new version shown in Fig. 9. The main step was to reduce the speculative and narrative part of physical anthropology in favor of thorough hypothesis testing. Cartmill (1990b, p. 189) puts it this way: “No doubt, people are different from the apes; but it is our job as scientists to explain those differences. Explanation, as opposed to mere storytelling, has to invoke law-like regularities connecting causes and effects.” This then was the challenge facing the evolutionary biological sciences (Popper 1968). Of greatest importance for the renewal of physical anthropology were the rejection of typological concepts and an increased interrelationship between the different parts of anthropology. The change from descriptive studies to the investigation of process and behavior brought about the integration of the problems of human evolution in the vast scientific field of mammalian evolutionary biology. Solutions to problems consequently followed, on the one hand, from paleontology, primatology, genetics, population genetics, ecology, and diverse medical sciences and, on the other hand, from the study of archaeology and ethnology. The great challenge of human evolutionary biology became the cultural factor, as adaptations, human migrations, mating systems, population densities, diseases, and human ecology all became factors seen as essential to the explanation of our special human way of life (Washburn 1953; Vogel 1966; Osche 1983; Foley 1987, 2010; Tattersall 1995, 1998, 2002, 2012; Wolpoff 1996–97; Cartmill and Smith 2009; Foley and Gamble 2009; overviews in Henke and Rothe 1994;

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Delson et al. 2000; Wood 2011; Begun 2013). Washburn’s (1953, p. 726) prognosis was: “If we would understand the process of human evolution, we need a modern dynamic biology and a deep appreciation of the history and functioning of culture. It is this necessity which gives all anthropology unity as a science.” The recognizable post-World War II shape of paleoanthropology resulted from the belated acceptance of neo-Darwinian principles of evolutionary biology, which were successively brought together in the 1930s and 1940s and unified evolutionary biology under a single roof, sweeping away a huge package of mythological narrative thinking (Henke and Rothe 2006; Goodrum 2009). Delisle (1995, p. 217) suggested “that the evolutionary synthesis directly influenced on human paleontology [during the decade 1950–1960] every day practitioners in human paleontology almost solely through the general concepts and methods of the new systematics. Instead of being only a common core shared by a host of disciplines, the evolutionary synthesis should also be defined by the extent to which that core has been guiding current research in any one field.” Washburn’s concept of a New Physical Anthropology was received with enthusiasm by the scientific community, and the impetus for the development of the individual subdisciplines has been tremendous (see Fuentes 2010; Lille and Kennedy 2010; Larsen 2010), though not by all, e.g., the German anthropologists who slumbered through the theory change (see Vogel 1983; Henke and Rothe 1994, 2006). Despite its generally positive reception, vehement critics have appeared since the 1970s, as it was asked: Was the Modern Synthesis a real step forward in the right direction? The dispute over evolutionary theory opened with a stimulating paper on “Punctuated equilibria: an alternative to phyletic gradualism” by Niles Eldredge and Stephen J Gould (1972), originally presented at the Annual Meeting of the Geological Society of America in 1971. This was an astonishing contribution, though not entirely unexpected as other evolutionary models, e.g., Weidenreich’s “trellis” (Fig. 7), had been under heavy criticism for a long time (see Howells 1959; overviews in Shipman 1994; Wolpoff and Caspari 1997). Gould and Eldredge contrasted the hypothesis of “punctuated equilibria” [which proposes that evolutionary changes occur in geologically rapid events of branching speciation called cladogenesis] against the hypothesis of “phyletic gradualism” [which assumes that evolution generally occurs by anagenesis, uniformly, and by the steady and gradual transformation of whole lineages]. Interesting enough, that research on the evolution of Paleozoic invertebrates had guided Eldredge (1971) to the suggestion that allopatric speciation might be the resolution instead of gradual evolution. His enlightening idea that the pattern of descent is marked by long periods of stasis alternating with rapid changes caused great evolutionary debate (e.g., Wolpoff 1971, 1980, 1996–1997; Eldredge and Gould 1972; Gould and Eldredge 1977; Gould 2007; Tattersall 1994, 1998, 1999, 2000a, 2002; Eldredge 1995; Wolpoff and Caspari 1997; Foley 2001; Cartmill and Smith 2011). Eldredge’s (1995) review of the history of the twentieth-century evolutionary theory is entitled “Reinventing Darwin” and deals from an insider perspective with the confrontation of the “UltraDarwinians” and the “naturalists,” whose disputes were not always collegial and unpolemic (see, e.g., Wolpoff and Caspari 1997). Those who want to know more about “The Growth of Paleobiology as an Evolutionary Discipline” should read David Sepkoski’s (2012) “Rereading the Fossil Record”; we will concentrate here solely on the history of paleoanthropology as a subdiscipline of paleobiology. Just at the time when the “reinvention” by Gould and Eldredge started, Ian Tattersall had finished his thesis on “Subfossil Lemurs of Madagascar” at Yale University. Inspired by his own research on the vast diversity and variability of the lemurs in combination with the burgeoning (re-) evolutionary views in the 1970s, he started an extremely fruitful cooperation with Niles Eldredge, whose colleague he became at the AMNH in New York (e.g., Eldredge and Tattersall 1982). Page 39 of 84

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Reviewing the last half-century, Tattersall (2000a, p. 2) reaches the following crushing conclusions about the influence of the Dobzhansky et al.’s “Synthesis”: “Sadly, however, the Synthesis was doomed to harden, much like a religion, into a dogma: a dogma whose heavy hand continues to oppress the science of human origins a half-century later.” Tattersall (2000a, p. 5) complains that paleoanthropology was laggardly “Slow to absorb the principles of the Synthesis, palaeoanthropology has been equally slow to augment these principles with recognition of the multifarious complexities of the evolutionary process.” He gives many convincing arguments for this judgment, e.g., Dobzhansky’s lumping of the fossil hominids, with the conclusion “that there existed no more than a single hominid species at any one time level” (Dobzhansky 1944, pp. 261–262). Furthermore, he criticizes Mayr’s claim that humans did not speciate (Mayr 1950), a position which opened for Weidenreich, and later proponents the so-called single species hypothesis which mainly “rests on the nature of the primary hominid adaptation: culture (structured learned behaviour). Because of cultural adaptation all hominid species occupy the same, extremely broad, adaptive niche. For this reason, allopatric homind species would become sympatric. Thus the competitive exclusion principle can be legitimately applied. The most likely outcome is the continued survival of only one hominid lineage” (Wolpoff 1971, p. 601). It became very soon evident that the controversial positions of “lumpers” versus “splitters” would lead to sharp disputes in paleoanthropology; and when the long-unsolved Neanderthal problem (overviews in Trinkaus 1989; Vandermeersch 2002; Bar Yosef and Vandermeersch 1991; Stringer and Gamble 1993; Trinkaus and Shipman 1993; Wolpoff 1999; Clark and Willermet 1997; Tattersall 1999; Henke and Rothe 1999b; Harvati and Harrison 2006; Vandermeersch and Maureille 2007; Cartmill and Smith 2009) merged into the controversy of “multiregionalists” versus “replacement proponents,” the big paleoanthropological issue of the last four decades was on the floor. An almost endless series of conferences, congresses, scientific papers, proceedings, readers, and last but not least popular science media has addressed this topic. It was shown above that the controversy of proponents of “unilinearism” versus “multiple species concepts” smoldered long before the 1970s, when William W. Howells (1908–2005) had interpreted Weidenreich’s view as the “Candelabra Hypothesis” (Howells 1959). Other prominent anthropologists joined Howells, in spite of the fact that this characterization didn’t match Weidenreich’s original statement. The hot debate started when the British paleoanthropologist Christopher Stringer (1974) presented the results of his thesis on “Population Relationships in Later Pleistocene Hominids: A Multivariate Study on Available Crania.” His Out of Africa model claimed – in a late version – a total replacement of the non-African archaic populations. Very similar to Stringer’s Recent African Origin model (RAO I) was G€ unter Bra¨uer’s “Afro-European sapiens hypothesis” (Bra¨uer 1984; RAO II). The habilitation thesis of the German anthropologist was based on a sophisticated morphological comparison of a broad cranial dataset, taking revised calibrations of the Middle Stone Age in Africa into account. In spite of many similarities between the models, there was a significant difference: Bra¨uer’s hypothesis assumes degrees of “hybridization” between modern and archaic humans (including the Neanderthals). Smith and Cartmill (2009, p. 473) summarize: “Bra¨uer’s model thus has strong flavor of replacement – if not so of species, at least of local populations.” The opposing Multiregional theory (MRE) by Wolpoff (1971, 2004) was – in some essential aspects – confronted by a further theory within the bundle of continuity and replacement hypotheses in Homo sapiens evolution, the so-called Assimilation Model (AM) proposed by Smith et al. (1989). Like the MRE, the AM too recognizes important gene flow between archaic and modern human populations in Eurasia. Concerning the Neanderthals, the AM rejects separate species status, and this is assumed for other Middle and Late Pleistocene populations too (Cartmill and Smith 2009, p. 473). Page 40 of 84

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If we follow the history of the “continuity or replacement” discussion in some prominent contributions, we have to admit that something must have gone wrong (see, e.g., Andrews and Franzen (1984), Smith and Spencer (1984), Wood et al. (1986), Giacobini (1989), Mellars and Stringer (1989), Smith et al. (1989), Trinkaus 1989; Bra¨uer and Smith (1992), Aitken et al. (1993), Frayer et al. (1993); Meikle et al. (1996), Clark and Willemet (1997), Tobias et al. (2001), Crow (2002), Barham and Mitchell (2008), Condemi and Weniger (2011)). Why was everybody trying to verify their own hypothesis, when falsification should be the method of choice? Why was it apparently so difficult to gain consensus on the underpinning theory and methodology? What made it so difficult to exclude the one or the other model by falsification? Next to these and many other scientific questions, there is a personal one: Why often so emotional? Scientists are not married to their scientific statements; they can “divorce” and admit when they were wrong. All this begs the question: Is paleoanthropology really a discipline apart from the mainstream of biological thinking, and has the Modern Synthesis really shadowed the scientific work of paleoanthropologists? During the last 50 years, the vestiges of the so-called step ladder model have been successfully refuted [no wonder, when we consider the increased fossil record and the flood of hominin taxa in the Mio-Plio-Pleistocene which can’t be ignored; see Table 2]. While the unilinear and chiefly anagenetic models vanished from the discussion [almost], it became increasingly obvious that the process of human evolution is convincingly represented by multiple species, cladogenesis, and adaptive radiations [when looking at the Mio-Pliocene] as well as by the processes of the punctuated equilibrium model. But, what has happened to the genus Homo? (see Henke and Hardt 2011). However, is this “mainstream” thinking on RAO in current paleoanthropology illusory, insofar as some of the opponents have thrown in the towel? It would be of great interest to know, via a scientific historic approach, which factors have played the decisive role: purely convincing scientific arguments or personal dynamics within the scientific community (coalitions and alliances)? And what about all the publicity and media attention? Paleoanthropology isn’t, and never was, operating in an ivory tower. What is the role of “embedded” scientific journalists in the acceptance or rejection of results of paleoanthropological research? Is anthropology, as a mediafriendly subject, particularly at risk? (See Franck 1997, 1998a, b; Stoczkowski 2002; Grim 2009). Was the Modern Synthesis really an obsolete theory which was uncritically used to give support for unilinearism? (Tattersall 1998, 2000a). Foley’s less negative comment on this centers on the point that paleoanthropology remained “in fact [. . .] blithely innocent of most theoretical issues.” Foley emphasizes that “anthropologists undoubtedly read the modern synthesis as suggesting that there can be no cladogenesis, but rather than seeing the true nature of Darwinian theory they merely saw their own theoretical reflecting” (Foley 2001, p. 5–9). Foley’s opinion that anthropology of the last half-century had many theoretical deficits agrees with that of my academic supervisor Christian Vogel (1933–1994), the former head of the Institute of Anthropology in Go¨ttingen. Vogel had formulated the “biological perspectives of anthropology and the so-called theory-deficit of the physical anthropology in Germany,” quoting Washburn (1953), who pleaded that the “application of a constituent, experimentally verified, evolutionary theory is the first task of the physical anthropologist” (Vogel 1983, p. 225). One should remember that Vogel’s paper was presented in 1981, reflecting that paleoanthropology, and in a wider sense physical anthropology, remained behind the other evolutionary sciences (Spiegel-Ro¨sing and Schwidetzky 1982). Although paleoanthropology was not the foremost field of anthropological research in Germany, new editions appeared of Die Evolution der Organismen (Heberer 1959, 1967–1974) and the textbook Menschliche Abstammungslehre (Heberer 1965a). In spite of these and other prominent publications in Germany in the 1960s and 1970s (Kurth 1962, 1968; Page 41 of 84

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Fig. 10 Venn diagram of human uniqueness and the human adaptive strategy as the intersection of the biological categories to which hominins belong (After Foley 1987, modified)

Heberer 1968b; Hofer and Altner 1972; Kurth and Eibl-Eibesfeldt 1975; overviews in Hoßfeld 1997, 2005a, b; Henke and Rothe 2006), there remained a theoretical vacuum in anthropology, and paleoanthropology seemed here – as well as in other European countries – much more fossil driven than hypothesis guided. A further appeal came from Cartmill (1990a, b, p. 173) who claimed in the early 1990s that: “Paleoanthropology should aim at increasing its theoretical content by reducing the list of qualitative human uniquenesses-and eliminating it altogether if possible.” The evaluation of the scientific reasons that perpetuated inadequate evolutionary approaches in paleoanthropology, and caused complacency with insufficient models, is still incomplete. Whether “the Synthesis was doomed to harden much like a religion, into a dogma”, as Tattersall claims (2000a, p. 2; contra Foley 2001), is a continuing issue; but most can agree with the statement that paleoanthropology was not explicitly theoretical, but was descriptive and in part excessively narrative (Bowler 1996, 2001; Foley 2001; Stoczkowski 2002; Ickerodt 2005; Henke 2007b, 2010a; Henke und Herrgen 2012). In contrast to the European situation, paleoanthropologists in the USA have traditionally been trained as physical and cultural anthropologists (see Lille and Kennedy 2010). This caused a different approach to research in human evolution; in the traditional European system, archaeologists as a rule dug up the fossils, and they or anatomists – not physical anthropologists – described them and perpetuated the problem. The simplicity of narrative approaches also hampered progress. The idea of human uniqueness was emphasized (Cartmill 1990a, b), and hominin fossils were treated casuistically. Foley (2001, p. 7) confesses that it was “frustration with the combination of an absence of evolutionary theory in human evolution and assumptions about human uniqueness that led me to write Another Unique Species (Foley 1987).” His sophisticated approach tries to explain the process of human evolution and the human adaptive Page 42 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

Fig. 11 Scientific disciplines that participate in reconstructing the process of human evolution (After Henke and Rothe 1994)

strategy as the intersection of the biological categories to which hominins (in Foley’s original hominids) belong (Fig. 10). Although most hominin diversity can be explained by evolutionary changes caused by geographical-climatological factors, there is a vast explanatory field within the life sciences, particularly comparative primatology, sociobiology, paleoecology, and paleogenetics. The multidisciplinarity of paleoanthropology is demonstrated in Fig. 11, but without a detailed special ranking of the importance of the cooperating disciplines. The preference for cooperation naturally depends on the paleoanthropological problems that have to be solved, but it should be remembered that inter-, multi-, and transdisciplinarity is a learning process, and an everlasting challenge for science (Mittelstraß 1989; Drilling 1992; Eggert 1995; Porr 1998; Henke and Rothe 2003; Henke and Herrgen 2012).

The Human Career: Revised How Many Hominin Species Have There Been? The last half-century has witnessed a dramatic improvement in our understanding of the process of human evolution, due to new approaches and techniques as well as a tremendous increase in the fossil record (Andrews and Franzen 1984; Franzen 1994; Henke and Rothe 1994; Ullrich 1995, 1999; Johanson and Edgar 1996; Hartwig 2002; Schwartz and Tattersall 2002, 2003, 2005; Cartmill and Smith 2009; Wood 2011; Begun 2013). Profound knowledge of the relationship between form and function has come from innovations in mechanical engineering, light microscopy and REM, and 2D and 3D tomography, as well as from innovative approaches in geometric morphometrics (Grupe and Peters 2003; Zollikofer and Ponce de Leon 2005; Bose 2013). Furthermore, evolutionary and developmental morphology (Minugh-Purvis and McNamara 2002) and primate physiology (Martin 1990) have contributed to a better understanding of form-function complexes (Ciochon and Corrucccini 1983; Oxnard 1984; Aiello and Dean 1990; Anapol et al. 2004; Ross and Kay 2004; Slice 2005). Hennig’s Phylogenetic Systematics (Hennig 1966, Page 43 of 84

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1982, 1984), which was first published in German in 1950 without gaining much attention (Hennig 1950), eventually revolutionized phylogenetic discussion in concert with tremendously increased skills in taxonomy and computer techniques (Rieppel 1999; Waegele 2000; Wiesem€uller et al. 2003). In spite of all the positive aspects of innovative methodological approaches, paleoanthropologists shouldn’t forget that all sophisticated quantitative approaches in taxonomy are used on extremely small fossil samples and limited datasets. In the context of taxonomy, Tim White (2000, p. 29) warned: “Hennig was not God, and parsimony is not God’s truth.” Wood and Lonergan (2008, p. 374) put it this way, and advised practitioners of paleoanthropology “to apply a healthy dose of skepticism to pronouncements about the taxonomy and systematics of the human clade.” A corrective to the “taxon federation” is Robert B. Eckardt’s (2000) textbook Human Paleobiology. His “attitude to the past” soundly criticizes “splitting” and calls for a check on it. Eckardt’s concept was highly influenced by Paul T. Baker (1927–2007), whose major field of research was human adaptability (“Man Must Adapt, or Be Damned,” Baker 1983). And his paleobiological approach embodies the “endeavor to reconstruct credible impressions of past populations and their members as they were in life: feeding; mating; giving birth to offspring and caring for them; avoiding predators; and enduring vagaries of weather, parasites, and diseases,” (Eckardt 2000, p. 1) a concept very near to Foley’s (1987, 1995a, b) and that of Henke and Rothe (1994, 1999a). With the improvement of absolute dating techniques (e.g., radiocarbon and other isotopic calibrations) and in relative dating by faunal complexes, the chronological pattern of human evolution was more precisely observed, and it became seen through the application of “molecular clocks” that the branching of the hominin line coincided with the aridification of the East African Rift Valley (Bishop and Miller 1972; Howell 1978; Vrba et al. 1995; Magori et al. 1996; Bromage and Schrenk 1999; Bobe´ and Behrensmeyer 2004). This allowed for a more effective exploration of hominin sites, increasing the chances of finding fossils of Mio-Plio-Pleistocene faunal complexes. However, as hominins are comparatively rare animals, it still needs much luck to find them. To increase the chances of doing so, taphonomy, the science of decay of organisms and the process of fossilization, first described in 1940 by Efremov, has become an important subdiscipline. Phenomena of biostratinomy, decomposition, and diagenesis are essential for the interpretation of fossils (Behrensmeyer and Hill 1980; Shipman 1981; Etter 1994; Vrba et al. 1995; Martin 1999; Wagner 2007). The more research on human evolution concentrated on the African continent, the more successful those paleoanthropologists with a licence to dig became, especially as they extended their campaigns into the Miocene as well as to Plio- and Pleistocene strata. Louis Leakey’s good fortune (Cole 1975; Isaac and McCown 1976) at Olduvai Gorge [discovered by the German neurologist Wilhelm Kattwinkel in 1911 (Glowatzki 1979) and successfully explored for the first time in 1913 by Reck (1925)], as well as that of his family members at Koobi Fora and diverse other East African sites, resulted from tremendous efforts (Leakey and Leakey 1978; Grine 1988; Wood 1991; Tobias 1991; Walker and Leakey 1993). Besides the activities of the Leakey family, there should be mentioned the successful expeditions of Francis Clark Howell in Omo, Glynn Isaac in Olorgesailie, and of course the famous Afar Research Expedition (Johanson and Edey 1980; Johanson and Edgar 1996). Finally, the Hominid Corridor Research Project of Timothy Bromage and Friedemann Schrenk in Malawi (Bromage and Schrenk 1999; Schrenk and Bromage 2002) must be alluded to, as well as the activities of Brigitte Senut and Michael Pickford in Tanzania (Pickford and Senut 2001) and Michel Brunet et al. (2002) in Chad. Many findings had to be corrected due to new research, and Pickford’s “Beyond the Evidence” demonstrates that forcefully.

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In the last decades, there have been impressive discoveries of early hominins in South African, at new sites, by Ron Clarke, Lee Berger, and colleagues. Africa has become the “Mecca” of paleoanthropologists. There is no longer any doubt now that Africa was the “cradle of mankind.” The hominin taxonomy presented in Table 2 presents the current list of species recognized by “splitters.” In spite of the fact that the “fossil hunting” has mostly been done in Africa, many activities in other parts of the Old World allow us to learn more about patterns of hominid migration and development. Exciting new fossils and findings from, e.g., Atapuerca (Spain) (Arsuaga et al. 1999), Apidima (Greece) (Pitsios 1999), Ceprano (Italy) (Ascenzi et al. 2000), Scho¨ningen (Thieme 1996), Dmanisi (Georgia) (Bra¨uer et al. 1995; Henke et al. 1995; Gabunia et al. 1999a, b, 2000, 2002; Vekua et al. 2002; Lordkipanidze and Vekua 2006), and many non-European and Eurasian sites (Delson 1985; Rightmire 1990; Franzen 1994; Johanson and Edgar 1996; Delson et al. 2000; Brunet et al. 2002; Schwartz and Tattersall 2002; Harvati and Harrison 2006), and the astonishing fossils from Flores (Indonesia) (Brown et al. 2004; Aiello 2010; Falk 2011) demonstrate that paleoanthropology is a field of research with never-ending surprises and new perspectives, albeit with never-ending problems. To say that the sample is too scarce is indeed right when we compare the fossil record with the assumed size of paleopopulations, and how about the number of recognized taxa? Foley asked in 1991, “How many hominid species should there be?” and again 15 years later, when there were claims of 28 hominin species (Foley 1991, 2005). Through highly elaborate comparative modeling, Foley concluded among other things that “it can be seen that the rate of discovery has rapidly increased in the last half-century, and there is no sign of an asymptote. To this extent, it may be proposed that we are still underestimating the number of hominin species” (Foley 2005, p. 69). This may have been a shock for “lumpers,” but some sentences later he says: “In considering the extent to which our knowledge of hominin evolutionary diversity is a challenge to how confident we are that the pattern is ‘real’, we come away with the conclusion of moderate confidence” (Foley 2005, p. 69). While we may underestimate the number of hominin species in the earlier periods, the “full diversity is not yet known even for later periods. What is almost certainly not the case is that we are overestimating diversity” (Foley 2005, p. 70). Good news for excavators and for laboratory scientists too. However, new fossils are not only solving problems but are raising new questions and providing new answers to that had seemed to have been solved. Here I mention two outstanding cases, both, interestingly enough, from Asia: One of the best illustrations of the phrase “humans are animals who wonder intensively and endlessly about their origin” is partial skeletons of nine hominin fossils (including one complete cranium) from Flores (Indonesia). The “Flores Man” represents a – possible – new species, Homo floresiensis (Brown et al. 2004). The most complete individual from the Liang Bua Cave, LB1, was nicknamed the “hobbit” due to its extremely small body size (106 cm) and cranial capacity (380 cc). The unusual anatomy of the fossils caused vehement discussion (e.g., on microcephaly, Laron syndrome, congenital hypothyroidism), and some skeptics regarded LB1 and LB6 as cretins; however, the pathological diagnoses have been largely falsified (Falk et al. 2007; contra, e.g., Martin et al. 2006). Given the case that genetic mutations, diseases, and growth disorders do not apply, the Flores hominins are most reasonably (or better: plausibly) explained as “Late-surviving species of early Homo” (5-year overview of H. floresiensis research in Aiello 2010). Public interest was unbelievably intensive due to the striking features of the fossils, and the unusual archaeology of the site, as well as to the diagnostic controversies and claimed skulduggery – a godsend for public media. Enormous scientific interest, and huge media hype, brought the tiny fossil remains from the Denisova Cave (southern Siberia) to fame. Paleogenetic research using DNA extracted from Page 45 of 84

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a finger bone revealed that this individual was from a group (hominin form) that shared a common origin with Neanderthals. Reich et al. (2010, abstract) conclude that “this population was not involved in the putative gene flow from Neanderthals into Eurasians; however, the data suggest that it contributed 4–6 % of the genetic material to the genomes of present-day Melanesians.” The authors suggest that the “Denisovans” may have been a widespread hominin population in Asia during the Late Pleistocene. The morphology of a single tooth, whose mitochondrial genome resembles that of the finger bone, suggests an evolutionary history apart from both Neanderthals and modern humans (Gibbons 2011). The floor is wide open for discussion! Or, to put it in Jonathan Marks’ words: “Fossil genomics is opening new windows to the past. But the view through them isn’t as clear as we like to think” (Marks 2012, p. 1).

Our Ancestors’ Great Leap Forward: Changing Explanations No doubt, the half-life of our theoretical models is very short. But there has undoubtedly been enormous progress, on balance. Besides the paleontological fieldwork, which has also produced valuable data for the reconstruction of the ecological niches of our ancestors (Bromage and Schrenk 1999), research in primatology has become increasingly important for anthropological modeling (Martin 1990; MacPhee 1993; Fleagle 1999; Groves 2001). Thanks to Louis Leakey’s encouragement, Jane Goodall, Diane Fossey, and Birute Galdikas started their primatological field researches many decades ago. Their results revolutionized our thinking on primate behavior, and this concept has been enlarged by many other field and laboratory primatologists (see, e.g., research projects of Cheney and Seyfarth; Premack, Fouts, Savage-Rumbough, de Waal, and the working groups of the Max Planck Institute of Evolutionary Anthropology in Leipzig, Germany). The paradigm of behavioral ecology and sociobiology has shaped our hypotheses on food choice, foraging patterns and food detection, as well as on food sharing and intra- and intergroup relations. It must be mentioned briefly that paleoanthropology as a multidisciplinary research field also brings the major events of primate evolution into focus, to disentangle the evolutionary trends in primate evolution, and to detect our constitutional preadaptation/predisposition (see Vogel). Weighty volumes have been edited, e.g., by Fleagle and Kay (1994), Delson et al. (2000), Hartwig (2002), Ross and Kay (2004), Wood (2011), and Begun (2013), proving that “the study of anthropoid origins continues to be a lightning rod for research in paleoanthropology” (Ross and Kay 2004, p. vii). As the focus of this overview is foremost on hominins, let’s look briefly at the evolution of bipedal walking as the assumed initial step into humanity. Despite the fact that bipedalism has evolved independently multiple times in primates, and this transition is deeply rooted in the primate behavior, in nonhuman contexts, it is merely facultative, not habitual or obligate. Since Darwin’s (1871) Freeing of the Hands hypothesis, the emergence of upright posture and bipedal gait has been discussed in many contexts, proposing alternative triggers and constructing alternative scenarios. Here are some of them: The Infant Carrying hypothesis by Etkin (1954); The Watching Out hypothesis by Dart (1959); The Aquatic Ape hypothesis, initiated by Alister Hardy (1960), presented in detail by Elaine Morgan (see 1997); The Carrying Food or Provisioning hypothesis by Hewes (1961); The Reaching for Food hypothesis by Jolly (1970); The Orthograde Scrambling hypothesis by Sugardijto and van Hoff (1986); The Display Hypothesis by Chaplin et al. (1993); The Scavenging Hypothesis by Blumenschine and Cavallo 1992 [see earlier untested versions by Eiseley (1953) and Bartholomew and Birdsell (1953)]; The Thermoregulation hypothesis (Ward and Underwood 1967; Wheeler 1984, 1991a,b); The Throwing hypothesis (Kirschmann 1999; Dunsworth et al. 2003; Young 2003); The Amphibian Generalist Theory by Niemitz (2002, 2004, 2010); and The exploitation of retained locomotor behavior hypothesis (Thorpe et al. 2007). Page 46 of 84

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While some of the hypotheses/theories are based on monocausal explanations (which shouldn’t be regarded per se as most parsimonious solutions), others are more complex and multifaceted, taking into account new paleoanthropological findings and biomechanical and energetic aspects of the anatomy of early hominids, as well as ecological and nutritional prerequisites and evolutionary psychological components. Though some proposals of primary “causes and consequences” seem quite plausible, it must be remembered that “plausibility” is an inadequate quality criterion to explain derived features (Foley 1987; Foley and Gamble 2009). The fatiguing, and in retrospect almost absurd, discussion on “facts and fiction” in regard to the Aquatic Ape Theory (Roede et al.1991) should remind us that it is not necessary to discuss each conceivable proposal in this field (see Stoczkowski 2002; Henke 2007a, b, 2010a). Scientific explanation, as opposed to mere narration or “just so stories” and myths, has to invoke lawlike regularities connecting causes and effects and to aim to a concise hypothesis testing or at least quasi-hypothesis testing (see Vogel 1975; Foley 1987; Henke and Rothe 1994, 1999a, 2005). Studies on the evolution of social-behavioral systems, kin selection, intersexual and intrasexual selection, cognitive abilities, tool using and tool making, Machiavellian strategies, competition, coalitions, and alliances, which is the total complexity of social systems in primates, especially in apes, have become essential for paleoanthropological modeling (Foley 1987, 1995a, b; Tattersall 1998, 2011; Eckardt 2000; Henke and Rothe 2003; Henke 2003a, 2008; Rothe and Henke 2005; Henke and Herrgen 2012). Besides primatological field studies, which have given us a totally new view on the cultural capabilities of nonhuman primates (Goodall 1986), there is much to learn about our brains and the development of language and our emotions from all kinds of laboratory research [e.g., molecular biology (O’Rourke et al. 2000; Relethford 2001; Enard 2005), psychobiology (Cartmill 1990a, b; Mithen 1996; Tomasello 1999; Withen 2000; Call and Tomasello 2008; Sommer 2007a, b; Sterelny 2012; Henke and Herrgen 2012)]. There is challenging news from the paleogenetic labs: Various genes are implicated in specifically human capabilities, e.g., language capabilities as indicated by FOXP2 (Enard et al. 2002; Enard 2005); autism (Green et al. 2010a, b); mental capacities (by Human accelerated regions – HAR; on abnormal spindle-like microcephaly-associated protein, ASPM (Pollard et al. 2006; Pollard 2009); on myosin heavy chain 16 (MYH16) is associated with masticatory structures (Stedman et al. 2005; overview in Jobling et al. (2004). Varki and Altheide (2005) are “Comparing the human and chimpanzee genomes: Searching for needles in a haystack.” I’m sure they will find many and inspire the field of human evolution tremendously. It seems – to say it cautiously – that ancient DNA findings have recently solved one of the “oldest questions” in paleoanthropology that remained unsolved for more than 150 years. After the excavation of the name-giving fossils from the Neander Valley, near D€ usseldorf in Germany, the “role of the Neanderthals” is subject to intense discussion (Spencer 1984; Stringer and Gamble 1993; Henke and Rothe 1994, 1999b; Tattersall 1995; Krings et al. 1997; Wolpoff 1999; Relethford 2001; Finlayson 2004; Harvati and Harrison 2006). As has been shown above, also heavily debated are the “Out of Africa” models, with and without hybridization: the Assimilation model and the Multiregional model (see above). After never-ending and often contradictory discussions on molecular biological results assuming a total replacement of all archaic non-African populations by anatomical-modern Homo sapiens dispersing from Africa (see, e.g., Henke 2005; Relethford 2009; Cartmill and Smith 2009), and after many supposedly “infallible” statements that there was no hybridization of Neanderthals and modern humans (e.g., cell cover: “Neanderthals Are not Our Ancestors” (Krings et al. 1997), now – what a surprise – the message is that “Neanderthals bred with modern humans” (Green et al. 2010a, b). Paleogeneticists from Harvard and the MPI EVA, Leipzig wrote: “Comparisons of DNA sequences between Neanderthals and present-day humans Page 47 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

Fig. 12 Conceptions of modern humans as animals which have culture as an evolved constitutional – tradigenetical – component (Designed by Herrgen 2008; adapted from Henke and Herrgen 2012)

have shown that Neandertals share more genetic variants with non-Africans than with Africans. This could be due to interbreeding between Neandertals and modern humans when the two groups met subsequent to the emergence of modern humans outside Africa. However, it could also be due to population structure that antedates the origin of Neandertal ancestors in Africa” (Sankararaman et al. 2012, abstract). Here is apparent strong support for the recent interbreeding hypothesis. Will this be the end of discussion? Time will tell!

Behavioral Modernity: What Pushed Us into Another League? As shown above, the conceptual transition toward the “New Physical Anthropology” sensu Washburn (1951) and the steady optimization and increase of methodological approaches and technical skills during the last 60 years have succeeded in explaining us as “another unique species,” to repeat Foley’s paradox (Howell 2003; Fuentes 2010; Larsen 2010; Stini 2010). Paleoanthropologists and their colleagues from neighboring disciplines succeeded in explaining in biological terms the specific morphological and physiological features that set us apart from other primates, e.g., upright bipedal walking, orthognathy, extensive neencephalization, reproductive physiology and biology, loss of body hair, and a wide set of further traits, including skin colors; the latter is insofar important as it breaks racial prejudice (see Jablonski and Chaplin 2010). Paleobiologists have solved [the] questions of when, where, and how these specific human patterns evolved, and sometimes “why” too. The most contentious answers are those on causes and consequences; in other words, we have a broad knowledge (or rather think we do) of the selective advantages of the human adaptive morphophysiological pattern. Tattersall (2006, p. 155) stressed wisely, that the acquisition of novelties cannot be driven by natural selection, which can only favor new structures after the fact, and explains subsequently: “. . .that any novelty has to rise initially as an exaptation [synonym for preadaptation, add. W.H.], a structure existing independently of any new function for which it might later be co-opted.” Paleoanthropologists have reached wide consensus on the long-term channeling of pathways in primate evolution. They have built up plausible scenarios on the evolution of uprightness and bipedal walking, on the formation of a gracile masticatory apparatus, and on the excessive increase of cranial capacities. So far so good; but evolutionary anthropologists also have to explain our

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special behavioral pattern (see Fig. 12). They have to elucidate how our specific human information and social systems arose, how humans reached their unique cognitive abilities for name-giving thinking processes, for verbal speech, for extremely complex social traditions, for an extremely complex Machiavellian intelligence, and for the capability of environmental buffering (overviews in Vogel 1975; Withen 2000; de Waal 2001; Rothe and Henke 2005; Ga¨denfors 2003; Mithen 2005; Tattersall 2006, 2011; Henke 2007a, b, 2008; Klein 2009; Henke and Herrgen 2012; Sterelny 2012; Henke 2014 in print). The challenge is also to explain the total pattern – human biology and culture (or better all cultural abilities!) – and to decipher the evolutionary factors and environmental influences that triggered the transitional process. After decades of very successful deciphering of the evolutionary trends within the order of Primates that led to the evolution of our genus Homo, we are – after a long “approach-run” – currently faced with the fundamental challenge to reconstruct the evolution of behavioral modernity, sometimes called “humanization,” as the last step of the process of “hominization”; both terms sound like a teleological program, what they aren’t; evolution has no goal! During the last decades, there has been done much innovative inter- and multidisciplinary research to get the right answers to ancient anthropological questions: How could an evolutionary process bring about a culturally dependent primate or animal rationale (sensu Artistotle) rsp. animal symbolicum (sensu Cassirer 1923–1929)? (See Herrgen 2008; Henke and Herrgen 2012; Henke 2014 in print.) It is becoming significantly evident from primatological research that neither tool using nor tool making, nor hunting, nor food sharing, nor social intelligence and coalitions, nor Machiavellian intelligence, is a unique feature of Homo sapiens. So human biologists, cognitive psychologists, and primatologists had to look for other traits which set us apart. The crucial question is: What pushed us into another league? The explanation has to come by “Darwinian” thinking (Sommer 2007a, b), as evolutionary anthropologists become increasingly critical about those caged in cultural prejudices. The uniquely human behavioral pattern which made our species so successful, which we call behavioral modernity, is commonly explained as a change in the intrinsic cognitive competence of modern humans. It is described in terms of new capacities for cognitive breakthroughs, like evolution and/or perfection of language, meaning creation (synonyms are theory of mind or mind reading), and symbol use (symbolicity or symbolic thoughts). Kim Sterelny’s definition of behavioral modernity is the following: “humans became behaviourally modern when they could reliably transmit accumulated informational capital to the next generation, and transmit it with sufficient precision for innovations to be preserved and accumulated” (Sterelny 2011, p. 809; see also Sterelny 2012; Henke 2014 in print). The last step of becoming human and even humane, i.e., an animal with the ability to empathize, to understand the intentions of others, to plan and to deceive, and to use symbols and language, is a recent topic of research. Three abilities of modern human behavior have come under special scrutiny: language, theory of mind, and symbolism (for a more complex approach, see, e.g., Cartmill 1990a, b; Noble and Davidson 1996; Mithen 1996, 1998, 2005; Tattersall 1998, 2002, 2006, 2012; Tomasello 1999; Withen 2000; Crow 2002; Ga¨rdenfors 2003; Henshilwood et al. 2004, 2009; Wuketits and Antweiler 2004; Haidle 2006; Balter 2008; Cartmill and Smith 2009; Conard 2009, 2010; Klein 2009; Henshilwood and d’Errico 2011; Henke 2014 in print). Cartmill and Smith (2009, p. 416) state: “it seems reasonable to think that language preceded the onset of art, religion, and other sorts of symbolic behavior in the course of human evolution.” But how do we know this is fact? Research on paleogenetic features as FOXP2, morphological studies on hyoid bones, and cranial endocasts currently give little hope of proving this. No doubt, we are on very difficult terrain here.

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And as regards mind reading and symbolism, there has been much progress from artifacts, mentifacts, and sociofacts (see Posner 1993; Renfrew and Zubrow 1994; Holzm€ uller 1997; Renfrew 1998; Mithen 1998; Marean and Thompson 2003; Wuketits and Antweiler 2004; Bar-Yosef and Zilha˜o 2006; Kappeler and Silk 2009; Klein 2009; Conard 2010; Nowell 2010; Sousa and Counha 2012; Sterelny 2012). However, detractors ask how we can reconstruct arbitrary, socially constructed conventions of our ancient Pleistocene antecedents, if understanding of symbols is often restricted to persons sharing a common cultural background, i.e., the same “cognitive map”? Bredholt-Christensen and Warburton (2003, p. 40) caution, referring to the insider/outsider debate, that we run the following risk: “In attempting to understand the people under study we create categories by which we distinguish phenomena of their culture. On this basis (prehistoric “symbols” being “our” interpretation of “their” world as “we” see it).” The authors emphasize that this doesn’t mean that posing questions about prehistoric symbolism and archaeological differentiations are irrelevant and illegitimate; however, such queries can only be answered on an etic, not on an emic, level (Bredholt-Christensen and Warburton 2003, p. 39; for more discussion on more “Criteria of Symbolicity,” see positions papers of the 9th Annual Meeting of the EAA, 2003; Bouissac 2003). When discussing “how Homo became sapiens” (see Ga¨rdenfors 2003, book title) and how our ancestor developed full modern behavioral modernity, we are faced with a major problem of anthropology (Marean and Thompson 2003). By an integrated multidisciplinary approach, including paleoanthropology, archaeology, primate ethology, ethnology, cognitive psychology, and evolutionary genetics, we can hope to find answers to the most intriguing question: How could the self-organizing process of hominization bring about a culturally dependent organism that has “culture as its nature” (sensu Vogel 2000)?. From a sociobiological perspective, we have to talk about “culture via nature” as there are convincing arguments “that culture has been so successful biologically because it gives humans improved possibilities for coping with the perils of life and so increases the chance of survival. [. . .] Whatever defines culture, it is based on adaptive imitation, or “imitation of the fittest”” (see Voland 2000b, p. 196). To perform the imperative “Nosce te ipsum!” we need a concentrated and concerted approach by all evolutionary biological and cultural sciences, taking a strictly “Darwinian perspective” and with special focus on the “human niche” of Homo sapiens. We have to know much more about the totality of the special conditions of early anatomical-modern Homo sapiens hunter-gatherers that made their lives – and survival – possible; otherwise, we will never understand the “constitutional preadaptation” affecting the final step to “behavioral modernity” and our specific “design” which evolved without a “designer.” To prove this Darwinian message is more than enough motivation for future research on the origin of the human mind.

Conclusion Don’t Expect Too Much: We Are Just Modeling! When we sum up the history of paleoanthropological research, it becomes evident that the paradigmatic change initiated by Darwin’s realization of a true historical genetic kinship of all living organisms stimulated enormous interest in questions of human origins. Those research subjects that promised to solve the enigma of anthropogenesis in Darwin’s days were the natural sciences (paleontology, geology, comparative anatomy rsp. morphology, zoology, and human biology), on the one hand, and the social sciences of prehistory and ethnology, on the other. The “conglomerate” of natural sciences contributed to a pretty slow formation of “human paleontology” rsp. “paleoanthropology” and was joined at its very beginning by the social Page 50 of 84

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sciences. However, the segregation of the diverse disciplines in the natural, medical, and social faculties hampered an integrative approach, even apart from the skepticism toward, and even rejection of, Darwinian evolutionary theory by a great part of the scientific community. Rudolf Virchow was by far no exception. In retrospect, it is apparent that paleoanthropology long failed to adopt a Darwinian evolutionary approach. Its methodology remained – with some commendable exceptions – mainly casuistic, descriptive, and nonanalytical. This didn’t even change at the beginning of the twentieth century, when classical genetics began after the rediscovery of the Mendelian laws. Notably, even after the formation of the “Modern Synthesis,” (paleo)anthropology perpetuated long-standing erroneous conceptions (i.e., polygenism, orthogenism, Eurocentrism, ethnocentrism, social Darwinism, racism). It can be concluded that paleoanthropology remained “simple minded” until after World War II, without conceptual integration of Darwinian and Neo-Darwinian concepts. However, subsequently, evolutionary biology has become the fundamental superstructure, as already explicitly formulated by the population geneticist Theodosius Dobzhansky (1937) and his outstanding colleagues from other biological sciences. As a recognizable, valid subject of evolutionary biological science, paleoanthropology was established for the first time in the early 1950s by Sherwood L. Washburn (1951, 1953). The conceptualization and foundation of paleoanthropology/paleobiology as a subdiscipline of the “New Physical Anthropology” was correlated with the adoption of the concepts of Darwinian theory and those of the “Modern Synthesis.” This was followed by a period of severe problems in the recognition of taxic diversification and speciation processes when paleoanthropological findings increased exponentially and the fossil record and the “Modern Synthesis” came under critical observation (Eldredge and Gould 1972; Tattersall 1998, 2000a, b; Foley 2001; see also Wolpoff 1996–1997). Once again, paleoanthropology had a slow start compared to other evolutionary sciences. However, due to crucial conceptual support by outstanding scientists, e.g., Sherwood L. Washburn, F. Clark Howell, Louis S. B. Leakey, Phillip V. Tobias, and many other enthusiastic colleagues, the field was revivified by new fossils and essential findings from field and laboratory research. Paleoanthropology has now evolved to become a complex research strategy of evolutionary biology that integrates all facets of comparative functional and evolutionary anatomy, primatology, behavioral ecology, cognitive primatology and sociobiology, molecular and population genetics, paleogenetics, as well as earth sciences, archaeology, archaeometry, and ethnology. Since the 1960s and 1970s, there has been developed a large body of empirical knowledge related to international collaborative networks, all underpinned by epistemological discourse. The enhanced armamentarium of perspectives and methodologies was drawn largely from the diverse natural sciences and from conceptual progress in archaeology and ethnology too. Paleoanthropology benefited from the high innovativeness of the natural and associated social sciences and from the increasing complexity of its approaches, as well as from exceptional fossils, surprising findings, and a vast public interest due to new media. Embedded in evolutionary biology, and adjacent to a broadly based scientific field with theoryguided empirical approaches, paleoanthropology has finally since the 1970s become a mature science. The consistent integration into the wider set of biological sciences underpinned by the revised System Theory of Evolution provides a road map for a successful research design in paleoanthropology. Students should follow this program to achieve reliable and valid findings and to build up reasonable scenarios of the past. However, one should have Robert Foley’s four “pathways to the past” always in mind: “Neither theory nor models on their own are sufficient in palaeoanthropology, for they would amount to composing the present on the past. [. . .] Just as the Page 51 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

fossils are mute without the frame work of theory, so, too, the theory is self-confirming when not put to empirical tests.” He suggests testing the strength of “inferences,” using “isolating techniques,” and applying “probabilistic” and “comparative biological” tests. Though this seems to be “the appropriate framework for investigating patterns in hominid evolution” (see Foley 1987, p. 90), it’s necessary to emphasize that the complexity of human origins can only be understood correctly if we are always aware of our potential prejudices.

Always Being Aware of Biases and Misunderstandings Paleoanthropologists should always be aware of the principal aims of scientific work (Mahner and Bunge 2000). This allows them to avoid the pitfalls of naı¨ve storytelling and of obscuring their aims with narrative. In spite of the paradigmatic change to a teleonomic explanation of life, there is plenty of evidence that even though “scientific thought is subject not only to the force of empirical knowledge, there doubtlessly is under changing conditions much impact from social constraints” (Stoczkowski 2002, p. 1; Henke 2010a; Sarasin and Sommer 2010). In his “Explaining Human Origins – Myth, Imagination and Conjuncture,” the prehistorian and archaeologist Wiktor Stoczkowski (2002) presents a table of distinctive characteristics of humans in general and of primitive humanity in particular, as described in our sample of hominization scenarios. The characteristics most often mentioned as triggering human evolution are ranked by their assumed importance: tools, bipedalism, free hands, language, social life, voluminous brain, superior mental faculties, reduced canines, cooperation, sexual division of labor, food sharing, hunting, perfectibility, family organization, productive success, prolonged childhood, absence of estrus, and carnivorous diet. Even when neglecting obviously outdated “traditionalist” and “Lamarckian” approaches to explain anthropogenesis in Darwinian terms, Stoczkowski (2002, p. 198) states that “contrary to what is often thought, scientists do not draw their conclusion from empirical data, any more than they rewrite history in terms of prevailing ideology.” Since the French original of this work, Anthropologie naı¨ve, anthropologie savante was published 20 years ago, in 1994, I am convinced that in saying this, the author has remained in ignorance of much of the theoretical and analytical progress made by current paleoanthropology. Stoczkowski clearly had not considered the more recent phase of “empirical tests” in modeling the past, although it is true that earlier human origin models were one sided and monocausal and missed the required complexity. This applies, for instance, to the “Man the Hunter” model of Lee and DeVore (1968), the “Food sharing behavior” model of Isaac (1978), the “Hunter-Gatherer” model of Zihlman and Tanner (1978), the “Pair bonding” model of Lovejoy (1981), the “Nutrition strategy” model of Hill (1982), and the “Scavenging” model of Blumenschine and Cavallo (1992). This is not the place to discuss the validity of analogue and concept models or the theoretical patterns of recognition techniques and the appropriateness of optimality principles (overviews in Foley 1987, 1995a, b; Henke and Rothe 1994); but it should be noted that more recent models of human origins, e.g., Aiello and Wheeler’s (1995) “Expensive tissue hypothesis,” O’Connell et al.’s (1999) “Grandmothering hypothesis,” and Wrangham et al.’s (1999) “The Raw and the Stolen; Cooking and the Ecology of Human Origins” model take into account the complexity of the network of causes for social transitions. Further, paying attention to life history, energetic and ecological components of the ecological niche concept have caused much improvement and progress (overviews in Henke 2007a, 2010c; Henke and Herrgen 2012; Kaplan et al. 2000). Foley and Gamble (2009, p. 3267) are aware that “the evolution of ‘human society’ is underpinned by ecological factors, but these are influenced as much by technological and behavioural innovations as external environmental change.” Page 52 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

However, our answers to the why-questions are still contentious and possibly will remain that way. Additionally, what has previously remained unmentioned is that some hominization models were severely flawed by the fact that anthropology was until recently a male-dominated science. The comparison of the prevailing male perspectives with views by feminist researchers demonstrates that paleoanthropology, prehistory, and sociobiology were in particular influenced by androcentrism. Adrienne Zihlman and Nancy Makepeace Tanner were the first (in the 1970s) to complain about androcentric misinterpretations of the female role in human evolutionary history. Their critique of the “Man the Hunter” scenario was a groundbreaking event for feminist anthropology (e.g., Tanner and Zihlman 1976; Zihlman 1978, 1981; Linda Fedigan 1986, 1992; Margaret Ehrenberg 1989; Inge Schro¨der 1994; Melanie Wiber 1997; Lori Hager 1997; Londa Schiebinger 1999; James M Adavasio et al. 1999; see also Henke et al. 1996; Henke 1997). Linda Fedigan (1992, p. 306) put it this way: “The assumption that females are losers in competition between the sexes, although widespread in sociobiological literature, does not seem to me inherently necessary to evolutionary theories, precisely because it is a cultural assumption rather than a biological given.” In this context, one should also ask: Are there still other biased perspectives that require a closer review by science history? This is quite likely, as some good research work has already been done on the presentation of “lost worlds” and paleoanthropological ideas in print media and movies, as well as in scientific art, popular scientific illustrations, and museum exhibitions (see, e.g., Ickerodt 2005; Kleeberg et al. 2005; Hurel 2006; Crawford 2007; Sommer 2008; Sommer et al. 2008; Goodall 2009; Kort and Hollein 2009; Sarasin and Sommer 2010; Ingensiep 2013). Furthermore, while it is well known that Christian doctrine and other religious beliefs have demonstrably influenced research on and discussion of human origins in the past, the impact of social and political ideologies on paleoanthropology is a largely unexplored field that offers great possibilities for future historical research. There is, especially, a need to study the impact of sociocentrism, ethnocentrism, and nationalism on interpretations of human origins, as well as national and regional museological conceptions (see, e.g., Schmalzer 2008, Africa; Vickery 2013; Durband (2009) Southeast Asia and Australia; Durband 2009, excellent overviews to the issue in Sarasin and Sommer 2010). A further issue of historical interest is the relationships of colonialism and paleoanthropology; Goodrum (2009, p. 349) remarks that: “The implications of European and American researchers conducting excavations and removing hominid fossils from Asian and African countries during and following the colonial period is another subject that remains largely unexplored.” And one can bring the same question to recent times: How has the experience of outstanding foreign students trained at American and European universities translated back to their native countries and their subsequent research? Did they bring back new perspectives, and have their researches specially influenced paleoanthropology and their own societies? (See, e.g., Sperber 1990; Lille and Kennedy 2010.) Knowledge Commits to Responsibility! Besides the diverse “-ism” issues mentioned above, there is a vast “construction site” in paleoanthropology based on transmitting facts – and not fiction – about human evolution to the general public. Paleoanthropologists benefit from enormous public interest in their field; but big problems can arise if the preconceptions of that public are wrong or if their understanding is merely superficial. Transmitting scientific findings to the public is not an easy task and demands great precision; the difficulties involved are proven by the daily experience of lecturers and teachers. Empirical-didactical research by Graf and Soran (2010) provided disillusioning results: Evolution Page 53 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

as pattern and process is even today very poorly understood and misinterpreted by the broad public, even though the basic theoretical framework is biologically undisputed. There is a reluctance to understand that there are still unsolved problems out there; science is a process (see Toepfer 2011; Wrede and Wrede 2013). Of greatest relevance is that there is widespread misunderstanding of evolution itself [e.g., that “evolution” aims the preservation of species; evolutionary adaptations are adaptations to recent environments; organisms are perfectly adapted; humans are the crown of evolution; evolution is a simultaneous progress and has an aim; nature is harmony; and nature is “good” and has morality (overview in Henke and Herrgen 2012)]. All this is of relevance for paleoanthropology, since one of the main general insights from the Darwinian paradigm is that we, as modern humans, have to take responsibility (“Das Prinzip Verantwortung,” formulated by Hans Jonas; see Altner 1981a), because we are the single organism on earth with morality (Vogel 2000; Cela-Conde and Ayala 2004; Bischof 2012). Washburn (1968, cit. by Fuentes 2010, p. 5) wrote that “human biology has no meaning without society [. . .] the evolution of man can only be understood as a biosocial problem.” A proper understanding of evolution is thus essential for modern societies; and when taking responsibility is a social concern, it is clearly necessary to publish scientific results on human evolution not only in scientific journals but also in the public media. Still, while sophisticated popular scientific writing is highly welcome and helpful (see call by Howell 2003; Fuentes 2008, p. 5), superficial and callow fossil – and journalism-driven science initiated by pure sensationalism – is counterproductive. What we need to do in our popular nonfiction is, as Howells (2003, cit. in Fuentes 2010, p. 5) urged, to “adopt modern perspectives of an emergent evolutionary biology, and practice analytical, comparative, and experimental methods, relevant to elucidation of the nature and roots of the Human condition.” Howells injunction remains the standard, and fortunately there are currently excellent popular expositions in the bookstores, e.g., Tattersall’s (2012) The Masters of the Planet and Stringer C (2013) Origin of our Species.

Yes, Science History Matters! With the methodological principles of the biological and neighboring sciences in mind, paleoanthropologists should also be aware of science history. In the words of Theunissen (2001, p. 147): “That ‘history matters’ is perfectly obvious if it is taken to mean that the present cannot be understood without reference to the past.” Although this statement might seem trivial, there is a dilemma, mentioned by Foley (1987); the past is a “foreign country” and our forerunners did things differently there. The challenge of paleoanthropology is to improve our scientific methodology, to learn more about us and our origin, in order to reach a biological and sociobiological selfconception (Vogel 2000). The historicist approach may give rise to reflexive doubt, so don’t expect too much. Dennell (2001, p. 64) is regrettably right when saying: “Whilst we might like to think that palaeoanthropology is a discipline that unifies humanity and helps combat racial, sexist, and other types of prejudice simply because of its focus on the origins of humankind, we should not forget it did the opposite for at least the first half of the twentieth century.” The confidence of being on the right road raises the risk of complacency. And therein lies the essential reason why history really matters; one should never be too comfortable for too long with an idea (Dennell 2001). What is needed is a real and intense dialogue between the many disciplines that cooperate to unravel the process of human origin. The history of paleoanthropology teaches us, in all its facets and complex details, quite how great a challenge of evolutionary biology reconstructing our origin is. McHenry (1996, p. 86) has put it neatly: “One needs to make the best of our tiny sample of life in the past, to be open to new discoveries and ideas, and to enjoy the pleasure of learning and changing.” No one will explain our human origins, if we don’t – and what a fascinating challenge! Page 54 of 84

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_1-7 # Springer-Verlag Berlin Heidelberg 2013

Cross-References ▶ Etter: Patterns of Diversification and Extinction ▶ Groves: Species Concepts and Speciation: Facts and Fantasies ▶ Gutmann & Weingarten: Paleoanthropology and the Foundation of Ethics: Methodological Remarks on the Problem of Criteriology ▶ Haidle: Archaeology ▶ Hardt, Hardt & Menke: Paleoecology: An Adequate Window on the Past? ▶ Holloway: The Evolution of the Hominid Brain ▶ Lieberman & McCarthy: The Evolution of Speech and Language ▶ Ohl: Principles of Taxonomy and Classification: Current Procedures for Naming and Classifying Organisms ▶ Sussmann & Hart: Modeling the Past: The Primatological Approach ▶ Vrba: Role of Environmental Stimuli in Hominid Origins ▶ Wuketits: Charles Darwin, Paleoanthropology, and the Modern Synthesis

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Wood B, Martin L, Andrews P (eds) (1986) Major topics in primate and human evolution. Cambridge University Press, Cambridge Wrangham RW, Jones JH, Laden G, Pilbeam D, Conklin-Brittain N (1999) The raw and the stolen. Cooking and the ecology of human origins. A theory of human life history evolution. Curr Anthropol 40(5):567–594 Wrede P, Wrede S (eds) (2013) Charles Darwin: Die Entstehung der Arten. Kommentierte und illustrierte Ausgabe. Wiley-VCH Verlag, Weinheim Wuketits FM (1978) Wissenschaftstheoretische Probleme der modernen Biologie. Erfahrung und Denken. Schriften zur Fo¨rderuung der Beziehungen zwischen Philosophie und Einzelwissenschaften, Bd. 54. Duncker & Humblot, Berlin Wuketits FM (2009a) Jean-Baptiste de Lamarck (1744–1829). Sein Werk und seine Bedeutung f€ur die Wissenschaft vom Leben. Naturw Rdsch 62:621–629 Wuketits FM (2009b) Charles Darwin (1809–1882) und seine Verdienste als Naturforscher außerhalb der Evolutionstheorie. Naturw Rdsch 62(6):296–305 Wuketits FM (2010) Tarnen, ta¨uschen, schwindeln – Wissenschaftsbetrug einst und jetzt. Naturwissenschaftliche Rundschau 63(11):578–581 Wuketits FM (2012) Spinner oder Wegweiser? Die Rolle von “Außenseitern” in der Wissenschaft. Naturwissenschaftliche Rundschau 65(11):575–580 Wuketits FM, Antweiler C (eds) (2004) Handbook of evolution, vol 1, The evolution of human societies and cultures. Wiley-VCH, Weinheim Wuketits FM, Ayala FJ (eds) (2005) Handbook of evolution, vol 2, The evolution of living systems (including hominids). Wiley-VCH, Weinheim Young R (2003) Evolution of the human hand: the role of throwing and clubbing. J Anat 202:165–174 Za¨ngl- Kumpf U (1992) Die Geschichte der ersten deutschen anthropologischen Gesellschaft. In: Preuschoft H, Kattmann U (eds) Anthropologie im Spannungsfeld zwischen Wissenschaft und Politik. Bibliotheks- und Informationssystem der Universita¨t Oldenburg (BIS) Verlag, Oldenburg Za¨ngl-Kumpf U (1997) Klaatsch, Hermann (1883–1916). In: Spencer F (ed) History of physical anthropology, vol 1 A-L. Garland, New York, pp 575–576 Za¨ngl-Kumpf U (1990) Hermann Schaaffhausen (1816–1893); die Entwicklung der neuen physischen Anthropologie im 19. Jahrhundert. Diss. FB Biologie, Universita¨t Frankfurt, pp S19–S32 Zihlman A (1978) Women in evolution. Part II: subsistence and social organization among early hominid. Signs 4(1):4–20 Zihlman AL (1981) Women as shapers of the human adaptation. In: Dahlberg F (ed) Women the gatherer. Yale University, New Haven, pp 75–120 Zihlman A, Tanner N (1978) Gathering and the hominid adaptation. In: Tiger I, Fowler HM (eds) The human revolution. Behavioural and biological perspectives on the origins of modern humans. University Press, Edinburgh, pp 212–231 Zmarzlik H-G (1969) Der Sozialdarwinismus in Deutschland-Ein Beispiel f€ ur den gesellschaftlichen Mißbrauch naturwissenschaftlicher Erkenntnisse. In: Altner G (ed) Kreatur Mensch. Moderne Wissenschaft auf der Suche nach dem Humanum. Heinz Moss Verlag, M€ unchen, pp 147–156 Zo¨ckler O (1860) Theologia naturalis: Entwurf einer systematischen Naturtheologie vom offenbarungsgla¨ubigen Standpunkte aus. Heyder & Zimmer Verlag, Frankfurt/M

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Zo¨ckler O (1876) Geschichte der Beziehungen zwischen Theologie und Naturwissenshaften mit besonderer Ber€ ucksichtigung der Scho¨pfungsgeschichte, Bd. 2. Von Newton und Leibniz bis zur Gegenwart. C Bertelsmann, G€ utersloh Zollikofer C, Ponce de Leon M (2005) Virtual reconstruction: a primer in computer-assisted paleontology and biomedicine. Wiley-Interscience, Weinheim

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Index Terms: Adaptation 40 Behavioral modernity 48 Comparative anthropology 17, 20 Darwinism, teleonomic explanation of life 7 Ecological niche 8, 19, 46, 52 Ethnocentrism 28, 51, 53 Eurocentrism 51 Exaptation 48 Hominization 49 Humanization 49 Hypothesis testing 3, 7, 47 Methodology 13 Migration 45 Modern Synthesis 8, 39, 41, 51 Narration 6, 47 Paradigmatic changes 13 Primatology 43, 46 Racism 30 Scenarios 46, 48, 52 Science history 3, 6–7, 13, 39–40, 42, 46, 48 behavioral modernity 48 Darwinian Revolution 7 historical approaches 3 hominid evolution and taxonomy 6 human evolution 46 hypothesis testing 3 Modern Synthesis 40 paradigmatic changes 13 physical anthropology 39 theoretical and methodological progress 13 theoretical deficits 42 Speciation 39 Systematics 39, 43 Taxonomy 6, 44 Theory deficit 41

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_2-3 # Springer-Verlag Berlin Heidelberg 2014

Evolutionary Theory in Philosophical Focus Philippe Huneman* Institut d’Histoire et de Philosophie des Sciences et des Techniques, CNRS/Université Paris I Sorbonne, Paris, France

Abstract This chapter surveys the philosophical problems raised by two Darwinian claims: the existence of a “tree of life” and the explanatory power of natural selection. The first part explores philosophical issues concerning the process of evolution by natural selection. After laying out the nature of selectionist explanations, their conditions, and some of their correlated properties such as fitness, we present the epistemic issues raised by such explanations. These include the role of optimality considerations and dynamical modeling, as well as the respective contributions of analytical explanation and historical narratives to evolutionary understanding. Then the metaphysical aspects of natural selection are examined: whether it is a law or supports natural laws; whether it is a cause, and if so, the cause of what. The consequences of the answers to these questions for scientific practice, and especially for current controversies about a possible extension or revision of the Modern Synthesis, are highlighted. The chapter then presents two classical controversies regarding the target and the limits of selective explanations – units of selection, adaptationism – in both cases pointing out the promises of explanatory pluralism. The third section considers issues raised by evolutionary patterns: first, the interpretation of the nodes in the tree of life, where the notion of species is controversial; then, the question of the relationship between macro- and microevolution, and, relatedly, the connection between putative processes and plausible patterns. Consequences for the current controversy about the fate of the Modern Synthesis are also explained. We further explicate issues raised by general features of large-scale phylogenetic patterns, such as increases in complexity, and the question of evolutionary contingency, and discuss the chances of an empirical solution to these longstanding puzzles. The last section considers some consequences of evolutionary theory for philosophical questions about human nature, given the rise of hypotheses on the universality of selectionist explanations; it is mostly concerned with epistemology and psychology.

Introduction The Darwinian theory of evolution provides a framework of explanatory strategies to explain diversity and adaptation in the living realm. Darwinian science suggested and justified two main claims: first, the existence of a “tree of life,” meaning that all extant living species are the historical results of common descent, and second, the selection hypothesis, meaning that one of the most important processes to account for those transformations is “natural selection.” Hence, Darwin’s theory added to the earlier life sciences a new explanandum (object to be explained) – phylogenesis – and a new explanans (way to explain) – natural selection – the latter of which could also serve as an explanatory device when applied to existing problems in those fields. The concept of evolution, then, having been solidly grounded in that of natural selection, could in turn explain aspects of diversity and adaptation. *Email: [email protected] Page 1 of 41

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Of course, the full consequences of Darwin’s two main claims were not recognized immediately; people were too much concerned with the two metaphysical antipodes of evolution versus creationism, and with the animal origins of man. It took almost a century to acquire the historical distance that enables us to fully appreciate the novelty of Darwinism. (On progressive extensions of Darwin’s theory, see Ospovat (1981) and Bowler (1989).) In the late nineteenth century August Weismann, by distinguishing between soma and germ line and postulating that there was no transmission of acquired characters, clarified the difference between Darwinism and Lamarckism and convinced his followers to regard only the germ line as the substrate of evolution, enabling the future integration of genetics with evolutionary biology. Weismann also demonstrated the impossibility of the theories of heredity and variation held by many biologists at the time, including Darwin himself, according to which hereditary traits could arise from within an individual organism’s cells and flow continuously from them. Heredity was a major theoretical problem for Darwinism after Darwin. After 1900, the Mendelians supported “particular” inheritance – i.e., inheritance conceived as the transmission of discrete “determinants” of traits, later to be called genes, which are randomly taken from the two parents in the case of sexual reproduction. This notion contrasted with the traditional concept, shared by Darwin, of a “blending inheritance,” according to which the offspring receives a mix of the values of the traits of each parent. Blending inheritance is problematic for Darwinism because it seems that with each generation change, the “best traits” – the ones that give the most advantages to their carriers – are diluted or lost in the mixing (except in the very improbable scenario where these carriers always mate with other carriers of the advantageous traits). Population genetics was developed in the 1920–1930s, especially by Ronald Fisher, Sewall Wright, J.B. Haldane, and Julian Huxley, as the science of the variation of gene frequencies in a population. Research in this field has shown that in the case of Mendelian inheritance, even a slightly advantageous gene will indeed increase in frequency in a population until its fixation. More generally, population genetics provided biologists with a mathematical model of the process of evolution by natural selection. Whereas previously, the Mendelian vision of organisms as mosaics of traits seemed to contradict the gradualist view of evolution as a kind of “continuous transformation” (Gayon 1998), the population genetic approach was now able to conciliate Mendelian genetic inheritance and Darwinian evolution, resulting in the form of evolutionary theory called the Modern Synthesis. (Mayr and Provine 1980) For this reason, population genetics holds a central status within evolutionary thinking, as indicated by the textbook definition of evolution as the “change of allele frequencies in the gene pool,” which clearly pertains to the field of population genetics. This central role of this field is not unanimously accepted today: many biologists, especially some of those working in the tradition of developmental theory and some ecologists, criticize the very framework of the Modern Synthesis, arguing that it leaves aside many important aspects of evolution, in particular developmental processes. Calls are being made for an “extended synthesis” (M€ uller and Pigliucci 2011) – by which is meant, among other things, that the process of evolution should be assumed to extend beyond the genes themselves (for instance, it should include cases of non-genetic inheritance that have recently been established and studied; e.g., Danchin et al. 2011 or it should include the molding of environments by organism themselves called niche-construction, Odling-Smee et al. 2003). But actually, many proponents of the Modern Synthesis, such as Simpson and Mayr, were not convinced themselves by its narrow definition. Labels aside, it seems important to ask whether allele frequency change constitutes evolution, causes evolution, or just indicates evolution. This philosophical issue appears to be at the heart of the interpretation of evolutionary theory and the assessment of any alternatives to the Modern Synthesis – which shows that, in the case of evolutionary biology, Page 2 of 41

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philosophical aspects are intertwined with contemporary scientific controversies, as this chapter will argue in detail. In order to grasp the new kinds of epistemological problems brought about by the two Darwinian contentions, it is useful to recall the features of the earlier biological framework that they replaced. The main explanans of diversity and adaptation before Darwin was, as we know, the notion of divine design, although alternative hypotheses were increasingly being proposed, especially the transformist theory of Lamarck, which was adopted by Saint Hilaire and many morphologists at the beginning of the nineteenth century. This design was invoked to account for some prima facie teleological features of the living world, such as the fine adaptation of organisms to their environment, the fine-tuning of the mechanisms of biological functions, or the proportions of individuals in various species and the geographical relationships between species. Divine design yielded simultaneously the individual designs of organisms, unlikely to be produced by the mere laws of physics, and the design of the entirety of nature that Linnaeus called the “economy of nature.” The selection hypothesis gave a powerful explanation of those two designs, since adaptations of organisms (Gardner 2009) as well as distributions of species in a population were plausible results of the process of natural selection (even if other mechanisms, such as Lamarckian ones, were also used by the first Darwinians). Selection, unlike divine design, explains adaptation as a fit between organisms and their environment (see below for further explication of this). The diversity of environments in which species find themselves implies a variety of adapted species; therefore, selection explains adaptation through what is called adaptive radiation. And finally, the striking similarity of forms between different species of the same genus, or even different genera of the same family, that has been noticed since the eighteenth century by authors like Buffon or Diderot, and then vindicated by, e.g., Geoffroy Saint-Hilaire, and the so-called “transcendental morphologists,” is explained by the fact that organisms of different taxa share a common ancestor – a fact that is entailed by the architecture of the tree of life. However, the rise of Darwinism did not bring about a complete shift in the questions and tools of biology. Rather than wiping out centuries of research in the science of life, Darwinism gave a new and coherent meaning to some accepted facts and descriptions. Instead of rejecting teleology outside science, it provided a way of interpreting teleological phenomena so that they did not depend upon non-naturalistic assumptions, such as hidden intentions on the part of organisms or their creator; it retained the results of traditional taxonomic efforts and conceived of the systematic proximities in the classification of species as historical entities, as Darwin himself noted at the end of The Origin of Species (even though, of course, the Darwinian view raised new questions and resulted in new criteria and methods for systematists; cf. Ghiselin 1980). Thus, evolutionary theory appears to us as the most successful and integrative framework for research strategies in biology generally. Before investigating the details of the philosophical challenges raised by the two Darwinian claims, it is useful to situate the evolutionary approach within the larger endeavor of biology. In this context, Mayr (1961) distinguished between two kinds of causes that can serve as answers to the question why. When asked “Why does this bird fly along the seashore to the South?” one can answer by pointing out its physiology, respiratory system, the diverse pressures on its wings, and the streams of air around it: these indicate the proximate causes of the bird’s flight. But one can also answer by emphasizing that the way the bird chooses to go to the South curiously corresponds to the old demarcation of the continents, implying that the migration trajectory is the result of natural selection acting on this species of bird. This is the ultimate cause of the bird’s flight towards the South. Notice that the proximate causes concern only one bird at a time, and that each bird is affected by them in the same way: they are generic causes. In contrast, the Page 3 of 41

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ultimate cause concerns the ancestors of this bird collectively, not only the one observed bird. In this respect, the two kinds of causes can be said to correspond to two kinds of biological disciplines. On the one hand, we have the sciences of the proximate causes: molecular biology, cellular biology, genetics, physiology, endocrinology, etc. On the other hand, we have the sciences of the ultimate causes, which are all those disciplines belonging to evolutionary biology: population genetics, quantitative genetics, behavioral ecology, systematics, phylogenetics, paleontology, etc. Having thus characterized evolutionary theory as a specific set of research programs within biology, and having defined those programs by their use of the hypothesis of natural selection, we can now put evolutionary theory in philosophical focus. This could, in principle, mean two things: either a focus on the philosophical problems raised by evolutionary theory, and on their putative solutions, or alternatively, a focus on philosophical problems that are illuminated by evolutionary theory. It could indeed be argued that the rise of Darwinism has been one of the most significant conceptual shifts in the history of science, and therefore has had tremendous impact on all areas of philosophy. However, most of this chapter will be concerned with the former theme: philosophical problems within the field of evolutionary biology. The last section will briefly sketch a few features of the latter. Philosophical issues in evolutionary biology can be grouped along two axes: first, in keeping with the distinction between the two main claims of Darwinism, there are issues concerning patterns (mostly, patterns captured in the structure of the tree of life) and issues concerning processes (mostly, natural selection). Second, philosophical issues may concern, foremost, our way of knowing things, in which case we refer to them as epistemological issues; or they may concern the things themselves, as exposed by science, in which case we refer to them as metaphysical issues. In the following, we will first address problems related to processes; these will essentially concern the nature and the limits of explanations that rely on natural selection. Some will be more epistemological, while others will be mostly metaphysical. In the second section, we will turn (less extensively) towards some problems regarding patterns; the discussion will be kept brief because many epistemological problems concerning patterns are related to methodological problems concerning proper classification, which are dealt with in other chapters of this book.

Evolutionary Biology: Philosophical Issues Concerning Processes What is a Selectionist Explanation? Selection, Population Genetics, and Fitness Natural selection is a process that is expected to take place in a set of individuals whenever the following requirements are fulfilled: (i) the individuals differ from each other; (ii) the traits that are different are hereditarily transmitted in such a way that the pattern of variation of traits in the new generation is not wholly different from that in the parent generation (e.g., taller parents tend to have tall offspring); (iii) these traits have a causal influence on the reproductive chances of their bearers. After Lewontin (1970) these requirements are often referred to as the condition of variation, the condition of heritability, and the condition of fitness. (It is worth noting that Godfrey-Smith 2009, in describing the various formulations of these conditions, shows that none of these versions can embrace all cases of natural selection.) As a consequence of these conditions, the frequency and the value of heritable traits may vary across generations, until one trait value becomes established in the population, or else an equilibrium between some values is reached. This, then, is evolution by natural selection. It must be kept in mind, as Fisher noted at the outset of his benchmark volume on natural selection (Fisher 1930), that natural selection is not evolution: that is, the changes brought Page 4 of 41

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about by natural selection may occur alongside other changes in such a way that in the end no salient change in the population has occurred; conversely, it may happen that evolution occurs, but without natural selection playing a causal role. For example, mere intergenerational random variation (called “drift”; see below) entails evolution. As they stand, the requirements for natural selection are not restricted to entities – or sets of entities – of a certain type, size, or level of complexity. Anything that meets the requirements is susceptible to the process of natural selection. Thus, researchers have proposed a theory of natural selection of macromolecules, in order to account for the origins of life (Eigen 1983; Maynard-Smith and Szathmary 1995), and – at the other end of the spectrum – theories of natural selection of ideas in order to explain cultural evolution (Cavalli-Sforza and Feldman 1981; Boyd and Richerson 1985; Campbell 1990; see last section below). By the same token, when one meets a set of individuals which fulfill these requirements, one can assume that those individuals have undergone natural selection, and that some of their current properties present its effects. Population genetics provides models of biological evolution by natural selection. These models often describe a state of equilibrium expected when no selection occurs, called the Hardy-Weinberg (HW) equilibrium, which is derived from Mendel’s Law in populations with sexual reproduction. (Conditions for this equilibrium include infinite populations and random mixing; these are of course idealizations.) The fact of natural selection means that organisms differ in their chances of reproductive success, which implies departures from HW equilibrium. Population genetic models describe evolutionary dynamics as a function of these chances for different genotypes. Models differ according to the way they present intergenerational change (whether generations overlap or not), population structure, etc.; among the most widely used ones are the Fisher-Wright model, the Moran model, and Kimura’s stepping-stone model (Ewens 2004). They generally handle gene frequency change at one locus, and sometimes at two loci, but seldom at more than two loci, because otherwise they would become intractable. One way to think about these models is to say that they take natural selection, mutation, migration, and random genetic drift (that is, stochastic fluctuations correlated to the size of the population) as forces acting on the population of genes and move that population away from its equilibrium, exactly as mechanical forces modify a zeroacceleration state that is the equilibrium state of a mechanical system. In this sense population genetics shares epistemic properties with classical mechanics. Fitnesses (often notated w) are the values of differential chances of being represented at the next generation inherent to different organisms, alleles, or genotypes. Natural selection can be seen as “the survival of the fittest,” as Darwin wrote in the last editions of the Origin, influenced by Spencer (and concerned by the risk of inducing an erroneous sense of agency with the word “selection”). After Fisher and the Modern Synthesis, “fitness” became a crucial technical term, because it entered as a variable into equations of population change. Controversies still rage about its proper interpretation (e.g., Ariew and Lewontin 2004; Bouchard 2011; Abrams 2007; Ramsey 2013; Sober 2001). For our purposes here, suffice it to say that “fitness” involves a mix of survival and fecundity: what counts for evolution is the chance of having heritable traits represented across generations, which in general is a function of the number of offspring, but may also be attested by an organism’s chance of survival. In some population genetic models, however, only viability is taken into account, for purposes of simplicity; whereas in some behavioral ecology models, fitness is represented by a proxy, e.g., energy intake. Either way, the logical form of selection remains the same. In most models, fitness is quantified as the number of representatives of a genotype or a trait in the next generation (or the probability distribution of representatives, given that the models are probabilistic). Often traits are not underpinned by one locus, but by a huge number of loci whose effects are small and additive, as is the case for, e.g., height in humans; often, too, they have continuous values. Page 5 of 41

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Quantitative genetics is the study of the evolution of continuous traits (such as size) in the absence of knowledge of their genetic makeup (Falconer 1981). It can also predict how phenotypes will evolve, by modeling their value and frequency as a function of the intensity of selection (formalized as a “selection coefficient”) and the value of heritability. Following Orr (2009) it is useful to distinguish between individual fitness – that is, the probability distribution of the offspring of an organism, that many philosophers interpret as a propensity, after (Mills and Beatty 1979) – and trait fitness, which is a “summary statistic” that denotes the probability distribution resulting from the aggregation of the individual fitnesses of all organisms belonging to the same type (for example, having the same trait value for a given trait, or sharing the same allele). Trait fitness is what enters into the equations of population genetics, and allows researchers to predict evolutionary dynamics. The Modern Synthesis placed population and quantitative genetics at the heart of the investigation of evolution because they provide a mathematical understanding of the process of natural selection. As modeling practices, these sciences simplify reality. In particular, real organisms have very complex genomes, consisting of thousands of genes (which in aren’t even necessarily physically discrete or continuous units), whereas population genetics models typically model only one locus, or at most two. However, given that each locus occurs against a huge variety of genetic backgrounds, the reasonable assumption is that all the effects that different genetic backgrounds – that is, interaction with other genes within the organism – will have on the phenotypes (and thus reproductive chances) of the alleles for this locus will cancel out. Indeed, population genetic one- or two-locus models do correctly represent and predict the evolution of traits in a given population of organisms (Gillespie 2004), as has been demonstrated many times since the 1930s. On the basis of this general understanding of evolution, the proponents of the Modern Synthesis made several assumptions that have recently came under criticism, in the light of certain empirical findings. First, they equated inheritance with genes, and variation with recombination and mutation, which was recently challenged by empirical evidence for non-genetic forms of inheritance (Jablonka and Raz 2009). Second, they assumed that development – that is, the process through which a zygote goes from conception to adult or reproductive stage – does not matter to evolution, since what counts evolutionarily are the chances of reproduction of a phenotype. The recent research program of “evodevo” aims to reintroduce development into evolutionary biology by arguing that differences in development result in important differences in evolution (Raff 1996; Hall 2003). In regards to variation as well, population genetic models make important assumptions that have at times been questioned. Obviously, if variation, for generation after generation, were to focus on the variants that are best adapted to the environment, selection would be superfluous (that is, even without selection the course of variation would lead to the fittest phenotypes). Modern Synthesis theory held that variation, consisting of mutation and recombination, is therefore “random,” in the sense that it is decoupled from the state of the environment – which, empirically, is usually the case. Yet claims that variation is actually not random have arisen on a regular basis since the Modern Synthesis took shape, including the recent revival of “Lamarckism” (though it is not properly called Lamarckism, see Merlin 2010) advocated by Jablonka and Lamb (2005). Indeed, the existence of some instances of non-random and beneficial variation need not be a threat to the validity of natural selection in general (Huneman 2014b). In this picture, each of the three conditions of natural selection exerts an effect on evolution: the more random the variation, the more room there is for selection; the greater the differences in fitness or selection coefficient, the faster does evolution proceed (fixation of high fitness traits); and of course, a greater degree of heritability, for a given selection coefficient, also increases the rate of evolution. Heritability can metaphorically be viewed as the strength of a “memory” that, generation Page 6 of 41

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after generation, retains the results of natural selection: if it is very weak, it will be difficult for selection to bring about the highest fitness variants. Finally, a fourth important variable is the population size. For a fixed level of heritability and a fixed selection coefficient (or fitnesses), the size of the population may change the outcome of the evolutionary dynamics, since in small populations stochastic fluctuations are large and may prevent the highest-fitness variants from reaching fixation, that is, having a frequency of 100% in the population. When population geneticists speak of “random genetic drift,” they refer to these stochastic fluctuations, especially emphasized by Sewall Wright (Wright 1932). The content of this concept is still controversial. Biologists have vacillated between seeing drift as a deviant outcome (deviant from what is expected based on fitness values) and as a proper cause of a proper outcome in their models (especially in gamete sampling) (Plutynski 2007). When fitnesses differ, drift and selection drive evolution, but the conceptual interpretation of their combination is problematic, since drift is not a force independent of selection but a stochastic fluctuation occurring during the selection process (see section “Metaphysics of Selection: Causation” below). By contrast, when fitnesses are equal, drift alone drives population changes, and diffusion models can be used to represent such dynamics. The overall relevance of drift in actual evolution depends upon what the most common population sizes are. In any case, when alleles do not harbor fitness differences, drift may drive some of them to extinction. Kimura used this insight as the basis of his neutralist theory of molecular evolution, which argues that large parts of the genome in many species have been shaped by neutral evolution, rather than natural selection (Kimura 1983). The relative amount of neutral evolution has been an important topic of controversy in population genetics since the 1980s (Gillespie 2004), when the huge importance of neutral evolution was first acknowledged; since then, there has been progressively more evidence of “positive selection” (Voight et al. 2006) (i.e., the process by which new advantageous genetic variants sweep a population). Properties of Selectionist Explanations Three general features of selectionist explanations should be noted. First, they belong to what Mayr (1959b) called “population thinking”; that is, selection is always understood to apply to a collection of entities, since only differences in relative fitness matter. In this respect, explanation by selection might be contrasted with what Sober (1984) called “developmental explanation,” namely, an explanation of a property that appeals to the process through which that property was acquired. The developmental explanation of the composition of a football team refers to the sum of the experiences of each of its players; the selectionist explanation refers to the choice of the team by the manager, who set a criterion of competence and then evaluated all available football players by this criterion. What is characteristic for selectionist explanations as instances of population-level thinking is the fact that there are no specified criteria of admission other than reproductive success. In this view, population genetics appears analogous to statistical mechanics – the science of ensembles of gas molecules, which defines state variables that allow physicists to model coarsegrained descriptions and make predictions for an ensemble’s collective evolution. Fisher (1930) proposed such analogy, comparing the mean fitness of populations to the property of entropy. A second important feature is that two traits can be correlated, either for morphological or for genetic reasons; an illustrative example of this is pleiotropy. The two correlated traits will always be selected together, and the two types of individuals they define will have the same fitness. Elliott Sober (1984) coined the terms “selection-for” and “selection-of” to distinguish between traits that are indeed the targets of natural selection, since their ecological consequences increase reproductive success, and traits that are selected because they are correlated to the former. Conceptually, this Page 7 of 41

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distinction involves an appeal to what philosophers call “counterfactual thinking”: when there is selection of a trait A, but only as by-product of selection for another trait B, it means that if organisms had A without having B, A would not have increased in frequency. However, population genetics has designed methods to distinguish between selected and correlated traits (Lande and Arnold 1983). A third important feature is that population and quantitative genetics use fitness values as variables associated with traits and alleles, but do not model the causes of fitness values. The latter goal is exogenous to population genetics, since what determines the fitness value of a genotype or a trait is the way it relates to environmental demands. Fitness values only record differential performances of types of individuals (types being defined by shared traits of interest) in the environment. When applied to extant species, population and quantitative genetic models can identify which traits are expressed (or will go to fixation) due to natural selection just by assessing the fitness values of traits – even without considering the problems associated with estimations of fitness in nature – but they don’t offer any explanation of why natural selection is taking place. Instead, the causes of fitness or selection are a subject of ecology (Wade and Kalisz 1990). Ecology was defined by Haeckel, the most famous Darwinian of the late nineteenth century, as the “science of the struggle for life.” Ecological interactions such as competition, predation, or mutualism between organisms of various species explain the differential successes of types of organisms, as well as the extinction and succession of species in a community or an ecosystem. Ecology studies the causes of fitness, with the fitness values being the variables through which population and quantitative genetics capture evolutionary change. Therefore, evolution by natural selection is the subject of two distinct sciences: population/quantitative genetics and ecology. The latter tries to understand the reasons why natural selection has designed organisms the way they are; in other words, it explains biological traits as adaptations to the environment. For instance, when behavioral ecology studies the mating behavior of gorillas, it asks why strategies such as monogamy or polygamy have emerged in a given species in a specific environment (Dunbar 2001), and then offers answers by demonstrating that one particular strategy optimizes reproductive success in these conditions. (See section “Genes, Dynamics, Optimality, and Strategies” below on optimality.) More generally, several evolutionary disciplines ask why organisms are the way they are, by asking why they have the traits they have. When it comes to species of the past, clearly one should use particular methods because, unlike in behavioral ecology, a straightforward modeling of the parameters is not possible; yet fundamentally, paleontology and behavioral ecology ask the same kinds of functional questions about the presence of traits and the design of organisms. The conceptual duality of natural selection becomes even more challenging when one considers that ecology is also dual, because it comprises not only the science of ecological interactions affecting individuals, i.e., behavioral ecology, but also the science of species interactions, i.e., community and population ecology. The latter of course defines the background against which the former takes place (e.g., the behavior of foraging organisms is partly determined by the general competition between species that prey on the same prey). Population genetics models a certain population of a given species, in which alleles are changing because of mutation and migration; in general, the environment is considered to be constant in this. (Sometimes it is variable in time, but nevertheless, its species composition is not part of what the model tries to explain.) In contrast, for community or population ecology the genes are an invariant factor, and the species of interest are what varies. In sum: the epistemic duality of evolutionary biology – population genetics vs. ecology – makes for a complex structure, which we will explore in more detail below.

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Epistemology of Selectionist Explanations Genes, Dynamics, Optimality, and Strategies Explanations based on natural selection thus gives rise to two different interpretations. On the one hand, population genetics analyzes the dynamics of alleles or genotypes in a population that contains different fitness values. Natural selection here is a specific feature of the dynamics (i.e., differences in relative fitness); the selectionist explanation therefore shares the epistemological status of a mechanical science. On the other hand, when biologists such as behavioral ecologists investigate, for example, the function of figure-eight-shaped waggle dance of bees, they assume that this behavior is somehow suited to the environment of the bees – in other words, that it is an adaptation. In so doing they assume that the behavior has resulted from natural selection, because it would have been selection that optimized the trait in response to the environment (Mayr 1983; Maynard-Smith 1984). Natural selection here is thus seen as an optimizing process: by constantly retaining highfitness variants it maximizes fitness, and fitness maxima correspond to optimal traits. (When the traits have a fitness value that is frequency dependent, we do not see optima but strategies that are such that when they are generalized, no variant strategy can invade the population.) Epistemologically, the status of such knowledge might be said to correspond to economics as a science of behavior based on the principle of maximization of utility. As a matter of fact. behavioral ecology uses evolutionary game theory (Maynard-Smith 1982), which is mostly an extension of economic game theory – one where the payoffs of the strategies are not defined in terms of utility but of fitness. Moreover, the two aspects of natural selection differ with respect to the kinds of objects they deal with. In population genetics, selectionist explanations pertain to the dynamics of allele frequencies. In behavioral ecology, it seems that entire organisms are what is at stake, since natural selection seems to optimize the traits of organisms in the face of environmental conditions. Notably, in this latter context one often does not know anything about the genetic make-up of the traits of organisms. Within evolutionary biology, intense controversy continues over the levels and units of natural selection: does it target mostly genotypes or phenotypes, mostly alleles or organisms? (See section “Targets and Limits of Selection 1:Levels of Selection” below.) But regardless of this controversy, the levels at which population genetics and behavioral ecology locate their subject are different: for the latter it is organisms, and for the former, genes. As “Formal Darwinism” (Grafen 2002, 2007) importantly emphasized, these two takes on natural selection do not always concur. In many cases, maximum fitness will not be reached by natural selection. This is especially true in the case of frequency-dependent selection (Moran 1964), but also in the simple case of heterozygote superiority (where for principled reasons, the heterozygote genotype cannot fix in the population). However, behavioral ecologists generally assume that the gene dynamics will match what an optimizing trend would predict and will therefore support their hypotheses. This is what Grafen (1984) called the “phenotypic gambit” – a bet about the relationship between phenotypes and genotypes. Formal Darwinism has shown that there are indeed isomorphisms between descriptions of evolution in terms of changing allele frequencies and descriptions in terms of optimization of organismal traits, so that the phenotypic gambit can be the default position. This formally justifies the intuition behind many proposals in behavioral ecology. Philosophically speaking, it justifies a unification of the two approaches to evolution, as the result of which it is understood as both the object of a kind of mechanics and that of a kind of economics (Huneman 2014a, c). Epistemology of Selectionist Explanations: Analyticity and Historicity Analyticity Population and quantitative genetics is mostly couched in the mathematical language of statistics. In this context, many authors have tried to provide very general formulations of Page 9 of 41

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evolution by natural selection. Fisher first forged what he called the “fundamental theorem of natural selection” (FTNS), which states that intergenerational change in the mean fitness of a population equals the additive genetic variance, hence is always positive (i.e., fitness always increases). He saw this as an analytic truth, a priori established, whose status equals the status of the second principle of thermodynamics (for Fisher, both population genetics and thermodynamics were sciences of macroscopic variables defined on the basis of collectives). Fisher’s theorem was controversial, since many authors opposed it on the grounds that population genetics, as indicated, does not always predict fitness maximization. Recent interpretations of the FTNS highlight that the quantity referred to by the theorem is not a global change in mean fitness but, more narrowly, a mean fitness change directly due to natural selection (Ewens 1989; Frank and Slatkin 1992; Edwards 1994). To this extent, the theorem can be made to accommodate empirical cases where mean fitness decreases; in these cases, negative changes in mean fitness due to what Fisher called “environmental deterioration” (a term whose interpretation is debatable) overwhelmed the positive effect of selection. In any case, the parallels that Fisher drew to statistical mechanics have been seriously considered by several authors, who tried to develop population genetics in a way rigorously analogous to statistical mechanics, viewing the construct of fitness as formally analogous to a kind of entropy (Barton and Coe 2009). But other general abstract formulations have been proposed as well. George Price suggested that evolutionary change can be captured in a simple quantitative genetics formula that can be analytically derived (Price 1970): Δz ¼ Covðwi , zi Þ=w þ Eðwi Δzi Þ=w where z (resp. w) is the mean trait value (resp. mean fitness), wi is the fitness of individuals i, zi their value of the trait, and Δzi the change of this value between individual and offspring. This so-called “Price equation” decomposes evolutionary change into the effect of natural selection (captured as covariance between fitnesses and traits) and the transmission biases (the expectation term) (Gardner 2008). Interestingly, Fisher’s FTNS can be derived from the Price equation if “fitness” is taken as the focal trait. But it should be made clear that the variable z, whose change is modeled by the equation, can also mean other properties, such as the frequency of alleles – hence the Price equation is even more general than the principles of quantitative genetics. Moreover, the Price equation, being mathematically true, is a description of evolutionary change, but cannot in itself provide causal information on evolutionary processes. Grafen’s Formal Darwinism (see above) construes its isomorphism between population genetics and optimization on the basis of the Price equation. Other general formulations of evolution have been proposed, some of them in the context of what is called “replicator dynamics,” others in the context of “adaptive dynamics” (Metz 2008). The above discussion of the analytical or formal side of evolutionary theory gives rise to an occasion to mention the so-called tautology problem. If natural selection is defined as “survival of the fittest,” one could object to Darwin that in the absence of other evidence regarding the capacities of organisms, the “fittest” are precisely those who survive, so the main principle of the theory constitutes a tautology. One response to this is that there are other, independent pieces of evidence for fitness (drawing on physiology, ecology, etc.), or that there are cases where the fittest do not overcome all others evolutionarily (i.e., in the case of drift), demonstrating that the statement is not analytical. But another plausible response consists in accepting the criticisms, and saying that current evolutionary theory has at its core a mathematical theory – mathematics being a system of

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analytical judgments. This concession does not therefore give up on the scientific validity of the theory (no more so than acknowledging the mathematical nature of modern physics would diminish the validity of physics). Historical Understanding As Bock and von Wahlert (1963) wrote, we must distinguish the processes of evolution, which involve – but are not to be equated with – natural selection, and the outcome of evolution, namely phylogenies and the phylogenetic tree. However, no actual process of evolution could be understood solely through theoretical knowledge of evolutionary mechanisms, in the absence of historical data. For instance, many terrestrial vertebrates are tetrapods: one could imagine a selectionist hypothesis concerning the adaptive origins of their four limbs, since this configuration is obviously adaptive for locomotion. However, there is another reason for those four limbs: marine ancestors of those vertebrates had four fins, so the four limbs are a legacy, resulting from what we might call “phylogenetic inertia.” The point is that natural selection often explains the appearance of such traits, but not their appearance in a particular clade. The selectionist explanation has to be historically situated in order to determine what the correct explanandum is – the one for which natural selection would be the right explanans. Thus, no explanation of the presence of characteristics in the members of a given population or species is available through the sole application of population genetic models of natural selection. The distinctive characteristic of evolutionary theory, if we assume that its explanatory strategies are always related to some use of the selectionist explanation, is that it brings together certain formal models, written in mathematical language in the modality of pure necessity, and certain historical narratives (Gayon 1993; see Richards (1992a) for an argument in favor of evolution as a narrative). Thus, evolutionary biology is indissolubly both a formal science, to the extent that evolutionary change can be captured through analytic formulae and models, and a historical science, as soon as it comes to understanding actual past and present evolution at any scale. This latter methodological aspect also implies that few empirical inquiries in evolution can be made without comparative data Endler (1986), in order to avoid incorrect, ahistorical invocation of natural selection mechanisms – such as in the tetrapod example above. Often a divergence of results between studies can be traced back to differences between the sets of comparative data used by the researchers (Sober and Orzack 1994, 2001; Griffiths and Sterelny 1999, pp. 240–250). This pervasive element of historical narrative in neo-Darwinism accounts for the historical meaning of all biological terms in evolutionary theory. Taxonomies are obviously and easily reinterpreted by history. The concept of homology - initially defined by (Owen 1843) as “the same organ in different animals under every variety of form and function” - that helps systematists build their classifications acquires in the light of evolutionary theory the historical status of “signs of common descent,” as for instance in the case of birds’ and bats’ wings. (See chapter “▶ Homology: A Philosophical and Biological Perspective”, Vol. 1.) Homoplasy, as the other kind of similarity across species, seems less of a historically significant concept at first glance: similar selective pressures gave rise to similar devices, representing similar adaptations to these pressures. But is it really the case that the concept of adaptation lacks any historical dimension? The question of whether adaptation is a historical concept is widely debated. Philosophers (Burian 1983; Sober 1984; Ruse 1986; Griffiths 1996) concede that “adaptation ascriptions are causalhistorical statements” (Brandon 1996), since to say that a trait is an adaptation is to say that it has somehow been selected for some of the advantages it gave to its bearer via differential reproduction. (Note that “adaptation” is a property of traits, whereas in a pre-Darwinian context, and often in non-evolutionary biology, “to be adapted” and “adaptation” are features of organisms; though many evolutionists as well often use “adaptedness” to refer to this latter kind of adaptation.) It remains to Page 11 of 41

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_2-3 # Springer-Verlag Berlin Heidelberg 2014

be decided whether this sums up the full meaning of the concept – given that biologists often do not appeal to historical facts in order to describe adaptations, but just forge optimality models with current data, as done in behavioral ecology. Reeve and Sherman (1993, 2001) advanced a powerful “currentist concept” of adaptation, as opposed to the historical concept: “An adaptation is a phenotypic variant that results in the highest fitness among a specified set of variants in a given environment” (1993, p. 9). Having distinguished two goals of evolutionary research – the first being the explanation of the maintenance of traits, and the second the reconstitution of a history of lineages – they argue that the former essentially needs the currentist concept, whereas the latter is much more closely related to the historical concept. Notwithstanding one’s view on this matter, the fact that there can be a historical component to adaptation ascriptions is important, since it allows biologists to distinguish between the origin of a trait as an adaptation and its current presence and maintenance. A trait that is adaptive might not have emerged as an adaptation, or might have emerged as an adaptation for some other use. This is captured by the concept of “exaptation,” suggested by Gould and Vrba (1982); an example would be insect wings, which probably emerged as thermoregulatory devices (Kingsolver and Koehl 1989). Exaptation has proved to be a useful concept for our understanding of a lot of features that appeared during the evolution of hominids (Tattersall 1998). However, one should not conflate the two meanings of the historical characterization of adaptation: there is a definitional meaning and an explanatory meaning. On the one hand, selection defines adaptation, since a trait being an adaptation means that it originated through natural selection. But on the other hand, we say that selection explains adaptation; this is not contradictory to the definitional meaning, because we now mean that the explanation of a given adaptation may refer to concrete selective pressures in the given environment, which provides an agenda for the experimental testing of hypotheses. An example of such experiments, and of the explanatory use of the historical concept of adaptation in their interpretation, is a study on the differential sensibility of plants to gradients of metal in soils (Antonovics et al. 1971).

Metaphysics of Selectionist Explanations Laws in Evolutionary Biology The hybrid epistemic status of evolutionary biology inclined philosophers to enquire about the status of laws in this discipline. Some of them argued that there are no laws in evolutionary biology (Beatty 1997; Rosenberg 2001; Brandon 1997 vs. Sober 1997), or in biology generally (Smart 1959). An analogous controversy occurred among ecologists, with Lawton (1999) doubting that ecological laws exist and other authors (e.g., McGill and Nekola 2010) arguing that ecology does indeed capture specific laws. Laws of nature are general statements formulated under the modality of necessity. The logicalpositivistic account of science viewed explanation as a deductive argument whose conclusion is the explanans, and whose premises combine certain laws of nature with particular statements of facts (the so-called “deductive-nomological” account of science; Hempel 1965). Even though the philosophy of science has mostly turned away from positivism since the 1970s, many authors still attribute a crucial explanatory status to laws (e.g., Lange 2009). The usual puzzle in philosophy of science is to find a criterion distinguishing accidental generalities (such as “All mountains are less than 100,000 m high”) from laws (Ayer 1956). As a solution, Dretske (1977) claimed that laws have to be conceived as relationships between “universals” (for instance, the law of gravitation holds between the natural properties mass and distance, which are universals, as opposed to individual bodies, which are particulars). In any case, laws should support counterfactuals; this means that if some variables are changed within them, the results should be affected in a predictable way. The

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implication is that law-like generalizations can be used in explanations, whereas accidental generalizations seem not to allow such a use, and even less a predictive use. Yet the very notion of law, as used by biologists, is often ambiguous. Some laws concern the correlation of variables in a given empirical range: for instance, the correlation between body size and latitude (“Bergmann’s rule”); or the species–area relation in ecology. Many laws in paleontology can also be seen as such generalizations: “Dollo’s law” about irreversibility, “Cope’s law,” etc. These laws actually concern patterns, and are mostly established through induction; often they are captured in what physicists call “phenomenological models.” However, one can still wonder why such pattern laws are found, hence investigate the processes supporting them. That then leads to the quest for what scientists often call mechanisms, captured in “mechanistic models.” Philosophers of science would mostly say that the “process laws,” related to the mechanistic model, are the most explanatory and hence have to be called genuine “laws” (whereas they would be content with calling the other laws “rules,” for instance “Bergmann’s rule”). Many controversies in ecology actually concern these underlying laws. Thus ecologists wonder, for example, whether there is one such underlying law yielding the species–area relationship. Advocates of the absence of laws in ecology argue that given the complexity of ecological systems, there may be many processes accounting for the various patterns of biodiversity we observe, but not a single, overarching mechanistic model likely to capture them all. Ecology aside, what about other aspects of evolutionary biology? Clearly, in evolutionary theory most generalizations do not seem as robust as typical laws of physics (in fields such as particle physics; though when it comes to cosmology, physics arguably does involve history, and law statements may be traced back to the contingency of primordial history). Most law statements concern species of organisms (e.g., “Bonobos are promiscuous”), and, because of the contingencies of evolution, these species could have been absent or different. They are not “natural kinds” in the metaphysical sense, unlike the chemical elements, of which any chemical substance is made and which can robustly and a historically be defined in terms of an atomic number - setting aside the complications added by the fact of a cosmological history. Any term in a putative biological law p instead seems to be contingent upon the facts of evolution, which makes statement p less than a law. As Beatty (1995) argued, Mendelian laws are contingent upon the fact of sexual reproduction, which is a possibly contingent product of evolution on earth. And even the universality of the genetic code is a generalization confined to our planet, where it holds due to the universal descent of life on earth from a contingent fact – a “frozen accident” (Crick 1968); the same correspondence laws between nucleotides and amino acids cannot be expected to hold on other planets. This contingency of generalized propositions affects the whole of the system of supposedly law-like statements in biology. The only evolutionary statement that could be a law is, thus, the one enunciating the process of natural selection itself, since it specifies no particular entity. And this indeed accounts for the important difference made between pattern laws and process laws. For instance, Bergmann’s rule states a pattern associated with the geographical distribution of clades or species or populations of species: larger ones tend to be found in colder environments (which of course correlate with latitude). This pattern is explained by the fact that larger animals have a lower surface area-tovolume ratio than smaller animals, which implies that they lose less body heat per unit of mass. This, in turn, entails that, the colder the environment in which a species is found, the more likely selection will favor the variants that better resist the cold, which are – everything else being equal – the larger ones. Thus the explanatory core of the process is natural selection: all else being equal, organisms better equipped to face the given environmental conditions (i.e., those having traits that allow them to live longer on average and to produce more offspring) tend to pass on their heritable traits, Page 13 of 41

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eventually leading to the dominance of these traits in the species. That adaptation-to-temperature process itself could hardly be seen as a law; rather, it is an instance of natural selection. (One would reasonably resist calling a law each case where natural selection yields a specific pattern regarding the distribution of some traits.) It is thus plausible, in our example, that the law underlying Bergmann’s rule would be something like “the law of natural selection,” a suggestion controversial among philosophers (Bock and von Wahlert 1963; Sober 1984, 1997; Brandon 1996, 1997; Rosenberg 1985, 1995, 2001). Rosenberg (2001) argued that what Brandon (1996) calls the Principle of Natural Selection (PNS) – briefly summed up as, “When variation is causally connected to differential ability to survive and reproduce, differential reproduction will probably ensue” – is the only law of biology. He relied on Williams’ (1970) axiomatization of the theory, which conceives of fitness as an undefined primitive term, e.g., a term for which some definitions, in some contexts, can be given only outside evolutionary theory, in another theory. But, even if by convention we say that the PNS is a law, we still face the question of how it differs from other kinds of law. In effect, unlike physical laws, the PNS does not refer to any natural kind of property such as mass, electric charge, etc. The sole property involved in some of its formulations is fitness, which only captures context-dependent consequences of some physical properties evolutionarily relevant in a given setting (for example, the color of moths is a fitness parameter in industrial melanism only because there are predators capable of vision). So the PNS can become the equivalent of a physical law – stated in probabilistic language – only if and when the physical characteristics of the properties contributing to fitness are specified, a specification that is always context dependent. For instance, the “optimal shift towards viviparity” in some marine fish described by Williams (1966) results from a kind of rule, since he states the parameters ruling the selection pressures (density of predators, physiological cost of reproduction); these parameters in turn determine a range of relevant physical properties for selection. In this case the PNS becomes predictive, and we can test it by building experiments in which the values of the proper variables vary. The PNS aside, there surely are a number of genuine laws in evolutionary theory; however, those kinds of propositions are not so much empirical laws as mathematical laws. In a way, evolution contains both statements modally stronger than physical laws (since they are purely mathematical statements) and statements nomothetically weaker, such as those derived from the PNS through its empirical instantiation. Rather than being a law, the PNS ultimately proves to be an explanatory schema, providing ways of explaining and building models through its more or less empirical instantiations. The least empirically instantiated models are the models of population genetics; the most empirically instantiated are rule-like generalizations, such as paleontological ones. Metaphysics of Selection: Causation Philosophers of science have moved away from logical positivism and Carl Hempel’s claim that explanation consists in subsuming phenomena under laws. Instead, the view has been on the rise that genuine explanation must be causal – under one of various possible conceptions of causation (probabilistic, physical, counterfactual, Humean, etc.; Tooley and Sosa 1983). Hence, notwithstanding the controversy over the existence and nature of laws in evolutionary biology generally, and over the status as law of the PNS in particular, philosophers are expected now to consider the causal role of selection. Two simple (and related) issues arise: What does natural selection causally explain? And, is it even a cause (vs. some other kind of explanation)? Attempts to answer the first question generally take one of two views. In the first, selection is a negative, attenuating force: it merely selects, and thus sorts high-fitness traits out from low-fitness ones. In the second view, by contrast, selection assumes a more positive role by being itself creative. Thus Mayr (1965) already claimed that selection is not a “purely negative force,” since it gradually Page 14 of 41

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improves existing traits. Among biologists, this positive view has been widely held: Dobzhansky, Simpson, and Gould shared it. “Creativity” was an important notion for the architects of the Modern Synthesis, since it enabled them to distinguish their view from Mendelian saltationism, which attributed the main evolutionary force to mutation and variation: if selection is creative, then one cannot locate the main reason for evolution at the level of variation (mutations). In the last decade the debate on the negative vs. positive role of selection has surfaced once more in the field of philosophy of biology. The basic question underlying this ongoing controversy is: what does selection actually explain? It does explain, at a population level, why a trait, once it had arisen, pervaded and persisted in a population (1). But is that all? Does selection not, ever, explain why a given individual displays a particular trait? (2) (Should that latter explanation always be given just in terms of developmental effects?) Sober (1984) for one subscribes to the negative view that selection is strictly a population-level explanation, so that the question “Why is trait A present in individual B?” does not fall into its domain. Neander (1995) challenges this view, in line with Mayr’s intuition. Apart from the two questions distinguished above (questions (1) and (2)), there is, according to her, the “creative question,” which is: “Why did the genetic and developmental devices underpinning a given trait arise in a population?” Neander contends that natural selection contributes an answer to this creative question, for the following general reason: even if the genotype conditioning a new trait is not created by selection, selection does increase the probability of occurrence of the many alleles composing this genotype. In a population of diploid organisms, suppose a pool of genotypes of nine loci, and suppose that the genotype G1-…-G9 has a higher fitness than all the genotypes comprising other alleles G′i (1 20. (3) The system may experience a secondary opening as a result of the geochemical mobility of the uranium. Originally the activity of the Th and U isotopes was analyzed by a-spectrometry. The introduction of thermo-ionization mass spectrometry (TIMS) by Edwards et al. (1986/87), which requires less than 1 g of sample material and provides high age precision, brought a great impetus for 230 Th/234U dating. More recently multicollector inductively coupled plasma mass spectrometry (MC-ICPMS) has been used. This can additionally provide spatial information when coupled with laser ablation (LA-MC-ICPMS), but at the cost of precision compared to solution MC-ICPMS or TIMS. Under favorable circumstances, age precisions better than 1 % can be obtained. The uranium content should be more than 0.1 mg g1. When sampling, e.g., speleothems (calcareous flowstones formed on the cave floor), dense and pure carbonates should be collected in order to minimize potential problems, i.e., open-system behavior and 230Th contamination by detrital components. This was carefully investigated in the dating of very thin secondary carbonate crusts, which had developed on top of Upper Paleolithic rock art or was already present at the time of the creation of the art. The resulting U-series ages obviously can provide only ante quem and post quem dates for the rock art, with uncertainties below 2 % at the 95 % confidence limit. It was shown that European rock art dates back to the Early Aurignacian period, with a minimum age of 40.8 Ka (Pike et al. 2012). Artwork therefore appears to have already been part of the repertoire of Homo sapiens

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when colonizing Europe at this time, or shortly beforehand, as also evidenced by painted stones and elaborate figurative art in southern German caves (cf. TL and radiocarbon dating). In the Tongtianyan Cave, Guangxi, China, one of the few Pleistocene fossils of Homo sapiens in Asia was discovered. Several speleothem layers, intercalated in the cave sediments, were dated by 230 Th/234U. The age results of 13.5
2.3 Ka, 63.1
2 Ka, and 148
4 Ka, for three layers from top to bottom, follow the stratigraphical order (Shen et al. 2002). Although the stratigraphic position of the hominid find is to some extent uncertain, it was certainly located below the second layer. This renders this find as one of the earliest in East Asia, indicating that modern humans arrived there before ca. 60 Ka ago. Depending on the measurement precision, the 230Th/234U system in speleothems older than 350 Ka often shows equilibrium, so that only a terminus ante quem can be given for the age. This situation was met in the fossil hominid sites known as the Sima de los Huesos, Spain, and the Caune de l’Arago, France. At Sima de los Huesos, the numerous human individuals, which are considered as evolutionary ancestors of the Neanderthals, are overlain by a speleothem in equilibrium and thus older than 350 Ka (Bischoff et al. 2003). Analogously, the pre-Neanderthals found in the Middle Pleistocene unit III at Caune de l’Arago have to be older than 350 Ka (Falgue`res et al. 2004). At the famous Zhoukoudian site near Peking, yielding the Homo erectus commonly known as Peking Man, speleothems which were intercalated in the fossiliferous sediments were 230Th/234U dated. In most samples the 230Th/234U system was close to equilibrium. However, high-precision analysis of these nuclides enabled to push the dating method to its upper limits, which is in the 500–600 Ka age range with the present instrumentation (Shen et al. 2001). The results indicate that the youngest member of Homo erectus at this site is >400 Ka and the oldest members from the lower layers are significantly older than 500 Ka. The 230Th/232Th–234U/232Th-isochron technique permits determining the initial 230Th/232Th ratio. Schwarcz (1989) used this technique for dating the sinter crust on the cranium of the classic Neanderthal at Monte Circeo, central Italy. The encrustation on the cranium consisted of a brighter inner and a dark-brown outer layer. The outer layer provided an age of 16 Ka. From the inner layer, which contained detrital contamination, several subsamples of different U/Th ratios were obtained through fractionated leaching. The slope of the straight line (isochron) through the data points in the 230Th/232Th–234U/232Th diagram provided a more reasonable age of 51
3 Ka. Precise 230Th/234U dating of travertine, a spring sinter built from secondary carbonates, is hampered by the common detrital 230Th-contamination and by open-system behavior. Applying a micro-sampling technique, in which 100 mg of sample material was selectively drilled from the micrite/sparite phases, Mallick and Frank (2002) dated successfully travertines from various Thuringian (Germany) sites, among them Weimar-Ehringsdorf with pre-Neanderthal remains. The results assign these finds firmly to oxygen-isotope stage 9. Buried teeth absorb uranium from the groundwater. The knowledge of the time function of the uranium uptake is crucial for the 230Th/234U-age evaluation. Since the exact temporal development of uptake is unknown, one has to rely on models, such as early (EU) or linear (LU) uptake (cf. ESR), and must also consider leaching. For instance, the age of Neanderthal remains from Payre´ (France) was constrained by direct LA-MC-ICPMS U-series analysis of a Neanderthal tooth yielding an apparent minimum age of 200 Ka, which is in good agreement with TIMS U-series ages for an underlying flowstone between 200 and 230 Ka (Gr€ un et al. 2008). The mode of uranium uptake can be constrained when 230Th/234U is combined with ESR dating (Gr€ un et al. 1988; Shao et al. 2012) which now is more common practice than stand-alone U series of organic tissue. With a combination of Th/U and Pa/U dating, it is theoretically possible to obtain ages back to 1 Ma, but analytical constraints limit the potential range to 600–700 Ka, and Page 9 of 31

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application is hampered by the required large sample size (Gr€ un et al. 2010). Falgue`res et al. (1997) 230 234 reported coupled Th/ U and ESR dating on horse teeth from Acheulian and Mousterian levels at la Micoque, France. The 230Th/234U ages of enamel and dentine ranged widely from 150 to >350 Ka. However, when combined with ESR dating, consistent ages between 300 and 350 were obtained. Open-system behavior is even more crucial for U-series dating of bones, and the development of new models is essential (Sambridge et al. 2012). Sophisticated techniques and multiple approaches are required to provide ages for bones by U series and preferentially should be supported by independent age evidence. However, this approach can serve as a tool for the verification of the antiquity of bones or determining if bones are intrusive and not of the same age as associated material. This was how the antiquity of one of the earliest modern humans (Omo Kibish 1) was confirmed. Agreement with Ar/Ar dating of 195 Ka for correlated material was obtained by a minimum age of 155–187 Ka with LA-MC-ICPMS U series, on bone fragments believed to belong to the calvaria (Aubert et al. 2012). In principle, nondestructive U-series dating techniques based on g-spectrometry can be used on valuable specimens. However, the complex detection geometries of human remains and the low resolution of the method prevent standard application, and uncertainties of results are large, usually preventing the determination of appropriate U-uptake models (e.g., Schwarcz et al. 1998 vs. Millard and Pike 1999).

Fission Track Although fission tracks (FT) are not applied as commonly as the other radiometric dating methods in paleoanthropology, they have made significant contributions at some important sites in volcanic regions. Fission tracks are formed by the spontaneous nuclear fission of uranium. Natural uranium consists of the isotopes 238U (99.3 %) and 235U (0.7 %), whereby 238U decays by spontaneous fission. The fission decay rate is 106 times less than that of the a-decay of the same isotope. During fission the uranium nucleus splits up into two fragments. Due to their kinetic energy, both fission fragments are expelled in opposite directions and leave along their path a zone of damage in the crystal lattice of a mineral. Both branches together form a straight fission track of 10–20 mm in length and several 103 mm in diameter. By chemical etching, the fission tracks can be made visible for optical microscopy. In the course of time, the tracks accumulate in the mineral, and if they are all preserved, their number is a function of the age of the event dated. Obviously, the track number depends also on the uranium content which is determined by exploiting the thermal-neutroninduced fission of 235U, where the number of the induced 235U fission tracks is proportional to the U content. Thus, the procedure of fission-track dating essentially involves the counting of spontaneous 238U fission tracks before and induced 235U fission tracks after a neutron irradiation. The principles and application of fission-track dating were described in detail by Wagner and Van den haute (1992). With fission tracks, either the age of mineral formation or its last heating when all previous tracks were erased, i.e., the clock was reset, is dated. The fission-track method is applicable for a time span of >10 Ka. This requires, however, sufficiently high uranium contents above 100 mg g1. Zircon, due to its high uranium content, is most frequently used in paleoanthropological applications. Of particular interest are volcanic ashes that are intercalated in sedimentary sequences containing hominid remains and Paleolithic sites. Also volcanic glass, such as obsidian and pumice, is frequently used for fission-track dating. A common problem in fission-track dating is the annealing of tracks. Latent fission tracks gradually fade over time. The fading is accelerated at elevated temperatures, in a process known Page 10 of 31

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_10-4 # Springer-Verlag Berlin Heidelberg 2014

as annealing. Since annealing reduces the apparent fission-track age, it is of fundamental importance to quantify this effect by track-length measurement, since annealing shortens the tracks. Fortunately, tracks in zircon are rather stable and do not show any signs of fading over several million years at ambient temperatures, although tracks in natural glasses certainly may fade under such conditions. For fission-track dating of tephra, mainly zircon grains and, to a lesser degree, also glass shards and apatite as well as titanite grains are used. When relying on heavy minerals, the possible different provenance of the various grains needs to be taken into consideration, a difficulty already discussed (cf. K–Ar dating). Primary volcanic grains in the presence of detrital ones can be identified – apart from mineralogical criteria – by single-grain fission-track data. A good case study was conducted for the Pliocene/Pleistocene sedimentary sequence of the Koobi Fora formation, Kenya. It contains several tuff horizons, which primarily consist of glass fragments and pumice cobbles, but shows signs of redeposition. Of particular interest is the KBS Tuff, which is intercalated in hominid-bearing layers. In the 1970s, K–Ar data on the KBS Tuff raised a controversy between supporters of a long chronology (2.61
0.26 Ma: Fitch and Miller 1970) and those of a short chronology (1.82
0.04 Ma; Curtis et al. 1975). FT dating on zircon (2.44
0.08 Ma; Hurford et al. 1976) at first seemed to support the high K–Ar age. A later FT study of zircon from the pumice yielded 1.87
0.04 Ma (Gleadow 1980) in accordance with the short chronology. Besides methodological aspects, the main reasons for the previous fission-track overestimate of the KBS Tuff are detrital, old zircon grains. A far-reaching study on tuffaceous zircon was reported by Morwood et al. (1998). At the site of Mata Menge, Flores (Indonesia), a layer with stone tools is intercalated in tuffaceous deposits. FT dating on zircon from the lower and the upper tuffaceous layer yielded 880
70 Ka and 800
70 Ka, respectively. Provided that these grains are primary and not reworked, these findings imply that at that time Homo erectus had already reached the island of Flores from Southeast Asia – a journey that requires an amazing sea-crossing capability, even at periods of lowest sea level. Ashes in prehistoric fireplaces may contain sufficiently heated grains of apatite, zircon, and titanite. At Zhoukoudian near Peking, with its numerous remains of Homo erectus (Peking man), several hundred grains of titanite in the size range of 50–300 mm were separated from ashes sampled from layers 10 and 4. The length of the fission tracks was utilized as criterion for discriminating completely from partially annealed titanite grains. Altogether, 100 grains showed complete resetting and gave mean ages of 462
45 Ka for layer 10 and 306
56 Ka for layer 4 (Guo et al. 1991), which are younger than the abovementioned uranium-series ages for this site (Shen et al. 2001).

Luminescence Since its introduction by Daniels et al. (1953), luminescence dating has gradually developed into a powerful chronometric technique, particularly for quartz- and feldspar-bearing materials (Aitken 1985, 1998; Bøtter-Jensen et al. 2003; Yukihara and McKeever 2011). In the meantime, luminescence dating has significantly contributed to paleoanthropology. As to the techniques of luminescence dating, one distinguishes between thermoluminescence (TL) and optically stimulated luminescence (OSL). For the latter the term “optical dating” is also used. Luminescence dating covers a wide age range between 10 and 105 years and thus is able to reach well beyond the limits of radiocarbon dating. Datable materials comprise various inorganic sediments, such as sand and loess, heated stones, and bleached stone surfaces. Page 11 of 31

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Luminescence dating is based on the time-dependent deposition of energy in the crystal lattice of minerals. This energy stems from ionizing radiation, which originates from natural radioactivity, as well as cosmic radiation and is omnipresent in nature. The radiation, consisting of energetic a- and b-particles as well as photons (g-rays), interacts with the atoms of a mineral and removes some electrons from their original valence-band position in the atom shell. Freed electrons diffuse for a short distance through the crystal lattice, and some of them become trapped in lattice imperfections. Such electrons are trapped at higher energetic levels than those in the valence band. With time t the electron traps are increasingly filled – the process that forms the basis of the luminescence clock. When the crystal is stimulated by heat or light, the electrons are released from their traps, enabling them to recombine with opposite charge carriers whereby the formerly trapped energy is set free. Some of this energy appears as emission of visible light, the luminescence. Depending on the kind of stimulation, one differentiates thermally (TL) from optically stimulated luminescence (OSL) from radiofluorescence (RF), the latter of which is stimulated by ionizing radiation. OSL is further differentiated according to the type of stimulating light, such as OSL by green/blue or IR-OSL (IRSL) by infrared stimulation. Recent approaches consist of various steps of heating and illuminating the samples (e.g., post-IR IRSL) or employ the isothermal decay of the luminescence signal (IT-TL) for dating. The intensity of the luminescence signal is related to the accumulated energy dose AD (in unit of Gray, Gy) and, thus, to the time interval t (age) during which the mineral has been exposed to the ambient ionizing radiation. The luminescence age is calculated from the accumulated AD and the rate of ionizing radiation DR (dose per time, in unit of Gy a1). t ¼ AD=DR

(7)

From this equation, it becomes clear that the dating procedure consists of two steps: the determination of AD and DR. With increasing radiation dose, the number of empty traps still available becomes fewer, so that the growth curve of the luminescence signal assumes the shape of exponential saturation. In most cases saturation is reached after doses of few 102 Gy. This behavior restricts luminescence dating to the last few 105 years. In order to convert the luminescence signal into a dose value (AD), the sensitivity S to ionizing radiation (luminescence signal per dose, i.e., the slope of the growth curve) has to be determined, varying from sample to sample. For a given sample, it is the same for b- and g-radiation but different for a-radiation. The sensitivity ratio Sa/Sb, the so-called a-value, needs to be determined, but is mostly around 0.1. Another behavior limiting the age range is fading of the latent luminescence signal in the course of time, violating the prerequisite that all centers involved in the signal generation are stable over the complete age range in question. Like any other type of radiation damage, latent luminescence signals are subjected to fading whose kinetics is essentially thermally controlled. As far as nearsurface materials at normal ambient temperatures are concerned, natural fading limits the datable age range up to a few 105 years. An important concept in dating is the resetting of the system: The luminescence systems need to have been reset at the event of interest. Complete or at least partial resetting of the latent luminescence signals is caused by exposure to heat or light. Consequently, the last occurrence of such an event can be dated, for example, the deposition of sediments or the heating of flint artifacts. The past few years have seen a lot of progress in laboratory protocols. Previously, it was common practice in AD evaluation to prepare multiple subsamples (aliquots) and apply various doses in addition to the natural one. Lately, the so-called SAR protocol (Single Aliquot

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_10-4 # Springer-Verlag Berlin Heidelberg 2014

Regeneration) is increasingly preferred, which regenerates the luminescence signal after artificial resetting (Murray and Wintle 2000). When using regenerated growth curves, AD is evaluated through the value of the artificial dose required to produce exactly the same luminescence intensity as the natural one. In order to normalize for sensitivity changes due to the laboratory procedure, a constant test dose is applied and measured for each aliquot at every step in the procedure. However, it is debated if the initial sensitivity changes can be accounted for (e.g., Singhvi et al. 2011). The advantages of the SAR protocol over the conventional multiple-aliquot (MA) technique are smaller sample size, less time for sample preparation, and improved analytical precision due to replicate AD determination. The present technology is directed towards singlegrain protocols that allow the differentiation of AD populations in order to select the results from grains showing the same apparent luminescence age on statistical grounds, which bears a great potential for novel applications (Roberts et al. 1997; Greilich et al. 2002; Greilich and Wagner 2006; Jacobs et al. 2003, 2013). Apart from the accumulated dose AD, the natural dose rate DR needs to be determined for the age calculation. The ionizing radiation at the Earth’s surface originates predominantly from the radionuclides 232Th, 235U,238U, and their daughter products, as well as 40K and 87Rb and, to a minor extent, from cosmic rays. These nuclides emit a-, b-, and g-radiation, each of which has a different penetration depth, amounting in rocks to ca. 20 mm, 2 mm, and 30 cm, respectively. The internal component originating within the luminescence sample as well as the external radiation from the immediate surroundings, i.e., sediment, has to be taken into account. The age determination requires materials of a uniform and defined dose rate. For this reason one separates the sample into certain sizes, usually the fine-grain (4–10 mm) or coarse-grain (100–200 mm) fractions. Since any water residing in pore volumes attenuates the dose rate, the moisture content and its possible temporal variation in the sample as well as its environment need to be estimated. Also the on-site intensity of the cosmic rays has to be assessed. It mainly increases with topographic altitude and decreases with depth below the surface. Temporal variation of the dose rate might be caused by changing contents of radionuclides in sediment due to disequilibrium within the decay chains. All these factors have to be considered carefully, since they may cause major uncertainties in luminescence dating. For dose-rate evaluation, several techniques are available, among them aand b-counting, g-spectrometry, atomic absorption, ICP-MS, and neutron activation analysis. Luminescence dating of clastic sediment enables to determine when it was deposited, provided all of the sedimentary grains were sufficiently exposed to daylight before and during deposition. In this way paleoanthropological remains which are embedded in such sediment series can be dated. In Central Europe – as well as in other periglacial areas – numerous loess profiles with Paleolithic finds have been TL dated (e.g., Zo¨ller et al. 1991). Also many sands have been dated by OSL. An example is the dune sands of the Acheulian open-air site of Holon/Israel where alkali feldspar and quartz fractions were dated by OSL as well as TL (Porat et al. 1999). The presence of sediment remnants in the endocranial cavity of a modern human from Hofmeyer (South Africa) allowed the OSL dating of the deposition of the skull, despite the impossibility of locating the original position of the specimen in its sedimentological context. Quartz grains were extracted and yielded OSL ages of 40.9
4.2 Ka, 33.0
2.5 Ka, and 34.7
3.4 Ka, which were combined to a depositional age of the endocranial sediment of 36.2
3.3 Ka (Grine et al. 2007). However, the presumption that all grains had been completely bleached at deposition is not necessarily fulfilled. In particular, fluvial sands, where grains were transported under water cover, may contain partially bleached or even unbleached grains. In this case the apparent luminescence age would be an overestimate. Also, post-depositional vertical mixing between sedimentary layers,

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_10-4 # Springer-Verlag Berlin Heidelberg 2014

such as bioturbation, leads to erroneous ages. In addition to such phenomena, trampling and human modifications might lead to sediment particles being displaced in archaeological sites. Luminescence measurements of individual grains enable the identification of such disturbances. Because of microdosimetric concerns, this might not always be straightforward because a priori it cannot be differentiated whether the determined ADs are influenced by bleaching or the heterogeneity of the radiation field (microdosimetry). Single-grain OSL dating is always based on the interpretation of statistical analysis of AD results. Strictly, the models applied are those for dose, and not “age” models, which are always analyzed under the assumption of the validity of the statistical parameters and models employed. The potential of single-grain OSL dating was convincingly demonstrated in the case of the Jinmium rock shelter in northern Australia. Fullagar et al. (1996) reported TL ages of 176
16 Ka and 116
12 Ka for the artifact-bearing deposit, which would predate other results for the first arrival of humans in Australia by more than 100 Ka. The data were determined on multiple-grain aliquots of quartz, despite the known presence of erosional fragments from the mother rock in this sandstone abri. An intensive OSL-dating program on the same deposits by Roberts et al. (1999), using the single-grain approach, yielded ages of less than 10 Ka when considering only those grains which had been fully bleached before burial. Furthermore, in Australia single-grain OSL ages of quartz from Malakunanja II now date the early human occupation to 55.5
8.2 Ka (Roberts et al. 1998) and the human burials of Lake Mungo to 40
2 Ka (Olley et al. 2006). Burned flint is well suited for TL dating. Due to a relatively low internal dose rate and good TL-stability behavior, its datable age range reaches back to at least 500 Ka and thus covers a large part of the Paleolithic period. TL dating of flint requires prehistorical annealing (>400  C) of the TL signal, which, fortunately, has been the case for a considerable number of flint artifacts. Because of the dosimetric heterogeneity of most archaeological sites, it is advisable to collect several flint samples from each layer to be dated. Heterogeneity of the internal dose rate can be suspected for flint or similar materials. Such heterogeneities were shown by autoradiography for some samples (Schmidt et al. 2013), but were significant for dose evaluation only in macroscopically well-visible inclusions or veins. Such samples are usually rejected from analysis in any case, because of suspicions of differences in mineralogy and thus luminescence properties, unless mineral phases can be separated. Most TL-dating applications of burnt flint follow MA protocols, which require individual sample sizes larger than can be provided from many sites where burnt material is scarce and small. Detecting the luminescence in a different wavelength, however, allows the successful application of the SAR protocol and thus on small sample sizes (Richter and Krbetschek 2006). Perfect agreement with independent other dating evidence is obtained for an Eemian age site, allowing the direct dating of a prehistoric human activity (Richter and Krbetschek 2014; Sier et al. 2011). Intensive TL-dating studies were carried out at several Levantine sites with rich Lower to Middle Paleolithic lithic industries and human remains of Neanderthals as well as early Moderns. From the site of Tabu¯n/Israel, Mercier and Valladas (2003) report stratigraphically consistent TL ages between 302
27 Ka and 165
16 Ka, indicating that the technological transition from the Acheulian to the Mousterian occurred some 250 Ka ago. Thermoluminescence dating of heated flint revealed the antiquity of the North African technocomplex of the Aterian and its problematic use as a chronostratigraphical meaningful unit. The TL dating of a stratigraphical succession of alternating Aterian (AT) and Mousterian (MOU) industries at Ifri n’Ammar (Morocco) resulted in 83.3
5.6 Ka (AT), 130.0
7.8 Ka (MOU), 145
9 Ka (AT), and 171
12 Ka (MOU) in correct stratigraphic order (Richter et al. 2010).

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_10-4 # Springer-Verlag Berlin Heidelberg 2014

Fig. 2 IR-RF (squares) and ESR/U-series (circles) ages with 1-s uncertainties of samples from the sand pit Grafenrain at Mauer (From Wagner et al. 2010)

At the site of Kebara (Israel), a skeleton of a Neanderthal and, at the sites of Qafzeh and Skhu¯l, remains of archaic early modern humans were recovered. TL dating on 20 flint fragments from the hominid-containing layer in Qafzeh yielded 92
5 Ka. At Kebara, 30 flint artifacts from several layers provided TL ages from 50 to 70 Ka, and the layer with the skeleton of the Neanderthal provided 60 Ka. At Skhu¯l six burnt flints from the level with the remains of archaic early modern humans yielded a TL age of 119
18 Ka (Mercier et al. 1993). These data reveal that early forms of anatomically modern humans were present in the same geographical area as Neanderthals long before modern humans spread into Europe. However, these findings do not reveal if both species were occupying this area at the same time and an alternating scenario related to climate changes is favored. At the early Upper Paleolithic site of Geißenklo¨sterle/Germany, seven flint artifacts from the Early Aurignacian, and two from the Aurignacian levels, ultimately satisfied the criteria of being sufficiently heated (Richter et al. 2000), providing weighted mean ages of 40.2
1.5 Ka and 37.0
1.4 Ka, respectively. The disagreement with radiocarbon ages on bones from the same levels was later determined to have been caused by insufficient removal of contaminants in radiocarbon dating (Higham et al. 2012). The radiocarbon ages confirm the TL data and show their accuracy, while altogether these data imply a much earlier beginning of the Upper Paleolithic figurative art in Central Europe than anywhere in Western and Southwestern Europe. A novel development is the OSL dating of stone surfaces, when daylight exposure in the past reset the OSL signal. Provided the surface was shielded from light since then, the moment of the last exposure to daylight can be determined. This approach opens – at least in principle – a large potential for archaeological, paleoanthropological, and geomorphological applications such as the dating of the construction and destruction of stone structures and buried lithic implements as well as deposited boulders. Hitherto, the new method has been corroborated for granitoid rocks and

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successfully applied in particular to the famous Nazca geoglyphs in southern Peru (Greilich et al. 2005; Greilich and Wagner 2006). Infrared radiofluorescence (IR-RF) is a new method developed by Trautmann et al. (1998) for potassium feldspar and is of particular interest for age ranges beyond 105 years because of its longterm signal stability (Erfurt and Krbetschek 2003). This new method has been shown to provide excellent agreement with a large number of independent age estimates (Degering and Krbetschek 2007). For example, IR-RF dating of the “Mauer sands” at the holotype site of Homo heidelbergensis is in excellent agreement with electron spin resonance dating of animal teeth from the sequence (Fig. 2). However, concerns have been raised on the general applicability (Buylaert et al. 2012), and more data from more than the currently only two laboratories is needed. Various other new luminescence techniques are applied to establish the time of bleaching of sedimentary deposits. Namely, thermally transferred optical stimulation (TT-OSL) and postinfrared infrared stimulated luminescence (post IR-IRSL or pIRIR) are more frequently applied, including sites of paleoanthropological interest (e.g., Sun et al. 2013; Schmidt et al. 2011, respectively). The accuracy of such recent developments, however, has not been shown by fully independent methods so far.

Electron Spin Resonance Electron spin resonance (ESR) dating is also based on the accumulation of radiation-induced energy in minerals and thus has close links to luminescence dating. Although first attempts to exploit the ESR phenomenon for dating go back to the 1960s (Zeller et al. 1967), it did not flourish as a dating method before the 1980s and is still being developed. The ESR method permits age determination up to a few million years, far beyond the range of the luminescence methods, and covers the whole Quaternary period. The most important material for paleoanthropological application is tooth enamel, but quartz separates from sediments at prehistoric sites also have a certain potential (Rink 1997), as well as fluvial sediments. With ESR dating, either the event of the death of a mammal (set equal to sediment deposition and/or, e.g., human occupation), the resetting of a previous system as a result of bleaching of sedimentary quartz grains, or the event of heating of stones is dated. The ESR phenomenon is caused by paramagnetic centers in the crystal lattice. Radiationinduced trapped electrons (see “Luminescence”) form such centers and give rise to characteristic ESR signals. The intensity of the ESR signal is a function of the number of trapped electrons and therefore of the accumulated energy dose AD that has been absorbed from the ionizing radiation in the course of time. In order to calculate the ESR age, the value of AD, obtained from the ESR measurement, is divided by the dose rate DR, in the same manner as already discussed for luminescence (Eq. 7). The quantity of AD is determined by ESR spectrometry, which exploits the fact that trapped electrons are unpaired. Brought into a variable magnetic field and exposed to a given microwave, unpaired electrons show spin resonance at a specific strength of the magnetic field. The condition at which resonance happens is described by the g-value, which is characteristic for the type of the paramagnetic center. The energy necessary for the resonance is absorbed from the microwave so that its intensity reduction is a measure for the concentration of the center. The resulting ESR spectrum shows the specific microwave absorption for various centers with different g-values. Owing to measurement-technical reasons, the ESR spectra of the microwave absorption are not directly recorded; instead their first derivation as a function of the field strength is plotted. For the Page 16 of 31

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evaluation of AD, known artificial doses are applied in addition to the natural one and a signal growth curve is established. ESR has the advantage over luminescence that the concentration of the probed centers is not disturbed by the measurement procedure, thus permitting one to establish an additive growth curve with accumulating doses on the same aliquot. Most samples show exponential saturation functions. At normal ambient temperature of sediment, most ESR centers are sufficiently stable for applying ESR dating up to a few million years. The dose-rate determination follows the same principles as already mentioned for luminescence. For ESR-dating samples of a few grams are sufficient, provided the material is homogenous, but usually larger sample sizes are preferred as they allow the separation of suitable materials in the laboratory to conduct microdosimetric measurements. ESR dating of fossil tooth enamel plays an important role for Paleolithic sites, mainly because teeth are commonly preserved. Mammalian dental issue consists essentially of enamel, dentine, and cementum layers. ESR dating is based on the mineral hydroxyapatite, in particular on its carbonate-containing subspecies dahllite, within the enamel. Dentin and cementum are less dense, contain more organic tissue, and take up uranium more easily than enamel. For these reasons, they are not used for ESR analysis, but must be taken into account for microdosimetric reasons. The ESR spectrum of tooth enamel has, at g ¼ 2.0018, a suitable signal of good sensitivity and high thermal stability. The quantity of the dose rate introduces considerable problems into ESR-age evaluation. Strongly varying uranium contents on the microscopic scale often cause steep dose-rate gradients in teeth, which is in particular the case for the b-component since the b-radiation range (ca. 2 mm) is similar to the thickness of the enamel layers. Teeth gradually take up uranium from the groundwater after burial. In vivo they contain less than 1 mg g1 of U, but fossil ones have up to 1,500 mg g1. This means that the dose rate increases with time and that the closed-system condition is not fulfilled. To allow for the time dependence of the dose rate, distinct models of uranium uptake are assumed, such as the early uptake (EU), the linear uptake (LU), and recent uptake (RU) models. The EU model results in a lower ESR age compared to the LU model due to a higher dose rate on the average. Both model ages may considerably differ from each other, especially for sample with high uranium contents so that samples low in uranium are preferable. Most published ESR-age data are based on assumed U-uptake models. In order to set constraints to the validity of the model, ESR dating is coupled with uranium-series dating (Gr€ un et al. 1988), with new uptake models developed by Shao et al. (2012). The comparison of theoretical closed-system ages of 234U/238U and 230Th/234U with that of ESR enables to discriminate among the hypothetical models. Combined ESR/uranium-series dating has become more and more the routine for tooth enamel dating. The Early and Middle Paleolithic sites of Tabu¯n, Kebara, Skhu¯l, Qafzeh, and Hayonim (Israel), with rich lithic and human bone inventories, play a fundamental role with respect to the early human out-of-Africa dispersion through the Levantine corridor. In order to establish a firm chronology of this process, ESR dating has been repeatedly applied to mammalian tooth enamel from these sites, in addition to uranium series and luminescence. Worth mentioning in this context are two results in particular. First, the combined ESR/uranium-series tooth age of 387
50 Ka confirms a 340
33 Ka TL age on burnt flint for the Lower Paleolithic Yabrudian lithic industry at Tabun, whereby the U uptake appears to be more recent than linear (Rink et al. 2004). Second, the ESR ages on teeth from Middle Paleolithic contexts support the early dating of anatomical Moderns to 80–120 Ka, with the amazing consequence that the Levant was alternating, inhabited by Moderns and Neanderthals for about 60 Ka.

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At the well-known South-African site of Swartkrans, with its wealth of remains of Australopithecus robustus, Curnoe et al. (2001) determined one of the oldest ESR ages so far reported. Coupled ESR/uranium-series dating on two human and two bovid teeth yielded 1630
160 Ka, with a possible maximum of 2110
210 Ka, indicating that ESR dating can provide reasonable results for samples of Late Pleistocene/Early Pleistocene age. Also the Atapuerca Gran Dolina site, northern Spain, with the earliest human remains in Europe of Homo antecessor, was investigated by combined ESR/uranium-series dating. From the bottom of the Aurora stratum, where the very early human remains were recovered, three ungulate teeth gave a mean age of 731
63 Ka, which is in agreement with the paleomagnetic age estimate of >780 Ka (Falgue`res et al. 1999). ESR also permits the dating of calcareous sinter deposits that show complex ESR spectra partially as a result of organic radicals. Important Paleolithic cave sites have been dated, among them Caune de l’Arago at Tautavel, southern France. ESR dating of calcareous deposits under- and overlying the hominid-bearing layer allowed its bracketing between 242 and 313 Ka as upper and 147 Ka as lower age limits, respectively. This result is in good agreement with uranium-series data of 315–220 Ka (Hennig and Gr€ un 1983). The holotype of Homo heidelbergensis was found in 1907 in fluvial sands at Mauer near Heidelberg. The associated mammalian fauna and the geological context place the find layer in the early Middle Pleistocene, but confirmatory chronometric evidence has only been recently achieved by the coupled ESR/U-series dating of mammal teeth and infrared-radiofluorescence dating (IR-RF) of feldspar grains from the sands (Wagner et al. 2010). These “Mauer sands” are subdivided into two distinct units, the “lower sands” and the “upper sands,” separated by a clay/silt layer (Fig. 2). The mandible of Homo heidelbergensis was recovered from a 0.1 m thick gravel layer within the “lower sands.” Both sand units are renowned for their rich early Middle Pleistocene mammal faunas, which clearly indicate warm climate conditions. The good preservation of the mammal bones – and in particular of the human mandible – indicates that they were transported from a nearby fluvial floodplain before becoming embedded in the river deposits, i.e., they have the same geological age as their surrounding sediment layers. Eight herbivore teeth (five from the “lower sands” and three from the “upper sands”) were analyzed with the ESR/U-series technique. Most of the Mauer dental-tissue samples show evidence of postmortem uranium uptake, allowing the calculation of reliable ages (Fig. 2). The IR-RF ages determine the last light exposure of sand grains, i.e., their depositional age. Ten samples from six sediment layers of both sand units were dated using small subsamples of K-feldspar grains (Fig. 2). The weighted mean of the two sand samples Mau 1 and Mau 2, and the dentine sample M0507, yields 609
40 Ka for the find layer of Homo heidelbergensis. This result demonstrates that the mandible is the oldest hominin fossil reported so far from Central and Northern Europe. ESR may also be applied to quartz grains from clastic sediments, provided the grains were exposed to light for about 6 months during sedimentary transportation so that the minimum signal level in Al centers is reached. However, there are so far only a few examples of successful application in paleoanthropology, one being the early Pleistocene Monte Pogglio site, Italy, where more than 4,000 Paleolithic flint artifacts were found in sandy beach deposits. Detrital quartz extracted from different archaeological levels provided a mean age of 1065
165 Ka, which is in agreement with paleomagnetical data (Falgue`res 2003).

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Radiocarbon (14C) Among the physical dating methods, radiocarbon is the most widely known and most commonly applied in archaeology. Essentially, it utilizes organic remains from the last 50 Ka. In the context of paleoanthropology, this covers only the periods from the Late Middle Paleolithic onwards, which comprise a relatively short section of human presence on Earth. Furthermore, its application in the pre-Holocene time range (>12 Ka) is complicated by the fact that calibration procedures for 14C dates cannot be based on high-precision tree-ring data, resulting in low accuracy of the true age. Towards the upper age limit, contamination by modern carbon becomes a dominating problem. Recent natural carbon consists of the two stable isotopes 12C (98.89 %) and 13C (1.11 %), and in very minor traces the radioactive 14C (14C/12C 1012) that decays (t1/2 ¼ 5730 a) under b-emission. 14C is naturally produced in the stratosphere by interaction of neutrons from cosmic rays with atmospheric nitrogen atoms according to the reaction 14 N(n,p)14C. The average global 14 C production rate is 7.5 kg a1, but is subject to considerable temporal variation. Depending on this rate, an equilibrium value between production and radioactive decay is established. Bound in CO2, 14C becomes quickly distributed throughout the atmosphere. By photosynthesis CO2 enters the plants and via the food chain the biosphere. Through dissolution and gas exchange, it is introduced into the hydrosphere, from where it is incorporated as CaCO3 into marine or limnic sediments and organisms. As long as these reservoirs participate in the carbon cycle, their 14C concentration maintains the atmospheric equilibrium value. The carbon becomes separated from the cycle with the death of the organism or with carbonate precipitation, so that the 14C input is interrupted. Thereupon, the 14C/12C ratio declines due to the radioactive decay of 14C. Initially it was assumed by Libby (1952) that the atmospheric 14C/12C was constant. According to this model, the conventional 14C age is calculated (cf. Eq. 5) from the present 14C/12C and an assumed fixed value for (14C/12C)0. The conventional 14C age is linked to the reference year 1950 AD, with the notation “BP” (before present). Conventional 14C ages do not directly provide the right age information, since the simple model condition of a constant initial 14C/12C is invalid. Tree-ring data, for instance, show that within the past 11 Ka, the initial 14C/12C decreased by ca. 10 %, so that a 10 Ka old sample results in a 14C age being ca. 1 Ka too young. In order to obtain accurate ages, the temporal fluctuation of 14C must be corrected for. This is achieved by 14C dating of samples of independently known age (e.g., tree rings). Apart from possible oscillations of the primary cosmic ray flux, the fluctuations in the atmospheric 14C/12C level are attributed to changes in the 14C-production rate, caused by the varying magnetic shielding of the primary cosmic rays; in particular the geomagnetic minimum ca. 40 Ka ago doubled the production rate (Beck et al. 2001). Also, magnetic disturbance originating from solar activity modifies the production rate, although to a lesser degree and on shorter time scales. In this way, high magnetic intensities imply low 14C-production rates and, thus, high apparent 14C ages. On the other hand, the carbon exchange between different reservoirs, mainly the ocean and the atmosphere, affects the atmospheric 14C/12C level. In periods, when the oceanic circulation slows down, less of the “aged” oceanic CO2 is released into the atmosphere, so that atmospheric 14C/12C level increases, leading to apparently younger 14C ages. Regardless of their origin, these fluctuations necessitate calibration of the 14C results. By calibration the chronologically irrelevant conventional radiocarbon age is converted to a calendar time scale. This is achieved via calibration curves, in which conventional 14C ages are plotted versus the true known calendar ages of the same samples determined by other means. For the Holocene this is achieved with high accuracy by dendro-calibration. For the late Pleistocene, other archives than tree rings are needed due to the scarcity of trees during glacial climate. Page 19 of 31

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Annually varved sediments, shallow-water corals, and planktonic foraminifera, which can be independently dated with uranium-series techniques, have been used for this purpose, with the latest efforts presented as the INTCAL09 curve (Reimer et al. 2009). While this calibration curve covers the entire radiocarbon age range of ca. 50 Ka, its reliance on marine material for the correction of terrestrial material is not favorable because of the required marine reservoir correction. However, the IntCal13 radiocarbon calibration curve under construction will be much more based on terrestrial high-precision records of the varved sediments from Lake Suigetsu (Bronk Ramsey et al. 2012) in its lower age range, together with speleothems from the Bahamas and Hulu Cave, and support from marine data for its entire time range (Reimer et al. 2013). Nevertheless, a particular complication resulting in lower precision is posed by the strong 14C fluctuations that are associated with the magnetic minima during the Laschamp and Mono Lake geomagnetic excursions around 40 and 33 Ka ago, respectively, which are crucial periods in the peopling of Europe. In order to distinguish calibrated 14C ages from conventional ones, they are characterized by the notations “cal BC” (calendar years BC), “cal AD” (calendar years AD), or “cal BP” (calendar years before 1950 AD). In publications it always has to be stated which calibration curve and which software were used. Furthermore, the original radiocarbon date should always be provided together with the lab code. This will allow future calibration with improved calibration curves that are expected to provide increased precision and accuracy, as has already been the case for the dendrocalibrated age range. Apart from the temporal fluctuations, problems arise from spatial 14C inhomogeneities in the materials and reservoirs participating in the carbon cycle. One distinguishes isotope fractionation and reservoir effects. Photosynthesis, for instance, enriches the light 12C over the heavy 13C, and in turn the latter over the even heavier 14C, so that the carbon in plants is isotopically lighter than in the atmosphere. For most materials, the age corrections caused by isotope fractionation are less than 80 Ka, but may amount up to several hundred years, as in the case of marine limestones and organisms. The reservoir effect deals with the isotopic variation of carbon within the reservoir, from which the organisms extract their carbon. Such spatial changes may have various causes. If the carbon stays long – with respect to the 14C half-life – within the same reservoir, the 14C concentration declines (“aging” of carbon). A prominent example is the “marine reservoir effect” in the oceans where upwelling regions have present-day apparent 14C ages of around 400 Ka. Also the admixture of “aged” carbon lowers the 14C concentration, such as in the “hard-water effect” in carbonaceous groundwater and surface water. Reservoir effects result in an apparent increase of the 14 C age and are difficult to assess. As in other radiometric dating methods, the 14C system has to remain closed, i.e., carbon must neither enter nor leave the sample. The 14C age is lowered by uptake of recent carbon. Common sources of contamination with recent carbon are the presence of rootlets, humic acid infiltration, and bioturbation. The smaller the authigenic 14C amount and the older the sample is, the more the danger of contamination by modern carbon increases. For this reason the applicability of 14C dating at old ages is limited by unavoidable contamination rather than by the instrumental capabilities of 14 C detection. The upper dating limit (maximum age) is reached when the 14C of an old sample cannot be discriminated with sufficient statistical confidence from the background. The AMS technique has the great potential to lower the instrumental background and thus to extend the maximum age, but the latter is effectively limited by the 14C background due to contamination of samples themselves and by sample preparation, as well as by techniques employed for sample purification. As a rule of thumb, the oldest radiocarbon age from a given context with unequivocal association with the sample and that satisfies all quality criteria would provide the closest Page 20 of 31

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_10-4 # Springer-Verlag Berlin Heidelberg 2014

radiocarbon age estimate of the true age where contamination of samples is believed to be a problem. Recent developments in pretreatment chemistry to remove contamination have yielded older radiocarbon age estimates for the majority of samples, but not all. The amount of sample required for 14C dating depends on the carbon content, the conditions of preservation, the degree of contamination, and the technique of 14C detection. For b-counting, either in gas or liquid scintillation counters, 5–10 g of extracted carbon usually is needed. The AMS technique requires carbon in the mg range. Note that the quoted amounts refer to carbon, and not to sample. The required amount of the latter one might be larger by a factor of 10 or so, depending on the carbon content. Bones and antler are among the most frequently used paleoanthropological sample materials for 14 C dating. As long as their inorganic fraction was used, bones were considered as a problematic material for 14C dating due to open-system behavior. However, their organic substance consisting predominantly of various proteins, generally classed as collagen, is more resistant to exchange. The collagen is chemically extracted as acid-insoluble residue, sometimes physically separated (e.g., ultrafiltration), and then usually subjected to AMS analysis. Contamination issues appear to be drastically reduced with procedures like ultrafiltration, but cannot be entirely ruled out a priori, especially for old bones with little collagen preservation or which had been subjected to preservation, e.g., with glue. This is particularly problematic with human bones, which are more frequently treated, and establishing the time of Neanderthal replacement by modern humans has been especially hampered by significantly varying radiocarbon dating results for the same human bones both between and within laboratories. However, by extraction, identification, and subsequent single amino acid radiocarbon dating of the collagen specific compound of hydroxyproline, it can be assured that only carbon from collagen of a particular bone is dated (Marom et al. 2012) and contamination is thus reduced to the maximum extent possible. This specific technique was applied to the early modern human skeleton from Kostenki 14 (Markina Gora), which has been attributed to the Upper Paleolithic but yielded direct radiocarbon ages between 4 and 14 Ka 14C. By single amino acid radiocarbon dating, an age of 33 Ka 14C was established and the Upper Paleolithic age confirmed (Marom et al. 2012). Such diversities in radiocarbon dating results have fed extended debates particularly on the Neanderthal replacement, which corresponds to the Middle to Upper Paleolithic “transition” of European lithic industries. Human remains are exceptional, and radiocarbon dating of archaeological layers is therefore usually based on associated animal bones, which provided AMS radiocarbon results, e.g., between 28 and 40 Ka 14C for the Aurignacian levels of the Geißenklo¨sterle Cave (Germany). This long time span, which is inconceivable with other evidence, was attributed to unusually strong variations in the production of atmospheric radiocarbon and/or taphonomic processes resulting in the mixing of the bones of various ages within the site. Only a systematic study with thorough decontamination (ultrafiltration) techniques eventually yielded consistent radiocarbon dating results for the site (Higham et al. 2012). The preexisting chronostratigraphy already established by thermoluminescence (TL) dating results on burnt flint (Richter et al. 2000) was confirmed by good agreement. These data show the presence of the Aurignacian and elaborate figurative art earlier than anywhere else in Europe. Within the same framework, radiocarbon dating of bone has shown the human burial at the Vogelherd Cave (Germany), believed to be associated with similar artwork, to be a Holocene intrusion (Conard et al. 2004). Similarly, a number of other supposedly Upper Paleolithic human remains from Europe were dated by radiocarbon to be of much younger age, emphasizing the crucial requirement of establishing an unequivocal association of dated sample and archaeological context. In light of the recent possibility of single amino acid radiocarbon dating, however, Page 21 of 31

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_10-4 # Springer-Verlag Berlin Heidelberg 2014

reinvestigations might need to be considered. On the other hand, the oldest directly dated anatomically modern human remains from Pes¸tera Cu Oase (Romania) are not associated with any archaeological remains and are dated by radiocarbon to 34,000–36,000 14C years BP (Trinkaus et al. 2003), which translates to ca. 42–37.8 Ka cal BP. Another important dating material is charcoal, which is often viewed as much more reliable than bone radiocarbon dating because of more efficient methods for decontamination. In the age range of interest in paleoanthropology, which is close to the limits of the method, however, the application of pretreatment methods indicates underestimation of many radiocarbon dates on charcoal in the 40 Ka range. Comparison of radiocarbon dating of charcoal associated with the independently well-dated Campanian Ignimbrite (CI) tephra showed consistent older and more accurate ages with ABOx-SC pretreatments, compared to the simpler chemical sample preparation of ABA (Wood et al. 2012). Charcoal radiocarbon dating shows the contemporaneity of the lithic technocomplexes of the Proto-Aurignacian and the Uluzzian, the latter of which is considered as a “transitional” industry. While the former is believed to be associated with modern humans, the latter is traditionally assigned to Neanderthals, and these species appear to have occupied different parts of Italy at the same time before the Campanian Eruption 39 Ka ago. Likewise bone radiocarbon dating, the association of charcoal samples should be shown first, e.g., by verification, if the plant species is in accordance with the paleoenvironmental setting. Limnic sediments form an important archive for the climatic fluctuations of the past, and if they contain organic matter, 14C dating can be directly applied, in particular to peat and sapropel. An excellent material for AMS 14C dating is macrofossils, such as nutshells, fruit kernels, and leaves, recovered from sediments. Such fossils are short-lived and free of the hard-water effect. When dating secondary calcareous sinter, the uptake of a certain fraction of “dead” carbon from geologically old limestone must be taken into account, which lowers the reliability of such dates. When using mollusk shells, the marine or hard-water reservoir effect, depending on the habitat of the mollusks, needs to be considered. Paleolithic rock paintings commonly contain organic material, such as charcoal, carbonized plant matter, pigments, plant fibers, blood, fatty acids, and beeswax, which enables 14C dating. Radiocarbon dating of micro-samples of charcoal from elaborate rock paintings at the cave of Chauvet-Pont-d’Arc (France), which was sealed by 21 Ka ago, provides further evidence on the early “artistic” expressions of modern humans, with radiocarbon ages around 30 Ka 14C (Valladas et al. 2005). These thus belong among the earliest examples of prehistoric rock art so far discovered.

Cosmogenic 26Al/10Be The Earth is exposed to a steady flux of cosmic rays – mainly hydrogen and helium nuclei – which interact with the atoms of the atmosphere and reach the Earth’s surface strongly attenuated and modified. There they are shortly stopped by nuclear reactions producing in situ radioactive as well as stable cosmogenic nuclei. For dating applications, the radioactive cosmogenic nuclides 10Be, 26 Al, 32Si, 36Cl, and 41Ca are used. Due to nuclear reactions, the cosmic rays become absorbed essentially within the upper few meters of the rock surface. Most cosmogenic nuclides occur in extremely low concentrations, requiring very sensitive detection techniques such as accelerator mass spectrometry. For radioactive cosmogenic nuclides, concentration N [atoms g1] grows gradually with the duration of exposure, until after about five half-lifes (t1/2) it reaches an equilibrium level Ng between production and decay. The “exposure age” of a sample, at first completely shielded Page 22 of 31

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_10-4 # Springer-Verlag Berlin Heidelberg 2014

from and later suddenly exposed to cosmic radiation, derives from the amount of the radioactive nuclides N according to
t ¼ ln 1  ln2=t1=2  N=P  t1=2 =ln2 (8) where P is the cosmogenic production rate of N. If a sample already at its level Ng is suddenly shielded from cosmic radiation, so that production is suspended, the nuclide content N declines by radioactive decay and the beginning of shielding, i.e., the “burial age,” can be dated according to
t ¼ ln N g =N  t1=2 =ln2 (9) The exact knowledge of the production rates of the various cosmogenic nuclides is a prerequisite for their dating application. These rates are derived by experimental measurements as well as theoretical calculations. The decrease from the poles to the equator is known as latitude effect. Also an altitude effect needs to be taken into account, since P increases strongly with altitude. The analysis of 26Al should always be combined with that of 10Be (26Al/10Be method), in order to eliminate uncertainties about production rates. For the production rate ratio 26Al/10Be in quartz, a value of 6.1 was reported (Nishiizumi et al. 1989). Once the rock is shielded from further cosmogenic production, this ratio decays with an effective half-life of 1.36
0.07 Ma, which enables its application in the 10 Ka to 10 Ma age range. Burial dating with cosmogenic 26Al and 10Be was first applied to quartz gravels in caves for deriving river incision rates (Granger and Muzikar 2001). Later the hominin sites at Sterkfontein (Partridge et al. 2003) and Sima del Elefante at Atapuerca (Carbonell et al. 2008) were dated with this technique. 26Al/10Be burial dating of quartz-bearing sediments and artifacts from the lower strata of the Zhoukoudian karstic cave, where early representatives of Homo erectus were discovered, has been carried out by Shen et al. (2009). There, the sediment was transported by fluvial processes from the source into the cultural layers, ca. 20–25 m below the current surface at the time of occupation. The weighted mean age of three sediment samples and three quartzite artifacts gave 770
80 Ka for the lower layers 7–10. However, these ages are substantially older than previous dating attempts (cf. uranium series and fission track).

Conclusion Dating methods based on radioactive decay are in principle independent clocks, that is, they rely solely on the measurement of radiometric quantities, on known physical constants, and on natural isotopic abundances. The potassium–argon, fission-track, luminescence, electron spin resonance, uranium-series, and 26Al/10Be methods exploit such independent clocks. Radiocarbon, on the other hand, is a dependent clock, since it requires calibration by independently derived ages, for instance, by dendrochronology, varve chronology, and/or uranium-series dating. Radiometric dating provides the baseline for calibration of other dating approaches, such as isotope stratigraphy, climate stratigraphy, bio-stratigraphy, and magneto-stratigraphy, as well as by astronomical and chemical means. All these latter techniques rely on natural changes with varying rates that are more or less predictable. Only through calibration do these techniques become chronometric tools. During the last few decades, a solid chronology for the time since hominids entered the scene some five million years ago has been established through radiometric dating. Present

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_10-4 # Springer-Verlag Berlin Heidelberg 2014

methodological developments focus primarily on improving the time resolution of these methods, a prerequisite of deciphering natural and cultural processes. Paleoanthropological knowledge and concepts have greatly benefited from these advances.

Cross-References ▶ Archaeology ▶ Dispersals of Early Humans: Adaptations, Frontiers, and New Territories ▶ Geological Background of Early Hominid Sites in Africa ▶ Origin of Modern Humans ▶ Overview of Paleolithic Archaeology ▶ Patterns of Diversification and Extinction ▶ Quaternary Deposits and Paleosites ▶ Quaternary Geology and Paleoenvironments ▶ The Earliest Putative Hominids ▶ The Earliest Putative Homo Fossils ▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments

References Aitken MJ (1985) Thermoluminescence dating. Academic, London Aitken MJ (1998) An introduction to optical dating. Oxford University Press, Oxford Aubert M, Pike AWG, Stringer C, Bartsiokas A, Kinsley L, Eggins S, Day M, Gr€ un R (2012) Confirmation of a late middle Pleistocene age for the Omo Kibish 1 cranium by direct uraniumseries dating. J Hum Evol 63:704–710 Balter V, Blichert-Toft J, Braga J, Telouk P, Thackeray F, Albarede F (2008) U-Pb dating of fossil enamel from the Swartkrans Pleistocene hominid site, South Africa. Earth Planet Sci Lett 267:236–246 Beck JW, Richards DA, Edwards RL, Silverman BW, Smart PL, Donahue DJ, Hererra-Osterheld S, Burr GS, Calsoyas L, Jull AJT, Biddulph D (2001) Extremely large variations of atmospheric 14 C concentration during the last glacial period. Science 292:2453–2458 Bischoff JL, Shamp DD, Aramburu A, Arsuaga JM, Carbonell E, Bermu´dez de Castro JM (2003) The Sima de los Huesos hominids date to beyond U/Th equilibrium (>350 ka) and perhaps to 400–500 kyr: new radiometric dates. J Archaeol Sci 30:275–280 Bøtter-Jensen L, McKeever SWS, Wintle AG (2003) Optically stimulated luminescence dosimetry. Elsevier, Amsterdam Bronk Ramsey C, Staff RA, Bryant CL, Brock F, Kitagawa H, van der Plicht J, Schlolaut G, Marshall MH, Brauer A, Lamb HF, Payne RL, Tarasov PE, Haraguchi T, Gotanda K, Yonenobu H, Yokoyama Y, Tada R, Nakagawa T (2012) A complete terrestrial radiocarbon record for 11.2 to 52.8 kyr B.P. Science 338:370–374 Brown FH, McDougall I (2011) Geochronology of the Turkana depression of Northern Kenya and Southern Ethiopia. Evol Anthropol 20:217–227 Brown FH, McDougall I, Fleagle JG (2012) Correlation of the KHS Tuff of the Kibish formation to volcanic ash layers at other sites, and the age of early Homo sapiens (Omo I and Omo II). J Hum Evol 63:577–585 Page 24 of 31

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Falgue`res C, Yokoyama Y, Shen G, Bischoff JL, Ku TL, de Lumley H (2004) New U-series dates at the Caune de l’Arago. J Archaeol Sci 31:941–952 Faupl P, Richter W, Urbanek C (2003) Geochronology (communication arising): dating of the Herto hominin fossils. Nature 426:621–622 Feibel CS, Brown FH, McDougall I (1989) Stratigraphic context of fossil hominids from the Omo group deposits: Northern Turkana Basin, Kenya and Ethiopia. Am J Phys Anthropol 78:595–622 Fitch FJ, Miller JA (1970) New hominid remains and early artefacts from northern Kenya. Nature 226:223–228 Fullagar RLK, Price DM, Head LM (1996) Early human occupation in northern Australia: archaeology and thermoluminescence dating of Jinmium rock-shelter, Northern Territory. Antiquity 70:751–773 Gleadow AJW (1980) Fission track age of the KBS tuff and associated hominid remains in northern Kenya. Nature 284:225–230 Granger DE, Muzikar PF (2001) Dating sediment burial with in situ-produced cosmogenic nuclides: theory, techniques, and limitations. Earth Planet Sci Lett 188:269–281 Greilich S, Glasmacher UA, Wagner GA (2002) Spatially resolved detection of luminescence: a unique tool for archaeochrometry. Naturwissenschaften 89:371–375 Greilich S, Glasmacher UA, Wagner GA (2005) Optical dating of granitic stone surfaces. Archaeometry 47:645–665 Greilich S, Wagner GA (2006) Development of a spatially resolved dating technique using HR-OSL. Radiat Meas 41:738–743 Grine FE, Bailey RM, Harvati K, Nathan RP, Morris AG, Henderson GM, Ribot I, Pike AWG (2007) Late Pleistocene human skull from Hofmeyr, South Africa, and modern human origins. Science 315:226–229 Gr€ un R, Schwarcz HP, Chadam J (1988) ESR dating of tooth enamel: coupled correction for U-uptake and U-series disequilibrium. Nucl Tracks Radiat Meas 14:237–241 Gr€ un R, Aubert M, Joannes-Boyau R, Moncel M-H (2008) High resolution analysis of uranium and thorium concentration as well as U-series isotope distributions in a Neanderthal tooth from Payre (Arde`che, France) using laser ablation ICP-MS. Geochim Cosmochim Acta 72:5278–5290 Gr€ un R, Aubert M, Hellstrom J, Duval M (2010) The challenge of direct dating old human fossils. Quatern Int 223–224:87–93 Gubbins D, Herrero-Bervera E (2007) Encyclopedia of geomagnetism and paleomagnetism, Encyclopedia of earth sciences series. Springer, Dordrecht Guo SL, Liu SS, Sun FS, Zhang F, Zhou SH, Hao XH, Hu RY, Meng W, Zhang PF, Liu JF (1991) Age and duration of Peking man site by fission track method. Nucl Tracks Radiat Meas 19:719–724 Hart WK, WoldeGabriel G, Katoh S, Renne PR, Suwa G, Asfaw B, White TD (2003) Geochronology (communication arising): dating of the Herto hominin fossils. Nature 426:622–622 Hennig GJ, Gr€ un R (1983) ESR dating in quaternary geology. Quatern Sci Rev 2:157–238 Higham T, Basell L, Jacobi R, Wood R, Ramsey CB, Conard NJ (2012) Τesting models for the beginnings of the Aurignacian and the advent of figurative art and music: the radiocarbon chronology of Geißenklo¨sterle. J Hum Evol 62:664–676 Hurford AJ, Gleadow AJW, Naeser CW (1976) Fission-track dating of pumice from the KBS Tuff, East Rudolf, Kenya. Nature 263:738–740 Ivanovich M, Harmon S (1992) Uranium-series disequilibrium: applications to earth, marine, and environmental sciences. Clarendon, Oxford

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Jacobs Z, Duller GAT, Wintle AG (2003) Optical dating of dune sand from Blombos Cave, South Africa: II – single grain data. J Hum Evol 44:613–625 Jacobs Z, Hayes EH, Roberts RG, Galbraith RF, Henshilwood CS (2013) An improved OSL chronology for the Still Bay layers at Blombos Cave, South Africa: further tests of single-grain dating procedures and a re-evaluation of the timing of the Still Bay industry across southern Africa. J Archaeol Sci 40:579–594 Kappelman J, Swisher CC III, Fleagle JG, Yirga S, Bown TM, Feseha M (1996) Age of Australopithecus afarensis from Fejej, Ethiopia. J Hum Evol 30:139–146 Leakey MG, Spoor F, Dean MC, Feibel CS, Anton SC, Kiarie C, Leakey LN (2012) New fossils from Koobi Fora in northern Kenya confirm taxonomic diversity in early Homo. Nature 488:201–204 Libby WF (1952) Radiocarbon dating. University of Chicago Press, Chicago Mallick R, Frank N (2002) A new technique for precise uranium-series dating of travertine microsamples. Geochim Cosmochim Acta 66:4261–4272 Marom A, McCullagh JSO, Higham TFG, Sinitsyn AA, Hedges REM (2012) Single amino acid radiocarbon dating of upper paleolithic modern humans. Proc Natl Acad Sci USA 109:6878–6881 McDougall I (1985) K-Ar and 40Ar/39Ar dating of the hominid-bearing Pliocene-Pleistocene sequence at koobi fora, Lake Turkana, northern Kenya. Geol Soc Am Bull 96:159–175 McPherron SP, Alemseged Z, Marean CW, Wynn JG, Reed D, Geraads D, Bobe R, Bearat HA (2010) Evidence for stone-tool-assisted consumption of animal tissues before 3.39 million years ago at Dikika, Ethiopia. Nature 466:857–860 Mercier N, Valladas H (2003) Reassessment of TL age estimates of burnt flints form the Paleolithic site of Tabun Cave, Israel. J Hum Evol 45:401–409 Mercier N, Valladas H, Bar-Yosef O, Vandermeersch B, Stringer CB, Joron JL (1993) Thermoluminescence date for the Mousterian burial site of Es-Skhul, Mt. Carmel. J Archaeol Sci 20:169–174 Millard AR, Pike AWG (1999) Uranium-series dating of the Tabun Neanderthal: a cautionary note. J Hum Evol 36:581–585 Morwood MJ, O’Suulivan PB, Aziz F, Raza A (1998) Fission-track ages of stone tools and fossils on the east Indonesian island of Flores. Nature 392:173–176 Murray AS, Wintle AG (2000) Luminescence dating of quartz using an improved single-aliquot regenerative-dose protocol. Radiat Meas 32:57–73 Nishiizumi K, Winterer EL, Kohl CP, Klein J, Middleton R, Lal D, Arnold JR (1989) Cosmic ray production rates of 10Be and 26Al in quartz from glacially polished rocks. J Geophys Res Solid Earth 94:17907–17915 Noller JS, Sowers JM, Lettis WR (2000) Quaternary geochronology: methods and applications, AGU reference shelf. American Geophysical Union, Washington Olley JM, Roberts RG, Yoshida H, Bowler JM (2006) Single-grain optical dating of grave-infill associated with human burials at Lake Mungo, Australia. Quatern Sci Rev 25:2469–2474 Partridge TC, Granger DE, Caffee MW, Clarke RJ (2003) Lower Pliocene Hominid remains from Sterkfontein. Science 300:607–613 Pike AWG, Hoffmann DL, Garcı´a-Diez M, Pettitt PB, Alcolea J, De Balbı´n R, Gonza´lez-Sainz C, Lasheras JA, Montes R, Zilha˜o J (2012) U-series dating of Paleolithic art in 11 caves in Spain. Science 336:1409–1413 Porat N, Zhou LP, Chazan M, Nyo T, Horwitz LK (1999) Dating the Lower Palaeolithic open-air site of Holon, Israel by luminescence and ESR techniques. Quatern Res 51:328–341 Page 27 of 31

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Reimer P, Baillie M, Bard E, Bayliss A, Beck J, Blackwell P, Bronk Ramsey C, Buck C, Burr G, Edwards R, Friedrich M, Grootes P, Guilderson T, Hajdas I, Heaton T, Hogg A, Hughen K, Kaiser K, Kromer B, McCormac F, Manning S, Reimer R, Richards D, Southon J, Talamo S, Turney C, van der Plicht J, Weyhenmeyer C (2009) IntCal09 and Marine09 radiocarbon age calibration curves, 0–50,000 years cal BP. Radiocarbon 51:1111–1150 Reimer PJ, Bard E, Bayliss A, Beck JW, Blackwell PG, Ramsey CB, Buck CE, Edwards RL, Friedrich M, Grootes PM, Guilderson TP, Hajdas I, Hatte´ C, Heaton TJ, Haflidason H, Hogg AG, Hughen KA, Kaiser KF, Kromer B, Manning SW, Niu M, Reimer RW, Richards DA, Scott EM, Southon JR, Turney CSM, Jvd P (2013) INTCAL13 and MARINE13 radiocarbon age calibration curves 0–50,000 years cal BP. Radiocarbon 55(4):1869–1887 Richter D, Krbetschek M (2006) A new thermoluminescence dating technique for heated flint. Archaeometry 48:695–705 Richter D, Krbetschek M (2014) Preliminary Luminescence Dating Results for two middle Palaeolithic occupations at Neumark-Nord 2. In: Gaudzinski-Windheuser S, Roebroeks W (eds) Multidisciplinary Studies of the Middle Palaeolithic record from Neumark-Nord (Germany). Volume 1. Vero¨ffentlichungen des Landesamtes f€ ur Denkmalpflege und Archa¨ologie Sachsen-Anhalt 68, Landesamt f€ ur Denkmalpflege und Archa¨ologie SachsenAnhalt, Halle, in press. Richter D, Waiblinger J, Rink WJ, Wagner GA (2000) Thermoluminescence, electron spin resonance and 14C dating of the late middle and early upper Palaeolithic site of Geißenklo¨sterle cave in southern Germany. J Archaeol Sci 27:71–89 Richter D, Moser J, Nami M, Eiwanger J, Mikdad A (2010) New chronometric data from Ifri n’Ammar (Morocco) and the chronostratigraphy of the Middle Palaeolithic in the Western Maghreb. J Hum Evol 59:672–679 Rink WJ (1997) Electron spin resonance (ESR) dating and ESR applications in Quaternary science and archaeometry. Radiat Meas 27:975–1025 Rink WJ, Schwarcz HP, Ronen A, Tsatskin A (2004) Confirmation of a near 400 ka age for the Yabrudian industry at Tabun cave, Israel. J Archaeol Sci 31:15–20 Roberts R, Walsh G, Murray AS, Olley J, Jones R, Morwood M, Tuniz C, Lawson E, Macphail M, Bowdery D, Naumann I (1997) Luminescence dating of rock art and past environments using mud-wasps nests in northern Australia. Nature 387:696–699 Roberts RG, Yoshida H, Galbraith RF, Laslett GM, Jones R, Smith M (1998) Single-aliquot and single-grain optical dating confirm thermoluminescence age estimates at Malakunanja II rock shelter in northern Australia. Ancient TL 16:19–24 Roberts RG, Galbraith RF, Olley JM, Yoshida H, Laslett GM (1999) Optical dating of single and multiple grains from Jinmium rock shelter, northern Australia: part II, results and implications. Archaeometry 41:365–395 Sambridge M, Gr€ un R, Eggins S (2012) U-series dating of bone in an open system: the diffusionadsorption-decay model. Quatern Geochronol 9:42–53 Schmidt ED, Frechen M, Murray AS, Tsukamoto S, Bittmann F (2011) Luminescence chronology of the loess record from the To¨nchesberg section: a comparison of using quartz and feldspar as dosimeter to extend the age range beyond the Eemian. Quatern Int 234:10–22 Schmidt C, Rufer D, Preusser F, Krbetschek M, Hilgers A (2013) The assessment of radionuclide distribution in silex by autoradiography in the context of dose rate determination for thermoluminescence dating. Archaeometry 55:407–422 Schwarcz HP (1989) Uranium series dating of Quaternary deposits. Quatern Int 1:7–17

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Schwarcz HP, Simpson JJ, Stringer CB (1998) Neanderthal skeleton from Tabun: U-series data by gamma-ray spectrometry. J Hum Evol 35:635–645 Semah S, Saleki H, Falgueres C (2000) Did early man reach java during the late Pleistocene? J Archaeol Sci 27:763–769 Semaw S, Rogers MJ, Quade J, Renne PR, Butler RF, Dominguez-Rodrigo M, Stout D, Hart WS, Pickering T, Simpson SW (2003) 2.6-million-year-old stone tools and associated bones from OGS-6 and OGS-7, Gona, Afar, Ethiopia. J Hum Evol 45:169–177 Shao Q, Bahain J-J, Falgue`res C, Dolo J-M, Garcia T (2012) A new U-uptake model for combined ESR/U-series dating of tooth enamel. Quatern Geochronol 10:406–411 Shen G, Ku TL, Cheng H, Edwards RL, Yuan Z, Wang Q (2001) High-precision U-series dating of locality 1 at Zhoukoudian, China. J Hum Evol 41:679–688 Shen G, Wang W, Wang Q, Zhao J, Collerson K, Zhou C, Tobias PV (2002) U-series dating of Liujiang hominid site in Guangxi, southern China. J Hum Evol 43:817–829 Shen G, Gao X, Gao B, Granger DE (2009) Age of Zhoukoudian Homo erectus determined with 26Al/10Be burial dating. Nature 458:198–200 Sier MJ, Roebroeks W, Bakels CC, Dekkers MJ, Br€ uhl E, De Loecker D, Gaudzinski-WindheuserS, Hesse N, Jagich A, Kindler L, Kuijper WJ, Laurat T, M€ ucher HJ, Penkman KEH, Richter D, van Hinsbergen DJJ (2011) Direct terrestrial-marine correlation demonstrates surprisingly late onset of the last interglacial in central Europe. Quatern Res 75:213–218 Singhvi A, Stokes S, Chauhan N, Nagar Y, Jaiswal M (2011) Changes in natural OSL sensitivity during single aliquot regeneration procedure and their implications for equivalent dose determination. Geophys J Roy Astron Soc 38:231–241 Smits F, Gentner W (1950) Argonbestimmungen an Kaliummineralen, I: Bestimmungen an tertia¨ren Kalisalzen. Geochim Cosmochim Acta 1:22–27 Sun X, Lu H, Wang S, Yi S, Shen C, Zhang W (2013) TT-OSL dating of Longyadong Middle Paleolithic site and paleoenvironmental implications for hominin occupation in Luonan Basin (central China). Quatern Res 79:168–174 Swisher CC III, Curtis GH, Jacob T, Getty AG, Suprijo AW (1994) Age of the earliest known hominids in Java, Indonesia. Science 263:1118–1121 Taylor RE, Aitken MJ (1997) Chronometric dating in archaeology, vol 2, Advances in archaeological and museum science. Plenum Press, New York Trautmann T, Krbetschek MR, Dietrich A, Stolz W (1998) Investigations of feldspar radioluminescence: potential for a new dating technique. Radiat Meas 29:421–425 Trinkaus E, Moldovan O, Milota S, Bıˆlgar A, Sarcina L, Athreya S, Bailey SE, Rodrigo R, Mircea G, Higham T, Bronk Ramsey C, van der Plicht J (2003) An early modern human from the Pes¸tera cu Oase, Romania. Proc Natl Acad Sci Am 100:11231–11236 Valladas H, Tisne´rat-Laborde N, Cachier H, Kaltnecker E´, Arnold M, Oberlin C, Evin J (2005) Bilan des datations carbone 14 effectue´es sur des charbons de bois de la grotte Chauvet. Bull Soc Pre´hist Franc¸aise 102:109–113 Wagner GA (1998) Age determination of young rocks and artifacts – physical and chemical clocks in quaternary geology and archaeology. Springer, Berlin/Heidelberg/New York Wagner GA, Van den haute P (1992) Fission-track dating. Enke, Stuttgart Wagner GA, Krbetschek M, Degering D, Bahain J-J, Shao Q, Falgue`res C, Voinchet P, Dolo J-M, Garcia T, Rightmire GP (2010) Radiometric dating of the type-site for Homo heidelbergensis at Mauer, Germany. Proc Natl Acad Sci USA 107:19726–19730 Walker M (2005) Quaternary dating methods. Wiley, Chichester

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Walter RC, Manega PC, Hay RL, Drake RE, Curtis GH (1991) Laser fusion 40Ar/39Ar dating of Bed I, Olduvai Gorge, Tanzania. Nature 354:145–149 Wood B (2011) Did early Homo migrate “out of” or “in to” Africa? Proc Natl Acad Sci USA 108:10375–10376 Wood RE, Douka K, Boscato P, Haesaerts P, Sinitsyn A, Higham TFG (2012) Testing the ABOxSC method: dating known-age charcoals associated with the Campanian Ignimbrite. Quatern Geochronol 9:16–26 Yukihara EG, McKeever SWS (2011) Optically stimulated luminescence: fundamentals and applications. Wiley-Blackwell, Oxford Zaim Y, Ciochon RL, Polanski JM, Grine FE, Bettis Iii EA, Rizal Y, Franciscus RG, Larick RR, Heizler M, Aswan EKL, Marsh HE (2011) New 1.5 million-year-old Homo erectus maxilla from Sangiran (Central Java, Indonesia). J Hum Evol 61:363–376 Zeller E, Levy P, Mattern P (1967) Geologic dating by electron spin resonance. In: Radioactive dating and methods of low-level counting: proceedings of symposium, international atomic energy agency in cooperation with joint commission on applied radioactivity (ICSU), Monaco, March 2–10, 1967. IAEA, Vienna, pp 531–540 Zo¨ller L, Conard NJ, Hahn J (1991) Thermoluminescence dating of Middle Palaeolithic open air sites in the middle Rhine valley/Germany. Naturwissenschaften 78:408–410

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Index Terms: Absolute dating 2 Ar/Ar 5 Chronometric dating 2–3 Cosmogenic nuclei 22 Cosmogenic nuclides 3 Dating method 4, 7, 10–11, 16 Electron-spin-resonance (ESR) 16 ESR 16 Fission-tracks 10 Numerical dating 2, 7 Optically stimulated luminescence (OSL) 13, 15 Palaeomagnetism 4 Potassium-Argon 4 Radioactive decay 3 Radiocarbon 19 Relative dating 4 Thermoluminescence 14 Uranium series 7

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_11-3 # Springer-Verlag Berlin Heidelberg 2013

Geological Background of Early Hominid Sites in Africa Ottmar Kullmer* Senckenberg Museum, Abt. Paläoanthropologie und Quartärpaläontologie, Frankfurt, Germany

Abstract Hominid remains are rare elements in the fossil record. Probably, the small population sizes of early hominids, in combination with preservation constraints, limit any probability of a higher frequency of fossil discoveries. The early evolution of mankind appears to be a Pan-African story, even though the distribution pattern of remains concentrates on eastern and southern Africa. More recent findings from the Chad Basin in central Africa demonstrate that fossil hominid remains are not restricted to the eastern part of Africa. The success of exploration in paleoanthropology depends on the discovery of appropriate sediment layers, mainly lake and river deposits with an upper Miocene through Pleistocene age. Knowledge of the geological framework is of great importance in evaluating the potential for fossil preservation in a certain area. To date, three major types of geological megastructures have yielded almost all fossil remains of early hominids: the East African Rift Valley (EARV), the intracratonic basin of Lake Chad, and the fossil-rich cave deposits in South Africa. Each of these regions provides a unique sedimentary setting bearing fossil-rich layers comprising a specific time-span within the last few million years.

Introduction The fossil record of humans is scanty, and discoveries are rare. It seems that the farther back in time we go, the fewer the fossil remains we can expect (Cooke 1983). There are probably several factors involved in diminishing the hard evidence of our own evolution. When a mammal dies in the open, scavengers will immediately work on the carcass, scatter its pieces, and probably destroy the bones (Shipman 1981). The surviving parts may be exposed to the hot sun during the daytime, and cooled down at night. Extreme temperature differences between day and night lead to cracking due to loss of water and reduction of organic material in the bone fibers. Usually, this process is accompanied by the activity of microorganisms, and may be also by physical transport in riverbeds or on floodplains during torrential rain falls. All of this modifies the original surface of bone, or even breaks elements apart. Most of the time, the history of an animal body ends in its complete destruction, unless the bones are covered and protected, e.g., by rapid burial with sediments (Cooke 1983). Sometimes animals are trapped in cavities, like fissures or pits, and their bones are preserved articulated. But even if we have a favorable environment for rapid covering, most of the time, postburial chemical and physical processes are destructive, with some rare exceptions favored by special geological environments.

*Email: [email protected] Page 1 of 16

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_11-3 # Springer-Verlag Berlin Heidelberg 2013

For this reason, the search for hominid fossils depends at a larger scale on the geological setting, because the sedimentary environment is a limiting factor upon chances of finding early hominids. Due to the multifarious influences for destruction, each fossil we collect seems to be a stroke of luck. In Africa, the hunt for the discovery of the origin of mankind concentrates on three major types of geological settings with a great potential for new discoveries. These are graben structures (e.g., Chorowicz 2005), cave deposits (e.g., Brain 1981), and intracratonic basins (e.g., Vignaud et al. 2002) that developed during the last 8 million years (Ma), after the hominids diverged from their last common ancestor with the African great apes. Consequently, the East African Great Rift Valley (EARV), with its widespread outcrops of fossil-rich Miocene to Pleistocene deposits, presents a unique situation for paleoanthropological field research. The Rift provided permanent water sources for our oldest ancestors and a rich fauna (WoldeGabriel et al. 2001; Pickford and Senut 2001). A very similar situation is found in intracratonic basins like the Chad depression, occurring as relatively static systems with large lake transgression and regression cycles, varying in time, and sometimes producing fossiliferous deposits of enormous lateral extension (Vignaud et al. 2002). In contrast, the famous South African cave sites, Makapansgat, Sterkfontein, Swartkrans, and Kromdraai, were formed by extensive freshwater karstification and sedimentation processes, and their complex cavities were used as shelters for hominids and probably functioned also as traps and scavenger caves (Brain 1981). Geological and paleoanthropological research at African hominid sites has produced a rich database during the last century (Bromage and Schrenk 1999). Today the geological background information influences the search for the origin of humankind, and the growing knowledge about geology helps us to understand the processes of fossilization and supports the interpretation of individual situations at fossil localities. And the application of digital geographical information systems (GIS), in combination with high-resolution satellite images, has provided a huge additional database for field investigations (e.g., Anemone et al. 2011). Potential fossil localities, in Rift valleys, intracratonic basins, and karstified limestone, can be localized by satellite image analysis. Nevertheless, extensive surveys by experienced field teams will continue to be the fundamental basis for the discovery of new fossil hominid remains (Fleagle and Gilbert 2008).

Geological Setting The geological setting at hominid localities is not only an important source of information about environmental settings and changes through time in specific localities or areas, but also an indicator of the probability of finding fossilized bones; and it is therefore an essential aspect influencing survey strategies. Moreover, it is an important aspect of the transfer of knowledge relevant to a broad understanding of human evolution as a Pan-African story (Schrenk et al. 2004). Sedimentary formations with a high potential for fossilization are the required geological setting. These consist of deposits that are products of weathering and transport, erosion, and deposition. Sediments are a mixture of different minerals and organic materials deposited on the earth’s surface, or in caves, in interaction with the atmosphere, hydrosphere, and biosphere. Common examples are clays, silts, sands, gravels, and breccias. Due to subsidence of some hundred meters, up to a few kilometers, deposits are typically transformed into sedimentary rock, like sandstone, claystone, or limestone. Accumulation areas of sediments are divided into marine and continental depositional space. Even if some of the fossil sites, like Saldanha or Klasies River Mouth in South Africa, are located closely to the ocean shoreline, the most important hominid fossil sites are located in continental Page 2 of 16

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_11-3 # Springer-Verlag Berlin Heidelberg 2013

deposits. Potential continental bone accumulation localities are fissures, caves, swamps, tar pits, river channels, flood plains, lagoons, and lakes. Such depositional areas can be described as geomorphological units characterized by climate, size, and shape of a sedimentary basin. Geometry and composition of sediments, and the relationship between units, provides information about the milieu of deposition (Reineck and Singh 1980). Physical, chemical, and biological parameters (Table 1) inform us about the depositional environment and climatic conditions. These parameters have to be recorded during fieldwork. The sum of all primary characteristics of a sedimentary unit defines the sedimentary facies (Reineck and Singh 1980). The analysis of the facies permits us to understand the sedimentary factors responsible for the appearance of the deposit and the fossils. Medium, current, wave intensity and velocity, as well as water depth, are relevant physical factors (Table 2); these are the important hydrodynamic conditions for the transport of animal remains. Mineral and groundwater composition, including climate, are understood to be the chemical factors of sedimentation and fossilization. Fortunately, sediments sometimes contain biological factors, faunal and floral remains, in different stages of preservation. The appearance of animal remains in a sedimentary matrix depends on its so-called taphonomic history (Shipman 1981). The taphonomy (Efremov 1940) includes two processes, biostratinomy and diagenesis, that describe the pathway from a carcass to a fossil. Biostratinomy (Weigelt 1927) deals with everything that happens to a carcass after an animal’s death, before the remains are buried. Afterward, the fossilization process, including mineral exchange and compaction, is called diagenesis. The fossilization process reduces information about an animal, but it also tells us a story that contains information about the paleoenvironment. The possibility that parts of a given animal will survive for some million years Table 1 Sedimentary parameters of depositional environments Physical Chemical Biological

Surface features (ripple marks, load casts, shrinking cracks, etc.) Depositional features (horizontal/cross bedding, grain size, etc.) Crystallization (carbonates, salts, etc.) Biogenetic remains (bones, teeth, shells, phytoliths, etc.) Bioturbation Excrements (coproliths, pellets, etc.) Organic remains (plants, bacteria, etc.) Bioerosion (gnawing marks, burrows, etc.) Biostratification (stromatoliths, etc.)

After Reineck and Singh (1980)

Table 2 Sedimentary factors of depositional environments Physical

Chemical

Biological

Medium Current Wave intensity Velocity Water depth Mineral composition Groundwater composition Climate Faunal remains Floral remains

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is relatively low due to taphonomic factors. Fossils are not randomly distributed. There are only a few spots on earth where we can find mammal remains, and there are even fewer places where we can discover hominid fossils. In most assemblages of large mammals from a single locality, the abundance of hominid specimens is less than 0.5 %. Nevertheless, the number of collected fossils has increased rapidly during the last decades. More and more research teams, with sophisticated survey strategies, explore for and investigate new fossil sites (Urbanek et al. 2005; Kullmer et al. 2008). Extensive sedimentologic and taphonomic analyses at known localities lead to a broad understanding of fossil site creation (Bobé et al. 2007). Commonly, the geographical distribution of hominid localities is used to interpret the origin of mankind and the migration patterns of early hominids (Coppens 1994). One has to consider, though, that the interpretation of the biogeography of a species, or even of an evolutionary lineage, can be heavily biased by the factors mentioned earlier, as well as by others such as burrowing and the preservation of animal remains (▶ Taphonomic and Diagenetic Processes). White (1988) pointed out that the fossil record in eastern Africa is biased toward a representation of the watered axial basins. Classic hinterland sites lacking permanent water sources, e.g., Laetoli, are rare indeed. But this does not imply that these were minor constituents; they may just have not been discovered yet. The preservation of fossils is heavily dependent on the sedimentological environment (e.g., WoldeGabriel et al. 2009). Fluviatile milieus do not necessarily grant permanent burial; many of the fossil localities in eastern Africa are associated with rivers, and a migrating channel bed can alter even a lake margin or a floodplain within a short time period. Chances of finding an original bone association decrease with the transport distance from the point of origin. When discovered, the bone assemblage is likely to represent different individuals from different localities and different time periods (Hanson 1980). Time averaging, the mixing of noncontemporaneous populations, has also to be considered when interpreting the history of bone assemblages. Nevertheless, beside sedimentological factors, the effects of time averaging are also dependent on stable or highly fluctuating populations (Behrensmeyer and Chapman 1993).

East African Rift Valley If we look at the geographical distribution of early hominid findings in Africa, we recognize that many of the famous sites are aligned in a chain along eastern Africa from Ethiopia via Kenya and Tanzania, to Malawi in the southeast. Localities like Hadar, Middle Awash, Omo, Lake Turkana, Olduvai, Laetoli, and others have yielded a great number of hominid specimens during the last 50 years (▶ The Species and Diversity of Australopiths; ▶ The Earliest Putative Homo Fossils; ▶ The Earliest Putative Hominids). These sites are positioned in a geological megastructure, the EARV (Fig. 1). The EARV extends about 6,400 km from northeast to southeast. The suture of the EARV follows a fault zone in the Continental crust. Plate tectonics explains the process of break-apart and rifting (Chorowicz 2005). The Nubian and Somalian plates diverge along the main rift axes and result in a great graben with an average width of 30–40 km. The flanks are uplifted, while subsidence forms the graben floor. Active east–west extension leads to an enlargement of the accumulation space. A sedimentary fault basin develops as soon as the subsidence is great enough that an initial drainage system grows along the main faults. Minor rivers and alluvial fans transport material into the basin from the rift shoulders. A complex erosion-sedimentation interaction system starts in the active rift zone. The expression “rift,” or “rift valley,” can be traced back to the definition of Gregory (Gregory 1896). Accordingly, a rift valley, like the Malawi Rift, is a parallel-sided down-faulted valley some Page 4 of 16

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Fig. 1 The geological megagraben of the EARV (gray area) with its famous hominid sites extends over more than 6,400 km from the Gulf of Aden and the Red Sea in the north into the Indian Ocean in the southeast, at the level of Madagascar. The main rift splits into eastern and western branches just north of Lake Victoria. A schematic transverse section (below) through the Rift Valley shows that the graben shoulders are composed of a stepped block-system separated by normal faults. The center is lowered due to crustal extension and divergence and uplift of the shoulders

tens of kilometers in width and at least a few hundred kilometers in length (Ring and Betzler 1995). Several smaller-scaled tectonic structures, like halfgrabens, horsts, warped blocks, major faults, transform faults, and pull-apart basins can occur within a rift system. All these geological structures provide space for accumulation, and for erosional processes to bury and unearth skeletal remains. In the history of a mature rift system, diverse environmental settings may be recorded, representing a wide range of habitats (▶ The Paleoclimatic recors and the Plio-Pleistocene Paleoenvironments). Rifting may end in a marine transgression phase and the birth of an ocean, when the continental breakup continues and rift floor subsidence extends toward the coast, as we can observe happening in the Red Sea and the Gulf of Aden. In other cases, the rifting dynamics may stop after some active phases. The EARV is probably one of the most attractive and interesting rift systems, reflecting several stages of rift development in its longitudinal extension. It therefore provides an important field of research for understanding crust breakup in a continental setting. Over the last 110 years, extensive research has been focused on the EARV (Gregory 1896; Wegener 1912; Krenkel 1922), making the East African rift system one of the best documented continental rift systems on Earth (Ring and Betzler 1995). Two areas have been of major interest: the Ethiopian Afar Triangle (Baker et al. 1972; Mohr 1987) in the Northeast at the horn of Africa, because of its special rifting situation as a triple junction of three crustal plates (Beyene and Abdelsalam 2005); and the Kenyan or Gregory Rift (Baker et al. 1972, 1988; King 1978; Crossley 1979; Strecker et al. 1990), as the eastern branch of the graben system.

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Extensive magmatism and volcanism has accompanied sedimentation in the graben. The oldest rifting phases are recognized in the northeastern part, at the western boundary of the Sinai Peninsula marking the boundary of the Arabian plate. The Red Sea and the Gulf of Aden are probably the oldest segments of the rift system, starting with its initial uplifts and doming of the crust, probably in the Oligocene. Initial volcanism is evident as early as the Eocene (e.g., Trap series), producing widespread lava (Beyene and Abdelsalam 2005). In the Miocene, thick flood basalts produced by large shield volcanoes filled the proto-rift in the Afar region. A highly active rifting phase followed in the Miocene, and produced accumulation space for extensive sedimentation of the erosional material from the rift shoulders and the rift volcanism. Sedimentation was always interrupted or accompanied by flood basalts and other volcanic eruptions, changing the landscape and sedimentation environments within the basins. There is no doubt that due to the spreading process, the EARV witnessed some habitat changes in eastern Africa. Faulting, uplifts, and subsidence support the development of all common fluvial processes, with meandering and braided rivers, flood plains, alluvial fans, oxbow lakes, and natural levees. Major rift lakes, like Lake Turkana, developed permanent water sources during long-term transgression phases. Regression/transgression cycles are evident through changes in sedimentary formations (Frostick et al. 1986).

Afar Depression The Afar Depression in Ethiopia (Fig. 2) is one of the world’s hotspots in two ways. The temperature can climb up to more than 45  C during daytime in the endless plains of the Afar, and fieldwork is a great challenge in the extreme African sun. Still, for paleoanthropologists and paleontologists who deal with the evolution of early humans, this investigation can be of the greatest interest since the area of about 150,000 km2 bears some of the richest hominid sites in the world. In that context, the Afar Depression contains fossils from the earliest time interval of humankind, 5–6 Ma, right up to the youngest (WoldeGabriel et al. 2001, 2009). Since the beginning of the 1970s, the Afar Triangle has been in the spotlight of international paleoanthropological field research. Numerous hominid findings, like the skeleton of the famous “Lucy,” come from here (Taieb et al. 1974) (▶ The Species and Diversity of Australopiths). Paleontological work in Ethiopia started in 1902, when the Frenchman Robert de Bourg de Bozas discovered fossil-rich deposits in the lower Omo Valley north of the Kenyan boundary (Fig. 2). Nevertheless, the first fossil hominid from Ethiopia, a lower jaw, was discovered only in 1933, in a cave close to Dire Dawa in the east. Likewise in 1933, the French paleontologist Camille Arambourg led an expedition to the fossiliferous sediments of the Omo River (Arambourg 1933). Although no hominid remains were discovered during the field trip, the team collected numerous animal fossils (Arambourg 1947). In 1967, an Ethiopian-American-French-Kenyan team under the direction of Clark Howell and Yves Coppens, and with the collaboration of Camille Arambourg, started the intensive search for hominid fossils in the Omo region (Arambourg et al. 1967; Arambourg and Coppens 1968a, b; Coppens et al. 1976). By 1973 they had recovered several hominid remains in the Usno, Mursi, and Shungura formations in the Omo River Basin. This initiated a “hominid-rush” in Ethiopia, which continues today. When the French geologist Maurice Taieb in 1970 announced the discovery of fossil-rich deposits at Hadar, further north in the Afar depression, the search for hominid remains shifted into the Afar region (Taieb et al. 1972, 1974). It was at Hadar that Donald Johanson and his team found the most complete A. afarensis skeleton in 1973 (Johanson et al. 1978). Inspired by a Beatles song, they named it “Lucy” (Johanson and Edey 1981). From 1975 to 1978, the American geologist Jon Kalb explored, with his colleagues of the “Addis Abeba Rift Valley Research Mission in Ethiopia” Page 6 of 16

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Fig. 2 The outlines of the Afar depression in the northeast of Ethiopia draw a triangle of about 150,000 km2. This huge basin contains fossiliferous sediments ranging in age from the Upper Miocene to recent times. The most famous hominid localities in the Afar triangle are at Hadar and in the Middle Awash. The Omo Valley is located far south in the main rift, where the Omo river crosses the border into Kenya. The fossil-rich area of Koobi Fora belongs to the Lake Turkana localities in Kenya, where thick sediment deposits surround the recent Lake. Olduvai and Laetoli are positioned within the eastern branch of the EARV, while the Chad Basin reflects an intracratonic depression about 2,500 km west of the Great Rift Valley with widespread deposits of the ancestral Lake Chad

(RVRME), the sediments in the “Middle Awash” region (Kalb et al. 1982a, b), where they documented one of the best known lithological sequences in the Afar Triangle containing fossil evidence of human evolution. The sediments cover a time-span of more than 6 Myr. Intercalated volcanic ash and lava horizons permit the absolute dating of sandwiched river and lake deposits, and thereby provide a unique insight into the evolutionary history of humankind. Since the early 1990s, Tim White and his “Middle Awash Research Project” have investigated these deposits successfully, collecting a large mammal assemblage including numerous hominid fossils such as the first remains of Ardipithecus ramidus (▶ The Earliest Putative Hominids) (White et al. 1994). Since the of 2000, the international PAR-Team (Paleoanthropological Research Team), under the direction of Horst Seidler, has investigated deposits further south of the “Middle Awash” in a fossil-rich area in the Somali region called Galili (Weber et al. 2001), about 100 km north of the Awash railway station and town, in the vicinity of the rift shoulder (Macchiarelli et al. 2004; Urbanek et al. 2005; Kullmer et al. 2008).

Central Rift Further South in the EARV, in the Turkana Basin of northern Kenya, Richard Leakey and his team started to explore the eastern shore of Lake Turkana from 1968 through the early 1970s (Leakey and Leakey 1978), while investigations in the Omo River Valley were continuing. They surveyed the areas in the vicinity of Koobi Fora (Fig. 2), a place where fossil bones were reported as early as 1940, and mentioned by the District Commissioner of Marsabit to Dr. L.S.B. Leakey, Richard Leakey’s

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father (Leakey 1978). The Koobi Fora Research Project collected fossils including many hominid remains from Plio-Pleistocene lake, river and flood plain silt, and sand deposits that are bordered by Miocene volcanic lava in the east and south, and by the recent Lake Turkana in the west. Extensive volcanic activity accompanied the rifting process along the major axis of the rift valley, forming depositional bodies with material from ash rains and lava flows. Those tuffs, basalts, and ignimbrites are important marker horizons, intercalated in the sediment successions. Radiometric dating allows the determination of their absolute age, and therefore also of the sandwiched fossilbearing sediments at many hominid sites, in a region running from north of Lake Turkana in the Omo Valley, along the eastern and western shoreline, and into the southwest at Kanapoi and Lothagam. The sediment succession tells a story of transgression and regression phases during the development of the great graben (Trauth et al 2005). Today, sediments of different age outcrop at the same level alongside them, due to small-scale tectonics producing uplift and subsidence of single blocks and leading to a patchwork of sedimentary deposits. To sort the sediments into a logical lithostratigraphic column at a particular fossil locality is one of the many challenges for sedimentologists reconstructing the sedimentary settings. It took many years to reconstruct the development of the sedimentary bodies deposited during the last 6 Myr at Lake Turkana. Further south in the EARV, the axis of the major graben seems to be nebulous. On a larger scale, the continental fracture in the earth’s crust splits in northern Tanzania into western and eastern branches, forming a large island structure between them that holds an intracratonic basin, a large depression with Lake Victoria at its center. The western branch of the EARV, with its northern deposits at Lake Albert in Uganda, has also produced a rich fauna, eroding from lake beds and river deposits from the Upper Miocene onward (Pickford et al. 1993). So far no hominid fossils have been discovered in these sediments, whereas in the southern part of the eastern branch, the fossil localities of the famous Olduvai Gorge in northern Tanzania have produced many hominid remains. In the vicinity of Olduvai, a remarkable magmatic province, with the Ngorongoro caldera, Lemagrut, Sadiman, and Oldeani volcanoes, produced immense amounts of ash during Plio-Pleistocene times, including the thick volcanics that mark the base of the Olduvai succession. The volcanic eruptions supported the creation of a fossil site that seems to be unique in the EARV. Most likely the oldest volcano, Sadiman (K-Ar age of 3.7 Ma), was the source of the volcanic sediments of the Laetoli region (Hay 1987). The distinctive geochemical composition is compatible with the Laetolil Beds, while Lemagrut and Ngorongoro produced lavas of a different petrology. The fossiliferous Laetolil Beds, close to the village Endulen, were discovered by some local Masai. Erosional processes unearthed several hominid remains, and in addition, a rich fauna was discovered. The first hominid remains at Laetoli were collected by a German explorer, KohlLarsen in 1939, 4 years after the first visit to Laetoli of Mary Leakey. She traveled again to Laetoli in 1959 (Leakey 1987), while she and her husband Louis were excavating in the sediments of the famous Olduvai Gorge in the North. Later in the 1970s, Mary Leakey discovered one of the most remarkable pieces of evidence for the upright gait of early hominids: a footprint trail in a volcanic ash deposit. The lowermost sediments, the Laetolil Beds, were deposited on an uplifted peneplain prior to movement along the Eyasi Fault (Hay 1987), a large fault creating the steep Lake Eyasi cliff. Some modern inselbergs give evidence of the uneven surface of the peneplain, where the sedimentary deposits in the valleys mark the paleodrainage and point to east–west as the major flowing direction. Obviously, the steep Eyasi fault did not exist when the water-laid deposits developed (Hay 1981), because today the river systems in the south flow more or less perpendicular to the Eyasi fault. The Laetolil Beds deposits are divided into dominantly water-laid tuffs in the south, with the addition of extensive aeolian tuffs in the north. In the upper sequence, some lava flows and clay

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deposits occur. In recent times, doming and resulting uplift led to erosion in the Laetoli region and to the exposure of the stratigraphic sequence of fossil-rich sediments (Ditchfield and Harrison 2011).

Chad Basin While today water erosion and fluviatile deposition during short and heavy rainy seasons is the most active land-forming process in the eastern African savanna, the Sahara desert is dominated by wind erosion and dune deposition. Brunet et al. (1995) reported the first Australopithecus remains far west of the EARV from the desert of central Africa, more than 30 years after Coppens (1961) announced the first hominid discovery in Chad. Since 1994, the Mission Paléoanthropologique FrancoTchadienne, led by Michel Brunet, has explored Miocene and Pliocene deposits in the Djurab Desert of northern Chad. The deposits are located in a large intracratonic basin, which includes modern Lake Chad in the southern sub-basin, and the Chad lowlands in the northern sub-basin (Vignaud et al. 2002). Fossiliferous sediments in the basin have been known since 1960, when Coppens reported Quaternary fossils from Koro Toro (Coppens 1960). Recent aeolian deflation in the northern sub-basin formed the Djurab Desert, with arid conditions, while the southern depression, under semiarid to wet conditions, reflects the latest lacustrine episode in the region. A “Mega Lake Chad” existed in Holocene times, but progressive desert extension of the Sahara toward the south reduced the water column of Lake Chad to its present shallow-water situation. An average water depth of 2–4 m can be measured today, and compares with a maximum depth of 180 m during ancient times. The basement of the Chad Basin is built of Precambrian rock, and forms a large depression which is filled with lacustrine, fluviatile, and lake sediments. The fluviatile facies is described by flooding channels, probably deposited during torrential rainfalls, because no mature river system, like meandering or braided channels, is reported (Vignaud et al. 2002). In the northern sub-basin, extensive aeolian sands contain well-sorted quartz grains, frequently formed since Upper Miocene times as dunes and shifting sands. The fossil content, including rich fish remains, crocodiles, and semiaquatic mammals like hippos, gives evidence of a permanent water source during the time when Sahelanthropus tchadensis (▶ The Earliest Putative Hominids), the oldest known hominid, lived probably in a gallery forest along the shoreline of Proto-Lake Chad. The so-called anthracotheriid unit of the Sahelanthropus site is interpreted to be a shallow perilacustrine environment, and consists of a well-sorted and well-cemented sandstone. It yielded all the terrestrial vertebrate remains (Vignaud et al. 2002). However, the desert already existed in the vicinity, and produced sedimentary material through aeolian deflation that gradually covered the lake floor and also animal carcasses. Along the flat margin of the ancient lakes, drainage systems developed during rainy seasons. Floods reworked the aeolian deposits surrounding the lake. Temporarily thin soil layers developed on floodplains, as confirmed by root casts developed in the major fossil layer at the Sahelanthropus locality Toros Menalla (Vignaud et al. 2002). The sedimentary situation in the Lake Chad Basin is controlled by transgression and regression phases of the lake and the Sahara desert (Schuster et al. 2006).

South African Caves In South Africa, the famous hominid sites of Sterkfontein, Swartkrans, Kromdraai, and Makapansgat (Fig. 3) are formed in a very specific geological setting that contrasts with the eastern Page 9 of 16

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Fig. 3 The caves at Makapansgat belong to a large Precambrian dolomite formation (above), showing profound karstification and sedimentation during Plio-Pleistocene times. Limestone cavities (below) are filled with travertine and characteristic carbonatic bone breccias. Mining for carbonates hollowed the filled cavities and brought thousands of fossils to light. The preservation of the fossils differs from sites in the EARV due to very different processes of site formation

African hominid localities. The fossil hominid-containing sediments accumulated in caves developed in Precambrian dolomite limestones, in Plio-Pleistocene times, through extensive karstification. The cave limestones belong to the Malmani Dolomite, which is part of the Transvaal Supergroup (Eriksson et al. 1976). The age of the Malmani dolostones, deposited in the intracratonic Transvaal Basin, is considered to be between 2.5 and 2.6 billion years (Button 1973). The thickness of the deposits reaches 1,450 m in the Sterkfontein area (Eriksson and Truswell 1974), and there is a large sedimentary hiatus from the Precambrian to the Late Tertiary. Abundant faulting and folding of the dolomite limestone makes determining the exact stratigraphic position of the basic cave material difficult. The occurrence of stromatoliths in the Makapan Valley led to the idea that at least some of the limestone sediments had been formed in the intertidal zone (Eriksson et al. 1976) near the shore line of the ancient sea. The initial cave development probably followed the fracture pattern in the dolomite rock, and extensive and deep karstification took place due to groundwater level changes. A typical feature of Page 10 of 16

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the Transvaal karst is the occurrence of a three-dimensional hyperphreatic maze of fissure passages (Martini et al. 2003), although large caverns did develop. As a result of erosion, cave ceilings collapsed and opened larger chambers. Carbonate solutions and mineralization built up thick travertine layers on the floors. The rich travertine deposits attracted miners at the end of the nineteenth century because of their pure calcium carbonate content. On the other hand, the carbonate is responsible for the consolidation of clastic sediments that filled up caverns through openings from the land surface. Sand, chert, dolomite, quartzite materials, and also bones were washed down into the caves. Winds probably brought fine grains, following the law of gravity. Possibly several transporting agents led to the high bone accumulation at some localities in the cave systems. Some of the caverns were completely filled up with exogenous material, and their sediments concreted to cave breccias with a fine-grained matrix and carbonate cement. Differences in color and grain size may indicate different modes and phases of sedimentation. Accessing the bones, which are enclosed in the breccias, demands sophisticated physical and chemical preparation techniques. Gravity and water transport, together with typical processes like collapses, solution, and remineralization, are responsible for the complex geological setting of many of the caves. The extensive lime works in the South African caves brought thousands of bone fragments to light, although blasting operations destroyed many natural features of the caves. Consequently, reconstruction of the diagenesis of the South African cave sites has been a real challenge, and many aspects still need further investigation. The analysis of the taphonomic history of bone accumulations at the South African cave sites needs detailed on-site observations, and also further lab work. Bob Brain and his team investigated many years at Swartkrans before he came up with his last model of cave development, in which he proposed nine diagenetic steps (Brain 1993). The formation started with a probably Miocene cavern below the level of standing water. After the opening of the cave, surface sediment began to accumulate inside the cave. The interpretation of the fossiliferous “pink breccia” of the Outer Cave, which was shown to be an infilled remnant, the Hanging Remnant Unit of Member 1, proved to be especially time-consuming. Swartkrans Members 1–3 yielded inter alia the remains of Australopithecus robustus, which is likely to have an age of 1.8–1 Ma. Members 4–5 are Middle Stone Age and ca. 11,000-year-old, respectively. Extensive investigations at Swartkrans and other South African cave sites have led to definitive models of the development of the deposits, and their fossil content in time and space. The experience and strategies used in the past provide the knowledge, which together with modern dating methods (Pickering et al. 2007) allow further exploration of development of fossil sites in the karstified limestones in South Africa.

Conclusions Although it seems to be clear that the chance of finding hominid fossils is limited by the factors mentioned earlier, there is no doubt that many fossils still await unearthing, either by erosion or by humans. The types of sediments and the geological contexts likely to yield hominid fossils are known. We just have to look for the right deposits. So far, early hominids have only been discovered in eastern and southern Africa, with the exception of the Chad Basin in central Africa. This is probably due to the auspicious geological setting and time represented in the EARV, rather than reflecting the paleobiogeographic distribution pattern of early hominids, although the occurrence of permanent freshwater sources, represented, e.g., by large rift lakes, probably attracted early

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hominids, because they were not capable of carrying a larger amount of water from one location to another. No doubt the hominid richness of the Rift sediments is unique altogether. There is still a high potential to recover more remains at long-known places, because erosion is always at work, and the immense deposits in the EARV are far from fully explored. Huge areas, for instance, in the Afar Triangle and in other places, have never been surveyed for fossils. New techniques, like satellite imagery with a resolution of a few meters on the ground, are of potential help for exploration work. Additionally, airborne survey can provide access to remote places such as the Danakil depression in the northern Afar. Nevertheless, extensive studies of satellite images will almost certainly discover new fossiliferous localities in smaller-scaled graben and basin structures at places in central, western, or southwestern Africa. It seems just a matter of time until the first early hominid is reported from the other side of the African continent.

References Anemone RL, Conroy GC, Emerson CW (2011) GIS and Paleoanthropology; Incorporating new approaches from the geospatial sciences in the analysis of primate and human evolution. Ybk Phys Anthrop 54:19–46 Arambourg C (1933) Découverte d'un gisement de mammifères Burdigaliens dans le bassin du lac Rudolphe (Afrique orientale). C R Somm Soc Géol France 14:221–222, Fasc Arambourg C (1947) Mission scientifique de l'Omo (1932–33), vol. 1, fasc. 3. Paléontologie, Mémoire, Museum national d'histoire naturelle, Paris, pp 231–562 Arambourg C, Coppens Y (1968a) Sur la decouverte dans le Pleistocene inferieur de la valle de l'Omo (Ethiopie) d'une mandibule d'Australopithecien. C R Acad Sci 265:589–590 Arambourg C, Coppens Y (1968b) Decouverte d'un Australopithecien nouveau dans les gisements de l'Omo (Ethiopia). S Afr J Sci 64:58–59 Arambourg C, Chavaillon J, Coppens Y (1967) Premiers résultats de la nouvelle mission de l'Omo (1967). C R Acad Sci (Paris), ser D 265:1891–1896 Baker BH, Mohr PA, Williams LA (1972) The geology of the eastern rift system of Africa. Geol Soc Am Spec Pap 136:1–66 Baker BH, Mitchell JG, Williams LA (1988) Stratigraphy, geochronology and volcanic-tectonic evolution of the Kedong-Naivasha-Kinangop region, Gregory rift valley, Kenya. J Geol Soc Lond 145:107–116 Behrensmeyer AK, Chapman RE (1993) Models and simulation of time-avaraging in terrestrial vertebrate accumulations. In: Kidwell SM, Behrenmeyer AK (eds) Taphonomic approaches to time resolution in fossil assemblages: the Paleontological Society short courses in paleontology, vol 6. Paleontological Society, University of Tennessee, Knoxville, pp 125–149 Beyene A, Abdelsalam MG (2005) Tectonics of the Afar Depression: a review and synthesis. J Afr Earth Sci 41:41–59 Bobé R, Alemseged Z, Behrensmeyer AK (eds) (2007) Hominin environments in the East African Pliocene: an assessment of the Faunal evidence. Springer, Dordrecht Brain CK (1981) The hunters or the hunted? An introduction to African Cave Taphonomy. University of Chicago Press, Chicago Brain CK (1993) Swartkrans: a cave’s chronicle of early men. Transvaal Museum Monograph, vol 8. Pretoria, Pretoria

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Bromage TG, Schrenk F (eds) (1999) African biogeography, climate change and human evolution. Oxford University Press, Oxford Brunet M, Beauvilain A, Coppens Y, Heintz E, Moutaye A, Pilbeam D (1995) The first Australopithecus 2500 km west of the Rift Valley (Chad). Nature 378:273–275 Button A (1973) The stratigraphic history of the Malmani Dolomite in the eastern and north eastern Transvaal. Trans Geol Soc S Afr 77:229–248 Chorowicz J (2005) The East African rift system. J Afr Earth Sci 43(2005):379–410 Cooke HBS (1983) Human evolution: the geological framework. Can J Anthropol 3(2):143–161 Coppens Y (1960) Le Quaternaire fossilifère de Koro-Toro (Tchad): Résultats d'une première mission. C R Acad Sci Paris, tome 251:2385–2386 Coppens YM (1961) Découverte d'un Australopithéciné dans le Villafranchien du Tchad. C R Acad Sci Paris 252:3851–3852 Coppens Y (1994) East side story: the origin of humankind. Sci Am 270(5):88–95 Coppens Y, Howell FC, Isaac GL, Leakey REF (1976) Earliest man and environment in the Lake Rudolf Basin-stratigraphy, paleoecology and evolution. In: Butzer KW, Freeman LG (eds) Prehistoric archeology and ecology. The University of Chicago Press, Chicago, p 615 Crossley R (1979) The Cenozoic stratigraphy and structure of the western part of the rift valley in southern Kenya. J Geol Soc Lond 136:393–405 Ditchfield P, Harrison T (2011) Sedimentology, lithostratigraphy and depositional history of the Laetoli area. In: Harrison T (ed) Paleontology and geology of Laetoli: Human evolution in context. volume 1: Geology, geochronology, paleoecology and paleoenvironment, vertebrate paleobiology and paleoanthropology. Springer, Dordrecht Efremov IA (1940) Taphonomy: a new branch in paleontology. Pan-Am Geol 74:81–93 Eriksson KA, Truswell JF (1974) Stratotypes from the Malmani Subgroup north-west of Johannesburg, South Africa. Trans Geol Soc S Afr 77:211–222 Eriksson KA, Truswell JF, Button A (1976) Palaeoenvironmental and geochemical models from an early proterozoic carbonate succession in South Africa. In: Walter MR (ed) Stromatolites. Dev Sed 20:635–643 Fleagle JG, Gilbert CC (2008) Modern human origins in Africa. Evolutionary Anthropology 17:1–2 Frostick LE, Renaut RW, Reid I, Tiercelin JJ (eds) (1986) Sedimentation in the African rifts. Geological Society Special Publication 25. Blackwell Scientific Publications, Oxford Gregory JW (1896) The Great Rift Valley. John Murray, London, p 424 Hanson CB (1980) Fluvial taphonomic processes: models and experiments. In: Behrensmeyer AK, Hill AP (eds) Fossils in the making. University of Chicago Press, Chicago, pp 157–181 Hay RL (1987) Geology of the Laetoli area. In: Leakey MD, Harris JM (eds) Laetoli, a Pliocene site in Northern Tanzania. Clarendon, Oxford, pp 23–47 Hay RL (1981) Paleoenvironment of the Laetolil Beds, northern Tanzania. In: Rapp GR, Vondra CF (eds) Hominid Sites: Their Geologic Settings, pp 7–24 Johanson DC, Edey MA (1981) Lucy: The beginning of humankind. Simon and Schuster, New York. Lucy, Deutsche Ausgabe. Die Anfänge der Menschheit. Piper-Verlag, M€ unchen Z€ urich, 1984. 492 S Johanson DC, White TD, Coppens Y (1978) A new species of the genus Australopithecus (Primates: Hominidae) from the Pliocene of eastern Africa. Kirtlandia 28:1–14 Kalb JE, Oswald EB, Tebedge S, Mebrate A, Tola E, Peak D (1982a) Geology and stratigraphy of Neogene deposits, Middle Awash Valley, Ethiopia. Nature 298:17–25

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Kalb JE, Jolly CJ, Mebrate A, Tebedge S, Smart C, Oswald EB, Cramer D, Whitehead P, Wood CB, Conroy GC, Adefris T, Sperling L, Kana B (1982b) Fossil mammals and artefacts from the Middle Awash Valley, Ethiopia. Nature 298:25–29 King BC (1978) Structural and volcanic evolution of the Gregory rift valley. In: Bishop WW (ed) Geological background of fossil man. Scottish Academic Press, Edinburgh, pp 29–54 Krenkel E (1922) Die Bruchzonen Ostafrikas. Gebr. Borntraeger, Berlin, p 184 Kullmer O, Sandrock O, Viola TB, Hujer W, Said H, Seidler H (2008) Suids, Elephantoids and Paleoecology of the Pliocene Galili hominid site, Somali Region, Ethiopia. Palaios 23:452–464 Leakey REF (1978) Introduction. In: Leakey MG, Leakey REF (eds) Koobi for a research project, the fossil hominids and an introduction to their context, 1968–1974, vol I. Clarendon, Oxford, pp 1–13 Leakey MD (1987) Introduction. In: Leakey MD, Harris JM (eds) Laetoli, a Pliocene site in Northern Tanzania. Clarendon, Oxford, pp 1–22 Leakey MG, Leakey REF (1978) Koobi fora research project, vol I. The fossil hominids and an introduction to their context, 1968–1974. Clarendon, Oxford, p 191 Macchiarelli R, Bondioli L, Falk D, Faupl P, Illerhaus B, Kullmer O, Richter W, Said H, Sandrock O, Schäfer K, Urbanek C, Viola TB, Weber GW, Seidler H (2004) Early Pliocene hominid tooth from Galili, Somali Region, Ethiopia. Coll Anthropol 28(2):65–76 Martini JEJ, Wipplinger PE, Moen HFG, Keyser A (2003) Contribution to the speleology of the Sterkfontein Cave, Gauteng Province, South Africa. Int J Speol 32(1/4):43–69 Mohr PA (1987) Pattern of faulting in the Ethiopian rift valley. Tectonophysics 143:169–179 Pickering R, Hancox PJ, Lee-Thorp JA, Gr€ un R, Mortimer GE, McCulloch M, Berger LR (2007) Stratigraphy, U-Th chronology, and paleoenvironments at Gladysvale Cave: insights into the climatic control of South African hominin-bearing cave deposits. J Hum Evol 53(5):602–619 Pickford M, Senut B (2001) The geological and faunal context of Late Miocene hominid remains from Lukeino, Kenya. C R Acad Sci, Science de la Terre et des Planètes 332:145–152 Pickford M, Senut B, Hadoto D (1993) Geology and palaeobiology of the Albertine Rift Valley Uganda-Zaire. vol I: Geology-CIFEG Publ Occas 24:1–190 Reineck HE, Singh IB (1980) Depositional sedimentary environments, with reference to Terrigenous Clastics. Springer Verlag, Berlin, p 549 Ring U, Betzler C (1995) Geology of the Malawi Rift: Kinematic and tectonosedimentary background to the Chiwondo Beds, northern Malawi. J Hum Evol 28:7–21 Schrenk F, Sandrock O, Kullmer O (2004) An “Open Source” perspective of earliest Hominid origins. Coll Anthropol 28(2):113–119 Schuster M, Duringer P, Ghienne J-F, Vignaud P, Mackaye HT, Likius A, Brunet M (2006) The age of the Sahara Desert. Science 311:821 Shipman P (1981) Life history of a fossil. An introduction to Taphonomy and Paleoecology. Harvard University Press, Cambridge, pp 1–222 Strecker MR, Blisniuk PM, Eisbacher GH (1990) Rotation of extension direction in the central Kenya rift. Geology 18:299–302 Taieb M, Coppens Y, Johanson DC, Kalb J (1972) Dépôts sédimentaires et faunes du Plio-pléistocène de la basse vallée de l'Awash (Afar central, éthiopie). C R Acad Sci Paris 275:819–822, série D Taieb M, Johanson DC, Coppens Y, Bonnefille R, Kalb J (1974) Découverte d'Hominidés dans les séries plio-pléistocènes d'Hadar (Bassin de l'Awash; Afar, éthiopie). C R Acad Sci Paris 279:735–738x, série D Page 14 of 16

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Trauth MH, Maslin MA, Deino A, Strecker MR (2005) Late Cenozoic moisture history of East Africa. Science 309:2051–2053 Urbanek C, Faupl P, Hujer W, Ntaflos T, Richter W, Weber G, Schaefer K, Viola B, Gunz P, Neubauer S, Stadlmayr A, Kullmer O, Sandrock O, Nagel D, Conroy G, Falk D, Woldearegay K, Said H, Assefa G, Seidler H (2005) Geology, paleontology and paleoantropology of the Mount Galili formation in the Southern Afar Depression, Ethiopia – Preliminary results. Joannea Geologie und Paläontologie 6:29–43 Vignaud P, Duringer P, Mackaye HT, Likius A, Blondel C, Boisserie JR, de Bonis L, Eisenmann V, Etienne ME, Geraads D, Guy F, Lehmann T, Lihoreau F, Lopez-Martinez N, Mourer-Chauvire C, Otero O, Rage JC, Schuster M, Viriot L, Zazzo A, Brunet M (2002) Geology and palaeontology of the Upper Miocene Toros-Menalla hominid locality, Chad. Nature 418:152–155 Weber GW, Seidler H, Macchiarelli R, Bondioli L, Faupl P, Richter W, Kullmer O, Sandrock O, Falk D (2001) New discovery of Australopithecus in the Somali region of Ethiopia. Am J Phys Anthropol Suppl 32:162 Wegener A (1912) Die Entstehung der Kontinente. Geologische Rundschau 3:276–292 Weigelt J (1927) Rezente Wirbeltierleichen und ihre paläobiologische Bedeutung. Max von Weg Verlag, Leipzig White TD (1988) The comparative biology of ‘robust’ Australopithecus: Clues from the context. In: Grine FE (ed) Evolutionary history of the “Robust” Australopithecines. Aldine de Gruyter, New York, pp S449–S483 White TD, Suwa G, Asfaw B (1994) Australopithecus ramidus: a new species of early hominid from Aramis, Ethiopia. Nature 371:306–312 WoldeGabriel G, Haile-Selassie Y, Renne PR, Hart WK, Ambrose SH, Asfaw B, Heiken G, White TD (2001) Geology and palaeontology of the late Miocene Middle Awash Valley, Afar rift Ethiopia. Nature 412:175–178 WoldeGabriel G, Ambrose SH, Barboni D, Bonnefille R, Bremond L, Currie B, DeGusta D, Hart WK, Murray AM, Renne PR, Jolly-Saad MC, Stewart KM, White TD (2009) The geological, isotopic, botanical, invertebrate, and lower vertebrate surroundings of Ardipithecus ramidus. Science 326:65e1–65e5

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_11-3 # Springer-Verlag Berlin Heidelberg 2013

Index Terms: Afar depression 6 Biostratinomy 3 Breccia 10–11 Caves 9 Central rift 7 Chad Basin 9 Continental deposits 3 Diagenesis 3 East African Rift Valley (EARV) 4 Facies 3 Fluviatile 4, 9 Geology 2, 4, 6–7, 9 Afar Depression 6 central rift 7 Chad Basin 9 EARV 4 sedimentation 2 South African caves 9 Graben 4, 6, 8 Intracratonic basin 2, 8–9 Intracratonic basins 2 Karstification 10 Lacustrine 9 Rift Valley 4 Sediments 2–3 Taphonomic factors 4 Taphonomy 3

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_13-5 # Springer-Verlag Berlin Heidelberg 2013

Paleosols Gregory Retallack* Department of Geological Sciences, University of Oregon, Eugene, OR, USA

Abstract Soils are known to be products of environmental factors such as climate, vegetation, topographic setting, parent material, and time for formation, so that paleosols, or fossil soils, can potentially reveal changing environments of the past. Evidence from paleosols for past climate and vegetation in East Africa does not support traditional narratives of human evolution during a single transition from primeval forest to dry climate and open grassland. Instead, paleosols indicate climatic oscillations between wet and dry, and alternating expansion of woodland and grassland, since at least 18 Ma (million years ago). Acquisition of dry grassland adaptations such as thick enamel by 18 Ma, adducted hallux by 14 Ma, and cursorial legs by 1.8 Ma, alternated with woodland adaptations such as short stiff back by 16 Ma, erect stance by 6 Ma, and flat face by 3.5 Ma. Our ancestors survived profoundly changing climate and vegetation, with some adaptations lasting only to the next environmental shift, but others proving to be of lasting value.

Introduction Our species, and its ancestors of millions of years ago, evolved on the soils of Africa (Darwin 1872; Fleagle 1998). Many of those soils have been eroded or altered beyond recognition by deep burial, but many paleosols are buried within floodplain, volcanic, lacustrine, alluvial plain, and cave deposits of Africa (Retallack 2001a). These paleosols provide much of the colorful banding and mottling seen in East African badlands and dongas, including many fossil hominoid localities (Fig. 1). Many fossils of human ancestors come from paleosols (Retallack et al. 1995, 2002; Radosevich et al. 1992; Wynn 2004a, b), which are also records of past environments of our evolutionary antecedents (Fig. 1). Modern soils are known to be products of environmental factors such as climate, vegetation, parent materials, topographic setting, and time for formation (Jenny 1941). These formative factors can be interpreted from fossiliferous paleosols to provide hitherto unavailable details of the habitats of fossil apes and humans. The vegetation of fossil ape and human sites is central to long-standing theories of the evolution of upright stance. “The hands and arms could hardly have become perfect enough to have manufactured weapons, or to have hurled stones and spears with a true aim, ‘. . . so long as they were especially fitted to climbing trees’” (Darwin 1872). Other ideas are that grasslands selected for upright stance because of the need to be vigilant against predators (Dart 1926), to manipulate

*Email: [email protected] *Email: [email protected] Page 1 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_13-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 1 Localities for paleosol studies in East Africa

small seeds (Jolly 1970), to minimize exposure to the sun (Wheeler 1984), or to cover long distances with less energy by walking (Rodman and McHenry 1980) or running (Bramble and Lieberman 2004). Wooded grasslands and open woodlands are also plausible sites for evolution of upright stance from squat feeding on the ground (Kingdon 2003) or moving between scattered fruiting bushes (Sanford 2003). Alternatively, upright stance may have evolved in forests because it allowed erect-back climbing (Tuttle 1981), hands free to care for premature infants (Lovejoy 1981), phallic display to females (Tanner 1981), or intimidation displays to rivals (Jablonski and Chaplin 1993). Paleosols are relevant to these questions, because the fine root traces and crumb structure of grassland soils are distinct from the thick clayey subsurface horizons of both woodland and forest soils (Jenny 1941). Woodland and forest soils differ markedly in their clay minerals and chemical composition (Retallack 1997). Even the aquatic theory of human origins (Morgan 1982) can be evaluated from paleosols because mangal, littoral, lake margin, and streamside paleosols are distinguished by virtue of relict bedding and common burrows of crabs and clams (Retallack 2001a). Page 2 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_13-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 2 Kenyan Miocene paleosols have been given field names using local Luo and Turkana languages. These pedotypes are objective field mapping units for paleosols: their interpretation and classification requires laboratory study

Paleoclimate also is of interest as a selective pressure on hominoid evolution through drought and other hardships. Paleoclimate was also a primary control of past vegetation in which hominoids found food and shelter. Paleoclimatic shifts to drier climate and more open grassy vegetation have been held responsible for major evolutionary innovations in hominoids and bovids (Vrba 1999), as Page 3 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_13-5 # Springer-Verlag Berlin Heidelberg 2013

have changes in degree of climatic variability (Potts 1996). Soils of dry climate have calcareous nodules at a shallower depth than soils of humid climate (Retallack 2005) and also are less leached of cationic nutrients (Ca2+, Mg2+, K+, Na+) than humid-climate soils (Sheldon et al. 2002). Paleosols can thus provide paleoclimatic records at the very sites of early human ancestors, rather than inferred from remote records of deep-sea cores (de Menocal 2004). This review emphasizes climate and vegetation, but other soil-forming factors of parent material, topographic position, and duration of soil formation can also be inferred from paleosols. Highly calcareous and saline carbonatite volcanics are an unusual parent material of many African hominid sites (Retallack 1991a), fortunate because of their remarkable preservative effects for fossil bones, seeds, and insects (Retallack et al. 1995). Many East African paleosols preserve a record of well-drained fluvial terraces, infrequently flooded, and some volcanic apron paleosols represent foothills environments (Retallack 1991a), thus revealing environments beyond the usual lowland constraints of sedimentary environments. Degree of soil development can also be used to infer duration of paleosol formation and rates of sediment accumulation, with implications for the geochronology of ape and human ancestor sites (Retallack et al. 1995, 2002).

Recognition of Paleosols Paleosols are often distinctive and striking bands of red clay (Bt horizon), calcareous nodules (Bk horizon), or coal (O horizon) in sedimentary and volcanic sequences (Fig. 2). Three general classes of observations are especially helpful in paleosol recognition: root traces, soil horizons, and soil texture (Retallack 1997). Root traces are the most diagnostic evidence of paleosols, and fossil roots may be made more obvious by erosion-resistant cementation (Kabisa pedotype of Fig. 2). Difficulties arise in recognition of root traces, because they are often replaced by other minerals and ramify in three dimensions in such a way that one rock face reveals little of the overall pattern. Few fossil roots are carbonaceous or reveal histological structures like permineralized fossil wood (Retallack 1997). The original root has commonly rotted out, and the hole it occupied is filled with claystone or siltstone, or encrusted with iron oxide or calcium carbonate. Drab haloed root traces are very distinct, green gray mottles, in reddish paleosol matrix, formed during early burial chemical reduction by microbes fueled by consumption of root organic matter (Retallack 1991b). In all these cases, root traces are truncated at the surface of the paleosol, and branch and taper downward. These features distinguish root traces from most kinds of burrows in soils, although the relationship between burrows and roots can be complex. Roots may preferentially follow soft fill of burrows rather than hard soil matrix, and burrows may congregate around roots on which the burrowing animals fed (Retallack 1991a). Soil horizons develop through thousands of years, whereas sedimentary beds are deposited in days. Unlike sedimentary beds, which have sharp bottoms and usually sharp tops as well, paleosols have a sharp top, representing the ancient land surface, but gradational lower contacts (Retallack 2001a). Sedimentary beds also include a variety of sedimentary structures, such as lamination, cross bedding, and ripple marks (as in Tek pedotype of Fig. 2), whereas soil horizons develop with obliteration of these original features (Tut pedotype of Fig. 2). Similarly, soil formation progressively destroys the original crystalline structure of volcanic or granitic parent materials (Retallack 1991a). In dry climate soils (Aridisols), primary sedimentary or volcanic structures are obscured at first by filaments and soft, small carbonate masses, then large, hard, carbonate nodules (calcic or Bk horizon of Chogo pedotype in Fig. 2), and finally thick carbonate layers (petrocalcic or K horizon of Page 4 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_13-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 3 Petrographic and chemical data for the Tek paleosol from the 18 Ma Hiwegi Formation of Rusinga Island, Kenya [Data from Retallack et al (1995)]

Soil Survey Staff 2000). In sod-grassland soils (Mollisols), primary lamination and crystalline structure is broken up by fine roots and replaced by dark, fecal pellets of earthworms to create a crumb-textured, organic surface horizon (mollic epipedon of Dite, Chogo, Yom, and Onuria pedotypes of Fig. 2). A variety of other kinds of soil horizons are recognized and important to soil classification (Retallack 1997, 2001a; Soil Survey Staff 2000). Soil structure also develops within soil horizons, and is very distinct from sedimentary bedding and igneous crystalline texture. The fundamental elements of soil structure are modified cracks and other surfaces (cutans), and the clods they define (peds). Cutans include clay skins (argillans) lining cracks in the soil and rusty weathering rinds (sesquans) around clods and pebbles in soil (Retallack 2001a). Peds have a variety of shapes: lenticular in swelling-clay soils (Vertisols: Aberegaiya pedotype of Fig. 2), blocky subangular in fertile forest soils (Alfisols: Tut pedotype of Fig. 2), and crumb shaped (small and ellipsoidal) in grassland soils (Mollisols: Dite, Chogo, Yom, and Onuria pedotypes of Fig. 2). Although cracks and other voids are not preserved in paleosols due to compaction by overburden, peds and cutans are common and conspicuous (Retallack 1991a). Other soil structures less diagnostic of soils include concretions, nodules, and crystals (Retallack 2001a).

Methods for the Study of Paleosols Just as soil individuals (pedons) are studied as soil columns in soil pits, paleosols are studied in columnar stratigraphic sections of the sort also used in sedimentology and stratigraphy (Fig. 3). Grain size is emphasized, because it is important to soil formation, as weathering transforms sand and silt grains to clay. A graphical representation of grain size profiles conveys important information on the abruptness of horizon transitions. Color from a Munsell chart should also be represented, as redness denotes the degree of chemical oxidation and drainage of soils and

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_13-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 4 Reconstruction of the Tek paleosol from the 18 Ma Hiwegi Formation of Rusinga Island, Kenya [Data from Retallack et al (1995)]

paleosols. Calcareousness determined by relative effervescence with dilute hydrochloric acid also is important as a guide to chemical leaching and soil nutrient status (Retallack 1997). Laboratory studies of paleosols do not employ techniques identical to those used in soil science because some important soil measures, such as base saturation, are altered upon burial of soils (Retallack 1991b). Petrographic thin sections are especially useful for revealing soil microfabrics, and the point counting of thin sections furnishes estimates of changes in grain size and mineral composition of paleosols. For example, increased subsurface clayeyness can be used to recognize diagnostic horizons (argillic horizon) for forest soils (Alfisols and Ultisols), whereas traces of nutrient-rich minerals, such as calcite and feldspar, distinguish fertile forest soils (Alfisols) from infertile forest soils (Ultisols: Retallack 1997). Chemical analyses also are useful in characterizing and classifying paleosols, especially molar ratios designed to gage the progress of common soil-forming chemical reactions. The hydrolysis reaction common in silicate weathering leaches cationic bases (Ca2+, Mg2+, K+, Na+) from host minerals, such as feldspar, to create clay (Al rich) and is thus indicated by high ratios of alumina/

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_13-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 5 Carbon isotopic (d13Corg) depth profiles of Kenyan Miocene pedotypes, showing strong surface humification in grassland paleosols (Chogo and Onuria pedotypes), subsurface humification in Alfisols (Tut), and mixing in vertic Inceptisols (Chido). Carbon isotopic data is from Bestland and Krull (1999) and Cerling et al. (1997a), and paleosols are described by Retallack (1991a), Retallack et al. (1995), and Bestland and Krull (1999)

bases. An alumina/base ratio higher than 2 is a good proxy for the transition from fertile forest soils (Alfisols) to infertile forest soils (Ultisols). Soda/potash molar ratios in excess of 1 indicate unusually salty soils. Ferrous/ferric molar ratios in excess of 1 indicate well-drained soils (Retallack 1997). By these criteria, the petrographic and chemical data on the 18 Ma Tek paleosol from Rusinga Island Kenya (Fig. 3) indicate a fertile Inceptisol that was nonsaline and welldrained. These data allow identification of analogous modern soils (Retallack et al. 1995) and refine understanding of the ancient landscape and its ecosystem (Fig. 4). Carbon isotopic compositions of paleosol carbonate were at first thought to be useful indicators of grasslands, because most tropical grasses have a C4 photosynthetic pathway which creates isotopically heavy carbon (Cerling 1992). The most prominent failure of this technique was in its application to the Middle Miocene (13.7 Ma) locality of Fort Ternan (Pickford et al. 2006), with paleosol carbonate isotopically like rain forest (Cerling et al. 1997a), but fossil soils, grasses, trees, and antelope like those of a mosaic of wooded grassland and grassy woodland (Retallack 1991a, 1992; Koch 1998; Turner and Anto´n 2004). Subsequently, it was found that even tropical grasses used the C3 photosynthetic pathway until about 7 Ma or younger (Cerling et al. 1997b; Fox and Koch 2003). The quality of graze (C3 more nutritious than C4) can be assessed by isotopic studies of teeth and paleosols, but the question of grass or shrub diet is better assessed from mammalian tooth microwear, hypsodonty, and cursoriality (MacFadden 2000). The advent of C4 grasses within tropical grasslands is most likely related to declining Late Miocene atmospheric CO2 content (Cerling et al. 1997a). Another failure of carbon isotopes to indicate past vegetation is Sike’s (1994) forest interpretation of the paleosol at Olduvai fossil locality FLK yielding Australopithecus boisei. This paleosol, with relict bedding, zeolites, little clay, and shallow carbonate, is unlike forest soils, and probably supported salt-tolerant, lake-margin shrubs (Retallack 2001a), which have a similar C3 isotopic value to forest (Sikes 1994). Isotopic values of carbon and oxygen in paleosols and animals are controlled by so many factors that biotic and pedogenic constraints are needed (Koch 1998). Carbon isotopic studies of paleosols are now more useful for assessing atmospheric CO2 from carbonate and organic isotopic offsets (Ekart et al. 1999) and soil

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_13-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 6 A 20 million year record of vegetation (a) and paleoprecipitation (b) from Kenya, compared with carbon (c) and oxygen (d) isotopic composition of marine foraminifera. Paleoprecipitation data from paleosols (b) is from depth to carbonate (open circles), clay minerals (diamonds), and chemical composition (squares) after Retallack (1991a), Retallack et al. (1995, 2002), Wynn (2001, 2004a, b), and Wynn and Retallack (2002). Paleobotanical estimates from Jacobs (2002) and Jacobs and Deino (1996). Modern vegetation precipitation limits are from Anhuf et al. (1999)

productivity from isotopic depth functions (Yapp and Poths 1994). Carbon isotopic depth profiles of paleosols also provide new insights into carbon cycling within different kinds of ancient ecosystems. Grassland paleosols (Chogo and Onuria pedotype of Fig. 5) show more effective humification at the surface (higher d13C values) than woodland soils (Tut of Fig .5), and swellingclay paleosols have flat carbon isotopic profiles due to soil mixing (Chido of Fig .5). Preservation of such carbon-cycling signatures known from modern soils within different pedotypes gives additional evidence for paleosol classification and interpretation (Bestland and Krull 1999).

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_13-5 # Springer-Verlag Berlin Heidelberg 2013

Paleosols as Proxies of Paleoprecipitation Climatic zonation of soils was a key element in the Russian origins of soil science (Jenny 1941), and a variety of relationships between particular soil features and climatic variables can be applied to East African paleosols in order to reconstruct paleoclimate. For example, depth to carbonate horizon (D in cm) is related to mean annual precipitation (P in mm) by a formula from Retallack (2005). This depth can be corrected for compaction due to overlying sediment using geological estimates of overburden and standard formulae (Sheldon and Retallack 2001). Also related to mean annual precipitation (P) is nutrient base content (C ¼ Al2O3/(Al2O3 + CaO + MgO + Na2O) in mol) of soil Bt horizons by a formula from Sheldon et al. (2002). Chemical weathering also alters the mineral content of soils, especially their clay minerals, which begin as smectites and then lose cationic bases with further chemical weathering to become kaolinite (Retallack 2001). This indication of paleoprecipitation works best with noncalcareous soils, which are found in climates receiving more than 1,000-mm mean annual precipitation (Retallack 2005). In East Africa today, smectite is dominant in soils receiving less than 1,200-mm mean annual precipitation, and kaolinite dominant in wetter climates (Mizota et al. 1988). Thus, noncalcareous, smectitic soils define a limited paleoclimatic window of 1,000–1,200-mm mean annual precipitation. A new compilation of Kenyan paleoprecipitation over the past 20 million years (Fig. 6b) includes previously published data on African depth to Bk (Wynn 2001, 2004a,b; Wynn and Retallack 2002; Retallack 2001b; Retallack et al. 2002), and paleosol chemical (Retallack et al. 1995, 2002; Bestland 1990; Retallack 1991a; Wynn and Retallack 2002) and clay mineral composition (Retallack 1991a; Behrensmeyer et al. 2002), as well as published inferences from size and shape of fossil leaves (Jacobs 2002). This compilation is limited to data from around Lake Victoria for the early-middle Miocene, the Tugen Hills for the mid-late Miocene, and the Turkana Basin for the Miocene to Quaternary. The geological time scale is from radiometric dating of these various fossil primate sites (Deino et al. 1990; Retallack 1991a; Jacobs and Deino 1996; Behrensmeyer et al. 2002; Hill et al. 2002; Pickford et al. 2006). These new data reveal not just one Neogene aridification event at about 7 Ma, as has long been implied by the “Tertiary pluvial hypothesis” (Leakey 1952), the “Miocene lake hypothesis” (Kent 1944), the “Miocene rain forest hypothesis” (Andrews and Van Couvering 1975; Andrews 1996), and the “Late Miocene grassland hypothesis” (Cerling 1992; Cerling et al. 1997a,b). These theories had already been discredited by discovery of earlier Miocene desert dunes, shrubland snails, alkaline lakes, open-country grasses, grazing mammals, and grassland paleosols in East Africa (Pickford 1986a, 2002a; Retallack et al. 1990, 2002). Instead the data (Fig. 6) reveal a Neogene paleoclimatic roller coaster of at least nine dry spells with intervening wet periods, of which humidity spikes at 16 and 13 Ma were the wettest of the last 20 million years. This new paleoprecipitation curve is similar to paleotemperature variations for Africa inferred from north-south oscillation through time of Ethiopian and Palearctic biogeographic realms (Pickford 2002a) and from paleoclimatic transfer functions from East African mammal assemblages (Retallack 2012). These new data are also similar to foraminiferal oxygen isotope curves from the deep sea (Zachos et al. 2001), commonly used as a basis for evaluating human evolution in Africa (de Menocal 2004), but the match is not precise (Fig. 6b,c). A general trend of extreme and volatile middle Miocene values, but subdued late Miocene to Quaternary values, is evident from both isotopic and paleosol data. The paleosol record reveals much greater variation in rainfall than would be inferred from carbon isotopic values of marine foraminifera, which are damped by global oceanic mixing with time lags of several thousand years. More Page 9 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_13-5 # Springer-Verlag Berlin Heidelberg 2013

Table 1 Geological age of African climatic events, selected adaptations, and hominoid diversity (D), origination (O), and extinction (E) Age (Ma) 20.2 dry 19.1 wet 17.7 dry 16.1 very wet 14.9 very dry 12.6 very wet 10.7 dry 8.6 wet 7.5 very dry 6.8 wet 5.4 dry 4.2 wet 2.5 dry 2.1 wet 1.8 dry 1.7 wet 1.0 dry 0.1 wet

Hominoid adaptations and extinctions Robust mandible for hard food (Rangwapithecus) Low cusp molars for folivory (Nyanzapithecus) Thick enamel for hard food (Afropithecus) Short back for suspension (Proconsul (“Morotopithecus”)) Adducted hallux for ground walking (Equatorius) Thin enamel molars for soft food (Otavipithecus) Large size for ground feeding (Samburupithecus) Ape extinction with monkey radiation (Microcolobus) Knuckle walking for ground (Pan-Gorilla ancestors) Upright stance for nest provisioning (Orrorin) Small incisiform canines for hard food (Ardipithecus) Flat face for stereoscopic vision (Kenyanthropus) Large molars for hard food (Paranthropus) Small molars for soft food (Homo habilis) Long legs for endurance running (Homo ergaster) Occipital bun for competition (Homo erectus) Globular brain for generalist roles (Homo antecessor) Magdalenian tools and culture (Homo sapiens)

D 10 5 6 4 7 2 3 1 1 1 3 1 6 3 5 4 4 1

O 9 0 1 3 4 2 3 1 1 1 1 1 4 0 3 0 2 1

E 0 5 2 6 2 5 0 3 1 1 2 3 2 4 2 3 1 4

profound damping is seen in oxygen isotopic values of marine foraminifera, which show a longterm increase unlike local rainfall and foraminiferal carbon records. This increase is plotted on reversed axes in Fig. 6d, because it has been interpreted as a long-term temperature decline (Zachos et al. 2001), but part of this long-term trend is due not just to temperature but to water recycling with plate tectonics (Veizer et al. 2001). The global oxygen isotope record also shows an increase after 3 Ma due to continental icecap sequestration of isotopically light oxygen, in addition to temperature effects (Zachos et al. 2001). Despite these problems, the East African paleosol record and global isotopic records present a very different concept of climatic variation experienced by our distant ancestors than the past idea of a seminal Late Miocene climatic event. Instead of a single origin of humanity at a turning point of environmental change, the new record implies rather that our lineage responded to a gauntlet of changing conditions with a variety of adaptations (Table 1), as discussed later.

Paleosols as Trace Fossils of Ecosystems Australopithecus afarensis is known from body fossils, such as the partial skeleton “Lucy” (Johanson et al. 1982), as well as from trace fossils, such as the footprints of Laetoli (Leakey and Harris 1987). The soils of A. afarensis also are known, especially at the “first family” site near Hadar, Ethiopia (Radosevich et al. 1992; Behrensmeyer 2008). Here a troop of at least 13 individuals, young and old, died, rotted, and were partially disarticulated, before being interred in flood deposits on a crumb-structured soil of grassy streamside woodland (Fig. 7). The paleosol is not only a matrix to the bones but a trace fossil of their ecosystem. Furthermore, paleosols by definition are in the very place they formed, not redeposited. Unlike the skeleton of “Lucy,” found Page 10 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_13-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 7 Reconstruction of paleosols at the “First Family site” for Australopithecus afarensis at Hadar [Data from Radosevich et al. (1992)]

in the sandstone of a former river channel (Johanson et al. 1982), and thus transported some distance from its natural habitat, the first family was found where it died and had lived (Radosevich et al. 1992; Behrensmeyer 2008). Thus, paleosols give a finer resolution of primate paleoenvironments in time (Fig. 6) as well as space (Fig. 7). The various paleosols containing Miocene ape fossils in southwest Kenya can also be used to constrain their habitats (Fig. 8). The fragmentary and weathered nature of most of these fossils is evidence that they accumulated through natural processes of death and decay on the paleosols in which they are found (Pickford 1986a). The great diversity of fossil apes in this region (Gommery et al. 2002; Harrison 2010; Ward and Duren 2002) is in contrast to the low diversity of great apes today (Fleagle 1998), leading to the idea that Miocene apes, defined from apelike dentition, were ecologically more like monkeys today (Andrews 1996). Analysis of their occurrence in paleosols shows that there was some ecological separation of different species to different soil types, but still high diversity within a soil type (Fig .8). In the 20 Ma sites of Koru and Songhor, for example, one very large taxon (Proconsul major) shows little habitat specificity through a variety of tropical dry forest habitats, but small taxa (Kalepithecus, Micropithecus) are found in upland soils and larger taxa (Proconsul, Rangwapithecus, Dendropithecus, Limnopithecus) remained in lowland forests closer to water. One paleosol type (Kiewo pedotype) has as many as six taxa including a large ground species (Proconsul major), three likely suspensory feeders (Limnopithecus evansi, L. legetet, Dendropithecus from small to large) and two likely overbranch feeders (Proconsul africanus, Rangwapithecus, from small to large). The contrasting sizes and other differences between these taxa suggest niche partitioning of forest canopy tiers. Diverse catarrhine communities persisted into the dry woodland landscapes of Rusinga Island at 17.8 Ma, when paleosols with the crumb peds and iron-manganese nodules of dambo grasslands (Yom pedotype) appear, but are rare and barren of primate fossils (Retallack et al. 1995). Other evidence for grasslands of about the same age is abundant bunch grasses at the Ugandan fossil site Page 11 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_13-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 8 Paleosols of Miocene apes from southwestern Kenya [Data from Retallack (1991a) with taxonomy after Retallack et al. (2002), Ward and Duren (2002), Harrison (2010)]

of Bukwa (Pickford 2002b). Yom paleosols of dambo grassland are much more common by 14.7 Ma on Maboko Island (Retallack et al. 2002), where they contain abundant vervet-like monkeys (Victoriapithecus: note change of scale for this exceptional collection in Fig .8). These seasonally

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_13-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 9 A scenario for stepwise evolution of East African grasslands with modern precipitation tolerances of African mammals related to those found fossilized in paleosols (Tut, Choka, Kwar) of pori woodlands that preceded the expansion of grasslands. The advent of grasslands disrupted formerly overlapping ranges of apes, bush babies, flying squirrels, mole rats, and spring hares. Climatic ranges of modern mammals are from Kingdon (1971, 1974a, b, 1979) and of paleosols from Retallack (1991a), Retallack et al. (1995)

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_13-5 # Springer-Verlag Berlin Heidelberg 2013

Table 2 Comparison of extinct pori woodland with extant East African vegetation Local name Vegetation Key genera Floral origins Spinosity Leaf set Fruit size Snails Snail origins Mammals Ungulates Primates Mammal origin Fire frequency Soil organics Soil fertility Soil type Parent material

Pori Dry woodland Celtis Zambezian Unarmed Semideciduous Large Cerastua Somalian Apes, rodents Walangania Proconsul Zambezian Low Low High Alfisol Volcanic

Miombo Dry woodland Brachystegia Zambezian Unarmed Deciduous Large Limicolaria Somalian Antelope Aepyceros Cercopithecus Zambezian High Low Low Oxisol, Vertisol Granitic

Nyika Dry bushland Acacia Zambezian Spinose Deciduous Small Achatina Somalian Antelope Tragelaphus Papio Zambezian High Low Low Aridisol Granitic

Savanna Wooded grassland Combretum Eurasian Spinose Deciduous Small Pupoides Somalian Antelope Connochaetes Papio Eurasian High High High Mollisol, Vertisol Volcanic

inundated grasslands of dry climates were not encouraging to fossil apes, which were more common in riparian woodlands (Nyanzapithecus, Mabokopithecus, and Micropithecus of Dhero paleosols). More wide ranging was Equatorius, found in both riparian woodland (Dhero) and nyika shrubland (Ratong), which it exploited more effectively than other apes because of its thick enameled, large molars useful for tough foods (Martin 1985) and its macaque-like limbs and feet (McCrossin et al. 1998). A similar pattern of wide ranging Kenyapithecus and forest-dependent other apes (Simiolus, Proconsul, Nyanzapithecine) persisted in grassland mosaics of Fort Ternan and Kapsibor at 13.7 Ma (Pickford et al. 2006), when well-drained short-grass, wooded grassland was widespread. The appearance of grasslands that was encouraging for victoriapithecine ancestors of vervets and colobines was not so hospitable to apes, which remained rare components of the fossil fauna. Reconstruction of rainfall from paleosols implies also vegetation belts (Fig .6a), by comparison with Holocene climatic ranges of plant formations (Anhuf et al. 1999). There was rainforest in central Africa during the past 20 million years as indicated by rare finds of fossil plants (Bancroft 1932, 1933), but evidence of rain forest has not yet been found in the East African areas yielding hominoid fossils (Retallack 1991a; Jacobs 2002). Paleobotanical interpretations (Fig .6a) are well in accord with indications of vegetation from paleosol classification, profile form and root traces (Retallack 1991a), as evidence that the climatic range of most vegetation types did not change over the past 20 million years. An exception is the evolution of grasslands, which expanded their climatic range to displace extinct kinds of woodlands (Figs. 6 and 9). There is not yet any East African evidence of grasslands before 17.8 Ma, when crumb-textured, brown, simple (A-Bk) profiles of dambo were rare at Rusinga Island (Retallack et al. 1995) and bunchgrasses grew luxuriantly at Bukwa (Pickford 2002b). Well-drained, short-grass, sod-grasslands were widespread by 14.4 Ma (Retallack 1991a; Retallack et al. 2002) and well-drained, tall-grass, sod-grasslands expanded their climatic range considerably by 7 Ma (Wynn 2004a, b). Grasslands were a newly coevolved ecosystem of the Page 14 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_13-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 10 Mean annual precipitation and hominoid diversity, extinctions, and originations in East Africa over the past 20 million years. The paleoprecipitation curve is from Fig. 6. Hominoid data is from Pickford (1986b, 1987), Ward and Duren (2002), and Carroll (2003)

Cenozoic, with grasses uniquely suited to grazing by virtue of their intercalary meristems, modular growth, basal tillering, and sod formation, and grazers uniquely suited to coarse grassy fodder by virtue of their wide muzzles, hypsodont teeth, and hard hooves (Retallack 2001a). A world without grasslands was transformed over some 20 million years to a Plio-Pleistocene world with grassland covering at least a quarter of the land surface. Holocene humans spread grassy agroecosystems to almost all parts of the world (Retallack 2001a). Neogene expansion of grasslands within the paleoclimatic belt roughly defined by the 300–750 mm per annum isohyet enabled grasslands to capture the planetary modal rainfall belt and most fertile soils, with consequences for global change including a significant contribution to global cooling (Retallack 2001b). Before the expansion of the grasslands, an extinct woody vegetation occupied their climatic range (Fig. 6). These extinct dry woodlands can be called pori (Table 2), from a Hadza word for bush (Woodburn 1968). A good example of a pori ecosystem is the Tek paleosol of Rusinga Island (Figs. 3 and 4), which has yielded fossil primates and other mammals, snails, and plants (Pickford 1995; Retallack et al. 1995). Other examples of pori ecosystems include Tut, Choka, and Kwar pedotypes of Songhor and Koru dated at 20 Ma (Retallack 1991a). From the soil perspective, these paleosols have no clear modern analog, because they are red and clayey, with large root traces and blocky structure like woodland soils, yet have shallow calcareous horizons like those found in modern African semiarid to subhumid grassland soils. Modern African soils with such shallow carbonate have very different crumb structure, fine root traces, and dark brown organic-rich surface horizons from abundant grasses. From the paleoanthropological perspective, these ancient communities have no modern analogs, because they have so many fossil hominoids, as many as six species in the Kiewo pedotype (Fig. 8). No community has so many species of hominoids today. Nor do modern hominoids live in such dry climates. Mt. Assirik in Senegal with 956 (854–1224) mm mean annual precipitation is the driest climate with chimpanzees (Kappelman 1993), although Kingdon (2003) gives anecdotes of chimpanzees in wooded grassland. It is now clear that Miocene apes filled a variety of niches like those today filled by vervets, baboons, and colobines as well as apes (Retallack et al. 2002).

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Pori ecosystems such as the Kwar paleosol at Koru (20 Ma) also show peculiar associations of other mammals, including a mix of dry climate taxa, such as mole rats (Bathyergoides), with wet climate taxa such as flying squirrels (Paranomalurus), giant elephant shrews (Miorynchocyon clarki), tenrecs (Protenrec tricuspis), golden moles (Prochrysochloris miocaenicus), and chevrotains (Dorcatherium songhorense: Retallack 1991a). Similarly, the Tut and Choka paleosols at Songhor (20 Ma) and Tek paleosols on Rusinga Island (17.8 Ma) have wet climate flying squirrels and tenrecs as well as dry climate mole rats and spring hares (Retallack 1991a; Retallack et al. 1995). These nonanalog combinations of fossil mammals can be explained by a theory of evolutionary replacement of pori with grassland within semiarid to subhumid regions. Before the advent of grasslands, woody vegetation became smaller in stature and biomass from wet to dry regions (Retallack 2012). This continuum was disrupted as grasslands evolved to usurp the climatic range of pori woodland. Grasslands expanded their range to create a biogeographic divide between nyika shrubland and miombo woodland (Fig. 9). Fossil primates of East Africa not only coped with changing mixes of animals, but with changing climate and vegetation (Fig. 6). Wynn (2004b) has introduced the concept of evolutionary entropy to explain effects of climate and vegetation change on hominoid diversity. Climatically dry episodes encouraged grassland mosaic environments with a more varied landscape of open grassland and local woodland, and thus greater landscape disorder or negentropy. Wet episodes of forest vegetation presented more uniform landscapes of higher entropy. Compilation of hominoid diversity, originations, and extinctions (Table 1, Fig. 10) supports the view that dry episodes correspond with diverse primates, whereas wet episodes lead to extinctions, particularly of specialized arid-adapted taxa. The concept of ecosystem entropy in hominoid evolution is similar in some respects to Vrba’s (1999) “turnover pulse hypothesis,” but ecosystem entropy presents diffuse and long-term selection pressures, rather than episodic crises or “turnover pulses.” Recent compilations of mammalian data from the Turkana region do not show such crises (Bobe et al. 2002), revealing instead an oscillating diversity compatible with less synchronized selection by ecosystem entropy. A major caveat for such theories is the generally inferior fossil record of climatic wet phases, because their soils and sediments are noncalcareous and so not favorable to the preservation of bone (Retallack 1998). There is still no primate fossil record from paleoclimatic wet phases of the early Miocene, but there are discoveries of wet climate human ancestors from 13 Ma (Hill et al. 2002), 6 Ma (Brunet et al. 2002; Galik et al. 2004), and 4–3 Ma (Carroll 2003). The soiltaphonomic bias against wet climate fossils makes the search difficult, not impossible (Peterhans 1993). Each fluctuation in climate and vegetation presented new crises and opportunities to primates. The correlation of climatic events with critical adaptations presented here (Table 1) is only an outline of a new research agenda, to be fleshed out with further studies of the critical intervals. The late Miocene paleosols and primate fossils of the Tugen Hills, for example, remain very poorly known compared with those of the Lake Victoria and Turkana basins. Nevertheless, there are general themes apparent from this compilation. We did not evolve from apes in one seminal event, but by a protracted process of growth and pruning of our evolutionary tree. Some specialized features such as procumbent incisors at 18 Ma evolved in dry grassy woodlands, but did not survive succeeding forest expansions (McCrossin and Benefit 1997). Some specialized features such as long arms by 20 Ma for suspensory locomotion in forests did not persist through succeeding grassland expansions (Harrison 2010). Other forest adaptations such as a short stiff back by 16 Ma (Pickford et al. 1999), erect stance by 6 Ma (Senut et al. 2001; Galik et al 2004), and flat face by 3.5 Ma (Leakey et al. 2001) proved advantageous in the long term, just as did grassland adaptations, Page 16 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_13-5 # Springer-Verlag Berlin Heidelberg 2013

such as thick enamel by 18 Ma (Martin 1985; McCrossin and Benefit 1997), adducted hallux by 14.7 Ma (McCrossin et al. 1998), and long legs for endurance running by 1.8 Ma (Bramble and Lieberman 2004). Although each of these ideas could be debated individually, the general concept of human evolution as a generalist path through a gauntlet of environmental challenges (Potts 1996) is increasingly supported by a burgeoning fossil record (Carroll 2003). There will always be a need for dating and finding more human ancestor fossils, but paleosols now provide new evidence of evolutionary selection pressures with high temporal and spatial resolution. Past hypotheses of a Miocene pluvial, lake and rain forest (Kent 1944; Leakey 1952; Andrews and Van Couvering 1976; Andrews 1996) and late Miocene grassland (Cerling 1992; Cerling et al. 1997a, b) find a counterpart in long-standing theories linking late Miocene evolution of human upright stance or large brains with hunting prowess (Darwin 1872), vigilance against predators (Dart 1926), manipulation of small seeds (Jolly 1970), minimization of sun exposure (Wheeler 1984), long-distance walking (Rodman and McHenry 1980) or running (Bramble and Lieberman 2004), squat feeding on the ground (Kingdon 2003), or moving between scattered fruiting bushes (Sanford 2003). Forest explanations of upright stance allowing erect-back climbing (Tuttle 1981), hands free to care for premature infants (Lovejoy 1981), phallic display to females (Tanner 1981), or intimidation displays to rivals (Jablonski and Chaplin 1993) move the event back into the “Miocene rain forest” (of Andrews and Van Couvering 1975; Andrews 1996), for which there is little evidence at hominoid sites in East Africa (Fig. 6a). All these views can be reassessed in light of the improved record of East African paleosols, which suggests that there were many alternating habitats in East Africa, not just one seminal environmental shift. Darwin’s (1872) idea that erect stance was linked to tool use and brain expansion has been out of favor since the discovery of “Lucy,” when it became clear that erect stance preceded tool use and brain expansion by millions of years (Johanson et al. 1982). Erect stance now appears to have occurred in wooded habitats by 6 Ma (Pickford and Senut 2001; Vignaud et al. 2002; White et al. 2009), perhaps selected by the use of hands in nest provisioning (Lovejoy 1981). We are a mosaic of a complex evolutionary history and no longer need to settle for simple or single allegories of human evolution.

Summary There is a copious and informative fossil record of soils at most of the fossil ape and human ancestor sites in Africa, and study of these paleosols is now giving important insights into the long evolutionary career of our ancestors. The primate evolutionary radiation of the Neogene has been a long saga of changing habitats and adaptations. The fossil record of soils now allows us to address its complexity on a scale appropriate to primate home ranges and to recognize nonanalog habitats of the past. Our distant ancestors have run an evolutionary gauntlet of changing vegetation and climate that has spawned many evolutionary innovations, some of them lasting only to the next shift in climate and vegetation, but others of them proven to be of lasting value.

Cross-References ▶ Charles Darwin, Paleoanthropology and the Modern Synthesis ▶ Dental Adaptation of African Apes ▶ Fossil Record of Miocene Hominoids ▶ Paleoecology, An Imperfect Window on the Past Page 17 of 23

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▶ Paleoclimatic Record and Plio-Pleistocene Environments ▶ Quaternary Geology and Paleoenvironments

References Andrews P (1996) Paleoecology and hominid palaeoenvironments. Biol Rev 71:257–300 Andrews P, Van Couvering JAH (1975) Palaeoenvironments in the East African Miocene. In: Szalay FS (ed) Approaches to primate paleobiology. S Karger, New York, pp 62–103 Anhuf D, Frankenberg P, Lauer W (1999) Die postglaziale Warmphase vor 8000 Jahren. Eine Vegetationsrekonstruction fur Afrika. Geogr Rundsch 51:454–461 Bancroft H (1932) A fossil cyatheoid stem from Mount Elgon, East Africa. New Phytol 33:241–253 Bancroft H (1933) A contribution to the geological history of the Dipterocarpaceae. Geol Fo¨ren Stockh Fo¨rh 55:59–100 Behrensmeyer AK (2008) Palaeoenvironmental context of the Pliocene AL333 “First Family” hominin locality, Hadar, Ethiopia. In: Quade J, Wynn JG (eds) The geology of early humans in the horn of Africa, vol 446, Geol Soc Amer Spec Publ., pp 203–214 Behrensmeyer AK, Deino AL, Hill A, Kingston JD (2002) Geology and geochronology of the middle Miocene Kipsaramon site complex: Muruyur Beds, Tugan Hills, Kenya. J Hum Evol 42:11–38 Bestland EA (1990) Miocene volcanicalstic deposits and paleosols of Rusinga Island, Kenya. University of Oregon, Eugene, Unpublished Ph.D. thesis Bestland EA, Krull ES (1999) Palaeoenvironments of early Miocene Kisingiri volcano Proconsul sites: evidence from carbon isotopes, palaeosols and hydromagmetic deposits. J Geol Soc Lond 156:965–976 Bobe R, Behrensmeyer AK, Chapman RE (2002) Faunal change, environmental variability and late Pliocene hominin evolution. J Hum Evol 42:475–497 Bramble DM, Lieberman BE (2004) Endurance running and the evolution of Homo. Nature 432:345–352 Brunet M, Guy F, Pilbeam D, Mackaye HT, Likius A, Ahounta D, Beauvilain A, Blondel C, Bocherens H, Boisserie JR, de Bonis L, Coppens Y, de Jax J, Denys C, Duringer P, Eisenmann V, Fanone G, Fronty P, Geraads D, Lehmann T, Lihoreau F, Louchart A, Mahamat A, Merceron G, Mouchelin G, Otero O, Campomanes PP, de Leon MP, Rage JC, Sapanet M, Schuster M, Sudre J, Tassy P, Valentin X, Vignaud P, Viriot L, Zazzo A, Zollikofer C (2002) A new hominid from the upper Miocene of Chad, central Africa. Nature 418:145–151 Carroll S (2003) Genetics and the making of Homo sapiens. Nature 422:849–857 Cerling TE (1992) Development of grasslands and savannas in East Africa during the Neogene. Palaeogeogr Palaeoclimatol Palaeoecol 97:241–247 Cerling TE, Harris JM, Ambrose SH, Leakey MG, Solounias N (1997a) Dietary and environmental reconstruction with stable isotope analysis of herbivore tooth enamel from the Miocene locality of Fort Ternan, Kenya. J Hum Evol 33:635–650 Cerling TE, Harris JM, Mac Fadden BJ, Leakey MG, Quade J, Eisenmann V, Elheringer JR (1997b) Global vegetation change through the Miocene/Pliocene boundary. Nature 389:153–158 Dart R (1926) Taung and its significance. Nat Hist 26:315–327 Darwin C (1872) The descent of man and selection in relation to sex. John Murray, London Page 18 of 23

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Deino AL, Tauxe L, Monaghan M, Drake R (1990)40Ar/39Ar calibration of the litho- and paleomagnetic stratigraphies of the Ngorora Formation, Kenya. J Geol 96:567–587 de Menocal PB (2004) African climate change and faunal evolution during the Pliocene-Pleistocene. Earth Planet Sci Lett 220:3–24 Ekart DP, Cerling TE, Montan˜ez IP, Tabor NJ (1999) A 400 million year carbon isotope record of pedogenic carbonate: implications for paleoatmospheric carbon dioxide. Am J Sci 299:805–827 Fleagle JG (1998) Primate adaptation and evolution. Academic Press, New York Fox DL, Koch PL (2003) Tertiary history of C4 biomass in the Great Plains, USA. Geology 31:809–812 Galik K, Senut B, Pickford M, Gommery D, Treil J, Kuperavage AJ, Eckhardt RB (2004) External and internal morphology of the BAR 1002’00 Orrorin tugenensis femur. Science 305:1450–1453 Gommery D, Senut B, Pickford M, Musime E (2002) Les nouveaux restes du squelette d’Ugandapithecus major (Miocene inferieur de Napak, Ouganda). Ann Paleontol 88:167–186 Harrison T (2010) Dendropithecoidea, Proconsuloidea, and Hominoidea. In: Werdelin L, Sanders WJ (eds) Cenozoic mammals of Africa. University of California Press, Berkeley, pp 429–469 Hill A, Leakey M, Kingston JD, Ward S (2002) New cercopithecoids and a hominoid from 12.5 Ma in the Tugen Hills succession, Kenya. J Hum Evol 42:75–93 Jablonski NG, Chaplin G (1993) Origin of habitual terrestrial bipedalism in the ancestor of the Hominidae. J Hum Evol 24:259–280 Jacobs BF (2002) Estimation of low-latitude paleoclimates using fossil angiosperm leaves: examples from the Miocene Tugen Hills, Kenya. Paleobiology 28:399–421 Jacobs BF, Deino AL (1996) Test of climate-leaf physiognomy regression models, their application to two Miocene floras from Kenya, and40Ar/39Ar dating of the late Miocene Kapturo site. Palaeogeogr Palaeoclimatol Palaeoecol 123:259–271 Jenny HJ (1941) Factors in soil formation. McGraw-Hill, New York Johanson DC, Taieb M, Coppens Y (1982) Pliocene hominids from the Hadar Formation, Ethiopia (1973–1977): stratigraphic, chronologic and paleoenvironmental contexts, with notes on hominid morphology and systematics. Am J Phys Anthropol 57:373–402 Jolly C (1970) The seed-eaters, a new model of hominid differentiation based on a baboon analogy. Man 5:5–26 Kappelman J (1993) Book review of Miocene paleosols and ape habitats of Pakistan and Kenya by GJ Retallack. Am J Phys Anthropol 92:117–126 Kent PE (1944) The Miocene beds of Kavirondo, Kenya. Q J Geol Soc Lond 100:85–118 Kingdon J (1971) East African mammals, vol I. Introduction, primates, hyraxes, pangolins, protoungulates and sirenians. Academic Press, London Kingdon J (1974a) East African mammals, vol IIA. Insectivores and bats. Academic Press, London Kingdon J (1974b) East African mammals, vol IIB. Hares and rodents. Academic Press, London Kingdon J (1979) East African mammals, vol IIIB. Large mammals. Academic Press, London Kingdon J (2003) Lowly origins: where, when and why our ancestors first stood up. Princeton University Press, Princeton Koch PL (1998) Isotopic reconstruction of past continental environments. Ann Rev Earth Planet Sci 26:573–613 Leakey LSB (1952) The environment of the Kenya lower Miocene apes. Actes Congr Panafr Prehist Com 18:323–324 Leakey MD, Harris JM (eds) (1987) Laetoli, a Pliocene site in northern Tanzania. Clarendon Press, Oxford Page 19 of 23

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Leakey MG, Spoor F, Brown FH, Gathogo PN, Klarie C, Leakey LN, McDougall I (2001) New hominin genus from Eastern Africa shows diverse middle Pliocene lineages. Nature 410:433–440 Lovejoy CO (1981) The origin of man. Science 211:341–350 MacFadden BJ (2000) Origin and evolution of the grazing guild in Cenozoic New World terrestrial mammals. In: Sues HD (ed) Evolution of herbivory in terrestrial vertebrates. Cambridge University Press, Cambridge, pp 223–244 Martin L (1985) Significance of enamel thickness in hominoid evolution. Nature 314:260–262 McCrossin ML, Benefit BR (1997) On the relationships and adaptations of Kenyapithecus, a largebodied hominoid from the middle Miocene of eastern Africa. In: Begun DR, Ward CV, Rose MD (eds) Function, phylogeny, and fossils: Miocene hominoid evolution and adaptation. Plenum, New York, pp 241–267 McCrossin ML, Benefit BR, Gitau SR, Palmer A, Blue K (1998) Fossil evidence for the origins of terrestriality in Old World monkeys and apes. In: Strasser E, Fleagle JG, McHenry HM (eds) Primate locomotion: recent advances. Plenum, New York, pp 353–376 Mizota C, Kawasaki I, Wakatsuki T (1988) Clay mineralogy and chemistry of seven pedons formed in volcanic ash, Tanzania. Geoderma 43:131–141 Morgan E (1982) The aquatic ape: a theory of human evolution. Souvenir Press, London Peterhans JLK (1993) Contribution to rain forest taphonomy: retrieval and documentation of chimpanzee remains from Kibale Forest. J Hum Evol 25:485–514 Pickford M (1986a) Sedimentation and fossil preservation in the Nyanza Rift system, Kenya. In: Frostick LE, Renaut RW, Reid I, Tiercelin TJ (eds) Sedimentation in the African Rifts. Spec Publ Geol Soc Lond 25: 345–367 Pickford M (1986b) The geochronology of Miocene higher primate faunas of East Africa. In: Else JG, Lee PC (eds) Primate evolution vol 1. Cambridge University Press, London, pp 20–33 Pickford M (1987) The chronology of the Cercopithecoidea of East Africa. Hum Evol 2:1–17 Pickford M (1995) Fossil land snails of East Africa and their paleoecological significance. J Afr Earth Sci 20:167–226 Pickford M (2002a) Early Miocene grassland ecosystem at Bukwa, Mt Elgon, Uganda. C R Paleovol 1:213–219 Pickford M (2002b) Paleoenvironments and hominoid evolution. Z Morphol Anthropol 83:337–348 Pickford M, Senut B (2001) The geological and faunal context of late Miocene faunal remains from Lukeino. C R Acad Sci Terre Planet Paris 332:145–152 Pickford M, Senut B, Gommery M (1999) Sexual dimorphism in Morotopithecus bishopi, an early middle Miocene hominoid from Uganda, and a reassessment of its geological and biological contexts. In: Andrews P, Banham P (eds) Late Cenozoic environments and hominoid evolution: a tribute to Bill Bishop. Geol Soc Lond, London, pp 27–38 Pickford M, Sawada Y, Tayama Y, Matsuda Y-K, Itaya H, Hyodo H, Senut B (2006) Refinement of the age of the middle Miocene Fort Ternan beds, Western Kenya: implications for Old World biochronology. C R Acad Sci Geosci Paris 338:545–555 Potts R (1996) Evolution and climate variability. Science 273:922–923 Radosevich SE, Retallack GJ, Taieb M (1992) A reassessment of the paleoenvironment and preservation of hominid fossils from Hadar, Ethiopia. Am J Phys Anthropol 87:15–27 Retallack GJ (1991a) Miocene paleosols and ape habitats in Pakistan and Kenya. Oxford University Press, New York

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Retallack GJ (1991b) Untangling the effects of burial alteration and ancient soil formation. Ann Rev Earth Planet Sci 19:183–206 Retallack GJ (1992) Middle Miocene fossil plants from Fort Ternan (Kenya) and the evolution of African grasslands. Paleobiology 18:383–400 Retallack GJ (1997) A colour guide to paleosols. John Wiley, Chichester Retallack GJ (1998) Fossil soils and completeness of the rock and fossil record. In: Donovan SK, Paul CBC (eds) The adequacy of the fossil record. Wiley, Chichester, pp 131–162 Retallack GJ (2001a) Soils of the past. Blackwell, Oxford Retallack GJ (2001b) Cenozoic expansion of grasslands and climatic cooling. J Geol 109:407–426 Retallack GJ (2005) Pedogenic carbonate proxies for amount and seasonality of precipitation in paleosols. Geology 33:333–336 Retallack GJ (2012) Mallee model for Mesozoic and early Cenozoic mammal communities. Palaeogeogr Palaeoclimatol Palaeoecol 342–434:111–129 Retallack GJ, Dugas DP, Bestland EA (1990) Fossil soils and grasses of a middle Miocene East African grassland. Science 247:1325–1328 Retallack GJ, Dugas DP, Bestland EA (1995) Miocene paleosols and habitats of Proconsul in Rusinga Island, Kenya. J Hum Evol 29:53–91 Retallack GJ, Wynn JG, Benefit B, McCrossin M (2002) Paleosols and paleoenvironments of the middle Miocene Maboko Formation, Kenya. J Hum Evol 42:659–703 Rodman PS, McHenry HM (1980) Bioenergetics and the origin of hominid bipedalism. Am J Phys Anthropol 52:103–106 Sanford C (2003) The evolutionary key to becoming human. Houghton-Mifflin, Boston Senut B, Pickford M, Gommery D, Mein P, Cheboi K, Coppens Y (2001) First hominid from the Miocene (Lukeino Formation, Kenya). C R Acad Sci Paris Sci Terre Planet 332:137–144 Sheldon ND, Retallack GJ (2001) Equation for compaction of paleosols due to burial. Geology 29:245–250 Sheldon ND, Retallack GJ, Tanaka S (2002) Geochemical climofunctions from North American soils and application to paleosols across the Eocene-Oligocene boundary in Oregon. J Geol 110:687–696 Sikes NE (1994) Early hominid habitat preferences in East Africa: Paleosol carbon isotope evidence. J Hum Evol 27:25–45 Soil Survey Staff (2000) Keys to soil taxonomy. Pocahontas Press, Blacksburg Tanner NM (1981) On becoming human. Cambridge University Press, Cambridge Turner A, Anto´n M (2004) Evolving Eden. Columbia University Press, New York Tuttle RH (1981) Evolution of hominid bipedalism and prehensile capabilities. Phil Trans R Soc Lond B 292:89–94 Veizer J, Godderis Y, Franc¸ois LM (2001) Evidence for decoupling of atmospheric CO2 and global climate during the Phanerozoic. Nature 408:698–701 Vignaud P, Duringer P, Mackaye HT, Likius A, Blondel C, Boisserie JR, de Bonis L, Eisenmann E, Etienne ME, Geraads D, Guy F, Lehmann T, Lihoreau F, Lopez-Martinez N, Mourer-Chauvire´ C, Otero O, Rage JC, Schuster M, Viriot L, Zazzo A, Brunet M (2002) Geology and palaeontology of the upper Miocene Toros-Menalla hominid locality, Chad. Nature 418:152–155 Vrba ES (1999) Habitat theory in relation to evolution in Neogene biota and hominids. In: Bromage TG, Schrenk F (eds) African biogeography. Oxford University Press, New York, pp 19–34 Ward SC, Duren DL (2002) Middle to Late Miocene African hominoids. In: Hartwig WC (ed) The primate fossil record. Cambridge University Press, Cambridge, pp 385–397 Page 21 of 23

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Wheeler PE (1984) The evolution of bipedality and loss of functional body hair in humans. J Hum Evol 13:91–98 White TD, Asfaw B, Beyenne Y, Haile-Selassie Y, Lovejoy CO, Suwa G, Woldegabriel G (2009) Ardipithecus ramidus and the paleobiology of early hominids. Science 326:75–86 Woodburn J (1968) An introduction to Hadza ecology. In: Lee RB, deVore I (eds) Man the hunter. Aldine, Chicago, pp 49–55 Wynn JG (2001) Paleosols, stable carbon isotopes, and paleoenvironmental interpretation of Kanapoi, Northern Kenya. J Hum Evol 39:411–432 Wynn JG (2004a) Miocene paleosols of Lothagam. In: Harris JM, Leakey MG (eds) Lothagam: the dawn of humanity in eastern Africa. Columbia University Press, New York, pp 31–42 Wynn JG (2004b) Influence of Plio-Pleistocene aridification on human evolution: evidence from paleosols of the Turkana Basin. Am J Phys Anthropol 123:106–118 Wynn JG, Retallack GJ (2002) Middle Miocene paleosols and paleoenvironments from the Nyakach Formation at Kaimagool, southwestern Kenya. J Hum Evol 40:263–288 Yapp C, Poths H (1994) Productivity of pre-vascular bioa inferred from Fe(CO3)OH content of goethite. Nature 368:49–51 Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate. Science 292:686–693

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Index Terms: Aridisols 4 Dendropithecus 11 Equatorius 14 Fort Ternan 7, 14 Hadar 10–11 Hominoid 10, 16 Kenyapithecus 14 Maboko Island 12 Mollisols 5 Paleoclimate 3 Paleosols 1–2, 4–5, 9–10 fossils of ecosystems 10 Paleosols localities in East Africa 1–2 methods 5 paleoprecipitation 9 recognition of 4 Proconsul 11, 14 Rain forest 7, 9, 17 Rusinga Island 5–6, 15 Woodland 2, 7, 10, 13–14, 16

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_14-3 # Springer-Verlag Berlin Heidelberg 2013

Quaternary Deposits and Paleo Sites Klaus-Dieter Jäger* Institut f€ ur Prähistorische Archäologie, Martin Luther-Universität Halle, Halle, Germany

Abstract Due to the mineral content of bones and teeth, the majority of fossil hominid remains are represented by these tissues; soft parts of the human body are preserved only very rarely. Whether or not fossils are well preserved depends not only on their own composition but also on the nature of the deposits that enclose them, which as a rule are sediments of the Pliocene, Pleistocene, or Holocene age. Numerous methods are now available for chronometric dating of hominid fossils, though none of them is applicable in all situations. However, it is still necessary to situate each hominid fossil within the larger stratigraphic framework. Hominid evolution began well over 4 million years ago and continued through the final part of the Neogene (Upper Tertiary). As a result, ongoing international discussions of stratigraphic boundaries over this time span are significant for the assessment of hominid evolution. In addition to providing stratigraphic information, paleoanthropological sites offer insights not only into the environmental background of the fossils they yield, but in later periods commonly also into the cultural evolution of mankind and its relatives.

Introduction The Tertiary-Quaternary boundary lies between the Pliocene and Pleistocene epochs. Due to the fact that the terms Tertiary (resp. “tertiaire”) and Quaternary (resp. “quaternaire”) were proposed in the early nineteenth century (for the scientific history of this question see Van Couvering, this volume) there is ongoing debate on the proper definition and even the usefulness of both terms (Cepek and Jäger 1988; Gradstein et al. 2004; Jäger and Ložek 2003, 2005; Pillans 2004). While in the past the most frequently accepted timing of the T-Q-boundary was around 1.8 Myr ago, with the beginning of the Calabrian Stage, in 2009 the International Union of Geological Sciences (IUGS) redefined it at the base of the Gelasian Stage, approximately coincident with the isotopic cold peak that occurred at about 2.6 Myr. The Quaternary, consisting of the Pleistocene and Holocene epochs, is a comparatively short geological period, characterized by a series of significant long- and short-term climatic fluctuations, by the origin and expansion of the genus Homo, and finally by the rise of anatomically-modern Homo sapiens. Since the Quaternary paleoenvironmental background is essential for fleshing out the evolution of our genus, this contribution focuses on the following seven aspects, in turn: (1) the characteristics of fossil remains; (2) the characteristics of fossiliferous deposits; (3) possible methods for dating; (4) geochronometric perspectives; (5) global stratigraphic contexts; (6) environmental dependencies of paleo sites; and (7) archaeological context.

*Email: [email protected] Page 1 of 11

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Characteristics of Fossil Remains Among preserved human remains, hard components from the skeleton, i.e., bones and teeth, are more commonly found, whereas soft parts are rare. The preservation of bones and teeth is determined by the content of calcium carbonate in the fossiliferous deposits. In the case of soft parts, their accessibility to decomposition is determined by the contemporaneous availability of water and atmospheric oxygen. If one of these two factors is kept to a minimum, the decomposition processes slow down or cease. The availability of atmospheric oxygen is reduced in the case of subaquatic sedimentation or sediment conservation (e.g., in inland waters) or in the case of deposits lying below the groundwater table (e.g., peat in boggy terrain). Such conditions characterize the sites of bog bodies. On the other hand, desert areas with minimal water supply provide plenty of access to atmospheric oxygen, but the decomposition of organic matter is impeded by the lack of water. In these areas, an essential precondition for a lot of chemical processes is missing. Consequently, under such conditions the decomposition of organic matter is reduced. Instead, deserts frequently offer the prerequisites for mummification. More often the preservation of fossil remains is restricted to hard components only. Independent of the local presence of water and atmospheric oxygen, the preservability of bones and teeth is a function of their apatite content, characterized by the formula 3Ca3(PO4)2
CaF2. Fossils in limeless deposits are protected from progressive corrosion and destruction since the superficial precipitation is not pure water. As rainwater passes through the atmosphere prior to precipitation, it is contaminated by carbon dioxide (CO2). Consequently, a weak carbonic acid (H2CO3) touches every surface, and the lime content in the soil comes in contact with the acid according to the following formula: CaCO3 þ H2 O þ CO2 ! CaðHCO3 Þ2 If the subsoil contains a lot of calcium carbonate or a diffuse lime distribution, the first stages of decalcification are concentrated on the lime content of fossiliferous deposits and buried soils, and for a while bones and teeth remain protected against corrosion and dissolution. In limeless deposits, by contrast, such fossils are the only objects vulnerable to corrosive processes.

Characteristics of Fossiliferous Deposits At more advanced stages of decalcification, even bones and teeth in limy deposits are exposed to corrosive destruction, but to a lesser degree. It is more or less insignificant whether the fossiliferous sediments in such limy deposits are loose ones with high porosity (such as sands or loess) or solid rocks (like travertine). Both provide sufficient and favorable conditions for the preservation of human skeletal remains, and this is why finds and sites of paleoanthropological significance are mainly connected with such deposits. Specifically, favorable conditions are shared mainly by the following sediment types: 1. Fresh-water lime deposits (calcareous deposits from inland waters, as a rule consisting of >90 % CaCO3, frequently modified by diagenesis and found especially in travertines)

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_14-3 # Springer-Verlag Berlin Heidelberg 2013

2. Loess (dust deposits of eolian origin, characterized by lime content usually ranging between 15 % and 30 % CaCO3) with dust layers, intercalated by buried soils, frequently with calcareous (and also with decalcified) humus horizons 3. Cave deposits, especially in karstified calcareous mountainous regions, where caves originated from subterranean drainage ways and were subject to human entry and settlement after drying (which often happened after rerouting of the original waterway) 4. Calcareous debris, especially in mountainous regions, in open-air sites (with the lime content of the rock detritus being identical to that of the solid rock, perhaps less in the intermediate matter) 5. Calcareous fluvial and deltaic gravels and sands (although these more commonly contain displaced objects) 6. Calcareous lacustrine and beach deposits, as a rule silty and clayey, sometimes laminated In addition to these site types, those favoring the preservation of soft parts (as in the case of bog bodies) have to be considered; these typically consist of peat and limnic mud layers. Finally, tephras, i.e., pyroclastic deposits traced back to nearby volcanic eruptions—as in the case of Vesuvius during August of AD 79—enable the origination and preservation of human body imprints, which can be replenished by means of gypsum after detection. The method for such a procedure has been applied since the 1860s (since the year 1863, to be precise), first of all by the Italian archaeologist Giuseppe Fiorelli. Fiorelli was the long-standing leader of the excavations at the ancient town Pompeii, which was covered by tephra and pumice on the occasion of the AD 79 Vesuvian eruption (Mau 1899). Exceptional finds of this type are, e.g., the brain endocasts from the Eemian travertine at Gánovce in Slovakia (Vlček 1955, 1958).

Possible Methods for Dating In many places, the geological preconditions for fossilized human remains coincide with sites of archaeological discoveries proving previous human presence or even settlement. That is why it is frequently the case that sites of significant paleoanthropological finds are also highly important in terms of archaeology. Not least, such in-site combinations facilitate the dating and the culturalhistorical assignation of the respective paleoanthropological observations. Moreover, the calcareous deposits mentioned above enable not only the preservation of human skeletal remains but also of comparable animal records. Both the paleozoological investigation of skeletal parts, yielding evidence for the early presence of micro- and macromammals, and the determination and examination of fossil shells, providing evidence of former molluscs or ostracods, contribute to biostratigraphic datings and paleoecological assessments. The investigation of mollusc remains is of special validity in central and western Europe, since precise species determinations have been achieved in these regions based merely on conchylia or even just their fragments (Ložek 1955, 1964). Comparable methods of dating are also in preparation in other parts of Eurasia (Meng 2003). However, investigations of micromammals as well as of molluscs are not restricted to qualitative records. On the contrary, both categories of fossils provide opportunities for quantitative analysis and statistical consolidation of results. Moreover, their examination permits the reconstruction of faunal assemblages as a basis for paleoecological interpretation (Rousseau 1990). They thus contribute to the characterization of the natural environment surrounding previous human populations. In travertines, the paleozoological record is often complemented by leaf imprints and incrustations of various plant structures, contributing both to the dating of sites and to their paleoecological Page 3 of 11

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characterization. In sequences of peat and limnic layers of mud or marl, pollen analysis frequently offers an adequate method for dating. Thus, paleobotany as well supports the dating of fossil human remains as well as the reconstruction of the paleoenvironment, especially in the case of travertine and bog sites. However, all of these paleontological and archaeological procedures and observations contribute only to the relative chronology of sites (see “▶ Chronometric Methods in Paleoanthropology”), whereas the establishment of an absolute chronology—or “calendar chronology”—covering the whole time span of fossil hominids requires another methodology.1 The calendar chronology of fossil hominids is based mainly on physical procedures, as summarized by Geyh (1980, 1983) and Wagner (1995, 1998), among others (see “▶ Chronometric Methods in Paleoanthropology”). The preferred methods are radiometry (based on 14C, uranium series, 40K/40Ar, and others) and luminescence procedures (TL, OSL, IR-RF). The last 10–12 Ka is also within the reach of the botanical method of dendrochronology, but in practical terms this method is restricted to wooden objects. Consequently, paleoanthropological finds can only be dated by means of dendrochronology when they are associated with preserved wood. In central Europe, the range of oak chronology provides “a high-resolution time scale for nearly the last 12,000 years” (Spurk et al. 1998, p. 1114). However, the preservation of wood is, as a rule, subject to the same prerequisites as mentioned above with regard to soft parts of human bodies.

Geochronometric Perspective The choice among procedures that are suitable for the numerical dating and calendar chronology of finds proving the presence of fossil men or early hominids is influenced to a high degree by the characteristics of the surrounding fossiliferous deposits. Different compositions of preserved material require the application of different methods. It follows that there will be differences in precision and range of dating. As a general rule, a short range is the inevitable consequence of precise temporal resolution and vice versa. Consequently, and independent of the datable material, the older the finds are, the more imprecise the numerical dating will be. The trade-off is comparable to the situation in optics, where the perceptibility of objects decreases with increasing distance. But this is only one aspect of geochronometry. Another aspect relates to the dated material. Fossil remains of men from historical times and, going back further, from the last millennia can frequently be dated directly, e.g., by using the radiocarbon method. In contrast, fossil remains from the Middle Pleistocene – that is, finds that are several hundreds of thousands of years old – are not datable directly; however, as a rule the enclosing fossiliferous deposits may be subjected to numerical dating, e.g., by means of uranium series in the case of travertine deposits or by application of luminescence procedures in the case of loessic deposits. A larger age characterizes the early stages of hominid evolution, as evidenced by the occurrence of australopithecines. Such discoveries can be dated with only a few methods, e.g., the potassium-argon method (40K/40Ar); as a result, only rocks and loose deposits of volcanic origin can be analyzed. This has the useful application, however, that layers of lava rocks and tephras can be dated at sites of fossil hominid remains, if such layers are included in the stratigraphic sequence. In 1

A note on terminology: As a rule, the search for more or less precise dates, both in the geosciences and in archaeological disciplines, is focused on so-called “absolute” chronology. However, already during the early 1980s, the paleontologist Jaeger (1981) claimed that this term is erroneous and – strictly speaking – inadmissible, since it assumes the existence of absolute time, which is physically and philosophically impossible. Page 4 of 11

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_14-3 # Springer-Verlag Berlin Heidelberg 2013

these cases, then, the materials subjected to dating are not the fossiliferous deposits themselves, but distinct layers in the sequence that includes the fossiliferous deposits. Consequently, the chronological investigation is restricted to time-marks in the local stratigraphy of the research site (cp., e.g., Fitch and Miller 1976; Ullrich 1983, Fig. 3).

Global Stratigraphic Context Hominid evolution started more than 4 Myr ago (cp Johanson and Blake 1996, p. 23). As mentioned in the Introduction, according to resolutions of the IUGS on the occasion of international congress meetings (London 1948, Moscow 1984), this time span was subdivided by the boundary between two different geological systems, i.e., the Tertiary and the Quaternary (see “▶ Quaternary Geology and Paleoenvironment”) (Aguirre and Pasini 1985; Partridge 1997; for background on the history of this decision, see Cepek and Jäger 1988). The chronological position of the boundary was set down at 1.64 or 1.8 Ma. The Tertiary and Quaternary systems share the common feature of significant long-term climate fluctuations, but are nevertheless noticeably distinguished by the average magnitude of the temperature oscillations around their mean values, especially in middle and higher latitudes of the globe. Recently, the International Commission on Stratigraphy (ICS), a body of the IUGS with the authority to make recommendations related to a worldwide geological timescale, has presented a proposal aimed at the removal of this stratigraphic boundary by extending the preceding system of the Neogene, i.e., the Upper Tertiary, to the present (Gradstein et al. 2004). However, there are serious objections to this proposal (Claque et al. 2004), in light of the fundamental environmental changes during the relevant period (Gibbard 2004; Pillans 2004; Van Couvering 1997). Independent of these ongoing discussions, the actual fixation of the debated global stratigraphic boundary at 1.64 or 1.8 Ma seems an unfortunate decision (Cepek and Jäger 1988). The chronological base of the younger system or period might be defined more properly at 2.6 Ma (Gelasian stage of the Pliocene series of the Neogene to date; Pillans 2004).

Environmental Dependencies of Paleo Sites Climatic fluctuations over several hundreds of thousands of years, as mentioned above, not only determined the environmental conditions for previous hominids both in the temperate zones and in polar and subpolar regions, but also influenced human site selection and the chances of fossil preservation. Varying climate conditions favored different processes of sedimentation and, consequently, different types of deposits. Thus, during prolonged cold periods, i.e., the glacials, the advance of glaciers in subpolar and mountainous regions was accompanied by periglacial and climatically continental circumstances in lowlands and hilly uplands of midlatitudes, which favored eolian deposition, mainly of dust. Consequently, hominid finds from glacial periods have frequently been made in loess sequences, as for instance at Dolní Vĕstonice in the Czech Republic and at Austrian sites. On the other hand, many sedimentation processes can take place under warm—frequently under warm and wet—environmental conditions only. The respective deposits could originate either under a constant warm climate, as in the tropics, in lower latitudes, or in the warm phases of glacial cycles, the so-called interglacials, in the midlatitudes. This is why the interglacials favored such deposits as

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_14-3 # Springer-Verlag Berlin Heidelberg 2013

travertine and peat. Travertines may be defined as consolidated freshwater lime deposits, especially calcareous tufas. As mentioned above, especially the travertines have provided excellent conditions for the preservation of finds, as well as for environment reconstruction. Moreover, the origination of these deposits required the proximity of springs and water, due to the dependence of all freshwater lime deposits on hard water. Owing to the significance of water for human life, sites of travertine formation were also frequently preferred locations of human presence and settlement. Consequently, man has often visited such sites and his remains can be discovered there frequently. Examples in central Europe are the well-known interglacial sites at Gánovce, Tata, Taubach, Stuttgart-Bad Cannstatt, Weimar-Ehringsdorf, Bilzingsleben, and Vértesszölös. Due to human presence and activities at such sites, they are significant not only when seen from a paleoanthropological angle but also as a result of archaeological discoveries. As a rule, interglacial deposits, such as peat, mud, or travertine, contain assemblages of floral and faunal fossils and thus provide opportunities for quantitative paleontological analyses. Differences in age are reflected in differences in assemblage composition recorded by pollen, conchylia, or micromammal bones and teeth. Consequently, suitable methods of quantitative paleontological analysis aimed at biostratigraphic indications and correlations are pollen analysis (peat, mud), paleomalacology, and the investigation of micromammal remains (especially in travertines). When differences related to the composition of the flora and fauna which accompany fossil hominid remains are taken into account, a relative chronology of sites can be developed based on biostratigraphy. This approach is exemplified by the application of paleomalacology to famous interglacial travertine sites in central Europe (Jäger and Ložek 2003), including significant places of paleoanthropological discoveries (Jäger and Ložek 2005). Sometimes biostratigraphic indications lead to revision of previous chronological assignations of particular sites. This was the case, e.g., at Weimar-Ehringsdorf in Thuringia, Germany (Jäger 2001; cp also Mania 1993; Steiner 1993). Such corrections may help clear up seeming discrepancies in the paleoanthropological record. At Weimar-Ehringsdorf the original stratigraphic assignation to the Eemian (last interglacial of the Pleistocene) seemed to recommend a classification of the finds within the realm of the Neanderthals, whereas their last examination by Emanuel Vlček (Prague) emphasized similarities of the cranium (e.g., the occiput) to stratigraphically earlier crania at Steinheim (Baden-Wurttemberg, Germany) and Swanscombe (UK) (see “▶ Neanderthals and Their Contemporaries”). As chronometric datings of the accompanying fauna and flora by Mallik et al. (2000) have confirmed, the stratigraphically determined age and the osteological record of the human remains are now in line.

Archaeological Context The majority of the sites providing fossil human remains, both from early hominids and from modern humans, have enabled archaeological observations. To be precise, at many sites bones and teeth prove the previous presence of human beings, while at the same time accompanying archaeological finds or man-made modifications of the site tell us about human activities, behavior, and lifestyle. This is why frequently at sites of paleoanthropological significance, archaeological discoveries are made as well. This is true both with respect to early hominids like Koobi Fora (in the Turkana Basin, Kenya: Coppens et al. 1976) or Hadas (Awash region, Ethiopia: Kimbel et al. 1982) and with respect to later humans (see “▶ The Species and Diversity of Australopiths”; “▶ Role of Environmental Stimuli in Hominid Origins”). Page 6 of 11

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Since the Middle Paleolithic, a considerable share of the available evidence has come from burials. This dating means that even Neanderthals are among the number of specimens recorded in this way (cp. the summarizing survey by Bosinski 1985, pp. 44–52). In this context one might mention, for example, the famous specimens at Le Moustier and La Chapelle aux Saints in France, or the “Old Man” from the Shanidar cave in Iraq (see “▶ Neanderthals and Their Contemporaries”; “▶ Dispersals of Early Humans: Adaptations, Frontiers, and New Territories”). During the Upper Paleolithic, the number of burials increased (see “▶ Cultural Evolution in Africa and Eurasia During the Middle and Late Pleistocene”; “▶ Dispersals of Early Humans: Adaptations, Frontiers, and New Territories”; “▶ Neanderthals and Their Contemporaries”). Among the finds from this era is a female individual from the Pavlovian site at Dolní Vĕstonice (Moravia, Czech Republic) who was portrayed in a contemporaneous ivory carving from the same site (Klima 1983, pp. 83–89). During the Holocene, comprising the last 11,600 years (Litt et al. 2001), Homo sapiens is represented not only by single burials but rather by multi-individual cemeteries of different age, occasionally comprising hundreds of burials or more (e.g., Hallstatt in Austria, Early Iron Age, mainly eighth to sixth century BC, where ca. 1,300 burials going forward all the way to the twentieth century AD have been discovered: Kromer 1959; Sacken 1868; later Pauli 1975). Burials favor the preservation of bones and teeth jointly, frequently even in the original articulation (see “▶ Taphonomic and Diagenetic Processes”). Burials aside, the previous presence of humans at a site of discovery can often be proved for other reasons. Thus the preselection of sites of later—or current—evidence of habitation for paleontological investigations could involve a sleeping site in the case of early hominids (see “▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments”), as exemplified by the cave system of Swartkrans in Southern Africa (with finds of Paranthropus, according to Brain 1983). In later periods, humans frequently used the sites of record for settlement as well as for activities of everyday life, art, and other cultural purposes. Well-known examples have been recovered in caves as well on open ground. An outstanding example of cave occupation by previous residents is given by site 1 at Chou Kou Tien (Zhoukoudian) near the Chinese capital Beijing (Peking), well known as the eponymous site of the so-called Peking Man (Sinanthropus respectively Homo erectus pekinensis; “▶ Later Middle uhl and Laurat 2000, Pleistocene Homo”; “▶ Defining Homo erectus”; Wei 1988; Huang 1998; Br€ pp. 9–10 and pp. 94–100). Evidence of Neanderthal men found in these caves has proved that these locations were both residential and burial sites. The former are usually distinguished from the latter by the irregular scattering of more or less isolated bones and teeth. The same feature of co-occurrence of paleontological and archaeological finds characterizes residential sites on open ground. However, if calcareous deposits are present in the subsoil to some extent, then such archaeological sites also favor the preservation of bones and teeth and, more frequently, of isolated and often fragmentary objects. In situ preservation of the original depositional conditions is provided especially at travertine sites (e.g., Vértesszölös in Hungary: Kretzoi and Dobosi 1990; Bilzingsleben in Germany: recently Mania 1999; Weimar-Ehringsdorf, likewise in Germany: comprising Steiner 1981; Vlček 1993) and at loess sections (e.g., Dolní Vĕstonice in Moravia, Czech Republic: Klima 1983; Vlček 1991; “▶ Dispersals of Early Humans: Adaptations, Frontiers, and New Territories”; “▶ Cultural Evolution in Africa and Eurasia During the Middle and Late Pleistocene”). Fluvial and deltaic as well as—rarely—marine deposits as a rule contain not only isolated and more or less fragmentary parts of the human skeleton, but also dislocated parts. Well-known examples are the famous early mandibles from Dmanisi in Georgia (Bosinski 1995; “▶ Homo ergaster and Its Contemporaries”; “▶ Defining Homo erectus”; Dzaparidze et al. 1992; summary by Page 7 of 11

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Justus et al. 2000; Lordkipanidze et al. 2013; Sander 2013) and from Mauer near Heidelberg in Germany (recent discussion of the local situation: Fezer 1992; Zöller and Stremme 1992; Löscher 1996; Von Koenigswald 1996; Wagner et al. 2007), as well as the cranium found at Steinheim/Murr in southwestern Germany (Adam 1988). By contrast, in the case of bog bodies preservation has frequently taken place not only of the original articulation of bones and teeth but also of soft parts of the human body (see a.o. Hahne 1918; Dieck 1965; Glob 1969; Brothwell 1986; Turner and Scaife 1995; Geb€ uhr 2002).

Conclusion Depending on the composition of fossil human remains (mainly bones and teeth), their preservation as a rule is associated with certain sediments— mainly calcareous ones—from either the late Neogene (Pliocene) or, quite often, the Quaternary (Pleistocene and Holocene). The stratigraphic position of these fossils within the realm of the Quaternary or Neogene enables chronological arrangement of the finds, with increasing precision towards the present. Remains of fossil flora and fauna provide additional insights into the environment and circumstances of life of past human beings. Frequently, the detection and discovery of fossil remains has been favored by archaeological excavations and investigations of former settlement and burial sites.

References Adam KD (1988) Der Urmensch von Steinheim an der Murr und seine Umwelt: Ein Lebensbild aus der Zeit vor einer viertel million Jahren. Jahrb Röm-German Zentralmus Mainz 35:3–23 Aguirre E, Pasini G (1985) The Pliocene-Pleistocene boundary. Episodes 8:116–120 Bosinski G (1985) Der Neandertaler und seine Zeit. Kunst und Altertum am Rhein. F€ uhrer des Rheinischen Landesmuseums Bonn, Nr. 118, Rheinland-Verlag GmbH, Köln in Kommission bei Dr. Rudolf Habelt GmbH, Bonn Bosinski G (1995) Die ersten Menschen in Europa. Jahrb Röm-German Zentralmus Mainz 39:131–181 Brain CK (1983) Swartkrans: a cave’s chronicle of early man. Transvaal Museum, Pretoria Brothwell DR (1986) The bog man and the archaeology of people. British Museum, London Br€uhl E, Laurat T (2000) Fr€ uhe Hominiden, Tl. II: Die erectoiden und praesapienten Formen in S€udund Ostasien - Indien, Indochina, China und Malaiischer Archipel. Praehistoria Thuringica 5:76–144 Cepek AG, Jäger KD (1988) Zum Stand der internationalen Diskussion € uber die Plio-/PleistozänGrenze. Ethnogr Archäolog Z 29(4):653–679 Claque J et al (2004) Revision of the geological time scale: implications for the “Quaternary.”. Quat Perspect 14(1):124–125 Coppens Y, Howell FC, Isaac GLL, Leakey REF (eds) (1976) Earliest man and environments in the Lake Rudolf Basin: stratigraphy, paleoecology and evolution. University of Chicago Press, Chicago/London Dieck A (1965) Die europäischen Moorleichenfunde. Karl Wachholtz, Neum€ unster Dzaparidze S et al (1992) Der altpaläolithische Fundplatz Dmanisi in Georgien (Kaukasus). Jahrb Röm-German Zentralmus Mainz 36:67–116

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Fezer F (1992) Die Mauerer Sande als Rest einer langgestreckten Aufschotterung. In: Beinhauer KW, Wagner GA (eds) Schichten von Mauer: 85 Jahre Homo erectus heidelbergensis. Reiß Museum, Mannheim, pp 98–100 Fitch FJ, Miller JA (1976) Conventional potassium-argon and argon-40/argon-39 dating of volcanic rocks from east Rudolf. In: Coppens Y, Howell FC, Isaac GLL, Leakey EF R (eds) Earliest man and environments in the Lake Rudolf Basin: stratigraphy, paleoecology and evolution. University of Chicago Press, Chicago/London, pp 123–147 Geb€uhr M, Verein zur Förderung des Archäologischen Landesmuseums e. V., Schloß Gottorf (eds) (2002) Moorleichen in Schleswig-Holstein. Wachholtz, Neum€ unster Geyh MA (1980) Einf€ uhrung in die Methoden der physikalischen und chemischen Altersbestimmung. Wiss. Buchges, Darmstadt Geyh MA (1983) Physikalische und chemische Datierungsmethoden in der Quartär-Forschung. Ellen Pilger, Clausthal-Zellerfeld Gibbard PH (2004) Revision of the geological time scale. Quat Perspect 14(1):125–126 Glob PV (1969) The bog people: iron-age man preserved. Faber, London Gradstein FM, Ogg J, Smith A (2004) A geological time scale. Cambridge University Press, Cambridge Hahne H (1918) Die geologische Lagerung der Moorleichen und Moorbr€ ucken. GebauerSchwetschke, Halle/Saale Huang PH (1998) Evolutional process and dispositional cycles of Peking Man Cave in relation to the living environments and cultural development of Peking Man. Hum Evol 13:21–28 Jaeger H (1981) Trends in stratigraphischer Methodik und Terminologie. Z Geol Wiss 9(3):309–332 Jäger KD (2001) Zur erdgeschichtlichen Einstufung der fossilen Menschenfunde von WeimarEhringsdorf. Proc 4 Kongr Ges f Anthropol 2000:27–29 Jäger KD, Ložek V (2003) On the practicability of palaeomalacological criteria for dating Pleistocene interglacial sites in Central Europe. Veröff Landesamt f Archäol (Festschr Mania) 57:273–280 Jäger KD, Ložek V (2005) On the contribution of palaeomalacology to the stratigraphical placement of Pleistocene travertine sites in Central Europe. Paper in 1st international conference and exhibition on travertine. Pamukkale University, Denizli Johanson D, Blake E (1996) From Lucy to language. Witwatersrand University Press, Johannesburg Justus A, Jöris O, Nioradze M (2000) Homo erectus vor 1,75 Millionen Jahren an der Schwelle Europas? Archäolog KorrBl 2000(2):12–16 Kimbel WH, Johanson DC, Coppens Y (1982) Pliocene hominid cranial remains from the Hadar formation, Ethiopia. Am J Phys Anthropol 57:453–499 Klima B (1983) Dolní Vĕstonice: Tabořištĕ mamutů. Academia, Praha Kretzoi M, Dobosi V (1990) Vértesszölös: site, man and culture. Akadémiai Kiadó, Budapest Kromer K (1959) Das Gräberfeld von Hallstatt, vol 1–2. Sansoni, Firenze Litt T, Brauer A, Goslar T, Merkt J, Balaga K, Muller H, Ralska-Jasiewiczowa M, Stebich M, Negendank JFW (2001) Correlation and synchronisation of lateglacial continental sequences in northern Central Europe based on annually laminated lacustrine sediments. Quat Sci Rev 20:1233–1249 Lordkipanidze D, Ponce de León MS, Margvelashvili A, Rak Y, Rightmire GP, Vekua A, Zollikofer PE (2013) A Complete Skull from Dmanisi, Georgia and the Evolutionary Biology of Early Homo. Science 342: 326–331

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Löscher M (1996) Die Schotterablagerung in der alten Neckarschleife von Mauer. In: Beinhauer KW, Kraatz R, Wagner GA (eds) Homo erectus heidelbergensis von Mauer (Mannheimer Geschichtsbl NF Beih 1). Thorbecke, Sigmaringen, pp 17–27 Ložek V (1955) Mĕkkýši českoslovenkého kvartéru. Nákl. ČSAV, Praha Ložek V (1964) Quartärmollusken der Tschechoslowakei. Tschechoslow Akad Wiss, Prag Mallik R, Frank N, Mangini A, Wagner GA (2000) Anwendung der UranreihenMikroprobendatierung an quartären Travertinvorkommen Th€ uringens. Praehistoria Thuringica 4:95–100 Mania D (1993) Zur Paläontologie der Travertine von Weimar-Ehringsdorf. In: Vlček E (ed) Fossile Menschenfunde von Weimar-Ehringsdorf. Konrad Theiß, Stuttgart, pp 26–42 Mania D (1999) The Bilzingsleben site: Homo erectus, his culture and his ecosphere. In: Ullrich H (ed) Hominid evolution: lifestyles and survival strategies. Edition Archaea, Gelsenkirchen/ Schwelm, pp 293–314 Mau A (1899) Pompeji, its life and art. Macmillan, New York Meng St (2003) Mollusken aus dem Quartär Mittelasiens, insbesondere aus S€ ud-Tadschikistan. Unpubl. dissertation, University Halle, Halle Partridge TC (1997) The Plio-Pleistocene boundary. Quat Int 40:5–10 Pillans B (2004) Proposal to redefine the Quaternary. Quat Perspect 14(1):125–126 € Pauli L (1975) Das Gräberfeld vom Salzberg zu Hallstatt – Erforschung – Uberlieferung – Auswertbarkeit, Mainz Rousseau DD (1990) Statistical analyses of loess molluscs for palaeoecological reconstructions. Quat Int 7(8):81–89 Sacken E (1868) Das Gräberfeld von Hallstatt in Oberösterreich und dessen Altert€ umer. Wilhelm Braum€ uller, Wien Sander J (2013) Homo-Schädel aus Dmanisi wirft neues Licht auf die menschliche Evolution. Naturwiss. Rundschau 66(12): 647–648 Spurk M et al (1998) Revisions and extension of the Hohenheim oak and pine chronologies: new evidence about the timing of the younger dryas/preboreal transition. Radiocarbon 40(3):1107–1116 Steiner W (1981) Der Travertin von Ehringsdorf und seine Fossilien (Die Neue Brehm-B€ ucherei 522). A Ziemsen, Lutherstadt/Wittenberg Steiner W (1993) Geologischer Aufbau und Bildungsgeschichte der Travertine von WeimarEhringsdorf unter besonderer Betrachtung der Hominiden- und Artefaktfundschichten. In: Vlček E (ed) Fossile Menschenfunde von Weimar-Ehringsdorf. Konrad Theiß, Stuttgart, pp 14–25 Turner RC, Scaife RG (1995) Bog bodies: new discoveries and new perspectives. British Museum Press, London Ullrich H (1983) “Lucy”- Anfänge der Menschheit. Das Altertum 29(4):216–225 Van Couvering JA (ed) (1997) The Pleistocene boundary of the beginning of the quaternary. Cambridge University Press, Cambridge Vlček E (1955) The fossil man of Gánovce, Czechoslovakia. J R Anthropol Inst 85:163–171 Vlček E (1958) Zusammenfassender Bericht € uber den Fundort Gánovce und die Reste des Neandertalers in der Zips (ČSR). Tschechoslowak Akad d Wiss, Archäolog Inst, Prag Vlček E (1991) Die Mammutjäger von Dolní Vĕstonice. Archäol u Museum, Heft 022, LiestalBaselland Vlček E (ed) (1993) Fossile Menschenfunde von Weimar-Ehringsdorf. Konrad Theiß, Stuttgart

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Von Koenigswald W (1996) Der Unterkiefer von Mauer: ein Zufallsfund in einer Faunenfundstelle! In: Beinhauer W, Kraatz R, Wagner GA (eds) Homo erectus heidelbergensis von Mauer (Mannheimer Geschichtsbl NF Beih 1). Thorbecke, Sigmaringen, pp 35–36 Wagner GA (1995) Altersbestimmungen von jungen Gesteinen und Artefakten. Ferdinand Enke, Stuttgart Wagner GA (1998) Age determination of young rocks and artefacts. Springer, Berlin/Heidelberg/ New York Wagner GA, Rieder H, Zöller L, Mick E (eds) (2007) Homo heidelbergensis - Schl€ usselfund der Menschheitsgeschichte. Konrad Theiss, Stuttgart Wei Q (1988) Le cadre stratigraphique, géochronologique et biostratigraphique dans sites plus anciens connu en Chine. Anthropologie 97:931–938 € €uber die quartäre Schichtenfolge von Mauer. In: Beinhauer Zöller L, Stremme HE (1992) Uberblick KW, Wagner GA (eds) Schichten von Mauer: 85 Jahre Homo erectus heidelbergensis. Reiß-Museum, Mannheim, pp 90–97

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Zoogeography: Primate and Early Hominin Distribution and Migration Patterns Alan Turnera and Hannah O’Reganb* a School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, UK b Department of Archaeology, University of Nottingham, Nottingham, UK

Introduction It is a commonplace observation that species of both plants and animals have patterns of distribution, and that everything is not found everywhere (Cox and Moore 2004). In many cases, such distributions can be explained by the presence of physical or biotic barriers such as mountains, deserts, or water and the absence of suitable foods, while some clearly owe much to modern human interference. But a species may not have always been where it is found now, while another may formerly have existed in areas from which it is now absent, so that many patterns reflect processes of movement that occurred from a few tens to thousands or millions of years ago. We live on a planet that has been constantly changing as the continents have shifted and climates have altered, and it is likely that many of the patterns we observe today have been affected by such events. Change in zoogeography over geological time, and its relationship to tectonic and climatic events, is one of the things that the fossil record can bring to providing a bigger picture of the past, although pitfalls must be overcome in the process. Identification and dating must be accurate, and while presence is clear enough from the fossils, firm evidence for absence in a region may be rather more difficult to distinguish from simple failure to look in the right place or simply to find. But the fossil record is never as good as it will become, and synthesis cannot forever be delayed on the grounds that we do not yet have enough data. As time goes on, and more evidence accumulates from more and more sites, even absence may start to be seen as a real feature of the record and attempts at synthesis of zoogeographic patterns may legitimately be made (Turner and Wood 1993). Paleoanthropology deals with the evolution of Homo and our close fossil relatives, the tribe Hominini or hominins, and may be extended, according to the interests of the enquirer, to include the evolution of the Hominoidea (the superfamily that includes lesser apes, great apes, and humans) or even more widely to other primates. In the case of the Hominoidea, one of the most important issues to understand is the question of dispersions, whether of the Primates into Africa in the first place or our closer hominin fossil relatives out of Africa in the later stages of their evolution. It could be argued that the dispersals of the Hominoidea are likely to be best understood within the context of dispersals in other elements of the mammalian fauna, and here this larger context is examined, beginning with a brief discussion of the initial movement of the Primates into Africa, followed by a review of the evidence for Miocene to Early Pleistocene distributions within Africa and between Africa and Eurasia.

Alan Turner passed away in January 2012. This chapter has subsequently been updated bu his co-author, but not rewritten *Email: Hannah.O’[email protected] Page 1 of 19

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Early Movements of Primates into Africa Recent molecular analyses of DNA sequences suggest that a small number of mammalian orders (the elephants, hyraxes, tenrecs, aardvarks, elephant shrews, golden moles, and the aquatic manatees or sea cows) together compose a unique group, the Afrotheria, whose members share a restricted common ancestry (Tabuce et al. 2008). The fact that the closest (sister) group to these is likely to be the South American order Xenarthra (the sloths, anteaters, and armadillos) makes sense in terms of continental separations (Asher et al. 2009). A significant absence from the Afrotheria, however, is Primates, which seem to have evolved in the Northern Hemisphere (Fleagle 1999). The Afrotheria owe their origins as a distinctive group to the fact that the continent was long isolated after the breakup of the southern landmass of Gondwana. Africa and the southern part of the Arabian Peninsula finally docked with the Eurasian plate in the Early Miocene, around 25–18 Ma, after a northward movement from the breakup estimated at around 14 of latitude (Ro¨gl 1999). In the process of closing with Eurasia, the eastern arm of the Tethys seaway was closed, providing a land connection. At what precise point movements across the shortening gap between Africa and Eurasia became possible for terrestrial animals is unclear, but primates are known in some numbers from the Fayum deposits of Egypt between 37 and 30 Ma, with an earlier appearance between 52 and 46 Ma suggested by material from Algeria (Tabuce et al. 2009). The implication is that some form of island hopping across the shortening gap was possible as tectonic forces buckled the floor of the Tethys and produced a series of small and no doubt short-lived areas of dry land. Following the contact between Africa and Eurasia, a transgression of the Tethys Sea southward left Africa connected to Eurasia via the southernmost part of the Arabian Peninsula across what are now the Bab el-Mandeb Straits (Tchernov 1992). Much of the later Miocene movement of faunas into and out of Africa therefore probably took place across this region, although our knowledge of the Miocene mammalian fauna of Arabia is currently very poor (Whybrow and Clements 1999). Those same enormous forces produced by the combined northward movement of Africa and India formed the mountain chains that run from southern Europe to the Himalayas. These include the Taurus and Zagros mountains of Turkey and Iran, which have combined with the frequently harsh conditions of the Arabian Peninsula to control movements into and out of Africa (Tchernov 1992) (see also later). Toward the end of the Miocene, during the Messinian salinity crisis, tectonic processes in the westernmost region closed the portal with the Atlantic and the Mediterranean began to dry up (Kirjksman et al. 1999). During the Early Pliocene, the Mediterranean refilled, while the Red Sea widened as the Arabian plate swung away and eventually broke the Bab elMandeb land bridge in the Late Pliocene, part of the eastern African rifting process that continues to the present day. Although some form of land bridge therefore existed between southern Spain and northern Africa during the Messinian (Gibert et al. 2013), there is no compelling evidence for one across the Gibraltar Straits since then. Most if not all subsequent mammalian movements between Africa and Eurasia during Plio-Pleistocene times are therefore likely to have been via the Levant and perhaps Arabia (see later). The Eocene to Oligocene primates of the Fayum were already quite diverse and numerous genera have been recognized (Seiffert et al. 2010), but their relationships to modern primates have yet to be established. Such diversity points to a well-established presence at that point, but the subsequent record of monkeys is poor until well into the Miocene, when records recommence in the rich deposits of eastern Africa where numerous remains referred to the family Victoriapithecidae occur (Jablonski and Frost 2010). Primitive apes appear in the fossil record of Africa a little later than the monkeys, and there is a reasonably good record from Late Oligocene to mid-Miocene Page 2 of 19

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deposits. One of the oldest specimens comes from Lothidok Hill in northern Kenya, in deposits that may be as early as 27 Ma, while others are found at a range of Early Miocene sites in Uganda and Kenya such as Rusinga Island in what is now Lake Victoria, at Koru and at Songhor in deposits dated to the period 22–17 Ma (Andrews and Humphrey 1999). These animals, belonging to the genera Proconsul, Rangwapithecus, and Nyanzapithecus and varying from large monkey-like up to female gorilla-like in size, are placed in the separate family Proconsulidae and best characterized as “arboreal quadrupeds” (see chapter “▶ Fossil Record of Miocene Hominoids”). More advanced apes appear in a further radiation in the period 17–12 Ma, and are referred to three superfamilies – the Dendropithecoidea (Family Dendropithecidae), Proconsuloidea (subfamilies Proconsulinae, Afropithecinae and Nyanzapithecinae), and the Hominoidea (subfamilies Kenyapithecinae and Homininae) (Harrison 2010). It is at this stage that primates appear to have moved back out of Africa. Although the Afropithecinae occur in Africa and Arabia, the Kenyapithecinae are known from Kenya but mostly occur in Turkey and southeastern Europe, while members of the Homininae (tribe Dryopithecini) are European in distribution (Begun 2009). In other words, the major known fossil distribution of the early Hominoidea is outside Africa. This early dispersion from Africa may have implications for our understanding of the later origins of the Homininae, the subfamily containing the African great apes and humans (see below). The earliest movement of the Primates into Africa may have been “accompanied” by a dispersal of the archaic predator order Creodonta, since members of the family Hyaenodontidae also first appear in Early Eocene deposits there, but further contemporary incursions of other groups are not evident. A clearer pattern emerges at the time of full contact around 20 Ma, when other immigrants from Eurasia included the first perissodactyls in the form of early rhinos, and the bizarre-looking chalicotheres, with their horse-like heads and clawed feet. More artiodactyls also made their appearances, with the incursion of the giraffoid climactocerids and first antelopes as well as primitive pigs of the genus Nguruwe, which must have traversed the continent since they are known from Namibia and Kenya at around 17.5 Ma (Turner and Anto´n 2004). More advanced cercopithecoid monkeys replaced the earlier primates, although in situ evolution is hard to distinguish from immigration. True Carnivora entered the continent with the first appearance of cats and the amphicyonid bear-dogs as well as of mustelids (Morales et al. 1998) and, at least in North Africa, of members of the extinct cat-like family Nimravidae, although the creodonts continued to prosper as the dominant meat eaters. In the other direction, the probable dispersion of dryopithecine apes was perhaps preceded by the appearance of anthracotheres in Europe and possibly accompanied by a dispersal of monkeys of the genus Pliopithecus, the creodont Hyainailouros (Agustı´ and Anto´n 2002) and the first movement of the proboscideans from Africa (Harzhauser et al. 2007). The latter consisted of movements not of elephants proper but of the fourtusked gomphotheres and the deinotheres, the latter marked by a single pair of tusks set in the lower jaw. The subsequent history of some of the various proboscidean genera during the Miocene and Pliocene suggests a good deal of interchange with Eurasia. On a general note, the structure of the African Early Miocene guild of larger carnivores seems to have divided into flesh-eaters among the early cats, nimravids and perhaps smaller creodonts, and bone-crunchers among the amphicyonids and larger creodonts, and by the mid-Miocene, the complexity in the guild structure of carnivores was enormous. Such a guild points to an equivalent complexity in the ecological relationships of predators and prey in Africa at this early period. The ungulates do not look particularly well adapted for speed, while the predators do not look equipped to chase anything moving particularly fast. Dog-like animals, in the form of some of the smaller hyenas of the genera Ictitherium, Hyaenictitherium, Lycyaena, and Hyaenictis, only appear much later in the Miocene (see later) and in the absence of the true dogs of the family Canidae until later Page 3 of 19

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_15-3 # Springer-Verlag Berlin Heidelberg 2013

still in the Pliocene it is difficult to assess the extent to which pack hunting might have been possible (Turner and Anto´n 2004). The larger amphicyonids are unlikely to have operated cooperatively, and would probably have taken a mixture of carrion and hunted meat. Overall, the zoogeography that can be pieced together supports interpretations of the earlier to Middle Miocene vegetation of Africa as generally quite closed (Cerling 1992; Cerling et al. 1997). It might therefore be presumed that most of the primates at that time would have found food and refuge among the closed vegetation, and as such have been fairly safe from predation, but the latest work on material from Kenya suggests that Miocene primates were preyed upon by a variety of animals (Jenkins 2011).

Zoogeographic Evidence for the Origins of the Hominidae Africa is usually taken to be the origin point of the human lineage, and so far as the later stages of the Pliocene and Pleistocene are concerned, this is generally accepted as true beyond reasonable doubt. Nevertheless some doubts about this matter have been raised in recent years – in particular regarding the origins of Homo erectus (White 1995; Dennell 2004) – and it would always be unwise to assume that there are no surprises left in the fossil record. However, as discussed above, the Primates themselves did not originate in Africa, and while emphasizing their incursion during the Early Eocene may seem like an academic nicety, it is worth stressing that the intermediate period of the mid- and later Miocene witnessed emigrations and perhaps also re-immigrations. The apes of the subfamilies Homininae and Kenyapithecinae that dispersed from Africa underwent a considerable radiation in Eurasia until the end of the Mid-Miocene, around 7–9 Ma (Andrews and Bernor 1999). In Africa, apes are scarce between perhaps 15 Ma and the very end of the Miocene (Andrews and Humphrey 1999; Leakey and Harris 2003), although fragmentary specimens are known from some 10 Ma onward (Begun 2009). Interpreting such scarcity in the fossil record is always hazardous, since it may indicate no more than an absence of suitable deposits or inadequate search and recovery. But if it is a real pattern, then it is perhaps the ancestor for the later great ape and human lineage of the subfamily Homininae may be found among these Eurasian advanced hominid apes. The possibility that the European Dryopithecini make the most plausible candidates has been both proposed (Begun 1993, 2009) and questioned (Andrews 1992; Andrews and Bernor 1999) on several details of taxonomy and systematics, but Solounias et al. (1999) raised the question again in the context of understanding wider issues of the relationship between faunas of southeastern Europe and Africa. The latter authors point out that many of the savanna-dwelling mammals of Africa may well have originated in what they term the Pikermi Biome, based on the rich Late Miocene Greek locality of Pikermi. They cite somewhat longer necked and thus more advanced giraffes, rhinos of the extant genera Diceros and Ceratotherium, the false sabretoothed cat Dinofelis and the larger bone-smashing hyenas Belbus beaumonti and Adcrocuta eximia as offering primary evidence for such an origin, and it is indeed clear that such animals do make their first appearance in Africa in the latter part of the Miocene. Overall, by around 8 Ma, over the middle part of the Miocene, there is an evidence of considerable incursion from Eurasia generally into Africa if we add to the above list the smaller to midsized and dog-like hyenas of the genera Protictitherium, Ictitherium, Hyaenictitherium, Lycyaena, and Hyaenictis, the sabretoothed cat Machairodus, a range of mustelids, and a number of antelopes (Vrba 1995; Werdelin and Turner 1996; Turner and Anto´n 2004). The impetus for this movement appears to have been a major shift in climate, changing the western European vegetation from subtropical evergreen forest to more deciduous and dry woodland and provoking a turnover in mammalian fauna that Agustı´ et al. Page 4 of 19

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_15-3 # Springer-Verlag Berlin Heidelberg 2013

(1999) termed the mid-Vallesian Crisis. By around 9 Ma, the dryopithecine hominids were extinct in Western Europe, although they managed to survive until perhaps 7.5 Ma in Italy and China (Andrews and Bernor 1999). A movement of early hominid apes back into Africa is therefore entirely plausible as part of this larger pattern of dispersion.

Zoogeography of African Pliocene Hominini Whether or not the common ancestor of later Hominidae was indeed of Eurasian dryopithecine-like morphology and origin, our African ancestors and relatives changed from being generalized apes to more sophisticated apes with tools over a period of a few million years, only becoming really recognizably human with the earliest appearance of the H. erectus lineage at around 1.8 Ma. This transition included shifts to an upright stance and fully bipedal walking and a massive increase in relative and absolute brain size, presumably accompanied by alterations in behavior, social interactions, and intelligence. Details of zoogeography however remain unclear. The earliest currently known putative hominins are from the late Miocene – Sahelanthropus tchadensis (6–7 Ma) from Toros Menalla in the Chad Basin (Brunet et al. 2002), Orrorin tugenensis (6.2–5.5 Ma) from Lukeino in Kenya (Senut et al. 2001), and Ardipithecus kadabba (5.77–5.2 Ma) from Gona in Ethiopia (Haile-Selassie and WoldeGabriel 2009). Both O. tugenensis and Ar. kadabba have been associated with wooded environments with a nearby water source, but the Chad Basin paleoenvironment appears to have been more of a mosaic association of lake-side gallery forest, wooded savanna, and open grasslands (Vignaud et al. 2002), and the precise preference of the primate is hard to determine (see Strait et al., ▶ Analyzing Hominin Phylogeny, this volume; Rown & Reed, ▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments, this volume). According to interpretations of the Early Pliocene material referred to Ardipithecus ramidus, first found in 4.4 Ma deposits of the Middle Awash Valley in Ethiopia (White et al. 1994, 1995), an attachment to a woodland habitat may have persisted until close to 4.0 Ma (WoldeGabriel et al. 1994). Material also referred to Ar. ramidus from 4.5 to 4.3 Ma sediments to the west of the Awash at As Duma (Semaw et al. 2005) is also said to be associated with moderate rainfall grassland and woodland/grassland, based on paleosols, soil carbonates, and faunal elements. However, stable carbon isotope values for ungulate dental enamels at the Gona Ardipithecus sites suggest a significant component of C4 grasses in the diet (Levin et al. 2008), and we should beware of the dangers of a small number of early hominin localities misleading us about habitat preferences and true distributions. We do know that the physical and biotic environment within which the hominins were evolving was itself undergoing significant changes. Rifting, volcanic activity, and uplift were continuing to change the topography of eastern and southern Africa as they had throughout the Miocene (Pritchard 1979; Adams et al. 1996), and as a result of these changes and their interaction with climatic events, the vegetation was opening out to provide the distribution and huge mosaic of habitats existing there today. Such physical and biotic changes underlie the distributions of the living African mammal fauna (Grubb 1999; Grubb et al. 1999) and must have had a major bearing on the zoogeography of the past (Turner 1995). Clearly, more open vegetation not only developed during the Pliocene but also became an attractive habitat for predators and in all probability early hominins (Turner and Anto´n 1999). The development of stone-tool technology can now be traced back in Africa to around 2.6 Ma at Gona in Ethiopia, and similarly dated stone-tool cut-marked bones have also been reported from Bouri in Ethiopia (Semaw et al. 2003). More recently, bones Page 5 of 19

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_15-3 # Springer-Verlag Berlin Heidelberg 2013

with damage interpreted as hominin-inflicted and dating from approximately 3.9 Ma have been reported from Dikika, Ethiopia (McPherron et al. 2010); however, these have not been widely accepted (see Dominguez-Rodrigo et al. 2011 and references therein). What happened in terms of hominin development before such lithic technology was developed, either to assist or to motivate the move to more open terrain, is unclear. An analysis of the zoogeography of African Pliocene hominins within the larger context of distributions in the rest of the Plio-Pleistocene large-mammal fauna was undertaken by Turner and Wood (1993), prior to the more recent discoveries referred to above but based on a larger body of hominin species and known distributions. The evidence available then, as now, suggested that the genus Australopithecus was apparently geographically split, and represented by A. afarensis in eastern Africa and A. africanus in the south. The genus Paranthropus, taken by Turner and Wood (1993) to be monophyletic, was considered to be represented by P. robustus and perhaps P. crassidens in the south and by P. aethiopicus and P. boisei in the east. More recent discoveries have extended the range of named hominin taxa in the eastern region but done little to alter that picture of regional distributions, although Bromage and Schrenk (1995) have extended the range of P. boisei southward to Malawi. The most primitive australopithecine species, A. anamensis, dating to approximately 3.9–4.2 Ma has been identified in both Kenya (Leakey et al. 1995) and Ethiopia (White et al. 2006), while another, A. bahrelghazali, has been recognized at Koro Toro in Chad in deposits of slightly later age (Brunet et al. 1996). A third species, A. garhi, has been identified in deposits of the Middle Awash Valley (Asfaw et al. 1999), and a fourth, placed in a new genus as Kenyanthropus platyops (Leakey et al. 2001), has been identified from deposits dated to 3.5 Ma at West Turkana. The newest (and latest) species of Australopithecus – A. sediba – has recently been recognized and dated to 1.97 Ma at Malapa in South Africa (Pickering et al. 2011). In the case of the genus Homo, assessing the geographic distribution of species is made more difficult by the increasingly evident fact that the taxonomy is more complicated than has previously been assumed. Homo is conventionally considered to be evident in Africa back to about 2.5 Ma, first represented in eastern Africa by the species H. habilis and H. rudolfensis, although the latter has also been identified in Malawi by Bromage and Schrenk (1995). The fact that stone tools appear in the archaeological record at about the same time has led to speculations about the relationship between evolutionary change and the development of tool-making abilities. However, it has long been apparent that the earliest taxa assigned to the genus Homo are a rather heterogeneous group (Wood 1991, 1992), and it has been argued that they could be removed from Homo altogether, in a scheme leaving H. erectus sensu lato as the earliest clear member of the genus (Wood and Collard 1999; see also Wood and Baker (2011), Schrenk et al., ▶ The Earliest Putative Homo Fossils this volume; Baab, ▶ Defining Homo erectus this volume; Tattersall, ▶ Homo ergaster and Its Contemporaries this volume). This would place the first evidence of our genus within the Olduvai Event (1.95–1.77 Ma) and sometime after the earliest appearance of stone tools, and it is this seemingly abrupt appearance of H. erectus that has led to suggestions of a possible origin outside Africa (White 1995; Dennell 2004). Of course, tool making by hominins of other genera is neither improbable nor implausible. Chimpanzees both make and use tools, albeit primitive ones that satisfy any sensible definition of such behavior, and it may be that a variety of evolutionary solutions that included some elements of manufacture and use of technology were developing among the African Pliocene hominins (Turner and Anto´n 2004). While our own lineage moved toward greater ecological generalization coupled to an emphasis on stone-tool technology and an increase in brain size, members of the genus Paranthropus appear to have developed larger jaws and teeth in order to cope with their food (see Rown and Reed, ▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments this Page 6 of 19

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_15-3 # Springer-Verlag Berlin Heidelberg 2013

volume). At least one hominin species traditionally referred to Homo, the east African H. rudolfensis, appears to have followed the same path as the paranthropines between 2.5 and 1.8 Ma with enlarged teeth but with a relatively large brain as well. If the H. rudolfensis material is indeed to be linked to the earlier K. platyops and referred to that genus, as suggested by Leakey et al. (2001), we may then very well have evidence of a separate lineage within which brains and teeth both developed. We may therefore identify at least three different evolutionary developments within Pliocene hominins, all of which enjoyed a considerable measure of success. Whatever the lineages involved, making sense of the zoogeography of Pliocene hominins is difficult. The record presents a complex series of morphologies and proposed taxa, and interpretations of identity, relationship, and adaptations of the various species, leave alone distributions, are impeded by the fragmentary state of much of the material and the fact that several taxa or putative taxa are represented by single specimens or localities. This underscores the value of looking at distributions within the rest of the fauna in order to see whether patterns that may appear to be present in the hominins make sense in terms of larger-scale patterning. The investigation by Turner and Wood (1993) extended to include just such a larger patterning in eastern versus southern African taxa and concluded that there was evidence for a high degree of regional differentiation in some families, particularly the Bovidae, coupled with evidence for significant dispersals in others. Among the Primates, the papionin monkeys appeared to show the most evidence for dispersals, and overall, it was apparent that regional isolation was not a matter of rigid demarcation. The implications of this for our understanding of hominin biogeography are that regionally restricted taxa would be a plausible interpretation of the material to hand, but that movements between regions are likely to have occurred and that identified genera such as Australopithecus and Paranthropus with differing species in each regions are indeed likely to be monophyletic. If monophyly is a correct interpretation, then a localized origin with subsequent dispersals is likely to have been the dominant pattern (Turner and Paterson 1991; Turner 1999a). The known distribution of Pliocene and perhaps Late Miocene hominin remains now stretches from Chad down through eastern Africa to South Africa, perhaps even from the Atlantic coast of the western Sahel down to the Cape as Brunet et al. (1995) argued, and any reasonable interpretation of that pattern would recognize it as a minimal statement of range. But how much the gaps in between known localities were filled in, or the limits of distribution extended, remains unknown. Artifactual evidence from northwestern Africa may indicate the presence of hominins with Oldowan tools as early as the Olduvai event (Sahnouni and van der Made 2009), but the best evidence appears to date from around 1.0 Ma (Raynal et al. 2001). Dennell (2004) has even suggested that if Pliocene hominins were in Chad some 2,500 km west of the Rift Valley by 3.5 Ma then why not as far to the north or east by the same period? This, of course, would place them in southwestern Asia.

Out of Africa The number, timing, and direction of earliest hominin dispersals from Africa have long been a major point of discussion, and opinions on these topics remain varied and contentious (Rolland 1998; Turner 1999b; Bar-Yosef and Belfer-Cohen 2001; Strauss 2001; Villa 2001; Dennell 2004, 2009; Abbate and Sagri 2012). Early Pleistocene assemblages from ‘Ubeidiya in Israel dated to around 1.5 Ma (Belmaker et al. 2002), perhaps Pakistan by 1.8 Ma (Dennell 2004), Iberia by 1.4 Ma (Oms et al. 2000; Toro-Moyano et al. 2013) and human material from Dmanisi in Georgia dated around 1.8 Ma (Lordkipanidze et al. 2013) set a minimal date for the original movement. Dispersals Page 7 of 19

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_15-3 # Springer-Verlag Berlin Heidelberg 2013

to eastern parts of Asia remain more contentious (see Dennell (2009) for review), with the best evidence so far from 1.66 Ma deposits with stone implements and what is interpreted as stone-tool processing of animal carcasses at Majuangou in the Nihewan Basin of northern China (Zhu et al. 2004). The stone tools resemble primitive Oldowan items found in African deposits, and the authors argue for a significant and flourishing early dispersion from Africa, although the rest of the mammalian fauna has no clear African elements. Hominin occupation appears to have been more extensive and intensive in Europe in particular and Eurasia in general after 0.5 Ma with a long tail of more sporadic appearances back into the Early Pleistocene (Turner 1999b; Roebroeks 2001), although Martı´nez et al. (2010) suggested that occupation in Iberia may have been continuous from the latest Early Pleistocene. But which route, or routes, was used? Several have been proposed – land across Sinai and the Levant, across the Bab el-Mandeb Straits at the south of the Red Sea and then across the Arabian Peninsula proper, or by the Gibraltar Straits? Here the evidence is reviewed from a faunal perspective, but see Abbate and Sagri (2012) for further information on the geomorphology.

Gibraltar Although the evidence available points to some part of the Arabian Peninsula as the most probable route for Plio-Pleistocene hominin dispersions, a route across the Gibraltar Straits has frequently been proposed. For example, Rolland (1998) argued for a reduction of the seaway through the Straits to 8 km during glacial maxima, without any increase in surface current and for sweepstakelike movements, especially during OI Stages 12 and 16. Flemming et al. (2003) argued that the Strait itself would not have narrowed significantly during sea-level falls, although they pointed out that now submerged areas to the west of the Strait would have formed substantial islands that might have provided “stepping stones.” Strauss (2001, p. 99) offered a thoughtful analysis of the issue but concludes that the record for human contacts is “at best spotty and ambiguous.” As far as other routes across the Mediterranean are concerned, particularly between Tunisia and Sicily, Flemming et al. (2003) reached no conclusion, and it is not evident that such possible routes have any strong scientific support. Villa (2001) provides a useful summary of some of the arguments and rejects the idea of such routes. As summarized elsewhere (O’Regan et al. 2006), among the extant and Holocene terrestrial mammals present in North Africa and Iberia, such as wild boar (Sus scrofa), red deer (Cervus elephas), otter (Lutra lutra), and the red fox (Vulpes vulpes), there are none that are not also present in the Levant. This suggests that these animals took a circum-Mediterranean route rather than crossing the Gibraltar Straits (Dobson 1998), although of course, the possibility of some individual animals swimming across cannot be completely ruled out. Some bat species are found on both sides of the Straits and further eastward in Europe but are not recorded in the Levant or elsewhere in North Africa, which could imply dispersion across the Gibraltar Straits (Dobson and Wright 2000). However, the extent to which recent human interference has played a part remains a concern, and of the 17 terrestrial mammal species inhabiting North Africa today only four are considered to have a natural circum-Mediterranean distribution, whereas the rest are thought to be recent introductions (Dobson 1998). Clearly, if populations of H. sapiens were capable of dispersing over substantial bodies of water to reach Australia in the Late Pleistocene (Bowler et al. 2003), then it is also possible that they may have been moving around the Mediterranean and transporting animals prior to the Holocene, a point stressed by Strauss (2001). However, the Gibraltar Straits cannot be shown convincingly to have been the scene of natural Pliocene, Pleistocene, or even Holocene movements of terrestrial mammals (with the possible exception of the hippopotamus (O’Regan 2008)) and thus

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the Arabian Peninsula remains the only established route of a two-way movement between continents.

Arabia In contrast, the possibility of hominin dispersions through the Arabian Peninsula and the Levant, either across the Sinai Peninsula or the Bab el-Mandeb Straits at the south of the Red Sea, is indicated by the mixed Afro-Eurasian nature of the fauna of the region since the later part of the Pliocene and in particular by the Early Pleistocene deposits at ‘Ubeidiya in Israel (Tchernov 1992; Belmaker et al. 2002; Belmaker 2010a). Later Pliocene African elements, chiefly bovids and giraffids, are known to the north of the Taurus-Zagros mountain chain that borders the northern boundaries of the Arabian Peninsula at localities such as Kuabebi in the Caucasus and Wolacks in Greece (Sickenberg 1967), the Oltet Valley in Romania (Radulesco and Samson 1990), and Hue´lago in southern Spain (Alberdi et al. 2001). However, many of these taxa have now been reinterpreted as Miocene relicts rather than African immigrants, leaving relatively little evidence for Late Pliocene and Early Pleistocene African dispersals (Agustı´ et al. 2009; Agustı´ and Lordkipanidze 2011). Reviews of faunal dispersal both into and out of Africa between 3.0 and 0.5 Ma can be found in O’Regan et al. (2011) and Martinez-Navarro (2010). The evidence for African faunal elements at Dmanisi has recently been reviewed and largely discounted by Agustı´ and Lordkipanidze (2011); while at ‘Ubeidiya the African faunal affinities were based on an undetermined giraffid, the bovids Pelorovis oldowayensis and Oryx sp., the hippo Hippopotamus gorgops, the suid Kolpochoerus olduvaiensis, and a number of carnivores including the spotted hyaena, Crocuta crocuta and possibly the honey badger cf. Mellivora sp. (Tchernov 1992; Belmaker 2010). The Acheulean industry at ‘Ubeidiya is unknown at Dmanisi and appears to have developed in Africa at a slightly later date. Other Early Pleistocene localities in Europe have relatively few African species. Much has been made of the appearance of the cercopithecine Theropithecus cf. T. oswaldi at Cueva Victoria in southeastern Spain (Gibert et al. 1995), and possibly at Pirro Nord in Italy (Rook et al. 2004) and ‘Ubeidiya (Belmaker 2010b), and of the African machairodont cat, Megantereon whitei, at Venta Micena, Dmanisi and the Greek locality of Apollonia (Martı´nez-Navarro and Palmqvist 1995, 1996; Palmqvist et al. 2007). The Hippopotamus, is also present at several Early Pleistocene sites such as ‘Ubeidiya and Venta Micena (O’Regan et al. 2006, 2011). Overall, the suggestions of possible hominin dispersions into Eurasia during the very earliest Pleistocene that appear in the literature from time to time (Bonifay and Vandermeersch 1991; Boitel et al. 1996), while unsupported by critical assessments of the evidence within Eurasia, cannot be dismissed a priori as impossible or even unlikely. These conclusions parallel some of those reached by Mithen and Reed (2002) in their computer simulation of dispersals and stressed elsewhere (Dennell 1998, 2004). If recent arguments summarized earlier about the status of later Pliocene species referred to the genus Homo are correct, then clearly the earliest hominin to have moved out of Africa would not have been a member of our own genus. However, whether such a view offers support for an extra-African origin for H. erectus remains unclear, particularly as the latest data from Dmanisi appear to demonstrate that the cranio-dental morphological variability seen in Homo erectus, H. ergaster, and H. georgicus are all present within the specimens from this single locality (Lordkipanidze et al. 2013; see also Baab, ▶ Defining Homo erectus this volume; and Tattersall, ▶ Homo ergaster and Its Contemporaries this volume).

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Precise routes If Arabia is indeed the only plausible route out of Africa for terrestrial mammals during the PlioPleistocene, it remains difficult to judge the relative contributions of the Sinai versus the Bab elMandeb as gateways. While knowledge of the Middle Paleolithic or later Middle Pleistocene hominin occupation of Arabia is rapidly improving (e.g., Crassard et al. 2013), there is still a relative paucity of evidence for Lower Paleolithic occupation (Petraglia and Alsharekh 2004). However, as Petraglia (2003) also showed, both Oldowan and Acheulean assemblages are known, and the eastern side of the Bab el-Mandeb Straits in particular appears to have been occupied by hominins with this technology. Unfortunately, the absence of good chronological control remains a major obstacle to assess the pattern of lithic assemblage distribution. As Petraglia and Alsharekh (2004) show, while movement across Sinai offers the possibility of movement along the Levant and then perhaps south into Northern Arabia either along the eastern Red Sea Coast or inland behind the highlands of the Hejaz Asir, movement across Bab el-Mandeb confronts any dispersing population directly with the highlands. These would tend to restrict movement to the coastal strips, north along the eastern Red Sea Coast or east along the Arabian Sea Coast. While annual rainfall today in the Hejaz Asir or in the Oman Mountains at the easternmost corner of the Peninsula can reach well over 100 mm, much of the southeastern portion, the Rub Al Khalil or Empty Quarter, may have no more than 50 mm with temperatures that exceed 50  C (Glennie and Singhvi 2002). The fact that Lower and Middle Paleolithic occupation did occur means of course that conditions were sometimes favorable, and substantial river systems appear to have existed certainly by MIS 5 (Crassard et al. 2013), but lack of evidence hampers interpretation of the earliest hominin dispersals. Little is known of the Plio-Pleistocene fauna of Arabia, which is even more sparsely represented than that of the Miocene. The sole exceptions are the small assemblages from An Nafud in northern Saudi Arabia, thought to be of Early Pleistocene age (Thomas et al. 1998) and which, with spotted hyaena, hexaprotodont hippo, horse, elephant (cf. Elephas recki), several bovids including a species of Pelorovis as well as crocodile and fish, are of distinctly African stamp. The range of species implies good grassland and standing water in the vicinity, an interpretation supported by isotopic analyses of herbivore teeth. However, as Glennie and Singhvi (2002) also point out, increased aridity is indicated during glacial periods, beyond even that seen today despite the fact that temperatures may have averaged somewhat lower, and this factor presumably played a large part in determining the extent to which mammals, including early hominins, could maintain any occupation throughout the Pleistocene. Current data indicate that these periods of aridity are related to the deposition of Aeolian sands over at least the last 0.2 Ma (Preusser 2009). Glacial periods with related sea-level changes are of course precisely the point at which the Bab el-Mandeb crossing is likely to have been at its most obvious and navigable to early hominins (Rohling et al. 1998; Cachel and Harris 1998), so that the easiest and most attractive access by that route is likely to have been at a point when conditions in southern Arabia, and for that matter on the corresponding coastal area of Africa, are likely to have been least appealing. Taken overall, the Bab el-Mandeb Straits do not seem likely to have offered a likely gateway out of Africa for terrestrial mammals during the Lower and Middle Pleistocene, suggesting that movement across Sinai and then northward along the Levant, southward into Arabia, or eastward and beyond is the most plausible route. However, movement across the Bab el-Mandeb during the later Pliocene, before the Straits had fully formed, and thus before the crossing into Arabia was dependent on sea-level fall, may have been an entirely different matter, as previously pointed out (Turner 1999b). The importance of the Afar region of Africa to the south and west of Bab el-Mandeb as an area of attractive resources for mammals, including hominins, following rivers into the developing depression as rifting progressed from Miocene times onward Page 10 of 19

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was highlighted by Kalb (1995, p. 366), who stressed “the step-by-step process of animal migrations into and dispersal across inter-continental areas prior to complete plate separation.”

Conclusions It seems clear that the wider context of movements between Africa and Eurasia throws useful light on the patterns of dispersion within Primates in general and Hominoidea in particular so that changes in primate distribution can be examined without having to treat them as a special case. In the earliest stages of the Oligocene and Early Miocene, we see that movements into Africa are accompanied by a range of other taxa. If dryopithecine apes first moved back into Europe during the Mid-Miocene and then back again into Africa toward the end of that epoch, then they did so as part of a much wider dispersal across a range of mammalian orders. Current knowledge of Pliocene hominins is at best incomplete, and while recent discoveries have extended the range of named species, they have done little to clarify the likely relationships between those taxa or the true nature of distributions. With the greater number of putative taxa now available, it will require some considerable time and quite a few more discoveries before real sense can be made of the patterns. However, as far as movement out of Africa by hominins is concerned, a number of points can be made. The Gibraltar Straits are unlikely to have been the site of any Pliocene or Pleistocene gateway for terrestrial mammals, and while movement across the Bab el-Mandeb region before the Red Sea opened fully toward the end of the Pliocene may have been possible, dispersal across the Straits once the glacial and interglacial cycle got underway seems to us unlikely. Sinai and the Levant, the scene of a two-way faunal movement between continents during the latest Pliocene and earliest Pleistocene, remains the only established route. Moreover, the diversity of elements using that gateway points to the relatively hospitable nature of the area in the Earliest Pleistocene, so that suggestions of possible hominin dispersions into Eurasia during this period are not inherently implausible. However, how long any dispersing populations were able to maintain their extended range is entirely another question. Early hominin movements into Arabia and the Levant may have been sporadic, and probably tenuous and subsequent movements out into Eurasia proper were probably even more so.

Cross-References ▶ Defining Homo erectus ▶ Defining the Genus Homo ▶ Dispersals of Early Humans: Adaptations, Frontiers, and New Territories ▶ Fossil Record of Miocene Hominoids ▶ The Biotic Environments of the Late Miocene Hominids ▶ The Earliest Putative Homo Fossils ▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments ▶ The Species and Diversity of Australopiths

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Raynal JP, Sbihi Alaoui FZ, Geraads D, Magoga L, Mohi A (2001) The earliest occupation of North-Africa: the Moroccan perspective. Q Int 75:65–75 Roebroeks W (2001) Hominid behaviour and the earliest occupation of Europe: an exploration. J Hum Evol 41:437–461 Ro¨gl F (1999) Mediterranean and Paratethys palaeogeography during the Oligocene and Miocene. In: Agusti Rook J, Andrews P (eds) The evolution of terrestrial ecosystems in Europe. Cambridge University Press, Cambridge, pp 8–22 Rohling EJ, Fenton M, Jorisson FJ, Bertrand P, Garissen G, Caulet JP (1998) Magnitudes of sealevel lowstands of the past 500,000 years. Nature 394:162–165 Rolland N (1998) The Lower Palaeolithic settlement of Eurasia, with special reference to Europe. In: Petraglia MD, Korisettar R (eds) Early human behaviour in global context. Routledge, London, pp 187–220 Rook L, Martı´nez-Navarro B, Howell FC (2004) Occurrence of Theropithecus sp. in the Late Villafranchian of Southern Italy and implication for Early Pleistocene “out of Africa” dispersals. J Hum Evol 47:267–277 Sahnouni M, van der Made J (2009) The Oldowan in North Africa within a biochronological framework. In: Schick K, Toth N (eds) The cutting edge: new approaches to the archaeology of human origin. Stone Age Institute Press, Gosport, pp 179–210 Seiffert E, Simons EL, Fleagle JG, Godinot M (2010) Paleogene anthropoids. In: Werdelin L, Sanders WJ (eds) Cenozoic mammals of Africa. University of California Press, Berkeley, pp 369–391 Semaw S, Rogers MJ, Quade J, Renne PR, Butler RF, Dominguez-Rodrigo M, Stout S, Hart WS, Pickering T, Simpson SW (2003) 2.6-Million-year-old stone tools and associated bones from OGS-6 and OGS-7, Gona, Afar, Ethiopia. J Hum Evol 45:169–177 Semaw S, Simpson SW, Quade J, Renne PR, Butler RF, McIntosh WC, Levin N, DominguezRodrigo M, Rogers M (2005) Early Pliocene hominids from Gona, Ethiopia. Nature 433:301–305 Senut B, Pickford M, Gommery D, Mein P, Cheboi K, Coppens Y (2001) First hominid from the Miocene (Lukeino Formation, Kenya). C R Acad Sci Paris 332:137–144 Sickenberg O (1967) Die unterpleistoza¨ne Fauna von Wolaks (Griechenland-Mazedonien). I. Eine neue Giraffe (Macedonitherium martinii nov. gen., nov. spec.) aus dem unteren Pleistoza¨ne von Griechenland. Ann de Ge´ol Pays Helle´niques 18:34–54 Solounias N, Plavcan JM, Quade J, Witmer L (1999) The paleocecology of the Pikermian biome and the savanna myth. In: Agustı´ J, Rook L, Andrews P (eds) Hominoid evolution and climatic change in Europe, vol 1, The evolution of Neogene terrestrial ecosystems in Europe. Cambridge University Press, Cambridge, pp 436–453 Strauss LG (2001) Africa and Iberia in the Pleistocene. Q Int 75:91–102 Tabuce R, Asher RJ, Lehmann T (2008) Afrotherian mammals: a review of current data. Mammalia 72:2–14 Tabuce R, Marivaux L, LeBrun R, Adaci M, Bensalah M, Fabre PH, Fara E, Rodrigues HG, Hautier L, Jaeger J-J, Lazzari V, Mebrouk F, Peigne´ S, Sudre J, Tafforeau P, Valentin X, Mahboubi M (2009) Anthropoid versus strepsirhine status of the African Eocene primates Algeripithecus and Azibius: craniodental evidence. Proc R Soc B 276:4087–4094 Tchernov E (1992) Eurasian-African biotic exchanges through the Levantine corridor during the Neogene and Quaternary. In: von Koenigswald W, Werdelin L (eds) Mammalian migration and dispersal events in the European Quaternary, vol 153. Courier Forschung-Institut Senckenberg, Frankfurt am Mein, pp 103–23 Page 16 of 19

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Thomas H, Gerrards D, Janjou D, Vaslet D, Memesh A, Billiou D, Bocherens H, Dobigny G, Eisenmann V, Gayet M, de Lapparent de Broin F, Petter G, Halawani M (1998) First Pleistocene faunas from the Arabian Peninsula: an Nafud desert, Saudi Arabia (De´couverte des premie`res faunes ple´istoce`nes de la pe´ninsule arabique dans le de´sert du Nafoud, Arabie Saoudite). C R Acad Sci Paris 326:145–152 Toro-Moyano I, Martı´nez-Navarro B, Agustı´ J, Souday C, Bermu´dez de Castro JM, Martino´nTorres M, Farfardo B, Duval M, Falgue`res C, Oms O, Pare´s JM, Anado´n P, Julia` R, Garcı´aAguilar JM, Moigne A-M, Espigares MP, Ros-Montoya S, Palmqvist P (2013) The oldest human fossil in Europe, from Orce (Spain). J Hum Evol 65:1–9 Turner A (1995) Plio-Pleistocene correlations between climatic change and evolution in terrestrial mammals: the 2.5 Ma event in Africa and Europe. Acta Zool Cracov 38:45–58 Turner A (1999a) Evolution in the African Plio-Pleistocene mammalian fauna. In: Bromage T, Schrenk F (eds) African biogeography, climatic change and early hominid evolution. Oxford University Press, New York, pp 369–399 Turner A (1999b) Assessing earliest human settlement of Eurasia: Late Pliocene dispersions from Africa. Antiquity 73:563–570 Turner A, Anto´n M (1999) Climate and evolution: implications of some extinction patterns in African and European machairodontine cats of the Plio-Pleistocene. Estud Geol 54:209–230 Turner A, Anto´n M (2004) Evolving Eden. An illustrated guide to the evolution of the African large mammal fauna. Columbia University Press, New York Turner A, Paterson HEH (1991) Species and speciation: evolutionary tempo and mode in the fossil record reconsidered. Geobios 24:761–769 Turner A, Wood B (1993) Taxonomic and geographic diversity in robust australopithecines and other African Plio-Pleistocene mammals. J Hum Evol 24:147–168 Vignaud P, Duringer P, Mackaye HT, Likius A, Blondel C, Boisserie JR, de Bonis L, Eisenmann V, Etienne ME, Geraads D, Guy F, Lehmann T, Lihoreau F, Lopez-Martinez N, Mourer-Chauvire C, Otero O, Rage JC, Schuster M, Viriot L, Zazzo A, Brunet M (2002) Geology and palaeontology of the Upper Miocene Toros-Menalla hominid locality, Chad. Nature 418:152–155 Villa P (2001) Early Italy and the colonization of Western Europe. Q Int 75:113–130 Vrba ES (1995) The fossil record of African antelopes (Mammalia, Bovidae) in relation to human evolution and paleoclimate. In: Vrba ES, Denton GH, Partridge TC, Burckle LH (eds) Paleoclimate and evolution with emphasis on human origins. Yale University Press, New Haven, pp 385–424 Werdelin L, Turner A (1996) The fossil and living Hyaenidae of Africa: present status. In: Stewart K, Seymour K (eds) The palaeoecology and palaeoenvironments of Late Cenozoic mammals: tributes to the career of C.S. Churcher. Toronto University Press, Toronto, pp 637–659 White TD (1995) African omnivores: global climatic change and Plio-Pleistocene hominids and suids. In: Vrba ES, Denton GH, Partridge TC, Burckle LH (eds) Paleoclimate and evolution with emphasis on human origins. Yale University Press, New Haven, pp 369–385 White TD, Suwa G, Asfaw B (1994) Australopithecus ramidus, a new species of early hominid from Aramis, Ethiopia. Nature 371:306–312 White TD, Suwa G, Asfaw B (1995) Australopithecus ramidus, a new species of early hominid from Aramis, Ethiopia. Corrigendum. Nature 375:88 White TD, WoldeGabriel G, Asfaw B, Ambrose S, Beyene Y, Bernor RL, Boisserie J-R, Currie B, Gilbert H, Haile-Selassie Y, Hart WK, Hlusko K, Howell FC, Kono RT, Lehmann T, Louchart

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A, Lovejoy CO, Renne PR, Saegusa H, Vrba ES, Wesselman H, Suwa G (2006) Asa Issie, Aramis and the origin of Australopithecus. Nature 440:883–889 Whybrow PJ, Clements D (1999) Arabian Tertiary fauna, flora, and localities. In: Whybrow PJ, Hill A (eds) Fossil vertebrates of Arabia. Yale University Press, New Haven, pp 460–473 WoldeGabriel G, White TD, Suwa G, Renne P, de Heinzelin J, Heiken WK (1994) Ecological and temporal placement of early Pliocene homininds at Aramis, Ethiopia. Nature 371:330–333 Wood BA (1991) Koobi Fora research project, vol 4, Hominid cranial remains. Clarendon, Oxford Wood BA (1992) Origin and evolution of the genus Homo. Nature 355:783–790 Wood B, Baker J (2011) Evolution in the genus Homo. Annu Rev Ecol Evol Syst 42:47–69 Wood BA, Collard M (1999) The human genus. Science 284:65–71 Zhu RX, Potts R, Xie F, Hoffman KA, Deng CL, Shi CD, Pan YX, Wang HQ, Shi RP, Wang YC, Shi GH, Wu NQ (2004) New evidence on the earliest human presence at high northern latitudes in northeast Asia. Nature 431:559–562

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Index Terms: African Pliocene hominini_5 Australopithecus_6–7 Bab el-Mandeb Straits_2 Hominidae_4 Hominoidea_1, 3 Miocene_3–4 Paranthropus_6–7 Pliocene hominini_5 Primates_2 ZoogeographyBab el-Mandeb_10 Zoogeography_1–2, 4–5, 8–10 Zoogeography African Pliocene hominini_5 Zoogeography Arabia_9 Zoogeography Bab el-Mandeb Straits_10 Zoogeography Gibraltar straits_8 Zoogeography hominidae_4 Zoogeography primates_2

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_16-3 # Springer-Verlag Berlin Heidelberg 2013

Patterns of Diversification and Extinction Walter Etter* Abteilung Geowissenschaften, Naturhistorisches Museum Basel, Basel, Switzerland

Abstract The history of life on Earth, from the earliest microscopic cells to the modern world populated by the rich variety of animals, plants, fungi, and microbes, is more than 3,500 Myr long. Documenting the diversity patterns through the Proterozoic and Phanerozoic has been a major task in the past decades and is fraught with many methodological problems. The emerging picture is one of a very irregular increase in diversity. The most significant episodes of diversification occurred during the Cambrian–Ordovician and throughout the Mesozoic–Cenozoic. In the Phanerozoic alone, 5 major and more than 15 smaller mass extinctions disrupted the diversification of life and sometimes drastically altered the way of evolution. There was no common cause for these events, but all were the consequence of large‐scale environmental perturbations. There is growing concern that we are currently entering a “Sixth” major extinction, caused by human impact on nature.

Introduction This chapter reviews the history of diversity, the “ups and downs” of life, during the past 3,500 Myr. There are many reasons why the history of life’s diversity on Earth is an important avenue of paleontological research. (1) Such studies can give us insight into the relative importance of various mechanisms of evolution. (2) The analysis of diversification and extinction can help to clarify the respective roles of biotic (intrinsic) versus abiotic (extrinsic) factors. (3) The importance of regional versus global patterns/mechanisms can be investigated. (4) The analysis of extinctions might enable us to see if there are common patterns. (5) The possibility that Homo sapiens is causing yet another mass extinction fosters interest in other such events in the geological past. One emergent theme when documenting patterns of diversification and extinction is that the major disruptions/discontinuities were not the consequence of some lineages’ “racial senility” or “genetic exhaustion” but rather caused by large‐scale environmental perturbations. The world as we know it today, with its current climatic and atmospheric conditions and present‐day biosphere, is not a good actualistic example for the remote past, where sea levels and mean annual temperatures were vastly fluctuating, continental plates had entirely different positions, and CO2 and O2 levels in the atmosphere showed secular changes.

*Email: [email protected] *Email: [email protected] Page 1 of 60

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This chapter is organized as follows: • First, an overview of major events in the history of life is given, together with an overview of changes in abiotic conditions. Here some emphasis is placed on the Precambrian. • The patterns of diversification of Phanerozoic life are reviewed, most extensively for marine animals with preservable hard parts. • Methodological problems in documenting diversity (as a measure of taxonomic richness) through time are discussed. • In a special subchapter, some of the most important radiations and extinctions are treated in stratigraphic order.

A Short History of Life on Earth According to the newest dating, the Earth is 4,567 Myr old (Fig. 1; Van Kranendonk 2012). Already ~4,500 Myr ago, the planet experienced probably its most dramatic event: the impact of the marssized protoplanet “Theia” led to the formation of the moon (Taylor 2007). Between 4,500 and 4,400 Myr ago, the Earth changed from a planet with a liquid magmatic surface to one with a solid surface. Some detrital zircon grains from the Jack Hills in Australia are up to 4,400 Myr old, and their composition might indicate that liquid water and a thin crust were already present at that early date (Wilde et al. 2001; Van Kranendonk 2012). The oldest rocks currently recognized (Acasta gneiss from the Northwest Territories, Canada) are dated as 4,030 Myr (Nelson 2004). The earliest Eon of Earth history, the Hadean, thus left no directly observable documents. It is nowadays assumed that the initially high temperatures following the accretion of the Earth had dropped by around 4,400–4,000 Myr ago to below 100
C. During the earliest Archean, the surface temperature was probably quite low (faint early sun). By that time, liquid water was present on the Earth’s surface, brought to the planet by icy asteroids (Kramers 2007). Yet, the “heavy bombardment” with bodies exceeding 250 km in diameter lasted until 3,800 Myr ago (Late Heavy Bombardment (LHB) between 3,900 and 3,800 Myr ago; Van Kranendonk 2012). This must have led to repeated boiling of the oceans and the vaporization of their water (Nisbet and Sleep 2001, 2003). Contrary to earlier beliefs (e.g., those assumed in the famous Miller experiment), most researchers today think that the Hadean and Early Archean atmosphere was only mildly reducing, with mainly CO2 and N2 present but also smaller amounts of CH4, NH3, and H2 (McClendon 1999; Raven and Skene 2003; McCollom 2013). Free oxygen perhaps built through photodissociation of water vapor in the upper atmosphere, but quickly reacted with Fe2+ and other unoxidized compounds. The early atmosphere was therefore devoid of free oxygen (McClendon 1999; Miller and Lazcano 2002; Westall 2012). Under these conditions life originated (for reviews, see Oró et al. 1990; Brack 1998; McClendon 1999; Fenchel 2002; Taylor 2005; Deamer 2011; Westall 2012). Organic compounds could form in the atmosphere through UV‐photolysis, electrical discharges, and major impact shocks (McClendon 1999; Lazcano 2001; McCollom 2013), and a major source of organic molecules was probably also comets and interplanetary dust (Lazcano 2001; Miller and Lazcano 2002). But early life certainly evolved in the sea (Raven and Skene 2003; Westall 2012). It is now widely assumed that an RNA world preceded life based on proteins and DNA (Lilley and Sutherland 2011; Gargaud et al. 2012). The first cells were probably heterotrophs (Lazcano and Miller 1996; Peretó 2011; but see Huber and Wächtershäuser 1997; Wächtershäuser 2000, 2006). As possible sites where cellular life evolved Page 2 of 60

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Fig. 1 Major events in earth history in the Precambrian (Modified after various sources)

from prebiotic precursors, continental thermal springs, volcanic vents, warm hypersaline lagoons (Darwin’s “warm little pond”), and deep submarine vents are the most likely candidates (Schopf 1999; Westall 2012). In this respect it is noteworthy that the earliest branches of both the Archaea and Bacteria are thermophilic (Pace 1997). Yet, an extraterrestrial origin of cellular life cannot totally be excluded (“Panspermia”; Horneck 2003). Perhaps life originated sequentially several times, but was always exterminated by the heavy meteorite bombardment (“impact frustration”; Schopf 2002). Yet, all life on Earth shares a common origin (Theobald 2010). The “Last Universal Common Ancestor” (LUCA) might have been a diverse community of cells that experienced extensive horizontal gene transfer (Woese 1998, 2002; Glansdorff et al. 2008). Organismal lineages established themselves with the subsequent Page 3 of 60

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splitting into the three domains “Bacteria”, “Archaea,” and “Eukarya” (Woese 1998). The tree of life is thus at its base a web (Doolittle 1999) or even a ring (Rivera and Lake 2004). The fossil record of the Archean is notoriously sparse. The presumed oldest cellular microfossils come from 3,500- to 3,450-Myr-old sediments in Western Australia (Schopf 1992a, 1993, 2004, 2006; Van Kranendonk et al. 2008; De Gregorio et al. 2009; Schopf and Kudryavtsev 2012; but see Brasier et al. 2004; Wacey 2009; Wacey et al. 2009). Almost as old (3,400–3,200 Myr) are microfossils in the metasediments of the Onverwacht and Fig tree groups (South Africa). Putative microfossils (Isuasphaera) were described (Pflug 1978) from even older (3,800 Myr) metamorphosed sedimentary rocks from Greenland (Isua Greenstone Belt) but are probably of inorganic origin (Bridgwater et al. 1981; Appel et al. 2003). According to most authors (Mooers and Redfield 1996; Sheridan et al. 2003; Hedges 2009), the split between bacteria and archaea–eukaryota must have occurred more than 3,500 Myr ago. The Proterozoic fossil record (Hofmann and Schopf 1983; Mendelson and Schopf 1992; Schopf 1992a, b) documents an increasing diversification and complexity of cells, but the evolution of metabolic pathways cannot be deduced from the morphology of the microfossils. Yet, by 2,700 Myr ago, oxygenic photosynthesis, methanogenesis, and methylotrophy had probably developed, perhaps also sulfate reduction and nitrogen fixation (Buick 2001; Sleep and Bird 2007; Copley and Summons 2012). In contrast to cellular fossils, the record of stromatolites is quite good. These are biosedimentary structures built by microbial mats which trap sediment particles (Riding 1991, 2000; Walter 2001; Bosak et al. 2013). The oldest stromatolites date from 3,500- to 3,200-Myr-old sediments in Australia and South Africa (Wacey 2009; Van Kranendonk 2012), but their fossil record remains spotty until the Neoarchean (Walter 1983, 2001; Grotzinger and Knoll 1999). They diversified considerably in the Proterozoic, and in the Mesoproterozoic a large number of different types had developed, growing sometimes to impressive sizes (Awramik and Sprinkle 1999; Walter 2001; Riding 2006a). Stromatolites declined both in diversity and abundance in the terminal Proterozoic, and in the Phanerozoic they remained largely restricted to marginal marine environments (Riding 2006a, b). This decline was traditionally seen as a consequence of the rise of the metazoans, which consumed the microbial mats (Mata and Bottjer 2012), but it might also have abiotic reasons (Awramik and Sprinkle 1999; Riding 2006a, b). Significant changes in the carbon and sulfur isotope signatures of rock and kerogen samples in the latest Archean between 2,750 and 2,500 Myr ago point to increased microbial productivity and rapid crust formation. For some time, biological and geological processes were out of equilibrium (Van Kranendonk 2012). Between 2,400 and 2,200 Myr ago, the atmosphere changed rather abruptly from reducing (pO2 < 0.01 % present atmospheric level PAL) to oxidizing (pO2 > 1 % PAL; Fig. 1), largely as a result of the activities of oxygenic photoautotrophs (Schopf 1992a; Holland 1994; Canfield 2005; Van Kranendonk 2012; for alternative scenarios of atmosphere evolution, see Ohmoto et al. 2004). This is known as the “Great Oxidation” in the Early Proterozoic (Goldblatt et al. 2006). Until about 2,400 Myr ago, free oxygen was constantly removed by oxidation of weathered reduced minerals (Nisbet and Sleep 2001; Lenton 2003; Goldblatt et al. 2006). Detrital pyrite and uraninite are common until 2,200 Myr ago and indicate still very low levels of free oxygen; otherwise these minerals would have been oxidized (Schopf 1992a; Holland 1994). Likewise, the genesis of banded iron formations (BIFs), which are absent in rocks younger than 1,700 Myr, requires reducing conditions in the deeper parts of the seas (Simonson 2003; Van Kranendonk 2012). From 2,450 to 2,200 Myr ago, the Earth witnessed the first well‐documented ice age, the “Huronian” or Makganyene glaciation (Pierrehumbert et al. 2011). As a consequence of insufficient Page 4 of 60

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time resolution, the exact duration of glacial intervals during this Paleoproterozoic time period is unknown (Young 2004; Van Kranendonk 2012). The onset and the termination seem to have been gradual (Young 2004). Perhaps the increase in atmospheric oxygen was the cause of the Huronian glaciation (Kopp et al. 2005). If methane was a major contributor to a greenhouse effect prior to that time, it would have been oxidized in a more oxygen‐rich atmosphere, and the removal of this greenhouse gas could well have led to global cooling and the onset of an ice age. However, the causes of the Early Proterozoic glaciation are still debated (Van Kranendonk 2012). The origin of the eukaryotes can be placed at some time before 2,100 Myr ago. Large and unquestionably eukaryotic acritarchs are known from 1,800-Myr-old rocks (Lamb et al. 2009), and the macroscopic “algae” Grypania is most likely also a eukaryote, putting the oldest eukaryotic record to 2,100 Myr (Han and Runnegar 1992). Eukaryote-specific biomarkers were even reported from 2,700-Myr-old metasediments of Western Australia (Brocks et al. 1999) but proved to be contaminants (Fischer 2008). Perhaps the origin of eukaryotes was linked to the increased oxygen content of the atmosphere and shallow waters where a nucleus and its protective membrane would be advantageous (Dyer and Obar 1994). Subsequent evolution of the eukaryotes took place by serial endosymbiosis (Margulis 1981) in which engulfed a‐purple bacteria became mitochondria and cyanobacteria became plastids (Dyer and Obar 1994; Pace 1997). In part, even secondary and tertiary endosymbiosis must have occurred in which photosynthetic eukaryotes were engulfed by nonphotosynthetic eukaryotes (Woese et al. 1990; Chan and Bhattacharya 2010). Little is known about the early evolution of the eukaryotes (Knoll et al. 2006). Apart from the acritarchs that are a heterogeneous assemblage of planktonic, unicellular eukaryotes known from the Late Paleoproterozoic and extending into the Phanerozoic (Martin 1993; Knoll 1994), other fossils of the eukaryotic clade include various carbonaceous films that are not easy to interpret (Hofmann 1994; Knoll et al. 2006). Judged from isotopic signatures and sedimentologic features, between 1,800 and 800 Myr ago was a time of environmental stability that has been dubbed “the boring billion” or “Earth’s dullest period of time” (Buick et al. 1995). Yet, this was also the time of formation of the supercontinent Rodinia and of major diversification of eukaryotes (Van Kranendonk 2012). New molecular dates, which are in reasonable agreement with paleontological findings, give some clues as to when new groups originated. The divergence between protists and crown‐group plants may be as young as 1,300–1,100 Myr, the origin of the fungi is placed at 1,200–1,000 Myr ago, the split between choanoflagellates and eumetazoans occurred 1,000–900 Myr ago, and the first bilaterians made their appearance 900–700 Myr ago (Douzery et al. 2004; see also Peterson et al. 2004, 2008; Peterson and Butterfield 2005; Bhattacharya et al. 2009; Blair 2009; Erwin et al. 2011). Between 800 and 600 Myr ago in the Cryogenian period, the Earth witnessed several large glaciations. The last two episodes are well dated. The Sturtian glaciation occurred around 715 Myr ago and the Marinoan (“Varanger”) glaciation around 635 Myr ago (Allen and Hoffman 2005; Pierrehumbert et al. 2011; Shields-Zhou and Och 2011). Some, perhaps most, continental land masses had near-equatorial positions at that time. Glaciers might have reached equatorial regions and perhaps extended down to the sea level. According to the most dramatic scenario (Hoffman et al. 1998; Hoffman and Schrag 2002; Hoffman 2009; but see Chandler and Sohl 2000; Poulsen 2003), temperatures initially dropped due to some unknown mechanism, but as soon as glaciers reached a critical extension in low latitudes, enough solar energy was reflected back into space that ice sheets could grow at an ever-increasing rate. In this “runaway albedo” model, not only all the land masses became ice covered, but the surface of the oceans were also globally frozen (“snowball earth”; Kirschvink 1992; Hoffman et al. 1998; Hoffman and Schrag 2002). The seas became anoxic and BIFs could accumulate again (Hoffman et al. 1998). Eventually, enough volcanic CO2 Page 5 of 60

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Fig. 2 Major events in earth history in the Phanerozoic (Modified after various sources)

accumulated, and the glaciations ended abruptly. Later Neoproterozoic glaciations are documented, but these did not reach equatorial regions (Pierrehumbert et al. 2011; Shields-Zhou and Och 2011). Shortly after the last of these major Neoproterozoic glaciations, the first metazoans enter the fossil record. Enigmatic soft‐bodied fossils 580–541 Myr old are known from localities around the world and named Ediacara assemblages (after the Ediacara Hills in South Australia). Although the nature of the flattened, segmented, or quilted Ediacara organisms is still disputed (mainly cnidarians and annelids (Glaessner 1983, 1984; Jenkins 1992) or organisms not related to any of the extant animal phyla (Seilacher 1989, 1992; Buss and Seilacher 1994)), they are accompanied by traces produced by bilaterian metazoans (Knoll and Carroll 1999; Valentine et al. 1999; Martin et al. 2000; Erwin and

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Valentine 2013). Yet, tracemakers were small and rare and did not disrupt the sediment. This only changed near the Precambrian–Cambrian boundary when bioturbation markedly increased, and the sediment became unstable (Erwin and Valentine 2013). This probably led to the extinction of the immobile Ediacara organisms (Seilacher 1999). Within a short time after the beginning of the Cambrian at 541 Myr, the most remarkable episode in the history of life started, the so‐called Cambrian explosion. Within only 20 Myr, all animal phyla with preservable hard parts (with the exception of the bryozoans) appeared (Knoll and Carroll 1999; Erwin 2001a; Valentine 2002, 2004; Erwin and Valentine 2013). With the beginning of the Cambrian, and continuing throughout the Phanerozoic (Fig. 2), we have a very reliable fossil record especially for the marine invertebrates with easily preservable hard parts. Fossiliferous localities that show exceptional preservation are interspersed in the stratigraphic record and provide us with information on the soft‐bodied fauna (Bottjer et al. 2002; Seldon and Nudds 2012). Information on the Phanerozoic history of life can be found in many textbooks on paleontology, evolution, and historical geology (Stanley 2009; Cowen 2013; Monroe and Wicander 2011; Storch et al. 2013), and extensive treatment is beyond the scope of that chapter. Details on selected episodes of radiation and extinction are given in the last part of this chapter. During the Cambrian, life was exclusively marine and dominated by trilobites and a variety of other arthropods. Because the trilobites were highly diverse, are easily determined, and show a high species turnover, trilobites are the most important index fossils for this period. Brachiopods were small and belonged mostly to the inarticulate groups. Among the mollusks, hyoliths and monoplacophorans were the most conspicuous, but in the Late Cambrian, the first small nautiloids appeared, marking the beginning of a highly successful group of marine predators. Cambrian echinoderms belonged mostly to groups that were immobile and became extinct during the Early Paleozoic. Already during the Early Cambrian, the first true reefs built by the spongelike archaeocyathans developed, but archaeocyathans became extinct at the end of the Early Cambrian, leaving a reef gap until the Middle Ordovician. The first chordates and agnathan fishes appear to have been rare, with the exception of the conodonts. The extinction events in the Late Cambrian affected most severely the trilobites and several echinoderm groups. Ordovician and Silurian seas became dominated by articulated brachiopods and stalked echinoderms (crinoids and blastoids). Although the first deep burrows appeared at that time, life was still mainly epibenthic. Large reefs dominated by tabulate and rugose corals and stromatoporoids developed, and bryozoans became an important component of marine hard bottoms. Among the planktonic organisms, the graptolites diversified considerably and have proven to be the most valuable index fossils for the Ordovician and Silurian. Large predators developed among the nektonic nautiloids and among the eurypterids. Several groups invaded freshwater environments, among them the arthropods and various fish groups. Colonialization of the land started in the Ordovician–Silurian, first by plants (although algal crusts and fungi may have been present earlier), then by mites, arachnids, millipedes, and scorpions. Among the vertebrates, the appearance of the first jawed fishes in the Late Silurian was a major innovation. During the Devonian and Carboniferous, land plants diversified in an explosive manner leading to the first true forests, and the first seed plants had developed by the Carboniferous. The first wingless insects appeared in the Early Devonian, but it was not until the Carboniferous that the first winged insects conquered the air. In the vertebrates, huge marine predators developed among the placoderms. The Devonian, also called the “age of fishes,” saw the first appearance of the chondrichthyans and actinopterygians, while the agnathans considerably diversified. The first tetrapods appeared during the Middle–Late Devonian, and the amniote egg evolved in the Late Carboniferous. Among the marine benthic organisms, tabulate–rugose–stromatoporoid reefs Page 7 of 60

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attained a new climax. Articulate brachiopods and stalked crinoids still dominated most seafloors. Among the nektonic organisms, the evolution of the ammonoids was a major innovation during the Early Devonian. This group provided the most important index fossils for the Devonian to Cretaceous periods. In the latest Paleozoic, life in the seas did not radically change, but the absence of the heavily armored fishes is notable, and among the cephalopods the stoutly shelled nautiloids also declined, while the ammonoids flourished. Reef building was confined to smaller constructs after the Late Devonian mass extinction. On land, the mammal‐like reptiles were the dominant herbivores and carnivores. After the end‐Permian mass extinction, life in the seas and on land dramatically changed. Seafloors were no longer dominated by epifaunal brachiopods and crinoids but by gastropods and burrowing bivalves. Reef production came to a halt during the Early Triassic, and it was not until the Middle Triassic that scleractinian coral reefs became established. This type of reef building would dominate throughout the rest of the Mesozoic and Cenozoic. Only during part of the Cretaceous were the corals replaced as principal reef builders by a group of aberrant bivalves, the rudists. The open waters were dominated by ammonoids and actinopterygian fishes, and during the Mesozoic three groups of planktonic organisms which play an eminent role in biogeochemical cycles made their appearance: the planktonic foraminifers, the coccoliths, and the diatoms. The largest creatures of the seas, and the top predators, were the marine reptiles: nothosaurs, plesiosaurs, ichthyosaurs, marine crocodiles, turtles, and mosasaurs. On land, the conifers, cycads, and ginkgos flourished and dominated the forests until the late Early Cretaceous when they became increasingly replaced by the flowering plants (angiosperms). Among the amphibians, the last stegocephalians died out, while the first frogs and salamanders appeared. After the end‐Permian mass extinction, the mammal‐like reptiles had become marginal players, and the archosaurs, most notably the dinosaurs, became the rulers of the Earth. The pterosaurs were the first vertebrates to conquer the air, by the Late Triassic; and in the Late Jurassic, the first birds evolved. Mammals arose already during the Late Triassic, but remained mostly small and peripheral throughout the Mesozoic. The mass extinction at the Cretaceous–Tertiary boundary, although much less severe than the extinction at the end of the Permian, nevertheless severely altered the structure of both marine and terrestrial ecosystems. In the seas, the shelled cephalopods became entirely extinct with the exception of a small group of nautilids, and among the marine reptiles, only the turtles survived. The vacant ecospaces were filled up by actinopterygian fishes and mammals. The mammals also played a central role in the restructuring of the terrestrial communities. During the remarkable radiation in the Paleogene, mammals occupied almost all available niches on land, invaded the seas (whales, pinnipeds, sea cows), and conquered the air (bats). Birds equally radiated considerably, and in some regions, large, flightless birds even became the top predators. After the Eocene–Oligocene climatic revolution, the flora and fauna had an essentially modern organization, and grasses as the most important terrestrial producers became widespread during the Miocene. The Miocene radiation of the apes ultimately led to the development of our species, Homo sapiens.

Directionality Versus Contingency During the Precambrian, eukaryotes evolved from prokaryotes, and in the Cambrian, most animal phyla evolved. Ever more environments were colonialized during the Phanerozoic, including the land and the air. For the evolution of the vertebrates, the long‐portrayed succession of the “age of fishes,” “age of reptiles,” and “age of mammals” is of course a gross oversimplification. Osteichthyans and chondrichthyans were never as diverse as today! Yet, although measuring morphological complexity is not straightforward, there was clearly a trend toward increasing Page 8 of 60

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Fig. 3 Genus diversity over the Phanerozoic ((a) After Sepkoski 1997; (b) After Alroy et al. 2008; (c) After Alroy 2010)

complexity in the evolution of life from bacteria to today’s biota (Carroll 2001; Rosslenbroich 2006; McShea and Brandon 2010; Korb and Dorin 2011). There are two fundamentally different views on this complexity increase. According to one view, the rise and ultimately dominance of complex life forms were an inevitable outcome of natural Page 9 of 60

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selection, whereby more complex organisms outcompete the more primitive ones. It also inevitably culminates with the development of intelligent animals. Such a view is championed, e.g., by Conway-Morris (1998, 2003) and is reminiscent of an Aristotelian “chain of being.” A radically different view of the evolution of life does not see complex mammals as superior to bacteria. The increase in diversity is not neglected, but is explained in a different way. Bacterial cells cannot evolve toward ever-smaller sizes, unicellular eukaryotes cannot evolve toward zero cells but only toward multicellularity, and marine organisms cannot evolve to colonialize a nonexisting environment, although they can evolve land‐dwelling species and among animals also flying taxa. The evolution toward greater complexity is thus simply a move away from an “impermeable left wall” and an increase in variance; but in a sense we still live in a bacteria‐dominated world (Gould 1996). Perhaps the truth lies somewhere in between. There is no necessity to evolve toward intelligence, but ultimately this was made possible through successive evolutionary steps after the increasing variance crossed several thresholds. In such a view, life on Earth followed a megatrajectory along the following sequence (Knoll and Bambach 2000): prokaryote diversification (including metabolic pathways, but inability for sexual reproduction), early eukaryote diversification (first consumers, multicellularity, increased size, sex), aquatic multicellularity (large size, packaging of biomass, fast movement, complex food chains), invasion of the land (huge biomass of producers, adaptation to widely fluctuating environments), and ultimately intelligence (which perhaps could also have evolved in the water). Nevertheless, if “life’s tape were replayed,” the outcome would certainly be totally different (Gould 2001).

Diversity Patterns: The Broad Picture The Textbook Version The last decades have witnessed a veritable boom of publications documenting the diversity patterns of life during Earth history and the pace of large‐scale evolution. Outstanding contributions came especially from the late “Jack” Sepkoski. His 1981 curve of Phanerozoic diversity patterns of marine families (and subsequent refinements down to the genus level; Fig. 3; Sepkoski 1996, 1997, 2002) is one of the most often reproduced figures in the paleontological literature (equaling perhaps the Berlin Archaeopteryx specimen; Benton 2001), and this benchmark is an ideal starting point for the discussion of life’s ups and downs during the last 541 Myr. Assembling literature‐based compilations of the worldwide temporal distribution of marine families (Sepkoski 1982, 1992) and genera (Sepkoski 2002), the number of described taxa and hence diversity for every successive stratigraphic interval (usually stages) could be determined. In addition, the times of origination (first occurrence) and extinction (last occurrence) of these taxa could be deduced. By means of a factorial analysis, Sepkoski (1981) could show that the marine families grouped into three rather well‐delineated entities each showing a common pattern of origination, diversification, and decline. These three “evolutionary faunas” were called “Cambrian fauna,” “Paleozoic fauna,” and “Modern fauna” (Sepkoski 1981). A division into finer intervals (nine “Ecological Evolutionary Units”) was suggested by Boucot (1983) and further refined by Sheehan (1996, 2001a); yet, these intervals mainly portray ecological communities and not evolutionary units. According to Sepkoski’s figures, diversity at the family level shows a sharp rise at the beginning of the Cambrian, continuing well into the Middle Cambrian. In the Middle Cambrian, a plateau was reached, and several drops in diversity occurred. The main representatives of this Cambrian fauna Page 10 of 60

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_16-3 # Springer-Verlag Berlin Heidelberg 2013

Fig. 4 Phanerozoic family diversity in tetrapods (After Benton 1999)

were trilobites, inarticulate brachiopods, hyolithids, monoplacophorans, archaeocyathids, and eocrinoids (Sepkoski 1981, 1984). During the Early Ordovician, diversity increased again to reach a level about three times that of the Cambrian. Responsible for that fast and unprecedented increase in diversity were members of the Paleozoic fauna, mainly articulate brachiopods, crinoids, rugose and tabulate corals, ostracods, cephalopods, bryozoans, asteroids, ophiuroids, and graptolites. The diversity reached by the Ordovician radiation remained almost constant through the rest of the Paleozoic, interrupted only by punctuations of extinctions and subsequent recoveries. The Late Permian witnessed a dramatic extinction pulse, and the members of the Paleozoic fauna lost their dominance. The Modern fauna (demosponges, bivalves, gastropods, gymnolaemate bryozoans, and malacostracan crustaceans) had its origins in the Paleozoic, but its members remained a minor component up to the Permian. During the Triassic, Jurassic, and Cretaceous, members of the Modern fauna originated at a considerably faster rate than members of the Paleozoic fauna, and overall diversity increased steadily throughout the Mesozoic. The end‐Cretaceous extinction appears at the family level only as a minor perturbation, and the diversity increase continues throughout the Cenozoic. By the end of the Neogene, family diversity had reached a level almost twice that of the Paleozoic. The taxic diversity trends observed by Sepkoski were accompanied by several other notable trends which relate to the structuring of marine communities. During the Phanerozoic, the species numbers within open marine assemblages increased through time (denser “species packing”; Bambach 1977), and between the three evolutionary faunas, a significant increase in the number of feeding types and occupied substrate niches (“guilds”) is documented (Bambach 1983). In addition, the proportion of mobile taxa and of predators increased (Bambach et al. 2002; Bush and Bambach 2011). This is paralleled by changes in the spatial structure of marine benthic communities. Animals of Cambrian communities neither extended high above nor burrowed deep into the substrate, but during the mid‐Paleozoic to mid‐Mesozoic, many suspension feeders evolved that stood highly erect above the substrate, and several tiers of epifaunal benthos developed (Ausich and Bottjer 1982; Bottjer and Ausich 1986; Signor 1990; Bush and Bambach 2011). A complex

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tiering, as documented by trace fossils, also developed among the burrowing endobenthos, although very deep burrows only became common in the latest Paleozoic. Following the broad interest in the Phanerozoic diversity trajectories documented for marine animals, various researchers also published figures for other groups of organisms (for earlier work, see Valentine 1985). For insects, a synoptic curve for the number of families was published that shows an increase in diversity from the Devonian to the recent. The only notable event that led to a significant decrease in the number of families seems to be the end‐Permian mass extinction (Labandeira and Sepkoski 1993; Labandeira 1999). Extensive data have also been assembled for fishes (Lloyd and Friedman 2013) and tetrapods (Benton 1993; Benton et al. 2013). Here, the most significant outcomes are an only slight overall diversity increase from the Devonian to the Late Cretaceous and a huge increase in the number of families after the end‐Cretaceous extinction (Benton 1999; Fig. 4). Plants differ from the various animal groups in that the family richness over the Phanerozoic follows a much smoother path, and extinctions had little effect on family diversity (Niklas 1997). At lower taxonomic levels, however, plants also suffered heavily from mass extinctions (McElwain and Punyasena 2007).

Methodological Problems and Newer Developments The documentation of Phanerozoic diversity patterns goes back to Phillips (1860), who used data from marine rocks in Great Britain to distinguish between Paleozoic, Mesozoic, and Cenozoic life, and showed that diversity increased throughout the Phanerozoic (see Miller 2000). Renewed interest in these large-scale patterns arose in the 1960s and 1970s, stimulated especially by the pioneering publications of Gregory (1955), Simpson (1960), and Newell (1967). The first diversity patterns published thereafter (Valentine 1969; Raup 1972, 1976a, b; Bambach 1977) showed mainly that this was a very difficult task. The results were, in part, grossly dissimilar, especially with respect to the diversity increase in the Cenozoic. Although a “consensus paper” was published shortly thereafter (Sepkoski et al. 1981), discussions of methodological problems continue. The interpretations of Phanerozoic diversity patterns have thus fluctuated between two extremes: it might be the real picture or an artifact of databases affected by different and heavy biases. A first problem is how to count. Should we omit taxa that occur in only one time bin? This would prevent taxa known only from Fossil-Lagerstaetten or a single monograph from summing up to exceptional high diversity in that time bin (Foote 2000). On the other hand, omission of single occurrences can exclude whole groups of short-lived taxa. There may be problems with the taxonomic databases used, which can add noise and possibly induce false signals (Signor 1985). Yet, two databases at the family level compiled by Sepkoski (1982, 1992) and a team of specialists (Benton 1993) produced very similar results. A further problem is unsampled ranges. A taxon can extend further back in time (“ghost range”) and also reach further upward (“zombie lineages”) than recorded in the database (Lane et al. 2005). Ghost ranges can potentially be elucidated with a phylogenetic approach, whereas zombie lineages cannot. Correcting for these errors has hitherto met with limited success (Lane et al. 2005). The “pull of the recent” is another potential source of error and refers to the fact that the modern biota is much more completely sampled than fossil strata. Therefore, it tends to extend the stratigraphic ranges of extant families, or species that are known from some time in the Cenozoic, through intervals where fossils of those taxa are missing. This bias was either seen to be a negligible quantity (Jablonski et al. 2003) or a major source of bias (Alroy et al. 2008; Aberhan and Kiessling 2012). Uneven sampling in different regions and in different periods is a fact that cannot easily be corrected for (Smith 2003). All the compendia are heavily biased toward occurrences in Europe and North America, with the important side effect that from the Jurassic onward tropical environments Page 12 of 60

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are underrepresented (Aberhan and Kiessling 2012). Uneven time spans of the sampled intervals (usually stages) are a further problem. To correct for this, longer stages are subdivided, and very short ones are amalgamated (Sepkoski 1996). Taphonomic biases (differential preservation) are usually thought of as occurring randomly through the Phanerozoic (Kidwell 2005; Cooper et al. 2006) although this is contentious (Alroy et al. 2008). But potential biases can occur, e.g., through taxa that are only rarely preserved (in extraordinary deposits, see above), producing a local peak in diversity for that stratigraphic interval (Sepkoski 1996). Culling of the data by removal of single occurrences (taxa that are confined to a single time bin) is the common procedure to remove this bias (Sepkoski 1996). Cenozoic samples are, on average, less often lithified than Paleozoic or Mesozoic ones (Hendy 2009) and therefore yield more fossils than their lithified counterparts. This again, like the “pull of the recent,” will lead to an overestimation of the Cenozoic diversity increase (Alroy et al. 2008). Perhaps the most distracting factor when analyzing diversity patterns is that the sedimentary rocks available for study are not evenly dispersed through the Phanerozoic (Raup 1972, 1976b; Ronov 1983; Peters and Foote 2001; Smith 2001; Smith and McGowan 2011). There is a correlation between sedimentary rock volume and apparent diversity, although its extent is still debated. Are the diversity trajectories real and independent of the outcrop area/sediment volume (Miller 2000), or does the close match even suggest a common cause for diversity increase and patterns of sedimentation (Hannisdal and Peters 2011)? Or does the correlation point to an important bias (Smith 2007) that needs to be corrected for? There are many more problems surrounding the analysis of Phanerozoic diversity trajectories (Sepkoski 1996; Smith 2007; Alroy et al. 2008; Aberhan and Kiessling 2012). Several of these cannot be addressed using the existing compendia, and it was felt necessary to develop a new database. The Paleobiology Database (PBDB) is a huge collection of locality‐specific inventories in the Phanerozoic record (Alroy et al. 2001, 2008; Adrain and Westrop 2003; Miller 2003; Aberhan and Kiessling 2012). Hopefully, the PBDB will allow for a much better correction of taphonomic and sampling bias (Alroy et al. 2001; Bush et al. 2004); will yield new insights into the respective contributions of alpha, beta, and gamma diversity to the Phanerozoic taxonomic richness (Bush and Bambach 2004); and will enable us to dissect geographical components of diversity changes. Two global diversity curves for the Phanerozoic using subsampling methods of the PBDB have been published (Alroy et al. 2008; Alroy 2010). These show important differences from the Sepkoski curve (Fig. 3): Paleozoic diversity was probably underestimated in earlier curves, and the diversity increase during the Cenozoic was much less pronounced. However, the PBDB suffers also from inherent limitations, and some maintain that currently it is not a good reflection of the fossil record (Krug et al. 2009; Erwin 2009; Marshall 2010). The differences between the 2008 and 2010 curves also show that there is still some way to go until a new consensus is reached (Marshall 2010).

Expansion and Equilibrium Models The interpretations of Phanerozoic diversity trajectories have remained problematic. For the increase in familial and generic diversity, three basic models derived from population ecology can be invoked to explain the pattern (Miller 1998; Benton 2001). First, if rates of species origination and extinction are unconstrained by existing diversity, and origination exceeds extinction rates, an exponential increase in taxic diversity will result, only interrupted by major extinction intervals. The second, linear model of diversity increase requires the addition of a fixed number of taxa in each unit time. This would require a constant decrease in the rate of evolution (speciation) or a regularly increasing rate of extinction, and this model is generally rejected as improbable (Benton 2001). The third, Page 13 of 60

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Fig. 5 Extinction intensities in the Phanerozoic. Mass extinctions clearly stand out against background intensities, which decreased during the Phanerozoic (After MacLeod 2003)

density-dependent, model assumes that after an initial slow diversity increase, a rapid rise occurs, followed by a slowing rate of increase and finally a plateau (logistic growth). In a “decoupled logistic” simulation of the three Phanerozoic evolutionary faunas at the family level, allowing for major mass extinctions, Sepkoski (1981, 1984) achieved a rather good fit to the observed picture. In a variation of the theme, it was proposed that the diversifications from Ordovician to recent were best matched by a series of four simple logistic curves without interaction between evolutionary faunas and only reset by mass extinctions (Courtillot and Gaudemer 1996). Exponential growth (Benton 1995) is currently no more supported for marine animals (Alroy 2010), but the nearly exponential increase in several terrestrial groups indicates that these taxa are still far from reaching saturation (Benton 2001).

Extinctions and Biotic Recovery: Generalities From the conservation biologist’s point of view, the extinction of even a single species is a catastrophe. From a paleontologist’s viewpoint, species extinction is normal, and more than 99 % of all the species that ever inhabited Earth are now extinct (Raup 1991b). Yet, there is a further, more important dimension to this: during the history of life, mass extinctions also provided huge opportunities for taxa that hitherto had played only minor roles, by removing or marginalizing incumbents (Jablonski 2001). The same databases used in diversity studies can be used to construct plots of extinction (and also origination) intensities over time. Two major points emerge from such an analysis: peaks of high extinction intensities are separated from each other by times of lesser extinction, and overall extinction intensities decline over the Phanerozoic (Sepkoski 1996; MacLeod 2003, 2013; Fig. 5). According to Raup and Sepkoski (1982), there were 5 major and at least 18 lesser mass extinctions in the Phanerozoic, and the “big five” major extinctions (Table 1) are also recognized in newer studies (Hallam and Wignall 1997; MacLeod 2003, 2013; Bambach et al. 2004; Taylor 2004). A “mass extinction” is an event that (1) was nearly global, (2) removed a significant proportion of the existing

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Table 1 Observed (families, genera) and calculated (species) extinction intensities at the five major Phanerozoic mass extinctions Mass extinction End Ordovician Late Devonian End Permian End Triassic End Cretaceous

Families extinct (%) 26 22 51 22 16

Genera extinct (%) 60 57 82 53 47

Species extinct (%) 85 81 95 80 73

Simplified after Hallam and Wignall 1997

species (perhaps more than 30 %), (3) affected species from a broad range of ecologies, and (4) happened within a (geologically speaking) short time. For the decline in background extinction intensity, widely disparate explanations have been proposed. The change might reflect the general decrease in “volatility” between the three evolutionary faunas (Sepkoski 1981) or secular changes in the geochemistry and nutrition levels in the seas (Martin 1996). Yet, it might also just be a taxonomic artifact: through the Phanerozoic, there is a trend toward more species per family/genus. More species therefore need to become extinct for the entire family/genus to become extinct (Taylor 2004). An extinction event can be abrupt, or stepped, or gradual. An abrupt or “pulse” extinction evidently leaves a species no time to adapt or migrate, whereas this would be possible during a gradual or “press” extinction (Erwin 1996b, 2001b). Yet, it has proven difficult to establish the exact times of disappearance of taxa, especially the rare ones. As a consequence of the imperfect fossil record, the observed last appearance of fossil taxa is always “smeared back” in time through a time interval before their actual extinction (Hallam and Wignall 1997; Taylor 2004). This “Signor–Lipps effect” (Signor and Lipps 1982) will lead to the perception of a gradual extinction pattern even if it was abrupt. The “zombie” lineage, that is, the unsampled portion of a taxon’s range occurring after the final appearance of the taxon in the fossil record prior to its actual extinction (Lane et al. 2005), can be inferred at some level of probability using statistical methods (Marshall 1990). Not even the largest mass extinctions acted in a completely random manner. Extinction selectivity can be geographical (e.g., tropical versus nontropical, terrestrial versus marine), taxonomic (different extinction rates among higher taxa, e.g., dinosaurs versus mammals, plants versus animals), or linked to trait (e.g., body size, trophic level; McKinney 1997, 2001; Twitchett 2006). The selectivity patterns seen during a major extinction interval can be the same as those acting during pre‐ and postextinction times (“fair game” selectivity) or they can differ (“wanton” selectivity; Raup 1991b). Random survival with respect to trait and taxonomy was termed “field of bullet” selectivity (Raup 1991b). Major discussion has centered on the question of whether mass extinctions qualify as a separate class of evolutionary mechanism and are, therefore, different from background extinctions (Jablonski 2001; Bambach et al. 2004). There is certainly a continuity of magnitude, with the “big five” and some Early Paleozoic events occupying the ranks of the highest intensities (MacLeod 2003; Wang 2003), although the simple relationship between extinction intensity and mean waiting time (kill curve; Raup 1991a) is no longer accepted because continuity of cause is lacking (Wang 2003; Prothero 2006). The processes operating during mass extinctions are not the same as those acting during background extinctions (Wignall 2004). Continuity of effects is also no longer tenable; for example, the end‐Ordovician and end‐Devonian mass extinctions both had about the same intensities, but the former had only minor consequences for the structuring of marine communities, Page 15 of 60

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Table 2 Environmental effects of the most commonly cited mass extinction mechanisms Environmental effect Increased atmospheric particulates Increased cloud cover Increased greenhouse gases Reduced greenhouse gases Acid rain Global wildfires Shock heating Habitat fragmentation Intensification of climate gradients Enrichment of trace elements

Extinction mechanism Comet/asteroid impact x x x

Flood-basalt volcanism x x x

Sea-level change x

x x x x x x

x x x

x x

After MacLeod 1998

while the latter had a profound impact on ecosystems (Droser et al. 2000). Mass extinctions therefore did have a major impact on the evolution of life even though most species have gone extinct during times of background extinction intensities (Taylor 2004). Did the major mass extinctions during the Phanerozoic have a common cause? This subject was treated by several authors, and the mechanisms include impacts (as assumed, e.g., by Raup and Sepkoski (1984); see review by Racki (2012)), sea‐level changes, and the spread of anoxia (Hallam and Wignall 1997; Peters 2008), large‐scale volcanisms (Courtillot 1999; Prokoph et al. 2013), and perhaps global cooling (Stanley 1988). It is not always easy to distinguish between the different mechanisms (MacLeod 2003, 2013; Table 2). Yet, there is now overwhelming evidence that the major mass extinctions had their individual signature, and at the present state of knowledge, the search for a common cause no longer makes sense (Prothero 2006; MacLeod 2013). It has been suggested several times that the history of life follows some large‐scale cyclic pattern (Fischer and Arthur 1977; Fischer 1984). Yet, the notion that Phanerozoic extinction patterns show a periodicity with an interval length of 26 Myr (Raup and Sepkoski 1984) has spurred intensive debates about extinction mechanisms. But with increasing accuracy of the geological time scale, it has received little support from other researchers. Currently, few paleontologists would subscribe to the idea that the mass extinctions show any periodicity, despite continued search for possible (mainly extraterrestrial) mechanisms (e.g., invisible companion of the sun, “nemesis,” inducing a comet shower when passing through Oort Cloud; an eccentrical “planet X” doing the same job; the passing of our solar system through the spiral arms of our galaxy, again perturbing bolides in the Oort cloud; movement of the solar system through the galactic plane; Sepkoski 1990). It comes as a major surprise that a new study indicates again that the diversity of life on Earth followed some cyclic pattern, this time with a 62‐Myr periodicity (Rohde and Muller 2005). This pattern was recently corroborated (Melott and Bambach 2011a, b); yet statistical support is weak (Melott et al. 2012) and it might just be the inevitable outcome of the applied methods (Smith 2007). The phase after a mass extinction usually shows a peculiar fauna and flora that change gradually during the time following the extinction. Some terms have proven to be helpful for the characterization of these intervals (Kauffman and Erwin 1995; Fig. 6). The extinction phase is the time where most of the affected taxa had their last appearance. This is followed by the survival phase, where some groups not severely affected by the extinction (holdover taxa) have already began to diversify. During the survival phase, there are usually a small number of opportunistic taxa that could temporarily spread at the expense of the other fauna. “Lazarus taxa” (Jablonski 1986) are those Page 16 of 60

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Fig. 6 Faunal patterns during extinctions and subsequent recovery (After Hallam and Wignall 1997)

that disappear, probably by becoming very rare (and not retreating to refugia; Wignall and Hallam 1999) during the survival phase, only to later reappear during the recovery phase when new ecosystems are being established, while “Elvis taxa” (Erwin and Droser 1993) are those that have newly entered the fossil record but mimic the shape of extinct taxa. The new communities are largely shaped by progenitor taxa, the most prolific during the recovery phase (Kauffman and Erwin 1995; Hallam and Wignall 1997). It has long been recognized that after mass extinctions reefs show a prolonged recovery interval. This “reef gap” (Hallam and Wignall 1997; Stanley 2001; Fl€ ugel and Kiessling 2002; Jablonski 2003), which is evident after all of the “big five” and also after the extinction event after the end of the Lower Cambrian (extinction of the Archaeocyatha; Copper 1988), probably reflects the longer time required to reassemble complex ecosystems (Jablonski 2003).

Selected Case Studies The Cambrian Explosion and Its Prelude The tracking of the appearance and early diversification of the animals in the fossil record (Fig. 7) is a rapidly progressing field of paleontology (Fedonkin et al. 2007; Erwin and Valentine 2013). New input has come especially from molecular systematics (Adoutte et al. 2000; Giribet 2002; Pennisi 2003; Halanych 2004; Peterson et al. 2004; Hedges 2009; Edgecombe et al. 2011) and through precise absolute dating of fossiliferous Late Neoproterozoic and Early Cambrian sections, allowing the establishment of a reliable chronostratigraphic framework (Martin et al. 2000; Knoll et al. 2004; Peng et al. 2012). Possibly the oldest metazoans are ring‐ and disk‐shaped impressions from the Mackenzie Mountains in Northwestern Canada, from the Late Cryogenian Period. This soft‐bodied fauna represents perhaps cnidarian grade animals (Erwin 2001a). Considerably more diverse but younger so-called Ediacaran (¼ Vendian) assemblages are known from a number of localities around the world (Bottjer 2002; Brasier and Antcliffe 2004; Narbonne 2005; McCall 2006). The fauna of these

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Fig. 7 Major events during the latest Neoproterozoic and the Cambrian (After Erwin and Valentine 2013)

assemblages consists exclusively of soft‐bodied forms. The body wall of these organisms must have been quite rigid as is evident from the taphonomic behavior of the Ediacaran biota. They are preserved, mostly intact, as impressions at the base of event beds (storm layers, turbidites) that quickly buried them (Erwin 2001a; Bottjer 2002).

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Most of the forms are flattened, segmented, or quilted, and some of them attain considerable sizes (Narbonne and Gehling 2003; Xiao and Laflamme 2009). Classification of these organisms has been highly controversial. Traditionally, the various species were assigned to extant groups like medusae, sea pens, polychaete worms, and stem group echinoderms (Wade 1972a, b; Glaessner 1983, 1984; Jenkins 1992), with most of them belonging to cnidarians. Today most researchers believe that the majority of the enigmatic Ediacaran organisms represent “lost constructions” (Seilacher 1989, 1992; Buss and Seilacher 1994; Narbonne 2004, 2005). With the exception of the 555‐Myr‐old Kimberella, which is now considered to be an ancestral mollusk (Fedonkin and Waggoner 1997; Fedonkin et al. 2007; but see Dzik 2003; Budd and Jensen 2004) and therefore the oldest body fossil of a bilaterian, Ediacaran organisms seem to lack a mouth and a digestive tract. Most were immobile, many of them recliners, but some also mud‐stickers (Seilacher 1999). Nutrient uptake was either through the body surface, or these organisms lived in symbiosis with photosynthetic/chemosynthetic protists or bacteria (McMenamin and McMenamin 1990; Narbonne 2005). Still another interpretation of these creatures as lichens (Retallack 2013) is rejected by most paleontologists (e.g., Xiao 2013). Although sponges and cnidarians were most probably also present, predators were notably absent. The immobile organisms thus lived in a “Garden of Ediacara” (McMenamin and McMenamin 1990). The sediment surface was frequently sealed by microbial mats that were not disrupted by larger burrowing animals. Traces including some radular scratch marks are small and rare and are proof of the presence of bilaterians. Claims for evidence of bilaterians earlier than the Ediacaran assemblages (e.g., traces from 1,200-Myr-old rocks in India; Seilacher et al. 1998) are published with some frequency but are not accepted (Erwin and Davidson 2002; Jensen et al. 2006). A new window into Late Proterozoic life recently opened with the discovery of 580–560-Myr-old fossiliferous phosphorites at Doushantuo, Southern China (Xiao et al. 1998). In addition to various algae, microscopic multicellular aggregates with preserved nuclei were found. These aggregates were initially described as metazoan embryos (Knoll and Carroll 1999; Valentine et al. 1999; Chen et al. 2000; Hagadorn et al. 2006) but rather seem to be cleavage stages of some unknown “holozoans” or germination stages of protists (Butterfield 2011; Huldtgren et al. 2011). Newer claims for small bilaterian animals (Vernanimalcula) with preserved coelom and digestive tract from the same locality (Chen et al. 2004) have been rejected (Stokstad 2004; Bengtson et al. 2012). The Ediacaran biota largely went extinct at the Precambrian–Cambrian boundary (Brasier and Antcliffe 2004; Xiao and Laflamme 2009), with perhaps a few survivors into the Middle Cambrian (Conway Morris 1993; Shu et al. 2006). The base of the Cambrian, defined by the first occurrence of the trace fossil Treptichnus pedum (Buatois and Mangano 2011) and now dated at 541 Myr (Peng et al. 2012), marks the beginning of an interval which is the most remarkable in the history of life. During the Early Cambrian, a wide range of skeleton‐bearing animals made their debut, and within only 20 Myr, almost all phyla with preservable hard parts entered the fossil record (sponges already earlier, bryozoans in the Late Cambrian; Valentine 2002, 2004; Marshall 2006; Erwin and Valentine 2013). This apparent explosion of animal bauplans, which had already puzzled Darwin, is still one of the greatest enigmas, although it has become clear in the last few years that there was a prelude of perhaps tens of million years (Lieberman 2003), seen both among traces and in the shelly fossils, but no lengthy time gap between the Ediacaran assemblages and the lowermost Cambrian (Knoll and Carroll 1999; Erwin 2001a; Valentine 2002; Erwin and Valentine 2013). At first we see an increasing size and complexity of burrows/traces across the Precambrian–Cambrian boundary and then an ever-increasing diversity during the Early Cambrian (Crimes 1992, 2001; Droser and Li 2001; Buatois and Mangano 2011). In parallel, there was a huge diversification Page 19 of 60

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_16-3 # Springer-Verlag Berlin Heidelberg 2013

in the so‐called small shelly fossils (Rozanov and Zhuravlev 1992; Conway‐Morris 1998, 2001; Grotzinger et al. 2000). The appearance of new animal phyla and other higher taxa was concentrated in an interval between the Late Terreneuvian and the early Series 2 spanning perhaps 10–20 Myr, and this interval is called the “Cambrian explosion” (Dzik 1993; Valentine et al. 1999; Conway Morris 2000). During this interval, biomineralization was acquired by a multitude of organisms, including mollusks, brachiopods, echinoderms, and chordates (see Lowenstam and Weiner 1989; Bengtson 1994; Zhuravlev and Riding 2001; Wood and Zhuravlev 2012 for an overview). Complex arthropods like trilobite enter the fossil record early in Series 2, and later in Series 2 a plateau in diversity was reached (Marshall 2006; Erwin and Valentine 2013). Our picture of the Cambrian explosion is facilitated by several wonderful, exceptional fossiliferous settings (Fossil-Lagerstaetten), including the Early Cambrian localities of Chengjiang (China; Xian‐guang et al. 2004), Sirius Passet (Greenland; Conway Morris 1998), Emu Bay Shale (Australia; Nedin 1995), and the most famous Middle Cambrian Burgess Shale (Canada; Briggs et al. 1994). Several very important questions surround debates about the Cambrian explosion. (1) Is it real or just an artifact of the imperfect fossil record? (2) Does the origin of metazoan phyla substantially predate their appearance in the fossil record? (3) If the event was real, what was the triggering mechanism? The current consensus is that the Cambrian explosion was indeed real and happened in just a 10–20‐Myr interval in the Late Terreneuvian and early Series 2 (Valentine et al. 1999; Chen et al. 2000; Conway Morris 2000; Marshall 2006; Erwin and Valentine 2013). Yet, the Cambrian explosion does not record the initial split of the metazoans, but rather the diversification at a high taxonomic level (so is therefore, strictly speaking, not a radiation; Erwin and Valentine 2013) of the three fundamental metazoan groups into the crown groups and the modern phyla (Douzery et al. 2004; Peterson et al. 2004; Valentine 2004; Erwin and Valentine 2013). Ecologically, the Cambrian revolution led to a massive restructuring of the marine benthos (Bush and Bambach 2011). An increasing percentage of animals were burrowers that fed on nutrients within the sediment or that constructed tubes. As a consequence of the increasing bioturbation (Droser and Li 2001), the sediment became destabilized, and the superficial microbial mats were lost. This “agronomic revolution” (Seilacher 1999) or “Cambrian substrate revolution” (Bottjer et al. 2000) led to an uppermost mixed layer, and besides the Ediacara organisms, many immobile recliners and mudstickers like the helicoplacoid echinoderms went extinct early in the Cambrian (Bottjer et al. 2000; Dornbos and Bottjer 2000; Dornbos et al. 2005). With respect to the triggering mechanism(s) of the Cambrian explosion, our explanations are still very speculative. The synchronous radiation of many disparate phyla has led strong support to the idea that there must have been an environmental trigger (physical or biological; Valentine 2002, 2004; Marshall 2006; Budd 2008). Among the hypotheses advanced is a significant increase in oxygen in the oceans, but this hypothesis is at odds with observations that oxygen reached sufficient levels to sustain metazoan life long before the Early Cambrian (Knoll 1996; Love et al. 2009; but see Hedges 2004). The amalgamation of continental plates, followed by a transgression, was also cited as a possible trigger (Brasier and Lindsay 2001). There were certainly dramatic changes in the chemistry of the oceans during the latest Precambrian as is evident from isotope studies. Increased nutrient levels in the oceans might have facilitated the radiation (Brasier 1992). Furthermore, a major increase in Ca2+ levels is documented during the earliest Cambrian, which certainly facilitated biomineralization (Brennan et al. 2004; Wood and Zhuravlev 2012; Kouchinsky et al. 2012). One of the most commonly involved biological explanations of the radiation is that skeletons developed in a number of groups as an answer to increasing predator pressure (Conway Morris 2001; Porter 2011; see also Stanley 1973) and perhaps also the evolution of animal vision (Parker 2003), thereby Page 20 of 60

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allowing new adaptational opportunities. The Cambrian saw the appearance of many carnivores and scavengers, and this trophic group accounted for up to 25 % of the species in the Middle Cambrian (Burzin et al. 2001). Furthermore, the development of planktonic habits in a range of groups greatly increased the complexity of food webs and was also responsible for animal diversification (Butterfield 2001, 2009). In more recent years, the evolution of developmental mechanisms has received much attention. It might well be that key innovations in gene regulation and recombination in early metazoans facilitated the Cambrian explosion (Valentine 2002; Erwin and Valentine 2013). Many paleontologists were deeply impressed by the wide variety of different body plans, especially among arthropods, that appeared during the Cambrian explosion. The number of taxa known from the famous Cambrian Lagerstaetten that do not fit easily into any classification scheme based on living animals is extraordinary. It was claimed that morphological disparity among Cambrian animals was even higher than that seen today (Gould 1989, 1991) and that some extraordinary evolutionary mechanisms acted during the Cambrian explosion. Measuring morphological disparity is a relatively new field and seems to be a promising avenue to complement measures of taxonomic diversity (Foote 1997; Wills 2001; Erwin 2007). Detailed analyses of arthropods showed that disparity among the Cambrian forms was not higher than among modern species, and the level of appendage specialization is much higher today than in the Cambrian (Briggs et al. 1992; Wills et al. 1994). Special evolutionary processes do not, therefore, seem to have operated during the Cambrian explosion. Yet, it remains nevertheless remarkable how early and synchronous the multitude of higher animal taxa appeared in the fossil record.

The Ordovician Radiation During the Ordovician, taxic diversity at the family and generic level reached a new maximum which was three to four times that of the Late Cambrian (Miller 1997, 2001). While during the Cambrian explosion numerous phyla and classes representing basic body plans originated, the Ordovician radiation was manifested by an unprecedented burst of diversification at lower taxonomic levels. According to the global picture of Sepkoski (1979, 1997), the Cambrian fauna (e.g., the trilobites) declined, while the articulated brachiopods, the crinoids, stenolemate bryozoans, and other members of the Paleozoic fauna showed a sharp increase. To a lesser degree, members of the Modern fauna like gastropods and bivalves also diversified (Miller 2001, 2012; Servais et al. 2009, 2010). The almost exponential increase in diversity was much more rapid during this Great Ordovician Biodiversification Event (GOBE) than at any other time of the Phanerozoic (Sepkoski 1997; Webby 2004; Servais et al. 2009). This global diversity increase seems to have been the combined result of an increase in a‐ (within community), b‐ (between communities), and g‐diversity (biogeographical differentiation between faunal provinces; Webby 2004). New ecological guilds appeared, and the spatial organization of the benthic communities became considerably more complex (Bottjer and Ausich 1986; Droser and Bottjer 1989, 1993; Servais et al. 2009, 2010). The Ordovician was also a time of marked shift in the reef biota. Whereas Early Ordovician reefs were mainly built of microbial mats and stromatolites, large metazoan‐dominated framework reefs had developed and spread on all continents by the end of the Ordovician (Webby 2004; Adachi et al. 2011). The diversification and spread of metazoan reefs was accompanied by an increase in bioeroding organisms colonizing reefs and hardgrounds (“bioerosion revolution”; Wilson and Palmer 2001). Yet, when the global picture is dissected at finer taxonomic, geographical, and environmental levels, some surprising results emerge (Miller 1997). The diversification seems not to follow a global trajectory but to respond much more to local conditions in paleogeography, sedimentary environment, and orogenic activity. The general decline of Sepkoski’s Cambrian fauna is an Page 21 of 60

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Fig. 8 Major events during the Late Ordovician mass extinction (Modified after Brenchley 2001)

oversimplification. The “smooth” global diversity increase during the Ordovician is thus the aggregate record of many regional patterns which were for the most part abrupt (Miller 1997, 2001, 2004, 2012; Westrop and Adrain 1998). Not a single reason, but rather a combination of paleogeographic, sedimentologic, geochemical, and perhaps intrinsic factors, seems to have been responsible for diversity increase during the Ordovician (Harper 2006a; Miller 2012). The paleogeographic situation was one of a highly fractured continental crust with many small continents. Together with a very high sea‐level stand and increasing nutrient inputs, this provided extensive shelf areas in many different parts of the world and, therefore, a multitude of colonizable areas (Miller 1997). There is also a good correlation between diversity increase and orogenic activity. Throughout the Ordovician and the remainder of the Paleozoic, there was clearly a trend toward increased primary productivity and away from oligotrophic conditions (Martin 1996). Whether climate change (Trotter et al. 2008) and a series of impacts (Schmitz et al. 2008) also promoted the diversity increase remains to be scrutinized.

The Late Ordovician Mass Extinction With 26 % of the marine families, up to 60 % of the genera and an estimated 85 % of all the species becoming extinct, the Late Ordovician mass extinction was one of the most severe extinction episodes in the Phanerozoic, surpassed in its magnitude only by the end‐Permian mass extinction. Its extent was global, and it affected nearly all benthic and pelagic groups (Hallam and Wignall 1997; Brenchley 2001; Sheehan 2001b; Rasmussen and Harper 2011; Fig. 8). During the Late Ordovician greenhouse conditions prevailed. But during the latest stage (Hirnantian), a short glaciation of approximately 0.5‐Myr duration occurred (Brenchley 2001; Sheehan and Harris 2004; Delabroye and Vecoli 2010). The glaciation probably started when Late Ordovician orogenic activities led to extensive exposure and weathering of silicate terrains and, therefore, CO2 consumption. Under falling CO2 levels, ice sheets started to grow and albedo feedback led to an extensive Gondwana glaciation. The ice cover in turn inhibited silicate

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weathering, and CO2 levels rose again. After a threshold was reached, greenhouse conditions returned and the ice caps melted quickly (Kump et al. 1999). It is now well documented that the mass extinction during the Late Ordovician was a two‐phase event, and the first extinction pulse at the base of the Hirnantian extraordinarius zone corresponded to the initiation of the Gondwana glaciation and the second pulse in the first third of the persculptus zone to the rapid decay of the polar ice cap. During the first extinction event, various groups suffered heavy losses, and the graptolites nearly died out. Thereafter, an impoverished and remarkably cosmopolitan benthic fauna was present on most shelves from high latitudes to the tropics. This so‐called Hirnantia fauna can be regarded as a cool‐adapted, opportunistic community that spread after the extinction removed the hitherto dominant species (Brenchley 2001; Sheehan 2001b; Jia‐Yu et al. 2002). Primary productivity was obviously much reduced during the Hirnantian. The second extinction phase was again sharp and hit most of the groups that had already suffered during the first extinction pulse. It eliminated much of the benthic Hirnantia fauna, but the recovery interval did not last very long. It is most surprising that the faunal turnover during the Late Ordovician mass extinction was accompanied by very little ecological change and the structure of Silurian communities is remarkably similar to those of the Late Ordovician (Droser et al. 2000; Bottjer et al. 2001; Sheehan 2001b; McGhee et al. 2004). The causes of the two extinction pulses were certainly linked to the rapid onset and the later abrupt termination of the Gondwana glaciation during an otherwise warm climatic mode (Fortey and Cocks 2005; Delabroye and Vecoli 2010). Responsible for the necessary lowering of the atmospheric CO2 was perhaps the expansion of the first land plants (Lenton et al. 2012). Global cooling of the oceans of perhaps as much as 8
C together with a loss of benthic habitat due to regression might have, in part, been responsible for the first extinction (Berry and Boucot 1973; Brenchley et al. 1994; Armstrong 1996). Yet, pelagic forms also suffered heavy losses, and changing circulation patterns in the oceans were probably crucial (Hallam and Wignall 1997). The widespread deep anoxic waters, the extensive dysoxic zone, and the nutrient‐rich surface waters vanished during the onset of the glaciation when cold, deep water led to intensified ocean circulation. During the second pulse, the termination of cold, deep water production led again to widespread stratified oceans with anoxic deep and intermediate dysoxic waters. Black shales accumulated again, and the transgressing dysoxic waters eliminated most of the benthic Hirnantia fauna and other benthic organisms not resistant to oxygen‐poor conditions (Hallam and Wignall 1997; Rasmussen and Harper 2011).

The Late Devonian Biodiversity Crisis Between 11 and 16 global events have been identified in the Givetian through Famennian stages (Walliser 1996; Becker et al. 2012), but only the lower and upper Kellwasser events (Frasnian–Famennian boundary) and the Hangenberg event (uppermost Famennian) are of a magnitude that would deserve the name mass extinction (Hallam and Wignall 1997). Yet, the stress imposed by the many smaller events, especially the earlier Taghanic event in the Late Givetian (Aboussalam and Becker 2011; Zambito et al. 2012), was probably crucial for the overall extinction patterns in maintaining a high level of environmental stress throughout the Late Devonian. The label “mass extinction” is somewhat misleading as it was rather an anomalously low speciation rate that was responsible for the drop in biodiversity (Bambach et al. 2004; Stigall 2012). At least 70 % and perhaps as many as 82 % of the marine species vanished during this time period (McGhee 1996, 2001; Fig. 9). Among the groups that were most severely hit were the reef builders (Fagerstrom 1994; Hallam and Wignall 1997; Copper and Scotese 2003), but other benthic organisms, especially tropical families, also suffered heavy losses during both major crises. The Page 23 of 60

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Fig. 9 Major events during the Late Devonian mass extinction (Modified after various sources)

toll was no less severe in planktonic and nektonic groups (Racki 2005), and the armored agnathans and the placoderms went completely extinct (Hallam and Wignall 1997). Quite important for the elucidation of the possible causes of the Late Devonian mass extinctions is that their selectivity differed between the different events. The Taghanic event affected mainly benthic taxa from low‐latitude, shallow‐water environments (Hallam and Wignall 1997). The Kellwasser events also affected mainly warm‐water species as well as planktonic and pelagic groups. During the Hangenberg crisis, it was the planktonic and nektonic groups that were most severely hit, while the benthic groups showed a better survival than at the Frasnian–Famennian boundary. The extinction patterns in the Late Devonian were highly complex and a result of several mechanisms spread over a time period of more than 10 Myr, with the most severe perturbations concentrated at the Frasnian–Famennian boundary and in the latest Famennian (Sandberg Page 24 of 60

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_16-3 # Springer-Verlag Berlin Heidelberg 2013

et al. 2002; Stigall 2012). Global cooling of the oceans (Copper 1986) was certainly one of the main causes of the extinctions (McGhee 1996, 2001; Brezinski et al. 2009), although the Gondwana glaciation only started in the Late Famennian (Caputo 1985; Algeo and Scheckler 1998). Yet, besides the cooling, frequent sea‐level changes including both eustatic rises associated with spreading anoxic waters and regressions responsible for habitat loss are also well documented (Sandberg et al. 2002; Ver Straeten et al. 2011). The Late Devonian was also a time of increased impact frequency. Well-dated craters, shocked minerals, and microtektites as well as iridium anomalies are known from different continents (McGhee 1996, 2001; Sandberg et al. 2002), and these impacts probably increased the environmental stress.

Devonian to Carboniferous Expansion of Land Flora Undisputed vascular land plants are known from Late Silurian strata, but spores occur already in the Middle Ordovician (Taylor et al. 2009; Kenrick et al. 2012). Colonization of the terrestrial environment, at least in moist lowlands, obviously happened rather quickly, and within only 45 Myr, all major land‐plant lineages and organizational grades (except for flowering plants) developed (Niklas 1997, 2004; Willis and McElwain 2002; Taylor et al. 2009). All the morphological adaptations including a protective outer covering (waxy cuticula) against desiccation, stomata to allow gas diffusion, specialized tissues for the transport of liquids, and rigid cell walls (Chaloner 2003) developed in the Devonian, although accompanied only by a modest diversification at the species level (Niklas 1997; Willis and McElwain 2002). By the end of the Devonian, the terrestrial environment saw the first globally distributed forests with large trees (Chaloner 2003; Taylor et al. 2009). This resulted in a huge increase in biomass that culminated in the Late Carboniferous. Much of this organic material was not decomposed and recycled, but instead buried in moist anoxic soils (acidic swamps; Chaloner 2003). This expansion of the land flora had a profound impact on Earth’s environmental conditions. Most important was the removal of large quantities of CO2 from the atmosphere through photosynthetic carbon fixation. The most widely accepted models for Phanerozoic CO2 show a sharp decrease from about 15 times the present level (15 PAL) at the beginning of the Devonian to 10 PAL at the Devonian–Carboniferous boundary and a further decrease to less than 2 PAL in the Late Carboniferous (Berner 1998; Royer et al. 2000). With the massive drop in available CO2, a high stomatal density became crucial, and the laminate leaf rapidly became widespread (Beerling et al. 2001) although at the cost of higher water loss through transpiration (Chaloner 2003; Taylor et al. 2009). During the Devonian, an increase in the sizes of the trees was accompanied by increasing depth and complexity of the roots (Algeo and Scheckler 1998). This in turn accelerated silicate weathering and led to a further drawdown of carbon as bicarbonate into rivers and ultimately into the seas (Kump et al. 2004). The most obvious consequence of this huge decrease in atmospheric CO2 was the onset of the Gondwana glaciation. In the Late Devonian, the southern continents were assembled near the South Pole, and the first polar ice caps developed in the latest Devonian. However, the main phase of the Late Paleozoic glaciation started in the Early Carboniferous. With its duration of more than 80 Myr (Crowley and North 1991; Frakes et al. 1992; Vaughan 2007), well into the Permian, this glaciation was by far the longest and also the latitudinally most extensive of the Phanerozoic ice ages. Yet, it was not associated with any major mass extinction pulse. The very high productivity of the plants during the Devonian and Carboniferous also led to a significant increase in atmospheric oxygen, with 30–38 % O2 in the Late Carboniferous (Berner 1999; Berner et al. 2003; Bergman et al. 2004). This seems to have had yet another impact on life. With increasing oxygen partial pressure, the diffusive flux is increased considerably, allowing the evolution of gigantic sizes (Graham et al. 1995; Dudley 1998), most notably among fish, terrestrial Page 25 of 60

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Fig. 10 Major events during the end‐Permian mass extinction (Modified mainly after Chen and Benton 2012; Sun et al. 2012)

arthropods, and amphibians (Briggs 1985; Graham et al. 1995; Dahl et al. 2010; Harrison et al. 2010). For the giant flying insects, the higher density of the atmosphere might also have played a role (Dudley 1998, 2000).

The End-Permian Mass Extinction and Subsequent Recovery The mass extinction at the end of the Permian has long been recognized as the most severe of all the Phanerozoic perturbations (Phillips 1860). The radical faunal change associated with this biotic crisis was the reason for distinguishing between the Paleozoic below and the Mesozoic above. More than 50 % of marine and terrestrial families went extinct and an estimated 80–96 % of all the species. Until recently (Erwin 1990, 1993), the end‐Permian mass extinction was seen as a protracted crisis, which lasted for approximately 10 Myr. Newer research has shown that there were actually two discrete events (Fig. 10). The first occurred in the latest Guadalupian (terminal Middle Permian) and affected only some groups in a more gradual way (Hallam and Wignall 1997; Clapham et al. 2009). The event at the very end of the Permian, and reaching slightly into the lowermost Triassic, was apparently of quite short duration (probably less than 0.2 Myr; Erwin et al. 2002; Shen et al. 2011). It is this interval that has been called “the mother of all extinctions,” “the great dying,” or the Page 26 of 60

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“Paleozoic nemesis” (Erwin 1996a, 2006; Benton 2003). This massive crisis affected all groups of organisms, both in the seas and on land (Benton and Twitchett 2003; Algeo et al. 2011). In the Middle Permian, the seas were teeming with life, and many different faunal provinces can be distinguished. Highly diverse stromatoporoid–coral reefs were widely distributed. On soft and hard bottoms, rich communities dominated by brachiopods and echinoderms flourished, and in the water column, numerous ammonoids and various fish groups had attained a high diversity. On land, insects had reached their highest diversity in the Paleozoic, and tetrapod communities were probably as complex as modern mammal communities (Benton 2003; Sahney and Benton 2008). Plants were also highly diverse and distributed in different biogeographical provinces. During the first extinction event, which occurred at the end of the Middle Permian (Guadalupian), some groups were affected both on land and in the seas, but none became entirely extinct (Hallam and Wignall 1997; Algeo et al. 2011). The reasons for this first extinction pulse are not well understood, but global cooling, loss of habitat area, and spread of anoxic waters have been cited as underlying causes (Stanley 1988; Hallam and Wignall 1997; Clapham et al. 2009). The second, and by far the more severe, extinction pulse near the Permian–Triassic (P–Tr) boundary affected all the taxonomic and ecological groups, both in the seas and in the terrestrial environment. Among the larger groups that went completely extinct in the seas were the rugose and tabulate corals, fenestrate bryozoans, and orthid brachiopods. On land, glossopterids and cordaitales were suddenly replaced by a low‐diversity conifer–lycopod–fern assemblage with little provinciality. Palynological samples from immediately above the P–Tr boundary are dominated by fungal spores which normally account for only a small proportion of the pollen and spores. This “fungal spike” (Eshet et al. 1995; Visscher et al. 1996; some fungal spores might rather be freshwater algae; see Wignall 2008) was similar in its magnitude to the “fern spike” at the Cretaceous–Tertiary boundary and might indicate vast areas of rotting plants which were decomposed by fungi (Hallam and Wignall 1997; Benton and Twitchett 2003). A wide range of tetrapods, among them the hitherto dominant pareiasaurs, went abruptly extinct, and the Early Triassic vertebrate faunas were completely dominated by the single genus Lystrosaurus (Hallam and Wignall 1997; Benton and Twitchett 2003; Ward et al. 2005; Sahney and Benton 2008). Both the magnitude (up to an estimated 96 % of the marine species) and the extraordinary long recovery interval were remarkable. It took almost 100 Myr for family diversity to reach preextinction levels and almost 10 Myr for complex ecosystems like reefs to become established again (Benton and Twitchett 2003; Erwin 2006). The first communities that appeared during the recovery interval are composed of a remarkably cosmopolitan, opportunistic fauna of thin‐shelled bivalves (e.g., Claraia) and lingulid brachiopods (Hallam and Wignall 1997). Burrowing organisms were almost completely absent, and disaster taxa like stromatolites became locally abundant (Schubert and Bottjer 1992). Lazarus taxa were especially common among the gastropods, and most of them were small (“Lilliput” effect; Twitchett 2006). The long‐term consequences for seafloor communities were the replacement of the hitherto dominant epibenthic sessile suspension feeders by a vagile, epi‐ and endobenthic, mollusk‐ dominated fauna (Hallam and Wignall 1997; Algeo et al. 2011; Campi 2012). The recovery interval after the end‐Permian mass extinction was longer than for any other extinction event (although not for all groups, e.g., ammonites; Brayard et al. 2009), indicating that the ecosystems were almost completely devastated and severe environmental perturbations continued through the Lower Triassic (Twitchett 1999; Payne et al. 2004; Chen and Benton 2012). The scenario for this mass extinction and its likely causes has received much attention in the last decade. All the evidence indicates that the mass extinction event lasted less than 200 kyr and occurred during a phase of marine transgression and severe global warming (Shen et al. 2011). The catastrophe probably started with the release of huge amounts of CO2 into the atmosphere, first Page 27 of 60

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_16-3 # Springer-Verlag Berlin Heidelberg 2013

Fig. 11 Major events during the Late Triassic mass extinction (Modified after McRoberts et al. 2012)

through volcanic eruptions in South China (Emeishan flood-basalt province; Lo et al. 2002) and perhaps also through coal oxidation (Hallam and Wignall 1997), later through vast eruptions in Siberia (Siberian traps; Courtillot 1999; Wignall 2001a; Benton and Twitchett 2003; Heydari et al. 2008). This led to global warming and in the seas to decreased ocean circulation and oxygen depletion (Wignall and Twitchett 1996), perhaps concentrated in the later part of the extinction event (Song et al. 2013). With further increasing CO2 levels, methane hydrates began to melt and released large quantities of methane, which first acted as greenhouse gas and later was oxidized to CO2. Through this positive feedback, a “runaway greenhouse” developed, which went out of control after some threshold was reached (Benton and Twitchett 2003). The seas flooding the shelves became hot, anoxic, and perhaps even sulfidic (Kump et al. 2005; Sun et al. 2012) and killed most of the benthic and pelagic organisms (Clapham and Payne 2011; Payne and Clapham 2012). Ocean acidification was especially deleterious for heavily calcified taxa (Knoll 2013). On land, the vegetation suffered a severe deterioration with equally devastating consequences for the animals, which perhaps also experienced hypoxic stress (Huey and Ward 2005). Inevitably, many additional or alternative explanations have been presented. A major global regression during the terminal Permian was long a popular explanation for the extinction, but this is no longer tenable. There was clearly a transgression during the P–Tr boundary interval (Hallam and Wignall 1997). Darkening and global cooling with a collapse in photosynthesis was also proposed as extinction cause (Campbell et al. 1992), but all the evidence points to global warming at the end of the Permian. Older suggestions include brackish oceans and an increase in cosmic radiation. The claim for evidence of an impact is relatively recent (Becker et al. 2001, 2004; Frese et al. 2009). However, the impact hypothesis has not received much support (Erwin 2003, 2006). The end‐ Permian mass extinction thus seems truly “homemade” (White 2002; Benton and Twitchett 2003; Erwin 2006; Payne and Clapham 2012).

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End-Triassic Extinction

The extinction at the end of the Triassic (Fig. 11) is recognized as one of the “big five” Phanerozoic mass extinctions, but documenting the exact timing and the causes of biotic overturn has proven difficult. There was a widespread regression at the end of the Triassic, and marine sections which span the Triassic–Jurassic (Tr–J) boundary are known from only a few localities (Hallam and Wignall 1999; Ogg and Hinov 2012a). Many marine groups suffered a dramatic and sudden decrease in diversity at the end of the Rhaetian, but others witnessed a major reduction in diversity already at the Carnian–Norian boundary and during the Early Rhaetian (Teichert 1990; Hallam 2002; Tanner et al. 2004; Wignall and Bond 2008). Terrestrial plant extinctions are concentrated around the Carnian–Norian boundary and at the Tr–J boundary (Deenen et al. 2010), and the latter boundary layer contains an unusually high fern spores/pollen ratio (Olsen et al. 1990, 2002). Among terrestrial vertebrates, a major extinction is undisputed, but the main turnover occurred near the Carnian–Norian boundary (Benton 1994; Lucas 1994). Habitat loss and changing substrates associated with the regression in the Late Rhaetian, followed shortly thereafter by a transgression at the Rhaetian–Hettangian boundary, together with shallow water anoxia and perhaps ocean acidification (Greene et al. 2012; McRoberts et al. 2012), were responsible for the observed pattern in the marine realm. The two extinction phases correspond to two pulses of flood-basalt volcanism (Deenen et al. 2010). This extensive and widespread volcanism related to the rifting of Pangaea around the North Atlantic at the Tr–J boundary was only recently recognized. The outgassing of CO2 from this Central Atlantic Magmatic Province (CAMP; Marzoli et al. 1999; Wignall 2001a) might have had truly deleterious effects like enhanced seasonal fluctuations and an increase in the number and severity of hot days as well as a decrease in ocean water oxygenation (Huynh and Poulsen 2004). Extreme greenhouse warming, perhaps combined with the release of toxic gases, also explains the extinction patterns on land (Deenen et al. 2010). An impact scenario (Olsen et al. 2002) is largely dismissed today because the extinction pattern is not a sudden, catastrophic one, various impact craters have been dated as Carnian–Norian, and claims for significant iridium anomalies and shocked quartz could not be verified (Hallam 2002; Tanner et al. 2004).

Mesozoic Marine Revolution

The term “Mesozoic marine revolution” (MMR) (Vermeij 1977) refers to the idea that during the Mesozoic, a profound reorganization in the marine communities led to a significant increase in predation pressure and prey species developed various adaptations (thicker shells, spines, behavioral responses) to cope with this increasing pressure (“arms race” or “escalation”; Vermeij 1987; Harper 2003, 2006b). It is undisputed that during the Mesozoic, especially during the Jurassic and Cretaceous, the number of marine grazers as well as durophagous and drilling predators increased considerably (Vermeij 1977, 1987, 2004; Bambach et al. 2007; Finnegan et al. 2011). This rise in predatory groups was accompanied by profound changes in marine benthic communities. The epifaunal guilds, like stalked crinoids and brachiopods, that were so characteristic of Paleozoic communities vanished from shallow‐shelf environments, and those epifaunal species that did persist in shallow water show a high frequency of regeneration and, therefore, of predator attacks (Vermeij 1987). A marked shift toward infaunal life modes is documented in post‐Paleozoic echinoids, gastropods, and especially bivalves (Stanley 1977; Thayer 1983; Vermeij 1987), although this shift predates the appearance of most shell crushers (Harper 2003, 2006). The most conspicuous changes during the MMR occurred in shell architecture. Overall, the shells became sturdier, more Page 29 of 60

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Fig. 12 Extinction patterns during the K–T mass extinction (Modified mainly after Schulte et al. 2010)

highly armored, and developed spines, ribs, and thickened and narrowed apertures (Vermeij 1977, 1987, 2004; Ward 1981, 1983). At least among gastropods, shell‐repair scars became much more frequent, pointing again to increasing predation pressure. According to Vermeij (1987), it was the biological interactions (competition, predator–prey relations) that led to the evolution of these long‐term trends. Yet, the biological evolution toward increasing predator‐resistant shells might also have been facilitated by changes in the abiotic conditions. Extensive volcanism, which in turn augmented water temperature, high nutrient levels, and a high sea-level stand, facilitated the production of energetically expensive massive shells (Vermeij 1995) and perhaps as well the general increase in diversity and increasing “fleshiness” of the fauna throughout the Mesozoic and Cenozoic (Bambach 1993; Bambach et al. 2007; Bush et al. 2007). For several groups, the timing of changes does not support biological interactions as driving forces (Harper 2003, 2006; Madin et al. 2006; Baumiller et al. 2010; Kosnik et al. 2011). Secular changes in oceanographic and geochemical conditions most certainly spurred other important changes in the marine biota during Middle and Late Mesozoic times. Planktonic foraminifers appeared in the Middle Jurassic and became numerically important during the Cretaceous. Coccoliths are known since the Triassic, but they became widespread and abundant during the Late Jurassic and the Cretaceous (Ogg and Hinov 2012a, b). This rise in planktonic calcifiers was perhaps facilitated by the intensified bioturbation of the seafloor which effectively recycled nutrients (Kelley and Hansen 2001), but had in turn tremendous effects on the carbon cycle and the CaCO3 saturation of the oceans (Ridgwell 2005).

End-Cretaceous Mass Extinction This is certainly the most widely known and probably also the best investigated of the major mass extinctions, simply because the popular (nonavian) dinosaurs disappeared at the Cretaceous–Paleogene (K–Pg) boundary (formerly known as the K–T boundary, but the Tertiary is no longer a formal unit of the revised time scale). Yet, it is, with a 16 % loss of the families, a 47 % loss of the genera, and an estimated loss of at least 70 % of the species in the marine realm, the least

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severe among the five major mass extinctions in Earth history (Jablonski 1994; Hallam and Wignall 1997; Fig. 12). Some marine groups disappeared completely at the end of the Cretaceous (e.g., ammonites, large marine reptiles), others suffered heavy losses (especially planktonic groups), but there were also groups that exhibited little or no reduction over the last Cretaceous to the lowermost Paleogene (MacLeod et al. 1997; Norris 2001; MacLeod 2013). On land, plants suffered a sharp decrease in diversity that was previously underestimated (Nichols and Johnson 2008), and in many sections a short proliferation of ferns at the expense of angiosperms (“fern spike”) is documented. Among the tetrapods, amphibians, turtles, crocodilians, and eutherian mammals were only mildly affected by the K–Pg boundary event, whereas lizards and marsupials suffered heavy losses (Archibald and Fastovsky 2004; Longrich et al. 2012). Primates had their origin in the Late Cretaceous (Chatterjee et al. 2009; Steiper and Young 2009). Yet, because the oldest primate fossils date from the Paleocene (Williams et al. 2010), it is unknown whether this group experienced losses during the K–Pg extinction. For the ornithischians and the (nonavian) saurischians, this event was of course the end of a long era. Land‐dwelling species were more severely hit than freshwater inhabitants, endothermic tetrapods (including ornithischians and saurischians) more than ectothermic, and larger more than smaller species (Archibald 1996, 2011; Archibald and Fastovsky 2004). Evidence for both a gradual decline in dinosaur species richness as well as for a catastrophic and (geologically spoken) instantaneous extinction of the dinosaurs has been presented (Hurlbert and Archibald 1995; Archibald and Fastovsky 2004; see review in Brusatte 2012), but recent data indicate that there was no gradual decline in dinosaur diversity in the latest Cretaceous (Upchurch et al. 2011). The picture is equally complicated in marine exposures in which again evidence for both a gradual as well as a sudden extinction was presented (see MacLeod et al. 1997; D’Hondt 2005). Yet, resampling of formerly investigated sections extended taxonomic ranges upward, and the reported gradual decline of many groups might well be a consequence of the Signor–Lipps effect (Ward 1990). Among the possible causes for the K–Pg mass extinction that are still considered today are volcanism, climatic fluctuations, and marine regression and an asteroid impact (Benton 1990; Archibald 2011; MacLeod 2013). There is indeed overwhelming evidence that the Earth was hit by a major asteroid perhaps 10 km in diameter that had a devastating impact on Earth’s life. This evidence includes molten sediment particles (glass spherules), shocked quartz grains, and a worldwide recognized enrichment in iridium in K–Pg boundary layers (Alvarez et al. 1980, 1995). The impact hypothesis received further support with the discovery of a 66‐Myr-old impact crater (Chicxulub) on the Yucatan peninsula, Mexico (Hildebrand et al. 1991). Yet, it has also been demonstrated that the latest Cretaceous was a time of major climatic fluctuations (Skelton 2003) and the pronounced marine regression at the end of the Maastrichtian has been recognized for a long time. In addition, intensive volcanism, which spanned less than 2 Myr over the K–Pg boundary, is documented from the so‐called Deccan Traps (Courtillot 1990, 1999). These represent immense outpourings of lava in what is today India and must have had a profound impact on the biosphere (Kelley 2003). Currently, there are two schools of thought to explain the K–Pg mass extinction. According to the gradualistic, multiple-causes scenario (Archibald 1996, 2011; Archibald and Fastovsky 2004; MacLeod 2013), the climatic fluctuations and the marine regression near the end of the Cretaceous profoundly changed the available habitats in both the terrestrial and marine environments. This biotic stress led to a gradual decline in the dinosaurs and other terrestrial vertebrates. Likewise, the regression also imposed a major stress on the marine animals by reducing the available shelf environments. Further stress was imposed by the Deccan Trap volcanism that erupted large amounts Page 31 of 60

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of dust into the atmosphere, with general cooling of the globe, drying of many terrestrial ecosystems, and slowing of the photosynthetic activity as the most likely consequences. The asteroid impact at the K–Pg boundary is not disputed by most in the gradualist camp, but is seen merely as a moderate “last strike” that led to the collapse of already weakened ecosystems and extinguished animal groups that were already in decline (MacLeod 2013). Only a few researchers deny that the Chicxulub impact played a crucial role in the K–Pg extinction. These maintain that the impact either postdated (Hildebrand et al. 1991) or predated (Keller et al. 2003; Keller and Adatte 2011; Keller 2012) the K–Pg boundary by several hundred thousand years and that there were perhaps several impacts, all unrelated to the extinction. Yet, it has been shown repeatedly that the impact and the extinction were synchronous (Schulte et al. 2010; Renne et al. 2013). Those researchers who favor a single cause for the mass extinction at the K–Pg boundary emphasize the almost apocalyptic effects a bolide impact would have (Alvarez et al. 1995). This impact ejected considerable volumes of molten rock particles and dust into the atmosphere. Furthermore, it produced huge tsunami-type waves that devastated the coastal plains, and an immense fireball ignited vast wildfires. The dust particles would remain in the atmosphere for months, perhaps even years, leading to global cooling and darkening. Photosynthesis came almost to a halt, at least in plants adapted to higher light intensities. The fern spike recorded from many terrestrial boundary sections testifies to this sudden decline in higher plants and the spread of the ferns which could cope with darker conditions. As a consequence of the collapse of the ecosystems, first the consumers and then the carnivores died out within years. Those animals that did survive were preferentially small, unspecialized, opportunistic species that could feed on a variety of diets. That ecosystems were also severely and almost instantaneously hit in the marine realm is indicated by the patterns of the stable carbon isotopes across the boundary. These were previously interpreted as indicating an almost lifeless ocean after the K–Pg boundary (“Strangelove Ocean”; Hsu and McKenzie 1985; Zachos et al. 1989). Yet, marine productivity probably collapsed for only a few years (Alegret et al. 2012). The normal succession in Caribbean coastal sections agrees well with the impact scenario (after Alvarez et al. 1995): above the Maastrichtian limestone, larger airborne particles (microtektites, glass spherules) were deposited first, then come tsunami deposits containing reworked Maastrichtian limestone and charcoal (from wildfires), and then dust‐borne iridium and shocked quartz, and finally we see a return to normal sedimentation. Yet, a modified multiple-causes scenario seems at present to explain best the observed patterns (Archibald 2011; MacLeod 2013). Such a scenario emphasizes sea-level fluctuations, climate change, and continental flood-basalt volcanism, but accepts the Chicxulub as a devastating event that played a crucial role in the mass extinction.

Eocene–Oligocene Transition In a diagram of Phanerozoic extinction intensities, the Eocene–Oligocene transition period barely stands out as an important event, and yet this time marked the most significant episode since the extinction of the dinosaurs (Prothero 1994). The Eocene was a time of warm temperatures, with widespread tropical forests, archaic mammals, and reptiles occurring above the Arctic Circle (Prothero 1994, 2006; Ivany et al. 2003). Within a time period of 10 Myr, this “greenhouse” world shifted to “icehouse,” with decreased global average temperatures and markedly increasing seasonality, accompanied by major shifts in the biota of terrestrial environments and the seas (Berggren and Prothero 1992; Pälike et al. 2006; Zachos et al. 2008; Vandenberghe et al. 2012). The record in the marine environment is one of a rather gradual turnover. A displacement of warm‐adapted taxa by invading high‐latitude forms is observable in both planktonic and benthic Page 32 of 60

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taxa and was obviously accelerated around the Middle–Late Eocene (Bartonian–Priabonian) boundary and within the Early Oligocene (Rupelian) (Berggren and Prothero 1992; Prothero 2006). As much as 90 % of the genera disappeared in some groups (Hallam and Wignall 1997). Fishes survived this period almost unaffected, while among the whales the more basal archaeocete whales were replaced by the first modern toothed and baleen whales (Prothero 1994). On land, the flora changed between the Middle Eocene and Early Oligocene from widespread forests to open shrublands (perhaps with early grasses), and the leaf record as well as the amphibian and reptile fauna show a marked cooling and drying trend (Prothero 1994, 2006). Among the mammals, a fundamental difference between the Eocene and Oligocene faunas, the “Grande Coupure,” has long been recognized (Stehlin 1909; Legendre and Hartenberger 1992). In Europe, there is a gradual replacement of archaic by modern mammals throughout the Late Eocene and Early Oligocene, with a pronounced peak of extinctions at the Grande Coupure (Hooker et al. 2004). This latter event is now dated to the Early (but not earliest) Oligocene (Prothero 2006). Almost all new taxa are immigrants from Asia, which could reach Europe after the closure of the Turgai strait in the Ural region. Similar trends are observable on the other continents (Prothero 1994, 2006). High‐resolution oxygen isotope studies over the past decades have considerably helped to clarify the climatic evolution from the Early Eocene to the Early Oligocene. Global temperatures reached a peak between 52 and 50 Myr ago, during the so‐called Early Eocene Climatic Optimum (EECO). This was followed by a 17‐Myr-long trend toward cooler conditions, with a dramatic increase in d18O at the Eocene–Oligocene boundary (Zachos et al. 2001; Vandenberghe et al. 2012). This latter shift in the oxygen isotope values reflects not only cooling but also a significant increase of the Antarctic ice cap. The first ephemeral ice sheets appeared already during the Late Eocene and were probably the result of both declining atmospheric CO2 levels (DeConto and Pollard 2003) and an increasing thermal insulation of Antarctica. Plate tectonic movements had led to the separation of Australia and Antarctica and to the opening of the Drake Passage between Patagonia and Antarctica. By the end of the Eocene, the passage south of Tasmania was deep enough that the circum‐Antarctic cold deep current could become established and the Antarctic ice cap rapidly grew (Prothero 1994, 2006; Ivany et al. 2003; Kennett and Exon 2004). Yet, on land, the extinctions associated with the Eocene–Oligocene transition were not simply the result of global cooling, increased seasonality, and increasing aridity but also a consequence of large‐scale migrations. As an alternative or perhaps additional cause of the terminal Eocene turnover, impacts by comet showers have been proposed (Poag et al. 2003). Yet, the biotic turnover patterns do not correspond to an impact scenario (Ivany et al. 2003), and the Siberian Popigai (100 km) and the Chesapeake Bay crater (85 km) have now been dated as Late Eocene, when no extinctions occurred (Prothero 2006).

Pleistocene and Modern Extinctions

During the Pleistocene, between 2.6 and 0.01 Myr ago, the Earth witnessed large climatic fluctuations. Both plants and animals on all continents showed large shifts in their geographical distribution during this period, but the extinction levels were not above background values (Alroy 1999). This is true for such disparate taxonomic groups as insects, amphibians, reptiles, birds, and mammals. Yet, there is one major exception to this rule: the so‐called mammalian megafauna (animals > 44 kg). Fifty thousand years ago, more than 150 genera of this megafauna populated the continents, but by 10,000 years ago, at least 97 of these genera were extinct (Barnosky et al. 2004; Koch and Barnosky 2006). There have been continued debates over whether these extinctions were caused mainly by environmental changes associated with climatic fluctuations or were the consequences of human impacts. It is undisputed that humans were responsible for the extinction of large mammals Page 33 of 60

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and large birds on islands such as Madagascar, Antillean, Mediterranean, East Asian Islands, and New Zealand (Barnosky et al. 2004; Burney and Flannery 2005). Here hunting and habitat fragmentation led to extinctions, even in the absence of climatic change. An important aspect is that mammalian megafaunal species on all continents became extinct, but both magnitude and timing of the extinctions differed between continents (Roy 2001; Barnosky et al. 2004; Koch and Barnosky 2006). The extinctions were most severe in Australia where 14 out of 16 (88 %) giant marsupials succumbed. In addition, all seven genera of megafaunal reptiles and birds went completely extinct (Barnosky et al. 2004). Humans arrived on that continent somewhere between 71,500 and 44,200 years ago, and most megafaunal species became extinct before 40,000 years ago (Koch and Barnosky 2006; McGlone 2012). In North America, 33 genera (72 %) went extinct (Roy 2001) within a short time interval between 11,500 and 10,500 years ago, closely correlating with the arrival of Clovis‐style hunters (Alroy 1999; Roy 2001; Koch and Barnosky 2006). In South America, 50 genera (83 %) vanished during the arrival and spread of humans about 12,900–10,000 years ago. In Eurasia (excluding Southern Asia), 9 genera out of 25 (36 %) became extinct during two pulses (45,000–20,000 years ago, 12,000–9,000 years ago). These extinction pulses correlate also with the spread and then the population increase of modern humans (Barnosky et al. 2004; Koch and Barnosky 2006). In Africa, the losses were relatively mild at only 8 genera (18 %). When considering only mammals >1,000 kg, the differences between continents are even more marked. In North America all four genera were lost, Eurasia saw the demise of four out of five, but in Africa, no such genus went extinct (Roy 2001; Koch and Barnosky 2006). Many phases of human colonization were coeval with marked climate changes. Because earlier, similar climate changes were not accompanied by marked extinctions, hunting by humans (overkill) was proposed as the main mechanism responsible for the extinctions (Martin 1984), either by heavy and selective hunting (“Blitzkrieg”) or through habitat fragmentation, nonselective hunting, and the introduction of exotic species (“Sitzkrieg”). The current consensus picture for megafaunal extinctions on the continents is that extinctions were most pronounced where a rapid spread and increase in H. sapiens populations coincided with marked climatic shifts (Burney and Flannery 2005). But it was not primarily large-sized but rather slow-breeding species (this is, in part, correlated with large body size), which were at the highest risk of extinction (Johnson 2002). Even if the proportion of deaths caused by humans was low at any one time, slow-breeding megafaunal mammals were driven to extinction. Yet, the story is not over. Since the age of colonialization, the exploitation of nature has reached a new level, and the fate of the dodo (Raphus cucullatus) is just one very sad and telling example of human impact. This flightless bird was discovered in 1598 on Mauritius after Portuguese sailors first reached this island in 1507 and became extinct by 1690, not only by hunting but also by the introduction of domestic species, such as goats, pigs, and rats, which devoured the eggs and the young. The list goes on, and even extremely common species like the passenger pigeon in North America (Ectopistes migratorius) have proven to be no match for intensive hunting humans. Starting during the epoch of industrialization, exploiting nature and destroying natural habitats have proceeded at an ever-increasing rate (Wilson 1994). The human impact on nature has become so profound and is already so visible in the stratigraphic record (Wolfe et al. 2013) that for the time since the beginning of the industrialization the new term “Anthropocene” was proposed (Crutzen and Stoermer 2000; Crutzen 2002). It became accepted rather quickly in the scientific literature (Steffen et al. 2011; Zalasiewicz et al. 2012; Ruddiman 2013). There is no question that current extinction rates for plants and animals have reached in the Late Anthropocene a level perhaps 2–3 magnitudes above background rates (Nott et al. 1995; Pimm et al. 1995; Ricketts et al. 2005; Page 34 of 60

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Barnosky et al. 2011). Scaling the available estimates of current extinctions up to a magnitude where we can compare them to past Phanerozoic mass extinctions reveals that if species losses continue at the present rate, 96 % of species will be extinct within just a few hundred or thousand years (May et al. 1995; Sepkoski 1997; “Sixth” extinction). This is the maximum estimate for species losses during the most severe of all the Phanerozoic mass extinctions, the one that occurred at the Permian–Triassic boundary! Yet, although the end‐Permian mass extinction is no longer seen as a crisis spanning millions of years, current estimates are still on the order of a hundred thousand years. There is even further concern. As several episodes of mass extinctions have shown, even a moderate increase in global temperatures of a few degrees, if it happened fast enough, has proven fatal for life on the entire planet.

Conclusions After more than 30 years of intensive research, the picture of life’s diversification on Earth has attained an unprecedented level of accuracy. Much progress has been made in Precambrian research, notably in the study of the oldest fossils and their environment. Major input into studies of radiations and extinctions has come from geochronology, which has provided a new, accurate time scale. Other important developments have been the establishment of a new animal systematics and the considerable advances made in the dating of lineage splits. The quintessence of diversity studies, the global diversity trajectories for the Phanerozoic, has been refined in many ways, and Sepkoski’s classical, iconographic figure of the marine animals has recently come under scrutiny. Many of the dogmas are being reevaluated, a new database is being developed, and methodological problems are receiving considerable attention. What is needed for further refinement will especially be studies at the local level that take into account ecological data and ultimately can be assembled into a new global picture. Mass extinctions have received a tremendous amount of attention since 1980, and for most of them, a consensus interpretation exists today. Emerging is that each extinction event had its own signature, and no common cause has been found. Hot topics at the moment are the diversification of the metazoans and the Cambrian and Ordovician radiations, and here we will most likely see much progress in the next few years.

Cross-References ▶ Fossil Record of the Primates from the Paleocene to the Oligocene ▶ Paleoecology: An Adequate Window on the Past? ▶ Quaternary Geology and Paleoenvironments ▶ Taphonomic and Diagenetic Processes ▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments

References Aberhan M, Kiessling W (2012) Phanerozoic marine biodiversity: a fresh look at data, methods, patterns and process. In: Talent JA (ed) Earth and life: global biodiversity, extinction intervals and biogeographic perturbations through time. Springer, Heidelberg, pp 3–22 Page 35 of 60

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Aboussalam ZS, Becker RT (2011) The global Taghanic Biocrisis (Givetian) in the eastern AntiAtlas, Morocco. Palaeogeogr Palaeoclimatol Palaeoecol 304:136–164 Adachi N, Ezaki Y, Liu J (2011) Early Ordovician shift in reef construction from microbial to metazoan reefs. Palaios 26:106–114 Adoutte A, Balavoine G, Lartillot N, Lespinet O, Prud’homme B, de Rosa R (2000) The new animal phylogeny: reliability and implications. Proc Natl Acad Sci 97:4453–4456 Adrain JM, Westrop SR (2003) Paleobiodiversity: we need new data. Paleobiology 29:22–25 Alegret L, Thomas E, Lohmann KC (2012) End-Cretaceous marine mass extinction not caused by productivity collapse. Proc Natl Acad Sci 109:728–732 Algeo TJ, Scheckler SE (1998) Terrestrial‐marine teleconnections in the Devonian: links between the evolution of land plants, weathering processes, and marine anoxic events. Philos Trans R Soc Lond B 353:113–130 Algeo TJ, Chen ZQ, Fraiser ML, Twitchett RJ (2011) Terrestrial–marine teleconnections in the collapse and rebuilding of Early Triassic marine ecosystems. Palaeogeogr Palaeoclimatol Palaeoecol 308:1–11 Allen PA, Hoffman PF (2005) Extreme winds and waves in the aftermath of a Neoproterozoic glaciation. Nature 433:123–27 Alroy J (1999) Putting North America’s end‐Pleistocene megafaunal mass extinction in context: large‐scale analyses of spatial patterns, extinction rates, and size distributions. In: MacPhee RDE (ed) Extinctions in near time: causes, contexts, and consequences. Plenum Press, New York, pp 105–143 Alroy J (2010) The shifting balance of diversity among major marine animal groups. Science 329:1191–1194 Alroy J, Marshall CR, Bambach RK, Bezusko K, Foote M, F€ ursich FT, Hansen TA, Holland SM, Ivany LC, Jablonski D, Jacobs DK, Jones DC, Kosnik MA, Lidgard S, Low S, Miller AI, NovackGottshall PM, Olszewski TD, Patzkowsky ME, Raup DM, Roy K, Sepkoski JJ Jr, Sommers MG, Wagner PJ, Webber A (2001) Effects of sampling standardization on estimates of Phanerozoic marine diversification. Proc Natl Acad Sci 98:6261–6266 Alroy J, Aberhan M, Bottjer DJ, Foote M, F€ ursich FT, Hendy AJW, Holland SM, Ivany LC, Kiessling W, Kosnik MA, Marshall CR, McGowan AJ, Miller AI, Olszewski TD, Patzkowsky ME, Wagner PJ, Bonuso N, Borkow PS, Brenneis B, Clapham ME, Ferguson CA, Hanson VL, Jamet CM, Krug AZ, Layou KM, Leckey EH, N€ urnberg S, Peters SE, Sessa JA, Simpson C, Tomasovych A, Visaggi CC (2008) Phanerozoic trends in the diversity of marine invertebrates. Science 321:97–100 Alvarez L, Alvarez W, Asaro F, Michel HV (1980) Extraterrestrial cause for the Cretaceous‐Tertiary extinction. Science 208:1095–1108 Alvarez W, Claeys P, Kieffer SW (1995) Emplacement of Cretaceous‐Tertiary boundary shocked quartz from Chicxulub crater. Science 269:930–935 Appel PWU, Moorbath S, Myers JS (2003) Isuasphaera isua (Pflug) revisited. Precambrian Res 126:309–312 Archibald JD (1996) Dinosaur extinction and the end of an era: what the fossils say. Columbia University Press, New York Archibald JD (2011) Extinction and radiation: how the fall of dinosaurs led to the rise of mammals. Johns Hopkins University Press, Baltimore Archibald JD, Fastovsky DE (2004) Dinosaur extinction. In: Weishampel DB, Dodson P, Osmólska H (eds) The Dinosauria, 2nd edn. University of California Press, Berkeley, pp 672–684

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_16-3 # Springer-Verlag Berlin Heidelberg 2013

Index Terms: Big five mass extinction 14, 29 Cambrian explosion 7, 17, 21 End–Cretaceous mass extinction 30 End‐Permian mass extinction 8, 12, 26 End–Triassic extinction 29 Eocene–Oligocene transition 32 Fossils 6–7, 15, 19–20 Glaciation 4–6, 22 Jurassic 11, 29 K-Pg boundary 30 Late Devonian mass extinction 23 Late Ordovician mass extinction 22 Mass extinction 8, 14–15, 31 Mesozoic marine revolution (MMR) 29 Neogene 11 Ordovician radiation 21 Origin of life 2–3, 5, 20, 31 Paleogene 8, 31 Paleozoic 13, 27, 29 Phanerozoic 4, 7–8, 10, 12–13, 16, 25, 32 Pleistocene 33 Reefs 7–8, 17, 21, 27 Sixth extinction 35 Stromatolites 4, 21

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

Paleoecology: An Adequate Window on the Past? Thorolf Hardta*, Peter R. Menkeb and Britta Hardtb a Museum, Senckenberg Gesellschaft f€ ur Naturforschung, Frankfurt am Main, Germany b Institut f€ ur Anthropologie (1050), Johannes Gutenberg-Universita¨t Mainz, Mainz, Germany

Abstract Starting from Ernst Haeckel’s famous definition of ecology, our review considers the premises and the meaning of paleoecological research. Unlike current ecology, paleoecology has to pay more attention when dealing with “real” reconstructions. The concept of uniformitarianism is presented and demonstrates the importance of philosophical constructs in scientific work. Middle-range theory attempts to filter out false conclusions. Abiotic factors have had a strong influence on adaptive evolution; volcanism, tectonics, and climate exemplify this. Subsequently, we address biotic aspects of fossil findings, and in this context we discuss taphonomy, stratigraphic research, and interactions between floral and faunal environment. In a synthesis, we present three cross sections of human evolution at different time horizons (early-middle-late) to exemplify the inevitable multidisciplinarity of paleoecology, and we present some key events that probably altered the direction of radiations among hominids. Obviously, human evolution is not a special kind of evolution; it follows the rules of evolutionary biology, and hence depends undoubtedly on environmental influences.

Introducing (Paleo)ecology In a strict sense, paleoecologists try to detect all processes which have affected a fossil organism antemortem (Behrensmeyer 1992). Postmortem events are analyzed by the methods of taphonomy and by studying diagenesis (Andrews 1992; Lyman 1996). One has to realize that these two fields are inseparably linked when dealing with fossils and the reconstruction of their environments. Here is illustrated briefly what (paleo) ecology is, followed by a discussion of actualism (or uniformitarianism) as an essential aspect of paleoecology.

Neoecology Versus Paleoecology? Haeckel (1866, p. 286), who introduced the term “ecology” (German, oecologie; nowadays, € Okologie) stated: “Ecology is a part of science that deals with the relationships between organisms and their surrounding environment, wherein we can place all conditions of being in the broadest sense. These are of partly organic, partly inorganic nature; and both are of utmost importance for the form of organisms, because they force it to adapt to them” (translated and shortened by the authors). Haeckel included the following aspects in his “conditions of being”:

*Email: [email protected] Page 1 of 44

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

Table 1 Subsections of ecological research: (1) autecology that aims at all aspects of an individual as representative of its species and intraspecific questions, respectively; (2) demecology that deals with the interactions of a certain population with its environment; and (3) synecology that refers to all questions of interspecific relationships within an ecosystem Autecology Demecology Synecology

Reference object Single organism Homotypical community of organisms (population) Heterotypical community of organisms

Reference parameter Environment Contemporaries and environment Contemporaries and environment

Translated according to Schwerdtfeger (1968) and Tischler (1993) Table 2 The differences between contemporary ecology or neoecology and paleoecology Contemporary ecology or neoecology Source: currently living organisms in an intact ecosystem Precise and comprehensive description of environments and organisms in an ecosystem, parameters can actually be measured Potentially all faunal and floral components are available in the observed biocenosis

Paleoecology Source: fossil assemblages and age estimation data Mostly characterization of a former milieu in order to subsequently state inferences on environmental and organismic factors Fossils are the only documents available; hardly ever is the fossil record complete and many questions remain unanswered Data acquisition is limited to a few years or even months/ Excavated facies span a time of thousands and even days millions of years Compiled and extended from Etter (1994)

1. Abiotic factors (physical, chemical, climatic, electricity conditions; inorganic food; composition of water and soil) 2. Biotic factors (all relationships between organisms) More recently, modern ecology has been defined as “the study of the relations between organisms and the totality of the physical and biological factors affecting them or influenced by them” (Pianka 1983, p. 3). Among its most interesting branches are the distribution and frequency of organisms/populations/communities, hence natality, mortality, and migration (Begon et al. 1998). It makes sense to divide ecological research into three subsections (Table 1). All of these definitions are crucial when talking about ecology; however, for several reasons, it is not that easy to simply insert the prefix “paleo” for the study of ancient ecologies (Andrews 1992; Rull 2010). There are not only strong connections between paleoecology and recent (neo, contemporary) ecology (sensu Rull 2010) but also some basic differences (Table 2). In spite of these differences, Rull (2010, p. 1) claims that “. . .ecology and paleoecology are only different approaches with a common objective, which is the ecological understanding of the biosphere. [. . .] It is recommended that ecologists and palaeoecologists develop joint projects,” and further on “. . . a palaeoecologist is not simply a palaeoscientist whose data may be of interest for ecology but is primarily an ecologist working on another time scale, with different methods.” Paleoecological research is aimed mainly at analyzing long-term trends because when dealing with fossils, short-term processes (e.g., successions, microevolution) are not recognizable, or recognizable only with difficulty. Frequently, paleoecological analyses focus on the development of communities, in particular paleoenvironments, over time spans of millions

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

of years (Stanley 1994; de Menocal and Bloemendal 1995). Or they combine the fossil record with molecular phylogenetics focusing on diversification patterns and speciation requirements (Benton and Emerson 2007). Despite the fact that there is a conspicuous nexus between organismic paleoecology and geologically orientated facies observations, it is preferable in practice to separate the two, since both disciplines are in themselves multilayered and sophisticated networks (Etter 1994; Seppa¨ 2009; Sahney et al. 2010). Contemporary paleoecological questions include: • Are similar as well as different morphological characters linked to adaptations in the same kind of habitat? • Are there interdependencies between paleomilieu and life cycles/life-history parameters/population densities? • How is distribution and diversity of life on Earth dependent on ecological requirements – especially biome shifts and ecosystem development (Sahney et al. 2010)? • How do these transformations interact to species adaptation/migration and population changes? • Can extinction and even speciation events be traced back to major changes in the environmental conditions, and if so, to which? • What are the rates of speciation and extinction? All of these questions require a high degree of multidisciplinarity and cannot be solved only in terms of single-factor analyses (Seppa¨ 2009). They also have to encompass multiple factors that build ecosystems like the one covering our planet. After a short look at the approach of actualism/uniformitarianism, we will take the previous quotation by Haeckel as a guidepost for the following sections. After touching on abiotic factors, we proceed to the biotic ones and finally merge them in a third step that we designate as synthesis. In the latter we try to focus on hominid or near-hominid evolutionary perspectives and ignore, because of solely talking about terrestrial systems, important paleoecological aspects that refer to marine ecosystems. “The Present Is a Key to the Past”: A Valid Premise? One of the most important concepts in the geosciences is uniformitarianism, a principle introduced by the Scottish physician and geologist James Hutton (1726–1797). Originally, this was framed as an antithesis to the idea that catastrophic phenomena might have formed the Earth’s surface. It was the establishment of the idea that the laws of nature stay constant that made geology a mature part of the scientific endeavor. This philosophical approach is axiomatic in physics, but it was Sir Charles Lyell, “Darwin’s guru and intellectual father figure” (Gould 1994, p. 6764), who placed this idea before a broader scientific community. The application of this principle inspired Darwin, although Gould (1994) warned against the pure extrapolationism of Darwin’s uniformitarian perspective. Gould’s (1994, p. 6768) attractive musings on paleontology’s meaning are more important than ever. The simplemindedness of universal reduction to lower levels must be abandoned: “Our evolutionary world is a hierarchy of levels, each of legitimacy and irreducible worth.” Riedl (1981) also emphasized the limitations of each methodological level. Based on Gould (1984); Etter (1994) reduced the philosophy of actualism to four principles: 1. 2. 3. 4.

Laws of nature do not change on Earth in time and space. Processes that influenced geological phenomena in the past occur in the same manner now. The speed of geological and biological processes does not change. In the past the same materials and the same conditions existed. Page 3 of 44

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

The first two of these are methodological assumptions that are necessary to conduct inductivist research. Points three and four are less definite. As Etter (1994) points out, the adoption of all four premises may be limited due to (1) constraints of observing the past and (2) the strong fluctuations of geological phenomena which occurred long ago (e.g., the circumstances of the dinosaurs’ extinction). Even if the core of uniformitarianism is still valid, today’s researchers expand their view, monitoring large-scale systemic processes or patterns that may explain what we are really able to learn about the guidelines in the continuum past-present and how we are able to adopt the results for future predictions (Dearing et al. 2006; Rull 2010). Although the mass of available data increases drastically, we should not forget to use the fossil record as a “litmus paper” to adequately evaluate the results (Jackson and Erwin 2006). Dodd and Stanton’s (1990) taxonomic uniformitarianism is a derivative of substantive uniformitarianism and an attempt to reconstruct ecological niches by assuming that the environment of a fossil will have been identical with that of the nearest extant relative. But it is obvious that reliable conclusions can only be made in this way if a fossil is a member of an extant species. This can virtually never be the case except for Pleistocene and Holocene deposits (Etter 1994), and even then there are also theoretical problems, one of which is the fragmentary knowledge researchers have of former ecological niches. An absence of enemies could, for example, have caused an expansion of the niche. Thus Etter (1994) admits that taxonomic uniformitarianism should be limited to fossils with extant representatives or relatives. Yet the method can be improved by investigating groups of species within a taxonomic group rather than just one. Tattersall (1998) reviewed such provocative ideas of evolutionary biologists as Dawkins’ “Selfish Gene” and Eldredge and Gould’s “Punctuated Equilibria” (Eldredge and Gould 1972) and also relativized the meaning of adaptationism (p 95: “. . .organisms may not be as exquisitely fine-tuned to their environments. . .”) in our evolutionary thinking. Therefore, no one should forget that there exists a possibility of overstraining positivism, thus using only verified results as a basis for the interpretation of our findings. Actio-reactio thinking is of course essential and the only way of doing science in general, but the danger of storytelling in paleoecology is acute (Henke 2010). Scientists are at risk of delivering explanations for adaptations which could be true, but actually might not be (see later). It is questionable whether the equation Bauplan : environment ¼ 1:1 is satisfied. Foley (1978) linked the past and the present by invoking Binford’s (1977, 1981) middle-range theory. This is actually an assemblage of theories that link observable aspects of the past to processes operating today and permit inferences about the conditions of geological and biological systems in the past. Such observations must be linked to observable past phenomena (i.e., an anatomical element) (Fig. 1). The connecting piece between a theory (deductions and predictions from a basis of axioms) and the data is the model (which describes and predicts the variation and structure of phenomena derived from theoretical principles). Foley (1987) also points out that there are different levels of model building, depending on behavioral (predepositional) and geological (postdepositional) factors. Furthermore, identical records might be produced by different behaviors (Hill 1984; Foley 1987), so the overlap of different models has to be taken into consideration. Four pathways are very useful for testing a theory in order to reduce the pure reflection of contemporary ideas: (1) a careful analysis of each link in an inferential chain; (2) like Binford (1981) not following the broad trend, but rather looking for small details that might appear comparatively insignificant; (3) the isolation of processes that may result in similar results and assigning (theoretically/experimentally) the probabilities of various outcomes; and finally, (4) the comparative biological approach, which investigates patterns

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

Fig. 1 Linking the past and the present. Interpreting the fossil record and reconstructing life in the past depend on the understanding of the process of transformation during fossilization. This is inferred by observations of contemporary fossil information or the way in which observable behavior in the present would be visible in the fossil record (After Foley 1987)

Fig. 2 Implications of the middle-range theory: a summary of pathways to the past (Modified from Foley 1987)

of interspecific and intraspecific variations that can be used to correlate biological variables (Fig. 2). Ecology and Cladistics The a priori assumption that a particular character (or character state) is the result of a particular evolutionary process may lead to far greater problems of circularity than does the incorporation of these characters into a global estimate of evolutionary history (Luckow and Bruneau 1997, p. 150). These authors infer that the exclusion of ecological information from a phylogenetic analysis when testing ecological hypotheses is not only unnecessary but also “undesirable.” Luckow and Bruneau (1997) justified their arguments by concluding that character exclusion would partition the data in an arbitrary way and that discrete homology statements would get lost.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

Abiotic Factors Throughout natural history, the physical conditions of the Earth have had a strong influence on evolution, adaptive or otherwise, and consequently on human evolution (Dearing et al. 2006). Environmental changes shape the habitats and the evolutionary “fates” of living systems (see also Vrba, “▶ Role of Environmental Stimuli in Hominid Origins”). One fundamental aim of evolutionary biology is to understand and reconstruct the interaction of physical environmental stimuli and the survival of organisms – even in human evolution (Potts 2012; Bailey et al. 2011). Wegener (2005, p. 222) wrote: “Only by summing up all fields of the geosciences may we hope to find out the “truth,” this means determining a picture that integrates all known facts in the best order and which seems to represent the utmost probability; even then we have to be aware that each discovery, regardless of which scientific field it emanates from, may modify the result” (translated by the authors). Earlier acceptance of this neglected genius’ appeal for an adequate scientific network might have accelerated the unraveling of the Earth’s physical secrets.

Geological Influences Volcanism In the truest sense of the word, volcanoes put pressure on their environments. Usually eruptions have a localized but strong influence. However, tephra (ejecta, e.g., ash or pumice) and lava do have the potential to modify water and soil chemistries, thereby eliminating or modifying habitats over wide areas. Occasionally they also support the conservation of important fossil footprints. Including sea floor and continents, about 80 % of the Earth’s surface has been produced by ascending melted rock, primarily at plate boundaries. Volcanic material creates a useful (though blurred) perspective on the Earth’s interior. The Earth’s lithosphere also delivers nutrients, chemical resources, and minerals (Press and Siever 1995). Feibel (1999) investigated eruptive activity in the Turkana area of northern Kenya and concluded that the higher assumed rate (38 events per 240,000 years) indicates one significant eruption per 6,300 years. Massive eruptions can also cause global impacts since they glut the atmosphere with climate affecting aerosols. Rampino and Shelf (1992) discussed the controversial idea of the Mount Toba explosion 74,000 years ago, which might have produced a sharp cooling and consequently a temporary shift to glacial conditions. Even today volcanoes are able to paralyze parts of Homo sapiens’ “modern life” if you imagine the eruption of Iceland’s Eyjafjallajo¨kull and ash-cloud-induced air-traffic breakdown in Northern and Middle Europe in 2010. Tectonic Aspects Faulting within local sedimentary basins, continental plate movement, and highland formation through uplift may greatly affect terrestrial habitats (Chernet et al. 1996; Trauth et al. 2007; King and Bailey 2006). Between 16 and 12 Ma, the Eurasian and the Afro-Arabian continental plates moved and allowed an exchange of the flora and fauna, e.g., an exodus of early African apes (Potts 2003). Between 7.0 and 5.0 Ma, the Atlantic Ocean and the western end of the Mediterranean were temporarily separated as Africa drifted northward. Here, a periodic drying and flooding of the Mediterranean basin occurred and huge salinity deposits were built up. Western Eurasia dried out due to an evaporation and salinization phenomenon. Between 4.5 and 3.0 Ma, the Isthmus of Panama was formed by the contact of continental plates and the following uplift (Stanley 1995). One result was the strengthening of the conveyor belt of Atlantic Ocean currents: the North Atlantic was “watered” by the warm Gulf Stream. The initiation of ice ages in the Northern Hemisphere

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

during the Late Pliocene can be explained by the development, over 36 Ma, of isolation of the Arctic Ocean caused by a high-salinity, warm, sinking, and returning current (Stanley 1994). Rift Valley formation in eastern Africa and the uplift of western North America and the Tibetan Plateau are examples of drying and cooling effects. Models of general circulation show that when major air currents are divided by elevated plateaus, the air is altered due to winter cooling and summer heating, causing high- and low-pressure areas to form over landmasses far from the plateaus (Ruddiman and Kutzbach 1989). One consequence is a greater seasonal variation and also the creation of seasonal monsoons. The overall effect is a cooler and drier global climate (Ruddiman et al. 1989). Even geochemical weathering on rocks can be traced back to uplifts: enhanced monsoons, steepening river gradients, and faster erosional rates increase weathering. Raymo and Ruddiman (1992) suggested that global cooling might result from the deposition of carbon from the highlands into the ocean as well as from weathering responses. A consequence would be a reduction in carbon dioxide and its removal from the atmosphere. The heat-retaining function of carbon dioxide as a major greenhouse gas would disappear as a result. Another effect occurs on the leeward sides of uplifted regions: upland depletion of air moisture and precipitation cause rain-shadow drying, a phenomenon partly responsible for the aridification of the area to the east of the African Rift Valley compared with its western counterpart. Another possibility is that the shapes of sedimentary basins are modified by the local impact of earthquakes. Availability of water to the local biota is obviously a very important factor, so the changes of fluvial systems by intrabasin faulting mechanisms are also a matter of paleoecological discussion. Eastern Africa is a superb example to illustrate intracontinental rifting phenomena. During the Cenozoic, a system of continental rifts developed from the Red Sea and the Gulf of Aden in a southward direction from the Afar region of Ethiopia, which is a triple junction where three developing tectonic plates come together (Figs. 3 and 4; Table 3). Such phenomena are widespread. A former triple junction existed where Africa and northern and southern America came together. The Amazon, the Mississippi, and the Niger all represent rivers that run through “failed rifts.” Afar is characterized by three spreading zones and represents a small portion of oceanic crust that has been uplifted and is now part of the continent (Stanley 1994).

Climatic Influence Cycling Planet Earth The Milankovitch cycles (Reed volume 1, “▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments”) are a consequence of the changing gravitational pull of other planets. Variation in solar heating, which is related to astronomical cycles that alter the orientation and shape of the Earth’s orbit around the Sun, is attributed to these periodic oscillations. The distribution and strength of solar radiation change over the globe in periods of 19, 23, 41, and 100 thousand years (Hewitt 2003). How can these periods be detected? Oxygen isotopes are documented in the deep-sea record and represent measurements of the global ice volume, ocean temperature, and evaporation. Around 3.0–2.5 Ma, the amplitude and frequency of d18 O oscillation changed significantly. Northern Hemisphere glaciations and greater aridity in the tropics both correspond to this pattern. Between 900 and 600 ka, the effects of 100,000-year-long cycles of glacial forming and interglacial warming came into play (Hewitt 2003). The 23,000-year cycle of the Earth’s rotational axis intensifies African monsoons, and the millennial-scale instability causes North Atlantic iceberg discharge. This involved huge masses of ice rafting and melting and a decrease of ocean salinity. Taylor et al. (1993) and Bond et al. (1997) traced this phenomenon back to decade- to century-scale fluctuations between near-glacial Page 7 of 44

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

a

ope

Eur

bia ra i-A ud Sa

Africa

Eurasian Plate

Arabian Plate Indian Plate African Plate

b

Eastern Rift System Western Rift System

Indian Ocean

Rifting process Plate boundaries African Rift Zone

Arabian Plate Triple junction Afar region Turkana Basin

c Fig. 3 African Great Rift Valley system (a) and rifting process (b) with accentuation of the Afar triangle and the Turkana basin (c)

conditions and interglacial warmth. Raymo et al. (1998) and McManus et al. (1999) linked these conditions to the Late Pleistocene and Early Holocene. Well-defined cycles are not necessarily well separated in terms of amplifying and buffer mechanisms. Their interactions show complex patterns, as Clemens et al. (1996) and Paytan et al. (1996) have demonstrated. Furthermore, Potts (2003, p. 365) stresses that “major environmental shifts occurred episodically throughout the Quaternary and did not necessarily coincide exactly with maximum changes in temperature, moisture, or any other single factor.” Lister and Rawson (2003) called attention to the rise and fall of sea level, one major effect of the climatic ups and downs: over the past 600,000 years, fluctuations of up to 120 m are documented. Inundations as well as the exposure of continental shelves created new barriers or pathways. Like others Maslin and Christensen (2007) assume coherence between, on the one hand, extreme climatic variability caused by tectonic changes and orbital forcing and, on the other hand, speciation and dispersal Page 8 of 44

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

Fig. 4 Schematic representation of tectonism, volcanism, and sedimentation processes within the Ethiopian Rift System (WoldeGabriel et al. 2000)

events in human evolution. Ann Gibbons brought together several researcher’s suggestions linking climatic variability to major events in human evolution like speciation or the development of modern stone tool technologies like the Acheulean (Gibbons 2013) under the title of “How a fickle climate made us human.” Our Planet’s Oceans The Earth’s climates were much wetter and warmer before Middle Eocene times, and deciduous and evergreen forests dominated the natural scenery. Antarctica was full of temperate rain forests, and Arctic landmasses were covered with trees (Askin 1992; Denton 1999). A strong seasonality and a general lack of aridity reduced the occurrence of grasslands and deserts. Sea ice and glaciers were limited in their volume expansion (Ruddiman and Kutzbach 1991). The world’s oceans were about 10  C warmer at depth than today. Furthermore, the atmospheric temperature gradient – from the equator to the pole – was much smaller than today (Savin et al. 1975; Shackleton and Boersma 1981). This changes when throwing a glance at the recent situation. Since the Middle Eocene, global climate has cooled down. Shackleton (1995) discussed the essential global paleoclimatic change at 2.95–2.52 Myr and the beginning of the oscillating ice ages. Over the past 0.95 Myr, each glacial maximum was on average 5  C cooler than today and the planet was drier, e.g., much of Northern Europe was covered by tundra and Africa was drier (Denton and Hughes 1981; Denton 1999). Another Unique Continent: Africa deMenocal (2004) gave us a very useful overview of the African climate: as Fig. 5 demonstrates, the combination of the seasonal migration of the intertropical convergence zone and the African

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Modified from WoldeGabriel et al. (2000)

Areas with paleoanthropological Location within Sedimentary sites the rift environments Age of tuffs Shungura Usno Fejej Omo rift Lacustrine, 4.1–1.39 Ma fluvial, overbank Konso-Gardula Southern MER Fluvial 2.0–1.35 Ma (Main Ethiopian Rift) Gademota (Middle Central MER Colluvium, 35–1.81 ka MSA) paleosol Gadeb Eastern rift Lacustrine, 2.51-ca. 0.7 Ma shoulder, fluvial Central MER Melka Kunture` Central MER Fluvial < or ¼ 1.5 Ma Kesem-Kebena Northern MER Lacustrine, 1.04–1.0 Ma (K-K6) fluvial, lacustrine Middle Awash Southern Afar Fluvial, 4.38–4.29 Ma overbank, lacustrine Hadar West-central Fluvial, 3.4–3.18 Ma Afar overbank, lacustrine 2.94–4

Estimated at 40

n.d. 62

Estimated at 50

n.d.

5

4

None

A. afarensis, H. erectus

A. ramidus, H. erectus, A. garhi

H. erectus H. erectus

H. erectus

H. sapiens

Percentage of tuffaceous sediments in stratigraphic column Hominid species Estimated at 70 A. afarensis, A. aethiopicus, A. boisei, H. habilis, H. erectus 95 H. erectus

Tuffs; percentage of stratigraphic section 9

Number of tuff beds/Ma (preserved) 13

Table 3 The Ethiopian Rift System and some important paleoanthropological sites

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

Fig. 5 (a) Regional map of North Africa vegetation zones, locations of DSDP and ODP drill sites ( filled circles), and locations of selected African mammal fossil localities (open diamonds). (b) Boreal summer (August) surface wind stress (unit vector ¼ 1 dyn/cm2), intertropical convergence zone (ITCZ, heavy dashed line) location, and boundaries of seasonal tropospheric dust plumes off NW Africa and NE Africa/Arabia. Dust plume contours were derived from haze frequency data. (c) Boreal winter (January) surface wind stress (unit vector ¼ 1 dyn/cm2), ITCZ location, and boundary of the seasonal tropospheric dust plume off NW Africa (Reprinted from deMenocal (2004), with permission from Elsevier.)

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

monsoon causes a highly seasonal range of North African rainfall. In the boreal summer, heat over the North African land surface, centered near 20 N, draws moist maritime air from the equatorial Atlantic into western and central subtropical Africa. Accordingly, woodland and grassland savannahs flourish (Hastenrath 1985; Harris 1980). Based partly on topographic rain-shadow effects, summer rainfall in East Africa is very variable. It is also related to the westerly airstream of the African monsoon (Nicholson 1993). East Africa’s subtropical rivers, such as the Omo and the Nile, are drained by the summer monsoonal runoff via the capture of moisture by Ethiopian and Kenyan Highlands. On the other hand, relative to adjacent oceans, Asian and African landmasses become cooler, and a reversion of the atmospheric circulation comes about (deMenocal 2004). Prospero and Nees (1986) showed that the changes of subtropical African summer rainfall are closely tied to West African dust export to the Atlantic. Additionally, these modifications have been linked by Giannini et al. (2003) to anomalies of the sea-surface temperature. Fig. 5b demonstrates that Indian monsoon surface winds are interconnected with summer dust plumes of Arabia and Northeast Africa (Nair et al. 1989). These winds carry mineral dust to the Arabian Sea and the Gulf of Aden. The study of mineralogical and sedimentological data reveals that windborne detritus “from these sources comprises the dominant source of terrigenous sediment to the eastern equatorial Atlantic and the Arabian Sea” (deMenocal 2004, p. 7).

Marine Paleoclimatic Records The last (ca.) 5 Myr, during the Late Neogene, showed progressive steplike increases in African aridity and periodical arid-humid climate cycles. This conclusion can be drawn from marine sediments accumulating off the western and eastern margins of the subtropical North African region. The isolation of the Atlantic basin via the Isthmus of Panama and the following gradual onset of high-latitude glacial cycles at 3.2–2.6 Ma seem to have influenced African climate variation patterns (Haug et al. 2001). The onset of glacial ice rafting and modest 41-kyr glacial cycles after 2.8 Myr caused Plio-Pleistocene cooling at high latitudes. Another step was a shift toward cooler conditions and, after ca. 1.6 Myr, higher-amplitude 41-kyr cycles after 1.2–0.8 Myr (Shackleton et al. 1984). Variability of subtropical African paleoclimate: deMenocal (2004) summarized the patterns of marine sediment records of Plio-Pleistocene eolian export from West and East Africa: • The variability of orbital-scale African climate variability persisted throughout the entire interval (and in some cases extending into the Miocene and Oligocene). • The onset and amplification of high-latitude glacial cycles was closely linked to the onset of large-amplitude African aridity cycles. • A gradually increasing increasing of eolian concentration and supply (flux) after 2.8 Myr. • At 2.8 (0.2), 1.7 (0.1), and 1.0 (0.2) Myr, there were steplike shifts in the amplitude and period of eolian variability. • There is evidence for 104- to 105-year “packets” of high- and low-amplitude paleoclimatic variability which were paced by orbital eccentricity. deMenocal (2004, p. 8) described the marine record as “a succession of wet-dry cycles with a long-term shift toward drier conditions, punctuated by step-like shifts in characteristic periodicity and amplitude.” de Menocal (1995) interpreted subtropical African climate prior to 2.8 Myr as varying at the 23- to 19-kyr period, mainly as a result of Asian monsoonal variability. At 2.8 (0.2) Ma, there was a shift toward climate variation periods longer than 41 kyr, and after 1.7 Page 12 of 44

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

(0.1) Myr, the cycles lengthened again, and an eolian variability shift toward longer- and largeramplitude 100-kyr cycles after 1.0 (0.2) Myr occurred. The onset and growth of high-latitude ice sheets and cooling of the subpolar oceans were synchronous with these shifts in the African eolian variability (Shackleton et al. 1990), and there was a coupling between high- and low-latitude climates after the glaciation onset near 2.8 Ma (deMenocal 1995). Dupont and Leroy (1995) showed that a pollen record from site 658 documents the phenomenon of greater variability and progressively xeric vegetation after ca. 3.0 Myr and concluded that a shift toward a drier and cooler African climate occurred during glacial maxima. The pollen record correlates with oxygen isotopes, indicating that large global ice volume and deep-sea temperatures correspond to aridity. These authors conclude that a comparison of short-term fluctuations of periods before and after 2.5 Myr demonstrates “that obliquity forcing of northwestern African climate started with the first large glaciations in the Northern Hemisphere” (p. 297). Which phenomenon is the fundamental impulse generator for African climate variability? The Plio-Pleistocene succession of sapropel layers in the Mediterranean Sea could be interpreted as a consequence of orbital precession (Hilgen 1991). Enhanced monsoonal and Nile river runoff led to increased Mediterranean stratification and reduced ventilation of the deep eastern basins (Rossignol-Strick 1985). During these humid periods, organic-rich layers were deposited. However, another stimulating factor could be a covariation of African climate with the high-latitude climate cycles at the 41- and 100-kyr periodicities, which is what marine sediments actually suggest. deMenocal (1995, 2004, p. 10) tried to reconcile the two different points of view “by acknowledging that precession was the fundamental driver of African monsoonal climate throughout the late Neogene, but that high-latitude glacial cooling and drying effects were superimposed on this signal only after 2.8 million years.”

Physical (Paleo)geography or the Beauty of Mosaics The African continent extends virtually equidistant into both the Southern and the Northern Hemispheres. It includes about 20 % of the world’s land surface and stretches 8,000 km from north to south. The configuration of the bordering oceans and landmasses has remained almost the same from the Early Pliocene up until today (O’Brien and Peters 1999). Based on the pioneering work of Lobeck (1946); O’Brien and Peters (1999) subdivided Africa into different physiographic regions (Fig. 6). In Low Africa, during most of the Pliocene, all of the interior basins may still have lacked outlets to the sea, a condition not existing today. Prerift Africa’s (Miocene-Pliocene) interior basins and associated drainage systems are nowadays etched by old deltas, strandlines, old terraces, and alluvial deposits. This might indicate (at least) seasonally expansive internal lakes, e.g., the Paleolake Congo. This was probably a perennial water body up to at least the Late Pliocene, and its eastern catchment extended to the High Interior Plateau and the volcanic highlands of the Eastern Rift Belt (O’Brien and Peters 1999). In the Oligocene, High Africa was tectonically driven by the African swell, which was active again in the Late Pliocene and Pleistocene. Different effects have influenced southern and eastern Africa: during the Late Pliocene, local environmental and increasing subregional fragmentation took place. During the Early as opposed to the Late Pliocene – up to 3.0 Myr – the rift grabens associated with doming were shallow and also at higher elevations than now (Brown 1995). The Ethiopian Massif was probably lower than now, while the High Eastern Interior Plateau may have been higher (Feibel 1999). Between 3.0 and 2.0 Ma, an uplift of rift shoulders by 1,000–1,500 m and a concomitant major subsidence of rift grabens occurred: (1) first in the Eastern Rift Belt areas and in the Afar region and later (2) in the Western Rift Belt, where some of the uplifted flanks rose Page 13 of 44

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

Fig. 6 Physiogeographical divisions of Africa (After O’Brien and Peters 1999)

to 4,000 and more meters above sea level (Partridge et al. 1995a, b). The eastern drainage perimeter for the Congo Basin was established by the escarpment mountains of the Western Rift Belt, which also caused a diversion of the westward drainage from the Eastern Rift Belt and the Interior Plateau, into the Sudd. The Rift Valley domain of the East African Highlands was particularly perforated by active volcanoes (O’Brien and Peters 1999). Africa’s Southern Platform was formed by subsidence events resulting in local fragmentation of the environment (exceptions: areas immediately adjacent to subsided or uplifted margins) and by broad-scale regional uplift. The Southern Platform was apparently lower in elevation than nowadays by some 200 m in the southern escarpment mountains and by as much as 1,000 m in the extreme southeast. The Transvaal, however, was somewhat higher than today (maybe by about 400 m). Furthermore, the paleolakes of the Southern Platform are of special interest for hominid ecogeography (e.g., Makarikari). The grabens of the Western and Eastern Rift belts in the East African Highlands contained intermittent rivers and lakes. Lake Malawi, however, obtained its present shape only at the end of the Pliocene (Partridge et al. 1995b; O’Brien and Peters 1999).

Biotic Factors Together, abiotic factors build a framework for living spaces that frequently harbor more than one population (Ziegler 1992). These spaces are called biotopes, with their enclosed organismic communities characterized as biocenosis. These often include highly adapted and specialized

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

Fig. 7 Four key events in the history of a fossil and the related paleontological disciplines (After Lawrence 1968)

species in numerous ecological niches; together they build the so-called ecosystems or biomes. The goal of paleoecologists is to reconstruct these systems or paleoenvironments based on organic and inorganic remains. In the following section, we concentrate mainly on fossils and their interpretation and on the factors that influence them and thus have to be analyzed when reconstructing paleoenvironments. We touch on questions of postmortem processes, stratigraphic research, and coevolution. Due to the fact that we spotlight hominid and accordingly terrestrial evolution, we omit an extensive debate on plant fossilization and exclude aquatic ecosystems.

Fossils A fossil is any remain or trace of any organism from all past periods. They are the key elements of paleontology and consequently of paleoanthropology and paleoecology and act as containers or archives that preserve information over a long period. Scientists who deal with fossils have to find the right tools to open and unravel the secrets lying within. The following paragraphs illustrate some of these “tools” and enlighten several approaches of paleoecological research. What Happened Antemortem and What Postmortem? It is unlikely that an organism will be preserved through time after death. Less than 1 % of all species of organisms are handed down to us (Ziegler 1992; deMenocal 2004), especially in terrestrial and tropical conditions, also in the case of hominoids (Carroll 1988; Martin 1990; Stanley 1994; Andrews 1990). Due to this, the density of relevant paleoanthropological fossils is very low – approximately one fossil per one hundred generations – and there are a lot of gaps that affect the phylogenetic and ecological reconstructions scientists strive for (see later). Besides this, most fossils are fragmentary or incomplete and require reconstruction by means of all available methods, now including 3D reconstruction using CT, MRT, or surface scanning (Weber, “▶ Virtual Anthropology and Biomechanics”). Additionally, researchers have to consider the limited erosion of noteworthy ancient fossil sites on the African continent, since most areas are covered with tropical forest, as well as the political and financial circumstances that impede excavations on the other hand. Every fossil contains a great deal of information on the evolutionary history (phylogeny), physical organization (morphology), and lifestyle (ecology) of the populations the organism once belonged to. Under ideal circumstances, it is possible to extract most of this information by careful analyses of the taphonomic and diagenetic processes involved. Taphonomy, as a special field of paleontology, represents the description and causal analysis of all factors that influence an organism after death (necrology and biostratinomy) (Fig. 7) and subsequently all processes of

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

Fig. 8 Three essential components of the study of fossils in context (Adapted from Behrensmeyer 1992)

embedding and fossilization (Efremov 1940; Lyman 1996; Grupe, “▶ Taphonomic and Diagenetic Processes”). In contrast, diagenesis characterizes only the biological, physical, and chemical alteration of the mineralogical elements affecting fossil-bearing sediments and is part of taphonomy and the lowest grade of rock metamorphism (Stanley 1994; Lyman 1996; Conroy 1997). The possibility that an organism will be fossilized after death – its transition from the bio- to the lithosphere – depends on many environmental factors (Foley 1978; Henke and Rothe 1999). With few exceptions, the soft tissue – if not eaten by predators or scavengers – undergoes the physiological processes of decomposition and decay in the first phase after death (necrology), and normally only hard materials like the teeth, bones, shells, and rarely scales and horn are suitable for being mineralized and thus fossilized. The most important participants in this process are calcium in the form of calcite and aragonite (CaCO3), bone apatite (Ca5(OH)(PO3)), silicic acidskeletal opal (SiO2), chitin, cellulose, and scaffold proteins (spongine, creatine). Who Are You? Where Do You Come From? What Brought You There? The only way to reconstruct ancient ecosystems is to examine the fossil record and elucidate the internal and external influences that led to the life-forms. Following Etter (1994), there are three crucial requirements that have to be fulfilled when analyzing fossils: 1. Accurate determination and systematic classification of the collected specimen 2. Putting all investigated profiles in a temporal and stratigraphic order as precisely as possible 3. Understanding the ecological context and the specific adaptations of the organisms that enable it to live in particular environments In brief, paleontologists and paleoanthropologists, respectively, have to study fossils in context to understand the processes occurring in interrelated evolving systems (Fig. 8).

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Who? Taxonomic classification is not only essential but also complicated and depends on whatever evolutionary theory, species concept, and taxonomic approach the researcher prefers (Delson 1990; Foley 1978; Tattersall 1992, 1996; Wood 1992, 1996; Wood and Collard 1999; Wolpoff 1999; Wheeler and Meier 2000; Sarmiento et al. 2002). All these questions go beyond the scope of this chapter and are discussed elsewhere in these volumes (Ohl, “▶ Principles of Taxonomy and Classification: Current Procedures for Naming and Classifying Organisms”). Academics need to overcome the subject-object problem (Stadler et al. 1977; Vogel 2000) when analyzing how we “became human” or even when assembling or disassembling new genera or species – not to mention new hypotheses or theories – as soon as possible after finding new hominid remains. In the words of Eric Delson: “The paleoanthropology community must look quite Pavlovian to outsiders – we all drool predictably every time a new fossil is discovered” (Delson 1997, p. 445). Obviously, new fossil findings complicate the puzzle of primate and hominid evolution (Foley 1991; Tattersall 1992, Marks, “▶ Genetics and Paleoanthropology”). Since Darwin’s ideas about natural selection and his groundbreaking theory of evolution via selective forces were published in 1859, much has been learned about the processes that generate species and the debate is still in progress. Using the individual specimens that constitute the fossil record, we can indirectly scrutinize ancient organic systems at definite points in time (“semaphoronts” sensu Hennig 1982). One affiliated evolutionary theory, “punctuationism” (antonym: gradualism) postulates rapid evolutionary development at the nodes of the “Tree of Life” and long periods (branches) with slow rates of evolutionary change. Associated with the latter is a crucial problem of fossil research, for the chance of finding and moreover identifying “node fossils” (once called “missing links”) is significantly lower than of finding “branch fossils.” Another accompanied question arises: Are “node fossils” detectable at all or are we entangled in fossils that show mosaic-like plesio- and apomorphic character stages making it nearly impossible to fix a borderline between species – even genera? However, human evolution is strongly embedded within the framework of evolutionary biology and has to be seen as a chain of adaptive radiations (Foley 2002) and extinction events. Where and When? One of the most important factors when reconstructing ancient ecosystems is the time dimension and thus the absolute and relative determination of age (dating). Stratigraphers subdivide sediment layers chronostratigraphically and put them in a hierarchic system (Table 4; Fig. 9). Each unit within a stratigraphic system has been defined by means of a basal Global Standard Section and Point (GSSP) by the International Commission on Stratigraphy. Absolute dating, or chronometrics, is done by direct chemical (e.g., amino acid racemization) or physical (e.g., radiometric, thermoluminescence, magnetism) analyses of the bone tissue, rocks, or fossil material in the facies (as the sum of all primary rock characteristics that incorporate inorganic (lithofacies) and organic (biofacies) elements) of interest, and different techniques attain different time depths (Conroy 1997; Wagner and Richter, “▶ Chronometric Methods in Paleoanthropology”). Relative dating methods are tightly related to the theory of, or directly on, stratigraphy and the idea of marker fossils, primarily developed by Nicholas Steno, a Danish anatomist, and upgraded by William Smith (alias “strata Smith”), an eighteenth-century English engineer (Ziegler 1992; Stanley 1994; Rothe 2000). Their perceptions led to three principles of sedimentation: (1) younger deposits overlie the older ones from the bottom up; (2) in the initial state, all layers are approximately horizontal; and (3) sediments extend laterally and can be parallelized over large areas (Rothe 2000). A further important law was established by Johannes Walther, a German geologist and Page 17 of 44

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Table 4 Summary of the categories and unit terms in stratigraphic classification

Stratigraphic categories Lithostratigraphic

Unconformity bounded Biostratigraphic

Magnetostratigraphic polarity Chronostratigraphic

Other (informal) stratigraphic categories (mineralogical, stable isotope, environmental seismic, etc.)

Principal stratigraphic unit terms Group Formation Member Bed(s), flow(s) Synthem Biozones Range zones Interval zones Lineage zones Assemblage zones Abundance zones Other kinds of biozones Polarity zone Eonothem Erathem System Series Stage Substage (Chronozones) -Zone (with approximate prefix)

Equivalent geochronological units Note: if additional ranks are needed, prefixes “sub” and “super” may be used with unit terms when appropriate, although restraint is recommended to avoid complicating the nomenclature unnecessarily

Eon Era Period Epoch Age Subage (or age) (Chron)

Murphy and Salvador (1999)

student of Ernst Haeckel, who based his inferences on the Swiss geologist Amanz Gressly’s fundamental contributions on stratigraphy in the eighteenth century and stated that the vertical succession of facies reflects lateral changes in past environments (Cross and Homewood 1997). Stratigraphic research can be roughly divided in three parts that differ in materials and methods: 1. Lithostratigraphy deals with the sequence and succession of sedimentary beds to yield diachronic zones; only a few “key beds” are nearly isochronic (Behrensmeyer 1992; Stanley 1994). 2. Biostratigraphy, which is based on organismic evolution, shows overlapping zones by analyzing facies-specific marker or index fossils that can be deemed as isochronic (Stanley 1994). Age estimations become more precise, the more closely index fossils are related (Behrensmeyer 1992). The life span of a fossil species, referred to as its “zone,” ranges from the first appearance of that species until a subsequently following species replaces it. Biostratigraphic time scales are often bound to a specific area. Both approaches offer the possibility of correlating sediments and

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Fig. 9 Geological time scales (Dates refer to the International Commission on Stratigraphy 2004)

time horizons continuously in regional areas (parastratigraphy) and worldwide (orthostratigraphy). 3. Chronostratigraphy, rock layers (strata) are sequenced and classified by absolute dating methods. Christian Leopold von Buch, an eighteenth-century German geologist, popularized the term “index fossils” as a marker for the correlation of contemporary strata, based on considerations by Charles Darwin and Charles Lyell concerning the irreversibility of changing morphologies through evolutionary time. Index fossils have to meet a number of requirements: (1) worldwide distribution, (2) rapid development that means a visible short time span of one species and evident morphological differences in comparison to other species, (3) high number of individuals, and (4) high chance of being preserved (Carroll 1988; Ziegler 1992). Obviously, marine organisms (plankton and nekton) are ideally suitable as index fossils, and for that reason paleontologists often focus on aquatic micro- and nanofossils to date sediments (e.g., foraminifers, diatoms). But macrofossils are also appropriate for stratigraphic positioning; these include the teeth (Kullmer 1999) and the hard tissues of smaller multicellular species (e.g., ammonites, graptoliths, conodonta). In addition to index fossils, there are also so-called “facies fossils” that are important for the characterization of a certain milieu with particular ecological conditions; early hominids fit in here. Problems for the chronological determination of strata are produced by geomorphological events like earthquakes, volcanism, dislocations, and disconcordance on the one hand and organism-induced disturbances like bioturbation and digging on the other. A special case in stratigraphy is sequence or cyclostratigraphy, which corresponds to the global correlation of tectonically independent eustatic sea-level fluctuations that happen synchronically in the form of transgressions (sea level raises over supratidal area) and regressions (sea level falls under the lowest tide gage) that are reflected in terms of changing communities (terrestrial/aquatic) and graphical curves. Further methods of dating involve measurements of cyclic events, e.g., seasonal temperature changes, among others: paleomagnetism, palynology (microflora and microfauna, e.g., spores, pollen, ostracods, radiolarians), dendrochronology (counting annual tree rings), dentin annulations (counting tooth dentin layers), diverse luminescence dating methods, Page 19 of 44

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stable isotope analysis in ice- or deep-sea cores, and microfossils (Lee-Thorp and Sponheimer, “▶ Contribution of Stable Light Isotopes to Paleoenvironmental Reconstruction”). Investigations of paleolimnological detritus layers are a method developed by the Swedish scientist Baron de Geer in 1878 and known as the exploration of “varves” (Swedish term that stands for “periodical recurrence”), annual laminated sediments in paleolakes. These methods all lack a link to “absolute” time, i.e., there is, with the exception of tree rings, no determination of a “null varve,” a starting point (Rothe 2000). An overview of relative and absolute dating methods is given in Table 5. What Context? Biotic information may be obtained from body fossils that deliver morphological insights (comparative morphology) and from trace fossils that contain ecological information in the form of organic tracks and inorganic marks (ichnology, e.g., footprints of Laetoli). In the case of body fossils, attention should be paid to the immense differences between life, death, and fossil assemblages (Fig. 10). A biocenosis simply represents all living species, i.e., the extant “community” in an ecosystem; in contrast, paleobiological remains are differentiated into autochthonous (thanatocoenosis ¼ death or indigenous assemblages, in situ communities) and allochthonous (taphocoenosis ¼ fossil assemblages) extinct communities. The latter may be affected by minor transport events (parautochthonous) or represent a mixture of local species and species that are brought in. Differences between life and fossil assemblages may result from “displacement” of various kinds (transport, accumulation, disarticulation, etc.), scavenging, destruction of hard materials (bio-erosion, abrasion), obliteration of specific elements (calcite vs. aragonite), etc., all of which may lead to misinterpretation in terms of taxonomy and ecological and chronological placement of fossils. However, even in contemporary communities, it is complicated to sort out decisive external and internal factors and to show which weighting each has on specific developments in an ecological system.

Floras, Faunas, and a Word on Coevolution There is – and always has been – a constrained relationship between flora and fauna. Since the first algae produced large amounts of oxygen, completely changing the atmosphere, animals and plants have had different interdependencies, though there is a comprehensive pattern of coevolution. To put it simply, coevolution or mutual selection is the process of reciprocal influence exerted by entities (mostly species) in an ecosystem (Begon et al. 1998), e.g., predator–prey or parasite-host relationships. The association of insects that need nectar and plants that require pollen transportation presents a common example. In the case of primate evolution, Sussman (1991) hypothesized that primates evolved in conjunction with the radiation of angiosperm plants and developed terminal branch feeding on nectar and flowers (Bloch and Boyer 2002; Silcox et al., “▶ Primate Origins and Supraordinal Relationships: Morphological Evidence”). “Sussman has proposed that grasping extremities and nails on the digits evolved for eating fruit on terminal branches of angiosperms” (Sargis 2002, p. 1564). Presumably, our own ancestors began to walk upright long before they developed larger brains, since monotonous coverage of the landscape by tropical forest was beginning to fail due to climatic changes from warm and wet to arid and cool conditions in the Late Miocene (Vrba 1985; Vrba, “▶ Role of Environmental Stimuli in Hominid Origins”; Wesselmann 1995; Bobe et al. 2002; Bobe and Behrensmeyer 2004). Sussman et al. (1985) and Rayner et al. (1993) suggested that, throughout the Pliocene, australopithecines showed arboreal

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

Table 5 An overview of dating methods (relative and absolute, no claim for completeness) Dating methods Relative dating methods Cation ratio Cultural affiliation Fluorine dating Obsidian hydration analysis (OHA) Patination Pollen analysis Rate of accumulation Seriation Varve analysis Fossils

Description in brief Geographical-dependent age determination of a rock by surface analyses (positivecharged ions in the varnish that is formed on a rock), very inaccurate Determination of temporal levels of tool industries, ceramics, etc. made by the temporal community in a certain area Fluorine accumulates in bone material (fluorapatite) that is deposited in groundwaterleading layers, thus providing information on the past time after burial Obsidian absorbs atmospheric humidity; old artifacts show a thicker “rind” of hydrate than younger ones (dependent on external factors like soil type, climate, erosion, burning, etc.) This technique is used when multiple artifacts of the same type are found in the same area and under the same conditions; several kinds of patina are related to time The study of chronological vegetational history by using microfossils in a target area Rock layers accumulate over time; thus, the deeper the layer, the older (applies also for artifacts associated with layers) Changes in ceramic forms over time to reconstruct consistent patterns of cultural trait change The thickness and shape of annually laminated sediments in a specific ecosystem (mostly paleolimnological) account for composition, displacement, and climate “Zones” of organismic remains (mostly species) are determined to classify certain strata

Absolute dating methods Archeomagnetism Astronomical dating Dendrochronology

Determination of variations (intensity, direction) in the Earth’s magnetic field Analysis of the Sun’s declination at the solstices Counting annual tree rings in order to determine the age of wood and reconstruct seasonal conditions Electron spin resonance Artifacts/fossils are exposed to radiation that predictably changes the magnetic field of the object (nondestructable) Thermoluminescence dating When reheating artifacts, the emitted light of specific crystals is proportional to the (TL) amount of radiation absorbed since the material was last heated, thus, provides a method to date pottery, hearths, fire-heated rocks, and burned minerals Optically stimulated Similar to TL, it uses light to innervate vacated electrons in sediments; comparisons luminescence (OSL) could be made through sediments with a known amount of added radiation Fission track Uranium (238U and 235U) radioactive elements create fission tracks by spontaneous splitting of uranium atoms and therefore exposing high amounts of energy that destroy the crystal lattice in a mineral Oxidizable carbon ratio (OCR) Soil bodies are analyzed to determine the linear progression of slow humus and charcoal recycling through time with an increase in readily oxidizable carbon and a decrease in the total amount of organic carbon Potassium-argon dating The measurement of the accumulation of argon in a mineral over time (40K/40Ar) Argon-argon dating Comparison of the amount of 40Ar and 39Ar; 40Ar is a stable isotope, thus does not 39 40 ( Ar/ Ar) decrease in time, whereas 39Ar is radioactive and consequently decreases over time Radiocarbon dating (14C) Age estimation for organic materials by measuring the disintegration of radioactive 14 C since an organism died; data indication is given by years before present (BP), whereas “present” means exactly AD 1950 (continued)

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Paleoecology: An Adequate Window on the Past?, Table 5 (continued) Dating methods Uranium-thorium dating (234U/230Th) Aluminum-beryllium dating (26Al/10Be) Uranium-lead dating Thorium-lead dating Rubidium-strontium dating Racemization

2

H, 13C, 15N, 18O, 34S stable isotopes

Description in brief Comparison which uses the properties of radioactive half-life 234U and 230Th and measures the equilibrium between these elements and not the accumulation of a decay product The ratio between aluminum and beryllium isotopes in the mineral quartz changes under cosmogenic radiation. The specific conditions of radiation must be previously determined The ratio of radioactive uranium and thorium isotopes to lead as decay product, dating of rock material with a tremendous time depth of billions of years Stable isotope ratio 87Sr/86Sr is measured in rock material Amino acids as subunits of proteins are widespread in organisms; living organisms contain only l-amino acids (turn polarized light to the left); in dead organisms l-amino acids degrade stepwise to d-amino acids (turn polarized light to the right) until the amounts are equal; thus, the ratio between both conformations provides information about the age of a sample (5,000–ca. 200,000 years depth) These isotopes are found for several reasons in different amounts in sample materials of different kinds and could be useful for agricultural, archaeological, ecological, nutritional, geochemical, or medical research

and bipedal tendencies in a mosaic-like habitat that was marked by significant patches of subtropical forest, large areas of grassland, and savannah of all kinds. “Upright posture, large brain, tool making, and other hominin characters as adaptations to a savannah habitat must be rethought, at least in the case of A. africanus” (Rayner et al. 1993, p. 228; Rowan and Reed,“▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments”). In 2004 Schrenk et al. published a PanAfrican so-called “open source” perspective suggesting that bipedal locomotion was developed several times at the margins of shrinking rainforest habitats during a global cooling trend in the Middle Miocene (Schrenk et al. 2004); for further discussions on the origins of bipedality, see Harcourt-Smith, “▶ The Origins of Bipedal Locomotion” and Senut, “▶ The Earliest Putative Hominids”). King and Bailey (2006, p. 282) state that the African Rift “. . . offers physical protection in the form of cliffs, lava flows and topographic enclosures, and hence small-scale topographic complexity in which a relatively defenceless species can find protection from predators.” The authors expand their view and suppose that rift-like complexity could not only be found in areas where human evolution took place but along the dispersal routes of early Homo in and beyond Africa as well. Potts (2012, p. 163) concludes in a very clear review about environmental change as “first driver” in human prehistory that “Evolutionary processes favored any response that could enhance survival in a changing world. [. . .] This observation makes sense in light of the environmental instability that ancient human predecessors encountered.” High plasticity and adaptability seem to be among the qualities that made Homo. Other factors, e.g., isolation, niche boundary shifts, and small population size, could also be a spur to evolutionary “innovations” in hominids (Wolpoff 1999; Henke and Rothe 2003). Just a few steps further in our evolutionary history, and in the debate concerning early Homo as well, there is a huge amount of different hypotheses that aim to link environmental constraints to specific adaptations and morphological transformations (Vrba, “▶ Role of Environmental Stimuli in Hominid Origins”). Because of the insufficient preservation of plants in toto, caused by increased decomposition in aerobic and particularly tropical conditions, paleobotanists rely heavily on pollen, spore, and phytolith analyses (Jolly et al. 1998; Elenga et al. 2000; African Pollen Database). However, such things can be Page 22 of 44

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Fig. 10 The differences between life, death, and fossil assemblages related to taphonomic principles (Compiled from Lyman 1996 and Behrensmeyer 1992)

dispersed well away from their original habitat through wind and water (Andrews 1992). Density and distribution of these palynological units in sediment layers give us an idea about the allocation of specific plant families, spatial scales of retraction or expansion, and potential plant food proposed. For example, isotopic data on hominin diets have shown an involvement with C4 grass – foods (Lee-Thorp and Sponheimer, “▶ Contribution of Stable Light Isotopes to Paleoenvironmental Reconstruction”; Sponheimer and Lee-Thorp, “▶ Hominin Paleodiets: The Contribution of Stable Isotopes”). Large herbivores (e.g., gramineous, foliaceous) are bound to the availability, dispersal, and capacity of particular plants; subsequently, hypotheses about migrations of herds and “predator–prey” relationships between carnivores and early hominins may, respectively, achieve wider temporal and spatial scales. Bovids are the most common faunal element at most Neogene hominid fossil localities and are often used as indicators to understand Plio-Pleistocene hominid ecological and behavioral changes (Vrba 1995; Kappelmann et al. 1997). Besides, the strong interrelations between fossil species, phytogeography, climate, biogeography, and faunal conditions may lead to improved recognitions of “turnover pulses” in ecological networks and reflect the importance of environmental changes on faunal adaptation, selection, and evolution (Foley 1978, 1994, 1995, 1999; Potts 1998a, b; Lahr and Foley 1998; O’Brien and Peters 1999; Owen-Smith 1999; Vrba 1995, 1999; Vrba, “▶ Role of Environmental Stimuli in Hominid Origins”; deMenocal 2004; Herna´ndez Ferna´ndez and Vrba 2006).

Syntheses Modifying Dobzhansky’s credo (1973) we state that Nothing in evolution makes sense except in the light of ecology. Corresponding to this “ecolution”, we try to depict cross sections in three-time horizons (early-middle-late) of hominid evolution from ca. 7 Ma until today (Fig. 11). This should Page 23 of 44

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_17-3 # Springer-Verlag Berlin Heidelberg 2013

Fig. 11 Summary diagrams of paleoenvironmental data and hominid evolution, compiled from different authors. There is a clear linkage between hominid evolution, macro- and micromammal report, climatic changes, stable isotope data, and dispersals within and out of Africa. Seemingly, colder and more arid conditions combined with adaptational changes among hominids initiated several processes that led to the currently accepted patterns of biogeographical processes in hominid evolution. Homo erectus was the first hominin species to spread into the Old World. The taxonomic relationship between late hominin species is by no means completed. The evolution of stone tools comprises the last 2 Myr and leads to an explosion of artistic expression ca. 18 ka

provide a basis for understanding how many different viewpoints have to be captured when looking at a complex process like hominoid and hominid evolution. It does not claim to circumscribe all factors in all periods; it can only provide insights and surely leaves many perspectives unseen. But is there an “ideal” environment that can be hypothesized for the evolution of African hominids? This and other questions are discussed in this section. Two different kinds of hypotheses can be discerned: (1) the habitat-specific and (2) the variability-selection hypothesis. The former considers faunal adaptations to a specific environment, while the latter emphasizes the importance of climatic instability as a trigger for adaptive changes. Modern interpretations support a step-by-step development of drier, cooler, and more open conditions since the Late Miocene. Both the influence of an arid-adapted fauna on early hominid evolution at the mid-Pliocene (near 3.2–2.6 Ma) and the aridification shift (Bonnefille 1983; deMenocal 1995; Dupont and Leroy 1995) are viewed as catalysts for human evolution.

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Vrba et al. (1980, 1995, 1998; Vrba, “▶ Role of Environmental Stimuli in Hominid Origins”) are prominent advocates of the turnover-pulse hypothesis that derives from the habitat-specific hypothesis, itself a variation of the savannah hypothesis. Fundamental shifts in African climate – 2.8, 1.8, and 1.0 Ma – initiated the so-called “turnovers.” These turnovers are focused bursts of biotic change. For example, between 3.0 and 2.5 Myr, many first appearances were of grazing species. This pattern links aridity and expanding grasslands to faunal changes (Vrba 1980; Bobe and Eck 2001). Graphically, the pulses are defined via clustering. Authors, such as Behrensmeyer et al. (1997) or Werdelin and Lewis (2001), do not, however, support this important view of climate-hominid evolution interaction. To make things more complicated, bipedality may have evolved in forest or woodland habitats, not savannah (Rayner et al. 1993; Wood and Harrison 2011); and maybe it was developed even in non-hominin primates like Oreopithecus (Rook et al. 1999). As concerns the evolution of early tool-making hominids, mosaic zones of grass- and woodland may have stimulated our evolution (Blumenschine 1986). On the other hand, the variability-selection hypothesis advocates the importance of climatic instability for introducing (1) genetic plurality, (2) natural selection, and (3) faunal innovations. Potts (1998b) suggested that many of the largest African faunal evolution events occurred when there were increases in the amplitudes of paleoclimatic variability (such as modifications in the durations and amplitudes of orbital-scale wet-dry amplitudes). Potts’ (1998b, p. 82) view stresses the inconsistency of selection over long time spans and “thus departs from the prevailing paradigm of adaptive evolution via long-term directional selection.” As many biologists (e. g., Sahney et al. 2010) assume a close match between an organism and its specific environment (that can be confirmed for organisms that are habitat specialists), the variability-selection model proposes that lineages experience factors over time that disrupt close connections to any specific environment – a decoupling mechanism that separates the organism from any environmental state.

Early Phase: Forerunners Among Miocene Primates In the Late Miocene (23.8–5.3 Ma), the hominoids, including Hylobatidae and Hominidae [Ponginae/orangutans and Homininae/African great apes and Homo; sensu Groves (2001)], had reached their greatest abundance and diversity, and with little doubt human origins lie somewhere within this group (Conroy 1997). Niches now occupied by cercopithecoids were additionally exploited by hominoids in Africa (Fleagle 1999). The fossil records of the Early, Middle, and Late Miocene are fairly good and include Proconsulidae and Oreopithecidae as well (Rasmussen, ▶ Chap. 3; Begun, “▶ Fossil Record of Miocene Hominoids”). However, the search for the root of hominid evolution and additionally for “. . . the identification of hominoids among the various genera and species of fossil apes from that epoch has proved a fruitless exercise thus far” (Fleagle 1999, p. 483). Some propose Dryopithecus as a possible predecessor of the clade that includes great apes and humans; others suppose Ouranopithecus to be directly ancestral to later humans. The earliest fossils that are proposed as being probable hominid ancestors are two species of the genus Ardipithecus (ramidus/kadabba) 5.2–4.4 Ma from Ethiopia (White et al. 1994, 2009; HaileSelassie 2001), Orrorin tugenensis  6 Ma from Kenya (Senut et al. 2001), and Sahelanthropus tchadensis 6–7 Ma from Chad (Brunet et al. 2002). All these specimens were found in the last 20 years, probably because excavation campaigns were targeted toward the “roots’ of hominids and the divergence point between apes and hominids, respectively. There is much debate about the “ape-or-human” status, the morphological features, the selection pressures, and the changes that have to be carried out on the tree of human evolution (Gibbons 2002), and of special interest here are the ecological circumstances around 7–4 Ma that these species were confronted by. Page 25 of 44

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Ardipithecus is the name given to 5.8–4.4-Myr-old fossils from the Middle Awash area of Ethiopia. Haile-Selassie (2001, p. 178) declared Ardipithecus to be the genus that “. . . postdated the divergence of lineages leading to modern chimpanzees and humans.” The fossils are associated with a relatively wet and wooded paleoenvironment (Haile-Selassie 2001; WoldeGabriel et al. 2001). WoldeGabriel et al. (2001, p. 175) suggested that similar habitats were found in the case of Orrorin (see later) and therefore that “. . . these findings require fundamental reassessment of models that invoke a significant role for global climatic change and/or savannah habitat in the origin of hominids.” Associated vertebrate fossil assemblages indicate woodland/forest habitats and small areas of open grassland around lake margins. Among the micromammals the rarity of lagomorphs shows that open grasslands are not well sampled in the habitat of Ardipithecus. Moreover, closed wooded environments, where fossils are less likely to be preserved, may explain the low numbers of hominoid/hominid fossils in the Late Miocene. An eleven-paper publication in 2009 by an international team on Ardipithecus ramidus remains, including 110 fossil specimens and “Ardi,” a partial female skeleton comparable to the remains of “Lucy,” draws the following picture: this extinct 4.4-Myr-old species was a small-sized arboreal climber (without specializations for knuckle walking and suspension) in a tree-dominated habitat that had a nonspecialized “soft” C3-food diet, showed minimal social aggression (reduced premolar/canine complex), and walked terrestrially as a facultative biped in a more primitive mode than Australopithecus. The unique compilation of traits in Ardipithecus ramidus perhaps helps us to develop a picture of the last common ancestor of humans and great apes. Thus, the authors concluded that a chimpanzeelike forerunner is unlikely (Science-Extra 2009). East African Orrorin seems to fall somewhere between the African great apes and humans and thus “. . . accords with the East Side Story proposed by Coppens” (Senut et al. 2001, p. 142). The “East Side Story” is a construct that invokes the geomorphologically induced allopatric development of African great apes and hominids (8 Ma) in the placement of the cradle of mankind in eastern Africa between the Great Rift Valley and the Indian Ocean (Coppens 1987, 1999; deMenocal 2004). A general trend of worldwide cooling, the extensive increase of grassland, and the retraction of tropical forests, rainforests, and wooded savannahs are perceptible 8 Ma. At the same time, a rifting process and an uplifting of the western rift shoulder led to the appearance of a topographic borderline that placed them in the more and more arid eastern part in the rain shadow of the wetter western part (Pickford 1990). This eastern “isolation” for several million years might have been behind endemic peripatric genetic drifts and consequently the origin of hominid features (Coppens 1999). After analyzing and interpreting postcranial morphological features, Pickford et al. (2002) conclude that Orrorin was a habitual biped with the ability to climb trees, and they found several apomorphic characters shared with australopithecines and Homo but none with Pan or Gorilla (Senut, “▶ The Earliest Putative Hominids”). The habitat of Orrorin was reconstructed, from faunal remains and geological analyses of the Late Miocene Lukeino Formation in the Tugen Hills of Kenya, as a mosaic of open woodland and forests around a lake. Orrorin seems to be a representative of a typical “edge species” that lived on the frontier between environmental units (Sussman and Hart, “▶ Modeling the Past: The Primatological Approach”). Associated faunal remains stem from colobines, carnivores, and ungulates (Pickford and Senut 2001). However, the allopatric “East Side Story” is challenged by Sahelanthropus tchadensis – a 6–7-Myr-old hominin from western Africa. S. tchadensis was found in Central Africa, in the western Djurab desert of Chad (Brunet et al. 2002). The locality is interesting because it lies far west to the Rift. Following the discovery of A. bahrelghazali in 1995, there was no further evidence for a western dispersal of hominids (Brunet et al. 1995) until Sahelanthropus, whose ecological circumstances are remarkable insofar as they Page 26 of 44

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are similar to those of the eastern fossil sites. This raises the possibility of analogizing evolutionary constraints for hominids in the eastern and western different areas. Vignaud et al. (2002) suggested that Sahelanthropus lived close to a vast lake with swamp areas and rivers (inferred from fish and amphibious forms) and not far from a sandy desert. As deduced from basicranial and facial structures, Brunet et al. (2002, p. 150) concluded that there are clear similarities between Sahelanthropus and “. . . later fossil hominids that were clearly bipedal.” The faunal record shows animals associated with a mosaic landscape with lacustrine gallery forest, open grassland, and savannah (primates, rodents, equids, bovids, and carnivores). All of these observations led Brunet and colleagues to arrive at the conclusion that Sahelanthropus lived in a more mosaic-like habitat than Ardipithecus, Orrorin, and the australopiths (Blondel et al. 2010; Strait et al., “▶ Analyzing Hominin Phylogeny”; Rown and Reed, “▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments”). Still, all three new genera are represented by little fossil evidence and lack intraspecific comparisons, limiting inferences facilitating taxonomic placement of these fossils into the ape or the human lineages (Brunet et al. 2002; Wolpoff et al. 2002; Wood 2002; Senut, “▶ The Earliest Putative Hominids”). In addition, for understanding the “start-up” of humanization, we also need to identify the selection pressures that triggered the evolution of bipedality and dental adaptations relating to dietary behavior shifts in changing habitats. Meanwhile, even the consensus from fossil and molecular evidence, that the human lineage diverged from that of the chimpanzees between 6 and 8 Ma, is uncertain caused by the inconsistent calibration of the molecular clock we use as our “rearview mirror” (Stauffer et al. 2001; Gibbons 2012). Besides this, many questions linger pertaining both to the taxonomic classification of these “ape men” (Begun 2004) and the reconstruction of the paleoenvironments they lived in. “The solution is in the mantra of all paleontologists: We need more fossils!” (Begun 2004, p. 1480; Menke, ▶ The Ontogeny-Phylogeny Nexus in a Nutshell: Implications for Primatology and Paleoanthropology).

Middle Phase: “Chewer” and “Thinker” Around 2.4–2.0 Ma, the genus Homo first appears in the fossil record of Africa. Its definition and the establishment of a hypodigm have given rise to a labyrinth of ideas and approaches about the number of species involved (Foley 1991; Tattersall 1992; Collard and Wood, “▶ Defining the Genus Homo”), morphological variability, distinctions from the australopiths, and phylogenetic relationships. Recently, the bush of hominid evolution and especially the split between Australopithecus and Homo were altered by the 1.95–1.78-Myr-“young” remains of Australopithecus sediba found in the Malapa cave in South Africa in 2010. Because its cranial and postcranial features showed a mosaic of primitive (australopith) and derived (Homo) features, A. sediba was identified as a transitional species and hence a potential forerunner of early Homo. Once more another possible ancestor of Homo had been found in the australopith branch (Berger et al. 2010). As might be expected, there are other ideas: (1) A. sediba is only a late version of A. africanus (Tim White and Ron Clarke in Balter 2010); (2) A. sediba is an early Homo (Donald Johanson cited by Wong 2010); and (3) A. sediba is a late form of australopiths that lived at the same time as early Homo, leaving taxonomic questions and coming back to paleoecology. Analyzing A. sediba’s dental phytoliths, stable carbon isotopes, and dental microwear, Henry et al. (2012) infer a C3-plant diet in a gallery forest like biome with C4-grassland and woodland in the vicinity. The home ranges of A. sediba could thus have been large and comparable to that of modern savannah chimpanzees striving for C3-fruits. The upper limb of A. sediba shows ape-like climbing and suspensory abilities than manipulation skills like in Homo (Churchill et al. 2013). Albeit the lower limb clearly shows the capability for bipedal walking, the gait mechanics seem to be different from what we knew Page 27 of 44

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Table 6 Hypotheses of how environmental changes relate to biotic evolution Hypothesis Description Refugial vs. biotidal areas Environmental changes affect two basic kinds of geographical areas differently: the biome resists in a refugium, whereas it does not in a biotidal area. Refugia are characterized by the persistence of dominant taxa (new species within these taxa may be added); in contrast, biotidal areas are shaped by the temporary appearance and disappearance of dominant taxa Turnover pulse (local/ Physical environmental change is required to initiate most speciations, extinctions, and widespread) distribution drift. Thus, most lineage turnover has occurred in pulses, near synchronous across diverse groups of organisms. Changes could either be widespread with independent evidence of environmental change or they are mostly local and form a largely random frequency distribution against time Coordinated stasis Organismic interactions are the reason for evolutionary stasis in a community. Only hypothesis radical physical changes can detach the coevolutionary bonds between the life-forms, comparable to the turnover-pulse hypothesis Climatic/tectonic A particular environmental cause of turnover was global, or at least widespread, climatic initiating cause change. Alternatively, the cause could be tectonic, and thus turnover signature is appropriately geographically restricted Variability-selection Advocates the importance of environmental variability for introducing (1) genetic hypothesis plurality, (2) natural selection, and (3) faunal innovations Compiled after Vrba (1988), Potts (1998); see also Vrba, “▶ Role of Environmental Stimuli in Hominid Origins”

previously in Australopithecus. DeSilva et al. (2013, p. 1232999-1) conclude that “. . . there may have been several forms of bipedalism during the Plio-Pleistocene.” The crucial questions regarding the borderline between Australopithecus and Homo, and exactly which forms gave rise to genus Homo and which ones originated the “robust” lineage around 2.5 Ma, are still unanswered. From the ecological point of view, the crucial question is: “Why did these two lineages split off ?” In our opinion the base of all “changes-driven” suggestions is the innate skill of organisms to adapt to environmental changes. Vrba (1988) provides an overview of general hypotheses that relate environmental changes to biotic evolution and thus provides a basis to speculate about divergence processes (Table 6). Late Pliocene and Early Pleistocene strata contain a number of hominid fossils that obviously belonged to different morphotypes and ways of living. On the one hand, there are robust forms with large faces, huge supraorbital structures, small brains, and enormous masticatory capacities; on the other hand there have been forms with small faces, larger brains, reduced supraorbital features, and reduced size of upper and lower jaws. The latter are associated with the first 2.4-Ma-old lithic tools (“pebble tools” and “choppers”) as attributed to the Oldowan industry and “handy man” H. habilis. It remains doubtful that australopithecines maintained the kind of Osteodontokeratic culture (bone, teeth, and horn) that Raymond Dart (1957) proposed. The focus here lies on the outstanding trends that divide two temporally sympatric genera and morphological/evolutionary “lineages”: Paranthropus and early Homo. The different ecological niches that could have been occupied by the species of both genera are limited by their basic needs as (1) large mammals, (2) terrestrial primates, (3) dwellers of tropical gallery forests/open savannah – or grassland – habitats, (4) interspecific competitors, and (5) K-strategists (Foley 1978; Henke and Rothe 1994, 1999). When reflecting on the possibilities of coping with the environment and niche separation as well as niche expansion, the encompassment of all kinds of “internal” influences like body size, population dynamics, abilities of locomotion and “thinking,” life-history strategies, behavior, and social system is required. Furthermore, the roles of “external”

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factors such as climate, biogeography, sympatric species, and predator–prey relationships have to be taken into account (Foley 1978). About 2.0 Ma, several kinds of hominids are found in northwestern Kenya and south Ethiopia around Lake Turkana (Tattersall 2002): Paranthropus boisei, P. (Australopithecus) aethiopicus, H. (Kenyanthropus) rudolfensis, H. (Australopithecus) habilis, H. erectus (ergaster); the genera and species names in parentheses indicate that the debate about their taxonomic status is still in progress. The Turkana Basin (Fig. 3), situated in the Great Rift Valley from southern Ethiopia into northern Kenya, covers an area of about 3,600 km2 and represents one of the richest fossiliferous areas in Africa. An exceptional breadth of “mosaic-like” geological and environmental diversity has been investigated by the Koobi Fora Research Project. It reaches from the lacustrine/fluvial sediments of the Omo River channel, with gallery forests and swamps, across thorn bush and grassy floodplains strongly influenced by seasonal flooding, to the basin margins with an arid climate and totally different sedimentation regimes (kfpr.com/prehistory_of_koobi_fora). The geological record provides volcanic tephra layers, amenable to chronometric dating, that are associated with unusually well-preserved fossils. The faunal record has a nearly gapless temporal as well as a lateral component, making it possible to reconstruct paleohabitats over large areas. The archaeological remains include Oldowan, Karari, and Acheulean tools that complement the evidence of the fossil hominins. The Omo basin sediments, fossils, and pollens provide a wealth of information about the ecological circumstances and the temporal distribution of hominids in this region. P. boisei and P. aethiopicus are strongly adapted to drier conditions in savannah habitats with gallery forests or patchy wooden refugia. Craniodental morphology and especially microdental analyses suggest an exclusively low-quality herbivorous subsistence with sometimes coarse gramineous parts, dependent on the availability of food in a highly variable seasonal environment that is characterized by both copiousness and scarcity (Rak 1983; Foley 1987; Kay and Grine 1988; Henke and Rothe 1999). In contrast, gracile australopithecines seem to have preferred more humid habitats with large spots of forest (Coppens 2002) and were able to accommodate to substantial environmental variability and dietary shifts (Teaford and Ungar 2000; Bonnefille et al. 2004). The most widely studied habitat-specific hypothesis is the savannah hypothesis. Dart (1925) already used the open savannah model as a tool to explain larger brains and bipedality in early Homo. This concept plausible prima facie was not confirmed by the data collected (Leakey and Hay 1979; Cerling 1992; Cerling and Hay 1988; Senut et al. 2001): bipedalism was apparently established millions of years before the savannah grassland expansion. Early Homo lived in fairly open, arid habitats, used an enlarged spectrum of food resources, and is best characterized as an opportunistic and omnivorous forager. Basic sustenance was surely provided by plant food, but the use of tools made accessible difficult-to-reach high-energy sources like edaphic storage organs (tubers and roots) (Laden and Wrangham 2005) and meat from scavenging complemented their diet (Foley 1987; Blumenschine et al. 1994). This latter is important when looking at coevolutionary processes and sympatric interdependencies between early Homo, herbivores, and carnivores (Turner 1984; Lewis 1997; Brantingham 1998). High-energy-density diets and unstructured feeding patterns (originated by the seasonal availability) still characterize present-day human eating behaviors, although today’s nutrition is largely uncoupled from seasonal cycles (Ulijaszek 2002). Hunting, as Lee and DeVore (1968) suggested, is widely accepted as unlikely in early Homo; it seems that the conception of a klepto-parasite seems to characterize the real natural situation best. Comparative primatological studies of chimpanzee populations and analyses of behavioral ecology and nutrition strategies in current African hunter-gatherer tribes (Lupo 2002; Marlowe 2005) support these assumptions. Vrba (1988, p. 422) stated that “. . . in some respects the Page 29 of 44

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Homo lineage evolved toward a greater ecological generalization, while in contrast the ‘robust’ lineage(s) became more specialized on resources prevalent in more open environments.” In the Middle and Late Pleistocene, the diversity of hominids decreased drastically; the “robust” australopithecines became extinct, maybe because they were too specialized and could not adapt to the changing environmental conditions (Klein 1988); and Homo constituted the only remaining genus in the bottleneck of hominid evolution. The questions of how and why that happened and what processes were involved are manifold (Henke and Rothe 1999; Tattersall 2002; Rightmire 1998, “▶ Later Middle Pleistocene Homo”).

Late Phase: Neanderthals and Colonizers As one of the most discussed topics in human evolution, the Neanderthal enigma is a prominent “problem” of the late phase. d’Errico and Sa´nchez Gon˜i (2003) investigated the millennial-scale climatic variability of OIS3 in the context of Neanderthal extinction. To the extent that population models seek climate as a triggering factor for the colonization of Europe by anatomically modern humans and the Neanderthal extinction, they appear to be highly contradictory due to (1) the lack of terrestrial continuous and well-dated paleoclimatic sequences, (2) the uncertainties in the dating methods, and (3) the doubts about the cultural attribution of archaeological layers. These authors therefore reviewed the paleoclimatic OIS3 evidence from Iberia and found a fragmentary, lowresolution, and poorly interpreted record. d’Errico and Sa´nchez Gon˜i (2003) concluded that Aurignacian moderns colonized the north of Iberia and France at the onset of the H4 event. They based their results on a correlation between archaeological data from western Europe and from two IMAGES pollen-rich deep-sea cores. Their scenario favors Neanderthal populations existing in desert-steppe-like environments (made up of Artemisia, Chenopodiaceae, and Ephedra which characterize the H4 of this area), while the Aurignacian moderns were probably not interested in colonizing these arid Mediterranean biotopes. Anatomically modern humans did this only after the H4 event. However, Finlayson et al. (2004) pointed out problems with this scenario. They admit that d’Errico and Sa´nchez Gon˜i’s (2003) paper is very useful in reinforcing the data showing that climatic events worldwide became increasingly unstable during OIS3, but as inferred by Finlayson et al. (2004, p. 1208), there are problems of cause and effect: “We suggest that this is a spurious correlation, and that what is being observed is two populations responding to the same variable (or variables) in opposite directions. Since no direct proof of cause and effect between Aurignacians and Neanderthals is advanced, this must remain the most parsimonious explanation.” Finally, they interpret d’Errico and Sa´nchez Gon˜i’s (2003) data in the opposite way by concluding that the available information points to climate instability fragmenting Neanderthal populations and emphasizing that not a single piece of evidence exists to demonstrate competition between Moderns and Neanderthals. Further questions that have to be answered when discussing anatomically modern humans in Eurasia, Australasia, and the New World are the following: Why and when did the expansion happen? Who and how many participated and where did they arrive? Fig. 12 provides an overview of potential migration waves and the time they probably took place. One consensus seems to crystallize from the fossil record: equipped with a stature shape and size near to ours (Turkana boy from Nariokotome), a large brain, and increased mobility; able to handle hunting weapons (400-ka-old spears of Scho¨ningen/Germany) as well as fire; and being provided with a significant curiosity, H. erectus (H. ergaster) migrated far from the continent of its birth at around 1.8 Ma (Dmanisi fossils) (Gabunia et al. 2001) and conquered the Old World. Thenceforward, there are diverse models/hypotheses that try to explain dispersal patterns over the last 1.5 Myr of human Page 30 of 44

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Fig. 12 Potential migration waves and migration periods of archaic Homo populations “Out of Africa” assumed by several paleoanthropologists (After Henke 2004)

evolution. The recent African origin model (RAO) holds that the biocultural transition from late archaic H. sapiens to anatomically modern humans was restricted to Africa, with subsequent dispersion and replacement of H. erectus ca. 200 ka. Another hypothesis assumes an anagenetic transition from the early hominins to H. erectus (earlier than 1.5 Ma), followed by dispersal. In the view of Templeton (2002), a second and a third expansion (Out of Africa “again and again”) shaped the modern human gene pool. The assumption that H. sapiens developed independently and in parallel in several regions of the world is mainly based on Asian fossils (e.g., Zhoukoudian, upper cave) and is summarized as the “Multiregional Continuity Model,” or the polyphyletic hypothesis, with gene flow maintaining some genetic homogeneity (Wolpoff 1999, 2002). The “mostly Out-ofAfrica hypothesis” (Relethford 1998, 2001) is a combination of the African replacement model with the multiregional model. All these hypotheses involve questions of whether migrating hominins replaced local populations, or interbred (for further discussions, see also Bra¨uer, “▶ Origin of Modern Humans”). Referring to the questions we formulated at the beginning of this section, we want to add a third one: how did hominins migrate from Africa? (Henke and Hardt 2011). In the early phase, hominids seem to have been restricted to certain African habitats (although there were relatively large numbers of “intra-African” dispersals Strait and Wood 1999); this restriction lapsed through the Pleistocene, and hominids seemed to become more eurytopic and thus became able to tolerate a wider range of conditions (Foley 1978; Vrba 1995, 1999; Lahr and Foley 1998). It is possible to see an ecological patterning in the colonization of temperate regions even when looking at the range of other species (mostly large mammals) that spread out of Africa alongside the hominids (Turner 1984; Lewis 1997; Brantingham 1998; Strait and Wood 1999). Certain characteristics of large mammals provide the capacity to exploit new environments, including (1) large body size, (2) carnivorous behavior, and (3) sociality in larger groups. Hence, scientists have to think Page 31 of 44

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about the general principles that encourage zoogeographic mobility (Foley 1987; Henke and Rothe 1999): • Carnivores are more eurytopic than herbivores. Meat requires less specialized and locally restricted adaptations than plants, thus carnivores are expected to migrate faster than herbivores, which are restricted to specific plants in a specific area. • Exogeny: the attribute of an organism to forage across a variety of niches, giving it higher tolerance, less specialization, increased interspecific competition. • Environmental physiology: increasing body size enhances the energetic situation of an organism in terms of the relation between body weight and surface (Bergmann’s rule 1847; Aiello and Wells 2002). Consequently, larger mammals are able to cope more efficiently with temperate conditions. The extremities tend to be reduced in colder environments to diminish frostbite as seen in the distal limb segments of Neanderthals (Allen’s rule 1906). “There is indeed some possibility that the increase in body size associated with Homo erectus [. . .] may have at least contributed to the success of human geographical spread” (Foley 1987, p. 268). Additionally, home range size and diet quality seem to be closely related to initial dispersals from Africa (Anto´n et al. 2002). Although these principles are able to account for the expansion of early hominins, certain problems related to surviving high-latitude habitats remain: (1) resource availability is highly seasonal and (2) the annual variation in day length shortens the time for foraging and other activities in winter. Favored strategies here are the extraction of resources yielding high returns and an increase in the efficiency with which resources are extracted. The former is linked to an increase in carnivory and high-energy food and the latter to increasing predatory efficiency and, especially in hominins, improved tool manufacturing and using. Additionally, producing complex and efficient stone tools demands advanced cognitive competence and accordingly constitutes an interaction between encephalization and culture (Klein 2000; Wynn 2002; Osvath and Ga¨rdenfors 2005; Biagi, “▶ Modeling the Past: The Paleoethnological Evidence”; Toth and Schick, “▶ Overview of Paleolithic Archeology”). Most likely, habitat structure and resource types were the driving forces that mainly influenced dispersals and the sequence of habitat colonization by hominids (Foley 1987).

Summary Human evolution is not a “Sonderweg” (exceptional way); it strictly follows the rules of evolutionary biology and neither constitutes a special case nor determines the terminal branch end in the Tree of Life, let alone creation’s crowning glory (Foley 1978, 2002). It is just the story of balanced interrelationships between environment and large mammalian genera possessing preadaptations that facilitated coping with the conditions during a specific time span. Corresponding to Foley (2002), the following key events altered the direction of radiations and dispersals in the hominid lineage: 1. Invasion of Africa from Asia of an ancestral lineage of Miocene primates and the outcome of African apes and potential “hominids” Ardipithecus, Orrorin, and Sahelanthropus. 2. Bipedal adaptations in australopithecines living in tree-dominated grassland-woodland mosaic habitats probably in dense gallery forest biomes and/or at the margin of the shrinking central

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3.

4.

5.

6.

7.

8.

African rainforest (taxa: A. anamensis, A. afarensis, A. africanus, A. garhi, A. bahrelghazali, A. sediba) in the Pliocene with nearly Pan-African dispersals. Megadonty and masticatory apparatus increase as adaptation to low-quality nutrition in a mosaic-like environment in the “robust” australopithecines (taxa: P. (A.) aethiopicus, P. (A.) boisei, P. (A.) robustus) during the latest Pliocene and Early Pleistocene leading to an extinct backside branch. Origin and radiation of earliest Homo is the most intriguing event of all because the phylogenetic position of the scarce fossils is extremely uncertain and variations within the group are extensive (taxa: A. (H.) sediba, Kenyanthropus platyops, H. (K.) rudolfensis, H. habilis). Nevertheless, there is a clear trend toward brain size increase. The diversification and dispersal of Homo 1.75 Ma (taxa: H. erectus, H. ergaster) and a second radiation of later forms of Homo 0.5 Ma (H. heidelbergensis), bound to several changes in dental/cranial morphology and behavior (carnivory, hunting, tradigenesis), the development of technologies (stone tools), and the usage of fire. Enhanced neural capabilities and improvement of lithic and hunting technologies (e.g., projectiles) in the context of interglacial/glacial cycles may have led to repeated dispersals following each other with the outcome of H. neanderthalensis and H. sapiens. Symbolic thought (Henke in press) combined with language and the opening of new resources (e.g., aquatic food) characterizes the radiation and global colonization of H. sapiens in the last 100 kyr ago. Why and how the Neanderthals became extinct is still a matter of debate. Recently, humans seem to have nearly detached themselves from selection pressures (except regarding their own species and some kinds of pathogens). Meanwhile, Homo is the large mammal species with the most individuals – there are seven billions of us now. This, however, brings with it great responsibility to safeguard “System Earth” in order to afford further evolutionary development in global ecosystems. The sheer mass of Homo sapiens is causing systemic changes in every sphere of the planet that are faster than ever before in the Earth’s history. We are now in the Anthropocene (Zalasiewicz et al. 2011). Or, as Potts put it (2012, p. 163): “The question remains as to how human societies in the future will apply their evolved adaptability in adjusting to the rapid changes we now create.”

We would like to stress that primate and consequently hominid evolution is a complex process that has to be seen from different angles and needs all of the different scientific approaches currently available. One question remains open: Is paleoecology an adequate window on the past? This is answered in the affirmative but, as in any other hypothesis-based scientific field, it is also realized that without paying attention to possible pitfalls and without interpreting the results in context, there is a danger of simply telling stories. Unfortunately, there are no “laws” in ecological science such as those that exist in chemistry and physics; there are merely a lot of hypotheses that have to be tested and one concept that is close to a “law”: natural selection (Pianka 1983). Hence, we conclude that paleoecology – when conceived with care – is an important field of evolutionary biological, and especially paleoanthropological, research. When discussing hominid evolution, and consequently our own evolutionary history, the danger of storytelling is potentially higher because fossils are rare, sample biases are high, and not least because hypotheses always stand on shaky ground when the subject is ourselves (White 2000). Actualism may be a path that leads to “true” inferences when ecological models and model organisms are selected carefully. For example, Pan, as our genetically closest relative, seems to be a good model from which to derive certain inferences, but as a restricted occupant of dense and Page 33 of 44

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humid forest habitats with significant morphological adaptations, it might not be the first choice for reconstructing the selective pressures that affected early humans living “on the edge” between open and closed habitats (see also Susman and Hart, “▶ Modeling the Past: The Primatological Approach”). It is obvious that paleoecology demands a multidisciplinary approach. However, nearly all researchers are specialized in their own “scientific niches” and struggle to keep and defend them. The great challenge ought to be the creation of a “scientific biocenosis” that helps us to understand evolutionary processes in terms of all the phenomena scientists are able to examine. The “scientific environment,” however, is sometimes harsh, and chilly winds wave the banner of publication quantities and impact factors. There is hope that a high adaptational species – such as ourselves –could change and improve this “habitat” to enhance the “ecology” of pure science.

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Ruddiman WF, Kutzbach JE (1991) Plateau uplift and climatic change. Sci Am 264:66–75 Ruddiman WF, Prell WL, Raymo ME (1989) Late Cenozoic uplift in southern Asia and the American West: rationale for general circulation modelling experiments. J Geophys Res 94:18379–18391 Rull V (2010) Ecology and palaeoecology: two approaches, one objective. Open Ecol J 3:1–5 Sahney S, Benton MJ, Ferry PA (2010) Links between global taxonomic diversity, ecological diversity and the expansion of vertebrates on land. Biol Lett 6:544–547 Sargis EJ (2002) Primate origins nailed. Science 298:1564–1565 Sarmiento EE, Stiner E, Mowbray K (2002) Morphology-based systematics (MBS) and problems with fossil hominoid and hominid systematics. Anat Rec (New Anatomy) 269:50–66 Savin SM, Douglas RG, Stehli FG (1975) Tertiary marine paleotemperatures. Geol Soc Am Bull 86:1499–1510 Schrenk F, Sandrock O, Kullmer O (2004) An “open source” perspective on earliest hominid origins. Coll Anthropol 28(2):113–119 € Schwerdtfeger F (1968) Okologie der Tiere (Ein Lehr- und Handbuch in drei Teilen) – Auto¨kologie. Verlag Paul Parey, Hamburg, p 461 Science-Extra (2009) Ardipithecus ramidus, http://www.sciencemag.org/site/feature/misc/ webfeat/ardipithecus/ Senut B, Pickford M, Gommery D, Mein P, Cheboi K, Coppens Y (2001) First hominid from the Miocene (Lukeino Formation, Kenya). C R Acad Sci 332:137–144 Seppa¨ H (2009) Palaeoecology. In: Encyclopedia of life sciences (eLS). Published online Shackleton NJ (1995) New data on the evolution of Pliocene climatic variability. In: Vrba ES, Denton G, Burckle L, Partridge T (eds) Paleoclimate and evolution with emphasis on human origins. Yale University Press, New Haven, pp 242–248 Shackleton NJ, Boersma A (1981) The climate of the Eocene ocean. J Geol Soc Lond 138:153–157 Shackleton NJ, Backman J, Zimmermann H (1984) Oxygen isotope calibration of the onset of icerafting and history of glaciation in the North Atlantic region. Nature 94:18379–18391 Shackleton NJ, Berger A, Peltier WR (1990) An alternative astronomical calibration of the lower Pleistocene timescale based on ODP Site 677. Trans R Soc Edin Earth Sci 81:251–261 Stadler M, Seeger F, Raeithel A (1975) Psychologie der Wahrnehmung. Juventa Verlag, M€ unchen, p 256 Stanley SM (1994) Historische Geologie. Spektrum Akademischer Verlag, Heidelberg, p 634 Stanley SM (1995) New horizons for paleontology, with two examples: the rise and fall of the cretaceous supertethys and the cause of the modern ice age. J Palaeontol 69:999–1007 Stauffer RL, Walker A, Ryder OA, Lyons-Weiler M, Hedges SB (2001) Human and ape molecular clocks and constraints on palaeontological hypotheses. J Hered 92:469–474 Strait DS, Wood BA (1999) Early hominid biogeography. Proc Natl Acad Sci U S A 96:9196–9200 Sussman RL, Stern JT, Jungers WC (1985) Locomotor adaptations in the Hadar hominids. In: Delson E (ed) Ancestors: the hard evidence. Wiley-Liss, New York, pp 184–192 Sussmann RW (1991) Primate origins and the evolution of angiosperms. Am J Primatol 23:209–223 Tattersall I (1992) Species concept and species identification in human evolution. J Hum Evol 22:341–349 Tattersall I (1996) Palaeoanthropology and preconception. In: Meikle WE, Howell FC, Jablonski NG (eds) Contemporary issues in human evolution. California Academy of Sciences, San Francisco, pp 47–54 Tattersall I (1998) Becoming human. Harcourt Brace, New York Page 41 of 44

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Index Terms: Abiotic factors 2, 6–7, 13 climatic influence 7 physicogeography 13 tectonism 6 volcanism 6 Biocenosis 20 Biomes 15 Biostratinomy 15 Biotic factors 2, 14 Coevolution 20 Dating methods 20–21 Ecology 1–2, 5 Ecolution 23 Ecosystems 15, 17 Facies fossils 19 Facies 17 Index fossils 19 Middle-range theory 5 Neoecology 2 See Ecology Paleoecology 1–2 Savannah hypothesis 29 Stratigraphy 17–19 Taphonomy 15 Turnover pulses 23, 25 Uniformitarianism 3–4 Variability selection hypothesis 25

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013

Hominin Paleodiets: The Contribution of Stable Isotopes Matt Sponheimera* and Julia Lee-Thorpb a Department of Anthropology, University of Colorado at Boulder, Boulder, CO, USA b Research Laboratory for Archaeology, Oxford University, Oxford, UK

Abstract Stable isotope ratio analysis is now regularly used to investigate early hominin diets based upon the principle that ‘you are what you eat’. Analysis of collagen from Neanderthals and anatomically modern humans prior to 20 Ka has shown them to be significantly enriched in 15N compared to contemporaneous carnivores and herbivores. This suggests that much of their dietary protein, although not necessarily their dietary energy, came from animal foods. Carbon isotope analysis of the enamel mineral of southern African australopiths and early Homo has revealed that these taxa consumed
30 % C4 foods such as tropical grasses, sedges, or animals that ate these foods. Moreover, the australopiths are characterized by remarkably variable d13C values. Chimpanzees, in contrast, are nearly pure C3 consumers even in environments with abundant C4 vegetation. These data suggest that when confronted with increasingly open areas, chimpanzees continue to exploit the foods that are most abundant in forest environments, whereas southern African australopiths utilized novel C4 resources in addition to forest foods. However, new data from eastern and central Africa show that not all australopiths follow this pattern. The earliest australopiths had nearly pure C3 diets, but by about 2 Ma others ate predominantly C4 vegetation. It also appears that increased masticatory robusticity in the australopiths is associated with greater C4 consumption.

Keywords Anatomically modern human; Australopithecus; Carbon; Early homo; Isotope; Neanderthal ; Nitrogen; Palaeodiet; Paranthropus

Introduction The nature of early hominin diets has been the subject of lively debate and not without good reason (e.g., Dart 1957; Robinson 1954; Jolly 1970; Brain 1981; Binford 1981; Grine and Kay 1988; Sillen 1992; Stiner 1994; Lee-Thorp et al. 1994; Sponheimer and Lee-Thorp 1999; Richards et al. 2000; Speth and Tchernov 2001). Most large primates spend at least 50 % of their waking hours searching for or consuming food (e.g., Altmann and Altman 1970; Teleki 1981; Goodall 1986; see “▶ The Biology and Evolution of Ape and Monkey Feeding,” “▶ Great Ape Social Systems,” “▶ The Biotic Environments of the Late Miocene Hominids”). Thus, if we seek to know what “a day in the life” of our ancestors was like, understanding what they ate would represent an enormous step in that direction (see “▶ Dental Adaptations of African Apes”). Furthermore, diet is considered among the *Email: [email protected] *Email: [email protected] Page 1 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013

most important factors underlying behavioral and ecological differences among extant primates (Ungar 1998; Fleagle 1999), and thus the story of our ancestors’ evolving diets is likely to be intertwined with that of how our species, Homo sapiens, came to be. We can glean paleodietary information from many sources (see “▶ Role of Environmental Stimuli in Hominid Origins”). Archaeological evidence in the form of stone tools and butchered animal bones is one source of dietary information, which tells us about the kinds of animals that hominins utilized as well as their procurement strategies (e.g., Binford 1981; Brain 1981; Blumenschine 1987; Stiner 1994; Speth and Tchernov 2001). Yet, such evidence tends to overemphasize the importance of animal foods at the expense of plant foods that make up the bulk of most primate diets (e.g., Lee 1979; Eaton and Konner 1985; Milton 2002). Moreover, the first potential hominins (Senut et al. 2001; Brunet et al. 2002; Haile-Selassie et al. 2004) precede the earliest archaeological traces by millions of years (Semaw et al. 1997; De Heinzelin et al. 1999), and thus the archaeological record remains silent with regard to the diets of the earliest hominins (see “▶ Archaeology” and “▶ Overview of Paleolithic Archeology”). As a result, paleoanthropologists have had to look for other sources of paleodietary information. Dental allometry/morphology and microwear have received much attention and provided important insights into the diets of our ancestors (see “▶ Hominoid Cranial Diversity and Adaptation,” “▶ Dental Adaptations of African Apes”; Robinson 1954; Grine 1981, 1986; Grine and Kay 1988; Ungar and Grine 1991; Teaford et al. 2002; Ungar 2004). Still, these techniques have limitations. For instance, the relatively large incisors and bunodont molars of modern Papio suggest a frugivorous diet (Hylander 1975; Fleagle 1999; Ungar 1998), and yet many Papio populations consume large quantities of grasses, for which they have no apparent dental specializations (Altmann and Altman 1970; Harding 1976; Dunbar 1983; Strum 1987). Ungar (2004) has also argued that the dental morphology of extant apes and early hominins may tell us more about their fallback foods than it does about their “typical” diets. Dental microwear, in turn, reveals a great deal about the mechanical properties of a primate’s food. Primates that eat hard, brittle foods, such as gray-cheeked mangabeys (Lophocebus albigena), have relatively more microscopic pitting on their molars than do those that eat more pliant, tough foods like mountain gorillas (Gorilla gorilla beringei) (Grine and Kay 1988; Ungar 1998). However, microwear is quickly obliterated and therefore provides dietary information for a few brief days, which may or may not be representative of an individual’s “average” diet. In addition, soft foods, such as animal flesh, may not always produce recognizable microwear signatures. Thus, even with these important techniques in our paleodietary arsenal, a great deal about the diets of early hominins remains unknown. Consequently, new paleodietary techniques have emerged in recent years, one of the most important of which is stable isotope analysis. The idea behind this technique is that “you are what you eat.” In other words, the isotopic composition of one’s food is ultimately traceable in one’s tissues. Thus, stable isotope analysis provides a direct chemical means of investigating the diets of modern and fossil primates. In this paper, we address the contribution of stable isotope analysis to our understanding of early hominin diets. The paper is divided roughly into two sections: stable isotope analysis of bone and dentine collagen, which has been used to investigate the diets of our close cousins the Neanderthals and early modern humans (Bocherens et al. 1991, 1999, 2001, 2005; Fizet et al. 1995; Richards et al. 2000, 2001; Pettitt et al. 2003; Schulting et al. 2005), and stable isotope analysis of enamel apatite, which has shed much light on the diets of the South African australopiths and early Homo (see “▶ Analyzing Hominin Phylogeny,” “▶ The Species and Diversity of Australopiths,” “▶ The Earliest Putative Homo Fossils”; Lee-Thorp et al. 1994, 2000; Sponheimer and Lee-Thorp 1999, 2003; van der Merwe et al. 2003; Sponheimer et al. 2005a). We proceed in this reverse chronological order in an effort to trace the general development of Page 2 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013

Table 1 Specimen numbers, taxon, d13C, d15N, and publication date for Neanderthals and anatomically modern humans (The 1991 publication is Bocherens et al. 1991; the 1995 publication is Fizet et al. 1995; the 1999 publication is Bocherens et al. 1999; the 2000 publication is Richards et al. 2000; the 2001a publication is Bocherens et al. 2001; the 2001b publication is Richards et al. 2001; the 2003 publication is Pettitt et al. 2003; the 2005a publication is Bocherens et al. 2005; and the 2005b publication is Schulting et al. 2005)) Specimen Marillac 9 Marillac 10 Scladina 4A-2 Vindija 207 Vindija 208 Scladina 1B-4 Engis 2 Spy OMO 1 Saint-Césaire 1 Marillac M70 c10 F10-41 Marillac H1 Marillac H2 Brno-Francouzska 2 Dolní Vestoniče 35 Kostenki 1 Kostenki 18 Mal’ta 1 Paviland 1 Sunghir 1 Sunghir 2 Sunghir 3 Arene Candide 1 Eel-1

Taxon Neanderthal Neanderthal Neanderthal Neanderthal Neanderthal Neanderthal Neanderthal Neanderthal Neanderthal Neanderthal Neanderthal Neanderthal AMH AMH AMH AMH AMH AMH AMH AMH AMH AMH AMH

d13C 20.2 19.1 19.9 19.5 20.5 21.2 19.6 19.8 19.8 19.1 19.5 21.8 19.0 18.8 18.2 19.1 18.4 18.4 19.2 19.0 18.9 17.6 19.2

d15N 9.3 11.6 10.9 10.1 10.8 11.8 12.6 11.0 11.4 11.5 11.4 8.4 12.3 12.3 15.3 13.1 12.2 9.3 11.3 11.2 11.3 12.4 11.2

Published 1991 1995 1999 2000 2000 2001a 2001a 2001a 2005a 2005a 2005a 2005a 2001b 2001b 2001b 2001b 2001b 2001b 2001b 2001b 2001b 2003 2005b

paleodietary stable isotope studies: collagen was first utilized in 1977 with enamel apatite studies appearing a decade later. In addition, the temporally and geographically restricted discussion herein (i.e., the emphasis on European Neanderthals and South African australopiths) is more a reflection of the limited degree to which stable isotopes have been used to investigate the diets of Plio-Pleistocene hominins, than selective presentation on our part. The only data we have excluded for the purpose of this paper are for specimens younger than 20 Ka. The stable isotope data for all older hominins, which we are aware of at least, are discussed herein and can be found in Tables 1 and 2.

Collagen

The first paleodietary study using stable isotopes sought to document maize consumption among Native American populations in New York State (Vogel and van der Merwe 1977). This application was made possible by differences in the photosynthetic pathways of plants. Tropical grasses, such as maize, use C4 photosynthesis, while virtually all other potential plant foods in New York State use C3 photosynthesis. The C3 photosynthetic pathway discriminates markedly against 13C, and as a consequence, C3 plants have very depleted 13C/12C ratios. In contrast, plants that utilize the C4 photosynthetic pathway discriminate less against 13C and are consequently relatively enriched in

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013

Table 2 Specimens, taxa, proveniences, d13C values, and references for South African australopith and early Homo specimens Specimen SK1512 SK879 SKX5015 SK878 SK879 SKX1312 SKX333 SKX35025 SK876 TM 1600 SK 19 SK 41 SK 57 SK 14000 SK 14132 SKW 6 SKW 3068 SKW 4768 MLD 30 MLD 41 MLD12 MLD28 STS 31 STS 32 STS 45 STS 72 STS 2218 STW 73 STW 276 STW 252 STW 211 STW 304 STW 14 STW 315 STW 309b (409) STW 229 STW 303 STW 236 STW 213i STW 207 SK 80/847 SK 27 SK 2635

Tooth P M LM3 RP3 M LM1 RM1 RM M LM2 RM3 LM3 LM3 LM3 RM3 LM3 LM2 LM2 RM1 M RM3 RM3 RM3 RM3 RM2 RM3 M RM2 LM1 RM1 M M LM1 Ldm2 LM1 P RM2 P LM1 ? P LM3 P

Taxon Paranthropus robustus Paranthropus robustus Paranthropus robustus Paranthropus robustus Paranthropus robustus Paranthropus robustus Paranthropus robustus Paranthropus robustus Paranthropus robustus Paranthropus robustus Paranthropus robustus Paranthropus robustus Paranthropus robustus Paranthropus robustus Paranthropus robustus Paranthropus robustus Paranthropus robustus Paranthropus robustus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus? Australopithecus africanus? Australopithecus africanus? Early Homo Early Homo Early Homo

Provenience SK1 SK1 SK1 SK1 SK1 SK2 SK2 SK3 SK1 KB3 SK1 SK1 SK1 SK1 SK1 SK1 SK1 SK1 MAK3 MAK3 MAK3 MAK3 ST4 ST4 ST4 ST4 ST4 ST4 ST4 ST4 ST4 ST4 ST4 ST4 ST4 ST4 ST4 ST4 ST4 ST4 SK1 SK1 SK1

d13C 8.8 8.5 9.6 6.8 8.1 8.1 10.0 7.9 6.7 7.9 –6.3 6.7 6.5 5.9 6.9 7.0 8.1 7.4 5.6 11.3 7.7 8.1 6.8 7.8 4.0 9.7 5.9 8.8 8.0 7.4 7.3 7.4 6.7 5.7 6.1 5.8 4.3 3.7 1.8 2.0 7.1 8.2 9.2

References Lee-Thorp et al. (1994) Lee-Thorp et al. (1994) Lee-Thorp et al. (1994) Lee-Thorp et al. (1994) Lee-Thorp et al. (1994) Lee-Thorp et al. (1994) Lee-Thorp et al. (1994) Lee-Thorp et al. (1994) Lee-Thorp et al. (2000) Sponheimer et al. (2005a) Sponheimer et al. (2005a) Sponheimer et al. (2005a) Sponheimer et al. (2005a) Sponheimer et al. (2005a) Sponheimer et al. (2005a) Sponheimer et al. (2005a) Sponheimer et al. (2005a) Sponheimer et al. (2005a) Sponheimer and Lee-Thorp (1999a) Sponheimer and Lee-Thorp (1999a) Sponheimer and Lee-Thorp (1999a) Sponheimer and Lee-Thorp (1999a) Sponheimer et al. (2005a) Sponheimer et al. (2005a) Sponheimer et al. (2005a) Sponheimer et al. (2005a) Sponheimer et al. (2005a) van der Merwe et al. (2003) van der Merwe et al. (2003) van der Merwe et al. (2003) van der Merwe et al. (2003) van der Merwe et al. (2003) van der Merwe et al. (2003) van der Merwe et al. (2003) van der Merwe et al. (2003) van der Merwe et al. (2003) van der Merwe et al. (2003) van der Merwe et al. (2003) van der Merwe et al. (2003) van der Merwe et al. (2003) Lee-Thorp et al. (2000) Lee-Thorp et al. (2000) Lee-Thorp et al. (2000)

In the provenience column, site abbreviations (SK Swartkrans, MAK Makapansgat, ST Sterkfontein, KB Kromdraai B) are followed by the appropriate Member number

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013 −10 −12 −14

δ13C (‰)

−16

n = 818

−18 −20 −22 −24

n = 650

−26 −28 −30

C4 Plants

C3 Plants

Fig. 1 13C/12C ratios of plants using C3 (trees, bushes, shrubs, and forbs) and C4 photosynthesis (grasses and some sedges) in Kruger National Park, South Africa. The boxes represent the 25th–75th percentiles (with the medians as horizontal lines), and the whiskers show the 10th–90th percentiles. The carbon isotope compositions of plants using these different photosynthetic pathways are highly distinct. Maize is a tropical grass that uses C4 photosynthesis, and thus it has a very different carbon isotope composition than other foods that were consumed by Native Americans in New York State (Vogel and van der Merwe 1977) 13

C (Smith and Epstein 1971; Fig. 1). These distinct isotopic signatures are passed down into the tissues of individuals that eat these plants. Thus, individuals who eat large quantities of C4 plants like maize will be relatively enriched in 13C compared to those who eat only C3 vegetation (see “▶ Role of Environmental Stimuli in Hominid Origins,” “▶ Origins of Homininae and Putative Selection Pressures Acting on the Early Hominins,” “▶ Analyzing Hominin Phylogeny,” “▶ The Species and Diversity of Australopiths”). Vogel and van der Merwe (1977) analyzed the bone collagen of individuals ranging in age from ~4,000 B.P. to ~500 B.P. They saw little evidence of maize consumption among the oldest individuals but found that maize had become a very important dietary resource by about 1,000 B.P. – sometimes representing up to 50 % of an individual’s diet. This study paved the way for a plethora of innovative applications in the following decades which relied on stable isotope abundances in bone collagen (see “▶ Taphonomic and Diagenetic Processes”); however, since collagen is rarely preserved for more than 10,000 years, these investigations were largely confined to the recent past. Yet, it has been shown that, under the right conditions, bone collagen can survive for 200,000 years or more (Jones et al. 2001). Thus, it has proven possible to analyze the bone collagen of late Pleistocene hominins in certain cases.

Collagen: Methodological Considerations Before proceeding to the hominin data, we will briefly discuss a few relevant methodological considerations. Much has changed since the early days of stable isotope analysis. Today, only small samples are required for analysis, and automation has led to significantly increased sample throughput in labs around the world. Nevertheless, the basic procedures have remained largely the same, even though the protocols vary somewhat from lab to lab. Here, we briefly summarize the operational protocols of the labs that have analyzed the collagen of early hominins. One must keep in mind, however, that this is meant to be a general summary, not an exhaustive step by step explication of analytical procedures. After surface cleaning, bone or dentine samples are demineralized in diluted HCl (0.5–1.0 M) for periods ranging from 20 min to 5 days. Performing this step at low temperature (5  C) is one recent innovation that allows collagen to be extracted from very old, fragile samples (Richards and Hedges 1999; Jones et al. 2001). The insoluble residue may then be soaked in 0.125 N NaOH to remove contaminating humic acids; but as this leads to collagen solubilization and decreased extraction Page 5 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013

yields, it is no longer favored. Fortunately, neglecting this step appears to have little effect on the resulting stable isotope ratios (Bocherens et al. 1999). The residue is then often gelatinized in weak HCl at 75–100  , filtered, and freeze-dried. A small (~1 mg) sample of this purified collagen is then combusted in an elemental analyzer, and the resultant CO2 and N2 gases are analyzed for 13C/12C and 15N/14N abundances in a stable isotope ratio mass spectrometer. Stable light isotope ratios are expressed as d values in parts per thousand (‰) relative to international standards, which are PDB (a marine carbonate) and atmospheric N2 for carbon and nitrogen, respectively. Standard deviations of replicate measurements are generally about 0.1 ‰ for carbon and 0.2 ‰ for nitrogen. Importantly, collagen degradation is known to alter stable isotope ratios significantly. To produce reliable results, collagen must generally have a carbon/nitrogen ratio between 2.9 and 3.6, with carbon and nitrogen percentages of at least 15 % and 5 %, respectively (Ambrose 1990). Our understanding of the relationship between dietary d13C and collagen d13C has improved significantly since the first use of stable isotopes for paleodietary reconstruction. Experimental studies of rodents on controlled diets have shown that collagen d13C is enriched by about +5 ‰ relative to dietary protein (Ambrose and Norr 1993; Tieszen and Fagre 1993), as dietary amino acids are preferentially utilized for tissue synthesis. In contrast, carbon from dietary carbohydrate and lipid makes much less of a contribution to bone collagen (or indeed hair, muscle, etc.). Consequently, bone collagen d13C (and d15N) tells you more about the protein component of an individual’s diet than it does about their “whole” or “bulk” diet. This is significant, as animal foods, which are high in protein, will be overrepresented in bone collagen at the expense of low-protein vegetable foods. This bias must be borne in mind when interpreting collagen stable isotope data.

The Neanderthals

Bocherens et al. (1991) performed the first stable isotope analysis of a Neanderthal and associated fauna from the site of Marillac in France. This study demonstrated that enough collagen could be extracted from bones more than 40,000 years old and paved the way for subsequent analyses of Neanderthals from Marillac and Saint-Césaire (Fizet et al. 1995; Bocherens et al. 2005); Scladina Cave, Awirs Cave, and Betche-al-Roche Cave in Belgium (Bocherens et al. 1999, 2001), and Vindija Cave in Croatia (Richards et al. 2000). Virtually all native European plants use the C3 photosynthetic pathway. As a result, these plants have similar carbon isotope compositions, although those in densely wooded environments are somewhat depleted in 13C due to the canopy effect (Vogel 1978; van der Merwe 1989). Thus, not surprisingly, carbon isotopes revealed little about the diets of Neanderthals, save for the possibility that they utilized few food resources from closed environments (Bocherens et al. 1999; Richards et al. 2000). The nitrogen isotopes in Neanderthal bone collagen, however, proved more revealing. Nitrogen isotopes ratios (15N/14N) are known to increase by about 3 ‰ up every step in the food chain (e.g., Minagawa and Wada 1984; Schoeninger and DeNiro 1984; Ambrose and DeNiro 1986). Thus, within a hypothetical food web, if plants have d15N values of 0 ‰, herbivores like reindeers have d15N values of about 3 ‰, while carnivores such as wolves have d15N values of about 6 ‰. And although nitrogen isotope distributions in food webs are more complicated than this hypothetical example suggests – due to heterogeneity in plant d15N and the disparate physiological adaptations and requirements of mammals (Ambrose and DeNiro 1986; Sealy et al. 1987; Sponheimer et al. 2003a) – the general pattern has been shown to be robust in both terrestrial and marine ecosystems. Thus, analysis of nitrogen isotopes in bone collagen can potentially reveal the trophic level at which a hominin was feeding. This is relevant for investigating Neanderthal diets, as their degree of carnivory and manner of carcass acquisition (hunting or scavenging) have been the subject

Page 6 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013 15 13

n = 12

n = 26 δ15N (‰)

11 n = 11 9

n = 132

7 5 3 H

al

re

re

rth

ivo

ivo

b er

C

n ar

e nd

H

AM

a

Ne

Fig. 2 d15N of Neanderthals, mid-Upper Paleolithic humans, herbivores, and carnivores. The boxes represent the 25th–75th percentiles (with the medians as horizontal lines) and the whiskers show the 10th–90th percentiles

of considerable debate (e.g., Binford 1981; Mellars 1989; Stiner 1994; Speth and Tchernov 2001; see “▶ Neanderthals and Their Contemporaries”). Intriguingly, all published studies have shown that Neanderthals have very high d15N, well above that of contemporaneous herbivores such as horses (Equus caballus), reindeer (Rangifer tarandus), and bison (Bison priscus) and similar to that of carnivorous wolves (Canis lupus), hyenas (Crocuta spelaea), and lions (Panthera spelaea) (Bocherens et al. 1991, 1997, 2001, 2005; Fizet et al. 1995; Richards et al. 2000). Indeed, analysis of variance and Fisher’s PLSD test of the combined datasets show that Neanderthal d15N (x ¼ 10.9 ‰, s.d. ¼ 1.1, n ¼ 12) is not only significantly higher than herbivore d15N (x ¼ 5.8 ‰, s.d. ¼ 1.6, n ¼ 132) (P < 0.001) but also slightly higher than carnivore d15N (x ¼ 9.7 ‰, s.d. ¼ 1.1, n ¼ 26) (P ¼ 0.02) (Fig. 2). We should note that the combined dataset contains specimens that accumulated over ~70,000 years and in locations throughout Europe and that such temporal and spatial mixing increases intrataxonomic variability making statistically significant differences between taxa less likely. For instance, Stevens and Hedges (2004) found that European horse (Equus spp.) d15N fluctuated by at least 4 ‰ over the last 40,000 years due to glacially mediated changes in the nitrogen cycle. Hence, it is particularly striking that significant differences are found between Neanderthals, herbivores, and carnivores without controlling for temporal and spatial variation. In general, the d15N data appear to suggest that Neanderthals received much of their dietary protein from animal foods (Richards 2000). Enrichment in 15N compared to (other) carnivores may suggest a dependence on herbivores with relatively high d15N such as mammoths (Mammuthus primigenius) or even the consumption of omnivorous bears (Ursus spp.) (Richards et al. 2000; Bocherens et al. 2001, 2005). While the interpretation of these data remains difficult, it is clear that Neanderthal diets were distinct from those of contemporary herbivorous fauna. This leads inexorably to the question, “Were Neanderthal diets distinct from those of their hominin contemporaries?” (see “▶ Neanderthals and Their Contemporaries”). While it has not yet been possible to compare the stable isotope compositions of Neanderthals and contemporaneous anatomically modern humans (AMH), Richards et al. (2001) were able to analyze nine near contemporaries from the mid-Upper Paleolithic (~28–20 Ka) at Brno-Francouzská and Dolní Věstonice (Czech Republic); Kostenki, Mal’ta, and Sunghir (Russia); and Paviland (Great Britain). They compared these anatomically modern humans to the five Neanderthals that had been published at the time and argued that the modern humans were even more elevated in d15N (x ¼ 12.0 ‰, s.d. ¼ 1.6, n ¼ 9). This suggested that anatomically modern humans were also highly dependent on Page 7 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013 2 0

δ13C (‰)

−2 n = 60

−4

n = 18

−6 −8

−10

n = 61

n = 19

−12 −14

s

er

ed

C4

a

it lop

str

Au

s

s

cu

he

Fe

r

Pa

s

er

pu

ed

ro

th an

C3

Fe

Fig. 3 d13C for australopiths, C3 plant consumers (browsing/frugivorous bovids and giraffids) and C4 plant consumers (grazing bovids and equids). The boxes represent the 25th–75th percentiles (with the medians as horizontal lines) and the whiskers show the 10th–90th percentiles. Given the size of this dataset, there can be no doubt that australopith d13C is highly distinct from that of associated browser/frugivores (This figure was produced using data available in 2006. The fully updated dataset is available in Sponheimer et al. (2013))

animal foods. Richards et al. (2001) argued, however, that even the consumption of high d15N herbivores like mammoth would not be sufficient to account for the extremely elevated d15N of these AMH. Instead, they suggested that these humans had begun to diversify their resource base to include freshwater aquatic resources such as fish and waterfowl, which can be more enriched in 15N than terrestrial resources (Dufour et al. 1999; Katzenberg and Weber 1999). This suggestion was rather surprising, as there is little direct archaeological evidence for exploitation of such foods at this time, although such evidence becomes abundant by the late Upper Paleolithic. Yet, with the subsequent publication of seven new Neanderthal specimens (Bocherens et al. 2001, 2005) and two more mid-Upper Paleolithic humans (Pettitt et al. 2003; Schulting et al. 2005), there is no longer any statistically significant difference in the d15N of AMH (x ¼ 11.8 ‰, s.d ¼ 1.6, n ¼ 11) and Neanderthals (P ¼ 0.06 t-test; P ¼ 0.09 Mann-Whitney U) (Fig. 3; Table 1). There is, however, a small but significant difference in the d13C of AMH (x ¼ 18.7 ‰, s.d. ¼ 0.5, n ¼ 11) and Neanderthals (x ¼ 20.0 ‰, s.d. ¼ 0.8, n ¼ 12) (P < 0.01 t-test and Mann-Whitney U), although the meaning of this difference is unclear. A greater reliance on open area resources such as 13Cenriched reindeer by AMH is one of many possible explanations. More salient from the perspective of dietary breadth, Levene’s test reveals no significant differences in the isotopic variability of Neanderthals and AMH (d13C, P ¼ 0.23; d15N, P ¼ 0.61), and thus there is little isotopic support for utilization of novel resources or greater resource breadth in AMH prior to 20 Ka. These stable isotope studies are an important complement to traditional archaeological paleodietary studies, as they represent a direct measure of the foods that an individual ate that is independent of the taphonomic biases that bedevil faunal analyses (Lyman 1994). Nevertheless, interpretation of these stable isotope data is not straightforward, and there remain a number of important unanswered questions. For instance, why are both hominins enriched by more than 5 ‰ compared to associated herbivores when an enrichment of about 3 ‰ would be expected for a carnivore? Stated otherwise, why is their d15N significantly higher than that of associated carnivores? As discussed earlier, this may be partially, but not satisfactorily, explained by the consumption of herbivores with unusually high d15N such as mammoths or even by the consumption of omnivores and/or aquatic resources. Another possibility, however, is that there is some

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013

physiological explanation for their extremely high d15N. Experimental studies have shown that when herbivores are fed diets with crude protein contents that are much greater than their nutritional requirements, their diet-tissue spacing can become much greater than 3 ‰ (Sponheimer et al. 2003a). This implies that if the prevailing environment forced Neanderthals to consume high-protein diets that considerably exceeded their crude protein requirements, their diet-tissue spacing might have exceeded 3 ‰, thus artificially increasing their d15N compared to other taxa. On the other hand, committed carnivores generally have smaller diet-tissue spacing than herbivores (Robbins et al. 2005). Regardless, the anomalously high d15N of mammoths and low d15N of cave bears (Bocherens et al. 1997; Ambrose 1998) may also hint at the importance of physiological adaptations in determining an organism’s nitrogen isotope composition. It is worth noting that while such interpretive difficulties exist, they do not diminish the significance of these studies. Even if the Neanderthals did have artificially increased diet-tissue spacing due to a high-protein intake, it might erase their distinctiveness from other carnivores, but would certainly not make them look herbivorous.

Enamel Apatite Older hominin material is not amenable to this form of analysis as bone collagen is rarely preserved from beyond the late Pleistocene (Jones et al. 2001). However, the carbon isotopes in the bone’s mineral component (a biological apatite) can also be used as dietary proxies (Sullivan and Krueger 1981, 1983; Lee-Thorp and van der Merwe 1987). But even though bone mineral clearly persists beyond bone collagen, it can be altered postmortem, often resulting in the loss of the biogenic dietary signal (Schoeninger and DeNiro 1982; Lee-Thorp and van der Merwe 1987; Lee-Thorp 2001). This is due to the bone’s high organic content, porosity, and small crystal size, which make it susceptible to dissolution/reprecipitation phenomena and facilitate the incorporation of diagenetic carbonate ions (e.g., LeGeros 1991; Lee-Thorp 2002; Lee-Thorp and Sponheimer 2003). Thus, bioapatite paleodietary studies were forestalled until Lee-Thorp and van der Merwe (1987) showed that dental enamel from ancient fauna with well-understood diets retained its biogenic isotope signal. For example, they showed that fossil equids, like their modern counterparts, had C4-dominated signatures, while fossil tragelaphines had C3-dominated signatures like their modern descendants. Since then, numerous empirical and theoretical studies have substantiated this finding (e.g., Lee-Thorp et al. 1989; Wang and Cerling 1994; Sponheimer and Lee-Thorp 1999b; Hoppe et al. 2003; Lee-Thorp and Sponheimer 2003; Trickett et al. 2003). The enamel’s resistance to diagenetic phenomena is conferred by its virtually organic-free and highly-crystalline state (LeGeros 1991), which renders it effectively “prefossilized.” Thus, tooth enamel offered the possibility of investigating the diets of early Pleistocene and even Pliocene hominins.

Enamel Bioapatite: Methodological Considerations For the reasons outlined above, only tooth enamel is sampled for stable isotope analysis of hominin and non-hominin specimens that are millions of years old. Initially, a sample of 200–400 mg was needed (about half of a baboon’s molar), but advances in mass spectrometry have reduced the necessary sample size to a few milligrams (Lee-Thorp et al. 1997; Sponheimer 1999). As a result, it has become possible to sample teeth while producing little to no readily observable damage. As a result, more teeth have become available for analysis. We will now give an overview of the recent sampling and pretreatment protocols, which are modified after Lee-Thorp et al. (1997) and Sponheimer (1999). Specimens are given a careful visual inspection prior to sampling, and those that are heavily stained or have mineral inclusions in the potential sampling areas are excluded from analysis. Generally, only permanent dentition is Page 9 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013

sampled, with a heavy emphasis on late-forming teeth such as M2s and M3s. Powdered enamel samples are acquired (usually from a tooth’s buccal surface) using a low-speed rotary drill with a diamond-tipped burr. However, most of the recently sampled hominin teeth had been previously fractured, which allowed sampling between the occlusal surface and the enamel-dentine junction so as to avoid damage to the external surface of the teeth. Although only small samples are taken (~2 mg), we generally attempt to sample over as extensive an area as is possible, so as to obtain enamel formed over a considerable period of time. The enamel powder is soaked for about 10 min in 1.5 % sodium hypochlorite to remove organic contaminants and then rinsed to neutrality. The remaining enamel powder is then pretreated with 0.1 M acetic acid for ~10 min to remove diagenetic carbonates, rinsed to neutrality, and freeze-dried. It is worth noting that these pretreatment protocols can vary from lab to lab, and even within labs over time. As different pretreatments can lead to small but significant differences in a sample’s stable isotope composition (especially oxygen), one must compare stable isotope values for the teeth analyzed following different protocols with caution. Finally, each sample is placed in an individual reaction vessel and analyzed for 13C/12C and 18O/16O using an autocarbonate device coupled to a stable isotope ratio mass spectrometer. Carbon and oxygen isotope ratios are expressed as d (13C, 18O) values in parts per thousand (‰) relative to the PDB standard. The standard deviation of replicate measurements is typically 0.1 ‰ and 0.2 ‰ for d13C and d18O, respectively. Oxygen isotopes do provide ecological information (Kohn et al. 1996; Sponheimer and Lee-Thorp 1999c; Sponheimer and Lee-Thorp 2001), although they are much better known as paleoclimatic proxies (e.g., Prentice and Denton 1988; Ayliffe and Chivas 1990). For this reason, and because of space constraints, we will not discuss them as paleoecological indicators here. The relationship between dietary d13C and enamel apatite d13C has been well-studied. Unlike collagen, apatite tends to reflect the d13C of the “whole” or “bulk” diet, and not just the protein component (Ambrose and Norr 1993; Tieszen and Fagre 1993). Thus, apatite and bone collagen d13C provide different perspectives on an individual’s diet. Indeed, if one wanted to obtain the most complete picture of an individual’s diet, one should analyze both collagen and apatite, although this rarely happens in practice. Most important for our purposes here, however, is that enamel apatite provides a good average dietary signal and will equally reflect the consumption of vegetable and animal foods. Interestingly, however, it is evident that the relationship between dietary d13C and apatite d13C is not constant. Rodent apatite tends to be enriched by about +10 ‰ compared to diet (Ambrose and Norr 1993; Tieszen and Fagre 1993), while large mammal apatite is enriched by about +13 ‰ (Lee-Thorp et al. 1989b; Cerling and Harris 1999; Passey et al. 2005). These differences must be borne in mind when comparing rodent and non-rodent d13C but are of little significance for the present discussion.

The South African Australopiths and Early Homo As in the initial bone collagen study by Vogel and van der Merwe (1977), the South African australopith studies were based upon the distinct isotopic signatures of C3 (trees, bushes, shrubs, and forbs) and C4 plants (tropical grasses and some sedges). In the early 1990s, it was generally believed that Australopithecus africanus had a diet that of fleshy fruits and leaves, much like the modern chimpanzee (Pan troglodytes), while Paranthropus robustus consumed smaller, harder foods such as nuts (Grine 1981, 1986; Grine and Kay 1988; Ungar and Grine 1991). As these are all C3 foods, one would then expect that Australopithecus and Paranthropus would have d13C values indistinguishable from those of C3 browsers and frugivores. Several studies have shown, however, that the d13C of both australopiths is very distinct from that of their C3-consuming coevals

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013 −3 −4

δ13C (‰)

−5 −6 −7 −8 −9 −10 −11 −12 1.6

1.8

2

2.2 2.4 2.6 AGE (Ma)

2.8

3

3.2

Fig. 4 d13C of South African hominins through time. No temporal trend is evident, despite abundant evidence that South African hominin environments changed during this time

(Lee-Thorp et al. 1994, 2000; Sponheimer and Lee-Thorp 1999a; van der Merwe et al. 2003; Sponheimer et al. 2005a). Figure 3 shows the combined australopith dataset from Makapansgat, Sterkfontein, Kromdraai, and Swartkrans. Analysis of variance and Fisher’s PLSD test show that both Australopithecus (x ¼ 7.1 ‰, s.d. ¼ 1.8, n ¼ 19) and Paranthropus (x ¼ 7.6 ‰, s.d. ¼ 1.1, n ¼ 18) are strongly different from contemporaneous C3 (x ¼ 11.5 ‰, s.d. ¼ 1.3, n ¼ 61) and C4 consumers (x ¼ 0.6 ‰, s.d. ¼ 1.8, n ¼ 60) (P < 0.0001), but cannot be distinguished from each other. This distinction between the hominins and other fauna cannot be ascribed to diagenesis, as there is no evidence that browser or grazer d13C has been altered, and diagenesis should affect hominins and non-hominin fauna alike. If we take the mean d13C of C4- and C3-consuming herbivores as indicative of pure C4 and C3 diets, respectively, this would indicate diets of about 35–40 % C4 vegetation for both Australopithecus and Paranthropus. Thus, both were eating considerable quantities of C4 resources, possibly grasses, sedges, or animals that ate these plants. None of these possibilities were expected, as extant apes are not known to consume these foods to a significant degree (see “▶ Great Ape Social Systems”; Goodall 1986; McGrew et al. 1982). Indeed, even in environments where C4 foods are readily available, chimpanzee d13C does not indicate any C4 consumption (Schoeninger et al. 1999; Carter 2001). This suggests a fundamental niche difference between the australopiths and extant apes, which is not so surprising given the vast differences in their craniodental morphology (Grine 1981; Kay 1985; Teaford et al. 2002; Ungar 2004). It is worth noting that the evidence of extensive C4 consumption was not the only surprise in the australopith dataset. Indeed, hominin d13C turned out to be more variable than virtually all modern and fossil taxa that have been analyzed in South Africa (Lee-Thorp et al. 1994, 2000; Sponheimer et al. 1999, 2001, 2003b; Codron 2003; van der Merwe et al. 2003). There is considerable evidence that South African australopith habitats became more open between ~3.0 Ma and ~1.7 Ma (Vrba 1980, 1985; Reed 1997; Luyt and Lee-Thorp 2003), and it might be argued that this environmental change forced the australopiths to modify their diets over time, leading to their unusually variable d13C. Yet, linear regression demonstrates that there is no relationship between hominin d13C and time (P ¼ 0.63, R2 ¼ 0.01; Fig. 4) and there are no significant differences in hominin d13C between 3.0 Ma Makapansgat Member 3, 2.5 Ma Sterkfontein Member 4, and 1.8 Ma Swartkrans Member 1 (ANOVA, P ¼ 0.14). Indeed, what is most striking about these data is the lack of change in hominin d13C in the face of pronounced environmental change. Somewhat paradoxically, however, within any given time period (Member), hominin d13C is highly variable. This might simply indicate

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013

that the australopiths were extremely opportunistic primates with wide habitat tolerances that always inhabited a similarly wide range of microhabitats. This would be consistent with Wood and Strait’s (2004) recent suggestion that early hominins were eurytopic rather than ecological specialists. In the case of A. africanus, the variability is so great that one might be excused for asking if there are not two ecologically distinct taxa presently commingled within its hypodigm (see “▶ Analyzing Hominin Phylogeny,” “▶ The Species and Diversity of Australopiths’). In fact, if one includes the numbers for the three teeth (STW 236, STW 213i, STW 207) that are possibly, but not definitively, attributed to A. africanus (van der Merwe et al. 2003), then this taxon would range from nearly pure C3 to nearly pure C4 diets. Stated otherwise, the range of d13C within A. africanus (1.8 to 11.3 ‰) would be nearly as great as the entire range for ecologically disparate Papio and Theropithecus combined (+0.4 to 12.6 ‰) (Lee-Thorp et al. 1989). In and of themselves, stable isotopes cannot address the question of A. africanus unity; but numerous researchers have suggested that A. africanus might demonstrate more morphological variability than would be expected for a single taxon (Kimbel and White 1988; Clarke 1994; Lockwood 1997; Moggi-Cecchi et al. 1998). Hence, the possibility of two taxa, one subsisting largely on C4 foods and the other on C3 foods, cannot be dismissed. Further work addressing this hypothesis is warranted, but for the time being, we continue to work under the assumption that the specimens currently assigned to A. africanus represent a single species. In short, both South African australopiths consumed about 35–40 % C4 vegetation and have highly variable carbon isotope compositions. But how does this compare with early Homo? Lee-Thorp et al. (2000) tested for isotopic differences between Paranthropus and rarer early Homo specimens from Member 1 at Swartkrans. They assumed that if Homo consumed more animal foods, as was widely held, then its d13C values should be enriched compared to the australopiths because many savannah animals eat C4 grasses. Surprisingly, though, Homo d13C was very similar to that of the australopiths, and the results must be interpreted in a similar way: roughly 25 % early Homo’s diet came from C4 sources that included C4 grasses, C4 sedges, C4 animal products, or some combination of these foods (see “▶ The Earliest Putative Homo Fossils,” “▶ Defining the Genus Homo”; Lee-Thorp et al. 2000). However, only three Homo specimens from one site have been analyzed and published, and thus comparisons with the more numerous australopith data must be viewed with caution.

What C4 Foods? Which C4 foods did the South African australopiths utilize? This question is quite significant, as the use of these different resources might have a variety of physiological, social, and behavioral implications. For instance, if australopiths had a grass-based diet similar to the modern gelada baboon (Theropithecus gelada), this would almost certainly indicate that their diets were less nutrient dense than those of modern apes, possibly placing important limitations on burgeoning hominin brains and sociality (Aiello and Wheeler 1995; Milton 1999). The converse that australopiths ate diets rich in animal foods would indicate a leap in dietary quality over modern apes. This could have been a crucial step toward hominin encephalization, the development of stone tool industries, and increased social complexity (Milton 1999). Similarly, it has been suggested that consuming the underground storage organs of plants like C4 sedges would represent an increase in dietary quality over that of extant great apes because they are lower in dietary fiber than ape fallback foods (Conklin-Brittain et al. 2002). We will now discuss the evidence for the consumption of C4 grasses, C4 sedges, and animal foods in turn.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013

The Case for Grasses Some researchers noted that the robust craniodental anatomy of the australopiths might have been an adaptation for eating grass seeds and roots as do modern gelada baboons (Theropithecus gelada) (Jolly 1970; Wolpoff 1973). A dental microwear study of modern geladas showed that their molar microwear is dominated by scratches with little evidence of pitting (Teaford 1992), however, which is quite unlike the heavily pitted molars of the australopiths (Grine 1986; Grine and Kay 1988). This result is hardly surprising, though, as it would seem unlikely that relatively large-brained hominins could be sustained on gelada-like diet (high in fiber, low in protein and long-chain polyunsaturated fatty acids) without supplementation with higher-quality foods. Furthermore, the stable isotope results do not indicate a pure C4 diet, but rather one in which C4 foods are very important, but not exclusive. Therefore, even if the C4 component did originate from grasses, one would not expect australopiths to have Theropithecus-like microwear. One might expect, however, that australopiths and savannah baboon populations that consume large quantities of grass seasonally would show similarities in dental microwear (Altmann and Altman 1970; Harding 1976; Dunbar 1983; Strum 1987), and indeed two recent studies of Papio molar microwear noted a more australopith-like frequency of pitting than was found in Theropithecus (Daegling and Grine 1999; Nystrom et al. 2004). In addition, a recent elemental analysis of australopith tooth enamel showed that while Australopithecus, and to a lesser extent Paranthropus, had higher Sr/Ca ratios than carnivores, browsers, and papionins, their Sr/Ca was quite similar to grazers. In fact, the unusual combination of high Sr/Ca and low Ba/Ca in Australopithecus has only been found in modern fauna that heavily utilize the underground portions of grasses such as warthogs (Phacochoerus africanus) and African mole rats (Cryptomys hottentotus) (Sponheimer et al. 2005b). These elemental data are still preliminary and certainly cannot be used to state affirmatively that early hominins consumed grasses. Nevertheless, they are entirely consistent with the possibility and suggest avenues for future research. The Case for Sedges Sedges have also received attention as a potential C4 food for australopiths. Conklin-Brittain et al. (2002) argued that a trend toward desiccation in the Pliocene eroded forests and ultimately forced australopiths into new, more open habitats (see “▶ Role of Environmental Stimuli in Hominid Origins,” “▶ Zoogeography: Primate and Early Hominin Distribution and Migration Patterns,” “▶ The Biology and Evolution of Ape and Monkey Feeding”). Although the degree, manner, and timing of this deterioration are a matter of some debate, the fact that it occurred is not (Vrba 1985; DeMenocal 1995; Feibel 1997). Conklin-Brittain et al. (2002) reasoned that this loss of forest habitat forced australopiths into environments that were most similar to their ancestral forest homes, namely, wetlands, swamps, and river margins. Sedges are readily available in these environments and have been argued to be among the possible sources of the C4 signal in australopiths (Sponheimer and Lee-Thorp 1999a; Conklin-Brittain et al. 2002). Some sedges have underground storage organs that have protein levels equal to those of most chimpanzee foods (9 % crude protein), but much lower fiber levels (16 % fiber) than foods consumed by chimpanzees (33 %) (ConklinBrittain et al. 2002). Thus, the regular inclusion of sedges in australopith diets might represent an increase in dietary quality over extant great apes. Equally important, the underground portions of sedges would be relatively inaccessible to most mammals, yet readily accessible to hominins with crude-digging implements (Hatley and Kappelman 1980), making sedges a high-quality resource for which there is very little competition. Such foods might have been particularly important during the dry season when other preferred dietary resources were scarce. Moreover, there is evidence of humans and other primates consuming sedges. Modern humans have consumed sedges like Cyperus Page 13 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013

esculentus and C. papyrus for thousands of years (Tackholm and Drar 1973; Defelice 2002). Western lowland gorillas (Gorilla gorilla gorilla) have also been observed consuming the pith of sedges, although in small quantities (see “▶ Great Ape Social Systems”; Doran and McNeilage 1998). Finally, Australopithecus’ high Sr/Ca is consistent with the consumption of sedge USOs (Sillen et al. 1995; Sponheimer et al. 2005b), although as previously mentioned this is also consistent with the consumption of grass USOs. But how likely is it that the observed C4 signal in early hominins was derived from C4 sedges? Although 33 % of the world’s sedges use the C4 photosynthetic pathway (Sage et al. 1999), it is incorrect to assume that all or even most sedges available to australopiths would have utilized the C4 pathway. Although 65 % of Kenyan sedges reportedly use C4 photosynthesis (Hesla et al. 1982), only 35 % do in South Africa (Stock et al. 2004). More to the point, a study of sedges in riverine habitats similar to those inhabited by australopiths found that only 28 % use C4 photosynthesis (Sponheimer et al. 2005a). Thus, unless the South African australopiths deliberately sought out C4 sedges or the distribution of sedges was markedly different during the Pliocene, the australopiths would have had to have had a diet of 100 % sedges to come close to producing the observed 35–40 % C4 signal. A slightly more probable scenario than this extreme sedge specialization is that the australopiths deliberately sought out C4 sedges with particularly well-developed rootstocks such as Cyperus papyrus, and thus a diet of 35–40 % sedges would have been sufficient to explain the australopith carbon isotope values. Yet, this too is unlikely, for although these highly edible sedges are common in extensive perennial wetlands like the Okavango Delta, they are rare in the woodland/ bushland habitats that were inhabited by australopiths (Reed 1997; Peters and Vogel 2005). All told, the available data suggest that even if sedges did constitute an important resource for early hominins, they were likely supplemented with other C4 foods. Alternatively, if other C4 foods were not consumed, australopiths would have had to have been true sedge specialists to account for the strong C4 signatures observed in most specimens. It is worth noting, however, that some early hominin habitats in East Africa such as the wetlands of the Eastern Lacustrine Plain at Olduvai Gorge (Hay 1976; Deocampo et al. 2002) might have been better sources of edible C4 sedges, and Puech et al. (1986) have also suggested that the dental microwear of early East African hominins is consistent with the consumption of such foods (see below for isotopic analysis of eastern African hominins). The Case for Animal Foods Animal foods can mean many different things including large and small vertebrates, invertebrates, and even bird’s eggs. These foods can also be acquired in a variety of ways including active hunting of large games, passive scavenging, and gathering of insects and eggs (see “▶ The Hunting Behavior and Carnivory of Wild Chimpanzees” and “▶ Cooperation, Coalition, and Alliances”). Although chimpanzees are known to hunt a variety of small vertebrates such as red colobus monkeys (Piliocolobus badius) and blue duiker (Cephalophus monticola), these are pure C3 consumers (Teleki 1981; Goodall 1986). Therefore, intake of these foods could not contribute to the C4 component of australopith diets. More likely sources of the reported C4 signal include small grass-eating taxa such as hyraxes (Procavia spp.) and cane rats (Thryonomys swinderianus). The young of larger species would also be tempting targets. For instance, the young of antelope like reedbuck (Redunca arundinum) lies hidden and largely helpless for the first several months of life, making them an easy prey for enterprising hominins. Arthropods are also potential C4 foods. Baboons are known to eat grass-eating grasshoppers (Acrididae) almost exclusively during temporary gluts (Hamilton 1987). Grass-eating termites represent another intriguing possibility, particularly given recent studies suggesting that bone Page 14 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013 −10 −12 −14 δ13C (‰)

−16

n = 777

−18 −20 −22

n = 550

−24

n = 40

−26 −28 −30

Grasses

Termites

Trees

Fig. 5 d13C for termites, trees, and grasses in Kruger National Park. The boxes represent the 25th–75th percentiles (with the medians as a horizontal line) and the whiskers show the 10th–90th percentiles. Note that while termites have highly variable carbon isotope compositions, the vast majority of specimens have mixed C3/C4 signatures

tools from Swartkrans were used to extract termites from mounds (Backwell and D’Errico 2001). Stable isotope studies of termites in African savannah environments have shown that they could have contributed to the australopiths’ 13C-enrichment (Boutton et al. 1983; Sponheimer et al. 2005a). While termites range from nearly pure C3 to pure C4 consumers, the vast majority of savannah termites, even in densely wooded riverine microhabitats, consume significant proportions of C4 foods. In fact, termites throughout Kruger National Park eat 35 % C4 vegetation on average (Sponheimer et al. 2005a; Fig. 5). Thus, termite consumption by australopiths in woodland savannah and even in riverine forest would be expected to impart some C4 carbon to consumers. On the other hand, the fact that so few termites have a pure C4 signal makes it unlikely that termite consumption alone was the source of the strong C4 signal of australopiths, because it would require a diet of nearly 100 % termites. Alternatively, if the hominins selectively preyed upon grass-specialist harvester termites (Trinervitermes, Hodotermes) with virtually pure C4 diets, a diet of about 35–40 % termites would be sufficient to produce the observed hominin carbon isotope ratios. This scenario, however, is highly unlikely because these C4 termites are much less common than those with mixed C3/C4 diets in woodlands today; and while harvester termites are more abundant in open grasslands and during acute droughts (Braack and Kryger 2003), there is no reason to believe that australopiths frequented such open environments or that drought conditions were so preponderant (see “▶ Role of Environmental Stimuli in Hominid Origins” and “▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments”). Moreover, while Trinervitermes builds highly visible aboveground nests (mounds), Hodotermes does not, making it much less conspicuous on the landscape (Carruthers 1997; Stuart and Stuart 2000). Thus, it is possible and even likely that termites contributed in some way to the unusual d13C values of australopiths, but other C4 resources were almost certainly consumed in considerable quantities. It has been suggested that hominid dental anatomy was not well suited for the processing of animal foods (Teaford et al. 2002), but this observation only pertains to a limited class of animal foods. A great many animal foods require little, if any, oral processing. Termites, grasshoppers, ants, grubs, eggs, and a variety of other insect delicacies may be consumed whole, and even small vertebrates can be swallowed whole or in a few pieces (Smithers 1983). Brains, marrow, and other soft tissues can also be consumed without oral processing. In addition, no experiments have been conducted to investigate the actual oral and/or preoral processing necessary to consume the muscle tissue of small vertebrates. Thus, it seems unwise to unduly limit the potential foods for australopiths until such studies have been undertaken. Furthermore, the consumption of animal foods is common

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among mammals without seemingly appropriate dentition. One obvious example is the aardwolf (Proteles cristatus) which consumes hundreds of thousands of termites per night with largely nonfunctional, obsolescent dentition (Smithers 1983). In some cases, this apparent disjunction between dental morphology and trophic behavior might result from the dentition being adapted for others, more mechanically challenging foods in an animal’s diet. For example, capuchin monkeys (Cebus apella) have large, bunodont dentition with thick enamel adapted for consuming fruits and hard nuts. Nonetheless, up to 50 % of capuchin diets can come from animal foods, although the average is closer to 25 % (Fleagle 1999; Rosenberger and Kinzey 1972; Rosenberger 1992). Similarly, Ungar (2004) has argued that among hominoids, differences in dental morphology primarily reflect their multifarious fallback foods, rather than their preferred foods during times of plenty.

What Does It Mean? All told, we still cannot be certain which C4 resources were utilized by South African australopiths. Grass roots, grasshoppers, bird’s eggs, lizards, rodents, and young antelopes might have been important C4 resources, particularly during the dry season when little other food was readily available. Succulent plants like euphorbias (Euphorbiaceae) and aloes (Aloaceae) (which are rare in most woodlands but have d13C values that are sometimes indistinguishable from those of C4 grasses) are also possibilities; for although they are often poisonous to humans (and presumably chimpanzees), they are occasionally utilized by baboons and humans (Codron 2003; Peters and Vogel 2005). Further work on dental microwear and morphology, elemental analysis, and the potential availability and nutritional properties of foods may make it possible to identify these C4 resources with greater confidence. At present, however, it seems likely that australopiths utilized a wide variety of these foods. Despite this uncertainty, we should not lose sight of the most significant aspect of these stable isotope data, namely, that australopiths increased their dietary breadth compared to extant apes by consuming novel C4 resources, regardless of what these resources were (see “▶ Role of Environmental Stimuli in Hominid Origins”). Similar evidence for increased dietary breadth is also evident in their thicker enamel, larger postcanine dentition, and greater mandibular corpus robusticity, all of which point to the consumption of hard objects beyond the capabilities of extant apes (Teaford et al. 2002). Thus, the fundamental trophic difference between australopiths and extant apes might be that when confronted with increasingly open areas, apes continue to exploit the foods that are most abundant in forest environments (McGrew et al. 1982), whereas australopiths utilized novel C4 resources in addition to forest foods. There would have been a number of advantages to such a dietary strategy. It would have allowed australopiths to survive and even thrive in a much greater variety of habitats than do modern great apes, potentially allowing expansion of their range. Similarly, the increased dietary breadth could have buffered australopiths against climatic change and habitat loss. Another implication of increased dietary flexibility might be decreased foraging time and mobility, allowing for increased social interaction and possibly greater social complexity. This flexibility could also have increased dietary quality over that of extant apes by adding low-fiber underground storage organs and protein- and lipid-rich animal foods to australopith menus. This might have been an important step leading to greater encephalization and development of the genus Homo (see “▶ Evolution of the Primate Brain”; Aiello and Wheeler 1995; Milton 1999; ConklinBrittain et al. 2002). If increased dietary breadth was a fundamental australopith adaptation, what are we to make of the later robust australopiths in which the dental adaptations reached their most specialized form? They are believed to have been specialist hard object feeders that were eventually replaced by our Homo Page 16 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013 2 0 −2

δ13C (‰)

−4 −6 −8 −10 −12 −14

Fig. 6 Early hominin taxa from southern Africa (open triangles), eastern Africa (open circles), and central Africa (closed circles) arranged from lowest to highest d13C values

forebears who, for the first time, had regular access to higher quality animal foods (Aiello and Wheeler 1995; Milton 1999). An alternative explanation, however, is that the robust australopithecines were the quintessence of the trend towards dietary diversity because they could access the foods of their progenitors as well as harder foods. One might then argue that they were supplanted by Homo not because they ate different kinds of foods, but because Homo was more efficient at procuring these resources due to increased use of extra-oral processing (e.g., stone tools) and greater planning depth. It is believed, for instance, that early Homo increased access to bone marrow from scavenged or hunted carcasses of medium to large mammals by using stone tools (e.g., Blumenschine 1987), whereas there is a debate as to whether or not robust australopiths utilized such technology (e.g., Leakey et al. 1964; Susman 1988; Semaw et al. 1995; de Heinzelin et al. 1999). Furthermore, where australopiths may have eaten antelope lambs only when they stumbled upon them, Homo may have had superior planning depth and followed female antelopes back to their young, capturing them only when the mother left once more.

New Data from Beyond South Africa For nearly 15 years, carbon isotope analysis had only been undertaken on South African early hominins, but now studies have been completed on both central and eastern African hominin specimens (van der Merwe et al. 2008; White et al. 2009; Cerling et al. 2011, 2013; Lee-Thorp et al. 2012; Wynn et al. 2013; Fig. 6). These new data have dramatically increased our understanding of the taxonomic, regional, and temporal dimensions of early hominin diet (data available at ▶ http:// dx.doi.org/10.6084/m9.figshare.710649; Sponheimer et al. 2013). For instance, it now appears that before 4 Ma, eastern African hominins had carbon isotope compositions indicating primarily C3 consumption (White et al. 2009; Cerling et al. 2013). It also appears that by about 3.5 Ma, C4 food consumption became significant, if highly varied, within eastern African taxa such as A. afarensis and Kenyanthropus platyops (Cerling et al. 2013; Wynn et al. 2013). There is also strong evidence for regional differences. Most notably, P. robustus in southern Africa and P. boisei in eastern Africa, despite their marked morphological similarities, have highly different d13C values (P < 0.001), suggesting that the latter had a diet dominated by C4 Page 17 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013 0 P. boisei

−2

δ13C (‰)

−4 P. aethiopicus

−6

A. africanus A. afarensis

−8

P. robustus

Ar. ramidus

−10

A. anamensis

−12 350 400 450 500 550 600 650 700 750 800 Postcanine Area (P4, M1, M2; mm2)

Fig. 7 Linear regression showing that australopith postcanine area predicts d13C values (r2 ¼ 0.86, t(5) ¼ 5.50, P < 0.01). The relationship between d13C values and mandibular cross-sectional area at M1 is not shown (see Sponheimer et al. 2013)

(or less likely CAM) vegetation (van der Merwe et al. 2008; Cerling et al. 2011). Concomitantly, there is now strong isotopic evidence of niche differentiation between Homo and Paranthropus in eastern Africa, which contrasts with the broadly similar d13C values of these genera in southern Africa (Lee-Thorp et al. 2000). Preliminary observations also suggest a relationship between masticatory morphology and australopith carbon isotope compositions, with postcanine tooth size and mandibular cross-sectional area at M1 both increasing as do d13C values (Sponheimer et al. 2013; Fig. 7). This could indicate that C4 food consumption was among the driving forces behind the trend toward masticatory robusticity within the australopiths. Given this, it is surprising that evidence for environmentally driven changes in australopiths d13C values remains equivocal. The transition to significant C4 consumption at about 3.5 Ma is not obviously related to increased availability of C4 grass (Sponheimer et al. 2013), and changes in the habitat of A. afarensis are not clearly reflected in its d13C values (Wynn et al. 2013). It remains possible that an environmental signal has become obscured by the poor temporal and environmental resolution of the existing hominin fossil record and that climatic/environmental change at precessional or shorter time scales did drive hominin d13C values (Hopley and Maslin 2010), but this cannot be tested at present. We note, however, that even if changes in the abundance of C4 grass did not influence hominin d13C values, it remains possible that other environmental parameters such as tree or mammalian diversity did (Sponheimer et al. 2013). As to what C4 resources hominins post 4 Ma ate, it should be remembered that “early hominin diet” or even “australopith diet” is chimerical given that the available carbon isotope data now span more than three million years, 11 species, and major differences in masticatory anatomy and associated archaeology (see “▶ Analyzing Hominin Phylogeny,” “▶ The Species and Diversity of Australopiths”; Sponheimer et al. 2013). Given this, and the likely corollary of marked diversity of early hominin diets, it is not only plausible but probable that C4 food acquisition and consumption differed among hominin species within a broad region like eastern Africa. For instance, given Paranthropus boisei’s high d13C values, thick, robust mandibles, low-cusped cheek teeth, and diminutive incisors and canines, it is improbable that its major C4 dietary input was meat. Even savannah carnivores may not attain such high d13C values (Codron et al. 2007). It is, therefore, most parsimonious to ascribe the preponderance of its C4 “signal” to the direct consumption of C4 plant foods like grasses or sedges. As to what parts of these plants were consumed, given the discussion

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earlier in this manuscript, we are a long way from knowing. The situation for contemporaneous Homo might be different, though. Its dental morphology (Ungar 2004), the general belief that it produced (rather than Paranthropus), the majority of its associated archaeological record (Leakey et al. 1964), and arguments derived from energetics (Aiello and Wheeler 1995) are consistent with Homo having consumed greater amounts of animal protein from which it might have derived its C4 carbon.

Conclusion Stable isotope studies have made an important contribution to our understanding of early hominin diets. In the case of Neanderthals, stable isotopes strongly support the contention that they were highly carnivorous, primary predators. As for the australopiths, stable isotopes suggest that they broadened the ancestral ape resource base to include C4 foods, which coupled with bipedalism, and allowed them to pioneer increasingly open and seasonal environments. Yet, as is the case with all paleodietary techniques, stable isotopes leave a great many important questions unresolved. Particularly important are the equifinality problems that are common in stable isotope studies. In other words, many different diets can lead to the same stable isotope signature. For instance, carbon isotopes often cannot distinguish between diets as different as folivory, frugivory, and carnivory. And although some progress has been made using oxygen isotopes to break such equifinalities (Sponheimer and Lee-Thorp 1999c; Carter 2001), there is little reason to believe that this problem can be circumvented entirely by relying on stable isotopes. In the end, stable isotopes are one tool among many, all of which provide a slightly different window into the diets of our ancestors. Thus, where stable isotopes cannot determine the favored prey of Neanderthals, faunal analysis has much to contribute (Speth and Tchernov 2001), and when carbon isotopes remain silent on the topic of australopith fallback foods, dental morphology may jump into the fray (Ungar 2004). Thus, stable isotopes will prove most informative when pursued as part of a larger, integrated paleodietary investigation. That being said, stable isotopes themselves still have a great deal to tell us about the diets of our ancestors. To date, only Pliocene and early Pleistocene African hominins, Neanderthals, and AMH have been analyzed for stable isotopes to any significant extent, leaving the entire continents and large periods of time virtually unexplored. Future stable isotope studies will surely bridge these gaps, and in so doing greatly increase our knowledge of early hominin diets. Yet, we should not be satisfied to merely work our way through previously neglected or unattainable material, but should seek to push the limits of the technique itself. Improving our knowledge of the stable isotope compositions of modern plants and mammals, investigating how physiology affects diet-tissue spacing, and refining organic extraction techniques so that nitrogen isotopes can be analyzed for a wider variety of taxa will not only improve our ability to reconstruct paleodiets but will also enable us to address questions in ways that were previously unimaginable. Hopefully, such actualistic and experimental work will serve to hone this already exciting paleodietary tool.

Cross-References ▶ Neanderthals and Their Contemporaries

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References Aiello LC, Wheeler P (1995) The expensive tissue hypothesis. Curr Anthropol 36:199–221 Altmann SA, Altman J (1970) Baboon ecology. University of Chicago Press, Chicago Ambrose SH (1990) Preparation and characterization of bone and tooth collagen for stable carbon and nitrogen isotope analysis. J Archaeol Sci 17:431–451 Ambrose SH (1998) Prospects for stable isotopic analysis of later Pleistocene hominid diets in West Asia and Europe. In: Akazawa T, Aoki K, Bar-Yosef O (eds) Origin of Neanderthals and humans in West Asia. Plenum, New York, pp 277–289 Ambrose SH, DeNiro MJ (1986) The isotopic ecology of East African mammals. Oecologia 69:395–406 Ambrose SH, Norr L (1993) Experimental evidence for the relationship of the carbon isotope ratios of whole diet and dietary protein to those of bone collagen and carbonate. In: Lambert JB, Grupe G (eds) Prehistoric human bone: archaeology at the molecular level. Springer, Berlin, pp 1–37 Ayliffe LK, Chivas AR (1990) Oxygen isotope composition of the bone phosphate of Australian kangaroos: potential as a paleoenvironmental recorder. Geochim Cosmochim Acta 54:2603–2609 Backwell LR, d’Errico F (2001) Evidence of termite foraging by Swartkrans early hominids. Proc Natl Acad Sci USA 98:1358–1363 Bocherens H, Billiou D, Mariotti A, Patou-Mathis M, Otte M, Bonjean D, Toussaint M (2001) New isotopic evidence for dietary habits of Neandertals from Belgium. J Hum Evol 40:497–505 Bocherens H, Billiou D, Mariotti A, Patou-Mathis M, Otte M, Bonjean D, Toussaint M (1999) Palaeoenvironmental and palaeodietary implications of isotopic biogeochemistry of last interglacial Neanderthal and mammal bones in Scladina cave (Belgium). J Archaeol Sci 26:599–607 Bocherens H, Billiou D, Patou-Mathis M, Bonjean D, Otte M, Mariotti A (1997) Isotopic biogeochemistry (13C, 15 N) of fossil mammal collagen from Scladina cave (Sclayn, Belgium). Quatern Res 48:370–380 Bocherens H, Drucker DG, Billiou D, Patou-Mathis M, Vandermeersch B (2005) Isotopic evidence for diet and subsistence pattern of the Saint-Césaire I Neanderthal: review and use of a multisource mixing model. J Hum Evol 49:71–87 Bocherens H, Fizet M, Mariotti A, Lange-Badre B, Vandermeersch B, Borel J-P, Bellon G (1991) Isotopic biochemistry (13C, 15 N) of fossil vertebrate collagen: implications for the study of fossil food web including Neandertal man. J Human Evol 20:481–492 Boutton TW, Arshad MA, Tieszen LL (1983) Stable isotope analysis of termite food habits in East African grasslands. Oecologia 59:1–6 Braack L, Kryger P (2003) Insects and Savannah heterogeneity. In: du Toit JT, Rogers KH, Biggs HC (eds) The Kruger experience: ecology and management of Savannah heterogeneity. Island Press, Washington, pp 263–275 Brain CK (1981) The hunters or the hunted? University of Chicago Press, Chicago Brunet M, Guy F, Pilbeam D, Mackaye HT, Likius A, Ahounta D, Beauvilain A, Blondel C, Bocherens H, Boisserie JR, De Bonis L, Coppens Y, Dejax J, Denys C, Duringer P, Eisenmann V, Fanone G, Fronty P, Geraads D, Lehmann T, Lihoreau F, Louchart A, Mahamat A, Merceron G, Mouchelin G, Otero O, Pelaez Campomanes P, Ponce De Leon M, Rage JC, Sapanet M, Schuster M, Sudre J, Tassy P, Valentin X, Vignaud P, Viriot L, Zazzo A, Zollikofer C (2002) A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418:145–151 Carruthers V (1997) The wildlife of Southern Africa. Southern Book Publishers, Halfway House Page 20 of 27

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Carter ML (2001) Sensitivity of stable isotopes (13C, 15N, and 18O) in bone to dietary specialization and niche separation among sympatric primates in Kibale National Park, Uganda. PhD dissertation, University of Chicago Cerling TE, Harris JM (1999) Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 120:347–363 Cerling TE, Mbua E, Kirera FM, Manthi FK, Grine FE, Leakey MG, Sponheimer M, Uno KT (2011) Diet of Paranthropus boisei in the early Pleistocene of East Africa. Proc Natl Acad Sci USA 108:9337–9341. doi:10.1073/pnas.1104627108 Cerling TE, Manthi FK, Mbua EN, Leakey LN, Leakey MG, Leakey RE, Brown FH, Grine FE, Hart JA, Kaleme P, Roche H, Uno KT, Wood BA (2013) Stable isotope-based diet reconstructions of Turkana Basin hominins. PNAS 110:10501–10506. doi:10.1073/pnas.1222568110 Clarke R (1994) Advances in understanding the craniofacial anatomy of South African early hominids. In: Corruccini R, Ciochon R (eds) Integrative paths to the past. Prentice Hall, Englewood Cliffs, pp 205–222 Codron DM (2003) Dietary ecology of Chacma baboons (Papio ursinus (Kerr, 1792)) and Pleistocene Cercopithecoidea in Savanna environments of South Africa. MSc thesis, University of Cape Town Codron D, Codron J, Lee-Thorp JA, Sponheimer M, de Ruiter D, Brink JS (2007) Stable isotope characterization of mammalian predator-prey relationships in a South African Savanna. Eur J Wildl Res 53:161–170 Conklin-Brittain NL, Wrangham RW, Smith CC (2002) A two-stage model of increased dietary quality in early hominid evolution: the role of fiber. In: Ungar PS, Teaford MF (eds) Human diet: its origin and evolution. Bergin & Garvey, Westport, pp 61–76 Daegling DJ, Grine FE (1999) Occlusal microwear in Papio ursinus: the effects of terrestrial foraging on dental enamel. Primates 40:559–572 Dart RA (1957) The osteodontokeratic culture of Australopithecus prometheus. Trans Mus Mem 10:1–105 Defelice MS (2002) Yellow nutsedge Cyperus esculentus L. – snack food of the gods. Weed Technol 16:901–907 de Heinzelin J, Clark JD, White TD, Hart W, Renne P, WoldeGabriel G, Beyene Y, Vrba E (1999) Environment and behavior of 2.5-Million-year-old Bouri hominids. Science 284:625–629 deMenocal PB (1995) Plio-Pleistocene African climate. Science 270:53–59 Deocampo DM, Blumenschine RJ, Ashley GM (2002) Wetland diagenesis and traces of early hominids, Olduvai Gorge, Tanzania. Quat Res 57:271–281 Doran DM, McNeilage A (1998) Gorilla ecology and behavior. Evol Anthropol 6:120–131 Dufour E, Bocherens H, Mariotti A (1999) Palaeodietary implications of isotopic variability in Eurasian lacustrine fish. J Archaeol Sci 26:627 Dunbar RIM (1983) Theropithecines and hominids: contrasting solutions to the same ecological problem. J Hum Evol 12:647–658 Eaton SB, Konner MJ (1985) Paleolithic nutrition. N Engl J Med 312:283–289 Feibel CS (1997) Debating the environmental factors in hominid evolution. GSA Today 7:1–7 Fizet M, Mariotti A, Bocherens H, Lange-Badré B, Vandermeersch B, Borel JP, Bellon G (1995) Effect of diet, physiology and climate on carbon and nitrogen isotopes of collagen in a late Pleistocene anthropic paleoecosystem (France, Charente, Marillac). J Archaeol Sci 22:67–79 Fleagle JG (1999) Primate adaptation and evolution, 2nd edn. Academic, New York Goodall J (1986) The Chimpanzees of Gombe. Cambridge University Press, Cambridge

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Grine FE, Kay RF (1988) Early hominid diets from quantitative image analysis of dental microwear. Nature 333:765–768 Grine FE (1981) Trophic differences between gracile and Robust australopithecines. S Afr J Sci 77:203–230 Grine FE (1986) Dental evidence for dietary differences in Australopithecus and Paranthropus: a quantitative analysis of permanent molar microwear. J Hum Evol 15:783–822 Haile-Selassie Y, Suwa G, White TD (2004) Late Miocene teeth from Middle Awash, Ethiopia, and early hominid dental evolution. Science 303:1503–1505 Hamilton WJ (1987) Omnivorous primate diets and human overconsumption of meat. In: Harris M, Ross EB (eds) Food and evolution: toward a theory of human food habits. Temple University Press, Philadelphia, pp 117–132 Harding RSO (1976) Ranging patterns of a troop of baboons (Papio anubis) in Kenya. Folia Primatologia 25:143 Hatley T, Kappelman J (1980) Bears, pigs, and Plio-Pleistocene hominids: case for exploitation of belowground food resources. Hum Ecol 8:371–387 Hay RL (1976) Geology of the Olduvai Gorge. University of California Press, Berkeley Hesla ABI, Tieszen LL, Imbaba SK (1982) A systematic survey of C3 and C4 photosynthesis in the Cyperaceae of Kenya, East Africa. Photosynthetica 16:196–205 Hopley PJ, Maslin MA (2010) Climate-averaging of terrestrial faunas: an example from the PlioPleistocene of South Africa. Paleobiology 36:32–50. doi:10.1666/0094-8373-36.1.32 Hoppe KA, Koch PL, Furutani TT (2003) Assessing the preservation of biogenic strontium in fossil bones and tooth enamel. Int J Osteoarchaeol 13:20–28 Hylander WL (1975) Incisor size and diet in anthropoids with special reference to Cercopithecoidea. Science 189:1095–1098 Jolly CJ (1970) The seed-eaters: a new model of hominid differentiation based on a baboon analogy. Man 5:5–26 Jones AM, O’Connell TC, Young ED, Scott K, Buckingham CM, Iacumin P, Brasier MD (2001) Biogeochemical data from well preserved 200 ka collagen and skeletal remains. Earth Planet Sci Lett 193:143–149 Katzenberg MA, Weber A (1999) Stable isotope ecology and palaeodiet in the Lake Baikal region of Siberia. J Archaeol Sci 26:651–660 Kay RF (1985) Dental evidence for the diet of Australopithecus. Annu Rev Anthropol 14:315–341 Kimbel WH, White TD (1988) Variation, sexual dimorphism, and taxonomy of Australopithecus. In: Grine FE (ed) Evolutionary history of the “robust” Australopithecines. Aldine de Gruyter, New York, pp 175–192 Kohn MJ, Schoeninger MJ, Valley JW (1996) Herbivore tooth oxygen isotope compositions: effects of diet and physiology. Geochim et Cosmochim Acta 60:3889–3896 Leakey LSB, Tobias PV, Napier JR (1964) A new species of genus homo from Olduvai Gorge. Nature 202:7–9 Lee R (1979) The !Kung san: men, women, and work in a foraging society. Cambridge University Press, Cambridge Lee-Thorp JA (2002) Preservation of biogenic carbon isotopic signals in Plio-Pleistocene bone and tooth mineral. Biogeochemical approaches to paleodietary analysis. Springer US, 89–115 Lee-Thorp JA, Manning L, Sponheimer M (1997) Exploring problems and opportunities offered by down-scaling sample sizes for carbon isotope analyses of fossils. Bull Soc Geol France 168:767–773

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Lee-Thorp JA, Sponheimer M (2003) Three case studies used to reassess the reliability of fossil bone and enamel isotope signals for paleodietary studies. J Anthropol Archaeol 22:208–216 Lee-Thorp JA, Thackeray JF, van der Merwe N (2000) The hunters and the hunted revisited. J Hum Evol 39:565–576 Lee-Thorp JA, van der Merwe NJ (1987) Carbon isotope analysis of fossil bone apatite. S Afr J Sci 83:712–715 Lee-Thorp JA, van der Merwe NJ, Brain CK (1989b) Isotopic evidence for dietary differences between two extinct baboon species from Swartkrans. J Hum Evol 18:183–190 Lee-Thorp JA, van der Merwe NJ, Brain CK (1994) Diet of Australopithecus robustus at Swartkrans from stable carbon isotopic analysis. J Hum Evol 27:361–372 Lee-Thorp J, Likius A, Mackaye HT, Vignaud P, Sponheimer M, Brunet M (2012) Isotopic evidence for an early shift to C4 resources by Pliocene hominins in Chad. PNAS. doi:10.1073/ pnas.1204209109 LeGeros RZ (1991) Calcium phosphates in oral biology and medicine. Karger, Paris Lockwood CA (1997) Variation in the face of Australopithecus africanus and other African hominoids. PhD dissertation, University of the Witwatersrand, Johannesburg Luyt J, Lee-Thorp JA (2003) Carbon isotope ratios of Sterkfontein fossils indicate a marked shift to open environments ca. 1.7 Ma. S Afr J Sci 99:271–273 Lyman RL (1994) Vertebrate taphonomy. Cambridge University Press, Cambridge McGrew WC, Sharman MJ, Baldwin PJ, Tutin CEG (1982) On early hominid plant-food niches. Curr Anthropol 23:213–214 Mellars P (1989) Major issues in the emergence of modern humans. Curr Anthropol 30:349–385 Milton K (1999) A hypothesis to explain the role of meat-eating in human evolution. Evol Anthropol 8:11–21 Milton K (2002) Hunter–gatherer diets: wild foods signal relief from diseases of affluence. In: Ungar PS, Teaford MF (eds) Human diet: its origin and evolution. Bergin & Garvey, Westport, pp 111–122 Minagawa M, Wada E (1984) Step-wise enrichment of 15 N along food chains: further evidence and the relationship between d15N and animal age. Geochim et Cosmochim Acta 48:1135–1140 Moggi-Cecchi J, Tobias PV, Beynon AD (1998) The mixed dentition and associated skull fragments of a juvenile fossil hominid from Sterkfontein, South Africa. Am J Phys Anthropol 106:425–466 Nystrom P, Phillips-Conroy JE, Jolly CJ (2004) The influence of age and sex on dental microwear patterns in baboons (Papio sp.) living in the Awash National Park, Ethiopia. Am J Phys Anthropol Passey B, Robinson T, Ayliffe L, Cerling T, Sponheimer M, Dearing MD, Roeder BL, Ehleringer JR (2005) Carbon isotope fractionation between diet, breath CO2, and bioapatite in different mammals. J Archaeol Sci 32:1459–1470 Peters CR, Vogel JC (2005) Africa’s wild C4 plant foods and possible early hominid diets. J Hum Evol 48:219–236 Pettitt PB, Richards MP, Maggi R, Formicola V (2003) The gravettian burial known as the Prince (‘Il Principe’): new evidence for his age and diet. Antiquity 95:15–19 Prentice ML, Denton GH (1988) The deep-sea oxygen isotope record, the global ice sheet system and hominid evolution. In: Grine FE (ed) Evolutionary history of the “robust” Australopithecines. Aldine de Gruyter, New York, pp 383–403 Puech PF, Cianfarani F, Albertini H (1986) Dental microwear features as an indicator for plant food in early hominids: a preliminary study of enamel. Hum Evol 1:507–515 Reed K (1997) Early hominid evolution and ecological change through the African Plio-Pleistocene. J Hum Evol 32:289–322 Page 23 of 27

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Richards MP, Pettett PB, Stiner MC, Trinkaus E (2001) Stable isotope evidence for increasing dietary breadth in the European mid-upper Paleolithic. Proc Natl Acad Sci 98:6528–6532 Richards MP, Pettitt PB, Trinkaus E, Smith FH, Paunovic M, Karavanic I (2000) Neanderthal diet at Vindija and Neanderthal predation: the evidence from stable isotopes. Proc Natl Acad Sci USA 97:7663–7666 Richards MP, Hedges REM (1999) Stable isotope evidence for similarities in the types of marine foods used by Late Mesolithic humans at sites along the Atlantic coast of Europe. J Archaeol Sci 26:717–722 Robbins CT, Felicetti LA, Sponheimer M (2005) Evaluating nitrogen isotope discrimination relative to dietary nitrogen in mammals and birds. Oecologia 144:534–540 Robinson JT (1954) Prehominid dentition and hominid evolution. Evolution 8:324–334 Rosenberger A (1992) Evolution of feeding niches in New world monkeys. Am J Phys Anthropol 88:525–562 Sage RF, Wedin DA, Li M (1999) The biogeography of C4 photosynthesis. In: Sage RF, Monson RK (eds) C4 plant biology. Academic, New York, pp 313–373 Schoeninger MJ, Moore J, Sept JM (1999) Subsistence strategies of two savannah chimpanzee populations: the stable isotope evidence. Am J Primatol 49:297–314 Schoeninger MJ, DeNiro MJ (1984) Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochimet Cosmochim Acta 48:625–639 Schulting RJ, Trinkaus E, Higham T, Hedges R, Richards M, Cardy B (2005) A mid-upper palaeolithic human humerus from Eel Point, SouthWales, UK. J Hum Evol 48:493–505 Sealy JC, van der Merwe NJ, Lee-Thorp JA, Lanham JL (1987) Nitrogen isotopic ecology in Southern Africa: implications for environmental and dietary tracing. Geochim et Cosmochim Acta 51:2707–2717 Semaw S, Renne P, Harris JWK, Feibel CS, Bernor RL, Fesseha N, Mowbray K (1997) 2.5-Millionyear-old stone tools from Gona, Ethiopia. Nature 385:333–336 Senut B, Pickford M, Gommery D, Mein P, Cheboi C, Coppens Y (2001) First hominid from the Miocene (lukeino formation, Kenya. C R Seances Acad Sci 332:137–144 Sillen A, Hall G, Armstrong R (1995) Strontium calcium ratios (Sr/Ca) and strontium isotopic ratios (87Sr/86Sr) of Australopithecus robustus and Homo sp. from Swartkrans. J Hum Evol 28:277–285 Smith BN, Epstein S (1971) Two categories of 13C/12C ratios for higher plants. Plant Physiol 47:380–384 Smithers RHN (1983) The mammals of the Southern African subregion. University of Pretoria Press, Pretoria Speth JD, Tchernov E (2001) Neanderthal hunting and meat-processing in the near East: evidence from Kebara cave (Israel). In: Stanford CB, Bunn HT (eds) Meat-eating and human evolution. Oxford University Press, Oxford, pp 52–72 Sponheimer M (1999) Isotopic ecology of the Makapansgat Limeworks Fauna. PhD dissertation, Rutgers University Sponheimer M, Lee-Thorp JA (1999a) Isotopic evidence for the diet of an early hominid, Australopithecus africanus. Science 283:368–370 Sponheimer M, Lee-Thorp JA (1999b) The alteration of enamel carbonate environments during fossilisation. J Archaeol Sci 26:143–150 Sponheimer M, Lee-Thorp JA (1999c) The ecological significance of oxygen isotopes in enamel carbonate. J Archaeol Sci 26:723–728

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Sponheimer M, Lee-Thorp JA (2001) The oxygen isotope composition of mammalian enamel carbonate: a case study from Morea Estate, Mpumalanga Province, South Africa. Oecologia 126:153–157 Sponheimer M, Lee-Thorp J, DeRuiter D, Smith J, van der Merwe N, Reed K, Ayliffe L, Heidelberger C, Marcus W (2003a) Diets of Southern African Bovidae: stable isotope evidence. J Mammal 84:471–479 Sponheimer M, Lee-Thorp J, de Ruiter D, Codron D, Codron J, Baugh A, Thackeray F (2005a) Hominins, sedges, and termites: new carbon isotope data from the Sterkfontein Valley and Kruger National Park. J Hum Evol 48:301–312 Sponheimer M, de Ruiter D, Lee-Thorp J, Spath A (2005b) Sr/Ca and early hominin diets revisited: new data from modern and fossil tooth enamel. J Hum Evol 48:147–156 Sponheimer M, Lee-Thorp JA, Reed K (2001) Isotopic ecology of the Makapansgat limeworks Perissodactyla. S Afr J Sci 97:327–329 Sponheimer M, Reed K, Lee-Thorp JA (1999) Combining isotopic and ecomorphological data to refine bovid paleodietary reconstruction: a case study from the Makapansgat limeworks hominin locality. J Hum Evol 34:277–285 Sponheimer M, Robinson T, Ayliffe L, Roeder B, Hammer J, West A, Passey B, Cerling T, Dearing D, Ehleringer J (2003b) Nitrogen isotopes mammalian herbivores: hair 15N values from a controlled-feeding study. Int J Osteoarchaeol 13:80–87 Sponheimer M, Alemseged Z, Cerling TE, Grine FE, Kimbel WH, Leakey MG, Lee-Thorp JA, Manthi FK, Reed KE, Wood BA, Wynn JG (2013) Isotopic evidence of early hominin diets. Proc Natl Acad Sci USA 110:10513–10518. doi:10.1073/pnas.1222579110 Stevens RE, Hedges REM (2004) Carbon and nitrogen stable isotope analysis of northwest European horse bone and tooth collagen, 40,000 BP-present: palaeoclimatic interpretations. Quaternary Sci Rev 23:977–991 Stiner M (1994) Honor among thieves. Princeton University Press, Princeton Stock WD, Chuba DK, Verboom GA (2004) Distribution of South African C-3 and C-4 species of Cyperaceae in relation to climate and phylogeny. Austral Ecol 29:313–319 Strum SC (1987) Almost human: a journey into the world of baboons. Random House, New York Stuart C, Stuart T (2000) A field guide to the tracks and signs of Southern and East African wildlife. Stuik Publishers, Cape Town Sullivan CH, Krueger HW (1981) Carbon isotope analysis of separate chemical phases in modern and fossil bone. Nature 292:333–335 Sullivan CH, Krueger HW (1983) Carbon isotope ratios of bone apatite and animal diet reconstruction. Nature 301:177–178 Susman RL (1988) Hand of Paranthropus robustus from member I, Swartkrans: fossil evidence for tool behavior. Science 239:781–784 Tackholm V, Drar M (1973) Flora of Egypt, vol II. Otto Koeltz Antiquariat, Koenigstein Teaford MF (1992) Dental microwear and diet in extant and extinct Theropithecus: preliminary analyses. In: Jablonski N (ed) Theropithecus: the rise and fall of a primate genus. Cambridge University Press, Cambridge, pp 331–349 Teaford MF, Ungar PS, Grine FE (2002) Paleontological evidence for the diets of African PlioPleistocene hominins with special reference to early Homo. In: Ungar PS, Teaford MF (eds) Human diet: its origin and evolution. Bergin & Garvey, Westport, pp 143–166 Teleki G (1981) The omnivorous diet and eclectic feeding habits of chimpanzees in Gombe National Park, Tanzania. In: Harding RSO, Teleki G (eds) Omnivorous primates. Columbia University Press, New York, pp 303–343 Page 25 of 27

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Tieszen LL, Fagre T (1993) Effect of diet quality and composition on the isotopic composition of respiratory CO2, bone collagen, bioapatite, and soft tissues. In: Lambert JB, Grupe G (eds) Prehistoric human bone: archaeology at the molecular level. Springer, Berlin, pp 121–155 Trickett MA, Budd P, Montgomery J, Evans J (2003) An assessment of solubility profiling as a decontamination procedure for the 87Sr/86Sr analysis of archaeological human skeletal tissue. Appl Geochem 18:653–658 Ungar P (2004) Dental topography and diets of Australopithecus afarensis and early Homo. J Hum Evol 46:605–622 Ungar P (1998) Dental allometry, morphology, and wear as evidence for diet in fossil primates. Evol Anthropol 6:205–217 Ungar P, Grine FE (1991) Incisor size and wear in Australopithecus africanus and Paranthropus robustus. J Hum Evol 20:313–340 van der Merwe NJ (1989) Natural variation in the 13C concentration and its effect on environmental reconstruction using 13C/12C ratios in animal bones. In: Price TD (ed) The chemistry of prehistoric human bone. Cambridge University Press, Cambridge, pp 105–125 van der Merwe NJ, Thackeray JF, Lee-Thorp JA, Luyt J (2003) The carbon isotope ecology and diet of Australopithecus africanus at Sterkfontein, South Africa. J Hum Evol 44:581–597 van der Merwe NJ, Masao FT, Bamford MK (2008) Isotopic evidence for contrasting diets of early hominins Homo habilis and Australopithecus boisei of Tanzania. S Afr J Sci 104:153–155 Vogel JC, van der Merwe NJ (1977) Isotopic evidence for early maize cultivation in New York State. Am Antiq 42:238–242 Vogel JC (1978) Recycling of carbon in a forest environment. Oecol Plantar 13:89–94 Vrba ES (1980) The significance of bovid remains as indicators of environment and predation patterns. In: Behrensmeyer AK, Hill AP (eds) Fossils in the making. University of Chicago Press, Chicago, pp 247–272 Vrba ES (1985) Ecological and adaptive changes associated with early hominid evolution. In: Delson E (ed) Ancestors: the hard evidence. Alan R. Liss, New York, pp 63–71 Wang Y, Cerling T (1994) A model of fossil tooth and bone diagenesis: implications for paleodiet reconstruction from stable isotopes. Palaeogeog Palaeoclimatol Palaeoecol 107:281–289 White TD, Ambrose SH, Suwa G, Su DF, DeGusta D, Bernor RL, Boisserie J-R, Brunet M, Delson E, Frost S, Garcia N, Giaourtsakis IX, Haile-Selassie Y, Howell FC, Lehmann T, Likius A, Pehlevan C, Saegusa H, Semprebon G, Teaford M, Vrba E (2009) Macrovertebrate Paleontology and the Pliocene habitat of Ardipithecus ramidus. Science 326:67–93. doi:10.1126/ science.1175822 Wolpoff MH (1973) Posterior tooth size, body size, and diet in South African Gracile Australopithecines. Am J Phys Anthropol 39:375–394 Wood B, Strait D (2004) Patterns of resource use in early Homo and Paranthropus. J Hum Evol 46:119–162 Wynn JG, Sponheimer M, Kimbel WH, Alemseged Z, Reed K, Bedaso ZK, Wilson JN (2013) Diet of Australopithecus afarensis from the Pliocene hadar formation, Ethiopia. Proc Natl Acad Sci USA 110:10495–10500. doi:10.1073/pnas.1222559110

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_18-3 # Springer-Verlag Berlin Heidelberg 2013

Index Terms: Australopithecus 10–12 Carbon isotopes 9 Collagen 3 C4 foods 12–14 animal foods 14 grasses 13 sedges 13 Enamel apatite 9 Enamel bioapatite 9 Neanderthals 6 Nitrogen isotopes 6 Palaeodiets 1, 9 Paranthropus 10–12 Stable isotope analysis 3, 6

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Estimation of Basic Life History Data of Fossil Hominoids Helmut Hemmer* Institut f€ ur Zoologie, Johannes Gutenberg-Universita¨t Mainz, Mainz, Germany

Abstract Relationships between the life cycle and body mass, brain mass, and relative brain size of extant primates can be used to estimate life history parameters of extinct species. Methods to predict these key variables from available cranial and postcranial materials of fossil hominoids, especially hominids, are compiled and evaluated. The use of different concepts of scaling relative brain size is discussed. Brain mass and constant of cephalization data were used as the source material for the estimation of the age at eruption of the first lower molar, the age at female sexual maturity, the age at first breeding, and the maximum life span. Such data support the interpretation of the Late Miocene Sahelanthropus tchadensis as a taxon possibly related to the hominid stem species near the splitting of chimpanzee and hominid lines; confirm the fundamental nature of the australopithecines as progressive apes, not as humans; and support the view of a close relationship of the Early Pleistocene Homo paleopopulation of Dmanisi (Georgia) to the earliest Pleistocene African Homo populations.

Introduction Fossil bones are the material of classic osteological studies as a base of systematic and phylogenetic conclusions as well as the understanding of functional correlations of morphological structures. They also bear information that may be used for a two-step computing procedure to estimate fundamental life history and ecological and behavioral data that open a progressive level of insight into ecological relations. Life history study is understood as an approach in evolutionary biology, identifying ontogenetic variables and then asking what impact those variables have on population size and composition. Relationships between the life cycle and anatomical variables, such as body size and brain size, are of particular interest because they can be used to estimate life history parameters of extinct species (Hemmer 1974, 2003; Gingerich et al. 1982; De Rousseau 1990; Harvey 1990; Smith and Tompkins 1995), even if there are also life history components independent of brain and body size (Harvey and Read 1988). The first step of such life history data calculation is the estimation of body mass as a key variable, supported by the estimation of brain mass, from available fossil remains. The second step then takes advantage of the first-level results to look for estimates of parameters of the individual’s life cycle, such as the age at first reproduction or the maximum life span. How this subsequently affects

*Email: [email protected] Page 1 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Table 1 Relationships between life history variables (days) and adult female body mass (FBM, g) in primates r 0.74 0.91 0.89 0.89 0.92 0.86 0.78

Life history variable Gestation length (GL) Weaning age (WA) Age at maturity, female (AMF) Age at maturity, male (AMM) Age at first breeding, female (AFB) Interbirth interval (IBI) Life span (LS)

Equation log GL ¼ 0.13 log FBM + 1.775 log WA ¼ 0.56 log FBM + 0.433 log AMF ¼ 0.51 log FBM + 1.253 log AMM ¼ 0.47 log FBM + 1.471 log AFB ¼ 0.44 log FBM + 1.638 log IBI ¼ 0.37 log FBM + 1.464 log LS ¼ 0.29 log FBM + 2.893 l

Harvey and Clutton-Brock (1985, Tables 4 and 5) or Harvey et al. (1987, Tables 16.3 and 16.4); correlation coefficients based not on the species but on the subfamily level

higher levels of organization as, e.g., ecological aspects or population growth and evolution, is an additional step of life history consideration (De Rousseau 1990; Hemmer 2003; Kappeler et al. 2003). This chapter focuses on the way to evaluate such basic information concealed in fossil bones, to look for hominoid, especially hominid, life history aspects. It does not deal with life history correlates as left by the processes of growth, with “osteobiographic” techniques (Boyde 1990; Bromage 1990).

Life History Correlations Basic primate life history dimensions were found to correlate with body mass (Harvey and CluttonBrock 1985; Harvey et al. 1987; Lee and Kappeler 2003; Table 1), with absolute brain size (Sacher 1975; Harvey et al. 1987; Smith 1989; Smith et al. 1995; Deaner et al. 2003), and with relative brain size (Hemmer 1974). Brain size is more closely correlated with several life history variables, such as the age at sexual maturity or at first breeding, than is body size (Harvey et al. 1987). Unfortunately, data compilation in landmark publications (Harvey and Clutton-Brock 1985; Harvey et al. 1987) was confounded by conversion of cranial capacity with brain mass using a relationship 1 cm3 ¼ 1 g (Smith et al. 1995). Other studies were based on either cranial capacity or brain mass (Sacher 1975; Smith et al. 1995; Table 2). The factor related to brain size was considered to be maturation rate as a whole rather than any one of its aspects (Smith 1989). There is an extremely high correlation of the age at eruption of the first lower molar, as a rather stable marker of growth with relatively low variance, and brain size (r ¼ 0.98). When the effect of body mass is held constant in multiple regression, the partial correlation of M1 eruption and adult brain size remains r ¼ 0.90 (Smith 1989). The use of relative brain size (constant of cephalization; see later) instead of absolute brain mass or cranial capacity in life history correlations (Hemmer 1974) eliminates the influence of body size and allows for some further improvement of the correlation coefficient with most variables. Table 2 Relationships between life history variables and brain size in anthropoid primates Life history variable r M1 eruption age (years) 0.98 (M1EA) Life span (years) (LS) 0.835

Equation ln M1EA ¼ 0.582 ln CrC  2.405 log LS ¼ 0.379 log BrM + 0.640

Source and sample Smith et al. (1995): 14 anthropoid species Sacher (1975): 43 anthropoid species

3

CC cranial capacity (cm ), BrM brain mass (g)

Page 2 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Table 3 New life history variable allometries in anthropoid primates Life history variable Age at sexual maturity, female (months) (ASMF)

Age at sexual maturity, male (months) (ASMM)

Age at first breeding, female (months) (AFB)

Life span (years) (LS)

Age at eruption of first lower molar (AME)

Age at complete dentition (ACD)

r 0.815

n 23

0.878

23

0.889

23

0.797

13

0.857

13

0.878

13

0.856

27

0.898

27

0.902

27

0.797

30

0.843

30

0.851

30

0.971

11

0.985

11

0.981

11

0.966

10

0.974

10

0.964

10

Equation log ASMF ¼ 0.341 log BM + 0.349 (LSR) log ASMF ¼ 0.418 log BM + 0.059 (RMA) log ASMF ¼ 0.482 log BrM + 0.697 (LSR) log ASMF ¼ 0.549 log BrM + 0.568 (RMA) log ASMF ¼ 0.693 log CC + 0.889 (LSR) log ASMF ¼ 0.776 log CC + 0.801 (RMA) log ASMM ¼ 0.287 log BM + 0.686 (LSR) log ASMM ¼ 0.360 log BM + 0.411 (RMA) log ASMM ¼ 0.440 log BrM + 0.919 (LSR) log ASMM ¼ 0.514 log BrM + 0.777 (RMA) log ASMM ¼ 0.664 log CC + 1.062 (LSR) log ASMM ¼ 0.756 log CC + 0.965 (RMA) log AFB ¼ 0.315 log BM + 0.584 (LSR) log AFB ¼ 0.368 log BM + 0.385 (RMA) log AFB ¼ 0.445 log BrM + 0.913 (LSR) log AFB ¼ 0.495 log BrM + 0.816 (RMA) log AFB ¼ 0.636 log CC + 1.096 (LSR) log AFB ¼ 0.704 log CC + 1.023 (RMA) log LS ¼ 0.227 log BM + 0.511 (LSR) log LS ¼ 0.285 log BM + 0.297 (RMA) log LS ¼ 0.322 log BrM + 0.747 (LSR) log LS ¼ 0.382 log BrM + 0.634 (RMA) log LS ¼ 0.461 log CC + 0.877 (LSR) log LS ¼ 0.541 log CC + 0.794 (RMA) log AME ¼ 0.492 log BM  1.773 (LSR) log AME ¼ 0.507 log BM  1.826 (RMA) log AME ¼ 0.589 log BrM  1.091 (LSR) log AME ¼ 0.598 log BrM  1.108 (RMA) log AME ¼ 0.796 log CC  0.814 (LSR) log AME ¼ 0.812 log CC  0.831 (RMA) log ACD ¼ 0.533 log BM  1.347 (LSR) log ACD ¼ 0.551 log BM  1.416 (RMA) log ACD ¼ 0.629 log BrM  0.588 (LSR) log ACD ¼ 0.648 log BrM  0.624 (RMA) log ACD ¼ 0.848 log CC  0.286 (LSR) log ACD ¼ 0.880 log CC  0.321 (RMA)

Reliability for prediction in hominid evolution 103 %, useless 68 %, useless 24 %, useless 3 %, useful 2 %, useful 15 %, less useful No observed value for Homo sapiens

84 %, useless 62 %, useless 15 %, less useful 1  5 %, useful; PE > 5  10 %, still useful; PE > 10  20 %, less useful; PE > 20 %, useless. Data for BM and BrM based on Bauchot and Stephan (1969); for CC, Hemmer (1971); for ASMF, ASMM, AFB, and LS, Harvey and Clutton-Brock (1985); and for AME and ACD, Smith (1989), with modifications by Smith et al. (1995) BM body mass, BrM brain mass, CC constant of cephalization, LSR least-squares regression, RMA reduced major axis

Page 3 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Allometric formulas that may be used as predictor equations for the estimation of life history data in fossil hominoid primates were calculated for the present contribution based on brain mass (brain and body mass data, Bauchot and Stephan (1969); life history data, Harvey and Clutton-Brock (1985)) to avoid the former 1:1 confusion with cranial capacity data. The results for the relationship of body size, brain size, and coefficient of cephalization with the life history corner-stages age at sexual maturity, age at first reproduction, and maximum life span (data taken from the compilation of Harvey and Clutton-Brock (1985): Table 1), as well as age at first lower molar eruption and at completion of the dentition [data taken from Smith (1989), with modifications by Smith et al. (1995)], are listed in Tables 3 and 4 and illustrated in Figs. 1 and 2

Estimating Body Mass Body size cannot be measured directly being an abstract concept not a concrete parameter. Size may variously be recorded, e.g., as head-body length or height at the withers in quadruped mammals or as stature in hominids, but for general use body mass undoubtedly is the most reliable measure and the size variable of choice (Gingerich et al. 1982; Jungers 1988; Ruff and Walker 1993; Aiello and Wood 1994; Hemmer 2004). Skeletal predictors may allow to estimate body mass on principle on the base of dentition (Table 5), skull (Table 6), and postcranial elements (Tables 7 and 8). There exists no direct biomechanical relationship between tooth and cranial variables and body mass (Jungers 1988), but such dimensions nevertheless depend on a general factor of size. Dentition measurements may allow us to predict a genetically programmed frame of body size than the real size an individual reached during its ontogeny. Allometric relationships between tooth size and body mass have been used to reach the goal of body mass estimation in extinct nongeneralized primates (Gingerich et al. 1982; Martin 1990; see discussion in Jungers 1990). This approach depends on what evolutionary grade of primate species is used to predict body mass (Conroy 1987), and would be a hazardous venture insofar as hominid evolution is concerned, in view of considerable changes of the relative size of the masticatory apparatus (Wolpoff 1973; Jungers 1988). The introduction of taxon-specific conversion factors (prediction by tooth size related to prediction by cranial or postcranial dimensions) may help to overcome that problem (as used in felid body mass prediction by Hemmer (2001, 2004)). It must also always be taken in mind that dentition-based body mass estimates cannot present real individual life weights but merely provide some idea about a statistic mean to be awaited at a given linear predictor measure within a population in question. Cranial dimensions should depend more closely than tooth dimensions on individual ontogenetic body size modeling. They allow us to predict some “normal mass” of an individual. Cranial dimensions prove in that generalized function in some cases to be nearly as good or even better mass predictors as are some of the best postcranial ones (Aiello and Wood 1994; Kappelman 1996). Nevertheless, cranial dimensions may also considerably mislead on the other hand. Comparing the average body mass estimated at the base of seven cranial predictors to the actual body mass of the respective species, the average prediction error (PE) was found to be 32.3 %, ranging from 0.5 % to 79.3 % (Martin 1990). In limb bones, the genetic influences are supplemented by loading-related stimuli to a higher extant. They give evidence of an individual’s muscular strength and development (Lanyon 1990). Just here is a crucial point in hominoid evolution, where quadrupedal gait changed to bipedal gait, or vice versa. Just skeletal structures that bear a direct functional relationship to body mass are to Page 4 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Table 4 New life history variable allometries in hominoid primates

Life history variable Age at first breeding, female (months) (AFB)

Life span (years) (LS)

r 0.837

n 5

Equation log AFB ¼ 0.268 log BrM + 1.450 (LSR) log AFB ¼ 0.320 log BrM + 1.314 (RMA)

0.938

5

0.913

5

0.950

5

log AFB ¼ 0.380 log CC + 1.563 (LSR) log AFB ¼ 0.405 log CC + 1.524 (RMA) log LS ¼ 0.296 log BrM + 0.888 (LSR) log LS ¼ 0.324 log BrM + 0.814 (RMA) log LS ¼ 0.389 log CC + 1.059 (LSR) log LS ¼ 0.410 log CC + 1.027 (RMA)

Reliability for prediction in hominid evolution Useless, no significant correlation Useless, no significant correlation 9 %, still useful 6 %, still useful 8 %, still useful 4 %, useful brain mass > brain volume (Smith et al. 1995). Unfortunately, this is not always done in comparative publications [e.g., cranial capacities labeled brain mass in Table 1 of Harvey and Clutton-Brock (1985), identical with Table 15.1 of Harvey et al. (1987); see Smith et al. 1995]. There is also no stable relationship between brain mass and cranial capacity [e.g., 1/1.05 as used for humans by different authors (Smith et al. 1995) or 1/1.14 as used by Hartwig-Scherer (1993), following Count (1947)] over the whole range of brain size variability. The repeatedly found allometric exponent of 1.02 (Martin (1990), for primates; Ro¨hrs and Ebinger (2001), for mammals other than primates) does not mean an isometric relationship

Page 8 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Table 6 Cranial predictors of body mass (g) in primates, selected for r  0.95 Dimension (mm) Skull length (SL)

r 0.98

Equation log BM ¼ 3.89 log SL  4.09

Bizygomatic width (BZ)

0.98

log BM ¼ 3.77 log BZ  3.19

Internal zygomatic length (IZ) 0.96

log BM ¼ 3.26 log IZ  0.96

Palate length (PAL)

0.96

log BM ¼ 3.68 log PAL  2.08

Occipital condyle area (OCCA) (LOCC  BOCC)

0.98

log BM ¼ 2.16 log OCCA

0.96

log BM ¼ 1.61 log OCCA  1.00 log BM ¼ 1.68 log OCCA  0.87

Occipital condyle length (LOCC)

0.96

log BM ¼ 3.75 log LOCC  0.10 log BM ¼ 3.91 log LOCC  0.27

Foramen magnum area (FMA) 0.98

log BM ¼ 2.15 log FMA  1.20

0.97

log BM ¼ 1.76 log FMA  0.28 log BM ¼ 1.81 log FMA  0.41

Foramen magnum length (LFM)

0.96

log BM ¼ 3.22 log LFM log BM ¼ 3.34 log LFM  0.15

Foramen magnum breadth (BFM)

0.97

log BM ¼ 3.83 log BFM  0.57 log BM ¼ 3.95 log BFM  0.70

Orbital breadth (BORB)

0.96

log BM ¼ 4.20 log BORB  1.89

0.96

log BM ¼ 4.38 log BORB  2.14 log BM ¼ 5.22 log BORB  3.35 log BM ¼ 5.46 log BORB  3.70

Source and sample Martin (1990): 36 nonhuman species, MA Martin (1990): 36 nonhuman species, MA Martin (1990): 36 nonhuman species, MA Martin (1990): 36 nonhuman species, MA Martin (1990): 36 nonhuman species, MA Aiello and Wood (1994): 23 simian species, both sexes, LSR Aiello and Wood (1994): 23 simian species, both sexes, RMA Aiello and Wood (1994): 23 simian species, both sexes, LSR Aiello and Wood (1994): 23 simian species, both sexes, RMA Martin (1990): 36 nonhuman species, MA Aiello and Wood (1994): 23 simian species, both sexes, LSR Aiello and Wood (1994): 23 simian species, both sexes, RMA Aiello and Wood (1994): 23 simian species, both sexes, LSR Aiello and Wood (1994): 23 simian species, both sexes, RMA Aiello and Wood (1994): 23 simian species, both sexes, LSR Aiello and Wood (1994): 23 simian species, both sexes, RMA Aiello and Wood (1994): 23 simian species, both sexes, LSR Aiello and Wood (1994): 23 simian species, both sexes, RMA Aiello and Wood (1994): 6 hominoid species, both sexes, LSR Aiello and Wood (1994): 6 hominoid species, both sexes, RMA (continued)

Page 9 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Estimation of Basic Life History Data of Fossil Hominoids, Table 6 (continued) Dimension (mm) Orbital height (HORB)

r 0.95

Equation log BM ¼ 4.19 log HORB  1.78

0.98

log BM ¼ 4.40 log HORB  2.14

0.961 log BM ¼ 4.42 log HORB  2.12 0.957 log BM ¼ 4.53 log HORB  2.29 log BM ¼ 4.718 log HORB  2.560 log BM ¼ 4.915 log HORB  2.841 log BM ¼ 4.445 log HORB  2.155 log BM ¼ 4.657 log HORB  2.472 Orbital area (ORBA)

0.96

log BM ¼ 2.14 log ORBA  1.94

0.98

log BM ¼ 2.22 log ORBA  2.16 log BM ¼ 2.47 log ORBA  2.92 log BM ¼ 2.52 log ORBA  3.05

Orbital area, measured by computer digitizing (OA)

0.987 log BM ¼ 2.284 log OA  2.239 0.987 log BM ¼ 2.313 log OA  2.321 log BM ¼ 2.258 log OA  2.176 log BM ¼ 2.287 log OA  2.261

Biorbital breadth (BIOR)

0.98

log BM ¼ 3.85 log BIOR  2.81

0.95

log BM ¼ 3.95 log BIOR  2.98 log BM ¼ 4.82 log BIOR  4.67 log BM ¼ 5.10 log BIOR  5.20

Biporionic breadth (BPOR)

0.97

log BM ¼ 3.32 log BPOR  2.07

0.98

log BM ¼ 3.42 log BPOR  2.25 log BM ¼ 3.77 log BPOR  2.95 log BM ¼ 3.84 log BPOR  3.10

Source and sample Aiello and Wood (1994): 23 simian species, both sexes, LSR Aiello and Wood (1994): 23 simian species, both sexes, RMA Aiello and Wood (1994): 6 hominoid species, both sexes, LSR Aiello and Wood (1994): 6 hominoid species, both sexes, RMA Kappelman (1996): 18 catarrhine sp. + ssp., both sexes, LSR Kappelman (1996): 18 catarrhine sp. + ssp., both sexes, RMA Kappelman (1996): 10 hominoid sp. + ssp., both sexes, LSR Kappelman (1996): 10 hominoid sp. +ssp., both sexes, RMA Aiello and Wood (1994): 23 simian species, both sexes, LSR Aiello and Wood (1994): 23 simian species, both sexes, RMA Aiello and Wood (1994): 6 hominoid species, both sexes, LSR Aiello and Wood (1994): 6 hominoid species, both sexes, RMA Kappelman (1996): 18 catarrhine sp. + ssp., both sexes, LSR Kappelman (1996): 18 catarrhine sp. + ssp., both sexes, RMA Kappelman (1996): 10 hominoid sp. + ssp., both sexes, LSR Kappelman (1996): 10 hominoid sp. + ssp., both sexes, RMA Aiello and Wood (1994): 23 simian species, both sexes, LSR Aiello and Wood (1994): 23 simian species, both sexes, RMA Aiello and Wood (1994): 6 hominoid species, both sexes, LSR Aiello and Wood (1994): 6 hominoid species, both sexes, RMA Aiello and Wood (1994): 23 simian species, both sexes, LSR Aiello and Wood (1994): 23 simian species, both sexes, RMA Aiello and Wood (1994): 6 hominoid species, both sexes, LSR Aiello and Wood (1994): 6 hominoid species, both sexes, RMA

LSR least-squares regression, RMA reduced major axis, MA major axis Page 10 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Table 7 Selection of postcranial predictors of body mass in hominoid primates, correlation coefficient  0.95 Dimension (mm) r Equation 12th thoracic vertebral body: 0.968 log BM ¼ 1.3782 log THV  2.3132 AP  transverse diameter of the superior surface (THV) log BM ¼ 1.4244 log THV  2.4440 0.999

5th lumbar vertebral body: 0.951 AP  transverse diameter of the superior surface (LUV) 0.983

Sacral body: AP  transverse 0.968 diameter of the superior aspect (SAC) Humerus length [M1] (HLEN)

0.98 0.99

0.95

Humerus head AP diameter (HHAP)

0.985

Humerus midshaft 0.98 circumference [M8] (HMSC) 0.96 0.98

Humerus minimum 0.98 circumference [M7] (HMIN)

Source and sample McHenry (1992): 7 hominoid species, both sexes, LSR McHenry (1992): 7 hominoid species, both sexes, RMA log BM ¼ 0.6552 log THV  0.2443 McHenry (1992): Homo sapiens, both sexes, 3 populations, LSR log BM ¼ 0.6556 log THV  0.2456 McHenry (1992): Homo sapiens, both sexes, 3 populations, RMA log BM ¼ 1.3574 log LUV  2.4210 McHenry (1992): 7 hominoid species, both sexes, LSR log BM ¼ 1.4277 log LUV  2.6288 McHenry (1992): 7 hominoid species, both sexes, RMA log BM ¼ 1.1593 log LUV  1.9630 McHenry (1992): Homo sapiens, both sexes, 3 populations, LSR log BM ¼ 1.1797 log LUV  2.0281 McHenry (1992): Homo sapiens, both sexes, 3 populations, RMA log BM ¼ 1.4991 log SAC  2.9735 McHenry (1992): Homo sapiens, both sexes, 3 populations, LSR log BM ¼ 1.5492 log SAC  3.1290 McHenry (1992): Homo sapiens, both sexes, 3 populations, RMA log BM ¼ 2.68 log HLEN  1.94 Aiello (1981): 23 anthropoid species, both sexes, LSR log BM ¼ 2.70 log HLEN  2.02 Aiello and Wood (1994): 21 simian species (17: both sexes), LSR log BM ¼ 2.75 log HLEN  2.15 Aiello and Wood (1994): 23 simian species, both sexes, RMA log BM ¼ 3.59 log HLEN  4.25 Aiello and Wood (1994): 4 hominoid species, both sexes, LSR log BM ¼ 3.78 log HLEN  4.74 Aiello and Wood (1994): 4 hominoid species, both sexes, RMA log BM ¼ 2.7018 log HHAP  2.6388 McHenry (1992): 7 hominoid species, both sexes, LSR log BM ¼ 2.7431 log HHAP  2.7022 McHenry (1992): 7 hominoid species, both sexes, RMA log BM ¼ 2.73 log HMSC  0.27 Aiello (1981): 23 anthropoid species, both sexes, LSR log BM ¼ 2.595 log HMSC  0.113 Hartwig-Scherer (1993): African apes, 19 individuals, RMA log BM ¼ 2.36 log HMSC  0.16 Aiello and Wood (1994): 21 simian species (17: both sexes), LSR log BM ¼ 2.69 log HMSC  0.25 Aiello and Wood (1994): 23 simian species, both sexes, RMA log BM ¼ 2.67 log HMIN  0.18 Aiello and Wood (1994): 21 simian species (17: both sexes), LSR log BM ¼ 2.73 log HMIN  0.27 Aiello and Wood (1994): 23 simian species, both sexes, RMA (continued)

Page 11 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Estimation of Basic Life History Data of Fossil Hominoids, Table 7 (continued) Dimension (mm) Humerus distal epiphyseal breadth [M4] (HEPI)

Humerus distal joint breadth (HDJT)

Humerus distal: capitular height  articular width (ELB) Radius head mediolateral diameter (RADH)

Radius midshaft circumference (RMSC) Acetabular capacity (cm3) (ACCA) Acetabulum height (ACET)

Femur length (FL) Femur head AP diameter [M19.3] (APFH)

r 0.98

Equation log BM ¼ 2.49 log HEPI + 0.26

Source and sample Aiello and Wood (1994): 21 simian species (17: both sexes), LSR log BM ¼ 2.56 log HEPI + 0.17 Aiello and Wood (1994): 23 simian species, both sexes, RMA 0.95 log BM ¼ 2.72 log HEPI  0.20 Aiello and Wood (1994): 4 hominoid species, both sexes, LSR log BM ¼ 2.88 log HEPI  0.48 Aiello and Wood (1994): 4 hominoid species, both sexes, RMA 0.98 log BM ¼ 2.44 log HDJT + 0.70 Aiello and Wood (1994): 21 simian species (17: both sexes), LSR log BM ¼ 2.49 log HDJT + 0.63 Aiello and Wood (1994): 23 simian species, both sexes, RMA 0.966 log BM ¼ 1.4115 log ELB  2.4855 McHenry (1992): 7 hominoid species, both sexes, LSR log BM ¼ 1.4617 log ELB  2.6280 McHenry (1992): 7 hominoid species, both sexes, RMA 0.955 log BM ¼ 1.9910 log RADH  0.8912 McHenry (1992): Homo sapiens, both sexes, 3 populations, LSR log BM ¼ 2.0859 log RADH  1.0132 McHenry (1992): Homo sapiens, both sexes, 3 populations, RMA 0.97 log BM ¼ 2.826 log RMSC + 0.031 Hartwig-Scherer (1993): African apes, 19 individuals, RMA 0.987 BM ¼ 4.162 ACCA  2.541 Suzman (1980): 7 chimpanzees 0.967 BM ¼ 3.842 ACCA  28.031 Suzman (1980): 6 gorillas 0.967 ln BM ¼ 2.8025 ln ACET  6.6459 Jungers (1988): 7 hominoid species, both sexes 0.997 ln BM ¼ 3.1824 ln ACET  7.9090 Jungers (1988): 6 nonhuman hominoid species, both sexes 0.987 log BM ¼ 3.498 log FL  6.750 Ruff (1990): 4 nonhuman anthropoid species, both sexes 0.98 log BM ¼ 2.45 log APFH + 0.92 Aiello and Wood (1994): 21 simian species (17: both sexes), LSR log BM ¼ 2.50 log APFH + 0.86 Aiello and Wood (1994): 23 simian species, both sexes, RMA 0.98 BM ¼ 2.239 APFH  36.5 Ruff et al. (1997): modern Homo sapiens sample (continued)

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Estimation of Basic Life History Data of Fossil Hominoids, Table 7 (continued) Dimension (mm) r Equation Femur head vertical diameter 0.970 log BM ¼ 2.6465 log VDFH  2.4093 [M18] (VDFH) log BM ¼ 2.7284 log VDFH  2.5310

Source and sample McHenry (1992): 7 hominoid species, both sexes, LSR McHenry (1992): 7 hominoid species, both sexes, RMA 0.976 log BM ¼ 1.7125 log VDFH  1.0480 McHenry (1992): Homo sapiens, both sexes, 3 populations, LSR log BM ¼ 1.7538 log VDFH  1.1137 McHenry (1992): Homo sapiens, both sexes, 3 populations, RMA 0.98 log BM ¼ 2.44 log VDFH + 0.95 Aiello and Wood (1994): 21 simian species (17: both sexes), LSR log BM ¼ 2.53 log VDFH + 0.83 Aiello and Wood (1994): 23 simian species, both sexes, RMA 0.988 log BM ¼ 2.466 log VDFH + 0.913 Kappelman (1996): 14 catarrhine sp. + ssp., mostly both sexes, LSR log BM ¼ 2.497 log VDFH + 0.872 Kappelman (1996): 14 catarrhine sp. + ssp., mostly both sexes, RMA 0.996 log BM ¼ 2.628 log VDFH + 0.718 Kappelman (1996): 13 catarrhine sp. + ssp., mostly both sexes, without Homo, LSR log BM ¼ 2.640 log VDFH + 0.702 Kappelman (1996): 13 catarrhine sp. + ssp., mostly both sexes, without Homo, RMA Femur head diameter (FHD) 0.974 ln BM ¼ 2.6142 ln FHD  5.4282 Jungers (1988): 7 hominoid species, both sexes 0.997 ln BM ¼ 2.9047 ln FHD  6.3233 Jungers (1988): 6 nonhuman hominoid species, both sexes Femur shaft AP  transverse 0.973 log BM ¼ 1.1823 log FS  1.5745 McHenry (1992): 7 hominoid diameter inferior to the lesser species, both sexes, LSR trochanter [M9  M10] (FS) log BM ¼ 1.2152 log FS  1.6605 McHenry (1992): 7 hominoid species, both sexes, RMA 0.978 log BM ¼ 0.7927 log FS  0.5233 McHenry (1992): Homo sapiens, both sexes, 3 populations, LSR log BM ¼ 0.8107 log FS  0.5733 McHenry (1992): Homo sapiens, both sexes, 3 populations, RMA log BM ¼ 1.475 log FS + 0.524 Hartwig-Scherer (1993): African apes, 19 individuals, RMA Femur shaft circumference 0.95 log BM ¼ 2.862 log FSC  0.779 Hartwig-Scherer (1993): African inferior the lesser trochanter apes, 19 individuals, RMA (FSC) Femur midshaft transverse 0.99 log BM ¼ 2.55 log FMTD + 1.19 Aiello (1981): 23 anthropoid diameter (FMTD) species, both sexes, LSR 0.981 log BM ¼ 2.492 log FMTD  1.696 Ruff (1990): 5 anthropoid species, both sexes 0.982 log BM ¼ 2.533 log FMTD  1.737 Ruff (1990): 4 nonhuman anthropoid species, both sexes 0.969 log BM ¼ 2.541 log FMTD  1.793 Ruff (1990): African apes and human, both sexes (continued)

Page 13 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Estimation of Basic Life History Data of Fossil Hominoids, Table 7 (continued) Dimension (mm) r Femur midshaft 0.98 circumference [M8] (FMSC)

Equation log BM ¼ 2.64 log FMSC  0.29 log BM ¼ 2.71 log FMSC  0.39

0.95

log BM ¼ 2.809 log FMSC  0.597

Femur biepicondylar  distal 0.961 log BM ¼ 1.0829 log FDIST  1.8467 shaft AP diameter (FDIST) log BM ¼ 1.1271 log FDIST  1.9840 0.968 log BM ¼ 0.9600 log FDIST  1.5678 log BM ¼ 0.9921 log FDIST  1.6762 Femur epicondylar breadth [M21] (FEPIML)

0.98

log BM ¼ 2.48 log FEPIML + 0.29 log BM ¼ 2.53 log FEPIML + 0.21

Femur epicondylar depth [M24] (FEPIAP)

0.97

log BM ¼ 2.59 log FEPIAP + 0.28 log BM ¼ 2.66 log FEPIAP + 0.18

Femur medial condyle posterior width (MCW)

0.978 ln BM ¼ 2.1224 ln MCW  2.6824 0.979 ln BM ¼ 2.1743 ln MCW  2.8023

Femur lateral condyle posterior width (LCW)

0.950 ln BM ¼ 1.9335 ln LCW  1.7269 0.977 ln BM ¼ 2.1865 ln LCW  2.3033

Tibia length (TL)

0.981 log BM ¼ 4.123 log TL  7.914

Tibia proximal AP  transverse diameter (TPR)

0.973 log BM ¼ 1.2770 log TPR  2.5918 log BM ¼ 1.3127 log TPR  2.7066 0.991 log BM ¼ 1.0583 log TPR  1.9537 log BM ¼ 1.0683 log TPR  1. 9880

Tibia distal AP  transverse 0.965 log BM ¼ 1.1806 log TDIST  1.5390 diameter of the talar facet (TDIST) log BM ¼ 1.2232 log TDIST  1.6493 0.991 log BM ¼ 0.9005 log TDIST  0.8790 log BM ¼ 0.9246 log TDIST  0.9743

Source and sample Aiello and Wood (1994): 21 simian species (17: both sexes), LSR Aiello and Wood (1994): 23 simian species, both sexes, RMA Hartwig-Scherer (1993): African apes, 19 individuals, RMA McHenry (1992): 7 hominoid species, both sexes, LSR McHenry (1992): 7 hominoid species, both sexes, RMA McHenry (1992): Homo sapiens, both sexes, 3 populations, LSR McHenry (1992): Homo sapiens, both sexes, 3 populations, RMA Aiello and Wood (1994): 21 simian species (17: both sexes), LSR Aiello and Wood (1994): 23 simian species, both sexes, RMA Aiello and Wood (1994): 21 simian species (17: both sexes), LSR Aiello and Wood (1994): 23 simian species, both sexes, RMA Jungers (1988): 7 hominoid species, both sexes Jungers (1988): 6 nonhuman hominoid species, both sexes Jungers (1988): 7 hominoid species, both sexes Jungers (1988): 6 nonhuman hominoid species, both sexes Ruff (1990): 4 nonhuman anthropoid species, both sexes McHenry (1992): 7 hominoid species, both sexes, LSR McHenry (1992): 7 hominoid species, both sexes, RMA McHenry (1992): Homo sapiens, both sexes, 3 populations, LSR McHenry (1992): Homo sapiens, both sexes, 3 populations, RM McHenry (1992): 7 hominoid species, both sexes, LSR McHenry (1992): 7 hominoid species, both sexes, RMA McHenry (1992): Homo sapiens, both sexes, 3 populations, LSR McHenry (1992): Homo sapiens, both sexes, 3 populations, RMA (continued)

Page 14 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Estimation of Basic Life History Data of Fossil Hominoids, Table 7 (continued) Dimension (mm) r Tibia midshaft circumference 0.97 [M10] (TMSC)

Equation log BM ¼ 2.84 log TMSC  0.43 log BM ¼ 2.92 log TMSC  0.94

Medial tibial plateau AP diameter [M4a] (TMED)

0.96

log BM ¼ 2.48 log TMED + 0.88 log BM ¼ 2.60 log TMED + 0.74

Lateral tibial plateau AP diameter (TLAT)

0.95

log BM ¼ 2.63 log TLAT + 0.79 log BM ¼ 2.76 log TLAT + 0.62

Tibia proximal breadth [M3] 0.98 (TPROX)

log BM ¼ 2.45 log TPROX + 0.35 log BM ¼ 2.51 log TPROX + 0.26

Distal tibial articulation AP diameter (DTB)

0.957 ln BM ¼ 2.5037 ln DTB  3.9397 0.988 ln BM ¼ 2.8561 ln DTB  4.8747

Source and sample Aiello and Wood (1994): 20 simian samples, LSR Aiello and Wood (1994): 20 simian samples, RMA Aiello and Wood (1994): 21 simian species (17: both sexes), LSR Aiello and Wood (1994): 23 simian species, both sexes, RMA Aiello and Wood (1994): 21 simian species (17: both sexes), LSR Aiello and Wood (1994): 23 simian species, both sexes, RMA Aiello and Wood (1994): 21 simian species (17: both sexes), LSR Aiello and Wood (1994): 23 simian species, both sexes, RMA Jungers (1988): 7 hominoid species, both sexes Jungers (1988): 6 nonhuman hominoid species, both sexes

Dimensions in mm (or mm2); numbers in square brackets refer to measurements numbers in Martin (Martin and Saller 1959). Body mass in g; equations in italics, body mass in kg LSR least-squares regression, RMA reduced major axis

between the two variables at correlation coefficients as high as 0.995–0.997 (Table 9). Therefore, all comparative work using brain size should either center on cranial capacities or brain masses. Calculations of relative brain size (cephalization, encephalization quotient) based on body mass clearly should proceed with brain mass. Unfortunately, the available predictive equations for primates or mammals in general give quite differing brain mass values (Table 10). The primate cranial capacity brain mass conversion formula (Martin 1990) is retained here, since it produces neither clearly excessive values in the upper (Homo sapiens) range in view of such conversion data as presented by earlier authors [compilation in Martin and Saller (1959)] nor nonsense values in the lower range, whereby brain volumes would become just larger than cranial capacities (as produced with the use of the formula of Ruff et al. (1997)). It should be noted that there are some pitfalls in the determination of the cranial capacity as basis for brain mass estimation. The usual method of packing the cranial cavity with small rounded particles as lead shot, mustard seed or millet grain, and other comparable materials is limited by the Table 8 Body mass prediction based on stature and bi-iliac breadth Equation BM ¼ 0.413 ST + 2.892 BI  84.8 BM ¼ 0.498 ST + 1.877 BI  74.6 BM ¼ 0.373 ST + 3.033 BI  82.5

r 0.941 0.965 0.90

Source and sample Ruff and Walker (1993): 21 males, worldwide adult population Ruff and Walker (1993): 306 male Karkar Islanders, 8–67 years Ruff et al. (1997): males

Only samples with r  0.90 were selected BM body mass (kg), ST stature (cm), BI bi-iliac breadth (cm): before applying these formulas, skeletal bi-iliac breadth is converted to living bi-iliac breadth using the equation living BI ¼ 1.17 skeletal BI  3 (Ruff et al. 1997) Page 15 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Table 9 Interspecific allometric relationship of cranial capacity and brain mass in primates and in mammals other than primates Allometric Sample equation 33 primate species CrC ¼ 0.94 BrM1.02 27 primate species – 17 mammal CrC ¼ 0.96 species BrM1.02

r Authors 0.996 Martin (1990, p 363 + Fig. 8.4) 0.995 Ruff et al. (1997) 0.997 Ro¨hrs and Ebinger (2001)*

Formula converted for mass estimation log BrM ¼ 0.98 log CrC + 0.0246 log BrM ¼ 0.976 log CrC + 0.0596 log BrM ¼ 0.98 log CrC + 0.0168

BrM brain mass, CrC cranial capacity (cm3) The authors present this equation as log CrC ¼ 0.0015 + 1.02 log BrV (BrV ¼ brain volume) and add the equation BrV ¼ BrM:1.036

a

need to condense the fill both in the skull and in the measuring cylinder in the same way. The method closing the foramina before packing the cranial cavity may also influence the result. A good standardized practice is needed to achieve a tolerable accuracy with this volumetric approach, and it may be combined with a weighing procedure (Smith et al. 1995). Measurements obtained by the packing method may surpass the volume of artificial endocasts (Martin 1990, Table 8.5: 10–11 % in the Eocene lemuroid primate Adapis parisiensis). The estimation of endocranial volume by double graphic integration derived from X-ray pictures may result in substantially diverging values (Martin 1990, Table 8.5: 10–12 % less than the artificial endocast in Adapis parisiensis). An assessment of cranial capacity in fossil primates also may be done by the use of linear cranial dimensions (Martin 1990; Table 11).

Calculating Relative Brain Size There are four main concepts of scaling relative brain size in primates (McHenry 1976). The constant of cephalization (CC) (Hemmer 1971) was developed on the base of a common mammalian intraspecific allometric exponent around 0.23 [BrM ¼ CC  BM0.23; BrM ¼ brain mass (g), BM ¼ body mass (g)]. The index of progression (IP) (Bauchot and Stephan 1966, 1969) gives the ratio of actual brain mass to brain mass predicted on the basis of an interspecific basal insectivore allometric equation with an exponent of 0.63. [The index of cranial capacity (ICC) as introduced by Martin (1990) follows just the same lines as the index of progression.] The encephalization quotient (EQ) (Jerison 1973) is also the ratio of actual to predicted brain mass, the latter based on an interspecific mammalian allometry (predicted brain mass ¼ 0.12 BM2/3). The extra-neuron count (Nc) (Jerison 1973) “is a numerical measure of progressiveness in brain development beyond the level required by increasing body size” (Jerison 1973). The results of the CC and Nc methods perfectly correlate on the one hand as do the results of the IP and EQ methods on the other (Fig. 3). This reduces the issues on principle to the choice of either the intraspecific (CC and Nc methods) or the interspecific (IP and EQ) type of brain to body mass allometries. EQ has been widely used in the last three decades by the overwhelming majority of authors (Hartwig-Scherer 1993; Kappelman 1996; Ruff et al. 1997; McHenry and Coffing 2000). The results of EQ calculations vary depending on which of the different equations is selected (Kappelman 1996) [allometric exponents varying from 0.60 (Old World simian EQ: Martin 1990) or 0.67 (Jerison 1973) close to 0.75 (0.74–0.76) (Martin 1990; Hartwig-Scherer 1993; Ruff et al. 1997; McHenry and Coffing 2000)]. Nevertheless, some writers have begun to feel

Page 16 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Table 10 Cranial capacity-based brain mass estimates (g) by the use of different equations (Table 9) Cranial capacity (cm3) 50 100 500 1,000 1,500

Brain mass estimated by the primate formula of Martin (1990) 49 97 467 922 1,371

Brain mass estimated by the primate formula of Ruff et al. (1997) 52 103 494 972 1,444

Brain mass estimated by the mammalian formula of Ro¨hrs and Ebinger (2001) 48 95 459 905 1,347

uncomfortable about the EQ method (McHenry 1988; Kappelman 1996; Arsuaga et al. 1999; Rightmire 2004). A negative allometric relationship between body size and EQ was raised, but the reasons were assumed to be unclear (Kappelman 1996). EQ being a function of body mass predicted for individuals using an interspecific equation, the comparison of EQ values determined for fossils was considered to be misleading (Rightmire 2004). Similarly, the EQ was not felt to be meaningful when closely related species with widely differing body mass are compared (Arsuaga et al. 1999). Curious EQ results like a position of Miopithecus talapoin above all nonhuman hominoids, the gorilla ranging below all cercopithecines (Hemmer 1971; Table 2), or Cebus albifrons lying between Homo erectus and Homo sapiens (Hartwig-Scherer 1993, Fig. 6) also indicate that this procedure may be seriously biologically inadequate. All such problems disappear when the CC intraspecific approach is followed instead of the EQ interspecific method (Hemmer 1971). As a by-effect of the low intraspecific allometric exponent, the influence of differences in body mass predictions on EQ calculations (Conroy 1987) is less profound with the CC method.

Life History Data Estimations in Fossil Hominids The final approach to life history data estimation in fossil hominoids, especially in fossil hominids, is a story of reliability of the prediction equations to be used. There is a wide variability in the results of body mass estimation obtained on the basis of different species samples used to create the equations, on the basis of different dimensions, and using different line-fitting techniques (Table 12). The availability of several parts of a single skeleton, as, e.g., in the female Australopithecus afarensis AL 288-1 specimen, allows for many independent estimates, which group together centrally to resemble a normal distribution, to give a clear and conclusive view of the most probable body mass of that individual and to allow easy recognition of outsider values (Fig. 4). In the AL 288-1 case, the peak of the density curve (made up of 54 estimates) is found Table 11 Estimation of cranial capacity (CrC) (cm3) by linear dimensions in primates (Martin 1990: Table 8.10) Dimension (mm) Braincase width (CW) Braincase height (CH) Braincase length (CL) Sum CW + CH + CL (SU) Product CW  CH  CL (PR)

r 0.99 0.98 0.98 0.995 0.995

Equation log CrC ¼ log CrC ¼ log CrC ¼ log CrC ¼ log CrC ¼

3.24 log CW  3.75 2.91 log CH  2.91 3.28 log CL  4.37 3.12 log SU  5.18 1.02 log PR  3.54

The formulas are based on the major axis, and the cranial capacities were determined by packing the cranial cavity with sintered glass particles Page 17 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Fig. 3 Bivariate log-log plots (lines: least-squares regressions) to demonstrate the mutual relationship of the main methods to scale relative brain size (Data from McHenry (1976), Table 2; hominoid primates). (a) Extra-neuron count (Nc) (Jerison 1973) against constant of cephalization (CC) (Hemmer 1971) (r ¼ 0.997). (b) Encephalization quotient (EQ) (Jerison 1973) against constant of cephalization (CC) r ¼ 0.971). (c) Encephalization quotient (EQ) against index of progression (IP) (Bauchot and Stephan 1966) (r ¼ 0.998)

near 29 kg, and the mean and the median range near 30 kg, allowing for a consistent estimation of body mass roughly around 30 kg, as also found in earlier studies (Jungers 1988, 1990; McHenry 1992). The existence of such a key specimen also allows us to judge empirically which predictors may be more useful and which should be excluded from the estimation process for a taxon for Page 18 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Table 12 Selected examples that characterize the broad variability of body mass estimates (kg) of fossil hominids derived at the base of different predicting equations Body mass predicted Species and by dental Body mass predicted Body mass predicted by postcranial specimen dimensions by cranial dimensions dimensions Australopithecus 52.8 30.4–30.4, 27.4–29.6, 32.3–36.0, afarensis AL 28832.2–35.5, 24.3–26.2, 26.3–28.5, 1 35.1–39.8, 38.9–29.9, 17.4-17.117.3–27.3-25.9-26.5, 16.5-16.0-16.1-30.7-30.0-29.9, 12.9-11.8-12.3–28.2-27.1-27.5, 24.1-23.6-23.7–32.5-32.5-32.5, 28.5-27.4-27.7-17.0-16.2-16.4, 27.9-27.6-27.7–27.9-27.4-27.6, 35.2-35.3-35.2–37.1-36.9-36.9, 32.2-32.2-32.2–27.8-27.7-27.7, 27.1-26.9-26.9–24.4-24.1-24.0, 37.0-36.8-36.9–27.6-26.1-26.6, 23.5, 29–30, 27, 26–41, 23–35, 34–34, 32–27, 34–26, 30, 41–31 A. (Paranthropus) 66.6–64.4–59.8–60.1, boisei KNM-ER 57.6–58.8–61.3–60.7, 406 92.3–96.9–85.8–85.4, 69.8 84.0-88.4-86.4–57.0-57.4-57.3, Homo sp. 50.3–48.7–57.1-58.2-58.0–51.3-51.4-51.4, (rudolfensis) 66.3-68.4-68.2–48.3-48.4-48.3, [Australopithecus 54.9-55.9-55.7–43.2-43.2-43.2, (Paranthropus) 55.8-57.1-56.9–42.4-42.3-42.3, 46, 58.4, boisei ?] KNM86.9–106.5, 45–41, 48–36, 50–35, 43 ER 1481 Homo sp. rudolfensis KNMER 1470

80.4–77.4–70.5–70.6, 50.7–51.9–54.2–53.9, 95.2–99.8–88.1–87.7, 45.6

Source Jungers (1988, 1990), McHenry (1988), McHenry (1992), Ruff and Walker (1993), HartwigScherer (1993)

Aiello and Wood (1994), Kappelman (1996) McHenry (1988), McHenry 1992, Ruff and Walker (1993), HartwigScherer (1993) Aiello and Wood (1994), Kappelman (1996)

Mass estimates separated by “–”: prediction based on the same dimension and the same species sample but different line-fitting technique; mass estimates separated by “–”: prediction based on the same dimension but different species samples; mass estimates separated by “,”: prediction based on different dimensions

which neither humans nor African apes are completely adequate models (Hartwig-Scherer 1993). For AL 288-1, dimensions of the humerus and radius heads and the elbow joint (McHenry 1992) produce clearly estimates that are too small based on general hominoid allometries as does the size of the sacral body (McHenry 1992). On the other hand, very large estimates result from the circumference of the humerus based on Homo sapiens allometry and from the circumference of the tibia based on an African ape allometry (Hartwig-Scherer 1993), while the dentition provides an outsider value (Jungers 1988). The availability of well-founded body mass estimates based on postcranial predictors allows us to determine which cranial predictors compare in reliability with them for Australopithecus and Page 19 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Fig. 4 Density curves of the distributions of body mass estimates in selected examples of early hominid specimens, based on published values as given in Table 12 (mean values when there are two or three different values based on the same dimension and the same species sample but different line-fitting techniques) (Plots created by use of MathSoft Axum 6.0)

early Homo as well. Orbital height was extracted as the cranial variable which produces body mass estimates that are most in line with postcranially generated estimates (Aiello and Wood 1994). This may be supplemented by estimates based on a computer digitizing measurement of the orbital area (Kappelman 1996). Published body mass estimates based on these cranial dimensions were used together with most relevant postcranially predicted data to extract rounded mean body mass for Australopithecus and Homo paleopopulations and to calculate in each case the CC with rounded mean brain mass converted from mean cranial capacity (Tables 13 and 14). These brain mass and CC data were then used as the source material for the estimation of life history traits. The evaluation of the reliability of the life history trait predictor equations (Tables 3 and 4) was done empirically based on the PE of the estimation of Homo sapiens [PE ¼ (observed – predicted)/predicted  100]. Only equations with a PE  5 % were considered to be useful for the life history estimation in fossil hominids. It must never be forgotten that most of the actually observed primate life history dimensions are subject to enormous variability produced by diverse ecological factors. Any prediction for extinct populations will be subject to this variability too. Nevertheless, the results then obtained confirm, correct, and supplement the earlier [Hemmer (1974) on the age at sexual maturity, at first breeding, and at teeth eruption in Australopithecus] and later calculations [Smith and Tompkins (1995) on first permanent molar eruption]. At the same time, they are supported by results of osteobiographic techniques. Australopithecus (afarensis, africanus, robustus) and early Homo specimens, aged at something like 3–3.5 years on the basis of incisor crowns with little or no root development, had first permanent molars coming into occlusion

Page 20 of 28

Female Both sexes Male Female Both sexes

Both sexes Male Female Male 38

27, 28

47

58,39 70, 58 26 32

30, 22

58e c.58

49 c.50

c.40

c.35

40 c.40 32 c.30 37–56 c.35–40

34 c.30 45–51 c.40–45

33–58

41 c.40 30 c.30

45 c.45 29 c.30 30–68 c.40

d

c

b

a

d

Brain mass estimate (g)

510, 530 500

410

428, 485

530

521

452

434

467

476,495

385

401, 454

c.320–380e 302–357

b

Cranial capacity (cm 3)

495 495

487 c.485

c.385

423 c.425

c.430

407 c.405

c.300–360

Retained brain mass (g)

c.44

c.42

c.34

c.38

c.40

c.35

c.24–29

Constant of cephalization

Original body mass values rounded to the next kg and retained body mass to the next 5 kg. Brain mass estimated on the basis of the formula given by Martin (1990, Table 9) and retained brain mass rounded to the next 5 g a Aiello and Wood (1994, mean of LSR and RMA estimates) b Kappelman (1996) c Jungers (1988) d McHenry and Coffing (2000) e Basic dimensions by Brunet et al. (2002): orbital height used to estimate body mass with equations (Table 6) published by Aiello and Wood (1994) and Kappelman (1996)

A. (Paranthropus) robustus

A. (Paranthropus) boisei

A. (Paranthropus) aethiopicus

Australopithecus africanus

Male?

Sahelanthropus tchadensis Australopithecus afarensis

Male Female Both sexes Male Female

Sex

Taxon

Body mass, postcranial estimate Retained body (kg) mass (kg)

Body mass, cranial estimate (kg)

Table 13 Estimates of body mass, brain mass, and constant of cephalization in Sahelanthropus and Australopithecus

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Page 21 of 28

Male Female Both sexes KNM-ER 1470 Both sexes Female Both sexes Both sexes

Homo sp. habilis, earliest Pleistocene

58

81–100/92

61

52 66 76

35f 94g 35f 52f

57–60

30e

47

30, 35

58–66

51

34, 26

56–66

51–60

37 32

76

d

c

b

a

c.55 c.90 c.75

c.60

c.60

c.30

c.35 c.30 c.35 c.50

Retained body mass (kg)

1,565 1,489d

1,166f 1,390g 1,100f 1,230f

1,015 1,030 1,004

c.600e 675 804–909

752

594, 509

b

871

612

c

1,430 1,370

1,071 1,273 1,012 1,129

935 949 925

c.559 627 744–839

697

553, 476

805

570

Cranial Brain mass capacity (cm 3) estimate (g)

c.1120 c.1430 c.1370

c.935

c.560 c.625 c.805

c.515 c.570 c.695

Retained brain mass (g)

c.91 c.104 c.104

74

c.64

c.52

c.48 c.51 c.58

Constant of cephalization

Original body mass values rounded to the next kg and retained body mass to the next 5 kg. Brain mass estimated on the basis of the formula given by Martin (1990, Table 9) and retained brain mass rounded to the next 5 g a Aiello and Wood (1994, mean of LSR and RMA estimates) b Kappelman (1996) c McHenry and Coffing (2000) d Ruff et al. (1997) e Basic dimensions of skull D 2700 by Vekua et al. (2002): orbital height used to estimate body mass with equations (Table 6) published by Aiello and Wood (1994) and Kappelman (1996); additional cranial capacities of D 2280 and D 2282 by Gabunia et al. (2000) f Rightmire (2004) g Arsuaga et al. (1999)

Homo sp. ergaster, Early Pleistocene Homo sp. erectus, Early Zhoukoudian XI Middle Pleistocene Zhoukoudian XII Sangiran 17 Both sexes Archaic Homo sapiens, Arago Middle Pleistocene, Sima d.l. Huesos Europe Steinheim Petralona Both sexes Late archaic Homo Male sapiens (Neanderthals) Both sexes

Homo sp. georgicus, Early Pleistocene

Homo sp. rudolfensis, earliest Pleistocene

Sex or specimen

Taxon

Body mass, postcranial estimate (kg)

Body mass, cranial estimate (kg)

Table 14 Estimates of body mass, brain mass, and constant of cephalization in Pleistocene Homo

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Table 15 Estimations of life history data in Sahelanthropus, Australopithecus, and Homo fossil samples Taxon Gorilla gorilla Pan troglodytes Sahelanthropus tchadensis Australopithecus afarensis Australopithecus africanus Australopithecus boisei Australopithecus robustus Homo sp. habilis Homo sp. rudolfensis Homo sp. georgicus Homo sp. ergaster Homo sp. erectus Archaic Homo sapiens, Europe Homo sapiens, Neanderthals Homo sapiens, observed values

Age at eruption of the first lower molar (years) – 3.15 2¼ 2½

Age at sexual maturity, female (years) 6.5 9.8 6 8

Age at first breeding, female (years) 9.9 11.5 8 10

Maximum life span (years) 39.3 44.5 38  44

2¾

8

10½

45

3

8½

11

46

3

9

11½

48

3

9

11½

49

3¼–3½ 3¾

9½–10 11

12–12½ 14

50–51 55

3½

10–10½

13

51–54

4¼ 4½ 5

12 13 14½

15 16 18

57 60 65

5¾

16

19½

69

5.4

16.5

19.3

70

Age at eruption of the first lower molar rounded to the next ¼ years, age at sexual maturity and at first breeding rounded to the next ½ year, and maximum life span rounded to the next year. All estimations based on the predictor equations evaluated as useful or very useful (Tables 3 and 4) (mean predicted value, if more than one equation per dimension meets the criteria). The actual observed Gorilla gorilla, Pan troglodytes, and Homo sapiens values are those used for the calculations of the predictor equations [Published by Smith et al. (1995) (molar eruption) and Harvey and CluttonBrock (1985)]

(Bromage 1990) just as predicted with first lower molar eruption at around 3 years (Table 15). The estimation of life history data confirms the fundamental nature of the australopithecines as progressive apes, not as humans, the early Australopithecus afarensis ranging within the modern African ape life history dimensions. Some important new fossil taxa discovered in the last years are included in the selected samples of life history data presentation (Table 15). The interpretation of the Late Miocene Sahelanthropus tchadensis (Brunet et al. 2002), as a taxon possibly related to the hominid stem species near the splitting of chimpanzee and hominid lines (Brunet et al. 2002; Wood 2002), may be supported by the estimation of life history dimensions that indicate an earlier evolutionary stage than all Australopithecus and Homo paleopopulations on the one hand and then the chimpanzee on the other. The Early Pleistocene (Upper Villafranchian) Homo paleopopulation of Dmanisi (Georgia) (Homo georgicus; Gabounia et al. 2002) has been interpreted as more closely related to the earliest Pleistocene habilis and rudolfensis than to the Later Early Pleistocene ergaster and erectus (Gabunia et al. 2000; Gabounia et al. 2002; Vekua et al. 2002). The life history estimates clearly

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

support this view. The so-called Homo floresiensis (Brown et al. 2004) is not integrated here, as this specimen obviously neither represents a new species nor an enigmatic branch of hominid evolution, but is just a classic microcephalic Homo sapiens individual, sharing the characteristic syndrome of pygmy size, very small (chimpanzee sized) brain, and considerably aberrant skull allometries (Hemmer 1967). Perhaps this fossil may be interesting as an example of the survival of handicapped people in a Paleolithic culture. It may also help to understand the dysregulation leading to microcephalic development as a possible key to an intrinsic relationship of brain, maturation, and life history.

Cross-References ▶ Analyzing Hominin Phylogeny ▶ Defining Hominidae ▶ Defining the Genus Homo ▶ Evolution of the Primate Brain ▶ Fossil Record of Miocene Hominoids ▶ General Principles of Evolutionary Morphology ▶ Hominoid Cranial Diversity and Adaptation ▶ Homo ergaster and Its Contemporaries ▶ Homo floresiensis ▶ Modeling the Past: The Primatological Approach ▶ Paleoecology: An Adequate Window on the Past? ▶ Primate Intelligence ▶ Primate Life Histories ▶ Primate Origins and Supraordinal Relationships: Morphological Evidence ▶ The Earliest Putative Hominids ▶ The Ontogeny-Phylogeny Nexus in a Nutshell: Implications for Primatology and Paleoanthropology

References Aiello LC (1981) Locomotion in the Miocene Hominoidea. In: Stringer CB (ed) Aspects of human evolution. Taylor and Francis, London, pp 63–97 Aiello LC, Wood BA (1994) Cranial variables as predictors of hominine body mass. Am J Phys Anthropol 95:409–426 Arsuaga JL, Lorenzo C, Carretero J-M, Gracia A, Martı´nez I, Garcı´a N, Bermu´dez de Castro J-M, Carbonell E (1999) A complete human pelvis from the Middle Pleistocene of Spain. Nature 362:534–537 Bauchot R, Stephan H (1966) Donne´es nouvelles sur l’ence´phalisation des insectivores et des prosimiens. Mammalia 30:160–196 Bauchot R, Stephan H (1969) Ence´phalisation et niveau e´volutif chez les simiens. Mammalia 33:235–275 Boyde A (1990) Developmental interpretations of dental microstructure. In: DeRousseau CJ (ed) Primate life history and evolution: monographs in primatology, vol 14. Wiley-Liss, New York, pp 229–267 Page 24 of 28

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Bromage TG (1990) Early hominid development and life history. In: DeRousseau CJ (ed) Primate life history and evolution: monographs in primatology, vol 14. Wiley-Liss, New York, pp 105–113 Brown P, Sutikna T, Morwood MJ, Soejono RP, Jatmiko Wayhu Saptomo E, Due RA (2004) A new small-bodied hominin from the Late Pleistocene of Flores, Indonesia. Nature 431:1055–1061 Brunet M, Guy F, Pilbeam D, Mackaye HT, Likius A, Ahounta D, Beauvilain A, Blondel C, Bocherens H, Boisserie J-R, de Bonis L, Coppens Y, Dejax J, Denys C, Duringer P, Eisenmann V, Fanone G, Fronty P, Geraads D, Lehmann T, Lihoreau F, Louchart A, Mahamat A, Merceron G, Mouchelin G, Otero O, Campomanes PP, De Leon MP, Rage J-C, Sapanet M, Schuster M, Sudre J, Tassy P, Valentin X, Vignaud P, Viriot L, Zazzo A, Zollikofer C (2002) A new hominid of the Upper Miocene of Chad, Central Africa. Nature 418:145–151 Conroy GC (1987) Problems of body-weight estimation in fossil primates. Int J Primatol 8:115–137 Count W (1947) Brain and body weight in man: their antecedents in growth and evolution. Ann New York Acad Sci 46:993–1122 De Rousseau CJ (1990) Life-history thinking in perspective. In: DeRousseau CJ (ed) Primate life history and evolution: monographs in primatology, vol 14. Wiley-Liss, New York, pp 1–13 Deaner RO, Barton RA, Van Schaik CP (2003) Primate brains and life histories: renewing the connection. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. The University of Chicago Press, London/Chicago, pp 233–265 Gabounia L, de Lumley M-A, Vekua A, Lordkipanidze D, de Lumley H (2002) De´couverte d’un nouvel hominide´ a` Dmanissi (Transcaucasie, Ge´orgie). CR Palevol 1:243–253 Gabunia L, Vekua A, Lordkipanidze D, Ferring R, Justus A, Maisuradze G, Mouskhelishvili A, Nioradze M, Sologashvili D, Swisher C III, Tvalchrelidze M (2000) Current research on the hominid site of Dmanisi. In: Lordkipanidze D, Bar-Yosef O, Otte M (eds) Early humans at the gates of Europe, vol 92. ERAUL, Lie`ge, pp 13–27 Gingerich PD, Smith BH, Rosenberg K (1982) Allometric scaling in the dentition of primates and prediction of body weight from tooth size in fossils. Am J Phys Anthropol 58:81–100 Hartwig- Scherer S (1993) Body weight prediction in early fossil hominids: towards a taxon “independent” approach. Am J Phys Anthropol 92:17–36 Harvey PH (1990) Life-history variation: size and mortality patterns. In: DeRousseau CJ (ed) Primate life history and evolution: monographs in primatology, vol 14. Wiley-Liss, New York, pp 81–88 Harvey PH, Clutton-Brock TH (1985) Life history variation in primates. Evolution 39:559–581 Harvey PH, Read AF (1988) How and why do mammalian life histories vary? In: Boyce MS (ed) Evolution of life histories of mammals: theory and pattern. Yale University Press, New Haven, pp 213–232 Harvey PH, Martin RD, Clutton-Brock TH (1987) Life histories in comparative perspectives. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 181–196 Hemmer H (1967) Allometrie-Untersuchungen zur Evolution des menschlichen Scha¨dels und seiner Rassentypen. Fischer, Stuttgart Hemmer H (1971) Beitrag zur Erfassung der progressiven Cephalisation bei Primaten. In: Proceedings 3rd international congress primatology, Z€ urich 1970, vol 1. Karger, Basel, pp 99–107

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Hemmer H (1974) Progressive Cephalisation und Dauer der Jugendentwicklung bei Primaten, nebst Bemerkungen zur Situation bei Vor- und Fr€ uhmenschen. In: Bernhard W, Kandler A (eds) Bevo¨lkerungsbiologie. Gustav Fischer, Stuttgart, pp 527–533 Hemmer H (2001) Die Feliden aus dem Epivillafranchium von Untermaßfeld. In: Kahlke R-D (Hrg) Das Pleistoza¨n von Untermaßfeld bei Meiningen (Th€ uringen), Teil 3. Monographien des Ro¨misch-Germanischen Zentralmuseums Mainz 40(3): 699–782, Tafel 132-143 € Hemmer H (2003) Pleistoza¨ne Katzen Europas-eine Ubersicht. Cranium 20(2):6–22 Hemmer H (2004) Notes on the ecological role of European cats (Mammalia: Felidae) of the last two million years. In: Baquedano E, Rubio Jara S (eds) Miscela´nea en homenaje a Emiliano Aguirre, vol II, Paleontologı´a: 214–232. Zona Arqueolo´gica, 4, Museo Arqueolo´gico Regional, Alcala´ de Henares Jerison HJ (1973) Evolution of the brain and intelligence. Academic, New York/London Jungers WL (1988) New estimates of body size in australopithecines. In: Grine FE (ed) Evolutionary history of the “robust” australopithecines. Aldine de Gruyter, New York Jungers WL (1990) Problems and methods in reconstructing body size in fossil primates. In: Damuth J, MacFadden BJ (eds) Body size in mammalian paleobiology: estimation and biological implications. Cambridge University Press, Cambridge, pp 103–118 Kappeler PM, Pereira ME, van Schaik CP (2003) Primate life histories and socioecology. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. The University of Chicago Press, London/Chicago, pp 1–20 Kappelman J (1996) The evolution of body mass and relative brain size on fossil hominids. J Hum Evol 30:243–276 Krantz GS (1977) A revision of australopithecine body size. Evol Theory 2:65–94 Lanyon LE (1990) The relationship between functional loading and bone architecture. In: DeRousseau CJ (ed) Primate life history and evolution: monographs in primatology, vol 14. Wiley-Liss, New York, pp 269–284 Lee PC, Kappeler PM (2003) Socioecological correlates of phenotypic plasticity of primate life histories. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. The University of Chicago Press, London/Chicago, pp 41–65 Martin RD (1990) Primate origins and evolution: a phylogenetic reconstruction. Chapman and Hall, London Martin R, Saller K (1959) Lehrbuch der Anthropologie. Gustav Fischer, Stuttgart McHenry HM (1976) Early hominid body weight and encephalization. Am J Phys Anthropol 45:77–84 McHenry HM (1988) New estimates of body weight in early hominids and their significance to encephalization and megadontia in ‘robust’ australopithecines. In: Grine FE (ed) Evolutionary history of the “robust” australopithecines. Aldine de Gruyter, New York, pp 133–148 McHenry HM (1992) Body size and proportions in early hominids. Am J Phys Anthropol 87:407–431 McHenry HM, Coffing K (2000) Australopithecus to Homo: transformations in body and mind. Ann Rev Anthropol 29:125–146 Rightmire GP (2004) Encephalization and behavior in Middle Pleistocene humans. In: Baquedano E, Rubio Jara S (eds) Miscela´nea en homenaje a Emiliano Aguirre, vol 3. Paleoantropologı´a, pp 336–348. Zona Arqueolo´gica, 4, Museo Arqueolo´gico Regional, Alcala´ de Henares Ro¨hrs M, Ebinger P (2001) Welche quantitativen Beziehungen bestehen bei Sa¨ugetieren zwischen Scha¨delkapazita¨t und Hirnvolumen? Mamm Biol 66:102–110

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Ruff C (1990) Body mass and hindlimb bone cross-sectional and articular dimensions in anthropoid primates. In: Damuth J, MacFadden BJ (eds) Body size in mammalian paleobiology: estimation and biological implications. Cambridge University Press, Cambridge, pp 119–149 Ruff CB, Walker A (1993) Body size and body shape. In: Walker A, Leakey R (eds) The Nariokotome Homo erectus skeleton. Harvard University Press, Cambridge, pp 234–265 Ruff CB, Trinkaus E, Holliday TW (1997) Body mass and encephalization in Pleistocene Homo. Nature 387:173–176 Sacher GA (1975) Maturation and longevity in relation to cranial capacity in hominid evolution. In: Tuttle RH (ed) Primate functional morphology and evolution. Mouton Publishers, The Hague/ Paris, pp 417–441 Smith BH (1989) Dental development as a measure of life history in primates. Evolution 43:683–688 Smith RJ (1993) Bias in equations used to estimate fossil primate body mass. J Hum Evol 25:31–41 Smith RJ (2002) Estimation of body mass in paleontology. J Hum Evol 43:271–287 Smith BH, Tompkins RL (1995) Toward a life history of the Hominidae. Ann Rev Anthropol 24:257–279 Smith RJ, Gannon PH, Smith BH (1995) Ontogeny of australopithecines and early Homo: evidence from cranial capacity and dental eruption. J Hum Evol 29:155–168 Steudel K (1980) New estimates of early hominid body size. Am J Phys Anthropol 52:63–70 Suzman IM (1980) A new estimate of body weight in South African australopithecines. Proc PanAfr Congr Prehist Quat Stud (Nairobi): 175–179 Vekua A, Lordkipanidze D, Rightmire GP, Agusti J, Ferring R, Maisuradze G, Mouskhelishvili A, Nioradze M, de Leon MP, Tappen M, Tvalchrelidze M, Zollikofer C (2002) A new skull of early Homo from Dmanisi, Georgia. Science 297:85–89 Wolpoff MH (1973) Posterior tooth size, body size and diet in South African gracile australopithecines. Am J Phys Anthropol 39:375–394 Wood B (2002) Hominid revelations from Chad. Nature 418:133–135

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_19-5 # Springer-Verlag Berlin Heidelberg 2014

Index Terms: Australopithecus 21, 23 Cephalization 6–7, 21 Cranial capacity 16 Gestation 2 hominoid 5, 9–15, 18 Homo 22–23 Life span 23 Regression 6–7 Sahelanthropus 21, 23 Weaning 2

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

Ancient DNA Susanne Hummel* Institut f€ ur Zoologie und Anthropologie, Historische Anthropologie und Humanökologie, Georg August Universität Göttingen, Göttingen, Germany

Abstract Ancient DNA research, defined as the retrieval and analysis of DNA sequences from various degraded biological source materials, has promoted many biological and medical research fields during the last three decades. In particular, historical anthropology and paleoanthropology stand to benefit from direct access to back-dating genetic data, as has already been shown through applications ranging from individual identification to reconstruction of kinship and marriage patterns to human phylogeny. The DNA-based prerequisites and basic methodological strategies for access to the various types of information are explained, as well as the characteristics of ancient DNA that limit the different approaches. Major restrictions arise from the degradation of ancient DNA down to fragment sizes of only a few hundred base pairs or less. This fact links ancient DNA analysis to either the PCR technique or to Next Generation Sequencing (NGS) approaches, both of which make it possible to deduce genetic information from degraded nucleic acids. Futhermore, ancient DNA extracts regularly consist of only a few intact target sequences, which may harbor sequence deviations due to the degradation process. Both these factors make the analysis vulnerable to the generation of non-authentic results. These pitfalls of ancient DNA analysis are explained and discussed in detail, with reference to the most recent relevant literature. Wherever available, suggestions for strategies to overcome commonly experienced obstacles in ancient DNA analysis are highlighted and evaluated.

Introduction Today, the analysis of ancient degraded DNA, extracted from forensic evidence samples and archaeological specimens hundreds and thousands of years old, is common practice. It was the coincidence of two events, three decades ago, that enabled this remarkable and comparatively rapid development. On the one hand, there were the first reports on the retrieval of ancient DNA from a specimen of an extinct quagga more than 100 years old (Higuchi et al. 1984) and a specimen of an Egyptian mummy 2,400 years old (Pääbo 1984) that electrified many scholars working on historic and prehistoric biological sample materials. On the other hand, PCR was invented, enabling the enzymatic amplification of short specific DNA sequences (Saiki et al. 1985), which proved to be a true breakthrough to a new level of information for any biological and medical discipline. Only through the PCR technique did ancient DNA research, defined as the retrieval and analysis of degraded DNA sequences from forensic evidence, museum specimens, archaeological finds, fossil remains, and any other degraded traces of DNA, become viable. In the context of population genetics, it is generally possible with the help of model calculations to deduce former states from present day genetic patterns (Barbujani and Bertorelle 2001; Cann 2001). *Email: [email protected] Page 1 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

However, these approaches may suffer from heuristic assumptions that fail to prove their applicability. Biases may be caused by, e.g., unknown bottleneck situations, unknown selective forces, or the unreliability of the molecular clock model. Therefore, direct access to historic and prehistoric genetic patterns has been a desideratum ever since ancient mitochondrial and nuclear DNA (nDNA) proved to be approachable through PCR (Hagelberg et al. 1989; Hummel and Herrmann 1991; Jeffreys et al. 1992; Gill et al. 1994). In the early days of ancient DNA research, the common aspect for scholars from different scientific backgrounds was the fact that their investigations dealt with a demanding sample material (Herrmann and Hummel 1993). However, within a short time, the field has diversified, and thousands of manuscripts that can claim to be ancient DNA research work have now been published. Among the various scientific contexts are, for example, epidemiology and public health (for reviews see, e.g., Zink et al. 2002; Greenblatt et al. 2003; Drancourt and Raoult 2005), nutritional sciences and food technology (Miraglia et al. 2004; Kato et al. 2005; Teletchea et al. 2005), histopathology and laboratory medicine (Leiva et al. 2003; Mariappan et al. 2005; Paik et al. 2005), forensic sciences (Iwamura et al. 2004; Valenstein and Sirota 2004; Budowle et al. 2005; Carracedo and Sanchez-Diz 2005; Sipoli Marques et al. 2005; Tamaki and Jeffreys 2005), human evolution (Cavalli-Sforza and Feldman 2003; Kaessmann and Pääbo 2004), paleobotany (Gugerli et al. 2005), and historical anthropology (Keyser-Tracqui et al. 2003; Hummel 2003a, Haak et al. 2008). Although the underlying scientific questions have significantly diversified since the beginning of the new millennium, a common theme for discussion remains, namely, the question of the authenticity of ancient DNA results. This discussion was prompted by a list of criteria (Cooper and Poinar 2000) which – according to the authors – ought to be adhered to in any ancient DNA analysis. However, it was obvious that these criteria concerned themselves only with rather general types of difficulties encountered in the analysis of ancient mitochondrial DNA (mtDNA), in particular where only few or single specimens were available, and should be replaced by a sensible experimental design focused on the actual concerns of each individual investigation (Hummel 2003a, b, Gilbert et al. 2005, Bandelt 2005). At present this long-lasting debate has fallen silent, which is most likely owed to the fact that new technologies involving whole genome sequencing entered the scientific scene a few years ago – technologies which rapidly turned out to be particularly promising for all kinds of evolutionary biology questions (for reviews see, e.g., Huynen et al. 2012, Rizzi et al. 2012, Disotell 2012). In the case of hominid evolution, this means that the effort to answer questions concerning the co-existence of Neanderthals and anatomically modern Homo sapiens from comparatively short parts of the mitochondrial genome (Krings et al. 1997, 2000; Ovchinnikov et al. 2000; Caramelli et al. 2003, 2006; Beauval et al. 2005; Lalueza-Fox et al. 2006; Orlando et al. 2006), which earlier had to be PCR-based, will soon be on firmer ground. This will be achieved as soon as complete genomes of Neanderthals (Green et al. 2010), Denisovan (Krause et al. 2010a), and anatomically modern human individuals (Krause et al. 2010b) have become more numerous. Some caution is called for, however: the initial studies of the so-called Neanderthal genome project (Green et al. 2006, Noonan et al. 2006) were soon controversial, since they revealed inconsistencies most likely due to modern human DNA contamination (Wall and Kim 2007). This case demonstrated that a contamination hazard exists whenever the species under investigation is close to or identical to the investigators. Next Generation Sequencing (NGS) technologies are designed not to exponentially amplify short fragments but to sequence the extracted DNA sequences, but this does not eliminate the hazard. Therefore, independent of whether PCR or NGS technologies are being employed, experimenters must take care to adhere to the basic guidelines for contamination prevention during all steps of

Page 2 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

DNA sample preparation. Beyond that, it seems of course reasonable to adapt the experimental design as closely as possible to the scientific question at hand.

Ancient DNA Sources and Characteristics Genetic information may be preserved in any type of biomaterial which at some point contained cells. In the average animal cell, basically the entire genetic information characterizing the respective individual is coded in the diploid set of chromosomes and hundreds to thousands of mitochondrial genomes. In plants, the chloroplasts also contribute to the genomic information. However, already in the living organism, cell organelles may suffer from normal processes of partial or complete degradation e.g., the decline of the nucleus in keratinous cells of hair and nails during growth. And whereas in plants, seeds are already designed by nature to preserve genetic information through time, a similar situation is not given in animals. However, even in animals, skeletal materials – such as bone and teeth – harbor cells in a more or less intact state of preservation through the ages. Within those tissues that are characterized by a high content of inorganic material and by high density, several different cell types are DNA sources: osteoblasts, osteoclasts, and osteocytes, which are responsible for bone remodeling and homeostasis, as well as all types of blood cells found in the Haversian canals. Aside from the cells representing the genotype of the organism whose skeletal remains were found, cells of pathogens that at some point entered the blood stream may also be preserved. Typically, the majority of ancient DNA is degraded down to fragments smaller than 200 base pairs (bp) in length. This can reproducibly be shown through multiplex approaches (Fig. 1) which simultaneously amplify DNA fragments of different lengths ranging from 100 to 350 bp. The typical signal patterns observable in electropherograms of multiplex amplifications indicate comparatively high yields of DNA fragments smaller than 200 bp and lesser yields of larger fragments. These patterns are not dependent on possibly varying amplification efficiencies of the different primers, or preferential amplification of shorter fragments, but entirely reflect the relative amounts of the target sequences. This should be considered when choosing and optimizing PCR parameters.

DNA Degradation Whether the genetic information of an organism will be preserved just for days and weeks or for hundreds and thousands of years depends on many chemical and biological factors; these factors are interconnected in a highly complex manner and are, therefore, hardly understood and almost impossible to predict. In light of the cumulative empirical findings of many researchers and a small number of systematic studies (Burger et al. 1999; Caputo et al. 2011), certain factors favoring the preservation of partly intact DNA seem undisputedly clear: low temperatures and the absence of humidity, accompanied by a neutral or slightly basic pH value. In general, however, only very few studies have investigated the link between characteristics of the sample material and DNA preservation (Ottoni et al. 2009; Sosa et al. 2013). Immediately after death, favorable conditions are best realized in bones and teeth, due to their high mineral content. When the environment of the decomposing body provides an optimal situation for preservation, the enzymatically driven autolytic decay is soon stopped; at the same time, the subsequent decomposition of remaining tissues through microfauna, bacteria, and fungi is less likely Page 3 of 24

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Fig. 1 Electropherograms of 40-cycle STR multiplex amplifications reveal characteristic differences in signal intensities depending on the length of the amplified fragment. The peaks reflect the typical degradation patterns of ancient DNA. While such pattern is only weakly present in 6-month-old dried blood stains, analyses of forensic and archaeological bone specimens reveal the patterns clearly. For the choice of amplification parameters, it may therefore be recommendable to work with varying cycle numbers, in order to enable proper detection and allele determination of amplification products of different lengths

to take place effectively. The result is a mummification of the cells which, once it has occurred, may well last for thousands of years. The DNA within the mummified cells is now protected from the initial, main destructive processes: hydrolysis and the activity of exonucleases and endonucleases. The DNA will still suffer from a certain amount of destruction (e.g., oxidative damage), but much less so than in the course of early decay. As a matter of fact, the mere preservation of macromorphologically intact skeletal material indicates pH values also favoring DNA preservation. If prehistoric pH values had been as acidic as was claimed in a paper (Lindahl 1993) that was often cited in the context of DNA degradation, the bone mineral of interest would have been turned into water-soluble brushite and thus would no longer have existed. Further, a more or less intact micromorphology that can be assessed by histological techniques indicates the absence of microorganisms, which is also favorable to DNA preservation. Finally, empirical findings indicate that preservation of DNA seems to be favored not only by the density of the bony material (compact versus spongeous bone) but also, possibly even more so, by location in a distal anatomical region, i.e., far from the torso with its large amounts of soft tissues. If these findings prove to be reproducible, this would result in enormously helpful guidance in the decision how to sample a skeleton. It would also indicate that the very early autolytic processes of Page 4 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

body decay are possibly greatly underestimated as a factor in DNA degradation and long-term DNA preservation.

Information from the Genome All genetic information in a cell is part of the so-called genome, regardless of its informational value, what type of cell organelle it originates from, and its mode of inheritance. In animal cells, the genome regularly consists of two types of DNA which differ from each other in many respects: chromosomal DNA, also known as nuclear DNA (nDNA), and mitochondrial DNA (mtDNA). While nDNA is organized in the form of densely packed chromosomes that are located within the nucleus of a cell, mtDNA is organized in up to ten identical plasmid-like rings within each mitochondrion of the cell. There is only a single nucleus in each cell, but there are many mitochondria per cell; depending on the intensity of the metabolic turnover of the specific tissue, there may be up to thousands. Both types of DNA, mitochondrial and nuclear, consist of coding and noncoding regions. The coding regions, also called genes, determine protein synthesis, i.e., they are expressed through the phenotype of an individual, which includes visible features as well as invisible ones (with the latter including, e.g., immunological characteristics). However, until now, it has been the noncoding regions of mtDNA and nDNA that have been the focus of ancient DNA research. This is due to the fact that noncoding regions allow a high degree of sequence and length polymorphism, which are the basis for identifying and reconstructing kinship from the phylogenetic to the genealogical level (Budowle et al. 2003; Pakendorf and Stoneking 2005; Rowold and Herrera 2005).

What Does Mitochondrial DNA Tell Us? Mitochondrial DNA is most suitable for estimating the time of divergence of two or more populations and, for example, for reconstructing migration patterns. This is due to its nonrecombinant mode of inheritance, which implies that all differences found in the mitochondrial sequence are the result of mutation events thought to occur at a constant rate, set by a “molecular clock.” Since the sequence divergence of mtDNA represents a measure of time in this sense, it can also be easily understood why it is in principle possible to investigate present-day populations in order to reconstruct events far back in time. Depending on the choice of sequence that is analyzed, it may be feasible to discriminate individuals on the species or subspecies level, or to assign the maternal lineage to a certain population. Factors that are thought to perhaps affect the precision of the molecular clock are changes in the amount of natural irradiation, e.g., due to volcanic eruptions, and the number and likelihood of back mutations, particularly at so-called mutational hot spots of the mitochondrial sequence. Other caveats that must be considered in the analysis of ancient mtDNA are the possibility of sequencespecific pseudo-mutations due to DNA degradation, nuclear insertions, and the particular high background of contamination through mtDNA – all of which may threaten the authenticity of the results. Inheritance of the Mitochondrial Genome The mitochondrial genome is inherited maternally, lacking recombination and therefore representing a so-called haplotype. This is due to the fact that each female oocyte possesses a full set of mitochondria, whereas a sperm needs just a few to generate energy for movement. For quite some time it was thought that the mitochondria of the sperm did not enter the oocyte at all, but there Page 5 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

now is evidence that male mitochondria do enter but are identified as foreign and destroyed by the oocyte. If this latter process is not effective, the result is a so-called heteroplasmy; that is, two different sequences with their particular sequence deviations are represented in an individual’s mtDNA. Heteroplasmy may also derive from replication errors during cell duplication, a phenomenon particularly often observed and well known from certain C-stretches of the hypervariable regions (Malik et al. 2002). In ancient DNA analysis, it may be challenging to distinguish between true heteroplasmy and an artifactual signal that may occur due to various reasons. Sequence Polymorphisms Mitochondrial DNA reveals a comparatively high density of genes. In humans, as many as 37 genes are represented within the total length of 16,569 bp of a single mtDNA genome. Most of these genes are involved in the metabolic turnover of the cell. Due to the nature of a gene, which codes for the synthesis of proteins, only very limited sequence deviations are possible without disrupting function. However, there are two regions within the human and animal mitochondrial genome, so-called D-loops, which are noncoding, i.e., not involved in protein synthesis. One of the D-loops, spanning almost 1,000 bp at the nomenclatoric origin of the mtDNA, is also known as the hypervariable region (HVR), because it reveals comparatively extensive sequence polymorphism. Besides base exchanges, there may also be base deletions and base insertions. The sequences of two randomly chosen individuals from a population differ on average at eight nucleotide positions within the HVR. The experimental design in ancient DNA analysis from prehistoric specimens must consider possible further deviations that may lead to mismatches in the primer binding sites, thereby causing amplification failure. Cambridge Reference Sequence In order to describe deviations unambiguously, the international scientific community has agreed to refer to a certain reference sequence. This sequence is either known as the Cambridge reference sequence (CRS) or the Anderson reference sequence. It represents the entire sequence of a human mitochondrial genome – the first that was ever analyzed entirely (Anderson et al. 1981). However, the originally published sequence was revealed to contain some rare polymorphism and sequencing errors (Andrews et al. 1999). The sequence belongs to an individual of haplogroup H, which is the major haplogroup in individuals of European descent. Since in phylogenetic terms this means that it is a comparatively young sequence pattern, there are fairly many nucleotide positions in the human mtDNA that are different from the CRS in all other haplogroups found worldwide. Moreover, the CRS mtDNA reveals two comparatively rare deletions in C-stretch regions of the HVR II, which means that the length of the average human mitochondrial genome is 16,570 or 16,571 bp, respectively. Haplotypes, Maternal Lineages, and Haplogroups The actual base sequence in the HVR of an individual is named a haplotype and represents the pattern specific to a maternal lineage. All individuals sharing this haplotype are members of the same maternal lineage, i.e., they are directly related in a genealogical sense, which is most likely when the haplotype is rare or even unique. Alternatively, they are at least closely related in a population genetic sense; that is the situation when many people who are not known to belong to the same genealogical family share this haplotype. The sequence differences found worldwide in the highly polymorphic HVRs of the mitochondrial genome are divided into more than 20 haplogroups consisting of further subgroups. Those groups are clusters of sequences revealing high intra-group similarities. In general, the assignment of Page 6 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

a sequence to a certain haplogroup depends on actual bases that are present at certain key nucleotide positions. While more than 95 % of individuals of European descent can be ascribed to one of seven major haplogroups (Richards et al. 1998), a similar percentage of Native Americans are ascribed to four haplogroups (Torroni et al. 1993). Particularly within highly branched ancient haplogroups, a further division into subgroups is common. These subgroups are defined, in turn, through an additional base pattern at further nucleotide positions that is shared by all representatives of the subgroup. Since ancient DNA is suspected to promote the generation of pseudo-polymorphisms due to degradation artifacts, sequence interpretation and any deductions with respect to phylogeny and migration based on the occurrence of rare or novel haplotypes must proceed with care. At least this holds true for PCR-based analyses; results from NGS analyses seem to be less prone to artifacts of this kind. Phylogeny and Migration The age and spread of haplogroups enable us to draw conclusions with respect to questions of human phylogeny and worldwide migration pattern (Soares et al. 2010; Oppenheimer 2012). The age of a haplogroup is basically deduced from its heterogeneity, i.e., the degree of sequence variation within the group. Basically, haplogroups that are more widespread and reveal more different branches and subgroups are older than those that are comparatively homogeneous (Fig. 2) (Brotherton et al. 2013). In this manner, it is also possible to determine the regional origin and migration patterns of a haplogroup that is represented over a geographically widespread area. At the place or region where representatives of the haplogroup originated, the sequence diversity is expected to be higher than in any other region where the haplogroup is found (Watson et al. 1997).

What Does Chromosomal DNA Tell Us? The analysis of chromosomal DNA sequences allows access to the unique genetic pattern of an individual. This pattern is represented by the specific combination of single polymorphic genetic traits, which characterize the individual on a level that enables identification. The number of genetic

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Fig. 2 The degree of heterogeneity of a haplogroup enables us to deduce the age and the geographical origin of the haplogroup. Ancient haplogroups (A) reveal more diversification, including the manifestation of subgroups, while more recent haplogroups (R) are comparatively homogeneous. Each dot in this type of depiction represents a single haplotype, each line connecting the dots a one-base-pair difference. The sizes of the dots correspond to the number of individuals revealing the particular haplotype Page 7 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

traits that must be observed to enable identification depends on the degree of polymorphism that is recorded for the observed traits. Most common for identification purposes in the context of, e.g., the reconstruction of genealogical kinship are so-called short tandem repeats (STRs). These markers reveal a comparatively high degree of polymorphism: on average 5–15 alleles of varying lengths are present in a population for each STR. These markers are also suitable for population genetic purposes, although data from many individuals are necessary in order to enable conclusions with respect to phylogeny and migration. Another target are single nucleotide polymorphisms (SNPs), which are usually biallelic markers revealing a sequence polymorphism at a certain nucleotide position. Unlike STRs, they are not investigated to reconstruct kinship, although this would be possible in principle, but in order to determine, e.g., the immunological properties of an individual. Since the immunological properties of a population are subject to strong selective forces, due to the presence of pathogens influencing morbidity and mortality rates, regional and/or diachronic changes in the allelic frequencies of SNPs allow us to draw conclusions on subjects such as the spread of epidemics or pandemics and everyday living conditions. In ancient DNA analysis, the accessibility of chromosomal markers is restricted, because of the comparatively low numbers of genomes originally present in a given sample volume. However, optimizations of DNA extraction protocols may compensate for this disadvantage. Once nDNA has been successfully extracted, the analysis of nuclear markers is much less prone to erroneous results due to contamination, given a careful experimental design. Inheritance of the Chromosomal Genome The chromosomal genome of an individual represents a novel and unique recombination of its parental organisms. Both parents contribute a so-called haploid set of chromosomes, which are randomly selected from their own diploid chromosomal sets. Therefore, each locus under investigation reveals a maternal and a paternal allele. In the analysis of coding regions, the genotypic level may often be determined without difficulties, but this does not necessarily hold true for the phenotypic level. Gene expression and suppression must be known in order to allow conclusions to be drawn from the genotype of an individual to its phenotype. In ancient DNA analysis, a particular situation that is suspected to be involved in many diseases remains a challenge: the phenomenon of compound heterozygosity. Compound heterozygosity describes a situation where two (or more) mutations, distant from each other on the same chromosome and responsible for a certain morbidity risk, have to be present in a heterozygous state, but one mutation must be located on the maternal, the other on the paternal allele. In ancient DNA with its highly fragmented target sequences, compound heterozygosity cannot be discriminated from a heterozygous state where both markers are mutated either on the maternal or the paternal allele. Length Polymorphisms and Sequence Polymorphisms Chromosomal DNA consists of coding and noncoding sequences. From the Human Genome Project it is known that the bulk of DNA is noncoding DNA, sometimes called junk DNA. About 20–30 % of this noncoding DNA consists of tandem repeated sequences. Some of them, the STRs (cf. above), are particularly interesting, since a set of them enables the genetic identification of an individual. Their alleles reveal a length polymorphism which is a function of the number of repetitions of the core unit. In fact, STRs are often identical (e.g., CAn or AGATn), but the unique nature of the neighboring sequences enables us to specifically target a certain STR locus. Other than sequence polymorphisms, the variations in fragment length are not suspected to suffer from specific DNA degradation leading to a result that, although reproducible, is still erroneous. However, ancient DNA Page 8 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

analysis must be carried out carefully, because STR amplifications also reveal typical so-called stutter artifacts. Since stutter bands occur stochastically, the artifact can be overcome through multiple analyses. Further, the occurrence of this typical artifact can be minimized through optimization of DNA extraction and a sophisticated choice of PCR parameters. Multiple analyses also prevent erroneous homozygous results, which may occur due to so-called allelic dropout when only a small number of intact target sequences are present. The analysis in ancient DNA of SNPs, which are spread throughout the genome, basically has to deal with the same pitfalls that are suspected to affect the analysis of mitochondrial sequence polymorphisms. Although the risk of non-authentic results due to contamination is much lower than in the analysis of mtDNA and, moreover, can efficiently be monitored through suitable experimental design, the risk of false results due to specific degradation patterns must be considered in the same way as in mtDNA analysis. Genetic Fingerprints and Identification The specific allele combinations from analysis sets consisting of 5–15 STRs are also known as genetic fingerprints. As the name implies, the specific allele combinations have an identifying character. Genetic fingerprints are suitable for genealogical kinship reconstruction and for the identification and the assignment of skeletal elements. In order to be suitable for genetic fingerprinting, the STRs combined in a set have to fulfill two major prerequisites: first, they must be located on different chromosomes in order to avoid haplotypes and to ensure a recombinant mode of inheritance. Second, they must not be linked to genes, in order to avoid the force of possible selective pressure, which would be indicated by strong deviations from a Gaussian allele distribution. If these criteria are fulfilled, the degree to which the value of the so-called matching probability (Pm) can be determined depends on the total number of STRs investigated and on their respective allele frequencies in a given population. The Pm is defined as the likelihood that a second, nonrelated individual reveals the respective allele combination just by chance. Typical Pm values for commercially available and customer-designed sets consisting of 9–15 STRs range from 10
10 to 10
24. Of course, these impressive values apply to ideal populations only (panmictic, no selective pressure, etc.). However, the situation in real, possibly even inbred, populations can be simulated approximately when calculating the likelihood that a given set of parents will give birth to two children revealing the same genetic fingerprint. If 10 STRs are observed, the likelihood of this event ranges from 10
5 to 10
7. These values indicate that individuals from an inbred population with a limited gene pool are still sufficiently discriminated. The identifying properties of genetic fingerprints also indicate that STR typing is more suitable than any other strategy to the identification of possible contaminations from a wide spectrum of sources. Reconstructing Kinship and Paternity Testing The reconstruction of kinship in a (pre-)historic skeletal series requires a different strategy than if it were a living population. Whereas in a living population, the ages of the individuals help to discriminate a priori the parental generation from the potential descendants, this information is not available in a skeletal series. It is theoretically possible to find the skeletal remains of an individual who died in early adulthood but who fathered an individual who reached the senile age class. Although individuals who are related vertically at first degree share an allele for each observed genetic marker, it is not feasible to deduce from genetic markers who is the parent and who is the offspring. Therefore, infant individuals who have not reached reproductive age play a key role in the reconstruction of kinship (Fig. 3). Page 9 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

b

a Individual A

c

Individual A 10/12

STR 1

11/14

STR 2

27/30

STR 2

29/33

STR 3

6/9

STR 3

7/8

mt H

Y1

mt J

---

Individual ? STR 1 11/?

STR 1

10/12

STR 2

27/30

STR 2 29/?

STR 3

6/9

STR 3 8/?

mt H

Y1

mt J

?

Individual C

STR 1

---

adult

adult

matur

Individual B STR 1 10/11 STR 2 29/30 infans 2

STR 3 8/9 mt J

infans2

Y1 Individual B STR 1 10/11 STR 2 29/30 STR 3 8/9 mt J

Y1

Fig. 3 If two individuals are found to share an allele for each STR system (¼STR 1, STR 2, and STR 3), they may be parent and child. (a) From the STR typing and the Y-Haplotype (¼Y1), it cannot yet be deduced who is the father and who is the son. (b) A morphological or histological age determination not only solves this problem but, moreover, enables us to predict the genotype of the mother, who is still missing. (c) If a female individual is found who reveals the respective STR alleles as well as the appropriate mitochondrial haplotype (¼mt J), she can be assumed to be the mother. The likelihood of parentage can now be calculated based on the allele frequencies of the investigated STRs

If two individuals – infant and adult – are found to share exactly one allele at each observed locus, a paternity (or maternity) test can be constructed as a deficiency case (i.e., one parent missing). If the allelic genotype of a second adult individual of the opposite sex suggests that this may be the missing parent, the likelihood of parentage for both assumed parents is calculated in the manner of two independent trio cases (Brenner and Morris 1990; Chakraborty and Jin 1993). This means that, e.g., in a first step the child-mother dyad is taken as fixed, enabling us to calculate the paternity index for the male individual, and then, in an analogous way, the maternity index is calculated. In particular, if individuals from a larger burial site are investigated with respect to their genealogical relatedness, the initial search for possible child-parent dyads is facilitated by mitochondrial and Y-chromosomal haplotyping. This strategy permits the assignment of individuals to family lineages. Analogous to autosomal genetic fingerprinting, Y-haplotyping is carried out through STR allele amplifications at the Y-chromosome. Immunogenetics and Epidemiology: Towards Phenotype The analysis of nuclear genetic markers that are known to be linked to the immunological properties of an individual is comparatively new. Usually these properties are represented through SNPs, which cause changes in the amino acid chain, thereby changing protein synthesis. Many of these markers are directly linked to the susceptibility of an individual to bacterial and viral infections and, as

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

a consequence, to his or her susceptibility to certain cancerous growths. These markers are also of interest in the context of heterogeneous reactions of individuals to pharmacological treatments. The allele frequencies of such markers exhibit considerable deviations worldwide, suggesting that they are subject to selective pressures, as well as genetic drift and bottleneck situations. It is striking that particular European populations or individuals of European descent often reveal allele distributions that deviate strongly from all other human populations worldwide. Not surprisingly, this is interpreted as a result of Europe’s unique epidemiological history during the past centuries, and to the selective forces that are linked to epidemic and pandemic infectious disease events (Scott and Duncan 2001). Many theories and hypotheses that claim to be able to name a particular historic epidemic event bearing responsibility for a certain uncommon allelic distribution are based on more or less thorough linkage studies carried out on modern populations (Stephens et al. 1998; Rannala and Bertorelle 2001). However, some must be classified as mere speculations (Altschuler 2000). In any case, all such studies lack direct proof. Therefore, direct access to historic and prehistoric genotypes will be invaluable. In particular, skeletal series that are known to be linked to epidemics or pandemics can play an important role as genetic archives. However, since the burial sites of skeletal series are often mass graves (e.g., of plague victims), the significant possibility of ancient cross-contaminations due to the special conditions of burials must be borne in mind when setting up the experimental design.

Authenticity The authenticity of a PCR-based ancient DNA analysis result must be tested in two ways: first, one must exclude the possibility that contamination is responsible for the outcome of the analysis; and second, it must be proved that the result indeed represents the authentic genotype of the (pre-)historic individual sampled, and is not biased due to DNA degradation or analytic artifacts. Depending on the scientific question, the actual sequence that is under investigation, the number of individuals investigated, and, finally, the origin of the samples, proving the authenticity of ancient DNA analysis results may require unique experimental design strategies. A comparison of PCR with NGS technology suggests that proofs of authenticity may be much more easily brought about for the latter, since NGS technology is not based on exponential amplification. However, if contaminating sequences are of the same species and outnumber the endogenous sequences of the investigated sample, the common strategy to identify contaminating sequences by their minor number is prone to fail with NGS as well.

Contaminations Since ancient samples usually consist of very few DNA targets, even minor contaminations may cause false results, at least in PCR-based analyses. Contaminations may originate from various sources and may reveal various degrees of degradation. Therefore, there is no simple strategy for how to avoid and detect them. Basically, we can distinguish four ways in which contaminations may enter the analysis: • • • •

Cross-contamination between the ancient sample materials Contaminations of the sample material by former or current investigators Contaminations in laboratory reagents and disposable material Contaminations of either sample materials or reagents by amplification product carryover from earlier PCR analyses Page 11 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

Cross-Contamination Cross-contamination of the sample material may in principle happen at any time. However, two situations in particular are suspected to increase the risk of sample cross-contamination: burials at a non-individual site (e.g., mass graves) and the laboratory processing of the samples (e.g., transfer of sample material through unclean laboratory devices or handling mistakes). Cross-contaminations are particularly hard to detect, since all sequences involved would reveal a degradation pattern as expected for ancient DNA. Further, their occurrence cannot be detected through use of the classical set of negative control samples, which includes no-template controls and extraction blanks. A possible cross-contamination event must therefore be detectable in the analysis result itself, as would be the case, for example, if amplification of DNA fragments showed up three or four alleles instead of one or two, clearly indicate the presence of material from a second individual. Contamination by Investigators This type of contamination may in principle happen anytime a sample is handled. What the contamination pattern looks like depends on the amount of contaminating cells and on whether the contamination happened recently or decades ago. It may vary from comparatively easily identified, fully intact DNA profiles to a hard-to-recognize type which resembles the typical cross-contamination. As in the case of cross-contaminations, negative control sample sets are not suitable for monitoring this type of contamination. Again, the analysis result itself must reveal indications of the problem. Unlike the case of a classical cross-contamination, contamination by an investigator is most likely (but not necessarily) a superficial one. Therefore, thorough removal of the sample surfaces minimizes the risk of this contamination type. This applies to both PCR-based analyses and NGS-based analyses. Contaminations in Laboratory Reagents and Disposables Laboratory reagents may already be contaminated when purchased (e.g., primers, reaction mixes), or they may become contaminated through handling by the investigators. In both cases, the degradation patterns of the contaminating DNA and the amount of contamination may vary strongly. If premixed PCR reaction components are used, particularly bovine serum albumine (BSA), which is a component enhancing the Taq DNA polymerase, may cause severe problems, due to residues of bovine DNA. This can be shown through cytochrome b sequence amplifications that indicate the species. However, this type of contamination can be monitored through suitable sets of negative controls. Ideally, the analysis result from the sample material itself will also provide information indicating possible contaminations. The situation is completely different where disposable laboratory materials are concerned. PCR reaction tubes turn out to be regularly contaminated right from the production process, with human DNA prevailing (Hauswirth 1994; Schmidt et al. 1995, Gill et al. 2010), although DNA of bovine origin has also been found (Hummel 2003a). The percentage of reaction tubes that suffer from contamination varies depending on the supplier, the brand, and the actual lot. The vast majority of these contaminations are of mitochondrial origin. The reason for this lies in the nature of the production process, which very often includes autoclaving steps. If there are just a few reaction tubes containing cellular contaminations at this stage of the manufacturing process, these cells will become lysated by the autoclaving temperature and, as a result, hundreds of thousands of mitochondrial genomes are distributed more or less uniformly. Typically, the number of tubes that show specific signals of mtDNA after 40 amplification cycles varies between 20 % and 80 % if fragments of less than about 150 bp are amplified. The reason why autoclaving is still part of the manufacturing process, even in so-called high-performance (e.g., “PCR clean,” “DNA free”) and high-price brands, Page 12 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

is that this allows producers to guarantee that they are staying below a certificated level of DNA for each tube in the lot, without having to invest in the cost of a truly DNA-free manufacturing process. All kinds of treatments applied to amplification reaction tubes (e.g., UV treatment, bleaching, rinsing with and without ultrasonic treatment) are inefficient in the sense that they cannot overcome the problem. At best, a more or less sizable reduction in the number of tubes revealing contaminations can be achieved. Since the contaminating mtDNA in reaction tubes consists of just a few targets per tube, and because it is typically just as degraded as ancient DNA, it is usually not even noticed in modern DNA applications. For ancient mtDNA applications, however, which may also start from just a few intact targets, it is the most severe contamination problem of all, since it is unavoidable and may be hard to detect. Typical sets of two or three negative controls in a PCR set-up are uninformative, simply due to their small number. If they stay blank, this is not necessarily representative of the tubes in which the samples were processed. Then again, if the negative controls do reveal signals, these cannot either be assumed to apply to the tubes in which the samples were analyzed. A way to improve the situation in mtDNA analysis is through numerous reproductions of the analysis, ideally amplifying only fragment lengths considerably greater than 200 bp. In order not to have to discard too many analysis results which reveal ambiguous signal patterns and are suspected of deriving from a mixture of precontaminating tube DNA and ancient sample DNA, researchers are advised to carry out checks with at least 30 negative controls each time a new lot of reaction tubes is in use. Further, depending on the target sequence and the number of samples intended to be analyzed, it may be preferable to choose a NGS-based approach for the analysis of mitochondrial genomes. Another option, although extremely laborious and inconvenient, is the use of glass tubes for PCR amplifications, manufactured from high-temperature-resistant glass. These can be reused after being tempered for a couple of hours at 600  C at least. It may be necessary to elongate the steps of the amplification cycle for efficient reactions carried out in glass tubes; however, if tempering has been done these reactions will be positively free of contamination. Contamination Through Product Carryover from Earlier PCR Product carryover, although a disaster if it occurs, is not a particular threat to ancient DNA analysis. This is because it is comparatively easy to detect and easy to prevent if some basic rules are strictly followed. Product carryover would block the easy and low-cycle amplificability of a certain marker, while other markers of similar fragment length would not yet be amplifiable. Also, as long as more than a single sample is contaminated (which is extremely likely in the case of product carryover), a series of samples would reveal identical analysis results if, e.g., an extraction buffer was contaminated. If product carryover found its way into a PCR reagent, the entire set of negative controls would all show signals, thus reacting in exactly the same way the samples do. A method to efficiently prevent product carryover contaminations, which is practiced in almost every ancient DNA laboratory, is the strict separation of pre- and post-PCR areas, including strict dedication of all equipment, such as pipettes, centrifuges, deep freezers, and so on.

Degradation and Analysis Artifacts Ancient DNA results may also be non-authentic due to degradation and analysis artifacts. That is to say, even though it was the authentic ancient DNA that was analyzed, the original sequential order of bases or the original fragment lengths may have been biased. If one counted up the number of publications that report degradation phenomena, one might believe that non-authenticity due to degradation artifacts is a critical point almost exclusively with respect to the base sequence, rather Page 13 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

than fragment length (Gilbert et al. 2003; Binladen et al. 2006). This reporting pattern, however, most likely reflects a bias as well, since only very few ancient DNA working groups have longstanding experience with fragment length analysis, which is mainly linked to autosomal and Y-chromosomal STR typing (Keyser-Tracqui et al. 2003; Hummel et al. 2000; Hummel 2003a). The bulk of the discussion of typical fragment length artifacts is taking place in the forensic sciences context, where STR typing of degraded DNA samples has been routine for many years (Butler 2005). Non-authenticity of the Base Sequence Base degradation is one of the major reasons why the analysis even of authentic ancient DNA may nevertheless reveal erroneous results. The most numerously occurring artifacts are reported to be the transition C > T/G > A and A > G/T > C; others have been observed much more rarely or not at all (C > G/G > C), at least not in nDNA (Binladen et al. 2006). Another important aspect is the question of whether mtDNA and nDNA are affected to the same extent in this. Although nDNA is thought less likely to suffer from degradation artifacts, owing to the protection the nucleic acid sequence receives from histones, an investigation by Binladen et al. (2006) could not detect major differences. Due to its obvious relevance, the C > T transition is most often discussed with respect to the cause of the artifact (cytosine may degrade to an apparent uracil, of which the complementary base is an adenine, which in turn would lead to the introduction of a thymine during the next elongation phase), its likelihood of occurrence, and available methods to overcome the artifact. One common strategy to prevent the amplification of DNA fragments containing apparent uracils is an enzymatic treatment of the DNA extract prior to amplification (Haak et al. 2005). This strategy claims to destroy all DNA fragments that contain uracil-like degraded cytosines – but it may result in total destruction of all potential target DNA sequences for the intended amplification. Further, transitions others than the C > T transition are not affected by this approach. Therefore, other strategies to overcome generation of non-authentic PCR-based results due to DNA degradation would be preferable, if available. These could be valid strategies for DNA repair or unbalanced initial PCR employing a single primer that results in a linear amplification of one strand only. Furthermore, in cases where the sample itself does not represent a mixture of DNA from different individuals, a combination of cloning strategies – which often suffer from too few clones being analyzed (Bower et al. 2005) – and direct sequencing could be informative. Another way to monitor and evaluate analysis results that are suspected to be biased by degradation artifacts could be the implementation of cross-checks through amplification of further loci which basically provide the same information, or at least parts of this information. In the case of mtDNA haplotyping, a suitable option might be the analysis of SNP markers on the mtDNA genome, which are known to be linked to haplogroups (Torroni et al. 1992). In the case of nuclear SNPs, the targeted loci for cross-checks might be additional polymorphic sites which are also known to be linked to certain genes, although possibly with a lower linkage rate. Non-authenticity of Fragment Lengths Typical fragment length artifacts are so-called stutter bands and allelic dropout. Both of these kinds of artifacts, which occur in the course of STR amplifications, are well known and extensively discussed in the ancient DNA and forensic literature (Butler 2005; Hummel 2003a). Unlike sequence degradation, allelic dropout and stutter artifacts are not a direct degradation phenomenon but rather an indirect one, since the likelihood that they prevail in the data, leading to an inaccurate analysis, depends on the number of intact targets that are submitted to amplification. Although a reduced number of intact targets is characteristic for ancient DNA extracts, these artifacts can occur Page 14 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

during amplification of modern intact DNA as well, if there are few targets throughout the first amplification cycles. But even when very few targets are submitted to the reaction, the generation of fragment length artifacts constitutes a stochastic event that is – except in the case of base degradation – not due to alterations of the target but an amplification artifact. Consequently, mere multiple repetition of the analysis will allow the experimenter to evaluate the authenticity of a result, on the basis of reproducibility. Moreover, strategies are available to lower the tendency of the amplification reaction to create these types of artifacts. The most obvious one is to optimize the DNA extraction, in order to increase the number of targets. This helps in particular to avoid allelic dropout. In order to minimize the generation of stutter bands, relaxation of the elongation temperature has proved to be successful. However, since Taq DNA polymerase activity is damped down by a lowering of the temperature, the time allowed for elongation should be correspondingly prolonged. In any case, the fact that STR amplifications are regularly carried out in multiplex approaches means that cross-checks are already built into the analysis, since the evaluation of authenticity is clearly simplified when based on the patterns of the entire set of amplified loci (Fig. 4).

Chromosomal STRs “Genetic fingerprints”

mtDNA cytochrome B 1

1

2

2

3

3

W

W chromosomal SNPs

Y-chromosomal STRs W

1 mtDNA HVRs

2 3

1

1 2 3

2 W

W 3 W

Fig. 4 Authentification power of genetic fingerprinting. The analysis strategy should consider the number of individuals that are being investigated, the number of people who worked on the sample material, and the underlying scientific question, including the sequence of interest, as shown in this example. Given that three skeletons (1–3) are being investigated and one person (W) is working on the samples, the analysis of different genetic markers may potentially have different results, therefore requiring different sets of control samples and cross-experiments. If, for example, a cytochrome b fragment is amplified, all samples, including ones from W, would reveal the same base sequence, and there would be no proof that W did not contaminate the samples. If a nuclear SNP is investigated, e.g., samples 1 and 2 may be homozygous, but sample 3 and W heterozygous. Again, the results do not exclude the possibility that samples 1 and 2 are cross-contaminated, or that W may have contaminated sample 3. The same may hold true for the investigation of mitochondrial HVRs. In the given example, analysis of the Y-chromosomal haplotypes can exclude cross-contamination between samples 1 and 2. However, only the investigation of autosomal STRs that represent individual genetic fingerprints enables us to prove that no contamination events are responsible for the ancient DNA results. While in all analyses except genetic fingerprinting, even extended sets of negative controls are not able to rule out direct contamination of sample 3 by W, autosomal STR typing would not even need a negative control to exclude contamination events such as carryover, contamination through laboratory personnel, and cross-contamination Page 15 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

Basic Strategies in Experimental Design There is no general strategy for how to carry out an ancient DNA analysis; the most decisive factors for the experimental set-up are the sample material itself, the underlying scientific question, and the properties of the DNA sequence in focus. These factors should be considered in making decisions on the need for pre-experiments (e.g., checks for contamination rates in amplification tubes), the choice of appropriate sets of negative and positive controls, and the design of the amplification and analysis strategy. The final experimental strategy ideally combines two aims: maximizing the likelihood of a result, and maximizing the likelihood that this result can positively be proved to be authentic (Fig. 4). Authentic results are achieved through entirely different strategies depending on, for example, whether human or animal DNA is under investigation, whether a single sample or series of samples are analyzed, whether mitochondrial or nDNA is the target, and whether base sequences or fragment lengths carry the desired information. It is unhelpful, therefore, to focus overly on abstract criteria for ancient DNA analysis per se, such as have been proposed in the past (Cooper and Poinar 2000). These broad criteria do not refer to any specifics of the research context; an experimental design following these published regulations would only directly meet the demands of the analysis of human mitochondrial HVR DNA from a single sample. But even for that particular scenario, observance of these standard criteria and regulations would not, in itself, result in full proof of authenticity, since crosscontaminations and contaminations by earlier investigators could never be ruled out.

Sample Preparation The preparation of ancient DNA samples has to be devoted to two main objectives: • Removal of possible contaminations • Optimal preparation of the sample for DNA extraction and further amplification reactions in subsequent analytic procedures Where superficial contaminations are concerned – i.e., most commonly, contaminations by present or former investigators – the first objective is achieved by thoroughly removing the surface of the sample. Further possible contaminations may also be removed by rinsing the sample surface with a strong oxidative reagent such as, e.g., household bleach. How the second objective is achieved depends on the sample material. However, in general, any increase in surface area through, e.g., crushing of the sample prior to chemical treatment has proven to improve later analysis results. Further, depending on the actually chosen extraction technique, factors such as centrifugation forces and the relation of the sample material to incubation buffers and reagents are also crucial. We recommend the development of a standard protocol with respect to given sample properties before valuable sample material is processed.

Optimizing DNA Extraction Optimal DNA extraction protocols are obviously a highly individual matter, dependent as they are on the exact biochemical state and composition of the sample material. However, standard protocols offer a valuable starting point. The basic aims of standard protocols are: • Maximization of the amount of DNA • Minimization of DNA degradation in the course of the extraction procedure • Minimization of the presence of inhibiting substance residues in the DNA extract Page 16 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

At present, these goals seem best achieved through automated DNA extraction using magnetic beads, although the amount of DNA in the extracts lags somewhat behind what, e.g., phenolchloroform procedures will accomplish. However, the advantage of the DNA extracts being practically free of inhibitors, as can be demonstrated through real-time PCR, may outbalance the possible loss of DNA. In case the sample material consists of very little intact target DNA and only minor amounts of inhibiting components, other strategies – such as retention of the DNA on silicacoated membranes – may be superior with respect to optimum DNA yield. In general, the use of any type of automation at this stage of sample processing is advantageous, since it minimizes the handling of the samples and thus the risk of contamination.

Amplification Strategies In general, there is no optimal amplification strategy; instead, the basic experimental design must be deduced from the scientific question and the sequence of interest (Fig. 4). However, there are some key aspects which should be considered. First, the more the investigated sequence is characterized by polymorphisms, the fewer crosschecking experiments are necessary. Ideally, the amplification result will be “individual,” in the sense of identifying a unique individual, since this enables an efficient check for any type of possible contamination. If, for example, nuclear STR typing is carried out, only a minimum of negative controls are necessary. It may be advisable to deviate from classical amplification parameters, in particular concerning the elongation temperature. A decrease in the elongation temperature, or a shift to a two-step PCR consisting of a denaturing phase and a prolonged annealing phase only, may result in a remarkable decrease in stutter bands, which are an STR-specific amplification artifact encountered even in modern DNA amplifications (cf. above). Second, in case the markers of interest are polymorphic but far from revealing results specific to an individual – as would hold for any type of biallelic SNPs or short deletions – the aim should be to link the analytic result to another, identifying one. This is realized through integration of the primers for, e.g., the SNP amplification to a multiplex assay designed for STR-based genetic fingerprinting. This approach has proved successful for nuclear markers (Bramanti et al. 2000; Fulge 2005; Hummel et al. 2005; Puder 2005), although it may require multistage fragment-length determinations, including a restriction fragment length polymorphism (RFLP) analysis. If the biallelic markers are multiplexed with nuclear STRs, only a minimum set of negative controls is necessary. Third, the amplification of mtDNA, which is regularly represented in ancient DNA extracts by a greater number of intact targets, is hard to carry out using the same technique as for the amplification of nDNA. One reason lies in the different demands for optimal amplification cycles. Moreover, the aim of mtDNA investigations is usually a sequence analysis, which, for technical reasons, cannot be combined with STR typing. We highly recommend re-checks of contamination rates for different brands of amplification tubes. These should be carried out with the primers that are intended for the actual investigation, using high cycle numbers (>45). If possible, the primers should reveal sensible mismatches against species that are not intended to be amplified but are suspected to be present as contaminating targets (humans, working animals). It may be necessary to launch experiments that check sequence-specific degradation patterns. Although mtDNA is regularly represented by more targets than chromosomal DNA in an ancient DNA extract, the particulars of the situation with respect to degradation pattern and contaminations in amplification tubes will significantly complicate the proof of authenticity. Due to these facts and the non-individual character of the polymorphisms, even in the HVRs of mtDNA well-adapted sets of control samples are necessary, since typical sets of negative controls do not apply.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

Enhancing Specificity and Sensitivity of a PCR The specificity of a PCR, i.e., the exclusive amplification of the targeted sequence, is a basic prerequisite for success, in particular if the subsequent analysis includes a so-called Taq cycle sequencing reaction. PCR specificity can be challenging to achieve. However, any other type of ancient DNA analysis also suffers from the generation of unspecific by-products. This holds true even if no confusion with the target sequences is possible, due to, e.g., entirely different fragment lengths. The reason is that sensitivity decreases as soon as by-products, including primer dimers, are generated in the amplification reaction, since the resources for the reaction (Taq polymerase activity, primers, dNTPs, and buffer) may be exhausted sooner in this competitive situation. The consequence is that the target product, though present, may not reach the detection limit, because the by-reaction has already led to attainment of the amplification plateau. Although optimization of the annealing temperature positively influences the specificity of the amplification reaction, even this step may not result in a highly specific reaction, or may compromise the reaction efficiency, if the annealing temperature approaches the melting temperature of the primers. A particularly effective means to increase the specificity and therefore the sensitivity of the reaction is given through primer design. The criteria for a good primer design can be summarized as follows. • Primers should reveal a minimum length of 20 bp if possible, preferably 23–30 bp. • The binding energy of the 50 -end must increase that of the 30 -end in order to enable elongation only if the entire primer matches. • 30 -end primer dimers and hairpin formation must be strictly avoided, since these formations will be elongated and cause generation of by-products. • Primers should not reveal possible mismatches to the intended target caused by sequence polymorphism within at least 3 bp from the 30 -end. If a primer pair meets these criteria, the amplification product increases considerably in quality and quantity. Further improvement in reaction efficiency can then be achieved through a step-wise decrease of the annealing temperature. Especially if only a very few intact DNA targets have been extracted from the sample material, this measure is likely to constitute the difference between an amplification failure, on the one hand, and a weak amplification product ready for further analysis, on the other.

Conclusion Over the last two decades ancient DNA analysis has evolved from an enthusiastically publicized yet controversial technique revealing some spectacular results to a sound practice generating biological data that help explain the past. For quite some time this positive development was not foreseeable, because the high sensitivity of the PCR technique is both its greatest advantage and its most significant drawback. The discussion was dominated by the question how to fully authenticate PCR results and how to optimize experimental strategies. We are now witnessing the early stages of the development of Next Generation Sequencing (NGS) approaches, which give access to entire genome information. The coming years will prove how well these very promising alternatives to PCR will come through their own teething troubles.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

Cross-References ▶ Genetics and Paleoanthropology ▶ Historical Overview of Paleoanthropological Research ▶ Investigation on Extracellular Matrix Proteins in Fossil Bone: Facts and Perspectives ▶ Molecular Evidence of Primate Origins and Evolution ▶ Neanderthals and Their Contemporaries ▶ Origin of Modern Humans ▶ Paleoecology: An Adequate Window on the Past? ▶ Phylogenetic Relationships (Biomolecules) ▶ Population Biology and Population Genetics of Pleistocene Hominins ▶ Prospects and Pitfalls ▶ The Evolution of Speech and Language

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Krause J, Fu Q, Good JM, Viola B, Shunkov MV, Derevianko AP, Pääbo S (2010a) The complete mitochondrial DNA genome of an unknown hominin from southern Siberia. Nature 464:894–897 Krause J, Briggs AW, Kircher M, Maricic T, Zwyns N, Derevianko A, Pääbo S (2010b) A complete mtDNA genome of an early modern human from Kostenki, Russia. Curr Biol 20:231–236 Krings M, Stone A, Schmitz RW, Krainitzki H, Stoneking M, Pääbo S (1997) Neanderthal DNA sequences and the origin of modern humans. Cell 90:19–30 Krings M, Capelli C, Tschentscher F, Geisert H, Meyer S, von Haeseler A, Grossschmidt K, Possnert G, Paunovic M, Paabo S (2000) A view of Neandertal genetic diversity. Nat Genet 26:144–146 Lalueza-Fox C, Krause J, Caramelli D, Catalano G, Milani L, Sampietro ML, Calafell F, MartínezMaza C, Bastir M, García-Tabernero A, De la Rasilla M, Fortea J, Pääbo S, Bertranpetit J, Rosas A (2006) Mitochondrial DNA of an Iberian Neandertal suggests a population affinity with other European Neandertals. Curr Biol 16:R629–R630 Leiva IM, Emmert-Buck MR, Gillespie JW (2003) Handling of clinical tissue specimens for molecular profiling studies. Curr Issues Mol Biol 5:27–35 Lindahl T (1993) Instability and decay of the primary structure of DNA. Nature 362:709–715 Malik S, Sudoyo H, Pramoonjago P, Suryadi H, Sukarna T, Njunting M, Sahiratmadja E, Marzuki S (2002) Nuclear mitochondrial interplay in the modulation of the homopolymeric tract length heteroplasmy in the control (D-loop) region of the mitochondrial DNA. Hum Genet 110:402–411 Mariappan MR, Zehnder J, Arber DA, Lay M, Fadare O, Schrijver I (2005) Identification of mislabeled specimen by molecular methods: case report and review. Int J Surg Pathol 13:253–258 Miraglia M, Berdal KG, Brera C, Corbisier P, Holst-Jensen A, Kok EJ, Marvin HJ, Schimmel H, Rentsch J, van Rie JP, Zagon J (2004) Detection and traceability of genetically modified organisms in the food production chain. Food Chem Toxicol 42:1157–1180 Noonan JP, Coop G, Kudaravalli S, Smith D, Krause J, Alessi J, Chen F, Platt D, Pääbo S, Pritchard JK, Rubin EM (2006) Sequencing and analysis of Neanderthal genomic DNA. Science 314:1113–1118 Oppenheimer S (2012) Out-of-Africa, the peopling of continents and islands: tracing uniparental gene trees across the map. Phil Trans R Soc B 367:770–784 Orlando L, Darlu P, Toussaint M, Bonjean D, Otte M, Hänni C (2006) Revisiting Neandertal diversity with a 100000 year old mtDNA sequence. Curr Biol 16:R400–R402 Ottoni C, Koon HE, Collins MJ, Penkman K, Rickards O, Craig OE (2009) Preservation of ancient DNA in thermally damaged archaeological bone. Naturwissenschaften 96:267–278 Ovchinnikov IV, Gotherstrom A, Romanova GP, Kharitonov VM, Liden K, Goodwin W (2000) Molecular analysis of Neanderthal DNA from the northern Caucasus. Nature 404:490–493 € Pääbo S (1984) Uber den Nachweis von DNA in altägyptischen Mumien. Das Altertum 30:213–218 Paik S, Kim CY, Song YK, Kim WS (2005) Technology insight: application of molecular techniques to formalin-fixed paraffin-embedded tissues from breast cancer. Nat Clin Pract Oncol 2:246–254 Pakendorf B, Stoneking M (2005) Mitochondrial DNA and human evolution. Annu Rev Genomics Hum Genet 6:165–183 Puder Y (2005) Molekulargenetische Identifikation der Allelhäufigkeit eines immungenetischen Markers der IL16-Promotorregion bei bronzezeitlichen Individuen aus Mitteleuropa. Diplomarbeit, Göttingen Rannala B, Bertorelle G (2001) Using linked markers to infer the age of a mutation. Hum Mutat 18:87–100 Richards MB, Macaulay VA, Bandelt H-J, Sykes BC (1998) Phylogeography of mitochondrial DNA in western Europe. Ann Hum Genet 62:241–260 Page 22 of 24

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Rizzi E, Lari M, Gigli E, De Bellis G, Caramelli D (2012) Ancient DNA studies: new perspectives on old samples. Genet Sel Evol 44:21 Rowold DJ, Herrera RJ (2005) On human STR sub-population structure. Forensic Sci Int 151:59–69 Saiki RK, Scharf S, Faloona F, Mullis KB, Horn GT, Erlich HA, Arnheim N (1985) Enzymatic amplification of P-globulin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science 230:1350–1354 Schmidt T, Hummel S, Herrmann B (1995) Evidence of contamination in PCR laboratory disposables. Naturwissenschaften 82:423–431 Scott S, Duncan CJ (2001) Biology of plagues: evidence from historical populations. Cambridge University Press, Cambridge/New York Sipoli Marques MA, Pinto Damasceno LM, Gualberto Pereira HM, Caldeira CM, Pereira Dias BF, de Giacomo Vargens D, Amoedo ND, Volkweis RO, Volkweis Viana RO, Rumjanek FD, Aquino Neto FR (2005) DNA typing: an accessory evidence in doping control. J Forensic Sci 50:587–592 Soares P, Achilli A, Semino O, Davies W, Macaulay V, Bandelt HJ, Torroni A, Richards MB (2010) The archaeogenetics of Europe. Curr Biol 20:174–183 Sosa C, Vispe E, Núñez C, Baeta M, Casalod Y, Bolea M, Hedges RE, Martinez-Jarreta B (2013) Association between ancient bone preservation and DNA yield: a multidisciplinary approach. Am J Phys Anthropol 151:102–109 Stephens JC, Reich DE, Goldstein DB, Shin HD, Smith MW, Carrington M, Winkler C, Huttley GA, Allikmets R, Schriml L, Gerrard B, Malasky M, Ramos MD, Morlot S, Tzetis M, Oddoux C, di Giovine FS, Nasioulas G, Chandler D, Aseev M, Hanson M, Kalaydjieva L, Glavac D, Gasparini P, Kanavakis E, Claustres M, Kambouris M, Ostrer H, Duff G, Baranov V, Sibul H, Metspalu A, Goldman D, Martin M, Duffy D, Schmidtke J, Estivill X, O’Brien S, Dean M (1998) Dating the origin of the CCR5-d32 AIDS-resistance allele by the coalescence of haplotypes. Am J Hum Genet 62:1507–1515 Tamaki K, Jeffreys AJ (2005) Human tandem repeat sequences in forensic DNA typing. Leg Med 7:244–250 Teletchea F, Laudet V, Hänni C (2005) Food and forensic molecular identification: update and challenges. Trends Biotechnol 23:359–366 Torroni A, Schurr TG, Yang CC, Szathmary EJ, Williams RC, Schanfield MS, Troup GA, Knowler WC, Lawrence DN, Weiss KM, Wallace DC (1992) Native American mitochondrial DNA analysis indicates that the Amerind and the Nadene populations were founded by two independent migrations. Genetics 130:153–162 Torroni A, Schurr TG, Cabell MF, Brown MD, Neel JV, Larsen M, Smith DG et al (1993) Asian affinities and continental radiation of the four founding Native American mtDNAs. Am J Hum Genet 53:563–590 Valenstein PN, Sirota RL (2004) Identification errors in pathology and laboratory medicine. Clin Lab Med 24:979–996 Wall JD, Kim SK (2007) Inconsistencies in Neanderthal genomic DNA sequences. PLoS Genet 3:1862–1866 Watson E, Forster P, Richards M, Bandelt H-J (1997) Mitochondrial footprints of human expansions in Africa. Am J Hum Genet 61:691–704 Zink AR, Reischl U, Wolf H, Nerlich AG (2002) Molecular analysis of ancient microbial infections. FEMS Microbiol Lett 213:141–147

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_21-4 # Springer-Verlag Berlin Heidelberg 2014

Index Terms: Ancient DNA 18 Authenticity 11 Chromosomal DNA 7 Contamination prevention 2 Contaminations 11 DNA degradation 3 DNA extraction 16 DNA sources 3 Genetic fingerprints 9 Genetic identification 9 Genetic information 5 Haplogroups 6 Haplotypes 6 Human phylogeny 7 Kinship reconstruction 9 Migration pattern 7 Mitochondrial DNA 5 Neanderthal Genome project 2 Next generation sequencing 1 Nonauthenticity 14 Nuclear DNA 2 Paternity testing 9 PCR specificity and sensitivity 18 STR typing 14, 17

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_22-3 # Springer-Verlag Berlin Heidelberg 2014

Paleodemography of Extinct Hominin Populations Janet Mongea* and Alan Mannb a Department of Anthropology, University of Pennsylvania, Philadelphia, PA, USA b Department of Anthropology, Princeton University, Princeton, NJ, USA

Abstract Paleodemography is the study of past population structure. The demographic structure of the population is both the outcome of evolutionary processes operating on groups of individuals and the basis on which future evolutionary forces can potentially operate. This review is concerned with a critical evaluation of paleodemographic studies of the hominin lineage prior to the development of agriculture. Because of the potential this research has for the generation of data about birth spacing, mortality, lifespan, sex ratio, patterns of fertility, and maturation, the study of the demography of earlier human populations has attracted much attention. Very limited and fragmentary sample sizes, however, combined with many uncertainties about depositional patterns, have led to major difficulties in the development of generally accepted hypotheses. Because of the nature of the preservation of skeletal materials, oftentimes past population structure has been modeled on known living populations. In the remote past, for example, at the inception of the human lineage, the choice of comparative living samples from which to derive models is problematic. Are the data from chimpanzees or modern humans more appropriate in these reconstructions? Or are the past and extinct populations completely different from any other population model constructed from living species? Since many population parameters are based on life history variables, and vice versa, the assessment of population parameters in the past must be based on an effective evaluation of those key features that influence virtually every aspect of population structure: mortality, fertility, and longevity, to name just a few. Published reevaluations of a number of widely accepted concepts, such as the simple association of life history variables with structures like gross body or brain size, have made these earlier studies increasingly untenable. Further, recently collected data on modern humans and free ranging chimpanzees has cast doubt on the idea that these two primates experience dramatically different timing in their maturation and lifespan events. Other life history parameters of extinct populations, however, such as life expectancy, age at maturation and age at weaning may be retrievable. While there are many useful variables of past population structure that can be analyzed, most social/cultural parameters (see Layton et al. 2012) cannot be retrieved from the earliest phases of human evolutionary history. These include settlement size and household size and especially changes in population size over time, growth, decline, and even population collapse.

*Email: [email protected] Page 1 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_22-3 # Springer-Verlag Berlin Heidelberg 2014

Introduction Demography is the study of population structure, its size, composition, and related features such as sex, age, geographic distribution, and other environmental, social, and cultural factors. The successful application of demographic studies in modern human societies relies on the accumulation of data on all members of a population or, more commonly, on a calculated sampling of the population (Yaukey and Anderton 2001). In contrast, paleodemography has been characterized as the field of inquiry that attempts to identify demographic parameters from past populations derived from archaeological contexts (Hoppa 2002, p. 9) (Bocquet-Appel 2010) and is primarily based on the analysis of human skeletal materials. The preservation of human skeletons in contexts of even the relatively recent prehistoric past, where agriculture and permanent settlement are present, is variable and dependent on environmental conditions such as soil type and pH, climate, and destructive geological events. Additionally, cultural factors, such as cremation, cannibalism, mass burials, indifference to the disposition of dead infants, and many other behavioral factors, also dramatically influence the preservation of human bones. This chapter is limited to an examination of the paleodemography of our earlier ancestors, prior to the development of agriculture. Reconstructing population structure from this more distant past is much more problematic. Some recent notable technical advances include the modeling of life tables for preindustrial human populations, predicting mortality patterns (Seguy et al. 2010) and, in the analysis of the skeletal series at Libben, exploring the fertility patterns in a nonagricultural village (Meindl et al. 2010). Population size, although strictly not a demographic parameter without other information about the structure of the population, has been used to understand factors like extinction in previous hominin populations using archaeological site samples from Western Europe (Mellars and French 2011; critiqued by Dogandzic and McPherron 2013) and to explain the genetic structure of modern human populations (Hawks 2010). Preagricultural hominins, it has been postulated, relied on a subsistence base founded on the gathering and collecting of wild foods, insects and small vertebrates, and the hunting of larger animals. Scattered and seasonally available food sources meant that for the most part, these peoples did not have permanent settlements. Rather, they established temporary camps, exploiting the local resources and moving on when these were depleted. The duration of a stay at a particular locale was dependent on the season, abundance of resources, size of the group, and other variables. The groups were small in size (Weiss 1973) often no larger than 30–50 individuals. Based on modern ethnographic examples (i.e., Lee and Devore 1968), groups were probably seasonally variable in membership. Temporary encampments and continuous movements imply that deaths would have occurred at different places and that, except for unusual circumstances, we should not expect to find remains of a number of individuals at a specific locale. The expectation is that many deaths will occur during movements and the body left or interred, along the route. Further, deaths would have been seasonal, occurring during those times of the year when resources were scarcest; this implies that hominin remains are more likely to be found at some locales and not others. These generalizations about early members of the human lineage, however, are overwhelmingly based on the anthropological study of living gatherers and hunters, and the accuracy of these observations when applied to earlier, now extinct humans, is uncertain (▶ Modeling the Past: The Primatological Approach). Layton et al. (2012) make the argument that the basic life and demographic parameters of a gatherer/hunter society were achieved by the time frame of Homo heidelbergensis (viewed by some as archaic Homo sapiens). There is, for example, no certainty that all earlier hominins actually were gatherer/hunters; they may have been more specialized in dietary choice and habitat and thus were organized in a different but unknown fashion. As there are periods in the hominin fossil record Page 2 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_22-3 # Springer-Verlag Berlin Heidelberg 2014

which suggest that multiple hominin species coexisted, perhaps in geographically close proximity, it remains possible that early hominin demography was based on very different adaptive patterns. Further, prior to about 115 Ka, the sample of hominin skeleton bones available for study is very small. Only after this time did the introduction of the deliberate burial of the dead result in many more bodies being preserved, and numbers of more or less complete skeletons excavated. Finally, the study of the earliest known members of the hominin lineage, mainly early members of the genus Homo and still earlier species of the genus Australopithecus, is fraught with difficulty (for the moment, fossil samples of the very earliest identified hominins, Sahelanthropus and Orrorin, are much too few even to be considered here). The Ardipithecus ramidus sample, while quite extensive (see collected papers in Science 326, 2009), remains relatively unknown from the perspective of demography. Bones of these creatures are discovered in very different circumstances than later hominins. These early remains are usually broken and very fragmentary; multiple bones from the same individual are rarely discovered. The deposits in which they have been preserved have been formed by long-term geological processes; and they are not directly associated with archaeological accumulations. The reconstruction of the taphonomic circumstances that led to the hominin bones being deposited in the geological sediments in which they were found is complex and often ends with uncertain results. However, survivorship curves have been developed recently on the dinosaur species Albertosaurus sarcophagus by Steinsaltz and Orzack (2011), an approach that might hold some promise in the analysis of fossil hominins in deep evolutionary time. The study of general paleodemographic variables is therefore limited by the recovered skeletal and fossil samples and their contexts. These do not yield valid population samples for the construction of the sort of demographic profiles possible in the study of extant humans. Thus, the techniques of analysis and the modeling of data accumulated on these skeletal samples, even under the best of circumstances, can provide only the most preliminary and shadowy details about population structure and basic life history variables.

Estimation of the Age at Death of Skeletal Remains A demographic study of a skeletal sample begins with the assessment of both the age-at-death and sex distribution of the skeletal material. These data are absolutely essential for the construction of other population statistics. Aging and sexing of skeletal samples of living humans has been the subject of extensive research focused on the development of techniques that can yield results with a high degree of accuracy. The problems associated with aging and sexing and the ways in which the resultant data have been modeled have been summarized by Hoppa and Vaupel (2002). When the sample is of nonmodern skeletal materials (e.g., Neanderthals or australopithecines), the criteria for judging these factors are far from certain. Establishing the age at death of a skeleton relies on knowledge of the life history of the species concerned and of the biological pathways within which these hominins grew and matured. There remains uncertainty and debate about the timing of maturational events in the dentition or the skeleton and about whether models based on living humans or chimpanzees provide greater accuracy. Recent considerations of the variation in growth that characterizes chimpanzees and living humans add a further complication to these estimations (Zihlman et al. 2004; Smith and Boesch 2010; Monge and Mann 2006). In their summation of the Ardipithecus ramidus materials, White et al. (2009) argue that the anatomical features of these primates indicate that “the last common ancestors of humans and the African apes were not chimpanzee-like and that both hominids [hominins in this review] and extant African apes are each highly specialized, but through very different evolutionary pathways” (White et al. 2009, p. 64). If this conclusion is confirmed by additional research, the use of chimpanzee biology in reconstructing early hominin lifeway patterns will need to be seriously reconsidered. Page 3 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_22-3 # Springer-Verlag Berlin Heidelberg 2014

Although they are often considered together as part of a single aspect of paleodemography, it is our contention that potential life variables, including lifespan (often referred to as the study of life history), should be dealt with separately from a consideration of the achievement of this life potential (which is often viewed as a central focus of paleodemographic studies). Potential lifespan is an evolutionary biological phenomenon (with important implications for the evolution of culture) whereas achievement of that life potential represents the complex interaction of biology and culture. Carey and Judge (2001) aptly summarized this dichotomy when they observed that modern humans probably achieve a level of life potential far earlier than this potential can be routinely achieved. Through biomedicine, diet, sanitation, insect control, and other cultural appliances, modern societies have been attempting to reconcile these two elements: to make life potential and individual lifespan the same phenomenon, not just for a favored few but for all humans. In reality, while all living human populations have the potential for the same potential life expectancy (Carey and Judge 2001), most people do not achieve this. Comparisons of differences between populations are one way to analyze the contributions and adequacy of cultural mechanisms to achieve this potential and are of possible use in paleodemography. For example, using a sample of 768 dental individuals spanning the course of most of human evolution, Caspari and Lee (2004) have argued that increased cultural complexity was primarily responsible for the increases in lifespan during the course of the latter phases of human evolution. When and under what circumstances members of the human lineage achieved a modern humanlike potential life expectancy is a matter of some debate. This includes debates on all phases of life history, from infancy through childhood and adolescence to adulthood. More fundamentally, even statements that the potential of life expectancy in humans is double of that in chimpanzees must now be questioned, especially the statement that potential lifespan in humans is double that of chimpanzees. Maximum age for humans is frequently quoted as 90–100 years, and 50 years for chimps (Sacher 1975; Hawkes et al. 1998; Bogin 1999). However, our knowledge of the lifespans of chimpanzees is presently limited to a few known-age captive animals and is hampered by the paucity of field observations of wild chimpanzees, even though some have been observed for 40–50 years. Cheeta, the chimpanzee who was featured (in all likelihood) in the Tarzan movies, died in 2011 at the age of 80 (or so it was claimed). The chimpanzees of Mahale have been studied for 34 years and are now providing a limited demographic data set that suggests death among older animals occurs between 31 and 48 years (Nishida et al. 2003). This is not radically different from the profiles of average age at death in many pre-1900 human populations and for what has been estimated for most of human history (Gage 2000; but see also Ascádi and Nemeskéri 1970, and see Robb 2007 for a discussion of the age at death in preindustrial France). The Mahale chimpanzee study also reports that approximately 25 % of older females had a postreproductive lifespan. This phenomenon, the equivalent of postmenopausal human females, has traditionally been cited as a uniquely human life history event. From these observational data, it is clear that this postreproductive phenomenon can no longer be considered a unique event in human life history; theories that have been associated with this pattern, e.g., the grandmother hypothesis, must be reconsidered in light of this data (Alvarez 2000; Hawkes 2003; Levitis et al. 2013), although it is possible that the extent of these postreproductive years might be greater in humans (Blurton Jones et al. 2002). Since the process of aging causes an exponential increase in virtually all pathologies (Harrison and Roderick 1997), evolutionary selection for increased longevity must target the genes responsible for aging and not focus exclusively on a reduction in fatalities associated with pathological conditions. In baboons, longevity has a reasonably strong genetic component (Martin et al. 2002), and it is possible that chimpanzees and humans have the same potential for longevity; via cultural Page 4 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_22-3 # Springer-Verlag Berlin Heidelberg 2014

mechanisms, humans have reduced the cumulative effect of pathological conditions directly associated with aging. Vaupel et al. (1998) have provided a more detailed discussion of the effect of increases in longevity on human demography. The causes of death in past populations are also difficult to determine. Nishida et al. (2003) have calculated that in the Mahale chimpanzees, just under half of deaths are caused by disease. This appears to exclude general causes associated with death by senescence. In a study of a population of chimpanzees in Guinea Bissau, Sugiyama (2004b) reported that under conditions of ecological stress, in this case deforestation, specific subsets of the group were more likely to die: infants (0–3 years of age), juveniles (4–7 years), and active adolescents (8–11 years). Mortality profiles of five gatherer/hunter groups are presented in Hill et al. (2007). The primary cause of death reported for the Hadza, a gatherer/hunter group in Tanzania, between the years 1985 and 1997 (Blurton Jones et al. 2002), appears to be disease, here also excluding death associated with the state of just being old. Sugiyama (2004a) has reported on the extent of injury in a foragerhorticultural group, the Shiwiar (Ecuador). The results of 678 injuries suffered by 40 individuals indicate that trauma is likely, in fact, common at all stages of life and that without group provisioning, the effects of these injuries would range from debilitating to lethal. If the same sorts of patterns existed in the past (Martin and Frayer 1997), it is reasonable to suggest that provisioning may have played a role in the social system of earlier hominin taxa. Berger and Trinkaus (1995) reported on the incidence and anatomical position of bone fractures in Neanderthals. The position and frequency indicated that the Neanderthals were living a challenging lifestyle with a preponderance of injuries on the upper part of the body. The Krapina Neanderthal collection also shows a significant number of nonlethal injuries (Kricun et al. 1999), some of which appear to have demanded provisioning of some sort, for example, the Krapina 34.7 parietal in which a large cranial depression shows a considerable amount of posttrauma healing (Mann and Monge 2006). Indeed, death from trauma may have been the main cause of death in earlier hominins. It is, however, extremely difficult to identify signs of disease in earlier hominins because few diseases leave any sign of abnormal bone change (Roberts and Manchester 2007). Further, before the advent of plant and animal domestication, most of the pathologies that have killed millions of modern humans were not a part of the environmental stressors earlier hominins were exposed to. Diseases such as tuberculosis, influenza, rhinoviruses (common cold), bubonic plague, typhus, cholera, polio, typhoid, pertussis, and diphtheria are the result of human settlement after agriculture and the close associations that developed with domestic animals (Crawford 2007). Except for the widespread signs of bacterial infection on the Middle Pleistocene Kabwe specimen from Zambia, virtually nothing is known about the cause of death in fossil hominins. Similarly, almost nothing is known about the cause of death in most recent human archaeological samples (see, e.g., a description of paleopathology in Lovell 2000). Pettitt (2000) argued, using the oldest aged Neanderthal skeletons, primarily Shanidar I and La Ferrassie 1, that life was difficult in the past and that death primarily resulted from repeated sustained trauma. He based this conclusion on the general robusticity of the Neanderthal skeleton, including dense bones and strong muscle markings which suggested that the body was repeatedly challenged in life. In contrast, X-ray analysis of the entire fossil skeletal sample from the site of Krapina (Kricun et al. 1999) concluded that the skeletons are of healthy individuals, with the dense bone structure indicative of an active lifestyle. On the basis of assemblages of bones showing a lack of representation of very young and old individuals, Bocquet-Appel and Arsuaga (1999) have argued that at the two largest hominin fossil sites in Europe, Krapina, and Atapuerca (SH), the hominin accumulations were the result of a catastrophe. Cannibalism has been considered a possible cause for the accumulation at Krapina (White 2000); that at Atapuerca (SH) has been attributed to trapping of hominins by bears (but see Page 5 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_22-3 # Springer-Verlag Berlin Heidelberg 2014

also Bermudez de Castro and Nicolas 1997). The age distribution at these sites, with an overabundance of adolescents and young adults, fits the paleodemographic profile of skeletal materials caught in a catastrophic event (Paine 2000). The death profile of many catastrophes, for example, the tsunami in the Indian Ocean in early 2005, often illustrates the overwhelming overabundance of children including adolescents in the death assemblage; estimates calculate that at least one-third of the deaths in South East Asia were of children. Carnivore activity is considered a possibly significant contributor to the australopithecine fossil assemblages in the South African dolomite caves (Brain 1981). In this instance, the preponderance of young (but not infant) individuals might be most reasonably explained by differential predation of the young, something that is documented for African ground-dwelling baboons (Mann 1975). Some sort of catastrophic event may apply to the proposed simultaneous death assemblage in the A.L. 333 site at Hadar, Ethiopia. In a series of papers, Bocquet-Appel and colleagues beginning in 1982 (Bocquet-Appel 2010) have emphasized the difficulties of achieving dependable paleodemographic parameters from the aging of skeletons. He has argued that no matter how they are modeled, population profiles can only incompletely represent the living group from which they derived and only in one small slice in time. Further, considering the small, nonrandom sample sizes that are the usual subject of study, if the population from which the skeletons derive is in the process of demographic change, for example, in a general or even brief trend of population increase, then the resulting death assemblage is likely to show a preponderance of young individuals relative to the number of adults. The same pattern can also be explained by a general increase in population in-migration. Thus, without large sample sizes covering a longer time period, it would appear inappropriate to propose any broad generalizations. Because of the nature of the fossil record, the bulk of efforts at aging concentrate on the dentition, the most likely element to preserve, although other parts of skeletal anatomy have also been used to age fossil skeletal elements. In forensic anthropology, the determination of as precise an age at death as possible is crucial for individual identification. In paleodemography, this level of accuracy is not required and the use of life table modeling is considered to be effective. Nevertheless, derived age structure must be used to model the population appropriately in the first place, with the assumption that age-at-death differences in populations form an inherently interesting question. In human evolutionary studies, the age-at-death distribution question is an interesting one since it allows us to attempt to understand evolutionary process from the perspective of mortality. One of the major critiques of paleodemography discussed by Bocquet-Appel and Masset (1996) involved the assumptions made in the process of aging a skeleton. This initiated a debate evaluating the criteria employed in the estimation of the age at death of skeletal samples (Bocquet-Appel 2010; Van Gerven and Aremelagos 1983; Greene et al. 1986; Konigsberg and Frankenberg 1994). Discussion focused on the use of aging standards based on the biases already present in the reference samples, to such an extent that the resulting aging profiles mimicked the age distribution of the reference sample. Bocquet-Appel and Masset’s (1982) principal concerns about the limitations of paleodemographic studies include the assumptions that the populations from which the skeletons derived were stable, life history patterns were the same throughout human evolution, and mortality patterns in the past can be understood using recent human and primate populations. Many of these same points were made by Howell (1982) on a paleodemographic study of the Native American Libben Site, Ohio (Lovejoy et al. 1977). A review by Milner et al. (2000) evaluates the issues first raised by Bocquet-Appel and Masset (1982). These discussions require critical appraisal of the published literature on the estimation of the age at death of the skeleton (for comprehensive reviews, see Katzenberg and Saunders 2000; White Page 6 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_22-3 # Springer-Verlag Berlin Heidelberg 2014

2000; Hoppa and Vaupel 2002), and some skeletal biologists have advocated for the use of functional life history stages rather than age categories within the paleodemographic analysis of skeletal samples (Roksandic and Armstrong 2011). In many cases, these standards have been developed in the USA on the Hamann-Todd Osteological Collection (curated at the Cleveland Museum of Natural History, 1 Wade Oval Drive, Cleveland, Ohio 44106) and the Terry Collection (curated at the Department of Anthropology, Smithsonian Institution, Museum of Natural History, Washington DC 20013), both reference collections of known age- and sex-at-death individuals. Early research that presented models of the lifespan of fossil hominins, summarized by Ascádi and Nemeskéri (1970), examined a variety of fossil hominin materials from Europe and Asia. Later, more elaborate discussions (Mann 1968, 1975; McKinley 1971) focused on the large fossil collection of Australopithecus robustus from the Swartkrans site in South Africa. On the basis of observed similarities in the pattern of dental development among the significant sample of immature individuals in the Swartkrans fossil collection to that established for modern humans, Mann argued that these early hominins matured in the prolonged period then thought to be unique to Homo sapiens. This conclusion was criticized by Sacher (1975, 1978), whose research on the correlation between brain size and longevity suggested that the life history trajectory of the small-brained robust australopithecines was more apelike than humanlike. Smith (1989) expanded on this work, arguing for a strong correlation between dental development and brain size. More recent data on primate biology has made some of Smith’s conclusions untenable. For example, factoring in variations in diet, Godfrey et al. (2001) have shown that cranial capacity alone is an insufficient predictor of dental development within primate taxa. Although not frequently quoted in anthropological reviews of life history, Carey and Judge (2001), using a large longevity sample, have shown that brain size is only one of a number of central aspects of life history. Gage (1998) has also pointed out that in order to extrapolate to primate life history, more information is needed on patterns of variation, especially environmentally induced variation. Finally, in this context, Leigh (2004) has shown that in primates, brain growth is an extremely complicated phenomenon and that adult brain size alone is not well associated with dental maturation or with the length of the juvenile growth period (and see Braga and Heuze 2007). Age profiles of more recent fossil hominin accumulations are not very different from those of living peoples, for example, the skeletal series of Natufians (the pre- or incipient agricultural groups of the Levant) analyzed by Karasik et al. (2000). In this study, using a traditional comparative series as the standard, the mean age at death was 31.5 years; in contrast, applying aging standards derived from local Sinai Bedouins produced a mean age at death of 36.5 years. Very few individuals were placed in the older adult category of 45–50 years of age. Unfortunately, the fossil record of earlier phases of human evolution, with fragmentary, incomplete bones of few individuals generally deriving from many generations, cannot be subjected to this sort of critical comparative study. Probably the best studied fossil assemblages for which paleodemographic profiles have been developed are those from Krapina and Atapuerca (SH). Each site contains a large number of individuals: for Krapina, between 75 and 92 (Wolpoff 1999), and at Atapuerca, a minimum of 32 individuals (Bermudez de Castro and Nicolas 1997). As mentioned previously, both sites have been interpreted as possessing assemblages indicative of a catastrophic event. This idea for the accumulation of the sample at Krapina was supported by White (2000) and Trinkaus (1985) but criticized by Russell (1987a, b). At Atapuerca, Bermudez de Castro and Nicolas (1997) have argued against the possible catastrophic event proposed by Bocquet-Appel and Arsuaga (1999). Age estimations based on tooth development and emergence and occlusal wear, the elements usually examined in deriving age-at-death determinations in fossil hominins, resulted in a relatively low average age at death at both sites. Profiles from both Atapuerca and Krapina reveal an age-at-death Page 7 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_22-3 # Springer-Verlag Berlin Heidelberg 2014

distribution with high adolescent and young adult mortality and a death of older individuals. In an extensive examination of Neanderthal paleodemography, using 206 European and Middle Eastern Neanderthal remains and comparisons to 11 modern human populations including gathering and hunting peoples, agricultural peoples, and archaeological collections, Trinkaus (1995) concluded that Neanderthal populations were under extensive environmental stress that resulted in a unique population profile. The elements of this profile included high levels of infant mortality extending into young adulthood, with few or no individuals surviving into older age categories (+40 years). This latter feature of the Neanderthal mortality profile is unique among all the modern human populations used in his analysis, including archaeological samples. Trinkaus (1995) considers other explanations for this mortality pattern and attempts to minimize the effect of the Krapina and Vindija samples on the resultant profile. These two Croatian sites account for the bulk of adolescent specimens in the overall Neanderthal sample, emphasizing the possibility of alternative explanations for the unusual mortality profiles represented at these sites. If the Middle Pleistocene Atapuerca (SH) site and the Late Pleistocene analyses by Trinkaus (1995) for Neanderthals are acceptable, using life tables from modern human populations it would not appear possible for these extinct hominins to replace their numbers in each subsequent generation. In another study, Trinkaus and Thompson (1987) concluded that there were no older individuals in Neanderthal populations. This leaves us in the perplexing situation of having to explain why, if these death assemblages are representative of living populations, these hominins did not become extinct after just a few generations. Clearly something is wrong with these analyses. In this context, Ogilvie et al. (1989) concluded that dental enamel hypoplasia indicates that Neanderthals sustained continuing stress from weaning to adulthood, resulting from an inadequacy of foraging technique. One major problem with this analysis is the “osteological paradox” (Wood et al. 1994) in which high frequencies of stress indicators on the skeleton are actually an indication of the adequacy of cultural and/or biological mechanisms in the individuals and populations at risk, in buffering the negative environmental effects. For Middle and Upper Pleistocene hominin samples, such as those from Atapuerca (SH) and the European Neanderthals, it might be possible to use life history parameters that have been described for modern humans (but see Dean et al. 1986; Bermudez de Castro et al. 2001; Ramirez Rozzi and Bermudez de Castro 2004). For earlier hominins, the issue is very controversial. Caspari and Lee (2004) attempted to circumvent the problems associated with life history differences in human evolution by using dental attributes to grossly divide the hominin fossil record (including members of Australopithecus) into younger and older age categories, pointing out that this division will reasonably apply to all the taxa, regardless of possible differences in growth and development.

Determining the Sex of Skeletal Materials There are also significant limitations in the identification of the sex of a skeleton. How applicable to extinct hominins are the anatomical criteria developed on modern human samples for determining the sex of individual specimens? In general, the sex determination of earlier hominins is based on the anatomy of the os coxae and on comparisons of the level of robusticity of the preserved postcranial bones in the sample. In the case of pelvic bones, unambiguous identification is often impossible, even when the bones are relatively complete and undistorted (Rosenberg 1988). Gracilization related to evolutionary change in fossil samples over time can confound the recognition of sex differences based on skeletal robusticity. For example, the locus H mandible from the Lower Cave, Zhoukoudian, has been identified as a female in comparison with other mandibular specimens. However, it is possible that this Locus was deposited later in time than the other fossil bearing loci, and the more gracile nature of this fossil may be indicative of a male from a later time (Mann 1981). Page 8 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_22-3 # Springer-Verlag Berlin Heidelberg 2014

The clear implication of these problems is that the recognition of sexual dimorphism within an extinct hominin species can be very difficult. Plavcan and Cope (2001) have attempted to determine the validity of species in the fossil record using metric criteria and sample variation. Other researchers have also examined this problem (Lockwood et al. 1996, 2000; Rehg and Leigh 1999), and much of this literature has recently been reviewed by Scott and Lockwood (2004). More broadly, Plavcan (2001) has reviewed the pattern of sexual dimorphism in primates. These studies consider the evidence for the presence of a range of variation that can be reasonably accommodated within a valid species; within such metrically defined species, sex differences are established along the continuum. Ultimately, however, since sample sizes of earlier hominins are very small, both sexes are often collapsed into one. As a consequence of this, the determination of sex in hominin fossil paleodemography has attracted less attention than the establishment of criteria associated with aging. However, the identification of the sex of fossil skeletal materials can yield significant data on population structure. This is because knowledge of female mortality is crucial to understanding patterns of fertility. Using comparative data from chimpanzees and modern humans groups, Lovejoy (1981) hypothesized a demographic transition at the origin of the hominin lineage, primarily based on decreasing birth intervals. Dall and Boyd (2004) have suggested that lactation in mammals probably evolved as a way to minimize the impact of fluctuations in food resources. Austin et al. (2013) assessed weaning patterns in a sample of modern human and macaque children as a comparative sample to a juvenile Neanderthal specimen. A demographic shift in age at weaning to the time frame of the early evolution of the genus Homo is proposed by Kennedy (2005). Thus, a decrease in time spent in lactation and its subsequent effect on birth interval may have been associated with a relatively more consistent food supply in human evolution. Birth interval, age at menarche, and age at first birth (first parity) are highly variable in both chimpanzees and humans (Eveleth and Tanner 1990). Sugiyama (2004b) summarized data on chimpanzees which showed that captive animals display reduced times in each of those categories associated with fertility; in contrast, fertility patterns among wild chimpanzees are quite varied. Although sexing the skeleton is relatively easy in strongly dimorphic species, the process in modern human populations is much more difficult. Populations and species have varied degrees of dimorphism, and it can be expressed in different ways. White (2000), in a summary of the techniques used to sex the skeleton in recent archaeological populations, recommends seriating the specimens and then determining the most appropriate features within that population to use as sexing criteria. Both White (2000) and Meindl and Russell (1998) provide detailed reviews of the extensive literature on the identification of the sex of skeletal materials. A somewhat different review of the pre-1980 literature is provided in the summary of the Workshop of European Anthropological Association, published in the Journal of Human Evolution (1980). In earlier, nonmodern hominins, the presence and extent of dimorphism is difficult to understand and quantify. Frayer and Wolpoff (1985) described various models for the identification and comprehension of sexual dimorphism in human evolution. More recent research has generated new models for understanding the context of dimorphism across the hominin lineage and among vertebrates in general. For example, if late secondary sex characteristics are primarily influenced by the production of testosterone, then an understanding of reduced dimorphism in hominins might be explained by a selection model directed toward a decrease in testosterone production or changes in its target cells. Thus, the immune suppression effect of testosterone production is reduced, influencing longevity, and the role of fathers in caregiving might have increased as male–male competition based on testosterone levels was reduced (Wingfield et al. 1997). This is a plausible explanation for

Page 9 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_22-3 # Springer-Verlag Berlin Heidelberg 2014

reduction of sexual dimorphism and provides an explanation for the evolutionary role of monogamy in human evolution. In general, however, the study of the regulation and evolution of sexually dimorphic characteristics from a physiological and genetic perspective is just beginning. It is reasonable to infer that some combination of hormonal and genetic factors plays an important role. For example, Skuse (1999) proposed a mechanism of genomic imprinting of the X chromosome as a possible mechanism, and Haqq and Donahoe (1998) reviewed the literature on individuals diagnosed with sexual ambiguity to construct a more holistic model of the factors contributing to the attribution of sex. Significant differences exist in the brains of human males and females, and sex differences are present in many biological systems (Maguire et al. 1999; Goldstein et al. 2001; Allen et al. 2003; Dubb et al. 2003; Raz et al. 2004; Shah et al. 2004; Vawter et al. 2004). Bolnick and Doebeli (2003) proposed a possible role of sexual selection and sexual dimorphism under conditions of ecological destabilization. The multiple outcomes of this theoretical model seem to indicate that there is a conflict between speciation and dimorphism, i.e., sexual selection for increased dimorphism reduces the possibility of speciation. In this model, under conditions of changing ecological landscapes during the course of human evolution, some species undergo an adaptive speciation while others evolve alternatives to speciation, including an increase in sexual dimorphism. This may be a useful explanatory factor in the differing levels of sexual dimorphism observed in hominin taxa. For the most part, although sexing is critical to almost all types of skeletal analysis, our ability to apply this to extinct members of the hominin lineage is difficult. Since the number of skeletons present in any analysis of the life history or paleodemography of fossil hominin samples is so small, it makes sense to pool both the male and female skeletons and consider them as a single sample. Among the confounding difficulties which have led to the pooling of samples is the inability to distinguish dimorphic characteristics among the earliest hominins (including Australopithecus). Numerous arguments focused on the evolution of sex differences in the pelvis and in other features related to dimorphism (i.e., female vs. male stature). Assuming the obstetrical dilemma in human evolution, and without knowledge as to the exact time frame when this would have occurred in human biological history, research has pointed to possible evolutionary mechanisms responsible for these differences including sexual selection for more fecund female mates. Guegan et al. (2000) presented data on populations in 38 countries to show that stature dimorphism in females in modern populations could be correlated with complications associated with pregnancy and the birthing process. Nettle (2002) has shown that female height is correlated with reproductive success but that maximum success occurred in females who were below the mean for height. Integrating the data from both of these studies suggests that over time, female height may be more conservative than male height. Thus, differences in dimorphism in human evolution may be related in large measure to variations in males, with female biology remaining somewhat stable. Studies of living humans appear to show that females are less vulnerable to environmental influences on growth processes than males (Stini 1985). Sexual selection has also been implicated in the evolution of body dimorphism. For example, Pawlowski and Grabarczyk (2003) have argued that the low center of gravity in females, manifest after puberty and adaptive for both pregnancy and the carrying of infants, is the result of sexual selection by males for this specific female body form. The os coxa is the single most dimorphic feature of humans and, according to Tague and Lovejoy (1986), probably has been for at least the last few million years. The anatomy of the known sample of hominin pelvic bones appears to be related to the conflicting needs of both efficient bipedality and the problems associated with birthing relatively large-brained babies with broad shoulders. It appears that some of the dimorphism present in adult pelvises might actually be present in utero Page 10 of 25

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(Holcomb and Konigsberg 1995). In addition, it is possible that geographic population affects the expression of sexual dimorphism in the pelvis (Patriquin et al. 2003). In modern populations, the accuracy of the assignation of sex using the pelvis is close to 95 % (Murail et al. 1999; Bruzek 2002). According to Leutenegger (1982), all primate females possess a greater ischiopubic index than males do. Although biases exist in the determination of sex based on features of the skull, there appear to be differential differences between the preservation of female versus male skeletons (Walker et al. 1988). There is a tendency to identify older female skulls as male (see Henke 1974). This is no doubt a direct consequence that the skull becomes more “masculine” as it ages (Meindl et al. 1985); it is difficult, however, to know if this bias applies to fossil hominin studies. Susanne et al. (1985) present data on age changes in cephalic dimensions. The distinctive features of the male and female os coxae are universal in living humans (and probably most extinct species as well), although there might be some variation in the degree of expression of the differences within these populations. The same, however, does not apply to other characteristics used in sexing the skeleton. Thus, in concert with the techniques applied to determining the age at death of a skeleton, sexing techniques must be population specific. This can be accomplished either through analysis based on the data accumulated on a reference sample of known sex (Steyn and Iscan 1997; Graw et al. 1999; Mall et al. 2000; Asala 2001; Schiwy-Bochat 2001; Pettenati-Soubayroux et al. 2002; Bidmos and Asala 2004) or through seriation of a group of unknown specimens (White 2000) and the application of a variety of statistical techniques to the data. Safont et al. (2000) have employed this method on a modern human sample. Since it can generally be assumed that an unknown sample contains both male and female skeletons, it is reasonable to sort the skeletal elements into male and female categories. In fossil hominin studies, in contrast, because it is not possible to derive a set of metric or nonmetric characteristics associated with sex (or age for that matter) on an applicable reference sample, it is necessary to derive a set a parameters that best describes (statistically or with other methods) the variation in the sample being examined. Depending on its place in the hominin timescale, comparisons can be made to hominoids, especially chimpanzees, or to living human populations. An example of this type of analysis was that of Reno et al. (2003) on a fossil sample from Afar Locality (A.L.) 333 and assigned to A. afarensis (see also the commentary by Larson 2003). Since the A.L. 333 locale is considered on geological grounds to be a simultaneous death assemblage, it was assumed that the fossil sample represented males and females of the same species. Simulations were undertaken to compare the Afar fossils to modern humans, chimpanzees, and gorillas. Using measurements of postcranial elements, A. afarensis was found to be closest to H. sapiens in degree of sexual dimorphism (with H. sapiens intermediate between the monomorphism of chimps and the extreme dimorphism of Gorilla in postcranial dimensions). These researchers also question the simple extrapolation of dimorphism to social categories in primates. They emphasized the striking dissimilarity in sexual dimorphism between canine tooth maturation in chimpanzees and their almost negligible postcranial dimorphism. They conclude that A. afarensis possessed a very distinct pattern from polygamous chimpanzees. In this analysis, monogamy is probably the most likely pattern of social organization among these early fossil hominins. Richmond and Jungers (1995) and Lockwood et al. (1996, 2000) have also investigated the pattern of sexual dimorphism in A. afarensis. Examinations of sexual dimorphism have been performed on A. (P.) boisei specimens (Silverman et al. 2001), face dimorphism in A. africanus (Lockwood 1999), sexual dimorphism in Australopithecus (P.) robustus and early Homo (Susman et al. 2001), and the mandibular metrics of

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a comparative sample of H. sapiens, Pan troglodytes, Pongo pygmaeus pygmaeus, and Gorilla gorilla gorilla (Humphrey et al. 1999). One of the most extensive investigations of sex assignation in a specific sample was undertaken by Bermudez de Castro and Nicolas (1997) on the fossil materials from the Spanish site of Atapuerca (SH). A total sample of 32 individuals was examined, with a 1:1 sex ratio derived from the specimens that could be sexed. They report an overrepresentation of females in the age category between 16 and 20 years. This may be a reflection of a high female mortality in early child bearing years. Additional studies on this collection have been done by Rosas et al. (2002) and Bermudez de Castro et al. (2001), who examined the level of sexual dimorphism in the sample as revealed in mandibular and dental measurements, respectively. Bermudez de Castro et al. (2001) concluded that the dentition showed greater sexual dimorphism than that found in modern humans. In the mandible, sexual dimorphic patterns were present but differed from those in modern humans. Arsuaga et al. (1997) looked at body size and cranial capacity dimorphism, reporting a degree of dimorphism similar to other Middle Pleistocene hominins and modern humans. Wolpoff (1999) noted that sexual dimorphic characteristics, including overall cranial size and capacity, vault thickness, superstructures and toruses (mastoid process, sagittal keel, nuchal torus), forehead curvature, and functionally related features of facial size and robustness, vary in expression in recent human geographic populations and are a reflection of the hominin evolutionary past in each region. On the basis of these observations, Wolpoff (1999) identified male and female sex differences in an extensive sample of Middle and Upper Pleistocene hominins. Weidenreich’s (1935, 1943) detailed studies of the morphology of the H. erectus sample from Zhoukoudian suggested a relatively low level of sexual dimorphism, a conclusion that was also found by Mann (1981), who studied the virtually complete Zhoukoudian cast collection. Other studies of the application of techniques of sexing to fossil hominin materials include the work of Coqueugniot et al. (2000) as well as the application of mandibular ramus posterior flexure to a sample of Neanderthals and early modern humans (Loth and Henneberg 1996), dimorphism in chin morphology in the specimens from Klasies River Mouth (Lam et al. 1996), and an analysis of the Kebara 2 pelvis using various bony dimensions (Tague 1992). Finally, Trinkaus (1980) employed indices of robusticity of postcranial elements to show that European and Near Eastern Neanderthal limb bones show the same degree of sexual dimorphism as modern humans in this feature. In a recent article by Lordkipanidze et al. (2013), the sample of 5 crania from the 1.8million-year-old site of Dmanisi was divided into male and female based on robusticity of cranial elements.

Other Paleodemographic Parameters Life History

Life history variables (▶ Primate Life Histories and ▶ Estimation of Basic Life History Data of Fossil Hominoids), including brain and body size, neonatal weight, length of gestation, lifespan, age of sexual maturation, and age of weaning, are all correlated to each other; various theories have been proposed to explain the evolutionary mechanisms through which this occurs. Using data on living primates, Harvey and Clutton-Brock (1985) noted that the distinctive features of this mammalian order are large brains, prolonged maturation, and long lifespans. Understanding the relationships of these variables to each other from an evolutionary perspective has been the subject of numerous projects and debates (Borries et al. 2013). Pereira (1993) has summarized this work, including a discussion of allometric or correlation analysis. Heterochrony has also been used to explain life Page 12 of 25

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history developmental processes that may have characterized human evolution (Gould 1977; Minugh-Purvis and McNamara 2002). The usefulness of heterochrony has been critically evaluated by Godfrey and Sutherland (1996) and Shea (1989). Gage (1998) compiled all known mortality and fertility data on a broad group of primates. He concluded that a comparison of human and chimpanzees life histories indicates that delayed maturation is a characteristic of humans, whereas an extension of the overall time frame of reproduction, along with an increase in the calculated rate of aging, appears characteristic of chimpanzees. Chimpanzee character state of life history is evolutionarily derived and thus does not make a useful model for understanding the last common ancestor of chimpanzees and humans (see discussions in Duda and Zrzavy 2013). Although this observation must be kept in mind, chimpanzees are our closest living relative; the use of the growing body of literature on chimpanzee studies, especially in the wild, can reasonably provide a point of comparison not only to living humans but also to extinct members of the human lineage. The human life history pattern as described by Smith and Tompkins (1995, p. 260) is that “humans take about twice as long to erupt teeth, twice as long to reach adulthood, and live about twice as long as great apes.” This probably represents an overstatement of the unique position of humans within the Primate Order. For example, the work of Zihlman et al. (2004) shows that wild chimpanzees take upward of 3 years longer to mature than animals in captivity. Using M1 eruption times as a proxy for other maturational events, chimpanzees now appear to overlap the range of modern humans. Recent work on sexual maturation of chimpanzees in the wild shows that some groups do not mature until 14 years of age (Sugiyama 2004b). A comprehensive description of life history in mammals was analyzed using an energetics model by Hill and Kaplan (1999), and an evolutionary model of longevity increases was presented by Carey and Judge (2001). Using game theory, Brommer (2000) also discussed the evolution of life history using the evolutionary concept of fitness. Using seven anthropoid primate species, Leigh (2004) has shown that life history among the primates cannot be related solely to brain size but more specifically to the point in life history in which brain growth occurs. The correlation of diet to primate life history has been addressed by Godfrey et al. (2001) and Kaplan et al. (2000). Day et al. (2002) associated life history variables across various species of animals with the level of predator pressure. Bolnick and Doebeli (2003) have also proposed that species confronted with ecological instability adapt in a number of ways, including changes in sexual dimorphism, speciation, or an alteration of ontogenetic processes that reduces the influence of the destabilizing ecological events. It is possible that some and all combinations of these outcomes have occurred in human evolution. Of critical importance is the plausible role of ontogenetic changes as an adaptive feature in at least some species in human evolution. If, for example, A. afarensis does indeed show little sexual dimorphism and, by extrapolation from primate models, this indicates a pattern of monogamy among these hominins, then it is indeed possible that altricial young were also part of this pattern, further supporting Lovejoy’s (1981) hypothesis. Since life history theory is built on the foundation of living animals, it becomes a challenge to integrate fossil hominin species into these analyses. It has been argued that correlations of brain and body size to life history variables supersede any possible analysis of the fossil materials and that all data must be interpreted in this context. Certainly, evolutionary events have produced unique combinations of life history features in the past; and if it is possible to integrate these into the correlation studies, it might serve to more fully represent the life history of hominins across time and space. There appears to be no consensus as to when in the course of hominin evolution modern humanlike life histories evolved. Various perspectives on the evolution of life history have been presented (Smith and Tompkins 1995; Tillier 1995; Bogin 1999; Minugh-Purvis and McNamara Page 13 of 25

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2002; Thompson et al. 2003). More recently Robson and Wood (2008) presented a synthesis of life history data from the fossil record of human evolution and concluded that in the time frame of Homo heidelbergensis (viewed by some as archaic Homo sapiens), the basic life history parameters similar to modern humans were attained. In order to reconstruct the life history patterns of earlier hominins, most research has concentrated on the examination of those biological patterns that may yield data documenting rates of maturation. Overwhelmingly, this has meant focusing on the developing dentition with the assumption that the maturation of dental hard tissues and the sequential eruption of the teeth are under strong genetic control, with a minimum of possible environmental influence. Unlike bone, which is subject to remodeling throughout life, dental enamel appears to be relatively stable, preserving the initial structures. Most research on the maturation patterns of earlier hominins focuses either on the pattern and sequential eruption of the developing dentition or on the examination of dental microstructures as time-dependent features. Comparisons between fossil hominins are most usually made to the living great apes, especially chimpanzees, and to modern humans. Patterns of Maturation Chimpanzees and humans are characterized by different life history strategies; this should be apparent in the dental calcification and eruption schedules of the two species. What if any pattern differences have been described? The most prominent is that chimpanzees have an accelerated development and eruption of the M1 especially in relationship to the development of I1 (Smith 1994, 2000; critique by Mann et al. 1990). It has also been observed that chimpanzees have a time overlap in the calcification schedule of the molar sequence (Anemone 2002). And finally, chimpanzees have a significant difference in the pattern of calcification and eruption of the permanent canines. Since this tooth is so functionally and anatomically distinct from that of humans, the canine is probably not a good indicator of life history pattern differences (Lampl et al. 1993). Various models have been used to explain these differences. These include differences in life history (see, e.g., Smith 2000 and the critique by Lampl et al. 2000), but other explanations have been proposed (Simpson et al. 1990; Simpson and Kunos 1998). Many scholars have undertaken general discussions of how dental development of fossil hominin samples can be understood as part of life history (Bogin 1999; Smith and Tompkins 1995; Bogin and Smith 1996; Kuykendall 2003). Discussions of life history in the early phases of human evolution have been extensively discussed (Dean 1985; Smith 1994; Conroy and Vannier 1989; Mann et al. 1987; Conroy 1988; Mann 1988; Wolpoff et al. 1988; Conroy and Kuykendall 1995; Smith and Tompkins 1995; Clegg and Aiello 1999; Dean et al. 2001; Moggi-Cecchi 2001). Many investigations have also focused on the later phases of human evolution (summarized in Robson and Wood 2008). Dental Microstructure Some researchers have maintained that dental enamel and dentin microstructures are useful tools for the reconstruction of the timing of dental development. Dental microstructure is a hard tissue relic of the ontogenetic processes that govern tooth growth (Ramirez Rozzi and Bermudez de Castro 2004; Guatelli-Steinberg et al. 2005). Conversely, it is also possible that these structures reflect a microworld of minianatomical detail that may or may not be useful in the timing of dental development or the reconstruction of phylogenetic relationships. Bromage and Dean (1985) presented data to support the idea that the timing of tooth development in fossil hominins could be estimated using microstructural details of enamel. Since then there has been much debate about the applicability of these hard tissues to understanding of the times of Page 14 of 25

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maturational events in earlier hominins (Dean and Reid 2001; Moggi-Cecchi 2001; Ramirez Rozzi and Bermudez de Castro 2004; Guatelli-Steinberg et al. 2005; Monge et al. 2006; Smith et al. 2010). Finally, growth and development studies have been undertaken on the femur (Tardieu 1998) and pelvis (Berge 1995) of fossil hominins. In both these studies, although a humanlike pattern of growth best describes all members of the genus Homo, australopithecine-grade hominins probably had growth trajectories similar to those in chimpanzees. What can be concluded from this diverse body of research? Even where a virtually complete skeleton of a youngster (KNM-WT 15000) has been recovered, it has been difficult to reach a consensus about its rate of maturation and its age at death (Clegg and Aiello 1999). The diversity of research on the patterns of maturation in earlier hominins is well illustrated in the edited volume, Patterns of Growth and Development in the Genus Homo (Thompson et al. 2003). Thus, it remains very difficult to compare the work presented by one researcher with that of another because the fossil samples and the techniques of analysis that are employed are often so different. However, and with some reservations, the research results appear to support the general recognition that, by the appearance of members of the genus Homo, there was a maturational shift to a more modern humanlike pattern, although that pattern might be manifested in slightly different ways in individual species within Homo. If this cautious conclusion continues to be supported by additional data, it will justify the use of the growth and development patterns of modern humans as reference data and for use in modeling population parameters within paleodemographic reconstructions. What sorts of patterns characterized the maturation of the still earlier members of the hominin lineage remains uncertain. However, recent information documenting significant variation in maturational events in both modern humans and chimpanzees suggests that the traditional notion of a uniquely human prolonged period of maturation may have to be reconsidered.

Conclusions 1. The paleodemography of extinct hominin taxa has not produced a corpus of dependable data, and it remains possible that reasonable population-based demographic parameters from fossil assemblages will remain unattainable into the foreseeable future. The use of modeling from archaeological samples holds more promise in an application to the more distant past to capture demographic parameters in long extinct populations in the hominin lineage (Konigsberg and Frankenberg 2013). 2. In contrast, life history reconstruction, establishing some basic parameters associated with demographic analysis, is a more achievable goal. Among these parameters are potential life expectancy, time of maturation, and age at weaning. The accumulation of additional information on living primates has made the simple association of life history variables with gross size variables (e.g., brain size and body size) increasingly untenable. 3. The larger the database on captive and wild chimpanzees, the more difficult it becomes to clearly distinguish their life history variables from those of living humans. This will certainly affect our interpretations of life history and extrapolations to demographic features that characterize fossil hominin species. Similarly, the more knowledge we have of the extent of modern human variation and plasticity, the more difficult it becomes to specifically categorize unique autapomorphic features of human life history. 4. Culture (in conjunction with significant developmental plasticity) may be more important as regard understanding human life history than biology, especially in variations in the expression of Page 15 of 25

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features such as longevity and age at weaning, and perhaps even maturation rates, general reduction in the age of first menstruation, and others. Such factors may better explain the large ranges of variation that have been observed in both humans and chimpanzees. In sum, we know very little of the demography including all aspects of population parameters of earlier members of the hominin lineage, and much that appears to be understood requires reevaluation on the basis of newly acquired data from nonhuman primates and the increasing comprehension of the range of variation characterizing human growth and maturation.

Cross-References ▶ Archaeology ▶ Dispersals of Early Humans: Adaptations, Frontiers, and New Territories ▶ Estimation of Basic Life History Data of Fossil Hominoids ▶ Modeling the Past: The Primatological Approach ▶ Primate Life Histories ▶ The Ontogeny-Phylogeny Nexus in a Nutshell: Implications for Primatology

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_22-3 # Springer-Verlag Berlin Heidelberg 2014

Index Terms: Aging 3–7, 9, 13 Australopithecus 3, 7–8, 10–11 chimpanzee 3–4, 13 demography 1–3, 5, 16 dental microstructure 14 fertility 1–2, 9, 13 genus Homo 3, 9, 15 grandmother hypothesis 4 growth and development 8, 15 life expectancy 1, 4, 15 life history 1, 3–4, 6–8, 10, 12–15 longevity 1, 4–5, 7, 9, 13, 16 maturation 1, 7, 11–16 mortality 1–2, 5–6, 8–9, 12–13 Paleodemography 1–2, 4, 6, 8–10, 15 population structure 1–3, 9 sexing 3, 9–12 sexual dimorphism 9–13

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_23-5 # Springer-Verlag Berlin Heidelberg 2013

Modeling the Past: The Primatological Approach Robert W. Sussmana* and Donna Hartb a Department of Anthropology, Washington University at St. Louis, St. Louis, MO, USA b Department of Anthropology, University of Missouri, St. Louis, MO, USA

Abstract Many models have been developed to depict the behavior and ecology of our earliest relatives. However, the Man the Hunter model has been the most widely accepted way of viewing human evolution. This theory gained ground in the mid-twentieth century and has been recycled ever since under various guises in the scientific and popular literature. Many human traits, such as bipedalism, monogamy, territoriality, tool use, technological invention, male aggression, group living, and sociality, are often linked to this perspective. Although theories and associations of human aggressive hunters abound, they are rarely based on the two evidentiary approaches that shed light on early hominin ecology and behavior – living primate models and the fossil record. Here, an outline is given on a methodology of reconstructing early human behavior by using both the fossil record and extant primate ecology and behavior. Data on early human fossils, on modern primates living in similar habitats to our earliest ancestors, and on rates of predation both today and in the distant past indicate that Man the Hunted may be a more accurate descriptor of our earliest relatives. Here evidence for the Man the Hunted theory, some of the behavioral patterns that were needed to protect our earliest ancestors from predation, and how this may lead to a new perspective on certain aspects of human nature are described.

Introduction In the early 1950s, the once thought missing link to our earliest human ancestor, the Piltdown Man, was confirmed to be fake (Weiner et al. 1953), and most scientists were beginning to believe that australopithecines were indeed hominins. It was becoming obvious that our earliest ancestors were small brained and probably more like nonhuman primates than modern humans in much of their behavior and ecology. The idea that there was a major “gap” between ancestral humans and nonhuman primates was no longer considered tenable, and the continuity between ourselves and our ancestors was emphasized. This stimulated scientists to begin thinking about using the living primates as potential models for the reconstruction of the behavior and ecology of our earliest ancestors. One of the first attempts at this was by Bartholomew and Birdsell (1953). Since then many models have been proposed.

*Email: [email protected] Page 1 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_23-5 # Springer-Verlag Berlin Heidelberg 2013

Reconstructing the Behavior of the Earliest Hominins There has been much debate about which type of model might best be employed in reconstructing the evolution of early human behavior. Tooby and DeVore (1987) describe three different types of models that have been used. The first is what they designate as referential models. In this case, a living species is used as a literal model for an extinct taxon (the referent species). For example, chimpanzees often are seen as the best referents for early hominins (e.g., Stanford 1999; McGrew 2010). Second is the conceptual model, in which a mosaic of morphological or behavioral traits is seen as a broad analogue to reconstruct early hominin species. As an example, one living primate species might be used to reconstruct the diet and another to reconstruct the social behavior. Tooby and DeVore label the third type as strategic modeling. In this case, it is assumed that species in the past were subject to the same fundamental evolutionary laws and ecological forces as species are today. Although no present species will correspond precisely to any past species, the principles that produced the characteristics of living species will correspond exactly to the principles that produced the characteristics of the species living long ago. There has been a great deal of disagreement as to which of these three types of models might produce the best results (e.g., Kinzey 1987; Potts 1999; Stanford 1999; Jolly 2001; Elton 2006; Sayers and Lovejoy 2008; McGrew 2010; Van Reybrouck 2012) or even whether labeling these models diminishes their usefulness. In the model presented in this paper, there is an attempt to use all of the above in what is considered a logical and appropriate manner but always taking into account whether any particular aspect of our model is inconsistent with the evidence presented in the fossil record. This brings up the question of what kinds of evidence should be used, and in what manner, in attempts to reconstruct the behavior and ecology of our earliest ancestors. The most important evidence is the fossils of hominins themselves; careful examination and understanding of the actual skeletal remains of the creatures. However, useful evidence would also include other fossil materials (such as tools or footprints) left by our earliest relatives and clues about the environment in which they lived (such as fauna, flora, or water sources). While fossils provide the most important data for an accurate reconstruction, many current theories of early hominin behavior fall short in their critical examination of the fossil evidence. In fact, they are often virtually fossil-free. Besides fossils, any other types of secondary evidence used in reconstructions are less reliable but, nonetheless, offer insights. These should be ranked in the following order as far as applicability to reconstructing early hominin lifestyles: (1) The behavior of nonhuman primates living under similar ecological conditions to those of our earliest ancestors (e.g., Elton 2006). It is best to keep timing in mind with this approach. Forests change and so do climates and so do species, as well. Hominins likely began as edge species (living in a mixture of wetlands and grasslands) but moved out onto more open savanna about 2.5 mya (Reed and Eck 1997; Reed 2008). (2) The behavior of our genetically closest primate relatives, such as chimpanzees, bonobos, and gorillas (e.g., McGrew 2010). However, lumping all the great apes together as one analogue when they are so diverse is dangerous, although some characteristics may remain conservative within a taxonomic group. For example, monogamous pair bonds among the lesser apes or gibbons, or upright posture among the apes, might be considered phylogenetically conservative traits shared by all or most species within a taxon. (3) Characteristics shared by certain (or all) modern humans that might also be similar to our earliest ancestors. Modern foragers, however, are just as advanced and evolved within their own culture and environment as any Western urban dwellers. The least confident recommendation is (4) the behavior of other animal species that might be living under similar conditions or that share some aspects of the lifestyle of early humans, such as certain carnivore or Page 2 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_23-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 1 (Large Plio-Pleistocene predators). Relative sizes of fossil cats and bears from the time period 8.5 million to 1 million years ago. Each square approximates 20 in. on each side; three squares equals 5 ft. From left to right: giant cheetah (Acinonyx); saber-toothed cat (Machairodus); ancestral leopard (Paramachairodus); bear (Indarctos); sabertoothed cat (Homotherium); saber-toothed cat (Megantereon) (C. Rudloff, redrawn from Turner 1997)

prey species. However, a cat is still a carnivore even if it eats some grass; early hominins included a few vertebrates in their diet, but they cannot legitimately be compared to obligate meat eaters. In using any of these types of secondary evidence, it is necessary to be extremely careful (because in many cases, similar-looking behaviors are not the same); we can end up comparing apples with oranges, lions with hominins, or even strangler figs with purse snatchers! (Yes, the analogy of invasive rainforest fig trees to purse snatching muggers has been made in the sociobiological literature (Ghiglieri 1999).) Obviously, words with loaded meaning for humans – war, rape, murder, infanticide, and genocide to name a few – must be used with extreme caution when referring to the activities of nonhuman species. In this regard Jonathan Marks (2002, p. 104) warns against “. . . a science of metaphorical, not of biological, connections.” One cannot, therefore, necessarily impute correlation between human ancestors and data based on extant carnivores, modern human foragers, or great apes. For example, even the concept of hunting in chimps and humans is quite different. Present-day human hunters purposely search for animal prey, but chimpanzees do not: “Instead, they forage for plant foods and eat prey animals opportunistically in the course of looking for fruits and leaves” (Stanford 1999, p. 48). Furthermore, reconstructions must always be compatible with the actual fossil data – the fossils are real but the models we construct are hypothetical and must constantly be tested and reconfirmed. Lastly, when attempting to construct models of our early ancestors’ behavior, it is necessary to be precise about timing (Tattersall 2010). If one says our earliest human ancestors (those who lived seven million years ago) behaved in a certain way, we cannot use fossil evidence from two million years ago, nor can we confuse those creatures from two million years ago with those who existed 500,000 years ago. As a case in point about timing, one poses the question: Could hunting have occurred without tools? The first evidence of stone tools comes from around 2.6 million years ago (Semaw 2000). The earliest hominin fossils, however, date from almost seven million years ago (Brunet et al. 2002), at least four million years before the first stone tools. The most popular and currently accepted theory of human evolution is the Man the Hunter model. In seeking to understand why this model is so captivating and easily adopted as the paradigm for human evolution, it is instructive to remember that the first hominin fossils to be found in the nineteenth century were European specimens well under 100,000 years in age, and most of the artifacts found with them were finely crafted spearpoints or tools used for slaughtering animals. The Paleolithic cave paintings in Europe also depicted a metaphysical connection between humans and hunting. Nevertheless, when one looks at the fossil evidence, hunting came quite late to our human family. Interpretations of hominin behavior, therefore, should be Page 3 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_23-5 # Springer-Verlag Berlin Heidelberg 2013

conservative and cautious, as stated by Klein (1999, p. 306): “. . . the mere presence of animal bones at archaeological sites does not prove that hominins were killing animals or even necessarily exploiting meat. Indeed, as was the case in the earlier South African sites, the hominin remains themselves may have been the meal refuse of large carnivores.” The diversity of large carnivores was extensive in the African paleo-past. Many groups of carnivores that are now extinct (such as the huge short-faced bear, Agriotherium africanum) may have preyed on hominins between 6 and 3.5 mya. Then at about 3.5 million years, new carnivores evolved to join the previous groups, meaning that as many as eight to ten different species of sabertoothed cats, false saber-toothed cats, conical-toothed cats, giant hyenas, and large wolflike canids were roaming the same African sites where hominin fossils have been found (Treves and Palmqvist 2007) (see Fig. 1). The transition to hunting as a dominant way of life does not appear to have started until after the appearance of our own genus, Homo, and may not have even begun with the earliest members of our genus. Homo erectus has been given credit in the past for existing as a large animal hunter, and dates as far back as 1.75 mya have been hypothesized for such a lifestyle. But if you take a conservative approach to this subject – looking only at facts and fossils and not imaginative speculations – the first indications of hunting are amazingly recent. In fact, according to some paleontologists, the first unequivocal evidence of large-scale, systematic hunting by humans is available from paleoarchaeological sites possibly only 60,000–80,000 years old (Binford 1992; Klein 1999). The earliest hominin fossils are 6–7 million years before the first factual evidence of systematic human hunting. No hard archaeological evidence, in other words no fossil evidence of tools designed for hunting, exists earlier in time than a finely shaped wooden spear excavated at Scho¨ningen, Germany, dated at approximately 400,000 years of age (Dennell 1997; Thieme 1997). The famous Torralba and Ambrona sites in Spain, dated at 500,000 years ago, contain huge numbers of large mammal bones. They were thought to represent unquestionable evidence of megafauna killed by Pleistocene hunters. Now these two sites are being reconsidered in light of better archaeological analysis. Elephant bones at these sites could just as likely represent natural deaths or carnivore kills as they do the remains of human hunting (Klein 1999; Klein et al. 2007). Further, no hominins were largescale hunters before they had the use of fire (because of their dentition and alimentary tract, points we will elucidate below), although insects, small vertebrates, lizards, and birds likely were eaten opportunistically. The best evidence for the controlled use of fire appears approximately 800,000 years ago in Israel (Goren-Inbar et al. 2004). Klein (1999, p. 160) states: “The assumption of consistent hunting has been challenged, especially by archaeologists who argue that the evidence does not prove the hunting hypothesis . . . it is crucial to remember (although not as exciting) that probably the majority of calories [came] from gathering plant foods.”

Dentition and Diet Whether Homo erectus or any other hominin before 800,000 years ago regularly hunted or scavenged may be a moot question. Hunting would only be an activity undertaken if early hunters could eat what they killed, and to eat raw meat, it is necessary to have teeth capable of masticating and processing meat. Obviously, Man the Hunter models of human evolution assume that a significant portion of our earliest ancestors’ diets must have come from killing and eating meat from relatively large mammals. By comparing the characteristics of the dental and jaw morphology of various living Page 4 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_23-5 # Springer-Verlag Berlin Heidelberg 2013

primates with those of fossils, one can make inferences about the diets of early hominins. Teaford and Ungar (2000, see also, Ungar 2011) carried out just such a comparison in an attempt to reconstruct the early hominin diet. Using such features as tooth size, tooth shape, enamel structure, dental microwear, and jaw biomechanics, they found that the earliest humans had a unique combination of dental characteristics and a diet different from modern apes or modern humans. Ungar (2004) extended this analysis by examining occlusal slope and relief of the lower molars. Australopithecus afarensis is characterized by jawbones that are thick, with relatively small incisors and canines in relation to molars. The molars, by comparison with other primates, are huge, flat, and blunt, show less slope and relief, and lack the long shearing crests necessary to mince flesh. A. afarensis also had larger front molars than back molars. The dental enamel is thick, and microwear on the teeth is a mosaic of gorilla-like fine wear striations (indicating leaf eating) and baboon-like pits and microflakes (indicating fruits, seeds, and tubers in the diet). These definitive pieces of evidence coming from fossil dentition all point away from meat eating. In studies of mid- to large-sized primates, such as macaques, baboons, chimpanzees, and modern human foragers, in which the amount of time spent obtaining animal protein has been quantified, the total is very low, usually making up less than 5 % of time spent feeding (Garber 1987; Sussman 1999). Given these facts, it is hypothesized that early humans were able to exploit a wide range of dietary resources, including hard, brittle foods (tough fruits, nuts, seeds, and pods) as well as soft, weak foods (ripe fruits, young leaves and herbs, flowers, and buds). They may also have been able to eat abrasive objects, including gritty plant parts, such as grass seeds, roots, rhizomes, and underground tubers. As stated by Teaford and Ungar (2000, p. 13508–13509): “this ability to eat both hard and soft foods, plus abrasive and nonabrasive foods, would have left early hominins particularly well suited for life in a variety of habitats, ranging from gallery forest to open savanna.” Dental morphology indicates that the earliest hominins would have had difficulty breaking down tough pliant plant foods, such as soft, fibrous seed coats and the veins and stems of mature leaves, although these foods may have been eaten occasionally (Ungar 2011). Interestingly, Teaford and Ungar (2000) stress that another tough pliant food that our early ancestors would have had difficulty processing was meat! They state (2000, p. 13509): “the early hominids were not dentally preadapted to eat meat – they simply did not have the sharp, reciprocally concave shearing blades necessary to retain and cut such foods.” Both modern chimpanzees and humans have an alimentary track that is neither specialized for eating leaves nor animal protein but instead is more generalized, similar to the majority of primates who are omnivorous and eat a mixture of food types (Chivers and Hladik 1980, 1984; Martin et al. 1985; Martin 1990; Price et al. 2012). Modern humans, especially in Western cultures, think of themselves as meat eaters. For Americans and a whole spectrum of other cultures, meat defines that ephemeral status of wealth and ease for which we strive. Because they, themselves, were rooted in these cultural stereotypes, anthropologists egregiously misnamed the modern forager cultures as hunters and gatherers and initially emphasized only the contributions of male hunters. Nevertheless, more than two-thirds of modern-day foragers’ food comes from women gathering plant foods and, in the process, opportunistically capturing small mammals and reptiles. Less than one-third of the diet (the meat portion brought in through dedicated hunting by men) serves to supplement their foraged nutritional intake, except in cold climates or where fishing is prevalent (Marlowe 2005). Yet, meat can have significance far beyond its mathematical contribution. Modern dietary concerns in industrial societies revolve around the amounts of both fat and red meat that are consumed by the average person. By the latter portion of the twentieth century, there was a full-blown red alert from the medical community warning that meat should be ingested in limited quantities. “Diseases of affluence” caused by high-protein, high-fat diets include raised Page 5 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_23-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 2 (Australopithecines walking at Laetoli). Reconstruction of two Australopithecus afarensis; successes or added advantages of bipedal locomotion were simply by-products of a preadaptation to upright posture (Used by permission of American Museum of Natural History, AMNH Library 4936[2])

cholesterol levels, high blood pressure, heart disease, stroke, breast cancer, colon cancer, and diabetes – all correlated to a diet exorbitantly rich in red meat. With colon cancer, in particular, startling data are available: Daily red-meat eaters are two and one-half times more likely to develop this cancer as are people adhering to a mostly vegetarian diet (Willett et al. 1990). T. Colin Campbell, who compared Chinese rural villagers (eating a traditional diet low in meat) and their urban compatriots (eating more meat), states: “We’re basically a vegetarian species and should be eating a wide variety of plant foods and minimizing our intake of animal foods” (Brody 1990, p. C2). In his Chinese study, Campbell even found that individuals following a low-fat, low-meat diet suffered less anemia and osteoporosis (conditions commonly associated with food low in animal products) than individuals higher on the meat-consuming ladder (Campbell and Campbell 2005). Lastly, no hominins hunted on a large scale before the advent of controlled fire. Again, early humans just did not have the dentition nor the digestive tract of a carnivore. Our anatomy and physiology did not particularly suit us for digesting meat until the mastery of cooking solved the problem. Our intestinal tract is short, and predigestion by fire had to precede any major meat eating (although humans still require certain nutrients that are not obtainable from a meat diet). As stated above, the oldest known hearths with good evidence for controlled use of fire are around 800,000 years old.

Locomotion By far the best known of early australopithecine species is A. afarensis, with many fossil remains dating from between 3.7 and 2.9 mya and possibly as far back as 5 mya. Collections have yielded close to 400 specimens in many East African sites (Kimbel and Delezene 2009). Specimens include the famous Lucy (dated at 3.2 mya), which is the most complete adult skeleton from this time period, and fossil footprints from Laetoli, Tanzania, ash deposits (dated at 3.6 mya). Furthermore,

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_23-5 # Springer-Verlag Berlin Heidelberg 2013

most hypotheses concerning human evolution position A. afarensis as a possible pivotal species from which all other later hominins, including Homo, evolved (Fleagle 1999; Tattersall 2010; Conroy and Pontzer 2012). Given the above facts, A. afarensis is seen as a good species to examine when attempting to reconstruct the appearance and behavior of one of our early human ancestors. Terrestrial bipedalism is a hallmark of the whole fossil hominin family. This mode of locomotion can be inferred from fossil specimens nearly seven million years old (Galik et al. 2004). It appeared long before the vast growth of open grasslands in Africa and before the expansion of human brain size and recognizable stone tool making. Besides the fossilized bones, direct evidence of early bipedalism comes from the footprints at Laetoli where two hominins were walking together in soft ash almost 4 mya (see Fig. 2) – prints that are remarkably like modern human footprints (White 1980; Tuttle 1985; Day 1985; Feibel et al. 1996). However, looking at the skeletal evidence, the locomotion of these early hominins was not exactly identical to ours. In fact A. afarensis seems to have been a primate equally at home in the trees or on the ground indicated by a number of factors. First, the limb proportions are different from anatomically modern humans. The arms are similar in proportion to modern humans, but the legs are relatively much shorter (i.e., more apelike), and this implies the use of suspensory locomotion in the trees (Kimbel et al. 1994). Other aspects of the upper limbs also retain a number of features indicating an ability to move easily in the trees. The wrist and hand bones are quite chimpanzee-like; the finger and toe bones are slender and curved as in apes, giving A. afarensis grasping capabilities compatible with suspensory behaviors; the toe bones are relatively longer and more curved than in Homo sapiens. The joints of the hands and feet and the overall proportions of the foot bones all reinforce evidence for climbing adaptations and arboreal activity. Nevertheless, the relative thumb length of these hominins is closer to that of modern humans than it is to chimpanzees (Susman et al. 1984; Smith 1995; Corkern 1997; Alba et al. 2003; Conroy and Pontzer 2012). The pelvis and lower limbs of A. afarensis are a mixture of humanlike and apelike features. These anatomical components and the shorter leg length indicate that A. afarensis may have used less energy while walking, whereas transition speeds from walking to running may have been lower with slower running speeds than modern longer-legged humans (Steudel-Numbers 2003; but see Conroy and Pontzer 2012). Overall, Rak (1991, p. 283) summarizes: “Although clearly bipedal and highly terrestrial, Lucy evidently achieved this mode of locomotion through a solution of her own.” A propensity to question the efficiency of primate locomotion is not new to anthropology. It was also once thought that the diminutive Neotropical marmosets and tamarins were restricted in their ability to move on small branches because they have claws instead of the standard primate nails on their hands and feet. However, it has subsequently been proven that claws do not restrict callitrichid locomotion on thin branches; indeed, their claws also enable them to utilize large trunks much like squirrels do. Claws allow them to be more versatile, and they can use a wider range of arboreal habitats than most other new-world monkeys (Garber 1984; Sussman and Kinzey 1984). It appears that the combination of skeletal characteristics found in A. afarensis enabled these hominins to be versatile in a similar way. They were able to use the ground and the trees equally and successfully for a very long time. These early hominins were well adapted to their environment and not in the least inhibited by switching back and forth from bipedalism on the ground to quadrupedalism in the trees. There are at least seven different “models” that have been proposed to account for bipedalism as a hominin adaptive strategy: the tool using and making model (Darwin 1874; Washburn 1960; Sinclair et al. 1986), the carrying model (Hewes 1961, 1964; Lovejoy 1981), the vigilance model (Dart and Craig 1959; Day 1986), the heat dissipation model (Wheeler 1984, 1991), the energy efficiency model (Rodman and McHenry 1980; Steudel 1994), the display model (Jablonski and Page 7 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_23-5 # Springer-Verlag Berlin Heidelberg 2013

Chaplin 1993), and the foraging model (Hunt 1994). Each one of the models has some merit, but none of the theories seem to be a strong enough catalyst for switching to a new mode of locomotion. Furthermore, there are many other primates who spend most of their time on the ground, and none of these has developed bipedalism, even though each of the theorized advantages presumably also would have accrued to them. It is difficult to separate consequence from causation. It cannot be concluded that any of the seven suggested models caused hominins to become bipedal. None of the theories may be causative; instead, all the theoretical “causes” may be results of a primate preadaptation to being bipedal. All the great apes are preadapted to bipedality. When our ancestors came down from the trees, bipedalism was possible because of body proportions and suspensory adaptations – longer arms and shorter legs that allow gibbons, orangutans, and chimpanzees to hang from trees and forage for fruit. All apes have varying capacities for erect posture and are able to walk upright for short periods of time; bonobos, especially, will stride upright with humanlike posture. However, when the earliest hominins began using the ground for a major portion of their activities, their body proportions were more suited for bipedalism than for other forms of locomotion, i.e., quadrupedalism or knuckle-walking. As stated by Fleagle (1999, p. 528): Although it is important to see early hominins in the context of hominin evolution, it is equally important to realize that in the same way that they were not little people, they also were not just bipedal chimps, but the beginning of a new radiation of very different hominoids. It is this uniqueness that makes reconstructing hominid origins so difficult. Thus although early hominids and their bipedal adaptations are certainly derived from an African apelike ancestry, human bipedalism is morphologically and physiologically different from the occasional facultative bipedal behaviors occasionally seen in other primates. The morphological and behavioral commitment to bipedalism that characterized early hominids suggests unique ecological and historical circumstances as well.

Some species of primates are intrinsically adapted to edge habitats and, therefore, are able to take advantage of changing environments. It is hypothesized that the earliest hominins were edge species (see below) and that they exploited a terrestrial habitat due to a developing mosaic environment that included climate change. Rather than seeking the factors that caused early human ancestors to become bipedal, it is proposed that it was a preadaptation that already existed and it was efficient in a new habitat; the successes or added advantages were simply a by-product. Tattersall (2003) has arrived at a similar conclusion regarding bipedality. Besides bipedalism and limb use, there are also solid conjectures of what our earliest ancestors were like as far as body build, height, weight, and brain capacity. From various A. afarensis specimens and by examining the skeleton of Lucy, it seems there was a considerable size difference between males and females (Kimbel and Delezene 2009). Although the canines of both sexes were relatively small and not at all dagger-like, they were larger and longer in the males than in the females. The range of body size for A. afarensis individuals is estimated to be 30–45 kg (Fleagle 1999). The height of the adults has been estimated at 1.0–1.7 m (Klein 1999). Lucy stood slightly over 1 m tall and weighed around 30 kg (she was definitely on the small side) (Conroy and Pontzer 2012). If these weights are accurate, we can extrapolate that female A. afarensis were the size of male baboons and males were the size of female chimpanzees. The cranial capacity of these hominins is estimated at 400–500 cm3 – about the size of a modern chimpanzee but twice as large as Miocene fossil apes. On average, australopithecines and modern chimpanzees have brains that are two to three times larger than similarly sized mammals, whereas modern human brain size is six to seven times larger than other mammals. Looking at brain size relative to body size, using the encephalization quotient as a measurement, the brain of A. afarensis was slightly larger in relation to its body than that of modern chimpanzees

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_23-5 # Springer-Verlag Berlin Heidelberg 2013

(EQ ¼ 2.4 for A. afarensis versus 2.0 for chimpanzees) (Boaz 1997). Thus, our ancestors were mid- to relatively large-sized primates with brains that were slightly larger than any nonhuman primate, although only a fraction bigger than modern chimpanzees. There are many speculations about the external appearance of australopithecines. Johanson and Edey (1981) added some details to the portrait of a living Lucy. They pictured her and her kin as small but extremely powerful – their bones were robust for their size, and they were probably heavily muscled. Their arms were longer in proportion to their legs and trunk than modern humans. Their hands were like ours, but their fingers were curled more when in a relaxed position. Heads were more apelike than humanlike with prognathic jaws and no chin. They may have possessed more body hair in comparison to modern humans. While hair color cannot be guessed at from the fossil remains nor can the color of the skin, living in tropical Africa, A. afarensis likely possessed darkly pigmented skin with sun-protective melanin (Jablonski 2012).

Habitat of Our Earliest Ancestor Although many early theories on the evolution of our earliest ancestors stress the importance of arid, savanna environments, these do not seem to be the primary habitats, according to the fossil record, until after 2 mya. The African climate was becoming more arid in the time between 12 and 5 mya, and equatorial forests were undoubtedly shrinking (Segalen et al. 2007; Conroy and Pontzer 2012). However, the process that led to this climatic phenomenon also greatly enlarged areas of transitional zones between forest and adjacent savanna. Closed woodland forests were still widespread in East Africa 3.5 mya, whereas the proportion of dry shrub to grassland habitats began to increase around 1.8 mya (deMenocal and Bloemendal 1995; Schekleton 1995). It is in these transitional zones that the behavioral and anatomical changes were initiated in early hominin evolution. The flora and fauna remains that are found in association with fossil hominins of this time period indicate a mixed, mosaic environment – mosaic in the sense that it was ecologically diverse and subject to seasonal and yearly changes in vegetation (Potts 1996; Wolpoff 1998; Kimbel and Delezene 2009; Conroy and Pontzer 2012). These environments were wetter than those in which later fossil hominins are found, and most fossil sites of this early time period contained some type of water source, such as rivers and lakes (White et al. 1994; WoldeGabriel et al. 1994, 2001; Reed 1997, 2008; Campisano and Feibel 2007; Wrangham et al. 2009). For example, at Hadar, Ethiopia, the mammalian faunal remains suggest that a lake existed, surrounded by marshy environments fed by rivers flowing off the Ethiopian escarpment; thus, a mosaic of habitats existed at Hadar consisting of closed and open woodland, bushland, and grassland (Reed 2008; Conroy and Pontzer 2012). The earliest hominins appear to be associated with variegated fringe environments or edges between forest and grassland. These habitats usually contain animal and plant species of both the forest and the grassland, as well as species unique to the borders between the two. The species adapted to these transitional habitats are often referred to as edge species or eurytopic (i.e., adapted to a wide range of habitats) (Kimbel and Delezene 2009). During these earliest times, it appears that hominins began to take advantage of the growing fringe environments, lessening competition with their sibling ape species which were better adapted to exploit the dense forest and thus partitioning the niche occupied by the parent species of both apes and hominins into two narrower and less overlapping adaptive zones (Klein 1999; LeeThorp et al. 2003; Reed 2008; Conroy and Pontzer 2012). From available evidence it is speculated that our early ancestors were able to exploit a great variety of food resources but were mainly fruit eaters, probably supplementing this diet with some Page 9 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_23-5 # Springer-Verlag Berlin Heidelberg 2013

young leaves and other plant parts, social insects, and a small amount of opportunistically captured small vertebrate prey – lizards, small snakes, birds, and mammals. They also likely exploited some freshwater and marine resources (Cunnane and Stewart 2010). Several other species of primates are intrinsically adapted to edge habitats and are also able to take advantage of changing environments. Ring-tailed lemurs in Madagascar, African baboons, and vervet monkeys, some Asian macaques and langurs, and, to some extent, Neotropical capuchin monkeys are nonhuman primate examples. These, not coincidentally, are some of the most common and numerous of all living primates other than humans. The macaque genus, for example, has the widest geographical distribution of any nonhuman primate in Asia. Many macaque species in Asia are endangered, but the ones that have the healthiest populations (e.g., long-tailed macaques, Macaca fascicularis, and rhesus macaques, M. mulatta) are edge adapted. Certain ecological niches may breed certain behavioral repertoires. Many argue that the closer the DNA comparison, the more similar the behaviors between two related species. In that case, chimps and bonobos might be the best prototype for early human ancestors. However, if ecology is paramount, then chimps and bonobos may be less suitable prototypes (although some traits between these close relatives may still be important and phylogenetically conservative) and edge species may be the best models for early humans. Nearly 40 years ago, Robin Fox (1967, p. 419) declared: But the problem of taking the great apes as models lies in the fact of their forest ecologies. Most modern students of primate evolution agree that we should pay close attention to ecology in order to understand the selection pressures at work on the evolving primate lines. This has been shown to be crucial in understanding . . . evolution.

Even if one were to learn everything about the hominin-ape common ancestor, many of the most crucial questions about distinctively hominin evolution would remain unanswered. Although there is a fairly impressive record of human fossils during the period of 7–2 mya, there is a lack of chimpanzee fossils at these early sites. It seems likely, therefore, that chimpanzee ancestors did not inhabit these fringe environments and were likely restricted to more wet, closed forest ecosystems – areas where fossils are less likely to be preserved (Stewart 2010). Some populations of chimpanzees moved into more mosaic, open habitats relatively recently, long after humans had moved into more arid environments. Furthermore, modern chimpanzees do not live in habitats in which modern humans lived in the past or are found today. The historical geographic range of chimpanzees is quite restricted, probably more restricted than even that of early humans before leaving Africa. To date, the best primate models to use as a basis for extrapolation about behavioral characteristics of our earliest ancestors are modern primate species living in similar edge habitats. Macaques can be extremely good colonizers of edge habitats. The macaque genus spread throughout Asia before humans reached that continent (Delson 1980). By the time Homo erectus arrived in Asia 1.8 mya, most hominins were no longer edge species (our more recent ancestors were exploiting more open habitats by this date (Tattersall 2010)), so hominins likely did not displace the macaques. True “weed” species, it is proposed that the macaques are excellent models for reconstructing how our early ancestors may have lived. However, even if macaques are used here, many of the features of the behavior and ecology of these monkeys are very similar to that of other primates living in similar habitats. It is these shared characteristics that make this such a strong model. After all, ultimately, it is the environment in which species find themselves that determines many of their evolutionary adaptations.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_23-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 3 (Long-tailed macaque). The ecology and social organization of the long-tailed macaque may offer an excellent model of how our early ancestors lived (R. W. Sussman)

The Macaque Model Long-tailed macaques (M. fascicularis) are small edge species that spend a good proportion of time both in the trees and on the ground (see Fig. 3). They are omnivorous and very versatile in their locomotion, although mainly quadrupedal. The most widespread of any Southeast Asian monkey, they occur from Burma through Malaysia and Thailand to Vietnam, while offshore populations are found on Java, Borneo, and numerous smaller islands as far east as the Philippines and Timor. Throughout this area, broadleaf evergreen and other forest types are interspersed with secondary and disturbed habitats, and it is the latter that long-tailed macaques prefer. Virtually all of the studies of this species make note that they are most commonly found in secondary forest habitat, preferably near water (Sussman et al. 2011). The success of the long-tailed macaque throughout its extensive Asian distribution is widely credited to its being an “adaptable opportunist” (Mackinnon and Mackinnon 1980, p. 187). Researchers emphasize that these monkeys are extremely adaptable and able to flourish in highly disturbed land. There is a sizable long-tailed macaque population on the island of Mauritius in the southwest Indian Ocean (Sussman and Tattersall 1981, 1986). Although the original transport of the species from Asia to Mauritius is totally undocumented, it is likely they were onboard the ships when the Portuguese first reached the island and were inadvertently or purposely introduced to the primatedeficient ecosystem. Cited from the first studies as an assertive colonizer of new habitat, the small number of original immigrants had increased to 40,000 animals (before recent exportation of macaques for medical research) – successfully living up to their reputation as colonizers of disturbed and varied habitats (Sussman and Tattersall 1986; Sussman et al. 2011).

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_23-5 # Springer-Verlag Berlin Heidelberg 2013

Long-tailed macaques are slender, active monkeys; average weight is 4–5 kg for females and 6–7.75 kg for males (Jamieson 1998). Long-tailed macaque society is organized around matrilineal hierarchies. There are always one or two dominant males visible within the group, as well as some lower-ranking adult males, plus the adolescent and subadult male offspring of the females. At sexual maturity males migrate to a new group. Female offspring are philopatric, mating with unrelated males who join their troop (Jamieson 1998). Many of the Man the Hunter models ignore or minimize the role of females in human evolution. In many terrestrial and edge-adapted nonhuman primate species, such as long-tailed macaques and baboons, females are the core of society, remaining with their female relatives from birth to old age. Each matriline consists of several generations and can be placed in a dominance hierarchy. Highly social females inherit the rank of their mothers, so the troop organization remains relatively stable over time. Man the Hunter scenarios typically depict male hunters as leaders, innovators, tool makers, and tool users. Since these aspects of gender specificity may never be revealed in the fossil record, it may be justifiable to construct theories based on the behavior of our primate relatives. When Japanese macaques were first studied in the wild, it was the young females who started innovative behaviors such as new ways of processing food (Kawai 1958). Chimpanzee tools are made primarily by females and used mainly in gathering activities such as nut cracking and termite fishing; it is also the female chimpanzees who teach the next generation how to use these tools (Boesch and Boesch-Achermann 2000; Sanz 2004). Furthermore, in most primates, females are the repositories of group knowledge concerning home ranges and scarce resources. Group knowledge and traditions are passed on from mother to offspring, and stability of the group, both in the present and over time, is often accomplished through female associations (Zihlman 1997). In most primates adapted to edge environments, it is the males who migrate. However, in the closest genetic relatives of humans, the gorillas, chimpanzees, and bonobos, females normally change groups when they mature. This appears to be a phylogenetically conservative characteristic among hominoids which makes it possible that among our earliest ancestors, females, not males, migrated between groups. However, most modern human foragers are multilocal, with individuals residing with their maternal relatives at times and with their paternal relatives at other times or sometimes with neither (Marlowe 2005). The ability of edge species to exploit a wide variety of environments is accompanied by a substantial flexibility of behavior. Long-tailed macaques appear to be primarily arboreal where suitable vegetation exists, but they come to the ground along riverbanks, seashores, and in open areas – and in some portions of their recently colonized range, such as Mauritius, they are highly terrestrial (Sussman and Tattersall 1981). They are eclectic omnivores with a distinct preference for fruit. But the variety of habitat they exploit is reflected in a wide selection of food items – besides fruit, they feed on leaves, grasses, seeds, flowers, buds, shoots, mushrooms, water plants, gum, sap, bark, insects, snails, shellfish, bird eggs, and small vertebrates (Sussman and Tattersall 1981; Yeager 1996; Sussman et al. 2011). Human-disturbed habitat or proximity to human settlements is not avoided; rather, they tend to live commensally with humans throughout their range, which results in crop raiding of sugar cane, rice, cassava, and taro fields. Long-tailed macaques live in large multi-male, multi-female groups of up to 80 individuals, although in some areas groups are much smaller. They show distinct flexibility in structure; the large basic social unit tends to split up into smaller subgroups for daytime foraging activities (Jamieson 1998; Sussman et al. 2011). Subgroups may be all males, but most often consist of adult males accompanying females and their young offspring. The number and size of subgroups tend to vary with the season and resource availability (Jamieson 1998). The entire troop reforms each Page 12 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_23-5 # Springer-Verlag Berlin Heidelberg 2013

evening and returns to the same sleeping site each night, usually on the edge of a water source. Because of their unique behavior of returning to a home base each night, long-tailed macaques have been labeled a “refuging” species.

Fossils and Living Primates Looking at the fossil evidence, it is apparent that human ancestors, living between 7 and 2.5 mya, were intermediate-sized primates, not smaller than male baboons or larger than female chimpanzees. Given their relative brain size, they were at least as clever as the great apes of today. They had diverse locomotor abilities, exploiting both terrestrial and arboreal habitats. They used climbing and suspensory postures when traveling in the trees and were bipedal when on the ground. It is believed that their bipedalism was a preadaptation, but walking on two feet freed the arms and hands and proved to be advantageous in a number of ways. Given their relatively small size and small canines, there is no reason to think that our early ancestors were any less vulnerable to predation than are modern monkeys – some of which have yearly predation rates generally comparable to gazelles, antelopes, or deer living in similar environments (Hart 2000; Hart and Sussman 2009). Indeed, edge species can be highly vulnerable to predation and because of this usually live in relatively large social groups with many adult males and adult females; adult males often serve as sentinels and provide protection against predators (Hart and Sussman 2009). Because a primate group with only one male and ten females can have the same reproductive output as a group with ten males and ten females, often the male role in primate groups is to act as a first line of defense. If he gets eaten there are other males to take his place, but if a sexually mature female gets eaten, then she and all her potential offspring (and living dependent infants) are lost. Like long-tailed macaques, our human ancestors may have lived in multi-male, multi-female groups of variable size that were able to split up depending on the availability of food and reform each evening at home base refuges. However, certain facts such as the exact size of the groups and subgroups, whether males or females migrated from the group when they reached sexual maturity, and the internal structure of the group (whether matrilineal or formed along male kinship lines) would be impossible to determine accurately. Indications of these social parameters cannot be found in the fossil record and are quite variable even in closely related living primates. In sum, the best archetype of early humans may be a multi-male, group-living, mid-sized, omnivorous, quite vulnerable creature living in an edge habitat near a large water source. These hominins may well have been a refuging species returning to the same well-protected sleeping site each night. (Most modern foragers are considered central place foragers, focusing their activities around a principal location, as are many birds, social carnivores, and primates (Marlowe 2005).) These creatures were adept at using both the trees and the ground, but when they exploited the terrestrial niche, they had upright posture and were bipedal. They depended mainly on fruit, including both soft fruits and some that were quite brittle or hard, but also ate herbs, grasses, and seeds and gritty foods such as roots, rhizomes, and tubers. A very small proportion of their diet was made up of animal protein, mainly social insects (ants and termites) and, occasionally, small vertebrates captured opportunistically. These early humans did not regularly hunt for meat and could neither process it dentally nor in their digestive tracts. Like all other primates and especially ground-living and edge species, these early humans were very vulnerable to predators, and this trait did not diminish greatly over time (Hart and Sussman 2009). Fossil evidence to this effect exists from Ethiopia and South Africa, from the Zhoukoudian Page 13 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_23-5 # Springer-Verlag Berlin Heidelberg 2013

Table 1 Hominin fossils Fossil Orrorin tugenensis Ardipithecus ramidus Australopithecus africanus Homo erectus

Paranthropus robustus Homo?

Homo? Homo erectus

Archaic Homo sapiens (“helmei”) Homo neanderthalensis

Approximate age Evidence 6 mya Tooth marks on several bones 4.4 mya Tooth marks on cranial and postcranial elements 2.5 mya Punctures and incisions at base of eye sockets; talon rakings on cranium Dmanisi, Rep. 1.8–1.7 mya Canine tooth indentations of Georgia on cranium; gnaw marks on mandible Swartkrans, 1.8–1.5 mya Canine tooth indentations South Africa at base of cranium Orce, Spain 1.6 mya Cranium fragment excavated from fossil hyena den

Site Tugen Hills, Kenya Aramis, Ethiopia Taung Quarry, South Africa

Olorgesailie, 900,000 ya Kenya Zhoukoudian, 450,000 ya China

Florisbad, South Africa

260,000 ya

Mt. Cicero, Italy

50,000 ya

Assumed predator Leopard-like carnivore Carnivore

References Senut 2001

WoldeGabriel et al. 1994 Extinct raptor Berger and Clarke (Stephanoaetus 1995; McGraw spp.) et al. 2006 Saber-toothed Gabunia et al. cat 2000; Gore 2002; Wong 2003 Fossil leopard Brain 1981 (Panthera spp.) Short-faced Borja et al. 1997 hyena (Pachycrocuta brevirostris) Bitemarks on the left Carnivore Fox 2004; Small browridge 2005 Crushing of facial bones, Short-faced Boaz et al. 2000; maxilla, and mandible; hyena Boaz and Ciochon enlargement of foramen (Pachycrocuta 2001; Boaz et al. magnum brevirostris) 2004 Canine tooth depression on Hyena Deacon and forehead Deacon 1999 Fractures on cranium; enlargement of foramen magnum; gnaw marks on mandible

Hyena

Bahn 2005

cave in China, from European sites such as the skulls uncovered at Dmanisi in the Republic of Georgia, and from Olorgesailie and Tugen Hills, Kenya (see Table 1).

Man the Hunted Given that the earliest hominin ancestors were medium-sized primates who did not have any inherent weapons to fight off the many predators that lived at that time – and given that they lived in edge environments which incorporate open areas and wooded forests near rivers – then, like other primates, they were vulnerable to predation. Because of this it is hypothesized that rates of predation were just as high in our early ancestors as they are in modern species of primates and that our origins are those of a hunted species (Hart and Sussman 2009) (see Fig. 4). Protection from predation is one of the most important aspects of group living, and it is believed this was true of our earliest ancestors. Based on the long-tailed macaque model, social groups of early hominins may have been organized in a way that allowed efficient exploitation of a highly

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_23-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 4 (Leopard capturing australopithecine). Fossil evidence from South Africa documents predation by leopards on our early ancestors (C. Rudloff, redrawn from Brain 1981)

variable and changing environment and also protected its members of the group from predators. If the human lineage started out as Man the Hunted, it is proposed that a number of strategies for protection from predators are based on the behavior and social organization we observe in longtailed macaques. • Relatively large groups of 25–75 individuals: Since safety lies in numbers, one of the main reasons all diurnal primates live in groups is predator protection which provides more eyes and ears alert to presence of predators as a first line of defense. In his research on modern human foragers, Marlowe (2005) found that the median group size is 30 individuals. • Versatile locomotion that exploits both arboreal and terrestrial milieus: The major advantage of agility in the use of diverse habitats is safety in trees and dense underbrush. An added advantage of upright posture is the ability to scan for predators. • Flexible social organization: For example, gathering scarce resources in small groups but reuniting as a larger group when predation requires strength in numbers allows small groups to quickly disperse and hide while large groups can mob and intimidate predators. Again, modern human foragers fit this pattern of flexibility (Marlowe 2005). • Multi-male social structure: This demographic feature provides more male protection both when traveling through open areas and when the group settles in evening or midday. When large groups break into subgroups, females and young are accompanied by one or more large males. • Males as sentinels: Males are usually larger in these species. Upright posture adds to the appearance of large size and also allows for better vigilance, as well as waving arms, brandishing sticks, and throwing stones. Males mob or attack predators since they are the more expendable sex. • Careful selection of sleeping sites: Refuging species bring the whole group together at night in a safe area. During daytime rest periods, staying in very dense vegetation is essential. Males should stay on high alert during these inactive periods and when the group is on the move. • Stay one step ahead of predators: Intelligence endows primates with the ability to monitor the environment, communicate with other group members, and implement effective anti-predator defenses (Hart and Sussman 2009). Reconstruction of the behavior and ecology of our earliest hominin ancestor reflects the pervasive influence of large ferocious predatory animals throughout human evolution. Many circumstances have been proposed as a catalyst for the evolution of the human species – competition for resources, intellectual capacity, male-male conflicts, and hunting. But Page 15 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_23-5 # Springer-Verlag Berlin Heidelberg 2013

looking at our primate relatives and the fossil record, it is believed that predation pressure was one of the most critical components in shaping the evolution of our earliest ancestors.

Conclusion While many models have been developed to depict the behavior and ecology of our earliest relatives, the Man the Hunter model has been the most widely accepted view of human evolution. Many human traits, such as bipedalism, tools, and fire, are often linked to this Man the Hunter perspective. Theories of human aggressive hunters abound but are rarely based on evidentiary approaches. Here, using a methodology based on the fossil record and extant primate ecology and behavior, data on fossil humans, on modern primates, and on rates of predation indicate that Man the Hunted may be the most accurate descriptor of our earliest relatives.

Cross-References ▶ Biology and Evolution of Ape and Monkey Feeding ▶ Cooperation, Coalitions, and Alliances ▶ Dental Adaptations of African Apes ▶ Evolution of Basic Life History Data of Fossil Hominins ▶ Geological Background of Early Hominid Sites ▶ Great Ape Social Systems ▶ Hominin Paleodiets ▶ Modeling the Past: The Paleoethnological Evidence ▶ Origins of Modern Humans ▶ Paleodemography of Extinct Hominin Populations ▶ Postcranial and Locomotor Adaptations of Hominoids ▶ Primate Intelligence ▶ Role of Environmental Stimuli in Hominid Origins ▶ The Biotic Environments of the Late Miocene Hominids ▶ The Hunting Behavior and Carnivory of Wild Chimpanzees ▶ The Origins of Bipedal Locomotion ▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments ▶ The Species and Diversity of Australopiths

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Tattersall I (2003) Stand and deliver: why did early hominids begin to walk on two feet? Nat Hist 112:60–64 Tattersall I (2010) Macroevolutionary patterns, exaptation, and emergence in the evolution of the human brain and cognition. In: Cunnane SC, Stewart KM (eds) Human brain evolution: the influence of freshwater fish and marine resources. Wiley, New York, pp 1–11 Teaford M, Ungar P (2000) Diet and the evolution of the earliest human ancestors. Proc Natl Acad Sci U S A 97(25):13506–13511 Thieme H (1997) Lower paleolithic hunting spears from Germany. Nature 385:807–810 Tooby J, DeVore I (1987) The reconstruction of hominid behavioral evolution through strategic modeling. In: Kinzey WG (ed) The evolution of human behavior: primate models. State University of New York Press, New York, pp 183–237 Treves A, Palmqvist P (2007) Reconstructing hominin interactions with mammalian carnivores (6.0-1.8 ma). In: Gursky S, Nekaris K (eds) Primate anti-predator strategies. Springer, New York, pp 355–381 Turner A (1997) The big cats and their fossil relatives. Columbia University Press, New York Tuttle RH (1985) Ape footprints and Laetoli impressions: a response to the SUNY claims. In: Tobias PV (ed) Hominid evolution: past, present and future. Alan R. Liss, New York, pp 129–130 Ungar P (2004) Dental topography and diets of Australopithecus afarensis and early Homo. J Hum Evol 46:605–622 Ungar P (2011) Dental evidence for the diets of Plio-Pleistocene hominins. Yearb Phys Anthropol 54:47–62 Van Reybrouck D (2012) From primitives to primates: a history of ethnographic and primatological analogies in the study of prehistory. Sidestone Press, Leiden Washburn S (1960) Tools and human evolution. Sci Am 203:63–75 Weiner JS, Oakley KP, Clark WE Le G (1953) The Piltdown forgery. Oxford University Press, London Wheeler PE (1984) The evolution of bipedality and loss of functional body hair in hominids. J Hum Evol 13:91–98 Wheeler PE (1991) The influence of bipedalism in the energy and water budgets of early hominids. J Hum Evol 23:379–388 White TD (1980) Evolutionary implications of Pliocene hominid footprints. Science 208:175–176 White TD, Suwa G, Asfaw B (1994) Australopithecus ramidus, a new species of early hominid from Aramis, Ethiopia. Nature 375:88 Willett W, Stampfer M, Colditz G, Rosner BA, Speizer FE (1990) Relation of meat, fat, and fiber intake to the risk of colon cancer in a prospective study among women. N Eng J Med 323:1664–1672 WoldeGabriel G, Haile-Selassie Y, Renne PR, Hart WK, Ambrose SH, Asfaw BA, Heiken G, White T (2001) Geology and palaeontology of the Late Miocene Middle Awash valley, Afar Rift, Ethiopia. Nature 412:175–178 WoldeGabriel G, White TD, Suwa G, Renne P, de Heinzelin J, Hart WK, Helken G (1994) Ecological and temporal placement of early Pliocene hominids at Aramis, Ethiopia. Nature 371:330–333 Wolpoff M (1998) Paleoanthropology, 2nd edn. McGraw Hill, New York Wong K (2003) Stranger in a new land. Sci Am 289(5):74–83 Wrangham R, Cheney D, Seyfarth R, Sarmiento E (2009) Shallow-water habitats as sources of fallback foods for hominins. Am J Phys Anthropol 140:630–642 Page 21 of 23

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Yeager CP (1996) Feeding ecology of the long-tailed macaques (Macaca fascicularis) in Kalimantan, Tengah, Indonesia. Int J Primatol 17:51–62 Zihlman A (1997) The Paleolithic glass ceiling: women in human evolution. In: Hager L (ed) Women in human evolution. Routledge, London, pp 91–113

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Index Terms: Australopithecus afarensis_5–8 Bipedalism_7, 13 Bonobos_10 Hominin Fossils_14 Macaque model_11 Preadaptation_8, 13 Predation_14 Primatological approach_1–2, 4, 6, 9, 11, 13–14 Primatological approach dentition and diet_4 Primatological approach early hominins_2 Primatological approach fossils_13 Primatological approach habitat_9 Primatological approach hunting_14 Primatological approach locomotion_6 Primatological approach macaque model_11

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_24-3 # Springer-Verlag Berlin Heidelberg 2013

Modeling the Past: The Paleoethnological Evidence Paolo Biagi* Department of Asian and North African Studies, Ca’ Foscari University – Venice, Venezia, Italy

Abstract This chapter considers the earliest Paleolithic, Oldowan (Mode 1), and Acheulean (Mode 2) cultures of the Old Continent and the traces left by the earliest hominids since their departure from Africa. According to the most recent archaeological data, they seem to have followed two main dispersal routes across the Arabian Peninsula toward the Levant, to the north, and the Indian subcontinent, to the east. According to recent discoveries at Dmanisi in the Caucasus, the first Paleolithic settlement of Europe is dated to some 1.75 Myr ago, which indicates that the first “out of Africa” took place at least slightly before this date. The data available for Western Europe show that the first Paleolithic sites can be attributed to the period slightly before 1.0 Myr ago. The first well-defined “structural remains” so far discovered in Europe are those of Isernia La Pineta in Southern Italy, where a semicircular artificial platform made of stone boulders and animal bones has been excavated. The first hand-thrown hunting weapons come from the site of Scho¨ningen in north Germany, where the first occurrence of wooden spears, more than 2 m long, has been recorded from a site attributed to some 0.37 Myr ago. Slightly later began the regular control of fire. Although most of the archaeological finds of these ages consist of chipped stone artifacts, indications of art seem to be already present in the Acheulean of Africa and the Indian subcontinent.

Introduction The aim of this chapter is to review the current evidence for the paleoethnology of the early hominids who inhabited the Old World from the time of their appearance up to the end of the Middle Pleistocene. Although the data presently available are not abundant, there is no doubt that they are of key importance for the understanding of early hominid behavior and lifestyles. The evidence is limited in most cases to stone tools and their contexts (Clark 1968, p. 277), almost exclusively due to natural and environmental factors both physical and biological (Stiles 1998, p. 134; McNabb 2009). Given that the term paleoethnology rarely occurs in the Anglo-Saxon literature, while it is, or better was, more common in several European countries, it may be useful to review the meaning of this term and how it originated. It derives from the Greek palaio`s e`thnos lo`gos (study of ancient populations) and was first used in France around the middle of the nineteenth century, and immediately afterward in Italy when prehistoric studies began to flourish, mainly in the Po Valley region of Emilia. The term paleoethnology (Pigorini 1866; Regazzoni 1885) was formally adopted

*Email: [email protected] *Email: [email protected] Page 1 of 25

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during a congress exclusively devoted to the new science (“scienza nuova”) held in La Spezia on September 20, 1865, by the Italian Society of Natural Sciences (Tarantini 2012, p. 30). At this meeting, the French engineer Gabriel de Mortillet proposed the foundation of an International Paleoethnological Congress that was enthusiastically accepted by all delegates. A few years later, in 1875, Luigi Pigorini (Guidi 1987), Gaetano Chierici (Magnani 2007), and Pellegrino von Strobel (von Strobel 1998) founded a new journal in Parma, “Bullettino di Paletnologia Italiana,” the first to exclusively deal with prehistoric archaeology”. In those years, the term paleoethnology was preferred to that of prehistoric archaeology because it was more strictly connected with the ethnographic discoveries under way in the Americas, Africa, and Asia (Figuier 1870, p. 415; Lubbock 1870) and favored analogy studies (Hodder 1982, p. 12) between the prehistoric finds recovered from excavations in European prehistoric sites and those still in use among the native communities of the above continents (Desittere 1988). In this respect, it is important to remark that even Boucher de Perthes (1864), the famous discoverer of Abbeville and the first Early Paleolithic hand axes in continental Europe (Prestwich 1860; LamdinWhymark 2009, p. 49), had a collection of flint tools from not only Europe but also Asia and Africa (Gowlett 2009, p. 18). This is the reason why paleoethnology courses are still delivered in the Italian university, due to the long tradition that goes back to the earliest prehistoric studies of the mid-nineteenth century. Reverting to the early stone tool assemblages of the first hominids, they are often associated with alluvial sedimentary processes (Isaac 1967) related to the geographic and geomorphologic location and distribution of the (sometimes ephemeral) sites (Brown 1997, p. 150) that in many cases are limited to the stone tools themselves and possibly to organogenic tools and the faunal remains derived from hunting and scavenging activities (Conard 2007). Nevertheless, the excavations carried out during the last 50 years, and the study of the settlement structures and tool assemblages of the Early Paleolithic sites of the Old World, “have shown that it is quite possible to find sealed occupation sites that have suffered little or no natural disturbance before or after burial” (Clark 1968, p. 276). As far as the remains of material culture and their chronotypological characteristics are concerned, this chapter deals almost exclusively with Mode 1 (Oldowan) and Mode 2 (Acheulean) complexes (Clark 1994; Toth and Schick 2007). Tools belonging to these two “modes” have been collected from a great number of sites, which are distributed between East Africa and the Indian subcontinent in the southeast and Europe in the northwest (Movius 1948, p. 409; Otte 2000, p. 111).

Out of Africa Much has been published dealing with the spread of the first hominids and the radiometric dating(s) of the “out of Africa” dispersal(s) (Chauhan 2005; Petraglia 2007; Rightmire 2007). Nevertheless, many questions are still unresolved, since “the triggers for the movement of humans out of Africa are not well known” (Bar-Yosef and Belfer-Cohen 2000, p. 81). Stone tool technotypological variability, between Africa and Asia, for instance, would suggest a series of cultural complexities (Braun et al. 2010). The chronology is also very variable and badly known, in India for instance (see Chauhan 2010 contra Gaillard et al. 2010). This state of affairs results from the absence or scarcity of reliable data from some of the key territories that hominids must undoubtedly have crossed to reach Eurasia (see, for instance, Petraglia 2003, Fig. 12). This is the case for Arabia, from which little information is currently available, especially from the southern portions of the peninsula, more precisely Yemen (Dhofar) and Oman, which were Page 2 of 25

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Fig. 1 The Arabian Peninsula with the indication of the most important Early Paleolithic sites (dots) and the potential main routes followed by hominids during their “out of Africa” dispersal(s) (arrows) (After Petraglia 2003, Fig. 12)

most probably reached by the Afar Depression across the dried Red Sea strait (Cachel and Harris 2007, p. 120). Effectively, the Early Paleolithic sites discovered in these countries come from a few, restricted areas where intensive surveys and excavations have been carried out in the last two decades (Whalen and Pease 1991; Cremaschi and Negrino 2002; Whalen et al. 2002; Whalen and Fritz 2004; Amirkhanov 2006). Even though many of them are represented by surface finds, the Soviet-Yemeni Archeological Mission excavated thick sequences in some caves of southeast Yemen, close to the Dhofar border. This led to the discovery of stratified complexes, which Amirkhanov (1994, p. 218) attributed to the pre-Acheulean (Oldowan: Mode 1) and Acheulean (Mode 2) periods. In this context, the only tool bearing evident traces of use, from the lowermost layers of Al-Guza Cave in Yemen (Amirkhanov 2006, p. 91), is of unique importance. This is the only pre-Acheulean worn chopper so far known from the entire south Arabian Peninsula. Although the Early Paleolithic sites so far discovered in this region are few, south Arabia is claimed to represent one of the key routes followed by the first hominids once they started to move out of Africa, initially moving along the coast of the peninsula, to reach its interior slightly later (Rose and Petraglia 2009, p. 6), moving to the central territories of the Indian subcontinent, undoubtedly earlier than 1.0 Myr ago (Bar-Yosef and Belfer-Cohen 2000, p. 82). A second route is said to have been followed “across the Sinai into western Asia . . . although this has not been adequately detailed to date” (Bar-Yosef 1994, p. 237; Petraglia 2003, pp. 168–169), where the oldest site known to date is located at Ubeidiya (Stekelis et al. 1969; Bar-Yosef 1995, p. 250) (Fig. 1). Important radiometric dates for the first human dispersal are available from Dmanisi (Fig. 2) in the Georgian Caucasus (Gabunia et al. 1999; Nioradze and Nioradze 2011). The excavations carried out at this site over a surface of some 300 sqm led to the discovery of a unique settlement with skeletal remains of early hominids, identified as Homo ergaster (Lordkipanidze and Vekua 2006), among which are five skulls, over 10,000 chipped stones obtained from different raw Page 3 of 25

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Fig. 2 Dmanisi (Georgia): A view of the hominid archaeological site with the Medieval pit (on the right) from which the first prehistoric bones were discovered (Photograph by P. Biagi)

materials (for instance, mostly available close to the site as river pebbles), mainly represented by choppers and flakes, and over 7,000 animal bones, belonging to a faunal assemblage of “Villafranchian type.” They undoubtedly show that this dispersal took place not later than 1.8 Myr ago (Gabunia 2000, p. 43; Vekua et al. 2011). Nevertheless, “le mouvement oriental paraıˆt a` la fois beaucoup plus complexe et, surtout, beaucoup plus ancien qu’en Europe” (Otte 2000, p. 108). Fortunately, the number of discoveries of Lower Pleistocene sites from this continent is systematically increasing (de Lumley 1976; Agustı´ et al. 2000; Mussi 2001, p. 20). Although the absolute age of some of these sites is problematic (Santonja and Villa 1990, p. 54), many are undoubtedly much older than supposed only a few years ago (Roebroeks and van Kolfschoten 1994, p. 500). Although the number of radiometric dates currently available from southern Europe is very limited, nevertheless they show that at least some north Mediterranean regions were undoubtedly settled by hominids as early as 1.3 Myr ago (see, for instance, de Lumley et al. 1988; Peretto et al. 1999; Toro-Moyano et al. 2003) as suggested by recent discoveries made at Pirro Nord, in southeastern Italy (Arzarello et al. 2007, 2012).

Chipped Stone Assemblages Bifaces and Other Tools As pointed out by Gowlett (2005, p. 51), “East Africa is the key territory for examining the Oldowan and early Acheulean,” in which the first “bifacial tools were created about 1.5 million years ago” (Porr 2005, p. 68) by Homo ergaster, as a consequence of a complex series of behavioral, economic, and social factors whose complexity has been pointed out by Porr (2005, p. 77). Until recently, however, they have been considered almost exclusively in the context of “artefacts as a functional form that varies sometimes according to raw material considerations and is manufactured with a recurrent technology within broader parameters” (Ashton and McNabb 1993, p. 190). But the fact that the manufacture of such tools continued for some 1.25 Myr indicates their importance, most probably not only as cutting and/or scavenging weapons (Domı´nguezRodrigo 2002) but also as social indicators independent of their functional meaning(s). According

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_24-3 # Springer-Verlag Berlin Heidelberg 2013

Fig. 3 Variation among lower Paleolithic biface assemblages of Eastern Asia and South Asia. The dashed line represents the Movius Line, the traditional demarcation between Mode 1 (Oldowan) and Mode 2 (Acheulean) industries (After Petraglia 1998, Fig. 11.8)

to Draper (1985, p. 7), “we could imagine a situation where an Early Paleolithic hominid might have fabricated a portable cutting tool for scavenging remnant meat from carnivore kills” that “was produced because a Middle Pleistocene knapper . . . was disposed to work stone in a way that produced an object we call a handaxe” (Hopkinson and White 2005, p. 21). The high variability (Sinclair and McNabb 2005, p. 185), the typological and dimensional characteristics (Isaac 1977), their eventual hafting (Ling 2011), and the “wide temporal and geographic distribution” (Wynn 1995, p. 11) of these tools have been noted by many authors, but from different perspectives and with different aims (Bordes 1968, p. 23; Camps 1979; Petraglia 1998, p. 371; McNabb et al. 2004; Hopkinson and White 2005) (Figs. 3 and 4). In Asia, their distribution covers a well-defined region, delimited in the east and the north by the so-called Movius Line (Movius 1944, p. 103), more of a “veil” than a real line according to Otte (2010, p. 274). This “line” is still nowadays often employed to mark the limit between hand axe and other technologies with no evidence of bifacial tools, like the Soanian of northern Pakistan (De Terra and Paterson 1939; Paterson and Drummond 1962), though bifacial tools are recorded from its more recent period of development (Graziosi 1964, p. 12), or the Anyathian of Burma (De Terra and Movius 1943) to make two well-known examples often referred to very different chronological periods of the Paleolithic. In this respect, the discovery of undated bifacial forms in Australia is intriguing and might possibly help clarify some aspects of their manufacture, meaning, and function (Brumm and Rainey 2011). Although the complexity involved in the production of the lithic artifacts has been openly questioned (Hassan 1988, p. 281), and analysis of manufacturing techniques and debitage dispersal (Andrefsky 2007) across the earliest Paleolithic sites (Gowlett 2005; Petraglia et al. 2005) is still rarely applied by the field archaeologists, a few interesting exceptions should be mentioned. Among these is the MNK chert factory site in the Olduvai Gorge (Tanzania), which is dated to some 1.6 Myr ago. Here chipped stone artifacts, obtained from both local and imported raw materials, show a complex sequence of activities carried out by “early man working a raw material chosen for its technological properties brought to a central locality from diverse sources” (Stiles Page 5 of 25

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Fig. 4 Different categories of hand axes according to the typological classification proposed by Camps (1979): different types of a flat bifacials, b thick bifacials, c diverse bifacials, and d hachereaux (After Broglio 1998, Fig. 22)

et al. 1974). FxJi50, in north Kenya, is a site 1.5 Myr old that “consists of a patch of stone artefacts interspersed with broken-up fragments of bone” (Bunn et al. 1980, p. 111), whose precise function is still difficult to define. The chipped stone assemblage, which is composed of flaked cobbles and flakes partly obtained on the spot, “has proved to consist of several dense clusters of material that interconnect with each other” (Bunn et al. 1980, p. 114). This is one of the earliest Paleolithic sites from which “the close association (of bones) with artefacts and the presence of butchering marks suggest that the toolmakers were the first accumulating agency” (Bunn et al. 1980, p. 125). This picture is rather unusual, if we consider that “for most of the sites excavated and reported we do not have certain indications of any specific activities that characterize them, and in very few instances has localization of subsidiary tool kits within a floor even been claimed” (Isaac 1972, p. 185) and that the interpretation of the variability of the spatial distribution pattern of the tools (Whallon 1973, p. 117) within a site surface is often difficult (Keeley 1991, p. 258). Experimental studies have also been made especially regarding hand-axe production employing different techniques and raw materials and using both hard and soft hammerstones (Madsen and Goren-Inbar 2004). Page 6 of 25

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Fig. 5 Ziara¯t Pir Shaba¯n on the Rohri Hills (Sindh, Pakistan): The Acheulean hand-axe factory ZPS1 before excavation (Photograph by P. Biagi)

Raw Material, Workshops, and Quarries When detailed recording methods have been applied, as for instance in the case of some localities excavated in the Indian subcontinent, they have revealed that characteristic tools, among them hand axes, cores, hammerstones, and different dimensional classes of debitage flakes, systematically cluster in well-defined spots (see Pappu 2001, pp. 25–54; Paddayya et al. 2002, p. 646). This fact is useful in helping us understand the development of the manufacturing areas within the site and the steps followed by the toolmakers during the production process (Hansen and Madsen 1983, p. 51), especially when refitting methods are applied to the entire complex (Bergman et al. 1990, p. 280). This is the case for the some Acheulean sites where different varieties of raw materials for tool production were available, including siliceous limestone (Isampur in India: Petraglia et al. 2005) and good-quality chert from local outcrops (Rohri Hills in Sindh [Pakistan]: Biagi et al. 1996). The evidence available from the latter shows that the waste products of large hand-axemanufacturing workshops were scattered along the edges of circular sandy areas representing zones that were comprehensively cleared of limestone and chert boulders in Paleolithic times, before the manufacturing activities took place. For instance, the excavations carried out at Ziara¯t Pir Shaba¯n 1 (Fig. 5), one of the many Acheulean workshops discovered on the Rohri Hills that were exclusively devoted to the production of hand axes (Biagi et al. 1996) (Fig. 6), have demonstrated that the perfect, finished bifaces were exclusively transported elsewhere, most probably to camps located in the adjacent Great Indian Desert that are at present buried beneath meters of sand inside thick, stabilized dunes (Misra and Rajaguru 1989). The maximum transfer distance is not known, due to the absence of any detailed research in the Thar Desert to the east of the hills, although the African parallels indicate transport between 15 and 100 km (Petraglia et al. 2005, p. 208). A situation similar to that of the Rohri Hills is known at Ongar, near Hyderabad in lower Sindh (Pakistan), where Acheulean workshops were discovered lying on the top of flat limestone mesas (Figs. 7 and 8). These deposits, very rich in seams of excellent chert, were exploited throughout the entire Paleolithic period, from the Acheulean onward (Biagi 2006, 2008). As far as these two latter cases in Sindh are concerned, there is no doubt that the abundance of excellent, workable raw material played a fundamental role in attracting prehistoric populations at least since the Acheulean period (Biagi and Cremaschi 1988, p. 425). The chert used by the earliest Page 7 of 25

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Fig. 6 Ziara¯t Pir Shaba¯n on the Rohri Hills (Sindh, Pakistan): Acheulean hand-axe rough-outs on the surface of workshop ZPS1 (Photograph by P. Biagi)

Paleolithic people was collected from large boulders or extracted from the top of the limestone terraces, as supported by the evidence from accurate surveys carried out along the top of the mesas that did not reveal any trace of Early Paleolithic mining activities. As far as we know, the first Paleolithic chert quarries were opened by Acheulean populations, both in the Levant (Gopher and Barkai 2011) and Upper Egypt, much earlier than until recently supposed (Smolla 1987, p. 129). According to Vermeersch et al. (1995, p. 22), “a few kilometres south of the Dandara temple . . .a. . . hill was clearly subjected to chert extraction by Acheulian people,” given the presence of an extractive pit discovered during the excavation of a small trench in an area rich in Late Acheulean tools. In contrast, almost nothing is known of Acheulean raw material procurement systems in this region, which yielded abundant traces of Middle and Upper Paleolithic flint-mining activities (Vermeersch et al 1997, p. 191).

Fig. 7 Ongar (Sindh, Pakistan): C-shaped Acheulean chert factory area (Photograph by P. Biagi) Page 8 of 25

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Fig. 8 Ongar (Sindh, Pakistan): In situ chert flakes concentration in an Acheulean workshop (Photograph by P. Biagi)

Habitation and Other Structural Remains Early Paleolithic Mode 1 and 2 sites are often characterized by “concentrations of debris, . . . which. . . have usually been interpreted to be the result of various processual phenomena” (Stiles 1998, p. 133). Only a few of them, of varied chronology, have provided us with complex archaeological evidence (see, for instance, Pappu 2001). In Africa, we know that most of the earliest settlements were located in environments close to lake shores or, more commonly, along (former) river courses (Isaac 1976, Fig. 3.3) (Fig. 9). They have been interpreted as sites that are inhabited during only one season, whose remaining components, mainly lithic artifacts and bones, show they had been planned (Binford 1989a, p. 469). The 1.75-Myr-old Mode 1 site of DK, in Lower Bed I of the Olduvai Gorge (Leakey 1971, p. 24, Fig. 7), yielded evident traces of man-made features, the most important of which consists of a circular structure of lava blocks, some 4.5 m in diameter (Fig.10), that the excavator interpreted as

Fig. 9 Schematic representation of a portion of landscape frequented by tool-using hominids, with the locus of discarded artifacts marked X (After Isaac 1976, Fig. 3.3) Page 9 of 25

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Fig. 10 Olduvai Gorge, site DK (Tanzania): Plan of the stone circle and the remains of the occupation surface: Stone artifacts shown in black, bones in outline (After Leakey 1971, Fig. 7)

resembling “temporary structures often made by present-day nomadic peoples who build a low stone wall round their dwellings to serve either as windbreak or as a base to support upright branches which are over and covered with either skin or grass” (Leakey 1971, p. 24). The excavations carried out at Gombore´ I, another Mode 1 site located at Melka Konture´ in Ethiopia, brought to light a 230 m2 living floor composed of rounded pebbles and rich in stone tools and faunal remains, with a central empty space of some 10 m2. The settlement, which has been dated at some 1.6 Myr ago, yielded a “higher platform . . . that . . . could have been roughly adapted for a shelter made of branches and animal skins” (Chavaillon 2004, p. 263). The research carried out at this site revealed the occurrence of “small stone circles aligned north-south in the eastern sector . . . whose . . . external diameter . . . varies from 20 to 40 cm,” which were interpreted as possible “wedging stones for pegs set in rather hard soil” (Chavaillon and Chavaillon 2004, p. 448), similar to those recorded from Garba XII in the same region. Recent radiometric dates obtained from a few Early Paleolithic localities in the area revealed a sequence of habitation covering a long period comprised between 1.7 and 0.7 Myr ago (Morgan et al. 2012, p. 108). Among the Mode 2 sites, extremely interesting and perfectly preserved remains were brought to light at Isernia La Pineta in Molise (Southern Italy). The chronology of this site is still rather controversial (Mussi 2001, p. 44), although the new radiometric dates indicate that the locality extends over an area of some 30,000 m2 and is some 0.60 million years old (Coltorti et al. 2005, p. 19), roughly contemporary with Notarchirico in the same region of central Italy (Orain et al. 2013). It yielded traces of four different occupation layers from which more than 10,000 lithic artifacts, chipped from different raw materials, including limestone and chert from diverse sources, were collected (Peretto 1994a). The site was located along the shores of a lake basin that was later buried

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Fig. 11 La Pineta (Isernia, Southern Italy): A general view of the semicircular animal bones and material culture remains concentration surrounded by limestone boulders, discovered in 1980 (Photograph by P. Biagi)

by fluvial sediments. The most interesting structural remains were discovered during the beginning of the excavations, when an accumulation of animal bones and stone tools was uncovered on an almost semicircular paleosurface that was very rich in remains of Bison skulls and horns and Rhinoceros cranial bones and was delimited by large, travertine boulders (Giusberti et al. 1983, p. 100) (Figs. 11, 12 and 13). These discoveries might help interpret the spatial variability and activities carried out within this settlement site (Bartram et al. 1991). Remarkable differences have been noted among the lithic assemblages excavated in different areas of the site, both in the raw material employed for producing artifacts and in the typology and dimension of the stone tools (Fig. 14) (Peretto 1983, p. 81). For example, while flint was mainly used to obtain flakes, limestone was employed for the production of pebble tools, often characterized by the removal of just a few flakes from the distal edge (Peretto 1994b). Traceological studies and the experimental

Fig. 12 La Pineta (Isernia, Southern Italy): Bison skull and long bone fragment from the main semicircular concentration discovered in 1980 (Photograph by P. Biagi) Page 11 of 25

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Fig. 13 La Pineta (Isernia, Southern Italy): Plan of the concentration of Fig. 11: a travertine, b pebbles, c faunal remains, d limestone tools, e flint tools, f red lacquerings (After Giusberti et al. 1983)

reproduction of the tool types and their chaine operatoire have shown that small flakes were the most important tools of the Isernia inhabitants, while denticulates that represent some 90 % of the total assemblage are in effect only core waste residuals (Crovetto et al. 1993). In central Italy, an interesting Mode 2 site dated to slightly later than 0.5 Myr ago, and with an assemblage consisting of both elephant long bones and stone bifacial hand axes, has been excavated at Fontana Ranuccio (Biddittu et al. 1979). The presence of bone hand axes is unique to the area (Biddittu 1982), where they become increasingly more common at the slightly later Mode 2 sites, like Castel di Guido in Latium (Radmilli and Boschian 1996), where the use of elephant carcass bones for making tools has been analyzed in detail (Sacca` 2012).

Fig. 14 La Pineta (Isernia, Southern Italy): Limestone choppers from the surface of the main semicircular concentration (Photograph by P. Biagi) Page 12 of 25

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Fig. 15 Bilzingsleben (Germany): Plan of the structuration of the Early Paleolithic camp: a limits of the excavated area, b geological fault lines, c shoreline, d sandy travertine sediments, e alluvial fan, f activity area at the lake shore, g outlines of living structures, h workshop areas, i special workshop area with traces of fire use, j circular paved area, k charcoal, l bone anvils, m stone with traces of heat, n bones with intentional markings, o linear arrangement of stones, p elephant tusk, q human skull fragments, r human tooth (After Mania and Mania 2005, Fig. 7.1)

Moving westward, the importance of the remains of structures brought to light by H. de Lumley (1966) at Terra Amata, near Nice, in Provence, is represented by a shallow, oval-shaped hut floor attributed to a Mode 2 group of people who inhabited the region around 0.4 Myr ago. Apart from the exceptional discovery of an almost “intact” habitation structure, the site is important because it yielded the first evident traces of a hearth indicating the use of fire by Paleolithic humans in Europe (de Lumley and de Lumley 2011, p. 41). Traces of fire that have long been suggested from a few Lower Pleistocene sites in East Africa (Clark and Harris 1985; Perle`s 1977) are known since some 0.8 Myr ago in Israel (Goren-Inbar et al. 2004), although the reanalysis of 30 Paleolithic sites made a few years before had suggested that controlled fires are not earlier than 0.3 Myr ago, most probably associated with very late Homo erectus (James 1996, p. 66) whether this taxonomy is still acceptable according to the new findings (Wagner et al. 2007). The site of Steinrinne near Bilzingsleben, in central Germany, is of extreme importance for the study of Mode 2 hominids, although the interpretation of its stratigraphy, some 1 m thick, is still debated (Mania and Mania 2005; M€ uller and Pasda 2011), as well as its chronology, which is referred, according to the different authors, either to 0.42–0.35 Myr ago or 0.25–0.20 Myr ago. The remains of three circular hut foundations, 3–4 m in diameter, with entrances systematically facing southeast and with workshop areas and fireplaces, have been discovered at this camp, dated to some 0.37 Myr ago (Fig. 15). The importance of this site is indicated by the occurrence of the earliest so far known intentionally decorated bone objects that suggest “non-utilitarian behaviours . . . connected to reflexive thinking” (Mania and Mania 2005, p. 110), as well as the indisputable traces

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of what is claimed to be a ritual paved area “with human skull fragments smashed in macerated condition” (Mania and Mania 2005, p. 113). According to Mania and Mania (2005, p. 114), these discoveries demonstrate that “Homo erectus was therefore a human being that had a fully developed mind and culture, capable in creating his own socio-cultural environment with living structures, the use of fire and special activity areas,” although other authors prefer to attribute the finds to Homo heidelbergensis (Henke and Hardt 2012). This also finds confirmation in the traces of Acheulean “art” both in Africa (Bednarik 2003) and in the Indian subcontinent (Bednarik 1990). Gran Dolina at Atapuerca in Spain is an even earlier multilayered site, where some kind of ritual activity has been supposed to have taken place. The site yielded 150 human bone fragments, which have been attributed to four individuals, classified into the new form Homo antecessor. Some of the hominid remains from Layer TD6, datable to at least 0.78 Myr ago (Falgue`res et al. 1999), “show clear cut marks which have been interpreted as evidence of cannibalism” (Mosquera Martı´nez 1998, p. 17). The chipped stone assemblage from this layer is characterized by relatively small artifacts, among which are utilized flakes, scrapers, denticulates, debitage flakelets, and byproducts suggesting the presence of a living floor where different activities had been performed (Carbonell et al. 1999). Returning to Mediterranean France, this region is very rich in Lower Paleolithic sites, both open air and in caves. Among the latter, the internal deposits of Lazaret Cave (de Lumley 1969), a late Mode 2 Acheulean site attributed to some 0.12 Myr ago, yielded traces of a unique hut structure that has been reconstructed, thanks to the occurrence of stone walls, fireplaces, and “masses of seaweeds possibly used as bedding for site occupants” (Mellars 1995, p. 285). Although this site does not represent the earliest known evidence of cave structural remains in Eurasia, given the traces of much older man-made stonewalls in China (Fang et al. 2004, Fig. 3) and Central Europe (Cyrek 2003, Fig. 6), Lazaret is the only one from which a detailed reconstruction of the events that took place inside the cave in Late Acheulean times has so far been possible (de Lumley and de Lumley 2011, p. 54).

Hunting Weapons Although, as mentioned earlier, the excavations carried out at Terra Amata in the 1960s had already revealed the presence of one single fireplace, the almost contemporary hunting site of Scho¨ningen, in North Germany, yielded not only the remains of four hearths, one of which is some 1 m in diameter, but even a charred wooden stick, which might “have functioned as a firehook to feed the fire as well as a spit to roast, and also smoke, strips or pieces of meat” (Thieme 2005, p. 127). This site is extremely important because of the occurrence of both the hunting weapons and the other wooden tools brought to light since 1994, which have radically revolutionized our view of the hunting methods and strategies followed by these hominids. The widely accepted view that early Homo was unable to conceive and construct throwing weapons is contradicted by the discovery of sophisticated spears, longer than 2 m, which suggest a long tradition in wood shaping and weapon craftsmanship showing that, in contrast to what was previously supposed, this species had already acquired that complex “sequence pattern of behavioural complexes” (Laughlin 1968, p. 305) commonly labeled hunting, which represent “a way of life . . . that . . . has dominated the course of human evolution for hundreds of thousands of years” (Washburn and Lancaster 1968, p. 293). More precisely, “Homo erectus in the Middle Pleistocene was fully capable of organising, coordinating and successfully executing the hunting of big game animals in a group using longdistance weapons” (Thieme 2005, p. 127). Although the Scho¨ningen specimens are not the only Page 14 of 25

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wooden pointed tools so far recovered from an Early Paleolithic site in Europe (Conard 2007, p. 2008), they undoubtedly represent the best preserved specimens discovered within a horse-hunting camp, a surface of some 3,500 m2 of which has already been excavated. Furthermore, it is important to point out that already in the 1980s, Isaac (1984, p. 17) had considered the use of throwing weapons by early hominids when he wrote “if the Lower Pleistocene tool-making hominids were hunting with equipment, they must have been using spears without stone tips (i.e. pointed staves or horns on staves), clubs, and, perhaps most important of all, thrown sticks and stones,” given that “none of the flaked stone artefacts can plausibly be regarded as ‘weapons’” (!). In effect, it has been widely demonstrated that stone hand axes and cleavers (see, for instance, Gilead 1973) are excellent butchering tools, but not hunting weapons, and, in particular, that “the sinuous retouched edge of a hand-axe retains its meat-cutting efficiency longer than a plain flake edge” (Isaac 1984, p. 15).

Conclusion Apart from the factors mentioned in the introduction, there are many others that make remains of early structures difficult to interpret. Among these are (1) the impossibility of “detailed” radiometric dating of the events that took place at short-term habitation sites, given that hunters periodically moved from site to site following their subsistence strategies (Binford 1978a, 1980), and (2) the difficulty of proving the supposed contemporaneousness of the structural remains within an apparently “homogeneous” area (Binford 1982). This is true even though it is widely assumed that “in inspecting the contents of a single structure, we can be fairly confident that the associated assemblage was all in use at one time, if not made at the same time” (Deetz 1968, p. 283). Besides the two above-mentioned factors, there are three others of major importance regarding (1) the complete excavation of an occupation unit, an enterprise that has been successfully undertaken only on very few occasions (Clark 1968, p. 277), (2) the functional nature of the (seasonal) site itself (Hehmsoth-Le Moue¨l 1999, p. 81), and (3) the eventual impact of scavengers on the bone remains originated by human activity (Binford et al. 1988). With the exception of a limited number of cases reported by Clark for East Africa, and a few others which have been described in the preceding chapters, most sites are characterized by more or less dense concentrations of stone artifacts and bones, often closely related to each other (Binford 1989b, p. 459) although differently disposed according to the activities performed (Stevenson 1991, p. 280), reflecting “a complex system of extraction, manufacture, transport, use, resharpening, re-use, renewed transport and eventual discard” (Isaac 1986, Fig. 15.6). Often, these have been subjected to a certain degree of weathering or represent a (complicated) sequence of depositional events that took place over a period of millennia, forming archaeological palimpsests (Hosfield 2005). Isaac (1968, p. 255) classified such concentrations in three main categories according to the vertical and/or horizontal diffusion of the stone tools. The first two of these “represent sporadic, intermittent occupations of great duration,” while the third “can probably be interpreted as fairly stable ‘home base.’” Finally, ethnographic analogies are sometimes uncritically accepted by both archaeologists and anthropologists, who often believe “that modern representatives of past stages of cultural development exist” (Freeman 1968, p. 263), sometimes they are simply unaccepted, considered to be unreliable and nonscientific (Hodder 1982, p. 14), even though “any consideration of the implications for archeological interpretation of new ethnographic data . . . requires an examination of the

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general relationships between ethnographic observations and archeological reasoning” (Binford 1968).

Cross-References ▶ Adaptations, Frontiers, and New Territories ▶ Archaeology ▶ Charles Darwin, Paleoanthropology, and the Modern Synthesis ▶ Cultural Evolution in Africa and Eurasia During the Middle and Late Pleistocene ▶ Defining Homo erectus ▶ Defining the Genus Homo ▶ Historical Overview of Paleoanthropological Research ▶ Homo ergaster and Its Contemporaries ▶ Neanderthals and Their Contemporaries ▶ Origin of Modern Humans ▶ Overview of Paleolithic Archeology

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Isaac GLI (1986) Foundation stones: early artefacts as indicators of activities and abilities. In: Bailey GN, Callow P (eds) Stone Age prehistory. Cambridge University Press, Cambridge, pp 221–241 James SR (1996) Early Hominid use of fire: recent approaches and methods for evaluation of the evidence. In: Bar-Yosef O, Cavalli-Sforza LL, March RJ, Piperno M (eds) The Lower and Middle Palaeolithic. XIII international congress of prehistoric and protohistoric sciences Forlı` – Italia – 8/14 September 1996. Section 5 – The Lower and Middle Palaeolithic. A.B.A. C.O., Forlı`, pp 65–76 Keeley LH (1991) Tool use and spatial patterning. Complications and solutions. In: Kroll EM, Price TD (eds) The interpretation of archaeological spatial patterning. Plenum Press, New York/ London, pp 257–268 Lamdin-Whymark H (2009) Sir John Evans: experimental flint knapping and the origin of lithic research. Lithics 30:45–52 Laughlin WS (1968) Hunting: an integrating biobehavior system and its evolutionary importance. In: Lee RB, De Vore I (eds) Man the hunter. Aldine, New York, pp 304–320 Leakey MD (1971) Olduvai Gorge. Excavations in beds I & II 1960–1963. Cambridge University Press, Cambridge Ling V (2011) The Lower Palaeolithic colonisation of Europe: antiquity, magnitude, permanency and cognition. BAR international series 2316. Archaeo Press, Oxford Lordkipanidze D, Vekua A (2006) Unique discoveries of ancient hominid fossils in Dmanisi (Eastern Georgia). Archaeol Caucasia 1:55–64 Lubbock J (1870) The origin of civilisation and the primitive condition of man. Longmans, Green, London Madsen B, Goren-Inbar N (2004) Acheulian giant core technology and beyond: an archaeological and experimental case study. Eurasian Prehistory 2(4):3–52 Magnani P (ed) (2007) Gaetano Chierici. Tutti gli Scritti di Archeologia. Diabasis, Reggio Emilia Mania D, Mania U (2005) The natural and socio-cultural environment of Homo erectus at Bilzingsleben, Germany. In: Gamble C, Porr M (eds) The hominid individual in context. Archaeological investigations of Lower and Middle Palaeolithic landscapes, locales and artefacts. Routledge, London/New York, pp 98–114 McNabb J (2009) The knight, the grocer, and the chocolate brownies; Joseph Prestwich, Benjamin Harrison and the second “antiquity of man” debate. In: Hosfield RT, Wenban-Smith FF, Pope MI (eds) Great prehistorians: 150 years of palaeolithic research, 1859–2009. Lithic Studies Society, London, Lithics 30:97–115 McNabb J, Binyon F, Hazelwood L (2004) The large cutting tools from the South African Acheulean and the question of social traditions. Curr Anthropol 45(5):653–677 Mellars P (1995) The Neanderthal legacy. An archaeological perspective from Western Europe. Princeton University Press, Princeton Misra VN, Rajaguru SN (1989) Palaeoenvironments and prehistory of the Thar Desert, Rajasthan, India. In: Frifelt K, Sørensen R (eds) South Asian archaeology 1985. Scandinavian Institute of ˚ rhus, pp 296–320 Asian studies occasional papers 4. A Morgan LE, Renne PR, Kieffer G, Piperno M, Gallotti R, Raynal J-P (2012) A chronological framework for a long and persistent archaeological record: Melka Kunture, Ethiopia. J Hum Evol 62:104–115 Mosquera Martı´nez M (1998) Differential raw material use in the Middle Pleistocene of Spain. Evidence from Sierra de Atapuerca, Torralba, Ambrona and Aridos. Camb Archaeol J 8(1):15–28 Page 21 of 25

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Movius HL Jr (1948) The Lower Palaeolithic cultures of Southern and Eastern Asia. Trans Am Philos Soc New Series 38(4):330–420 Movius HL Jr (1944) Early man and Pleistocene stratigraphy in Southern and Eastern Asia. Papers of the Peabody Museum of American Archaeology and Ethnology, Harvard University. XIX (3):7–125 M€uller W, Pasda C (2011) Site formation and faunal remains of the Middle Pleistocene site Bilzingsleben. Quarta¨r 58:25–49 Mussi M (2001) Earliest Italy. An overview of the Italian Paleolithic and Mesolithic. Kluwer Academic/Plenum, New York/Boston/Dordrecht/London/Moscow Nioradze M, Nioradze G (2011) Early Palaeolithic site of Dmanisi and its lithic industry. Archaeol Caucasus 4:103–147 (in Russian) Orain R, Lebreton V, Russo Ermolli E, Se´mah S, Shao Q, Bahain J-J, Thun Hohenstein U, Peretto C (2013) Hominin responses to environmental changes during the Middle Pleistocene in Central and Southern Italy. Clim Past 9:687–697 Otte M (2000) Recherches re´centes sur le Pale´olithique Infe´rieur d’Asie. In: Lordkipanidze D, BarYosef O, Otte M (eds) Early humans at the Gates of Europe, vol 92. ERAUL, Lie`ge, pp 107–111 Otte M (2010) Before Levallois. Quat Int 223–224:273–280 Paddayya K, Blackwell BAB, Shaldiyal R, Petraglia MD, Fevrier S, Chaderton DA II, Blickstein JIB, Skinner AR (2002) Recent findings of the Acheulian of the Hunsgi and Baichbal valleys, Karnataka, with special reference to the Isampur excavation and its dating. Curr Sci 83(5):641–647 Pappu RS (2001) Acheulian culture in Peninsular India. DK Printworld, New Delhi Paterson TT, Drummond HJH (1962) Soan the Palaeolithic of Pakistan. Department of Archaeology, Government of Pakistan, Ferozsons, Karachi Peretto C (1983) Le industrie litiche di Isernia La Pineta. In: Isernia La Pineta un accampamento piu` antico di 700.000 anni. Calderini, Bologna, pp 81–93 Peretto C (1994a) Il Giacimento Paleolitico. In: Peretto C (ed) Le industrie litiche del giacimento Paleolitico di Isernia La Pineta: La tipologia, le tracce di utilizzazione, la sperimentazione. Cosmo Iannone, Isernia, pp 29–40 Peretto C (1994b) Le industrie liitche. Conclusioni di carattere generale e riassuntivo. In: Peretto C (ed) Le industrie litiche del giacimento Paleolitico di Isernia La Pineta: La tipologia, le tracce di utilizzazione, la sperimentazione. Cosmo Iannone, Iserbnia, pp 453–460 Peretto C, Amore FO, Antoniazzi A, Bahain J-J, Cattani L, Esposito P, Falgue`res C, Gagnepain J, Hedley J, Laurent M, Lebreton L, Longo L, Milliken S, Vanucci S, Verrge´s JM, Wagner JJ, Yokoyama Y (1999) L’industrie lithique de Ca’ Belvedere di Monte Poggiolo. Stratigraphie, matie`re premie`re, typologie, remontages et traces d’utilisation. L’Anthropologie 102:1–120 Perle`s C (1977) Pre´histoire du feu. Masson, Paris Petraglia MD (1998) The Lower Palaeolithic of India and its bearing on the Asian record. In: Petraglia MD, Korisettar R (eds) Early human behaviour in global context. The rise and discovery of the Lower Palaeolithic record. One world archaeology. Unwin Hyman, Boston/ Sidney/Washington, pp 343–390 Petraglia MD (2003) The Lower Palaeolithic of the Arabian Peninsula: occupations, adaptations, and dispersal. J World Prehistory 17(2):141–179. New York/London Petraglia MD (2007) Mind the gap: factoring the Arabian peninsula and the Indian subcontinent into Out of Africa models. In: Mellars P, Boyle K, Bar-Yosef O, Stringer C (eds) The human revolution revisited. McDonald Institute Archaeological, Cambridge, pp 671–684

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Petraglia MD, Shipton C, Paddaya K (2005) Life and mind in the Acheulean. A case study from India. In: Gamble C, Porr M (eds) The hominid individual in context. Archaeological investigations of Lower and Middle Palaeolithic landscapes, locales and artefacts. Routledge, London/ New York, pp 197–219 Pigorini L (1866) Paleoetnologia. Annuario Scientifico Industriale II:211–250 Porr M (2005) The making of the biface and the making of the individual. In: Gamble C, Porr M (eds) The hominid individual in context. Archaeological investigations of Lower and Middle Palaeolithic landscapes, locales and artefacts. Routledge, London/New York, pp 68–80 Prestwich J (1860) On the occurrence of flint implements, associated with the remains of animals of extinct species in beds of the late geological period, in France at Amiens and Abbeville, and in England at Hoxne. Philos Trans R Soc Lond 150:277–317 Radmilli AM, Boschian G (1996) Gli scavi a Castel di Guido. Origines. Istituto Italiano di Preistoria e Protostoria, Firenze Regazzoni I (1885) Paleoetnologia. Hoepli, Milano/Napoli/Pisa Rightmire P (2007) Later Middle Pleistocene Homo. In: Henke W, Tattersall I (eds) Handbook of paleoanthropology, vol III, Phylogeny of hominids. Springer, Berlin/Heidelberg/New York, pp 1695–1715 Roebroeks W, van Kolfschoten T (1994) The earliest occupation of Europe. Antiquity 68(260):489–503. Cambridge Rose JI, Petraglia MD (2009) Tracking the origin and evolution of human population in Arabia. In: Petraglia MD, Rose JI (eds) The evolution of human populations in Arabia. Springer, Netherlands, pp 1–12 Sacca` D (2012) Taphonomy of Palaeloxodon antiquus at Castel di Guido (Rome, Italy): proboscidean carcass exploitation in Lower Palaeolithic. Quat Int 276–277:24–71 Santonja M, Villa P (1990) The Lower Palaeolithic of Spain and Portugal. J World Prehistory 4(1):45–94. New York and London Sinclair A, McNabb J (2005) All in a day’s work. Middle Pleistocene individuals, materiality and the lifespace at Makapansgat, South Africa. In: Gamble C, Porr M (eds) The hominid individual in context. Archaeological investigations of Lower and Middle Palaeolithic landscapes, locales and artefacts. Routledge, London/New York, pp 176–194 Smolla G (1987) Prehistoric flint mining: the history of research: a review. In: Newcomer MH, de G Sieveking G (eds) The human uses of flint and chert. Cambridge University Press, Cambridge, pp 127–129 Stekelis M, Bar-Yosef O, Schick T (1969) Archaeological excavations at Ubeidiya, 1964–1966. Israel Academy of Sciences and Humanities, Jerusalem Stevenson MG (1991) Beyond the formation of hearth-associated artifact assemblages. In: Kroll EM, Price TD (eds) The interpretation of archaeological spatial patterning. Plenum Press, New York/London, pp 269–299 Stiles DN (1998) Raw material as evidence for human behaviour in the lower palaeolithic Pleistocene: the Olduvai case. In: Petraglia MD, Korisettar R (eds) Early human behaviour in global context. The rise and discovery of the Lower Palaeolithic record. One world archaeology. Unwin Hyman, Boston/Sydney/Washington, pp 133–150 Stiles DN, Hay RL, O’Neil JR (1974) The MNK chert factory site, Olduvai Gorge, Tanzania. World Archaeol 5(3):285–308 Tarantini M (2012) La nascita della Paletnologia in Italia (1860–1877). Quaderni del Dipartimento di Archeologia e Storia delle Arti, Sezione Archeologia – Universita` di Siena. All’Insegna del Giglio, Firenze Page 23 of 25

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Thieme H (2005) The Lower Palaeolithic art of hunting. In: Gamble C, Porr M (eds) The hominid individual in context. Archaeological investigations of Lower and Middle Palaeolithic landscapes, locales and artefacts. Routledge, London/New York, pp 115–132 Toro-Moyano I, de Lumley H, Barsky D, Celiberti V, Cauche D, Moncel M-H, Fajardo B, Toro M (2003) Las industria lı´ticas de Barranco Leo´n y Fuenta Nueva 3 de Orce. Estudio te´cnico y typolo´gico. Ana´lisis traceolo´gico. Resultados preliminaires. In: El Pleistocenico Inferior de Barranco Leo´n y Fuenta Nueva 3, Orce (Granada). Memoria cientifı´ca campan˜as 1999–2002. Archeologı´a monografı´as, Junta de Andalucı´a, Consejerı´a de, Cultura, pp 183–206 Toth N, Schick K (2007) Overview of palaeolithic archeology. In: Henke W, Tattersall I (eds) Handbook of paleoanthropology, vol III, Phylogeny of hominids. Springer, Berlin/Heidelberg/ New York, pp 1943–1963 Vekua A, Lordkipanidze D, Bukhsianidze M (2011) Dmanisi – the oldest Eurasian site of fossil hominines. Archaeol Caucasus 4:16–94 (in Russian) Vermeersch PM, Paulissen E, Van Peer P (1995) Palaeolithic chert mining in Egypt. Archaeol Polona 33:11–30. Warsaw Vermeersch PM, Paulissen E, Stokes S, Van Peer P, De Bie M, Steenhoudt F, Missotten S (1997) Middle Palaeolithic chert mining in Egypt. In: Ramos-Milla´n A, Bustillo MA (eds) Siliceous rocks and culture. Monogra´fica Arte y Arqueologı´a, vol 42. Universidad de Grenada, pp 173–193 von Strobel V (1998) Universita¨tsprofessor Dr.Dr. Peregrin von Strobel Naturwissenschaftler zwischen Europa und der neuer Welt. In Various Authors (eds) Pellegrino Strobel (1821–1895) Omaggio nel Centenario della morte. Pubblicazione del Museo di Storia Naturale. Universita` di Parma, vol 9, pp 21–31 Wagner GA, Rieder H, Zo¨ller L, Mick E (eds) (2007) Homo heidelbergensis. Schl€ usselfund der Menschheitsgeschichte. Konrad Theiss, Stuttgart Washburn SL, Lancaster CS (1968) The evolution of hunting. In: Lee RB, De Vore I (eds) Man the hunter. Aldine, New York, pp 293–303 Whalen NM, Fritz GA (2004) The Oldowan in Arabia. Adumatu 9(1):7–18. Riyadh Whalen NM, Pease DW (1991) Archaeological surveys in southwest Yemen. Pale´orient 17(2):127–131 Whalen NM, Zoboroski M, Schubert K (2002) The Lower Palaeolithic in southwestern Oman. Adumatu 5(1):27–34. Riyadh Whallon R Jr (1973) Spatial analysis of palaeolithic occupation areas. In: Renfrew C (ed) The explanation of culture change. Models in prehistory. Duckworth, London, pp 115–130 Wynn T (1995) Handaxes enigmas. World Archaeol 27(1):10–24

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Index Terms: Chipped stone assemblages_4, 7 Chipped stone assemblages bifacial tools_4 Chipped stone assemblages raw material, workshops, and quarries_7 Hunting weapon_14 Paleoethnology_1–4, 9, 14–15 Paleoethnology Arabian Peninsula_3 Paleoethnology chipped stone assemblages_4 Paleoethnology Dmanisi_4 Paleoethnology factors_15 Paleoethnology habitation_9 Paleoethnology hunting weapon_14 Paleoethnology stone tool technotypological variability_2

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_26-5 # Springer-Verlag Berlin Heidelberg 2013

General Principles of Evolutionary Morphology Gabriele A. Macho* Research Laboratory for Archaeology (RLAHA), University of Oxford, Oxford, England

Abstract Anthropologists analyzing morphology for phylogenetic, functional, or behavioral purposes are confronted by a plethora of obstacles. Morphology is not free to vary but is subject to a number of constraints, which may be historical, developmental, and/or functional, while equivalency in function can be achieved by different means. This, together with the fact that the fossil record is scant, confounds meaningful interpretation of phylogenetic pathways and the reconstruction of function and behavior from fossilized remains. To overcome these difficulties, paleoanthropology is becoming increasingly inter- and multidisciplinary, whereby researchers draw on, and incorporate, approaches and findings obtained in other, sometimes very diverse, disciplines. This contribution briefly reviews the constraints acting on morphology, the limitations faced when interpreting form/function and behavior from morphology, and the different approaches currently explored in paleoanthropology to obtain a better understanding of hominin paleobiology. While offering exciting new possibilities, researchers should however be mindful of the limitations inherent in new technologies.

Introduction With rare exceptions (e.g., endocasts, footprints, permafrost remains, peat bodies), only the hard tissues of the body become fossilized. Phylogenetic, functional, and behavioral interpretations of extinct taxa are thus almost exclusively based on analyses of bones and teeth. Yet, fossil remains are mostly incomplete and distorted, while taphonomic biases prevent a good representation of all parts of the body and/or functional units for detailed analyses (chapter “▶ Homo ergaster and Its Contemporaries”). It is therefore unsurprising that the search for more fossil material is a priority in paleoanthropology. These shortcomings aside, there exist other more fundamental problems in analyzing and interpreting morphology. Resolving these issues is the aim of diverse research areas, whose integration has only just begun. Morphology is highly constrained and determined by a cascade of interactions between genetic, epigenetic, and environmental factors modulated through past and present selective pressures. Consequently, morphology and function must not only be interpreted with respect to present-day function and the fitness it confers to the species but should also be viewed against the backdrop of past form, function, and selective pressures. Phenotypic correlations due to pleiotropy, epigenetics or correlated selection, genetic drift, and co-option of characters for functions that were not initially

*Email: [email protected] *Email: [email protected] Page 1 of 15

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_26-5 # Springer-Verlag Berlin Heidelberg 2013

selected for compound appraisals of morphology within a phylogenetic and functional framework. The fact that developmental pathways for various structures are only poorly (if at all) understood complicates this endeavor even further. Questions as to whether form followed function or whether it was the reverse largely remain unanswered. This is problematic though, as speciation is commonly associated with the acquisition of novel morphological characters and/or the exploitation of new ecological niches. Resolving form/function relationships is thus pivotal for evolutionary inquiry. To overcome problems associated with the interpretation of morphological structures and variation in both extant and extinct populations, evolutionary studies have become increasingly multi- and interdisciplinary. Traditional comparative approaches prevail, but two main strands of distinct research lines have started to emerge. First, evolutionary developmental biology, despite its long (and sometimes misguided) history (Haeckel 1866), is now a well-established discipline (Hall 1992). Such studies combine an experimental, developmental research protocol with comparative analyses of the fossil record in order to determine the developmental and phylogenetic pathways of morphological structures and the constraints acting on their formation. Despite their high power of resolution, experimental developmental studies are not part of mainstream paleoanthropological inquiry: they require specialized knowledge, are time consuming, and are financially costly. Second, new comparative, functional, and biomechanical tools are increasingly incorporated in paleoanthropological research protocols and have made, and continue to make, a valuable contribution to our understanding of the functional adaptations of extinct species. A comprehensive review of the various strands of inquiry is beyond the scope of this contribution. Instead, this chapter aims to highlight some of the general problems and limitations associated with interpreting the morphology of fossil remains and when employing new technology.

Comparative Morphology and Constraints Morphology is not free to vary but is subject to a number of developmental, physical, and historical constraints (Maynard Smith et al. 1985), while, except for more recent hominins like Neanderthals, for example (Green et al. 2010), genetic information is not available and identification of constraints relies exclusively on comparative analyses of hard tissue remains. This limits what can be learned about the paleobiology of our ancestors.

Comparative Morphology and Evolutionary Constraints Phylogenetic systematics or cladistics is the main tool for reconstructing the phylogenetic relationships of taxa (Hennig 1966) and should precede paleobiological inquiry and functional analyses (Felsenstein 1985; Harvey and Pagel 1991). While the strengths and weaknesses of this method, as well as its assumptions, are reviewed elsewhere in this handbook (chapters “▶ Zoogeography: Primate and Early Hominin Distribution and Migration Patterns,” “▶ The Biotic Environments of the Late Miocene Hominids,” and “▶ Origins of Homininae and Putative Selection Pressures Acting on the Early Hominins”), some limitations pertaining to the analysis and interpretation of morphology need to be briefly reiterated. Relevant for the discussion of constraints are issues regarding homology and the independence of characters. Analyses of homologous traits are at the heart of cladistic methodology, but experimental studies have provided unequivocal evidence for the hierarchical nature of homology, whereby homologies at one level of organization need not lead to homologies at another (Hall 1994); in fact, Hall (2007) argued for homology and homoplasy to be viewed as opposite extremes of a continuum only. This seems justified as anatomical traits are Page 2 of 15

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_26-5 # Springer-Verlag Berlin Heidelberg 2013

not independent, but result from pleiotropy, correlated selection, modular networks, and genetic linkage. Although this arguably obscures the elucidation of the phylogenetic history of taxa and hampers inferences about the relationships between form, function, and behavior, such correlations are themselves useful and provide meaningful insights into the evolvability of complex systems (e.g., Marroig et al. 2009), i.e., the tempo and mode of evolution. Unsurprisingly thus, the study of covariances has experienced a renaissance in recent years (Olson 2012). On the basis of methodologies originally developed in population genetics, various quantitative tests have been employed to appraise the covariations and correlations of traits with the aim of inferring developmental and phylogenetic constraints (Cheverud et al. 1989). In the last few years, paleoanthropology has seen a boom in the application of this approach, aided by the affordability of powerful computers and mathematical advances, such as geometric morphometrics (Bookstein 1991). Investigations tend to focus on serially homologous structures, like hominoid limbs (Rolian et al. 2010; Young et al. 2010) and teeth (Hlusko et al. 2004), and on developmentally and/or functionally integrated (and complex) systems, such as the skull and mandible (Ackermann 2009; Lieberman et al. 2000, 2004; Zelditch et al. 2009) and the pelvis (Grabowski et al. 2011). An understanding of the integration and modularity of various structures is starting to emerge, including their potential for evolutionary change, i.e., evolvability, and the rate at which these changes can occur during evolution. For example, Hlusko et al. (2004) estimated that enamel thickness in baboons could theoretically double in only 50,000 generations. If correct, this character would be prone to homoplasy, and enamel thickness as a defining trait in hominins should be interpreted with caution. Also, the low levels of integration found in the pelvis (Grabowski et al. 2011; Lewton 2012) are likely to underlie both the rapid evolution of bipedality and the diversity of locomotor patterns among hominins (e.g., DeSilva et al. 2013).

Comparative Morphology and Functional Constraints Comparative studies are at the heart of paleoanthropology, even though hominins do not have a modern analog and have adapted to their environment in unique ways, both behaviorally and morphologically. Unfortunately, natural experiments which directly inform hominin evolution are rare. The only exception is perhaps ▶ Homo floresiensis (Brown et al. 2004), whose diminutive size and small brain continues to be subject of study (Kubo et al. 2013). While the species’ taxonomic affiliation remains unresolved, most researchers view the unique morphology of H. floresiensis as a typical response to the environmental conditions encountered on islands, i.e., resource limitations and lack of natural predators (chapter “▶ The Species and Diversity of Australopiths”). For other hominins the link between environment and morphology is far less obvious and inferences are derived predominantly from analyses of hard tissue remains. Teeth Teeth are among the most abundant remains within the fossil record and contain a wealth of information for the taxonomists and functional morphologist (chapter “▶ Modeling the Past: The Paleoethnological Evidence”). Owing to their pivotal role in the breakdown of food (Strait 1997), overall size, shape, and enamel thickness are considered good indicators of the dietary niches exploited by extinct species (Janis and Fortelius 1988); when analyzed across lineages and clades with specialized diets, they even provide information about global climatic fluctuations (Fortelius et al. 2002). The importance of tooth morphology for functional inferences is thus undisputed, but the high level of homoplasy compromises the usefulness of teeth for taxonomic purposes. For example, the hypocone probably evolved independently more than 20 times (Hunter and Jernvall 1995), while thick enamel among primates could be the result of convergent evolution also (Janis Page 3 of 15

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_26-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 1 Scanning electron microscope images (SEM) of naturally broken enamel structures of hominin teeth. (a) Australopithecus afarensis (LH6, I), (b) Kenyanthropus platyops (WT38356, RM1/2), (c) Paranthropus boisei (OH30, RM1), (d) Australopithecus africanus (Stw208, RM1), and (e) early Homo from Swartkrans, South Africa (SKX269, RC). Arrows are placed at the dentinoenamel junction and point toward the cusp tip; note that the arrow for P. boisei is directed slightly into the enamel to indicate that the break for this specimen, as for most P. boisei specimens, is somewhat oblique. For A. afarensis (a) and early Homo (e), images are from more cervical regions, thus explaining the thinner enamel; all other images are from mid-crown levels. Prism undulations are species-specific and levels of decussation vary substantially from high (e) to low (c)

and Fortelius 1988; Hlusko et al. 2004). For a functional assessment the most useful, yet underexploited, feature is the way in which dental material, particularly the hard and brittle enamel, is strengthened to prevent the propagation of cracks (Rensberger 2000). Structural strengthening is achieved through enamel decussation, which has evolved in large-bodied taxa and those that employ high bite forces (von Koenigswald et al. 1987). Although attempts have been made to deduce prism decussation from their optical manifestations, i.e., the Hunter-Schreger, these optical phenomena do not adequately capture the levels of decussation in primates. Prismatic enamel is a characteristic trait of Eutheria: it is brought about by the movement of ameloblasts from the dentinoenamel junction to the outer enamel surface during ontogeny and the differential orientation of hydroxyapatite crystals within the prism heads and its surrounding matrix (Boyde 1989; Osborn 1981). As the undulating prisms of one layer are (usually) offset with regard to layers of prisms above and below them (Fig. 1), bundles of prisms (crystals) will not be aligned in parallel, but will be angled in relation to each other. This apparent “crossing-over” provides a powerful crack-stopping mechanism (Rensberger 2000; von Koenigswald et al. 1987). This is because cracks tend to travel along the prism boundaries, i.e., the protein-rich prism sheaths (Fig. 1). Prism boundaries constitute the path of least resistance, whereas considerably more energy

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_26-5 # Springer-Verlag Berlin Heidelberg 2013

is required for a crack to traverse the strong hydroxyapatite crystals (Boyde 1989). By aligning prisms/crystals at angles relative to each other, cracks initiated while biting or through external forces, e.g., a blow to the head, will be stopped and crack propagation and catastrophic tooth failure will be prevented (except in rare circumstances). Differences in enamel prism organization thus hold information about the loading conditions habitually encountered by a species but also about wear resistance. As a case in point, the angles at which prisms intersect the wear surfaces will affect the rate at which the tissue is worn (Shimizu et al. 2005), an information that can be used to appraise whether the thick enamel of hominins is indeed an adaptation to wear resistance, as often conjectured (Macho and Shimizu 2009). Evidently thus, enamel microanatomy provides a wealth of information for an understanding of the ecological niches of hominins, but quantification of these differences remains difficult. Enamel is dense and chemically homogenous such that structural differences are achieved solely by the different orientations of hydroxyapatite crystals/ prisms. The means to retrieve microanatomical details are therefore limited and include serial sectioning of the tissue (Hanaizumi et al. 1998; Osborn 1968), using high-resolution specialized imaging techniques such as the synchrotron (Tafforeau et al. 2012), or reconstructing the prism undulations from naturally broken surfaces (Macho et al. 2003; Macho 2004; Jiang et al. 2003). Despite the relative paucity of data resulting from these difficulties, however, it is clear that prism decussation is the combined outcome of prism undulation in 3D space and the rate at which prism paths are offset in relation to each other apico-cervically. This appears a simple mechanism, yet it suffices to yield remarkably different patterns among closely related hominins (Fig. 1). The biomechanical consequences of these differences are significant too and are not anticipated from analyses of external morphology alone (Macho and Shimizu 2010; Shimizu and Macho 2008). Functional interpretations and dietary inferences based on overall tooth morphology, including enamel thickness, should therefore be viewed cautiously. Bone Unlike enamel, bone is a plastic material and continues to remodel throughout life in response to loads placed on it (Wolff 1892; for review see Pearson and Lieberman 2004; Ruff et al. 2006). Not all aspects of bone are equally informative as to their function in vivo (Currey 2002). Joints have evolved to confer both optimal orientation with regard to the direction of load and mobility, although the relative contribution of each of these aspects, as well as the magnitude of loads, remains uncertain. Until recently, the study of joint surfaces has been relatively neglected in paleoanthropology. With the affordability of more powerful computers and with advances in capturing and analyzing complex 3D shapes, this has begun to change (Parr et al. 2011; Tocheri et al. 2007). Analyses of joint surfaces is likely to become an important aspect of functional studies, especially when combined with an assessment of the subchondral bone densities underlying these surfaces (Carlson and Patel 2006; Nowak et al. 2010). Weight-bearing bones (e.g., vertebrae, calcaneus) or weight-bearing aspects of long bones (i.e., proximal ends) gain their structural stability through a meshwork of interconnected trabeculae. Such an arrangement ensures maximum strength while, at the same time, minimizing weight; unsurprisingly 70 % of all the bone is thus trabecular bone (Huiskes 2000). In order to optimize the functional adaptations of bone, trabeculae tend to align along the principal stress trajectories (Abel and Macho 2011; Biewener et al. 1996). In an innovative comparative study, Ruff et al. (1994) investigated the response of bone remodeling during different stages of ontogeny. They found that increased mechanical loading prior to (or during) adolescence leads to an increase of cortical bone thickness due to periosteal expansion. Conversely, increased loading during later stages of development results in endosteal Page 5 of 15

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_26-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 2 (a) Illustration of the predominant collagen fiber orientation patterns of osteons and (b) their appearance in histological sections, i.e., linearly polarized light (top) and circularly polarized light (bottom) (Adapted from Skedros et al. (2011) and Bromage et al. (2003) with permission)

contraction with external diameters remaining relatively unaltered (Ruff et al. 1994). In addition, cortical bone responds systemically to increased activity levels during ontogeny, even in the absence of direct loading (Lieberman 1996). Increase in bone length, in contrast, is largely stimulated through the effects of growth hormone at the growth plates and indirectly through muscle action (Vogl et al. 1993). Taken together thus, physical activity during development, i.e., during adolescence in particular, will have the greatest effect on bone remodeling through direct and indirect stimulation, whereas activity levels during adulthood will result in comparatively minor changes. With these provisos in mind, activity levels, particular behaviors, and the timing of their onset can be deduced from cortical bone thickness and cross-sectional shapes in archaeological samples and fossil hominins (e.g., Stock 2006). What has thus far been underappreciated in paleoanthropological studies is the potential importance of collagen fiber orientation within the bone matrix, its response to loading and its significance for functional interpretations (McFarlin et al. 2008; Skedros et al. 2011). Like enamel, bone is a structured hierarchical material, whose consequences for mechanical behavior and abilities to absorb and/or distribute loads may be more significant than anticipated from gross anatomy alone (Bechtle et al. 2010) (Fig. 2). Trabecular alignment within bones similarly responds to loading. Although the main trajectories are developed relatively early during development (Biewener et al. 1996; Tanck et al. 2001), trabeculae continue to grow differentially in areas where strengthening is needed and are resorbed

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_26-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 3 Systematic differences in isotropy, trabecular thickness, and density between weight-bearing (navicular) and nonweight-bearing (capitate) bones in modern humans (Adapted from Macho et al. 2005). C capitate, N navicular; asterisks indicate significance levels using paired t-tests

where it is not (Abel and Macho 2011; Biewener et al. 1996; Tanck et al. 2001; Frost 1990; Kobayashi et al. 2003). The potential of trabeculae for (re)modeling later in life offers exciting possibilities for anthropological inquiry. That is, when viewed against overall bone shape, which tends to be phylogenetically and ontogenetically more constrained, trabecular architecture is a better indicator of an animal’s behavior in vivo than gross morphology. Combined analyses of external and internal morphology therefore shed light on fundamental questions in paleoanthropology, e.g., whether a primitive morphology constitutes a plesiomorphic character (phylogenetic constraint), whether it has been retained by stabilizing selection (behavior), or whether it has simply not been selected against (phylogenetic inertia) (Ward et al. 2001). These possibilities were recently explored for the capitate of Australopithecus anamensis and A. cf. afarensis (Macho et al. 2011). Carpals and tarsals are particularly useful when addressing such questions: they lack epiphyseal plates and, with some rare exceptions, muscles attachments (Bryant and Simpson 1984; Dainton and Macho 1999a, b). Consequently, their development is influenced less by hormones and muscle pull, while the internal bony architecture will directly reflect the loading conditions encountered (Fig. 3).

Determination of Functional Adaptations Adaptations are traits which enhance the fitness of the species and have arisen over evolutionary time as a result of natural selection for present biological roles (Rose and Lauder 1996). Inferring the functional adaptations is not trivial even when the traits under investigation do not constitute evolutionary novelties. Comparative analyses based on analogy with extant taxa assume that structure and function are intricately linked, but this is seldom the case (Lauder 1997). Importantly, most biological structures have evolved to fulfill more than one function and many complex systems are mechanically redundant: similar outcomes can be achieved through different means, as shown for the masticatory apparatus, for example (Koolstra 2002). From an evolutionary perspective, redundancy is advantageous, because it increases a structure’s evolvability (Wainwright et al. 2005), but for the paleoanthropologist it is troublesome, because it reduces the confidence with which function can be inferred from morphology. Traits which are advantageous and enhance the fitness of the species may in fact have evolved for a different purpose or they could initially have been the result of random genetic drift, pleiotropy, or correlation with other structures (Gould and Lewontin 1979; Gould and Vrba 1982). Until

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recently, exaptations have been assumed to be rare, especially in hominins. Two possible exaptations have now been identified: the crack-stopping morphology of the dentine-enamel interface (Shimizu and Macho 2007) and hominin finger proportions which then facilitated the emergence of stone tool technology (Rolian et al. 2010). In order to affirm that evolution has selected for a certain trait, it is imperative that extant analogs exist and that the function is similar in all living species. Inferences about functional adaptations thus formulated should then be supported by biomechanical analyses. Additionally, the first appearance of the feature must be found to coincide with (and be supported by) ecological and environmental evidence, for which the feature and its functional adaptation had apparently been selected (Lauder 1982; Anthony and Kay 1993). Hominin morphology should therefore always be interpreted within the ecological and environmental settings of that species (Vrba et al. 1995; Bromage and Schrenk 1999). On theoretical grounds the procedure for identifying functional adaptations is straightforward but, in reality, it is challenging: the hominin lineage contains only one extant taxon, Homo sapiens; the fossil record is incomplete; experimental data on extant species are scarce; and there is much to learn about the environment in which early hominins evolved (chapters “▶ Primate Origins and Supraordinal Relationships: Morphological Evidence” and “▶ The Earliest Putative Hominids”). To overcome some of these limitations, sophisticated experimental tools are now routinely used in paleoanthropology, particularly finite element stress analysis (FESA). This method is well suited to determine the functional constraints of morphologies, provided the limitations and assumptions underlying model creation are borne in mind. The usefulness of FESA for (paleo)anthropological inquiry was first explored over a decade ago (Macho and Spears 1999; Spears and Macho 1998), and this method has now become part of the mainstream paleoanthropological tool kit (e.g., Ross 2005). FESA is a numerical modeling technique that examines the deformation of a virtual model composed of a meshwork of elements with given material properties, such as elasticity (Young’s modulus), Poisson’s ratio (the change in width after a given change in length), shear properties (shear modulus), density, bone mineral fraction, etc. (see Rayfield 2007 for a simplified review of the principles of FESA and applications in paleontology). This technique is particularly useful where an assessment of the internal mechanical behavior of structures is sought and/or where noninvasive approaches are required, as is the case for hominin fossils. However, FESA is not without pitfalls. Perhaps most crucial for an assessment of the functional adaptations (apart from overall geometry) is the input of material properties. Both teeth and bone are highly complex hierarchical structures (Figs. 1 and 2). Unfortunately, computer capacities are limited and only a finite number of details can be inputted. Put simply, the larger the structure under investigation, the cruder the model. Although efforts are being made to improve the input parameters and diversity of material properties used, many more improvements are necessary when dealing with large complex objects, like the primate skull. As a case in point, to create the complexity of the entire skull, Strait et al. (2010) used some 311,000 (macaque) and 778,000 (Australopithecus africanus) elements. In contrast, the average number of elements used to represent a small block of enamel was 440,000 (Macho et al. 2005; Macho and Shimizu 2010). Despite the apparently high level of detail, these enamel models are still simplifications though: the protein-rich prism sheaths separating enamel prisms were not modeled, although their biomechanical significance is undisputed (Ge et al. 2005). Inputting these data would have surpassed the computational capabilities. Deciding on the boundary conditions, i.e., the loads and constraints placed on the models, is another problematic area and a potential source for misleading results, particularly when investigating complex systems. For example, the masticatory system is redundant (Koolstra 2002) and the mandibular stroke varies within and between individuals depending on the size and properties of food, age, individual preference, pathology, muscle Page 8 of 15

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physiology, motor control, etc. (Woda et al. 2006). Deciding on the bite direction is therefore difficult, even more so when dealing with extinct taxa that are represented by incomplete skulls only. This is important, as the orientation of the applied load, and the locations of restraints, i.e., where the model was fixed, will significantly affect the stress flow within that structure. This highlights that while engineering techniques provide powerful and useful tools for functional analyses, models are only as good as the data inputted and the assumptions made.

Determination of Behavior Determination of behavior is probably the most difficult and contentious aspect of anthropological inquiry. The correspondence between morphology, performance, and behavior is generally inadequate (Lauder 1997). Behavioral inferences largely rest on comparative approaches aiming to deduce the biological role of morphology (bone and tooth size and shape, muscle markings, etc.) from modern analogs. But fossil species are unique: they do not have modern analogs. What is more, the farther back in time, the more fragmented the hominin fossil record becomes with associated partial skeletons being extremely rare (Berger et al. 2010; Johanson et al. 1982, 1987; Toussaint et al. 2003; Walker and Leakey 1993; White et al. 2009). Reconstruction of the bony elements therefore relies on the expertise of the morphologist working with comparative material and/or composite constructs; morphological differences between individuals, as well as temporal changes in morphology, can become obscured. The fact that a species was capable of performing certain functions and behaviors does not necessarily imply that it habitually did do so. Both modeling and biomechanical analyses can only determine the boundary conditions, i.e., constraints, of morphological structures and infer their potential capabilities. A distinction must be made between what a species could do and what it did do. An animal’s behavior is contingent on many factors other than morphology, such as the environment, competition among sympatric species, resource limitations, etc. The evolutionary success of a species will ultimately depend on how it negotiates the challenges and vicissitudes posed by the biotic and abiotic environment within the confines of its own biology. It will be challenging for the paleoanthropologist to separate these aspects. Among hominoids, for example, sympatric Pan and Gorilla feed on the same fruits during the fruiting season, but food selection changes more dramatically among gorillas than chimpanzees during the dry season (Kuroda et al. 1996). Similar scenarios are possible for sympatric hominins, e.g., Homo and Paranthropus.

Conclusions Fossil remains of hard tissue, such as teeth and bones, provide a wealth of information for the evolutionary biologist aiming to reconstruct the phylogenetic history and functional adaptations of extinct species. Unfortunately, disentangling these various aspects is not trivial and requires that paleoanthropologists employ a number of analytical tools, draw on information obtained in other disciplines (i.e., behavioral, developmental, and experimental), and collaborate with researchers in other areas. It has become abundantly clear that no single approach or technique suffices to shed light on the functional adaptations and behaviors of extinct hominins. At the same time each technique has inherent limitations and is built on assumptions that cannot always be overcome. Choosing the appropriate research tools and bearing in mind limitations specific to each approach is essential when interpreting the results. Nonetheless, the increasingly multi- and interdisciplinary Page 9 of 15

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nature of paleoanthropological research has much to offer and has begun to generate new and exciting (as well as partially testable) hypotheses at a faster rate than ever before. Given that hominins are large-brained primates that display behavioral flexibility and dietary selectivity, it is perhaps prudent not to ask what they did do but rather what they were incapable of doing. By turning the fundamental question about form, function, and behavior of extinct hominins around, better insights into the evolutionary biology of our lineage can be gained.

Acknowledgments I thank Winfried Henke and Ian Tattersall for the invitation to contribute to the Handbook of Paleoanthropology, and John Skedros and Tim Bromage for permission to reproduce their figures. This chapter is the result of various research projects, funded mainly by the Natural Environment Research Council (UK), The Leverhulme Trust (UK) and the Ministerio de Economı´a y Competitividad (Spain).

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Index Terms: Behavior, hominins_9 Cladistics_2 Evolutionary morphology_1–3, 7, 9 Evolutionary morphology behavior_9 Evolutionary morphology functional adaptations_7 Evolutionary morphology morphology vs. evolutionary constraints_2 Evolutionary morphology morphology vs.functional constraints_3 Evolutionary morphology phenotypic correlations_1 Finite element stress analysis (FESA)_8 Fossil material_3, 5 Fossil material bone_5 Fossil material teeth_3 Functional adaptations, hominins_7 Homo floresiensis_3 Morphological constraints_2–3 Morphological constraints evolutionary constraints_2 Morphological constraints functional constraints_3

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_28-5 # Springer-Verlag Berlin Heidelberg 2014

Prospects and Pitfalls Jean-Jacques Hublin* Department of Human Evolution, Max-Planck-Institute for Evolutionary Anthropology, Leipzig, Germany

Abstract Paleoanthropology is primarily rooted in the study of fossils and the analysis of sites. Dependence on these resources leads to challenges resulting from difficulty in gaining access to scarce, precious, and sometimes overprotected materials and from issues of control over field sites. The development of virtual paleoanthropology can sometimes be a way to partially solve the first problem. However, on some occasions, the access to and utilization of numerical data has also become an issue of dispute. In parallel, recent advances in studies focusing on microstructures, isotopic composition, and paleogenetics require direct sampling of the fossils. The trend in paleoanthropology is to integrate approaches from different scientific fields, and this is especially visible in developmental sciences, genetics, and environmental studies. In the meantime, dealing with human evolution remains a sensitive topic, subject to clear ideological and religious biases. The interest of the media and of the public in this science does not always contribute to an objective approach to the questions. Finally, among other issues, the expansion of paleoanthropological studies in developing countries must depend on a decline in its colonial image.

Introduction In many respects, paleoanthropology is a paradoxical science. Although it addresses the oldest origins of humans, the discipline itself developed quite recently in the history of science. The first fossil hominid specimen on record, an immature Neanderthal skull, was discovered in 1830 in Engis (Belgium). However, it was not until the end of the nineteenth century that certain fossil specimens were truly accepted by the majority of the scientific community as evidence for the evolutionary process that gave birth to the human species. Although very significant discoveries occurred during the first half of the twentieth century and provided the basic framework for paleoanthropological studies, the last three decades of that century witnessed a spectacular increase in the available fossil record as well as in major advances in the knowledge of past environments and the chronological background of human evolution. Moreover, the birth of paleogenetics added a new dimension to the analysis of relationships among fossil hominid species. The current state of the discipline results not only from methodological progress but also from a major effort of field research. For the public, the media, and students, it is always a matter of amazement, and sometimes of criticism, to realize that the field of paleoanthropology is such a changing terrain. If prediction is always a difficult exercise, in science as in many other domains, it is even more challenging in this particular science, which is relatively newly born and still rapidly evolving. Another distinctive aspect of paleoanthropology lies in the fact that the study of fossil specimens remains the core of the discipline. These are rare and precious objects. It is often emphasized that for the study of some extinct groups, the specimens are fewer than the specialists who analyze them, and *Email: [email protected] Page 1 of 13

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_28-5 # Springer-Verlag Berlin Heidelberg 2014

sometimes the competition is harsh. After an undefined period during which they remain under the relatively rigid control of individuals or groups responsible for publishing descriptions of them, they are usually curated in museums or other institutions. While the specimens are in their possession, the curating institutions may also restrict access to the fossil specimens, emphasizing their conservation rather than their scientific study. On the one hand, there is therefore strong pressure to consult the fossil material, and on the other, growing restrictions that result from a multitude of reasons that range from the desire to maintain scientific monopoly to the legitimate policy of protecting fragile and valuable objects. In parallel, new techniques for the study of the specimens have been developed. However, while these new methods sometimes resolve issues, sometimes they generate new difficulties.

Virtual Paleoanthropology Since the 1980s, new techniques in medical and industrial imaging have revolutionized the fields of human paleontology and physical anthropology (Wind 1984; Wind and Zonneveld 1985; Zonneveld and Wind 1985) allowing the development of what has become commonly called as “virtual paleoanthropology.” The growing use of computed tomography as well as industrial imaging techniques (microtomography and laser scanners) has allowed the production of 3D images of fossil specimens. Combined with stereolithography and other techniques of 3D printing, these virtual representations have opened a number of new possibilities for the analysis of the specimens. Most notable among these are: • Virtual extraction and reconstruction (including correction of plastic distortions) (Kalvin et al. 1992; Zollikofer et al. 1995; Ponce de León and Zollikofer 1999) • Precise quantitative analysis of inaccessible internal structure (including tiny structures, such as middle and inner ears, bony tables, and vascular foramina) and their comparison with living references (Zonneveld et al. 1989; Hublin et al. 1996; Spoor et al. 1996) • 3D morphometric analysis with the development of new mathematical tools (Harvati 2002) • Modeling of ontogenetic processes, biomechanical properties, and of evolutionary changes themselves (Ponce de León and Zollikofer 2001; Mitteroecker et al. 2004; Gunz et al. 2010; Freidline et al. 2012) Growing evidence suggests that, with increasing frequency, the anatomy of fossil hominins will be systematically studied not from the specimens themselves but from virtual representations. Principal among all the new possibilities opened by virtual paleoanthropology is the reduced need to manipulate real objects. Consequently, these techniques should be welcomed by many curators. However, they also raise new questions. One is related to the quality of the data. Until recently, the CT scanners that have been used to acquire the data were primarily those available in the medical environment. Although they evolve rapidly, machines of this type have their own limitations and are not specifically designed to explore fossilized specimens filled with dense sediments. The resolution of the 3D pictures produced in this way does not allow for the assessment of fine structures at an appropriate resolution. In recent years, large museums curating fossils, as well as research institutions, have been increasingly equipped with microCT scanners, initially designed for industrial uses, which provide high-resolution data in the order of magnitude of a micron or even under. Imagery techniques based on the use of synchrotrons such as the face contrast allow the study of microstructures otherwise inaccessible to the analysis in a nondestructive way (Tafforeau and Smith 2008). Page 2 of 13

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_28-5 # Springer-Verlag Berlin Heidelberg 2014

Among the pitfalls related to the development of virtual paleoanthropology is a shift from a situation where access to the fossil specimens was difficult to a situation where access to the numerical data is even more challenging. Curators are sometimes reluctant to allow repeated acquisitions of these numerical data, while the techniques and equipment evolve rapidly. Often, the data are monopolized by those who acquired them initially, and they are hard to upgrade. In the long term, databases may develop in some institutions and on the Internet (Hublin 2013). To date, however, the development of such databases has faced insuperable difficulties. The commercialization of some of these data by the institutions concerned, or the simple trading of data between teams, will remain, for some time, the only alternative. Another concern relates to the possibility that repeated irradiation of fossil material may alter biomolecules such as ancient DNA. Although this problem has been to date little investigated, it may in the future lead to necessary choices in priorities regarding the analysis of recent fossil material.

Into the Matter of Bone In a somewhat opposite direction to virtual paleoanthropology, there are a number of other new approaches that have been developed in the fields of human paleontology, physical anthropology, and archaeology. Such techniques were initially based on rather invasive analyses of the specimens, inherited primarily from histology and geochemistry. However, with the rise of non- (or less) destructive methods, this field is rapidly expanding. In the future, study of the actual fossil remains will likely be reserved for the kinds of analyses that cannot be performed on virtual representations. At present, such analyses include, on the one hand, histological approaches mainly addressing bone and tooth microstructures and, on the other hand, chemical analyses addressing either geochronological or paleobiological questions. Microstructural studies have developed mostly in the field of dental anthropology. The recognition of different types of incremental mineralized structures in the dentine and the enamel since the middle of the twentieth century has led to systematic analyses of their variation in extant and fossil primates (Dean 1987; Stringer et al. 1990; Lieberman 1993; Zhao et al. 2000; Dean et al. 2001; Martin et al. 2003; Schwartz et al. 2003; Smith et al. 2003). This development has been made possible by the improvement of technical equipment such as the scanning electron microscope, the confocal microscope, and computer-assisted microscopy for 3D visualization. The interest in these studies comes from the knowledge that microstructures could be the main, if not the only way, to assess life history in extinct species (Fitz Gerald 1998). This issue has been given increasing attention in an evolutionary perspective since the genetic bases of development have become better understood and their importance for evolutionary changes better appreciated. Future research in this direction will certainly include extensive work on modern variability and more experiments to assess the biological significance of accretional microstructures and their relevance for calibrating the growth patterns of extinct species. Although it is possible to work on externally visible features, such as perikymata (Ramirez Rozzi and Bermudez de Castro 2004), a drawback of these methods is the necessity of slicing precious fossil specimens to analyze fine internal microstructures. However, the technique of thin slicing has greatly improved, and it is possible today to “rebuild” a specimen after analysis following minimal destruction of tissue. In the future, new techniques of imaging may also partly resolve this problem. Although, to date, it remains a very expensive technique, the use of synchrotrons allows access to bone and tooth microstructures without destruction (Tafforeau et al. 2006).

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_28-5 # Springer-Verlag Berlin Heidelberg 2014

Chemical analyses of fossil specimens have been aimed at reconstructing paleobiological features and are mostly concerned with the extraction of organic molecules. Nonorganic chemical properties of the fossil remains are primarily relevant to the determination of their geological age and are marginally useful in addressing paleobiological issues. To date, DNA and collagen have been the main targets of the research on ancient biomolecules. Techniques based on the use of restriction enzymes have allowed the duplication and subsequent sequencing of tiny and rare fragments of DNA chains. So far, this work has been based primarily on the analysis of mitochondrial DNA, which is smaller and much more abundant than nuclear DNA. The sequencing of a fragment of mitochondrial DNA of the Feldhofer 1 (Neanderthal) specimen in 1997 opened a new era of paleoanthropological studies (Krings et al. 1997). Future development of this research will involve the reconstruction of the entire sequence of the mitochondrial DNA in specimens such as Neanderthals. With the development of new techniques, future work will also address the issue of nuclear DNA in fossil hominids. However, the natural degradation of DNA under given physical conditions imposes a chronological barrier that today seems oddly unsurpassable. Another serious problem in paleogenetic studies comes from the potential for contamination. Paradoxically, the DNA of modern and relatively recent humans remains very difficult to identify as genuine fossil DNA and to distinguish from subsequent contamination (Serre et al. 2004). Studies on the taphonomic processes affecting the deterioration of DNA chains in archaeological or geological deposits may provide an answer to this problem. Isotopic compositions of the mineral portions of hominid fossils have been used to assess biological issues. These studies face the difficult questions of the taphonomic transformation of the chemical composition of fossils in geological layers (Radosevich 1993; Fabig and Herrmann 2002). Most researchers have thus focused on the more stable component of bone, the protein collagen (Schoeninger 1985; Ambrose 1986; Bocherens et al. 1991, 1997; Richards et al. 2000, 2001). Collagen has been the primary source for the analysis of stable isotopes such as oxygen, nitrogen, and carbon. These isotopes are fixed in the living tissues antemortem, either at an early stage of individual development (e.g., in the teeth) or at some time before death. They are an essential source of information about the environment and the diet of individuals during their lifetimes. One constraint of these studies is that they are limited by the long-term preservation of collagen. For older hominins, carbon fixed in the mineral part of the dental tissues has also been used to investigate what type of plants (C3 or C4) herbivores and their predators extracted their food. One can expect that, as with the study of recent archaeological series, such analyses in the future will bring unexpected knowledge of issues such as migration, seasonality, or even mating strategies among relatively ancient hominids. New research into extracting other longer-surviving proteins, such as osteocalcin, has the potential to provide material for isotopic studies for much older material. An interesting development comes from the combination of microstructural studies and isotopic analyses to assess fine timescale changes in the diet or the environments of fossil individuals (Humphrey et al. 2004). The extension of isotopic analyses to new elements may also lead to interesting developments in this field. For example, sulfur isotopes in collagen, along with strontium and oxygen in minerals, can tell a lot about migration and movement patterns (Nehlich et al. 2010). Isotopic studies (especially of oxygen) will also likely contribute to a much greater knowledge of past environmental conditions and their rapid variation in continental environments, a topic that so far remains much less explored than in oceanic environments and the ice caps.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_28-5 # Springer-Verlag Berlin Heidelberg 2014

Understanding Evolutionary Processes The reconstruction of the evolutionary history of hominoids, and more specifically of fossil humans, has for a long time focused primarily on taxonomic and phylogenetic questions. Important methodological progress has been made in this field during recent decades. In particular, the use of cladistic approaches has provided a better theoretical background. Although these approaches also have their own limitations (Trinkaus 1990), they have become indispensable for assessing the significance and the polarity of features. However, it should be underlined that the development of mathematical techniques to analyze size and shape, including 3D morphometrics, has at times led to the regression of some studies to a precladistic stage. The emphasis placed on the shape distances should not lead researchers to forget that morphological similarity is not a reliable way to analyze phylogenetic relationships when the polarity of the features is not taken into account. A major problem, discussed extensively in recent years, resides in the features used by paleoanthropologists for cladistic analyses. These discussions have focused on features’ significance and relationships either to genetic determinism or to environmental conditions and behavior or to an interaction between the two. Beyond these discussions lie issues such as the independence of such features in their development and their homology when one passes from one species to another (Lieberman 1999; Wood 1999). These are critical questions for the analysis of the fossil evidence and the reconstruction of phylogenetic relationships from a parsimony perspective. However, one may be reasonably optimistic in this matter, as experimental data and a better understanding of the precise genetic and epigenetic mechanisms underlying the development of features will resolve these questions. These may also bring answers to related problems such as the discrepancy sometimes underlined between biomolecular evidence and phylogenetic reconstructions based on the analysis of morphological features of the phenotype (Collard and Wood 2000; Strait and Grine 2004). They may also bring new light to the debate surrounding modular versus integrative models in the biological development of extinct organisms (Wagner 1996; Wagner and Altenberg 1996; Williams and Nagy 2001; Winther 2001). As far as the recent stages of human evolution are concerned, it is reasonable to expect that taxonomic and phylogenetic issues will become of minor interest in the future as the main taxa are identified and their phylogenetic relationships understood. However, better understanding of variability, not only in extinct taxa but also in living forms, remains a crucial issue. Although some have predicted the decline of such anatomical studies, it is still striking to contemplate the lack of knowledge of the variability in living humans with respect to many features commonly used in paleoanthropological research. After several centuries of anatomical studies, longitudinal data on the growth and development of many anatomical features is still desperately needed. This lack of data is even more dramatic when one considers the populations of living apes, the closest relatives of humans in the animal world; most of them will likely become extinct in the wild before they have been properly studied. Research may focus more on paleobiological issues. Changes in growth and development processes during life history, in terms of timing and pattern, are increasingly seen as powerful mechanisms to explain evolutionary changes. Studies of extinct species consider this dimension with increasing frequency, and developmental trajectories will hopefully be identified for different taxa as will the effects of epigenetic phenomena. This is, of course, dependent on an increase in the available paleontological material and also on a greater interaction between paleoanthropology and developmental genetics. 3D morphometrics and other mathematical tools have been identified recently as powerful tools for the reconstruction of those developmental trajectories that can sometimes be modeled (Ponce de León and Zollikofer 2001). Establishing reliable tools to assess Page 5 of 13

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_28-5 # Springer-Verlag Berlin Heidelberg 2014

the calendar ages of immature individuals in the fossil record is of crucial importance in this matter (Coqueugniot et al. 2004), and developing studies of skeletal microstructure seems an inevitable way to address this problem. Other aspects of the biology of extinct species might also become accessible through progress in the extraction of biomolecules such as proteins. Osteocalcin has recently been extracted from Neanderthal remains and sequenced (Nielsen-Marsh et al. 2005). In the future, extraction of proteins or lipids from ancient material may even shed new light on the physiology of our ancestors and cousin species. It should also be noted that the extraction of ancient proteins and their sequencing may be extended much further back in time as some of these molecules seem to resist taphonomic degradation much better than DNA. In recent years, paleodemographic questions have become more and more interesting to paleoanthropologists. Topics such as life history and longevity are critically important to understanding the biological and social adaptations of ancient groups, as well as to addressing questions of learning time during individual life and the transmission of knowledge from one individual to another. Other paleodemographic parameters that appear to be important are the questions of population densities in given areas in a geological time frame and their possible catastrophic variation in relation to environmental changes. Although paleodemographic parameters have long appeared unreachable (Bocquet-Appel and Masset 1982, 1996), different methods of evaluating size fluctuation in ancient populations have emerged from genetic or paleogenetic studies. In addition to providing new understanding of phylogenetic relationships, gene flow between groups, and differences in gene coding for some characters in ancient hominids, paleogenetics has also introduced a new way to assess group size through time in ancient humans (Meyer et al. 2012). Although paleogenetic studies on the Neanderthals did not revolutionize views of their phylogenetic relationships, they did bring a new way to assess genetic variability in ancient populations and, consequently, population size changes (Currat and Excoffier 2004; Serre et al. 2004). The animal models appear to be a tempting alternative for testing demographic fluctuations and their effects on genetic variability during the recent periods of the Pleistocene (Orlando et al. 2002). Such knowledge will allow a better understanding of the possible effects of demographic crashes and genetic bottlenecking on evolutionary processes themselves, as well as the relative roles of genetic drift and natural selection. Combining isotopic analysis and microstructural studies will also allow the garnering of information such as the weaning age of fossil individuals. A fine knowledge of climatic environmental changes, sometimes perceptible on the scale of one human life, also brings new light to the way human populations have adapted biologically and culturally. In this perspective, a better integration of biological and cultural evidence seems necessary for a more thorough understanding of human evolution.

Chronology The determination of the geological age of fossil hominids is central to paleoanthropological work. Until recently, such determination has centered on the application of radiometric methods to the archaeological context of the discoveries. Although available methods require improvement in their precision and in their calibration, their direct application to hominid specimens also represents major progress, especially for specimens anciently discovered and/or for which the context is unknown or inaccessible. Once more, the development of such approaches has been limited initially by the destructive aspects of these investigations. However, the emergence of new techniques, such as laser ablation, makes the analysis of light or heavy isotopes on precious specimens almost completely Page 6 of 13

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_28-5 # Springer-Verlag Berlin Heidelberg 2014

nondestructive. In the future, these studies may be applied routinely and become the best way to establish a precise chronology. As far as the radiometric methods based on C14 disintegration are concerned, the development of mass spectrometry has allowed the direct dating of fossil specimens by requiring only small amounts of matter for analysis. Since 2009 the calibration curve for C14 dates has been extended back to 50,000 BP, which makes the method more reliable in this time range that is of such crucial importance to the history of modern human dispersal (Reimer et al. 2009). In addition to calibration, contamination remains a major problem and the origin of the sampled carbon must be securely established; methods such as the ultrafiltration of the collagen may allow for the control of this factor. Another future development will be to work with organic carbon from biomolecules such as amino acids that can be identified as genuine fossil molecules belonging to the extinct organisms from which they were extracted. In practice, all this means that many C14 dates acquired during the last decades may become meaningless because of the limitations of the techniques used to establish them. Large databases that have been built to process these dates by the thousands and that provide a picture of biological and cultural evolution of humans, especially at the time of the replacement of Neanderthals by modern humans in Europe, can be improved by a critical assessment of the compiled dates. However, the screening process has provided very contrasting pictures and has not satisfactorily solved all questions. This probably results from some bias in the selection process of the data retained, partly depending on the views that different authors have on the evolutionary and peopling processes involved. Eventually, such databases may become obsolete and will need to be rebuilt with more reliable geochronological information.

Picture of an Ancestor Every human society has built up physicotheological explanations to deal with the question of its origins. In the historical record, such explanations have been furnished by religions and mythologies, but from the middle of the nineteenth century, western societies substituted a scientifically based explicatory model for biblically based explanations. The question of human origins became the concern of scientists rather than priests. However, in 1863, T. H. Huxley, a major supporter of Darwin’s views, wrote: “The question of questions for mankind, the problem which underlies all others, and is more deeply interesting than any other, is the ascertainment of the place which man occupies in nature, and of his relationship to the universe of things. Whence our race has come; what are the limits of our power over nature; to what goal are we tending are the problems which present themselves anew, and with undiminished interest, to every man born into the world.” Almost 150 years later, this issue is still not free of ideological, if not metaphysical, constraints. This may partly explain why the public has developed such an interest in this field of science. Aside from the inherent attraction of pictures of extinct worlds, any piece of evidence in paleoanthropological studies also becomes a matter of opinion and feeling, even for non-knowledgeable audiences. Prehistory is also consistently the topic of novels, films, and documentaries in which science always has to defend itself against fantasy (Sommer 2006, 2007; Stoczkowski 1994). Museums and educational centers have become incredibly successful with this subject, showing increasing sophistication in their ways of responding to the demands of the public for pictures or 3D reconstructions. Although some of these reconstructions are produced today (Fig. 1) using advanced techniques, they have their own limitations. It is certainly possible to provide reasonable reconstructions of the general anatomy of well-known fossil species. However, to date, many fine anatomical details, such as skin, hair, and eyes, remain beyond the range of scientific assessment. Page 7 of 13

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_28-5 # Springer-Verlag Berlin Heidelberg 2014

Fig. 1 A reconstruction of a pre-Neanderthal at the Landesmuseum f€ur Vorgeschichte (Halle, Germany). Accurate methods have been developed to reconstruct soft tissues in fossil hominids. However today, like in the past, the picture of ancient humans primarily remains a projection of human fantasies

Unfortunately, they are also of crucial importance to the way other species of humans appear from a modern perspective. The “scientifically based” reconstructions of fossil hominids filling the museums in Europe and America may say much more about the way human diversity is perceived than about the actual aspects of these hominins. In this respect, the progress of the reconstructions since the beginning of the twentieth century may be more limited than is often assumed. Underlying notions of humans as belonging to different species, and possibly contemporaneous in the past, are difficult to integrate, not only for the public but also for scientists from sister disciplines. The humanist framework within which the human and social sciences developed in universities may explain the difficulty that cultural anthropologists and archaeologists, attached to the notion of “uniqueness” of the human being, face in dealing with notions such as ape cultures or the multispecific nature of hominins. More generally, in the post-Second World War era, new conceptions understandably developed around human diversity that provided an ideological framework to which paleoanthropological evolutionary models had to adapt. The questions of Neanderthal nature and abilities and their relationship to extant humans, in other words the last well-documented divergence in the human phylogenetic tree, is one arena in which science and ideological preconceptions have clashed in a complex way. In this interaction between scientists and the public, the media play an important role. There are many reasons why scientists need to communicate with the public. One is that the interest of the public partly justifies society’s investment in this field of pure research. Another may result from more personal reasons. For a department, for a team, for an individual, the visibility of the scientific results obtained becomes increasingly important as it impacts on possible personal promotion and political decisions to support this field of research in general, or a project in particular. Thus, the Page 8 of 13

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_28-5 # Springer-Verlag Berlin Heidelberg 2014

scientist and the reporter face each other in a dialogue where each needs the other. The reporter needs material for exciting articles; the scientist needs a reporter for publicity (Henke 2010). In the past few decades, this interaction has become increasingly important and has sometimes led to undesirable effects. One obvious pitfall is that the public and reporters are more interested in some issues than in others. Those problems most debated in the media may be of limited interest to the scientific community, and vice versa. Sex between Neanderthals and modern humans is an example of a question universally addressed to paleoanthropologists, and one danger is that, in the need to be well represented in the media, scientists might be led to pander to such questions or even to develop research interests geared to public attention. It is amazing to see how well-developed press services have become, not just in institutions dedicated to public education and communication but also within research structures as well. Recently these interactions between scientists and the media have entered a new dimension, as personal issues or rivalries between individuals have become of themselves a matter of interest for the press. High-profile international scientific journals have developed “people sections” that deal almost exclusively with these subjects. Reporters have therefore become part of the scientific debate and actors in rivalries, by promoting opinions and sometimes by fueling controversies and conflicts in a way designed to make their articles more exciting.

The Unbalanced Ecology of Paleoanthropology Paleoanthropology is based on the study of specimens to which access may be difficult. It is also based on sites and fieldwork. The result is that it can be a highly territorial activity, to an extent unequaled in other fields of science. Indeed, aside from scientific problems, the paleoanthropologist must also face a series of political and ethical issues. Although specimens discovered and published a long time ago should be fully accessible to the scientific community, this is not always the case. The situation is even more complex regarding specimens soon after their discovery and/or after a partial description. So far, the scientific community has not established a consensus on resolving such questions. The discoverer of a new specimen has a scientific and moral right to it and is granted priority in providing a scientific analysis of this material, alone or in collaboration with other specialists. However, this well-accepted notion is often blurred by complications. One such complication can result from the multiplicity of the discoverers involved and from lack of agreement at the time of the discovery, or later. And many discoveries occur during the course of archaeological excavations conducted by teams that were not anticipating the possibility of hominin discoveries. Another problem can result from an abusive extension of the time spent between a discovery and the publication of a reasonably comprehensive description of it. The competition that is natural in science is sometimes displayed in a negative form, such as preventing challengers from accessing material, which may be used as a more efficient way to surpass them than producing better scientific results. Similar situations have developed with respect to site and field access. Most commonly, research teams obtain the monopoly of the study of one site or a geographical area for a certain length of time in order to conduct a defined scientific program. However, apart from this formal arrangement, there are a number of situations where informally and based on political influence, tradition, or nationalistic issues, institutions manage to secure a geographical domain of influence. This is often the case when excavations or field operations are conducted by scientists from western countries in less developed areas. Often, this is facilitated by the fact that the studied areas are located in countries lacking indigenous research in the field of paleoanthropology and/or scientists trained in this Page 9 of 13

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_28-5 # Springer-Verlag Berlin Heidelberg 2014

discipline. In such cases the work is conducted under the authorization of local administrations that are primarily preoccupied by the conservation of their national patrimony. Here again, different institutions or scientific communities may develop some level of competition in guaranteeing their access to the field. Different countries have developed different regulations restricting the exploitation of archaeological and paleontological material. Situations in which fossil specimens can simply be transferred from the country of their discovery to scientific institutions or museums in Europe or America have almost completely disappeared today. Many scientists have felt compelled to develop balanced collaborations with the host countries in which they conduct their research, in particular, by helping with the conservation of the material and with the training of local scientists. Furthermore, many countries outside of the western world have managed to develop their own programs and scholars, and the trend is more and more to develop joint projects, although a very unequal equilibrium in terms of financial contribution and/or scientific expertise can lead to bitter conflicts. Although the time of scientific colonialism is over, and in an ideal world, fossils and sites should be accessible to “everyone,” this ideal situation is still far from being reality. Archaeological and paleontological materials are considered as part of the national patrimony in most counties, yet the future of the field lies in fair and fruitful international collaborations.

Conclusion In summary, although the development of virtual paleoanthropology has opened new venues to access the fossil evidence and to study it, paleoanthropology remains a science primarily centered on objects and sites to which access for researchers is far from being guaranteed. In the last two decades, the field has witnessed spectacular methodological progress providing new insights into the processes of human evolution. However, the question of the origin and nature of humankind remains a sensitive issue. In addressing these questions, science is challenged by many preconceptions.

Cross-References ▶ Chronometric Methods in Paleoanthropology ▶ Evolutionary Theory in Philosophical Focus ▶ Historical Overview of Paleoanthropological Research ▶ Hominin Paleodiets: The Contribution of Stable Isotopes ▶ Virtual Anthropology and Biomechanics

References Ambrose SH (1986) Stable carbon and nitrogen isotope analysis of human and animal diet in Africa. J Hum Evol 15:707–731 Bocherens H, Fizet M, Mariotti A, Lange-Badre B, Vandermeersch B, Borel JP, Bellon G (1991) Isotopic biogeochemistry (13C, 15N) of fossil vertebrate collagen: application to the study of a past food web including Neanderthal man. J Hum Evol 20:481–492

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Bocherens H, Billieu D, Patou-Mathis M, Bonjean D, Otte M, Mariotti A (1997) Paleobiological implications of the isotopic signatures (13C, 15N) of fossil mammal collagen in Scladina Cave (Sclayn, Belgium). Quat Res 48:370–380 Bocquet-Appel JP, Masset C (1982) Farewell to paleodemography. J Hum Evol 11:321–333 Bocquet-Appel JP, Masset C (1996) Paleodemography: expectancy and false hope. Am J Phys Anthropol 99(4):571–583 Collard M, Wood B (2000) How reliable are human phylogenetic hypotheses? Proc Natl Acad Sci 97(9):5003–5006 Coqueugniot H, Hublin J-J, Veillon F, Houët F, Jacob T (2004) Early brain growth in Homo erectus and implications for cognitive ability. Nature 431:299–302 Currat M, Excoffier L (2004) Modern humans did not admix with Neanderthals during their range expansion into Europe. PLoS Biol 2:2264–2274 Dean MC (1987) Growth layers and incremental markings in hard tissues: a review of the literature and some preliminary observations about enamel structure in Paranthropus boisei. J Hum Evol 16:157–172 Dean C, Leakey MG, Reid D, Schrenk F, Schwartz GT, Stringer C, Walker A (2001) Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins. Nature 414:628–631 Fabig A, Herrmann B (2002) Trace elements buried in human bones: intra-population variability of Sr/Ca and Ba/Ca ratios - diet or diagenesis? Naturwissenschaften 89:115–119 Fitz Gerald CM (1998) Do enamel microstructures have regular time dependency? Conclusions from the literature and a large-scale study. J Hum Evol 35:371–386 Freidline SE, Gunz P, Harvati K, Hublin J-J (2012) Middle Pleistocene human facial morphology in an evolutionary and developmental context. J Hum Evol 63:723–740 Gunz P, Neubauer S, Maureille B, Hublin J-J (2010) Brain development after birth differs between Neanderthals and modern humans. Curr Biol 20:R921–R922 Harvati K (2002) Models of shape variation within and among species and the Neanderthal taxonomic position: a 3-D geometric morphometric approach on temporal bone morphology. In: Mafart B, Delingette (eds) Three dimensional imaging in paleoanthropology and prehistoric archaeology. BAR, Liege Henke W (2010) Zur narrativen Komponente einer theoriegeleiteten Paläoanthropologie. In: Engler B (ed) Erzählen in den Wissenschaften. Positionen, Probleme, Perspektiven. 26. Kolloquium (2009) der Schweizerischen Akademie der Geistes- und Sozialwissenschaften. Academic Press, Fribourg, pp 83–104 Hublin (2013) Palaeontology: free digital scans of human fossils. Nature 497:183 Hublin J-J, Spoor F, Braun M, Zonneveld F, Condemi S (1996) A late Neanderthal associated with Upper Palaeolithic artefacts. Nature 381:224–226 Humphrey LT, Jeffries TE, Dean MC (2004) Investigation of age at weaning using Sr/Ca ratios in human tooth enamel. Am J Phys Anthropol 123(Suppl 38):117 Kalvin AD, Dean D, Hublin J-J, Braun M (1992) Visualization in anthropology: reconstruction of human fossils from multiple pieces. In: Kaufman AE, Neilson GM (eds.), Proceedings of IEEE Vizualization 92. IEEE Computer Society Press, 404–410 Krings M, Stone A, Schmitz RW, Krainitzki H, Stoneking M, Pääbo S (1997) Neanderthal DNA sequences and the origin of modern humans. Cell 90:19–30 Lieberman D (1993) Life history variables preserves in dental cementum microstructure. Science 261:1162–1164

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Lieberman DE (1999) Homology and hominid phylogeny: problems and potential solutions. Evol Anthropol 7:142–151 Martin LB, Olejniczak AJ, Maas MC (2003) Enamel thickness and microstructure in pitheciin primates, with comments on dietary adaptations of the middle Miocene hominoid Kenyapithecus. J Hum Evol 45:351–367 Meyer M, Kircher M, Gansauge M-T, Li H, Racimo F, Mallick S, Schraiber JG, Jay F, Pr€ ufer K, de Filippo C et al (2012) A high-coverage genome sequence from an archaic Denisovan individual. Science 338:222–226 Mitteroecker P, Gunz P, Bernhard M, Schaefer K, Bookstein FL (2004) Comparison of cranial ontogenetic trajectories among great apes and humans. J Hum Evol 46:679–697 Nehlich O, Borić D, Stefanović S, Richards MP (2010) Sulphur isotope evidence for freshwater fish consumption: a case study from the Danube Gorges, SE Europe. J Archaeol Sci 37:1131–1139 Nielsen-Marsh CM, Richards MP, Hauschkad PV, Thomas-Oatese JE, Trinkaus E, Pettitt PB, Karavanic’ I, Hendrik Poinari H, Collins MJ (2005) Osteocalcin protein sequences of Neanderthals and modern primates. Proc Natl Acad Sci 102(12):4409–4413 Orlando L, Bonjean D, Bocherens H, Thenot A, Argant A, Otte M, Hänni C (2002) Ancient DNA and the population genetics of cave bears (Ursus spelaeus) through space and time. Mol Evol 19:1920–1933 Ponce de Leon MS, Zollikofer CPE (1999) New evidence from Le Moustier 1: computer-assisted reconstruction and morphometry of the skull. Anat Rec 254:474–489 Ponce de León MS, Zollikofer CPE (2001) Neanderthal cranial ontogeny and its implications for late hominid diversity. Nature 412:534–538 Radosevich SC (1993) The six deadly sins of trace element analysis: a case of wishful thinking in science. In: Sandford MK (ed) Investigations of ancient human tissue: chemical analyses in anthropology. (Food and nutrition in history and anthropology, vol. 10). Gordon and Breach, Langhorne, pp 269–332 Ramirez Rozzi FV, Bermudez de Castro JM (2004) Surprisingly rapid growth in Neanderthals. Nature 428:936–939 Reimer PJ, Baillie MGL, Bard E, Bayliss A, Beck JW, Blackwell PG, Bronk Ramsey C, Buck CE, Burr GS, Edwards RL et al (2009) Intcal09 and Marine09 radiocarbon age calibration curves, 0–50,000 years Cal BP. Radiocarbon 51:1111–1150 Richards MP, Pettitt PB, Trinkaus E, Smith FH, Paunovic M, Karavanic I (2000) Neanderthal diet at Vindija and Neanderthal predation: the evidence from stable isotopes. Proc Natl Acad Sci 97:7663–7666 Richards MP, Pettitt PB, Stiner MC, Trinkaus E (2001) Stable isotope evidence for increasing dietary breadth in the European mid-Upper Paleolithic. Proc Natl Acad Sci 98:6528–6532 Schoeninger MJ (1985) Trophic level effects on N-15 N-14 and C-13 C-12 ratios in bone collagen and strontium levels in bone mineral. J Hum Evol 14:515–525 Schwartz GT, Liu W, Zheng L (2003) Preliminary investigation of dental microstructure in the Yuanmou hominoid (Lufengpithecus hudienensis), Yunnan Province, China. J Hum Evol 44:189–202 Serre D, Langaney A, Chech M, Teschler NM, Paunovic M, Mennecier P, Hofreiter M, Possnert G, Pääbo S (2004) No evidence of Neanderthal mtDNA contribution to early modern humans. PLoS Biol 2:313–317 Smith TM, Martin LB, Leakey MG (2003) Enamel thickness, microstructure and development in Afropithecus turkanensis. J Hum Evol 44:283–306

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Sommer M (2006) Mirror, mirror on the wall: Neanderthal as image and ‘distortion’ in early 20thcentury French science and press. Soc Stud Sci 36(2):207–240 Sommer M (2007) The lost world as laboratory: the politics of evolution between science and fiction in early twentieth-century America. Configurations 15(3):299–329 Spoor F, Wood B, Zonneveld F (1996) Evidence for a link between human semicircular canal size and bipedal behaviour. J Hum Evol 30:183–187 Stoczkowski W (1994) Anthropologie naïve, anthropologie savante. De l’origine de l’homme, de l’imagination et des idées reçues. CNRS Editions, Paris, 246 p Strait DS, Grine FE (2004) Inferring hominoid and early hominid phylogeny using craniodental characters: the role of fossil taxa. J Hum Evol 47:399–452 Stringer CB, Dean MC, Martin RD (1990) A comparative study of cranial and dental development within a recent British sample and among Neanderthals. In: DeRousseau CJ (ed) Primate life history and evolution. Wiley-Liss, New York, pp 115–152 Tafforeau P, Smith TM (2008) Nondestructive imaging of hominoid dental microstructure using phase contrast X-ray synchrotron microtomography. J Hum Evol 54:272–278 Tafforeau P, Boistel R, Boller E, Bravin A, Brunet M, Chaimanee Y, Cloetens P, Feist M, Hoszwska J, Jaeger J-J, Kay RF, Lazzari V, Marivaux L, Nel A, Nemoz C, Thibault X, Vignaud P, Zabler S (2006) Applications of X-ray synchrotron microtomography for non-destructive 3D studies of paleontological specimens. Appl Phys A 83(2):195–202 Trinkaus E (1990) Cladistics and the hominid fossil record. Am J Phys Anthropol 83:1–11 Wagner GP (1996) Homologues, natural kinds and the evolution of modularity. Am Zool 36:36–43 Wagner GP, Altenberg L (1996) Perspective: complex adaptations and the evolution of evolvability. Evolution 50:967–976 Williams TA, Nagy LM (2001) Developmental modularity and the evolutionary diversification of arthropod limbs. J Exp Zool 291:241–257 Wind J (1984) Computerized X-ray tomography of fossil hominid skulls. Am J Phys Anthropol 63:265–282 Wind J, Zonneveld FW (1985) Radiology of fossil hominid skulls. In: Tobias PV (ed) Hominid evolution: past, present and future. Proceedings of the Taung Diamond Jubilee international symposium, Johannesburg and Mmabatho, Southern Africa, January 27-February 4, 1985. Alan R. Liss, New York, pp 437–442 Winther RG (2001) Varieties of modules: kinds, levels, origins, and behaviors. J Exp Zool 291:116–129 Wood B (1999) Homoplasy: foe and friend? Evol Anthropol 8:79–80 Zhao L-X, Lu Q-W, Xu Q-H (2000) Enamel microstructure of Lufengpithecus lufengensis. In: Wu X, Zhang S, Dong W (eds) Proceedings of 1999 Beijing international symposium on paleoanthropology: in commemoration of the 70th anniversary of the discovery of the first skull-cap of the Peking man. Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, pp 77–82 Zollikofer CPE, Ponce de Leon MS, Martin RD, Stucki RD (1995) Neanderthal computer skulls. Nature 375:283–285 Zonneveld FW, Wind J (1985) High-resolution computed tomography of fossil hominid skulls: a new method and some results. In: Tobias PV (ed) Hominid evolution: past, present and future. Proceedings of the Taung Diamond Jubilee international symposium, Johannesburg and Mmabatho, Southern Africa, January 27-February 4, 1985. Alan R. Liss, New York, pp 427–436 Zonneveld FW, Spoor CF, Wind J (1989) The use of CD in the study of the internal morphology of hominid fossils. Medicamundi 34:117–128 Page 13 of 13

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_29-5 # Springer-Verlag Berlin Heidelberg 2013

Morphological Evidence for Primate Origins and Supraordinal Relationships Mary T. Silcoxa*, Eric J. Sargisb, Jonathan I. Blochc and Doug M. Boyerd a Department of Anthropology, University of Toronto Scarborough, Toronto, ON, Canada b Department of Anthropology, Yale University, New Haven, CT, USA c Florida Museum of Natural History, University of Florida, Gainesville, FL, USA d Biological Sciences Building, Duke University, Department of Evolutionary Anthropology, Durham, NC, USA

Abstract There are five major scenarios that have been advanced to account for the early events in the origination of the order Primates: a transition from terrestriality to arboreality, the adoption of a grasp-leaping mode of locomotion, the evolution of features for visual predation, an adaptation to terminal branch feeding occurring during angiosperm diversification, or a combination involving terminal branch feeding followed by visual predation. These hypotheses are assessed using both neontological and fossil data. Of the five scenarios, the angiosperm diversification hypothesis is not contradicted by modern data and is found to be the most consistent with the fossil record. In particular, the evolution of features for manual grasping and dental processing of fruit in the earliest primates (primitive plesiadapiforms), and the subsequent development of features for better grasping and more intense frugivory in the common ancestor of Euprimates and Plesiadapoidea, is consistent with a close relationship between early primate and angiosperm evolution. All the other scenarios are less consistent with the pattern of trait acquisition through time observed in the fossil record. Consideration of non-euprimates (e.g., scandentians and plesiadapiforms) is found to be essential to viewing primate origins as a series of incremental steps rather than as an event.

Introduction: What Is a Primate? Perhaps the most fundamental issue facing students of primate origins can be summarized by a simple question: what is a primate? A clear concept of the diagnosis and taxonomic composition of Primates is essential to providing a coherent understanding of when and why the order separated from the rest of Mammalia. Attempts to define the order Primates have typically started by considering which features of modern primates are present in multiple primate species and are distinctive relative to other mammals. Four major adaptive complexes of traits have been recognized as characteristic of primates of modern aspect (¼Euprimates Hoffstetter 1977; see Mivart 1873; Le Gros Clark 1959; Napier and Napier 1967; Martin 1968, 1986, 1990; Szalay 1968; Cartmill 1972, 1992; Szalay et al. 1987):

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1. Traits associated with grasping. These include relatively longer hand and foot phalanges, a divergent thumb and big toe, and digits tipped with nails rather than claws. 2. Traits associated with leaping. Although such features have been lost in some extant primates (e.g., Homo sapiens), the most primitive euprimates have leaping characteristics that include hind limbs that are long relative to the forelimbs and modified ankle bones. 3. Traits associated with improvements to the visual system. These features include large eyes, convergent orbits, and a postorbital bar or septum. The larger and more complex brain in modern primates compared to other euarchontans may also be associated, in part, with this complex (Barton 1998; Kirk 2006; Silcox et al. 2009b, 2010a). A smaller apparatus for the sense of smell is presumably associated with an increasing reliance on vision as well, leading to a short snout and proportionally reduced related areas of the brain (Silcox et al. 2011). 4. Dental traits associated with herbivory. Relative to specialized insectivores, primates possess teeth that are low crowned, with blunt and bulbous (bunodont) cusps and broad talonid basins, which are features related to eating non-leafy plant materials (e.g., fruit) rather than insects or meat. Presence of a petrosal bulla has also often been cited as an ordinally diagnostic primate trait (e.g., Cartmill 1972). However, the ubiquity of this feature is questionable since developmental data are required to definitively document it (MacPhee et al. 1983), and its adaptive significance (if any) is unclear. Defining the order Primates using observations on living taxa as a starting point is problematic because any traits chosen are unlikely to have evolved simultaneously. Instead, a definition that recognizes the process of primate evolution and that encompasses the earliest, possibly stem, members of the order will have greater explanatory power. This problem is discussed further below.

Ecological Scenarios for Primate and Euprimate Origins Researchers investigating primate origins have typically focused on building an ecological scenario that could explain the evolution of one or more of these adaptive complexes. The earliest such scenario is the arboreal hypothesis of primate origins, which traces its roots back to the work of G. Elliot Smith and F. Wood Jones in the early part of the twentieth century. The arboreal hypothesis was extended and broadly popularized by W.E. Le Gros Clark (1959). In this hypothesis, grasping extremities were seen as having value for more secure climbing, and the distinctive primate orbital features were explained as being useful for judging distances in the trees during leaping. All the other ecological scenarios that have been developed assume a life in the trees for ancestral primates but seek to go beyond simple arboreality to consider more specific types of behavior. Szalay and colleagues (e.g., Szalay and Delson 1979; Szalay and Dagosto 1980, 1988; Szalay et al. 1987; Dagosto 1988) considered a derived locomotor mode, grasp-leaping, to have driven the evolution of most of the features that characterize euprimates, including those of the visual apparatus. They linked the ability to rapidly jump from branch to branch with the need to be “. . .subsequently securely anchored” (Szalay and Delson 1979, p. 561) to the landing point. Visual changes were relevant to judging distances in rapid, leaping locomotion (Szalay and Dagosto 1980, 1988: Dagosto 2007). Crompton (Crompton et al. 1993; Crompton 1995; Crompton and Sellars 2007) subsequently argued that acrobatic leaping in euprimates requires visual specializations and Page 2 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_29-5 # Springer-Verlag Berlin Heidelberg 2013

that leaping may have evolved as a predator evasion strategy, based on studies of leaping mode and proclivity in modern strepsirhines. In Szalay’s hypothesis, anatomical changes for grasp-leaping were preceded by a shift to a more herbivorous diet in primitive primates (i.e., plesiadapiforms) thought to be ancestral to Euprimates (Szalay 1968, 1972; Szalay and Dagosto 1980; Szalay et al. 1987). Cartmill (1972, 1974, 1992, 2012) focused on visual predation as key to the origin of Euprimates. The visual predation hypothesis as originally conceptualized (see below) linked visual features beneficial to accurately gauging the distance to prey items with grasping hands and feet that could provide both a secure hold on narrow supports and a prehensile apparatus for snatching prey (Cartmill 1974). Because he thought they lacked orbital specializations and grasping features, Cartmill advocated excluding plesiadapiforms from Primates. Sussman (1991; Sussman and Raven 1978; Sussman et al. 2013) suggested a link between the origin of Primates and the Cenozoic diversification of angiosperms (i.e., trees that produce fruit and flowers). He agreed with Szalay that a key event in early primate evolution was the invasion of the “arboreal mixed feeding adaptive zones” (Sussman and Raven 1978, p. 734) in the Paleocene. This involved increased use of non-leafy plant resources by early primates as angiosperms developed features that made them more tempting to non-insect seed and pollen dispersers, such as specialized flowers and larger fruit. With the appearance of still larger propagative plant organs (e.g., fruit, seeds) near the Paleocene-Eocene boundary, the ancestral euprimates developed features for entering terminal branches to better exploit these resources. Two major classes of data have been used to assess the relative validity of these various ecological scenarios. The first “tests” various ecological functions assigned to character complexes in the different models using the comparative method (e.g., Kay and Cartmill 1977; but see Bock and von Wahlert 1965; Bock 1977). The second employs the fossil record to document the sequence of anatomical changes that occurred in primate evolution and seeks to tie these changes to adaptive shifts (e.g., Bloch and Boyer 2002; Bloch et al. 2007).

Comparative Method Cartmill (1970, 1972, 1974) assessed the then prevalent arboreal hypothesis from the point of view of the diversity of modern arboreal animals. He argued that if living in an arboreal habitat could explain the distinctive features of primates, then these traits should also be found in other arboreal forms, and particularly in the arboreal members of groups that also include terrestrial species. Cartmill found that arboreal animals in general do not have features similar to those seen in modern primates. For example, arboreal squirrels are not more primate-like than terrestrial squirrels in certain specialized grasping traits, such as a reduction of the claws, or in vision-related features like the degree of orbital convergence. Nonetheless, arboreal squirrels are successful at many of the same behaviors practiced by primates, including making reasonably long jumps and foraging among slender branches. He argued that forward-facing orbits, while enhancing stereoscopy, decrease parallax and with it the ability to judge distance at longer ranges. For this reason, orbital convergence is not a very useful trait for gauging distances in a jump, but is very effective for visualizing objects close to the face. Based on these comparisons, it seems unlikely that the distinctive adaptive complex of euprimates can be simply linked to a shift to an arboreal mode of life. Cartmill’s hypothesis of primate origins, visual predation, has also been challenged from the standpoint of modern analogy. Sussman (1991; Sussman et al. 2013; see also Crompton 1995) pointed out that most living primates are omnivores, not specialized insectivores. This includes, for example, cheirogaleids (Atsalis 2008), which are often viewed as good living models for the Page 3 of 27

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ancestral euprimate (Sussman et al. 2013). What’s more, for many primates their methods of prey capture emphasize scent and hearing over vision (Sussman et al. 2013). For example, tarsiers have been observed to capture their prey with their eyes closed (Niemitz 1979), and the most orbitally convergent primates, the lorises, use scent to detect their slow-moving and often smelly prey (Sussman et al. 2013). If living primates are not typically specialized visual predators, it is not clear why one would expect morphologically similar extinct species to be. Alternatively, some authors (e.g., Sussman and Raven 1978; Sussman 1991; Crompton 1995) have sought analogues for early primates among frugivores, such as Old World fruit bats. The absence of primate-like visual features in some modern visual predators (e.g., mongooses, tupaiid treeshrews, many species of birds; Cartmill 1992; Sussman et al. 2013) and the presence of convergent orbits in some exclusively herbivorous taxa (koalas, sloths, fruit bats, kinkajous; Rasmussen and Sussman 2007; Sussman et al. 2013) suggest that there is no simple relationship between forward-facing orbits and visual predation. A possible “solution” to this criticism that the euprimate-like mechanism of orbital convergence for prey capture is only needed in nocturnal animals (Allman 1977; Cartmill 1992) could be refuted if the earliest euprimates were not nocturnal (see below). Sussman’s (1991; Sussman and Raven 1978; Sussman et al. 2013) angiosperm diversification hypothesis has been criticized based on the lack of an association between the diversification of angiosperms and the evolution of adaptations in arboreal marsupials that converge on those seen in primates (Cartmill 1992). Nonetheless, in a study of the somewhat primate-like South American didelphid marsupial Caluromys derbianus, Rasmussen (1990) did find some support for Sussman’s model, in that a substantial part of its diet comes from terminal branch fruit feeding in a manner similar to modern primates. Rasmussen and Sussman (2007) found similarly analogous species among the Australian marsupial radiation, including, for example, the pygmy-possum Cercartetus nanus. These species do eat insects, which they capture by grasping them with their hands, perhaps providing some support for Cartmill’s model; Cercartetus in particular has quite convergent orbits (Cartmill 1974). However, Caluromys does not have orbits that compare with primates in their degree of convergence (Rasmussen 1990), and a more detailed understanding of the behavior of C. nanus has led to its characterization as a flower specialist that only eats insects opportunistically, rather than as a visual predator (Rasmussen and Sussman 2007). These observations substantially weaken the link between convergent orbits and visual predation. Rasmussen’s (1990) study can be seen as providing a fifth, composite scenario for primate origins that has ancestral primates initially venturing out onto terminal branches to find fruit and other plant parts, with the secondary evolution of features for prey capture to capitalize on the insect resources they found in this milieu (Rasmussen 1990; Cartmill 1992). The grasp-leaping scenario of primate origins (Szalay and Delson 1979; Szalay and Dagosto 1980, 1988; Szalay et al. 1987; Dagosto 1988) is less susceptible to criticisms based on modern analogy than the other ecological scenarios because it does not depend on a general evolutionary relationship for its validity. Rather, it stems from a “fossil-first” approach to considering adaptive change, beginning with the evolutionary transitions documented in the fossil record, and then attempting to determine their adaptive meaning in a form-functional context. This highlights a major contrast in approaches to the question of primate origins among the major participants in the debate. Under Szalay’s approach, the unique origins, constraints, and evolutionary histories of different mammalian lineages mean that adaptive explanations applied to one group need not apply to any other. Cartmill, however, argues that “[t]he only evolutionary changes we can hope to explain are. . .parallelisms: recurrent modifications that show up over and over again in different lineages for the same structural or adaptive reasons. . .” (Cartmill 1993, p. 226). Page 4 of 27

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One limitation of Cartmill’s approach is that it assumes that all adaptive shifts of interest must be parallelisms, because otherwise there would be no possibility of explaining them. This reflects a more general issue with the use of modern analogy to test hypotheses about evolution. Any historical event is by definition a unique occurrence, even if it is more or less similar to other such unique occurrences that have taken place in other lineages. There is no reason to believe that everything that has happened once has happened twice. The evolutionary process that produced primates began at a unique starting point (i.e., the divergence of this clade from the rest of Mammalia), at a particular point in time, with a unique environmental and geographical context, and finished at a unique endpoint (i.e., the diversity of extant species). The starting point was heavily constrained by the evolutionary history of what went before, and the adaptive significance of the features evident at the current endpoint is dependent not only on the current usage of a given trait but also on the biological needs of all the animals that existed along the evolutionary lineage leading to a particular modern species. Modern non-primates that appear similar to primates might have passed through series of adaptive stages quite different from those experienced by primates’ distant ancestors and thus may have arrived at their current form by a very different path. For this reason, arguments that ancient marsupials did not acquire their primate-like traits as a result of angiosperm diversification are not directly relevant to the question of whether or not primates did. The study of modern primates, or modern non-primate analogues, in isolation cannot provide a demonstrably accurate picture of the process of primate origins – it can only yield hypotheses that are more or less plausible for subsequent testing by the fossil record. A somewhat analogous situation occurred in the early history of human paleontology. In the early part of the twentieth century, quite plausible scenarios were proposed that suggested either a large brain or bipedal locomotion as being the first-occurring distinct human trait (Lewin 1987). With the discovery and then acceptance of australopiths (primitive human ancestors with adaptations for bipedal locomotion but relatively small brains; McHenry and Coffing 2000) as hominins any “brains first” scenario was decisively falsified, no matter how plausible it may have seemed on the surface. And so too must any ecological scenario of primate origins be considered falsified, if the predicted pattern of trait acquisition is not matched by the fossil record.

Fossil Record Primate Supraordinal Relationships While in a strict sense the origin of Primates was no more dramatic than a single speciation event (Henke and Tattersall 2007; Cartmill 2012), the fossil record suggests that many of the characteristics thought to distinguish Euprimates were acquired incrementally through the first ten million years of primate evolution in the Paleocene (Bloch et al. 2007). It is to this process that the ecological hypotheses for Primate origins apply. Elucidation of this adaptive process relies centrally on knowing the relationships of taxa at the base of the primate tree, to understand the evolutionary steps taken to build the first euprimate. There is a growing consensus on the broader relationships of Primates within Mammalia. Molecular analyses have fairly consistently recovered a group including Primates, treeshrews (Scandentia), and colugos (Dermoptera; Adkins and Honeycutt 1991; Waddell et al. 1999; Liu et al. 2001; Murphy et al. 2001a, b; Springer et al. 2003, 2004). Waddell et al. (1999) suggested the name Euarchonta for this clade. This name makes allusion to an earlier hypothesis of primate supraordinal relationships: the group Archonta, which included bats with these three orders (Gregory 1910; Novacek 1992; McKenna and Bell 1997). Molecular studies have consistently failed to find a close relationship between bats and the other archontans – rather, chiropterans have generally grouped with carnivorans and ungulates (e.g., Pumo et al. 1998; Miyamoto et al. 2000; Page 5 of 27

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Fig. 1 Illustration of P. lowii, the pen-tailed treeshrew. This arboreal species may be the best living model for the ancestor of Euarchonta and of Primates (Photo by Annette Zitzmann # 1995)

Liu et al. 2001; Murphy et al. 2001a, b; Springer et al. 2003, 2004). As a result, the concept of Archonta sensu lato has fallen out of favor. Rodents and rabbits (Glires) are supported as the closest relatives to Euarchonta (Murphy et al. 2001a, b; Madsen et al. 2001). The resulting clade has come to be known as Euarchontoglires (Murphy et al. 2001b). Euarchontoglires is linked to a clade including ungulates, whales, lipotyphlan “insectivores,” carnivorans, and bats (Laurasiatheria) in Boreoeutheria (Springer and de Jong 2001). Within Euarchonta, there is less of a consensus about the branching pattern among the three ordinal groups. In terms of the sister taxon of Primates, all three possibilities have been recovered in various analyses: Scandentia (e.g., Novacek 1992; Liu et al. 2009), Dermoptera (e.g., Janecˇka et al. 2007), and Sundatheria (Scandentia + Dermoptera; e.g., Liu et al. 2001; Murphy et al. 2001a, b; Springer et al. 2003, 2004; Bloch et al. 2007; Nie et al. 2008; Ni et al. 2010). In an analysis that combined molecular data with the largest morphological dataset yet compiled for the study of mammalian interrelationships, O’Leary et al. (2013) found strong support for Sundatheria as the sister taxon of Primates. If this hypothesis is correct, it implies that the best model for the ancestor of primates based on extant forms is represented by the reconstructed common ancestor of Euarchonta, not by treeshrews in isolation. In particular tupaiids, the diurnal family of treeshrews often used for comparison to primates (e.g., Beard 1993a), become less relevant as ancestral primate models. The sole living member of the family Ptilocercidae, Ptilocercus lowii, is the extant treeshrew closest to the base of Scandentia (Olson et al. 2004, 2005; Roberts et al. 2011) and shares many more features than tupaiids do with dermopterans (Sargis 2001a, 2002a, b, c, d, 2004, 2007). These shared features are present in Ptilocercus and dermopterans in spite of some fundamental differences between their locomotor modes (gliding in dermopterans, arboreal quadrupedalism in Ptilocercus; Sargis 2001a, 2002a, b, c, d, 2004, 2007), implying that they

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may be ancestral for the common ancestor of Dermoptera and Scandentia, or even of Euarchonta. As such, Ptilocercus lowii might provide the best living model for the common ancestor of Primates (Fig. 1). Even if this hypothesis of relationships is not correct, and either Scandentia or Dermoptera is the true sister taxon to primates, the fact that Ptilocercus is consistently recovered as the most basally divergent treeshrew (Olson et al. 2004, 2005; Roberts et al. 2011), coupled with the extremely specialized morphology of all living dermopterans, implies that Ptilocercus is probably still the best living model for the common ancestor of Primates. In terms of extinct taxa, the group most critical to evaluating the supraordinal relationships of primates are the plesiadapiforms. “Plesiadapiformes” is a paraphyletic grouping of extinct fossil mammals known from the Paleocene and Eocene of North America, Europe, and Asia (Russell 1964; Beard and Wang 1995; Fu et al. 2002; Smith et al. 2004; Silcox and Gunnell 2008). Although Tabuce et al. (2004) argued that there was also an African family of plesiadapiforms (Azibiidae), they later revised their interpretation and classified the relevant species into Euprimates as primitive strepsirhines (Tabuce et al. 2009). Represented by over 140 named species classified into 11 families, plesiadapiforms represent a very diverse radiation and form a significant component of the fauna recovered from many Paleocene localities (Rose 1981; Gunnell et al. 1995). The systematic position of plesiadapiforms has been a matter of long-standing debate. Based largely on dental similarities, most early workers classified plesiadapiforms in Primates, often specifically in Tarsiidae (e.g., Matthew and Granger 1921; Gidley 1923). More recently plesiadapiforms have been thought of as the first radiation of the order Primates, more primitive than any modern group (e.g., Szalay and Delson 1979; MacPhee et al. 1983; Szalay et al. 1987). This idea has been challenged on a variety of fronts. Martin (1968) and Cartmill (1972) advocated removing plesiadapiforms from Primates to allow for a clearer definition of the order. However, in failing to provide a clear alternative classification for plesiadapiforms (beyond dumping them in a wastebasket “Insectivora”), this approach did little to clarify primate supraordinal relationships. Wible and Covert (1987) also suggested removing plesiadapiforms from the order Primates, on the grounds that cranial evidence was more supportive of a scandentian-euprimate tie than a plesiadapiform-euprimate one. They argued that the dental evidence linking plesiadapiforms to euprimates (excluding scandentians) consisted only of ill-defined “trends” (Wible and Covert 1987, p. 9). This conclusion was not based on any detailed consideration of teeth, however, which is particularly problematic since the euprimate-plesiadapiform relationship had always been supported largely by dental evidence. And, like earlier objections to classifying plesiadapiforms in Primates, this argument dealt only with the issue of euprimate relationships, without providing any clear resolution to the question of where plesiadapiforms would be classified. Finally, in the early 1990s, an alternative systematic position for plesiadapiforms was suggested by Beard (1989, 1990, 1993a, b) and Kay et al. (1990, 1992), who argued that at least some members of this group (Paromomyidae and Micromomyidae) shared closer ties to Dermoptera than Euprimates. Although these authors agreed on this point, their hypotheses of relationships were in disagreement in virtually every other way, including which taxon was the sister group to Euprimates (Scandentia in the case of Kay et al. 1992; Dermoptera + plesiadapiforms according to Beard 1993a). And, as in Wible and Covert (1987), very little consideration was given to the dentition. Beard’s (1989, 1990, 1993a, b) and Kay and colleagues’ (1990, 1992) conclusions have been challenged by numerous studies on both phylogenetic and functional grounds (e.g., Krause 1991; Szalay and Lucas 1993, 1996; Wible 1993; Wible and Martin 1993; Van Valen 1994; Runestad and Ruff 1995; Stafford and Thorington 1998; Hamrick et al. 1999; Bloch and Silcox 2001; Sargis 2002d, 2007; Bloch and Boyer 2002, 2003; Silcox 2001, 2003, 2008; Bloch et al. 2007; Boyer and Page 7 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_29-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 2 Skeletons representing three plesiadapiform families were recovered from Late Paleocene limestones (Bloch and Boyer 2007, Fig. 3). Paromomyidae is represented by (a) Acidomomys hebeticus (UM 108207) and (b) Ignacius cf. I. graybullianus (UM 108210). Carpolestidae is represented by (c) Carpolestes simpsoni (UM 101963; Bloch and Boyer 2002, Fig. 2a). Plesiadapidae is represented by (d) Plesiadapis cookei (UM 87990). Scales ¼ 5 cm

Bloch 2008). As one example, a key character proffered (Beard 1990, 1993b) in support of a relationship between some plesiadapiforms (paromomyids and micromomyids) and dermopterans to the exclusion of euprimates was unusual hand proportions, with elongate intermediate phalanges (Beard 1990, 1993b). Subsequent discoveries of better-associated plesiadapiform postcranial fossils have demonstrated that this inference was incorrect – the calculated hand proportions were the product of mixing hand and foot bones (Bloch et al. 2007; Boyer and Bloch 2008; see also Krause 1991; Hamrick et al. 1999). Discovery of numerous new specimens of plesiadapiforms, documenting previously poorly known or totally unknown anatomical regions (Bloch and Boyer 2002, 2003; Bloch and Silcox 2001, 2006; Bloch et al. 2007; Boyer and Bloch 2008; Boyer 2009; Fig. 2), has prompted a reconsideration of plesiadapiform relationships. These data were included in an analysis that

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_29-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 3 (a) Single most parsimonious tree from a maximum parsimony analysis of 173 dental, cranial, and postcranial characters by Bloch et al. (2007). (b) Strict consensus tree of three most parsimonious trees from a maximum parsimony analysis of 240 dental, cranial, and postcranial characters by Silcox et al. (2010b). Note that in both analyses plesiadapiforms form a series of paraphyletic stem taxa at the base of Primates, and Plesiadapoidea is the sister taxon of Euprimates

sampled the cranium, dentition, and postcranium (Bloch et al. 2007; Fig. 3a) and incorporated observations on Ptilocercus. The results of this analysis failed to support the plesiadapiformdermopteran relationship. Rather, plesiadapiforms formed a paraphyletic stem group at the base of the order Primates. One subset of plesiadapiforms, the plesiadapoids (Plesiadapidae + Carpolestidae + Saxonellidae), was the sister taxon of Euprimates, making them crucial for establishing primitive states for that clade. Results from a subsequent analysis that included a broader sampling of mammals outside Euarchonta and a wider range of cranial and postcranial characters (Silcox et al. 2010b; Fig. 3b) were largely congruent with those of Bloch et al. (2007), apart from some details of the branching order among primitive plesiadapiforms (micromomyids and microsyopids).

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_29-5 # Springer-Verlag Berlin Heidelberg 2013

One implication of these results is that plesiadapiforms might be best included in the order Primates (Bloch et al. 2007; Silcox 2007), in a return to earlier conceptions of how to define the group (e.g., Szalay 1975; Szalay and Delson 1979; Szalay et al. 1987). This notion has received some support from a previous proponent of the plesiadapiform-dermopteran clade (Kay 2003) and was recently incorporated into papers by workers on opposite sides of the debate over the ecological context of primate origins (Cartmill 2012; Sussman et al. 2013; but see Ni et al. 2010, 2013 for an opposing view). The ecological scenarios discussed above take as their starting point the common features of modern primates. Plesiadapiforms do not possess all of these traits. If plesiadapiforms constitute the primate stem lineage, discussing “primate origins” then involves dealing with at least two sets of evolutionary transitions – first, the branching off of the primate stem and evolution of the earliest primate (Purgatorius; Van Valen and Sloan 1965; Johnston and Fox 1984; Fox and Scott 2011) and, second, the origin of Euprimates. Earlier discussions of “primate origins” that explicitly endeavored to explain only the latter transition (e.g., Cartmill 1972; Rasmussen 1990; Sussman 1991) are inherently flawed in trying to account for the concerted evolution of character complexes that did not arise at the same time, mixing the effect of multiple evolutionary transitions. This is true even if one chooses to classify plesiadapiforms as a non-primate sister group to the order. Using the hypothesis of primate supraordinal relationships given in Fig. 3a, Bloch et al. (2007) tested predictions about the sequence in which anatomical transformations occurred pursuant to the various ecological scenarios (e.g., Cartmill 1992). In the same way that “brains first” scenarios of human origins relied on the evolution of large brains before features for bipedalism, so the ecological scenarios of primate origins require a certain order for the addition of traits through time for them to be considered valid. Predictions for Ecological Scenarios of Primate and Euprimate Origins Under the arboreal hypothesis, the prediction is inherent that the evolution of characteristically primate traits coincided with a move into an arboreal habitus. If, on the other hand, the ancestors of primates were already arboreal while lacking such traits, then the arboreal hypothesis would be effectively falsified. It would also be falsified if the evolution of characteristic primate features pre-dated a move to the trees, for example, if forward-facing orbits were found in an animal otherwise adapted for a terrestrial habitus. The grasp-leaping hypothesis posits a relationship between the evolution of features for grasping and those for leaping. As such, if grasp-leaping is to function as an explanatory hypothesis for euprimate origins, then the evolution of these features should coincide in time. Visual features for improved stereoscopy should also coincide with the adoption of a more rapid, leaping, locomotor mode. Although it may still be true that early euprimates were functionally grasp-leapers, if such a coincident evolution of the relevant traits is not found, then this hypothesis would lose its explanatory power as a central motivating force in euprimate origins. It is more difficult to generate a set of predictions for the visual predation hypothesis because Cartmill’s views appear to have changed through time with respect to how the various distinctive primate traits are supposed to have evolved in the context of this scenario. Cartmill (1974) made an explicit link between the utility of specialized grasping with hindfeet and visual predation: “. . .these visually guided predators [Cercartetus and Caluromys] also have grasping hindfeet. The utility of this trait to their way of life is evident” (p. 69). “. . .it is reasonable to conclude that these novelties [“grasping extremities and large, convergent orbits”] were functionally related. . .” (p. 70). At the time he apparently did not consider clawlessness per se to be part of this complex:

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_29-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 4 Results from a maximum parsimony analysis of 173 dental, cranial, and postcranial characters by Bloch et al. (2007), with the most significant evolutionary transitions for primates mapped on. “Dental features” include molars that are low crowned, with bunodont cusps and broad talonid basins (all three of which are related to increased herbivory; Szalay 1968), an enlarged M3 hypoconulid, and a postprotocingulum (nannopithex or postprotocone fold) on P4. Evidence for euprimate-like manual grasping includes an increase in the relative length of the digits. Pedal grasping involves the evolution of a divergent big toe with a nail. Visual features include increased orbital convergence and the postorbital bar. Note that these transitions occur in a steplike fashion, with only visual features and leaping being added at the euprimate node

“Reduction of the claws and development of grasping specializations of the hand have occurred independently, in different ways and for different reasons in various primate lineages” (p. 76). On the other hand, in 1992 Cartmill suggested that grasping extremities and claw loss, he suggested, had also originated as predatory adaptations (Cartmill 1992, p. 107; emphasis ours) based on the habits of small prosimian primates like Microcebus, Loris, and Tarsius, which track insect prey by sight and seize them in their hands. This implies that these features should be tied together temporally, since they were acquired as part of the same adaptive shift to more predatory behaviors. However, Kirk et al. (2003, p. 741b) claimed that Bloch and Boyer (2002) mis-characterized visual predation suggesting that “[a]s originally formulated (Cartmill 1972), Cartmill’s thesis interprets the prehensile, clawless extremities of primates as adaptations for locomotion on slender arboreal supports,” and Cartmill (2012, p. 216) stated that “[c]omparative anatomy reveals no necessary connection between grasping hind feet and visual predation.” This suggests that Cartmill now considers visual predation not to be the explanation for the evolution of grasping characteristics in primate evolution in spite of his earlier assertions. What is impossible to deny, however, is that visual predation is a dietary hypothesis. Since visual predation involves an increasing reliance on insect prey, this should also be reflected in the teeth of the earliest euprimates. This is true even if these forms were grasping prey with their hands rather than with their teeth (contra Cartmill 1972, 1974), because dental features for insectivory reflect not only prey capture but also processing of food items with the unique physical properties of insects. If early primates or euprimates were found to be equally or less insectivorous than their forbears, visual predation would be refuted as a central motivating force in early primate evolution. Since visual predation also relies to some degree on nocturnality (Allman 1977; Cartmill 1992), a finding that the earliest primates or euprimates were diurnal would substantially weaken this hypothesis. The angiosperm diversification hypothesis predicts two stages in the evolution of primates. First, with the initial exploitation of the arboreal mixed feeding adaptive zone, a dental shift reflecting Page 11 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_29-5 # Springer-Verlag Berlin Heidelberg 2013

more use of plant resources should be seen. Second, as the terminal branches were invaded and the use of the food resources from this milieu was intensified, grasping and dental features reflecting these changes should appear. Disassociation between traits for eating fruit or flowers, and those indicating the ability to access terminal branches, would weaken the explanatory power of this hypothesis. Similarly, the combined hypothesis suggested by Rasmussen (1990), involving first terminal branch feeding on fruit, and then visual predation, requires that “the earliest euprimates had grasping feet and blunt teeth adapted for eating fruit, but retained small, divergent orbits like those of Plesiadapis” (Cartmill 1992, p. 111). Subsequent evolution should add features for visual predation, such as forward-facing orbits and teeth with improved capabilities for processing insects, to this basic model. If, however, convergent orbits evolved at the same time as grasping feet or blunt teeth or their appearance was not coincident with the evolution of teeth better designed for eating insects, then this model would be effectively falsified. Assessment of Ecological Scenarios With the well-supported pattern of relationships found by the current authors (Bloch et al. 2007; Fig. 3a), it becomes possible to consider the predictions outlined above in light of what is known about the fossil record (Fig. 4). In terms of the arboreal hypothesis, the inferred arboreal habits of all plesiadapiforms known from postcranials (Szalay and Decker 1974; Szalay et al. 1975; Szalay and Drawhorn 1980; Szalay and Dagosto 1980; Szalay 1981; Gingerich and Gunnell 1992; Beard 1989; Bloch and Boyer 2002, 2003, 2007; Bloch et al. 2007; Boyer and Bloch 2008) make it clear that the ancestors of Euprimates were already arboreal. Identification of arboreal features in ankle elements of the most primitive known primate, Purgatorius, underlines the antiquity of this feature in the context of the primate radiation (Chester et al. 2012). This is further reinforced by the inclusion of Primates in Euarchonta, because this supraordinal group likely had an arboreal ancestor (Szalay and Drawhorn 1980; Sargis 2001a, 2002e). As such, distinctively euprimate traits cannot be linked to a simple move from a terrestrial to an arboreal habitus. The fact that Ptilocercus lowii, an arboreal mammal, may be the best living model for the ancestor of Euarchonta, and thus possibly for Primates (Sargis 2001a, 2002e; Bloch et al. 2003; see above), strongly suggests that arboreality is a feature that evolved prior to the base of the primate radiation (Szalay and Drawhorn 1980). Many of the features that have been cited as possible euarchontan synapomorphies (Szalay and Drawhorn 1980; Szalay and Lucas 1996; Sargis 2002d; Silcox et al. 2005) can also be linked to arboreal locomotion. It is likely that arboreality evolved in the ancestor of Euarchonta (Szalay and Drawhorn 1980; Sargis 2001a, 2002e) and that this trait was retained (but did not originate) in the ancestor of Primates. The evolution of grasping is central both to the assessment of the grasp-leaping hypothesis and to the visual predation hypothesis as outlined by Cartmill in 1992. With a better fossil record for plesiadapiforms, it is now clear that grasping is not a single character state or set of coordinated transformations. The ancestral euarchontan was likely capable of Ptilocercus-like grasping (Szalay and Dagosto 1988; Sargis 2001b, 2002b, e, 2004; Sargis et al. 2007). As Bloch and Boyer (2002, 2003; see also Sargis et al. 2007) demonstrated, the evolution of fully euprimate-like grasping was at least a two-stage process. Features for manual grasping, including relatively long digits of the hand, are present in all plesiadapiforms known from relevant material, with the exception of plesiadapids who are inferred to have secondarily lost this trait (Bloch and Boyer 2002, 2003; Boyer et al. 2004; Kirk et al. 2008; Boyer 2009). Euprimate-like pedal grasping, including an opposable big toe with a nail, is present in Carpolestes simpsoni and can be reconstructed as having evolved in the common ancestor of Plesiadapoidea and Euprimates (Bloch and Boyer 2003; Sargis Page 12 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_29-5 # Springer-Verlag Berlin Heidelberg 2013

et al. 2007). Although Gebo (2009) took issue with the characterization of the morphology of Carpolestes simpsoni as euprimate-like, the shared possession of critical features such as the saddle-shaped distal facet on the entocuneiform for articulation with the first metatarsal, proximal expansion of the medial surface of this facet, and torsion of the first metatarsal (Bloch and Boyer 2002, 2003; Sargis et al. 2007) demonstrates that these groups both possess key elements of the grasping functional complex. As such, Cartmill’s (2012, p. 216) assertion that grasping feet “probably evolved independently in C. simpsoni and euprimates” is a matter of opinion that has not been demonstrated in a phylogenetic framework. Plesiadapiforms lack features associated with specialized leaping (Szalay et al. 1975; Szalay and Dagosto 1980; Gingerich and Gunnell 1992; Beard 1989; Bloch and Boyer 2002, 2007; Bloch et al. 2007). Carpolestes simpsoni, for example, lacks the relatively long legs typically seen in a leaping mammal, indicating that it was a more generalized arboreal quadruped (Fig. 2c; Bloch and Boyer 2002). The semicircular canal evidence also supports the inference that plesiadapiforms known from cranial material did not use “jerky patterns” of locomotion characteristic of leaping primates (Silcox et al. 2009a). The first primate taxa with some leaping characteristics are early euprimates such as Cantius, Teilhardina, and Omomys (Rose and Walker 1985; Anemone and Covert 2000; Gebo et al. 2012). Although current evidence suggests leaping and visual traits did evolve at the same time, there is a distinct offset between the evolution of features related to grasping and those for leaping. In light of this, although early euprimates were likely grasp-leapers and leaping may have evolved in the ancestral euprimate (Szalay and Dagosto 1980, 1988; Dagosto 1988), the evolution of grasp-leaping was not the event that shaped the origin of Primates or Euprimates. Similarly, no known plesiadapiforms show any of the specialized features of the orbital system that are associated with euprimate-like vision, including a complete postorbital bar, convergent orbits, reduced snout, or an enlarged and reorganized brain (McKenna 1966; Szalay 1969, 1972; Russell 1964; Kay and Cartmill 1977; Kay et al. 1992; Bloch and Silcox 2006). Therefore, there is an offset between the evolution of grasping and visual features. As such, their coordinated acquisition as part of a shift to a new mode of feeding, visual predation, was not the decisive event in shaping primate or euprimate origins. It is still possible that adding visual predation to the behavioral repertoire of Euprimates was an important event in the evolution of this group, in which grasping features effectively acted as an exaptation (“preadaptation,” Gould and Vrba 1982). There are multiple lines of evidence that lead one to doubt this scenario, however. First, as discussed above, visual predation becomes mechanistically implausible if the earliest euprimates were diurnal (Allman 1977; Cartmill 1992). The primitive activity pattern of Primates is very much in debate. For example, Ni et al. (2004) interpreted a primitive euprimate skull from Asia as having been diurnal. Although there are some problems with this conclusion (Martin 2004; Heesy and Ross 2004; Bloch and Silcox 2006), it draws attention to the fact that the ancestral activity period for euprimates cannot be assumed to have been nocturnal. Indeed, Ankel-Simons and Rasmussen (2008) suggest that early euprimate communities likely included a mix of nocturnal and diurnal species. This would make it difficult to argue that nocturnal visual predation would have been universally important to early euprimates. Second, if euprimates did undergo a transition to becoming more focused on visual predation, then they should have teeth that are indicative of a more insectivorous diet than their precursors. This is not demonstrably true. The earliest known euprimate, Altiatlasius koulchii, has extremely low-crowned teeth with very bunodont cusps (Sige´ et al. 1990), which is not consistent with a predominantly insectivorous diet. Of the two best-documented groups of early euprimates, adapoids are usually viewed as being frugivorous and omomyoids as omnivorous (Rose 1995; Page 13 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_29-5 # Springer-Verlag Berlin Heidelberg 2013

Bloch and Boyer 2003). The only gut contents known for a primitive fossil primate (the adapoid Darwinius from Messel) include fruit remains and no insects. This is likely a real reflection of diet, rather than a taphonomic artifact because in other Messel specimens insect remains preserve well (Franzen and Wilde 2003). Cartmill (2012, p. 216) responded to this objection by suggesting that “[w]e cannot determine which dietary preference is oldest by counting noses.” It is certainly true that commonness of a feature does not imply primitiveness (Maddison et al. 1984). However, it is possible to use optimization techniques to infer, from the distribution of traits across a set of relationships, what is most parsimoniously considered to be primitive. Boyer (2007) performed precisely such a test and found no evidence for a shift in dietary behavior toward insectivory at the basal Euprimate node. What’s more, if early euprimates were succeeding and diversifying primarily because they were improving their insect-harvesting abilities, then they should show dental features that indicate that they were at least as well adapted for processing insects as insectivorous mammals living at the same time. This is not the case – most specialized insectivores from the Paleocene and Eocene have much higher crowned teeth and sharper cusps than early primates. It is precisely the absence of such features and the presence of characteristics for processing non-leafy plant material, such as low-crowned molars with broad talonid basins, that makes it possible to separate primitive primate and insectivore teeth in the fossil record. The insectivores most similar to primates in dental form can be reconstructed as having a more omnivorous diet than their specialized insectivorous kin. For example, the erinaceomorph Macrocranion tupaiodon from Eocene deposits at Messel, which has superficially primate-like teeth, is known from stomach contents to have eaten not only insects but also plant material and substantial quantities of fish (Storch and Richter 1994). Cartmill (2012, p. 216) suggested that the fossil record is too incomplete to be used to understand adaptive events around the euprimate node, so that “the main evidence for the ecological correlates of the euprimate peculiarities has to come from functional and comparative anatomy,” presumably of extant species. As discussed above, there are numerous incidences of a lack of fit between visual predation and orbital convergence from such studies. Furthermore, there are competing adaptive hypotheses for having convergent orbits. For example, Changizi and Shimojo (2008) argued for a distinct adaptive context for this feature, related to picking out items from a cluttered environment, such as a tree with leaves. These items include any object of greater interest than the clutter, whether it be the location of a branch, a flower, an insect, or a predator. Not only are forward-facing eyes more useful in a cluttered environment, but laterally placed eyes (as in squirrels) are less critical for predator detection since inhabiting a “cluttered” environment also bestows cover from the eyes of hunting predators. The features suggesting a more herbivorous diet in early primates and euprimates are supportive of the angiosperm diversification hypothesis (Sussman et al. 2013). Within various plesiadapiform lineages and early euprimate groups, improved features for exploiting plant propagative organs continue to appear through the Paleocene and Eocene (Gingerich 1976; Biknevicius 1986; Rose 1995; Bloch and Boyer 2002). It has been argued (Cartmill 1992) that the angiosperm diversification hypothesis fails to explain the rest of the distinctive traits seen in modern primates (i.e., visual features and leaping). However, Changizi and Shimojo (2008) consider this hypothesis to be consistent with their ideas about the evolution of convergent orbits for differentiating objects in a cluttered environment. Crompton (1995, p. 18) also made this point, suggesting that convergent orbits might have been beneficial in allowing detection of the “small, and often very inconspicuous” food items taken by small primates. Cartmill’s (2012, p. 217) response to this proposal was to suggest that special visual features are not needed to perceive fruits or flowers because angiosperms advertise their presence Page 14 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_29-5 # Springer-Verlag Berlin Heidelberg 2013

with “shiny bright colors and sweet smells.” However, it seems important to remember that angiosperms are not advertising their fruit to any possible frugivore. It does an angiosperm no good to have its seeds destroyed or deposited too close to the parent tree, so fruiting trees do not necessarily produce fruit that will be conspicuous to all. Not all fruit in a tropical environment is as easy to see as a domesticated banana. In terms of leaping, Rasmussen’s (1990, p. 273) observations of Caluromys also offer a potential explanation for the value of this locomotor mode to a terminal branch feeder: “[t]he grasping and leaping acrobatics exhibited by C. derbianus in Costa Rica enabled them to gain access to fruit that was apparently off limits to most of the other nocturnal frugivores of the study area.” Perhaps it was refinements to terminal branch feeding technique, offering new access to previously inaccessible food sources and greater abilities for discriminating food choice, that marked the transition to Euprimates. Rasmussen’s combination hypothesis might be seen as offering an alternative to the angiosperm origins scenario that explains, first, the grasping and fruit-eating dental features of basal primates and then the visual characteristics of euprimates. However, this combination hypothesis suffers from the same problems as visual predation in linking the evolution of orbital traits to increased insectivory in the absence of evidence for such a dietary shift. Based on the current evidence, the angiosperm diversification hypothesis applies best to the evolution of early primates. Furthermore, Szalay’s (1968) view of the key event in primate origins being a dietary transition to a more plantdominated repertoire is also supported by the current evidence.

Timing and Place of Origin of Primates and Euprimates The earliest occurring primate known is Purgatorius. Although one possible specimen of this genus is described as coming from the latest Cretaceous (Van Valen and Sloan 1965; Van Valen 1994), it is not a particularly diagnostic tooth (Clemens 2004; Silcox 2008) and comes from a deposit that is time averaged (Lofgren 1995). The earliest, well-dated, diagnostic primate material that has been published in detail pertains to Purgatorius coracis from the earliest Paleocene (Pu2) of Saskatchewan (Johnston and Fox 1984; Fox and Scott 2011; see Clemens and Wilson 2012 for a possible even earlier occurrence). Most of the rest of the early primate fossil record is North American, including all definitive micromomyids and palaechthonids, most microsyopids, and all the most primitive paromomyids, carpolestids, plesiadapids, and possibly saxonellid (Fox 1991). Plesiadapiforms have only been known from Asia since 1995 (Beard and Wang 1995), which suggests that this geographic bias may be a sampling phenomenon. The only Asian species that shows relatively primitive plesiadapiform morphology is Asioplesiadapis youngi Fu, Wang and Tong 2002 which is similar in some ways to the most primitive families of plesiadapiforms, the Purgatoriidae and “Palaechthonidae,” and differs in other ways including having a relatively reduced dental formula (Silcox 2008). As a relatively late-occurring species (early Eocene), A. youngi hints at the presence of more primitive lineages of primates in Asia. There remain, however, no Asian taxa as primitive in morphology as North American Purgatorius, implying that the fossil record is still most supportive of a North American origin for Primates. Springer et al. (2012) supported an Asian origin for Euprimates. However, their analysis was based on a molecular phylogeny, without the inclusion of any fossils. Since it is clear that the biogeographic patterns of many mammalian groups have changed over the last 65+ million years, it is critical to consider fossil evidence when assessing the place of origin for any group. Using evidence from the fossil record, Beard (1998) also argued that the origin of Euprimates could be Page 15 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_29-5 # Springer-Verlag Berlin Heidelberg 2013

reconstructed as unequivocally Asian. Silcox (2001, 2008) and Bloch et al. (2007) are more conservative in their interpretation of the fossil record, with origins in Asia, Africa, North America, or even Europe being possible in the context of current knowledge. Causes for this equivocation include the African location of the earliest known euprimate, Altiatlasius koulchii; the Asian location of the primitive euprimate Altanius orlovi; the North American location of much of the primitive plesiadapoid and euprimate record; and the European location of both some early euprimates (e.g., Donrussellia) and the poorly sampled plesiadapiform family Toliapinidae, which may be related to early euprimates (Silcox 2001). The time of origin of Primates and Euprimates can only be minimally constrained using fossil data. As noted above, the earliest known primate, Purgatorius, is from the earliest Paleocene (Fox and Scott 2011). In light of the primitive nature of this taxon, the fossil record is not consistent with a date much earlier than this, putting the origin of the group in the earliest Paleocene or latest Cretaceous. The fossil record for mammals more generally suggests a period of very rapid diversification shortly after the Cretaceous-Paleogene boundary (O’Leary et al. 2013). The earliest occurring euprimate, Altiatlasius koulchii, is late Paleocene in age (Sige´ et al. 1990; Gheerbrant et al. 1998), implying a divergence for Euprimates before the early Eocene. Furthermore, since the sister group to Euprimates (i.e., Plesiadapoidea) had diverged from their common stem by the latest early Paleocene, Euprimates must be at least that old. Recent molecular dating estimates, which take into account some of the more problematic assumptions inherent in molecular clock models, are starting to approach this timeframe. For example, Springer et al. (2012) estimated that living Primates shared a last common ancestor 71–63 million years ago, which suggests that molecular and fossil datasets are not as divergent as they once seemed (contra Cartmill 2012).

Conclusions: What Is a Primate? (Coda) When Cartmill developed the visual predation hypothesis, he suggested the removal from Primates of any taxa that lacked modern primate-like orbital and grasping features and thus presumably had not used this mode of feeding (Cartmill 1972, 1974). This was the primary basis for his suggested removal of plesiadapiforms from Primates. Such an approach to defining primates was perhaps an over-optimistic view of the support for visual predation – if, as suggested here, an evolutionary transition to this pattern of behavior is not clearly indicated by the fossil record, then this is surely not an appropriate criterion by which to determine inclusion or exclusion of taxa in the order Primates. This view is underscored by the fact that, of the three “ordinally diagnostic” traits that Cartmill (1972, p. 121) named to diagnose a plesiadapiform-free order Primates – “. . .the petrosal bulla, complete postorbital bar, and divergent hallux or pollex bearing a flattened nail. . .” – two are now known in plesiadapoid plesiadapiforms (Bloch and Boyer 2002, 2003; Bloch and Silcox 2006; Boyer 2009). The fossil record demonstrates that the characteristic primate traits listed in the introduction arose in a steplike fashion (Fig. 4). Thus, the criterion that all of these features must be present in a particular taxon for it to be considered a primate is biologically unnatural. Doing so would exclude taxa on the primate stem, which have some, but not all, of these traits, but postdate the divergence of the primate lineage from the rest of Mammalia. As demonstrated above, such stem taxa are critical for understanding the origin and early evolution of Primates, as well as the accumulation and modification of crucial features within this lineage. As advocates of phylogenetic taxonomy have made clear, there are some distinct advantages to formal taxonomic definitions that are based on specifying a particular ancestor, rather than on a list Page 16 of 27

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of mutable characters (Rowe 1987; De Queiroz and Gauthier 1990; Silcox 2007). For this reason, although compiling lists of distinctive primate traits is useful to the process of understanding primate origins, it is inappropriate to consider them formal definitions. Using the precepts of phylogenetic taxonomy, Silcox (2007) suggested the following definition for Primates: “the clade stemming from the most recent common ancestor of Purgatorius and Euprimates.” New discoveries will almost certainly change the prevailing views on the early parts of primate evolution. There is a number of substantial holes in the fossil record for primate origins which, when filled, may fundamentally shift perceptions of primate evolutionary history. First, there is a sizeable spatial discontinuity in the fossils currently available. Plesiadapiforms have only been discovered in Asia in the last 18 years (Beard and Wang 1995). For early euprimates, the few specimens of primitive forms known from Asia and Africa are suggestive of a much larger radiation that is almost completely unknown (Silcox 2001, 2008). Even in North America, the geotemporal patterning of the plesiadapiform and euprimate fossil records means that there are still substantial areas at crucial times that remain unsampled. Second, some taxonomic groups are also undersampled. Two families of plesiadapiforms, “Palaechthonidae” and Toliapinidae, have the potential to be crucial to an understanding of early primate and euprimate evolution, but both are very poorly known (but see Chester et al. 2011). The best-known plesiadapoids are all relatively derived members of their respective families. In light of the important position of Plesiadapoidea as the sister taxon to Euprimates, finding more, and more complete, primitive plesiadapoid specimens is vital (e.g., Boyer et al. 2004, 2012; Boyer 2009). Perhaps most importantly, a gap still exists between the known plesiadapiforms and the earliest euprimates. No known plesiadapoid has the morphology that would be expected in a euprimate ancestor – they are all too derived in features such as dental reduction, enlargement of the anteriormost incisors, and/or the shape of P4. Because the earliest plesiadapoids are late early Paleocene in age, Euprimates must have a ghost lineage, stretching through the middle and late Paleocene, which is entirely unsampled. Filling this particular gap will be central to clarifying the evolutionary and adaptive significance of traits for euprimate-like vision and leaping. In light of the complete absence of taxa to fill this gap from the comparatively well-sampled North American record, it seems most plausible that they were living in the Old World. Finally, since understanding the supraordinal relationships of primates is central to reconstructing events at the base of the order, a better fossil record for other euarchontan groups is also central to the problem of primate origins. As it stands, the Paleogene fossil record for scandentians and dermopterans is virtually nonexistent, with the exception of dentognathic remains that already exhibit peculiarities of extant dermopterans (Ducrocq et al. 1992; Marivaux et al. 2006), fragments of scandentian teeth from the Eocene of China (Tong 1988), and plagiomenids, which may be fossil dermopterans (Bloch et al. 2007; but see Yapuncich et al. 2011). Furthermore, a better understanding of various other fossil groups for whom a tie to Euarchonta, or specifically to Primates, has been suggested (e.g., apatemyids, nyctitheriid insectivores, mixodectids; Szalay and Lucas 1996; Hooker 2001; Silcox 2001; Silcox et al. 2005) has the potential to further clarify the evolutionary events downstream from Primates in the euarchontan evolutionary tree (Silcox et al. 2010b). Although this discussion of missing data in the fossil record may seem disheartening, the enormous progress that has been made in the last 15 years in understanding primate origins suggests some of these holes may soon be filled. Researchers interested in this topic have moved from a position analogous to that of early anthropologists arguing about whether brains or bipedalism arose first in human evolution, without having any relevant data to choose between the two, to being able to actually test hypotheses about the order of acquisition of traits in early Page 17 of 27

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primate evolution. It can only be hoped that continuing diligence on the part of researchers interested in primate origins will serve to fill some of these gaps and allow knowledge of the earliest chapters in human evolution to continue to expand.

Cross-References ▶ Phylogenetic Relationships (Biomolecules) ▶ Principles of Taxonomy and Classification: Current Procedures for Naming and Classifying Organisms ▶ The Biology and Evolution of Ape and Monkey Feeding ▶ Zoogeography: Primate and Early Hominin Distribution and Migration Patterns

Acknowledgments Our thanks to JG Fleagle, SGB Chester, PD Gingerich, KD Rose, FS Szalay, and AC Walker for conversations relevant to this chapter. We thank Annette Zitzmann for providing the photo of Ptilocercus in Fig. 11. Research was funded by grants from Wenner Gren, the Paleobiological Fund, Sigma Xi, NSF (SBR-9815884), the University of Winnipeg, and NSERC to MTS; NSF (BCS-0129601) to G.F. Gunnell, P.D. Gingerich, and JIB; NSF (SBR-9616194), Field Museum of Natural History, Sigma Xi, and the Yale University Social Science Faculty Research Fund to EJS; 2002 NSFGRF, NSF DDIG (BCS-0622544), a Leakey Foundation Grant, and NSF (BCS-1317525) to DMB. A portion of this updated manuscript was written when JIB was supported as an Edward P. Bass Distinguished Visiting Environmental Scholar in the Yale Institute for Biospheric Studies (YIBS).

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Sargis EJ (2002a) Functional morphology of the forelimb of tupaiids (Mammalia, Scandentia) and its phylogenetic implications. J Morphol 253:10–42 Sargis EJ (2002b) Functional morphology of the hindlimb of tupaiids (Mammalia, Scandentia) and its phylogenetic implications. J Morphol 254:149–185 Sargis EJ (2002c) A multivariate analysis of the postcranium of tree shrews (Scandentia, Tupaiidae) and its taxonomic implications. Mammalia 66:579–598 Sargis EJ (2002d) The postcranial morphology of Ptilocercus lowii (Scandentia, Tupaiidae): an analysis of primatomorphan and volitantian characters. J Mamm Evol 9:137–160 Sargis EJ (2002e) Primate origins nailed. Science 298:1564–1565 Sargis EJ (2004) New views on tree shrews: the role of tupaiids in primate supraordinal relationships. Evol Anthropol 13:56–66 Sargis EJ (2007) The postcranial morphology of Ptilocercus lowii (Scandentia, Tupaiidae) and its implications for primate supraordinal relationships. In: Ravosa MJ, Dagosto M (eds) Primate origins: adaptations and evolution. Springer, New York, pp 51–82 Sargis EJ, Boyer DM, Bloch JI, Silcox MT (2007) Evolution of pedal grasping in Primates. J Hum Evol 53:103–107 Sige´ B, Jaeger J-J, Sudre J, Vianey-Liaud M (1990) Altiatlasius koulchii n. gen et sp., primate omomyide´ du pale´oce`ne supe´rieur du Maroc, et les origines des euprimates. Palaeontographica 212:1–24 Silcox MT (2001) A phylogenetic analysis of Plesiadapiformes and their relationship to Euprimates and other archontans. PhD dissertation, Johns Hopkins School of Medicine, Baltimore Silcox MT (2003) New discoveries on the middle ear anatomy of Ignacius graybullianus (Paromomyidae, Primates) from ultra high resolution X-ray computed tomography. J Hum Evol 44:73–86 Silcox MT (2007) Primate taxonomy, plesiadapiforms, and approaches to primate origins. In: Ravosa MJ, Dagosto M (eds) Primate origins: adaptations and evolution. Springer, New York, pp 143–178 Silcox MT (2008) The Biogeographic origins of Primates and Euprimates: East, West, North, or South of Eden? In: Sargis EJ, Dagosto M (eds) Mammalian Evolutionary Morphology: a tribute to Frederick S. Szalay. Springer, Dordrecht, pp 199–231 Silcox MT, Gunnell GF (2008) Plesiadapiformes. In: Janis CM, Gunnell GF, Uhen MD (eds) Evolution of Tertiary mammals of North America vol 2: marine mammals and smaller terrestrial mammals. Cambridge University Press, Cambridge, pp 207–238 Silcox MT, Bloch JI, Sargis EJ, Boyer DM (2005) Euarchonta (Dermoptera, Scandentia, Primates). In: Rose KD, Archibald JD (eds) The rise of placental mammals: origins and relationships of the major extant clades. Johns Hopkins University Press, Baltimore Silcox MT, Bloch JI, Boyer DM, Godinot M, Ryan TM, Spoor F, Walker A (2009a) Semicircular canal system in early primates. J Hum Evol 56:315–327 Silcox MT, Dalmyn CK, Bloch JI (2009b) Virtual endocast of Ignacius graybullianus (Paromomyidae, Primates) and brain evolution in early Primates. Proc Natl Acad Sci USA 106:10987–10992 Silcox MT, Benham AE, Bloch JI (2010a) Endocasts of Microsyops (Microsyopidae, Primates) and the evolution of the brain in primitive primates. J Hum Evol 58:505–521 Silcox MT, Bloch JI, Boyer DM, Houde P (2010b) Cranial anatomy of Paleocene and Eocene Labidolemur kayi (Mammalia: Apatotheria) and the relationships of the Apatemyidae to other mammals. Zool J Linn Soc 160:773–825 Page 24 of 27

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Silcox MT, Dalmyn CK, Hrenchuk A, Bloch JI, Boyer DM, Houde P (2011) Endocranial morphology of Labidolemur kayi (Apatemyidae, Apatotheria) and its relevance to the study of brain evolution in Euarchontoglires. J Vertebr Paleontol 31:1314–1325 Smith T, Van Itterbeeck J, Missiaen P (2004) Oldest Plesiadapiform (Mammalia, Proprimates) from Asia and its palaeobiogeographical implications for faunal interchange with North America. C R Palevol 3:43–52 Springer MS, de Jong WW (2001) Which mammalian supertree to bark up? Science 291:1709–1711 Springer MS, Murphy WJ, Eizirik E, O’Brien SJ (2003) Placental mammal diversification and the Cretaceous-Tertiary boundary. Proc Natl Acad Sci U S A 100:1056–1061 Springer MS, Stanhope MJ, Madsen O, de Jong WW (2004) Molecules consolidate the placental mammal tree. Trends Ecol Evol 19:430–438 Springer MS, Meredith RW, Gatesy J, Emerling CA, Park J, Rabosky DL, Stadler T, Steiner C, Ryder OA, Janecˆka JE, Fisher CA, Murphy WJ (2012) Macroevolutionary dynamics and historical biogeography of primate diversification inferred from a species supermatrix. PLoSOne 7:e49521 Stafford BJ, Thorington RW Jr (1998) Carpal development and morphology in archontan mammals. J Morphol 235:135–155 Storch G, Richter G (1994) Zur Pala¨obiologie Messeler Igel. Natur u Museum 124:81–90 Sussman RW (1991) Primate origins and the evolution of angiosperms. Am J Primatol 23:209–223 Sussman RW, Raven RH (1978) Pollination of flowering plants by lemurs and marsupials: a surviving archaic coevolutionary system. Science 200:731–736 Sussman RW, Rasmussen DT, Raven PH (2013) Rethinking primate origins again. Am J Primatol 75:95–106 Szalay FS (1968) The beginnings of primates. Evolution 22:19–36 Szalay FS (1969) Mixodectidae, Microsyopidae, and the insectivore-primate transition. Bull Am Mus Nat Hist 140:195–330 Szalay FS (1972) Paleobiology of the earliest primates. In: Tuttle RH (ed) The functional and evolutionary biology of primates. Aldine-Atherton, Chicago, pp 3–35 Szalay FS (1975) Where to draw the nonprimate-primate taxonomic boundary. Folia Primatol 23:158–163 Szalay FS (1981) Phylogeny and the problem of adaptive significance: the case of the earliest primates. Folia Primatol 36:157–182 Szalay FS, Dagosto M (1980) Locomotor adaptations as reflected on the humerus of Paleogene Primates. Folia Primatol 34:1–45 Szalay FS, Dagosto M (1988) Evolution of hallucial grasping in primates. J Hum Evol 17:1–33 Szalay FS, Decker RL (1974) Origins, evolution, and function of the tarsus in late Cretaceous Eutheria and Paleocene primates. In: Jenkins FA Jr (ed) Primate locomotion. Academic, New York, pp 223–359 Szalay FS, Delson E (1979) Evolutionary history of the primates. Academic, New York Szalay FS, Drawhorn G (1980) Evolution and diversification of the Archonta in an arboreal milieu. In: Luckett WP (ed) Comparative biology and evolutionary relationships of tree shrews. Plenum, New York, pp 133–169 Szalay FS, Lucas SG (1993) Cranioskeletal morphology of archontans, and diagnoses of Chiroptera, Volitantia, and Archonta. In: MacPhee RDE (ed) Primates and their relatives in phylogenetic perspective. Plenum, New York, pp 187–226

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Szalay FS, Lucas SG (1996) The postcranial morphology of Paleocene Chriacus and Mixodectes and the phylogenetic relationships of archontan mammals. Bull New Mex Mus Nat Hist Sci 7:1–47 Szalay FS, Tattersall I, Decker RL (1975) Phylogenetic relationships of Plesiadapis: postcranial evidence. In: Szalay FS (ed) Approaches to primate paleobiology. Karger, Basel, pp 136–166 Szalay FS, Rosenberger AL, Dagosto M (1987) Diagnosis and differentiation of the order Primates. Yearb Phys Anthropol 30:75–105 Tabuce R, Mahboubi M, Tafforeau P, Sudre J (2004) Discovery of a highly-specialized plesiadapiform primate in the early-middle Eocene of Northwestern Africa. J Hum Evol 47:305–321 Tabuce R, Marivaux L, Lebrun R, Adaci M, Bensalah M, Fabre PH, Fara E, Gomes Rodrigues H, Hautier L, Jaeger JJ, Lazzari V, Mebrouk F, Peigne´ S, Sudre J, Tafforeau P, Valentin X, Mahboubi M (2009) Anthropoid versus Strepsirhine status of the African Eocene primates Algeripithecus and Azibius: craniodental evidence. Proc Biol Sci 276:4087–4094 Tong Y (1988) Fossil tree shrews from the Eocene Hetaoyuan formation of Xichuan, Henan. Vertebr Pal Asiat 26:214–220 Van Valen LM (1994) The origin of the plesiadapid primates and the nature of Purgatorius. Evol Monogr 15:1–79 Van Valen LM, Sloan RE (1965) The earliest primates. Science 150:743–745 Waddell PJ, Okada N, Hasegawa M (1999) Towards resolving the interordinal relationships of placental mammals. Syst Biol 48:1–5 Wible JR (1993) Cranial circulation and relationships of the Colugo Cynocephalus (Dermoptera, Mammalia). Am Mus Novit 3072:1–27 Wible JR, Covert HH (1987) Primates: cladistic diagnosis and relationships. J Hum Evol 16:1–22 Wible JR, Martin JR (1993) Ontogeny of the tympanic floor and roof in archontans. In: MacPhee RDE (ed) Primates and their relatives in phylogenetic perspective. Plenum, New York, pp 111–146 Yapuncich G, Boyer D, Secord R, Bloch JI (2011) The first dentally associated skeleton of Plagiomenidae (Mammalia,? Dermoptera) from the Late Paleocene of Wyoming. J Vertebr Paleontol 31(Suppl 2):218, Program and Abstracts

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_29-5 # Springer-Verlag Berlin Heidelberg 2013

Index Terms: Altiatlasius koulchii 16 Angiosperms 3 Dermoptera 7, 17 Eocene 14 Euprimates 2–3, 5, 9–11, 13, 15 Grasp-leaping 2–4, 10 Paleocene 3, 16 Phylogenetic taxonomy 16 Plesiadapiforms 7–8, 13, 15 Plesiadapoidea 17 Primates 1 Ptilocercus 6, 12 Purgatorius 15–16 Scandentia 7, 17 Visual predation 3, 11

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

Fossil Record of Miocene Hominoids David R. Begun* Department of Anthropology, University of Toronto, Toronto, ON, Canada

Abstract Hominoids, or taxa identified as hominoids, are known from much of Africa, Asia, and Europe since the Late Oligocene. The earliest such taxa, from Africa, resemble extant hominoids but share with them mainly primitive characters. Middle and Late Miocene taxa are clearly hominoids, and by the end of the Middle Miocene, most can be attributed to either the pongine (Pongo) or hominine (African ape and human) clade. Interestingly, there is no definitive fossil record of the hylobatid clade (gibbons and siamangs), though there have been some proposed candidates. Miocene hominoids experienced a series of dispersals among Africa, Europe, and Asia that mirror those experienced by many other contemporaneous land mammals. These intercontinental movements were made possible by the appearance of land bridges, changes in regional and global climatic conditions, and evolutionary innovations. Most of the attributes that define the hominids evolved in the expansive subtropical zone that was much of Eurasia. Hominines and pongines diverge from each other in Eurasia, and the final Miocene dispersal brings the hominine clade to Africa and the pongine clade to Southeast Asia. Having moved south with the retreating subtropics, hominines and pongines finally diverge in situ into their individual extant lineages.

Introduction Nonhuman fossil hominoids represent a highly diverse and successful radiation of catarrhine primates known from many localities ranging geographically from Namibia in the south, Germany in the north, Spain in the west, and Thailand in the east, and temporally from Oligocene deposits in Kenya to the Pleistocene of China (Fig. 1). More than 50 genera of nonhuman hominoids are known (Table 1), probably a small percentage of the total number that have existed. Given the focus of these volumes on ape and especially human evolution, this survey of the fossil record of Miocene hominoids will concentrate on taxa that most or all researchers agree are hominoid and in particular on taxa that are most informative on the pattern and biogeography of modern hominoid origins.

What Is a Hominoid? Most of the fossil taxa attributed to the Hominoidea or the Hominidea (new rank, Table 2) in this chapter are known to share derived characters with living hominoids. Because the two living families of the Hominoidea, Hylobatidae and Hominidae, share characters that are either absent or

*Email: [email protected] Page 1 of 66

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

Fig. 1 Map showing the location of the Miocene taxa discussed in this chapter. Namibia (southern Africa), from which Otavipithecus was recovered, is not shown

ambiguous in their development in Proconsul and other Early Miocene taxa, a new rank is proposed here to express the monophyly of the Hominoidea and the monophyly of catarrhines more closely related to extant hominoids than to any other catarrhine. The magnafamily Hominidea (a rank proposed in a work on perissodactyl evolution; Schoch 1986) unites Proconsuloidea with Hominoidea to the exclusion of other catarrhines. This differs from Harrison’s use of the term proconsuloid that he sees as referring to the sister taxon to cercopithecoids and hominoids (Harrison 2002). A few taxa are included in this review if they are too poorly known to preserve unambiguous hominoid synapomorphies but closely resemble other better-known fossil hominoids. In general, fossil and living hominoids retain a primitive catarrhine dental morphology. This makes it difficult to assign many fossil taxa to the Hominoidea since a large number are known only from teeth and small portions of jaws. Dentally, the most primitive Hominidea differ only subtly from extinct primitive catarrhines (propliopithecoids and pliopithecoids) (Fig. 2, node 1). Propliopithecoids (Propliopithecus, Aegyptopithecus) are usually smaller and have much more strongly developed molar cingula, higher cusped premolars, and smaller incisors and canines (Begun et al. 1997; Rasmussen 2002; see “▶ Potential Hominoid Ancestors for Hominidae”). Pliopithecoids (Pliopithecus, Anapithecus) are also generally smaller and have molars with more strongly expressed cingula, more mesial protoconids, and relatively small anterior teeth (Begun 2002).

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

Table 1 Genera of fossil ape or apelike taxaa Important localities Harrat Al Ujayfa Rukwa Rift Lothidok Meswa Bridge

Country Saudi Arabia Tanzania Kenya Kenya

Materialb Facial cranium Mandibular fragment Craniodental fragments Craniodental fragments

Moroto

Uganda

Moroto

Uganda

Cranial, dental, postcrania Dental

Napak/Songhor

K/U

Xenopithecusc Proconsul

Koru Songhor/Koru

Kenya Kenya

Limnopithecusc Rangwapithecusc Micropithecusc Kalepithecusc Dendropithecusc

Koru/Songhor Songhor Napak/Koru Songhor/Koru Rusinga/Songhor/Napak/Koru

Kenya Kenya K/U Kenya K/U

Napak Rusinga/Mfangano

Uganda Kenya

1 2 3 4

Age Oligo. Oligo. Oligo. eM

Ma 28–29 25.2 25 21

Genera Saadanius Rukwapithecus Kamoyapithecusc “Proconsul meswae”d Morotopithecus

5

eM

6

eM

7

eM

? 20–17.5 ? Kogolepithecusc 20–17.5 19 Ugandapithecusd

8 9

eM eM

19 19

10 11 12 13 14

eM eM eM eM eM

19 19 19 19 18–19

15 e M 16 e M

19 Lomorupithecus 19.5–17 cf. Proconsule

17 e M

17.5

Turkanapithecus

Kalodirr

Kenya

18 e M

17.5

Afropithecus

Kalodirr

Kenya

19 e-m M 20 e-m M 21 e M 22 e M 23 e M

17.5–15 Simiolus

Kalodirr/Maboko

Kenya

17.5–15 Nyanzapithecus

Rusinga/Maboko

Kenya

17 16.5 16

Heliopithecus Ad Dabtiyah cf. Griphopithecus Engelswies Griphopithecus Pas¸alar/C ¸ andır

S. Arabia Germany Turkey

24 m M

15

Equatorius

Maboko/Kipsarimon

Kenya

25 m M 26 m M 27 m M

15 15 13

Mabokopithecus Nacholapithecus Kenyapithecus

Maboko Nachola Fort Ternan

Kenya Kenya Kenya

28 29 30 31 32

13 12.5 12.5 12.5 12.5–7

Otavipithecus Pierolapithecus Dryopithecus Anoiapithecus Sivapithecus

Otavi Els Hostalets de Pierola St. Gaudens, La Grive Els Hostalets de Pierola Potwar Plateau

Namibia Spain France Spain Pakistan

mM mM mM mM m-l M

Cranial, dental, postcrania Craniodental fragments Cranial, dental, postcrania Craniodental Craniodental Craniodental Craniodental fragments Cranial, dental, postcrania Craniodental fragments (Cranial, dental, postcrania)+ Cranial, dental, postcrania Cranial, dental, postcrania Cranial, dental, postcrania Craniodental fragments Dental Dental Cranial (dental)+, postcrania (Cranial, dental, postcrania)+ Dental Partial skeleton Cranial, dental, postcrania Craniodental, vertebra Partial skeleton Mandibles+teeth Craniodental (Cranial, dental, postcrania)+ (continued) Page 3 of 66

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

Fossil Record of Miocene Hominoids, Table 1 (continued) Age Ma Genera 33 m-l M ?13.5–7 Khoratpithecusf 34 l M

10

Rudapithecus

Important localities Magaway (M), Khorat)/Ban Sa (Th.) Rudaba´nya

35 l M

10–9

Hispanopithecus

Can Llobateres/Can Ponsic

Spain

36 l M 37 l M

11–8? 10

Neopithecusg Ankarapithecus

Salmendingen Sinap

Germany Turkey

38 39 40 41

9.5 10.25 9.85 9.5

Samburupithecus Chororapithecus Nakalipithecus Ouranopithecus

Samburu Chorora Fm Nakali Ravin de la Pluie

Kenya Ethiopia Kenya Greece

42 l M 43 l M

9–8 9–8

Graecopithecus Lufengpithecus

Pygros Lufeng

Greece China

44 l M 45 l M

8–7 7

New taxon Oreopithecus

C¸orakyerler Baccinello/Monte Bamboli

Turkey Italy

46 47 48 49 50

7–6 6.5 6 5.8–5.2 1–0.3

Sahelanthropus Indopithecus Orrorin “Ardipithecus”h Gigantopithecus

Toros-Menalla Potwar Plateau Lukeino Alayla (Middle Awash) Liucheng

Chad Pakistan Kenya Ethiopia East Asia

lM lM lM lM

lM lM lM lM Pl.

Country Thailand/ Myanmar Hungary

Materialb Craniodental fragments (Cranial, dental, postcrania)+ (Cranial, dental, postcrania)+ m3 Cranial, dental, postcrania Craniodental fragments Isolated teeth Mandible and teeth (Craniodental)+, 2 phalanges Mandible (Cranial, dental)+, postcrania Mandible, maxilla (Cranial, dental, postcrania)+ Craniodental Mandible Craniodental, postcrania Craniodental, postcrania Mandibles, teeth

Oligo. Oligocene, e M Early Miocene, e-m M early Middle Miocene, m M Middle Miocene, m-l M Middle-Late Miocene, l M Late Miocene, K/U Kenya and Uganda, Pl. Pleistocene, M Myanmar (Burma), Th. Thailand a These 50 genera include taxa from the Oligocene and Early Miocene that share mainly primitive characters with the Hominoidea but that appear to be derived relative to pliopithecoids and propliopithecoids. Please see text for further discussion b Material briefly described by part representation. Dental¼mainly isolated teeth; Dental, mandible, maxilla¼known only from these parts; Craniodental fragments¼teeth and few cranial fragments; Craniodental¼larger samples of more informative cranial material; Cranial, dental, postcrania¼good samples from each region; ( )+¼very good representation of parts in parentheses c Unclear attribution to Hominoidea d Large taxon possibly distinct from Proconsul e Proconsul from the Rusinga and Mfangano localities in Kenya is likely to be distinct at the genus level from the Proconsul type material f Middle Miocene samples attributed to this taxon are more fragmentary and may not be congeneric g The Neopithecus brancoi type is an isolated M3 that some attribute to the Pliopithecoidea while other to Dryopithecus (Begun and Kordos 1993). I regard this as a nomen dubium h “Ardipithecus kadabba.” The type of the genus, Ardipithecus ramidus, is younger and shares derived characters with australopithecines not present in A. kadabba, making Ardipithecus in my opinion paraphyletic

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

Table 2 A taxonomy of the Hominidea Cercopithecidea (Magnafamily, new rank) Hominidea (Magnafamily, new rank) Proconsuloidae Proconsul cf. Proconsul Samburupithecus Micropithecus Hominoidea Hylobatidae Hylobates Hominidae Dryopithecusa Hispanopithecus Rudapithecus Ouranopithecus Graecopithecus Sivapithecus Lufengpithecus Khoratpithecus Ankarapithecus Gigantopithecus Indopithecus Chororapithecus Nakalipithecus Sahelanthropus Orrorin Homo Ardipithecusb Praeanthropus Australopithecus Paraustralopithecus Paranthropus Pongo Pan Gorilla a

Crown hominoids of uncertain status Kenyapithecus Oreopithecus Family incertae sedis Afropithecus Morotopithecus Heliopithecus Griphopithecus Equatorius Nacholapithecus Otavipithecus

Superfamily incertae sedis Rangwapithecus Nyanzapithecus Mabokopithecus Turkanapithecus Magnafamily incertae sedis Kamoyapithecus

Dendropithecus Simiolus Limnopithecus Kalepithecus

Includes Pierolapithecus and Anoiapithecus Includes two genera

b

However, the differences between Late Miocene hominids and Late Miocene pliopithecoids are more marked than between Early Miocene Hominidea and pliopithecoids, making defining features less than clear-cut. Cranially Hominidea have a completely ossified tubular ectotympanic, which distinguishes them from both propliopithecoids and pliopithecoids but not from cercopithecoids. Saadanius shares a completely ossified tubular ectotympanic with crown catarrhines (Hominidea and Cercopithecidea). This has led some researchers to conclude that Saadanius represents the common ancestor of crown catarrhines and that its age (28–29 Ma) must be the oldest

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

Fig. 2 Cladogram depicting the relations among most Miocene Hominidea discussed in this chapter. The cladogram is resolved only at the level of the family in many cases, except within the Hominidae, where most clades are resolved. Numbered nodes refer to characters or suites of characters that serve to define clades. They are not intended as comprehensive lists of synapomorphies. For clarity, Hispanopithecus and Rudapithecus, together a sister clade to Dryopithecus, are not shown. Node 1: reduced cingula, delayed life history (M1 emergence), incipient separation of the trochlea and capitulum, increased hip and wrist mobility, powerful grasping, coccyx (no tail). Node 2: thick enamel, increased premaxillary robusticity, further reduction in cingula, increase in P4 talonid height, possible increases in forelimb-dominated positional behaviors. Node 3: further “hominoidization” of the elbow. The position of Kenyapithecus is extremely unclear. Without this taxon, node 3 features the numerous characters of the hominoid trunk and limbs related to suspensory positional behavior. Node 4: Hominidae (see text). Node 5: Homininae (see text). Lack of resolution of the hominini reflects continuing debate on relations among Pliocene taxa that is beyond the scope of this chapter. Pierolapithecus may be a stem hominid or stem hominine, as depicted here. Node 6: Ponginae (see text). Gigantopithecus is probably a pongine but the relations to other pongines are unclear

possible age of divergence of the Old World Monkeys and apes (Zalmout et al. 2010). This conclusion, however, does not follow from the evidence. While Saadanius may preserve characters

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

that approximate or even duplicate those of the last common ancestor of Old World Monkeys and apes, its geological age is irrelevant to the question of the age of divergence of these two lineages Pozzi et al. 2011. We have no idea how long Saadanius or its relatives lived before the 28–29 Ma specimens that were discovered. The taxon could be millions of years older, and in fact, we have this very problem with the pliopithecoids. Most if not all pliopithecoids are known from Eurasia, and they range in age between about 18 and 9 Ma, but they lack synapomorphies of the crown catarrhini. Using the same logic applied to the interpretation of Saadanius, the age of the pliopithecoids would indicate a divergence date of not more than 18 Ma for Old World Monkeys and apes, or even 9 Ma, if the last appearance of the Pliopithecoidea is taken as the divergence date. Clearly this lineage is millions of years older than the age of the oldest fossils we have of the group, and these oldest specimens remain to be discovered. Pliopithecoids represent what we call a ghost lineage, with a huge gap between their origin and first appearance in the fossil record. The same can be said of gibbons or for that matter, African apes. While we have convincing evidence of the Pongo clade at 12 Ma or so and the human lineage at 7 Ma or so, there is no evidence of Pan or Gorilla at all, with the possible exception of teeth attributed to Pan from a 500 Ka site in Kenya (McBrearty et al. 2005), many millions of years after their divergence from humans. The same is very probably true of Saadanius. When coupled with the convincing genetic data suggesting a divergence date of at least 30 Ma (Disotell et al. 2011), the claims of a more recent divergence based on Saadanius do not hold up. Unfortunately, few Miocene Hominidea fossils preserve the portion of the temporal bone that includes the ectotympanic, so in many cases, we simply do not know if this key crown catarrhine synapomorphy was present or not. In addition, hylobatids, cranially the most primitive extant hominoid, share many features found in short-faced Old and New World monkeys, again making it difficult to tease out synapomorphies. Hominoids show a tendency to expand the length and superoinferior thickness or robusticity of the premaxilla, with increasing overlap with the palatine process of the maxilla over time, but once again this is not present in hylobatids or in early wellpreserved specimens of Proconsul, for example (Begun 1994a). Only one specimen of Early Miocene Hominidea is complete enough to say much about the brain, and there are no unambiguous synapomorphies linking it to hominoids. The brain of Proconsul is similar relative to body size to both hylobatids and papionins, the Old World monkeys with the largest brains, and the sulcal pattern, while debatable, lacks most if not all hominoid features (Falk 1983; Begun and Kordos 2004). Like hylobatids, most cercopithecoids, and most mammals other than hominids, a portion of the brain of Proconsul occupied a large the subarcuate fossa of the temporal bone. Cranial and dental evidence also suggests that Proconsul was moderately delayed in terms of life history, another similarity with extant hominoids (Kelley 1997, 2004). Postcranially, Proconsul more clearly represents the ancestral hominoid morphotype, though this too is the subject of debate. Proconsul fossils exhibit hominoid attributes of the elbow, wrist, vertebral column, hip joint, and foot, though in all cases these are subtle and disputed (Beard et al. 1986; Rose 1983, 1988, 1992, 1994, 1997; Ward et al. 1991; Ward 1993, 1997a; Begun et al. 1994; but see Harrison 2002, 1987). Proconsul has a suite of characters consistent with the hypothetical ancestral morphotype of the hominoids, and it should not be surprising that these are poorly developed at first, only to become more defined as hominoids evolve. In comparison with the hominoid outgroup (cercopithecoids), we can expect the earliest hominoids to show subtle indications of increased orthogrady, positional behaviors with increased limb flexibility and enhanced grasping capabilities and no tail, generalized (primitive) dentition, encephalization at the high end of extant cercopithecoids of comparable body mass, and life history variables closer to

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extant hominoids than to extant cercopithecoids(see “▶ Estimation of Basic Life History Data of Fossil Hominoids”). Proconsul has all of these attributes. If these are the features that define the Hominidea, which taxa among Miocene fossil catarrhines are not Hominidea? Even the earliest cercopithecoids (victoriapithecids) are easily distinguished from hominoids (Benefit and McCrossin 2002). Pliopithecoids, often grouped with the “apes,” are even more distantly related. They are clearly stem catarrhines lacking synapomorphies of all crown catarrhines including Proconsul and Victoriapithecus (Begun 2002). The most informative among these synapomorphies are the tubular ectotympanic and the entepicondylar groove (often referred to as the absence of an entepicondylar foramen). In the following sections, I will summarize current knowledge of the Miocene Hominidea, focusing on well-known taxa that serve to illustrate important events in hominoid evolutionary history (Fig. 2).

Origins of Hominidea It is likely that hominoids originated in Africa from an ancestor that, if known, would be grouped among the Pliopithecoidea. Pliopithecoids, currently known only from Eurasia, share with all catarrhines the same dental formula and possibly with crown catarrhines a reduction of the midface, subtle features of the molar dentition, and a partial ossification of the ectotympanic tube (Begun 2002). The presence of pliopithecoids in Africa is suggestive but remains to be demonstrated (Andrews 1978; Begun 2002; Rossie and MacLatchy 2006). The oldest and most primitive catarrhine that can lay claim to hominoid status however is African (Table 1). Kamoyapithecus, from the Oligocene of Kenya, differs from other Oligocene catarrhines (propliopithecoids) in being larger and having canines and premolars that more closely resemble Miocene hominoids than Oligo-Miocene non-hominoids (Leakey et al. 1995). Only craniodental material of Kamoyapithecus has been described, and it is so primitive as to make attribution to the Hominoidea difficult. Though it would fail to fall among the Hominoidea in a quantitative cladistic analysis due to its fragmentary preservation and primitive morphology, it makes in my view a good Hominidean precursor. Stevens et al. (2013) report on a new taxon, Rukwapithecus, from 25.2 Ma sediments in Tanzania. The specimen consists of a nicely preserved right mandible of a juvenile individual with the p4 to m2 erupted and the m3 still in its crypt. Unfortunately, and this is frustratingly common, no teeth can be directly compared between Kamoyapithecus and Rukwapithecus, as the latter is known only from lower postcanine teeth, none of which are known for Kamoyapithecus. We cannot rule out the possibility that Rukwapithecus is a junior subjective synonym of Kamoyapithecus and only more fossils will help to resolve this question. On the other hand, Stevens et al. (2013) characterize Rukwapithecus as the oldest known fossil ape and tentatively classify it among the nyanzapithecines, a poorly defined and possibly paraphyletic taxon that includes Rangwapithecus and Nyanzapithecus. These taxa do have some unusual features of the lower dentition, but given the tiny sample size, it is premature in my opinion to consider the “nyanzapithecines” and Rukwapithecus in particular to be more closely related to Middle Miocene and later hominoids than Proconsul, as Stevens et al. (2013) suggest. Koufos (see “▶ Potential Hominoid Ancestors for Hominidae” this volume) covers some of the same fossils as covered here, with some differences in interpretation. Senut (“▶ The Earliest Putative Hominids” this volume) proposes some radically different interpretations of some of the material presented here, in addition to interpretations of the latest Miocene and the Pliocene hominin fossil record that differ from any other published interpretation of which I am aware. Both authors and Schwartz (“▶ Defining Hominidae” this volume) employ the term hominid to mean humans and taxa more Page 8 of 66

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Plate 1 Proconsul from the Tinderet localities of Songhor and Koru. The two P. africanus specimens to the left are male as is the P. major mandible to the right. From left to right, M 14084 (P. africanus type), KNM-SO 1112, M 16648. Not to scale. P. major is much larger

closely related to humans than to any other taxon. The vast majority of researchers employ the term as it is used here, referring to great apes and humans and all fossil taxa more closely related to these crown taxa than to hylobatids.

Proconsuloidea Proconsul The superfamily Proconsuloidea, as defined by Harrison (2002), includes many mainly Early Miocene taxa. As noted, in this chapter, a number of taxa from this group are interpreted to represent primitive Hominidea or hominoids. A hypothetical ancestral morphotype for the Hominidea is given in Fig. 2 (node 1). Node 1 represents the bifurcation of Proconsul from hominoids with more apparent synapomorphies to living hominoids. Proconsul as described here is based mainly on the sample from Rusinga Island and Mfangano, two localities that are close together on Lake Victoria, western Kenya. These sites are often referred to as the Kisingiri Proconsul localities, as opposed to the Tinderet localities of Songhor, Koru, Legetet, and Chamtwara, among others. The Kisingiri include the species Proconsul heseloni (Walker et al. 1993) and Proconsul nyanzae (Le Gros Clark and Leakey 1950). The type specimen of Proconsul africanus (Hopwood 1933) is from Koru, and the type of Proconsul major (Le Gros Clark and Leakey 1950) is from Songhor, both of which are Tinderet localities (Drake et al. 1988). Historically the Tinderet localities have been considered to be older than the Kisingiri sites (Drake et al. 1988), but this new evidence indicates that there is some overlap in ages (Table 1) (McNulty personal communication). There is strong evidence that the Kisingiri species of Proconsul that are the basis of the description here actually belong to a different genus from the Tinderet types (see below). However, as this is not the appropriate venue to name a new genus, I will follow convention and refer to the Rusinga sample as Proconsul. In the end, both taxa traditionally attributed to Proconsul are most likely to be sister taxa, so whether it is one genus or two is only of interest to those who are working directly on this material, though when worked out it will give us a much better idea of the actual specimen composition of each taxon, which is the necessary precursor to any analysis of the paleobiology of fossil taxa (Plates 1, 2, and 3).

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Plate 2 “Proconsul” heseloni from Rusinga. KNM-RU 2036 on the left is the type specimen and is female, while the specimen to the right (KNM-RU 2087) is a male

Plate 3 “Proconsul” nyanzae from Rusinga. M16647 on the right is the type specimen and male. KNM-RU 7290 is a female

Postcranial Morphology Proconsul and other proconsuloids are defined by a large number of characters. Proconsul is a generalized arboreal quadruped but is neither monkey-like nor apelike (Rose 1983). The following summary is mainly from Rose (1997), Ward (1997a), and Walker (1997). In addition to the characters noted that emphasized its hominoid affinities, Proconsul has limbs of nearly equal length (though the forelimbs were probably slightly longer than the hindlimbs), with scapula positioned laterally on the thorax and the ovoid and narrow glenoid positioned inferiorly, as in generalized quadrupeds. The thorax is transversely narrow and deep superoinferiorly, and the vertebral column is long and flexible, especially in the lumbar region. The innominate is long with a narrow ilium and an elongated ischium. The sacrum is narrow, and its distal end indicates that it articulated with a coccygeal and not a caudal vertebra, in other words Proconsul had a coccyx and not a tail (Ward et al. 1991). In the details of limb morphology, Proconsul also combines aspects of monkey and ape morphology. Proconsul forelimbs lack the characteristic elongation of ape forelimbs, though this trend in ape evolution may be represented by some slight forelimb elongation in Proconsul. The humeral head is oriented posteriorly relative to the transverse plane, and the humeral shaft is convex anteriorly, both of which are consistent with the position of the glenoid fossa and the shape of the thorax. The distal end of the humerus lacks the enlargement of the capitulum and trochlea and other details of the hominoid elbow, but it does have a narrow zona conoidea and a mild trochlear notch. These are characters that are more strongly developed in extant apes that are universally regarded as indications of suspensory positional behavior. It is interesting that

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Proconsul shows incipient signs of apelike morphology in the elbow while lacking other more definitive indicators of orthogrady or suspension. It is possible that these early, subtle changes in the elbow and in other areas of the postcranium of Proconsul are related to the positional demands of an animal moving around in the trees without a tail (see below). The medial epicondyle is more posteriorly oriented as in monkeys. The proximal ends of the radius and ulna are consistent with the morphology of the distal humerus. The radial head is small and ovoid, the ulnar trochlea is narrow and has a poorly developed keel, and the radial notch is positioned anteriorly. The ulna also has a large olecranon process. All of these features are consistent with generalized pronograde (above branch) quadrupedalism as opposed to antipronograde (suspensory or below branch) (Ward 2007). Distally, the radial carpal surface is flat and articulates mainly with the scaphoid. The ulnar head is comparatively large with a long and prominent styloid process that articulates directly with the pisiform and triquetrum, unlike living hominoids, which have greatly reduced ulnar styloids and no contact with the carpals. However, the nature of the contact between the ulnar styloid and the pisiform and triquetrum differs from that of monkeys and does suggest a greater degree of mobility, or at least a different pattern of mobility, than seen in Old World Monkeys (Beard et al. 1986). The carpals are small transversely. The scaphoid is separate from the os centrale and the midcarpal joint is narrow. The hamate hamulus is small, and the surface for the triquetrum is flat and mainly medially oriented (Beard et al. 1986). However, the manner in which the bones of the wrist come together in Proconsul shares attributes with monkeys and apes, making it unique. Nevertheless, in my view, the Proconsul wrist does provide evidence of an incipient transformation for a more stable pronograde-dominated posture to more diverse habitual postures. The metacarpal surfaces of the distal carpals are small and comparatively simple as are the corresponding surfaces on the metacarpal bases. The metacarpals are short and straight and their heads transversely narrow. The proximal ends of the proximal phalanges are slightly dorsally positioned as in palmigrade quadrupeds. All the phalanges are short and straight compared with apes, though secondary shaft features, in particular of the proximal phalanges, suggest powerful grasping (Begun et al. 1994). The hindlimbs of Proconsul are also dominated by monkey-like characters. The long bones are long and slender. The femoral head is small compared to apes, but its articulation with the acetabulum indicates more mobility compared to most monkeys. The feet of Proconsul are monkey-like in their length-to-breadth ratio (they are narrow compared to great ape feet). Proconsul tarsals are elongated relative to breadth and the metatarsals long compared to the phalanges. Like those of the hands, the foot phalanges of Proconsul are straighter and less curved than in apes but with more strongly developed features related to grasping than in most monkeys. The hallucial phalanges are relatively robust, suggestive of a powerfully grasping big toe. Body mass estimates for the species of Proconsul, based mainly on postcranial evidence, range from about 10 to 50 kg (Ruff et al. 1989; Rafferty et al. 1995). The lower estimate is based in part of juvenile specimens, and it is probable that the smallest adult Proconsul weighed about 15 kg. In addition to morphological evidence, the range of body mass estimates in Proconsul from Rusinga and Mfangano strongly suggest that at least two species are represented. Craniodental Morphology As noted, Proconsul has a moderate amount of encephalization (comparable to hylobatids and papionins), a short face with a fenestrated palate (Fig. 3), a smoothly rounded and somewhat airorhynchous face (Fig. 4), and a generalized dentition. Morphologically, the dentition is consistent with a soft fruit diet, and microwear analysis suggests the same (Kay and Ungar 1997; “▶ Dental Adaptations of African Apes”). The somewhat enlarged brain of Proconsul implies Page 11 of 66

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Fig. 3 Midsagittal cross section of a number of Hominidea palates showing some of the features described in the text. Proconsul has a small premaxilla and a fenestrated palate (large foramen and no overlap between the maxilla and premaxilla). Nacholapithecus has a longer premaxilla with some overlap. It is similar to Afropithecus and conceivably could be the primitive morphotype for the Hominidae. Pongo and Sivapithecus have a similar configuration but with further elongation and extensive overlap between the maxilla and premaxilla, producing a smooth subnasal floor. Hominines have robust premaxillae that are generally shorter and less overlapping than in Sivapithecus and Pongo. Dryopithecus is most similar to Gorilla, which may represent the primitive condition for hominines. Pan and Australopithecus have further elongation and overlap, but the configuration differs from Pongo. This morphology is suggested to be an important synapomorphy of the Pan/Homo clade (Begun 1992b) (Modified from Begun 1994)

Fig. 4 Lateral views of some Hominidea crania showing possible changes through time. A mildly airorynch Proconsul may be a good ancestral morphotype for hominoid craniofacial hafting, as a similar degree of airorhynchy is also found in hylobatids (Shea 1988). Rudapithecus shares with other hominines neurocranial elongation (though this also occurs in hylobatids), the development of supraorbital tori, klinorhynchy, and, probably in association with the latter, a true frontoethmoidal sinus (Modified from Kordos and Begun (2001))

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a degree of life history delay approaching the hominoid pattern (Kelley 1997, 2004; Kelley and Smith 2003; Smith et al. 2003). One aspect of the cranium of Proconsul that has received some attention is the frontal sinus. Walker (1997) interprets the presence of a frontal sinus in Proconsul to indicate its hominid status, citing the presence of large frontal sinuses in some great apes. Other researchers have suggested that the frontal sinus is a primitive character, as it is found in Aegyptopithecus and many New World monkeys (Andrews 1992; Rossie et al. 2002). The confusion stems from the use of one term to describe several different characters. As Cave and Haines (1940) noted long ago, frontal sinuses in primates have various ontogenetic origins, and it is likely that they are not homologous across the primates. New World monkeys have frontal sinuses that are outgrowths from the sphenoid sinus, as is also the case for hylobatids. On the other hand, Pongo, which occasionally has a frontal sinus, derives it from the maxillary sinus (see “▶ Defining Hominidae”). African apes and humans normally have large frontal sinuses derived from the ethmoidal sinuses. “Frontal sinuses” then are actually three different characters, frontosphenoidal sinuses, frontomaxillary sinuses, and frontoethmoidal sinuses. While it is possible to establish the ontogenetic origin of a pneumatized frontal bone in living primates, it is more difficult in fossil primates. However, the placement and size of the frontal sinuses correlate very well with their ontogenetic origin, offering a protocol for identifying the specific type of frontal sinus present in a fossil (Begun 1994a). Frontosphenoidal sinuses invade large portions of the frontal squama but not the supraorbital or interorbital regions. Frontomaxillary sinuses are infrequent in Pongo, but when they occur, they are associated with narrow canals or invaginations connecting the maxillary sinuses to a small pneumatization of the frontal via the interorbital space. In African apes and humans, the frontoethmoidal sinuses arise from a spreading of the ethmoidal air cells in the vicinity of nasion, resulting in large pneumatizations from below nasion into the supraorbital portion of the frontal. The actual amount of frontal pneumatization is variable, while the presence of a large sinus around nasion is constant. Therefore, while we cannot observe the development of frontal pneumatization in fossil primates, and we do not have adequate ontogenetic series to directly reconstruct this growth, we can infer the type of frontal pneumatization from its position, extent, and connection to the source sinus. In Proconsul, as in hylobatids, New World monkeys, and Aegyptopithecus, the frontal pneumatization is extensive and occupies the frontal squama, consistent with a frontosphenoidal sinus. Thus, the “frontal sinus” in Proconsul is a primitive character, as suggested by Andrews (1992), but for different reasons. The frontal pneumatization of Rudapithecus, on the other hand, conforms to the pattern seen exclusively in African apes and humans (see below). In summary, Proconsul was an above branch mid- to large-sized catarrhine with a diet dominated by soft fruits and a somewhat slower life history than cercopithecoids. Encephalization may imply other similarities to hominoid behavioral or social ecology, or it may simply be a consequence of relatively large body mass and/or a slower life history (Kelley 2004; Russon and Begun 2004). The slightly enhanced range of motion in Proconsul limbs may imply some degree of orthogrady, it may be a consequence of the absence of a tail, of large body mass in an arboreal milieu, or, most likely, some combination of all three (Beard et al. 1986; Begun et al. 1994; Kelley 1997).

Other Possible Proconsuloids A number of taxa are regarded by many researchers as having a probable close relationship to Proconsul. The three with the best evidence for affinities to the proconsuloids are Proconsul sensu stricto, Micropithecus, and Samburupithecus. As noted, the type species of the genus Proconsul is Page 13 of 66

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P. africanus. P. africanus and P. major, both from Tinderet sites, are never found together with Proconsul from Rusinga and are also more primitive and lack synapomorphies shared by Proconsul from Rusinga and other hominoids (see below). Other taxa listed in Table 2 are either more likely to be hominoids given similarities to known hominoids (Rangwapithecus, Nyanzapithecus, Mabokopithecus) or they are so primitive or poorly known as to make unclear their magnafamily status. Proconsul Sensu Stricto The species of Proconsul sensu stricto from Songhor and Koru (P. africanus and P. major) probably represent a different genus from P. heseloni and P. nyanzae, the samples on which the descriptions of Proconsul presented here are based. A new genus would replace P. heseloni and P. nyanzae, as P. africanus has priority. Proconsul sensu stricto from Songhor and Koru has elongated postcanine teeth, more strongly developed cingula, upper premolars with strong cusp heteromorphy, and conical, individualized molar cusps, all of which suggest that the older species are in fact more primitive. The two Tinderet species differ from each other mainly in size. Postcrania attributed to Proconsul from the Tinderet Proconsul sensu stricto localities are distinct from postcrania from the younger Proconsul localities such as Rusinga, in details that have been correlated to paleoecological differences (Andrews et al. 1997). While sufficiently similar to the better-known younger Proconsul sample to warrant placing both in the same superfamily, the more modern morphology of the younger Proconsul sample will almost certainly require taxonomic recognition. Ugandapithecus, based on the sample of P. major, adds to the confusion (Senut et al. 2000). Ugandapithecus is not a useful nomen in that it mixes a number of specimens from different localities, different sizes, and even different morphologies, and it has not been effectively compared with and distinguished from either Proconsul sensu stricto or the Kisingiri sample. Therefore, the nomen is not recognized here except as a junior subjective synonym of Proconsul. Nevertheless, it turns out that Proconsul as traditionally defined probably does represent more than one genus. Senut et al. (2000; see “▶ The Earliest Putative Hominids”) have suggested that large-bodied hominoids from Moroto, in Uganda, that is, P. major, may also be attributed to Ugandapithecus (hence the name, though the type is from Kenya), calling into question the interpretation that hominoid cranial and postcranial fossils from Moroto belong to one taxon (Morotopithecus). However, the evidence for more than one large hominoid genus at Moroto is not strong (see below). Micropithecus Micropithecus (Fleagle and Simons 1978) is a small catarrhine with comparatively broad incisors and long postcanine teeth with low cusps and rounded occlusal crests. The cingula are less strongly developed than most other Early Miocene catarrhines. Males and females exhibit marked size dimorphism. Comparisons with living catarrhines suggest a body mass of about 3–5 kg (Harrison 2002). While Harrison (2002, 2010) considers this taxon to be even more distantly related to the Hominoidea than are the Proconsuloidea, the subtly more modern features of the dentition suggest that it may belong to the Proconsuloidea. Fleagle and Simons (1978) in fact attribute Micropithecus to the Hominoidea, although as noted the features shared with hominoids are very subtle. If Micropithecus is a proconsuloid, as preferred here, it would indicate that the proconsluoids were quite diverse in body mass, as is the case in all catarrhine superfamilies.

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Samburupithecus Samburupithecus is another possible proconsuloid, known only from a large maxillary fragment from the Late Miocene of the Samburu region of Kenya (Ishida and Pickford 1997). Ishida and Pickford (1997) have suggested that Samburupithecus is an early member of the African ape and human clade, while others place it within the hominoids, but without specific affinities to any living clade (e.g., Harrison 2010; see “▶ The Earliest Putative Hominids”). However, Samburupithecus retains many primitive characters of the Proconsuloidea. These include a low root of the zygomatic processes, a strongly inclined nasal aperture edge, the retention of molar cingula, and thick enamel with high dentine relief (Begun 2001). Samburupithecus is most likely to be a late surviving proconsuloid. Its unusual dental characters (e.g., large molars with individualized cusps separated by deep narrow fissures) are reminiscent of morphological “extremes” found in terminal lineages with long evolutionary histories. Oreopithecus, Gigantopithecus, Paranthropus, Daubentonia, and Ekgmowechashala all share with Samburupithecus exaggerated occlusal features compared with other members of their respective clades. The size and occlusal morphology of Samburupithecus that superficially resembles Gorilla (Ishida and Pickford 1997) may be related in part to the fact that both are ends of long phylogenetic branches. In a pattern analogous to long branch attraction in molecular systematics, there is a tendency for separate long isolated lineages to converge in certain aspects of their morphology (Begun 2001). For whatever the reason, in its details Samburupithecus is primitive and more likely to belong to the proconsuloids than the hominoids (Plate 4). Nyanzapithecines In contrast to the phylogeny presented in Stevens et al. (2013), I consider Rangwapithecus and Nyanzapithecus to be proconsuloids and not more closely related to more modern apes. Harrison (2010) includes the nyanzapithecines among the proconsuloids, and that is the view adopted here. Nyanzapithecines as defined by Harrison (2002, 2010) include a diverse assemblage of fossil taxa ranging in dental size from somewhat smaller that Proconsul to the size of Proconsul heseloni or P. africanus. Several of these specimens are beautifully preserved, including the holotypes of Rangwapithecus and Turkanapithecus. There is a nicely preserved mandible of Nyanzapithecus as well. Yet, these taxa have proven extremely resistant to classification. I am not convinced that the Nyanzapithecinae as constituted by Harrison (2010) is a natural group. While there are superficial similarities in the occlusal morphology of the molars of all three genera and Mabokopithecus as well, these taxa are mostly distinguished from Proconsul by the complexity of their occlusal surfaces rather than being linked by morphological details. In many cases, these types of molars with more complicated patterns of crests and taller cusps that tend to be more isolated from one another occur in conjunction with selection for a more folivorous diet. This may explain in part some of what I consider to be superficial convergences in the morphology of the teeth of these taxa. In sum, I find the case for a specific relationship between Mabokopithecus and Nyanzapithecus fairly convincing, but I would not include Rangwapithecus or Turkanapithecus in the same subfamily. All of these taxa are most likely to be proconsuloids with more folivorous adaptations than other proconsuloids. As noted earlier, at this point it is premature to link the 25 Ma Rukwapithecus with the much younger sample of Rangwapithecus.

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Plate 4 Comparison between Samburupithecus, KNM-SH 8531 (left) and “Proconsul” (KNM-RU 1677a). Note the strongly developed molar cingula and the small M1 relative to M2 in both specimens. The molars are similar in overall morphology as well

Early Hominoids Afropithecus A number of late Early Miocene and Middle Miocene taxa share characters with extant Hominoids and are included here in the Hominoidea. Afropithecus (Leakey and Leakey 1986) is known from several localities in northern Kenya dated to 17–17.5 Ma (Leakey and Walker 1997). Afropithecus shares an increase in premaxillary robusticity and length with most extant hominoids (Fig. 3). Like many Late Miocene and Pliocene hominids, Afropithecus has very thick occlusal enamel as well (Smith et al. 2003). On the other hand, similarities have been noted between Afropithecus cranial morphology, particularly the morphology of the midface, and that of Aegyptopithecus. Leakey and Walker (1997) have suggested that the unusual primitive-looking face of Afropithecus may be related to a specialized scerocarp seed predator adaptation. This is functionally consistent with the robust, prognathic premaxilla; large, relatively horizontal incisors; large but relatively low-crowned canines; expanded premolars; thick enamel; and powerful chewing muscles of Afropithecus. A similar set of features is found in modern primate seed predators such as pithecines. It may be that some of the primitive appearance of the Afropithecus face is homoplastic with Aegyptopithecus. However, another possibility is that the unusual morphology of the face of the single specimen of Afropithecus on which this morphological characterization is based is the result of postmortem deformation. My observations of the original specimen and other more fragmentary specimens of Afropithecus lead me to conclude that the type is deformed and probably resembled Proconsul more closely than Aegyptopithecus. Nevertheless, the characters noted above related to the development of the premaxilla, the implantation of the incisors, and the implantation and morphology of the canines are real differences from Proconsul. Thus, as with Proconsul, Afropithecus has a mosaic of primitive and derived characters (Leakey et al. 1991; Leakey and Walker 1997; Plate 5). The large, albeit deformed, type specimen of Afropithecus reveals some information on neurocranial morphology. KNM-WK 16999 preserves a portion of the braincase immediately

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Plate 5 The type specimen of Afropithecus, KNM-WK 16999 (left) and a well preserved mandible, KNM-WK 17012 (right). Note the lack of bone surfae around the nasal aperture and incisors and the exceptionally large interorbital area, indicative of deformation

behind the orbits. Postorbital constriction is very marked, though I believe this is the result in part of postmortem deformation. However, there is no doubt that the anterior temporal lines are very strongly developed. These converge to form a pronounced and very anteriorly situated sagittal crest. The small portion of the anterior cranial fossa preserved indicates a cerebrum that was constricted rostrally, lacking the frontal lobe expansion typical of extant and fossil great apes. The increased robusticity of the masticatory apparatus of Afropithecus in comparison with Proconsul is undeniable, despite some caveats related to preservational issues. The large mandibles, robust zygomatics, thickly enameled teeth, and powerfully developed attachment sites for chewing muscles all indicate that the dietary adaptations of Afropithecus differed significantly from those of Proconsul, and more closely approach those of some later Miocene apes. These differences from Proconsul are confirmed by more recently described specimens (Rossie and MacLatchy 2013). Afropithecus is similar in size to Proconsul nyanzae, based on cranial, dental, and postcranial dimensions (Leakey and Walker 1997). Afropithecus postcrania are very similar to those of Proconsul, so much so that Rose (1993) found them essentially indistinguishable. However, Afropithecus postcrania are much less well known than Proconsul, and it is conceivable that as more fossils of Afropithecus are discovered, some differences from Proconsul will emerge. Nevertheless, given our current state of knowledge, the postcranial adaptation of Afropithecus, in terms of body mass and positional behavior, is Proconsul-like, while the craniodental anatomy is markedly distinct. Another early hominoid taxon, Heliopithecus, is contemporaneous with Afropithecus and morphologically very similar, though it is only known from a fragmentary hemimaxilla and a few isolated teeth (Andrews and Martin 1987). Both Heliopithecus and Afropithecus share characters that are found next in the fossil record in Eurasia, which suggests that Heliopithecus and Afropithecus taxa may have a closer relationship to late Early Miocene and Middle Miocene hominoids from Europe than do proconsuloids. Certainly the most important piece of the puzzle of ape evolution to be provided by Heliopithecus is its geography. Heliopithecus is from the site of Ad Dabtiyah, in Saudi Arabia. While that sounds extraordinary, it is useful to recall that geologically the Saudi Arabian peninsula is part of the African plate, and until fairly recently much of the fauna of Africa was present in the Arabian peninsula as well. During the Early Miocene, the Arabian peninsula was much more humid than today and supported large and diverse forest communities. Given my interpretation that Afropithecus-like adaptations may have permitted hominoids to

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

disperse into Eurasia in the late Early Miocene (see below), the presence of a very similar taxon on the road to Eurasia from East Africa is certainly telling.

Morotopithecus Morotopithecus is a fossil hominoid from Uganda dated to about 21 Ma by some and 17 Ma by others (Gebo et al. 1997; Pickford et al. 2003). It is best known from a large cranial specimen including most of the palate (Pilbeam 1969). For many years, this specimen was attributed to Proconsul major, but it is clear that it and other specimens from Moroto are sufficiently different to justify a genus distinct from Proconsul. Morotopithecus is similar in size to Proconsul major and larger than Proconsul nyanzae and Afropithecus. It lacks the distinctive subnasal morphology of Afropithecus and has a Proconsul-like premaxilla that is short, gracile, and does not overlap the palatine process of the maxilla, resulting in a large incisive fenestration (Fig. 3). Morotopithecus has a broad palate; large anterior teeth, especially the canines, which are tusklike; a piriform aperture broadest about midway up; and an interorbital space that appears to be relatively narrow, though it is damaged. However, the most important distinction of Morotopithecus is the morphology of the postcrania, which are said to be modern hominoid-like. Newly described specimens of Morotopithecus include the shoulder joint, hip joint, and details of the vertebral column (MacLatchy 2004). Walker and Rose (1968) described the vertebrae as hominoid-like, which has been confirmed by more recent discoveries and analyses. The glenoid fossa of Morotopithecus suggests a more mobile shoulder joint as does the morphology of the hip joint. However, it is the hominoid-like position of the transverse processes of the vertebrae that represents the strongest evidence for the hominid affinities of Morotopithecus. The roots of the transverse processes of the lumbar vertebrae of Morotopithecus are positioned posteriorly, as in extant great apes, suggesting a stiff lower back and an axial skeleton like that of extant hominoids. However, this interpretation has not gone unchallenged, and for the time being, I consider the degree to which Morotopithecus was orthograde to be unresolved (Nakatsukasa 2008).

Eurasian Hominoid Origins As noted, Heliopithecus and Afropithecus have more robust jaws and teeth than Early Miocene proconsuloids, and this may represent a key adaptation that permitted the expansion of hominoids into Eurasia at about 17 Ma, when during a marine low stand, a diversity of terrestrial mammals moved between Africa and Eurasia (Made 1999; Begun 2001, 2009; Begun et al. 2003a, b, 2012; Nargolwalla 2009). Toward the end of the Early Miocene, the movement of the southern landmasses northward, combined with a number of other developments (the Alpine and Himalayan orogenies, the earliest appearance of the polar ice caps, and the Asian monsoons), leads to a sequence of connections and barriers to terrestrial faunal exchange (Ro¨gl 1999a, b; Adams et al. 1999; MacLeod 1999; Hoorn et al. 2000; Zhisheng et al. 2001; Guo et al. 2002; Liu and Yin 2002; Wilson et al. 2002; Nargolwalla 2009). This period of global turbulence affected sea levels between continents cyclically such that for the remainder of the Miocene, there would be periodic connections (low stands) and disconnections (high stands) between the continents. At about 17 Ma, a low stand that had permitted the exchange of terrestrial faunas between Eurasia and Africa (the Proboscidean datum) was coming to an end but not before hominoids possibly resembling Afropithecus and Heliopithecus had dispersed from Africa into Eurasia (Heizmann and Begun 2001; Begun 2002, 2004; Begun et al. 2003a, b, 2012). At the end of the Early Miocene, about 16.5 Ma, hominoids of more modern dental aspect first appear in Eurasia. The oldest Eurasian hominoid is cf. Griphopithecus, known from a molar fragment from Germany (Heizmann and Begun 2001). Griphopithecus (Abel 1902) is known Page 18 of 66

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

mainly from large samples from Turkey of roughly the same age, while the type material is known from a probably later (14–15 Ma) locality, Deˇvı´nska´ Nova´ Ves, in Slovakia (Heizmann 1992; Andrews et al. 1996; Heizmann and Begun 2001; Begun et al. 2003a, b). cf. Griphopithecus from Engelswies in Germany is a tooth fragment that has the more modern features of being thickly enameled with low dentine penetrance (tall dentine horns did not project into the thick enamel cap as in Proconsul and probably Afropithecus). cf. is the designation for a taxon that is similar enough to another taxon for there to be a strong likelihood that they are the same, but with some formally acknowledged uncertainty. Griphopithecus is better known from over 1,000 specimens, mostly isolated teeth, from two localities in Turkey (C¸andır and Pas¸alar). One species, Griphopithecus alpani (Tekkaya 1974), is known from both localities, while a second somewhat more derived taxon is also found at Pas¸alar (Alpagut et al. 1990; Martin and Andrews 1993; Kelley and Alpagut 1999; Ward et al. 1999; Kelley et al. 2000; Kelley 2002; Gu¨lec¸ and Begun 2003).1 Griphopithecus alpani has a robust mandible with strongly reinforced symphysis; broad, flat molars with thick enamel; and reduced cingulum development compared with Proconsul. It retains primitive tooth proportions (small M1 relative to M2), anterior tooth morphology, and postcanine occlusal outline shape. A few fragments of the maxilla from Pas¸alar indicate a primitive morphology for the anterior palate (Martin and Andrews 1993). The morphology of Griphopithecus molars as well as their microwear indicates a diet allowing the exploitation of hard or tough fruits, though it is not clear if this means simply that they could exploit these resources when needed (a keystone resource) or if they were a favored source of food. Two postcranial specimens, a humeral shaft and most of an ulna, from the younger site of Klein-Hadersdorf, Austria, are also similar to Proconsul and indicate that Griphopithecus was a large-bodied above-branch arboreal quadruped similar in size and positional behavior to Proconsul nyanzae (Begun 1992a). Phalanges from Pas¸alar are also said to be most similar to those of Proconsul and extant arboreal quadrupeds (Ersoy et al. 2008) (Plates 6 and 7).

East African Middle Miocene Thick-Enameled Hominoids Shortly after the appearance of Griphopithecus in western Eurasia (but see footnote 1), dispersals between Eurasia and Africa were interrupted by the Langhian transgression (Ro¨gl 1999a). Following the Langhian, at about 15 Ma, dispersals resumed in a number of mammal lineages, probably also including hominoids (Begun et al. 2003a, b; Begun (2009); Nargolwalla 2009; Begun et al. 2012). Hominoids closely similar to Griphopithecus in dental morphology appear in Kenya at this time. Equatorius is known from 15 Ma localities in the Tugen Hills and at Maboko, both in Kenya. This taxon, previously attributed to Kenyapithecus, is very similar to Griphopithecus but has a distinctive incisor morphology and reduced cingula, probably warranting a distinct genus status (Ward et al. 1999; Kelley et al. 2000; Ward and Duren 2002; contra Begun 2000, 2002; Benefit and McCrossin 2000). Equatorius is also known from a good sample of 1

Some researchers have suggested that the specimen from Engelsweis, which we all agree is at least 16.5 Ma, if not more than 17 Ma, is more likely to be an Afropithecus or a relative thereof, with no relationship to Griphopithecus (Casanovas-Vilar et al. 2011). These researchers are in agreement with Bo¨hme et al. (2011) that Griphopithecus in Anatolia is later in time (ca. 13.5 Ma). My analysis of the biostratigraphy of the C ¸ andır locality indicates that it is likely to be at least 16 Ma (Begun et al. 2003a). Until more research is concluded, there will remain uncertainty about the ages of the C ¸ andır and Pas¸alar localities, though at 13.5 Myr this makes them much younger than previously thought. However, even if the Anatolian Griphopithecus sites are 3 Myr younger than Engelsweis, that is no justification for the claim that the latter must have been the result of a separate dispersal event as opposed to the simpler scenario in which hominoids with thickly enameled teeth enter Europe at 17 Ma and evolve in situ. As noted earlier, the tooth from Engelsweis more closely resembles those from Anatolia and Slovakia than it resembles Afropithecus. Page 19 of 66

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

Plate 6 Top row, Nacholapithecus palate. Left, lateral view, right, palatal view. Bottom row, Nacholapithecus mandible (left), Equatorius mandible (right). The Nacholapithecus specimens belong to the partial skeleton KNM-BG 35250, and the Equatorius mandible to the partial skeleton KNM-TH 28860

Plate 7 Kenyapithecus and Griphopithecus. Top row, Kenyapithecus wickeri (type specimen, KNM-FT 46), lateral (left) and occlusal (center) views. Equatorius (type specimen, M16649) occlusal (right). Bottom row, Griphopithecus alpani type mandible (MTA 2253) (left) and three upper central incisors, from left to right, “Proconsul” (KNM-RU 1681), Equatorius (KNM-MB 104) and Kenyapithecus wickeri (KNM-FT 49)

postcrania, including most of the bones of the forelimb, vertebral column, hindlimb long bones, and a few pedal elements (McCrossin 1997; Ward and Duren 2002). Like Griphopithecus, which is much less well known postcranially, Equatorius is similar to Proconsul nyanzae in postcranial size and morphology. Nacholapithecus (Ishida et al. 1999) is known from deposits of the same age as Equatorius in the Samburu Basin of Kenya (Nakatsukasa et al. 1998). Like Equatorius, Nacholapithecus is known from a relatively complete skeleton, more complete in fact than the best specimen of Equatorius. From this exceptional skeleton, we know that Nacholapithecus is similar to other Middle Miocene hominoids in most aspects of the jaws and teeth but unique in aspects of limb morphology. While they are not especially elongated, the forelimbs of Nacholapithecus are more robust, that is, they are more strongly built, than are the hindlimbs. In a fascinating comparison, Ishida et al. (2004) show that Nacholapithecus has forelimb joints the size of a chimpanzee but hindlimb joints closer in size to those of a baboon, of much smaller body mass. The forelimbs were not elongated as in Page 20 of 66

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

modern apes, but they were enlarged. This is difficult to understand, but it probably has something to do with some increase in the degree to which Nacholapithecus was loading its forelimbs relative to its hindlimbs, even if it was not suspensory. Once again, we have a weird, unique fossil ape without a modern counterpart. Kunimatsu et al. (2004) provide evidence that the anterior portion of the palate of Nacholapithecus is more hominid-like in its length and degree of overlap with the palatine process of the maxilla (Fig. 3). This morphology is the principal evidence for the hominoid status of this species. However, in its details, the anterior palate of Nacholapithecus is unlike that of hominids (see below). In my opinion, there is also evidence of some postmortem compression that may contribute to the impression that the anterior portion of the palate of Nacholapithecus is more modern looking than it actually was. Otherwise, the postcranial skeleton of Nacholapithecus is similar to other Middle Miocene hominoids in having the general signature of a generalized, palmigrade, arboreal quadruped, but differs from Equatorius, also known from fore and hindlimb, in the enlarged size and robusticity of its forelimb. While not like extant nonhuman hominoids in forelimb length relative to the hindlimb, Nacholapithecus forelimbs are large and powerful, indicating a form of positional behavior emphasizing powerful forelimb grasping (Ishida et al. 2004). Interestingly, several wrist bones are well preserved in both Nacholapithecus and Equatorius, and they are quite similar to each other and to Proconsul and Afropithecus (personal observations). Kenyapithecus (Leakey 1962) is the most derived of the Middle Miocene African hominoids, and may be the earliest hominid (Table 2), although I should add that it is the least well known. Kenyapithecus is known only from a small sample from Fort Ternan in Kenya, though a second species may be present in Turkey (see below). Like other Middle Miocene hominoids, Kenyapithecus has large flat molars with broad cusps and thick enamel. The maxilla of Kenyapithecus, however, is derived in having a high root of the zygomatic, a probable hominid synapomorphy. While McCrossin and Benefit (1997) believe that Equatorius and Kenyapithecus represent a single species, most researchers have concluded that two genera are present and that Kenyapithecus is derived relative to Equatorius (Harrison 1992; Ward et al. 1999), and that is the view adopted here. As noted, it has been suggested that Kenyapithecus is also present at Pas¸alar. If so, and if Kenyapithecus is indeed an early hominid, this would date the origin of the hominid family to at least 16 Ma (but see footnote 1). However, there is a roughly 3 Ma gap between possible Kenyapithecus at Pas¸alar and the type material from Fort Ternan. One last Middle Miocene hominoid deserves mention here. Otavipithecus is the only Miocene hominoid known from southern Africa, from the 13 Ma site of Berg Aukas in Namibia (Conroy et al. 1992). Several specimens have been described, including the type mandible, a frontal fragment, and a few postcrania (Conroy et al. 1992; Pickford et al. 1997; Senut and Gommery 1997). It has been suggested that Otavipithecus has affinities to hominids (Conroy et al. 1992; Ward and Duren 2002), but it preserves primitive proconsuloid characters such as a small M1 compared to M2, a long M3, parallel tooth rows, a small space for the mandibular incisors, low P4 talonid, and tall, centralized molar cusps (Begun 1994b). Singleton (2000) carried out the most comprehensive analysis of Otavipithecus and concluded that it may be related to Afropithecus, which is broadly consistent with the placement of the taxon in Fig. 2. Like Heliopithecus, the most informative piece of information from the sample of Otavipithecus comes from its biogeography. Otavipithecus is a huge geographic outlier, suggesting that hominoids were widespread in equatorial and southern Africa but have yet to be found. Otavipithecus is morphologically somewhat atypical of Early and Middle Miocene hominoids, and I expect that when other taxa are found between Kenya and Namibia or elsewhere in Africa, they will be equally surprising.

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Summary of Middle Miocene Hominoid Evolution The radiation of Middle Miocene hominoids in Africa was relatively short-lived and less diverse than the Early Miocene radiation (see Table 1). Having apparently dispersed from Eurasia by about 15 Ma, they are mostly extinct by 12.5–13 Ma. Aside from a few fragmentary specimens that most likely represent the end of the Proconsul lineage (Hill and Ward 1988), hominoids would not appear again in Africa until the Late Miocene. Given the rarity of hominoid localities in the early Middle Miocene, the biogeographic hypothesis of the dispersal of Middle Miocene hominoids presented here is debatable. It is certainly possible, for example, that Early Miocene Griphopithecus-like fossils will be found in Africa that will show that Equatorius, Nacholapithecus, and Kenyapithecus all evolved in situ in Africa and that apparently earlier fossils from Eurasia are either misdated or are early offshoots of this clade with no direct relationship to later hominids (Ward and Duren 2002). In the end, perhaps the best way to think about Middle Miocene hominoids is in terms of a group of closely related genera that occupied the circumMediterranean region and the contiguous regions north into Germany and south into Kenya (with one known long distance dispersal into Namibia). Movements within the geographic area of these taxa were probably very complex and numerous over time, but from this melting pot of Middle Miocene thickly enameled hominoids, the first true hominids appear.

Early Hominids While Kenyapithecus shares a synapomorphy with the Hominidae (position of the zygomatic root), the first clear-cut hominids are known from Eurasia and share numerous cranial, dental, and postcranial synapomorphies with living hominids. This is the most important body of data supporting the Eurasian origins hypothesis. If that hypothesis is incorrect, we need to account for the absence of fossil hominids in Africa (which could just be bad luck) and also the presence of apparent hominid synapomorphies in both the Asian and European hominid fossil records. The extant Hominidae is divided into two subfamilies, Ponginae and Homininae, and the earliest representatives of both subfamilies are roughly contemporaneous. The earliest hominines are represented by Dryopithecus and possibly Pierolapithecus and Anoiapithecus (see below). Much better known and with clearer hominine synapomorphies are Rudapithecus, Hispanopithecus, and Ouranopithecus (see “▶ Potential Hominoid Ancestors for Hominidae”). The earliest pongines are represented by Ankarapithecus, Sivapithecus, and relatives. Miocene hominines are known from western Eurasia, while Miocene pongines are known from South and East Asia, reflecting the basic biogeographic division of the two hominid subfamilies today [but see Kelley and Gao (2012)].

Fossil Pongines The oldest sample of fossils widely interpreted as pongine is of Sivapithecus from the middle Chinji formation in the Siwaliks of Pakistan (Raza et al. 1983; Rose 1984, 1989; Kappelman et al. 1991; Barry et al. 2002). Specimens referred Sivapithecus indicus that are known to come from the middle Chinji formation share characters with later Sivapithecus and other hominids including reduced or absent molar cingula; relatively large M1; reduced premolar cusp heteromorphy; long, buccolingually compressed canines; broad-based nasal aperture; elongated and robust premaxilla partly overlapping the maxilla; and, as in Kenyapithecus, a high position to the zygomatic root. They share specifically with later Sivapithecus fewer clear-cut characters, such as probably strongly heteromorphic upper incisors (known only from the roots), and broad, flat cusped molars with thick enamel, though these characters are also found in most other Middle and many Late Page 22 of 66

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Miocene hominoids. One specimen of Chinji Sivapithecus, GSP 16075, represents a portion of the palate with the connection between the maxilla and premaxilla partially preserved. The maxillarypremaxillary relationship is highly diagnostic of Sivapithecus and the pongine clade, and the morphology of the Chinji specimen has been interpreted to share characters of this complex (Raza et al. 1983; Ward 1997b; Kelley 2002). However, while the specimen does have a relatively elongated, horizontal, and robust premaxilla, the area of the incisive fossa and foramen is not preserved. In the absence of this region, it is difficult to distinguish Chinji Sivapithecus from later Sivapithecus, including later Sivapithecus indicus, to which it is assigned, versus another pongine, Ankarapithecus. Ankarapithecus preserves a morphology of the anterior palate that lacks the synapomorphies of Sivapithecus and Pongo (Begun and Gu¨lec¸ 1998), and this may also be the case for the Chinji jaw. Resolution of this uncertainty would help to clarify the biogeography of pongine origins (see below).

Sivapithecus Sivapithecus Craniodental Evidence Most of the Sivapithecus samples, including the best-known specimens with the clearest evidence of pongine affinities, are from younger localities of the Siwaliks of India and Pakistan, dated between 10.5 and 7.5 Ma (Barry et al. 2002). In the following section, I discuss Sivapithecus in some detail because it is in many ways critical to understanding Late Miocene hominoid evolution. Three species are generally recognized in this sample, the best known of which is Sivapithecus sivalensis (Lydekker 1879), from localities ranging in age from 9.5 to 8.5 Ma (Kelley 2002). In addition to the characters outlined above, Sivapithecus sivalensis is known from a suite of cranial characters strongly indicative of pongine affinities (Pilbeam 1982). These include unfused tympanic and articular portions of the temporal bone; a posterosuperiorly directed zygomatic arch with deep temporal and zygomatic processes; vertically oriented frontal squama; supraorbital costae or rims; a narrow interorbital space; elongated nasal bones; tall, narrow orbits; wide, anteriorly oriented zygoma; narrow, pear-shaped nasal aperture; externally rotated canines; long, horizontally oriented nasoalveolar clivus that is curved along its length but flat transversely; and a subnasal region with the posterior pole of the premaxilla merging into the anterior edge of the maxillary palating process to form a flat, nearly continuous subnasal floor (Fig. 3) and a strongly concave facial profile from glabella to the base of the nasal aperture. Sivapithecus is also likely to have been airorhynchous (having a dorsally deflected face), as in Pongo (Fig. 4). All of these and other characters are described in more detail in Ward and Pilbeam (1983), Ward and Kimbel (1983), Ward and Brown (1986), Brown and Ward (1988), and Ward (1997b). Sivapithecus sivalensis is not identical to Pongo in cranial morphology, however, even if the similarities are striking and detailed. Sivapithecus sivalensis is more robust than similarly sized (female) Pongo in features related to the masticatory apparatus, including aspects of the zygomatic and temporal bones, maxillary robusticity, and molar morphology. The molars in particular are easily distinguished from those of Pongo in having thicker enamel and in lacking the complex pattern of crenulations seen in unworn Pongo molars. However, overall the number of derived characters shared with Pongo is impressive (Ward 1997; Kelley 2002) (Plates 8, 9, and 10). Sivapithecus indicus (Pilgrim 1910) is the oldest species, and if the middle Chinji fossils are included, it would range from 12.5 to 10.5 Ma (Kelley 2002). It is the smallest species, at least in terms of dental size, and appears to have a slightly shorter nasoalveolar clivus or premaxilla compared with Sivapithecus sivalensis (see above). Sivapithecus parvada (Kelley 1988) is considerably larger than the other species and is known from the Nagri formation locality Y311, about 10 Ma. Sivapithecus parvada males are about the dental size of female gorillas. The upper central Page 23 of 66

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

Plate 8 GSP 15000, the best preserved specimen of Sivapithecus. To the right is a lateral view of the face without the mandible (Courtesy of Milford Wolpoff)

Plate 9 Sivapithecus palates. GSP 15000 to the left and YPM 13799 (formerly Ramapithecus) to the right (Courtesy of Milford Wolpoff)

incisors are especially long mesiodistally, the M3 is larger than the M2, the premolars are relatively large, and the symphysis of the mandible is very deep (Kelley 2002). Sivapithecus Postcrania Sivapithecus postcrania have been described in many publications (Pilbeam et al. 1980, 1990; Rose 1984, 1986, 1989; Spoor et al. 1991; Richmond and Whalen 2001; Madar et al. 2002). They combine a mixture of characters, some suggesting more palmigrade postures and others suggestive of more suspensory positional behavior (see “▶ Postcranial and Locomotor Adaptations of Hominoids”). This has been interpreted by some to indicate that Sivapithecus is more primitive than any living hominoids, all of which, even humans, share numerous characters of the shoulder and forelimbs related to suspensory behavior or an ancestry of suspensory behavior (Pilbeam 1996, 1997; Pilbeam and Young 2001, 2004). This view, also shared by McCrossin and Benefit (1997), has dramatic implications for the interpretation of the hominoid fossil record. All Late Miocene Page 24 of 66

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

Plate 10 Sivapithecus mandibles, showing substantial diversity in size and morphology. The two specimens to the left courtesy of Milford Wolpoff. From left to right, GSP 15000, GSP 9564, M. 15423

hominoids, including Sivapithecus, share many characters of the cranium and dentition with living hominoids. If Sivapithecus is more primitive than extant hominoids, given its apparently primitive postcrania, then all the apparently derived hominid features of Sivapithecus would have evolved in parallel in Sivapithecus, and as these authors suggest, by extension in all Late Miocene hominoids (Oreopithecus, Dryopithecus, Rudapithecus, Ouranopithecus, Lufengpithecus, etc.). These parallelisms include not only craniodental morphology but also details of life history and, as it turns out, many postcranial characters as well. In fact, the apparently primitive characters of Sivapithecus postcrania are small in number compared with the large number of clearly derived hominid characters from throughout the skeleton and known biology of all Late Miocene hominids. Rather than rejecting the hominid status of Sivapithecus and other Late Miocene hominids because not all of their postcranial morphology is strictly hominid or even extant hominoid-like, it is much more likely that these few characters reflect mosaic evolution of the hominid skeleton, uniquely derived features of the anatomy of Sivapithecus, as well as some parallelism in extant hominoids (Begun 1993; Begun et al. 1997; Begun and Kivell 2011; see below). Sivapithecus postcrania, though they have been the subject of more discussion related to phylogeny, are actually less well known than those of Proconsul, Equatorius, or Nacholapithecus. The following is summarized mainly from Rose (1997), Richmond and Whalen (2001), and Madar et al. (2002). Much more information is available from all the references cited earlier. Two species of Sivapithecus are known from the humerus, which is unlike that of modern hominoids in the curvature of the shaft and the development of the deltopectoral plane. The bicipital groove is also broad and flat and suggests a posteriorly oriented humeral head, as in the Early and Middle Miocene Hominidea described earlier. However, the humerus has such an unusual morphology that the orientation of the head, which is already somewhat difficult to predict from bicipital groove position (Larson 1996), cannot be reconstructed with great confidence. Nevertheless, the morphology of the proximal humerus in Sivapithecus is suggestive of some form of pronograde quadrupedalism as seen, for example, in extant cercopithecoids. If the humeral head were oriented more posteriorly, it would also be consistent with a scapula that is placed on the side of a compressed rib cage, as in typical mammalian quadrupeds, and unlike extant hominoids (Rose 1989; Ward 1997a). No direct evidence is available for the thorax or any part of the axial skeleton of Sivapithecus, however, so this will also have to await further discoveries. The deltopectoral plane and the curvature of the shaft of the humeri in Sivapithecus are quite strongly developed compared with most cercopithecoids and indicate in my view a unique form of positional behavior that is neither extant hominoid nor extant cercopithecoid-like (Madar, et al. 2002). The distal end of Page 25 of 66

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the humerus is in the main hominoid-like, including a well-developed trochlea separated from the capitulum by a deep, well-defined groove (the zona conoidea), though in a few details of the posterior surface, there are similarities to Proconsul and Kenyapithecus (Rose 1997). Overall, however, the functional morphology of the elbow of Sivapithecus is most like the hominoid elbow in its ability to resist movements other than flexion and extension at the elbow joint, a hallmark of the Hominoidea (Rose 1988). The Sivapithecus forearm is poorly known, especially the proximal portions of the ulna and radius, which would help to more fully understand the Sivapithecus elbow. A juvenile radial shaft is known that is described as Proconsul-like, though as a juvenile, it is not clear to what extent we might expect any hominoid-like characters, such as curvature and the nature of the ligamentous/ muscular insertions, would be expressed. On the other hand, the few carpal bones that are known show a mixture of hominoid and non-hominoid features. The capitate of Sivapithecus has a somewhat expanded and rounded head, as in great apes, but overall is transversely narrow and elongated proximodistally compared with great apes. The joint surface for the third metacarpal is irregular as in great apes. The hamate is similar in length/breadth proportions and has a less strongly projecting hammulus than do great ape hamates (Spoor et al. 1991). The joint on the hamate for the triquetrum is oriented as in gorillas and also most other non-hominoid anthropoids, and its shape suggests a stabilizing function at the wrist, which differs fundamentally from the typical mobility of the ulnar side of the wrist in extant hominoids. The proximal end of a first metacarpal is similar in morphology to hominids and Early Miocene Hominidea in being saddleshaped, a configuration considered to represent a good compromise between mobility and stability in a wide variety of positions. The manual phalanges are long and curved, with strongly developed ridges for the flexor muscles and their sheaths. One complete phalanx has a relatively deep and somewhat dorsally positioned articular surface for the metacarpal head, which is more typical of palmigrade quadrupeds. However, it is not completely clear if this is from a hand or a foot, and if the latter is the case, a similar morphology exists in some hominoids as well. Begun and Kivell (2011) undertook a reanalysis of the carpal bone of Sivapithecus in light of recent discoveries of carpal bones of Rudapithecus (see below). They concluded that there are a number of terrestrial and even knuckle-walking characteristics of the capitate and hamate of Sivapithecus, though the capitate and hamate of Sivapithecus are nevertheless easily distinguished from those of African apes. The authors suggest that if the Sivapithecus species to which these carpals belong (S. sivalensis for the capitate and S. parvada for the hamate) did knuckle-walk, they did so in a manner that was biomechanically different from extant African apes (see “▶ The Hunting Behavior and Carnivory of Wild Chimpanzees,” “▶ Great Ape Social Systems,” “▶ The Origins of Bipedal Locomotion”). It is worth remembering of course that African apes today are biomechanically distinct from one another in their knuckle-walking. Whatever this means in terms of the big picture of hominoid evolution is unclear, but one mystery that is potentially solved by this analysis is the biogeography of the Miocene pongines (see below). The hindlimb of Sivapithecus is less well known but generally more similar to extant hominoids than the forelimb. The femur is known from proximal and distal ends but not from the same individual (Rose 1986; Madar et al. 2002). The hip joint as represented by the femoral head and neck was mobile in many directions, though it has a well-developed fovea capitis, unlike Pongo, which is highly distinctive (but not unique) in lacking a ligamentum teres of the femur and thus its attachment site to the femur, the fovea capitis. The distal end of the femur preserves evidence of a knee joint that is consistent with this interpretation, implying a knee joint loaded in positions away from the sagittal plane. The knee also has a number of features allowing for rotation of the leg Page 26 of 66

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

and foot to adjust the lower extremity to a variety of positions close to and further away from the center of mass (Madar et al. 2002). In all of these features, the femur is more like that of hominoids than other anthropoids. Other hindlimb elements include several tarsal bones, phalanges, and a well-preserved hallucial skeleton (Conroy and Rose 1983; Rose 1984, 1986, 1994). The tarsals are perhaps more like those of great apes than any other part of the postcranium of Sivapithecus (Rose 1984; Madar et al. 2002), indicating the presence of a broad foot, able to assume many positions but stable in all of them, and supportive of body mass loading from many directions. The hallux or big toe is strikingly robust, much more so than in Pongo, and indicates a strongly developed grasping capability in the foot. The phalanges are also by and large hominoid-like, with well-developed features related to powerful flexion of the toes, a critical function in antipronograde activities (climbing as well as suspension). Sivapithecus Phylogeny and Paleobiology Overall, the morphology of Sivapithecus strongly supports a close phylogenetic relationship to Pongo but an adaptation that differed from Pongo in important aspects. Microwear suggests that Sivapithecus had a diet that was similar to that of chimpanzees, while gnathic morphology suggests more of a hard-object diet (Teaford and Walker 1984; Kay and Ungar 1997; “▶ Dental Adaptations of African Apes”). Perhaps this reflects a capacity to exploit fallback or “keystone” resources in times of scarcity. Most hominoids are known to practice this strategy (Tutin and Fernandez 1993; Tutin et al. 1997). The case of gorillas may be most relevant to the question of the diet of Sivapithecus. Most gorillas have diets similar to chimpanzees but are able to exploit terrestrial herbaceous vegetation (THV) in lean seasons when soft fruit is less available or in contexts in which they are sympatric with chimpanzees (Tutin and Fernandez 1993; Tutin et al. 1997). The microwear results may reflect the preferred and most common components of the diet, while the morphology of the jaws and teeth may reflect a critical adaptation to a keystone resource on which survival would depend during stressful periods (see “▶ Role of Environmental Stimuli in Hominid Origins,” “▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments”). Postcranial evidence clearly indicates that Sivapithecus was not orang-like in its positional behavior. In fact, it was unique; there are probably no living analogues. Sivapithecus combines clear indications of pronograde forelimb postures and a palmigrade hand position with more antipronograde activities such as vertical climbing and clambering implied by elbow joint stability over a wide range of flexion/extension, powerful grasping hands and feet, an especially powerful hallux, and hindlimbs capable of wider ranges of joint excursions than in extant pronograde quadrupeds (Madar et al. 2002). It is difficult to imagine exactly what the positional behavior of Sivapithecus might have been like. One constant in the postcranial functional morphology of Sivapithecus is arboreality. Perhaps Sivapithecus used its powerful limbs in climbing and bridging or clambering activities, spreading the limbs across multiple supports to access smaller branches. In a sense, it is orang-like without the suspension. While Sivapithecus managed to distribute its considerable body mass across the tops of several branches, orangs do the same but from below. In large animals, the advantage to suspension is added stability on horizontal supports, since they otherwise need to generate very high levels of torque to stay atop a branch (Grand 1972, 1978; Cartmill 1985). Orang males are larger than Sivapithecus and may be beyond the threshold where pronograde limb postures are possible in the trees. The fact that the proximal half of the humerus of Sivapithecus, while similar to that of a pronograde quadruped, is exceptionally robust, with extremely well-developed shoulder muscle attachments, may be an indication of a unique approach to this problem. Page 27 of 66

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

Sivapithecus does share numerous postcranial features, especially of the elbow and hindlimb, with extant hominoids and Dryopithecus. It is therefore possible that the more monkey-like morphology of the proximal humerus and portions of the hands and feet are actually homoplasies with cercopithecoids caused by the adoption of more pronograde postures in a hominoid that evolved from a more suspensory ancestor (Begun et al. 1997). This requires many fewer homoplasies than the alternative hypothesis that all extant hominoid characters in all Late Miocene hominoids are homoplasies (Pilbeam 1996, 1997; McCrossin and Benefit 1997; Pilbeam and Young 2001, 2004). There is some evidence from the functional morphology of Sivapithecus to support the hypothesis that its form of pronograde arboreal quadrupedalism is actually superimposed on a suspensory hominoid groundplan (see “▶ The Origins of Bipedal Locomotion”). The problem of angular momentum causing instability in a large mammal standing on top of a branch is alleviated in part by spreading the limbs apart on a wide support, or across several supports, which Sivapithecus seems to have been capable of doing (Madar et al. 2002). It can also be all alleviated by placing the center of mass closer to the support, which is suggested for Griphopithecus (Begun 1992a), and may have also occurred in Sivapithecus, as a consequence of its habitually more laterally placed limbs (Madar et al. 2002). The positioning of the limbs more laterally in hominoids is part of the suite of characters related to trunk morphology and scapular position. It is not facilitated by monkey-like trunks and scapular positions, which promote more parasagittal limb movements. Finally, an important response to angular momentum is to increase the torque generated by the limbs on the support, to prevent excessive excursions from a balanced position, especially when a single support of only modest size is used, again suggested to be an aspect of the positional behavior of Sivapithecus (Madar et al. 2002). Higher torque results from more powerful gripping, also characteristic of Sivapithecus (Madar et al. 2002), and may have been boosted by especially powerfully developed shoulder joint adduction and medial rotation, particularly if the shoulder is in a relatively abducted position to begin with, as in hominoids. The morphology of the proximal half of the humerus in Sivapithecus is consistent with very powerful adduction and medial rotation by deltoideus and pectoralis major. These muscles left extremely prominent scars on the humerus of Sivapithecus. If the arm of Sivapithecus were positioned as in extant hominoids, laterally on a posteriorly positioned scapula, the adduction and medial rotation capacities of deltoideus and pectoralis would be increased by increasing the relative mass of the clavicular portion of deltoideus, which is unknown in Sivapithecus. However, in addition to the need for powerful muscles, which existed in Sivapithecus, these functions would also be enhanced by other attributes known in Sivapithecus. The extension of the muscles along the shaft distally and the possible decreased humeral neck torsion would increase the moment arm for these muscles in adduction and reposition the insertions of these muscles medially, possibly to make more of the deltoideus available for adduction and medial rotation. The strong mediolateral curvature of the shaft may result from high mediolateral bending stresses that would result from very powerful shoulder adduction on a fixed limb. The proximal shaft is also very broad mediolaterally, suggestive of strong mediolaterally directed stresses. While speculative, it is certainly conceivable that the upper part of the forelimb of Sivapithecus was less monkey-like than generally perceived and may not imply that much of the trunk was of the primitive anthropoid type. A small number of autapomorphies of the shoulder of Sivapithecus may have allowed this taxon to practice a relatively efficient form of arboreal pronograde quadrupedalism while maintaining the capacity for many of the antipronograde activities of hominoids, though probably not for frequent upper limb below-branch suspension. This hypothesis is functionally consistent with the morphology of the Sivapithecus postcranium in general and is certainly more Page 28 of 66

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

parsimonious than the hypothesis that would interpret all Late Miocene hominoid characters as homoplasies (Begun and Kivell 2011).

Ankarapithecus Aside from some material from Nepal attributed to Sivapithecus (Munthe et al. 1983), Sivapithecus is known only from India and Pakistan. Specimens from central Anatolia, Turkey, once attributed to Sivapithecus (Andrews and Tekkaya 1980) are now assigned to Ankarapithecus, following the original conclusions of Ozansoy (1957, 1965). Ankarapithecus meteai is known from a male palate and mandible from two different individuals and a female partial skull (mandible and face) from a third locality, all close to each other in location and geological time (Kappelman et al. 2003). Begun and Gu¨lec¸ (1995, 1998) resurrected the nomen Ankarapithecus based mainly on the morphology of the premaxilla and the relationship between this bone and the maxilla but concluded that Ankarapithecus is nonetheless in the pongine clade. Alpagut et al. (1996) and Kappelman et al. (2003) described newer and much more complete fossils of Ankarapithecus and concluded that it is a stem hominid (sharing a common ancestor with both pongines and hominines). The new fossils discovered and described by these authors include the region around the orbits, which lacks some of the characters of Sivapithecus. The interorbital region is intermediate in breadth between Pongo, with the narrowest interorbitals, and African apes and the orbits themselves are broad rather than tall and narrow. Alpagut et al. (1996) and Kappelman et al. (2003) also interpret the supraorbital region as a supraorbital torus, characteristic of African apes and humans and some European Late Miocene taxa, and they interpret a frontal sinus in the cranium of Ankarapithecus as a frontoethmoidal sinus. These authors see the mixture of hominine and pongine characters as an indication that Ankarapithecus precedes their divergence (Plate 11). Craniodental Evidence The frontal sinuses in Ankarapithecus appear to be confined to the frontal squama and do not invade the frontal supraorbital region from a broad expansion of the ethmoidal sinuses. They are positioned and developed as in extant taxa with frontal pneumatizations derived either from the sphenoidal or maxillary sinuses and are unlike those derived from the ethmoid (see above discussion). The frontal pneumatization in Ankarapithecus is unlikely to be a frontoethmoid sinus and thus is not a synapomorphy of the hominines. The supraorbital region, while robust, is morphologically similar to the robust supraorbital costae of large orangs or Cebus and also unlike the bar-like supraorbital tori of African apes. Thus, the supraorbital region of the Ankarapithecus cranium is more pongine than hominine-like and, like the maxilla, probably represents the primitive morphology for the pongines (see below). In Ankarapithecus, the premaxilla, the portion of the palate with the alveoli for the incisors and the mesial half of the canines, is unlike that of Sivapithecus and more like that of African apes. The premaxilla is long, but it does not overlap the palatine process of the maxilla to fill the incisive fossa to the degree seen in Sivapithecus. Instead, the subnasal fossa is stepped (there is a drop between the base of the nasal aperture and the floor of the nasal cavity) into an incisive fossa that is most like that of some chimpanzees, a relatively large depression opening into a canal (the incisive canal that runs between the premaxilla and maxilla to exit on the palatal side via the incisive foramen). Rudapithecus has a similar configuration of the subnasal fossa, incisive canal, and incisive foramen, though the fossa is larger and the canal is shorter in length and larger in caliber, as in some gorillas (Begun 1994a; Fig. 3). The premaxilla of Ankarapithecus is curved or convex anteroposteriorly as in Sivapithecus, African apes, and Rudapithecus, but it is also convex transversely, as in African apes and Rudapithecus unlike Sivapithecus, which has a transversely Page 29 of 66

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

Plate 11 Ankarapithecus (MTA 2125)

flatter premaxilla. In all of these features, Ankarapithecus expresses a condition intermediate between pongines and hominines, which I consider primitive for the pongines (Begun and Gu¨lec¸ 1998). Alpagut et al. (1996) and Kappelman et al. (2003) have suggested that these characters indicate that Ankarapithecus precedes the divergence of pongines and hominines and is thus a stem hominid. Other features of the morphology of Ankarapithecus resemble pongines more clearly, including canine implantation, zygoma size and orientation, orbital margin morphology, nasal length, and dental morphology. Overall, Ankarapithecus most closely resembles Sivapithecus and Pongo but retains a more primitive palatal morphology that suggests it is at the base of the pongine clade. Postcranial Evidence Some postcrania of Ankarapithecus are known, including a well-preserved radius and two phalanges (Kappelman et al. 2003). A femur tentatively identified as primate is more likely in my opinion to be from a carnivore. The radius shares characters with extant great apes including features of the radial head and a comparatively long radial neck (Kappelman et al. 2003). Other hominoid-like features described or figured in Kappelman et al. (2003) but not identified as hominoid-like by these authors include a proximodistally compressed and more circular radial head, a deep radial fovea, flat as opposed to concave shaft surface along the anterior surface, a more distal origin of the interrosseous crest, and a smooth distal dorsal surface. The specimen actually strikes me as quite hominoid-like with a few features more normally associated with large non-hominoid anthropoids, a pattern more or less in keeping with other Late Miocene hominoids. The phalanges are said to be relatively straight and thus non-hominoid-like, but only distal portions are preserved. They too strike me as more hominoid-like than Kappelman et al. (2003) suggest, given its distal shaft robusticity, dorsopalmar compression, and distopalmarly projected condyles. The curvature and ridges for the flexor musculature are said to be poorly developed compared with hominoids, but this may be related to many factors (preservation, age, digit attribution). Overall, Ankarapithecus is characterized by many features found in other pongines and is probably the most basal known member of that clade. Like Sivapithecus, it was much more massive in the development of its masticatory apparatus than Pongo, and its postcranium, though very poorly known, suggests arboreality and at least some features of hominoid-like antipronograde positional behaviors, but probably lacking the degree of suspension seen in dryopithecins, Oreopithecus, and extant hominoids (but see Kappelman et al. 2003).

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Other Probable Fossil Pongines Indopithecus-Gigantopithecus Extremely large fossil hominoids, larger than any extant primate, have been known from Asia since the early part of the twentieth century. Gigantopithecus blacki (Koenigswald 1935) is a Pleistocene taxon known from numerous isolated teeth and a few mandibles. It is recent enough to be outside the purview of this review and has been described many times elsewhere. Sivapithecus giganteus (Pilgrim 1915) is the oldest nomen attributed to samples from the Late Miocene of South Asia that may be related to Gigantopithecus. This sample, only known from a lower M3 from the Late Miocene of the Siwaliks, is mainly distinguished from Sivapithecus by size. When a mandible with teeth of similar size was found, a new species, Gigantopithecus bilaspurensis, was named, but more recently most researchers have combined the mandible with the type of Sivapithecus giganteus (the lower molar), thus making the new combination Gigantopithecus giganteus (Kelley 2002). Von Koenigswald (1949) proposed the nomen Indopithecus for the M3. In my view, the type of G. bilaspurensis is sufficiently distinct from Pleistocene Gigantopithecus that I place both the mandible and the M3 in Indopithecus, making the new combination Indopithecus giganteus. The jaws and teeth of Indopithecus are larger than any Sivapithecus, and the only known mandible is distinctive in having reduced anterior tooth crown heights and molarized or enlarged premolars. G. blacki, on the other hand, is larger still and has highly complicated postcanine occlusal morphology and relatively even larger mandibles and smaller anterior teeth. Because I. giganteus and G. blacki share characters of the lower jaws and teeth that appear commonly during the course of hominoid evolution (in fact, in many other mammal lineages as well), the relationship between the two is uncertain. Jaws and teeth in general, and mandibles in particular, are magnets for homoplasy in primate evolution (Begun 1994b, 2007), and this may be another example. In the end, the morphology of the jaw and teeth of Indopithecus much more closely resembles that of Sivapithecus, while certain dental proportions more closely resemble Gigantopithecus. Given the age and morphological differences, I prefer to recognize two genera, though I do recognize that they are closely related. The most parsimonious hypothesis is that I. giganteus is a primitive member of the Gigantopithecus clade and that the strong similarity to Sivapithecus in the molars, apart from size, suggests that it is the sister clade to that taxon (Table 1, Plate 12). Lufengpithecus Thousands of fossils, mostly isolated teeth, are known from a number of localities in Yunnan Province, southern China. These are attributed to the genus Lufengpithecus (Wu 1987). Lufengpithecus is most commonly recognized as a pongine. Kelley tentatively recognizes three species of Lufengpithecus, distinguished mainly by size and geography (each is known from a single site). Lufengpithecus shares a few cranial characters with other pongines including a small, pear-shaped nasal fossa, aspects of the implantation of the canine roots in the maxilla, a deep canine fossa, supraorbital costae, and anteriorly oriented zygoma (Schwartz 1997 and personal observations). However, while it lacks many of the detailed similarities of the face between Sivapithecus and Pongo, its teeth are much more like those of Pongo than Sivapithecus in details of occlusal morphology, including the unusual presence of highly complex wrinkling or crenulations (Kelley 2002). The face of Lufengpithecus is unlike those of Sivapithecus and Pongo in having broad orbits, a broad interorbital space, a comparatively short premaxilla, high crowned incisors and canines, and compressed and very tall crowned male lower canines. Though very damaged, my impression is that the nasal floor is unlike the smooth floor of Sivapithecus and Pongo but possibly more similar to the morphology in Ankarapithecus. There are intriguing similarities Page 31 of 66

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

Plate 12 Two mandibles of Gigantopithecus compared with a modern human mandible. Gigantopithecus images courtesy of Milford Wolpoff

between Lufengpithecus and dryopiths, especially in the incisors and premaxilla, and Kelley and I have independently reached the conclusion that they might be more closely related to one another than Lufengpithecus is to pongines. This, however, is a hypothesis that needs a lot more investigation, and for now I follow Kelley (2002) in placing Lufengpithecus among the pongines (Plates 13 and 14). L. lufengensis (Xu et al. 1978) from a site near Shihuiba, in Lufeng county, is the best-known species of the genus and is also known from a number of postcranial remains including fragments of a scapula, clavicle, radius, first metatarsal, and two phalanges. None have been published in detail, but all of these specimens show clear indications of modern hominid morphology associated with suspensory positional behaviors (personal observations). This is especially true of the phalanges, which are strongly curved and bear the markings of powerful flexor tendons. The metatarsal is similar to that of Sivapithecus in its relative robusticity. Until the fossils attributed to Lufengpithecus are published in detail, it will be impossible to be confident in assessing their taxonomic and phylogenetic relations. At this point, it seems likely that Lufengpithecus is a pongine and probably a sister taxon to the Pongo-Sivapithecus-Ankarapithecus clade. However, the generally more Pongo-like morphology of the molar occlusal surfaces and the more clearly hominoid-like morphology of the postcrania are enigmatic and suggest caution in interpreting evolutionary relationships. Kelley and Gao (2012) describe a juvenile specimen of Lufengpithecus from a different locality, Yuanmou, also in Yunnan Province. The Yuanmou specimen is interpreted by these authors as having more similarities with dryopithecins than previously supposed for Lufengpithecus, which is consistent with my impressions of the adult specimens from Shuhuiba. However, we both come short of concluding that there is definite evidence of a phyletic link between Lufengpithecus and the dryopithecins. Interpreting the morphology of a taxon from a juvenile specimen can be very tricky. More detailed comparisons between the Yunnan Province Lufengpithecus samples and those of dryopithecins from Europe are needed to determine if there really are phylogenetic connections between the two groups of hominids independent of the Siwalik taxa. This, however, would represent a dramatic development in our understanding of Late Miocene ape biogeography and would falsify an observation I made some years ago about the separation of the Asian and European samples (Begun 2005). Another possibility of course is that the Yunnan samples represent another lineage of hominid not specifically related to any living great ape (Ji et al. 2013). Only more detailed comparisons among these samples will help to resolve this issue.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

Plate 13 Female (upper left, PA 586) and male (upper right, PA 548) mandibles of Lufengpithecus in occlusal view, and, below, an anterior view of the male. Note the high crowned and narrow anterior dentition

Plate 14 Two Lufengpithecus babies. To the left, from Yuanmou (YV 0999) and to the right, from Shuitangba (ZT 299) (Courtesy of Jay Kelley)

Khoratpithecus Three samples of Southeast Asian Miocene hominoids have recently come to light. Chaimanee et al. (2003) describe a Middle Miocene sample of hominoids from Thailand they originally attributed to a species of Lufengpithecus. The age of the locality is not completely certain, and it is possible that the fauna could be correlated with a more recent magnetostratigraphic interval, but for now the sample is considered to date to the late Middle Miocene or early Late Miocene (13.5–10 Ma). However, on the basis of more recently discovered Late Miocene hominoid fossils from Thailand, Chaimanee et al. (2004) described a new genus, Khoratpithecus, and revised their previous taxonomic conclusions to include the Middle Miocene taxon in the newly named genus as well. The fossils, a sample of isolated teeth and a well-preserved mandible, are very similar to Lufengpithecus but show a number of differences in the anterior dentition and lower jaw (Chaimanee et al. 2004). Chaimanee et al. (2004) interpret Khoratpithecus to be more closely related to Pongo than is any other pongine, mainly based on the shared derived character of a missing anterior digastric muscle. More fossils are needed to test this hypothesis more fully. The greater significance of these discoveries is the location, in Thailand, and the possibly early age, Middle Miocene. In 2011 the same research group described a new species of Khoratpithecus from Page 33 of 66

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Myanmar (formerly Burma), to the northwest of Thailand (i.e., in the direction of the Siwaliks of India and Pakistan) (Jaeger et al. 2011). The three species of Khoratpithecus are represented only by a small number of mandibles and isolated teeth, and it is not clear if three different species are represented, but they do appear to be distinct from Sivapithecus and Lufengpithecus. All four genera of Asian great apes described here range in age from possibly as old as 13.5 Ma to possibly as young as 6 Ma. If the dates are correct, Khoratpithecus ayeyarwadyensis, from Myanmar, is the oldest of this group and is roughly contemporary with Kenyapithecus from Fot Ternan, Kenya. Lufengpithecus lufengensis from Shuhiba (Yunnan Province, China) and Indopithecus from the Siwalik Hills are the youngest, at about 6–7 Ma, and are roughly contemporaneous with Sahelanthropus, from Chad, the earliest known hominin.

The Earliest Fossil Hominines: The Dryopithecins 1 At about the same time that hominids appear in Asia, they make their first appearance in Europe. As is the case with the earliest pongines, the earliest hominines lack a number of synapomorphies of living hominines (African apes and humans) and are less distinct from related non-hominines than are more recently evolved hominines. This has led naturally to differences of opinion regarding the systematics of this group (see “▶ Defining Hominidae,” “▶ Hominoid Cranial Diversity and Adaptation”). There are three main interpretations of the evolutionary relations among the taxa included here in the Homininae. As noted, some researchers conclude that no known Eurasian Late Miocene taxon has a specific relationship to extant hominoids (Pilbeam 1996, 1997; McCrossin and Benefit 1997; Pilbeam and Young 2001, 2004). Most researchers, however, accept the hominid status of these fossil taxa but are divided as to their interrelationships. Some researchers (Andrews 1992) have concluded that European Late Miocene hominids are best viewed as stem hominids, preceding the divergence of hominines and pongines. Others interpret most or all Eurasian hominines to be members of the pongine clade (Moya`-Sola` et al. 1995). Finally, some researchers interpret most or all European hominids to be hominines, although there is disagreement among them as to the precise pattern of relations (Bonis and Koufos 1997; Begun and Kordos 1997; see “▶ Potential Hominoid Ancestors for Hominidae”). As my interpretation falls with the last group, this will be reflected in this chapter. I will however attempt to outline the major arguments from each perspective. Nomenclatural History The taxonomic history of Dryopithecus and the dryopithecins is very complicated (see Begun 2002 for a more complete history). At one time, most of the well-known taxa described here were attributed to Dryopithecus (Proconsul, Sivapithecus, Ouranopithecus, Ankarapithecus, Griphopithecus). More recently Dryopithecus was restricted to the sample European great apes from Spain, France, Germany, Austria, Hungary, and Georgia that all share features in common with African apes, in particular thinly enameled teeth with less robust jaws than Sivapithecus or Ouranopithecus. This was the consensus when the first version of this review was published in 2007. Since then the concept of Dryopithecus has become even more narrowly defined. As of this writing, Dryopithecus is restricted more or less to the original sample from St. Gaudens, a mandible from Austria and a maxilla from Spain. The important distinctions between Dryopithecus and most of the other samples that have until recently been attributed to Dryopithecus are age and morphology. All Dryopithecus, along with Pierolapithecus and Anoiapithecus, are more primitive in dental morphology (persistent cingula, small first molars, short premolars, robust canines) (Begun et al. 2012; Alba 2012). Postcranially, Pierolapithecus is more primitive than the later-occurring Hispanopithecus and Rudapithecus (see below). Dryopithecus, Pierolapithecus, and Page 34 of 66

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Anoiapithecus all occur in the Middle Miocene. Later-occurring and more modern-looking dryopithecins are all from the Late Miocene in Europe. Specimens from the Middle Miocene of Spain have been attributed to Dryopithecus but also to two new taxa, Pierolapithecus and Anoiapithecus. The latter is known only from a distorted facial fragment, while the former is known from many parts of a skeleton, though unfortunately the face is seriously damaged. Because Dryopithecus sensu stricto is known only from male mandibles, it is extremely difficult to compare it with Pierolapithecus and Anoiapithecus, both of which are known mainly from upper teeth and postcrania. There is a mandibular fragment of Anoiapithecus that can be compared directly with Dryopithecus, and in my opinion, the differences between the two samples do not warrant a genus level distinction. Pierolapithecus is not known from lower teeth or jaws, and it is impossible to compare this sample with Dryopithecus. In addition, when they were first described, each of these taxa was assigned to different hominid clades. Pierolapithecus and Anoiapithecus were first described as stem hominids, predating the divergence of pongines and hominines (Moya`-Sola` et al. 2004, 2009a). Dryopithecus, when it was discovered at Hostalets, was first described as a hominine and possibly a sister clade to Gorilla (Moya`-Sola` et al. 2009b). In addition, Hispanopithecus, also from the Valle`s Penede`s but from younger deposits (see below), was first described as a pongine. This represents three separate hominid clades present in a relatively restricted temporal and geographic span, which I consider unlikely. The most current interpretation of all of these taxa places them in the Ponginae (Alba 2012, Fig. 8, p. 265), though this author acknowledges that other interpretations, including the alternatives that they are all hominines or stem hominids, are possible. The practical difficulties in comparing Pierolapithecus, Anoiapithecus, and Dryopithecus to each other, given the few comparable parts preserved (see below), led me to be skeptical that three different genera and possibly three different clades can be effectively identified from these samples. The fact that all three Middle Miocene genera were found within a few kilometers of one another from essentially the same time period and same geological formation made me even more skeptical that three different genera are represented. All three are Middle Miocene and are more primitive than Late Miocene apes including Hispanopithecus. However, this is not the place for a taxonomic revision of these genera, so I will use the nomena originally proposed by the describers while noting that they are probably all closely related and possibly all Dryopithecus. Dryopithecus fontani Dryopithecus is the first-named taxon, and it is agreed by most researchers that this taxon is Middle Miocene and more primitive than Late Miocene European great apes. There is disagreement as to whether or not other early hominids taxa lived in Western Europe during the same time as Dryopithecus. Dryopithecus was first identified from St. Gaudens, on the northern slopes of the French Pyrenees (Lartet 1856). Dryopithecus sensu stricto, that is, D. fontani, is only known from three mandibles, a few isolated associated teeth, and a humeral shaft, all from St. Gaudens. Two isolated teeth from La Grive, also in France but in a geologically completely different context (Alpine as opposed to Pyrenean), are also traditionally attributed to Dryopithecus. These sites are considered to be Middle Miocene, based exclusively on their fauna, and the apes from these sites are more primitive dentally than apes that occur later on in Europe. D. fontani is known from three male mandibles and a humerus, all from the same locality in France, a female mandible from Austria, and a partial face from Spain (Begun 2002; Begun et al. 2012; Moya`-Sola` et al. 2009b). Two isolated upper teeth from La Grive in France are also usually attributed to D. fontani. The mandibles and their dentitions are typically hominid in being comparatively robust with well-developed symphyseal tori, large incisors, compressed canines, Page 35 of 66

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elongated postcanine teeth with peripheralized cusps and lacking cingula, P4 with trigonids and talonids of nearly equal height, and molars of nearly equal size, especially M1 and M2. The teeth of all Dryopithecus are thinly enameled with dentine horns penetrating well into the enamel caps. D. fontani is distinguished from other species of Dryopithecus in having a mandible that shallows (becomes lower compared to breath) distally, a high frequency of buccal notches on the lower molars, and comparatively robust lower canines. The more recently described material attributed to Dryopithecus from Catalonia include a palate that cannot be directly compared with the fossils from France and Austria but does allow a comparison with Anoiapithecus and Pierolapithecus. Alba (2012) maintains that the morphological differences among these three samples are sufficient to justify the recognition of three different genera, all of which he places within the ponginae. In my view, the differences are minor and the samples, while including well-preserved specimens, are small, making it very difficult to assess ranges of variation within each group. This being the case, I think it is more likely that a single genus is represented, and by the rule of taxonomic priority, that taxon would be Dryopithecus (Begun et al. 2012). D. fontani is also known from a humeral shaft from the type locality that has been described as chimpanzee-like (Pilbeam and Simons 1971; Begun 1992a). It is the only nearly complete humerus of the genus. It is comparatively long and slender with poorly developed muscle insertion scars and a slight mediolateral and anteroposterior curvature. Neither the proximal nor the distal epiphyses are preserved, but the diaphysis preserved close to each epiphysis is hominoid-like. Proximally, it is rounded in cross section with a bicipital groove position suggesting some degree of humeral torsion (but see Rose 1997; Larson 1998). Distally, it is mediolaterally broad and anteroposteriorly quite flat, with a large, broad, relatively shallow olecranon fossa (Begun 1992a). Finally, the proximal end of a femur has been tentatively attributed to Dryopithecus (cf. Dryopithecus). This specimen has been described as less suspensory than Hispanopithecus, with indications of a more quadrupedal form of locomotion (Moya`-Sola` et al. 2009b). If this is truly Dryopithecus, this interpretation is somewhat at odds with the interpretation of suspensory locomotion based on the humerus, but as we see very often in the fossil record, different anatomical regions evolve somewhat independently, leading to morphological mosaics that have no analogues among living taxa. Pierolapithecus catalaunicus The best-known Middle Miocene hominine genus is represented by the very nicely preserved partial skeleton of Pierolapithecus (Moya`-Sola` et al. 2004). The specimen, from northern Spain, is dated to 11.93 Ma (Casanovas-Vilar et al. 2011). The specimen includes most of a face which, though distorted, preserves nearly all the teeth and many informative facial characters. It also includes a partial postcranial skeleton, the most informative parts of which are some lumbar vertebrae, ribs, and a number of hand and foot bones. Moya`-Sola` et al. (2004) interpret Pierolapithecus as a basal or stem hominid. More recently, Alba (2012) prefers the hypothesis that Pierolapithecus is a pongine. Moya`-Sola` et al. (2004) cite the lumbar vertebrae, which preserve evidence of a hominoid-like vertebral column and by extension rib cage. This is indicated by the position of the lumbar transverse processes, placed more posteriorly in hominoids to stiffen the lower back (Ward 1993). However, the morphology of the lumbar vertebrae in Pierolapithecus is more hylobatid-like, extant hominids having even more posteriorly positioned transverse processes. Other aspects of the postcranium that clearly support the hominoid status of Pierolapithecus include ribs, indicative of a broad, anteroposteriorly compressed rib cage, robust clavicle, and a wrist morphology indicating no direct contact between the carpus at the triquetrum Page 36 of 66

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and the ulna (Moya`-Sola` et al. 2004). These features are shared with all extant hominids. Hylobatids are unique in their carpal/ulnar contact, having a large intervening articular meniscus (Lewis 1989). The homologous surface of the triquetrum in Pierolapithecus indicates a great ape and not a hylobatid configuration. The carpals in general are hominid-like in their overall morphology, including relative size, robusticity, and general pattern of the orientation of the joint surfaces. The lunate, triquetrum, and hamate in particular closely resemble small chimpanzees, but it is not clear if these are derived characters for hominines or hominids. Moya`-Sola` et al. (2004) describe the phalanges of Pierolapithecus as being relatively shorter, less curved, and with metacarpal joint surfaces facing more dorsally than in Rudapithecus and Hispanopithecus, clearly suspensory hominines, which they interpret to mean that Pierolapithecus had a palmigrade hand posture (see also Alba et al. 2010). At the same time, the attributes of the thorax and hand suggest antipronograde (suspensory) limb positions, which is somewhat contradictory. They resolve this dilemma with the suggestion that Pierolapithecus was a powerful vertical climber but not suspensory. This is similar to the suggestion made earlier regarding Sivapithecus, though the morphology of the phalanges does not in fact rule out suspension. The phalanges are curved compared with most arboreal primates and have strongly developed flexor muscle attachments, even if these are not so strongly expressed as in Hispanopithecus and Rudapithecus (Begun and Ward 2005). Deane and Begun (2008) concluded that the phalanges of Pierolapithecus were in the range of curvature seen in Hylobates, Pongo, Rudapithecus, and Hispanopithecus. Based on phalangeal curvature, Deane and Begun (2010) considered Pierolapithecus to be more suspensory than Old World monkeys and African apes but less than in Asian apes. Moya`-Sola` et al. (2004) interpret various craniodental attributes of Pierolapithecus to reflect its stem hominid status as well. The face is prognathic with an enlarged premaxilla. The zygomatic root is high, the nasal aperture broad, and the postcanine teeth have a typical hominid morphology (elongated, relatively large M1, absence of cingula, reduced premolar cusp heteromorphy, buccolingually large incisors, compressed canines). The premaxilla is expanded compared with early and exclusively Middle Miocene hominoids and appears to have an overlap posteriorly with the maxilla, as in hominids. However, according to these authors, it lacks the distinctive attributes of either the hominine of pongine clade. Some of the distinctive attributes of Pierolapithecus are clearly related to distortion. The glabella is unlikely to have been as posterior as it appears, the midface is clearly badly damaged and was not as prognathic as in Afropithecus, despite what the authors suggest, and the premaxilla is obviously displaced relative to the palatine process of the maxilla (Begun and Ward 2005). In my view, the face much more closely resembled Hispanopithecus, though it is still distinct enough to justify a separate genus. The similarities with Afropithecus are probably related to a similar pattern of distortion (see above). All in all, Pierolapithecus closely resembles Dryopithecus, known from contemporaneous localities in France and Austria, and Hispanopithecus and Rudapithecus, known from younger localities in Spain and Hungary. Based on this level of similarity, a consensus is emerging that all of these taxa belong in the tribe Dryopithecini (Begun et al. 2012; Alba 2012). Attributes of the postcrania and dentition are more primitive in Pierolapithecus and justify a separate genus from Late Miocene Hispanopithecus and Rudapithecus. There is evidence to suggest that Pierolapithecus is a stem hominine and not as Moya`-Sola` et al. (2004) conclude, a stem hominid, or as Alba (2012) concludes, a stem pongine (Begun and Ward 2005; Begun 2007, 2009; Begun et al. 2012). Details of dental morphology are strikingly similar to other dryopithecins (Dryopithecus, Rudapithecus, Hispanopithecus). Despite the unusually small M3 and elongated Page 37 of 66

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upper canine, most of the teeth could easily be mistaken for those of other dryopithecins and show features distinctive for that tribe, including relatively tall crowned and mesiodistally narrow upper incisors, compressed canines, premolars with prominent cusps separated by a broad deep basin, and molars with marginalized or peripheralized, relatively sharp cusps. The contact between the premaxilla and the maxilla appears to also have been very similar to Rudapithecus in being stepped with only a modest degree of overlap between the two (Alba 2012; Begun 2007, 2009; Begun et al. 2012). The supraorbital region, though described by Moya`-Sola` et al. (2004) as having thin supraorbital arches, actually closely resembles Rudapithecus and Hispanopithecus specimens from Spain and Hungary, with subtle tori emerging from a more prominent glabella. In my view, Pierolapithecus is close to the common ancestor of the Hominidae but already shares a common ancestor with the Homininae (Begun and Ward 2005; Begun 2009). Its postcranial morphology, however, is probably very close to that of the hominid ancestral morphotype (Fig. 2). Anoiapithecus Anoiapithecus is the third genus of Middle Miocene hominine from Hostalets de Pierola (Moya`-Sola` et al. 2009a). As noted, it was originally interpreted to be a stem hominid and more recently a stem pongine. The stem hominine attribution is largely on the basis of its short face (hence the trivial name brevirostris). The dental morphology, which is the best preserved parts of Anoiapithecus, is very similar to other dryopithecins, and without the facial portions, it would certainly be assigned to Dryopithecus. The facial portions that are preserved are quite fragmentary, and I am doubtful that a reliable reconstruction of the palate relative to the upper part of the face can be achieved. When the most complete and well-preserved parts of the Anoiapithecus specimen are considered, their similarity with Dryopithecus is undeniable. Whether or not the reconstruction provided in Moya`-Sola` et al. 2009a holds up will depend in my view on the recovery of a more completely preserved face.

Late Miocene European Hominines: The Dryopithecins 2 Hispanopithecus Hispanopithecus crusafonti (Begun 1992c) is known from a sample of isolated teeth and a palatal fragment from Can Ponsic and a well-preserved mandible from Teuleria del Firal, both in northern Spain and both dated to between 10.4 and 10 Ma (Casanovas‐Vilar et al. 2011). H. crusafonti is dentally similar to other dryopithecins but has distinctive upper central incisors, a more robust mandible lacking the distal shallowing of Dryopithecus, upper molars of nearly the same size, and a number of other subtle features of dental morphology (Begun 1992c) (Plates 15, 16, 17, and 18). Hispanopithecus laietanus (Villalta and Crusafont 1944) is known from several slightly younger sites in Spain. Dentally, it is smaller but similar to other dryopithecins and lacks the unique dental characters of H. crusafonti. It is the best-known species of the genus. Like H. crusafonti, H. laietanus has tall, relatively narrow upper central incisors, though not to the degree seen in H. crusafonti. The mandible is relatively robust. A partial cranium of H. laietanus displays numerous hominid cranial characters (broad nasal aperture base, high zygomatic roots, shallow subarcuate fossa, and probable enlarged premaxilla with maxillary overlap, although the specimen is damaged in that area). A few hominine characters are found on this specimen as well (supraorbital tori connected to glabella, frontoethmoidal sinus, inclined frontal squama, and thin enamel) (see Alba 2012 for a different interpretation). The most significant specimen of H. laietanus is a partial skeleton, an exceptional and important specimen ( Moya`-Sola` and Ko¨hler 1996). The most significant features of the postcranial skeleton of H. laietanus are the numerous and unambiguous indications of both well-developed suspensory Page 38 of 66

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Plate 15 Rudapithecus. The two crania (RUD 77, left and RUD 200, right) include the most complete brain cases of a European hominine. The RUD 200 image is a virtual reconstruction superimposed on a chimpanzee skull (Courtesy of Philipp Gunz). RUD 12 (bottom left) is a female left hemi-palate mirror imaged to make a complete palate. RUD 14 (bottom right) is juvenile male mandible

Plate 16 RUD 44 in medial view. Note the stepped subnasal fossa (blue lines between the alveolar process and the palatine process of the maxilla (yellow lines))

positional behavior and clear hominid synapomorphies. These include elongated forelimb; large hands with powerful, curved, elongated digits; comparatively short and robust hindlimb; and a hominid-like lumbar region. Other attributes interpreted to be present in this partial skeleton, such as an elongated clavicle and limb proportions approaching those of Pongo, are based on fragmentary evidence and are less reliable. The specimen has some unusual features for a hominid such as short metacarpals, but overall it is quite modern. The humerus, though fragmentary, is like that of D. fontani and unlike that of Sivapithecus. While there is universal agreement that Hispanopithecus is orthograde and suspensory, there is disagreement on the degree to which it was suspensory (Alme´cija et al. 2007; Deane and Begun 2008, 2010; Alba et al. 2010).

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Plate 17 Hispanopithecus (IPS 18000). The frontal bone in anterior view is mirror imaged from the left side. Black arrows, rudimentary supraorbital tori; white arrows, torus in lateral view; yellow arrow, frontal sinus penetrating into the interorbital space; red arrow, zygomatic portion of the frontozygomatic suture

Plate 18 Hispanopithecus reconstruction (left) and Rudapithecus in three fourth view (right)

Rudapithecus hungaricus Rudapithecus hungaricus Kretzoi 1969 was named based on the sample of hominines from Rudaba´nya, Hungary (Begun and Kordos 1993). Most researchers rejected to generic distinctiveness of Rudapithecus, preferring to include the Rudaba´nya sample in Dryopithecus brancoi (Begun and Kordos 1993), myself included. In the second half of the nineteenth century, shortly after the initial discovery and description of Dryopithecus fontani, additional fossil hominoid teeth began to turn up in Germany. These were eventually assembled to define the new species, D. brancoi (Schlosser 1901), though not before considerable taxonomic shuffling (see Begun 2002 for more historical details). D. brancoi is based on an isolated M3 which, while not the ideal type specimen, can be effectively distinguished from the other species. To help in species identification, the species diagnosis was revised by Begun and Kordos (1993) based on the excellent sample from Rudaba´nya, Hungary. This was the majority view through 2009. At that time, researchers working on the Spanish and Hungarian samples had independently come to the conclusion, as described earlier, that Dryopithecus as originally described should include only Middle Miocene more primitive European hominines, while the Late Miocene taxa traditionally attributed to Dryopithecus should be reassigned to their original nomena (Rudapithecus and Hispanopithecus). The nomenclatural history of these samples is described more fully in Begun (2009).

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Rudapithecus hungaricus is only known from Rudaba´nya (Hungary) and is dated to about 10 Ma. Six other localities in Germany, Austria, and Georgia may also contain Rudapithecus, but as the specimens are all isolated teeth, it is difficult to be certain. Rudapithecus shares all the hominid characters already described for other Late Miocene hominids, but the cranium is better preserved in this taxon than in any other and provides additional details (Table 3). Rudapithecus shares with other dryopithecins all the details of canine and postcanine tooth morphology outlined above. It shares relatively narrow and labiolingually thick upper central incisors with other dryopithecins, though not to the degree seen in H. crusafonti. Rudapithecus preserves a few details of the face and many details of the neurocranium and basicranium, with further evidence of its hominid status. The zygoma are high, prominent, and oriented anterolaterally, as in hominines, and the number and position of the zygomaticofacial foramina is variable (this character has been proposed as one that could establish the pongine affinities of Hispanopithecus, but the configuration in Rudapithecus is hominine-like (Kordos and Begun 2001)) The neurocranium is large, with a reconstructed cranial capacity in the range of extant chimpanzees (Rudapithecus is the only Late Miocene hominid for which cranial capacity reconstruction is possible from direct measurements of the brain case [in two individuals]) (Kordos and Begun 1998, 2001; Begun and Kordos 2004). Among the hominine characters preserved in the cranial sample of Rudapithecus are a relatively low and elongated neurocranium, with the inion displaced inferiorly (Table 3). The interorbital and supraorbital regions have sinuses that are largest above glabella. Glabella is prominent and continuous with small supraorbital tori separated from the frontal squama by a mild supratoral sulcus (Begun 1994a). The temporal bone, in addition to preserving evidence of a shallow subarcuate fossa (a hominid character), suggests fusion of the articular and tympanic portions and preserves details of the temporomandibular joint found only in hominines (Kordos and Begun 1997). RUD 200 (also known as RUD 197-200), the best preserved cranium of a dryopithecin, is the first to include a well-preserved neurocranial and facial skeleton in connection and shows clearly that the cranium of Dryopithecus was klinorhynch (having a ventrally deflected face), which it shares with African apes among the hominoids (Kordos and Begun 2001; Fig. 4). The nasoalveolar clivus or premaxilla is hominine like in its orientation, size, surface anatomy, and relations (Fig. 3). It is biconvex, long compared to Early Miocene Hominidea and hylobatids (proportionally equal in length to Gorilla), with a posterior pole that is elevated relative to the nasal floor, giving a stepped morphology to the subnasal fossa (Begun 1994a; Fig. 3). The resulting incisive fossa of the subnasal floor is deep and well defined, the incisive canal is short and large in caliber, and the incisive foramen on the palatal side is comparatively large. This suite of characters is found in Gorilla as well, which suggests that this is the ancestral morphology for hominines. Pan and Australopithecus share the synapomorphic condition of a more elongated but still biconvex premaxilla, which along with their spatulate upper central incisors and neurocranial morphology is among the most important morphological synapomorphies of the chimpanzee-human clade (Begun 1992c). Rudapithecus is well represented by postcrania, including a distal humerus that is hominid-like in all details related to trochlear and capitular morphology as well as having broad and shallow fossae for the processes of the radius and ulnae (see above). The ulna is robust with a strongly developed trochlear keel and a radial facet orientation that indicates forearm bones positioned for enhanced antipronograde postures (Begun 1992a). The scaphoid is Pongo-like in morphology and was not fused to the os centrale, as it is in African apes and humans (Begun et al. 2003c). The capitate is large with a complex metacarpal articular surface, as in African apes, but the head is comparatively narrow and the bone overall is elongated compared to African apes, again more like Page 41 of 66

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Table 3 Great ape and African ape craniodental character states of Rudapithecus Great ape character states Labiolingually thick incisors Compressed canines Elongated premolars and molars M1¼M2 No molar cingula Reduced premolar cusp heteromorphy High root of the zygomatic Elongated midface Broad nasal aperture below the orbits Reduced midfacial prognathism Elongated, robust premaxilla Premaxilla-palatine overlap Shallow subarcuate fossa Enlarged semicircular canals Large brain High cranial base (Begun 2004)

African ape character states Biconvex premaxilla Stepped subnasal fossa Patent incisive canals Broad, flat nasal aperture base Shallow canine fossa Supraorbital torus Inflated glabella Frontal sinus above and below nasion Projecting entoglenoid process Fused articular and tympanic temporal Broad temporal fossa Deep glenoid fossa Elongated neurocranium Moderate alveolar prognathism Klinorhynchy

the condition in Pongo and Sivapithecus. The triquetrum and pisiform provide evidence that the ulna did not contact the medial carpals in any way, an important synapomorphy of the great apes and humans. The phalanges are long, strongly curved, and marked by sharp ridges for the flexor musculature, indicative of suspensory positional behavior (Begun 1993). The femora of are short, with a large head, long neck, and extremely robust shaft, consistent with the hominoid pattern, and again especially similar to Pongo. The foot is also apelike in its broad, flat talar body and mobile but large entocuneiform and hallux. Ouranopithecus A large hominid sharing characters of Dryopithecus and Sivapithecus was first described from northern Greece and attributed to the genus Dryopithecus (to which Sivapithecus was also attributed at the time) (Bonis et al. 1975). Soon it became clear that the sample from Greece was distinct from both Sivapithecus and Dryopithecus, and the new nomen Ouranopithecus (see “▶ Potential Hominoid Ancestors for Hominidae”) was proposed (Bonis and Melentis 1977; Plate 19). Ouranopithecus is a large hominid, the approximate size of a large male chimpanzee or female gorilla, whose morphology is similar to that of other dryopithecins but with a much more robust masticatory adaptation (Begun and Kordos 1997). Ouranopithecus has a palate that is similar to other dryopithecins in the degree and pattern of overlap of the maxilla and premaxilla (Bonis and Melentis 1987; Begun and Kordos 1997). The morphology of the nasoalveolar clivus is also similar to dryopithecins and extant hominines. The nasal aperture is broad at its base, the interorbital space is broad, and the orbits are rectangular. The zygomatic roots arise relatively low and anteriorly on the maxilla, which is interpreted as a homoplasy with Early Miocene taxa, as a similar condition is also found in robust australopithecines that share with Ouranopithecus a very robust masticatory apparatus (Begun and Kordos 1997; Begun 2007). The glabella is projecting, and like Hispanopithecus and Rudapithecus, it is continuous with subtle tori above each orbit. The frontal squama is concave above glabella, as in Hispanopithecus, but this is somewhat exaggerated by Page 42 of 66

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

Plate 19 Ouranopithecus and “Ouranopithecus” turkae. Top, palatal, anterior, lateral and medial views of “Ouranopithecus” turkae (CO-205). Bottom, from left to right, RPL 128 and two views of ZIR 1

damage. Dentally, Ouranopithecus is similar to dryopithecins and other hominids in tooth proportions and overall dental morphology. It differs from dryopithecins in having hyperthick occlusal enamel, molars with broad cusps and flat basins, mesiodistally longer incisors, and relatively low-crowned male upper canines. The mandibles are also more robust than in other dryopithecins and have strongly reinforced symphyses. The female mandibles tend to be more robust (or shallower) than the male mandibles. One mandible preserves the condylar process, which is large and strongly convex anteroposteriorly. Ouranopithecus is also known from two unpublished phalanges. In many publications, summarized in Bonis and Koufos (1997), it has been argued that Ouranopithecus is a hominin (specifically related to humans), mainly on the basis of canine reduction and masticatory robusticity. However, these features occur repeatedly during hominoid evolution. Ouranopithecus is most parsimoniously interpreted as a terminal member of the dryopithecin clade, with a number of craniodental specializations related to an increase in masticatory robusticity (Begun and Kordos 1997; Begun 2001, 2002, 2007, 2009). The large jaws and teeth and hyperthick enamel, as well as microwear studies, suggest an ability to exploit hard and/or tough fruits, nuts, and other dietary resources (Kay 1981; Ungar 1996; Bonis and Koufos 1997; Kay and Ungar 1997). Graecopithecus Another taxon, Graecopithecus (Koenigswald 1972), is also known from Greece but from a much younger locality over 200 km from the Ouranopithecus localities. It is similar to Ouranopithecus, and some have suggested that the two samples belong to the same genus, which would be called Graecopithecus, since this nomen has priority (Martin and Andrews 1984). In my view, the generic distinction is warranted. Graecopithecus, known only from a poorly preserved mandible with a fragmentary M1, a much worn M2, and root fragments, is similar to Ouranopithecus in apparently having thick occlusal enamel. However, it is the overall size of female Ouranopithecus but has an M2 bigger than some male Ouranopithecus, and the M2 is actually broader than the mandibular

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corpus at the level of the M2. The symphysis is more vertical and the M1 is relatively small (Begun 2002, 2009). Graecopithecus is morphologically distinguishable from Ouranopithecus, much younger in age, and geographically distant from Ouranopithecus localities. There are two other samples of Late Miocene hominines that have affinities with Ouranopithecus. Gu¨lec¸ et al. (2007) described a new species of Ouranopithecus, O. turkae, based on a large maxilla recovered from the site of C¸orakyerler, in Central Anatolia. The site is unique for Eurasian Late Miocene apes in being an open habitat and being young in age (about 8–8.5 Ma). Only Oreopithecus in Europe and Lufengpithecus in Asia are younger. Having studied the maxilla from C¸orakyerler in detail, it is my view that it represents a new genus of hominine (Sevim et al. 2001; Begun 2009; Begun et al. 2012). It is much larger than Ouranopithecus, the maxilla fitting comfortably on the mandible of Indopithecus, and the anterior dental morphology is quite distinct. However, until more recently recovered specimens are described, I refrain from naming a new genus. The other sample of Late Miocene hominine that may be attributed to Ouranopithecus is the isolated p4 from the site of Azmaka, near Chirpan, Bulgaria (Spassov et al. 2012). The site may be as late as 7 Ma, but only one P4 is known. The specimen is clearly a hominid, and more closely resembles thickly enameled taxa, but its precise affinities remain to be determined. The greater significance of these two samples from Bulgaria and Turkey are not their taxonomic or phylogenetic affinities, but their location in geographic and temporal space. Both are much later than some have predicted for Miocene apes in Europe, and both are associated with paleoecological settings that some have said excludes the presence of apes (Bernor et al. 2004; Bernor 2007). There are many problems with the naı¨ve preconception that hominines could not have dispersed between Eurasia and Africa in the Late Miocene (see Begun et al. 2012 for a detailed critique). We now know that Late Miocene hominines lived in much drier conditions than previously supposed, and we also know that even without these adaptations, ample evidence exists for forest corridors and refugia in southeastern Europe and North Africa that could have allowed forest-adapted taxa to disperse between the two continents (Begun et al. 2012) The presence of hominines from C ¸ orakyerler and Azmaka demonstrate that it is unwise to exclude a priori an ecological association resulting from the wondrous and unpredictable interaction of natural selection, anatomy, behavior, and ecology. Paleobiology of the Dryopithecins Most dryopithecins display dental morphological characters that are very similar to extant Pan and suggest a soft fruit diet (Begun 1994a). Microwear analyses support this assessment (Kay and Ungar 1997). The dryopithecin gnathic is gracile compared to many other Late Miocene hominids (less robust mandibles, thinner occlusal enamel, smaller attachment sites for the muscles of mastication), which is both consistent with a soft fruit diet and more similar to extant African apes, Pan in particular. Postcranially, Hispanopithecus and Rudapithecus are unambiguously suspensory, but they do lack a few synapomorphies, particularly of the extremities, which characterize all extant hominids. These have to do mainly with the robusticity of the bones of the carpus and tarsus, which may be attributable to a “red queen” phenomenon, as in the case of the progressive development of shearing quotients during the course of hominoid evolution (Kay and Ungar 1997). In the fossil record of many mammals, there is evidence of a shift toward a certain adaptation (folivory, frugivory, suspension, climbing, bipedalism, etc.) that becomes increasingly refined in individual lineages descended from the common ancestor initially expressing the behavior. In order to remain competitive, the descendants must, in essence, run to stay in the same place, as increasingly efficient versions of the same adaptation appear independently (van Page 44 of 66

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Valen 1973). Rudapithecus and Hispanopithecus were arboreal, suspensory, soft fruit frugivores with a dentition similar to Pan, living in seasonal subtropical forests but probably capable of exploiting a variety of resources, possibly including meat (Kordos and Begun 2002). The exception to this general pattern among the dryopithecins is Ouranopithecus, which was a hard/tough object feeder. While the postcrania have not been described in Ouranopithecus, it has been suggested that it was probably more terrestrial than other dryopithecins, given its diet and habitat, which was more open country than any other dryopithecin (Bonis and Koufos 1994). However, a definitive answer to the question of the positional behavior of Ouranopithecus must await analysis of the phalanges.

Oreopithecus The other European Miocene hominoid discovered and described during the nineteenth century is the highly unusual Oreopithecus (Gervais 1872). Over the years, Oreopithecus has been called a pig, prosimian, monkey, and ape, the last being the attribution most researchers agree on today (Harrison and Rook 1997; Moya`-Sola` and Ko¨hler 1997; Begun 2002). Oreopithecus is younger than other Late Miocene European hominoids and is known from about 6 to 7 Ma localities in Italy. At the time, most of the Italian peninsula was separated from the rest of Europe by the sea, as is today the Italian island of Sardinia, where one Oreopithecus locality is found. In the Late Miocene, all Oreopithecus localities were insular, and the faunas associated with them are unique and difficult to compare to continental European faunas (Harrison and Rook 1997). Oreopithecus is a product of its insular environment as well and is characterized by many unique adaptations that make it difficult to understand its relations to other hominoids. In its craniodental morphology, Oreopithecus is similar to dryopithecins and African apes in having apparently thin enamel, but otherwise the morphology of the teeth is quite unique. Like other hominids, Oreopithecus has compressed canines, reduced premolar cusp heteromorphy, and reduced or absent molar cingula. However, the incisors are small and low crowned; the P4 has a primitive-looking low talonid compared to the trigonid; the postcanine dentition has tall, isolated cusps; and the lower molars have a unique occlusal morphology with a centroconid connected to the four principal cusps by a well-developed system of crests. The upper molars are also strongly “cristodont,” which makes them appear similar to the lower molars, superficially resembling the condition of upper and lower molar bilophodonty in Old World monkeys. The mandible is strongly built with some specimens being quite robust transversely and others deeper. The ramus is expansive to accommodate large temporalis and masseter muscles, which is also evidenced by the prominent temporal crests and pronounced postorbital constriction. The face is badly damaged but appears to have had a short and relatively gracile premaxilla, which is consistent with the small incisors. The brain case is also badly damaged but was clearly small, housing a much smaller brain than great apes of comparable body mass (Harrison 1989; Begun and Kordos 2004). Like Sivapithecus and non-hominids, the articular and temporal portions of the temporal bone are not fused, but like hominids the subarcuate fossae are small. The ectocranial crests are very strongly developed, while the frontal is comparatively smooth, without tori, and the postorbital constriction is marked. The most impressive aspect of Oreopithecus is its postcranium. A remarkably complete but crushed skeleton along with many other isolated postcranial elements is known from Oreopithecus. The axial skeleton (rib cage and trunk) is hominoid-like in its short lower back and broad thorax, and the pelvis is also comparatively short and broad, as in hominids. The forelimbs are very elongated compared with the hindlimbs, the glenoid fossa of the scapula is deep, and the elbow has all the typical hominoid features described previously. The femur is short and robust with a large Page 45 of 66

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head, and the knee joint indicates mobility in several planes. The hand is long but narrow, and the foot is comparatively short, though in both the hand and foot, the digits are long and curved. The carpals and tarsals are primitive hominoid-like in being transversely gracile compared to their length. They more closely resemble the carpal and tarsal bones of Proconsul than those of hominids. Oreopithecus combines primitive and derived hominoid characters that ironically make it extremely difficult to place phylogenetically, despite its relatively complete preservation. Harrison and Rook (1997) consider Oreopithecus to be a stem hominid closely related to the dryopithecins. Moya`-Sola` and Ko¨hler (1997); Moya`-Sola` et al. (1999) interpret both the dryopithecins and Oreopithecus to be stem pongines (see “▶ Defining Hominidae”), and they have also concluded that Oreopithecus was an arboreal biped with a well-developed precision grip. However, these conclusions are based in part on an erroneous reconstruction of the hand of Oreopithecus (Susman 2004 and personal observations) and a very unlikely reconstruction of the foot (Ko¨hler and Moya`-Sola` 1997 and personal observations). Rook et al. (1999) interpret CT scans of the innominate of Oreopithecus to imply a remodeling of bone consistent with bipedalism, but alternative interpretations are in my view more likely (Wunderlich et al. 1999). Overall, the overwhelming signal from the postcranium of Oreopithecus is of a suspensory arboreal adaptation. The long, curved phalanges are unambiguous indicators of suspension and incompatible with either bipedalism or a precision grip. Though some have interpreted aspects of the cranial morphology of Oreopithecus to have resulted from neoteny leading to a superficially primitive morphology (Moya`-Sola` et al. 1997; Alba et al. 2001), it is very difficult to identify heterochrony in fossil taxa (Rice 1997), and the much more straightforward interpretation is that Oreopithecus does in fact retain a number of primitive characters not found in other Late Miocene or extant hominids (Harrison 1986; Harrison and Rook 1997; Begun 2002). These include a short, gracile premaxilla, large incisive foramen, low position of the zygomatic root, small brain, a number of features of the basicranium, and several postcranial characters (gracile phalanges; transversely small carpals; short, relatively gracile tarsals; etc.). It is very unlikely that a single growth process resulting from selection for bipedalism and an omnivorous diet, as suggested by Alba et al. (2001), would have produced such a diversity of consistently primitive characters throughout the skeleton. The extraordinary morphology of the cranium and dentition of Oreopithecus are probably related to a specialized folivorous adaptation. Oreopithecus molars have the highest shearing quotients of any hominoid, which is consistent with a high-fiber diet (Kay and Ungar 1997). The exceptionally developed chewing muscles of Oreopithecus, its robust mandibles, and even the small size of its brain are all consistent with a folivorous diet requiring high-bite forces but relatively little planning or “extractive foraging” (Begun and Kordos 2004).

Late Miocene East African Hominines? At the same time that Late Miocene apes are flourishing in Eurasia, two taxa, recognized from small samples, are known from East Africa. Chororapithecus is recognized from a small number of isolated teeth from Ethiopia dated to between about 10 and 10.5 Ma (Suwa et al. 2007). They accept, based on molecular clock evidence, that the divergence of Pongo and the African apes and humans occurred at about 20 Ma, that for Gorilla at about 12 Ma, and that for Pan and humans at about 9 Ma. These divergence dates are of course the subject of much discussion. These authors cautiously assign Chororapithecus to the gorilla clade, suggesting that Chororapithecus represents Page 46 of 66

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

an early gorilla. The main line of evidence is a crest revealed by CT scans on the dentine surface of one of the molars, which the authors suggest is an indication of an adaptation to shearing, characteristic of gorillas. However, the ridge in question is only present on the dentine surface and not the surface that would have been in contact with food. Therefore, even if this dentine crest is homologous with a ridge on the teeth of gorillas, it is very doubtful that it represents an adaptation to shearing, since it could never have encountered a single fiber of food (being buried under the enamel cap). At best this crest, if found to be homologous with a crest on the enamel surface of a gorilla tooth, would be considered an exaptation and not evidence of selection for a gorilla-like mode of adaptation suggested by Suwa et al. (2007). The sample of Chororapithecus is fragmentary, and frankly, if found anywhere outside of Ethiopia, it would be considered inadequate to support any particular phylogenetic hypothesis. It is in the right place the right time, according to some scenarios, but when examined in detail, it fails to demonstrate the presence of a gorilla at 10 Ma, or even a hominine. The fragmentary nature of these specimens does not allow for a definitive assignment of Chororapithecus to a hominid clade. I would not exclude the possibility that it is a late surviving Proconsul. Another collection of fossils from East Africa is Nakalipithecus, from Kenya, dated to about 9.8 Ma (Kunimatsu et al. 2007). The sample consists of a fragmentary mandible and some isolated teeth. Sadly, the teeth in the mandible are highly worn, making it difficult to use this most complete specimen to assign this taxon to the sister clade to Ouranopithecus, as suggested by the authors. There is, however, a female upper canine that does bear a strong resemblance to Ouranopithecus (Kunimatsu et al. 2007). In my view, Nakalipithecus is more likely to be a hominine and to be related to Eurasian apes than Chororapithecus. Kunimatsu et al. (2007) suggest that Nakalipithecus, because its known range is slightly older than the known range of Ouranopithecus, might be ancestral to the Greek ape. The time difference between the two samples however is minimal by paleontological standards (9.5 vs. 9.8). Nakalipithecus represents the best connection in the Late Miocene between Europe and Africa, but there is no good evidence that Nakalipithecus is ancestral to Ouranopithecus. Given the close ages of both samples, it cannot be said which is ancestral to which. It remains true, however, that the earliest hominines are at least 12.5 Ma from Europe, so that whatever the relationship is between Nakalipithecus and Ouranopithecus, the Eurasian taxa came first.

Late Miocene Hominid Extinctions and Dispersals Hominids first appear in the Middle Miocene of Eurasia and quickly radiate, but between about 10 and 9 Ma they begin to disappear. The view presented here is that the hominids from western Eurasia are hominines, and those in the east are pongines (Begun 2004, although see above for an alternative interpretation). Descendants of each subfamily eventually disperse south of the Tropic of Cancer as other taxa become extinct in Eurasia (Begun et al. 1997, 2012; Begun 2001, 2004). This view has been supported by genetic evidence (Stewart and Disotell 1998) and criticized based on differing interpretations of the fossil record. For example, it has been noted that Africa is a more likely place for the origin of the Hominidae and the Homininae, presumably because African apes still live there and because it is said to be poorly sampled, especially in the Late Miocene. The fossils that would support this interpretation remain to be discovered. In fact, many Late Miocene localities are known from Africa, a number with paleoecological indications of forested settings (Begun 2001, 2004; Begun et al. 2012), yet no hominines have ever been identified in Africa dating between Kenyapithecus and Sahelanthropus apart from Chororapithecus and Nakalipithecus, Page 47 of 66

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which, as noted, may be hominines but are much younger than the earliest European hominines. Samburupithecus is also present in this time period, but it is even more primitive and less likely to be a hominine than Chororapithecus and Nakalipithecus. Samburupithecus retains many primitive dental and maxillary characters (Begun 2001). Isolated teeth from Ngorora have been described as having affinities primarily with the Proconsuloidea or Middle Miocene East African hominoids (e.g., Equatorius) (Hill and Ward 1988; Begun 2001; Hill 2002). Pickford and Senut (2005) have recently reported teeth from Ngorora and Lukeino described as chimpanzee and gorilla-like, but in my view, the older teeth cannot be distinguished from others with affinities to the Proconsuloidea, and the younger teeth are probably from Orrorin (see “▶ The Earliest Putative Hominids”), known from the same locality (Lukeino) (Senut et al. 2001). Most importantly, an African origin of the hominines to the exclusion of the European taxa fails to explain the widespread pattern, from Spain to Hungary, of morphology associating Eurasian apes with those from Africa. To deny a European origin of the Homininae based on the evidence to date is to evoke ad hoc hypotheses of convergence or homoplasy to explain away the documented similarities between dryopithecins and crown hominines. One can choose not to believe a hypothesis because of an a priori expectation that evidence disproving it will eventually be found (e.g., Bernor 2007), but in my view, this is not an acceptable approach to science. Hominids appear to have moved south from Eurasia in response to global climate changes that produced more seasonal conditions in Eurasia toward the end of the Miocene (Quade et al. 1989; Leakey et al. 1996; Cerling et al. 1997; Begun 2001, 2004, 2009; Fortelius et al. 2006; Agustı´ 2007; Agustı´ et al. 2003; Nargolwalla 2009) (see Begun et al. (2012) for a comprehensive review of the evidence of faunal dynamics and climate change in the Late Miocene). Much evidence exists for climate change throughout much of Eurasia in the Late Miocene, which led to the development of more seasonal conditions. This culminates in the Messinian Salinity Crisis that led to the desiccation of the Mediterranean basin at the end of the Miocene (Hsu¨ et al. 1973; Clauzon et al. 1996; Krijgsman et al. 1999). Other consequences include the development of Asian monsoons, desertification in North Africa, the early phases of Neogene polar ice cap expansion, and the expansion of North American grasslands (Garce´s et al. 1997; Hoorn et al. 2000; Zhisheng et al. 2001; Griffin 2002; Guo et al. 2002; Janis et al. 2002; Liu and Yin 2002; Wilson et al. 2002). In both Europe and Asia, subtropical forests retreat and are increasingly replaced by more open-country grasslands and steppes (Bernor et al. 1979; Bernor 1983; Fortelius et al. 1996; Cerling et al. 1997; Bonis et al. 1999; Magyar et al. 1999; Solounias et al. 1999; Fortelius and Hokkanen 2001). In some places, forests persisted and elsewhere more severe changes occurred, creating a number of refugia, some of which continued to host hominids well into the period of climatic deterioration. This is the case for the Oreopithecus localities of Tuscany and Sardinia (Harrison and Rook 1997). Other wellknown localities, such as Dorn-Du¨rkheim in Germany, retain a strongly forested character, though they lack hominoids (Franzen 1997; Franzen and Storch 1999). There is a gradient of extinctions of forest forms from west to east corresponding to the gradient of appearance of more open-country faunas from east to west (Bernor et al. 1979; Fortelius et al. 1996, 2001; Begun 2001, 2004). Between about 12 and 10 Ma, Dryopithecus disappears from localities in Europe, becoming very rare by 9.5 Ma in Spain and Germany. This wave of extinctions ends coincident with an important faunal event in Western Europe known as the mid-vallesian crisis, when a major turnover of terrestrial faunas leads to the widespread extinction of local taxa generally attributed to the development of more open conditions (Moya`-Sola` and Agustı´ 1990; Fortelius et al. 1996). The youngest specimens possibly attributable to Dryopithecus are the most easterly, currently assigned to Udabnopithecus from the 8 to 8.5 Ma locality of Udabno in Georgia (Gabunia et al. 2001). Page 48 of 66

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In the eastern Mediterranean, hominids persist to the end of this time. Ouranopithecus in Greece is mainly known from the end of the hominid presence in Europe and may be a terminal taxon of the Dryopithecus clade (Begun and Kordos 1997). In Anatolia, at the eastern edge of the faunal province that includes Greece and the eastern Mediterranean (the Greco-Iranian province (de Bonis et al. 1999)), a very large hominid resembling Ouranopithecus may be as young as 7–8 Ma in age (Sevim et al. 2001). At this time, forest taxa are increasingly replaced by more opencountry forms. This is true of virtually all mammalian orders. Among the primates, hominoids decline and cercopithecoids are on the increase (Andrews et al. 1996). Grazing ungulates and grassland or dry ecology-adapted micromammals also become more common (Fortelius et al. 1996; Agustı´ et al. 1999; de Bonis et al. 1999; Solounias et al. 1999; Agustı´ 2007). The dispersal of Late Miocene faunas between Eurasia and Africa is complex and includes both open and more forest-adapted taxa. Among the more open-country taxa, horses disperse from North America to the Old World, and modern bovids and giraffids appear to have dispersed from Europe to Africa (Dawson 1999; Made 1999; Solounias et al. 1999; Agustı´ et al. 2001). Among the more close setting mammals, hippos move from Africa to Europe, and pigs of varying ecological preferences move from Asia to Europe and Africa (Fortelius et al. 1996; Made 1999). Small carnivores (mustelids, felids, and viverrids), larger carnivores (ursids, hyaenids) porcupines, rabbits, and chalicotheres, most of which also prefer more closed settings, also disperse from Eurasia to Africa (Leakey et al. 1996; Ginsburg 1999; Heissig 1999; Made 1999; Winkler 2002). Many of these dispersals involved forest or wetter ecology taxa (hippos, some suids, primates, carnivores, rodents, and chalicotheres), which is consistent with the evidence of climate change at that time. There is ample time between 10 and 7 Ma for the dispersal of forest-adapted taxa between Eurasia and Africa before the onset of the severe dry spell that culminates in the Messinian, including evidence of forest corridors and refugia well into the Late Miocene in the Balkans and North Africa (Pickford et al. 2006; Begun et al. 2012). Taxa disperse south into Africa as conditions continue to deteriorate leading to the Messinian crisis, among them probably the ancestors of the African apes and humans. This scenario has hominid ancestors leave Africa in the Early Miocene and return as hominines in the Late Miocene, but this is precisely what seems to have occurred in several mammalian lineages, including those represented by Late Miocene African species of Orycteropus (aardvark), several small carnivores, the hippo Hexaprotodon, and possibly the proboscideans Anancus, Deinotherium, and Choerolophodon (Leakey et al. 1996; Ginsburg 1999; Heissig 1999; Made 1999; Boisserie et al. 2003; Werdelin 2003; Begun and Nargolwalla 2004).

Conclusion The Miocene epoch witnesses several adaptive radiations of hominoids and hominoid-like primates. It was indeed the golden age of the Hominoidea. Many catarrhines appear in East Africa in the Early Miocene, some of which are surely related to living hominoids. A few of the basic attributes of the Hominoidea appear at this time, including the absence of a tail, somewhat extended life history, and a hylobatid level of encephalization, and hints of powerful hand and foot grips and a propensity for more vertical climbing. Among the diversity of Early Miocene Hominidea, a group emerged that may have had an adaptation to a diet dependent on more embedded resources, leading to a dispersal into Eurasia. Once there, hominoids flourish and expand, splitting into eastern and western clades that led to extant hominids (hominines in the west and pongines in the east) and an early southern clade that becomes extinct. Early in the Late Miocene, the hominid radiation in Eurasia began to dwindle, with the earliest extinctions occurring in the west and progressing Page 49 of 66

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eastward. Hominids and many other mammals experienced extinction events at this time, and many clades of Eurasian mammals also dispersed south, probably as a result of major global climatic events. Western Eurasian hominines dispersed into Africa, leading to the evolution of the African apes and humans, and eastern pongines dispersed into Southeast Asia, leading to the appearance of the Pongo clade. Shortly after their dispersal into Africa, hominines diverged into their respective clades, probably relatively quickly. Gorillas remain the most conservative in many respects, though they achieve some of the largest body masses in any primate and specialize in their ability to exploit high-fiber keystone resources. Chimpanzees and humans diverged, possibly within a million years of the emergence of the gorilla clade, the chimp clade remaining relatively conservative and the human clade experiencing much more rapid and dramatic evolutionary changes. Human ancestors retain the imprint of their Eurasian and African ape ancestors and were very probably similar to extant African apes, particularly chimpanzees, that is, the fossil record of hominoid evolution suggests that humans evolved from a knuckle-walking, forest-dwelling soft fruit frugivore/omnivore, not a chimpanzee in the modern sense, but more chimp-like than anything else nonetheless. The details of the evolutionary events leading to the origin of the individual lineages of the Homininae remain to be worked out, a process hampered in part by a poor fossil record that, for example, includes almost no fossil relative of gorillas or chimpanzees (but see McBrearty and Jablonski 2005).

Cross-References ▶ Defining Hominidae ▶ Dental Adaptations of African Apes ▶ Estimation of Basic Life History Data of Fossil Hominoids ▶ Great Ape Social Systems ▶ Hominoid Cranial Diversity and Adaptation ▶ Postcranial and Locomotor Adaptations of Hominoids ▶ Potential Hominoid Ancestors for Hominidae ▶ Role of Environmental Stimuli in Hominid Origins ▶ The Earliest Putative Hominids ▶ The Hunting Behavior and Carnivory of Wild Chimpanzees ▶ The Origins of Bipedal Locomotion ▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments ▶ Zoogeography: Primate and Early Hominin Distribution and Migration Patterns

References Abel O (1902) Zwie neue Menschenaffen aus den Leithakalkbildungen des Wiener Beckens. S Ber Akad Wiss Wien Math Nat 1:1171–1202 Adams CG, Bayliss DD, Whittaker JE (1999) The terminal Tethyan event: a critical review of the conflicting age determinations for the disconnection of the Mediterranean from the Indian Ocean. In: Whybrow PY, Hill A (eds) Vertebrate faunas of Arabia. Yale University Press, New Haven, pp 477–484

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Rose MD (1993) Functional anatomy of the elbow and forearm in primates. In: Gebo DL (ed) Postcranial adaptation in nonhuman primates. Northern Illinois University Press, DeKalb, pp 70–95 Rose MD (1994) Quadrupedalism in some Miocene catarrhines. J Hum Evol 26:387–411 Rose MD (1997) Functional and phylogenetic features of the forelimb in Miocene hominoids. In: Begun DR, Ward CV, Rose MD (eds) Function, phylogeny and fossils: Miocene hominoid evolution and adaptations. Plenum, New York, pp 79–100 Rossie JB, MacLatchy L (2006) A new pliopithecoid genus from the early Miocene of Uganda. J Hum Evol 50(5):568–586 Rossie JB, MacLatchy L (2013) Dentognathic remains of an Afropithecus individual from Kalodirr, Kenya. J Hum Evol 65(2):199–208 Rossie JB, Simons EL, Gauld SC, Rasmussen DT (2002) Paranasal sinus anatomy of Aegyptopithecus implications for hominoid origins. Proc Natl Acad Sci USA 99:8454–8456 Ruff CB, Walker A, Teaford MF (1989) Body mass, sexual dimorphism and femoral proportions of Proconsul from Rusinga and Mfangano Islands, Kenya. J Hum Evol 18:515–536 Russon AE, Begun DR (2004) A composite of the common ancestor, and the evolution of its intelligence. In: Russon AE, Begun DR (eds) The evolution of thought: evolutionary origins of great ape intelligence. Cambridge University Press, Cambridge, pp 353–368 Schlosser M (1901) Die menschena¨hnlichen Za¨hne aus dem Bohnerz der Schwa¨bischen. Alb Zool Anz 24:261–271 Schoch RM (1986) Phylogeny reconstruction in paleontology. Van Nostrand Reinhold, New York Schwartz JH (1997) Lufengpithecus and hominoid phylogeny: problems in delineating and evaluating phylogenetically relevant characters. In: Begun DR, Ward CV, Rose MD (eds) Function, phylogeny, and fossils: Miocene hominoid evolution and adaptations. Plenum, New York, pp 363–388 Senut B, Gommery D (1997) Postcranial skeleton of Otavipithecus, Hominoidea, from the middle Miocene of Namibia. Ann Paleontol 83:267–284 Senut B, Pickford M, Gommery D, Kunimatsu Y (2000) Un nouveau genre d’hominoı¨de du Mioce`ne infe´rieur d’Afrique orientale: Ugandapithecus major (Le Gros Clark & Leakey, 1950). CR Acad Sci Paris 331:227–233 Senut B, Pickford M, Gommery D, Mein P, Cheboi K, Coppens Y (2001) First hominid from the Miocene (Lukeino formation, Kenya). CR Acad Sci Paris 332:137–144 Sevim A, Begun DR, Gu¨lec¸ E, Geraads D, Pehlevan C (2001) A new late Miocene hominid from Turkey. Am J Phys Anthropol Supl. 32:134–135 Shea BT (1988) Phylogeny and skull form in the hominoid primates. In: Schwartz J (ed) OrangUtan biology. Oxford University Press, New York, pp 233–245 Singleton M (2000) The phylogenetic affinities of Otavipithecus namibiensis. J Hum Evol 38:537–573 Solounias N, Plavcan JM, Quade J, Witmer L (1999) The paleoecology of the Pikermian Biome and the Savanna myth. In: Agusti J, Rook L, Andrews P (eds) The evolution of neogene terretrial ecosystems in Europe. Cambridge University Press, Cambridge, pp 436–453 Spassov N et al (2012) A hominid tooth from Bulgaria: the last pre-human hominid of continental Europe. J Hum Evol 62(1):138–145 Spoor CF, Sondaar PY, Hussain ST (1991) A hominoid hamate and first metacarpal from the later Miocene Nagri formation of Pakistan. J Hum Evol 21:413–424

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Stevens NJ, Seiffert ER, O’Connor PM, Roberts EM, Schmitz MD, Krause C, Gorscak E, Ngasala S, Hieronymus TL, Temu J (2013) Palaeontological evidence for an Oligocene divergence between Old World monkeys and apes. Nature 497(7451):611–614 Stewart C-B, Disotell TR (1998) Primate evolution: in and out of Africa. Curr Biol 8:582–588 Susman RL (2004) Oreopithecus bambolii: an unlikely case of hominidlike grip capability in a Miocene ape. J Hum Evol 46:105–117 Suwa G, Kono RT, Katoh S, Asfaw B, Beyene Y (2007) A new species of great ape from the late Miocene epoch in Ethiopia. Nature 448(7156):921–924 Teaford MF, Walker AC (1984) Quantitative differences in the dental microwear between primates with different diets and a comment on the presumed diet of Sivapithecus. Am J Phys Anthropol 64:191–200 Tekkaya I (1974) A new species of Tortonian anthropoids (primates, mammalia) from Anatolia. Bull Miner Res Explor Inst Turkey 83:1–11 Tutin CEG, Fernandez M (1993) Composition of the diet of chimpanzees and comparisons with that of sympatric lowland gorillas in the Lope Reserve, Gabon. Am J Primatol 30:195–211 Tutin CEG, Ham R, White LJT, Harrison MJS (1997) The primate community of the Lope´ Reserve in Gabon: diets, responses to fruit scarcity, and effects on biomass. Am J Primatol 42:1–24 Ungar PS (1996) Dental microwear of European Miocene catarrhines: evidence for diets and tooth use. J Hum Evol 31:335–366 van der Made J (1999) Intercontinental relationship Europe-Africa and the Indian subcontinent. In: Ro¨ssner GE, Heissig K (eds) The Miocene land mammals of Europe. Dr. Friedrich Pfeil, Mu¨nchen, pp 457–472 van Valen L (1973) A new evolutionary law. Evol Theory 1:1–30 Villalta JF, Crusafont M (1944) Dos nuevos antropomorfos del Mioceno espanol y su situacion dentro del la moderna sistematica de los simidos. Notas Commun Inst Geol Min 13:91–139 von Koenigswald GHR (1935) Eine fossile Sa¨ugetierfauna mit Simia aus Su¨dchina. Proc Konink Neder Akad Wetenschappen 38:872–879 von Koenigswald GHR (1949) Bemerkungen zu “Dryopithecus giganteus” Pilgrim. Eclogae Geol Helv 41:515–519 von Koenigswald GHR (1972) Ein Unterkiefer eines fossilen Hominoiden aus dem Unterplioza¨n Griechenlands. Proc Kon Nederl Akad Wet B 75:385–394 Walker A (1997) Proconsul: function and phylogeny. In: Begun DR, Ward CV, Rose MD (eds) Function, phylogeny and fossils: Miocene hominoid evolution and adaptations. Plenum, New York, pp 209–224 Walker AC, Rose M (1968) Some hominoid vertebrae from the Miocene of Uganda. Nature 217:980–981 Walker A, Teaford MF, Martin LB, Andrews P (1993) A new species of Proconsul from the early Miocene of Rusinga/Mfango Island, Kenya. J Hum Evol 25:43–56 Ward CV (1993) Torso morphology and locomotion in Proconsul nyanzae. Am J Phys Anthropol 92:291–328 Ward CV (1997a) Functional anatomy and phyletic implications of the hominoid trunk and hindlimb. In: Begun DR, Ward CV, Rose MD (eds) Function, phylogeny and fossils: Miocene hominoid evolution and adaptations. Plenum, New York, pp 101–130 Ward S (1997b) The taxonomy and phylogenetic relationships of Sivapithecus revisited. In: Begun DR, Ward CV, Rose MD (eds) Function, phylogeny and fossils: Miocene hominid origins and adaptations. Plenum, New York, pp 269–290

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Ward CV (2007) Postcranial and locomotor adaptations of hominoids. In: Henke W, Tattersall I (eds) Handbook of paleoanthropology, vol 2, Primate evolution and human origins. Springer, Berlin, pp 1011–1030 Ward S, Brown B (1986) The facial skeleton of Sivapithecus indicus. In: Swindler DR, Erwin J (eds) Comparative primate biology. Alan R. Liss, New York, pp 413–452 Ward SC, Duren DL (2002) Middle and late Miocene African hominoids. In: Hartwig W (ed) The primate fossil record. Cambridge University Press, Cambridge, pp 385–397 Ward SC, Kimbel WH (1983) Subnasal alveolar morphology and the systemic position of Sivapithecus. Am J Phys Anthropol 61:157–171 Ward SC, Pilbeam DR (1983) Maxillofacial morphology of Miocene Hominoids from Africa and Indo-Pakistan. In: Corruccini RL, Ciochon RS (eds) New interpretations of ape and human ancestry. Plenum, New York, pp 211–238 Ward CV, Walker AC, Teaford MF (1991) Proconsul did not have a tail. J Hum Evol 21:215–220 Ward S, Brown B, Hill A, Kelley J, Downs W (1999) Equatorius: a new hominoid genus from the middle Miocene of Kenya. Science 285:1382–1386 Werdelin L (2003) Mio-Pliocene carnivora from Lothagam, Kenya. In: Leakey MG, Harris JM (eds) Lothagam: the dawn of humanity in Eastern Africa. Columbia University Press, New York, pp 261–328 Wilson G, Barron J, Ashworth A, Askin R, Carter J, Curren M, Dalhuisen D, Friedmann E, Fyodorov-Davidov D, Gilichinsky D, Harper M, Harwood D, Hiemstra J, Janecek T, Licht K, Ostroumov V, Powell R, Rivkina E, Rose S, Stroeven A, Stroeven P, van der Meer J, Wizevich M (2002) The mount feather diamicton of the sirius group: an accumulation of indicators of Neogene antarctic glacial and climatic history. Palaeogeogr Palaeoclimatol Palaeoecol 182:117–131 Winkler AJ (2002) Neogene paleobiogeography and East African paleoenvironments: contributions from the Tugen Hills rodents and lagomorphs. J Hum Evol 42:237–256 Wu R (1987) A revision of the classification of the Lufeng great apes. Acta Anthropol Sin 6:81–86 Wunderlich RE, Walker A, Jungers WL (1999) Rethinking the positional repertoire of Oreopithecus. Am J Phys Anthropol 108:528 Xu Q, Lu Q, Pan Y, Zhang X, Zheng L (1978) Fossil mandible of the Lufeng Ramapithecus. Kexue Tongbao 9:544–556 Zalmout IS, Sanders WJ, Maclatchy LM, Gunnell GF, Al-Mufarreh YA, Ali MA, Nasser AA, Al-Masari AM, Al-Sobhi SA, Nadhra AO, Matari AH, Wilson JA, Gingerich PD (2010) New Oligocene primate from Saudi Arabia and the divergence of apes and Old World monkeys. Nature 466(7304):360–364 Zhisheng A, Kutzbach JE, Prell WL, Porter SC (2001) Evolution of Asian monsoons and phased uplift of the Himalaya-Tibetan plateau since late Miocene times. Nature 411:62–66

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

Index Terms: Afropithecus_16 Ankarapithecus_29–30 Ankarapithecus craniodental evidence_29 Ankarapithecus postcranial evidence_30 Anoiapithecus_38 Ape-like taxa_3 Dryopithecins 1_34–36, 38 Dryopithecins 1 Anoiapithecus_38 Dryopithecins 1 Dryopithecus fontani_35 Dryopithecins 1 nomenclatural history_34 Dryopithecins 1 Pierolapithecus catalaunicus_36 Dryopithecins 2_38, 40, 43–44 Dryopithecins 2 Graecopithecus_43 Dryopithecins 2 Hispanopithecus_38 Dryopithecins 2 paleobiology of_44 Dryopithecins 2 Rudapithecus hungaricus_40 Early hominids_22–23, 29, 34, 38, 45–46 Early hominids Ankarapithecus_29 Early hominids earliest fossil hominines_34 Early hominids fossil pongines_22 Early hominids late Miocene European hominines_38 Early hominids Miocene East African hominines_46 Early hominids Oreopithecus_45 Early hominids Sivapithecus_23 see Sivapithecus_23 Early hominoids_16, 18–19 Early hominoids Afropithecus_16

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

Early hominoids Eurasian hominoid origins_18 Early hominoids Middle Miocene thick-enameled hominoids_19 Early hominoids Morotopithecus_18 Eurasian hominoid origins_18 Fossil ape_3 Fossil pongines_22, 31, 33 Fossil pongines Indopithecus-Gigantopithecus_31 Fossil pongines Khoratpithecus_33 Fossil pongines Lufengpithecus_31 Graecopithecus_43 Hispanopithecus_38 Hominidea taxonomy_5 Indopithecus-Gigantopithecus_31 Khoratpithecus_33 Late Miocene hominid extinctions and dispersals_47 Lufengpithecus_31 Micropithecus_14 Middle Miocene thick-enameled hominoids_19 Miocene Hominidea_6–7 Miocene taxa_2 Morotopithecus_18 Nonhuman fossil hominoids_1 Nyanzapithecines_15 Oreopithecus_45 Origins of Hominidea_8 Pierolapithecus catalaunicus_36 Pliopithecoids_2 Proconsul sensu stricto_14 Proconsuloidea_9, 14–15 Proconsuloidea Micropithecus_14 Proconsuloidea Nyanzapithecines_15 Proconsuloidea Proconsul sensu stricto_14 Proconsuloidea Proconsul_9 see Proconsul_9 Proconsuloidea Samburupithecus_15 Proconsul_7, 9–11 Page 65 of 66

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_32-3 # Springer-Verlag Berlin Heidelberg 2013

Proconsul craniodental morphology_11 Proconsul hypothetical ancestral morphotype_9 Proconsul localities_9 Proconsul postcranial morphology_10 Propliopithecoids_2 Rudapithecus hungaricus_40 Saadanius_5, 7 Samburupithecus_15 Sivapithecus_23–24, 27 Sivapithecus craniodental evidence_23 Sivapithecus phylogeny and paleobiology_27 Sivapithecus postcrania_24

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_33-2 # Springer-Verlag Berlin Heidelberg 2013

The Biotic Environments of the Late Miocene Hominids Jordi Agustí* ICREA-Institute of Human Paleoecology, Universitat Rovira i Virgili, Tarragona, Spain

Abstract The habitat of the Middle and Late Miocene hominoids from western Europe, like Dryopithecus, was characterized by the prevalence of subtropical conditions. As a consequence, those environments were mainly dominated by fruit eaters and browsers, including a large variety of suids, cervids, rhinos, chalicotheres, and proboscideans. In contrast, in large parts of Eurasia, from eastern Europe (Greek-Iranian province) and northern Africa to China, the Middle Miocene climatic crisis led to the development of a xerophilous woodland, dominated by bovids, giraffids, and pursuit carnivores. At first, the worldwide dispersal of the hipparionine horses changed this scenario very little. However, at 9.6 Ma, a significant event, the Vallesian Crisis, led to the extinction of most of the fruit eaters that had prevailed in the Middle Miocene European faunas. Hominoids persisted for a time in the Tusco-Sardinian Island and in the low latitudes of southwestern Asia. The worldwide spread of grasses between 8 and 7 Ma led to the final extinction of those hominoids. Hominoid evolution continued in eastern and southeastern Africa, in a habitat that strongly resembles that of the Greek-Iranian province.

Introduction The Late Miocene, that is, the timespan between 11.6 and 5 Ma, is a crucial period in understanding the configuration of our present world. This is the time when the persisting laurophyllous evergreen woodlands (also called laurisilvas), which had spread over large parts of the Old World during most of the Miocene, were replaced by drier and more seasonal ecosystems, including savannas and steppes. It has been argued that the spread of this kind of environment may have played a key role in hominid evolution, by enhancing the appearance of new locomotor innovations, such as bipedalism (Lovejoy 1980; Coppens 1983). However, this change toward increasing dryness and seasonality was not a sudden one. Instead, this general trend appears to have been punctuated by a number of faunal and environmental events, which predated the onset of glacial-interglacial dynamics in the Northern Hemisphere. Significant physiographic and tectonic events appear also associated with this biotic turnover, such as the uplift of the Himalayas and the Tibetan Plateau, the final closure of the Atlantic-Indian seaway throughout the Mediterranean, and the desiccation of the Paratethys and Mediterranean seas. These paleogeographic events severely affected the continent-ocean interplay system, leading to changes in the overall circulation pattern, enhancement of the monsoonal dynamics, and the development of the first Arctic glacials.

*Email: [email protected] *Email: [email protected] Page 1 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_33-2 # Springer-Verlag Berlin Heidelberg 2013

The Middle Miocene Environmental Background: The World of Dryopithecus Despite the climatic crisis that affected the Early Miocene terrestrial ecosystems, the last part of the Middle Miocene was characterized by very favorable biotic conditions in parts of western Eurasia, specially in western and central Europe (Agustí and Antón 2002; Fortelius et al. 2003). The faunal associations from these regions were characterized by high mammalian diversity levels, with a high amount of large- to medium-sized browsers, together with several medium-sized carnivores. At the top of the large browser guild were the proboscideans, represented by the large gomphotheres of the genus Tetralophodon and the deinotheres of the genus Deinotherium. Tetralophodon was a late immigrant in the Middle Miocene terrestrial ecosystems and replaced the once worldwide gomphotheres of the genus Gomphotherium. Tetralophodon was a large proboscidean which had more hypsodont teeth than the earlier gomphotheres. Moreover, its skull, although still bearing four tusks, was shorter and more elephant-like, with a pair of long, straight tusks in the maxilla and a small pair of tusks at the end of the mandible. In contrast, Deinotherium represents a completely different kind of proboscidean. Members of this group had only two strong tusks, not placed in the upper jaw but at the end of the mandible. Moreover, this lower pair of tusks was recurved downward. The molars were very simple, formed of two cutting ridges, interpreted as an adaptation to browsing leaves and tough vegetation. Another main component of the large browser community was the chalicotheres, a group of bizarre perissodactyls distantly related to horses that prolonged the trend observed in other ungulates to enlarge the forelimbs relative to the hind limbs. This trend reached an extreme in some Miocene representatives, such as Chalicotherium, which developed gorilla-like limb proportions, with very long forelimbs and short hind limbs. The chalicotheres bore claws at the end of their arms, instead of the typical hoofs of the odd-toed ungulates. These enabled them to grasp small branches and leaves with the help of their forefeet. These large perissodactyls were probably capable of standing on their hind limbs and using their forelimbs as “hands” to reach the higher vegetational levels. However, the most diversified group of large browsers were the rhinoceroses, represented by several different forms, such as Brachypotherium, Hoploaceratherium, Alicornops, or Lartetotherium. Brachypotherium was a large teleoceratine with hypsodont teeth, short legs, and hippolike body proportions, which probably had a semiaquatic lifestyle. Another group was the aceratherine rhinos, represented by the genera Hoploaceratherium and Alicornops. Hoploaceratherium tetradactylum was a medium-sized acerathere with long limbs and slender body proportions. As in most aceratherines, the characteristic horns were highly reduced (only a small one was present). In contrast, they displayed very big lower incisors, which were larger in the males. Alicornops simorrense was a small acerathere with short, tridactyl legs and strongly curved lower incisors (although, as in Hoploaceratherium, a small horn was present). The rhinocerotines or “modern horned rhinos” were represented by Lartetotherium and “Dicerorhinus” steinheimensis. Lartetotherium sansaniense was a cursorial rhino that had a unique, long horn. According to its rather brachydont teeth, its diet must have contained a higher quantity of soft plants and a lower proportion of wooden parts of shrubs than in the case of the aceratherine rhinos (Heissig 1989). Represented only by the genus, Anchitherium, the equids were also significant elements of the Miocene ecosystems. Anchitherium was a member of the group of North American horses that experienced a significant evolutionary radiation during the Oligocene. This medium-sized anchitherine, about 1 m or less at the withers, crossed the Bering area in the Early Miocene and rapidly dispersed over the whole of Eurasia, from China to Spain. They bore low-crowned

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_33-2 # Springer-Verlag Berlin Heidelberg 2013

(brachydont), lophodont teeth adapted to browsing soft leaves. Their limbs were also adapted to locomotion on soft substrates, still retaining two lateral, fully functional toes. The undergrowth of the Middle Miocene laurisilva was populated by a wide array of suids, which included hyotherines (Hyotherium), peccary-like suids (Taucanamo, Albanohyus), tetraconodontines (Conohyus and its offshoot Parachleuastochoerus), and listriodontines (Listriodon). Taucanamo was a small peccary-like pig (about 12 kg), which developed lophodont teeth and large, elongated premolars. Its dental morphology, with high cusps and variable lophodonty, resembles that of some cercopithecoid primates and tragulids, being probably related to a browsing regime in a forest biome. Albanohyus was a small peccary-like suid also found at Fort Ternan that resembled Taucanamo but had smaller, shorter premolars. Listriodon was a fully lophodont, browsing listriodontine, which dispersed over the whole of Eurasia, from China to the Iberian peninsula throughout eastern and central Europe (Made 1996). Analysis of microwear in Listriodon has shown a rather uniform diet with a smaller minerogenic component, which indicates a variation from the typical rooting behavior of generalized suids and a specialization in the browsing of vegetation. Lengthening of distal limb segments might indicate that these listriodontines preferred more open habitats. Together with the listriodontines, a new subfamily of suids, the tetraconodontines, became the dominant suiforms in the circum-Mediterranean area (including five genera: Conohyus, Parachleuastochoerus, Sivachoerus, Notochoerus, and the African Nyanzachoerus). The tetraconodonts bore thick-enameled cheek teeth and conical premolars with hyena-like wear, which probably indicates a diet based on hard food items such as seeds. A trend toward reducing size is present in this group during the Middle Miocene, from the 70 kg of the medium-sized Conohyus to the 40 kg of the small Parachleuastochoerus. Later on, at the end of the Middle Miocene, the suid diversity increased again with the appearance of the first representatives of modern suids (Propotamochoerus). Propotamochoerus was a large suid (about 120 kg), which probably evolved in southern Asia from a hyotherine pig during the Middle Miocene and subsequently extended its range westward into southwestern Asia and Europe. It is the first recognizable member of all modern swines. The molars of this group show a trend toward the proliferation of several minor cusps, concomitant with loss of cusp identity. This peculiar dental evolution resembles some bears and indicates a further adaptation to omnivory. Other significant members of the medium-sized browser community were the deer or cervids, represented by a number of genera such as Heteroprox, Dicrocerus, and Euprox. According to their limb proportions and low-crowned (brachydont) dentitions, most of these archaic deer were semiaquatic browsers that lived in closed forests in humid conditions (Köhler 1993). They still displayed rather simple, two-pronged antlers, although in some cases like Euprox, there was a differentiation between a principal, posterior prong and a secondary, smaller anterior prong. Some of them, like Dicrocerus and Euprox, showed a burrlike area, indicating for the first time the border between the deciduous and permanent segments of the antlers. Besides cervids, other related taxa, such as the moschid Micromeryx and the tragulid Dorcatherium, testify to the persistence of very humid conditions in western and central Europe. Micromeryx was a very small and slender moschid of less than 5 kg that, as in the case of the living moschids, lacked horns but displayed very prominent canines (in the males). Micromeryx probably foraged in the lower vegetation of the closed forest, again living on soft plants and fruits, larvae, and carrion (Köhler 1993). It was a very successful moschid that spread over a wide area covering western and eastern Europe and that persisted until the Late Miocene (Early Turolian). Among these small browsers, other significant elements were the tragulids of the genus Dorcatherium. The tragulids or chevrotains are small ruminants that today live close to the water in the closed forests of tropical Africa and east Asia. Like the moschids, they lack any kind of cranial appendages, having in their Page 3 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_33-2 # Springer-Verlag Berlin Heidelberg 2013

turn a pair of long canines which are longer in the males. Moreover, they retain a very primitive limb structure, with four well-developed toes on each foot (the two central metapodials are not yet fused in the cannon bone). The recent relatives of Dorcatherium, the chevrotains Hyemoschus aquaticus and Tragulus meminna, live in dense tropical forests close to rivers or water courses, which act as a refuge in the case of sudden attack by predators. Dorcatherium was nearly identical in all aspects to the recent Hyemoschus and probably developed a similar lifestyle. In contrast, the bovids were poorly diversified at this time, mainly represented by Eotragus. The first bovids such as Eotragus probably originated in Asia, to the south of the Alpine belt. Later, in the Early Miocene, they colonized Europe and Africa simultaneously, their presence in this latter continent having been reported from Gebel Zelten (Libya) and also from Maboko and Ombo (East Africa). Eotragus was a small ruminant, the size of the living dik-dik or dwarf antelopes of the tribe Neotragini. The horn cores were short and conical, placed directly over the orbits. The teeth were brachydont, indicating a diet based on soft plants, fruits, larvae, insects, or even carrion. Their limb proportions were primitive, close to those of a cervid. They probably occupied a closed, wooded habitat where they probably ducked under the undergrowth (Köhler 1993). At the opposite extreme, the small herbivore guild was extensively represented by a variety of rodents, including several species of hamsters (cricetids), dormice (glirids), eomyids, squirrels (sciurids), and beavers (castorids). The laurophyllous forests at this time were populated by a variety of flying rodents, such as flying squirrels of different sizes (from the large Albanensia to the small Blackia) and, probably, the eomyids Eomyops and Keramidomys. But other groups of small rodents, such as some glirids of the genus Glirulus, also developed “flying” forms with a patagium. This is very unusual among dormice and provides a strong indication of the persistence of closed forests at that time in western and central Europe. Another indication of the persistence of humid conditions in this part of the Old World is the frequent discovery of beavers in these faunas. One of them, Chalicomys, strongly resembled in size and morphology of the recent Castor fiber and, like the living form, was probably highly dependent on permanent rivers. A second smaller beaver, Trogontherium, is widely present at this time and was probably associated with more unstable environments. Among the carnivores, the large predator guild was represented by amphicyonids and nimravids. The amphicyonids, or “bear dogs,” resembled canids in their dentition but developed ursidlike characteristics such as very large size and robust canines (with double cutting edges in the case of the upper ones). The heavy carnassials with horizontal abrasion were probably used for bone crushing, an interpretation supported by the high sagittal crests in the skull, which housed a powerful musculature probably used for breaking bones. All these adaptations suggest that the amphicyons were probably occasional scavengers, at a time when truly scavenging specialists were still absent. However, despite these scavenging adaptations, the body plan of the amphicyonids indicates active hunting. They were probably active and agile predators practicing the solitary stalk-pounce hunting mode of recent felids and bears. Their long tails were probably used to balance the pounce, as in the case of the modern felids (Viranta 1996). The Middle Miocene records the first appearance of one of the most successful amphicyonid species in the Miocene, Amphicyon major (starting from NeudorfSpalte and several localities in Spain, France, Germany, Czechia, Turkey). This was a large form, attaining the size of a lion. Amphicyon major had a long skull, with an elongated snout and relatively long and massive canines. The general limb proportions were similar to those of a bear, with short metapodials. Besides bearlike forms, like Amphicyon major, the amphicyonids also produced at this time hypercarnivorous forms such as Thaumastocyon and Agnotherium. Both were medium- to large-sized amphicyonids with a cursorial body plan that probably indicates pursuit hunting habits.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_33-2 # Springer-Verlag Berlin Heidelberg 2013

However, the typical hypercarnivorous predators of this time were the nimravids, a family of carnivores that developed felidlike, sabertooth adaptations. At the end of Middle Miocene, this family was represented by Sansanosmilus jourdani, a large species which reached 80 kg. The true felids were represented at that time by smaller species, all included in the genus Pseudaelurus: P. turnauensis, P. lorteti, and P. quadridentatus. The true ursids were represented at this time by two mesocarnivore forms, Hemicyon and Plithocyon, as well as a typical omnivore form, Ursavus. This last genus of small ursids was represented by U. primaevus of about 90 kg. The hyenids were represented by slender forms, such as Protictitherium, Plioviverrops, and Thalassictis. Different from the living members of this family, these primitive hyenids were more civetlike generalized carnivores than true scavengers. Protictitherium was an archaic insectivore/omnivore form, with very generalized dentition displaying a full set of premolars and molars. The postcranial skeleton suggests a semiarboreal existence and a diet consisting of small mammals, birds, and insects, far removed from the lifestyle of the modern hyenas. Plioviverrops was a mongoose-like insectivore/ omnivore carnivore, which shows a progressive adaptation to insectivory, as indicated by the reduction of the sectorial portion of the dentition and the increase in the number of high, puncture-crushing cusps on the cheek teeth. Its skeleton was apparently more adapted to a terrestrial lifestyle than Protictitherium. Thalassictis, represented by the species T. montadai and T. robusta, was the first member of a hyenid lineage characterized by wolflike meat- and bone-eating habits. They still retained an unspecialized dentition, in some way similar to that of canids, although with a major emphasis on bone eating. The postcranial skeleton indicates terrestrial locomotion but without special adaptations to cursoriality. Unlike Protictitherium and Plioviverrops, it indicates an adaptation to a more open woodland environment (Wenderlin and Solounias 1991, 1996). Finally, at the very end of the Middle Miocene, a number of elements of probable African origin entered Eurasia again. This was the case, for instance, for the giraffids of the genus Palaeotragus. Palaeotragus was a relatively small, slender giraffid of about 250 kg bearing a pair of parallel ossicones standing upright over the orbits. They had long legs and limb proportions resembling those of the living okapi. The structure of the foot indicates that they were probably open-country runners and, perhaps, good jumpers (Köhler 1993). They probably ate soft plants, mainly leaves, which they took hold of by grasping them with their long tongues. Besides Palaeotragus, other immigrants at the end of the Middle Miocene were the hominoid dryopithecines of the genera Pierolapithecus and Dryopithecus, which joined the previously existing pliopithecid anthropoids of the genus Pliopithecus. The coexistence of dryopithecids and pliopithecids is probably explained by the different dietary habits. While Pliopithecus and other pliopithecids were folivorous primates that settled on sclerophyllous woodlands, the dryopithecids, such as Dryopithecus, were frugivorous forms that lived in the canopy of the evergreen laurophyllous forests. In central Europe, the thinenameled dryopithecids replaced the last thick-enameled hominoids of the genus Griphopithecus, which entered this region at the beginning of the Middle Miocene.

The Greek-Iranian Province While, as we have seen, the Middle Miocene polar cooling and East Antarctic Ice growth did not imply a significant decrease in diversity in the evergreen woodland ecosystems of western and central Europe, its effects were much more severe in middle- to low-latitude terrestrial environments. There was a climatic trend toward cooler winters and decreased summer rainfall. Seasonal, summer drought-adapted sclerophyllous vegetation progressively evolved and spread geographically during the Miocene, replacing the laurophyllous evergreen forests which were adapted to Page 5 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_33-2 # Springer-Verlag Berlin Heidelberg 2013

moist, subtropical, and tropical conditions with temperate winters and abundant summer rainfalls (Axelrod 1975). These effects are clearly seen in a wide area to the south of the Paratethys realm, extending from eastern Europe to western Asia. According to Bernor (1984), this region, known as the Greek-Iranian or sub-Paratethyan province, acted as a woodland environmental “hub” for a corridor of open habitats which extended from western North Africa eastward across Arabia into Afghanistan, northwest into the eastern Mediterranean area, and northeast into north China. The Greek-Iranian province records the first evidence of open woodlands through which a number of derived, open-country large mammals, such as hyenids, thick-enameled hominoids, bovids, and giraffids, diversified and dispersed into East Africa. The mammal composition of the Greek-Iranian province was very different from that of the more wooded environments that persisted in most of western and central Europe and approached in some ways that of the recent African savannas. This is why it has often been regarded as a “savanna-mosaic” (Bernor 1984) or “protosavanna” (Harris 1993) chronofauna. But in fact, as demonstrated by several analyses, this eastern biome was closer to an open sclerophyllous woodland than to the extensive grasslands present today in parts of Africa (Eronen et al. 2009; Koufos 2006). Nevertheless, the peculiar biotope that developed in the GreekIranian province acted as the background from which the African savannas evolved during the Plio-Pleistocene (Solounias et al. 1999). They also include a number of genera common to the opencountry chronofauna, which dominated the Late Miocene Old World. This evolution has been documented in East Africa, where a similar ecosystem of seasonally adapted, sclerophyllous woodland, with terrestrial hominoids (Kenyapithecus), was present in Fort Ternan (Kenya) as early as 14 Ma, in association with the first grasslands in eastern Africa (Dugas and Retallack 1993). At the taxonomic level, this habitat change in the western European low latitudes involved the rapid adaptive radiation of woodland ruminants (bovids and giraffids). Thus, although the small Eotragus persisted and is found to have been widespread throughout Europe, western Asia, and Africa, a new group of larger bovids, the boselaphines, spread at this time, becoming the most successful elements of this family during most of the Miocene. The boselaphines, today represented by the nilgai (Boselaphus tragocamelus) from India, began a successful evolutionary radiation in the Middle Miocene, which led to a high generic diversity. Miotragocerus, the first boselaphine to appear in Europe, is found from Byelometcheskaya in the Caucasus to Tarazona in central Spain. It was a medium-sized bovid of about 80 kg with strong horn cores that looked very different from those of Eotragus. Its teeth were still primitive but with some cementum. The limb bones and foot anatomy indicate that Miotragocerus lived in very humid habitats, where it probably fed on soft plants (Köhler 1993). At that time, a second boselaphine bovid in the Greek-Iranian province, Austroportax, displayed a quite different aspect. Austroportax was a large and surprisingly advanced bovid for its time. It weighed about 300 kg and was supported by short, heavy extremities resembling those of the living buffalos and other modern members of the tribe Bovini. Its foot morphology indicates that it lived in humid and wooded habitats. A second group of successful bovids that spread at that time over southern Europe and Africa originated from a Middle Miocene Asian form called Caprotragoides. Following the Middle Miocene environmental changes, Caprotragoides spread over Europe and northern Africa throughout the Greek-Iranian province, leading to Tethytragus and Gentrytragus, respectively. They were medium-sized bovids of about 30 kg with horn cores curved backward and slightly outward. The teeth morphology indicates a diet based on a great variety of plants. Most of their characters seem to be adaptations to dwelling in open country, but others indicate more wooded preferences. This mosaic of features indicates that Caprotragoides, Tethytragus, and Gentrytragus were probably eurytopic bovids with a high capability of invading very diverse biotopes.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_33-2 # Springer-Verlag Berlin Heidelberg 2013

A third group of advanced bovids that spread at this time were the hypsodontines. Hypsodontus was a medium to large (about 110 kg) slender and specialized long-legged bovid. It differed from the Boselaphini, Eotragus, or Tethytragus in its extremely hypsodont cheek teeth, indicating a diet based on grass and tough plants. It attained a broad Old World distribution in the Middle Miocene, from China to India, eastern Europe, and Africa. A second genus related to Hypsodontus, Turcocerus, was present in Turkey at the same time. Turcocerus was a very small bovid with slender, though massive, metapodials. It bore two short conical horns showing a clockwise torsion. The teeth were also very hypsodont and with cement, indicating a diet based on leaves, herbs, and grasses. A fourth group of advanced bovids that spread in the Middle Miocene were the Antilopini, mainly represented by the gazelles. The first gazelles (Gazella) come from the Early Miocene beds of the Chinji zone of Siwaliks and from Majiwa in Kenya (Thomas 1984). According to these data, Gazella and other Antilopini could have originated in Africa or the Siwaliks from a form close to Homoiodorcas or a related Neotragini. Gazelles dispersed into Europe at this time from their possible Afro-Arabian origins, perhaps taking part in the same dispersal event as Giraffokeryx and the kubanochoerus (see below). Not only gazelles but also the giraffids experienced a wide adaptive radiation in Africa after their dispersal from Asia. One of these giraffids, Giraffokeryx, dispersed out of Africa and became widespread at this time, its remains having being found at several Middle Miocene localities of the Greek-Iranian province, such as Paçalar and Prebreza, as well as in the Bugti beds of Pakistan. Giraffokeryx displayed two pairs of rather short, unbranched ossicones. The anterior pair was situated in front of the orbits, while the second pair arose directly behind the orbits. A second giraffid, Georgiomeryx, has also been found in some Middle Miocene localities of the Greek-Iranian province, like Chios in Greece and Byelometcheskaya in the northern Caucasus. Georgiomeryx was closely related to Giraffokeryx but displayed a unique pair of flat, laterally extended ossicones over the orbits and a more archaic dentition with brachydont teeth (de Bonis et al. 1997a). In contrast with this highly diversified bovid and giraffid fauna, the cervoid representation in the open woodland areas of the Greek-Iranian province was extremely poor, almost reduced to primitive moschids of the genera Hispanomeryx and Micromeryx. Suids never attained the high diversity levels observed in western and central Europe, the ubiquitous Listriodon splendens becoming the most common element. The listriodontines evolved in a peculiar way in North Africa, leading to giant forms such as Kubanochoerus, which may have reached 800 kg in some cases. Kubanochoerus was found for the first time in the Caucasus (Byelometcheskaya) and probably derives from the African Libyochoerus (from the Early Miocene locality of Gebel Zelten). The most striking feature of these giant listriodontines was the presence in the males of an enormous horn above the orbits, which was probably used for intraspecific fighting and which indicates a unique case of territoriality in suids. While the tetraconodonts, such as Conohyus, were dominant in western Europe, a group of archaic, small-sized suids, the sanitheres, persisted and succeeded in the Greek-Iranian province by developing selenodont cheek teeth. Their molarized premolars and molars bore wrinkled enamel formed of several cuspules and ridges, well adapted to browse on sclerophyllous vegetation (de Bonis et al. 1997b). A second browsing pig was Schizochoerus, a small peccary-like suid related to Taucanamo that developed lophodont molars and short, broad premolars. This dentition resembles that of the contemporaneous advanced listriodontines and, as in that group, was probably well adapted to browsing in the vegetation of the sclerophyllous evergreen woodland, which covered most of the Greek-Iranian province at that time.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_33-2 # Springer-Verlag Berlin Heidelberg 2013

From the Asian side, members of the central Asian aceratherine hornless genus Chilotherium became the most common rhinos in the Greek-Iranian province. They were a group of grazing animals that occupied different niches and radiated into a number of (sub)genera such as Subchilotherium or Acerorhinus. Their legs were shorter than in any other aceratherine, mimicking those of the teleoceratines. A few of them were still clear browsers, like the brachydont Acerorhinus, while most of them were grass eaters (although certainly their diet included a number of nongraminean herbs). The shortening of the legs in this group can be explained by this grassbased diet. As aceratherines, they were hornless rhinos equipped with tusklike incisors probably used in fighting. Accordingly, but in contrast with the living grass-eater rhinos, the head maintained a horizontal position, so grazing was only possible after the shortening of the legs (Heissig 1989). This time also records the first appearance of the hyenids (Protictitherium) in eastern Europe and western Asia. However, this does not mean in any way that the hyena-like scavenger niche was empty at that time, since a peculiar family of carnivores, the percrocutids, occupied that place in the Greek-Iranian province. The percrocutids seem to correspond to an early feloid radiation covering the “hyena guild,” at a time when the true hyenids (Protictitherium) had not yet developed the dental and locomotory adaptations to scavenging and the bone-cracking characteristic of the later members of the family. The first percrocutids belong to the genus Percrocuta and are found in late Middle Miocene localities of western (Sansan, La Grive) and eastern Europe (Çandir, Paçalar), where they tended to coexist with the small, arboreal primitive hyenids of the genera Protictitherium and Plioviverrops. The Middle Miocene Percrocuta had not yet developed the bone-cracking adaptations which would be common in the Late Miocene members of the family (Dinocrocuta).

Southwestern Asia: The Environment of Sivapithecus In contrast with the Greek-Iranian province, conditions were very different to the south of this region. Actually, the environment in southwestern Asia seems to have remained much closer to that in western and central Europe. According to the rich mammalian record of the Siwalik sequence in the Potwar Plateau (northern Pakistan), warm tropical-subtropical forest zones persisted in this area during most of the Miocene. Therefore, the Chinji and Nagri faunas, equivalent to those of the late Middle and early Late (Vallesian) Miocene of Europe, are basically composed of a mixed assemblage of archaic carnivores, poorly diversified browsing ruminants, and woodland/bushland omnivores (Bernor 1984; Barry et al. 1985). A number of large- to medium-sized browsers are reminiscent of the Greek-Iranian province, such as the sivatherine giraffids of the genus Giraffokeryx (G. punjabiensis), the rhino Chilotherium intermedium, or the small suid Schizochoerus gandakasensis. Despite these common elements, the faunas from the Kamlial and Chinji beds are very different from those of the Greek-Iranian province (including the Middle Miocene sites of eastern Africa such as Fort Ternan), maintaining low diversity levels of bovids and giraffids. Although the species are different, the Siwalik record includes taxa that are similar to those of the coeval western and central Europe faunas: proboscideans (Deinotherium sp.), rhinoceroses (Brachypotherium permense), chalicotherids (Chalicotherium salinum), suids (Listriodon pentapotamidae, Conohyus sindiensis, Propotamochoerus hysudricus, Hippopotamodon sp.), tragulids (several species of Dorcatherium and Dorcabune), carnivores (Agnotherium and other amphicyonids, nimravids like Sansanosmilus and Barbourofelis), cricetids (Democricetodon sp., Megacricetodon sp.), flying squirrels, and shrews. As in the case of western Europe, this assemblage strongly points to a rather closed, forested environment. Particularly significant is the presence of hominoids with climbing locomotory adaptations of the genus Sivapithecus (Pilbeam et al. 1996). Page 8 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_33-2 # Springer-Verlag Berlin Heidelberg 2013

A case that is peculiar to the Siwaliks, and is not shared with western or eastern Europe, is the persistence of the anthracotherids, a family of archaic artiodactyls distantly related to the hippos. The anthracotheres were large suiforms with selenodont molars well adapted to a browsing regime. However, unlike the living suids, they still retained five digits on the forefeet and four on the hindfeet (although the lateral ones were more reduced). This was a unique combination of ruminant-like, selenodont dentition, coexisting with a generalist, pig or hippolike shape, with relatively short, stout legs and still functional lateral digits (actually, a combination very close to that of the living hippos). In the Middle to Late Miocene of Siwaliks, the anthracotherids are represented by two species of different size, Microbunodon punjabiense and Hemimeryx sp. The observed differences between the sclerophyllous woodland faunas of the Greek-Iranian province and those from the Siwaliks can probably be explained on the basis of the lower latitudinal location of the latter region and the influence of the rising Tibetan Plateau on the development of the monsoonal climatic regime (Kutzbach et al. 1993). The Potwar Plateau is flanked to the north and the west by north-south lying Sulaiman and Kirthar ranges and Baluchistan and Sind. The uplift of these encircling mountain ranges would have trapped moist Indo-Pacific monsoons of the slopes facing the Siwaliks and nourished the less seasonal environments there (Bernor 1984).

The Hipparion Dispersal Event Between 12 and 11 Ma, a drastic cold pulse led to a new growth of the Antarctic Ice Sheet and a global sea-level fall of about 140 m (Haq et al. 1987). The oceans dropped about 90 m below the present sea level, and a number of land bridges came again into existence, thus enabling faunal exchange between previously isolated terrestrial domains. As a consequence, a new corridor was reestablished between Asia and North America across what is now the Bering isthmus. The main result of the reopening of this land bridge was the quick dispersal into Eurasia of the hipparionine horses of the genus Hipparion and their relatives. The hipparionine horses arose in North America during the Middle Miocene and differed significantly from Anchitherium and other similar equids in the development of very high-crowned cheek teeth as a response to the more sclerophyllous, harder vegetation. Moreover, the tooth enamel became folded in several ridges, which were in their turn filled with dental cementum. The two persisting lateral toes in the hipparionine horses became more reduced than in Anchitherium, thus concentrating most of the body weight on the central toe. After the establishment of the Bering land bridge, the hipparionine horses quickly invaded the whole of Eurasia, from China to Iberia, their presence having been reported from hundreds of fossiliferous localities. Existing data suggest that, after their entry into Eurasia, the hipparionine horses spread very quickly across Europe, their presence having been reported at 11.1 Ma both in the Vienna and the Vallès-Penedès Basins (Garcés et al. 1997). They probably colonized first the more northern latitudes of Asia and spread later to the south and east. The dispersal of the hipparionine horses appears therefore as an Old World event and defines the lower boundary of the Vallesian Mammal Stage, the continental equivalent of the early Late Miocene in Eurasia. Hipparion primigenium, the first hipparionine species to enter Europe, was a relatively large form standing about 1.5 m at the withers (the stature of a Burchell’s zebra). Its slender axial skeleton suggests it was well adapted for leaping and springing rather than for sustained running and high speed (Bernor and Armour-Chelu 1999). This and other archaic hipparionine horses are included by some authors in the separate genus Hippotherium. Although a single taxon event, the dispersal of Hipparion dragged on other immigrants from the open woodlands of central and western Asia into the laurophyllous forests of western Europe. Page 9 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_33-2 # Springer-Verlag Berlin Heidelberg 2013

This was the case for the first European leporids of the genus Alilepus, the sivatherine giraffids of the genus Decennatherium, and the saber-toothed felids of the genus Machairodus. Among lagomorphs, the leporids (the family that includes the living hares and rabbits) had a long evolutionary history in North America since the Eocene. However, it was not until the Early Vallesian that they settled in Europe, at that time still dominated by the pikas of the genus Prolagus. Another immigrant in this time, Decennatherium, was one of the first members of the sivatherines, a lineage of large, robust giraffids which differed from the more slender Palaeotragus in the possession of not two but four ossicones, a first pair over the orbits and a second larger pair at the rear of the skull. The sivatherines became the dominant giraffids of the Late Miocene terrestrial ecosystems and persisted in Africa until the Early Pleistocene, coexisting with the first hominids. As in the case of other primitive sivatherines, such as Bramatherium and Hidaspitherium, from the Siwalik Hills in Pakistan, Decennatherium probably had an enlarged anterior pair of ossicones (or a unique fused anterior ossicone) and a less prominent posterior pair. Its limb bones were longer and more slender than the later members of this group. Another typical Early Vallesian newcomer was Machairodus, a large saber-toothed cat that coexisted with the last nimravids of the genus Sansanosmilus. Apart from the large amphicyonids, all the other Middle Miocene hypercarnivorous predators were relatively small forms of less than 100 kg, but members of the genus Machairodus were large saber-toothed cats which could attain 220 kg (the size of a lion). As in the case of nimravids, the most characteristic feature of these predators was their long, laterally compressed and flattened upper canines, which greatly surpassed the size of the lower ones. The first machairodontine cats are recorded in the Middle Miocene of the Greek-Iranian province and persisted there until the Early Vallesian (Miomachairodus pseudailuroides from Yeni-Eskihisar and Eşme-Akçaköy in Turkey). Machairodus aphanistus is the most common Late Miocene species in Eurasia, ranging from the Iberian Peninsula to North America. Its limb anatomy was very different from that of the modern cats, with forelimbs longer and more robust than the posterior limbs, a feature which enabled them to grasp and immobilize their prey (Turner and Antón 1997). It seems that, at a first glance, the entry of Machairodus, a felid filling the large predator guild previously occupied by Sansanosmilus, would have had serious consequences for these nimravids, including their final extinction by competition. However, this was not the case and both Machairodus and Sansanosmilus coexisted for more than a million years without replacement of one by the other. A similar case was found in the Greek-Iranian province, where the large nimravid Barbourofelis coexisted with Miomachairodus in the Early Vallesian beds of the Sinap Formation in Turkey. Barbourofelis was larger than Sansanosmilus, the size of a lion, and in the Late Miocene attained a very broad distribution, from North America to eastern Europe. The diversity also increased among the large browser perissodactyls such as rhinos and tapirs. From the rhino side, the most common form at that time was Aceratherium. This hornless aceratherine, close to the Middle Miocene Hoploaceratherium, was one of the most long-lasting genera of the Late Miocene, surviving until the Miocene-Pliocene boundary about 5 Ma. It was a medium-sized rhino with long limbs and a still functional fifth metacarpal. The cheek teeth were brachydont, indicating a browsing diet based on leaves and soft vegetation. Its limb proportions, close to those of the living tapirs, suggest a similar lifestyle (Heissig 1989). The males of Aceratherium incisivum bore a pair of strong tusks which enabled them to browse the dense vegetation of the Early Vallesian laurophyllous woodlands. As in other aceratherines, these tusks were much smaller in the females. In the Greek-Iranian province, other advanced rhinos of probable African origin joined Chilotherium in the Late Miocene. This was the case of Ceratotherium, the genus that includes the living white rhino. The early representatives of Ceratotherium (C. neumayri) were only partly grass eaters, but a trend is observed in this group throughout the Miocene and the Page 10 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_33-2 # Springer-Verlag Berlin Heidelberg 2013

Pliocene to develop more open-country adaptations such as large body dimensions and slightly hypsodont cheek teeth. Another group of perissodactyls that flourished at this time were the tapirs (Tapirus priscus), which reappeared in western Europe after their disappearance in the very Early Miocene. The anchitherine horses were represented by larger, more advanced species of Anchitherium which developed longer limbs and higher-crowned dentitions. These anchitherine horses persisted in central Europe until the latest Vallesian, although in some regions (Spain) they disappeared shortly after the entry of the first hipparionine horses. Among the smaller browsers, peculiar elements in Europe were the hyraxes, which are found at a number of Vallesian localities such as Can Llobateres (Vallès-Penedès, Spain), Melambes (Crete, Greece), and Eşme-Akçaköy (Turkey). Despite its small size and rabbitlike appearance, the hyraxes are archaic ungulates that today inhabit the rocky and steppe environments of central and southern Africa (although its range extends up to Lebanon). Their molars are brachydont and selenolophodont, strongly resembling those of some archaic perissodactyls. Although the living hyraxes are hare sized (about 50 cm in length), the Late Miocene European forms such as Pliohyrax reached large body dimensions, comparable to those of a tapir. The first hyraxes that settled in Europe in the Early Vallesian certainly had an African origin. Therefore, a limited exchange with northern Africa still existed in the Early Vallesian, although the possibility that hyraxes entered with the dryopithecids at the end of the Middle Miocene cannot be excluded. Among the carnivores, the large amphicyonids of the species Amphicyon major persisted. The hypercarnivorous and cursorial amphicyonids Thaumastocyon dirus and Agnotherium antiquus persisted also in the Early Vallesian. Agnotherium antiquus is a poorly known species present in several localities from western and central Europe (Pedregueras, Eppelsheim, Rudabanya) and known also from northern Africa (Bled Douarah). It was similar to the better known Middle Miocene Agnotherium grivensis but smaller in size (160 kg). Among the bears, the small omnivorous ursids of the genus Ursavus diversified into the species U. brevirhinus and U. primaevus, while the mesocarnivore Hemicyon was represented by H. goeriachensis (of about 120 kg). But the most significant event in this group was the appearance of the first large ursids of the genus Indarctos. Indarctos vireti, of about 175 kg, was the first member of a lineage of large mesocarnivore ursids, which were characteristic elements of the Late Miocene carnivore community. In the Early Vallesian, the true hyenids were still represented by the civetlike Protictitherium, the mongoose-like Plioviverrops, and the wolflike Thalassictis. At this time, Protictitherium also colonized northern Africa, being present in the Early Vallesian of Tunisia (P. punicum). The cursorial canidlike hyenid guild was enriched with new forms close to Thalassictis such as Ictitherium and Hyaenictitherium. Both may have been originated in the Greek-Iranian province or elsewhere in Asia and spread later into Europe. This time also records a high diversity of old viverrids (such as Semigenetta ripolli from Can Llobateres) and mustelids, which inherited the variety of forms present at the Middle Miocene: badgers (Sabadellictis), skunks (Promephitis, Mesomephitis), otters (Sivaonyx, Limnonyx, Lutra), wolverines, and glutton-related forms (Trochictis, Circamustela, Marcetia, Plesiogulo). Some of these glutton-related forms were relatively large sized for a mustelid, reaching 50 kg in the case of Hadrictis and Eomellivora. Therefore, despite its significant zoogeographic importance, the spread of the hipparionine horses and their cohort of Asian immigrants was a quite limited event which did not result in a significant change in the structure of the previously existing western Old World mammalian communities. Newcomers like Machairodus, Alilepus, Hipparion, or Decennatherium joined the already highly diversified western European faunas without a clear and immediate replacement of the potential Page 11 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_33-2 # Springer-Verlag Berlin Heidelberg 2013

competitors which were there occupying similar guilds. The same situation is observed in the Potwar Plateau, where no significant mammal turnover is associated with the entry of Hipparion. Only the extinction of older species, notably suids and cricetids, is recorded at the base of chron C5N (ca. 10.8–10.9 Ma), shortly before the first occurrence of this equid in the Siwaliks sequence (Barry et al. 1985; Pilbeam et al. 1996). The Early Vallesian faunas in Europe are thus characterized by the “peaceful” coexistence of a number of species which seem to have filled similar ecological guilds. This led to a sort of “climax” situation in the western European ecosystems, which reached levels of mammalian diversity unknown in any other Late Cenozoic epoch. With more than 60 mammal species, localities such as Can Ponsic and Can Llobateres 1 in Spain or Rudabanya in Hungary are good examples of these Early Vallesian “inflated” faunas. Despite the presence of new immigrants like Hipparion, Decennatherium, or Machairodus, the western European Vallesian ecosystems were composed of almost the same elements that populated the Middle Miocene subtropical forests, retaining a similar community structure. In this environmental context, the Eurasian hominoids reached an extraordinary diversity, which included the forest-adapted, suspensor Dryopithecus and Sivapithecus; the dry-adapted Ankarapithecus; and the robust, gorilla-like Graecopithecus.

The Vallesian Crisis After the high diversity levels attained in the Early Vallesian, an abrupt decline in the Vallesian mammalian faunas took place at about 9.6 Ma in what is known as the Vallesian Crisis (Agustí and Moyà- Solà 1990; Agustí et al. 2013). The Vallesian Crisis was first recognized in the VallèsPenedès Basin of Spain and involved the sudden disappearance of most of the humid elements that characterized the Middle Miocene and Early Vallesian faunas from western Europe. Among the large mammals, this crisis particularly affected several groups of perissodactyls such as the rhinoceroses Lartetotherium sansaniense and “Dicerorhinus” steinheimensis and the tapirs (only the small tapirs of the badly known Tapiriscus pannonicus persisted until the Early Turolian in central Europe; Franzen and Storch 1999). These losses were only partly compensated by the entry just before the onset of the Vallesian Crisis of Dihoplus schleiermacheri, a large species of browsing rhino which bore a pair of massive horns and was the largest rhino of its time. Among the artiodactyls, the high diversity attained by the suids in the Early Vallesian times suddenly dropped and several characteristic elements vanished. This was the case for the browsers Listriodon and Schizochoerus (which made a short-lived incursion in western Europe at the beginning of the Late Vallesian), as well as for the tetraconodontines Conohyus and Parachleuastochoerus. In contrast, the “modern” suinae, such as Propotamochoerus, persisted and even enlarged their diversity with a new eastern immigrant Microstonyx. Microstonyx was a giant pig (about 300 kg), with a skull more than half a meter long. The Vallesian Crisis also involved the final decline of the Middle Miocene forest community of cervoids (the cervid Amphiprox and the moschid Hispanomeryx) and the spread of the boselaphine bovids like Tragoportax, which replaced their semiaquatic relatives of the genus Protragocerus. Tragoportax was a medium-sized bovid of about 80 kg with relatively long limbs, which suggests that it was a fast runner and a good jumper which lived in the open woodland. It possessed a short-faced skull with a long neurocranium and large backwardly curved horns. The teeth were high crowned and with cementum, resembling those of the living Boselaphus (Köhler 1993).

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_33-2 # Springer-Verlag Berlin Heidelberg 2013

Among the rodents, the Vallesian Crisis involved the disappearance of most of the cricetids and glirids of Early or Middle Miocene origin (Megacricetodon, Eumyarion, Bransatoglis, Myoglis, Paraglirulus, Eomuscardinus), flying squirrels (Albanensia, Miopetaurista), and beavers (Chalicomys, Euroxenomys). However, other less diversified small mammal groups, such as lagomorphs and insectivores, remained almost unaffected by this crisis. In western and central Europe, this event coincided with the first dispersal of the murid rodents, the family that includes the living mice and rats. After their entry into Europe, this group became the dominant rodents in the Late Miocene communities and diversified into a number of genera: Progonomys, Occitanomys, Huerzelerimys, and Parapodemus. Another group which was severely affected by the Vallesian Crisis was the large carnivores of the families Nimravidae and Amphicyonidae. Among the amphicyonids, all the genera and species still existing in the Early Vallesian disappeared: Pseudarctos bavaricus, Amphicyon major, and Thaumastocyon dirus. Only some poorly known Amphicyon representatives persisted in the Late Vallesian and Early Turolian in some parts of central Europe. Among the ursids, the Vallesian Crisis had an ambivalent effect. While the slender cursorial forms of Early Miocene origin like Hemicyon vanished, the robust ursids of “modern” aspect persisted, represented by larger species. This was the case with Indarctos, represented by the species I. vireti and I. arctoides, as well as Ursavus represented by U. depereti, the largest species of the genus. In turn, the mustelids were severely affected by the Vallesian Crisis, which involved a significant decrease in the once highly diversified Vallesian fauna. At the same time, a number of eastern immigrants appeared for the first time such as the large hyenids of the genus Adcrocuta and Hyaenictis. These genera represent two opposite trends in the evolution of Late Miocene hyenids. Hyaenictis was a cursorial meat and bone eater, which prolonged the trend initiated by Thalassictis toward increasing cursoriality. They show also a trend toward the reduction of the bone-crushing portion of their dentition, developing and extending at the same time the sectorial part, so that the posterior molars were reduced or lost. At the other end of the scale, Adcrocuta, at about 70 kg, was the first representative of the modern bonecracker hyenids leading to the living Crocuta and Parahyaena. They were characterized by advanced adaptation to bone crushing, with enlarged bone-cracking premolars. Adcrocuta had short stocky limbs, indicating that it was not a cursorial form. Like Hyaenictis, it was of probable Asian origin. Among the large predator guild, the nimravids finally came to an end with the Vallesian Crisis, after representing the “large cat” guild for millions of years. Their extinction was compensated with the entry of Promegantereon, a new genus of machairodontine cats. Promegantereon ogygia, the oldest species of this genus, was smaller and more slender than Machairodus aphanistus (about 44 kg), retaining the archaic anatomy inherited from its ancestor Pseudaelurus quadridentatus. With their robust forelimbs and slender hind limbs, the members of this species were probably able to climb trees, carrying large prey as do living leopards. Their long muzzled skull was also superficially leopard-like, although, as a true machairodont, their upper canines were characteristically long and laterally flattened (Turner and Antón 1997). Last but not least, the Vallesian Crisis led to an abrupt end of the hominoid experiment in Europe. Hominoids like Dryopithecus, Ankarapithecus, or Graecopithecus disappeared entirely from the fossil record, and only Oreopithecus in its island refuge and Sivapithecus in southwestern Asia survived this extinction event (see the next sections). Dryopithecus is still found in some early Late Vallesian localities dated at about 9.6 Ma (Can Llobateres 2, Viladecavalls) but disappeared from the fossil record shortly after. In the Greek-Iranian province, the robust Graecopithecus also disappeared at the beginning of the Late Vallesian. A similar case was that of the Turkish Page 13 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_33-2 # Springer-Verlag Berlin Heidelberg 2013

Ankarapithecus, its record ending again in the Late Vallesian. The extinction of these robust hominoids in this province coincides with the spread of the colobine monkeys of the genus Mesopithecus. This was not the case in western Europe, where the extinction of the slender dryopithecines did not involve its replacement by any other kind of primate species. Only the persistence until the latest Vallesian of the advanced folivorous pliopithecids of the genus Anapithecus can be quoted in this area, some hundred thousand years after the last Dryopithecus. In China, the pliopithecids survived even longer, until the latest Miocene, being represented by a large-sized form (Laccopithecus).

Causes of the Vallesian Crisis What could have caused the set of extinctions and deep faunal restructuring which took place at 9.6 Ma during the Vallesian Crisis? Some evidence, such as the exit of several forest forms and the development of sigmodont teeth by some groups of rodents, would support the replacement at that time of the laurophyllous forests by grasslands. However, the spread of grasses over large extensions of Eurasia has been dated by Cerling and coworkers to between 8.3 and 7 Ma, and geochemical analyses carried out on teeth and soil nodules older than that timespan do not detect any sign of such an environmental change. Nevertheless, the fact that this major ecological restructuring of the western European mammal assemblages affected especially those taxa with tropical forest affinities, and the latitudinal character of these extinctions (a number of forest-adapted taxa survived until the Early Turolian in central Europe), strongly suggests its climatic forcing. This is supported by the Late Miocene oceanic evolution, which was a continuation of the processes started at the MiddleLate Miocene transition. Enhancement of the latitudinal thermal gradient resulted in the generation of new erosive oceanic surfaces (NH5) by intensification of the deep circulation. Further cooling resulted in new d18O-positive shifts (i.e., Mi6 and Mi7; Miller et al. 1987, 1991). Changes in benthic and planktonic assemblages also indicate colder climatic conditions and increasing isolation between low and middle latitudes. All these oceanic changes were nearly synchronous with some significant changes in low-latitude Old World terrestrial domains. In particular, there is a noticeable synchronism between the Mi7 isotopic shift at 9.3–9.6 Ma and the age of 9.6 Ma obtained for the Vallesian Crisis in the Vallès-Penedès stratigraphic sections. The Vallesian Crisis is also close to the beginning of the NH5 hiatus, one of the most important sets of deep oceanic discontinuities recognized in the Late Miocene (Keller and Barron 1983), which is dated between 9.0 and 9.5 Ma. NH5 has been also related to a period of cooling and major restructuring of the deep oceanic circulation and to the growth of ice sheets in western Antarctica (Keller and Barron 1983). But how did these changes affect the composition of the terrestrial vegetation? A change to more open environments did not start until 8 Ma, the extension of grasslands taking place almost 2 Myr after the Vallesian Crisis. The pre-Vallesian floras in the region indicated the persistence of humid subtropical conditions, with abundance of broad-leaved mega-mesotherm elements such as Ailanthus, Caesalpinia, Cassia, Cinnamomum, Ficus, Sapindus, etc. (Sanz de Siria 1994). Indeed, the very rich mammal locality of Can Llobateres 1 yielded remains of some of these subtropical elements such as Sabal, Ficus, and others. However, we know that the laurophyllous subtropical woodland prevailing until the beginning of the Late Miocene in Europe was profoundly affected in some way. The answer arrived in 1994, when for the first time a well-calibrated Late Vallesian flora was discovered in a section close to the city of Terrassa in the Vallès-Penedès Basin (Sanz de Siria 1997). This flora has been dated by paleomagnetism at somewhat more than 9 Ma and therefore records the kind of vegetation that was dominant just after the Vallesian Crisis (Agustí et al. 2003). The flora from the Terrassa section includes 36 different taxa from the families Lauraceae, Ulmaceae, Hamamelidaceae, Juglandaceae, Myricaceae, Fagaceae, Betulaceae, Tiliaceae, Page 14 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_33-2 # Springer-Verlag Berlin Heidelberg 2013

Salicaceae, Ericaceae, Sapotaceae, Myrsinaceae, Celastraceae, Aquifoliaceae, Rhamnaceae, Sapindaceae, Aceraceae, Oleaceae, Poaceae, and Typhaceae. Close to 45 % of this flora is composed of deciduous trees such as Acer, Alnus, Fraxinus, Carya, Juglans, Populus, Parrotia, Zelkova, Ulmus, or Tilia, that is, the elements that are now dominant in the temperate forests of the middle latitudes. In contrast, warm evergreen elements, represented by Myrsine, Sapindus, Sapotacites, etc., decreased to 7 %. Supporting the argument that this change was not related to the extension of grasslands was the persistence of a “hard core” of subtropical elements, represented by 33 % of evergreen trees, able to endure a certain level of seasonality, and which persisted in Europe until the Early Pliocene (Laurophyllum, Laurus, Rhamnus, Daphnogene, and others). The existence at that time of a dry season (summer drought) is confirmed by the presence at Terrassa of a 15 % of Mediterranean or pre-Mediterranean taxa (Quercus cf. ilex, Q. praecursor). From a physiognomic point of view, 56.4 % of the species display leaves with entire margins, while the remainder present dentate or serrated margins. Regarding leaf size, most of the taxa are microphyllous (83.3 %) or nanophyllous (10 %). According to these data, the Terrassa association is comparable to floras that are found today in parts of central-east China, south Japan, eastern North America, and North Africa, where a similar mixture of evergreen broad-leaved, warm-temperature, and deciduous elements is present (Wang 1961; Barbero et al. 1982; Richardson 1990; Barbour and Chistensen 1993). In these regions, similar mega-mesotherm taxa (Lauraceae, Myrsine, Sapotacites, Sapindus, and others) are concentrated in the lower levels of vegetation, with mean annual temperatures between 16  C and 19  C and mean annual precipitation levels above 1,000 mm. A clear winter season is already present at this stage. In some areas, drier, sclerophyllous elements (Q. ilex, Rhamnus, Rhus) coexist with the former ones. An evergreen broad-leaved forest is present at a medium stage because of the concentration of humidity due to the marine influence (Cinnamomum, Persea, Laurus, etc.). At higher altitudes a deciduous broad-leaved forest (including most of the temperate, deciduous elements like Acer, Fraxinus, Juglans, Populus, Quercus, Tilia, Zelkova, and others) is dominant. Mean annual temperatures at this stage decreased to around 12  C. Therefore, a similar zonation probably developed in the transition from the Early to the Late Vallesian, causing a significant decrease of Middle Miocene evergreen elements (33 %) and the expansion of a deciduous broad-leaved forest at a medium stage (45 % of deciduous elements), where intake of fruit during the winter season must have been much more difficult. The flora from Terrassa suggests that the deep faunal change at 9.6 Ma was not the consequence of the replacement of the subtropical Miocene forest by grasslands but rather the substitution of one kind of woodland by another. The intensification of the thermal gradients between the middle and low latitudes, probably enhanced by the Himalayan and Tibetan uplifts, led to an abrupt change in the previously existing evergreen subtropical woodlands of western Europe. These were probably replaced by an association in which more seasonally adapted, deciduous trees were dominant. Rather than the moderate cooling associated with the Mi7 isotopic shift, it was this change in the structure of the vegetation which determined the set of extinctions that took place during the Vallesian Crisis. Most members of this fauna, including Dryopithecus and other European hominoids, were mainly frugivorous, with a diet based on fruits and the soft vegetables common in the evergreen broadleaved forests of the Early and Middle Miocene. Therefore, although the decrease in temperature and increasing latitudinal gradient had little direct effect on the Vallesian mammals, the replacement of most of the evergreen trees by deciduous ones, well adapted to the new conditions of seasonality with colder winters and dryer summers, had much more dramatic effects. In this way, a number of elements, such as certain pigs, rodents, and primates, had to subsist during several months without Page 15 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_33-2 # Springer-Verlag Berlin Heidelberg 2013

fruit, a basic and highly nutritional component of their diet. This dietary factor, and not the extension of grasslands or the shift of temperature, was probably the direct agent that caused the abrupt drop of the rich Early Vallesian faunas. In turn, the sudden disappearance of most of the medium-sized herbivores that had lived in Europe for millions of years probably led to a critical situation for the old predators of Middle Miocene origin, such as the nimravids and the amphicyonids, which until the Early Vallesian had successfully endured the competition from the machairodont cats and the large ursids. These carnivores were also indirect victims of the vegetation change that took place 9.6 Ma. An interesting element is that, contrary to Dryopithecus, the crouzeline pliopithecid Egarapithecus survived the Vallesian Crisis, a fact that is probably related to a folivorous rather than frugivorous diet.

Asian Survivors The general absence of long sections of Vallesian age makes difficult the recognition of the Vallesian Crisis in other Old World regions, although there exist significant exceptions. In the well-calibrated succession of the Potwar Plateau in central Asia, a significant decay in the relative abundance of tragulids (from 45 % to 10 % of ruminant artiodactyls; Barry et al. 1991) is observed between 9.8 and 9.3 Ma, while the bovids became the dominant artiodactyls in the area (from 45 % to 80 %; Barry et al. 1991). However, the changes operating at 9.6 Ma in the region of the Siwaliks can hardly be compared with the dramatic effects of the Vallesian Crisis in western Europe. In contrast with Europe, the mammal faunal association linked to the existence of warm tropical-subtropical forested zones persisted in Siwaliks until chron 4r, at 8.3 Ma. It still included archaic carnivores and rhinoceroses (Brachypotherium), proboscideans (Deinotherium), dormice, shrews, and hominoids with climbing adaptations (Sivapithecus). As we have seen, the persistence of this kind of fauna in the Late Miocene of the Siwaliks can probably be explained by the settling of monsoon atmospheric dynamics in the latter region, which could have maintained the forested subtropical conditions there until 8.3 Ma. However, between 8.3 and 7.8 Ma, a set of extinctions similar to those of the earlier Vallesian Crisis took place (Pilbeam et al. 1996). Several cricetid, bovid, and tragulid species disappeared, and the hominoid Sivapithecus was replaced by colobine monkeys. These faunal changes coincide in the southwestern central Asian region with a shift in the d13C isotopic composition of the paleosoil and dental carbonates, indicating a climatically forced change from a forest and woodland vegetation in which C3 plants (trees and bushes) were dominant to grasslands dominated by grasses and other C4 plants (Quade et al. 1989; Morgan et al. 1994; Cerling et al. 1997). They were also largely coeval to further oceanic cooling (White et al. 1997), development of extensive oceanic erosive surfaces (NH6) and development of ice sheets in the Arctic (Eyles 1996). Therefore, the change from C3- to C4-dominant vegetation had dramatic effects to the south of the Himalayas and led to the development of an open woodland also in southwestern Asia. However, Dryopithecus may have subsisted for more time in some refuges of western Eurasia. One of these refuges seems to have been the southern Caucasus, where the presence of a slender dryopithecine (Udabnopithecus garedziensis, actually a small form of Dryopithecus) was reported a long time ago in the Early Turolian beds of Udabno (Georgia; Gabunia et al. 2001). According to its mammalian association, the age of the Udabno levels is close to 8.5 Ma. It means that Dryopithecus or another genus of thin-enameled hominoids persisted in the Black Sea region when this kind of primates went extinct elsewhere in Europe. The persistence of the evergreen Page 16 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_33-2 # Springer-Verlag Berlin Heidelberg 2013

subtropical forests to the south of the Caucasus, linked to the retention of special climatic conditions, probably enabled Udabnopithecus to survive in this region. In Asia, the dryopithecines may have survived for longer in the Late Miocene, as suggested by the presence of Lufengpithecus in the Late Miocene of Chiang Muang, in Thailand (Chaimanee et al. 2003; Pickford et al. 2004), and Keiyuan and Lufeng in China (Zhang Xingyong 1987; Harrison et al. 2002). Chiang Muang presents a typical pre-Hipparion fauna with gomphotherids (Tetralophodon cf. xiaolongtanensis), rhinos (Chirotherium intermedium), peccaries (Pecarichoerus sminthos), large suids (Hippopotamodon cf. hyotherioides), tetraconodontine suids (Conohyus sindiensis, Parachleuastochoerus sinensis), and tragulids (Dorcatherium sp.) in a wooded context that resembles that of the late Middle Miocene of western Europe and Siwaliks. Similar in age and environment is the locality of Keiyuan, in China, which presents the same kind of hominoid (Lufengpithecus keiyuanensis). Lufengpithecus is still present in type locality of the genus, Lufeng, a site dated in 8 Ma (equivalent, therefore, to the Early Turolian levels of Europe).

The Oreopithecus Fauna: Survivors in an Island Environment Even more significant was the case of Oreopithecus, an enigmatic hominoid which lived in the Tuscany area (northern Italy) from 9 to 7 Ma. At the time when Oreopithecus occupied the Tuscany region, Italy had a very different aspect from today. The territories which form the present Italian peninsula were in the Early Turolian an arch of isolated islands which extended from central Europe to northern Africa. One of these islands, close to the European mainland, was formed by Tuscany and the Corso-Sardinian block. A number of European immigrants settled in this area at some time between the Vallesian and the Turolian and persisted there until the end of the Miocene. The Oreopithecus faunas appear in several localities from Tuscany, like Casteani, Montebamboli, Ribolla, Montemassi, and also Fiume Santo in Sardinia. However, the best sequence is recorded in the Bacinello Basin, again in Tuscany, where a succession of fossiliferous levels has been recorded (Rook et al. 1999). The lowermost ones, called V 0 and V 1, are Early Turolian in age and still include some “common,” nonendemic elements like the cricetid Kowalskia and the murids Huerzelerimys and Parapodemus. However, most of the Oreopithecus faunas of the Baccinello levels V 1 and V 2 are basically composed of endemic elements. These faunas appear as a sort of impoverished, “miniaturized” Vallesian ecosystem. Thus, although already modified by the new insular conditions, most of the large mammalian components of this Late Miocene immigration wave can be referred to common elements of the Late Vallesian or Early Turolian European ecosystems, such as hypsodont bovids (Thyrrenotragus, Maremmia), giraffids (Umbrotherium), Microstonyx-like suinae (Eumaiochoerus), dryopithecids (Oreopithecus), or Indarctos-like ursids. Umbrotherium is a poorly known giraffid, probably related to a sivatherine stock. Thyrrenotragus and Maremmia were small bovids with very hypsodont dentitions. Both forms were once interpreted as African immigrants in the area: Tyrrhenotragus as a neotragine (the tribe that includes dwarf antelopes and gazelles) and Maremmia as a precocious alcelaphine (the tribe that includes the African gnus, hartebeests, and impalas). However, some of the features that relate them to these African groups, like the short metapodials of Thyrrenotragus and the probably ever-growing incisors of Maremmia, could have developed independently as specializations linked to an island environment. A small suid, Eumaiochoerus, is also present in the lignites of Bacinello (V 2) and in Montebamboli. It bore a short snout, elongated spatulate upper incisors and small-sized, chisel-shaped lower

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tusks. Despite these dental specializations and its small size, other features closely relate this endemic suid to the large Microstonyx major. However, other elements in the Baccinello succession suggest that a previous Middle Miocene faunal background already existed on the Tusco-Sardinian Island before the Late Miocene settlement of Oreopithecus and its allies. This is the case, for instance, of Anthracoglis, a dormouse close to the Middle Miocene Microdyromys and Bransatoglis but significantly larger. A second unnamed giant dormouse is scarcely present in the level V 1 of Baccinello. Besides these endemic dormice, a third small mammal, the lagomorph Paludotona, is present in the V 1 level. Paludotona was an ochotonid whose body dimensions were again larger than those of its coeval relatives in Europe. The most striking feature of Paludotona is its archaic dental morphology, which relates it to some Early to Middle Miocene ochotonids like Lagopsis. But the last Lagopsis disappeared from Europe in the Middle Miocene, some million years before the deposition of the Bacinello lignites! It seems therefore that at the time of deposition of the V 1 level, there was a long history of isolation on the Tusco-Sardinian Island. The existence of a previous Early to Middle Miocene settlement of the Tusco-Sardinian Archipelago is also supported by the presence in Casteani (equivalent to level V 1 of Bacinello) of an anthracothere. The Tuscan anthracothere is a very archaic one which clearly differs from the advanced Late Miocene anthracotherids of northern Africa. Since the last anthracotheres disappeared from Europe in the Early Miocene, its presence in this area can only be explained as a result of an immigration event from Africa or by assuming its persistence as an Early Miocene relict as in the case of Anthracoglis and Paludotona. The environment in which the Oreopithecus fauna developed was a mixed mesophytic forest, similar to those that today are found in east central China along the Yangtze River. Thus, tropicalsubtropical trees, like Engelhardia, and warm-temperate trees and shrubs, like Taxodium, Myrica, etc., are well represented in the pollen analysis of the levels V 0 and V 1 of Bacinello, while more temperate and Mediterranean elements, such as Quercus, Carpinus, Tilia, Carya, Pterocarya, etc., are rare (Harrison and Harrison 1989; Benvenuti et al. 1994). The pollen analysis developed in the level V 2 shows an increase in temperate, cold-temperate, and mountain elements such as Picea and Abies (Benvenuti et al. 1994). However, a cold phase cannot clearly be recognized due to the scarcity of grains of elements such as Tsuga or Cedrus. The increase of temperate and cold-temperate trees in the level V 2 of Baccinello may be the result of a change in the climatic conditions (as in the case of the Late Vallesian floras) but could also be associated with the uplift of the Tuscan area. The Tusco-Sardinian experiment came finally to an abrupt end when a connection to the continent was established at about 6.5 Ma. New herds of European immigrants entered the Tusco-Sardinian area, including such large predators as Machairodus and Metailurus. Not surprisingly, Oreopithecus and the other endemic elements of the Tuscan fauna underwent a rapid extinction, unable to resist the competition of the continental newcomers. This change in the faunal composition is also paralleled by a vegetation change. Therefore, the pollen analysis developed in the V 3 unit of Bacinello shows an increase in herbs (Chenopodiaceae, Compositae, Dipsacaceae, etc.) and sclerophyllous trees (Pinus t. haploxylon, Cathaya; Benvenuti et al. 1994). The Oreopithecus experiment came to an end, and the Tusco-Sardinian biome finally followed the general trend toward more open and dry environments that was dominant in the whole of Eurasia.

The Late Miocene African Record As in other parts of the Old World, the beginning of the Late Miocene in Africa is characterized by the dispersal of the first hipparionine horses on this continent. As happened in Europe, the entry of Page 18 of 26

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these hipparionine horses at the beginning of the Sugutan (an African equivalent of the Eurasian Vallesian) did not involve a significant restructuring of the existing terrestrial ecosystems. Most of the elements which composed these ecosystems at the beginning of the Late Miocene in Africa were close relatives of similar taxa in western Eurasia. Faunas of this age, such as those of the Ngorora Formation (Tugen Hills, Kenya; Hill et al. 1985), Narumungule Formation (Samburu Hills, Kenya; Nakaya 1994), or Chorora Formation (Ethiopia; Geraads et al. 2002), are based on a mixture of Middle Miocene African survivors associated with several elements that are common to the Siwaliks and Greek-Iranian provinces. Large browsers include proboscideans (Choerolophodon, Tetralophodon, Deinotherium cf. bozasi), rhinos (Chilotheridium, Paradiceros, Brachypotherium), chalicotheres (Ancylotherium), hipparionine horses (Hippotherium primigenium), and a variety of ruminants of western Eurasian affinities (Palaeotragus, Samotherium, Protagocerus, Miotragocerus, Palaeoreas/Sivoreas, Homiodorcas, Ouzoceros, Pseudotragus, Pachytragus, Gazella). The persistence of forest conditions is indicated by the presence of tragulids (Dorcatherium pigotti) and gliding rodents (Paranomalurus). However, the presence of an iranotherine rhino (Kenyatherium) at Narumungule suggests the existence of more open conditions close to the woodlands. Typical African components of these faunas are the climacoceratid giraffoids (Climacoceras), listriodontine, and tetraconodontine suids (Lopholistriodon and Nyanzachoerus), and archaic hippos (Kenyapotamus coryndoni). As happened at the beginning of the Vallesian in Europe, the dispersal of the hipparionine horses involved other Asian elements, such as the saber-toothed machairodontine cats and the “false hyenas” of the genus Percrocuta. These elements joined other persisting Middle Miocene carnivores of Eurasian origin, such as the hypercarnivore amphicyonid Agnotherium and the ratel-like mustelid Eomellivora. The persistence of forest conditions in this part of Africa is probably explained on the same basis as in southwestern Asia, that is, as a consequence of the monsoonal dynamics in this region. However, as happened in Siwaliks, a dramatic change is observed between 8 and 7 Ma in the mammalian communities of East Africa. At this time, there is a significant faunal turnover, involving the replacement of close to 75 % of the mammal species. Most of the old Middle Miocene holdovers are replaced by close relatives of the elements found today on the modern savannas. Therefore, this time records the first occurrence in Africa of leporids, hominids, new and extant viverrids, extant hienids, new felids, extant and diverse elephantids, new hippopotamids, extant giraffids, and several extant bovids. The former small- to medium-sized browser-based faunas are replaced by a new assemblage in which medium- to large-sized grazers, large browsers, and pursuit carnivores are dominant (Harris 1993). This change parallels in many ways the one observed at the same time in the Siwaliks, when the former woodland biome opened and C4 grasslands expanded over large parts of western Eurasia. Similarly, the period between 8 and 7 Ma records the expansion of the true savannas in the African continent, leading to the kind of open woodland and grasslands that are present in most of eastern and southern Africa. This is best exemplified by such latest Miocene faunas (Kerian) as Lothagam and Lukeino in Kenya or those of the Adu-Asa and the Sagantole Formations in Ethiopia. At Lothagam, recovery of more than 2,000 identifiable remains has produced a faunal list of more than 30 mammalian species (Leakey and Harris 2003). A number of new browsers replaced the medium-sized community of Middle Miocene origin, largely based on climacoceratid giraffoids and tragulids. Among them we find modern suids of the genera Potamochoerus and Phacochoerus, the peccary-like Cainochoerus, the tragelaphine antelope Tragelaphus, the black rhino Diceros, and the gomphotheres of the genus Anancus. These medium to large browsers joined a number of persisting elements that root in the former Sugutan faunas, such as the suids Kubanochoerus and

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Nyanzachoerus, the giraffid Palaeotragus, the bovids Tragoportax and Sivatherium, and the rhino Brachypotherium. However, the most distinctive feature of the new fauna was the sharp increase in medium to large grazers, such as the large sivatherine giraffids of the genus Sivatherium; the first giraffines of the genus Giraffa; the elephantids Stegotetrabelodon, Primelephas, and Elephas; the modern hippos of the genus Hexaprotodon; and the white rhino Ceratotherium. A new form of slender, grazer hipparionine horse, Eurygnathohippus, replaced the former mix-feeder Hippotherium primigenium. But the change to a grazer-dominated community is best exemplified by the bovids. Therefore, the new faunas include the first and abundant record of antelopes of the tribes Alcelaphini (Damalacra), Hippotragini (Hippotragus), Reduncini (Kobus, Menelikia), Aepycerotini (Aepyceros), and Antilopini (Gazella), which inhabit the present-day savannas. The increase in diversity of large browsers and grazers led also to a change in the predator community. While the bear dog amphicyonids persisted, the number of pursuit carnivores suddenly increased. Thus, at Lothagam are represented several species of cursorial, wolflike hyenas (Ictitherium, Hyaenictitherium, Hyaenictis, Ikelohyaena), two species of machairodontine cats (Lokotunjailurus, Dinofelis), hunting viverrids (Genetta), and mustelids (Ekoromellivora, Ekorus). Therefore, the change operated between 8 and 7 Ma from predominantly closed to predominantly open savanna environments led to a significant change in the mammalian communities, characterized by a dramatic increase in the number of medium to very large grazers, an increase in guild depth of large and very large browsers, and the presence of abundant and diverse pursuit carnivores (Harris 1993). As evidenced by the Lothagam association, this is the environment where the first hominids succeeded. Besides a number of baboons (Parapapio, Theropithecus) and colobine monkeys (Cercopithecoides), Lothagam records the presence of an unidentified hominid, represented by some isolated teeth and a fragmented mandible. The site of Lukeino, dated between 6.2 and 5.6 Ma, also delivered remains of a hominid, Orrorin tugenensis, in a context that resembles that of Lothagam, with elephants (Primelephas, Stegotetrabelodon, Loxodonta), gomphotherids (Anancus), deinotheres (Deinotherium), rhinos (Ceratotherium, Diceros), chalicotheres (Ancylotherium), hipparions (Eurygnathohippus), hippos (Hippopotamus, Hexaprotodon), suids (Nyanzachoerus), giraffids (Giraffa), and a variety of antelopes: Cephalophini (Cephalophus), Reduncini (Kobus), Aepycerotini (Aepyceros), Tragelaphini (Tragelaphus), and Neotragini (Pickford and Senut 2001). The first hominids of the genus Ardipithecus, from the latest Miocene (5.7–5.5 Ma) of the Adu-Asa and Sagantole Formations in the Middle Awash, lived in a somewhat different environment (Wolde Gabriel et al. 2001). Although, as in Lothagam and Lukeino, large grazers are present (the elephants Primelephas and Stegotetrabelodon, the giraffid Sivatherium, the reduncine antelope Kobus, as well as hipparions), the dominance of browsing forms such as gomphotherids (Anancus), deinotheres (Deinotherium), rhinos (Diceros), hippos (Hexaprotodon), suids (Nyanzachoerus), and boselaphine and tragelaphine bovids (Miotragocerus, Tragelaphus) points to more wooded conditions. Different again was the association found at Toros-Menalla 266, in Chad, dated between 7.4 and 5.2 Ma, where another early hominid species, Sahelanthropus tchadensis, was described (Vignaud et al. 2002). The faunal assemblage of Toros-Menalla shares with Lothagam and Lukeino the presence of a variety of large grazers: antelopes (Kobus, Hippotragini, Antilopini), elephants (Loxodonta), giraffids (Sivatherium), and hipparions (Eurygnathohippus cf. abudhabiense). However, the remaining association is based on medium to large browsers or mix feeders: Anancus, Nyanzachoerus, Hexaprotodon, and aff. Palaeoryx. Particularly surprising is the presence of the large, advanced anthracothere Libycosaurus petrocchii (also referred as Merycopotamus petrocchii), Page 20 of 26

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an element which is absent from the faunal associations of the same age in the eastern African basins. In fact, the Toros-Menalla 266 faunal assemblage fits better with the association found at the site of Sahabi (Libya), south of Benghazi. The fauna from the Sahabi Formation (Boaz et al. 1987) shares a number of elements in common with the eastern basins, such as monkeys (Macaca, Libypithecus), archaic elephants (Stegotetrabelodon), rhinos (Diceros), hipparions (Eurygnathohippus), hippos (Hexaprotodon), tetraconodontine suids (Nyanzachoerus), giraffids (Samotherium), and a variety of antelopes: Reduncini (Redunca), Alcelaphini (Damalacra), Hippotragini (Hippotragus), and Antilopini (Gazella). However, a significant part of the association is composed of taxa that were common to the Greek-Iranian province and the Siwaliks region. This is the case, for instance, with the abovementioned anthracotherid Libycosaurus (related to Merycopotamus); the bovids Miotragocerus, Prostrepsiceros, and Leptobos; the amebelodontid gomphothere Amebelodon; and the whole carnivore taxocoenosis (Machairodus, Chasmaporthetes, Hyaenictitherium, Adcrocuta, Indarctos, Agriotherium; Howell 1987). In Sahabi, the botanical evidence provided by wellpreserved fossil wood indicates an environment dominated by wooded savanna and semidesert grassland, with dominance of Acacia (64 %) and Mimosaceae (Dechamps and Maes 1987). The existence of periodic fires (a usual phenomenon in a savanna environment) is recorded as traumatic rings in fossil wood. The estuarine context of this site is reflected by the relative high proportion (13.5 %) of Salicaceae (Populus euphratica). The western Asian character of the Sahabi fauna, which partly extends south to the Chad Basin (Toros-Menalla 266), opens the question of the origin of the Late Miocene African faunas, after the crisis at 7 Ma. It has been suggested that much of the current savanna fauna did not evolve in situ from the Early and Middle Miocene African mammals but migrated from more northern latitudes in the Late Miocene, replacing the previous forest endemic dwellers (Maglio and Cooke 1978). More specifically, with the drying out of Africa between 8 and 7 Ma, large mammals from the Greek-Iranian province may have colonized the lower latitudes, their adaptations to a sclerophyllous woodland (hypsodont teeth, cursorial skeletons) having acted as exaptations (sensu Gould and Vrba 1982) to a savanna biome (Solounias et al. 1999). This was probably the case for bovids, giraffids, equids, hyenas, rhinos, and hominids. The faunal composition of sites like Toros-Menalla and Sahabi strongly supports this scenario.

Conclusions 1. The Middle Miocene terrestrial ecosystems of western and central Europe were characterized by increasing levels of mammalian diversity of taxa associated with a woodland biome: proboscideans, chalicotherids, rhinoceroses, suids, cervids, tragulids, moschids, and hominoids; many of them were fruit eaters and browsers. This high diversity of forest dwellers is also confirmed by the small mammal association, which includes eomyids, flying squirrels, dormice, and beavers. These high levels of diversity were probably a consequence of prevailing subtropical conditions. 2. In eastern Europe, however, we observe during the Middle Miocene a trend toward drier conditions, reflected in the abundance of hypsodont, grazing ruminants, mainly bovids and giraffids. This is the so-called Greek-Iranian Province, which extended from Greece to central Asia. 3. At the beginning of the Late Miocene (during the Vallesian Mammal Stage), diversity increased in Western Europe with the entry of new elements, like the hipparionine horses, giraffids, machairodont cats, ursids, and other eastern immigrants. Page 21 of 26

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4. About 9.6 Ma, increasing seasonality and extension of deciduous forest led to the extinction of most of the browser taxa that had populated the Middle Miocene woodlands, such as suids, cervids, rhinoceroses, and hominoids (the so-called Vallesian Crisis). This loss of diversity is not clearly recognized in the Greek-Iranian Province, nor it is in western Asia, where a highly diversified mammalian fauna including hominoids is still present in the Siwaliks sequence. 5. However, worldwide extension of grasses at 7–8 Ma led to the final extinction of most of these elements in Eurasia, with the exception of eastern and southeastern Asia. 6. At this point, an extension to the south of the Greek-Iranian Province can be recognized. This led to the Plio-Pleistocene savanna biome, characterized by a high diversity of hypsodont bovids, large grazers like rhinoceroses and giraffids, and most probably the hominoids that led to the first hominins in Africa.

Cross-References ▶ Fossil Record of Miocene Hominoids ▶ Origins of Homininae and Putative Selective Pressures Acting on the Early Hominins ▶ Role of Environmental Stimuli in Hominid Origins ▶ Zoogeography: Primate and Early Hominin Distribution and Migration Patterns

References Agustí J, Antón M (2002) Mammoths, sabertooths, and hominids. Columbia University Press, New York, 325 pp Agustí J, Moyà- Solà S (1990) Mammal extinctions in the Vallesian (Upper Miocene). Lect Notes Earth Sci 30:425–432. Berlin-Heidelberg Agustí J, Sanz de Siria A, Garcés M (2003) Explaining the end of the hominoid experiment in Europe. J Hum Evol 45(2):145–153 Agustí J, Cabrera L, Garcés M (2013) The Vallesian Mammal turnover: a late Miocene record of decoupled land-ocean evolution. Geophys J Roy Astron Soc 46:151–157 Axelrod DI (1975) Evolution and biogeography of Madrean-Tethyan sclerophyll vegetation. Ann Missouri Bot Gard 62:280–334 Barbero M, Benabid A, Peyre C, Quezel P (1982) Sur la présence au Maroc de Laurus azorica (Seub). Anales Jard Bot Madrid 37(2):467–472 Barbour MG, Chistensen NL (1993) Vegetation. In: Flora of North America, vol 1. Flora of North America Editorial Committee, pp 97–131 Barry JC, Johnson NM, Mahmood-Raza S, Jacobs LL (1985) Neogene mammalian faunal change in southern Asia: correlations with climatic, tectonic, and eustatic events. Geology 13:637–640 Barry JC, Morgan ME, Winkler AJ, Flynn LJ, Lindsay EH, Jacobs LL, Pilbeam D (1991) Faunal interchange and Miocene terrestrial vertebrates of southern Asia. Paleobiology 17:231–245 Benvenuti M, Bertini A, Rook L (1994) Facies analysis, vertebrate paleontology and palynology in the late Miocene Bacinello-Cinigiano Basin (Southern Tuscany). Mem Soc Geol It 48:415–423 Bernor RL (1984) A zoogeographic theater and biochronologic play: the time/biofacies phenomena of Eurasian and African Miocene mammal provinces. Paleobiol Continent 14(2):121–142 Bernor R, Armour-Chelu M (1999) Family Equidae. In: Rössner GE, Heissig K (eds) The Miocene land mammals of Europe. Verlag F. Pfeil, M€ unchen, pp 193–202 Page 22 of 26

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Boaz NT, El-Arnauti A, Gaziry AW, de Heinzlein DD (1987) Neogene paleontology and geology of Sahabi. Alan R. Liss, New York, 401 pp Cerling TE, Harris JR, MacFadden BJ, Leakey MG, Quade J, Eisenmann V, Ehleringer JR (1997) Global vegetation change through the Miocene/Pliocene boundary. Nature 389:153–158 Chaimanee Y, Jolly D, Benammi M, Tafforeau P, Duzer D, Moussa I, Jaeger JJ (2003) A middle Miocene hominoid from Thailand and orangutan origins. Nature 422:61–65 Coppens Y (1983) Le singe, l’Afrique et l’homme. Fayard, París de Bonis L, Koufos GD, Sen S (1997a) A giraffid from the middle Miocene of the island of Chios, Greece. Palaeontology 40(1):121–133 de Bonis L, Koufos GD, Sen S (1997b) The Sanitheres (Mammalia, Suoidea) from the Middle Miocene of Chios Island, Aegean Sea. Greece Rev Paléobiol Genève 16(1):259–270 Dechamps R, Maes F (1987) Paleoclimatic interpretation of fossil wood from the Sahabi Formation. In: Boaz NT et al (eds) Neogene paleontology and geology of Sahabi. Alan R. Liss, New York, pp 43–81 Dugas DP, Retallack GJ (1993) Middle Miocene fossil grasses from Fort Ternan. J Paleont 67(1):113–128 Eronen JT, Ataabadi MM, Micheels A, Karme A, Bernor RL, Fortelius M (2009) Distribution history and climatic controls of the late Miocene Pikermian chronofauna. Proc Natl Acad Sci USA 106:11867–11871 Eyles N (1996) Passive margin uplift around the North Atlantic region and its role in Northern Hemisphere Late Cenozoic glaciation. Geology 24:103–106 Fortelius M, Eronen J, Liu LP, Pushkina D, Tesakov A, Vislobokova I, Zhang ZQ (2003) Continental-scale hypsodonty patterns, climatic paleobiogeography and dispersal of Eurasian Neogene large mammal herbivores. Deinsea 10:1–11 Franzen JL, Storch G (1999) Late Miocene mammals from Central Europe. In: Agustí J, Rook L, Andrews P (eds) The evolution of Neogene terrestrial ecosystems in Europe. Cambridge University Press, Cambridge, UK, pp 165–190 Gabunia L, Gabashvili E, Vekua A, Lordkipanidze D (2001) The late Miocene hominoid from Georgia. In: de Bonis L, Koufos GD, Andrews P (eds) Phylogeny of the Neogene Hominoid Primates of Eurasia. Cambridge University Press, London, pp 316–325 Garcés M, Cabrera L, Agustí J, Parés JM (1997) Old World first appearance datum of “Hipparion” horses: late Miocene large mammal dispersal and global events. Geology 25(1):19–22, 2 figs Geraads D, Alemseged Z, Bellon H (2002) The late Miocene mammalian fauna of Chorora, Awash basin, Ethiopia: systematics, biochronology and the 40K-40Ar ages of the associated volcanics. Tert Res 21(1–4):113–122 Goldsmith NF, Hisrch F, Friedman GM, Tchernov E, Derin B, Gerry E, Horowitz A, Weinberger G (1988) Rotem mammals and Yeroham Crassostreids: stratigraphy of the Hazeva Formation (Israel) and the paleogeography of Miocene Africa. Newslett Strat 20(2):73–90 Gould SJ, Vrba E (1982) Exaptation: a missing term in the science of form. Paleobiology 8:4–15 Haq BU, Hardenbol J, Vail PR (1987) Chronology of fluctuating sea levels since the Triassic. Science 235:1156–1167 Harris J (1993) Ecosystem structure and growth of the African savanna. Glob Planet Change 8:231–248 Harrison TS, Harrison T (1989) Palynology of the late Miocene Oreopithecus-bearing lignite from Baccinello, Italy. Paleogeogr Paleoclim Paleoecol 76:45–65 Harrison T, Xueping J, Su D (2002) On the systematic status of the late Neogene hominoids from Yunann Province, China. J Hum Evol 43:207–227 Page 23 of 26

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Heissig K (1989) The rhinocerotidae. In: Prothero DR, Schoch RM (eds) The evolution of the perissodactyls. Oxford University Press, New York, pp 399–417 Hill A, Drake R, Tauxe L, Monaghan M, Barry JC, Behrensmeyer AK, Curtis G, Fine Jacobs B, Jacobs L, Johnson N, Pilbeam D (1985) Neogene palaeontology and geochronology of the Baringo basin, Kenya. J Hum Evol 14:759–773 Howell FC (1987) Preliminary observations on Carnivora from the Sahabi formation. In: Boaz NT, El-Arnauti A, Gaziry AW, de Heinzlein J, Boaz DD (eds) Neogene paleontology and geology of Sahabi. Alan R. Liss, New York, pp 153–181 Keller G, Barron JA (1983) Paleoceanographic implications of Miocene deep-sea hiatuses. Geol Soc Am Bull 94:590–613 Köhler M (1993) Skeleton and habitat of recent and fossil ruminants. M€ unchner Geowissench. Abhandlungen. Reihe A. Geol Paläontol 25:1–88 Koufos G (2006) Paleoecology and chronology of the Vallesian (Late Miocene) in the Eastern Mediterranean region. Palaeogeogr Palaeoclimatol Palaeoecol 234:127–145 Kutzbach JE, Prell L, Ruddiman WF (1993) Sensitivity of Eurasian climate to surface uplift of Tibetan Plateau. J Geophys Res 101:177–190 Leakey M, Harris JM (2003) Lothagam: the dawn of humanity in Eastern Africa. Columbia University Press, New York, 665 pp Lovejoy CO (1980) Hominid origins: their role in bipedalism. Am J Phys Anthropol 52:250 Maglio VJ, Cooke HBS (1978) Evolution of African mammals. Harvard University Press, Cambridge, MA Miller KG, Faibanks RG, Mountain GS (1987) Tertiary oxygen synthesis, sea level history, and continental margin erosion. Paleooceanography 2:1–19 Miller KG, Wright JD, Faibanks RG (1991) Unlocking the ice house: Oligocene-Miocene oxygen isotopes, eustasy and margin erosion. J Geophys Res 96:6829–6848 Morgan ME, Kingston JD, Marino BD (1994) Carbon isotopic evidence for the emergence of C4 plants in the Neogene from Pakistan and Kenya. Nature 367:162–165 Nakaya H (1994) Faunal change of Late Miocene Africa and Eurasia: mammalian fauna from the Namurungule Formation, Samburu Hills, Northern Kenya. Afr Study Monogr 20(Suppl):1–112 Pickford M, Senut B (2001) The geological and faunal context of Late Miocene hominid remains from Lukeino, Kenya. CR Acad Sci Ser IIa 332:145–152 Pickford M, Nakaya H, Kunimatsu Y, Saegusa H, Fukuchi A, Ratanasthien B (2004) Age and taxonomic status of the Chiang Muan (Thailand) hominoids. CR Palevol 3:65–75 Pilbeam D, Morgan M, Barry JC, Flynn LJ (1996) European MN units and the Siwalik faunal sequence of Pakistan. In: Bernor R, Fahlbusch V, Mittman W (eds) The evolution of western Eurasian Neogene mammal faunas. Columbia University Press, New York Quade J, Cerling TE, Bowman JR (1989) Development of Asian monsoon revealed by marked ecological shift during the latest Miocene in northern Pakistan. Nature 342:163–164 Richardson SD (1990) Forest and forestry in China. Island Press, Washington, DC Rook L, Abbazi L, Engesser B (1999) An overview on the Italian Miocene land mammal faunas. In: Agustí J, Rook L, Andrews P (eds) Evolution of Neogene terrestrial ecosystems in Europe. Cambridge University Press, Cambridge, UK, pp 190–204 Sanz de Siria A (1994) La evolución de las paleofloras en las cuencas cenozoicas catalanas. Acta Geol Hisp 29:169–189 Sanz de Siria A (1997) La macroflora del vallesiense superior de Terrassa (Barcelona). Paleont I Evol 30–31:247–268. Sabadell

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Solounias N, Plavcan JM, Quade J, Witmer L (1999) The paleoecology of the Pikermian Biome and the savanna myth. In: Agustí J, Rook L, Andrews P (eds) Evolution of Neogene terrestrial ecosystems in Europe. Cambridge University Press, Cambridge, UK, pp 436–453 Tchernov EL, Ginsburg L, Tassy P, Goldsmith NF (1987) Miocene mammals from the Negev (Israel). J Vert Paleont 7(3):284–310 Thomas H (1984) Les Giraffoidea et les Bovidae Miocènes de la formation Nyakach (Rift Nyanza, Kenya). Palaeontographica 183:64–89 Turner A, Antón M (1997) The big cats and their fossil relatives. Columbia University Press, New York, 234 pp, 16 pl Van der Made J (1996) Listriodontinae (Suidae, Mammalia), their evolution, systematics and distribution in time and space. Contrib Tert Quat Geol 33(1–4):3–160. 44 pl, 4 tb Vignaud P, Duringer P, Taïsso Mackaye H, Likius A, Blondel C, Boisserie J-R, de Boins L, Eisenmann V, Etienne ME, Geraards D, Guy F, Lehmann T, Lihoreau F, López-Martínez N, Mourer-Chauviré C, Otero O, Rage J-C, Schsuter M, Viriot L, Zazzo A, Brunet M (2002) Geology and paleontology of the Upper Miocene Toros-Menalla hominid locality. Chad Nat 418:152–155 Viranta S (1996) European Miocene Amphicyonidae-taxonomy, systematics and ecology. Acta Zool Fennica 204:1–61. Helsinki Wang CW (1961) The forest of China. Harvard University Press, Cambridge, 313 pp Wenderlin L, Solounias N (1991) The Hyaenidae: taxonomy, systematics and evolution. Fossils Strata 30:1–104. Oslo Wenderlin L, Solounias N (1996) The evolutionary history of Hyaenas in Europe and western Asia during the Miocene. In: Bernor R, Fahlbusch V, Mittman W (eds) The evolution of Western Eurasian Neogene mammal faunas. Columbia University Press, New York, pp 290–306 White JM, Ager TA, Adam DP, Leopold EB, Liu G, Jetté H, Schweger CE (1997) An 18 million year record of vegetation and climate change in northwestern Canada and Alaska: tectonic and global climate. Palaeogeogr Palaeoclim Palaeoecol 130:293–306 Wolde Gabriel G, Hale-Selassie Y, Renne PR, Hart WK, Ambrose SH, Asfaw B, Heiken G, White T (2001) Geology and palaeontology of the late Miocene Middle Awash valley, Afar rift, Ethiopia. Nature 412:175–181 Zhang X (1987) New materials of Ramapithecus from Kaiyuan, Yunnan. Acta Anthropol Sin 6:82–86

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Index Terms: Aceratherium 10 Amphicyon 4, 11, 13 Chalicotherium 2, 8 Chilotherium 8, 10 Deinotherium 2, 8, 16, 19–20 Dorcatherium 3–4, 8, 17, 19 Dryopithecus 1–2, 5, 12–16 Gazella 7, 19–21 Giraffokeryx 7–8 Hipparion 9, 11–12 Lartetotherium 2, 12 Listriodon 3, 7–8, 12 Machairodus 10–13, 18, 21 Micromeryx 3, 7 Miotragocerus 6, 19–21 Palaeotragus 5, 10, 19–20 Propotamochoerus 3, 8, 12 Sivapithecus 8, 12–13, 16 Tetralophodon 2, 17, 19

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_34-3 # Springer-Verlag Berlin Heidelberg 2014

Postcranial and Locomotor Adaptations of Hominoids Carol V. Ward* Department of Pathology and Anatomical Sciences, University of Missouri, Columbia, MO, USA

Abstract Extant apes are adapted to various forms of below-branch forelimb-dominated arboreal locomotion and share morphologies associated with the shared aspects of their locomotor behaviors. With the expanding record of Miocene hominoid fossils, paleoanthropologists are coming to realize that although some shared characters may indeed be homologous, at least some almost certainly represent homoplasies. The apparently more primitive body plan of Sivapithecus than seen in Asian and African great apes indicates that at least some homoplasy has occurred within these clades. Furthermore, the expanding fossil record may be indicating a greater diversity of positional behaviors within the Hominoidea than previously appreciated; for example, Pierolapithecus has been argued to indicate the evolution of suspensory locomotion in combination with arboreal quadrupedalism, and Nacholapithecus is unique with its enlarged forelimb but otherwise primitive body plan. These new fossils reveal that variation is prevalent and critical to appreciate for reconstructing hominoid evolutionary history. Furthermore, it seems increasingly likely that many postcranial and locomotor specializations of great apes may have evolved from ancestors that were more generalized than are living hominoids. This realization is critical for interpreting the ancestral morphology from which hominins were derived.

Introduction One of the most distinctive shared characteristics of modern apes is their specialization for belowbranch forelimb-dominated arboreal locomotion, many adaptations for which are still seen in humans today (Huxley 1863; Keith 1923). Extant apes all exhibit an overlapping set of adaptations to suspension and orthograde climbing in their torsos, limbs, hands, and feet. They have elongated forearms and hands; high-intermembral indices; laterally oriented shoulder joints; limb joints adapted to loading in a variety of postures; short, broad torsos; and absence of a tail. Given this suite of apomorphies, parsimony would seem to dictate that ancestral apes should have been suspensory as well (Gregory 1916). If not, extant hominoids must have developed these adaptations independently, which would, on the face of it, seem to involve an unlikely amount of homoplasy. However, while below-branch forelimb-dominated arboreality distinguishes all modern ape taxa from other catarrhines (Schultz 1930, 1969a, b), it is not a monolithic adaptation (Larson 1988). Young (2003) has suggested that great ape postcranial adaptations are homologous (see also Pilbeam 2002) and that hylobatids may be autapomorphic, due to their small size and exclusively arboreal specialization for brachiation that involves moving rapidly through the trees in ricochetal fashion. Yet arboreal adaptations actually vary among extant ape genera more than is often emphasized in considerations of the evolution of hominoid locomotion, reflecting specialization on different types and amounts of climbing and suspensory behavior. Orangutans almost never use the ground, yet, *Email: [email protected] Page 1 of 22

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given their large body size, they move cautiously through the upper levels of the canopy with quadrumanous climbing and arm hanging. Their forelimbs are astonishingly long and all joints are flexible and employed in diverse postures (MacKinnon 1974; Cant 1987). Chimpanzees, arboreal when foraging, hunting, and sleeping, spend much of their time as terrestrial knuckle walkers (Goodall 1965; Hunt 1990), as do bonobos, although the locomotor behavior of the latter is less well studied (Doran 1993). Gorillas are extremely large and are even more terrestrial than chimpanzees or bonobos, yet particularly in certain habitats they habitually climb trees frequently for feeding and sleeping (Tuttle and Watts 1985; Remis 1995). Hominins, of course, modified their locomotor skeletons to specialize in the most distinctive of all primate locomotor behaviors, habitual terrestrial bipedality, although they likely evolved from ancestors that were at least somewhat adapted to climbing or suspensory arboreal locomotion. Given this variation among taxa, a certain level of independence in the acquisition of some suspensory traits should perhaps not be considered entirely unlikely. The burgeoning fossil record is strengthening the hypothesis that climbing and suspensory adaptations developed in mosaic fashion over evolutionary time and occurred in different ways and even multiple times in separate hominoid lineages (Sarmiento 1987; Pilbeam et al. 1990; Moyà Solà and Köhler 1995; Begun et al. 1997; Finarelli and Clyde 2004; Moyà Solà et al. 2004; Crompton et al. 2008; Lovejoy et al 2009; Almécija et al. 2013; Hammond et al. 2013). Timing of wrist bone development differs among chimpanzees and gorillas, also suggesting some homoplasy even between these taxa (Kivell and Schmitt 2009). The hominoid fossil record now includes over 28 genera known from as early as 20 Ma, and many taxa are known from postcranial elements (see Hartwig 2002; Begun et al. 2012). Among these fossil taxa, there is much wider range of known locomotor modes than among extant ones. Adaptations seen in some, and even all, extant apes do not occur as a block. For example, Nacholapithecus has elongated forelimbs but a long, narrow torso and apparently pronograde quadrupedal posture (Rose et al. 1996; Senut et al. 2004; Ishida et al. 2004). Pierolapithecus has what appears to be a hylobatid-like torso structure, yet does not seem to have particularly long digits (Moyà Solà et al. 2004; Hammond et al. 2013). Considering variation within living and fossil hominoids may lead us away from dichotomous views on whether the euhominoid ancestor was “great apelike” or “basal hominoid-like” (Pilbeam et al. 1990; Young 2003; Crompton et al. 2008) and may lead us to a more nuanced and more accurate understanding of how hominoids evolved. The positional behavior variation among extant and fossil hominoids provides an important set of information about hominoid phylogeny and evolution. This chapter will summarize the postcranial adaptations of extant and the best-known fossil hominoid genera and put these taxa into phylogenetic context in order to explore evolutionary patterns in hominoid postcranial and locomotor adaptations.

Extant Hominoids Living apes all share a suite of adaptations to below-branch, forelimb-dominated arboreality, although they do not exploit this locomotor niche identically and are distinguishable postcranially, although particularly among great apes differences are poorly characterized (Young 2003; but see Larson 1988; Inouye and Shea 1997; Drapeau 2001). All, though, have evolved to negotiate terminal branches of arboreal substrates by hanging below branches and distributing their weight among multiple supports. Their relatively large body sizes and long forelimbs allow them to bridge gaps in the canopy rather than leaping. They lack tails, which are no longer necessary for balance within this Page 2 of 22

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type of locomotor regime. As a consequence, the musculature usually associated with tails in nonhominoid primates has become restructured to form a muscular pelvic floor, providing support for the viscera during the orthograde postures common in all ape species today (Elftman 1929). Apes have high-intermembral indices (Schultz 1930; Aiello 1981; Jungers 1985). When climbing, their long forelimbs and relatively short hindlimbs improve their ability to negotiate large-diameter vertical supports. The long arms also assist in increasing their reach for bridging gaps and grasping branches. Limb proportions vary however (Aiello 1981; Jungers 1984, 1985). Orangutans and hylobatids have proportionally longer forearms and hands than do chimpanzees, and chimpanzees and bonobos alone have differentially elongated metacarpals more than other extant apes (Drapeau 2001). Ape torsos are broad, with the scapulae positioned dorsally and glenoid fossae oriented laterally (Keith 1923; Schultz 1930, 1961, 1969a; Benton 1965, 1976; Sarmiento 1987; Ward 1993). Their ribs have higher costal angles, sterna are broad, scapulae have a cranially oriented glenoid fossa, and their clavicles are long (Schultz 1937; Cartmill and Milton 1977; Larson 1993). The broad torso and wide pectoral girdle results in a shoulder position that places the scapulothoracic musculature more in the coronal plane, facilitating adduction of the upper limb (Erickson 1963; Benton 1965, 1976; Ward 1993). Adduction is accomplished primarily by the latissimus dorsi muscle along with others that are important in hoisting the body up from an arm-hanging position and in pulling the body among supports in the trees (Swartz et al. 1989; Hunt 1991). Extant hominoid pectoral girdle form also increases the reach of the forelimbs and circumduction at the shoulder (Cartmill and Milton 1977). Extant hominoid lumbar spines are reduced in length, with only 5–6 lumbar vertebrae in lesser apes, compared with the typical primate number of 7, and great apes have only 3–4, so that the lower ribs approximate the iliac crest (Schultz and Straus 1945; Erickson 1963; Ankel 1967, 1972; review in Ward 1993). African apes differ from humans, orangutans, and hylobatids in having 13 rather than 12 thoracic vertebrae and ribs (Schultz 1930, 1969a, b). This variation in thoracic vertebral count among extant hominoids is noteworthy and may be yet another small line of evidence supporting hypotheses of postcranial homoplasy among extant apes. All great ape lumbar spines are almost completely inflexible (Slijper 1946; Schultz 1969a, b; Benton 1976). Their iliac blades are craniocaudally elongated, expanding the distance between hip and sacroiliac joints (Waterman 1929; Ward 1993). Part of latissimus dorsi inserts directly upon the iliac crest (Sonntag 1923, 1924; Waterman 1929; Gregory 1950). The reduced lumbar spine provides a stiffer platform for these muscles to act upon the upper limb and protects the vulnerable lumbar spine from excessive lateral bending moments during latissimus dorsi contractions (Cartmill and Milton 1977; Jungers 1984; Sarmiento 1985; Ward 1993). Reaching overhead during climbing requires the ability to adduct the wrist, which apes can do due to a reduced ulnar styloid that has lost contact with the carpus (Lewis 1971, 1972, 1989; Sarmiento 1988; Whitehead 1993). The pisiform is more distally situated, facilitating extensive adduction at the wrist up to 90
(Sarmiento 1988). Apes rely on a hook grip during suspensory behaviors and have relatively long fingers with strong flexor musculature and reduced thumbs (Schultz 1930; Rose 1988). They also have strong grasping pollices and halluces, along with well-developed musculature for adduction. The fibula, site of attachment of the long hallucal flexor muscles, is well developed (Schultz 1930; Sonntag 1923, 1924; Gregory 1950; Swindler and Wood 1973). Manual and pedal phalanges have well-developed attachment sites for digital flexors (review in Begun 1994a). The curved forearm bones of apes have been linked to the presence of strong hand and finger flexors (Miller 1932; Knussmann 1967).

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These adaptations are better developed in great apes than in lesser apes (review in Young 2003). Mechanical constraints on mechanical function, and stresses on the musculoskeletal system, increase exponentially with increasing body size; thus some differences between lesser and great apes may represent allometric issues (Aiello 1981; Jungers 1984). The small body size of hylobatids may be secondarily derived, as is their unique adaptation for ricochetal brachiation (Cartmill 1985). Their forelimbs and hands are particularly elongate (Jungers 1984), their thumbs particularly short, and their body mass relatively low. Their lumbar vertebral columns are 5–6 segments long and their thoracic columns 12 (Schultz and Straus 1945). Differences between African apes and orangutans have also been noted, including a smaller supraspinous region of the scapula, smaller acromion processes, and shorter scapulae in orangutans (Oxnard 1984; Larson 1988; Young 2003). Orangutans have higher intermembral indices (Aiello 1981), a nonuniformly curved iliac crest, and an anterior longitudinal ligament ridge on the anterior surfaces of the vertebral bodies. They also lack a ligamentum teres of the femoral head, along with particularly mobile knee and midtarsal joints. Orangutans alone among large hominoids retain separate centrale and scaphoid bones rather than the fused os centrale seen in extant African apes. These differences are presumably related to the highly developed and nearly exclusively quadrumanous arboreal locomotor behavior of orangutans on one hand compared with the partly terrestrial knuckle-walking habits of African apes on the other. It is worth noting, however, that little work has been done to explore the extent of morphological variation among great apes and their functional significance. So, although apes do share a distinctive suite of morphologies, they are not identical in their behavior nor anatomy. Therefore, although a subset of shared morphologies undoubtedly was present in their common ancestor and represents synapomorphies of the hominoid clade, such differences indicate a combination either of locomotor specialization within each lineage or independent acquisition within lineages undergoing broadly similar selective pressures. Only careful examination of the currently known fossil record, and discovery of new hominoid fossils, will allow us to determine which scenarios led to the diversity of known hominoid locomotor adaptations.

Fossil Non-hominin Hominoids Hominoids can essentially be grouped into temporal and adaptive grades, basal hominoids, and euhominoids (Begun et al. 1997, 2012; Begun 2010; Begun 2001) (Fig. 1). Basal hominoids are stem taxa known from the Early and Middle Miocene and comprise taxa that are not crown hominoids and that lack postcranial specializations for extant apelike below-branch arboreality. Euhominoids are members of a crown hominoid clade, and so demonstrate extant hominoid synapomorphies, of which the postcranial anatomy is significant to this discussion. In an analysis of relatively well-known taxa (Begun et al. 1997), basal hominoid taxa include Proconsul and Afropithecus from the Early Miocene and Kenyapithecus, which in the analysis includes Equatorius (Ward et al. 1999), Griphopithecus (Begun 2000) from the Middle Miocene, and to which should now be added Nacholapithecus from the Middle Miocene (Ishida et al. 1984, 2004; Rose et al. 1996; Nakatsukasa et al. 1998). Euhominoids include Sivapithecus, Oreopithecus, Pierolapithecus, Rudapithecus, Hispanopithecus, and Dryopithecus

Proconsul and Afropithecus Postcranially the best-known genus of Early Miocene hominoid is Proconsul, although Afropithecus is also represented by several postcranial elements. While these taxa differed craniodentally, Page 4 of 22

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_34-3 # Springer-Verlag Berlin Heidelberg 2014 Proconsul Nacholapithecus Afropithecus Morotopithecus Griphopithecus Hylobatids Oreopithecus Equatorius/Kenyapithecus Pongo Sivapithecus Pan Homo Australopithecus Ardipithecus Gorilla Pierolapithecus Rudapithecus Hispanopithecus Dryopithecus

Fig. 1 Hypothesized phylogeny of hominoid relationships (based on Begun et al. 2012) followed in this chapter

Afropithecus is strikingly similar in preserved postcranial bones to Proconsul nyanzae (Ward 1998). These taxa, among others less well known postcranially, represent a stem group referred to as basal hominoids (Begun et al. 1997). Comprehensive reviews of these taxa can be found in Walker (1997) and Leakey and Walker (1997). Proconsul was a genus composed of at least four species of pronograde, quadrupedal, arboreal frugivores that ranged in size from that of colobus monkeys to that of female gorillas. Proconsul individuals were very generalized animals. They were certainly above-branch arboreal quadrupeds that would have been capable, as most primates are, of limited below-branch postures and movement but that show no specialization for below-branch arboreality. Proconsul had a roughly even intermembral index and retained ulnar contact with the wrist (Beard et al. 1986). It also had a relatively long torso with six lumbar vertebrae, lacking the stiffening of the lumbar spine seen in extant apes (Ward 1993; Ward et al. 1993). The vertebrae have transverse processes arising from the vertebral body as in most monkeys, distinct accessory processes that suggest large erector spinae musculature, reflecting a narrow rib cage, and narrow and laterally facing iliac blades (Ward 1993). The pelvis was narrow, as, presumably, was the thoracic cage. The humerus is retroflexed with little torsion, reflecting ventrally oriented glenohumeral joints (Napier and Davis 1959; Larson 1988). The sternebrae are wider than those of cercopithecids, instead resembling atelines, but were not as broad as those of apes. Proconsul is distinguished postcranially from earlier generalized catarrhines such as Aegyptopithecus (Rose 1997; Walker 1997) by a shoulder adapted to a wider range of loading, an elbow joint emphasizing joint loading in a variety of flexion-extension and pronation-supination postures, longer distal limb segments, a foot that may have been better adapted to inversion-eversion (Walker 1997, Table 1 p. 221), and the lack of a tail (Ward et al. 1991; Nakatsukasa et al. 2004). It is also true that Proconsul had a hip joint with a high neck-shaft angle, a femoral head set high on the

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neck, a centrally placed fovea capitis, and a greater trochanter that was shorter than that of many monkeys, indicating a hip joint adapted to loading in at least somewhat abducted postures (Ward 1992; Ward C 1997), although not necessarily with a greater range of possible abduction than found in most monkeys (Hammond 2013). The knee joint was broad, with a broad, flat patella, also indicating a very generalized and adaptable use of the lower limb. Most monkeys and earlier, generalized catarrhines have joints designed for fairly stereotypical loading environments principally comprising of quadrupedal postures in which the limbs are relatively adducted and the hands are pronated and palmigrade. Thus in comparison to Aegyptopithecus, Proconsul and other known Early Miocene basal hominoids were adapted for using their limbs in more abducted postures, with hands and feet grasping arboreal supports in a variety of positions. The hands and feet of Proconsul have relatively well-developed first rays and supporting bones such as the large fibula. The phalanges are fairly long, with clear ridges for attachment of the finger and toe flexors (Begun 1993). The hallux and pollex were long relative to the other digits, suggesting that actual grasping was used rather than emphasizing the hook grips characteristic of extant apes. Before the discovery of taillessness in Proconsul, reduction of a tail and commensurate restructuring of the pelvic floor musculature had been equated with the evolution of orthograde posture, which requires muscular support of pelvic viscera. However, the lack of a tail in Proconsul, and also in Nacholapithecus (Ward et al. 1991; Nakatsukasa et al. 2004), reveals that tail loss in hominoids was not associated with orthogrady, but rather with a decreased reliance on running and leaping behaviors and an emphasis on more deliberate arboreality, emphasizing manual and pedal grasping with weight distributed over multiple supports (Kelley 1995). Taillessness was likely a characteristic of all basal hominoids and one of the defining features of this superfamily. In summary, a reasonable locomotor reconstruction of early hominoids is possible. The positional repertoire of the earliest known hominoids likely was distinguished from that of primitive catarrhines such as Aegyptopithecus by a specialization for deliberate arboreal climbing and clambering, using strong manual and pedal grasping to maintain balance and to move about in the arboreal environment. The emphasis on grasping meant that tails were no longer needed for balance, and thus an external tail became lost. A grasping adaptation enabled many hominoids to attain larger body sizes than seen in extant monkeys, yet still remain arboreal. This emphasis on cautious climbing and clambering enabled basal hominoids to reach fruit on the terminal branches and cross gaps in the canopy by giving them the ability to distribute their weight over multiple supports. They almost certainly also practiced vertical climbing and limited suspension but had not yet evolved selection for specialized adaptations to these behaviors; instead they spent most of their time above the branches. Their limb joints were adapted to loading in a wider variety of postures than is typical for most nonhominoids, including those involving an abducted hip and supinated elbow. They were certainly capable of orthograde postures and probably employed them often. Yet their narrow torso structure with ventrally oriented shoulder joints and ulnocarpal contact that limited ulnar deviation of the wrist indicate locomotion primarily with the limbs positioned mainly underneath the body or slightly abducted. This generalized arboreal locomotor habitus permitted this early radiation of basal hominoids to exploit a variety of body sizes, as well as a breadth of ecological niches. Proconsul was likely a ripefruit frugivore and Afropithecus a seed predator (Leakey and Walker 1997). Rangwapithecus, less known postcranially, seemed to be at least partly folivorous (Kay and Ungar 1997). Thus, except for Morotopithecus (below), Early Miocene apes seem to be an adaptive radiation that shared a broadly similar set of locomotor adaptations.

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Morotopithecus Morotopithecus bishopi is the earliest Miocene ape known from eastern Uganda and dated at over 20.6 Ma (Gebo et al. 1997). The palate of this taxon resembles those of other basal hominoids and has been compared to both Proconsul (P. major) and Afropithecus (review in Leakey and Walker 1997). As such, this species is placed phylogenetically as a basal hominoid rather than as a euhominoid. Postcranially, however, it differs from other Early Miocene apes in displaying a more derived, modern apelike postcranial skeleton in some respects. The only postcranial elements known from Morotopithecus include a glenoid fossa, a lumbar vertebra and associated fragments of other lower vertebrae (Walker and Rose 1968), and partial femora. The Morotopithecus glenoid fragment is similar to its counterpart in extant great apes, being ovoid and shallow and lacking a narrow, laterally concave cranial portion (MacLatchy et al. 2000). This suggests a shoulder joint adapted to loading in a variety of postures and may be associated with a broader upper torso morphology. A more extant apelike torso in Morotopithecus compared with Proconsul is also suggested by the lumbar vertebrae (Ward 1993; Sanders and Bodenbender 1994; Nakatsukasa 2008), which are morphologically similar to those of hylobatids in having short bodies relative to endplate dimensions (Nakatsukasa 2008) and have lumbar vertebral transverse processes which arise from the junction of the vertebral body and pedicle (Walker and Rose 1968) rather than from the body as in Proconsul (Ward 1993; Ward et al. 1993) or Nacholapithecus (Nakatsukasa et al. 1998; Nakatsukasa 2008). This is correlated with the lack of accessory processes (Ward 1993). The body is also not hollowed out laterally, although a rounded median keel or bulge (Nakatsukasa 2008) is present. The Morotopithecus femur is robust, with a small head, but displays the typical hominoid pattern of having a high neck-shaft angle and centrally placed fovea capitis. The distal femur is very broad mediolaterally, with condyles asymmetric in size, and there is a large popliteus groove as in extant apes, suggesting adaptation to habitual loading in a variety of postures, and a high degree of rotation of the knee joint. Still, Morotopithecus may have had more lumbar vertebrae than typical great apes based on additional vertebral fragments from the site showing more ventral wedging of the vertebral bodies than typical for great apes, variable placement of the transverse processes relative to the vertebral body and pedicle (Nakatsukasa 2008), and mediolaterally narrow laminae. This suggests that the overall vertebral column was not as derived as seen in extant apes. Altogether Morotopithecus shares several key features with extant apes, suggesting adaptation for more below-branch arboreal activities. The shoulder, hip, and knee appear to suggest adaptation to a variety of postures, and the vertebrae suggest a certain amount of broadening and stiffening of the torso, but not perhaps as much as in extant great apes at least. There is also nothing in the Morotopithecus skeleton that is substantially more derived than that of hylobatids except for a broader knee joint and the presence of a gluteal ridge and perhaps also transverse process inclination (Young and MacLatchy 2004). The femoral characters may be related to body size variation, and the transverse process inclination is actually somewhat intermediate between that of gibbons and great apes (Shapiro 1993). Still, the hominoid similarities have led MacLatchy (2004), MacLatchy et al. (2000), and Young and MacLatchy (2004) to hypothesize that Morotopithecus is a basal member of the euhominoid clade and that other basal hominoids, like Proconsul, Afropithecus, Nacholapithecus, and Equatorius/Kenyapithecus at least, are more distantly related to extant apes. This hypothesis assumes that the postcranial adaptations shared by extant hominoids in torso restructuring, below-branch locomotion, and knee mobility are synapomorphies. Given its primitive craniodental and perhaps some vertebral characters, the phylogenetic placement and thus the evolutionary implications of Morotopithecus are difficult to assess. But considering the homoplastic similarities between ateline monkeys, Pliopithecus, and extant hominoids, Page 7 of 22

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and the variation among extant hominoids, it certainly seems plausible that shared features of Morotopithecus and great apes represent homoplasies. Regardless of its phylogenetic affinities, it seems apparent that Morotopithecus was a more forelimb-dominated below-branch arboreal animal with a greater emphasis on orthograde postures than is typical for other basal hominoids.

Nacholapithecus Nacholapithecus kerioi is a Middle Miocene ape from northern Kenya (Ishida et al. 1984, 2004; Pickford et al. 1987; Rose et al. 1996; Nakatsukasa et al. 1998; Nakatsukasa 2003a, b). It displays an unusual suite of morphologies in a very different combination than known for other hominoids. Its overall body plan is similar to that of Proconsul. It has a long vertebral column with six lumbar vertebrae shaped like those of Proconsul (Nakatsukasa et al. 1998). It appears to have had a narrow torso shape and no tail, yet its feet were long, its shoulder joints mobile, and its upper limbs very large (Nakatsukasa et al. 1998; Senut 2003; Ishida et al. 2004). The hands and feet reflect palmigrade, plantigrade quadrupedalism. The body proportions of Nacholapithecus are striking, having very large forelimb and relatively small hindlimb elements, outside the observed ranges for even extant apes (Ishida et al. 2004). The lower limb is comparatively small, but there is a high neck-shaft angle of the femur and a short neck. Otherwise, the tibia, fibula, and tarsal bones are similar to those of Proconsul. What is different are the very long pedal digits found in Nacholapithecus, which are similar in size to those of chimpanzees despite the fact that it is thought to have weighed about half of what chimpanzees weigh (22 kg; Ishida et al. 2004). The ribs are relatively large, and it has a long clavicle and scapular spine (Ishida et al. 2004; Senut et al. 2004; Nakatsukasa et al 2007). The distal humerus is derived relative to that seen in Proconsul, with a better-developed ball-and-socket morphology of the humeroradial joint and a more symmetrical humeroulnar joint. It had a relatively long clavicle with ligament markings, suggesting that protraction of the humerus into overhead postures would have been emphasized rather than abduction (Senut et al. 2004). The morphological similarity between the shoulder bone morphologies and those of colobine monkeys underscores this interpretation. This difference in inferred upper limb use in climbing between Nacholapithecus and euhominoids is likely related to its lack of torso restructuring from the primitive condition. Nacholapithecus retained six or seven lumbar vertebrae with ventral median keels and hollowed sides, transverse processes arising from the body-pedicle junction, and small accessory processes are present as in Proconsul (Nakatsukasa et al. 2007). This restructuring to make the torso shorter, stiffer, and broader is seen in apes emphasizing abduction-adduction movements of the upper limb (Ward 1993). This is consistent with the caudal orientation of the spinous processes in the lower thoracic and lumbar vertebrae as well (Nakatsukasa et al. 2007). Thus, Nacholapithecus does seem to have been adapted for more extensive forelimb-dominated climbing locomotion than were earlier basal hominoids, with enlarged forelimbs and small hindlimbs and long pedal phalanges, but in a fundamentally different way from what is seen in later euhominoids.

Equatorius/Kenyapithecus The Middle Miocene African fossil sample originally attributed to Kenyapithecus has now been partly divided by some researchers and placed into Equatorius (Ward et al. 1999) or Griphopithecus (Begun 2000), with the result that there is now only one humerus known for Kenyapithecus wickeri (summary by Ward and Duren 2002). Given the taxonomic debate, here all samples are treated together. Equatorius resembles other basal hominoids in several respects (Sherwood et al. 2002). It has a monkey-like scapula and a retroflexed humeral shaft, indicating a pronograde posture at the Page 8 of 22

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shoulder. The ulna still contacts the carpus, and the os centrale is unfused to the scaphoid. Equatorius has the mobile hip and knee joint morphology characteristic of all hominoids and slightly broader sternebrae than typical for monkeys, although it is reconstructed to lack the laterally expanded torso of extant apes. Equatorius (¼ Kenyapithecus) from Maboko Island has been interpreted as semiterrestrial based on its retroflexed humeral shaft, medial humeral epicondyle, and olecranon process, along with long radial head, short phalanges, and morphology of the metacarpal heads (McCrossin and Benefit 1997). However, it has also been described as resembling extant apes in having a straight humeral shaft and strong grasping capabilities (McCrossin 1997). It is difficult to reconcile these divergent descriptions at present. Equatorius does not display evidence of thoracic reorganization typical of Morotopithecus or extant apes, but instead was a more generalized pronograde quadruped that may have spent some time on the ground. If indeed Equatorius/Kenyapithecus is more closely related to euhominoids than is Proconsul (Ward and Duren 2002), it reinforces the hypothesis that the ancestral euhominoid was generalized postcranially.

Griphopithecus Griphopithecus is known from the early Middle Miocene of central and eastern Europe and Turkey. Postcranially, phalanges from the site of Paşalar, Turkey, are fairly short and straight, lacking evidence of climbing adaptations (Ersoy et al 2008). A partial ulna and humerus from Kleinhadersdorf, Austria, also appear to be those of a generalized quadruped (Begun 2002; Alba et al. 2010).

Sivapithecus Sivapithecus is known from more than one species from the Middle and Late Miocene of Pakistan (review in Ward 2007). It shares an extensive suite of craniodental characters with orangutans, suggesting that they are sister taxa (see Ward 2007). Postcranially, however, these taxa are not similar. The discovery of humeral shafts attributed to Sivapithecus (Pilbeam et al. 1990) led to a startling revelation about the evolution of hominoid locomotion, referred to as the “Sivapithecus dilemma” by Pilbeam and Young (2001). The hand and foot remains known for Sivapithecus up to that time all exhibited a more derived modern apelike morphology than earlier hominoids such as Proconsul. It had longer, stronger phalanges, a better-developed hallux, and a more mobile elbow, and these morphologies were presumed to indicate at least a somewhat extant great-apelike overall postcranial gestalt (Rose 1986). To most researchers the marked craniofacial similarities between Sivapithecus and Pongo indicate a close phylogenetic relationship (Ward and Brown 1986; Wards 1997; Kelley 2002; Begun 2010; Alba et al. 2012), so the apparently modern apelike postcranial fossils fit a phylogenetic position of Sivapithecus well within the hominid clade. The humeri, however, appear to paint a different picture. Although missing their proximal ends, both specimens appear to be inclined posteriorly and medially, the morphology seen in primates like most monkeys, Proconsul, and Nacholapithecus that have posteriorly directed humeral heads, ventrally facing scapular glenoid fossae, and narrow torso structures (Pilbeam et al. 1990; Richmond and Whalen 2001; Madar et al. 2002; Almécija et al. 2007; Desilva 2010). If Sivapithecus had a narrow torso, and yet was a member of the pongine clade, this means that many of the postcranial apomorphies shared among Pongo, Pan, and Gorilla must represent homoplasies rather than homologies as previously interpreted. Pongo must have evolved a similar torso structure, limb proportions, and other below-branch specializations independently from African apes. This presented paleoanthropologists with the initially uncomfortable realization that the unique locomotor mode essentially shared by extant apes evolved independently, at least twice. Page 9 of 22

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Pierolapithecus The hypothesis that postcranial homoplasy has occurred among extant hominoids is bolstered by the recent discovery of Pierolapithecus catalaunicus from the Middle Miocene of Spain (Moyà Solà et al. 2004). Pierolapithecus was originally interpreted as a basal hominid (Moyà Solà et al. 2004; 2009; Casanovas-Vilar et al. 2008, 2011) but has also been considered a member of the hominine (African ape and human) clade (Begun and Ward 2005; Begun 2009; Begun et al 2012). The vertebrae of Pierolapithecus resemble those of Morotopithecus and, among extant apes, are most like those of hylobatids. It had a high costal angle, revealing that its torso shape was also hominoidlike. It lacked ulnar contact with the carpus, indicating the ability for substantial ulnar deviation. All of these features are also seen in extant hominoids and suggest an orthograde locomotor adaptation involving some climbing at least. However, Pierolapithecus is more primitive than are extant apes in some ways. It lacks some shared specializations of extant great apes, such as dorsally positioned vertebral transverse processes, elongated curved phalanges, some reorganization of the carpus, or a flaring iliac blade as seen in large hominoids (Almécija et al. 2009; Moyà Solà et al. 2004; Alba et al. 2010; Hammond et al. 2013). Still, the vertebrae and pelvic fragment appear to resemble those of hylobatids, which are highly suspensory, and the phalanges are similarly curved to those of chimpanzees, so some features in which the morphology does not resemble all great apes may not mean lack of orthogrady or even suspensory behaviors. Too few elements are known from both Sivapithecus and Pierolapithecus to make extensive direct comparisons, so it is hard to say if they represent an ancestral morphology from which all extant apes evolved. But, because it lacks some of the shared specializations of extant great apes, Pierolapithecus provides more evidence that Pongo is convergent upon African apes in its specialized below-branch arboreal locomotor skeleton.

Oreopithecus Oreopithecus bambolii is a Late Miocene ape from Italy represented by a deformed but nearly complete skeleton, as well as other isolated postcranial elements. It is known from most skeletal elements and has been the subject of intense debate regarding its locomotor behavior (Schultz 1960; Harrison 1986; Sarmiento 1987; Harrison and Rook 1997; Pilbeam 2004; Moyà Solà et al. 1999; Rook et al. 1999). It has even been considered to be bipedal (Straus 1963; Köhler and Moyà Solà 1997; Moyà Solà et al. 1999, 2005; Rook et al. 1999; Macchiarelli et al. 2001), although its vertebral anatomy does not support this hypothesis as the lumbar vertebrae lack dorsal wedging and a caudal increase in interfacet distances (Russo and Shapiro 2013). Furthermore, many of the features argued to suggest bipedality are also found in suspensory mammals (Wunderlich et al. 1999). Oreopithecus has extremely high-intermembral and brachial indices, resembling only those of orangutans. It has five lumbar vertebrae, as do humans and hylobatids, but without a lumbar lordosis (Russo and Shapiro 2013). It had a pelvis that is broader than those of hylobatids with enlarged anterior inferior iliac spines. Its upper thoracic and pectoral girdle morphology is more difficult to assess due to the crushing experienced by the published fossil bones. Oreopithecus also has a relatively large femoral head relative to neck size, associated with extensive hip joint mobility (Ruff 1988). It was clearly adapted for below-branch arboreality, although its metacarpals and phalanges are not particularly long (Moyà Solà et al. 1999; Rook et al. 1999), perhaps suggesting that manual grasping was done between the pollex and medial digits rather than with the hook grip typical of extant apes. This would be yet another example of variations on the below-branch forelimb-dominated theme. Oreopithecus also demonstrates that hominoids can specialize in this type of locomotor behavior without having every specialization seen within any given extant ape taxon. Because of its apomorphic craniodental morphology, the phylogenetic position of Page 10 of 22

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Oreopithecus is debated (Harrison and Rook 1997; Begun et al. 2007; Begun 2009, 2010; Casanovas-Vilar et al. 2011), but it is considered to be a crown hominoid and probably a basal one (Begun et al. 2007; Begun 2009, 2010; Casanovas-Vilar et al. 2011). Thus, its clear adaptation to orthogrady supports the hypothesis that euhominoids were orthograde at least by the Middle Miocene in Europe, although its unusual morphology and unusual environment suggests that some of its extreme suspensory adaptations may represent homoplasies with extant large hominoids.

Dryopithecus Miocene ape fossils from Spain, France, and Hungary until recently were all referred to the genus Dryopithecus but now are recognized as belonging to the distinct genera Dryopithecus, Hispanopithecus, and Rudapithecus (recent review in Begun et al. 2012). Dryopithecus fontani from the Middle Miocene of Spain and France is known postcranially only from some phalanges (Almécija et al. 2011), a proximal femur (Moyà-Solà et al. 2009; Alba et al. 2010; Pina et al. 2011), and two humeri (Lartet 1856; Alba et al. 2010; Alba et al. 2012). Dryopithecus does not appear to have been well adapted for suspensory behaviors, differing from extant apes in having a lower femoral neck-shaft angle and higher trochanter and somewhat curved humeri resembling those of quadrupedal catarrhines.

Hispanopithecus Hispanopithecus catalaunicus is a Late Miocene euhominoid from Spain that appears to have among the most derived postcranial skeleton of any Miocene ape (Begun 1993, 1994b; Moyà Solà and Köhler 1996; Almécija et al. 2007, 2009; Alba et al. 2012). Hispanopithecus has dorsally positioned lumbar transverse processes that arise from the neural arch and are inclined posteriorly, although not as far as in extant great apes (Moyà Solà and Köhler 1996). Its robust femur has a high neck-shaft angle and low trochanter, suggesting adaptation to using the hip in a variety of postures and in many respects is similar to that of orangutans (Köhler and Moyà Solà 1997), and an extant apelike distribution of bone in its femoral neck (Pina et al. 2012). It is not possible to determine how many were originally present. It has long, powerful manual phalanges coupled with short, robust metacarpals and limb proportions similar to those of modern chimpanzees and bonobos (Moyà Solà and Köhler 1996; Almécija et al. 2007, 2009; Alba et al. 2012; Pina et al. 2012). The ulna did not contact the wrist (Begun 1994b; Moyà Solà and Köhler 1996), and the forelimb bones are elongate. Altogether, Hispanopithecus appears to have been orthograde and more highly suspensory than earlier Miocene apes.

Rudapithecus Rudapithecus hungaricus is a Late Miocene ape from Hungary that also is a member of the crown hominid clade. Like Hispanopithecus, Rudapithecus appears to have had numerous adaptations to suspensory behavior. It has long, curved manual phalanges, although these are less robust than seen in Hispanopithecus (Begun 1992, 1993; Kivell and Begun 2009; Begun et al. 2012). The elbow shows signs of considerable mobility, and the femur is short with a large head, as in extant great apes (Begun et al. 2012). The wrist has no contact with the ulna, and there was a deep carpal tunnel suggesting powerful forearm flexors. The Rudapithecus scaphoid and capitate anatomy is similar to those of Hispanopithecus (Kivell and Begun 2009). The pelvis also appears to be quite flaring, as in great apes, although not elongate (Ward et al. 2008). All of this suggests an orthograde, suspensory adaptation, even though its morphology is not identical to any of the other living or fossil apes.

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Conclusion Putting the fossil evidence of locomotor evolution in hominoids together, it appears that an emphasis on deliberate arboreal quadrupedalism with weight support over multiple branches, hereafter referred to as clambering, probably served as a preadaptation for the below-branch specializations of later hominoids, as well as for Morotopithecus. Once the tail was lost, the tail musculature was in a position to become a strong pelvic floor, facilitating more extensive orthogrady. The strong manual and pedal grasping of multiple supports, and relatively mobile limb joints, provided a platform for more frequent hanging below branches, and this in turn would have selected for longer forearms, fingers, and toes, increased capacity for wrist adduction, and reorganization of the torso to enhance forelimb adduction. Knees and elbows would also have been selected to become even more mobile and support loading in a wider variety of postures. All of these morphologies do not come as a thoroughly integrated package, as illustrated by Nacholapithecus. On the other hand, Pierolapithecus and perhaps Morotopithecus show a different suite of adaptations, with a broader rib cage and pelvis and more widely set pectoral girdle yet with a hand and foot that displays shorter phalanges. This pattern is reminiscent of that seen in extant great apes and to a lesser extent Oreopithecus and Dryopithecus. These variations underscore the growing realization that hominoids evolved below-branch arboreal adaptations more than once. Combining fossil data with data from extant apes, it seems increasingly likely that many of the postcranial and locomotor specializations of great apes may have evolved from ancestors that were more generalized, although not, perhaps, as generalized as basal hominoids like Proconsul. The hypothesis that such homoplasy has possibly occurred multiple times within the Hominoidea is becoming more and more well supported by increased evidence. All hominoids likely evolved from similar ancestors with a deliberate clambering mode of positional behavior. With similar selective pressures to exploit terminal branch arboreal settings, selection favored similar adaptations. Ateline monkeys resemble hominoids in having a slightly reduced lumbar region, broader thoracic cage, longer clavicle, mobile limb joints, and other adaptations to frequent suspension. Epipliopithecus also resembled lesser apes in its semisuspensory adaptations (Zapfe 1960) yet bears no close phylogenetic relation to apes. The Sivapithecus dilemma initially appeared to suggest that perhaps postcranial anatomy could not be used to make phylogenetic inferences among hominoids. However, more recent discoveries of partial skeletons of Equatorius, Nacholapithecus, Pierolapithecus, and Hispanopithecus, as well as multiple postcranial elements known for Rudapithecus, show that, while there indeed may be postcranial homoplasy, the variation among these taxa is greater than supposed. Patterns of similarities and differences can, in fact, inform phylogenetic understanding, and so the understanding of the patterns of selection that led to the evolution of various hominoid taxa. Once paleoanthropologists can accurately interpret the phylogenetic relations among these taxa, they can reconstruct vectors of morphological change within clades. These vectors, in turn, will provide a record of the directional selection that shaped the various lineages. This provides us the opportunity to interpret the pressures that led to the observed morphological change and thus why different hominoid taxa evolved, which is what paleoanthropologists want to know above all. The current picture of hominoid postcranial evolution is, therefore, one of recurring homoplasy. Different taxa represent different experiments in exploiting terminal branch arboreal habitats at relatively large body sizes, which requires the distribution of weight among different supports. Extant apes have all done this in somewhat different ways as did fossil ones. So rather than thinking about progressive stages evolving from an ancestral taxon like Proconsul to one like a modern great ape, researchers need to refocus their efforts and to explore the detailed similarities and differences Page 12 of 22

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among this growing collection of fossil ape skeletons to explore the diversity of locomotor adaptations within hominoids. The presence of homoplasy in hominoid evolution must not be looked at as an all-or-none phenomenon. This approach to considering morphology is perhaps most visible to anthropologists in the origin of hominins. At present, there is no reason to assume that the most recent chimpanzee-human ancestor had such a dramatically stiffened torso, narrow cranial thorax with cranially oriented glenoid fossae and narrow scapula, or long metacarpals, and it may or may not have been a knuckle walker when terrestrial. Instead, a slightly less derived ancestor, perhaps something like Pierolapithecus or Oreopithecus in torso morphology and perhaps other characters, might be a more reasonable guess. Only more careful morphological analysis of known fossils, comparative anatomical study of extant apes, and of course discoveries of new fossils will lead to a better resolution of the ancestral condition. Australopithecus differs from later hominins in retaining morphologies that evolved as adaptations to arboreal locomotion yet shows unequivocal strong selection for habitual terrestrial bipedality. The adaptive significance of these primitive morphologies is inherently unknowable. The extent to which Australopithecus and even earlier hominins, such as Ardipithecus, Orrorin, and Sahelanthropus, differed from the last common ancestor reveals the vector of selection that shaped hominin origins. All of these fossils indicate that the last common ancestor of them all was likely largely orthograde and adapted for some amount of vertical climbing and perhaps suspension. That Australopithecus evolved from a highly derived African apelike ancestor adapted to knuckle walking appears less and less likely. Rather, mounting evidence from the Miocene suggests that the australopith ancestor was orthograde, not a terrestrial quadruped (also see recent review in Crompton et al. 2008). If so, anthropologists may need to revisit the perennial question about australopith origins: the idea that hominins were selected to stand up on two legs from all fours. Rather, considering the evidence from the Miocene, including the Late Miocene hominin Ardipithecus (Lovejoy et al. 2009), the question that perhaps should be asked is, “why did early hominins remain orthograde when they began exploiting terrestrial niches?” To understand why our own lineage diverged from that of other apes, it is necessary first to understand the ancestral morphology from which hominins evolved. Only then can paleoanthropologists determine, for example, whether australopith forearms reduced from the primitive condition or not. The expanding hominoid fossil record affords us ever more opportunities to appreciate the diversity, past and present. What may seem at first like an increasingly confusing picture of homoplasy must be viewed as an opportunity to obtain a more accurate and nuanced understanding of the adaptive diversity present throughout the hominoid radiation.

Cross-References ▶ Defining Hominidae ▶ Dental Adaptations of African Apes ▶ General Principles of Evolutionary Morphology ▶ Geological Background of Early Hominid Sites in Africa ▶ Hominin Paleodiets: The Contribution of Stable Isotopes ▶ Hominoid Cranial Diversity and Adaptation ▶ Homology: A Philosophical and Biological Perspective ▶ Potential Hominoid Ancestors for Hominidae

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_34-3 # Springer-Verlag Berlin Heidelberg 2014

▶ Principles of Taxonomy and Classification: Current Procedures for Naming and Classifying Organisms ▶ The Earliest Primitive Hominids ▶ The Origins of Bipedal Locomotion ▶ The Species and Diversity of Australopiths

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Kelley J (2002) The hominoid radiation in Asia. In Hartwig W, Ed. The primate fossil record. Cambridge University Press, Cambridge, pp 369–384. Kivell TL, Begun DR (2009) New primate carpal bones from Rudabánya (late Miocene, Hungary): taxonomic and functional implications. J Hum Evol 57:697–709 Kivell TL, Schmitt D (2009) Independent evolution of knuckle-walking in African apes shows that humans did not evolve from a knuckle-walking ancestor. Proc Natl Acad Sci 106:14241–14246 Knussmann VR (1967) Humerus ulna und radius der simiae. S. Karger, Basel Köhler M, Moyà Solà S (1997) Ape-like or hominid-like? The positional behavior of Oreopithecus bambolii reconsidered. Proc Natl Acad Sci U S A 94:11747–11750 Kunimatsu Y, Nakatsukasa M, Sawada Y, Sakai T, Hyodo M, Hyodo H, Itaya T, Nakaya H, Saegusa H, Mazurier A, Saneyoshi M, Tsujikawa H, Yamamoto A, Mbua M. (2007) A new Late Miocene great ape from Kenya and its implications for the origins of African great apes and humans. Proc Natl Acad Sci USA 104:19220–19225. Larson SG (1988) Parallel evolution in the hominoid trunk and forelimb. Evol Anthropol 6:87–99 Larson SG (1993) Functional morphology of the shoulder in primates. In: Gebo D (ed) Postcranial adaptation in nonhuman primates. Northern Illinois University Press, DeKalb, pp 45–69 Lartet E (1856) Note sur un grand singe fossile qui se rattache au groupe des singes superieurs. C R Acad Sci (Paris) 43:219–223 Leakey M, Walker A (1997) Afropithecus: function and phylogeny. In: Begun DR, Ward CV, Rose MD (eds) Function phylogeny and fossils: Miocene hominoid evolution and adaptations. Plenum Press, New York, pp 225–239 Lewis OJ (1971) Brachiation and the early evolution of the Hominoidea. Science 230:577–578 Lewis OJ (1972) Evolution of the hominoid wrist. In: Tuttle RH (ed) The functional and evolutionary biology of primates. Aldine-Atherton, Chicago, pp 207–222 Lewis OJ (1989) Functional morphology of the evolving hand and foot. Oxford University Press, Oxford Lovejoy CO, Suwa G, Simpson SW, Matternes JH, White TD (2009) The great divides: Ardipithecus ramidus reveals the postcrania of our last common ancestors with African apes. Science 326:73–106 Macchiarelli R, Rook L, Bondioli L (2001) Comparative analysis of the iliac trabecular architecture in extant and fossil primates by means of digital image processing techniques: implications for the reconstruction of fossil locomotor behaviours. In: Agustí J, Rook L, Andrews P (eds) Hominoid evolution and climatic change in Europe. Cambridge University Press, Cambridge, pp 60–101 MacKinnon J (1974) In search of the red ape. Collins, London MacLatchy LM (2004) The oldest ape. Evol Anthropol 13:1–14 MacLatchy M, Gebo D, Kityo R, Pilbeam D (2000) Postcranial functional morphology of Morotopithecus bishopi with implications for the evolution of modern ape locomotion. J Hum Evol 39:159–183 Madar SI, Rose MD, Kelley J, MacLatchy L, Pilbeam D (2002) New Sivapithecus postcranial specimesn from the Siwaliks of Pakistan. J Hum Evol 42:705–752. McCrossin ML (1997) New postcranial remains of Kenyapithecus and their implications for understanding the origins of hominoid terrestriality. Am J Phys Anthrop Suppl 24:164 McCrossin ML, Benefit BR (1997) On the relationships and adaptations of Kenyapithecus a largebodied hominoid from the Middle Miocene of Eastern Africa. In: Begun DR, Ward CV, Rose MD (eds) Function phylogeny and fossils: Miocene hominoid evolution and adaptations. Plenum Press, New York, pp 241–267

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Miller RA (1932) Evolution of the pectoral girdle and forelimb in the primates. Am J Phys Anthropol 17:1–56 Moyà Solà S, Köhler M (1995) New partial cranium of Dryopithecus lartet 1863 (Hominoidea, Primates) from the upper Miocene of Can Llobateres, Barcelona, Spain. J Hum Evol 29:101–139 Moyà Solà S, Köhler M (1996) A Dryopithecus skeleton and the origins of great-ape locomotion. Nature 379:156–159 Moyà Solà S, Köhler M, Rook L (1999) Evidence of hominid-like precision grip capability in the hand of the Miocene ape Oreopithecus. Proc Natl Acad Sci U S A 96:313–317 Moyà Solà S, Köhler M, Alba DM, Casanovas-Vilar I, Galindo J (2004) Pierolapithecus catalaunicus, a new Middle Miocene great apes from Spain. Science 306:1339–1344 Moyà-Solà S, Köhler M, Rook L (2005) The Oreopithecus thumb: a strange case in hominoid evolution. J Hum Evol 49:395–404 Moyà-Solà S, Köhler M, Alba DM, Casanovas-Vilar I, Galindo J, Robles JM, Cabrera L, Garcés M, Almécija S, Beamud E (2009) First partial face and upper dentition of the middle Miocene hominoid Dryopithecus fontani from Abocador de Can Mata (Vallès-Penedès Basin, Catalonia, NE Spain): taxonomic and phylogenetic implications. Am J Phys Anthropol 139:126–145 Nakatsukasa M (2003a) Comparative and functional anatomy of phalanges in Nacholapithecus kerioi, a Middle Miocene hominoid from northern Kenya. Primates 44:371–412 Nakatsukasa M (2003b) Definitive evidence for tail loss in Nacholapithecus, an East African Miocene hominid. J Hum Evol 45:179–186 Nakatsukasa M (2008) Comparative study of Moroto vertebral specimens. J Hum Evol 55:581–588 Nakatsukasa M, Yamanaka A, Kunimatsu Y, Shimizu D, Ishida H (1998) A newly discovered Kenyapithecus skeleton and its implications for evolution of positional behavior in Miocene East African hominoids. J Hum Evol 34:657–664 Nakatsukasa M, Ward CV, Walker A, Teaford MF, Kunimatsu Y, Ogihara N (2004) Tail loss in Proconsul heseloni. J Hum Evol 46:777–784 Nakatsukasa M, Kunimatsu Y, Nakano Y, Ishida H (2007) Vertebral morphology of Nacholapithecus kerioi based on KNM-BG 35250. J Hum Evol 52:347–369 Napier J, Davis P (1959) The forelimb skeleton and associated remains of Proconsul africanus. Foss Mamm Afr 16:1–70 Oxnard CE (1984) The order of man. Yale University Press, New Haven Pickford M, Ishida H, Nakano Y, Yasui K (1987) The middle Miocene fauna from the Nachola and Aka Aiteputh Formations Northern Kenya. Afr Stud Monogr 5(Suppl):141–154 Pilbeam D (2002) Perspectives on the Miocene Hominoidea. In: Hartwig WC (ed) The primate fossil record. Cambridge University Press, Cambridge, pp 303–310 Pilbeam D (2004) The anthropoid postcranial axial skeleton: comments on development, variation and evolution. J Exp Zool B Mol Dev Evol 302:241–267 Pilbeam D, Young NM (2001) Sivapithecus and hominoid evolution: some brief comments. In: de Bonis L, Koufos GD, Andrews P (eds) Hominoid evolution and climate change in Europe. Phylogeny of the Neogene hominoid primates of Eurasia, vol 2. University Press Cambridge, Cambridge, pp 349–364 Pilbeam D, Rose MD, Badgley C, Lipschultz B (1990) New Sivapithecus humeri from Pakistan and the relationship of Sivapithecus and Pongo. Nature 348:237–239 Pina M, Alba DM, Almécija S, Moyà-Solà S (2011) Is the cortical thickness of the femoral neck a diagnostic trait for inferring bipedalism? Paleontol Evol Memòria especial núm 5:313–317 Pina M, Alba DM, Almécija S, Fortuny J, Moyà-Solà S (2012) Brief communication: paleobiological inferences on the locomotor repertoire of extinct hominoids based on femoral neck cortical Page 18 of 22

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thickness: the fossil great ape Hispanopithecus laietanus as a test-case study. Am J Phys Anthropol 149:142–148 Remis M (1995) Effects of body size and social context on the arboreal activities of lowland gorillas in the Central African Republic. Am J Phys Anthropol 97(4):413–433 Richmond BG, Whalen M (2001) Forelimb function, bone curvature and phylogeny of Sivapithecus. In: de Bonis L, Koufos G, Eds. Eurasian neogene hominoid phylogeny. Cambridge University Press, Cambridge, pp 326–348. Rook L, Bondioli L, Köhler M, Moyà Solà S, Macchiarelli R (1999) Oreopithecus was a bipedal ape after all: evidence from the iliac cancellous architecture. Proc Natl Acad Sci USA 96(15):8795–8799 Rose MD (1986) Further hominoid postcranial specimens from the late Miocene Nagri Formation of Pakistan. J Hum Evol 15:333–367 Rose MD (1988) Another look at the anthropoid elbow. J Hum Evol 17:193–224 Rose MD (1997) Functional and phylogenetic features of the forelimb in Miocene hominoids. In: Begun DR, Ward CV, Rose MD (eds) Function phylogeny and fossils: Miocene hominoid evolution and adaptations. Plenum Press, New York, pp 79–100 Rose MD, Nakano Y, Ishida H (1996) Kenyapithecus postcranial specimens from Nachola, Kenya. Afr Stud Monogr 24(Suppl):3–56 Ruff CB (1988) Hindlimb articular surface allometry in Hominoidea and Macaca, with comparisons to diaphyseal scaling. J Hum Evol 17:687–714 Russo GA, Shapiro LJ (2013) Reevaluation of the lumbosacral region of Oreopithecus bambolii. J Human Evol 65:253–265 Sanders WJ, Bodenbender BE (1994) Morphometric analysis of lumbar vertebra UMP 67–28: implications for spinal function and phylogeny of the Miocene Moroto hominoid. J Hum Evol 26:203–237 Sarmiento EE (1985) Functional differences in the skeleton of wild and captive orangutans and their adaptive significance, Ph.D. dissertation, New York University, New York Sarmiento EE (1987) The phylogenetic position of Oreopithecus and its significance in the origin of the Hominoidea. Am Mus Nov 2881:1–44 Sarmiento EE (1988) Anatomy of the hominoid wrist joint: its evolutionary and functional implications. Int J Primatol 9:281–345 Schultz AH (1930) The skeleton of the trunk and limbs of higher primates. Hum Biol 2:303–438 Schultz AH (1937) Proportions variability and asymmetries of the long bones of the limbs and clavicles of primates. Hum Biol 9:281–328 Schultz AH (1960) Einige Beobachtungen und Maße am Skelett von Oreopithecus im Vergleich mit anderen catarrhinen Primaten. Z Morphol Anthropol 50:136–149 Schultz AH (1961) Vertebral column and thorax. Primatologia 4:1–66 Schultz AH (1969a) The life of primates. Universe Books, New York Schultz AH (1969b) Observations on the acetabulum of primates. Folia Primatol 11:181–199 Schultz AH, Straus WL (1945) The number of vertebrae in primates. Proc Am Philosoph Soc 89:601 Senut B, Nakatsukasa M, Kunimatsu Y, Nakano Y, Takano T, Tsujikawa H, Shimizu D, Kagaya M, Ishida H (2004) Preliminary analysis of Nacholapithecus scapula and clavicle from Nachola Kenya. Primates 45:97–104 Shapiro L (1993) Functional morphology of the primate lumbar spine. In: Gebo D (ed) Postcranial adaptation in nonhuman primates. Northern Illinois Press, DeKalb, pp 121–149

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Sherwood RJ, Ward S, Hill A, Duren DL, Brown B, Downs W (2002) Preliminary description of the Equatorius africanus partial skeleton (KNM-TH 28860) from Kipsaramon Tugen Hills Baringo District Kenya. J Hum Evol 42:63–73 Slijper EJ (1946) Comparative biologic-anatomical investigations on the vertebral column and spinal musculature of mammals. Verh Kon Ned Akad Wet. 42: Series 2: 1–128 Sonntag CF (1923) On the anatomy physiology and pathology of the chimpanzee. Proc Zool Soc (Lond) 22:323–429 Sonntag CF (1924) On the anatomy physiology and pathology of the orang-outan. Proc Zool Soc (Lond) 24:349–450 Straus WL (1963) The classification of Oreopithecus. In: Washburn SL (ed) Classification and human evolution. Aldine, Chicago, pp 146–177 Suwa G, Kono RT, Shigehiro K, Asfaw B, Beyene Y (2007) A new species of great ape from the late Miocene epoch in Ethiopia. Nature 448:921–924 Swartz SM, Bertram JAE, Biewener AA (1989) Telemetered in vivo strain analysis of locomotor mechanics of brachiating gibbons. Nature 342:270–272 Swindler DR, Wood CD (1973) An atlas of primate gross anatomy. Krieger, Malabar Tuttle R, Watts DR (1985) The positional behavior and adaptive complexes of Pan gorilla. In: Kondo S (ed) Primate morphophysiology, locomotor analysis and human bipedalism. University of Tokyo Press, Tokyo, pp 261–288 Walker A (1997) Proconsul: function and phylogeny. In: Begun DR, Ward CV, Rose MD (eds) Function phylogeny and fossils: Miocene hominoid evolution and adaptations. Plenum Press, New York, pp 209–224 Walker A, Rose MD (1968) Fossil hominoid vertebra from the Miocene of Uganda. Nature 217:980–981 Ward CV (1992) Hip joints of Proconsul nyanzae and P. africanus. Am J Phys Anthropol Suppl 14:171 Ward CV (1993) Torso morphology and locomotion in Proconsul nyanzae. Am J Phys Anthropol 92:291–328 Ward CV (1997) Functional anatomy and phyletic implications of the hominoid trunk and hindlimb. In: Begun D, Ward CV, Rose MD (eds) Function, phylogeny and fossils: Miocene hominoid evolution and adaptations. Plenum Press, New York, pp. 101–130 Ward SC (1997) The taxonomy and phylogenetic relationships of Sivapithecus revisited. In: Begun DR, Ward CV, Rose MD (eds) Function phylogeny and fossils: Miocene hominoid evolution and adaptations. Plenum Press, New York, pp 269–290 Ward SC, Brown B (1986) The facial skeleton of Sivapithecus indicus. In Swindler DR, Erwin J (Eds) Comparative primate biology, Alan R. Liss, New York, pp 413–452. Ward CV (1998) Afropithecus, Proconsul and the primitive hominoid postcranium. In: Strasser E, Fleagle J, Rosenberger AL, McHenry HM (eds) Primate locomotion: recent advances. Plenum Press, New York, pp 337–352 Ward S, Duren DL (2002) Middle and late Miocene African hominoids. In: Hartwig WC (ed) The primate fossil record. Cambridge University Press, Cambridge, pp 385–398 Ward CV, Walker A, Teaford MF (1991) Proconsul did not have a tail. J Hum Evol 21:215–220 Ward CV, Walker A, Teaford MF, Odhiambo I (1993) A partial skeleton of Proconsul nyanzae from Mfangano Island Kenya. Am J Phys Anthropol 90:77–111 Ward S, Brown B, Hill A, Kelley J, Downs W (1999) Equatorius: a new hominoid genus from the Middle Miocene of Kenya. Science 285:1382–1386

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Ward CV, Begun D, Kordos L (2008) A new partial pelvis of Dryopithecus brancoi from Rudabanya, Hungary. Am J Phys Anthropol Suppl 46:218 Waterman HC (1929) Studies on the evolution of the pelvis of man and other primates. Am Mus Nat Hist Bull 58:585–642 Whitehead PF (1993) Aspects of the anthropoid wrist and hand. In: Gebo D (ed) Postcranial adaptation in nonhuman primates. Northern Illinois University Press, DeKalb, pp 96–120 Wunderlich RE, Walker A, Jungers WL (1999) Rethinking the positional repertoire of Oreopithecus. Am J Phys Anthropol 28:282 Young NM (2003) A reassessment of living hominoid postcranial variability: implications for ape evolution. J Hum Evol 45:441–464 Young NM, MacLatchy LM (2004) The phylogenetic position of Morotopithecus. J Hum Evol 46:163–184 Zapfe H (1960) Die Primatenfunde aus der miozanen Spaltenf€ ullung von Neudorf an der March (Devinská Nová Ves), Tschechoslowakei. Schweiz Paleontol Abhand 78:1–293

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_34-3 # Springer-Verlag Berlin Heidelberg 2014

Index Terms: Afropithecus 4 Dryopithecus 11 Equatorius 8 Femur 7, 11 Griphopithecus 9 Hispanopithecus 11 Hominoid locomotion 1, 9 Homoplasy 1, 10, 12 Intermembral index 5 Kenyapithecus 8 Miocene hominoids 4, 7, 9–11 Morotopithecus 7 Nacholapithecus 8 Oreopithecus 10 Pelvis 5, 11 Phalanges 6, 10 Pierolapithecus 10 Postcranial adaptations 1, 5, 7, 9, 12 Proconsul 4 Rudapithecus 11 Sivapithecus 9 Suspension 1 Ulnocarpal contact 6 Vertebrae 3, 5, 10

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

Hominoid Cranial Diversity and Adaptation Alan Bilsborougha* and Todd C. Raeb a Department of Anthropology, University of Durham, Durham, UK b Department of Life Sciences, University of Roehampton, London, UK

Abstract The hominoid cranium represents a tightly constrained, functionally and developmentally integrated structure subject to multiple selective influences. Modern apes are the remnant of a much more diverse radiation, raising issues about their suitability as models for earlier hominoids. Among gibbons the folivorous siamang is cranially distinctive. The markedly airorynchous Pongo is cranially highly variable and lacks the anterior digastric muscle, thereby contrasting with other hominoids (except Khoratpithecus). African apes share a common cranial pattern differentiated by varying growth rates, not duration. Airorhynchy is common among fossil hominoids and differentiates hominoids from non-hominoids, suggesting that African ape klinorhynchy is derived. Bonobos are cranially smaller, lighter, and less dimorphic than chimpanzees. These are comparatively uniform, with extensive overlap between subspecies, whereas gorillas display considerable contrasts, especially between east and west populations. Early Miocene hominoids are already cranially diverse, with most species probably soft- or hard-fruit feeders. Middle and Late Miocene forms from Africa, Europe, and Western Asia are thicker enameled with more strongly constructed crania suggesting harder diets, although Dryopithecus (soft frugivory) and Oreopithecus (folivory) are exceptions. South and East Asian fossil hominoid diets ranged from soft fruits through harder items to bulky, fibrous vegetation. All extant ape crania are relatively lightly constructed compared with fossil forms, again prompting questions about their suitability as adaptive models of earlier hominoids.

Introduction The hominoid fossil record has expanded markedly over the last two decades, sufficiently to indicate marked morphological diversity. This in turn reflects a major radiation or, more likely, series of radiations. The great bulk of the material is from Miocene contexts – apart from hominins there is still comparatively little from Plio-Pleistocene deposits – so that fossil and living hominoids are largely detached from one another. Whatever the details of this array, it is clear that the extant nonhuman apes represent but the surviving fragment of a significantly more numerous, geographically more extensive, and ecologically more diverse group of catarrhine primates. The extremely restricted modern comparative base and its (at best) tenuous links with the earlier material pose real challenges for adaptive and phylogenetic interpretations of the fossil hominoid record. An outcome of this is that detailed phylogenies often differ appreciably from author to author, depending on the significance accorded to particular apomorphies and on the extent to which other similarities are deemed homoplasies. The upshot is a whole series of individual phylogenies and widespread disagreement about the status of particular groups which usually translate through into *Email: [email protected] Page 1 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

the taxonomies preferred by individual researchers. Since the thrust of this chapter is primarily adaptational, we do not concern ourselves with taxonomic or phylogenetic details; in what follows suprageneric categories are used informally and generally follow majority consensus usage. For those requiring more detailed information on phylogenetic issues concerning the Miocene hominoid record, the chapters by Begun, Ward, etc., in volume 2, and the papers by Harrison (2002), and contributors in Hartwig (2002) are excellent recent surveys. Cranial form is influenced by multiple factors. Functionally, the head houses the visual, olfactory, and auditory organs and those of vocalization, taste, and balance; it contains the openings for the respiratory and alimentary tracts; and it houses and protects the brain. It incorporates structures for food acquisition and processing, while postural and respiratory factors influence basicranial morphology. Its superficial tissues may be patterned and convey information to conspecifics about sex and ontogenetic status. The interplay of these features, and especially the size and configuration of those concerned with food processing relative to neurocranial proportions, may lead to the development of external structures such as crests and tori on the skull. There are clearly intense selection pressures determining effective developmental and functional integration of these varied aspects of cranial function throughout the individual life cycle. Fleagle et al. (2010) undertook a 3D geometric morphometric study (Procrustes and Principal Components Analysis) of primate crania to quantify broad aspects of cranial diversity. Their first PC differentiated on cranial flexion, orbit size and orientation, and relative brain size, while PC 2 reflected differences in cranial height and snout length. Eulemur, Mandrillus, Pongo, and Homo represent the limits in cranial shape. Overall, hominoids display the greatest diversity in cranial shape among extant primate clades, although much of this is driven by the atypical and highly distinctive cranium of H. sapiens. Adult African apes including humans, known as hominids, share a broadly common pattern of covariation in cranial traits, with the oral and zygomatic regions primary integrative influences and with a lesser contribution from the nasal region, i.e., those craniofacial components primarily associated with mastication (Ackermann 2002, 2005). This differs from the pattern in both Old and New World monkeys, in which the oral region is the exclusive primary contributor to facial integration. Ackermann suggests that this contrast may reflect innovatory functional or developmental shifts after the differentiation of hominoids from other Anthropoidea or be an allometric consequence of increased body size. Orangutans and gibbons were not represented in the analyses, but the extent to which they share the primary oral/zygomatic integrative pattern should help decide between these possibilities and assist in determining whether the pattern is a hominoid or hominid synapomorphy. There are similar allometric patterns in the midface and common opposite relationships between lower and upper face in the adults. Whereas visual inspection and morphological distance place adult Pan troglodytes and Gorilla gorilla close together and Homo sapiens distant, craniofacial covariation patterns accord with molecular data in indicating closer affinity between P. troglodytes and H. sapiens, with G. gorilla distant (Ackermann 2002). Such concordance, however, does not hold throughout ontogeny, with differing patterns of affinity between juveniles and subadults of the above taxa on the one hand and infants and “adolescents” on the other (Ackermann 2005). Nonetheless, some general patterns emerge: in particular, across the species earlier and later (subadult and adult) integration appears to reflect different drivers. Oral integration is especially influential in the earlier stages, as well as thereafter, but there are specific differences in the onset of zygomatic integration. In P. paniscus and P. troglodytes, it appears during the juvenile/adolescent periods, whereas in Gorilla it occurs from infancy, perhaps a correlate of its rapid growth. In all species, zygomatic integration intensifies in later ontogeny. Where evident, nasal integration occurs Page 2 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

in mid-/late ontogeny, its intensity varying inversely with oral integration, suggesting that separate developmental modularities underlie these regions. While the most highly integrated species as adults, humans are more developmentally labile than the other African apes prior to maturity. While differing in detail, however, all species show a common pattern of intensified integration throughout development, with a particular shift toward more constrained variation around sexual maturity or just after. The extent to which these similarities reflect shared, genetically determined, developmental pathways, or common selection pressures associated with vital functional requirements – the need for effective food processing mechanisms, for instance – remains to be determined. In the latter case, some proportion of the resemblance could be homoplastic. A recent study by Singh et al. (2012) based on covariation in 56 morphometric landmarks representing the functional modules of the face, vault, and basicranium (Moss and Young 1960; Moss 1973) extends the analysis of cranial integration to include Pongo as well as the African apes. The results point to complex integrated shape changes, but despite marked contrasts in adult cranial morphology, all species display close similarities in covariation patterns between the face, basicranium, and vault. The implication is that the pattern of hominoid cranial integration has been conserved at least since the separation of the Asian ape and hominid clades, presumably due to strong stabilizing selection constraining developmental processes. While some cranial features are relatively invariant in catarrhines (e.g., positioning of orbits; structure of the auditory region), others (e.g., orbital size and shape) are highly variable within genera, species, and even subspecies (Seiffert and Kappelman 2001). Some features seem to be determined less by their “primary” function than by influences reflecting the interactions of other functional systems; e.g., the size and proportions of the orbits appear to be determined more by the growth trajectories of the mid- and upper face and by requirements to resist the biomechanical forces generated by food processing as they affect those regions than by the dimensions of the visual organs housed within them (Schultz 1940). Other traits (e.g., the structure of the nasal floor and premaxilla/ palatal relationships; Ward and Kimbel 1983; Ward and Pilbeam 1983) exhibit contrasts, the functional basis of which is poorly understood, but which serve as useful phylogenetic indicators (see below). The compilation of long lists of character states as the raw data for computer-based cladistic analyses has been criticized by some (Rak 1983; Suwa et al. 1997; Asfaw et al. 1999, 2002) as resulting in the fragmentation or “atomization” of morphology as multiple discrete traits, rather than an integrated whole. It is therefore worth noting here the recent accounts that stress the importance of broader functional and developmental perspectives in analyzing morphology and its evolutionary/ phylogenetic and adaptive contexts (Lovejoy et al. 1999, 2003; Lieberman et al. 2000a, b; McCollum and Sharpe 2001; Rae and Koppe 2000; Ackermann 2002, 2005; Singh et al. 2012). These build upon earlier studies such as those of Moss and Young (1960), Moss (1973), Enlow (1968, 1990), and Cheverud (1982, 1996); and biomechanical analyses such as that of Endo (1966); see also Rak (1983). An example of this approach is McCollum’s analysis of Paranthropus cranial morphology (McCollum 1997, 1999; McCollum and Sharpe 2001), which concludes that limited changes in the relative growth rates of jaws and teeth on the one hand and of the orbit and upper face on the other would be sufficient to produce in mature individuals the distinctive set of features that characterize the robust australopithecine cranium/face. Such growth rate changes are doubtless under simple, limited genetic control and, as such, are readily elicited in appropriate selective contexts. It is not difficult to envisage comparable pressures operating on Miocene hominoids, and so a variety of cranial forms thereby rapidly resulting from relatively limited genetic changes. So, for example, the contrasting morphologies of Proconsul and Afropithecus might both be derived relatively simply Page 3 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

from an Oligocene precursor such as Aegyptopithecus, and purely phenetic measures of affinity between these forms could be seriously awry as indicators of phylogenetic relationship. One outcome of cladistic studies has been the general recognition of the pervasiveness of homoplasy in the fossil record. From an adaptive perspective, instances of homoplasy can provide important clues as to the contexts of, and likely selective forces impacting on, hominoid communities. In such cases, the influence of phylogenetic constraint and contingency may be considerable. Minor initial differences between spatially distributed populations of a single species (or of closely related species), when further influenced by bottlenecking or other stochastic factors – easily occurring in small, localized arboreal groups, where gaps in tree cover impede gene flow – may result in significantly different morphological outcomes as responses to common selection pressures associated with similar niches. The evolution from the nasal/palatal structure seen in Proconsul and other Early Miocene forms of distinct anatomical configurations for that region in Middle/Late Miocene Afro-European and Asian hominoids may be an example of such a process and its outcomes. A fundamental division of extant hominoids is that between gibbons (hylobatids) and largebodied apes – the Asian orangutan (Pongo) and the African chimpanzee and bonobo (Pan), gorilla (Gorilla), and human (Homo), although the last taxon will be discussed elsewhere. Pongo and Pan are both largely frugivorous, with common dental adaptations (large anterior teeth and relatively small check teeth with enamel wrinkling) but differing in cranial features, whereas the more herbivorous Gorilla closely resembles Pan cranially despite its contrasting dietary niche (see below). These differing patterns of affinity illustrate the importance of developmental constraints and phylogenetic inertia in determining morphology and thus the lack of any necessary one-to-one correspondence between morphology and adaptation (for further discussion of this, see below). It is possible in principle to extend the limited insights provided by the few extant great apes into the earlier radiation by supplementing them with modeling based on early hominins, which can be thought of as phenetically and adaptively “apes” in some respects. Apart from the dangers of circular reasoning (using modern ape data as inputs into constructing early hominin models that are then used to “extend” the ape comparator base) and the appropriateness of such models (what form and degree of terrestrial orthogrady, if any, is compatible with using hominins as analogues for non-hominins?), however, there are major issues of contextual relevance. All extant apes (here and throughout meaning non-hominin hominoids) and early hominins are essentially from tropical contexts (forest, woodland, and savannah) with none present in higher latitudes, reflecting a comparatively narrow environmental range compared with earlier ape habitats. Even incorporating early hominins within the comparator base provides a time depth of little more than 4+ Myr, characterized by broadly modern faunas that include groups rare or absent in the earlier record. In contrast, Miocene hominoids are components of markedly distinct and diverse faunas, often including entire mammalian families now extinct. So community relationships within earlier faunas will have differed from contemporary ecological webs, and the place(s) of earlier hominoids in their ecological communities are unlikely to correspond closely to those of modern ape analogues. An obvious primate example of this is the expansion and radiation of cercopithecoids over the last 10 Myr or thereabouts, so forming a major dimension of the community ecology of all recent hominoids, unlike that of earlier taxa. Floral communities also fluctuated as climatic conditions changed, with notable contrasts between Early to Middle Miocene habitats and those of the Late Miocene and Pliocene. Against these differentiating features are some factors that make for modeling continuity: the range of potential (plant) food items is limited, and their physical properties even more so, limiting the nature and magnitude of the masticatory forces influencing hominoid cranial morphology. Page 4 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

Metabolic and biomechanical constraints on body size and on locomotor form and activity, allometric influences on growth, and the functional and developmental interdependences of cranial form noted above all allow for a more comparative approach to hominid cranial variation. Below we review the probable ancestral condition for Hominoidea, then examine some aspects of cranial form in extant nonhuman hominoids before summarizing craniodental information on the more complete fossil forms.

Ancestral Hominoid Cranial Morphology The combination of outgroup analysis of extant forms and the morphology of stem catarrhines provides an indication of the ancestral hominoid cranial morphotype. The Fayum fossil primates represent an early diversification of basal catarrhines, presumably reflecting dietary specialization. For example, the small and dentally and gnathically primitive Catopithecus (35.5–36 Ma) combines the characteristic 2.1.2.3 dental formula, postorbital closure (primarily formed from the zygomatic), fused frontals, and C1/P3 honing facet with triangular upper molars with only limited hypocone development and lower molars with high trigonids and sharp crests. Catopithecus had a deep and projecting face, with an especially broad premaxilla; small, widely separated orbits; and a small neurocranium with anteriorly prominent temporal lines merging to form a sagittal crest along the rear half of the vault and well-developed nuchal crests. The tympanic region is like that of platyrrhines, not catarrhines, and the mandibular symphysis is unfused. The anterior dentition displays broad, spatulate incisors and projecting, dimorphic canines, suggesting a predominantly frugivorous niche. Many of these features, including the contribution of the premaxilla to facial proportions, small neurocranium with marked muscle attachments and pronounced ectocranial cresting, and ceboidlike tympanic region, are also seen in the younger (33.1–33.4 Mya) and dentally more derived propliopithecid Aegyptopithecus. The zygomatic is again deep and the face in general strongly constructed, with a characteristic angled profile, and the mandibular symphysis is fused. The gonial region is strongly constructed and the ramus broad and high. The interorbital distance is again broad, with bony septa separating the high, narrow orbits and the interorbital region projects anteriorly from the medial orbital margins. Semicircular supraorbital tori extend over each orbit and, meeting medially, anteriorly bound a diamond-shaped frontal planum, whose posterior limits are defined by the anterior temporal lines. The anterior teeth are small compared to the postcanine dentition, making a narrow anterior palate. The molars are inflated and highly bunodont, especially the second, and the elongated lower third molar has a centrally placed hypoconulid; the trigonid is reduced in occlusal area and height and lacks the paraconid, while the talonid is expanded with a large distal fovea. The upper molars are quadritubercular, with a well-developed hypocone. There is marked canine dimorphism, with upper canine honing capabilities increased by a lengthening of the anterior surface of P3. Overall morphology points to the generation of greater occlusal pressures than in Catopithecus and a craniofacial form better able to withstand the resulting forces. When the details of stem catarrhine facial morphology are considered with the evidence from extant outgroups of the Catarrhini (e.g., Platyrrhini), it is possible to infer the major changes that underlie the ancestral hominoid craniofacial skeleton. Unlike stem catarrhines or platyrrhines, hominoids are characterized by a palate that is wide at the level of the canines, nasals that are nonprojecting and lie near the medial orbital margin in transverse section, and a premaxillomaxillary suture that contacts the nasals inferiorly near the nasal aperture (Rae 1999). Unlike previous interpretations, it is also evident that the overall shape of the ancestral hominoid morphotype is Page 5 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

more cercopithecine-like (Benefit and McCrossin 1991), with tall zygoma and a deep face. This suggests that the shared craniofacial configuration of gibbons and colobine monkeys (short face, sloping zygoma) is convergent.

Extant Hominoids Hylobates Gibbons represent a radiation of small-bodied, brachiating suspensory hominoid species with attendant postcranial specializations, distinguished from each other primarily by pelage color and patterning and by vocalization. Four main groups are usually recognized, sometimes accorded subgeneric or generic rank, depending on the author. Three groups – Hylobates hoolock, H. concolor, and H. syndactylus – are comparatively well defined; the H. lar group is more problematic. Valuable reviews of extant gibbon characteristics and diversity include Groves (1972), Marshall and Sugardjito (1986), and Groves (2001); see also Geissmann (2002) and Mootnick and Groves (2005) for recent findings on gibbon diversity that support generic distinction, although the traditional use of the single genus Hylobates is maintained here. Gibbons are craniodentally primitive in some characteristics (see above), compared with other extant hominoids, whether by plesiomorphy (McNulty 2004) or reversal (Rae 2004); appreciation of this led to the realization that similarities with Miocene taxa, such as Limnopithecus and Pliopithecus, previously taken as grounds for regarding these as likely gibbon ancestors, do not betoken any especially close phylogenetic relationship. The upshot is that, in the absence of a fossil record other than dental remains from Quaternary deposits of China and Indonesia referable to the modern genus, the early evolutionary history of gibbons is wholly obscure. Overall, the Hylobates skull is rather lightly constructed (Fig. 1). The neurocranium is thin walled and the vault low and ovoid in profile, with a capacity of about 80–125 cm3. The frontal extends rearward between the parietals, and in most individuals the sphenoid sutures with the parietal on the vault wall. The orbits are rectangular and relatively large, with strongly developed lateral margins;

Fig. 1 (Upper) Frontal and profile views of H. hoolock skull (Photograph # The Grant Museum of Zoology, University College London). (Lower) Frontal and profile views of H. symphylangus skull (Photograph courtesy C.P. Groves) Page 6 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

a torus also develops laterally above the orbits but is not continuous, fading out medially. The lacrimal fossa extends beyond the orbital rim onto the maxilla, and the interorbital breadth is large; the short, broad nasals are usually fused above the ovoid nasal aperture. Overall the face is short, broad, and fairly projecting. Within the nasal cavity, the premaxilla and maxillary palatine process are separated by broad palatine fenestra linking the nasal and oral cavities (Fig. 2 upper left); the vomer extends only as far as the fenestra, and the bony nasal septum is continued anteriorly by the premaxillary prevomer, which fuses to the vomer and forms a small bony crest in the incisive region in all gibbon species except the smallest, H. klossi (McCollum and Ward 1997). The palate and mandible are long; both corpus and symphysis are comparatively lightly built, although external thickening of the latter may be evident in some individuals, as well as the usual internal reinforcement by a superior transverse torus. The ramus is short, broad, and vertical, with some expansion of the gonial region. Reflecting gibbons’ predominantly frugivorous niche, the anterior dental arcade is relatively broad compared with the rear. The upper incisors are markedly heterodont – I1 broad and spatulate and I2 narrow and pointed – the lowers more similar, vertically implanted, and subequal in size. The canines are long, curving, transversely slightly narrowed, and sharply pointed, with minimal sexual dimorphism. There is well-developed honing of the upper canine against the long, highly compressed anterior face of the sectorial P3, which is orientated in line with the molars. Cheek teeth exhibit considerable metric and morphological variation, but the rear molars are usually reduced compared with the first and especially the second molars except in H. (Symphalangus) syndactylus (see below). The basicranium is long, with the foramen magnum and occipital condyles well behind the auditory meatus; there is no distinct mastoid process. The nuchal area is quite extensive, rising well up the occipital, with a distinct crest laterally that usually fades medially, although it may be continuous in some individuals. A sagittal crest is usually absent but may occur in small-brained individuals. Detailed accounts of intra- and interspecific variation in Hylobates are given in Groves (1972, 2001) and Marshall and Sugardjito (1986) as above. Albrecht and Miller (1993) summarize their reanalysis, with caveats, of Creel and Preuschoft’s (1976) craniometric data: canonical variate

Fig. 2 Subnasal morphology of hominoids seen in sagittal section. Upper left: Morotopithecus, showing no overlap of the premaxilla on the maxilla (the primitive condition seen in extant Hylobates and most fossil hominoids). Lower left: Pongo, showing the smooth overlapped subnasal condition also seen in Sivapithecus. Right: Pan (upper) and Gorilla (lower) showing the stepped overlapped condition usual in extant African apes (Modified after Ward and Kimbel (1983)) Page 7 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

analysis (CVA) reveals H. hoolock, H. concolor, and H. syndactylus as cranially distinct from each other and from the H. lar group. This consists of a primary cluster including H. lar, H. agilis, H. moloch, and H. muelleri subspecies, with H. pileatus as an outlier and H. l. vestitus and H. klossi grouped together as a second, distinct, outlier. A subsequent analysis (Creel and Preuschoft 1984) produced patterns of resemblance that generally accord with geographical distribution but not always with the usually recognized species limits. A recent study by Leslie (2010) extends analysis to the relative orientation of internal cranial features and their variation across the recognized hylobatid groupings; the findings generally accord with those of the earlier studies based on external cranial features. The only distinctive form noted here is the siamang H. (S.) syndactylus (Fig. 1, lower). This large, heavily built gibbon is more folivorous than other taxa and has a larger cranial capacity, a long, broad palate, and an inflatable air sac in the throat to aid calling. Postorbital constriction is more marked, and, despite the larger cranial capacity, sagittal cresting is both more frequent and larger than in other gibbons, an allometric correlate of greater body size (see below). In the dentition, the canines are less lingually curved than in other gibbons, the protocone on P3 and P4 larger; and on the upper molars, crowns are elongated, the hypocone variable in size, and lingual cingula almost always absent. Third molar reduction occurs in only a minority of cases, and some individuals possess supernumerary molars. Again consistent with its more folivorous niche, relative shearing-crest development is greater than in other gibbon species (Kay and Ungar 1997, 2000). H. (S.) syndactylus has a larger, more airorhynchous (i.e., more dorsally flexed) face than other gibbons (Shea 1988) – see below.

Pongo The Asian great ape, the orangutan, exhibits a distinctive overall cranial form (Fig. 3). In profile the large face is markedly prognathic subnasally, with a projecting, convex alveolar clivus. The comparatively small neurocranium is set above the facial skeleton, so that both frontal and occipital contours are relatively vertical. The orbits are elliptical, with their major axis vertical, and are surmounted by separate semicircular supraorbital costae rather than a continuous torus. The interorbital distance is very small, the ethmoid correspondingly constricted and set at a lower level than in the African apes (Shea 1988). There is no frontoethmoid sinus (Fig. 4), and the floor of the anterior cranial fossa forms a large part of the orbital roof (Winkler et al. 1988). In the fossa, the two wings of the frontal bone fail to meet behind the ethmoid, which retains contact with the sphenoid. The nasal bones are small, typically fused at an early age, and continue beyond the

Fig. 3 Frontal and profile views of Pongo pygmaeus skull (Specimen courtesy of the Oxford University Museum of Natural History) Page 8 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

Fig. 4 Virtual three-dimensional reconstruction of Pan cranium from serial CT scans. The bone has been made transparent to show the paranasal sinuses and tooth roots. F frontal sinus, E ethmoidal sinus, S sphenoidal sinus, M maxillary sinus (Image courtesy of T. Koppe)

frontomaxillary suture, extending as a narrow wedge into the glabellar region of the frontal. On the medial orbital wall the lacrimal sutures with the ethmoid. The midface region is short, the zygomatics are wide, deep, and flared, and there is usually a pronounced notch on the zygomatic process of the maxilla. The nasal cavity is tall and broad, the maxillary sinuses invade the interorbital pillar (sometimes as far superior as the frontal), and the lateral maxillary walls are obliquely inclined. The convex nasoalveolar clivus passes smoothly into the nasal cavity, extensively overlapping the anteriorly thin maxillary palatine process without a stepped incisive fossa; the fossa and canal are narrow, the latter long and orientated almost horizontally (Fig. 2 lower left). The vomer usually extends to the rear of the incisive canal but occasionally does not, in which case a small prevomer may be present (Ward and Kimbel 1983; Ward and Pilbeam 1983; McCollum and Ward 1997). Overall the palate is orientated anterosuperiorly. The mandible is massive, the symphysis reinforced by a robust superior transverse torus and an especially pronounced inferior transverse torus extending back as far as P4 or M1 (Brown 1997). The corpus is deep and comparatively short. As in the African apes, there is a strongly developed platysma muscle extending laterally over much of the facial musculature and strongly attached to the swollen base of the mandibular corpus from the symphysis to the area of masseter insertion. Brown and Ward (1988) speculate that the massive platysma is associated with the orangutan’s extensive laryngeal air sac system – greater than in other apes – aiding the regulation of air pressure and volume within the sac during vocalization. A distinctive feature of Pongo is the absence of the anterior digastric muscle (and so of the digastric fossae on the base of the symphysis) and associated separation of the posterior digastric from the hyoid and stylohyoid muscle (Dean 1984; Brown and Ward 1988). Instead the large posterior digastric, originating on the cranial base adjacent to rectus capitis lateralis, inserts onto the gonial region between the medial pterygoid and masseter muscles, acting to depress the mandible. The orangutan’s mylohyoid muscle is especially well developed, as are the geniohyoids. Rectus capitis lateralis, originating from a narrow area on the front of the atlas and inserting on the basioccipital anterior to the foramen magnum, is a more fan-shaped muscle than its homologue in the chimpanzee. Page 9 of 68

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The cranial base is wider than in the African apes (Dean and Wood 1981, 1984), but the eustachian process is much smaller, providing the origin for only tensor palati, with levator palati originating from the apex of the petrous temporal (Dean 1985). The mastoid processes are poorly developed. In the articular region, there is a long preglenoid plane, an indistinct articular eminence, and a prominent postglenoid tubercle. The roof of the glenoid fossa is coronally oblique, slightly sloping inferomedially, so that the entoglenoid is less prominent than in the African apes. The temporomandibular ligament is well developed laterally but lacking the deeper horizontal band, suggesting closer approximation of the rear of the working condyle and the postglenoid tubercle during chewing (Aiello and Dean 1990). The foramen magnum and occipital condyles are set well back on the skull base. A nuchal crest is present in all mature individuals, and a prominent sagittal crest develops posteriorly in most males, uniting with the nuchal crest but, reflecting the orangutan’s greater airorhynchy, typically not extending as far beyond the rear of the vault proper as in Gorilla (see below). Anteriorly the temporal muscles diverge as lines or simple crests bounding a triangular area of the frontal. As in the African apes, the bulk of the temporalis muscle is orientated obliquely, with an emphasis on the posterior fibers. The dentition reflects the orangutan’s predominantly frugivorous niche. The upper incisors are the most heteromorphic of any extant hominoid: I1 is very broad and spatulate, but I2 is smaller, more pointed, and more convex in curvature. Well-developed median and marginal ridges reinforce the incisor crowns in biting. Lower incisors, high crowned and narrower than the uppers, are also reinforced by lingual ridging. Canines are conical, markedly dimorphic, and especially robust in males; females display more pronounced lingual cingula. Upper premolars are bicuspid; P3 is sectorial with a narrow, elongate protoconid as the honing face; P4 is bicuspid. Upper molars are more oval in occlusal outline than in other apes (Swarts 1988; Swindler and Olshan 1988; Uchida 1998b). Cheek teeth are relatively large compared to body size, low crowned, and with extensive, deep secondary wrinkling that further increases occlusal area. Molar shearing crests are rather well developed considering the emphasis on fruit (although significant quantities of bark and leaves are also ingested), exceeding those of chimpanzee species but considerably less than gorillas (Kay and Ungar 1997). They perhaps provide an instance of phylogenetic inertia, suggesting a more folivorous ancestor. Orangutans are remarkably variable in cranial morphology (Wood Jones 1929; Rohrer-Ertl 1988a, b; Winkler 1988). Rohrer-Ertl (1988b) has shown that the most stable region is the midface, other cranial areas varying according to age, sex, dental eruption and masticatory development, hormonal status, dietary composition, and tooth use. Both the neurocranium and face exhibit greater growth in breadth than in length or height, a differential that is more marked in males than in females. While there is much individual and intrapopulational diversity, at least some variation reflects geographic factors: Groves (1971, 1986, 2001) and Rohrer-Ertl (1988a, b) review cranial patterning and Brown (1997) mandibular form, while Uchida (1998b) summarizes dental differences. Within a context of admittedly high variability, Sumatran orangutans are characterized by an oblique but straight (not concave) facial profile with highly protuberant anterior teeth, a convex cheek region lacking a suborbital fossa, relatively short nasals, a shorter neurocranium but with a longer nuchal region, and a longer foramen magnum. The mandibular symphysis tends to be long and narrow, with an extensive inferior transverse torus. Dentally they exhibit relatively small paracones on P3 and M1 compared with their Bornean counterparts, M1 larger than M2 rather than subequal, and a broader M3. Bornean orangutans have a generally more prognathous and concave facial profile, display a distinct suborbital fossa on the cheek, and have more labially positioned incisors, a “trumpetPage 10 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

shaped” nasal aperture that becomes triangular in cross section at the level of the nasal tubercle (Rohrer-Ertl 1988a), and a more prominent interorbital pillar (Groves 2001). Their mandibles are deeper and broader anteriorly, and the symphysis is usually larger, thicker, and more bulbous than that of Sumatran orangutans. Taylor (2006) explored the relationships between feeding behavior, diet, and mandible morphology, specifically the greater exploitation of bark and relatively tough vegetation during low fruit periods by some Bornean orangutan populations compared with Sumatran ones. She found that the Bornean mandibles display a relatively deeper corpus, deeper and wider symphysis, and relatively greater condylar area, arguing that these features enable greater load resistance to masticatory and incisal forces, reflecting ingestion of harder food items. There is a gradient within Borneo, with populations in NE Kalimantan and Sabah (P. p morio) displaying fullest expression of these traits, those in SW Kalimantan (P. p. wurmbii) rather less, and with those in NW Kalimantan (P. p. pygmaeus) generally intermediate between P. p. morio and the Sumatran mandibles, thus implying a spectrum of hard food exploitation in Bornean orangutans. There is other craniodental differentiation within Borneo between populations from Sabah, NW and SW Kalimantan separated by the Kapuas River (Groves 1986, 2001; Courtney et al. 1988; Groves et al. 1992), often of comparable magnitude to that between Bornean and Sumatran orangutans. For example, Taylor and Schaik (2007) document variability in absolute and relative brain size in orangutan populations, finding significantly smaller brains among the north east Kalimantan/Sabah group (P. p. morio) compared with those from elsewhere in Borneo and from Sumatra. They relate these findings to differences in resource quality and life history: P. p. morio has the least productive habitat, lowest energy intake during extended periods of scarcity, and the shortest interbirth intervals, arguing that brain size and prolonged food scarcity may be inversely correlated. Uchida (1998b) was unable to identify any consistent pattern of dental differences between Pongo populations from W Borneo, SW Borneo, and Sumatra, with the Bornean groups often as distinct from each other as either was from the Sumatran sample. Bornean orangutans were significantly different from each other (but not from Sumatra) in P4 and M1 shape, but virtually identical in their narrow M3 shape, with Sumatran orangutans having broader rear molars. Differences in molar cusp proportions showed similarly inconsistent patterning between the three groups. There were no obvious links to dietary differences, and Uchida concluded that on dental evidence, river and mountain systems within Borneo were as significant biogeographic barriers and so promoters of differentiation, as flooding of the Sunda shelf. Bornean and Sumatran orangutans have generally been accorded subspecific status as Pongo pygmaeus pygmaeus and P. p. abelii, respectively (Schwartz 1988). In his latest revision, however, Groves (2001) distinguishes them as separate species (P. pygmaeus and P. abelii) on the basis of the more comprehensive morphological information now available and molecular differences well above levels usually associated with subspecies, which indicate a long period (c. 1.5 Ma) of isolation between the two forms. He also formalizes the intra-Bornean diversity noted above as subspecies of P. pygmaeus. This taxonomic framework, which is also followed, for example, by Taylor (2006), is reinforced by a study of multiple genetic loci which extends Sumatran and Bornean orangutan divergence back to 2.7–5.0 Mya, with isolation thereafter (Steiper 2006). The data also point to contrasting population histories, with Bornean orangutans having undergone recent population expansion beginning 39–64 Kya, while Sumatran populations remained stable. The Sumatran and Bornean orangutans also exhibit developmental contrasts. Uniquely, male Sumatran orangutans may delay for many years full expression of secondary sexual characters, including their characteristic cheek flanges, whereas such long delays are much less common among Bornean males. Pradhan et al. (2012) relate such flexible developmental arrest to sociobiological factors and in particular to the potential for high-ranking males (flanged or unflanged) to monopolize Page 11 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

sexual access to females. When the potential is low, no developmental arrest is the prevailing pattern, whereas at high monopolization potential the flexible, arrested development pattern is the stable one. Their model accords with field data indicating different monopolization potentials between Bornean and Sumatran flanged males and a lower proportion of these in the Sumatran orangutan population. Harrison and Chivers (2007) relate the evolution of developmental arrest to the onset of longer, more severe periods of low food availability reflecting climate change 3–5 Mya, with females dispersing more widely in search of food and adult flanged males less able to effectively guard a female harem, so providing an opening for the unflanged male as a quiet, quick, opportunistic “sexual predator.” Hominoids exhibit more dorsal flexing of the face relative to the cranial base (airorhynchy) than non-hominoids; their orbital axes and palates are both shifted more dorsally relative to their degree of basicranial flexion than those of other primates (Ross and Ravosa 1993; Ross and Henneberg 1995). While the functional basis for this is disputed (Ross and Ravosa 1993) and may well have multiple causes, within this context many of the orangutan’s distinctive features can be plausibly related to its extreme airorhynchy (Delattre and Fenart 1956, 1960; Biegert 1964; Shea 1985, 1988; Brown and Ward 1988). Biegert (1964) argued that the hypertrophied laryngeal sac in Pongo is a prime determinant of its skull form, comparing it with the enlarged hyoid and associated throat organs of Alouatta. Shea (1985, 1988) and Brown and Ward (1988) have criticized this interpretation. Shea considers laryngeal specialization as just one potential determinant of airorhynchy, interacting with other factors, largely unknown. Brown and Ward consider the Pongo-Alouatta analogy invalid in view of contrasts in the submandibular anatomy of these two genera, and it has also been rejected by Hershkovitz (1970) and Zingeser (1973). Shea argues that pronounced dorsal flexion of the face links Sivapithecus and Pongo and that a degree of airorhynchy (although not to the extent seen in these two genera) is primitive for catarrhines and hominoids generally. On this view, the more ventral positioning of the face relative to the neurocranium seen in African apes and hominids is synapomorphous and, as such, a significant phylogenetic indicator (see also Ross and Ravosa 1993; Ross and Henneberg 1995; and below). The distinctiveness of Pongo is emphasized by its pattern of ectocranial suture closure (Cray et al. 2010). Vault suture synostosis is similar to Gorilla (but contrasts with that of Pan and Homo – see below), but the lateral-anterior pattern of fusion, with its strong superior to inferior gradient, is unique to Pongo, reflecting its relative phylogenetic isolation among hominoids.

The African Apes As is well known, the African apes (hereinafter meaning gorillas, chimpanzees, and bonobos, i.e., non-hominin hominines) share a basic similarity of cranial form and in many respects are scaled variants of a common bauplan (Figs. 5 and 6). Many of the craniodental differences between them have been related, with varying degrees of success, to differences in dietary niche (see Chaps. ▶ 8, ▶ 11, ▶ 12, ▶ 13, ▶ 14, and ▶ 15). Taylor (2002) also provides a useful recent summary of African ape diets. Within a highly variable context of local preferences and seasonal fluctuations and with considerable overlap in the fruits exploited, gorillas are, broadly speaking, more folivorous than chimpanzees. Gorillas consume less fruit than chimpanzees and exploit leaves, pith, bark, bamboo, and terrestrial herbaceous items. The eastern mountain gorilla (G. g. beringei) is the most exclusively folivorous form; the western lowland gorilla (G. g. gorilla) exploits the most varied diet, with a significant fruit component. In contrast, chimpanzee diets are dominated by fruits, although it is unclear whether the bonobo (P. paniscus) exploits more terrestrial herbaceous vegetation than the common chimpanzee (P. troglodytes) (Taylor 2002). Page 12 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

Fig. 5 (Upper) Frontal and profile views of Pan paniscus skull (Specimen courtesy of the Oxford University Museum of Natural History). (Lower) Frontal and profile views of Pan troglodytes skull (Specimen courtesy of the Oxford University Museum of Natural History)

Compared with the orangutan, African apes exhibit longer, lower, narrower neurocrania set at a lower level relative to the facial skeleton (klinorhynchy). The frontal contour is low and retreating, the parietal region flat, and the occipital more curved than in the large-bodied Asian ape. There is a prominent supraorbital torus that is usually continuous across the glabellar region as well as above each orbit, although in some P. troglodytes individuals it may be divided by a slight depression. A supratoral sulcus, its lateral limits defined by the anterior temporal lines, delimits the torus from the frontal squama. The orbits are subrectangular, usually broader than high, and interorbital breadth is greater than in the orangutan, reflecting the broader ethmoid of African apes. On the medial orbital wall, the ethmoid’s orbital plate is reduced, and the ethmolacrimal suture is usually much less extensive than in the orangutan and in some individuals may be replaced by contact of the interposed frontal and maxilla. There is an extensive frontoethmoid sinus (Fig. 4). On the floor of the anterior cranial fossa, the frontal may separate the ethmoid from the sphenoid, more commonly in Gorilla (>50 %) than Pan (15 %). Frontotemporal contact predominates on the lateral cranial wall of the chimpanzee and gorilla, but sphenoparietal contact is common in the bonobo. The root of the maxillary zygomatic process arises relatively close to the occlusal plane, above M1 or M2. In the chimpanzee, the zygoma’s facial (malar) aspect is limited in height and breadth; in the gorilla, it is deeper and extends further laterally. In both apes, it is remarkably thin in sagittal cross section when compared with most early hominins but is strengthened by the sagittal angulation of its upper and lower portions. Rak (1983) has emphasized the structural importance of the zygomatic region as a transverse buttress, linking the lateral and medial components of the face and resisting masticatory forces. In both gorilla and chimpanzee, the zygoma’s temporal process is sharply angled from its malar surface, with the zygomatic arches orientated parasagittally/posteriorly slightly divergent (Pan) and parasagittaly/posteriorly slightly convergent (Gorilla), reflecting differing ratios of mid-facial and bitemporal breadths in the two genera. The greater facial breadth in Gorilla means that the masseters, especially their anterior fibers, have a greater lateral component to their contraction than in Pan.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

Fig. 6 Left (Upper) Frontal and profile views of Gorilla gorilla gorilla skull (Photograph courtesy of C.P. Groves). (Lower) Frontal and profile views of G. g. diehli skull (Photograph courtesy of E. Sarmiento). Right (Upper) Frontal and profile views of G. g. graueri skull (Photograph courtesy of C.P. Groves). (Lower) Frontal and profile views of G. g. beringei skull (Photograph courtesy of C.P. Groves)

The zygomatic arch is thin in cross section but vertically deeper, its inferior border marked anteriorly for the superficial masseter fibers, and in Gorilla posteriorly scalloped for the origin of the muscle’s deeper portion. A part of this, sometimes differentiated as the zygomaticomandibularis muscle, fuses with anterior temporalis fibers, to attach to the temporalis tendon, the coronoid process, and anterior ramus edge (Raven 1950; Sakka 1984; Aiello and Dean 1990). In mature male gorillas, the arch is reinforced sagittally in its mid-region by a “step” with convex upper border which increases its vertical depth compared with immediately adjacent areas and strengthened transversely toward its rear by the broad, flat base of the temporal’s zygomatic process. Additional support against the masseter’s pull is provided by the temporalis fascia, inserting on the upper border of the zygomatic arch; again, it is particularly extensive in male gorillas.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

Anteriorly the face is braced against masseteric force by the zygomatic buttress (see above) and by the beam of the supraorbital torus, which links with the zygoma via its frontal process (Rak 1983). The greater facial breadth of Gorilla combined with its more marked postorbital constriction and so deeper infratemporal fossa means that the lateral component of the torus is unsupported behind by the anterior neurocranial wall and so is massively thickened vertically and sagittally, while the postorbital bar is broadened compared with Pan. These structures, the canine roots, and nasal septum also reinforce the palate and face against bending (sagittal), torsional (coronal), and shearing forces generated during biting by the anterior teeth. Such forces are highest rostrally and of greatest magnitude in large-jawed forms such as Gorilla (Preuschoft et al. 1986). Within the nasal cavity, the incisive canal is wide and the fossae are broad and bowl shaped. In Pan, the extent by which the premaxilla overlaps the palate, and so the length of the incisive canal, is comparable to that in the orangutan, although the canal is angled more steeply than in the latter because of the African ape’s less convex premaxilla (Fig. 2 upper right). In Gorilla, the overlap is much less and the incisive canal shorter, and there is always a distinct step in the nasal floor between premaxilla and palate (Fig. 2 lower right). In Pan, the step is much less marked and may be absent altogether in about one third of individuals, who evince a smooth floor comparable to that of the orangutan (McCollum and Ward 1997). In Gorilla, a long prevomer is interposed between the vomer and the premaxilla, with the inferior parts of both the former bones descending into the incisive canal, dividing its posterior wall and eventually partitioning it into two channels. A septal groove along the nasal sill is seen only in younger individuals; in adults, it is confined to the rear of the sill. In Pan, the prevomer is much smaller, and, while it descends into the incisive canal to divide the posterior wall, together with the vomer, complete partitioning into two channels is much less frequent than in Gorilla. Unlike the latter, a septal groove is present on the nasal sill in adults as well as younger individuals. Fusion of the facial aspect of the premaxillomaxillary suture in chimpanzees begins prenatally and is usually completed before the permanent dentition is fully erupted, with the nasal aspect being completely fused around the eruption of M2. Facial growth in Gorilla continues for longer, with both facial and nasal aspects of the premaxillomaxillary suture and the prevomeral-vomeral sutures remaining open until well into maturity (McCollum and Ward 1997). Accessory premaxillary sutures are also quite common (>20 %) in Gorilla, indicating separate ossification centers for the palate and facial components of the premaxilla (Schultz 1950). The palate is long in both Pan and Gorilla; externally it is shallow anteriorly with no clear alveolar border but deeper along the postcanine row. Internally, the maxillary palatine process of Pan is distinctive in thickening anteriorly and containing the palatine recess, a medial extension of the maxillary sinus. Laterally the maxillary alveolar process is thin, with the contours of the tooth roots evident; medially the process is thicker. Rak (1983) argues that the maxillary zygomatic process acts as a mid-palatal buttress, reinforcing the hard palate against shearing stresses generated between the chewing and balancing sides of the dental arcade, primarily from the latter’s medial pterygoid muscle. Both medial and lateral pterygoids are particularly well developed in Gorilla. As in the orangutan, the preglenoid plane of African apes is long, the articular eminence only slightly developed so the glenoid fossa is sagittally shallow, and the postglenoid tubercle is well developed. The roof of the glenoid fossa is coronally more horizontal than in the orangutan and the entoglenoid more distinctly differentiated from it, especially in Gorilla, where it is very large, extending beyond the level of the articular eminence and preventing any medial shift of the condyle prior to moving onto the preglenoid plane (Du Bruhl 1977). In some of these features and in temporal bone shape overall, Pan is more derived than Gorilla (Lockwood et al. 2004). Terhune (2012) notes that joint surfaces in the mandibular fossa are sagittally extended in chimpanzees, Page 15 of 68

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whereas in gorillas the surfaces are sagittally contracted and in orangutans intermediate, and that much variation is associated with morphologies that promote gape rather than bite force. A prominent temporomandibular ligament is present in Gorilla and is apparently variably developed in Pan (Aiello and Dean 1990). In Pan species, the dentitions are basically similar, although P. paniscus teeth are smaller and less sexually dimorphic than those of P. troglodytes. A comparative study of root length development (Dean and Vesey 2008) revealed that in P. troglodytes, anterior tooth root growth rose quickly to higher rates and then plateaued, with the highest rates in canines, followed by incisors (the reverse of the H. sapiens pattern). In both modern humans and apes, molar tooth roots grew in a nonlinear pattern, with peak rates reducing from M1 to M3. A recent study (Boughner et al. 2012) showed no significant differences in the relative timing of permanent tooth crown and root formation in bonobos and chimpanzees. Similarly, dental topographic analyses that reflect contrasts in occlusal form related to diet among primate species identified differences between wear stages within subspecies in surface slope, relief, and angularity, but failed to differentiate between Pan subspecies (Klukkert et al. 2012). Discriminant analysis of size transformed and untransformed molar traits (Pilbrow 2006), however, yielded more effective separation (see below). Smith et al. (2010) present data on crown and root formation in Taï Forest chimpanzees to evaluate claims that wild chimpanzees display delayed dental development compared with captive ones. They conclude that crown formation onset and development markedly overlap captive chimpanzees, whereas root development may be accelerated in captive specimens, and wild individuals fall near the middle or latter half of captive eruption ranges. Overall the authors conclude that while minor developmental differences are evident in some comparisons, the results do not show a consistent pattern of slower tooth formation in wild individuals. A later paper (Smith and Boesch 2011) extends the analysis to estimate that delayed tooth emergence in wild individuals is more moderate than previously recorded, averaging about 1 SD of the captive distribution, rising to 1.3 SD if age estimate criteria are relaxed; M1 emergence is estimated at 3.66–3.75 years in wild chimpanzees. The authors point out that “wild” data are usually skewed, often deriving from diseased, debilitated, or otherwise pathologically affected corpses of immatures, who cannot be considered fully representative of a healthy population. The maxillary incisors are curved mesiodistally, with I1 larger than I2, although the difference is smaller in P. paniscus than in P. troglodytes. In the mandibular incisors, these proportions are usually reversed. The upper canine is larger in males than females of both species; its mesial surface is more convex in P. troglodytes and, with the lingual surface, displays grooving absent in a small sample of P. paniscus (Swindler 1976). In the upper jaw, M1 and M2 are subequal in size, M3 reduced, with the hypocone the smallest cusp and reducing progressively along the molar row. Reduction is more pronounced in P. paniscus, and the cusp may even be completely absent from M1 and M2 in some individuals, whereas it is always present on those teeth in P. troglodytes. The hypocone may be entirely absent on some M3s of both species but is more weakly developed in bonobos (fully developed in 21 % of P. troglodytes teeth, compared with only 9 % of P. paniscus). The preprotocrista (anterior transverse crest between paracone and protocone) is more angled and transversely orientated in P. paniscus, running from closer to the protocone to mesial of the paracone rather than to its tip, as in P. troglodytes. The distoconule, an accessory cusp between hypocone and metacone, is absent in bonobos but present in all chimpanzee subspecies, generally at low frequency but up to 40 % of M3 in one collection of P. t. troglodytes (Kinzey 1984). A lingual cingulum is often present, most frequently on M1 but larger on M3 and better developed (longer distally) in bonobos than chimpanzees.

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M2 is usually the largest mandibular molar, M3 the smallest; a Y-5 cusp pattern is almost universal on M1 but only occurs in 93 % cf. 19 %, respectively, of individuals with M1 erupted; Braga 1998). This early synostosis results in a vertically and horizontally shorter face and reduced dental arch, consistent with the bonobo’s significantly smaller incisors, compared with P. troglodytes. Kinzey (1984) notes the greater degree of incisor wear in P. paniscus than P. troglodytes, which he suggests may be related to a greater incidence of pith and leaf petioles in the diet; he also speculates that the combination of a more transversely orientated and angled preprotocrista, with a more mesially sited metaconid and deeper groove between protoconid and hypoconid into which the crest occludes (see above), produces a more efficient shearing mechanism that again may reflect a more folivorous dietary component in bonobos. Comparison of small samples of immature captive and wild female P. paniscus with P. troglodytes showed similar patterns of skeletal fusion in the two captive groups with the pattern of tooth eruption to bone fusion also generally consistent between species save for minor variations in late juveniles and subadults. While displaying similar patterns, direct age comparisons showed skeletal growth in the captive bonobo group to be accelerated compared with both captive and wild P. troglodytes samples (Bolter and Zihlman 2012). Morphometric studies illustrate the relative homogeneity of chimpanzee cranial form compared with other great apes. While usually distinguishing P. paniscus from P. troglodytes, differentiation within the latter is, not unexpectedly, less secure, with extensive overlap between subspecies; see, for example, Shea and Coolidge (1988). These authors found that discrimination just about reached the subspecies threshold and that separation was considerably less than in orangutans or gorillas (see below). They considered that this comparative uniformity might reflect a more recent differentiation of P. troglodytes subspecies, more frequent or extensive contact – and so gene flow – between them, marked ecological flexibility for the species overall so precluding close matching of subspecific features to habitat, or any combination of these. A subsequent study (Groves et al. 1992), with specimens sorted by location rather than subspecies, produced neither meaningful geographic patterning nor subspecific grouping among males. Female crania, however, exhibited better separation, with P. paniscus distinct, P. t. schweinfurthii grading geographically toward P. t. troglodytes, and with evidence for east–west differentiation within P. t. schweinfurthii based on facial proportions. Page 20 of 68

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Shea et al. (1993) compare the results of both raw and size-adjusted analyses. For the former, there is 100 % correct classification for P. paniscus females and about 75 % correct classification for P. troglodytes, of which P. t. verus and P. t. schweinfurthii are furthest apart, according with their geographic separation. Confining the analysis to P. troglodytes, however, removes this geographic gradient, with maximal separation now between P. t. troglodytes and schweinfurthii. As expected, size adjustment reduces separation of P. paniscus from P. troglodytes, so that the distance between P. t. verus and P. t. schweinfurthii, now the most widely divergent subspecies, approaches that between the latter and P. paniscus. Principal Components Analysis shows P. paniscus clustering with immature P. troglodytes crania along PC 1, indicating their common growth trajectories and emphasizing that shape contrasts between bonobo and chimpanzee reflect the smaller size and truncated growth of the former relative to the latter, within which the major differences between P. t. troglodytes and P. t. schweinfurthii are also due to size and associated allometric factors (see below). Separate analysis of mandibular variation in Pan accords generally, but not completely, with the above (Taylor and Groves 2003). Mandibular separation within P. troglodytes is less than that within Gorilla, but contrasts between P. paniscus and P. troglodytes are greater than Gorilla, and there is clear separation of bonobos and chimpanzees. There is extensive overlap of P. troglodytes subspecies, maximally between P. t. schweinfurthii and P. t. troglodytes, and greatest distinction between the latter and P. t. verus (contrast to Shea et al.’s cranial finding of greatest overlap between P. t. troglodytes and P. t. verus). Size adjustment again reduces separation, so that bonobos, while remaining the most distinctive, now partly overlap with chimpanzees; and P. t. verus, while still the most isolated of chimpanzee subspecies, is now furthest from P. t. schweinfurthii (as on the cranial data). P. t. verus’s; distinctiveness on mandibular traits, while relatively slight (Taylor and Groves 2003), nonetheless accords with Braga’s finding (1998) that premaxillomaxillary suture closure differs significantly between P. t. verus and other subspecies, with P. t. verus displaying later complete closure of the suture’s facial component and earlier closure of its palatal component compared with P. t. troglodytes and P. t. schweinfurthii (Braga 1998). This points to a longer, deeper lower face in P. t. verus than other subspecies. A recent morphometric study of mandibular form (Robinson 2012) broadly accords with Taylor and Groves’ findings: size-adjusted corpus shapes in P. paniscus and P. troglodytes could be assigned with 93 % accuracy, with much of the shape differences size related, but subspecies could only be correctly identified 700 gorilla skulls, grouped by origin into 19 and Page 21 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

10 geographic localities for crania and mandibles, respectively (Groves 1967, 1970). D2 values were calculated for each of the ten cranial and six mandibular representative variables, allowing the localities to be grouped into eight larger regions which could be further combined on the basis of intra- and intergroup differences into three clusters: a relatively homogeneous western cluster (four regions, of which the Cross River sample was rather more distant from the other three), a distinctive eastern group from the Virunga volcano region, and a further eastern group (three regions). These correspond to the western lowland gorilla (G. g. gorilla), the eastern highland gorilla (G. g. beringei), and the eastern lowland gorilla (G. g. graueri) (Fig. 6). G. g. gorilla is the smallest subspecies, with fairly broad face, small jaws and teeth, a short palate, a single mental foramen under P3 or P4 (more usually under the latter), and a jaw condyle without a cleft. G. g. graueri is the largest subspecies, with a high, narrow face; larger jaws and teeth; and a longer palate. The mental foramen is often multiple and set under P3, while the jaw condyle is often cleft. The mountain gorilla, G. g. beringei, is distinguished by a low, broad face; very large jaws and teeth; a very long tooth row and palate; anteriorly sited (under C or P3) multiple mental foramina; and a jaw condyle that is usually cleft. Stumpf et al. (1998), adjusting for size, demonstrated that the Cross River sample was more distinctive than Groves’ original analyses indicated, so providing support to the growing movement advocating its recognition as a further subspecies, G. g. diehli (see Sarmiento and Oates 1999, 2000; Groves 2001, 2003). G. g. diehli is distinguished by its shorter skull, shorter molar row, narrower palate, shorter cranial base, and more steeply angled nuchal plane than other western gorillas, which Sarmiento and Oates speculate may be associated with a diet of smaller, drier, and harder food items than that of other western gorillas. A further reanalysis of Groves’ data (Stumpf et al. 2003) confirmed a primary east–west separation on the latter’s smaller values for palatal and tooth row lengths, nasal aperture and nasal bone breadths, lateral facial height, and supraorbital torus thickness. They also demonstrated the distinctiveness of the Cross River and Virunga populations from other west and eastern groups on the basis of their narrower interorbital breadths, narrower palates, and reduced lateral facial height. Analyses restricted to the western populations further indicate the distinctiveness of G. g. diehli on overall and neurocranial lengths, bicanine and bimolar breadths, interorbital and neurocranial widths, palatal length, and medial and lateral facial heights. Stumpf et al., however, emphasize that the fundamental distinction is between east and west Gorilla populations, with the corollary that G. g. graueri is more closely related to G. g. beringei than it is to western lowland gorillas. The implications of this, together with recent data from molecular and other studies, have led Groves (2001, 2003) to revise his earlier taxonomy and to differentiate western and eastern gorillas at the species level as G. gorilla (G. g. gorilla and G. g. diehli) and G. beringei (G. b. beringei and G. b. graueri), respectively. This also accords with the zoogeographical evidence, but for consistency with other sources referred to herein, we retain the traditional single species classification. Leigh et al. (2003), however, apply Wright’s FST (an indicator of microdifferentiation, measuring the extent to which subdivision within species – i.e., between subspecies – departs from random mating) to Groves’ craniometric data and to discrete trait variation and reach different conclusions. Their approach requires assumptions about population sizes and the heritability of craniometric traits but is considered to be robust, especially, when subspecies sizes differ markedly, as they do in Gorilla. FST calculated from the craniometric data yields unexpectedly low levels of between group variation, only c. 20 % between subspecies compared with 80 % within subspecies assuming equal population sizes. Adjusting for different population estimates between the subspecies results in even lower values of FST, with correspondingly more variation within subspecies. FST derived from discrete trait analysis gives rather higher, but still modest, levels of divergence. Leigh et al. argue that Page 22 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

much gorilla variation reflects ontogenetic changes and sexual dimorphism, and as such is intrasubspecific, and that their results offer no support for differentiating eastern and western gorillas at the specific level. See also Albrecht et al. (2003) for a detailed analysis of Gorilla cranial diversity at locality, deme, subspecies and species levels, and its potential evolutionary and sociobiological implications. Interestingly, genetic data indicate much deeper levels of differentiation among African ape species than the morphological evidence does (Gagneux et al. 1999; Lockwood et al. 2004). Caillaud et al. (2008) explore the possible sociobiological basis for sexual dimorphism – specifically male body size and head crest development – in G. g. gorilla, through photogrammetry and field observations. Their findings show the number of females belonging to a mature male correlates with head crest size, body length, and musculature and that female numbers at male-male encounters, where larger individuals could be expected to be at an advantage, strongly affect the number of male agonistic displays. Exaggerated male traits therefore convey a mating advantage, whether through male-male fighting or female mate choice. Similar drivers may well be influencing the evolution of dimorphism in other, larger-bodied gorilla taxa. Breuer et al. (2012) also explored the relationships of body length, crest size, and gluteal muscle size with long-term male reproductive success in western gorillas. They found that all three traits correlated with the average number of mates per male, but that only crest size and gluteal development significantly correlated with offspring survival and the annual rate of siring offspring who survive to weaning. Dental variation in Gorilla is considerable: molar shapes and cusp proportions, relatively invariant within subspecies, differ between subspecies, as do tooth dimensions (Uchida 1998a). Male (but not female) G. g. beringei canines are larger than those of G. g. gorilla and G. g. graueri. In the postcanine dentition, G. g. graueri is, surprisingly, significantly larger than G. g. beringei, which is larger than G. g. gorilla. While upper molars of beringei show B-L enlargement, those of graueri are expanded in both length and breadth. G. g. gorilla has wider incisors relative to molar length than the eastern subspecies, while G. g. beringei displays higher crowned cheek teeth with sharper cusps and ridges than G. g. gorilla. G. g. graueri has a relatively smaller talonid on P4 and, together with G. g. beringei, has larger distal cusps on the upper and lower molars than G. g. gorilla. Patterns of dental sexual dimorphism differ among gorilla subspecies: G. g. beringei displays greatest dimorphism in canine and lower molar size, graueri greatest dimorphism in upper molars, with G. g. gorilla least dimorphic both in canines and molars. This reflects a larger canine relative to molar size in females of this subspecies, which Uchida considers to reflect heightened female-female competition, possibly related to greater frugivory. She stresses the importance of local dietary adaptation influencing tooth form and proportions, with considerable variation but with more extensive frugivory in G. g. gorilla and lowland G. g. graueri than in highland populations of that subspecies and G. g beringei. Similarly, Pilbrow (2010) has analyzed molar morphometrics to assess gorilla geographical diversity. Her results support species distinction between G. gorilla and G. beringei, with subspecies G. g. diehli, G. g. gorilla, G. b. graueri, G. b. beringei, and a possible further subspecies, G. b. rex-pygmaeorum; dental metrics thus accord with other evidence for gorilla population diversity. Dental separation increased with altitude differences but not geographical distance, so that altitudinal segregation better explains gorilla population divergence better than isolation by distance. Pilbrow argues that the historic center of gorilla distribution was West Africa and that PlioPleistocene climatic oscillations combined with mountain building promoted drift and population differentiation. Further analyses of the gorilla masticatory system are discussed below.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

Allometric and Biomechanical Studies The greater size of the gorilla relative to the chimpanzee is an instance of peramorphosis (Shea 1983c). Length of maturation is comparable in all three African ape species, but gorillas grow much more rapidly and to greater sizes than chimpanzees, while bonobos grow somewhat more slowly than chimpanzees (rate hypermorphosis) to rather lesser sizes (although there is considerable overlap); within each species, males grow for longer than females (time hypermorphosis). The pattern indicates that the interspecies differences reflect selection for greater body size, perhaps associated with increasing terrestrial folivory rather than selection for delayed maturation (Shea 1983c). Significant differences between Pan and Gorilla growth in body weight only become apparent after about 2 years, with gorillas pulling away increasingly strongly from the chimpanzee growth curve thereafter (Shea 1983d; Fig. 6). Since neural growth is predominantly prenatal/immediately postnatal, there is no corresponding increase in Gorilla brain size in later ontogeny; the natural consequence is that, while having absolutely larger brains than chimpanzees, gorillas have lower brain–body ratios and lower encephalization quotients, with male value particularly depressed compared with females. “In the case of the African pongid species . . . the developmental pathway utilized to increase body size ensures that relative brain size decreases as a consequence” (Shea 1983d, p 58). It follows that attempted explanations of behavioral and/or ecological contrasts between the species based on differences in relative brain size should be regarded with skepticism. Shea (1983a, 1984) also summarizes evidence that the differences in body form between adult P. troglodytes and P. paniscus result from ontogenetic scaling. The extension of common growth allometries to different end sizes holds within the skull, trunk, and limbs but not between them, so that adult bonobos do not match any single stage in chimpanzee ontogeny. Relative to the latter, the P. paniscus skull is most strongly reduced in size, forelimbs and trunk less reduced, and hind limbs not reduced at all, so that for a given body size, P. paniscus has a smaller skull than P. troglodytes. This is turn results in a more paedomorphic cranial shape compared with the chimpanzee through the decoupling of growth rates for the head and body, with the former slowed relative to the latter – an instance of neoteny. The selective factors underlying this process are obscure, although Shea speculates that the reduced sexual dimorphism and different social organization of P. paniscus compared with P. troglodytes may be important drivers in the evolution of its distinctive cranial proportions. A more recent morphometric study by Lieberman et al. (2007) also concluded that the bonobo skull is largely paedomorphic relative to the chimpanzee, but that not all shape differences between the species, particularly in the face, could be explained in such terms, and that other developmental differences were also responsible for the contrasts in form. Durrleman et al. (2012) document ontogenetic changes in endocranial size and shape in sizeable samples of P. paniscus (n ¼ 60) and P. troglodytes (n ¼ 59) aged on dental criteria. They identify in bonobos an early, strong anisotropic endocranial expansion and bending due to localized expansion of the frontal pole, occipital lobe, and superior parietal lobe, which contrasts with developmentally later endocranial expansion in the chimpanzee. Patterns of expansion also differ in magnitude between the species, with a phase of rapid increase in endocranial volume occurring later in chimpanzees than bonobos. Earlier suggestions (Ackermann and Krovitz 2002) of a common cranial postnatal ontogenetic shape trajectory or of separate but parallel shape trajectories that merely accentuate differences established in early (prenatal) ontogeny have been refuted by Cobb and O’Higgins (2004), who show hominin postnatal shape trajectories to be divergent with differing shape changes between species, even in early postnatal ontogeny (Vidarsdottir and Cobb 2004). The directions of scaling Page 24 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

trajectories between Pan species, however, are not significant (so changing postnatal facial shape in a similar manner from different starting points), whereas those between Pan and Gorilla are directionally distinct. Cobb and O’Higgins (2007) explore the role of ontogenetic scaling in determining sexual dimorphism in the facial skeleton of African apes (G. g. gorilla, P. paniscus and P. troglodytes). Using geometric morphometric analysis, they found that on average males and females shared a common ontogenetic shape trajectory and a common ontogenetic scaling trajectory until around M2 eruption. Thereafter, males and females diverged from each other and from the common juvenile trajectories within each species, indicating ontogenetic scaling as a mechanism until around “puberty” and the development of secondary sexual characters, but that subsequent sexual dimorphism occurs through divergent trajectories and not via ontogenetic scaling. In general, the degree of adult cranial sexual dimorphism is greater in the larger apes (gorilla and orangutan) than in the chimpanzee and bonobo. Gorilla males display more size and shape variability than females, and a similar difference appears to be present in Pongo, but not in Pan (O’Higgins and Dryden 1993). Most of the differences reflect greater male facial prognathism, in turn a consequence of canine dimorphism. Adult cranial dimorphism appears to result from distinct mechanisms in the African and Asian apes. Whereas in Pan and Gorilla cranial dimorphism follows from extending the growth period of males for most cranial proportions (Shea 1983c), in Pongo only about half the growth allometries exhibit this process, with the other half displaying accelerated growth in males compared with females (Leutnegger and Masterson 1989a, b). Male and female chimpanzees display significant cranial size differences but no shape differences, perhaps because the period of extended growth is a short one and/or the scaling coefficients are minor, so resulting in insignificant shape differences given the comparatively modest size of chimpanzees. As with the bonobo-chimpanzee comparison above, these differing patterns of cranial dimorphism in the great ape genera have been linked to socioecological contrasts between them (O’Higgins and Dryden 1993); see also Caillaud et al. (2008) and above. Shea has also explored allometric influences on African ape craniofacial and dental form and their relationships to diet using bivariate and multivariate techniques. Many facial proportions in the bonobo, chimpanzee, and gorilla exhibit ontogenetic scaling, i.e., a common pattern of size/shape change. There are also instances, however, where this does not obtain: for example, chimpanzees have shallower zygomatic roots, narrower bizygomatic breadths, smaller infratemporal fossae, and narrower anterior cranial bases than bonobos with the same basicranial lengths. In other words, these features are reduced in chimpanzees compared with the values expected in bonobos ontogenetically scaled to their sizes (Shea 1984). Similarly, in those features in which chimpanzees are reduced relative to bonobos, gorillas tend to be reduced relative to chimpanzees (Shea 1984). As Shea points out, such allometrically adjusted analyses point to the opposite conclusion from that usually drawn from the study of absolute skull sizes – cranially; bonobos are relatively the most robust, and gorillas relatively the most gracile of the African apes. Additionally, gorillas have significantly longer and higher cranial vaults, higher orbits, and longer foramen magnums than chimpanzee crania of equivalent basicranial lengths. They also exhibit longer, more projecting nasal regions that are sited lower on the face, than comparably sized chimpanzees. As overall skull size increases in the sequence bonobo-chimpanzee-gorilla, the three species also exhibit relatively narrower faces and neurocrania, reflecting in the latter case, the fact that increased brain size results primarily from growth in length, not width, during the prenatal and early postnatal phases. During late postnatal growth, occipital length and breadth in gorillas increase appreciably compared with chimpanzees, reflecting the development of sagittal and nuchal crests as Page 25 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

a functional response to the enlarged temporal and nuchal muscles “outgrowing” their areas of attachment on the exterior cranial wall. This, in turn, is a consequence of the respectively positive and negative allometric relationships between splanchnocranial and neurocranial proportions and body size. Dental metrics indicate that gorillas have relatively smaller incisors and relatively larger cheek teeth than comparably sized chimpanzees, while, surprisingly, temporal fossa area (and so temporal muscle size) becomes relatively smaller across the three species as size increases. Despite these differences, the predominant pattern among the African apes is essentially one of similarity in craniofacial growth. Multivariate analysis yields a common allometry vector incorporating >93 % of total variance confirming this general picture, with a second vector (3.4 %) distinguishing chimpanzees and gorillas. Shea considers that the differences in midface proportions between Pan and Gorilla may reflect differences in soft-tissue function or dietary contrasts, although the influence of the latter is by no means clear. In fact, he notes that while dental contrasts between the two apes can fairly clearly be linked to diet, no significant reorganization of the face occurs, with its form being primarily determined by the endpoints of common allometric trajectories. This suggests that the face and masticatory apparatus may be less strongly coupled to diet than is the dentition and/or that chimpanzee and gorilla diets, while differing in their constituent items, may not differ appreciably in their physical properties, in particular the force required to process them. For Shea, the African ape masticatory complex provides an example of an integrated functional system preadapted to extension into new size ranges and dietary shifts. Molar crown area scales positively in hominoids, so that larger forms have relatively as well as absolutely larger crown areas, associated with their generally increased folivory, primarily achieved through increased tooth lengths rather than breadths (Demes et al. 1986). There are associated increases in palatal and mandibular lengths and relative narrowing of upper and lower dental arcades in larger taxa. Allometrically determined snout elongation produces greater bite force in larger animals, by lengthening the horizontal distance between the mandibular joint and the molar row, which Demes et al. have shown scales with a mean value of c. +1.6 in hominoids. Bite force is maintained by lengthening the masticatory muscles’ power arms, by increasing their cross-sectional area, or by a combination of these. The temporal muscle’s power arm scales from +1.16 (male great apes) to +1.62 (female gibbons) and that of the masseters and medial pterygoids, which is strongly influenced by facial height, between +1.54 and +1.64. A rough estimate of temporalis crosssectional area scales from c. +1.4 to +1.9, indicating that the greater load of the allometrically lengthened lever arm is more than matched in larger species by the positive allometry of the power arm and of muscle cross-sectional area and so muscle force. Larger species produce more bite force for their size than smaller ones due to the allometric changes in masticatory biomechanics following from increased body size, a point neatly illustrated by Demes et al., who demonstrate that skulls of H. klossi and P. paniscus enlarged isometrically to the size of H. (S.) symphylangus and G. gorilla, respectively, produce lesser bite forces than the “real” latter two forms do. Bite pressure (bite force/crown area) is maintained if bite force increases at the same rate as crown area; broadly similar relationships for these variables hold within hylobatids and great apes, indicating that in hominoids, crown area and bite force increase at about the same rate, at least over the size range of extant taxa. Estimated bite pressure is generally greater in great apes than hylobatids, although the orangutan is an exception here. Bite pressure shows no obvious relationship to between-species differences in size or diet; interestingly, P. troglodytes males produce the greatest scaled bite pressure, exceeding even G. gorilla males. Within species, males generally produce greater pressures than females, although whether this is selected for (implying differences in food processing or paramasticatory activity between the sexes) Page 26 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

or is a by-product of selection for larger body size is a moot point. Demes et al. make the important point that similar allometric relationships obtaining within hylobatids and great apes provide strong evidence that biomechanical constraints associated with increased body size elicit similar functional responses across the Hominoidea. This is strong presumptive evidence that they should also be applicable to fossil forms. Ravosa (2000) undertook such a combined allometric analysis of mandible size and form in fossil and extant apes, comparing them with cercopithecoids. Deeper corpora counter parasagittal bending while the more robust cross sections of larger species, especially the fossils, counter axial torsion. The positive allometry of corpus and symphysis cross sections suggests increased masticatory stresses due to greater balancing side muscle activity during powerful mastication, probably reflecting a tougher, harder diet. In addition, the allometry of jaw length and breadth point to greater wishboning stresses at the symphysis at the end of the masticatory powerstroke, countered by a thicker symphysis and increased anterior jaw breadth. After allometric scaling, the most robust mandibles include Proconsul africanus and P. nyanzae, Rangwapithecus, Turkanapithecus, Afropithecus, Ankarapithecus, Lufengpithecus, and Ouranopithecus; the more slender include hylobatids, Simiolus, Hispanopithecus laietanus, Pan paniscus, and P. troglodytes (see also below). In the broader context of fossil (as well as extant) hominoids, even G. gorilla has a comparatively low and slender corpus, only average symphyseal height and a slightly broader than expected symphysis for its mandible length. Pongo has a higher but rather thinner corpus than expected and a higher symphysis of expected width; P. paniscus has a corpus and symphysis of expected height but rather thinner than expected, while P. troglodytes has a shallower, narrower corpus and symphysis, although the latter is closer to the values expected on jaw length than the former. These findings have implications for the dietary reconstruction of fossil forms: many Middle/ Later Miocene hominoids are notably more robust than modern apes and so are plausibly reconstructed as exploiting harder, more resistant food items requiring substantial force in processing, while the categorization of proconsulids as “frugivorous” may also well underplay the variety and toughness of their dietary items. Such reconstruction, however, is difficult to reconcile with the evidence provided by dental morphology and wear patterns in Proconsul and by some other aspects of jaw form (see below). In some respects, hominoid and cercopithecoid mandibular cross-sectional scaling patterns are similar; smaller apes are notably gracile, resembling cercopithecine proportions, but larger ones have both deeper and relatively wider corpora more reminiscent of colobines to resist greater axial torsion during chewing – perhaps reflecting larger, more laterally placed masseters that contribute relatively more to unilateral mastication, together with the medial pterygoids. This is especially so in the largest apes which have absolutely and relatively very thick corpora exceeding colobine proportions, suggesting diets with at least comparable, and very possibly greater, physical properties of hardness and/or toughness. Smaller apes also display symphyseal curvature comparable to cercopithecines, whereas, with increasing body size, curvature reduces to a shallower, colobine-like, arc, eventually falling below even that in the largest apes. This has traditionally been interpreted in dietary terms (frugivores requiring large incisors and so a wide anterior dental arcade), but the bulk of the fossil evidence points to diets other than frugivory. Ravosa (2000) therefore interprets the broader anterior dental arcade combined with a relatively thick symphysis as hominoid adaptations to resist concentrated wishboning forces at elevated levels resulting from a hard-object diet. The exception to this is Afropithecus, which has a notably narrow, tightly curved anterior mandible with, presumably, correspondingly concentrated wishboning forces, raising interesting issues about dietary

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

composition and food processing activities in that genus. Again, findings from the dental evidence do not easily accord with those based on mandibular proportions. More recently, Taylor (2002, 2003) has used morphometric methods to investigate masticatory variation in African apes as a function of dietary differences. She compared allometrically adjusted mandibular, cheek, and facial dimensions, quantifying masticatory parameters associated with bite force and load resistance in ontogenetic series of bonobo, chimpanzee, and gorilla, to test the hypothesis that more folivorous forms would show greater development of these features. The results are complex. Unsurprisingly, all species show allometric increases during growth in traits indicating improved muscle and bite force and the capacity to resist greater loads. Masticatory muscle sizes are especially strongly allometric. After adjusting for allometry, however, only a few traits differ consistently across African ape species as predicted by dietary preferences. A more resistant diet is generally correlated with a thicker mandibular corpus, although the thicker corpus of chimpanzees compared with bonobos is not matched by evidence of corresponding dietary differences. Compared with Pan, Gorilla has a relatively wider mandibular corpus to resist axial torsion, a wider symphysis so resisting “wishboning,” a higher temporomandibular joint which contributes to improved mechanical advantage of the jaw lever and distributes forces more evenly along the cheek teeth, and a higher mandibular ramus, increasing the moment arm of the temporal and masseter muscles and providing a larger attachment area for the latter and the medial pterygoids. Moreover, within Gorilla, eastern gorillas exhibit greater values than western ones and also have larger masseter muscle than the latter, in accord with their more resistant diet. Other analyses, however, do not conform to the pattern predicted from diet; for example, gorillas do not have the relatively deeper corpora expected to resist parasagittal bending (Hylander 1979a, b), and there was no regular association of the deeper symphysis providing increased resistance to bending and shearing forces with greater folivory (see also Ravosa’s findings summarized above, although Demes et al. (1984) and Wolff (1984) considered the torsional resistance of the gorilla mandible “remarkable,” and maximal at the symphysis). Overall, gorillas do not have the shorter deeper faces and more anteriorly positioned masticatory muscles predicted to improve the mandible’s power arm ratio and to reduce bending moments in the face, and there was no consistent differentiation of bonobos and chimpanzees. Taylor concludes that while some of the distinctive craniofacial features of the African apes can plausibly be considered as dietary adaptations, the link is not especially strong. Dental development and allometric and other ontogenetic constraints are doubtless important influences, while more information is needed on the composition, variability, and especially the physical properties of ape diets. The equivocal nature of these results accords with those from some other studies; for example, despite their dietary contrasts, Rak’s indices quantifying relationships between the palate, masseter origin, and their positions relative to the calvaria fail to discriminate between Pan and Gorilla (Rak 1983: table 3, p 25). Further analysis of the Gorilla masticatory system with larger samples, and including G. g. graueri in the analysis, confirms and extends the earlier findings (Taylor 2003). G. g. beringei has a significantly larger face than the other two subspecies and differs from G. g. graueri in the same features that distinguish it from G. g. gorilla and which differentiate Gorilla and Pan. Despite being more folivorous, however, G. g. graueri does not differ from G. g. gorilla in those features, and G. g. beringei fails to express the full set of masticatory traits predicted by its diet. In this last respect, it may well be the case that an investigative model assuming optimization of each and every variable is simply inappropriate; rather than a spectrum or continuum of values for every trait, some may be more appropriately considered in terms of thresholds. For example, if food availability is not a constraint and provided the face is structurally sufficiently strong to resist masticatory forces, there seems little reason to suppose that selection will necessarily promote further shortening and Page 28 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

deepening of the face in hominoid folivores to achieve “optimal” values, particularly if to do so will disrupt pervasive, well-established allometric trajectories. Covariation within a tightly integrated functional system, such as the head, is likely to impose multiple constraints on the variation of any given character or character complex. Taylor et al. (2008) report a detailed analysis of the relationships between jaw form, diet, and food properties in orangutans, chimpanzees, and gorillas, using area moments of inertia and condylar area ratios to estimate moments imposed on the mandible to assess relative ability to counter mandibular loads. They took data on elastic modulus and fracture toughness of food types to derive food material properties and generated bending and twisting moments on the mandible to estimate minimally required bite forces. Based on food properties, they hypothesized improved resistance to mandibular loads in Pongo p. wurmbeii compared to African apes and in Gorilla b. beringei compared to Pan t. schweinfurthii. The predictions were, in fact, only applicable when bite forces were estimated from maximum fracture toughness of non-fruit, non-leaf vegetation; for all other tissues (fruit, leaves) and material properties, results were contrary to predictions. As food material properties changed, moments imposed on the mandible changed, so altering ratios of relative load resistance to moment, so that species appear over- or under-designed for the moments imposed on the mandible. Reliable estimates of average and maximum bite forces from food material properties accordingly require information about the physical properties of the full range of dietary items. A recent study (Taylor and Vinyard 2013) incorporates data on masticatory muscle physiologic cross-sectional area (PCSA) and muscle fiber length and broadly confirms an allometric influence on masticatory power while underlining the need for caution when inferring chewing forces from skull form. Hominoid muscle fiber architecture reflects both absolute size and allometric influences; PCSA is close to isometry relative to jaw length in anthropoids but trends to positive allometry in hominoids. Extant large-bodied apes therefore probably generate absolutely and relatively greater muscle forces compared with hylobatids and monkeys, possibly reflecting changes in food composition, ingestive behavior, and/or increased emphasis on mastication as opposed to ingestion with greater body size. The study also revealed that craniometric estimates of masseter and temporalis PCSA may be seriously awry, underestimating the actual figures by >50 % in gorillas and overestimating masseter PCSA by up to 30 % in humans. Given the lack of concordance in masticatory morphology and diet in living hominoids, and the discongruities between craniofacial morphology and dental evidence among fossil forms, detailed dietary reconstruction based on craniofacial form in fossil hominoids appears questionable. There seems no secure basis on which to go beyond the most general of statements about dietary properties. Shea’s conclusions about the relative decoupling of masticatory morphology and diet in the African apes may be applicable to hominoids generally (see also Daegling and Hylander (1998, 2000) and Daegling (2004)). Dental evidence (crown proportions and morphology, crest development and structure, chemical composition, and wear patterns) may well prove a better guide to hominoid diets than the analysis of craniofacial form, no matter how elaborate the biomechanical models employed (Ungar 1998; Teaford and Ungar 2000). These provisos should be kept in mind in relation to the following summary of craniofacial form in fossil hominoids, which for its framework draws especially on the chapters by Harrison, Begun, Kelley, and Ward and Duren in Hartwig (2002).

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Fossil Hominoids Africa Oligocene/Early Miocene African Hominoids The splitting event between the two crown groups of the Catarrhini, apes and Old World monkeys, was an African phenomenon, as the earliest members of both lineages are found in sub-Saharan Africa. The earliest evidence for the divergence is known from late Oligocene (25.2 Ma) deposits in the Rukwa Rift Basin in southwestern Tanzania; Nsungwepithecus gunnelli shows evidence of bilophodont, a cercopithecoid synapomorphy, while Rukwapithecus fleaglei, from the same deposits, shares two dental traits with crown hominoids – M2 hypoconulid positioned buccally and a hypoconid positioned opposite the lingual notch between the metaconid and the entoconid (Stevens et al. 2013). The dental similarities of the latter taxon with Rangwapithecus from the early Miocene of Kenya may suggest a similar dietary adaptation, namely, folivory (see below).

Kamoyapithecus The other known late Oligocene catarrhine that has been considered a possible hominoid is Kamoyapithecus, from Lothidok, Kenya (Leakey et al. 1995). No explicit shared derived traits link the form with later hominoids. Although very little can be said about the maxillary bone preserved in the type specimen, the dentition is consistent with a high degree of anterior tooth use, albeit with thinner dental enamel than that seen in later, similarly sized forms, such as Afropithecus. More extensive evidence from Early Miocene sites in East Africa indicates an array of forms, variously regarded as hominoid or non‐hominoid (see Begun volume 2 Chap. ▶ 4). Evidence from the oldest (19–20 Mya) sites of Songhor and Koru (Kenya) points to predominantly tropical forest habitats, with later (16–17 Mya) sites on Rusinga Island (Kenya) ranging from flood plain to riverine contexts. The picture here is of drier, more seasonal environments than Songhor or Koru, but with persistent wooded conditions, varying from forest to deciduous woodland according to rainfall (Andrews 1996; Andrews et al. 1997). Similar habitats are indicated at the rather later Middle Miocene sites of Maboko Island (15–16 Mya) and Fort Ternan (14.5 Mya; see below).

Micropithecus The small (ca. 3.5 kg) Micropithecus contrasts the bulk of the Early Miocene non-cercopithecoid fauna dentally in having relatively larger anterior teeth compared to the cheek teeth, broad incisors, and narrow premolars and molars, with only weakly developed occlusal ridges. It differs cranially from the similarly sized Dendropithecus in its shallow, broader palate and nasal aperture, short face and clivus, and moderately high and lightly built mandible corpus, with only modest symphyseal tori. Phylogenetic analyses (Rae 1993, 1997; Stevens et al. 2013) suggest that this taxon may be a stem hominoid, as it lacks some of the characteristic hominoid cranial synapomorphies. The frequency of dental pitting and pit shape in Micropithecus clarki (19–20 Mya) points to folivory (Ungar et al. 2004), while M. leakeyorum (15–16 Mya) shows similarities to the rather earlier Simiolus enjessi (16.5–18 Mya) that probably also reflect folivorous adaptations (Harrison 1989; Benefit 1991).

Proconsul At least two broad cranial morphologies are represented among the Lower Miocene fossils. The genus Proconsul is particularly well known, with species differing in size and dental and gnathic details, but linked by fundamental similarities in craniodental morphology (Fig. 7). Knowledge of Proconsul is primarily based on the material recovered from sites on Rusinga Island, Kenya, Page 30 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

Fig. 7 (Upper) Frontal and profile views of Proconsul heseloni cranium (Photograph # National Museums of Kenya). (Lower) Frontal and profile views of Proconsul nyanzae part face (Photograph # National Museums of Kenya)

including much of a skull in 1948 (Le Gros Clark and Leakey 1951) and a partial skeleton from 1951 and subsequently (Napier and Davis 1959; Walker and Teaford 1989; Walker et al. 1993) supplemented by other material. Initially assigned to the type species P. africanus, the 1948 and 1951 specimens were later transferred to P. heseloni (Walker et al. 1993; Walker 1997) on the basis of differences in dental size and morphology and in mandibular proportions and symphyseal reinforcement from the type of P. africanus from Koru. Compared with later hominoids, the P. heseloni cranium is lightly constructed: the globular neurocranium largely lacks pronounced tori or crests, although the medial portion of the nuchal crest is evident above the steeply angled nuchal area, and the external occipital protuberance is located high on the skull rear. The frontal is short but broad, reflecting the limited postorbital constriction, while the superior temporal lines are prominent anteriorly and converge toward the vault rear but do not meet to form a crest. On the face, the premaxilla rises on either side of the nasal aperture, contacting the nasal bones above their tip, so excluding the maxilla from the rim of the nasal aperture, which narrows inferiorly between the central incisor roots above a short nasoalveolar clivus. Above it, the nasal bones are nonprojecting, long, and narrow, extending upward beyond the frontomaxillary suture and expanding in breadth in the glabellar region. There is a prominent jugum above the upper canine root and a shallow canine fossa. The lightly built zygomatic arch originates low down, curving backward and upward, and has a well-developed malar tuberosity. The subrectangular orbits are widely separated, surmounted by weak supraorbital ridges and with a slightly swollen glabella over a large frontal sinus (which may represent a frontoethmoid sinus; see Rossie 2005) between, but there is no distinct supraorbital torus. The palate is long, rectangular, and shallow. A large, transversely broad incisive fossa joins directly with the nasal cavity, so there is no true incisive canal, and the hard palate is retracted from the subnasal alveolar process (Ward and Pilbeam 1983; McCollum and Ward 1997). There is a pronounced tuberosity on the alveolar process behind M3. The maxillary sinus extends anteriorly to the premolars and laterally into the root of the zygomatic arch. The articular eminence and postglenoid process are well developed, and the auditory region has a tubular ectotympanic as in modern catarrhines, while the prominent, well-pneumatized mastoid process is coronally narrow and rather bladelike.

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The mandibular symphysis exhibits a moderately to well-developed superior transverse torus but a much weaker and variable inferior torus, absent altogether in some individuals. The corpus displays limited lateral buttressing below the cheek teeth and shallows posteriorly; the relatively high ramus is lightly constructed, and the gonial region only slightly marked by muscle attachments. The slightly earlier, similarly sized and evidently closely related P. africanus differs from P. heseloni in numerous dental details, mandibular proportions, and symphyseal reinforcement: the P. africanus corpus is deeper anteriorly and posteriorly shallows more strongly, while the symphysis lacks an inferior transverse torus but bears a pronounced superior torus (Walker et al. 1993). An inferior transverse torus is also absent in the larger P. nyanzae. Views differ on Proconsul’s brain size and encephalization: Walker et al. estimated the 1948 cranium’s capacity as 167 cm3 and inferred that P. heseloni was more encephalized than modern cercopithecoids of similar size. Manser and Harrison (1999), however, using foramen magnum area as a size surrogate, estimated brain size as the markedly lower 130 cm3 and close to the mean encephalization value for anthropoids. The endocast’s relatively small frontal lobe and cortical sulcal pattern were considered primitive and cercopithecoid by Le Gros Clark and Leakey (1951) and Le Gros Clark (1962) but definitely not so by Radinsky (1974) who judged it hominoid and most like gibbons. More recently, Falk (1983) has argued that the sulcal pattern resembles that of extant New World monkeys, such as Ateles, rather than any group of catarrhines and approximates the inferred common ancestral sulcal pattern for Anthropoidea. Relative shearing-crest lengths in those Proconsul species studied (P. heseloni, P. nyanzae, and P. major, the last sometimes referred to the genus Ugandapithecus; see below) are less than those of any extant ape and considered to indicate frugivory (Kay and Ungar 1997), while the proportion of pits to scratches on molar wear facets (37–39 %) also indicates soft-fruit eating (Ungar 1998; Ungar et al. 2004). Despite the findings of Ravosa (2000), see above, mandibular form and proportions are also compatible with this interpretation. At the symphysis, the prominent superior transverse torus and minimal or absent inferior torus produce a broadly triangular cross section, especially in larger individuals, resistant to torsional or bending stresses produced by medial (jaw opening) or lateral (masticatory power stroke) bending (Hylander 1984; Brown 1997). Below the cheek teeth, the corpus is relatively deep vertically and narrow coronally, and, while it may be reinforced by the rear of the superior transverse torus, the mylohyoid ridge, and the lateral eminence, there is relatively little change in cross-sectional shape along the corpus compared with other fossil apes (Brown 1997). This suggests chewing activity generating comparatively high vertical forces but only limited transverse or torsional forces during food processing. It is also possible to infer aspects of the locomotor pattern of fossil taxa with reference to their cranial morphology via the semicircular canals of the middle ear; there is a general correlation between the radius of curvature of the organ of balance and the relative agility of primate taxa (Ryan et al. 2012). The ancestral catarrhine adaptation, judged from stem forms such as Aegyptopithecus, is that of a medium-slow arboreal quadruped. P. heseloni, however, is characterized by larger semicircular canals, which suggests more agile, medium-speed locomotion, much like that seen in extant macaques. One species previously assigned to Proconsul is now considered by some to be distinct at the generic level (Senut et al. 2000); Ugandapithecus is held to contain as many as four species of varying sizes and chronological ages (Pickford et al. 2009b), including the only-just-named Proconsul meswae (Harrison and Andrews 2009). The largest (and least contentious) of the species, U. major from Songhor in Kenya and Napak in Uganda, has little in the way of cranial material preserved, although all of the taxa assigned to Ugandapithecus are said to share a distinctive

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mandibular corpus that becomes shallower posteriorly. It is worth noting, however, that the generic distinction is not recognized universally (MacLatchy and Rossie 2005).

Afropithecus The contemporary Afropithecus turkanensis contrasts markedly with Proconsul in its cranial form (Leakey and Walker 1997) (Fig. 8). The large face is dominated by the long domed muzzle and deep, flaring zygomatic processes. The projecting premaxilla forms a deep nasoalveolar clivus and extends up on both sides of the broad, oval nasal aperture to contact the narrow, medially elevated nasal bones. There is an extensive maxillary sinus; the shallow palate displays large paired openings for the incisive foramen. The canine roots form prominent juga; the root of the zygomatic process is deep, anteriorly inferiorly sloping, and originates low down on the face. The cordiform orbits are broader than high, inferolaterally sloping and widely separated. The glabellar region is prominent, the slender supraorbital torus curving above each orbit and delimiting a frontal trigon with its lateral limits marked by well-defined anterior temporal lines which merge to form a distinct sagittal crest. Postorbital constriction is marked, and the temporalis muscles are well developed. The mandibular corpus is very deep with a distinct fossa, while the ascending ramus is set obliquely to the corpus. The symphysis bears moderate superior and inferior transverse tori, a long and strongly sloping subincisive planum, and a low-genial pit, implying a deep, narrow tongue. Overall facial proportions of Afropithecus are reminiscent of A. zeuxis, but absolutely much larger; finite element scaling analysis reveals marked size contrasts but minimal shape differences in the snout and some shape differences (but reduced size contrasts) in the zygomatic and maxillary tuberosity regions (Leakey et al. 1991). These authors conclude that the similarities in Aegyptopithecus and Afropithecus facial form indicate the persistence into the Early Miocene of a functionally integrated mosaic of features that characterized the primitive hominoid face. Benefit and McCrossin (1991) draw attention to craniofacial similarities between Aegyptopithecus, Afropithecus, and the Miocene cercopithecoid Victoriapithecus, indicating that many of these facial traits are primitive catarrhine characters rather than basal hominoid synapomorphies.

Fig. 8 (Upper) Frontal and profile views of Afropithecus turkanensis cranium (Photograph # National Museums of Kenya). (Lower) Frontal and profile views of Turkanapithecus kalakolensis cranium (Photograph # National Museums of Kenya) Page 33 of 68

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With its large, procumbent, and mesially inclined upper central incisors; stout, low-crowned canines; and cheek teeth covered with very thick enamel and complex wrinkling, Afropithecus has been compared, especially in its anterior dentition, to pithecines exploiting seeds and hard fruits, where the incisors crop food items and the large canines apply considerable force to puncture hard fruits, as in Chiropotes (Leakey and Walker 1997; Kinzey 1992). Cusp morphology, the high incidence of pitting in the single Afropithecus individual sampled – at 43 %, the highest of the early African forms studied (Ungar et al. 2004) – and a lack of prominent shearing crests on the cheek teeth are also consistent, like the anterior dentition, with frugivory. Overall, Leakey and Walker (1997) conclude that Afropithecus was a sclerocarp forager. Other aspects of mandible reinforcement (e.g., strong basal buttressing, a pronounced lateral tubercle where the oblique line meets the corpus, a hollowed buccal surface above the mental foramen with a marked canine jugum anteriorly) that support this interpretation are also seen in Sivapithecus (see below) and probably reflect comparable biomechanical responses to reliance on food items with similar physical properties rather than any especially close phylogenetic link. The somewhat smaller but otherwise similar Heliopithecus from the early Middle Miocene of Saudi Arabia may be no more than specifically distinct from Afropithecus (Andrews et al. 1978; Andrews and Martin 1987).

Morotopithecus The large (chimpanzee-sized) hominoid Morotopithecus bishopi (Gebo et al. 1997), based on the palate from Moroto initially assigned to P. major (Pilbeam 1969), resembles Afropithecus in many respects and may be congeneric with it. It is of Early (20–21 Mya) or Middle (15–17 Mya) Miocene age, depending on 40Ar39/Ar dating (Gebo et al. 1997) or faunal correlation (Pickford et al. 1999). It combines an anteriorly broad palate with comparatively narrow, procumbent incisors offset by a pronounced diastema from the large, stout canines, whose massive roots form pronounced juga. The molars resemble those of P. major in their bunodont cusps, wrinkled enamel, and beaded lingual cingulum, but contrast in their relative sizes, while the anterior dentition is much larger and the interobital breadth narrower than in P. major. Overall the face is relatively long and narrow, with a broad nasal aperture, a short clivus, and an extensive maxillary sinus. The undoubted resemblances in face and dentition to Afropithecus may reflect dietary convergence in exploiting hard-cased fruits rather than phylogenetic propinquity. Postcrania referred to Morotopithecus resemble those of Proconsul in some respects but are also markedly more derived in the direction of modern hominoids in the lumbar, shoulder, hip, femur, and knee regions and point to forelimb suspension and slow brachiation, as well as climbing and quadrupedal activity in an arboreal habitat (MacLatchy 2004).

Nyanzapithecus Nyanzapithecus is much less well known, but premaxillary and maxillary fragments of two species, N. vancouveringorum from the Early Miocene (17–18.5 Mya) and N. pickfordi from the Middle Miocene (15–16 Mya), indicate contrasts with Afropithecus in their smaller size; shorter faces; low, broad nasal apertures; and robust premaxillary regions (Harrison 2002). These species and the rather smaller Middle Miocene N. harrisoni (13–15 Mya) display broad, strongly built upper and lower incisors, while the cheek teeth are long and narrow; the molars bear low, expanded cusps and rounded occlusal crests. Mabokopithecus, represented by two isolated rear lower molars and an almost complete mandible, is dentally very similar to N. pickfordi and may well be congeneric with Nyanzapithecus, in which case the former genus has priority.

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Rangwapithecus The Early Miocene (19–20 Ma) Rangwapithecus gordoni, similar in size and probable locomotor pattern to the smaller Proconsul species, contrasts dentally with them in numerous respects, including molars with low cusps and well-developed crests, enamel wrinkling, and a pronounced wear differential. Cranial material indicates a comparatively short premaxilla and long, narrow palate widening toward the rear. The maxillary sinus is deep and the zygomatic root set low down the face above M1–M2; the mandible is deep and the symphysis reinforced with a pronounced superior transverse torus. Kay and Ungar (1997) and Ungar et al. (2004) have argued that, on the basis of its molar crest development (greater than that of any other Early Miocene form) and the low incidence and long, narrow form of dental pitting, Rangwapithecus is likely to have been folivorous. Dental proportions and macrowear, facial morphology, palatal proportions, and mandible structure are all compatible with this interpretation.

Turkanapithecus The somewhat younger (16.6–17.7 Mya) Turkanapithecus kalakolensis is another medium-sized form, rather smaller than P. heseloni, and represented by a partial cranium preserving the upper dentition save for the incisors and a mandible with left M2 and right M3 (Fig. 8). The skull exhibits a relatively short face with broad, domed snout; a wide, oval nasal aperture flanked by prominent canine pillars, with expanded nasal bones; and a broad, flat interorbital region above. The palate is narrow, with posteriorly convergent tooth rows, and there is an extensive maxillary sinus. The zygomatic process originates low down on the face, and the arch is relatively deep and flaring. This, combined with pronounced postorbital constriction, makes for a deep infratemporal fossa and, presumably, well-developed temporalis muscle – a view also supported by the strongly marked and convergent temporal lines, pointing to a sagittal crest. The rear of the saddle-shaped glenoid cavity is bounded by a well-developed postglenoid process, but there is no distinct articular eminence. The nuchal area is comparatively short and the crest strongly developed, reflecting both the rugged facial architecture and comparatively small neurocranium, estimated at c. 85 cm3 – absolutely and relatively smaller than P. heseloni (Manser and Harrison 1999). Given this cranial morphology, it is rather surprising that the mandibular symphysis displays neither strongly developed superior nor inferior transverse tori. The corpus is shallow and relatively slender, with constant depth below the molars, while the ramus is broad, low, and sloping, with an expanded gonial region, so according with zygomatic architecture indicating well-developed masseter muscles – and a knoblike condyle. Upper first premolars are large, and while both upper and lower molar teeth increase in size posteriorly, the gradient is much less than in comparably sized Proconsul species. Overall, craniodental features suggest a resistant diet, possibly consisting of hard-cased fruits or leaves.

Dendropithecus There is also a cluster of small- to medium-sized forms (perhaps 3–9 kg), usually grouped together as dendropithecoids. The siamang-sized Dendropithecus macinnesi, based on material originally assigned to Limnopithecus, displays narrow, high-crowned incisors; strongly dimorphic canines; broad premolars; and molars with high cusps, sharp occlusal crests, and well-defined foveae. The palate is narrow, as is the nasal aperture; the maxillary sinus is extensive and the mandible corpus low and robust, with the symphysis reinforced by fairly prominent superior and inferior transverse tori. Among Early Miocene hominoids, Dendropithecus has the least well-developed molar shearing crests of those studied other than Proconsul and a fairly high incidence of pitting, pointing to a predominantly soft-fruited dietary niche (Kay and Ungar 1997; Ungar et al. 2004). Page 35 of 68

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Limnopithecus Other small Early Miocene forms, known principally from isolated teeth and part jaws, include Limnopithecus legetet and L. evansi. These have a short lower face, with anteriorly positioned orbits; narrow, elliptical nasal aperture; and a shallow clivus, an inflated maxillary sinus, and a shallow, lightly built mandible reinforced symphyseally by a strongly developed superior transverse torus but with an inferior torus that is weak (L. evansi) or absent (L. legetet). L. legetet combines broad, low-crowned incisors and small canines with an ovoid P3 that suggests only part development of the C–P3 honing complex, and cheek teeth with high, sharp cusps and occlusal crests. L. evansi has narrower, higher crowned incisors, larger canines, and a better developed sectorial face on P3, cheek teeth with lower, rounded cusps, and less sharply developed occlusal crests. Relative shearing-crest development suggests a fairly folivorous niche (Kay and Ungar 1997).

Kalepithecus Less well known than these forms is the broadly contemporary Kalepithecus songhorensis, similar in dental size to L. legetet, but differing in most other respects. The anterior teeth are relatively large, with I1 broader and more spatulate, the upper premolars relatively narrow but the molars relatively broad; P3 is moderately sectorial, the short, broad lower molars with low, rounded, and expanded cusps, and poorly developed occlusal crests. Kalepithecus contrasts with other Early Miocene forms in its inferiorly broad nasal aperture and deep clivus, while dental morphology and proportions suggest a frugivorous diet.

Middle and Late Miocene African Hominoids Fossil hominins apart, evidence of African hominoids from the Middle Miocene onward is limited, especially, when contrasted with the comparatively abundant Early Miocene material. Nonetheless, recent discoveries have both significantly increased the number of fossils (Ward and Duren 2002) and led to major reappraisals of earlier finds, notably of the material assigned to “Kenyapithecus” africanus (Leakey 1967), which has been reallocated to distinct taxa, with consequent systematic and phyletic implications.

Nacholapithecus One such taxon is the large, markedly dimorphic Nacholapithecus kerioi (Ishida et al. 1999, 2004), based on material from Middle Miocene (15 Mya) sites in Samburu District, Kenya. Cranial remains display overlap of the posterior premaxilla and hard palate, forming a short incisive canal (Kunimatsu et al. 2004), which may indicate an intermediate condition between the nonoverlapping subnasal configuration of gibbons and fossil stem hominoids and the longer incisive canal that is a diagnostic trait of the clade that includes the extant large-bodied apes (Nakatsukasa and Kunimatsu 2009), or Hominidae. The incisive foramen is small, while the face bears strong canine pillars and deep fossae, and the zygomatic process originates low down on the maxilla. The mandible corpus is tall but thin, with a near vertical symphysis, a moderate inferior transverse torus, and a lateral fossa below the premolars. I1 is high crowned and robust, while both lower incisors are tall and narrow. Canines are low crowned, upper premolars display marked cusp heteromorphy, and molars are thick enameled.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

Equatorius

Other material previously assigned to “K.” africanus has been incorporated, along with new discoveries (including a part skeleton (KNM-TH 28860) from Kipsaramon, Tugen Hills, and multiple finds at Maboko Island and adjacent localities, Kenya), in another, broadly contemporary (14–15.5 Mya) large-bodied, dimorphic species Equatorius africanus (Ward et al. 1999). While initially criticized – see, for example, Begun (2000) and Benefit and McCrossin (2000) and response by Kelley et al. (2000) – the current consensus is that E. africanus is a valid taxon. The species is characterized by broad I1s with marginal ridges, markedly asymmetrical lateral incisors, with a spiral lingual cingulum, and relatively large upper premolars with reduced cusp heteromorphy (contra Nacholapithecus). The procumbent, narrow lower incisors are tall, whereas the mandibular canines are low crowned with convergent roots. The thick-enameled, bunodont lower molars increase markedly in size along the tooth row. The maxilla exhibits a very low, broad root for the zygomatic process and an extensive sinus extending into the premolar region, while the mandible displays a long, inclined sublingual planum, a prominent inferior transverse torus, and a robust corpus. The partial skeleton and other postcranial fossils indicate some resemblances to earlier forms such as Proconsul and Afropithecus, but with forelimb and hind limb contrasts that point to significant terrestriality (Sherwood et al. 2002; Patel et al. 2009). It remains to be determined whether ground vegetation formed an appreciable component of Equatorius’ diet, but dental similarities to Afropithecus (and “Heliopithecus”), especially in canine form and premolar proportions, suggest resistant foods, such as seeds and/or hard-cased fruits, as major dietary items.

Kenyapithecus The genus Kenyapithecus is retained for the rather later (14 Mya) species K. wickeri, known from partial jaws and isolated teeth from Ft. Ternan, Kenya. The maxilla exhibits marked canine fossae, a relatively low and anteriorly positioned origin for the zygomatic process above M1, little extension of the maxillary sinus into the inflated alveolar process (in contrast to Equatorius), and a relatively highly arched palate. The upper incisors are markedly heteromorphic, with I2 much smaller than I1, which is reinforced by strong lingual marginal ridges extending across the base of the crown surface. The upper canines exhibit marked dimorphism: robust, tall, and externally rotated in presumed males, more conical in females. P4 is relatively broad with subequal cusps; M1 is quadritubercular and lacks a lingual cingulum, while M2 is similar but larger. The postcanine teeth are closely packed, with low cusp relief and appreciable wear. The mandible, considered female, displays a shallow symphysis, sharply retreating at 30–40
to the alveolar margin, with pronounced inferior transverse torus extending to below the mesial root of M1, rather weak superior torus and long sublingual planum, a short incisor row, and a robust, comparatively shallow but thick corpus. As reconstructed, the mid-lower face overall was broad and flat, with wide cheeks and a short snout (Andrews 1971; Walker and Andrews 1973). The relatively tall-crowned lower canine bears only a slight lingual cingulum, while P3 is obliquely set and sectorial, with a distinct honing facet for the upper canine, and P4 bears prominent mesial and smaller, lower distal cusps; the poorly known lower molars apparently lack buccal cingula. The narrow anterior dental arcade, procumbent incisors with curved roots, anteriorly positioned zygomatic origin, restricted maxillary sinus and mandible with markedly sloping symphysis, pronounced inferior transverse torus, and shallow, robust corpus differentiate K. wickeri from most other African hominoids. Andrews (1971) and Walker and Andrews (1973) interpret these traits as a functional set adapted for powerful chewing activity with a strong lateral grinding component and pronounced incisal action. There are similarities, especially in the anterior dentition, Page 37 of 68

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with Afropithecus, and, as with that genus, pithecines have been proposed as the most plausible dietary analogues (Leakey and Walker 1997; McCrossin and Benefit 1997). This model of K. wickeri as a sclerocarp feeder, exploiting hard-cased/hard-stoned fruits, seeds, and nuts, is compatible with reconstruction of the Ft. Ternan environment as drier and more seasonal than many earlier African sites, predominantly closed-canopy woodland with both open country and forested conditions nearby (Andrews 1996; Andrews et al. 1997). A second species of this genus, K. kizili (Kelley et al. 2008), has been named for material found outside of Africa and will be treated below.

Otavipithecus Broadly contemporary at 13 + 1 Mya, the more southerly Otavipithecus namibiensis is known from a part mandible and frontal bone from Berg Aukas, Namibia (Conroy 1997; Conroy et al. 1992). The incisor region of the mandible is narrow and the symphysis reinforced by a short inferior transverse torus. The corpus is robust, of constant depth, and relatively long, with the ramus originating behind M3 and with a distinct retromolar space. Premolar and molar cusps are inflated and bunodont, mesial, and distal foveae small and enamel thin. The frontal bears superciliary ridges rather than a transverse torus, with marked temporal ridges adjacent to glabella, relatively wide interorbital dimensions and an extensive frontal sinus. The last of these traits has been used to link Otavipithecus with extant hominines (Pickford et al. 1997), but the current lack of clarity as to the polarity of frontal sinus evolution in catarrhines renders this interpretation premature at best. The narrow incisor region does not support a niche of specialized frugivory, while the thin enamel and minimal wear differential on the molar teeth point to a nonabrasive diet; there are no obvious dental adaptations to folivory. Conroy argues that O. namibiensis probably subsisted on a range of plant foods that required little preparation by the anterior teeth prior to chewing.

Samburupithecus A later Miocene (9.5 Mya) large‐bodied species from the Samburu Hills of north central Kenya named Samburupithecus kiptalami is known only from one left maxilla with P3–M3 crowns and the canine alveolus (Ishida and Pickford 1997). The palate displays a marked arch, a shallow postcanine fossa, a low origin for the zygomatic root, and invasion of the zygomatic process by the extensive maxillary sinus. The nasal floor has a sharp margin, and the tooth row is straight from the canine alveolus to M3. The three-rooted premolars have elongated crowns with coequal main cusps, while the molars display inflated, bunodont cusps and thick enamel. S. kiptalami’s affinities are unknown; some workers consider it to show some similarities with the gorilla, although there are also undoubted differences, e.g., the size of lingual cingulae. This and other traits make it most likely that Samburupithecus is a late-surviving part of the stem hominoid radiation that included Proconsul (Olejniczak et al. 2009). Two newly discovered taxa have increased our knowledge of the later Miocene of Africa substantially. Nakalipithecus nakayamai is a large ape (>50 kg) from the early Late Miocene (9.9–9.8 Mya) site of Nakali, Kenya (Kunimatsu et al. 2007). Although known from only a few dentognathic remains, its striking resemblance to the slightly younger Ouranopithecus from Greece suggests that the popular paleobiogeographic scenario of large-bodied apes originating in Eurasia before reinvading Africa (Stewart and Disotell 1998) may need to be reexamined. The mandible of the holotype has a well-developed simian shelf (inferior transverse torus) and the thick dental enamel, reduced molar cingulae and reduced upper premolar cusp heteromorphy seen in Eurasian forms that have been considered more closely related to living hominids than African forms, although it retains the primitive non-compressed lower mesial premolar shape. A second largePage 38 of 68

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bodied form, Chororapithecus is known from dental remains found in 10–10.5 Mya deposits in the Afar region of Ethiopia (Suwa et al. 2007). Aside from their similar size, the Chororapithecus molars are also similar to those of Gorilla in their relative development of molar shearing crests associated with folivory. Although not linked directly with the extant taxon, partly due to its thicker enamel caps, the resemblance suggests to the describers that it may belong to same clade. Two other possible new taxa, Kogolepithecus from the ca. 17 Mya site of Moroto II in Uganda (Pickford et al. 2003), and a single mandibular fragment from between 11 and 5 Mya in Niger (Pickford et al. 2009a) are too fragmentary to allow any convincing analysis. Other, later taxa, closer to the Mio-Pliocene boundary (Sahelanthropus, Orrorin), are as yet only incompletely described but are claimed as basal hominins (see volume 3 Chap. ▶ 6 by Senut). The known time span of Pan has recently been extended by the recovery of four fossil teeth (r and l I1, l M1, r M3) from Middle Pleistocene deposits of the Kapthurin Formation of the Tugen Hills, Kenya, within the eastern Rift (McBrearty and Jablonski 2005). The broad, spatulate incisors bear deep mesial and distal foveae separated by a prominent lingual tubercle and the molars are low crowned, while all teeth exhibit thin enamel. The large hypocone on M1 suggests P. troglodytes rather than P. paniscus, although McBrearty and Jablonksi are cautious in attributing specific identity, preferring assignment to Pan sp. indet. The finds date from around 0.5+ Mya, and the site lies some 600 km east of the present chimpanzee range. The teeth were discovered close to localities yielding part mandibles of Homo (H. erectus or H. heidelbergensis/H. rhodesiensis) pointing to sympatry and suggesting that adaptive scenarios which reconstruct differentiation of chimpanzee and hominin populations through the Rift Valley acting as an isolating barrier are unlikely to be correct. Fossil evidence for bonobos and gorillas is entirely lacking.

Europe and Asia Minor While there is limited evidence dating from 15 to 17 Mya, the bulk of the European and west Asian hominoid material is from later Miocene sites between 6 and 12 Mya (Kay and Simons 1983; Pilbeam 2002). Many of these suggest subtropical seasonal forest or woodland as the dominant habitat; there is evidence of swamp conditions at some sites, while possibly harsher, more open environments are indicated at sites in Greece and Turkey yielding Ouranopithecus and Ankarapithecus, respectively.

Griphopithecus The earliest evidence (13.5–17 Mya) consists of several low-crowned, large‐cusped, and thick‐ enameled molars from Germany, Austria, and Slovakia assigned to Griphopithecus, a genus better known from Turkey, where a mandible with cheek teeth from Çandır and maxillary teeth from Paşalar dating from c. 15 Mya are referred to G. alpani (Alpagut et al. 1990). Like their European counterparts, the lower molars have bunodont, thick‐enameled cusps, and well-developed buccal cingula. The upper central incisors are relatively narrow with a distinct median lingual pillar, and the male canines, especially in the upper jaw, are robust and comparatively low crowned. The mandible is strongly constructed, with both a prominent superior and well‐developed inferior transverse torus at the symphysis and a long, shallowly inclined planum alveolare. Heizmann and Begun (2001) suggest that Griphopithecus evolved from an Afropithecus/ Heliopithecus-like thick-enameled ancestor and that this feature, together with the associated trait of low-dentine penetrance, was crucial to the expansion and success of dentally modern hominoids in the more seasonal Middle and Late Miocene habitats of Eurasia. However, at least one successful Page 39 of 68

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European form – Dryopithecus – had comparatively thin enamel, pointing to this as either a secondarily derived trait evolved from a thicker-enameled European ancestor or that the genus represents a second hominoid radiation into Europe. Also at Paşalar, the species Kenyapithecus kizili (Kelley et al. 2008) is found. It has been linked to the African genus primarily due to the lack of lingual pillars in the upper central incisors, by which it differs from the other Paşalar hominoid Griphopithecus, although there are also some maxillary similarities. Unusually, the entire hypodigm of the taxon is thought to be from a single birth cohort, as all are the same developmental age and show identical enamel hypoplasias (Kelley 2008). As the molar teeth are extremely similar to those of Griphopithecus, it is assumed that their adaptation was similar, as well.

Dryopithecus The thin molar enamel of Dryopithecus results in frequent dentine exposure, especially on the cusps, which lie close to the crown margins around a broad, shallow fovea. Below the narrow, low P3 crown enamel extends onto the anterior root, pointing to at least partial honing against the upper canine (Begun 2002), while the upper central incisors are narrow and high crowned. Larger (presumed male) mandibles are generally more robust than in the Early Miocene east African forms but are not as strongly built as more thickly enameled taxa (Begun 2002). All species in which evidence is available display a relatively high root for the maxillary zygomatic process. Compared with Proconsul and other Early Miocene forms, Dryopithecus has reduced cingula, relatively short lower molars (Szalay and Delson 1979), expanded occlusal surfaces, and reduced molar crown flare and a mandibular symphysis reinforced by a prominent inferior transverse torus. Until recently, the type species, D. fontani (11–12 Mya), was among the less well‐known fossil hominoids cranially. New material from Catalonia, NE Spain (Moyà-Solà et al. 2009a, b), however, has dramatically improved our understanding of this chimpanzee-sized ape. A partial cranium dated to 11.8 Mya preserves several hominoid and hominid synapomorphies: a large nasal aperture with its widest portion located inferiorly and its margin constructed primarily of the maxilla, over a hard palate that is wide anteriorly. Unlike other large-bodied apes, however, the zygomatic slopes posteriorly from the orbital margin to the root, although there is mid-facial prognathism as well. The authors describe the steep face and vertical orientation of the nasal aperture as resembling extant Gorilla, in contrast to earlier stem hominoids with more sloping anterior maxillae. The subnasal morphology is stepped, as in extant hominines, but the premaxilla does not overlap the maxilla at the midline, which suggests a more primitive condition than that seen in Nacholapithecus. It has rather broader canines than other species, frequent cingula on the lower molars, while in larger mandibles the corpus shallows markedly from the symphysis toward the rear, unlike other species.

Rudapithecus Although formerly placed in Dryopithecus, the slightly younger (9.5–10 Mya) Rudapithecus hungaricus (Kivell and Begun 2009) is also well known cranially (Fig. 9). Comparable in tooth size to D. fontani, it differs in its labio‐lingually thicker incisors, narrower canines, reduced molar cingula, and more tapered M3. The mandibles have weak symphyseal tori, but the corpus is reinforced below M1–M2 by a lateral eminence. Cranial morphology is comparatively well known from several incomplete specimens from Rudabanya, Hungary (Begun and Kordos 1997; Kordos and Begun 2001). The braincase is elongated, with a flat frontal displaying moderate postorbital constriction and strong anterior temporal ridges; supraorbital reinforcement is weak, but there is a fair‐sized frontal sinus.

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Fig. 9 (Upper) Frontal and profile views of Rudapithecus hungaricus part skull (Photograph courtesy D. Begun). (Lower) Frontal and profile views of Pierolapithecus catalaunicus cranium (Photograph courtesy S. Moyà-Solà)

At the skull, rear inion is relatively highly positioned, while the mandibular fossa is transversely deep, with marked entoglenoid and postglenoid processes. The face is moderately projecting and deflected downward. The maxillary sinuses are larger than those of the East African fossils, and the nasal aperture has a broad base with subvertical sides. Again, in contrast to the early East African specimens where preserved, the subnasal floor is stepped, with the rear of the subnasal alveolar process extending over the palatal process of the maxilla, and an incisive canal is present. The long and projecting premaxilla is sagittally and transversely convex. The preserved semicircular canals suggest that Rudapithecus practiced relatively slow locomotion (Ryan et al. 2012).

Hispanopithecus A smaller contemporary of Rudapithecus and also previously considered a species of Dryopithecus (Cameron 1997), Hispanopithecus laietanus is known from several sites in NE Spain (Begun 2002). Two partial skeletons have been discovered: a presumed male (39 kg) from Can Llobateres (Moyà-Solà and Köhler 1996) and a female (22–25 kg) from Can Feu (Alba et al. 2012). Mandibular teeth resemble those of Rudapithecus, but the premolars are relatively smaller, the molar cusps more rounded and expanded around the occlusal margins, and M3 less tapered. CLI‐18800 preserves the upper dentition: the incisors are like those of Rudapithecus, the canines have strongly curved roots and narrow crowns, and the molar teeth increase in size posteriorly. In its known craniofacial structures, Hispanopithecus shows many similarities with Rudapithecus, including periorbital and maxillary morphology, the supraorbital region, frontal sinuses, and a locomotor pattern reconstructed as low, as determined via semicircular canal size. There are also contrasts, however, with CLI‐18800 displaying a very high root for the zygomatic process and a relatively deep and flatter anterior aspect of the zygoma. The upper incisor row is more strongly curved, and the premaxilla is strongly biconvex. Overall the facial profile of Hispanopithecus is more concave.

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The slightly earlier (c. 10.5 Mya) H. crusafonti, also from NE Spain, is known only from a mandible and some isolated teeth. Dentally slightly larger than H. laietanus, it is distinguished by comparatively broad upper canines, relatively longer upper premolars than in Rudapithecus, and relatively broader upper molars than H. laietanus. The mandible combines an exceptionally robust corpus with comparatively small tooth crowns; the symphysis is reinforced by a strong inferior transverse torus and the corpus bulges laterally below M1–M3. Hispanopithecus differs from the geographically close Anoiapithecus in that the molar crowns are relatively narrower, as are the buccal cuspulids, the hypoconulid is less centrally placed, and cingulids are lacking (Alba et al. 2012). Overall, dental features of all three genera, such as relative shearing-crest development (Ungar 1996; Kay and Ungar 1997), pitting incidence of >35–58 %, the highest of any fossil ape studied) and distinct wear on the incisors (Ungar 1996; Ungar et al. 2004), while the Ouranopithecus shearing quotient (and so relative shearing-crest development) is lower than that of any modern hominoid or other European fossil ape studied (Ungar and Kay 1995; Kay and Ungar 1997). In all these features, Ouranopithecus resembles extant hard-object feeders, pointing to exploitation of a similar niche – perhaps seeds, nuts, roots, and tubers, and other terrestrial vegetation. There are obvious resemblances here to some reconstructions

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of early (Plio-Pleistocene) hominine dietary niche(s), although these are unlikely to mirror any specially close phylogenetic link. De Bonis and Koufos (1997) argue that this model of Ouranopithecus’ diet is consistent with reconstruction of its open habitat (De Bonis et al. 1992), although Andrews (1996) and Andrews et al. (1997) urge caution, considering the overall fauna to be undiagnostic other than indicating a strongly seasonal, possibly harsh, environment. The poorly known Graecopithecus freybergi (von Koenigswald 1972), based on a single mandible from Tour la Reine, Pyrgos, Greece, and dated around 6.5–8 Mya, is often regarded as congeneric or even conspecific with O. macedoniensis (Martin and Andrews 1984; Andrews 1996), although Begun (2002) makes a strong case for its retention as a separate taxon based on molar size and mandible proportions.

Ankarapithecus Ankarapithecus meteai (Ozansoy 1965), from sites in the Sinap Formation of Anatolia, Turkey, dated at c. 10 Mya, is a strongly built form known from cranial material including the type mandible and a partial face (Fig. 10), together with undescribed postcrania (Alpagut et al. 1996; Begun and Gulec 1998). The face is tall and markedly prognathic in both midface (unlike Sivapithecus and Pongo) and premaxillary regions. The clivus is biconvex, with large, low-crowned, and labiolingually thick central incisors and smaller lateral incisors. Male upper canines are relatively low crowned, and their roots form strong juga converging on the broad nasal aperture, with relatively shallow canine fossae beyond. The palate is deep, with the root of the zygomatic process set comparatively high above M1 and into which the large maxillary sinuses extend. The vertically orientated, laterally flaring zygomatic process imparts strong anteriorly and laterally directed components to masseteric action, while the deep temporal fossa allows for a powerful temporalis muscle. The subnasal fossa is stepped and the incisive fossa large. The orbits are square, with a narrow interorbital space, very long nasal bones, broad, rounded orbital pillars, and prominent anterior temporal lines. Rather surprisingly in view of the rugged mid- and lower face, the superciliary arches above the orbits do not form a true torus. The massive mandible is strongly buttressed, with a very deep, narrow, and vertical symphysis and the inferior traverse torus extending to the level of M1. The rear of the corpus is very thick and the ramus broad. The lower incisors are labiolingually thick, narrow, and tall crowned, set almost vertically in a straight line between the low-crowned canines, which in males are more massive than in Dryopithecus or Ouranopithecus in basal section, while female canines are more premolariform, as in the latter genus. P3 is large, oval, and elongated, with a large mesial beak comparable to Dryopithecus but smaller than Ouranopithecus, and P4 is large and relatively broad, while M1 is small relative to M2. Upper and lower molars are broader relative to their lengths than in other later Miocene forms; their occlusal surfaces have broad, flat cusps and shallow basins and lack cingula. Andrews and Alpagut (2001) provide a valuable functional analysis of this taxon as a hard-object feeder in dry seasonal subtropical forest (Andrews 1996), illuminating aspects of A. meteai morphology and also that of other Miocene hominoids. In many features, Ankarapithecus resembles Ouranopithecus: dentally in the large, low-crowned and worn incisors; large cheek teeth; thick enamel; flat occlusal wear; poor shearing-crest development; and also in aspects of facial architecture and mandibular reinforcement. However, there are also differences: the supraorbital region differs, the Ankarapithecus interorbital region is narrower as are the lateral orbital margins, the midface is more prognathic, and the zygomatic root originates higher on the maxilla, while the mandibular corpus is massively thickened under the rear molars, so that it is actually broader than deep, whereas that of Ouranopithecus is deeper and narrower in cross section.

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Oreopithecus Oreopithecus bambolii, a comparatively large-bodied form dating from 6 to 7 Mya, is represented by multiple specimens from northern Italy, including a largely complete skeleton, making it the bestknown European fossil primate. This has not prevented protracted debate about its affinities, although in recent years there has been a growing consensus that Oreopithecus is a primitive hominoid. Whatever its phyletic status, it is clear that Oreopithecus differs markedly in adaptive features and inferred niche from other Late Miocene European and West Asian hominoids. The Oreopithecus skull combines a relatively small, low, but globular neurocranium with a deep, broad, and moderately projecting face that reflects anterior placement and projection of the midface and nasal region, for the premaxilla and clivus are short and comparatively vertical. The supraorbital torus is well developed, the interorbital region broad, and the nasal bones short and salient. Strong canine pillars are bounded by shallow canine fossae, while the zygomatic process is comparatively deep with a low, anteriorly placed root originating above P4/M1, and the zygomatic arch is long, flaring, and upwardly curved posteriorly. The alveolar region has deep but restricted sinuses. The saddle-shaped articular eminence is broad and long, with a large entoglenoid process. The articular and tympanic portions of the temporal are not fused, but the temporal petrous is hominid-like in its shallow, indistinct subarcuate fossa. The mastoid is broad and continuous with the extensive, strongly marked nuchal area. Zygomatic flare and mandibular proportions point to powerful, fleshy temporal muscles, as do the deep nuchal and sagittal crests, meeting high on the skull rear; the sagittal crest continues well forward before dividing into two prominent anterior temporal lines. The strongly built mandible is large, with corpus height decreasing slightly along the cheek teeth row, and with strong reinforcement provided by the pronounced lateral eminence below the molar region. The ramus is broad and high with an expanded gonial region. There are pronounced markings for the masseters and medial pterygoids, while the condylar processes, below the broad and convex condyles, display strong markings for the lateral pterygoids. Many of these cranial features can be considered representative of the primitive catarrhine morphotype (Harrison 1986); the exceptions are those features of the maxilla, zygomatic region, and mandible summarized above that can be related to masticatory power (see below). The dentition is highly derived: the incisor teeth are small overall and vertically implanted; those in the mandible are labiolingually compressed, while the uppers are heteromorphic with I1 exhibiting a distinctive projecting lingual cusp. Canines are basally stout but not very tall and only loosely interlock, with a diastema small or absent. Larger (male) upper canines are strongly compressed and with a sharp rear edge, the lowers are more rounded in section; smaller (female) upper canines are rather incisiform. Much canine wear is from the tips; there was some C1/C1 honing, and some larger upper canines show evidence of slight honing against P3, but smaller ones lack this, and the anterior face of C1 did not hone against I2. The lower premolars are bicuspid, with P3 oval in outline and P4 more rectangular; upper premolars are oval with subequal cusps. Upper and lower molars are elongated and bear tall, spiky cusps with deep notches between. Besides the four main upper molar cusps, a metaconule is positioned centrally on the crista obliqua, often linked to the hypocone by a crest. On the lower molars, the protoconid and hypoconid (buccally) and meta- and entoconid (lingually) are joined by sharp crests to a well-developed centroconid on the cristid obliqua, so mirroring the upper molars in their distinctive occlusal pattern. The hypoconulid is frequently split into several smaller cusps. M1 usually bears a small paraconid, which is rarely present on M2 and never on M3. M1 and M2 are subequal in size, and M3 is the largest tooth. The inner ear shows adaptations to medium-slow agility, somewhat more active than in Rudapithecus/Hispanopithecus, but marginally less so than Proconsul.

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Although it displays some primitive features, the postcranial skeleton is apelike, indicating a degree of orthogrady, forelimb suspension, and strong grasping capabilities in the feet. The thorax is broad, the lumbar region short, and the iliac blades are short and broad, with a prominent anterior inferior iliac spine. The forelimbs are much longer than the hind limbs and display multiple adaptations to stability and hyperextension at the elbow joint and rotation in the forearm. There were a wide range of movements at the wrist, with short palms and long, curved fingers. The femora show weight-bearing adaptations at hip and knee, with flexible, wide-ranging movements at the ankle, and a short midfoot with long, strongly muscled digits including a powerful, opposed hallux. Oreopithecus postcrania’ reduced anterior dentition, expanded cheek teeth with complex occlusal morphology, relatively deep and orthognathic face, small neurocranium combined with large ectocranial crests and powerful chewing muscles, and robust mandible all point to a specialized folivorous diet of bulky, relatively low-grade food items which, judging by postcranial morphology and proportions, it exploited largely via an underbranch milieu. This conclusion is reinforced by study of relative shearing-crest development (Ungar and Kay 1995; Kay and Ungar 1997), which shows it to have the highest shearing quotient of any catarrhine studied, substantially in excess of any extant or other fossil hominoid. Further support is provided by dental microwear patterns, with a very low proportion (17 %) of pitting on phase II facets (Ungar 1996; King 2001; Ungar et al. 2004), consistent with extreme folivory. This wholly accords with reconstructions of Oreopithecus’ paleoenvironment, which indicates lowland mixed broad-leaved and coniferous forest, with bushes, ferns, and sedges accumulated under swampy conditions (Andrews et al. 1997; Harrison and Rook 1997). However, see Alba et al. (2001) for an alternative and, to our minds, less convincing interpretation of the Oreopithecus skull based on biomechanical constraints associated with orthograde posture and bipedalism. These authors derive Oreopithecus cranial morphology from a Dryopithecus-like ancestor by a process of neoteny.

South and East Asia Sivapithecus The best-known Asian fossil ape genus is Sivapithecus, from Late Miocene (8.5–12.7 Mya) deposits in the Siwalik Hills of India and Pakistan and including material assigned to Ramapithecus prior to the 1980s (Pilbeam 2002). Sivapithecus is rare throughout the Siwalik record, comprising only c. 1 % of the mammalian community (Ward 1997). Despite this, aspects of its cranial morphology are relatively well known through discoveries over the last three decades; in particular, a partial skull (GSP 15000) from Potwar, Pakistan, provides much information on facial and gnathic morphology (Fig. 11). It consists of the left side of the face with zygomatic arch, palate, mandible, and complete adult dentition (Pilbeam 1982). The specimen indicates many similarities with Pongo in its overall facial proportions (but see below): the orbits are taller than broad and high-set, ovoid in outline, and the zygomatic foramina are large. The interorbital distance is very narrow, while the lateral orbital pillars are slender, especially sagittally, and there are distinct supraorbital ridges but no continuous torus. Postorbital constriction is marked, with the anterior temporal lines strongly convergent, implying a well-developed sagittal crest in larger individuals. The frontal rises more steeply above the orbits than in extant nonhuman African apes and is orangutan-like in its contour and the absence of a frontoethmoid sinus. The nasoalveolar clivus is long and strongly curved, intersecting the alveolar plane at a shallow angle. As in the orangutan but in contrast to Dryopithecus, Ouranopithecus, and Ankarapithecus, the Page 47 of 68

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

Fig. 11 Three-quarter frontal and profile views of Sivapithecus indicus (Photograph courtesy D. R. Pilbeam)

nasal floor is smooth, with the premaxilla curving into the nasal cavity and joining the palatal process without a step; the incisive fossa and incisive foramen are both tiny, linked by a very narrow incisive canal. The long, medially convergent canine roots are externally rotated, while the deep zygomatic process is thin and Pongo-like in its flare. These features result in exceptionally prominent canine pillars reinforcing the robust anterior midface and well-marked canine fossae lateral to them (Ward and Pilbeam 1983). The GSP 15,000 mandible is deep and strongly built, the symphysis exhibits pronounced buttressing, the corpus is of fairly constant depth along the tooth row, while the ramus is high and broadest at the level of the occlusal plane, tapering slightly superiorly. The facial contour is Pongo-like in its marked concavity, nasoalveolar clivus projection, superoposterior slope to the zygomatic process and lateral orbital pillar, and the upward inclination of the zygomatic arch itself. Nonetheless, there are contrasts with the orangutan: the Sivapithecus midface is much longer, the nasal bones especially so, and the maxillary sinus is more restricted (Ward 1997). The mandible in particular contrasts with Pongo in most features other than its high ramus; while highly variable (Brown 1997), all Sivapithecus specimens display markings for the anterior digastric muscles which are absent in orangutans (see above), and the inferior transverse torus does not extend as posteriorly as in Pongo (Brown 1997). There are also contrasts in corpus cross section: Sivapithecus specimens have robust, broad corpora, ovoid below the premolars, more triangular below M3, with smaller specimens relatively shallow, larger ones deeper. They show marked relief, with an intertoral sulcus near the lingual base below the cheek teeth, and a pronounced lateral eminence which continues to the base, whereas in orangutans the lateral eminence is usually a much less prominent swelling restricted to the upper part of the corpus. Sivapithecus mandible proportions have been interpreted as resisting sagittal bending loads on the balancing side and pronounced torsional and shearing loads on the working side, associated with powerful molar action and, as a possible secondary factor, incisal biting (Kelley and Pilbeam 1986; Brown 1997). Dental features accord with this interpretation: the upper incisors are strongly heteromorphic, and the central teeth are very wide and spatulate with a heavily crenulated, extended lingual tubercle; the laterals are much narrower. The canines are moderately tall, compressed, and outwardly rotated and display only limited dimorphism. P3 is larger than P4, while the mandibular premolars are broad, with P3 expanded mesiobuccally and displaying only limited evidence of upper canine honing. The thickly enameled molars lack cingula and display expanded, bunodont cusps and so limited occlusal foveae. In the upper jaw, M2 is the largest tooth, while M3 is the largest of the relatively short and broad lower molars. The cheek teeth are closely packed, with clear interproximal wear facets and, despite the thick enamel, often display a pronounced wear gradient with, in older individuals such as GSP 15,000, destruction of crown relief and extensive dentine exposure.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_35-6 # Springer-Verlag Berlin Heidelberg 2014

Overall, evidence points to Sivapithecus as a frugivore/hard-object feeder, possibly nuts, seeds, bark, or hard-pitted fruits, requiring powerful mastication by the postcanine teeth. Earlier scenarios of the genus as an open habitat form, exploiting terrestrial vegetation, have been replaced by reconstructions of its environment as predominantly seasonal tropical or subtropical closed-canopy forest or woodland, albeit with patchiness and expanding areas of more open grassland in the later phase of its presence in the Siwalik record (Andrews et al. 1997; Ward 1997). While this shift could reflect broader climatic changes that, through the contraction and break up of its forested habitat, eventually resulted in the extinction of Sivapithecus, it also might be the case that the taxon was more adapted to open habitats than previously thought. Analysis of some Siwalik carpals suggests that Sivapithecus may have been a knuckle-walker (Begun and Kivell 2011). Three Sivapithecus species are recognized, differentiated primarily on dental proportions: S. sivalenis from Siwalik sites dating between 8.5 and 9.5 Mya is the type species. S. indicus, represented by GSP 15,000 and other material, is earlier (10.5–12.5 Mya) and with absolutely rather smaller teeth than S. sivalensis, but with a proportionately larger M3 compared with M2, and with a rather shorter premaxillary region. A humerus with a retroflexed and mediolaterally strongly curved shaft and a prominent deltopectoral crest is assigned to this species. S. parvada is a recently recognized, appreciably larger form, dating around 10 Mya. Its I1 is particularly wide relative to its breadth, the premolars, especially the lower ones, are expanded relative to molar size, and M3 is again much larger than M2. The mandible’s symphysis and anterior corpus region are exceptionally deep, while a humerus referred to S. parvada broadly resembles that of S. indicus but is much bigger, implying larger body size overall.

Gigantopithecus

Many workers regard the Asian genus Gigantopithecus (von Koenigswald 1952) – known from massive mandibles and individual teeth from the Late Miocene/Pleistocene of southern China, Vietnam, and the Siwaliks of India and Pakistan – as closely related to Sivapithecus. While extremely large, it is characterized by a reduced anterior dentition, with relatively small lower incisors and low-crowned but basally large canines without honing facets, strongly worn down from the tip and functionally incorporated in the premolar/molar rows. The expanded premolars are strongly molarized: P3 is bicuspid with a large talonid and is larger than P4, which is almost square with a large trigonid taller than the talonid. The upper molars are almost square, the lowers elongated; all have very thick enamel, high crowns, and low cusps. The symphysis is reinforced by a moderate superior transverse torus and a much more extensive inferior torus that may extend as far back as M1. Gigantopithecus giganteus is known from specimens found from the 1960s onward from Haritalyangar and other Siwalik sites, especially a mandible CYP359/68 (Pilbeam et al. 1977), usually considered late in the Siwalik sequence at 33 % of the mammalian fossils (Andrews et al. 1997). Kelley (2002) recognizes three species of Lufengpithecus: L. lufengensis, the type species, is the best known; L. keiyuanensis and L. hudienensis have smaller postcanine teeth and rather greater molar cingulum development than L. lufengensis, with L. keiyuanensis possibly also having thinner enamel.

Khoratpithecus The recent discovery of teeth and a part mandible from Middle and Late Miocene deposits at sites in northern Thailand, and so within the geographical range of Pleistocene Pongo, sheds further light on orangutan ancestry (Chaimanee et al. 2003, 2004). The finds have been assigned to the new genus Khoratpithecus and display numerous dental and gnathic similarities with Pongo, as well as with Lufengpithecus and, to a lesser extent, Sivapithecus. Khoratpithecus piriyai (9–7 Mya) is a large form (estimated 70–80 kg body weight) from a locality in Khorat, NE Thailand, and represented by Page 50 of 68

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a mandible body with the left canine – right I2 roots – and with the right canine and all cheek teeth crowns preserved on both sides (Chaimanee et al. 2004). The symphysis is strongly sloping, thicker in overall cross section than usual in Pongo, with a weaker superior traverse torus, shallow genial fossa, and strongly developed inferior torus that, while wide and extending to below the anterior part of the M1 crown, is less posteriorly extensive than in the orangutan. While the geniohyoid muscle facets are distinct, Khoratpithecus, like Pongo, lacks any impression for the anterior digastric muscle. The corpus is uniformly deep, with a marked depression on the lateral surface below the C/P3 region and thickening posteriorly, accentuated by a pronounced lateral eminence below M3. Judging by anterior jaw proportions and alveoli, the procumbent incisors were larger than in Lufengpithecus but smaller than Pongo and arranged in a slightly convex arc. Enamel wrinkling, while present, is less complex than in the orangutan, the P4 is shorter, and the molar cusps are more centrally located than in the modern ape. The site indicates a riverine setting with palms and dipterocarps, together with proboscids, anthracotheres, pigs, rhinos, bovids, and rare Hipparion, corresponding to the Upper Nagri/Lower Dhok Pathan Formation faunas in the Siwalik sequence. An earlier species, Khoratpithecus chiangmuanensis (13.5–10 Mya), is based on upper and lower teeth of a single individual from Ban Sa in the Chiang Muan basin (Chaimanee et al. 2003). Enamel wrinkling, markedly heterodont upper incisors, P3 crown form, lack of molar cingula and comparable degrees of relative enamel thickness, and dentine penetrance again align it with Pongo, but it differs from the latter in its smaller central incisors, in the weaker median lingual pillar of the upper and lower incisors, in the greater buccal flare of the lower molar crowns, and in its less intensive enamel wrinkling. Contextual evidence associated with K. chiangmuanensis indicates a mosaic of tropical freshwater swamps and lowland forest that contrasts with the temperate flora from Lufeng, instead resembling modern African habitats such as those in the southern Sudan around the source of the White Nile. Chaimanee et al. take this to indicate a Middle Miocene floral and faunal dispersal corridor linking South East Asia and Africa that may have been critical in hominoid dispersion. Overall, Khoratpithecus closely resembles Lufengpithecus in its dentition, but its similarities with Pongo, especially the absence of digastric fossae, point to closer affinity with the modern genus than any other fossil ape.

Conclusions Early Miocene hominoids already show considerable craniodental diversity, probably associated with dietary niche differentiation. Better known genera (Afropithecus, Proconsul) have contrasting morphologies but span a range of frugivory: Proconsul sp. and Dendropithecus were probably softfruit feeders, Afropithecus exploited hard-cased fruits. Among the less well-known genera, some (e.g., Morotopithecus, Turkanapithecus) bear cranial and/or dental similarities to Afropithecus, suggesting a hard-fruit niche, and that the most familiar cranial morphology – that of Proconsul – is not necessarily characteristic of many Early Miocene hominoids. Limnopithecus and Micropithecus appear to have been folivores on the basis of their dentition. Middle and Late Miocene forms from the region (Nacholapithecus, Equatorius, Kenyapithecus, Samburupithecus) are thick enameled and probably hard-cased fruits and seed feeders, while environmental evidence suggests more open, rather drier, and more seasonal habitats. The more southerly Otavipithecus is an exception, with thin enamel and minimal dental wear, pointing to a soft-fruit diet.

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By the Middle Miocene, hominoids are known from Europe and Western Asia. The earliest (Griphopithecus) are thick enameled, as are many later genera which are also generally more robust cranially than Proconsul, some especially so. At least one successful genus (Dryopithecus), however, has thin enamel and an only moderately strongly constructed cranium, although occlusal area, inferior symphyseal reinforcement, and, in larger individuals, mandibular cross section are expanded compared with Proconsul. Dryopithecus also contrasts with early East African fossils in its stepped nasal floor with the alveolar process overriding the palate and an incisive canal present. Overall, evidence suggests Dryopithecus primarily exploited soft fruits. The recently described, markedly prognathous Pierolapithecus is much more reminiscent of Afropithecus in its morphology and, as such, probably a sclerocarp feeder. Broadly contemporary with the younger Dryopithecus species at 9–10 Mya, Ouranopithecus and Ankarapithecus are more strongly built forms whose cranial reinforcement, muscle markings, gnathic proportions, and dental features all point to impressive masticatory power and hard-object feeding, characteristics shared with the less well-known and rather younger Graecopithecus. Of about the same age (7–8 Mya) is the (masticatory power apart) generally contrasting Oreopithecus. This genus retains many primitive cranial traits together with features making for enhanced chewing capability and a distinctive dentition adapted to specialized folivory. A similar trend to more robust morphologies is seen in South Asian hominoids, although details differ. The Late Miocene Sivapithecus (8.5–50 58

20 28

Boesch (1996) Doran (1997) Sakura (1994) Boesch (1996) White (1988) White (1988) White (1988) Badrian and Badrian (1984) Kuroda (1979) Mulavwa et al. (2008)

plant food items ranges from 55 to 328, depending on the habitat. Their diet varies seasonally, and this results in seasonal body weight fluctuations (Nishida 1990; Tutin and Fernandez 1993; Basabose 2002). The home ranges (or territories) of chimpanzee communities vary according to habitat, season, community size, and the risk of encountering neighboring communities. The mean size is 21.6 km2. In open landscapes, where food is dispersed widely, the density is very low and the home range extraordinarily large, up to 560 km2. Home ranges of neighboring communities overlap (Yamagiwa 1999; Boesch and Boesch-Achermann 2000). Within the community’s home range, each adult has his/her own core area. Most females show strong fidelity to an area once they settle there as an adult (Williams et al. 2002b, 2004). Males have larger home ranges than females (Hasegawa 1990; Chapman and Wrangham 1993; Lehmann and Boesch 2005). The mean daily travel distance of individuals is about 3 km (Doran 1997; Boesch and Boesch-Achermann 2000). In Taı¨, leopards attack chimpanzee; at other sites, lions prey on them (Tsukahara 1993; Boesch and Boesch-Achermann 2000). About 50 % of the day chimpanzees stay above ground level. They spend the night in nests that are usually built in trees up to 50-m high (Poulsen and Clark 2004),

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although terrestrial nesting has also been observed in some areas, for example, in Guinea (Koops et al. 2004). Life Histories and Dispersal Chimpanzee infants are nursed for about 3–4 years. The interbirth interval is usually 4–7 years (Nishida et al. 1990; Boesch and Boesch-Achermann 2000). Females may first conceive at about 9–11 years. The mean weight of adult male Pan troglodytes troglodytes is 53 kg, of females 43.8 kg; Pan troglodytes schweinfurthii males weigh 40.5 kg and females 32.9 kg (Groves 2001), but even within each subspecies, there is great variation both within and between populations. The maximal age of wild chimpanzees is not yet very well known. Boesch and BoeschAchermann (2000) assume that they may reach 50 years. In captivity, they have lived for almost 60 years. In most populations, females usually leave their natal groups upon maturity. At Gombe, most or all adolescent females visit other communities, and some may even conceive there, but only 50 % of them emigrate permanently, the others returning to their natal communities (Pusey et al. 1997). In Taı¨, on the other hand, almost all females transfer (Boesch and Boesch-Achermann 2000). In Mahale, the transfer process lasts from 6 months to 2 years, while the females associate and mate with the males of the two communities, and 13 % of the females transfer more than once there (Nishida et al. 1990). Male chimpanzees do not emigrate and cannot migrate between communities (Goodall 1986). Nevertheless, captive chimpanzees can be induced to accept new males into their group (Wilson and Wrangham 2003). Size and Structure of Social Units Chimpanzees live in fission-fusion groups within their communities. They have two levels of social unit: the smaller association unit is the party or subgroup – temporary and very variable – and the higher-level unit is the (stable) community or unit group (Table 12.3). Members of a community meet occasionally (fusion) and travel for longer or shorter periods in parties until they separate again (fission). On average, a party stays constant in size and composition for 24 min in Taı¨, in Gombe for 69, in Bossou for 126, and in Budongo for 14 min (Boesch and Boesch-Achermann 2000). In Gombe, the average party size is 3.5 for females only, 10.7 for mixed parties, and 4.0 for males only. Single-sex parties are significantly smaller than mixed-sex parties, and parties with more estrous females contain more males (Williams et al. 2002a). Estrous females are more gregarious than other classes, and they are especially associated with males (Goodall 1986; Pepper et al. 1999). In several populations, nursery parties – several females with their infants – have been observed. In Gombe, females spend 65 % of their time alone or with their offspring, in Kibale even 70 %, while in Taı¨ they are alone only 18 % of their time when fruits are abundant (Wrangham et al. 1996; Pusey et al. 1997; Lehmann and Boesch 2004). During fruit scarcity, their day range is reduced and the mean party size decreased (Doran 1997). In Mahale and Kibale, food availability and the number of estrous females are positively correlated with party size (Mitani et al. 2002), but in Budongo, Newton-Fisher et al. (2000) found no positive correlation, and Basabose (2004) found in Kahuzi-Biega that fruit abundance per se does not affect party size but seasonality and fruit distribution do. Party size is also determined by their function. During hunts for vertebrate prey, such as monkeys in Kibale, Watts and Mitani (2002) found a significant positive relationship between Page 14 of 34

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hunting party size and the number of kills per hunt. Success also increases with the number of males per hunting party at Gombe and Taı¨. Party size depends also on community size; in large communities parties occasionally are larger than a whole small community. Therefore, Boesch and Boesch-Achermann (2000) suggest that relative mean party sizes should be compared. According to their calculation, chimpanzees have a relative mean party size of 9–21 % of the community size. The community size may lie between 20 and 150 members. It must contain at least one adult male, but a higher number of males is usual, often more than ten. It seems that small communities retain a fission-fusion structure, but this loses much of its flexibility and the parties remain stable for much longer periods of time than in larger communities. Male-Female Relationships and Mating Strategies Relationships between male and female chimpanzees are usually not very close. Grooming between them, for example, is rather infrequent compared with male-male grooming. Constant and frequent proximity is particularly found in mother-son dyads. Chimpanzee females use a tactical strategy of mating promiscuously to confuse paternity (Stumpf et al. 2008). In Gombe, consortships have been observed in all males, and 25 % of conceptions occur during consortships (Constable et al. 2001). In Mahale, however, they are very rare and only 8.3 % of conceptions are the result of consortship (Hasegawa and HiraiwaHasegawa 1990), while in Taı¨ only one offspring was conceived during consortship; half of the males and 56 % of the females are never seen to consort. Matsumoto-Oda (2002) reported from Mahale that females copulate more often with continuously affiliative males; therefore, males interact with anestrous females to increase the chance of mating when they are in estrus. Most authors, however, found persistent coercing male aggression for eastern chimpanzees and the females most frequently solicited the most aggressive males (Muller et al. 2011). Prime males dominate all adult females and often try to monopolize them. Estrous females are more selective in their partners (Stumpf and Boesch 2006) and most frequently stay around the alpha male in Mahale and Kibale (Takahata 1990a; Muller et al. 2011). In Gombe, the alpha male is responsible for 36–45 % of all conceptions and high-ranking males for 50 %; in Taı¨, 71 % of all infants are sired by high-ranking males (Constable et al. 2001; Boesch et al. 2006). According to Williams et al. (2002b), male aggression in boundary areas forces the females to be members of their community by settling in the center of their home range. Male coercion of females is an important element, and violence toward unfamiliar females near the edges of the defended range is particularly fierce. Nevertheless, estrous females sometimes disappear for a few days and may make temporary visits to neighboring males (Boesch and Boesch-Achermann 2000). In Gombe, 13 % of copulations are with males from other communities (Goodall 1986). These extracommunity matings do not very often result in conception: in Taı¨, extragroup paternity was found only for 7 % of the offspring (one infant), and in Gombe, all tested offspring were sired by males of the same community (Constable et al. 2001; Vigilant et al. 2001). Infanticide has been observed in several chimpanzee populations, especially in Mahale (Nishida et al. 1990). In Taı¨ and Gombe, infanticide and cannibalism by females were observed (Pusey et al. 1997; Boesch and Boesch-Achermann 2000; Pusey et al. 2008). In Gombe and Mahale, more cases of infanticide were recorded within the community than between communities. These cases do not provide any evidence that infanticide is a successful male reproductive strategy in chimpanzees (Wilson and Wrangham 2003).

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Female-Female Relationships High-ranking females are the most social with other females; low-ranking females are the least. This suggests that contest competition is an important aspect of female association patterns. In Mahale and Gombe, immigrant females experience aggression from resident females (Williams et al. 2002a, b; Pusey et al. 2008). But females may also have affiliative relationships (Lehmann and Boesch 2008; Langergraber et al. 2009). In Taı¨, close female associations (friendships) can last for years and are very stable; some pairs spend up to 79 % of their time together. According to Boesch and Boesch-Achermann (2000), higher intrasexual competition and higher involvement in the social interactions of males make it profitable for females in Taı¨ to develop long-term friendships with other females and to form stable alliances. Male-Male Relationships Male chimpanzees associate more strongly with one another than do females with other females and males with females. They form coalitions in all populations studied (Boesch and BoeschAchermann 2000; Newton-Fisher 2002), and apart from coalitions, friendship between males has also been observed (Nishida and Hosaka 1996). Which individuals form affiliative relationships is not clear; genetic studies in Kibale showed that maternal kinship is not strongly associated with male-male association (Kapsalis 2004). Among the males there is a linear dominance hierarchy, and rank reversal generally results from dyadic fights (Takahata 1990b; Muller 2002). The alpha male is the most active groomer; he tends to move first and be followed by subordinates (Takahata 1990b). In Taı¨, the leader of a community announces his presence by drumming; this also gives information to other individuals about the direction and speed of group movement (Boesch and Boesch-Achermann 2000). Agonistic confrontations between males are observed regularly, and they are most aggressive between the two highest-ranking males. Coalitions in attacks are frequent; in Taı¨ it is mostly low-ranking males coalescing against dominant individuals (Boesch and Boesch-Achermann 2000). Coalitions are also formed for hunting, for the intragroup control of widely dispersed females, and to monitor territorial borders (Stanford 1998). Intergroup Interactions Most interactions of chimpanzee males with neighboring communities involve only auditory contact-pant-hoots, a long-distance call. These pant-hoots are also used to advertise their presence and numerical strength. Males almost always show fear or hostility to strange males (Wilson and Wrangham 2003). Chimpanzee males invest considerable time and energy in defending the home range of their community or locating their neighbors; the home range is controlled by groups of at least four males on a weekly basis in Taı¨ (Boesch and Boesch-Achermann 2000). During those patrols, they remain silent and actively search for signs of the neighbors. They make incursions into the home ranges of the neighbor communities, sometimes of more than 1 km, and if they encounter strange males, they attack them. In Tai, they are sometimes joined by females (Lehmann and Boesch 2005). Not only males are attacked but females too, except for tumescent females (Pusey 2001; Williams et al. 2004; Watts et al. 2006). Females with or without infants often join attacks, but they tend to avoid direct physical contact with members of the other community. Hostile intercommunity relations have been observed at all sites. Intraspecific violence is one of the leading causes of mortality for eastern chimpanzees (Wilson et al. 2004). At Gombe and Mahale, the destruction of a small community by a larger one, including systematic attacks and Page 16 of 34

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killing of individuals by males from a larger community, has been observed. Wilson and Wrangham (2003) provide a good overview of such intercommunity conflicts. So far, there is no consistent evidence from the field that the communities find more or better sexual partners and new resources as a result of the fights (Boesch and Boesch-Achermann 2000, but see Mitani et al. 2010). Extensive female transfer after a violent fight between communities was observed only in Mahale (Wilson and Wrangham 2003). In Gombe, adult parous females join other communities only when all males of their community have been killed. Williams et al. (2004) conclude that male chimpanzees cooperatively defend territories that contain food resources for themselves, their long-term female mates, and their offspring, and they try to extend the size of the community’s home range because a larger area means greater availability of food and higher female reproduction. Infanticide during intercommunity encounters can also be interpreted as the removal of future competitors. Concerning intercommunity killings by adult males, data from various study sites most strongly support the hypothesis that attackers reduce the future coalition strength of rival communities.

Bonobo (Pan paniscus) The most important sites where bonobos have been studied are listed in Table 12.1. Ecology The typical habitat for bonobos is the lowland rain forests and swamp forests of the Congo Basin. In some areas, they also live in dry forest and visit grassland. They eat up to 147 food items; 72–90 % of their diet consists of fruits (Kano and Mulavwa 1984; White 1992; Yamagiwa 2004). The amount of meat consumption is not as high as in some chimpanzee populations but seems to fall within the general range of chimpanzees. Bonobos (including females) hunt small mammals, usually solitarily (Fruth and Hohmann 2002; Surbeck and Hohmann 2008). In Wamba as well as in Lomako, the home ranges of communities overlap extensively (Idani 1990; Hohmann and Fruth 2002). Their size lies between 22 and 58 km2 in Wamba (Idani 1990). Each adult has an individual home range or core area within the community’s home range (White 1996). Bonobos may experience lower leopard predation pressure than chimpanzees because they spend more time off the ground (Boesch 1991). Outside the forest, they seem to be very careful; if they feed on fruit in the grassland, they remain quiet (Myers Thompson 2002). Life Histories and Dispersal Bonobo infants are weaned at 3–4 years of age, and the interbirth interval is about 4–7 years (Lee 1999; Yamagiwa 2004). Females conceive for the first time at about 10–14 years. Adult males have a mean weight of 39.2 kg, and females weigh 31.5 kg (Groves 1986). Females transfer to other communities as older juveniles or early adolescents (Furuichi 1989). Paternity analyses suggest that there must be a large exchange of females between communities (Gerloff et al. 1999). Males tend to stay in their natal community. Occasionally, they may transfer to other communities, but this is rare (Hohmann 2001). Size and Structure of Social Units Much like common chimpanzees, bonobos live in a fission-fusion social system. Parties usually contain mature individuals of both sexes with more females than males. The proportion of all-female parties in Lomako is high and of all-male parties low (Hohmann and Fruth 2002). If

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estrous females are present, the proportion of males increases (Hohmann and Fruth 2002). Lone individuals are rare – usually males travel alone (White 1996). Party sizes are determined by food availability: if more fruits are available and if the food patch is large, the parties grow larger. Males disperse when food becomes scarce, but females do not (White 1998; Furuichi et al. 2008). As bonobo food includes herbaceous plants that are abundant in the rain forest during all seasons, feeding competition is low. In general, bonobo parties are large in Lomako and Wamba, compared to chimpanzees. While chimpanzee parties are 9–21 % of the community size, bonobo parties consist of 21–89 % of the community. Bonobo parties last longer than those of the chimpanzees at Taı¨ and Gombe (in Wamba 86 min, in Lomako 102 min; Boesch and Boesch-Achermann 2000). Community sizes in Wamba are very variable, ranging from 33 to more than 100 members (Idani 1990). The cohesion of community members is high, and they stay together most of the time. In Lomako, several parties may congregate in the evening to nest in proximity to each other (Hohmann and Fruth 2002). Community members may be separated by kilometers for days or weeks (White 1996). Male-Female Relationships and Mating Strategies It is usually stated that in bonobo communities, either females are dominant over males or both sexes are codominant/egalitarian (Gerloff et al. 1999), but recent studies suggest that males dominate females – except for feeding situations (White and Wood 2007). Long-term bonds are found predominantly between heterosexual dyads and involve not only close kin but also unrelated individuals. Relatives associate and groom more often, however, and kinship ties are important between males and females. The highest association rates are observed between adult females and their adult sons: males receive agonistic aid from their mothers in conflicts with other males (Hohmann et al. 1999; Kapsalis 2004). Aggression by males toward females is less intense than in chimpanzees. Females may form alliances to attack males (Furuichi 1989; Hohmann and Fruth 2002). Bonobo mating is opportunistic and promiscuous and involves no or little aggression between males. The maximal swelling lasts for a large proportion of the cycle; therefore, males establish long-term bonds with females that exceed tumescence (Fruth et al. 1999). Nevertheless, sexual coercion is found in some populations; high-ranking males have a strong tendency to monopolize tumescent females and they sire more offspring (Kano 1996; Gerloff et al. 1999; White and Wood 2007; Surbeck et al. 2011). In low- and mid-ranking males, the mother’s presence increases mating success (Surbeck et al. 2011). Extracommunity copulations are not uncommon, and females are rarely prevented from mating with members of neighboring communities. The number of infants sired by nonresident males is low; more than 80 % of the infants in Lomako are fathered by resident males. No infanticide was observed so far in bonobos (Fruth et al. 1999; Gerloff et al. 1999). Female-Female Relationships Female bonobos are more affiliative and cohesive with each other than chimpanzees. Contact frequencies between females are higher than between females and males or between males. They associate and forage in larger parties for most of the year, share food, and support each other in food defense (Hohmann and Fruth 2002). These affiliative bonds are not particularly observed between related females; female associations are not based on kinship (Kapsalis 2004). Female bonobos groom less than male-male and male-female dyads but show a unique behavior called genito-genital rubbing, especially in the context of feeding: two females embrace each other Page 18 of 34

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ventro-ventrally and rub their genital swellings together with rapid sideways movements. The function of this behavior was discussed by various authors, such as Hohmann and Fruth (2000), who observed genito-genital rubbing six times as often as female-female aggression. According to their analysis it serves reconciliation and tension regulation. Male-Male Relationships Although strong bonds between males exist, especially at Wamba, they are less prominent than the bonds among females (Hohmann and Fruth 2002). Unlike chimpanzee males, bonobo males have even fewer contacts with other males than with females (White 1998). High-association rates are observed between maternally related adult brothers (Kapsalis 2004). Alliances are unusual between males (Hohmann et al. 1999). The males establish dominance relationships with each other, but aggression is less intense than in chimpanzees and conflicts are often settled in a nonagonistic way (Hohmann and Fruth 2002; Surbeck et al. 2011). Intergroup Interactions Bonobo communities do not seem to search for and contact neighboring communities. Lomako males have never been seen to make border patrols (Hohmann and Fruth 2002). In Wamba, intergroup encounters vary from group fights to peaceful intermingling. In general, encounters are peaceful and communities may spend hours together. Females take the initiative in the temporary fusion of communities. During these community meetings, males keep a certain distance from the males of the other group. The most prominent form of intergroup interaction between males and females is copulation, and relations between resident and unknown females are characterized by friendly contacts (Idani 1990; Kano 1996; Gerloff et al. 1999). There are frequently aggressive interactions between males when they approach, but direct body contact and cooperative attacks are rare; the aggressive interactions are never as fierce as those reported for chimpanzees (Idani 1990; Hohmann and Fruth 2002). Agonistic aid during conflicts between members of different communities has never been reported. Severe aggression does occur, however, when mixed-sex parties encounter unknown males; in such a case, the strangers are charged by the males and also by the females (Hohmann et al. 1999). No fatal aggression was observed between bonobo communities at Wamba (Kano 1996).

Discussion: Genus Pan Usually the chimpanzee social system has been regarded as male-bonded, with strong kinship ties between the males of a community but no relationships between the females. Experience from various field sites does not always support this idea and indicates that it is much more complicated and variable. In Taı¨, males within a community are on average not significantly more related than females, and the group members have more relatives within their home community than outside (Vigilant et al. 2001). Association patterns do not support the view of strong bonds between males in general (Pepper et al. 1999). Taı¨ chimpanzees may be bisexually bonded, while other populations are male-bonded, and more cooperation is found in Taı¨ than in eastern chimpanzees. The reasons are presumably differences in habitat. Boesch and Boesch-Achermann (2000) assume that the forest environment allows or forces bonobos and chimpanzees to build larger and more cohesive parties. Doran et al. (2002b) hypothesize that permanent female association with males is a female counterstrategy to infanticide risk and that more infanticide occurs in habitats with considerable annual variance in fruit production. Bonobos live in a still more stable environment than Taı¨ chimpanzees – this may lead to even more stable party sizes (Doran 1997). Bonobo parties seem to be large compared to Page 19 of 34

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chimpanzees (Table 12.3), but the within-species variation is larger than the interspecies variation (Hohmann and Fruth 2002; Furuichi 2009). Bonobo communities seem to be composed of unrelated females who are highly affiliative with each other and related males who are not highly affiliative with each other; females directly control competition with homosexual behavior (Boesch and Boesch-Achermann 2000). Aggression between males and between the sexes is less intense than in chimpanzees, and conflicts are often settled in a nonagonistic way. Bonobos in general have more relaxed relationships than chimpanzees that do not depend on kinship, as paternity studies show that there is no matrilineal organization (Gerloff et al. 1999). The typical chimpanzee/bonobo social structure is a multimale group with a fission-fusion structure. Similarities are obvious with respect to party size and association patterns. Female bonding in bonobos does not exceed that of some chimpanzee populations; differences between the two species are the proportion of female party members and the frequency of mixed parties (Hohmann and Fruth 2002). Chimpanzees as well as bonobos have the potential for great social variability, with considerable capacity for cooperation, reciprocal interactions, and coalitional behavior (Boesch and Boesch-Achermann 2000). Despite the common basis, the two species show some differences in social behavior. Wrangham et al. (1996) think that this can partly be explained by the differences in feeding competition: chimpanzees and gorillas live sympatrically in many areas while bonobos do not have a great ape competitor.

Sympatric Ape Populations Sympatric apes share a great part of their diet – in Asia as well as in Africa (Morgan and Sanz 2006; Vogel et al. 2009; Yamagiwa et al. 2012). This is especially visible in fruits. Sugardjito et al. (1987) observed some competition between orangutans and siamangs in Gunung Leuser, and one benefit of grouping for Sumatran orangutans may be that siamangs cannot drive the youngsters away from fruiting trees. More obvious, however, is the interspecific competition between chimpanzees and gorillas in Africa. The dietary overlap between gorillas and chimpanzees ranges from about 50 % at Kahuzi-Biega to 60–80 % at Lope´ and Ndoki. In Kahuzi-Biega, all fruit species eaten by gorillas are also eaten by chimpanzees. Overt interspecific competition between chimpanzees and gorillas has not been observed at any site; instead, competition avoidance is commonly seen (Kuroda et al. 1996; Morgan and Sanz 2006; Head et al. 2011). Interspecies relationships are more peaceful than intergroup relationships within the two species (Yamagiwa et al. 2003b). In Gabon, Okayasu (2004) observed close interactions between gorillas and chimpanzees; occasionally the groups would mix and play and even sleep at the same site. During fruit scarcity, gorillas increase the proportion of herbaceous vegetation in their diet, while chimpanzees as obligatory frugivores continue to search for fruit. The two species obviously find different niches (Yamagiwa et al. 2003b, 2012), and some habitats are used almost exclusively by one species (Tutin and Fernandez 1993; Malenky et al. 1994; Kuroda et al. 1996; Rogers et al. 2004). Kuroda et al. (1996) suggest that the low population densities of gorillas and chimpanzees in Lope´ and Kahuzi-Biega might partly be due to competition. Possibly interspecific competition over food affects foraging strategies and may have caused divergence in grouping patterns. The larger party sizes of bonobos are possible because of the high density of terrestrial herbaceous vegetation; Page 20 of 34

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as gorillas mainly eat these plants, sympatric chimpanzees may be forced to take a different foraging strategy and to form smaller parties (Wrangham et al. 1996; Yamagiwa and Takenoshita 2004). The effects of competition have not been analyzed yet, but they are difficult to study – also because additional competitors like elephants have to be considered (Rogers et al. 2004).

Conclusions and the Genus Homo Although some great ape populations have been studied for decades, their social systems are not yet completely understood. The Asian apes seem to be less social than the African apes; this may be due to food types and distributions in Southeast Asian forest, which may differ strongly from African forests. All great apes lead “individual-centered lives,” but they need interaction with familiar conspecifics. Despite their tendency to congregate, their social structure is characterized by weak ties, compared to female philopatric primates. Female transfer is common to all species. They have a tendency toward fission-fusion grouping; females lack sharply defined dominance relations, and intrasexual bonds among non-kin can be relatively strong. Van Noordwijk et al. (2012) hypothesize that this ability to form and maintain bonds has freed females from the necessity to be strictly philopatric. It is difficult to assign a social system to each ape species (or to the family Hominidae in general) because there is remarkable intraspecific variability in social organization and structure. Especially frugivory requires a mobile and flexible population. Compared to the great apes, humans show an even greater variability in social structure – nevertheless, there are certain trends across all human societies (Rodseth et al. 1991): males maintain consanguineal kin ties; females maintain consanguineal kin ties; males cooperate in conflicts against other males; and females also cooperate but rarely in physical conflicts with other females. According to Knauft (1991), simple human societies are decentralized, and there tends to be active and assiduous devaluation of adult male status differentiation. Among complex huntergatherers and with the advent of sedentism and horticulture/agriculture, male status differentiation increased. There seems to be a similarity between great apes and middle-range human societies in terms of competitive male dominance hierarchies. Such dominance relations may not be particularly adaptive in environments of low resource density and predictability; this may have led to the simple egalitarian hunter-gatherer societies that nowadays live in extreme environments. Most human societies are characterized by female-biased dispersal and male philopatry. Longterm pair bonds between males and females are common, although their form, strength, and duration vary between societies. Moreover, these bonds are not identical with mating and grouping patterns (Pusey 2001). And according to the cooperative breeding model, these bonds allowed the increase of brain size during the development of Homo (Hrdy 2005; van Schaik and Burkart 2010; Isler and van Schaik 2012). There has been much speculation on the “natural” human mating system. Although fossils of man’s early ancestors show extreme sexual dimorphism, modern human males are only about 15 % larger than females; the relative size of testes in humans is much smaller than in chimpanzees and comparable to “monogamous” or one-male group species. Polygamy with only some males producing many offspring thus cannot be the common mating system in humans, but social monogamy is not common either (Low 2003). According to Plavcan (2012) size dimorphism is not a robust indicator for breeding systems.

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The social system of humans certainly has several levels, like the social system of Pan (Layton et al. 2012). Dunbar (1993) developed the hypothesis that there is a species-specific upper limit to group size that is set by cognitive constraints. This would mean that human groups can be much larger than those of the great apes. According to Dunbar, group size depends on the maximum number of individuals with whom an individual can maintain personal contact. He discerns (in modern hunter-gatherer societies) the group levels overnight camp (30–50 members), band/ village (100–200 members), and tribe (1,000–2,000 members). Dunbar’s overnight camp certainly is not the smallest human grouping above the individual. Rodseth et al. (1991) and Pusey (2001) state that the majority of human societies consist of conjugal families united in stable communities, but also relatively autonomous families. Apart from these units, associations of men usually play an important role too (Rodseth 2012). But what is the central, stable component of the human social system? Even ape specialists have contradictory opinions. De Waal (2001) thinks that the nuclear family is the basic social grouping of humans and that this unit is unique to the species Homo sapiens, although Low (2003) states that it is rather unusual in human societies. Perhaps the nuclear family is an especially successful social structure in modern industrialized societies. Ghiglieri (1989) calls the social structure of humans a multimale kin group, a stable, semiclosed fission-fusion community.

References Badrian A, Badrian N (1984) Social organization of Pan paniscus in the Lomako Forest, Zaire. In: Susman RL (ed) The pygmy chimpanzee: evolutionary biology and behavior. Plenum Press, New York, pp 325–346 Basabose AK (2002) Diet composition of chimpanzees inhabiting the Montane Forest of Kahuzi, Democratic Republic of Congo. Am J Primatol 58:1–21 Basabose AK (2004) Fruit availability and chimpanzee party size at Kahuzi Montane Forest, Democratic Republic of Congo. Primates 45:211–219 Bermejo M (1999) Status and conservation of primates in Odzala National Park, Republic of the Congo. Oryx 33:323–331 Bermejo M (2004) Home-range use and intergroup encounters in western gorillas (Gorilla g. gorilla) at Lossi Forest, North Congo. Am J Primatol 64:223–232 Boesch C (1991) The effects of leopard predation on grouping patterns in forest chimpanzees. Behaviour 117:220–242 Boesch C (1996) Social grouping in Taı¨ chimpanzees. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 101–113 Boesch C, Boesch-Achermann H (2000) The chimpanzees of the Taı¨ Forest. Oxford University Press, New York Boesch C, Kohou G, Ne´ne´ H, Vigilant L (2006) Male competition and paternity in wild chimpanzees of the Taı¨ Forest. Am J Phys Anthropol 130:103–115 Bradley BJ, Robbins MM, Williamson EA, Steklis HD, Gerald Steklis N, Eckhardt N, Boesch C, Vigilant L (2005) Mountain gorilla tug-of-war: silverbacks have limited control over reproduction in multimale groups. Proc Natl Acad Sci USA 102:9418–9423 Bradley BJ, Doran-Sheehy DM, Vigilant L (2007) Potential for female kin associations in wild western gorillas despite female dispersal. Proc Biol Sci/The Royal Soc 274:2179–2185

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Galdikas BMF (1984) Adult female sociality among wild orangutans at Tanjung Puting Reserve. In: Small MF (ed) Female primates. Alan R. Liss, New York, pp 217–235 Galdikas BMF (1988) Orangutan diet, range, and activity at Tanjung Puting, Central Borneo. Int J Primatol 9:1–35 Galdikas BMF (1995) Social and reproductive behavior of wild adolescent female orangutans. In: Nadler RD, Galdikas BMF, Sheeran LK, Rosen N (eds) The neglected ape. Plenum Press, New York, pp 163–182 Gatti S, Levrero F, Menard N, Gautier-Hion A (2004) Population and group structure of western lowland gorillas (Gorilla gorilla gorilla) at Lokoue, Republic of Congo. Am J Primatol 63:111–123 Gerloff U, Hartung B, Fruth B, Hohmann G, Tautz D (1999) Intracommunity relationships, dispersal pattern and paternity success in a wild living community of bonobos (Pan paniscus) determined from DNA analysis of faecal samples. Proc R Soc Lond B 266(1424):1189–1195 Ghiglieri MP (1989) Hominoid sociobiology and hominid social evolution. In: Heltne PG, Marquardt LA (eds) Understanding chimpanzees. Harvard University Press, Cambridge, pp 370–379 Goldsmith ML (2003) Comparative behavioral ecology of a lowland and highland gorilla population: where do bwindi gorillas fit? In: Taylor AB, Goldsmith ML (eds) Gorilla biology. Cambridge University Press, New York, pp 358–384 Goodall J (1986) The chimpanzees of Gombe. Belknap Press, Cambridge/London Gray M, Fawcett K, Basabose A, Cranfield M, Vigilant L, Roy J, Uwingeli P, Mburanumwe I, Kagoda E, Robbins MM (2010) Virunga Massif Mountain Gorilla census – 2010 summary report. ICCN, UWA, RDB, unpublished Groves C (2001) Primate taxonomy. Smithsonian Institution Press, Washington, DC Groves C, Meder A (2001) A model of gorilla life history. Australas Primatol 15(1):2–15 Groves CP (1986) Systematics of the great apes. In: Swindler DR, Erwin J (eds) Comparative primate biology, vol 1. Alan R. Liss, New York, pp 187–217 Harcourt AH (1981) Can Uganda’s gorillas survive? A survey of the bwindi forest reserve. Biol Conserv 19:269–282 Harrison ME, Chivers DJ (2007) The orang-utan mating system and the unflanged male: a product of increased food stress during the late Miocene and Pliocene? J Hum Evol 52:275–293 Hasegawa T (1990) Sex differences in ranging patterns. In: Nishida T (ed) The chimpanzees of the Mahale Mountains. University of Tokyo Press, Tokyo, pp 99–114 Hasegawa T, Hiraiwa-Hasegawa M (1990) Sperm competition and mating behavior. In: Nishida T (ed) The chimpanzees of the Mahale Mountains. University of Tokyo Press, Tokyo, pp 115–132 Head J, Boesch C, Makaga L, Robbins MM (2011) Sympatric chimpanzees (Pan troglodytes troglodytes) and gorillas (Gorilla gorilla gorilla) in Loango National Park, Gabon: dietary composition, seasonality, and intersite comparisons. Int J Primatol 32:755–775 Hohmann G (2001) Association and social interactions between strangers and residents in bonobos (Pan paniscus). Primates 42:91–99 Hohmann G, Fruth B (2000) Use and function of genital contacts among female bonobos. Anim Behav 60:107–120 Hohmann G, Fruth B (2002) Dynamics in social organization of bonobos (Pan paniscus). In: Boesch C, Hohmann G, Marchant LF (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, New York, pp 138–150

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Hohmann G, Gerloff U, Tautz D, Fruth B (1999) Social bonds and genetic ties: kinship, association and affiliation in a community of bonobos (Pan paniscus). Behaviour 136:1219–1235 Hrdy SB (2005) Evolutionary context of human development: the cooperative breeding model. In: Carter CS, Ahnert L, Grossmann KE, Hrdy SB, Lamb ME, Porges SW, Sachser N (eds) Attachment and bonding: a new synthesis. MIT Press, Cambridge, MA, pp 9–32 Idani G (1990) Relations between unit-groups of bonobos at Wamba, Zaire: encounters and temporary fusions. Afr Stud Monogr 11(3):153–186 Isler K, van Schaik CP (2012) How Our ancestors broke through the gray ceiling. Comparative evidence for cooperative breeding in early Homo. Curr Anthropol 53(Suppl 6):S453–S465 Itoh N, Nishida T (2007) Chimpanzee grouping patterns and food availability in Mahale Mountains National Park, Tanzania. Primates 48:87–96 IUCN (2012) The IUCN red list of threatened species. http://www.iucnredlist.org/ Jones C, Sabater Pı´ J (1971) Comparative ecology of Gorilla gorilla (Savage and Wyman) and Pan troglodytes (Blumenbach) in Rı´o Muni, West Africa. Karger, Basel Kalpers J, Williamson EA, Robbins MM, McNeilage A, Nzamurambaho A, Lola N, Mugiri G (2003) Gorillas in the crossfire: population dynamics of the Virunga mountain gorillas over the past three decades. Oryx 37:326–337 Kano T (1996) Male rank order and copulation rate in a unit-group of bonobos at Wamba, Zaire. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 135–145 Kano T, Mulavwa M (1984) Feeding ecology of the pygmy chimpanzees (Pan paniscus) of Wamba. In: Susman RL (ed) The pygmy chimpanzee. Plenum Press, New York, pp 233–274 Kappeler PM, van Schaik CP (2002) Evolution of primate social systems. Int J Primatol 23(4):707–740 Kapsalis E (2004) Matrilineal kinship and primate behavior. In: Chapais B, Berman CM (eds) Kinship and behavior in primates. Oxford University Press, Oxford, pp 153–176 Knauft BM (1991) Violence and sociality in human evolution. Curr Anthropol 32:391–428 Knott C (1999) Orangutan behavior and ecology. In: Dolhinow P, Fuentes A (eds) The nonhuman primates. Mayfield Publishing, Mountain View, pp 50–57 Knott CD (2009) Orangutans: sexual coercion without sexual violence. In: Muller MN, Wrangham RW (eds) Sexual coercion in primates: an evolutionary perspective on male aggression against females. Harvard University Press, Cambridge, MA, pp 81–111 Knott C, Beaudrot L, Snaith T, White S, Tschauner H, Planansky G (2008) Female–female competition in Bornean orangutans. Int J Primatol 29:975–997 Koops K, Humle T, Matsuzawa T, Sterck EHM (2004) Terrestrial nesting in the chimpanzees of the Nimba Mountains, Guinea, West Africa: environmental or social? Folia Primatol 75(Suppl 1):387 Kummer H (1971) Primate societies. Aldine Atherton, Chicago Kuroda S (1979) Grouping of the pygmy chimpanzee. Primates 20:161–183 Kuroda S, Nishihara T, Suzuki S, Oko RA (1996) Sympatric chimpanzees and gorillas in the Ndoki Forest, Congo. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 71–81 Langergraber K, Mitani J, Vigilant L (2009) Kinship and social bonds in female chimpanzees (Pan troglodytes). Am J Primatol 71:840–851 Layton R, O’Hara S, Bilsborough A (2012) Antiquity and social functions of multilevel social organization among human hunter-gatherers. Int J Primatol 33:1215–1245

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Lee PC (1999) Comparative ecology of postnatal growth and weaning among haplorhine primates. In: Lee PC (ed) Comparative primate socioecology. Cambridge University Press, Cambridge, pp 111–139 Lehmann J, Boesch C (2004) To fission or to fusion: effects of community size on wild chimpanzees (Pan troglodytes verus) social organisation. Behav Ecol Sociobiol 56:207–216 Lehmann J, Boesch C (2005) Bisexually bonded ranging in chimpanzees (Pan troglodytes verus). Behav Ecol Sociobiol 57:525–535 Lehmann J, Boesch C (2008) Sexual differences in chimpanzee sociality. Int J Primatol 29:65–81 Lehmann J, Korstjens AH, Dunbar RIM (2007) Fission-fusion social systems as a strategy for coping with ecological constraints: a primate case. Evol Ecol 21:613–634 Leighton M, Seal US, Soemarna K, Wijaya M, Adijsasmito, Mitra Setia T, Perkins L, TraylorHolzer K, Tilson R (1995) Orangutan life history and VORTEX analysis. In: Nadler RD, Galdikas BMF, Sheeran LK, Rosen N (eds) The neglected ape. Plenum Press, New York, pp 97–107 Levre´ro F, Gatti S, Me´nard N, Petit E, Caillaud D, Gautier-Hion A (2006) Living in nonbreeding groups: an alternative strategy for maturing males. Am J Primatol 68:275–291 Low BS (2003) Ecological and social complexities in human monogamy. In: Reichard UH, Boesch C (eds) Monogamy. Cambridge University Press, Cambridge, pp 161–176 Magliocca F, Querouil S, Gautier-Hion A (1999) Population structure and group composition of western lowland gorillas in north-western Republic of Congo. Am J Primatol 48:1–14 Magliocca F, Gautier-Hion A (2004) Inter-Group Encounters in western lowland gorillas at a forest clearing. Folia Primatol 75:379–382 Malenky RK, Kuroda S, Vineberg EO, Wrangham RW (1994) The significance of terrestrial herbaceous foods for bonobos, chimpanzees, and gorillas. In: Wrangham RW, McGrew WC, de Waal FBM (eds) Chimpanzee cultures. Harvard University Press, Cambridge, MA, pp 59–76 Markham R, Groves CP (1990) Weights of wild orang utans. Am J Phys Anthropol 81:1–3 Maryanski AR (1987) African ape social structure: is there strength in weak ties? Social Networks 9(3):191–215 Matsumoto-Oda A (2002) Social relationships between cycling females and adult males in Mahale chimpanzees. In: Boesch C, Hohmann G, Marchant LF (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, New York, pp 168–180 McNeilage A (2001) Diet and habitat use of two mountain gorilla groups in contrasting habitats in the Virungas. In: Robbins MM, Sicotte P, Stewart KJ (eds) Mountain gorillas. Cambridge University Press, Cambridge, pp 265–292 McNeilage A, Plumptre AJ, Brock-Doyle A, Vedder A (2001) Bwindi Impenetrable National Park, Uganda: Gorilla census 1997. Oryx 35:39–47 € Meder A (1993) Gorillas. Okologie und Verhalten. Springer, Heidelberg Mitani M, Yamagiwa J, Oko RA, Moutsambote JM, Yumoto T, Maruhashi T (1993) Approaches in density estimates and reconstruction of social groups in a Western lowland gorilla population in the Ndoki Forest, Northern Congo. Tropics 2:219–229 Mitani JC, Watts DP, Lwanda JS (2002) Ecological and social correlates of chimpanzee party size and composition. In: Boesch C, Hohmann G, Marchant LF (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, New York, pp 102–111 Mitani JC, Watts DP, Amsler SJ (2010) Lethal intergroup aggression leads to territorial expansion in wild chimpanzees. Curr Biol 20:R507–R508 Mitra Setia T, Delgado RA, Utami Atmoko SS, Singleton I, van Schaik CP (2009) Social organization and male-female relationships. In: Wich SA, Utami Atmoko SS, Mitra Setia T, van Schaik Page 26 of 34

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CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. New York, pp 245–253. Morgan D, Sanz C (2006) Chimpanzee feeding ecology and comparisons with sympatric gorillas in the Goualougo Triangle, Republic of Congo. In: Hohmann G, Robbins MM, Boesch C (eds) Feeding ecology in apes and other primates. Cambridge University Press, Cambridge, pp 97–122 Morrogh-Bernard HC, Morf N, Chivers DJ, Kr€ utzen M (2011) Dispersal patterns of orang-utans (Pongo spp.) in a Bornean peat-swamp forest. Int J Primatol 32:362–376 Mulavwa M, Furuichi T, Yangozene K, Yamba-Yamba M, Motema-Salo B, Idani G, Ihobe H, Hashimoto C, Tashiro Y, Mwanza N (2008) Seasonal changes in fruit production and party size of bonobos at Wamba. In: Furuichi T, Thompson J (eds) Bonobos: behavior, ecology, and conservation. Springer, New York, pp 121–134 Muller MN (2002) Agonistic relations among Kanyawara chimpanzees. In: Boesch C, Hohmann G, Marchant LF (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, New York, pp 112–124 Muller MN, Emery Thompson M, Kahlenberg SM, Wrangham RW (2011) Sexual coercion by male chimpanzees shows that female choice may be more apparent than real. Behav Ecol Sociobiol 65:921–933 Murnyak DF (1981) Censusing the gorillas in Kahuzi-Biega National Park. Biol Conserv 21:163–176 Myers Thompson JA (2002) Bonobos in the Lukuru Wildlife Research Project. In: Boesch C, Hohmann G, Marchant LF (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, New York, pp 61–70 Newton-Fisher NE (2002) Relationships of male chimpanzees in the Budongo Forest, Uganda. In: Boesch C, Hohmann G, Marchant LF (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, New York, pp 125–137 Newton-Fisher NE, Reynolds V, Plumptre AJ (2000) Food supply and chimpanzee (Pan troglodytes schweinfurthii) party size in the Budongo Forest Reserve, Uganda. Int J Primatol 21:613–628 Nishida T (1990) A quarter century of research in the Mahale Mountains: an overview. In: Nishida T (ed) The chimpanzees of the Mahale Mountains. University of Tokyo Press, Tokyo, pp 3–35 Nishida T, Hosaka K (1996) Coalition strategies among adult male chimpanzees of the Mahale Mountains, Tanzania. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 114–134 Nishida T, Takasaki H, Takahata Y (1990) Demography and reproductive profiles. In: Nishida T (ed) The chimpanzees of the Mahale Mountains. University of Tokyo Press, Tokyo, pp 63–97 Okayasu N (2004) Intimate interactions of wild gorillas and chimpanzees observed in Moukalaba National Park, Gabon: preliminary report. Folia Primatol 75(Suppl 1):179 Parnell RJ (2002) Group size and structure in western lowland gorillas at Mbeli Bai, Republic of Congo. Am J Primatol 56:193–206 Pepper JW, Mitani JC, Watts DP (1999) General gregariousness and specific social preferences among wild chimpanzees. Int J Primatol 20:613–628 Plavcan JM (2012) Implications of male and female contributions to sexual size dimorphism for inferring behavior in the hominin fossil record. Int J Primatol 33:1364–1381 Poole TB (1987) Social behavior of a group of orangutans (Pongo pygmaeus) on an artificial island in Singapore Zoological Gardens. Zoo Biol 6:315–330 Poulsen JR, Clark CJ (2004) Densities, distributions, and seasonal movements of gorillas and chimpanzees in swamp forest in northern Congo. Int J Primatol 25(2):285–306 Page 27 of 34

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Pusey A, Williams J, Goodall J (1997) The influence of dominance rank on the reproductive success of female chimpanzees. Science 277:828–831 Pusey AE (2001) Of genes and apes: chimpanzee social organization and reproduction. In: de Waal FBM (ed) Tree of origin. Harvard University Press, Cambridge, MA, pp 9–37 Pusey A, Murray C, Wallauer W, Wilson M, Wroblewski E, Goodall J (2008) Severe aggression among female chimpanzees at Gombe National Park, Tanzania. Int J Primatol 29:949–973 Reichard UH, Barelli C (2008) Life history and reproductive strategies of Khao Yai Hylobates lar: implications for social evolution in apes. Int J Primatol 29:823–844 Remis MJ (1997) Ranging and grouping patterns of a western lowland gorilla group at Bai Hokou, Central African Republic. Am J Primatol 43:111–133 Rijksen HD, Meijaard E (1999) Our vanishing relative: the status of wild orang-utans at the close of the twentieth century. Kluwer Academic, Dordrecht/Boston/London Robbins MM (1995) A demographic analysis of male life history and social structure of mountain gorillas. Behaviour 132:21–47 Robbins MM (1999) Male mating patterns in wild multimale mountain gorilla groups. Anim Behav 57:1013–1020 Robbins MM (2001) Variation in the social system of mountain gorillas: the male perspective. In: Robbins MM, Sicotte P, Stewart KJ (eds) Mountain gorillas. Cambridge University Press, Cambridge, pp 29–58 Robbins MM (2003) Behavioral aspects of sexual selection in mountain gorillas. In: Jones CB (ed) Sexual selection and reproductive competition in primates: new perspectives and directions. American Society of Primatologists, Norman, pp 477–501 Robbins MM, Bermejo M, Cipolletta C, Magliocca F, Parnell RJ, Stokes E (2004) Social structure and life-history patterns in western gorillas (Gorilla gorilla gorilla). Am J Primatol 64:145–159 Robbins MM, Nkurunungi JB, McNeilage A (2006) Variability of the feeding ecology of eastern gorillas. In: Hohmann G, Robbins MM, Boesch C (eds) Feeding ecology in apes and other primates. Cambridge University Press, Cambridge, pp 25–47 Robbins MM, Robbins AM, Gerald-Steklis N, Steklis HD (2007) Socioecological influences on the reproductive success of female mountain gorillas (Gorilla beringei beringei). Behav Ecol Sociobiol 61:919–931 Robbins MM, Roy J, Wright E, Kato R, Kabano P, Basabose A, Tibenda E, Vigilant L, Gray M (2011) Bwindi Mountain Gorilla census 2011 – summary of results Rodseth L, Wrangham RW, Harrigan AM, Smuts BB (1991) The human community as a primate society. Curr Anthropol 32:221–254 Rodseth L (2012) From bachelor threat to fraternal security: male associations and modular organization in human societies. Int J Primatol 33:1194–1214 Rogers ME, Abernethy K, Bermejo M, Cipolletta C, Doran D, McFarland K, Nishihara T, Remis M, Tutin CEG (2004) Western gorilla diet: a synthesis from six sites. Am J Primatol 64:173–192 Rowe N (1996) The pictorial guide to the living primates. Pogonias Press, East Hampton/New York Sakura O (1994) Factors affecting party size and composition of chimpanzees (Pan troglodytes verus) at Bossou, Guinea. Int J Primatol 15:167–183 Satkoski JA, van Schaik CP, Andayani N, Melnick DJ, Supriatna J (2004) Bimaturism: an evolutionary strategy of male Sumatran orangutans. Folia Primatol 75(Suppl 1):409 Schaller GB (1963) The mountain gorilla. Chicago University Press, Chicago

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Sicotte P (1994) Effect of male competition on male-female relationships in bi-male groups of mountain gorillas. Ethology 97:47–64 Sicotte P (2001) Female mate choice in mountain gorillas. In: Robbins MM, Sicotte P, Stewart KJ (eds) Mountain gorillas. Cambridge University Press, Cambridge, pp 59–87 Singleton I, van Schaik CP (2002) The social organisation of a population of Sumatran orangutans. Folia Primatol 73:1–20 Singleton I, Knott CD, Morrogh-Bernard HC, Wich SA, van Schaik CP (2009) Ranging behavior of orangutan females and social organization. In: Wich SA, Utami Atmoko SS, Mitra Setia T, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. New York, pp 205–213 Sommer V, Reichard U (2000) Rethinking monogamy: the gibbon case. In: Kappeler PM (ed) Primate males. Cambridge University Press, Cambridge, pp 159–168 Stanford CB (1998) Predation and male bonds in primate societies. Behaviour 135:513–533 Stoinski TS, Vecellio V, Ngaboyamahina T, Ndagijimana F, Rosenbaum S, Fawcett KA (2009a) Proximate factors influencing dispersal decisions in male mountain gorillas, Gorilla beringei beringei. Anim Behav 77:1155–1164 Stoinski TS, Rosenbaum S, Ngaboyamahina T, Vecellio V, Ndagijimana F, Fawcett K (2009b) Patterns of male reproductive behaviour in multi-male groups of mountain gorillas: examining theories of reproductive skew. Behaviour 146:1193–1215 Stokes EJ (2004) Within-group social relationships among females and adult males in wild western lowland gorillas (Gorilla gorilla gorilla). Am J Primatol 64:233–246 Stokes EJ, Parnell RJ, Olejniczak C (2003) Female dispersal and reproductive success in wild western lowland gorillas. Behav Ecol Sociobiol 54:329–339 Stumpf R, Boesch C (2006) The efficacy of female choice in chimpanzees of the Tai forest, Coˆte d’Ivoire. Behav Ecol Sociobiol 60:749–765 Stumpf RM, Emery Thompson M, Knott CD (2008) A comparison of female mating strategies in Pan troglodytes and Pongo spp. Int J Primatol 29:865–884 Sugardjito J, te Boekhorst IJA, van Hooff JARAM (1987) Ecological constraints on the grouping of wild orang-utans (Pongo pygmaeus) in the Gunung Leuser National Park, Sumatra, Indonesia. Int J Primatol 8:17–41 Surbeck M, Hohmann G (2008) Primate hunting by bonobos at Lui Kotale, Salonga National Park. Curr Biol 18:R905–R907 Surbeck M, Mundry R, Hohmann G (2011) Mothers matter! maternal support, dominance status and mating success in male bonobos (Pan paniscus). Proc Royal Soc B 278:590–598 Takahata Y (1990a) Adult males’ social relations with adult females. In: Nishida T (ed) The chimpanzees of the Mahale Mountains. University of Tokyo Press, Tokyo, pp 133–148 Takahata Y (1990b) Social relationships among adult males. In: Nishida T (ed) The chimpanzees of the Mahale Mountains. University of Tokyo Press, Tokyo, pp 149–170 Tsukahara T (1993) Lions eat chimpanzees: the first evidence of predation by lions on wild chimpanzees. Am J Primatol 29:1–11 Tutin CEG (1996) Ranging and social structure of lowland gorillas in the Lope´ Reserve, Gabon. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 58–70 Tutin CEG, Fernandez M (1991) Responses of wild chimpanzees and gorillas to the arrival of primatologists: behaviour observed during habituation. In: Box HO (ed) Primate responses to environmental change. Chapman & Hill, London, pp 187–197

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Tutin CEG, Fernandez M (1993) Composition of the diet of chimpanzees and comparisons with that of sympatric lowland gorillas in the Lope´ Reserve, Gabon. Am J Primatol 30:195–211 Tutin CEG, Fernandez M, Rogers ME, Williamson EA (1992) A preliminary analysis of the social structure of lowland gorillas in the Lope´ Reserve, Gabon. In: Itoigawa M, Sugiyama GP et al (eds) Topics in primatology, vol 2. University of Tokyo Press, Tokyo, pp 245–253 Utami Atmoko S, van Hooff JARAM (2004) Alternative male reproductive strategies: male bimaturism in orangutans. In: Kappeler PM, van Schaik C (eds) Sexual selection in primates. Cambridge University Press, New York, pp 196–207 Utami SS, Goossens B, Bruford MW, de Ruiter JR, van Hooff JARAM (2002) Male bimaturism and reproductive success in Sumatran orang-utans. Behav Ecol 13:643–652 Utami Atmoko SS, Mitra Setia T, Goossens B, James SS, Knott CD, Morrogh-Bernard HC, van Schaik CP, van Noordwijk MA (2009a) Orangutan mating behaviour and strategies. In: Wich SA, Utami Atmoko SS, Mitra Setia T, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, New York, pp 235–244 Utami Atmoko SS, Singleton I, van Noordwijk MA, van Schaik CP, Mitra Setia T (2009b) Malemale relationships in orangutans. In: Wich SA, Utami Atmoko SS, Mitra Setia T, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, New York, pp 225–233 van Hooff JARAM (1995) The orangutan: a social outsider. A socio-ecological test case. In: Nadler RD, Galdikas BMF, Sheeran LK, Rosen N (eds) The neglected ape. Plenum Press, New York, pp 153–162 van Noordwijk MA, Arora N, Willems EP, Dunkel LP, Amda RN, Mardianah N, Ackermann C, Kr€utzen M, van Schaik CP (2012) Female philopatry and its social benefits among Bornean orangutans. Behav Ecol Sociobiol 66:823–834 van Schaik CP (1999) The socioecology of fission-fusion sociality in orangutans. Primates 40:69–86 van Schaik CP (2000) Social counterstrategies against infanticide by males in primates and other mammals. In: Kappeler PM (ed) Primate males. Cambridge University Press, Cambridge, pp 34–54 van Schaik CP, Burkart JM (2010) Mind the gap: cooperative breeding and the evolution of our unique features. In: Kappeler PM, Silk JB (eds) Mind the gap: tracing the origins of human universals. Springer, Berlin, pp 477–496 van Schaik CP, van Hooff JARAM (1996) Toward an understanding of the orang-utan’s social system. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 3–15 Vigilant L, Hofreiter M, Siedel H, Boesch C (2001) Paternity and relatedness in wild chimpanzee communities. Proc Natl Acad Sci 98:12890–12895 Vogel ER, Haag L, Mitra-Setia T, van Schaik CP, Dominy NJ (2009) Foraging and ranging behavior during a fallback episode: Hylobates albibarbis and Pongo pygmaeus wurmbii compared. Am J Phys Anthropol 140:716–726 Watts DP (1989) Infanticide in mountain gorillas: new cases and a reconsideration of the evidence. Ethology 81:1–18 Watts DP (1991) Mountain gorilla reproduction and sexual behavior. Am J Primatol 24:211–225 Watts DP (1996) Comparative socio-ecology of gorillas. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 16–28

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Watts DP (2000) Causes and consequences of variation in male mountain gorilla life histories and group membership. In: Kappeler PM (ed) Primate males. Cambridge University Press, Cambridge, pp 169–179 Watts DP (2001) Social relationships of female mountain gorillas. In: Robbins MM, Sicotte P, Stewart KJ (eds) Mountain gorillas. Cambridge University Press, Cambridge, pp 215–240 Watts DP, Mitani JC (2002) Hunting behavior of chimpanzees at Ngogo, Kibale National Park, Uganda. Int J Primatol 23:1–28 Watts D, Muller M, Amsler S, Mbabazi G, Mitani J (2006) Lethal inter-group aggression by chimpanzees in the Kibale National Park, Uganda. Am J Primatol 68:161–180 Weber AW, Vedder A (1983) Population dynamics of the Virunga gorillas (Gorilla gorilla): 19591978. Biol Conserv 26:341–366 White FJ (1988) Party composition and dynamics in Pan paniscus. Int J Primatol 9:179–193 White FJ (1992) Activity budgets, feeding behavior, and habitat use of pygmy chimpanzees at Lomako, Zaire. Am J Primatol 26:215–223 White FJ (1996) Comparative socio-ecology of Pan paniscus. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 29–41 White FJ (1998) Seasonality and socioecology: the importance of variation in fruit abundance to bonobo sociality. Int J Primatol 19:1013–1027 White FJ, Wood KD (2007) Female feeding priority in bonobos, Pan paniscus, and the question of female dominance. Am J Primatol 69:837–850 Wich SA, Geurts ML, Mitra ST, Utami Atmoko SS (2006) Influence of fruit availability on Sumatran orangutan sociality and reproduction. In: Hohmann G, Robbins MM, Boesch C (eds) Feeding ecology in apes and other primates: ecological, physical and behavioral aspects. Cambridge Univ Press, New York, pp 337–358 Wich SA, de Vries H, Ancrenaz M, Perkins L, Shumaker RW, Suzuki A, van Schaik CP (2009) Orangutan life history variation. In: Wich SA, Suci Utami Atmoko SS, Mitra Setia T, van Schaik CP (eds) Orangutans: geographical variation in behavioral ecology and conservation. Oxford Univ Press, New York, pp 65–75 Williams JM, Liu HY, Pusey AE (2002a) Costs and benefits of grouping for female chimpanzees at Gombe. In: Boesch C, Hohmann G, Marchant LF (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, New York, pp 192–203 Williams JM, Pusey AE, Carlis JV, Farm BP, Goodall J (2002b) Female competition and male territorial behaviour influence female chimpanzees’ ranging patterns. Anim Behav 63:347–360 Williams JM, Oehlert GW, Carlis JV, Pusey AE (2004) Why do male chimpanzees defend a group range? Anim Behav 68:523–532 Wilson ML, Wrangham RW (2003) Intergroup relations in chimpanzees. Ann Rev Anthropol 32:363–392 Wilson ML, Wallauer WR, Pusey AE (2004) New cases of intergroup violence among chimpanzees in Gombe National Park, Tanzania. Int J Primatol 25:523–549 Wrangham RW (1979) On the evolution of ape social systems. Soc Sci Inform 18:335–368 Wrangham RW, Chapman CA, Clark-Arcadi AP, Isabirye-Basuta G (1996) Social ecology of Kanyawara chimpanzees: implications for understanding the costs of great ape groups. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 45–57 Yamagiwa J (1983) Diachronic changes in two eastern lowland gorilla groups (Gorilla gorilla graueri) in the Mt. Kahuzi region, Zaire. Primates 24:174–183

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Yamagiwa J (1987) Male life histories and the social structure of wild mountain gorillas. In: Kawano S et al (eds) Evolution and coadaptation in biotic communities. University of Tokyo Press, Tokyo, pp 31–51 Yamagiwa J (1999) Socioecological factors influencing population structure of gorillas and chimpanzees. Primates 40:87–104 Yamagiwa J (2004) Diet and foraging of the great apes: ecological constraints on their social organizations and implications for their divergence. In: Russon AE, Begun DR (eds) The evolution of thought: evolutionary origins of great ape intelligence. Cambridge University Press, Cambridge, pp 210–233 Yamagiwa J, Basabose AK, Kahekwa J, Bikaba D, Ando C, Matsubara M, Iwasaki N, Sprague DS (2012) Long-term research on Grauer’s gorillas in Kahuzi-Biega National Park, DRC: life history, foraging strategies, and ecological differentiation from sympatric chimpanzees. In: Kappeler PM, Watts DP (eds) Long-term field studies of primates. Springer, Heidelberg/Berlin, pp 385–411 Yamagiwa J, Kahekwa J (2001) Dispersal patterns, group structure, and reproductive parameters of eastern lowland gorillas at Kahuzi in the absence of infanticide. In: Robbins MM, Sicotte P, Stewart KJ (eds) Mountain gorillas. Cambridge University Press, New York, pp 90–122 Yamagiwa J, Kahekwa J (2004) First observations of infanticides by a silverback in Kahuzi-Biega. Gorilla J 29:6–9 Yamagiwa J, Takenoshita Y (2004) Sympatric apes: socioecological divergence and evolution of great apes. Folia Primatol 75(Suppl 1):177 Yamagiwa J, Maruhashi T, Yumoto T, Hamada Y, Mwanza T (1989) Distribution and present status of primates in the Kivu district. Grant-in-Aid for overseas scientific research report “Interspecies relationships of primates in the tropical and montane forests”, vol 1, pp 11–21 Yamagiwa J, Mwanza N, Spangenberg A, Maruhashi T, Yumoto T, Fischer A, Steinhauer-Burkart B (1993) A census of the eastern lowland gorillas, Gorilla gorilla graueri, in Kahuzi-Biega National Park with reference to mountain gorillas, G. g. beringei, in the Virunga region, Zaire. Biol Conserv 64:83–89 Yamagiwa J, Kahekwa J, Basabose AK (2003a) Intra-specific variation in social organization of gorillas: implications for their social evolution. Primates 44:359–369 Yamagiwa J, Basabose K, Kaleme K, Yumoto T (2003b) Within-group feeding competition and socioecological factors influencing social organization of gorillas in the Kahuzi-Biega National Park, Democratic Republic of Congo. In: Taylor AB, Goldsmith ML (eds) Gorilla biology. Cambridge University Press, New York, pp 328–357 Yamagiwa J, Kahekwa J, Basabose AK (2009) Infanticide and social flexibility in the genus Gorilla. Primates 50:293–303

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_40-6 # Springer-Verlag Berlin Heidelberg 2013

Index Terms: Bonobo 17 Chimpanzee 12 Diet 4, 12, 17 bonobo 17 chimpanzee 12 orangutan 4 Dispersal 5, 8, 14, 17 Dispersal bonobo 17 chimpanzee 14 gorilla 8 orangutan 5 estrus 15 Gorillas 8 Group size, gorilla 9 Home range 5, 8, 13, 17 bonobo 17 chimpanzee 13 gorilla 8 orangutan 5 Intergroup interaction 11, 16, 19 bonobo 19 chimpanzee 16 gorilla 11 Life history 5, 8, 14, 17 Life history bonobo 17 chimpanzee 14 gorilla 8 orangutan 5 Mating strategy 6, 10, 15, 18 Mating strategy bonobo 18 chimpanzee 15 gorilla 10 orangutan 6 Orangutans 4 Pan paniscus 17 See Bonobo Pan troglodytes 12 See Chimpanzee Species/subspecies DistributionStudy sites mentioned hereHabitat 4 sire 18 Social relationships 7

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_40-6 # Springer-Verlag Berlin Heidelberg 2013

Social systems 1 Sympatric ape 20

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_41-9 # Springer-Verlag Berlin Heidelberg 2013

Primate Intelligence Prof. Richard W. Byrne* Centre for Social Learning & Cognitive Evolution, School of Psychology & Neuroscience, University of St Andrews, Scotland, UK

Abstract Brain size has traditionally been employed as a measurable proxy for species intelligence. Using allometric scaling of brain size relative to body size shows the biological cost suffered from investment in brain tissue. Shifts in diet type are the engine permitting increased investment in brain tissue because higher energy diets allow a larger brain at any given body size. Relative brain size, however, confounds effects of gut size required for particular diets with effects of brain size required for enhanced cognitive function. In contrast, the absolute size of brain parts specialized for particular functions gives evidence of the computational power of those systems. Correlational analyses strongly imply that demands of social complexity, rather than difficulties associated with frugivory or embedded foods, led to evolutionary increase in simian primate brain size. Primate brain expansion has largely involved the neocortex, with correlated increases in the cerebellum; among living primates, neocortex size predicts frequency of use of tactical deception and of innovative responses. These capacities likely rely on extensive memory for social information. Only among great apes is there evidence of understanding how systems work, whether social or technical, and this ape/monkey difference may be mediated by specifically cerebellar expansion. Representational understanding may derive from the ability to parse complex behavior, allowing imitative learning of elaborate new skills.

Introduction There are three ways in which physical anthropologists might be interested in primate intelligence, corresponding to different theoretical formulations. Firstly, a very widespread view among social scientists is that human intelligence is unique and indivisible, shared with no other species (Macphail 1982, 1985). This does not mean “unique, just as each species’ intelligence is unique,” nor simply “uniquely large,” both of which are undeniable; rather, human intelligence is seen as incomparable, and anyone seeking seriously to relate animal and human intelligences is misled. Human intelligence is taken to be a consequence of developing the faculties of language and speech. Thus, on this stance, the key question for human evolution is at what point in human evolution did our makeup change in a way that permitted the development of language. The (unique) origin of intelligence equates to the (unique) origin of language. Replacing a hard question with a famously intractable one leads to no obvious avenue for further research. Moreover, while in the end it may turn out that the gulf between human intelligence and that of any other animal is an

*Email: [email protected] Page 1 of 18

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_41-9 # Springer-Verlag Berlin Heidelberg 2013

unusually large one, to assume a priori that there is no comparison makes good sense only for a creationist. This position will therefore not be considered further. At the opposite extreme, intelligence has been treated as a continuously varying quantity: traditionally called “g” in psychometric psychology, for “general intelligence,” or IQ in common parlance. On this view, the evolutionary issue is whether intelligence changed gradually or in steps, and comparative phylogenetic data of primates can be used to pin down when in human evolution such changes occurred (see Chapters “▶ Principles of Taxonomy and Classification: Current Procedures for Naming and Classifying Organisms,” “▶ Modeling the Past: The Primatological Approach,” in volume 1). Further, by exploring the ecological correlates of intelligence in living primate species, insight can be gained into the current adaptive value (usefulness) of intelligence and thereby reveal clues to its evolutionary origin. What primatology needs to bring to this enterprise is the equivalent of an intelligence test for animals: a fair way of comparing the intellects of living species. This has been the most popular and to date the most productive approach to primate intelligence, but in this chapter, I will suggest that it is only a rough approximation to the truth and may be of limited future value. Finally, lying between the two extremes of intelligence-as-language and intelligence-as-quantity, intelligence can be treated as a heterogeneous skill package: a mixed bag of devices and processes, endowments, and aptitudes, in fact all those capacities that lead us to label everyday behavior as “intelligent.” I will argue that this rather messy vision in fact offers the most promise for the future use of comparative data in understanding the evolution of our most vaunted feature, human intelligence.

Intelligence-as-Quantity Intelligence as measured within psychology is a matter of differences in ability among people. Strictly speaking, then, intelligence is an individual-level phenomenon. However, over and above the differences in problem-solving ability among humans (and presumably also in other species), individuals share a “common denominator” potential for intelligence by virtue of species membership. It is this genetically based, common denominator that is meant by talking of “differences in intelligence between species.” Species differences in intelligence are clearly liable to be much greater than the small differences within human intelligence. How can species intelligence be measured? An obvious starting point is to co-opt and adapt the tools of psychometric psychology: surely measures designed for the small variations in human intelligence will prove sensitive enough for the larger species differences. In practice, this is not as easy as it might seem. One reason is that, although most people consider they can deduce intelligence from everyday behavior, psychologists have preferred to define intelligence operationally, as “what IQ tests measure.” As a result, sadly little expertise in psychometrics is available to inform how to infer intelligence from behavior. Still, a considerable battery of tests, broadly comparable to the items of an IQ test, has been applied to animals, using the tools of the animal learning laboratory: Skinner boxes, Wisconsin General Test Apparatus, and so on. Unfortunately, the results have been disappointing, as far as measuring species intelligence goes – and perhaps this should not be a surprise. Human intelligence testing has shown the inappropriateness of grabbing a test, devised in one culture, and using it on people from another culture. The problem is that tests must be calibrated against some other achievement (for human IQ tests, usually educational success), and these measures of achievement are not culture-free; the difficulty is obviously far greater across species. Only a few animals are motivated by rewards similar to those that motivate Page 2 of 18

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_41-9 # Springer-Verlag Berlin Heidelberg 2013

us, see the world in rather human ways, and interact with the world in a similar way to humans. If researchers rely on human estimation of difficulty in some “behavioral IQ test for animals,” they are liable to equate cleverness with similarity to humans. The history of laboratory-based comparative psychology has gone through a series of cycles, with striking species differences in intelligence first claimed and then the difference later discovered to lie rather in perceptual capacity, motivation, or species-typical traits better understood as special-purpose adaptations for particular environmental features (see reviews by Warren 1973; Macphail 1985). Goldfish were once considered less intelligent than rats, because they could not learn visual discrimination tasks – until it was realized that their visual acuity was greater in a downward direction. When tasks were presented on the bottom of the tank, the difference vanished. Among primates, colobines were (and still often are) considered unintelligent compared to cercopithecines – but the latter are frugivorous, readily motivated to perform tasks in return for fruit or other concentrated food. Colobines are folivores, not adapted to compete for (or even able to digest) small items of highquality food; it is hardly a level playing field. Barn swallows show phenomenal abilities to find their way over great distances to return to the same barn after many months, using the positions of sun and stars, polarized light, and magnetic fields; but they show no other signs of great intelligence, and migratory abilities are not helpfully seen as evidence of intellectual level. Small wonder then that some biologists have doubted whether intelligence is an appropriate measure by which to compare animals at all. Animal adaptations are fascinating, they argue, but calling that intelligence adds nothing to our understanding. Often, psychologists’ definitions of intelligence stress the need to deal with environmental challenges: e.g., “the aggregate or global capacity of the individual to act purposefully, think rationally, and to deal effectively with his environment” (Wechsler 1944) or “the faculty of adapting oneself to circumstances” (Binet and Simon 1915). If intelligent for an animal species means “well adapted to the environment,” then presumably all species are “intelligent” in their own, nonhuman ways. And while many performances of animals look intelligent in the human sense, there is every reason to suppose that their development is under tight genetic guidance. Surely, however, adaptations specific to solving particular environmental problems should be distinguishable from real intelligence by its quality of flexibility, allowing individuals to find their own solutions even to novel problems. Species-typical performances are most likely adaptations (although not all will prove to be: the wearing of bodily adornment or coverings is, after all, species-typical in humans!). But the importance of species-level intelligence is its potential for allowing individual flexibility in learning and problem solving. This approach points to the use of observational data of natural behavior to deduce intelligence, just as we do every day among ourselves. However, in examining natural behavior for signs of the individual-level flexibility and creativity that can signal species intelligence, the same danger of confusing genetic adaptations with flexible intelligence occurs as with laboratory testing. An anecdote of my own error may serve as a cautionary tale. Watching border collies herd sheep, I did not doubt the dog’s greater intelligence. The sheepdog responds to the whistles of a shepherd with flawless outmaneuvering and controlling of a hundred sheep. Of course, this wonderful performance depends on the innate antipredator reactions of sheep. Bunching and running in tight-packed flocks when attacked makes it difficult for a wolf to single out a potential kill but easy for a sheepdog to maneuver a group. The dog is also equipped with innate tactics, partly as a result of its wolf ancestry and partly as a result of thousands of years of domestication; these tactics can be seen in any untrained sheepdog let out to chase some sheep. But the dog is also able to learn the complex system of whistle signals and is then able to deploy its tactics to order; the sheep, in contrast, are unable to overcome their innate restrictions. My faith in this simple picture was shattered by spending some time with Gujarati Page 3 of 18

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_41-9 # Springer-Verlag Berlin Heidelberg 2013

shepherds on the Little Rann of Kutch in India. Like British shepherds, they whistle their commands; it seemed a familiar scene. Eventually, I noticed the sheepdogs: asleep. The sheep in Gujarat learn to understand the shepherds’ commands and follow them, treating the shepherd as herd leader. The dogs’ role is not one of herder but only a source of protection from wolves. Dogs may seem especially intelligent to people because they happen to use facial musculature for visual communication, giving rise to expressions that resemble our own and have similar meanings, and because their forward-facing eyes and long nose make their direction of attention obvious. We can “see” what they are thinking, and recent work shows that domestication has equipped dogs with particular traits that fit into this two-way cooperation (Miklosi et al. 2004). Sheep are foreign to us, because they rely more on olfaction and their facial expressions are relatively cryptic to us, but it is premature to assume them unintelligent. A proper comparison of intelligence, shown by each of the species relevant to reconstructing human cognitive evolution, is therefore a tall order. Attempts to use general-purpose laboratory tests have often foundered on extraneous differences in natural aptitudes, perceptual capacities, and motivation; in any case, relatively few species are available for detailed examination in captive settings, and comparative phylogenetic analysis depends on using a broad range of species. Yet to accurately attribute differences in natural behavior to intelligence, rather than other evolved aspects of the species biology, requires in-depth study of each species under a range of conditions and so is almost as restricted in what data are available. In consequence, most progress in evaluating animal intelligence as a quantity has been made by using an indirect indication of intelligence, brain size, which can be accurately measured anatomically.

Brain Size as a Measure of Intelligence The clearest evidence that brain enlargement confers adaptive advantage comes from examining the costs of a large brain: species can tolerate retention of neutral traits, but for a costly organ to evolve necessitates compensating advantages. Brain tissue is metabolically expensive (Aiello and Wheeler 1995). In adulthood, the human brain consumes about 20 % of the basal metabolic rate, and during childhood this percentage rises to 50 %. Moreover, this demand for energy is remorseless: unlike other organs, the energy supply to the brain has to be constant, and irreparable damage results from only a few minutes of interruption. Having a large brain has incurred other disadvantages for us, as well as this energetic drain. At birth, the human child’s head is a tight fit in the birth canal compared with the easy passage of other great ape babies (Leutenegger 1982). Birth is consequently a prolonged, often painful, and sometimes dangerous process for mothers; among other great apes, birth takes only a few minutes. Finally, human brains grow for an unusual amount of time, considering their already-large size at birth (Harvey and Clutton-Brock 1985). During this phase of postnatal brain growth, human babies are relatively immature and helpless, so they require years of time-consuming care from the mother or family. Among primates, the only plausible explanation for brain enlargement in the face of such clear costs is an intellectual benefit. To measure species intelligence, then, it should be possible to use brain enlargement. Difficulties arise, however, in deciding the baseline for measuring enlargement. Larger animals, in general, have larger brains. As the absolute size of living things changes, the relative proportions of their parts are generally found to change. In this case, absolutely larger animals have relatively smaller brains than expected from linearly scaling-up smaller ones (Jerison 1963, 1973). These regular trends have led to the use of allometry to calibrate brain enlargement, against a baseline of the size expected from body weight. In allometric scaling, for a given group of Page 4 of 18

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_41-9 # Springer-Verlag Berlin Heidelberg 2013

animals, a double logarithmic plot of the parameter at issue is made against body size; provided some sort of power relationship is involved, this forces the species points onto a straight line. For brain size, plotting against body size on logarithmic coordinates gives a reasonably straight line for primates, as for other groups of animals (Passingham 1981). Whether a species lies above the line (has a relatively larger brain than expected), on the line (has average brain size), or below the line (has a relatively small brain) is taken to index its intelligence. For instance, “encephalization quotient” refers to the actual size of a mammal’s brain divided by that expected for a typical mammal of its body size (Jerison 1973; see also Clutton-Brock and Harvey 1980). This technique has been used most often in evolutionary analyses of animal intelligence. However, comparing species in intellectual ability by using their relative brain sizes calibrated with allometric scaling leads to a paradox which brings the whole approach into question. Scaling brain size against body size is implicitly making a strong claim about the functioning of neural tissue. The implication is that an animal with an expected brain size of 2.0 g and a real brain weighing 2.1 g and an animal with an expected brain size of 200 g and a real brain weighing 210 g are “really” equally brainy – even though the latter differs from the expected brain weight by 100 times as much neural tissue as the former. This is a very puzzling result for anyone used to computational (Turing) machines, since these are ultimately limited in power by the number of their elements. The paradox comes from mixing metaphors of what the brain is doing. If the brain is a sort of “on-board computer” (Dawkins 1976) that governs intelligent function, then the absolute number of neurons available for computation must be relevant, not the number relative to body size. (The logic here is that neural transmission speed is known to be the same in all mammalian brains, and evolution will have optimized neural programming in each species: thus differences will not reflect relative efficiency or hardware or software, as is the case in most artificial computers.) Bigger brains will be better brains, when it comes to flexible and intelligent responses, regardless of the species’ body size. In contrast, using allometric scaling against body size presupposes a more traditional scheme in which animal brains function by making responses to stimuli in a more-or-less reflex manner. The underlying model of the mind is then closer to an automatic telephone exchange than to a computer. Lines from/to subscribers in the telephone system model correspond, in bodies, to sensory and motor neurons. So, input/output connections will determine how big the system to handle them needs minimally to be. Larger bodies need larger brains for these prosaic purposes, and only measuring brain tissue relative to body size will show the extent to which processing can be more flexible and intelligent than the minimum. The on-board computer and telephone exchange models cannot both be right – or rather, they will be appropriate for different systems within a single brain, and the error is to assume that one or other can be neglected entirely (Byrne 1995b, 1996b). Accepting this more complex view, those brain parts involved in noncomputational body function should increase in size in some regular way with body size, whereas those parts used for computation should not. The absolute amount of brain tissue free for computation should give us an idea of the potential intelligence the brain can show, not the amount relative to body size. (Note that it is slightly more complicated than that, as neurons vary in size and packing density across species.) It should be no surprise, then, that allometric analysis of brain size relative to body size and alternative methods that in some way measure absolute sizes produce conflicting results (see Deaner et al. 2000).

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_41-9 # Springer-Verlag Berlin Heidelberg 2013

Fig. 1 Brain size and diet. Schematic illustration of the relationships for primates among diet quality, brain encephalization (i.e., size in relation to body size), and the cognitive skills required to find and process foods. Note that specialization in low-quality food/cognitively undemanding/relatively small brain is just as effective as an evolutionary strategy as high-quality food/cognitively demanding/relatively large brain

Relative Brain Size: The Value of a Brain Allometric scaling shows that, among mammals, the primate order as a whole is larger brained than most other groups (Jerison 1973). But when strepsirhine primates are partitioned from the rest, they turn out to have brains about the size predicted from mammalian body size (Passingham and Ettlinger 1974). The monkeys and apes, however, have brains twice as large as those of average mammals of their size. What does this mean? Following the arguments of this chapter, disproportionate brain size in relation to body size is not simply a matter of greater intelligence and must be understood in terms of costs as well as benefits. Any species with brain relatively large for its body size inevitably incurs greater risks than a small-brained relative, from the remorseless demand for higher metabolic energy. The relatively large-brained monkeys and apes are thus bearing a much greater cost from their larger brains, on average, than most mammals: how, and why, are these increased costs acceptable? Primates with home ranges that are large in area tend to have relatively large brains (CluttonBrock and Harvey 1980), and this has been used to argue that environmental complexity has a powerful influence on primate brain size. But there is an alternative explanation for that correlation: as an artifact of selection for bigger bodies in more folivorous species (Byrne 1996b). Folivory relies on a complex or at least large stomach: for example, the foregut fermentation chamber of colobine monkeys or the large hindgut of gorillas. Leaves are relatively abundant in most primate habitats, so primates with more folivorous diets can find sufficient food for their nutrition in smaller home ranges. By contrast, frugivory requires a larger range area, for year-round access to a variety of fruit species and other sources of nutrients, but the high sugar content allows digestion by a shorter gut. Other things being equal, primates that eat more fruit will have smaller bodies and larger home ranges than those that eat more leaves, causing a correlation between frugivory and relative brain size, regardless of any differences in intelligence. Variations in brain size relative to body size may therefore be a side effect of differences in body size due to diet type rather than a direct result of selection for larger brain size. Since gut tissue is metabolically as costly as brain tissue, and diets requiring only small guts (frugivory, meat eating) often provide a surplus of energy by the time a nutritional balance is obtained, primates with small guts are on the whole likely to be better able to “afford” larger brains (Aiello and Wheeler 1995). Clearly, the grade shift toward meat-based diets in the later hominins might be related to the massive brain expansion in these species. The relationship between energy supply and the size of brain that can be afforded for a given body size does not, however, explain

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_41-9 # Springer-Verlag Berlin Heidelberg 2013

why larger brains should have evolved in some taxa and not others: the opposite is just as feasible, a trend toward smaller brains in species with less need for high-quality diets (see Fig. 1). Moreover, the fact that the energy demands of the brain are constant suggests that the large brain/high-energy diet is a particularly risky evolutionary strategy for which a compelling competitive advantage must exist. One possibility is that a niche for a high-quality diet specialist may happen to become available, and the survival cost of large brain size is thereby lessened for any species that exploits that opportunity, resulting in a new equilibrium at a higher relative brain size. However, higher quality diets are usually based on sparse, hard-to-find, hard-to-access, or hard-to-process foods (e.g., fruit, nuts, meat), so this is not entirely plausible. More often, the causal chain is likely to run in the opposite direction: from a real need for higher intelligence, precisely in order to exploit a new, high-quality food supply. It might even sometimes be the case that ecological pressures for greater intelligence – and thus a larger brain – drive selection for a larger body, in order to support it. The frequently noted trend over geologic time for species of the same taxa to increase in size might sometimes be a consequence of an arms race of intellectual competition, selecting for larger brains and consequently larger bodies to support them at the same level of survival risk, coevolving with changes in diet.

Absolute Brain Size: The Power of a Brain To measure the computational power of a brain, it will be necessary to estimate the absolute number of neurons available for flexible, problem-solving purposes: the lack of any overwhelming correlation between overall brain size and observed smartness in animals suggests that simply using the total brain volume will not do. Jerison (1973) was well aware of the need and developed an index of “extra neurons” by calculating the absolute number of neurons beyond what was minimally necessary for bodily function. With a similar aim, Bauchot and Stephan (1966) attempted to identify the taxonomic group with least intelligence, as a baseline from which all others deviated. However, difficulties in deciding what volume of neural tissue is minimally necessary, or whether any species entirely lacks flexible intelligence, have prevented general adoption of these approaches. In recent years, the same problem has generally been tackled in a different way by comparing the volume of one part of the brain, the neocortex, against the rest. There are two assumptions involved here. First, that the primate brain has undergone mosaic evolution, with some parts growing in size and power at the expense of others, for a given overall size (Barton 1998; Barton and Harvey 2000). On a broad scale, this assumption is hard to doubt: for instance, haplorhine primate brains are clearly more dominated by visual cortex and less by olfactory lobes than those of most other mammals, including strepsirhines. The second assumption is that a primary function can be safely assigned to expansions of particular regions – in particular, that the neocortex is involved in abstraction, thinking, and executive functions such as effective problem solving. This is supported by a long history of deducing brain function from task failures after accidentally or deliberately inflicted lesions, somewhat problematic to interpret but consistent in pattern, and more recently supplemented by the differences in patterns of energy use revealed by brain imaging. (Note, however, that most published brain images conveniently omit the “lower” cerebellum: I return to the role of the cerebellum later in the chapter.) More pragmatically, it can be noted that the increase in brain volume in the primates over that of other mammal groups is chiefly due to neocortical enlargement; and among primates, it is the neocortex that varies most strikingly between species, with correlated changes in cerebellum (Whiting and Barton 2003), whereas the Page 7 of 18

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_41-9 # Springer-Verlag Berlin Heidelberg 2013

rest of the brain shows much less evolutionary change. This implies a strong selection pressure for neocortical enlargement in primates, and an intellectual function is the only serious candidate for this selection pressure. If it is taken, then, that primate neocortical enlargement measures specialization in some sort of intelligence, can ecological correlates indicate the function it subserves? Sawaguchi and Kudo (1990) found that the neocortex was larger in species living in bigger social groups, both in strepsirhines and in frugivorous platyrrhines. Also, in frugivorous haplorhines, polygynous species (one male living with more than one female) had larger neocortices than monogamous species. These findings hint at a social origin of intelligence (Jolly 1966; Humphrey 1976; Byrne and Whiten 1988), and Dunbar (1992, 1995, 1998) has gone further to support this idea, examining whether neocortex size correlates with measures of social or environmental complexity in living primates. He used both raw neocortical volume and several more complex functions; all gave similar trends but neocortex ratio (ratio of neocortex size to that of the rest of the brain) gave the clearest effects. Measures of environmental complexity – range area, day journey length, and the amount of fruit in the diet – were found to be unrelated to neocortex ratio when body size effects were removed. In contrast, average species group size correlated with measures of neocortical enlargement, supporting a predominantly social function of primate intellect. Dunbar proposes specifically that neocortical size limits the social complexity that an individual can cope with: social complexity increases with group size, so groups begin to fragment when their size increases past a complexity limit set by neocortical size. These analyses can be criticized on statistical grounds – for instance, neocortical ratio is correlated with body size, and using species as data points brings problems of phylogenetic independence – but the broad findings have been confirmed, using absolute neocortex volume and the volume of the rest of the brain as independent predictors and the method of independent contrasts to avoid phylogenetic bias (Barton 1996; Barton and Dunbar 1997; Barton and Harvey 2000). Neocortical expansion is clearly linked with increased social group size in primates (and indeed also in bats, carnivores, and cetaceans). These correlations give little clue, however, as to precisely what social skills are possible, or enhanced, by the possession of a larger neocortex. The problem is, of course, the difficulty of finding a species-fair and widely applicable measure of social skill, but there are now some steps in this direction. The most detailed analyses so far have been applied to the use of deception by primates within their own social group. Social manipulation of affiliated conspecifics, avoiding the disruptive use of violence, lies at the heart of the Machiavellian intelligence hypothesis (Humphrey 1976; Byrne and Whiten 1988). Cases where an individual achieves its ends by successfully deceiving another have long fascinated primatologists (Goodall 1971; de Waal 1982, 1986; Byrne and Whiten 1985), which made it possible to assemble an extensive corpus of carefully documented records, spanning all major groups of primates (Byrne and Whiten 1990). Preliminary analyses showed that most acts of deception were carried out with little sign of intentional understanding but nevertheless served effectively to manipulate the visual attention of other individuals and thence their understanding of the situations (Whiten and Byrne 1988a, b). These visual perspective-taking abilities were confirmed experimentally, in chimpanzees, when researchers modified naturally occurring situations of food competition for laboratory testing (Hare et al. 2000, 2001); the field data indicates, however, that visual perspective taking is widespread also in monkeys. A larger corpus confirmed that only in the great apes did any of the accounts seem most parsimoniously explained as a result of mental state attribution (Byrne and Whiten 1991, 1992); even in these cases, alternative, nonmentalistic possibilities are entirely possible (Byrne 1993; Povinelli and Vonk 2003). However, the frequency of use of deception was clearly not uniform across species, nor easily explained as a result of observer effort (Byrne Page 8 of 18

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_41-9 # Springer-Verlag Berlin Heidelberg 2013

and Whiten 1992). Byrne and Corp (2004) investigated whether neocortical specialization was involved. Correcting the raw frequencies of observed deception for observer effort by using the number of long-term field studies of habituated individuals over the period, and using independent contrasts to correct for phylogenetic bias, they found that neocortical enlargement – whether measured by neocortex ratio or absolute volume – strongly predicted the rate of use of deception. In contrast, neither the volume of the rest of the brain nor even the species’ average group size had significant effects (note that the number of species for which data were available was smaller than in Dunbar and Barton’s analyses of group size, so the difference may relate to statistical power). It seems that the use of deception for social manipulation critically depends on neocortex size. What cognitive processes are likely to be involved in using deception? Given the lack, in the vast majority of cases, of any sign of intentionally planned deceit (Byrne and Whiten 1992; Byrne 1997a), the main attribute would seem to be rapid memory in social contexts: memory of who was present on which occasion, who did what to whom, and so forth (Byrne 1996a). This suggestion finds support from the finding that social grooming is correlated with group size in Old World primate species (Dunbar 1993): for grooming to be valuable as a social currency, a good memory of grooming debts to and from social companions is essential. Innovation of novelty has been shown, similarly, to vary with neocortical enlargement in primates (Reader and Laland 2001). It is less clear what may be minimally needed for the ability to innovate successfully, but an analysis of the innovations employed in primate deception found that most cases involved only generalization of familiar behavior to slightly novel contexts (Byrne 2003b).

The Intelligence to Understand the World Learning and memory are certainly critical aspects of intelligence to the extent that they allow efficient, rapid, and flexible performance. But there is more to human intelligence than quick learning and reliable memory: to quote one definition, “grasping the essentials in a situation and responding appropriately to them” (Heim 1970). Putting this in more cognitive terms, intelligence implies the ability to represent the processes, social or physical, which are going on around us, and to use those mental representations to plan actions that may later be put into effect. Can evidence from living primates be used to deduce when, and in which ancestral species, this sort of intelligence evolved? Getting evidence of such capacities without using the medium of language is tricky, but this is a topic of extensive current research and some progress has been made. With very few exceptions, the evidence comes from great apes, although the interpretation of negative evidence is always problematic. Outside the great ape clade, it is very possible that primate behavior is not based on representational, mental models; even for great apes, interpretations remain controversial and are likely to change both as a result of improved data and sharper theoretical analyses. Signs of social understanding, which include some level of theory of mind ability, have long been reported from analyses of observational data; these have included empathy and sympathy, intentional deception, and pedagogical teaching (de Waal 1982; Boesch 1991; Byrne and Whiten 1991). Until recently, however, the consensus of laboratory experimentation was that great apes entirely lacked any such ability (Povinelli and Eddy 1996; Tomasello and Call 1997; Heyes 1998; Tomasello 1998). However, a number of experimental results have now brought the experimental and observational data sets into closer alignment (for reviews, see Call 2001 and Tomasello et al. 2003): using more naturalistic paradigms to examine great ape problem solving, a series of experiments have shown aspects of intentional understanding. These capacities closely match Page 9 of 18

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_41-9 # Springer-Verlag Berlin Heidelberg 2013

those apparent in some of the most complex cases of great ape deception, mentioned above (see Byrne and Whiten 1991): the ability to respond appropriately to differences in intention (e.g., accidental versus deliberate, inability versus unwillingness), visual perspective (hidden to a competitor but in view to self, partial versus completely hidden), and other individuals’ knowledge (e.g., known to one competitor but not another). Signs of technical understanding have long been claimed for apes, because of the evidence of tool use and tool manufacture in the chimpanzee (and one population of orangutan), but there has been little attempt to work out exactly what understanding is needed for these skills to be learnt (Seed and Byrne 2010). Many animals use detached objects as tools (Beck 1980), the process of tool manufacture is usually quite simple (McGrew 1992), and the strongest argument that great ape tool use relies on representational understanding is that sometimes tools are prepared or selected in advance, out of sight of the place of use (Byrne 1998; Byrne et al. 2013). Most studies of chimpanzee tool use emphasize product rather than process, and in fact the evidence for unusual abilities in manual skill learning is stronger for the case of plant processing than tool use (Byrne 2004). Circumventing the physical defenses of herbivorous plants leads to the use of complex processing (Corp and Byrne 2002a), and both mountain gorillas and chimpanzees have been found to employ hierarchically organized procedures consisting of several modules employed in series or as subroutines (Byrne 1999b; Byrne and Byrne 1993; Byrne and Russon 1998; Byrne et al. 2001; Stokes and Byrne 2001; Corp and Byrne 2002b). Learning by imitation links social and technical intelligence: by means of social learning, technical skills are acquired. Imitation, in the rich sense of learning new, useful behavioral routines directly from observation, is often thought to rely on prior understanding of mental entities, e.g., “the child must imaginatively place herself in the circumstances of the adult and determine what is the purpose of the behavior and how one goes about accomplishing that purpose” (Tomasello et al. 1993; my italics). Acquisition of novel behavioral routines by observation has been strongly argued for mountain gorillas, orangutans, and chimpanzees (Russon and Galdikas 1993; Byrne and Russon 1998; Byrne 1999a, b, 2002; Byrne and Stokes 2002; Lonsdorf et al. 2004), variously on the basis of (a) resemblance in fine detail between behavior of mother and offspring, (b) the fact that disabled individuals learn group-typical manual processes rather than devising more efficient, idiosyncratic versions, and (c) the sheer improbability of highly specific and complex organizations of behavior developing so similarly in each individual without some learning by imitation. It is also usually presumed that the site-specific differences in chimpanzee behavior reflect socially learned traditions in which useful skills are passed on by imitative learning of the critical aspects of processes which are hard for any individual to discover on any reasonable timescale, simple “cultures” (Whiten et al. 1999; Whiten 2000; but see Byrne et al. 2004, Laland and Janik 2006, for caveats). A tidy picture is thereby painted of great apes – and perhaps only great apes – able to understand other individuals’ behavior in terms of intentional properties, giving them the ability to learn novel technical procedures from watching others who already have skills, leading to the elaborate, groupspecific traditions in skills of significant technical sophistication described in wild chimpanzees. Given the close relationship of chimpanzees to ourselves, these similarities to human intelligence would be interpreted as resulting from common descent from a shared Miocene ancestor, having the ability to mentally represent intentional and causal-functional aspects of complex processes. This picture may not be all it seems, however. Over just the same 20-year period in which evidence of richly complex behavior in great apes, once dismissed by experimentalists, has become hard to doubt, a number of theoretical analyses have begun to question what the evidence implies about the mental processes involved. It is important to stress that this challenge is not a reworking of early behaviorist critiques; behaviorism was hamstrung by its insistence on not postulating Page 10 of 18

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_41-9 # Springer-Verlag Berlin Heidelberg 2013

mental processes as “intervening variables,” whereas that is no longer at issue. However, if great apes were equipped with powerful systems for detecting and extracting patterns of statistical regularity in the world around them – patterns that correspond to intentions, plans, and causeand-effect relationships – such use of statistical regularities might be sufficient to explain what the apes do, without their having concepts that correspond to human ideas of mental states and causal relationships. Those may all be dependent on language and function in other ways than as primary causes of behavior. Consider the case of imitation. There is a body of evidence, sketched above, that suggests great apes are able to learn by imitation the organizational structures of complex skills: how actions are grouped into often-used modules, how modules may be incorporated as subroutines into an overall plan (and thus repeated or omitted, depending on particular conditions of a given task), how sequential ordering affects outcomes, and so on. This is called program-level imitation (Byrne and Byrne 1993; Byrne 1995b; Byrne and Russon 1998) and involves the use of hierarchical organization to structure novel actions. But where do the programs come from: is it essential to discern the demonstrator’s intentions, and the cause-effect of how actions achieve their results, to derive a useful program? Not necessarily: if a sufficiently large corpus of behavior can be observed, then recurring patterns among the natural variability of behavior can in principle reveal all the organization underlying skilled action that is necessary for program-level imitation (Byrne 1999a, 2002): “imitation without intentionality” is a real possibility. The process of extracting statistical regularities from the messiness of natural, goal-directed action has been termed behavior parsing (Byrne 2003a) and serves to reveal the underlying deep structure of behavior, but it does not depend on explicit representation of intentions and causes. Instead, the extracted structures of behavior link prior circumstances to resulting outcomes, so that if a particular outcome is desired, then those circumstances can be sought and that structure of behavior applied (see also Byrne 1995a, b). In principle, it is possible that behavior parsing might also underwrite other behavioral routines that appear to rely on understanding ignorance, knowledge, intentions, and dispositions of others. While nothing so specific as for imitation has been worked out to date, Povinelli and Vonk (2003) point out that claimed mental processes of chimpanzees are “suspiciously similar” to those of humans and suggest that this may be because humans (alone) construe behavior in those terms. The implication is that the cognitive system of nonhuman great apes is adept at extracting and using complex patterns of behavioral action but does not represent these patterns in the form of attributions about the mental states of others. None of these critics suggest that humans lack the powerful mental processes for extracting statistical regularities from behavioral observations: indeed, even 8-month-old infants are able to extract statistical regularities from spoken strings of letters, after only a few hours of exposure to monotonously spoken letter strings built according to particular rules (Saffran et al. 1996). And the area of the brain most closely associated with development of patterned motor behavior (Marr 1969), the cerebellum, is especially enlarged in humans, even as compared to other great apes and greatly more than in monkeys (Barton 2012). The point is rather that the way we describe behavior in everyday talk, in terms of goals, plans, and intentions, may be uniquely human. Mention of “everyday talk” may give the clue to the function of intentional-causal representation: rather than primary cause of behavior, such representations may be valuable because they allow pedagogy, explanation, and deliberate retrospective misrepresentation of behavior, using the medium of spoken language (Byrne 2006). Heretical as it may sound, it is worth questioning whether much everyday human behavior relies on intentional-causal analyses of situations: the alternative is that the same, powerful mechanisms for automatically extracting and using statistical regularities (regularities that themselves result, of course, from underlying intentions and causal Page 11 of 18

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dependencies) allow us to function in a “fast and mindless” fashion, responding appropriately and efficiently without deep thought about underlying mechanisms (and see Bargh and Chartrand 1999). Perhaps only when in contemplative mood, when asked directly or when trying to explain (away) our actions, do we invoke the machinery of causal-intentional representation.

Conclusion People often speak as if intelligence were unitary, as if it could be measured on a single scale, but that is perhaps unlikely. If it is accepted that intelligence is not a single “thing” but rather a mixed bag of devices and processes, endowments, and aptitudes that together produce behavior we see as “intelligent,” then it makes sense to study separate facets of intelligence independently of each other. Modern psychometric work, following Rozin (1976), recognizes several “intelligences”: social-empathic, technical-mathematical, and commonsense-practical (Sternberg and Kaufman 2002). Presumably, in comparing across species, the different types of intelligence are likely to be even more sharply defined, and many cognitive capacities may need to be distinguished – each of them contributing to an impression of intelligent action but originating in different evolutionary circumstances and often at different periods of evolutionary history. Taking that line, it is possible to summarize what is currently most likely to have happened over the evolutionary timescale that we share with living primates. Primate evolution has seen two separate changes in intellectual potential, with concomitant brain changes. In the first, well-accepted, evolutionary event, selective pressures to cope with and succeed within larger social groups led to a greater ability to learn in social situations, resulting in species with enhanced abilities in social perception (including sophisticated visual recognition of identity and demeanor) and memory (including subtle correlates of past events). This intellectual change was permitted by increased neocortical capacity, with correlated cerebellar enlargement, and gave the ability to learn impressive-seeming tactics of behavior such as deception and cooperation. Deep understanding of the mechanism of these social tactics was lacking in the individuals of these species themselves, and they (like modern monkeys) were not able to imitate novel skills or show insight into causal relationships in the physical sphere. In the second evolutionary event, ancestral great apes acquired extra abilities. The selective pressure that resulted in this change may indeed have been competition from Old World monkeys, species that now compete with apes for food in almost all their habitats and have clear advantages in terms of more efficient long-range locomotion and digestion (Byrne 1997b). The result was a clade of modern great apes, all of which have “special” abilities valuable for food acquisition, based on their ability to learn novel routines of skilled, bimanually coordinated manual action, sometimes involving tool use, sometimes involving locomotion, and reliant on imitation by behavior parsing as well as exploration. This intellectual change was permitted by an increase in cerebellum size, going beyond that expected from the already large brains of animals much larger than monkeys. Behavior parsing gave these apes a rudimentary ability to understand the intentions (as physically attainable goals) of other individuals and a rudimentary ability to understand the causal logic (as correlational likelihood) of physical events. For individuals to go beyond this “behavioral approximation” of intentions and causality, to a deeper understanding of theory of mind and cause and effect, may have required representation of propositions for which there is no evidence in living nonhuman species – and it may indeed have required language. Comparative psychology cannot help, in that case, since the necessary adaptations must be uniquely human. On the other hand, widening the scope of comparative analysis Page 12 of 18

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_41-9 # Springer-Verlag Berlin Heidelberg 2013

beyond the nonhuman primates, to examine other taxa entirely, offers the prospect of a more general understanding of the evolution of intelligence. Already a promising start has been made, with some cognitively sophisticated species: parrots (Pepperberg 1999), cetaceans (Herman 1986; Rendell and Whitehead 2001), pigs (Held et al. 2000, 2001, 2002), canids (Miklosi et al. 2004), elephants (Bates et al. 2008; Plotnik et al. 2011; Smet and Byrne 2013), corvids (Emery and Clayton 2004; Dally et al. 2010), and tortoises (Wilkinson and Bugnyar 2012). With converging evidence from all these taxa, and a solid body of data on a significant range of nonhuman primates, it will be time to attack once more the persisting problems of studying intelligence: How many kinds of intelligence are there? To what extent are different intellectual capacities localized in the brain? What adaptive pressures select for particular abilities? And so on.

Cross-References ▶ Modeling the Past: The Primatological Approach ▶ Molecular Evidence of Primate Origins and Evolution ▶ Origin of Modern Humans ▶ Theory of Mind: A Primatological Perspective ▶ The Evolution of Speech and Language ▶ The Evolution of the Hominid Brain

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Smet AF, Byrne RW (2013) African elephants can use human pointing cues to find hidden food. Curr Biol 23:2033–2037. doi:10/1016j.cub2013.08.037 Sternberg R, Kaufman J (2002) The evolution of intelligence. Lawrence Erlbaum Associates, Mahwah Stokes EJ, Byrne RW (2001) Cognitive capacities for behavioural flexibility in wild chimpanzees (Pan troglodytes): the effect of snare injury on complex manual food processing. Anim Cogn 4:11–28 Tomasello M (1998) Uniquely primate, uniquely human. Dev Sci 1(1):1–30 Tomasello M, Call J (1997) Primate cognition. Oxford University Press, New York Tomasello M, Kruger AC, Ratner HH (1993) Cultural learning. Behav Brain Sci 16:495–552 Tomasello M, Call J, Hare B (2003) Chimpanzees understand psychological states: the question is which ones and to what extent. Trends Cogn Sci 7:153–156 Warren JM (1973) Learning in vertebrates. In: Dewsbury DA, Rethlingshafer DA (eds) Comparative psychology: a modern survey. McGraw Hill, New York, pp 471–509 Wechsler D (1944) The measurement of adult intelligence. Williams and Wilkins, Baltimore Whiten A (2000) Primate culture and social learning. Cogn Sci 24(3):477–508 Whiten A, Byrne RW (1988a) The manipulation of attention in primate tactical deception. In: Byrne RW, Whiten A (eds) Machiavellian intelligence: social expertise and the evolution of intellect in monkeys, apes and humans. Clarendon, Oxford, pp 211–223 Whiten A, Byrne RW (1988b) Tactical deception in primates. Behav Brain Sci 11:233–273 Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V, Sugiyama Y, Tutin CEG, Wrangham RW, Boesch C (1999) Cultures in chimpanzees. Nature 399:682–685 Whiting BA, Barton RA (2003) The evolution of cortico-cerebellar complex in primates: anatomical connections predict patterns of correlated evolution. J Hum Evol 44:3–10 Wilkinson A, Bugnyar T (2012) Cold-blooded cognition: reptilian cognitive abilities. In: Vonk J, Shackleford TK (eds) The Oxford handbook of comparative evolutionary psychology. Oxford University Press, New York, pp 129–143

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Index Terms: Absolute brain size 7 Allometry 4 Behavior parsing 11 Brain size 4 Encephalization 5 Frugivory 6 General intelligence 2 Imitation 10 Intentionality 10 IQ/intelligence testing 2 Machiavellian intelligence 8 Mental state attribution 8 Relative brain size 6 Social intelligence 9 Social manipulation 8 Species intelligence 2 Theory of mind 9

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_42-3 # Springer-Verlag Berlin Heidelberg 2014

The Hunting Behavior and Carnivory of Wild Chimpanzees Nicholas E. Newton-Fisher* School of Anthropology and Conservation, University of Kent, Canterbury, Kent, UK

Abstract The pursuit, capture, and consumption of small- and medium-sized vertebrates appear to be typical of all chimpanzee (Pan troglodytes) populations, although large variation exists. Red colobus monkeys (Piliocolobus sp.) appear to be the preferred prey, but intensity and frequency of hunting vary from month to month and among populations. Hunting is a predominately male activity and is typically opportunistic, although there is some evidence of searching for prey. The degree of cooperation during hunting, as well as prey selection, varies between East and West African populations and may be related to the way the kill is divided: in West Africa, hunters often collaborate, with kills tending to be shared according to participation, whereas in East Africa, cooperation in hunting is more limited, and the kill is typically consumed selfishly or divided in response to harassment (begging) by others. In some cases, it may be shared tactically, trading meat with other males to strengthen alliances. The adaptive function of chimpanzee hunting is not well understood, and a variety of hypotheses have been proposed. Ideas that chimpanzees hunt to make up for nutritional shortfalls, or to acquire meat to trade for sex, have failed to find empirical support, while recent work favors nutritional benefits of some kind. Nevertheless, cross-population studies evaluating multiple hypotheses are in their infancy, and there is much to be learned. In particular, very little is known about hunting of nonprimates, particularly ungulates, or the impact that variation in levels of hunting, and of carcasses to share and consume, has on patterns of chimpanzee behavior. If one goal of studying this topic is to shed light on the behavioral ecology of hominins, then efforts to understand the diversity of hunting and carnivory in wild chimpanzees are needed.

Introduction Hunting – the pursuit, capture, and consumption of small- and medium-sized vertebrates – appears to be typical of all chimpanzee (Pan troglodytes) populations. Such behavior has aroused considerable interest among anthropologists since it was first reported (Goodall 1963). Hunting, the division of the kill, and the consumption of meat all play an important role in the lives of modern hunter-gatherer societies (Lee 1979; Kaplan and Hill 1985; Hawkes et al. 2001; Hawkes and Bird 2002) and factor in a number of hypotheses concerning human evolution (Washburn and Lancaster 1968; Isaac 1978; Hill 1982; Tooby and DeVore 1987; Stanford 1996, 1998, 2001). While early ideas such as “Man the Hunter” (Washburn and Lancaster 1968) have been largely discredited, hunting as a means to acquire meat remains important in many modern scenarios (Domı´nguez-

*Email: [email protected] Page 1 of 27

Primates Red colobus Piliocolobus badius Piliocolobus tephrosceles Black and white colobus Colobus guereza Colobus polykomos Colobus satanas Olive colobus Procolobus verus Gray-cheeked mangabey Lophocebus albigena Sooty mangabey Cercocebus atys Olive baboon Papio anubis Yellow baboon Papio cynocephalus Vervet monkey Chlorocebus pygerythrus Red-tailed monkey Cercopithecus ascanius Campbell’s monkey Cercopithecus campelli Diana monkey Cercopithecus diana L’Hoest’s monkey Cercopithecus l’hoesti Blue monkey Cercopithecus mitis

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Pan troglodytes schweinfurthii Budongo Gombe Kahuzi

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Table 1 Diversity of mammalian prey hunted by chimpanzees across Africa

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P. t. troglodytes Lope Ndoki

P. t. verus Assirik Bossou

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_42-3 # Springer-Verlag Berlin Heidelberg 2014

Page 2 of 27

Mona monkey Cercopithecus mona Lesser spot-nosed monkey Cercopithecus petaurista Crowned monkey Cercopithecus pogonias Bushbaby Galago sp. Potto Perodicticus potto Chimpanzee Pan troglodytes Ungulates Forest duiker Cephalophus sp. Blue duiker Cephalophus monticola Bushbuck Tragelaphus scriptus Bushpig Potamochoerus porcus Warthog Phacochoerus aethiopicus Others Giant elephant shrew Rhynchocyon sp. Yellow-spotted hyrax Heterohyrax brucei White-tailed mongoose Ichneumia albicauda ✓

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✓

✓

Pan troglodytes schweinfurthii Budongo Gombe Kahuzi

The Hunting Behavior and Carnivory of Wild Chimpanzees, Table 1 (continued) Semliki

✓

✓

✓

P. t. troglodytes Lope Ndoki

✓

✓

✓

P. t. verus Assirik Bossou

✓

Taı¨

(continued)

Tenkere

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_42-3 # Springer-Verlag Berlin Heidelberg 2014

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✓

✓

Kasakati

Ngogo ✓ ✓

Mahale

Semliki

✓ ✓

P. t. troglodytes Lope Ndoki

✓

✓

P. t. verus Assirik Bossou

✓

Taı¨

Tenkere

Populations (study sites) of chimpanzees are arranged by subspecies. A ✓ indicates that the species has been recorded being killed or consumed. Not all species of prey are present at all sites

Civet Civettictis civetta Rodents (various spp.) Pangolin

Pan troglodytes schweinfurthii Budongo Gombe Kahuzi

The Hunting Behavior and Carnivory of Wild Chimpanzees, Table 1 (continued)

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_42-3 # Springer-Verlag Berlin Heidelberg 2014

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Rodrigo 2002; Hawkes and Bird 2002). Animal tissue has high calorific value relative to plant material, is rich in fat and protein, and contains essential amino acids (Milton 1999). It is therefore a valuable resource. The nonrandom sharing of meat has been proposed as an important selective force driving the evolution of intelligence (Stanford 2001), and the consumption of meat has been invoked as an important proximate factor enabling the evolution of larger brains in the Homo lineage (Aiello and Wheeler 1995). Chimpanzees show large variation between populations in the choice of prey species, frequency of hunting, and the techniques employed. Understanding both how and why chimpanzees hunt is important for the framing of evolutionary hypotheses; chimpanzees provide our best evidence for the behavioral capabilities of early hominins (Domı´nguez-Rodrigo 2002). In this chapter, substantially revised and updated from the previous version (Newton-Fisher 2007), I review the data concerning hunting behavior among wild chimpanzees and address current hypotheses concerning the reasons why chimpanzees hunt, drawing out both similarities and differences between populations in their hunting behavior.

Characteristics of Chimpanzee Hunting All known populations of chimpanzees show some evidence of hunting and consuming vertebrate prey. Such hunting has been documented systematically among the East African chimpanzees (Pan troglodytes schweinfurthii) of the Gombe (van Lawick-Goodall 1968; Teleki 1973; Busse 1977; Stanford 1998; Gilby 2006; Gilby et al. 2006, 2010) and Mahale (Nishida et al. 1979; Takahata et al. 1984; Uehara 1997) National Parks in Tanzania and of the Kibale Forest National Park (Mitani and Watts 1999; Watts and Mitani 2002; Teelen 2008; Gilby et al. 2008; Watts and Amsler 2013) in Uganda, as well as among the West African chimpanzees (P. t. verus) of the Taı¨ National Park, Cote D’Ivoire (Boesch and Boesch 1989; Boesch and Boesch-Achermann 2000; Gomes and Boesch 2009). Other reports of hunting by chimpanzees come from East African populations in the Budongo Forest, Uganda (Newton-Fisher et al. 2002), Kahuzi-Biega National Park, DRC (Basabose and Yamagiwa 1997), Kasakati, Tanzania (Kawabe 1966), and Semliki, Uganda (Hunt and McGrew 2002); from central African populations (P. t. troglodytes) of Lope´, Gabon (Tutin and Fernandez 1993) and Ndoki, Cameroon (Kuroda et al. 1996; Takenoshita 1996); from the Ebo forest, Cameroon (P. t. ellioti) (Morgan et al. 2013); and from West African populations of Mt. Assirik, Senegal (McGrew 1983; Hunt and McGrew 2002), Bossou, Guinea-Bissau (Sugiyama and Koman 1987), and Tenkere, Sierra Leone (Alp and Kitchener 1993).

Prey Diversity Across populations, prey diversity is high with at least 40 species of vertebrates targeted. Chimpanzees show a clear focus on mammalian prey (Table 1) and are known to consume a variety of primate species as well as ungulates and rodents but will also eat birds, lizards, and frogs. Some populations have a diverse range of prey, whereas others are more specialized. The Mahale chimpanzees, for instance, are known to hunt at least 17 species of mammals, while in Taı¨, chimpanzees hunt only 7 (all primates) of the 15 sympatric mammal species (Boesch and Boesch-Achermann 2000; Boesch et al. 2002). Prey are typically small, up to a maximum of around 20 kg – the weight of an adult male black and white colobus monkey (Colobus guereza) (Kingdon 1997) or a part-grown bushpig (Potamochoerus porcus) – but often much smaller (Goodall 1986).

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Prey Specialization Monkeys, in particular colobus monkeys, appear to be the main prey of chimpanzees wherever the species are sympatric. Red colobus (Piliocolobus tephrosceles in East Africa, Piliocolobus badius in West Africa) are the primary prey for many populations of chimpanzees, with black and white colobus (Colobus guereza in East Africa, Colobus polykomos in West Africa) as a secondary target. The degree to which chimpanzees specialize on monkeys to the exclusion of other prey species varies between populations. In the Taı¨ Forest, chimpanzees show a notably strong specialization. Between 1984 and 1995, 249 of 267 known kills were of colobus monkeys: 80.5 % red colobus (Piliocolobus badius) and 12.7 % black and white colobus (Colobus polykomos) (Boesch and Boesch-Achermann 2000). A similar specialization is apparent among the Ngogo chimpanzees of the Kibale forest, where between 1995 and 2000, 92.5 % of all prey were colobus monkeys: 87.8 % red colobus (Piliocolobus tephrosceles) and 4.7 % black and white colobus (Colobus guereza). At Gombe, the specialization is less extreme but still noticeable: red colobus (there are no black and white colobus at this site) constituted 59 % of the chimpanzees’ prey between 1970 and 1975, 66 % between 1976 and 1981, and 84.5 % between 1990 and 1995 (Goodall 1986; Stanford 1998). By contrast, red colobus constituted only 53 % of all prey for the Mahale chimpanzees (Nishida et al. 1992), while black and white colobus (Colobus guereza) were 43.8 % of all prey for the Sonso chimpanzees of the Budongo Forest, where there are no red colobus (Newton-Fisher et al. 2002). These two populations appear to differ from the others in that the chimpanzees also prey upon small ungulates, particularly blue duiker (Cephalophus monticola), to an appreciable degree: 34 % of all prey in Mahale (Nishida et al. 1992) and 25 % of all prey in Budongo (Newton-Fisher et al. 2002). Data from Budongo are sparse, but observations support the idea that these chimpanzees do not demonstrate the extreme prey specialization seen in Taı¨ and Ngogo (Newton-Fisher unpublished data). Forest ungulates, particularly duiker and bushpig, are in fact hunted by all the East African chimpanzee populations that have been studied (Gombe: Goodall 1986; Mahale: Nishida et al. 1992; Budongo: Newton-Fisher et al. 2002; Kibale: H. Sherrow personal communication) but do not appear to be regarded as prey by West African chimpanzees (Uehara 1997; Boesch and BoeschAchermann 2000). More research is needed regarding chimpanzee predation on ungulates. Chimpanzee populations also appear to differ in their choice of the age and sex of prey. For the Taı¨ chimpanzees, half of their colobus monkey prey are adult, mostly females (Boesch and BoeschAchermann 2000). This is in contrast to chimpanzees at Mahale and Gombe, where the vast majority of colobus prey are juveniles and infants (Goodall 1986; Uehara 1997) and some chimpanzee hunters target very young colobus monkeys, snatching them from their mothers (Stanford 1998). Somewhere between 75 % (Stanford et al. 1994) and 86 % (Stanford 1998) of red colobus prey at Gombe are immature individuals. For the Ngogo (Kibale) chimpanzee, the figure is somewhat less: 53–75 % (Mitani and Watts 1999; Watts and Mitani 2002). There is less information on the age and sex of non-colobus prey. Among the ungulates, bushbucks are targeted only as infants (fawns), as typically are bushpig (piglets) (Goodall 1986). Age and sex estimates of duiker kills are more difficult to obtain, given that the prey is rapidly torn apart and consumed entirely by the chimpanzees; however, it is clear that chimpanzees are quite capable of killing adult blue duiker (personal observations).

Sex Bias in Hunting The hunting of monkeys is a predominately male activity. Among the chimpanzees of the Ngogo (Kibale) community, adult or adolescent males made 98.8 % of all kills recorded between 1995 and 2000 (Watts and Mitani 2002). In two decades of data from Gombe, adult males were responsible for 91.5 % of all kills (Stanford 1998). Female chimpanzees will and do hunt, however. Data from Page 6 of 27

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Gombe for 1977–1979 showed that females joined an average of 26 % (median: 25 %, range: 0–67 %) of red colobus hunts for which they were present and those females who were more likely to join males in a hunt were also more likely to hunt when apart from the males (Goodall 1986). One female, Gigi, contributed 4 % of the total kills (Stanford 1998). Any kills that females made as part of mixed-sex hunting party were likely to be taken by males (Goodall 1986), however, which may in part explain female unwillingness to hunt when males are present. Females may prey more on ungulates (Uehara 1997), but quantitative data are difficult to collect, in part due to the nature of ungulate hunting. The hunting of lesser bushbabies (Galago senegalensis) in Fongoli, Senegal, is rather different to the typical group hunts of monkeys: it is tool assisted, extractive, and individualistic; it also shows a strong female bias, with 14 of 22 observations of female hunters and only one of an adult male hunting in this way (Pruetz and Bertolani 2007).

Hunting Frequency Detecting hunting in a chimpanzee population can be problematic, particularly if the chimpanzees are poorly habituated to human observers. Typically in this situation, hunting is rarely if ever seen, and studies rely on finding animal remains such as skin or bone in chimpanzee feces (McGrew 1992). Unfortunately, feces do not appear to provide a reliable indicator of hunting: while the presence of remains can confirm that consumption does occur, little can be said about its frequency (cf. Uehara 1997). For example, long-term observations of habituated chimpanzees in the Taı¨ Forest have revealed a pattern of frequent hunting and consumption that is not mirrored in the pattern of prey remains found in fecal samples (Boesch and Boesch-Achermann 2000). Further, fecal sampling can say nothing about the number of hunting attempts that fail to secure prey, the division of the prey once obtained, or the relative importance of scavenging as a method of acquiring meat. Similar problems may also occur when hunting is actually rare or when prey species are alerted or scared away by the presence of humans accompanying the chimpanzees, although in some cases chimpanzees may exploit their prey’s fear of humans to increase hunting success (Goodall 1986; Boesch 1994).

Predation Pressure While in some populations chimpanzees hunt only rarely, in others they are significant predators who hunt at levels that appear to be unsustainable (Goodall 1986; Wrangham and van Zinnicq Bergmann Riss 1990; Teelen 2008; Watts and Amsler 2013). Estimates for Gombe suggest that anything from 8 % to 42 % of the colobus population can be killed annually, with this proportion varying from year to year, 8–13 % (1973–1974: Busse 1977), 41.6 % (1972–1975: Wrangham and van Zinnicq Bergmann Riss 1990), and 16.8–32.9 % (1982–1991: Stanford et al. 1994), while at Taı¨ during the 1980s, the figure was between 3 % and 8 % (Boesch and Boesch-Achermann 2000). For Ngogo, Teelen (2008) estimated 15–53 % of the red colobus population is killed by chimpanzees annually, while Watts and Amsler (2013) estimated that almost 2,500 red colobus monkeys were killed in the period 1998–2012, an average of 20.4–24.8 % of the population per year. By contrast, the Mahale chimpanzees were estimated to kill only around 1 % of the red colobus population each year during the 1980s (Boesch et al. 2002). Basabose and Yamagiwa (1997) estimate that the chimpanzees of Kahuzi-Biega kill 11–18 % of the Cercopithecus monkey population each year (predominately Cercopithecus mitis but also Cercopithecus l’hoesti). Hunting of ungulates may also impose high levels of mortality. Wrangham and van Zinnicq Bergmann Riss (1990) estimated chimpanzee-imposed mortality on bushbuck at 27 % (although this figure Page 7 of 27

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includes bushbuck fawns killed by baboons and subsequently stolen by chimpanzees) and on bushpig at 7 %, for populations in the Gombe National Park between 1972 and 1975. These estimates, both for primates and ungulates, are based on comparing the number of kills with the population density of prey within the chimpanzee community’s home range. There is potential for error in the estimates of each of these variables. If, for example, home range is overestimated (cf. Newton-Fisher 2004), then predation pressure will be underestimated, while underestimating the number of potential prey will inflate the estimate of predation pressure (Wrangham and van Zinnicq Bergmann Riss 1990). Nevertheless, the level of predation by some chimpanzee communities on red colobus monkeys is extreme. As a reference point, predation by crowned eagles on the total cercopithecoid monkey population at Ngogo is estimated at 2 %: Mitani et al. (2001). There is good evidence that a significant decline in red colobus monkeys in the Ngogo region of the Kibale forest, at least since the mid- to late 1990s and possibly since the 1970s, is the result of chimpanzee predation (Teelan 2007, 2008; Lwanga et al. 2011; Watts and Amsler 2013). Simulations using 3 years (2001–2003) of Ngogo data showed that chimpanzee predation was likely to drive the red colobus population to local extinction within two decades without a dramatic change in the level, or success, of chimpanzee hunting (Teelen 2008). Local extinction is more probable if neighboring communities of chimpanzees also impose significant predation pressure (Watts and Amsler 2013) as this removes any “source” population from which immigrants can be drawn (contra Lwanga et al. 2011). The decline in red colobus in Ngogo has, however, been accompanied by a decline in chimpanzee hunting (encounters, hunts, and prey offtake) which appears to be a consequence of the reduced availability of prey: when these chimpanzees expanded their territory in 2009 (Mitani et al. 2010), they increased rates of both prey encounters and hunting (Watts and Amsler 2013).

Variation in Hunting Frequency Estimates of hunting frequency and predation pressure typically disguise wide variation. Within a single community, the total number of hunts can vary from month to month and year to year. Across populations, chimpanzees appear to have hunting “seasons” during which the number of kills increases as a result of either more hunting, more successful hunting, or both. For the chimpanzees at Gombe, Mahale, and Taı¨, this hunting season falls toward the end of the year, peaking in September and October. At Gombe, this corresponds to the later part of the dry season (Stanford 1998; Gilby 2004). At Mahale, the peak is slightly later, reaching into November, and appears to coincide with the end of the dry season and the first rains of the wet season (Takahata et al. 1984). Preliminary work at Budongo suggested a dry season (December to February) peak in hunting activity (Newton-Fisher et al. 2002), but subsequent work has failed to confirm this idea (Newton-Fisher unpublished data). The hunting behavior of the Ngogo chimpanzees does not appear to correspond to timing of rainfall, but hunting seasons instead occur during periods of fruit abundance (Watts and Mitani 2002) that are not correlated with rainfall (Mitani et al. 2002). Similarly, the hunting season at Mahale occurs when more fruit is available (Uehara 1997), and among the Kanyawara chimpanzees of the Kibale forest, hunting rates were higher when preferred species of ripe fruit were abundant (Gilby and Wrangham 2007). At Taı¨, the hunting season runs from mid-August to midNovember, between periods of low and high fruit abundance, and ends when chimpanzees switch to highly calorific Coula edulis nuts from which they gain sugar, protein, and fat. The peak in hunting is also in September and October, but this is during the wet season at the time of greatest rainfall (Boesch and Boesch-Achermann 2000).

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In addition to these seasonal changes, hunting frequency within a single community varies between years, which may be related to changes in the abundance of prey species or the number of chimpanzees who might hunt. A comparison of hunting success for Mahale chimpanzees between the 1980s and early- to mid-1990s showed a threefold increase in the percentage of the red colobus population killed by the chimpanzees, rising from around 1 % to at least 3 % of the population per year (Boesch et al. 2002). This seemed to accompany an expansion in the red colobus population. Hunting success then fell in the later part of the 1990s, following a decrease in the number of chimpanzees in the study community (Boesch et al. 2002): a similar reduction in the level of hunting was seen following a decrease in the number of adult males in the study community in the Taı¨ Forest (Boesch and Boesch-Achermann 2000). Impact Hunters Chimpanzees may also experience greater hunting success when individuals with a flair for hunting are present. These individuals (“impact” hunters) demonstrate both a high willingness to hunt and a consistently high probability of success (Goodall 1986; Stanford 1998; Boesch and BoeschAchermann 2000). Typically, one or two males in each study populations where monkey hunting is prevalent have been identified as impact hunters (Goodall 1986; Stanford 1998; Boesch and Boesch-Achermann 2000; Gilby et al. 2008), with anecdotal evidence suggesting that these individuals are responsible for initiating hunts, climbing first toward prey. Other male chimpanzees may be spurred into hunting by the actions of these impact hunters. A recent increase in hunting of black and white colobus monkeys by Sonso (Budongo) chimpanzees has been ascribed to the actions of a particular male, while Stanford (1998) found that two males of the Kasekela (Gombe) community were highly successful when hunting alone and that one of these, Frodo, was both a catalyst for hunts and a fearsome predator of red colobus monkeys, killing at least 50 in the period 1990–1992. Gilby et al. (2008) tested the influence of impact hunters among the Kanyawara (Kibale) chimpanzees and found that the likelihood of a hunt occurring was much greater when an impact hunter was present, even when controlling for the number of adult males, and that the chance of other males joining a hunt increased if an impact hunter was hunting.

Hunting Binges A further source of variation in hunting frequency within a community is the occurrence of hunting “crazes” (van Lawick-Goodall 1968) or “binges” (Stanford 1998). These are periods during which the chimpanzees hunt “almost daily”: more than three hunts in a 7-day period, with chimpanzees appearing to hunt on contact with prey (Stanford 1998). In the Kasekela (Gombe) community, 23 binges were recorded between 1990 and 1995. The longest of these lasted 74 days and consisted of 38 observed hunts and at least 76 kills, all red colobus. Correcting the number of kills for observation time suggests that over 100 colobus monkeys were killed during this 74-day period (Stanford 1998). The Ngogo chimpanzees went on a 57-day hunting binge in 1998, during which they hunted 22 times, killing 69 red colobus, one mangabey (Lophocebus albigena), and one red duiker (Cephalophus sp.). Only 4 of the 22 hunts were unsuccessful, including two attempts to hunt black and white colobus (Colobus guereza). This and other hunting binges at Ngogo coincided with major fruit crops, and most hunting occurred when large parties of males were traveling together (Watts and Mitani 2002). Large parties with high numbers of males also seem to be linked to hunting binges at Gombe (Stanford 1998). Large numbers of chimpanzees traveling together suggest that fruit is particularly abundant, and so hunting binges at Gombe may also be linked to periods of food abundance.

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How Do Chimpanzees Hunt? Many hunts are opportunistic, in that chimpanzees appear to decide to hunt after encountering prey during the course of normal foraging activities or travel around the home range. This seems to be the typical pattern at Gombe (Goodall 1986; Stanford 1998) and at Ngogo (Mitani and Watts 2001). Chimpanzees in Taı¨, however, show evidence of actively searching for prey, listing for the vocalizations of either colobus monkeys or Diana monkeys (Cercopithecus diana) with whom the colobus are frequently associated (Boesch 1994; Boesch and Boesch-Achermann 2000). The likelihood of a hunt when chimpanzees encounter potential prey varies: it is relatively high for the Kasekela (Gombe) community (40 %: Gilby et al. 2006) and the Ngogo (Kibale) community (37 %: Mitani and Watts 2001) but somewhat lower in the Kanyawara (Kibale) community (15 %: Wrangham, cited in Gilby et al. 2006). Chimpanzees hunt the majority of their prey without the use of tools or weapons, although there are a few reports of rocks or branches being hurled, possibly in an attempt to panic defensive formations of adults (Goodall 1986), and tools (sticks and leaves) are sometimes used to aid in the processing of the carcass (McGrew 1992). In Fongoli, Senegal, chimpanzees fashion tools from branches, at times biting the end to create a point, which are forcibly jabbed into tree cavities: observations suggest that this is done to immobilize or kill lesser bushbabies (Galago senegalensis) that are then extracted and consumed (Pruetz and Bertolani 2007). During a monkey hunt, prey are typically chased, seized, and then killed either by a bite, by disembowelment, or by being torn apart (Goodall 1986). Hunts may yield single or multiple kills (or, indeed, may fail completely). Between 1973 and 1981, Gombe chimpanzees made multiple kills in 37.5 % of colobus hunts; most of these were two kills per hunt. A typical colobus hunt at Gombe will produce two (Watts and Mitani 2002) or three (Stanford 1998) kills and at Ngogo, four kills (Mitani and Watts 2001). Single kills seem to be more usual for Taı¨ chimpanzee hunters (Stanford 1998), although typically such kills are of adult monkeys (mean number of kills per successful hunt: 1.2: Watts and Mitani 2002). Failure rates (i.e., failure to kill any prey during a hunt) vary between communities. For the Tai and Gombe chimpanzees, around 50 % of hunts fail (Boesch and Boesch-Achermann 2000; Gilby et al. 2006), while for Ngogo chimpanzees the rate is lower, at 16 % (Mitani and Watts 2001). In an analysis of hunting by chimpanzees of the Kanyawara community, Gilby et al. (2008) found that an individual hunter had around a 65 % chance of acquiring meat in any hunt that was successful; among the Taı¨ chimpanzees, a male had access to meat in around 48 % of successful hunts (Boesch and Boesch-Achermann 2000). Analysis of hunting data from both Ngogo (Watts and Mitani 2002) and Gombe (Wrangham 1975; Stanford et al. 1994; Gilby et al. 2010) indicates that hunting is responsive to habitat structure. At Ngogo, chimpanzees were more likely to hunt red colobus when encountering prey in, or close to, areas with broken or no tree canopy than when in primary forest (Watts and Mitani 2002); at Gombe, hunts were more likely and more successful in woodland and semi-deciduous forest than in evergreen forest. These observations suggest that, as with obligate predators, chimpanzees are more likely to hunt in areas where it is harder for prey to escape and hunting costs are lower (Gilby et al. 2010). The hunting of ungulates is less well described. Bushpigs are probably the most difficult of ungulate prey. Chimpanzees are wary, if not fearful, of the adults, and they retreat to the trees in the face of aggression by adult pigs (personal observations). At Gombe, chimpanzees have been described using stealth to seize piglets before the adults are alerted to their presence and also of using aggressive displays to panic the adults, capturing piglets either in the confusion or if abandoned by adults that run off (Goodall 1986). Bushbuck fawns hide in dense cover as an Page 10 of 27

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antipredator strategy, while adults typically freeze or flee. Chimpanzees search for hiding fawns when their attention is drawn to particular areas by the presence of adult bushbuck or possibly auditory or olfactory cues. A captured fawn’s mother may be aggressive toward chimpanzees, but this is difficult to determine as human presence causes them to flee (Goodall 1986). Duiker captures are typically opportunistic, with chimpanzees seizing them if they come within reach. Chimpanzees sometimes show interest in duiker vocalizations (personal observations), but the extent to which they search for duiker is unclear.

Cooperative Hunting? Chimpanzees will hunt alone as well as in the company of others. Solitary hunts occur rarely at Taı¨ (16 % of hunts: Boesch and Boesch-Achermann 2000) and Mahale (28 % of hunts: Takahata et al. 1984; Uehara et al. 1992), while they are more common at Gombe (64 % of hunts: Busse 1978; Teleki 1973) where the chimpanzees appear to be highly effective solo hunters. Boesch (1994) found that Gombe chimpanzees had a success rate of around 50 % when hunting alone, capturing an average of 2.46 kg of prey within 7 min of hunting. In contrast, his estimate for the success rate of lone hunters at Taı¨ was only 13 %. The forest canopy is lower and more broken at Gombe than it is at Taı¨, which may make it easier for lone chimpanzees to isolate colobus monkeys and so allow them to capture and kill their prey more often and more quickly (Boesch 1994). Group hunts are often a case of individual chimpanzees making their own efforts in a collective setting, perhaps exploiting the panic in the prey produced by the presence of multiple hunters, and reacting to the actions of other chimpanzees. Collaborative hunting, where males take particular roles such as “drivers” and “blockers” (Boesch and Boesch 1989), appears to be the primary form of hunting among the Taı¨ chimpanzees (77 % of hunts: Boesch and Boesch-Achermann 2000) but is rare among the East African chimpanzees (Boesch 1994; Stanford 1998; Boesch and BoeschAchermann 2000; Watts and Mitani 2002). A division of roles between those that pursue the prey and those that wait on the ground to capture monkeys that fall from the canopy is, however, fairly common among East African chimpanzees. There is little consensus over the degree to which such collaborative hunting can be described as cooperative. To the extent that chimpanzees take different roles and are responsive to one another’s behavior during a hunt targeting monkeys, there is good evidence for social cooperation. To demonstrate that chimpanzee hunting is functionally cooperative, however, individuals need to do better when hunting as a group. Thus, if cooperation occurs, hunting attempts should be more successful when more individuals take part, or at least certain number of hunters should be more successful than solitary hunters. At Gombe, Ngogo, and Taı¨, the probability of killing prey during a red colobus hunt increases with the number of hunters present, but this appears to be a simple effect of more hands grabbing at the monkeys; there does not appear to be an additional effect from males working together (Stanford 1998; Gilby et al. 2006); at Kanyawara, however, there does appear to a synergistic effect (Gilby et al. 2008). Many chimpanzees, hunting together, may be able to overwhelm the defensive strategies of the red colobus and reduce the opportunities for panicked monkeys to escape. However, the mass of prey obtained per hunter does not correlate with the number of males hunting at Ngogo (Watts and Mitani 2002), and while Stanford (1998) found that Gombe chimpanzees gained a higher return (greater mass of prey per hunter) when more than seven are hunting together, Gilby et al (2006), using a larger dataset from the same community, found that the mass of prey per hunter actually decreased with the number of adult male chimpanzees present. By contrast, among Taı¨ chimpanzees the number of hunters is strongly correlated with the mass of prey caught because the

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likelihood of capturing an adult monkey increases, but gains per hunter peak at four males (Stanford 1998) presumably because most hunts terminate after the first kill.

Scavenging Chimpanzees are reluctant scavengers: only a handful of reports describe such behavior. Most of these observations concern the seizing of fresh kills from other predators, a behavior often labeled “piracy” (Goodall 1986; Uehara 1997; Stanford 1998), although “plundering” – the forcible stealing of goods – might be more appropriate term. At Gombe, chimpanzees have been recorded plundering fresh kills from baboons (Morris and Goodall 1977; Goodall 1986), and at Budongo, the body of infant blue monkey (Cercopithecus mitis) was stolen from the adult blue monkey who killed it (Newton-Fisher et al. 2002). Boesch and Boesch-Achermann (2000) report three instances of Taı¨ chimpanzees plundering red colobus captures from eagles while the monkeys were still alive and a further four instances of chimpanzees eating the kills of eagles: presumably these monkeys were freshly killed, although this information is not reported. Given that chimpanzees are quite willing, if they can steal or beg part of the carcass, to eat prey that chimpanzees other than themselves have killed, it is not surprising that they are similarly willing to take fresh kills from other species. True scavenging – acquiring meat from an abandoned carcass – appears particularly rare, however. In 36 years of observation at Gombe, fewer than 20 instances were recorded (Stanford 1998), and at least nine of these (all red colobus) were likely, or known, to have been previous chimpanzee kills (Goodall 1986). Similar low rates have been recorded at Mahale, seven cases in over 25 years of observation: six ungulates and one red-tailed monkey (Cercopithecus ascanius) (Hasegawa et al. 1983; Uehara 1997). Scavenging has not been reported from Taı¨: Boesch and Boesch-Achermann (2000) record ten encounters with fresh carcasses, none of which were eaten by the chimpanzees. Most encounters with fresh carcasses result in apparently curiosity-driven behaviors in the chimpanzees, with no indication that the chimpanzees regard these carcasses as a source of meat. Stanford (1998) reports an observation from Gombe of a juvenile male briefly chewing on 1- or 2day-old colobus meat that was ignored by the adults, and Muller et al. (1995) record a further observation from the same community of a party of chimpanzees encountering a dead bushbuck, presumed to be killed by a leopard. The chimpanzees showed strong curiosity over the body, even grooming it, and one female rolled around inside the eviscerated carcass, but they did not feed (Muller et al. 1995). By contrast, chimpanzees at Mahale did feed on the carcasses of two adult bushbuck thought to be the remains of leopard kills (Hasegawa et al. 1983).

Meat Eating All populations of chimpanzees subsist on a primarily frugivorous diet. Typically, fruit constitutes 60–80 % of the time spent feeding (Gombe: 63 %, Wrangham 1977; Kibale: 79 %, Wrangham et al. 1996; Budongo: 64.5 %, Newton-Fisher 1999a). This is supplemented by leaves, as well as other plant materials. Even in communities that hunt frequently, such behavior constitutes a very small portion of the time spent foraging. Watts and Mitani (2002) recorded 131 predation episodes in 6 years at Ngogo (1.8 hunts per month), while Boesch and Boesch-Achermann (2000) recorded 413 hunts in a 12-year period at Taı¨ (2.9 hunts per month). Nevertheless, as discussed above, chimpanzees do hunt, kill, and consume meat, while competition over the division of the kill can be high. Page 12 of 27

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The Value of Meat Animal tissue, including muscle, internal organs, brain, and bone marrow, provides an easily digestible nutritious package (Stanford 1996; Milton 1999). Beyond any particular calorific value, it provides high-quality protein containing all essential amino acids, as well as long-chain polyunsaturated fatty acids, and a range of key micronutrients such as calcium, potassium, magnesium, zinc, B-group vitamins, and vitamin K. Commonly, chimpanzees consume the entire animal, including bones and skin, and will compete for the smallest scraps. A single carcass can, therefore, represent an important resource, despite variation in body size between prey species: adult Colobus guereza weigh up to 23 kg, although Ugandan populations may not reach this size, while the western black and white colobus (Colobus polykomos: adult male body weight of 8–12 kg) is smaller and similar in size to the eastern red colobus (Piliocolobus tephrosceles: adult male body weight of 13 kg); the western red colobus (Piliocolobus badius) are lighter, with an adult body weight of only 5–10 kg (Kingdon 1997); and blue duiker (Cephalophus monticola) can weigh up to around 9 kg, with duiker (Cephalophus sp.) meat providing 20.8 g/100 g of protein and 3.4 g/100 g of fat (Ntiamoa-Baidu (FAO) 1997). The quantity of meat, including the associated elements of the carcass, that is consumed by some individuals may be relatively significant. In good hunting years, the total amount of meat consumed may be more than double that consumed in poorer years. The 45 chimpanzees of the Kasekela (Gombe) community in 1992 consumed over 500 kg of red colobus meat, and their total meat consumption for the year was probably close to 700 kg. The previous year (1991), colobus meat consumption was less than 200 kg, and in 1988, this figure was less than 150 kg (Stanford 1998). Averaged over years, the level of consumption in the 1980s and 1990s seems similar to the estimate of 441 kg of meat per year for the same community in the 1970s (Wrangham and van Zinnicq Bergmann Riss 1990; Stanford 1998). Boesch and Boesch-Achermann (2000) estimated that, averaged across the year, male Taı¨ chimpanzees consumed 186 g per day, while females consumed 25 g per day. Their estimates for Gombe chimpanzees, similarly averaged, were 55 g per day for males and 7 g per day for females. These are similar to estimates made by Stanford (1998) of 70 g per day for males during peak hunting season and by Wrangham (1975) of 22 g averaged over males and females. Gilby (2006) estimated that, for adult males of this community in 1999–2002, an individual in possession of a kill consumed between 0.25 and 2.5 kg (mean ¼ 1.16 kg) of meat during each feeding bout. For the Taı¨ chimpanzees between 1987 and 1991, males consumed a mean of 0.48 kg of meat per successful hunt, while females consumed a mean of 0.13 kg (Boesch and Boesch-Achermann 2000). Thus, meat should be a valued resource for chimpanzees, although there are observations that question this conclusion. In particular, captured prey may be eaten only partly before being discarded. In the Taı¨ Forest, adult cercopithecine monkeys have been treated in this way (Boesch and Boesch-Achermann 2000); at Gombe, chimpanzees have been observed discarding captured adult red colobus in favor of pursing immature monkeys (Boesch 1994; Stanford 1998) and giving a carcass to another individual in order to hunt again (Goodall 1986), while in the Budongo Forest, an adult male chimpanzee captured and killed an elephant shrew (Rhynchocyon sp.) but took only a single bite before discarding the carcass (Newton-Fisher unpublished data). Similarly, bodies of infant chimpanzees killed by adults are sometimes only partially eaten before being handed on to another individual or discarded completely (Newton-Fisher 1999b). Furthermore, any kills made during a group hunt are typically divided in some way among some or all of the chimpanzees present.

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Begging and Food Sharing Following a kill, there is commonly a degree of competition for the meat, the intensity of which reinforces the idea that chimpanzees desire and value this resource. If the chimpanzee in possession of the carcass has companions, these individuals will attempt to acquire part of the carcass. More dominant individuals may attempt to steal the entire carcass for themselves. Others will sit around the possessor and beg for a share of the meat. Begging individuals seem to exert a lot of pressure both by their presence and by their harassing gestures and vocalizations. Chimpanzees unwilling to share will commonly move away from the crowd of begging individuals, although they are likely to be followed. When harassed by one or two others, a chimpanzee may simply turn its back to prevent them reaching toward the carcass. Sharing of prey can be either an active or passive process. Most sharing is passive and ranges from an individual patiently scrounging the scraps that fall from a carcass as the possessor feeds, through harassment of the owner of the carcass by gestures and vocalizations, to an individual who is not in possession of the kill taking a portion of carcass without the use of aggression. Active sharing is less common and involves the individual who possesses the carcass handing part, or all, of the carcass to another chimpanzee. There are a number of theories to explain why food should be shared and the patterns of sharing observed. These include tolerated theft, reciprocity, kin selection, mutualism, buy-off, and harassment. As they apply to chimpanzees, these theories have been discussed extensively elsewhere (de Waal 1989; Mitani and Watts 2001; Fruth and Hohmann 2002; Stevens 2004; Stevens and Gilby 2004; Gilby 2006). Patterns of sharing appear to differ between West and East African chimpanzees. In the Taı¨ Forest, West African chimpanzees tend to divide the kill among the individuals who participated in the hunt. Older and more dominant males gain a greater share of the meat, but hunters tend to receive more than nonhunters, even when socially subordinate. The amount of meat obtained by females is not dependent on participation in the hunt, but females will support hunters over nonhunters when there is competition (Boesch and Boesch-Achermann 2000). In East Africa, at Gombe (Stanford 1998), Mahale (Nishida and Hosaka 1996), Ngogo (Mitani and Watts 2001), and Budongo (Newton-Fisher unpublished data), chimpanzees use a different strategy for the division of the carcass: males tend to monopolize the carcass and share only with particular other adults, both male and female (although it is worth noting that while Gilby (2006) found that Kasekela (Gombe) males, particularly the alpha, controlled carcasses, these males only shared preferentially with adult females with whom they exchanged grooming and did not preferentially share with particular males). The particular sharing strategy employed by West African chimpanzees may oblige them to hunt adult monkeys. Collaborative group hunting appears necessary to increase hunting success and to reduce the time spent hunting in a habitat that favors escape by the prey but may only work if males are rewarded for participating in the hunt (Stanford 1998). Colobus monkeys are smaller in West Africa than they are in East Africa, and this might make targeting juveniles unprofitable if the meat has to be shared among all hunters. For East African chimpanzees, the larger body size of the colobus monkeys may pose a greater hazard, and East African chimpanzees show greater fear of adult colobus monkeys than do those in West Africa. Adult colobus monkeys can successfully threaten and rout chimpanzees, chasing them from trees on occasion (Nishida et al. 1979; Goodall 1986; Boesch and Boesch 1989). Given that the strategy adopted by East African chimpanzees of targeting juvenile and infant chimpanzees appears to be profitable (Boesch 1994), the additional costs of targeting adult monkeys together with a less reliable, more individualistic approach to sharing may make hunting adult monkeys a less attractive option.

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Why Do Chimpanzees Hunt? This question, which addresses the adaptive value of hunting, remains to be answered. It is only recently that quantitative analyses comparing the various hypotheses have been undertaken (Mitani and Watts 2001; Gilby et al. 2006) and, while there are efforts to draw together results from different populations (Uehara 1997; Boesch et al. 2002), systematic analyses across populations are limited (Gilby et al. 2010). Chimpanzees are omnivores, and while those who eat meat, particularly in large quantities, should gain nutritional benefits, carnivory does not appear to be critical for survival or reproduction, and thus various hypotheses have been advanced to explain the existence of their hunting behavior.

Hunting for Nutrition Early views of chimpanzee hunting favored the view that it was driven by nutritional demands. Teleki (1973) proposed that Gombe chimpanzees hunt to compensate for nutritional shortfalls, given the strong seasonality at this site. The body weights of Gombe chimpanzees are lower during the dry season (Williams et al. 2002), which may to be the consequence of low food availability, and hunting at Gombe is more pronounced during the dry season than it is during the wet season (Stanford 1998; Gilby et al. 2006). A nutritional perspective was also emphasized by Wrangham (1975), with a similar view emerging from research at Mahale (Takahata et al. 1984). Energy Shortfall The particular hypothesis that chimpanzees switch to hunting to compensate for energy shortfalls finds little support: Gilby et al. (2006) found that once party size and number of swollen (i.e., likely to be ovulating and therefore sexually attractive) females were taken into account, there was no association between diet quality and hunting among the Gombe chimpanzees. Furthermore, Mitani and Watts (2001) and Gilby and Wrangham (2007) found that chimpanzees from the Kibale forest hunted more frequently as fruit became more abundant, suggesting that chimpanzees are more likely to hunt when they have enough surplus energy. This makes sense if hunting is energetically costly, and individuals risk not gaining enough meat following division of the kill to offset such costs. Whether this relationship between food abundance and frequent hunting applies to all populations of chimpanzees remains to be determined, but, as discussed above, hunting seasons coincide with fruit abundance in Mahale (Takahata et al. 1984; Uehara 1997) although apparently not at Taı¨ (Boesch and Boesch-Achermann 2000) where chimpanzees may gain shares of the kill that depend on their participation in hunting (Boesch 1994). If the Taı¨ chimpanzees capture and kill a sufficiently large prey in each hunt and if they can rely on this system of dividing the meat, then net nutritional gains would accrue to all participants. Meat Scraps Boesch and Boesch-Achermann (2000) suggested that the nutritional value of meat beyond its calorific value might make even small amounts significant for chimpanzees. Gilby et al. (2008) and Tennie et al. (2009) formalized this idea as the “meat-scrap” hypothesis, which assumes that hunting functions as a means of acquiring micronutrients such as vitamins B12 and B6 and the minerals iron and zinc which are important for primate health and present at relatively high levels in meat but at low levels or virtually absent from primate plant foods. By consuming small amounts of meat (“scraps”), chimpanzees gain these micronutrients without having to consume vast

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quantities of plant material. This hypothesis assumes a threshold, a minimum amount of meat necessary to accomplish this goal (Tennie et al. 2009). Both Gilby et al. (2008) and Tennie et al. (2009) provide support for this hypothesis. Among the Kasekela (Gombe) chimpanzees, the probability of an individual acquiring some meat increased by 18 % with each additional hunter, while the total amount of meat per hunter was not correlated to the number of hunters (Tennie et al. 2009) and in fact declined when all adult males present were considered (Gilby et al. 2006). For chimpanzees of the Kanyawara (Kibale) community, males were also more likely to obtain meat as the number of hunters increased, although once there were five or more hunters, males could do as well by begging: accordingly, focal males were less likely to hunt when more than five other males were present (Gilby et al. 2008).

Hunting for Trade Goods The nutritional content of meat and associated tissue, together with the fact that it is both divisible and portable, means that each portion has an inherent value and can be either consumed or given to another individual. Meat could therefore be considered to be a commodity that can be traded with other individuals for other goods or services, which for chimpanzees are likely to be biases in future social interactions such as support in agonistic confrontation or increased levels of grooming. Such a “biological markets” (Noe and Hammerstein 1995) perspective is implicit in two further hypotheses concerning chimpanzee hunting, both of which see an adaptation in the nonrandom sharing of kills. While the “meat-for-sex” and “male-social-bonding” hypotheses are commonly presented as alternatives (Mitani and Watts 2001; Watts and Mitani 2002), they could be considered to be different, context-dependent outcomes of the same social strategy. This “meat-ascommodity” hypothesis proposes that chimpanzees hunt to gain possession of a commodity (part or all of an animal carcass) which has economic value within chimpanzee society (Stanford 1998); they can then trade this to further whatever proximate goals are most pressing, providing meat to females in an effort to coerce their mating behavior or to allies when they have need of them. Meat for Sex The first of these trade-based hypotheses, labeled “meat for sex” by Mitani and Watts (2001), was proposed by Teleki (1973). He noted that cycling females with conspicuous anogenital swellings tended to receive meat from adult males more frequently than did females without these sexual swellings and suggested that males shared meat with females in exchange for sexual access. Swollen females are attractive to males (Dixson 1998) as the swellings generally indicate approaching ovulation, although females will also show swellings when pregnant (Wallis and Lemmon 1986). Supporting evidence for this hypotheses was provided by Stanford (1998) who found that, at Gombe, the presence of a swollen female in a party of chimpanzees was the best predictor of a hunt occurring when encountering a group of red colobus and reported five observations of females begging for meat from males and only being given part of the kill after copulating. However, in detailed analyses of the Gombe data together with data from the Kanyawara community, Gilby et al. (2006, 2010) found no support for the “meat-for-sex” hypothesis: specifically, males did not preferentially share with potentially ovulating females, and males were not more likely to hunt when such females were present. Furthermore, very few copulations occurred in close temporal proximity to meat-sharing events (Gombe: 0.6 %; Kanyawara: 0.1 %: Gilby et al. 2010), and when sharing of meat did occur between a male and a swollen female, mating was equally likely before as after (Gilby et al. 2010). Parous females at Gombe were more successful than nulliparous females at obtaining meat from males, but this was the case whether Page 16 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_42-3 # Springer-Verlag Berlin Heidelberg 2014

swollen (72 % vs. 44 % of bouts) or not (60 % vs. 30 % of bouts), and Kanyawara females showed a similar trend (Gilby et al. 2010). This is likely to be due to increased persistence or intensity of begging by parous females, rather than strategic sharing by males. Similarly, at Ngogo, the presence of swollen females was not a significant predictor of hunting once the effect of the number of males was removed. Males of this community did preferentially share meat with swollen females but did not copulate with those females at a level above chance after sharing. Furthermore, they did not gain a larger share of matings if they did share with a female, comparing female cycles in which the male shared with those in which he did not (Watts and Mitani 2002). Among the Taı¨ chimpanzees, Gomes and Boesch (2009) found no evidence of direct exchanges of meat for sex or of a relationship between meat sharing and mating frequency. There are also theoretical reasons to question this particular hypothesis. Female chimpanzees show a highly promiscuous mating strategy (Nishida 1968; Sugiyama 1968), typically copulating hundreds of times with multiple males during a single ovulatory cycle (Wrangham 2002). As a result, it seems unlikely that they would require meat from males before mating; furthermore, males in possession of meat are typically high ranking: such males may be those most able to coerce female mating behavior through the use of aggression and so the least likely to need to trade anything with females in return for sex. For a more detailed discussion of this topic, see Gilby et al. (2010). Male Social Bonding The other theory that involves using prey as a trade good is the “male-social-bonding” hypothesis. Nishida (Nishida et al. 1992; Nishida and Hosaka 1996) provided data to support the idea that males trade meat with other males in order to develop and maintain the alliances that are thought to play an important role in male-male competition for status. Mitani and Watts (2001) showed that, at least for the Ngogo chimpanzees, while the presence of a female with a sexual swelling was a significant predictor of the decision to hunt, this was an artifact of the relationship between the presence of such females and the number of adult males and that it was the number of adult males alone that predicted hunting. They also showed that males shared reciprocally, at least when considering all pairs of males simultaneously, and that there was a positive association between sharing of carcasses and support in agonistic coalitions (Mitani and Watts 2001; Watts and Mitani 2002). By contrast, this hypothesis did not account for patterns of sharing between male chimpanzees at Gombe (Gilby et al. 2006). Hunting was more likely in parties with more males, but increasing male party size did not increase the likelihood that an individual focal male would hunt. Furthermore, these males did not share preferentially with those with whom they groomed or associated frequently (Gilby 2006). Similarly, an analysis of hunting among chimpanzees of the Kanwayara community found no support for this hypothesis, again using grooming and association as proxies for alliance partnerships (Gilby et al. 2008).

Hunting to Assess Reliability Male chimpanzees vary in their hunting ability, as demonstrated by the proportion of hunts that they join, the number of kills that they make, and their success at hunting alone (Stanford et al. 1994; Stanford 1998; Boesch and Boesch-Achermann 2000; Watts and Mitani 2002). Among the Ngogo chimpanzees, and potentially elsewhere, good hunters are also more frequent members of the territorial patrols that monitor and probe boundaries with neighboring communities. Furthermore, males that hunt together patrol together, and the frequency of joint patrolling is correlated with the frequency with which males form coalitions and the amount of grooming between them Page 17 of 27

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(Watts and Mitani 2001, 2002). This leads to the hypothesis that hunting itself may have a function that is independent from acquiring meat: it demonstrates risk-taking and allows males to assess the reliability of others when faced with danger (Watts and Mitani 2001). This is essentially a refinement of Kortlandt’s (1972) “hunting-to-display-social-prowess” hypothesis. Given the risks associated with patrolling and intercommunity encounters (Goodall et al. 1979; Boesch and Boesch-Achermann 2000; Muller 2002), these kinds of mutual assessments may be important for male chimpanzees. The “hunting-as-risk-assessment” hypothesis might apply to the monkey-hunting specialists of the Taı¨ Forest, as it appears to apply to the Ngogo chimpanzees, although it will be necessary to disentangle “hunting to assess reliability” from “male social bonding” (meat for allies) in testing the relative importance of these two ideas at both sites. This hypothesis may be interesting to consider in relation to the “show-off” hypothesis proposed to explain hunting behavior in human males (Hawkes 1991; Hawkes and Bird 2002).

So Why Do Chimpanzees Hunt? The possibility that chimpanzees achieve nutritional benefits directly from hunting cannot be easily dismissed. The necessary nutritional studies quantifying chimpanzee diet have not been conducted, and for either of the trade-goods hypotheses to operate, there must be a nutritional gain to the individuals who receive and consume parts of the carcass. If there were not, the carcass would hold no value and could not be traded. While it appears that chimpanzees hunt to gain meat, this is not to compensate for nutritional shortfalls. There is also essentially no support for the meat-for-sex trading hypothesis, and this can be largely discounted. That said, Gomes and Boesch (2009) found some evidence for this over a longer term (i.e., not in the immediate sharing context) among the Taı¨ chimpanzees, which remains intriguing. The one context where females refrain from their promiscuous mating strategy is the consortship mating context (Tutin 1979). Does previous meat sharing by males increase the likelihood that females will comply with male efforts to initiate or maintain consortships? This remains to be determined. While it seems that nutritional (i.e., calorific) gain appears to be sufficient to explain hunting in West African chimpanzees (at least at Taı¨: Stanford 1998) given the pattern of sharing in relation to participation, evidence that 47 % of individuals sharing a carcass appear to cheat the system (Boesch and Boesch-Achermann 2000), as well as the possibility that other factors influence hunting, needs investigation before any firm conclusions can be drawn. For the Ngogo chimpanzees, there is evidence for both the male social bonding and assessing reliability hypotheses. For the Gombe chimpanzees on the other hand, sharing appears to come down to successful harassment of those individuals possessing meat (begging), and there is no support for the male social bonding hypothesis. The adaptive value – the function – of hunting thus remains unclear. Future work will need to consider variation in both predator and prey demography and perhaps determine more precisely the nutritional gains and energetic costs of hunting. It may also be worth testing hypotheses that address the behavior directly, rather than looking for a function in terms of relationships. It is becoming clear that chimpanzees hunt monkeys more frequently in locations where hunting costs are lower or at least where the prey should find it harder to escape; that hunting typically occurs when other food is abundant, such that hunters can absorb the calorific costs of failure; and that hunters who secure meat can gain substantial quantities in any particular bout. The question that needs to be addressed is whether the additional nutrition gained from meat translates into fitness: is there a direct fitness benefit to hunting?

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Marginal Gains McGrew (1992) showed that female chimpanzees who were more successful at gaining meat had greater numbers of surviving offspring, but it remains unclear whether males who gain more meat also derive fitness benefits. While it seems unlikely in calorific terms (there is no support for the energy shortfall hypothesis), there may be particular nutrients that are valuable, as suggested by the “meat-scrap” hypothesis. That hypothesis, however, focuses specifically on micronutrients, considering macronutrients such as protein and fat merely as helping to reduce dietary bulk (Tennie et al. 2009), and, with its focus on the minimum threshold, encounters problems explaining the variation in hunting between communities: if obtaining these micronutrients is critical, why are chimpanzees from communities where meat eating is rare able to maintain health and fertility? If the threshold is so low that these chimpanzees can reach it, why do then chimpanzees hunt substantially more frequently elsewhere? The route out of this conundrum is to recognize that fitness is relative and that for male chimpanzees their primary reproductive competitors are the other males of their community. Thus, any benefits of meat eating need to be evaluated against these rivals, rather than in absolute terms. Here, I propose a new hypothesis that broadens the “meat-scrap” hypothesis as well as recognizes this relative nature of fitness. This new “marginal gains” hypothesis assumes (1) that meat is valuable specifically for both macro- and micronutrients, rather than its calorific value, and (2) that individuals benefit through marginal gains over their competitors. For instance, small amounts of high-quality protein may provide an edge in sustaining muscle mass and thereby improving success in competing for high social rank. This “marginal gains” hypothesis predicts that individuals should value even the smallest scraps, as there is no threshold, and should attempt to gain more than rivals. “Marginal gains” is therefore consistent with patterns of begging and food sharing seen in East African chimpanzees: individuals without meat are strongly motivated to acquire whatever they can, yet males gain over their rivals by not sharing and so need to suffer harassment costs before sharing. In communities where males willingly share with alliance partners, the need for allies may also outweigh any marginal gains from consumption: it may be no accident that the strongest evidence for sharing with allies comes from the community (Ngogo) with the largest number of adult males. If marginal gains show diminishing returns, this would account for individuals relinquishing possession of kills after feeding and diminishing motivation to acquire and consume meat with the quantity ingested. Parenting Effort As a final note, even if there are no nutritional benefits to be gained by males, simply by virtue of hunting they create a resource supply (converting live prey into food) for females that would be otherwise unavailable. If, on average, the most successful hunters are also, for whatever reason, the most successful at fathering offspring, then hunting will function as a form of parenting effort (as has been suggested for male chimpanzee territoriality: Watts and Mitani 2001) without any need for active sharing or provisioning by males. The natural variation in hunting and meat eating within and across chimpanzee communities should provide the opportunity to test such ideas, and more detailed, cross-site studies are needed.

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Conclusions Chimpanzees are not the only primates that hunt vertebrate prey. Baboons (Papio spp.) also hunt opportunistically, targeting small ungulates (Morris and Goodall 1977; Strum 1987), while redtailed monkeys (Cercopithecus ascanius) stalk green pigeons (Treron calva) (Furuichi 2006). Among New World primates, capuchin monkeys (Cebus spp.) prey upon a variety of species with Cebus capucinus, perhaps best studied, showing a focus on squirrels, infant coatis, and birds (Rose 1997; Rose et al. 2003), while some squirrel monkeys (Saimiri sp.) hunt bats (Boinski and Timm 1985; Souza et al. 1997). Among the great apes, vertebrate predation appears to be rare or absent in both gorillas and orangutans, although bonobos (Pan paniscus), the phylogenetic sister species to chimpanzees, do hunt vertebrates. Recorded prey species include black and white colobus (Colobus angolensis), red-tailed monkeys (Cercopithecus ascanius) (Sabater Pi et al. 1993), bushbabies (Galago demidovii) (Hohmann and Fruth 2008), flying squirrels (Kano and Mulavwa 1984), and forest duiker (Cephalophus spp.) (Hohmann and Fruth 1993; Fruth and Hohmann 2002). Hunting by bonobos typically occurs at a lower rate than in chimpanzees: Fruth and Hohmann (2002) report only nine kills in 46 months of observation, seven of which were duiker, although data from the Lui Kotale site shows higher rates of predation: 18 kills in 60 months of observation (Hohmann and Fruth 2008). While hunting is thus not unique to chimpanzees among the primates, it does appear to be a ubiquitous aspect of their behavior, occurring in all populations studied thus far. The picture that has emerged from these studies is one of diversity but with some common themes. Across populations, hunting is a predominately male activity. Chimpanzees hunt a variety of vertebrate prey, but there is a common focus on medium-sized mammals, particularly primates, and especially colobus monkeys. Red colobus appear to be the preferred prey, although the species (and body size) of red colobus varies across Africa. Chimpanzees appear to impose significant predation pressure on their main prey species, but the intensity and frequency of hunting vary between populations and from month to month within single communities. Hunting is typically opportunistic on encountering potential prey, although there is some evidence of searching. Hunts can be solo or group efforts, and the degree to which individual chimpanzees hunt together varies between East and West African populations. This appears to be related to the way the kill is divided following the hunt. In West Africa, the kill tends to be shared according to participation in the hunt and individual hunters collaborate, taking different roles, whereas in East Africa, the kill is often consumed selfishly or shared under pressure and may be shared with other males in the hope of future coalitional support; group hunts are more akin to multiple, simultaneous individual efforts to secure prey. In both East and West African populations, the presence of particularly skilled or motivated “impact” hunters increases hunting frequency and success. It is important to recognize that this picture comes largely from detailed systematic studies of only a handful of communities (Gombe, Mahale, Taı¨, Ngogo, Kanyawara). Comparable systematic studies of hunting by chimpanzees in other populations are lacking, although some data are available from almost every population studied. In addition, much of the research effort has focused on chimpanzees and red colobus monkeys. Far less is known about chimpanzee hunting of other species and the nature and importance of hunting in populations that are not sympatric with red colobus. Certainly, chimpanzees without red colobus to hunt appear to hunt less frequently (Basabose and Yamagiwa 1997; Newton-Fisher et al. 2002), and it is unclear what impact low levels of hunting, providing fewer carcasses to share and consume, have on patterns of chimpanzee behavior. Page 20 of 27

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Addressing these shortcomings is essential if we are to use an understanding of chimpanzee hunting behavior to shed light on the behavioral ecology of the hominins. The ubiquitous nature of chimpanzee hunting, the common occurrence of food sharing, and the diversity in the patterns of these behaviors, together with the close phylogenetic relationship between chimpanzees and humans, ensure that consideration of chimpanzee hunting is essential in any discussion of the role played by meat eating and food sharing in the behavioral ecology of early hominin species. The radiation of early hominins encompassed a number of species with different morphologies, and it seems likely that these hominins showed both within and between species variation in habitat and behavioral ecology (Foley 1997). The chimpanzee-red colobus system may be a useful model for some of that variation, but it remains necessary to understand the role of hunting and meat eating across chimpanzee populations, including those with an impoverished resource base. Already it is clear that different populations target different arrays of species, specialize or generalize their choice of prey, and hunt and use meat in different ways. Future studies of new populations are likely to increase this picture of diversity, and systematic tests of the hypotheses for hunting and meat sharing will clarify both why chimpanzees hunt and the importance of this behavior for the study of human evolution.

Cross-References ▶ Dental Adaptations of African Apes ▶ Great Ape Social Systems ▶ Hominin Paleodiets: The Contribution of Stable Isotopes ▶ Modeling the Past: The Primatological Approach ▶ The Biology and Evolution of Ape and Monkey Feeding ▶ The Species and Diversity of Australopiths

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Hohmann G, Fruth B (1993) Field observations on meat sharing among bonobos (Pan paniscus). Folia Primatol 60:225–229 Hohmann G, Fruth B (2008) New records on prey capture and meat eating by bonobos at Lui Kotale, Salonga National Park, Democratic Republic of Congo. Folia Primatol 79:103–110 Hunt KD, McGrew WC (2002) Chimpanzees in the dry habitats of Assirik, Senegal and Semliki Wildlife Reserve, Uganda. In: Boesch C, Hohmann G, Marchant LF (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, New York, pp 35–51 Isaac G (1978) Food sharing behavior of proto-human hominids. Sci Am 238:90–109 Kano T, Mulavwa M (1984) Feeding ecology of the pygmy chimpanzees (Pan paniscus) of Wamba. In: Susman RL (ed) The pygmy chimpanzee: evolutionary biology and behavior. Plenum Press, New York, pp 233–274 Kaplan H, Hill K (1985) Food sharing among ache foragers: tests of explanatory hypotheses. Curr Anthropol 26:223–246 Kawabe M (1966) One observed case of hunting behavior among wild chimpanzees living in the savanna woodland of western Tanzania. Primates 7:393–396 Kingdon J (1997) The Kingdon field guide to African mammals. Academic, London, p 464 Kortlandt A (1972) New perspectives on ape and human evolution. Stichting voor Psychobiologie, Amsterdam, p 130 Kuroda S, Suzuki S, Nishihara T (1996) Preliminary report on predatory behavior and meat sharing in tschego chimpanzees (Pan troglodytes troglodytes) in the Ndoki forest, northern Congo. Primates 37:253–259 Lee RB (1979) The !Kung san: men, women and work in a foraging society. Cambridge University Press, Cambridge Lwanga JS, Struhsaker TT, Struhsaker PJ, Butynski TM, Mitani JC (2011) Primate population dynamics over 32.9 years at Ngogo, Kibale National Park, Uganda. Am J Primatol 73:997–1011 McGrew WC (1983) Animal foods in the diets of wild chimpanzees (Pan troglodytes): why crosscultural variation? J Ethol 1:46–61 McGrew WC (1992) Chimpanzee material culture: implications for human evolution. Cambridge University Press, Cambridge Milton K (1999) A hypothesis to explain the role of meat-eating in human evolution. Evol Anthropol 8:11–21 Mitani JC, Watts DP (1999) Demographic influences on the hunting behavior of chimpanzees. Am J Phys Anthropol 109:439–454 Mitani JC, Watts DP (2001) Why do chimpanzees hunt and share meat? Anim Behav 61:915–924 Mitani JC, Sanders WJ, Lwanga JS, Windfelder TL (2001) Predatory behavior of crowned hawkeagles (Stephanoaetus coronatus) in Kibale National Park, Uganda. Behav Ecol Sociobiol 49:187–195 Mitani JC, Watts DP, Lwanga JS (2002) Ecological and social correlates of chimpanzee party size and composition. In: Boesch C, Hohmann G, Marchant LF (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, New York, pp 102–111 Mitani JC, Watts DP, Amsler SJ (2010) Lethal intergroup aggression leads to territorial expansion in wild chimpanzees. Current Biology 20:R507–R508 Morgan BJ, Suh JN, Abwe EE (2013) Attempted predation by Nigeria-Cameroon chimpanzees (Pan troglodytes ellioti) on Preuss’s red colobus (Procolobus preussi) in the Ebo forest, Cameroon. Folia Primatol 83:329–331 Morris K, Goodall J (1977) Competition for meat between chimpanzees and baboons of the Gombe National Park. Folia Primatol 28:109–121 Page 23 of 27

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Muller MN (2002) Agonistic relations among Kanyawara chimpanzees. In: Boesch C, Hohmann G, Marchant LF (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, Cambridge, pp 112–124 Muller MN, Mpongo E, Stanford CB, Boehm C (1995) A note on scavenging by wild chimpanzees. Folia Primatol 65:43–47 Newton-Fisher NE (1999a) The diet of chimpanzees in the Budongo Forest Reserve, Uganda. Afr J Ecol 37:344–354 Newton-Fisher NE (1999b) Infant killers of Budongo. Folia Primatol 70:167–169 Newton-Fisher N (2004) Data resolution and analysis technique in observational studies of ranging patterns. Folia Primatol 75(S1):312–313 Newton-Fisher NE (2007) Chimpanzee hunting behavior. In: Henke W, Tattersall I (eds) Handbook of paleoanthropology. Springer, New York, pp 1295–1320 Newton-Fisher NE, Notman H, Reynolds V (2002) Hunting of mammalian prey by Budongo forest chimpanzees. Folia Primatol 73:281–283 Nishida T (1968) The social group of wild chimpanzees in the Mahale mountains. Primates 9:167–224 Nishida T, Hosaka K (1996) Coalition strategies among adult male chimpanzees of the Mahale mountains, Tanzania. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 114–134 Nishida T, Uehara S, Nyundo R (1979) Predatory behaviour among wild chimpanzees of the Mahale mountains. Primates 20:1–20 Nishida T, Hasegawa T, Hayaki H, Takahata Y, Uehara S et al (1992) Meat-sharing as a coalition strategy by an alpha male chimpanzee? In: Nishida T, McGrew W, Marler P, Pickford M, de Waal F (eds) Topics in primatology, vol 1, Human origins. Tokyo University Press, Tokyo, pp 159–174 Noe R, Hammerstein P (1995) Biological markets. Trends Ecol Evol 10:336–340 Pruetz JD, Bertolani P (2007) Savanna chimpanzees, Pan troglodytes verus, hunt with tools. Curr Biol 17:412–417 Rose LM (1997) Vertebrate predation and food-sharing in Cebus and Pan. Int J Primatol 18:727–765 Rose LM, Perry S, Panger MA, Jack K, Manson JH, Gros-Louis J, Mackinnon KC, Vogel E (2003) Interspecific interactions between Cebus capucinus and other species: data from three Costa Rican sites. Int J Primatol 24:759–796 Sabater Pi J, Bermejo M, Illera G, Vea JJ (1993) Behavior of bonobos (Pan paniscus) following their capture of monkeys in Zaire. Int J Primatol 4:797–804 Souza LL, Ferrari SF, Pina A (1997) Feeding behaviour and predation of a bat by Saimiri sciureus in a semi-natural Amazonian environment. Folia Primatol 68:194–198 Stanford CB (1996) The hunting ecology of wild chimpanzees: implications for the evolutionary ecology of pliocene hominids. Am Anthropol 98:96–113 Stanford CB (1998) Chimpanzee and red colobus. Harvard University Press, Cambridge, MA Stanford CB (2001) The ape’s gift: meat-eating, meat-sharing, and human evolution. In: de Waal FBM (ed) Tree of origin: what primate behavior can tell us about human social evolution. Harvard University Press, Cambridge, MA, pp 95–117 Stanford CB, Wallis J, Matama H, Goodall J (1994) Patterns of predation by chimpanzees on red colobus monkeys in Gombe National Park, 1982–1991. Am J Phys Anthropol 94:213–228 Stevens JR (2004) The selfish nature of generosity: harassment and food sharing in primates. Proc R Soc Lond Ser B 271:451–456 Page 24 of 27

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Stevens JR, Gilby IC (2004) A conceptual, framework for non kin food sharing: timing and currency of benefits. Anim Behav 67:603–614 Strum SC (1987) Almost human: a journey into the world of baboons. Random House, New York Sugiyama Y (1968) Social organisation of chimpanzees in the Budongo Forest, Uganda. Primates 92:225–258 Sugiyama Y, Koman J (1987) A preliminary list of chimpanzees’ alimentation at Bossou, Guinea. Primates 28:133–147 Takahata Y, Hasegawa T, Nishida T (1984) Chimpanzee predation in the Mahale mountains from August 1979 to May 1982. Int J Primatol 5:213–233 Takenoshita Y (1996) Chimpanzee research in the Ndoki forest. Pan Afr News 3:7–8 Teelen S (2008) Influence of chimpanzee predation on the red colobus population at Ngogo, Kibale National Park, Uganda. Primates 49:41–49 Teleki G (1973) The predatory behaviour of chimpanzees. Bucknell University Press, Lewisburg Tennie C, Gilby IC, Mundry R (2009) The meat-scrap hypothesis: small quantities of meat may promote cooperative hunting in wild chimpanzees (Pan troglodytes). Behav Ecol Sociobiol 63:421–431 Tooby J, DeVore I (1987) The reconstruction of hominid behavioral evolution through strategic modelling. In: Kinzey W (ed) The evolution of human behavior: primate models. State University Press of New York, Albany, pp 183–238 Tutin CEG (1979) Mating patterns and reproductive strategies in a community of wild chimpanzees (Pan troglodytes schweinfurthii). Behav Ecol Sociobiol 6:29–38 Tutin CEG, Fernandez M (1993) Composition of the diet of chimpanzees and comparisons with that of sympatric lowland gorillas in the Lope Reserve, Gabon. Am J Primatol 30:195–211 Uehara S (1997) Predation on mammals by the chimpanzee (Pan troglodytes). Primates 38:193–214 Uehara S, Nishida T, Hamai M, Hasegawa T, Hayaki H, Huffman MA, Kawanaka K, Kobayashi S, Mitani JC, Takahata Y, Takasaki H, Tsukahara T (1992) Characteristics of predation by the chimpanzees in the Mahale Mountains National Park, Tanzania. In: Nishida T, McGrew W, Marler P, Pickford M, de Waal F (eds) Topics in primatology, vol 1, Human origins. Tokyo University Press, Tokyo, pp 141–158 van Lawick-Goodall J (1968) The behaviour of free-living chimpanzees in the Gombe Stream Reserve. Anim Behav Monogr 1:165–311 Wallis J, Lemmon WB (1986) Social behavior and genital swelling in pregnant chimpanzees (Pan troglodytes). Am J Primatol 10:171–183 Washburn S, Lancaster CS (1968) The evolution of hunting. In: Lee R, DeVore I (eds) Man the hunter. Aldine, Chicago, pp 293–303 Watts DP, Amsler SJ (2013) Chimpanzee-red colobus encounter rates show a red colobus population decline associated with predation by chimpanzees at Ngogo. Am J Primatol 75:927–937 Watts DP, Mitani JC (2001) Boundary patrols and intergroup encounters in wild chimpanzees. Behaviour 138:299–327 Watts DP, Mitani JC (2002) Hunting and meat sharing by chimpanzees at Ngogo, Kibale National Park, Uganda. In: Boesch C, Hohmann G, Marchant LF (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, New York, pp 244–255 Williams JM, Liu HY, Pusey AE (2002) Costs and benefits of grouping for female chimpanzees at Gombe. In: Boesch C, Hohmann G, Marchant LF (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, New York, pp 192–203

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Wrangham RW (1977) Feeding behaviour of chimpanzees in Gombe National Park, Tanzania. In: Clutton-Brock TH (ed) Primate ecology. Academic, London, pp 504–538 Wrangham RW (1975) The behavioural ecology of chimpanzees in the Gombe National Park, Tanzania. PhD thesis, Cambridge University Wrangham R (2002) The cost of sexual attraction: is there a trade-off in female Pan between sex appeal and received coercion? In In: Boesch C, Hohmann G, Marchant LF (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, New York. pp. 204–215 Wrangham RW, van Zinnicq Bergmann Riss E (1990) Rates of predation on mammals by Gombe chimpanzees, 1972–1975. Primates 31:157–170 Wrangham RW, Chapman CA, Clark-Arcadi AP, Isabirye-Basuta G (1996) Social ecology of Kanyawara chimpanzees: implications for understanding the costs of great apes groups. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 45–57

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Index Terms: Begging 14 Bonobos 20 Chimpanzee 1–2, 10 Collaborative hunting 11 Cooperation 11 Hunting to assess reliability 17 Hunting 1 Hunting-to-display-social-prowess 18 Male social bonding 18 Male-social-bonding 17 Marginal gains 19 Meat eating 12 Meat-for-allies 18 Meat-for-sex 16 Meat-scrap 15, 19 Nutritional-shortfall 15 Predation pressure 7 Prey diversity 2 Scavenging 12 Sex bias, hunting 6 Trade goods 16

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Cooperation, Coalition, and Alliances Charlotte K. Hemelrijka*, Ivan Puga-Gonzalezb and Jutta Steinhauserc a Behavioural Ecology and Self-organization, Centre for Ecological and Evolutionary Studies, University of Groningen, Groningen, The Netherlands b Behavioural Ecology and Self-organization, Centre for Ecological and Evolutionary Studies, University of Groningen, Groningen, CC, The Netherlands c Behavioural Ecology and Self-organization, Centre for Ecological and Evolutionary Studies, University of Groningen, Groningen, The Netherlands

Abstract In primates, cooperative acts have been observed such as communal rearing of offspring, cooperative mobbing of predators, supporting others in fights, and grooming others. Grooming builds up a social bond between the partners, helps in repairing relationships, and produces all kinds of benefits for the groomee, such as the reduction of parasites and of tension. Although the costs for the groomer are low, it has been regarded as an altruistic act and therefore is expected to be preferably directed toward kin or to be repaid by being reciprocated or exchanged for another service (e.g., support in fights, help in rearing offspring in the case of communal breeding systems, or access to some object, such as food, or some individual such as a female, an infant, or members of another group). The formation of coalitions may result in the maintenance or in the increase of the dominance of an individual, in the expulsion of certain individuals from a group, in taking over a group, in the defense of the home range against other groups, in getting access to estrous females, and in the protection of an infant or adult female. The degree of cognition involved in coalitions is unclear. Which members of a group cooperate differs from species to species; it may be influenced by genetic and social relationships, by the size and the composition of the group (the sex ratio), by the degree of competition, and by the distribution of food.

Introduction Cooperation in primates varies greatly among members of a group. For instance, individuals groom the fur of others, help others in fights, collect food together (for communal hunting in chimpanzees, see volume 2 Chapter 14), share food, and may help in raising the offspring of others. Furthermore, group members cooperate against danger from the outside. They mob predators together and form coalitions to defend their home range against other groups. For a long time, behavioral acts such as coalition formation, grooming, and food sharing have been regarded as “altruistic” (costing the actor more than it receives), and therefore, the main explanations have been the theories of kin selection (Hamilton 1964) and reciprocal altruism *Email: [email protected] Page 1 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_43-4 # Springer-Verlag Berlin Heidelberg 2013

(Trivers 1971). However, it has become increasingly clear that these supposedly altruistic acts are beneficial for both cooperation partners. For instance, grooming not only reduces tension in the receiver but also in the performer (Shutt et al. 2007), and grooming a high-ranking individual serves as a protection against aggression for the subordinate. Coalition partners may increase their access to fertile females or help maintain their status quo within the dominance hierarchy. Furthermore, whereas coalitions were originally supposed to require high cognitive abilities, it is increasingly acknowledged that these patterns may arise from simple behavioral rules (as for cognitive mechanisms, see also volume 2 Chapter 17). Besides, cooperation depends on the social system and the kind of primate involved (such as Old World monkeys vs. New World monkeys). We will treat these aspects below.

Social System Cooperation among individuals of a group depends on the species and its social system. There are many species of primates, and they live in many different kinds of social systems, as solitary individuals, monogamous pairs, single-male groups, multimale groups, or fission-fusion systems (Chapter 12). In group-living species with many females, the males usually migrate and the females remain in their natal group for life (female-philopatry), e.g., baboons, macaques, and vervets. Wrangham (1980) refers to these species as “female-bonded,” because the females are more kin related than the males. In such groups, female social relationships and cooperation are developed much further than among the males of the group and also further than among females of species that are not female-bonded, the so-called female-transfer species. In line with this, grooming reciprocation among individuals of the resident sex is higher than among those of the sex that transfer (Hemelrijk and Luteijn 1998). In chimpanzees, for instance, males stay together and females migrate. Here, relationships among males are more cooperative than among females (male bonded). Greater cooperation among the resident than the migrating sex has been attributed to the closer relatedness of the resident sex. Evidence for closer relatedness in the resident sex is found among macaques (Ruiter 1998) and chimpanzees (Goldberg and Wrangham 1997). Although it has also been argued that male chimpanzees that cooperate are more often more closely related than those that do not, this is not supported by evidence from DNA-typing methods (Goldberg and Wrangham 1997; Langergraber et al. 2007). Furthermore, social relationships differ between Old World monkeys and New World monkeys: among Old World monkeys, they are more developed (Dunbar 1993). The causes of these differences are unknown.

Grooming Grooming occurs in all primate species (Goosen 1987), and of all affiliative social acts, it is the one that is displayed most frequently. It consists in picking through the fur to remove parasites and to clean small injuries. An individual may clean its own fur (autogrooming) or that of another (allogrooming). Because allogrooming is a social act, it has sometimes been questioned whether it has any cleaning function at all. That allogrooming actually aims at cleaning is shown by Zamma (2002): Japanese macaques groom more often those spots of others and of themselves that tend to house more lice and eggs. Furthermore, in his study of 17 spots on the bodies of 19 species of primates, Barton (1985) has shown that individuals groom others particularly at spots that they themselves cannot easily reach. Therefore, spots on the skin that are groomed more often by others are groomed less often by the individual itself and vice versa.

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Since in species that live in larger groups, individuals spend more time grooming, grooming clearly also has a social function (Dunbar 1991, 2003). Note that this correlation with group size appears more clearly among Old World monkeys than among New World monkeys. This may arise because coalition formation is more important in Old World monkeys and grooming may be helpful in building up alliances. In line with this, it has been found that individuals groom more often those partners they also support more frequently. This has been observed in several species such as female chimpanzees (Hemelrijk and Ek 1991), male chimpanzees (Watts 2002), gorillas (Watts 1997), baboons (Seyfarth 1976; Smuts 1985b), female vervet monkeys (Seyfarth 1980), and several species of macaques (Hemelrijk 1994; Kapsalis and Berman 1996; Schino et al. 2007; Silk 1992b; Ventura et al. 2006). Grooming relationships among males of the genus Macaca (Hill 1994) and among females of a number of female-bonded species (Hemelrijk and Luteijn 1998) are influenced by the identity of the migrating sex and by the composition of the group, namely, the sex ratio. As to the sex ratio, it has been shown that food provisioning led to a female-biased sex ratio in a number of groups of species of the genus Macaca (Hill 1994, 1999). This arose because provisioned food was offered in clumps and thus led to stronger competition, and this drove several males away. Groups that were not provisioned had a more equal sex ratio, because in these groups, competition for concentrated food sources was less. This may have allowed males to be friendlier among themselves and groom each other more often. Further, in the case of an even sex ratio, more grooming among males may arise because the number of males to be groomed is greater and the number of females to groom with is smaller than in groups with a female-biased sex ratio. This results in a higher number of potential male partners to affiliate with and therefore more affiliation among males. Among females, grooming relationships seem to be influenced by competition for access to males. In a large comparative study of female-bonded species of primates, Hemelrijk and Luteijn (1998) discovered that the degree of reciprocation of grooming among females increased with the increase in the relative number of adult males in the group. This was attributed to female competition for access to males; the lower the number of males present, the stronger the competition among females to affiliate with males. This competition hindered females from building up good relationships among themselves. This argument is supported by the fact that grooming reciprocation increases more strongly with sex ratio among females in a single-male group (where sex ratio depends on group size) than in a multimale group. Even if the number of males increases in multimale groups, this increase is not entirely to the profit of the time the males have available for females. There are two reasons for this: first, because males will intervene in interactions of other males with females and second, because males will interact among themselves, which reduces the time available for positive social interaction with females. In single-male groups, however, interactions and interventions among males are lacking. The positive effect of grooming on relationships is supposed to be a reduction of tension, increase of trust, and restoration of the relationship after a fight. As regards tension, grooming calms and relaxes the groomee and the groomer (Terry 1970; Goosen 1975; Shutt et al. 2007). In the groomee, the heartbeat slows down (Boccia et al. 1989) and the rate at which it shows a displacement behavior, such as scratching, decreases (Schino et al. 1988). Keverne and coauthors (1989) have shown that being groomed is pleasurable because it increases the concentration of endorphins in the brain. Grooming is supposed to maintain relationships in the light of competition, because hamadryas females with an established relationship are observed to groom each other more often if a dyad is accompanied by others than if the dyad is temporarily separated in cages (Stammbach and Kummer 1982). Furthermore, grooming is also supposed to restore a relationship: often after fights, the frequency of grooming and other affiliative behavioral acts between former Page 3 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_43-4 # Springer-Verlag Berlin Heidelberg 2013

opponents is higher than when no fights take place. This is known as “reconciliation” and has been shown to occur in species of all major radiations of primates (Aureli et al. 2002; Silk 2002). Being attacked implies that there is a high chance that more aggression will follow. Friendly postconflict reunions reduce this aggression and restore the relationship. This function appears from the elegant experiments by Cords (1992). She determined at what distance pairs of long-tailed macaques could drink next to each other without trouble. Then she showed that after aggression among the members of a pair, its ability to jointly exploit the resource was seriously reduced. If, however, after such a conflict, a friendly reunion took place, the use of the resource was completely restored to normal. Relationships are, however, not always damaged by aggression; the damage depends on the context in which the aggression takes place. In the case of competition over food, the relationship keeps its status quo even without reconciliation. Furthermore, the occurrence of reconciliation depends on the value of the relationship. According to the “valuable relationship hypothesis,” reconciliation particularly occurs in relationships of great value (Aureli et al. 2002; Silk 2002). This theory is supported by the following experiment by Cords and Thurnheer (1993): when macaque partners are obliged to cooperate with each other to obtain food, they reconcile three times more often than when cooperation is not necessary. In line with this, reconciliation has been shown to occur more often in those relationships that are characterized by a high frequency of support (such as in macaques among members of a matriline; and in gorillas reconciliation occurs in the cooperative relationship between the sexes rather than among females (Watts 1995a, b)). Further, in general, more friendly postconflict reunion occurs among those individuals that exchange high levels of friendly behavior. As to the cognition used in displaying reconciliation, there is debate. According to de Waal and Yoshihara (1983), the cognitive capacities needed are memory of the former opponent and conciliatory predisposition. On the other hand, the cognitive requirements must be slight because juveniles already reconcile in the same way as adults do (Aureli et al. 2002). No cognition specific for reconciliation is required however according to an individual-based model concerned with individuals that group, groom, and fight (GrooFiWorld, see Puga-Gonzalez et al. 2009). According to this spatially explicit model, statistically “reconciliation” is observed, because former opponents are closer after a fight than they are on average otherwise. Consequently, former opponents have more opportunities to groom each other after a fight than otherwise. Since individuals are more likely to groom partners that are close by and to groom others when they themselves feel stressed (which individuals do after a fight), this results in behavior which primatologists have labeled reconciliation. Thus, empirical studies should control for effects of proximity. Indeed in the few empirical studies that controlled to some degree for proximity, the rate of reconciliation was significantly reduced (Call 1999; Call et al. 1999; Majolo et al. 2009; Matsumura 1996). Another reason to take the need for further control of proximity seriously is that the model GrooFiWorld also shows that the reconciliation-like behavior happens, like in empirical data, more often among “valuable relationships.” Yet, individuals in the model are not aware of who their friends are. Further, like in empirical data, reconciliation-like behavior in the model is more frequent in egalitarian than in despotic societies. In the model, this is a side effect of the relative rate of grooming versus fighting which is higher in egalitarian than in despotic societies; in empirical data, it was supposed to be caused by a greater uncertainty about dominance relationships in egalitarian societies. Further, it has been shown that the frequency and stability of grooming relationships over time have a positive impact on the fitness of the individual. For instance, in a population of wild baboons studied over 15 years, Silk and coauthors (Silk et al. 2010, 2003, 2009) show that strong social bonds among females increase their life span and that of their offspring. This effect was Page 4 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_43-4 # Springer-Verlag Berlin Heidelberg 2013

independent of dominance rank and environmental conditions. Similarly, in a study of wild Assamese macaques, the strength of the social bonds among males appeared to be directly and positively related to the number of offspring they sired (Schuelke et al. 2010). Grooming: Kin Selection, Reciprocation, and Exchange Grooming does not only lead to social bonding but may also be considered an altruistic trait because of the costs to the actor and the advantage for the receiver. Although its cost (expenditure of energy) is low (Wilkinson 1988), grooming may cost time that might be used for (a) vigilance and (b) foraging. Two studies report a decrease in vigilance, one among captive rhesus monkeys and the other among wild blue monkeys. In rhesus macaques, mothers become less vigilant during grooming, and consequently their infants were more often harassed by group members (Maestripieri 1993). Blue monkeys became significantly less watchful of predators when grooming than when foraging or resting (Cords 1995). Grooming does not diminish time for foraging (Dunbar and Sharman 1984): in two species of baboons (olive baboons and gelada baboons), increased foraging time was associated with a decrease in the length of time spent resting, but time spent grooming remained the same. This may be an indication of the importance of grooming. Indeed, baboons and macaques devote up to 20 % of their time to grooming others (Dunbar 1988). Within the framework of grooming as an altruistic act, the distribution of grooming partners can be explained either by the theory of kin preference (Hamilton 1964) or by reciprocal altruism (Trivers 1971). In support of kin selection, the most intense grooming bonds are found between mother and offspring, and in general in most primates, individuals aim their grooming primarily at their kin (Gouzoules and Gouzoules 1987; Schino 2001). When altruistic acts are directed toward unrelated individuals, the expectation is that something should be received in return (Trivers 1971). Recent models suggest that parceling of grooming bouts in small periods, in which the role of actor and receiver alternates, is a method of achieving reciprocation (Connor 1995). During a certain part of their grooming bouts – ranging from 5–7 % for M. radiata (Manson et al. 2004) to 74 % in Callithrix jacchus (Lazaro-Perea et al. 2004) – partners groom each other alternately. In grooming bouts of female chacma baboons, where both partners groom each other in turn, the total grooming duration by both partners is indeed significantly correlated between bouts (Barrett et al. 1999, 2000). Similar findings were made in white-faced capuchin monkeys and bonnet macaques (Manson et al. 2004) but not in Japanese macaques (Schino et al. 2003). Furthermore, it was argued that the time during which an individual grooms another should increase as a sign of the increasing trust among partners (model of “raise the stakes,” Roberts and Sherratt 1998). Increasing bout lengths have not, however, been confirmed in empirical studies of either capuchin monkeys or baboons (white-faced capuchins, Manson et al. 2004; chacma baboons, Barrett et al. 2000). Instead in chacma baboons, bout length even decreased over time. Grooming may either be reciprocated for its own sake or interchanged for another service, e.g., support, reduction of aggression, or access to something or someone (such as food, a female, an infant, or another group) or support in rearing offspring (in communal breeding systems). Here, a major problem is how to define reciprocation operationally. Reciprocation and interchange may be considered as a correlation between the number of times each individual gives something to a partner and how often it receives this service from him/her in return. This summed value over a period of time may be studied at the group level, the so-called actor-receiver model (Hemelrijk 1990a, b). Reciprocation in grooming occurs in many species, for instance, among both males and females in chimpanzees in captivity (Hemelrijk and Ek 1991) and among male chimpanzees under natural conditions (Watts 2000a), among female Samango monkeys (Payne et al. 2003), blue Page 5 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_43-4 # Springer-Verlag Berlin Heidelberg 2013

monkeys (Rowell et al. 1991), baboons (Seyfarth 1976), marmosets (Lazaro-Perea et al. 2004), female Japanese macaques (Schino et al. 2003), and gorillas (Watts 1994). Such a correlation of reciprocation may, of course, occur as a side effect of other correlations. For instance, when higherranking individuals groom others more often and when everyone grooms others more often according to the rank of the partner, grooming reciprocation follows automatically (Hemelrijk 1990b). To exclude such alternative explanations, partial matrix correlations are useful (Hemelrijk 1990a). Both in chimpanzee males and females (Hemelrijk and Ek 1991; Watts 2002) and in savannah baboons (Seyfarth 1976; Hemelrijk 1991), grooming reciprocation remained significant even after partialling out the effect of other variables such as dominance and support. In other studies, grooming reciprocation was present while controlling for kinship (hamadryas baboons, Stammbach 1978; vervet monkeys, Fairbanks 1980; Japanese macaques, Muroyama 1991). Only in a few studies no reciprocation of grooming was observed (bonobos, Franz 1999). Recently, reciprocation of grooming among female primates was confirmed in a meta-analysis of 48 groups of 22 species. Results remained significant even after controlling for kinship (Schino and Aureli 2008a). Apart from being reciprocated, grooming may also be exchanged for other services. For instance, Seyfarth (1977) argues that higher-ranking females are more attractive to groom because from them more effective support in fights can be expected in return. Since females will compete to groom the highest-ranking partners, and since higher-ranking females will win this competition, each female will in the end groom most frequently with those partners adjacent in rank and be groomed most often by those ranking just below her. Seyfarth used this model to explain the observation that in several female-bonded primate species, such as baboons (Seyfarth 1976), vervets (Fairbanks 1980), and stump-tailed macaques (Estrada et al. 1977), females aimed at grooming up the hierarchy and mainly at those that were next in hierarchy (Seyfarth 1980). Since then, these patterns have statistically been studied in many species. In a number of them, particularly Old World monkeys (such as certain species of macaques, e.g., rhesus monkeys (Kapsalis and Berman 1996), chimpanzees (Hemelrijk and Ek 1991; Watts 2000b), and bonobos (Franz 1999; Vervaecke et al. 2000)), these patterns were, at least partly, confirmed, but in others evidence is lacking, for instance, in female langurs (Borries et al. 1994), in blue monkeys (Cords 2000, 2002), and in New World monkeys, such as wedge-capped capuchins, Cebus olivaceus (O’Brien 1993), and tufted capuchins, Cebus apella, in both wild (Di Bitetti 1997) and captive colonies (Parr et al. 1997; Schino et al. 2009), but not always (see Tiddi et al. 2012). There was even a trend against grooming higher-ranking animals because individuals groomed down the hierarchy among capuchins and in callitrichids (Lazaro-Perea et al. 2004). In callitrichids, this is suggested to have a function in the communal breeding system: the breeding female (i.e., the alpha-female) uses grooming to make lower-ranking individuals stay in her group in order to help her bring up her young. Furthermore, the relation between grooming and the receipt of support is doubted. Although correlations were found in studies of several species, such as vervets (Seyfarth 1980), baboons (Seyfarth 1976; Hemelrijk 1990a), female chimpanzees (Hemelrijk and Ek 1991), male chimpanzees (Watts 2002), bonobos (Vervaecke et al. 2000), capuchins (O’Brien 1993), and one group of bonnet macaques (Silk 1992a), they were lacking in an earlier study of the same group of bonnet macaques (Silk 1982), in rhesus macaques (de Waal and Luttrell 1986), and female baboons (Silk et al. 2004). The relation is supported by two experimental studies dealing with vervets and longtailed macaques. Seyfarth and Cheney (1984) recorded a call of vervets that seems to solicit support from others. They played it back to individuals of a natural colony of vervets that had recently been groomed by the caller and to others that had not. The length of time individuals looked up at the Page 6 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_43-4 # Springer-Verlag Berlin Heidelberg 2013

speaker was considered to be an indication of the tendency to support the caller. Among nonrelatives, individuals looked at the speaker longer when the caller had recently groomed them. In this experiment, it remains uncertain, however, whether looking up at the speaker actually indicates a readiness to support him or her. Therefore, in an experiment with long-tailed macaques (Hemelrijk 1994), actual support was measured directly. Trios of females were separated from the group. After two high-ranking individuals had been given the opportunity to groom, a fight was provoked between one of them and a low-ranking female. The frequency with which the third highranking female intervened in the fight was counted. The third female appeared to support only the other high-ranking female, and she did so more often after she had been groomed by her than if not. This supports the notion of a relationship between being groomed and supporting. It is not definitive evidence for an exchange, however, because being groomed may increase the tendency to support in general, even on behalf of those by whom the supporter was not groomed at all. Furthermore, individuals appear to support the aggressor but not the victim; therefore, it is as yet unknown whether a similar association with grooming holds also for victim support (which is more risky). Besides, these experiments do not show whether varying amounts of grooming lead to varying amounts of support. A recent meta-analysis of grooming and support based on 36 studies from 14 species of primates, Schino (2007) states that pairs of females that groomed each other preferentially also supported each other more. However, in this study, it was not specified whether grooming was given or received, and thus it is not clear whether an actual positive correlation for the exchange between grooming and support exists at all in their data. Henzi and Barrett (1999) suggest that the receipt of support is not the major benefit of grooming because grooming occurs also among females that do not support at all, for instance, in certain groups of chacma baboons (in the Drakensberg). Instead, they argue that the short-term benefit of grooming is the decrease risk of aggression and harassment from others during the grooming bout itself (as suggested for bonnet macaques (Silk 1982) and capuchin monkeys (O’Brien 1993)), because support is rare in female-bonded species, although those females groom each other. Further, Henzi and Barrett (1999) argue that the degree to which grooming should be reciprocated or exchanged for something else depends on the competitive regime; when resources are widely distributed and cannot be monopolized, competition is weak, individuals equal each other in power, and grooming should be reciprocated. If resources can be monopolized, however, competition is intense, power differences are great, and grooming should be exchanged for increased access to resources. In line with this, in a comparison between groups and in a study of the changes in the same group over time, grooming appears to be reciprocated if competition is weak rather than intense (Barrett et al. 1999, 2002). Similarly, in a meta-analysis (Schino and Aureli 2008b) and in an individual-based model (Puga-Gonzalez et al. 2009), grooming reciprocation becomes weaker when the dominance hierarchy is steeper (thus competition is stronger). For this, different cognitive explanations are given. Schino and Aureli (2008b) argue that individual primates adjust their distribution of grooming depending on their competitive regime. According to the computational model, GrooFiWorld model (Puga-Gonzalez et al. 2009), reciprocation of grooming is directly influenced by the asymmetry of risks of losing a fight from an opponent. Here, reciprocation of grooming decreases if the hierarchy is steeper because high-ranking individuals experience less risk in attacking the lower-ranking ones, and therefore, they are more likely to attack them than to groom them, whereas for the lower-ranking ones, the opposite holds. Conversely, if the hierarchy is weaker, risk asymmetries are smaller and individuals are more similar in their tendency to attack and groom each other. A third explanation for the decrease of reciprocation of grooming when competition is more intense is found in the fact that intense competition is associated with a sex ratio that is more skewed toward adult females. Weaker grooming reciprocation in groups with Page 7 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_43-4 # Springer-Verlag Berlin Heidelberg 2013

more females has been discovered in several primate species by Hemelrijk and Luteijn (1998) and is attributed to stronger competition among females for access to males. Note that differences in degree of competition for access to males may also explain the pattern of grooming reciprocation in the baboons studied by Barrett and coworkers. Grooming is also supposed to be exchanged for access to food. The best evidence for this comes from two experiments, one with long-tailed macaques by Stammbach (1988) and the other with vervet monkeys by Fruteau et al. (2009). In both studies, authors trained individual members of a group to become experts in operating a food apparatus. During the period in which it was the expert, this individual appeared to be groomed significantly more often. Note that “food sharing” in primates almost exclusively means passive tolerance toward others when others take away a bit of food and that active giving is extremely rare (McGrew 1992). In a food exchange experiment among captive chimpanzees, de Waal (1997) found some evidence that females allow others to take away food more easily if they have been groomed by them in the preceding 2 h than if not. Food sharing and its reciprocation seems, however, largely a matter of mutual tolerance rather than intentional reciprocation, as is shown in experiments with brown capuchin monkeys (Waal 2000). If males groom females, this is further supposed to increase a male’s access to mating partners and thus reproductive success, for instance, in chimpanzees, baboons, and rhesus monkeys. In chimpanzees, this has been regarded as a kind of “bargaining for sex” (Goodall 1986). For instance, Gumert (2007) shows that male long-tailed macaques groomed preferentially those females with whom they mated more. Similarly, chimpanzee males groomed more often those females with whom they mated more frequently mainly during the period of female tumescence; this relation, however, resulted neither in a long-term bond (Hemelrijk et al. 1992) nor led to more offspring from the females that were groomed more often by the male (Hemelrijk et al. 1999; Meier et al. 2000). Hence, male grooming of females may simply function to calm down the male’s aggressive tendency or the tendency of the female partner to flee, and therefore, it need not be considered as a kind of exchange or currency. Furthermore, male rhesus monkeys mainly groom females during the mating season, and captive females prefer males who groom them most (Michael et al. 1978); yet, there are no long-term reciprocal bonds between the sexes (Maestripieri 2000). Long-term sociopositive relationships between males and females have been described, however, for savannah baboons (Seyfarth 1978a, b; Smuts 1985b; Palombit et al. 2000). In several species, grooming and embraces are used to get access to newborn infants, e.g., in baboons (Rowell 1968; Frank and Silk 2009), patas monkeys (Muroyama 1994), moor macaques (Matsumura 1997), sooty mangabeys and vervet monkeys (Fruteau et al. 2011), and spider monkeys (Slater et al. 2007). Furthermore, if low-ranking female chacma baboons want access to a newborn from a higher-ranking mother, they need to groom the mother longer in proportion to the size of the difference in rank (Henzi and Barrett 2002).

Coalition Formation Here we deal only with those coalitions that are targeted at other group members and not at other groups (for coalitions against other groups, see section “Collective Defense of Home Ranges”). A coalition (or alliance) is a coordinated attack by two or more individuals (the coalition partners or allies) on one or more opponents, the so-called targets (Chapais 1995). Coalitions may start in several ways: two individuals may attack a common victim, a coalition partner may spontaneously Page 8 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_43-4 # Springer-Verlag Berlin Heidelberg 2013

participate in an ongoing fight, or it may join after being enlisted by one of the combatants. Several types of coalitions are distinguished on the basis of their form and their effect (Chapais 1995; van Schaik et al. 2004). As regards form, the distinction is between coalitions of members (a) that rank above the target (called “all-down”), (b) that rank below the target (called “all-up”), or (c) of which one ranks above the target and another below it (called “bridging” coalitions or alliances). As regards effects, a distinction is made between (a) alliances that reinforce the existing rank order and therefore are “conservative”; (b) coalitions that cause one individual to change rank and thus are “rank changing”; or (c) coalitions that cause more individuals to change rank, e.g., when two lowerranking individuals defeat a top male, and thus are “revolutionary.” Coalitions usually involve three individuals (a triad), but more individuals may participate (a polyad). As regards the cognition involved in the formation of coalitions, opinions differ. Harcourt (1988) suggests that primates form coalitions for strategic reasons and that they must take into account a complex set of information about their own power and that of their allies in comparison to that of their opponent and allies. For instance, when recruiting support, an individual should not only be aware of the social relationships between itself and other individuals but also of the relationships among the other individuals, so-called triadic awareness (Harcourt and de Waal 1992; Paxton et al. 2010; Schino et al. 2006; Silk 1999). Along these lines, in a comparative study between a captive group of long-tailed macaques and one of chimpanzees, coalitions of chimpanzees appeared to be more frequent and larger than those of macaques, and this was considered as an indication of their greater cognition (de Waal and Harcourt 1992). Others argue, however, that coalition behavior may develop with little planning and anticipation of the results because individuals may passively learn to recognize the advantage of joining forces (Chapais 1995). Along similar lines, the pattern of coalitions in sooty mangabeys and Barbary macaques may result from simple behavioral rules such as “support the higher-ranking individual in a conflict,” “solicit support from potential allies that outrank yourself and the target,” and “choose the strongest partner at hand” (Range and Noe 2005; Bissonnette et al. 2009). The simplest cognition involved in coalitions is given in a modeling study of individuals that group and attack each other diadically (Hemelrijk and Puga-Gonzalez 2012). Here incidental coalitions were observed following the empirical definition of coalitions, namely, that after a fight between two individuals, a third nearby individual attacked one of the former opponents. Remarkably, these incidental coalitions are of the three different types (i.e., conservative, bridging, and revolutionary) with a frequency of occurrence similar to that in empirical data. During fights, individuals may display so-called enlisting behavior by which they seem to try to attract others into the fight. This may consist of a rapid movement of the head between the opponent and the individual from whom help is requested, called “headflagging” and “pointing” (de Waal et al. 1976; Noe¨ 1992; Silk 1999). Male bonnet macaques recruit support via “headflagging” with a success rate of 24 % (Silk 1999). In chimpanzees, several behavioral actions are shown by fighting animals to a third individual that is not (yet) involved in the fight, and these are indicated as “side-directed behavior” (de Waal and van Hooff 1981). One action is the so-called “hold-outhand” gesture in which an individual stretches out its hand toward a potential helper (de Waal and van Hooff 1981). The effectiveness of such solicitation behavior in chimpanzees is unclear. In contrast to the positive results by de Waal and van Hooff (1981), in another study of the same colony by Hemelrijk et al. (1991), most support was obtained without preceding side-directed behavior, and it was clear that side-directed behavior was not a precondition for acquiring help in fights. Besides, side-directed behavior was rarely followed by support, and there was no indication that it increased the chance of receiving help. Note that also if the analysis was confined to cases of hold-out-hand behavior, hold-out-hand appeared not to result in obtaining support. This is in line Page 9 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_43-4 # Springer-Verlag Berlin Heidelberg 2013

with the experimental observations of chimpanzees by Hare and coauthors (2004): they discovered that chimpanzees are unable to understand pointing toward an object (Tomasello et al. 1997) but that chimpanzees easily anticipate the stretching arms of those who want to take away something that is of interest to them. Thus, it appears that they are better equipped to compete than to cooperate. Side-directed behavior is mostly displayed by females when they are threatened and is significantly concentrated on higher-ranking individuals; thus, side-directed behavior may be beneficial to the soliciting individuals in the sense that it tends to bring them nearer to a highranking individual, which may have a protective effect as a threat to the original opponents (Hemelrijk et al. 1991). In interventions in fights, it is usually the aggressor and the winner of the fight that is supported. This is less risky than supporting the victim. Notable exceptions are mothers supporting their offspring (see section “Youngsters”) and the “control role” of the alpha-male. For instance, in a captive colony of Japanese macaques (Watanabe 1979), the alpha-male more often than other males supports aggressees, in particular babies and youngsters, against adults. This is called a “control role.” A similar control role in the form of supporting losers is described for the alpha-male in gorilla groups by Watts (1997). Here, males intervene in fights among females. Because this may promote egalitarianism among females, the male may use it to keep females in his group. Male intervention hinders, however, the formation of alliances among females.

Functions of Coalition As regards their function, Smuts (1987) distinguishes a number of main types of coalitions: 1. Coalitions to take over a single-male group: This has been reported for males of gray langurs (Hrdy 1977). 2. Coalitions among males to get access to an estrous female that is in consort with another male: These coalitions do not affect dominance relationship and are common in savannah baboons (Smuts 1985a). Coalition partners are typically of middle rank (Noe and Sluijter 1995). Packer (1977) found that the male that enlisted help from another was the one to obtain the female, but in a later study, Bercovitch (1988) showed that males that were solicited were as likely to obtain the female as those that solicited, and Noe¨ (1992) himself observed that both partners of a coalition may enlist each other’s help simultaneously. 3. Coalitions to repel outside males: This has been reported among females as well as among males. Coalitions among males occur between groups of species living in single-male groups such as gorillas, hamadryas baboons, and gelada baboons. Coalitions among males of a single group have been described in multimale groups of chimpanzees, red colobus monkeys, spider monkeys, white-faced capuchin monkeys, and sometimes also among savannah baboons. In chimpanzees (Wrangham 1999; Wilson and Wrangham 2003) and white-faced capuchin monkeys (Gros-Louis et al. 2003), male coalitions may even result in killing an adult of another group. 4. Coalitions among females or between a male and a female to protect infants: Although the main protectors of youngsters are their mothers, in all species virtually all group members will defend an infant if it is in danger (for instance, against an attack by an adult male), and female baboons are even suggested to maintain close associations with particular males in order to be protected against aggression from males (Palombit et al. 2000, 1997). 5. Coalitions among females to protect an adult female against an attack by a male: Mobbing a male to protect a female may be useful for females (even unrelated ones) since it warns males that hostility to females is risky. Page 10 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_43-4 # Springer-Verlag Berlin Heidelberg 2013

6. Coalitions to increase the dominance position of one or both member(s): Here, we will treat results for youngsters and for adults separately.

Adults Coalitions to increase the dominance position among adults have been reported for Japanese macaques, rhesus, Barbary macaques, stump-tailed macaques, mantled howlers, red howlers, chimpanzees, and gray langurs. When females are observed to attack males together, they are assumed to increase their dominance over males. This is mentioned for Japanese monkeys, rhesus monkeys, and bonobos (Chapais 1981; Thierry 1990; Parish 1994), and indeed in these species, certain females are dominant over certain males. Such coalitions may not be a precondition for female dominance, however, because a spatial model of individuals that group and compete (via dominance interactions) shows that female dominance can also arise only from competitive interactions in the absence of coalitions (Hemelrijk et al. 2003, 2008). According to this model, the stronger female dominance in bonobos compared to common chimpanzees may be due to their greater cohesion in grouping. Furthermore, stronger female dominance among rhesus macaques as compared to Celebes macaques (Thierry 1990) may arise from their higher intensity of aggression. Besides, also a higher percentage of males in the group increases intensity of aggression on average in the group and, herewith, female dominance relative to males. Both factors, cohesion and intensity of aggression, increase hierarchical differentiation; and this reduces the size of the initial difference in dominance between the sexes (Hemelrijk et al. 2003, 2008). When males support females, males usually benefit in terms of dominance. For instance, in Japanese macaques, an alpha-male supported females of lower-ranking matrilines against the alpha-female with whom he had an unstable dominance relationship. Similarly, in rhesus monkeys and chimpanzees, females supported the alpha-male against other males, and in vervets support by females influenced dominance relations among males (Chapais 1995). Among the three top-ranking males in chimpanzees, coalitions may induce changes of dominance in several ways. For instance, among wild chimpanzees, a top-ranking alpha-male (A) had an unstable relationship with the stronger beta (B). When the gamma-male (C) supported the alpha against the beta, (C) rose in rank above (B) (Nishida 1983). One-and-a-half years later, however, support by the now gamma-male to the alpha-male caused them (B and C) to reverse dominance again (Uehara et al. 1994). Thus, the gamma-male played out the alpha-male against the beta-male and this happened also in captivity (de Waal 1982). In captivity, at other times, the beta-male and gamma-male were observed to join against the alpha-male (a revolutionary alliance). Thus, both rose in rank above the alpha-male (de Waal 1982). Such competition among males has sometimes fatal consequences (Watts 2004). Revolutionary alliances have further been described for male langurs, Barbary macaques, and rhesus macaques (Chapais 1995; Higham and Maestripieri 2010; Bissonnette et al. 2011). However, in none of these species did males form coalitions to obtain estrous females. Youngsters In a number of female-bonded species (Wrangham 1980), there is also a complex support system that provides young females with approximately the dominance rank of the mother. It has been called a “matrilineal dominance system” and a “nepotistic hierarchy,” because the support involves kin. The nepotistic hierarchy implies that all daughters rank immediately below their mother and that among sisters the youngest sister has the highest rank (so-called youngest ascendancy). This Page 11 of 27

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_43-4 # Springer-Verlag Berlin Heidelberg 2013

classical form of a nepotistic dominance hierarchy is found in rhesus macaques, Japanese macaques, and long-tailed macaques. The formation of hierarchies between matrilines has been investigated in a series of admirable experimental studies of Japanese and long-tailed macaques by Chapais and coworkers (Chapais 1995, 1996; Chapais et al. 2001; Chapais and Gauthier 2004). They created subgroups of three or six juvenile Japanese macaques (with one or two peers of the same matriline) and then added an adult. In this situation, a low-ranking juvenile female appeared to be able to outrank peers in the presence of closely related females but not in the presence of more distantly related kin, such as aunts, grandaunts, or cousins, due to lack of support from them. After female dominance over a lower-ranking matriline was “assigned,” it was maintained by mutual support among members of the same matriline against those of a lower matriline: from that time onward, the young females joined opportunistically in ongoing conflicts against lower-ranking females (called “the common targeting principle”). Within matrilines, younger sisters become dominant over older ones, the so-called “youngest ascendancy” rule. This is caused by the mother’s support of a younger daughter against her older ones. If the mother is absent, dominant unrelated individuals will also support younger sisters against older ones. Thus, the network of alliances of females extends beyond her kin. However, in some groups, the matrilineal dominance system is incomplete (weakly nepotistic) (Chapais 2004). For instance, youngest ascendancy is lacking in some feral groups of Japanese macaques (Hill and Okayasu 1995), provisioned groups of Barbary macaques (Prud’homme and Chapais 1993), and one captive group of Tonkean macaques (Thierry 2000). Furthermore, in baboons, daughters may outrank their mother during adulthood (Combes and Altmann 2001). Chapais and Lecomte (1995) give three explanations of weak nepotism: demographic, (phylo)genetic, and ecological. The demographic explanation comes from a model by Datta and Beauchamp (1991), who simulated the effects of demography on female dominance relations by comparing two populations that differ in their growth rate. One population is growing fast (with 2.8 offspring per female) and the other is declining (with 0.6 offspring per female). Thus, in the declining population, matrilines are smaller, and potential allies are fewer than in the increasing population. Since a mother needs support from one of her dominant sisters to remain dominant over her daughter(s) and this ally is more likely to be lacking in a declining population than a growing one, mothers will more often become subordinate to their daughters. Similarly, for a youngster to become dominant over her older sister, she needs another sister and her mother as allies. These are more often alive in a growing than in a declining population, and according to Datta (1992), this explains the consistency of the youngest ascendancy rule in provisioned and expanding groups of rhesus macaques and Japanese macaques and the lower occurrence of outranking older sisters in the declining population of baboons. A genetic explanation is given to explain the absence of the youngest ascendancy rule in provisioned colonies of Barbary macaques and in a feral colony of Japanese macaques, where allies were present. In Barbary macaques, Prud’homme and Chapais (1993) suggest this difference may be a genetic one because they discovered that unrelated individuals rarely supported a younger sister against her older sister (although they support her against lower-born females). This differs from what is known of rhesus macaques and Japanese macaques. An ecological cause is suggested for the absence of the youngest ascendancy rule in feral colonies of Japanese macaques (Hill and Okayasu 1995). Due to the wide spatial dispersion during foraging, the frequency of aggression was rare, and, consequently, support was rare too. Note that apart from species that are weakly nepotistic, there are also those that are clearly non-nepotistic such as Hanuman langurs (Koenig 2000). Furthermore, in nonfemale-bonded Page 12 of 27

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species, such as gorillas and chimpanzees, matrilineal dominance does not exist and young females rank according to their age and power. How can we explain why the matrilineal system evolved in some female-bonded species but not in others? In a comparative study of egalitarian and despotic species of the genus Macaca, Thierry (2000) attributes this to differences in degree of despotism. He argues that the matrilineal dominance system is more complete in despotic species due to the higher frequency of support among kin (so that more power differentiation develops between matrilines). He believes that this also implies a lower frequency of acts of support among non-kin and that in egalitarian species support is distributed the opposite way, that is, it is more frequent among non-kin than among kin. Furthermore, he shows that dominance styles are phylogenetically conserved (Thierry et al. 2000). This begs the question of what caused the start of the interspecific differences in degree of nepotism between egalitarian and despotic macaques. According to Chapais (2004), this originates from a difference in the “strength of competition” due to the distribution of food. In the case of clumped food, supporting others will be more advantageous. Thus, a nepotistic system develops in which there is a high frequency of support of both kin and non-kin (in contrast to only kin as suggested by Thierry). When food is dispersed and causes scramble competition, it cannot be monopolized and support becomes less useful (both among kin and among non-kin).

Support: Kin Selection, Reciprocation, and Exchange Support in fights, or coalition formation, is often thought to be “altruistic” because of the energetic costs and risks of injury to the actor and the benefits to the receiver. As regards the benefits of receiving support, it increases the likelihood of winning a fight, as larger coalitions beat smaller ones (wedge-capped capuchin monkeys (Robinson 1988), bonnet macaques (Silk 1992a)). The cost of coalitions is difficult to estimate, but often it is assumed that one partner bears most of the costs while the other reaps the benefits (presenting thus a case of altruism). If so, the theory of kin selection and that of reciprocal altruism are believed to explain these supposedly altruistic acts. As regards kin selection, in Old World primates, individuals support kin more often than non-kin, e.g., in pigtails (Massey 1977), rhesus (Widdig et al. 2006), Japanese (Chapais et al. 1997), Tonkean (Petit and Thierry 1994), Barbary macaques (Widdig et al. 2000), chacma and yellow baboons (Silk et al. 2004; Walters 1980), and gorillas. Furthermore, individuals aid kin more often if they are more closely related (pig-tailed macaques, chimpanzees, and rhesus monkeys). In cases of reciprocal altruism, support is supposed to be reciprocated or exchanged for something else. Reciprocation of support is found in a comparative study of rhesus macaques, stump-tailed macaques, and chimpanzees by de Waal and Luttrell (1988). Since the authors statistically partialled out effects of proximity, kinship, and same-sex combination, they argue that reciprocation indicates that individuals keep mental records of the number of acts received from each individual and that they match the number of acts they give to what they have received from each partner, so-called calculated reciprocity. However, in this study, the effects of dominance ranks and grooming behavior are ignored, and data over five consecutive seasons were lumped together. Therefore, what seems to be proof of keeping mental records may have been simply a side effect. Reciprocation appears to be a side effect, for instance, in the long-term study of the same colony of chimpanzees analyzed per season by Hemelrijk and Ek (1991). It involves a sex difference since chimpanzee males reciprocated support whereas females did not. Males, however, Page 13 of 27

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only reciprocated support if their hierarchy was stable; if it was unstable, males supported those they groomed (Hemelrijk and Ek 1991). Because of this, and since there was insufficient indication that there was any negotiation for support because individuals did not significantly comply with requests from others (Hemelrijk et al. 1991), it seemed that males might have joined in one another’s fights opportunistically in order to attack common rivals. This may have been the cause of the reciprocation among males. Since males may benefit directly from such joint attacks, supporting behavior is selfish (Bercovitch 1988; Noe 1990; Chapais 1996; Prud’homme and Chapais 1996), and there is no need for the participants to keep records. Also a modeling study confirms the possible occurrence of reciprocation and exchange as a side effect (Hemelrijk and Puga-Gonzalez 2012). The model represents grouping individuals that groom and fight with others nearby. It suggests that reciprocation and interchange emerge as a side effect of proximity. In the model, the spatial position of individuals in the group appears to be relatively stable, and thus individuals interact more frequently with partners that are in proximity than those that are far away. Therefore, they groom, fight, and support each other more frequently which results in the emergence of these patterns (Hemelrijk and Puga-Gonzalez 2012). As in chimpanzee males, reciprocation of support has been reported in one study of male baboons (Packer 1977) but not in another (Bercovitch 1988). This difference possibly is related to a difference in the stability of the hierarchy (Hemelrijk and Ek 1991). The sex difference in reciprocation of support is in line with detailed earlier studies by de Waal (1978, 1984), in which he found that coalitions by males were mainly opportunistic and only corresponded with their social bonds during periods in which the position of the alpha-male was clear (de Waal 1984). Female coalitions, however, were more stable and always coincided with their social bonds (Hemelrijk and Ek 1991). Thus, whereas male coalitions seem to serve status competition, female coalitions are directed toward protection of kin and affiliation partners. Recently, an alternative mechanism to explain reciprocity has been proposed, “emotional bookkeeping” (Schino and Aureli 2009). It suggests that the frequency and quality of previous and present social interactions with a particular partner elicits a specific emotional state. This emotional state may lead to reciprocation and interchange of beneficial acts without relying on high cognitive mechanisms. Furthermore, de Waal and Luttrell (1988) studied reciprocity of “revenge.” By revenge, one means attacking someone while supporting another for the reason that the subject has received similar “contra-support” before. In this study, it was found that revenge is reciprocated only among chimpanzees, not among the two monkey species (i.e., macaques). This is interpreted as if the individuals aim their support against some individual because they have been attacked in a similar way: they have suffered support against themselves. De Waal and Luttrell consider this a sign of a greater cognitive capacity in chimpanzees because chimpanzees keep track not only of acts of support but also of revenge. However, there are three alternative explanations for this pattern. First, the authors lumped together data of five seasons despite changes in dominance ranks and in the stability of the power of the top male. In a study in the same colony, but in an analysis of support data per season, Hemelrijk and Ek (1991) found no reciprocation of revenge. Therefore, the apparent reciprocation of revenge may have resulted from the lumping together of data, and in any case, it is unlikely that individuals keep track of acts of revenge over a period longer than one season. Second, reciprocation of revenge has also been observed in monkeys, e.g., bonnet macaques (Silk 1992a), and also among related female gorillas (Watts 1997), which pleads against the hypothesis of the need of high cognition for such reciprocation. Third, reciprocity of “revenge” emerges in an individual-based model as a side effect of the gradient of the hierarchy (Hemelrijk and Puga-Gonzalez 2012). When the hierarchy is shallow, aggression is known to be bidirectional, Page 14 of 27

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because it involves little risks for both partners, and when the hierarchy is steep, aggression is unidirectional (i.e., from dominants to subordinates). In this model, incidental coalitions are observed when, by accident, after a fight between two individuals, a third nearby individual attacks one of the former opponents. Opposition in such incidental coalitions follows automatically the same pattern as dyadic aggression: it is unidirectional when the dominance hierarchy is steep and bidirectional when the dominance hierarchy is shallow. This is statistically recorded as reciprocation of contra-support or opposition but lacks cognitive rules for revenge and for its reciprocation.

Communal Rearing and Allomothering Usually the mother takes care of the infant alone. In callitrichids (tamarins and marmosets), however, everyone (both parents and mature offspring) assists in rearing the newborns by carrying them and provisioning them. Mature offspring postpone their departure from their natal territory and delay independent breeding (Rapaport 2001). In a number of female-bonded species, youngsters are protected and helped in fights so that they rank immediately below their mothers (matrilineal dominance system, see preceding section), and in all species youngsters are protected in fights that are dangerous. Furthermore, in many species, unrelated individuals may nurse and carry youngsters (allomothering); they cuddle the infant, embrace it, groom, and protect it (McKenna 1979). Allomothers are usually young, nulliparous females, ranking below the mother; often they are sisters of the infant. In this way, the allomother learns how to handle an infant, which increases the chance of survival of her own offspring (Lancaster 1971). An advantage to the mother seems to be the shortening of the interbirth interval (Fairbanks 1990) and the increase of her reproductive success (Ross and MacLarnon 2000). On the basis of detailed comparative studies of macaques, Thierry (2004) argues that two assumptions suffice to explain interspecific variation in degree of allomothering in Macaca: (a) attraction to infants and (b) constraints of social structure (McKenna 1979). First, all females are strongly attracted to all infants. Second, in certain species, mothers protect the infants with greater care than in others, and therefore, in these species, allomothering is counteracted. These species are the species that belong to the two despotic grades of macaques, whose aggression is intense and among whom power differences are great. This may cause problems for females when they have to retrieve their infants. In contrast to this, in egalitarian species, power differences are small and aggression is mild. Thus, differences in the degree of allomothering result from a kind of social epigenesis.

Collective Defense of Home Ranges Species and groups differ in the way in which they use their home range. Depending on this, fights with other groups may aim at the defense of only one food source (e.g., fruit tree) or of a whole territory (Cheney 1987). A number of species have special intergroup calls that are meant to separate the groups spatially (e.g., in mantled howler, capuchin, mangabey, siamang, yellowheaded titi). Most territorial species, however, have intergroup calls that incite the other group to fight them (e.g., dusky titi, gibbon spp., vervet, colobus). If actual fights between groups occur, in chimpanzees this may lead to killing an adult of the other group (Wilson and Wrangham 2003; Wilson et al. 2004). Usually, males are more active than females in fights between groups. In macaques, however, females may also participate. In both sexes, higher-ranking individuals participate more often than lower-ranking ones (Cooper 2004).

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Behavior Against Predators When primates meet a predator, they flee individually (so do large species) or hide (in particular, smaller species). Furthermore, they may protect themselves and their group members in other ways such as (a) by mobbing the predator, (b) by scanning the environment for early discovery of predators, and (c) by warning other group members. Mobbing predators has been described for baboons, rhesus monkeys, and all three ape species. Each of these species was observed to attack tigers or lions (Cheney and Wrangham 1987). Scanning the environment has been described for a number of primate species such as red-bellied tamarins (Caine 1984) and chacma baboons (Hall 1960). In a series of experiments, tamarins appeared to scan most frequently during the most dangerous periods of the day and in the presence of the most dangerous stimuli. Further, tamarins appeared to divide the duty of scanning among group members. In relation to protection against predators, the spatial distribution of the individuals of the different sex age categories in progressions has also been studied in baboons (Altmann 1979; Rhine and Westland 1981). Most primates use alarm calls to warn against predators. Such calls are altruistic in the sense that they are harmful to the sender, because it attracts the attention of the predator to the caller, but beneficial to others that are close by. It has been debated whether kin selection is the main evolutionary force behind these calls because it is usually kin that is protected by these calls. However, newly immigrant males also tend to call loudly in spite of the fact that they have no kin members in the group (Cheney and Seyfarth 1981). Many species of primates use different alarm calls for different predators. Such a differentiation is described for vervets, red colobus, Goeldi marmosets, pygmy marmosets, cotton-top tamarins, and gibbons (Cheney and Wrangham 1987; Dugatkin 1997). Vervets emit different calls when the predator is a leopard, an eagle, or a snake (Struhsaker 1976). In playback experiments of the different calls, vervets appeared to respond to leopard alarms by climbing into the trees; at eagle alarms they looked up, and at snake alarms they looked down. Because of the fine distinction between these alarm calls (almost resembling human language), it has been asked whether alarm calling can be considered intentional warning. Evidence points against this, because vervets continue to give alarm calls after everyone in the group has heard them (Cheney and Seyfarth 1985) and because the intensity of these alarm calls and other protective actions by mothers remained similar whether or not their daughters were informed about the presence of the predator (Cheney and Seyfarth 1990).

Conclusion Cooperation within a group of primates mainly concerns grooming and coalition formation. Sometimes it involves communal hunting, food sharing, and helping to raise young of others and defense against danger from the outside. Such defense involves collective defense of a home range against another group or defense of a group against a predator. The specific patterns of cooperation depend on the social system and the kind of primate involved. Behavioral acts, such as grooming, coalition formation, and tolerance during feeding, have originally been considered as “altruistic” but are presently often considered advantageous for both parties, the actor and receiver. Furthermore, patterns of coalitions and their exchange and patterns of grooming (such as “reconciliation” and “consolation”) have for long been considered to reflect sophisticated cognition, but it is increasingly acknowledged that these patterns may also arise from simple behavioral rules.

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Cross-References ▶ Evolution of the Primate Brain ▶ Great Ape Social Systems ▶ Primate Intelligence ▶ Primate Life Histories ▶ The Hunting Behavior and Carnivory of Wild Chimpanzees ▶ Theory of Mind: A Primatological Perspective

References Altmann SA (1979) Baboon progressions: order or chaos? A study of one-dimensional group geometry. Anim Behav 27:46–80 Aureli F, Cords M, van Schaik CP (2002) Conflict resolution following aggression in gregarious animals: a predictive framework. Anim Behav 64:325–343 Barrett L, Henzi SP, Weingrill T, Lycett JE, Hill RA (1999) Market forces predict grooming reciprocity in female baboons. Proc R Soc Lond B 266:665–670 Barrett L, Henzi SP, Weingrill T, Lycett JE, Hill RA (2000) Female baboons do not raise the stakes but they give as good as they get. Anim Behav 59:763–770 Barrett L, Gaynor D, Henzi SP (2002) A dynamic interaction between aggression and grooming reciprocity among female chacma baboons. Anim Behav 63:1047–1053 Barton R (1985) Grooming site preferences in primates and their functional implications. Int J Primatol 6:519–532 Bercovitch FB (1988) Coalitions, cooperation and reproductive tactics among adult baboons. Anim Behav 36:1198–1209 Bissonnette A, de Vries H, van Schaik CP (2009) Coalitions in male Barbary macaques, Macaca sylvanus: strength, success and rules of thumb. Anim Behav 78:329–335 Bissonnette A, Bischofberger N, van Schaik CP (2011) Mating skew in Barbary macaque males: the role of female mating synchrony, female behavior, and male-male coalitions. Behav Ecol Sociobiol 65:167–182 Boccia ML, Reite M, Laudenslager M (1989) On the physiology of grooming in a Pigtail Macaque. Physiol Behav 45:667–670 Borries C, Sommer V, Srivastava A (1994) Weaving a tight social net: allogrooming in freeranging female langurs (Presbytis entellus). Int J Primatol 15:421–443 Caine NG (1984) Visual scanning by tamarins. Folia Primatol 43:59–67 Call J (1999) The effect of inter-opponent distance on the occurrence of reconciliation in stumptail (Macaca arctoides) and rhesus macaques (Macaca mulatta). Primates 40:515–523 Call J, Aureli F, de Waal FBM (1999) Reconciliation patterns among stumptailed macaques: a multivariate approach. Anim Behav 58:165–172 Chapais B (1981) The adaptiveness of social relationships among adult rhesus monkeys. PhD dissertation, University of Cambridge, Cambridge Chapais B (1995) Alliances as a means of competition in primates: evolutionary, developmental and cognitive aspects. Yrbk Phys Anthropol 38:115–136 Chapais B (1996) Competing through co-operation in nonhuman primates: developmental aspects of matrilineal dominance. Int J Behav Dev 19:7–23

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Chapais B (2004) How kinship generates dominance structures: a comparative perspective. In: Thierry B, Singh M, Kaumanns W (eds) How societies arise: the macaque model. Cambridge University Press, Cambridge, UK, pp 186–204 Chapais B, Gauthier C (2004) Juveniles outrank higher-born females in groups of long-tailed macaques with minimal kinship. Int J Primatol 25:429–447 Chapais B, Lecomte M (1995) Induction of matrilineal rank instability by the alpha male in a group of Japanese macaques. Am J Primatol 36:299–312 Chapais B, Gauthier C, Prud’homme J, Vasey P (1997) Relatedness threshold for nepotism in Japanese macaques. Anim Behav 53:1089–1101 Chapais B, Savard L, Gauthier C (2001) Kin selection and the distribution of altruism in relation to the degree of kinship in Japanese macaques (Macacfuscata). Behav Ecol Sociobiol 49:493–502 Cheney DL (1987) Interactions and relationships between groups. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. Chicago University Press, Chicago, pp 267–281 Cheney DL, Seyfarth RM (1981) Selective forces affecting the predator alarm calls of vervet monkeys. Behaviour 76:25–61 Cheney DL, Seyfarth RM (1985) Vervet alarm calls: manipulation through shared information. Behaviour 94:150–166 Cheney DL, Seyfarth RM (1990) How monkeys see the world. University of Chicago Press, Chicago Cheney DL, Wrangham RW (1987) Predation. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. Chicago University Press, Chicago, pp 227–239 Combes SL, Altmann J (2001) Status change during adulthood: life-history byproduct or kin-selection based on reproductive value? Proc R Soc Lond B 268:1367–1373 Connor RC (1995) Impala allogrooming and the parcelling model of reciprocity. Anim Behav 49:528–530 Cooper MA (2004) Inter-group relationships. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization. Cambridge University Press, New York, pp 204–208 Cords M (1992) Post-conflict reunions and reconciliation in long-tailed macaques. Anim Behav 44:57–61 Cords M (1995) Predator vigilance costs of allogrooming in wild blue monkeys. Behaviour 132:559–569 Cords M (2000) Agonistic and affiliative relationships in a blue monkey group. In: Whitehead PF, Jolly CJ (eds) Old world monkeys. Cambridge University Press, Cambridge, pp 453–479 Cords M (2002) Friendship among adult female blue monkeys (Cercopithecus mitis). Behaviour 139:291–314 Cords M, Thurnheer S (1993) Reconciling with valuable partners by long-tailed macaques. Ethology 93:315–325 Datta SB (1992) Effects of availability of allies on female dominance structure. In: Harcourt HA, de Waal FBM (eds) Coalitions and alliances in humans and in other animals. Oxford University Press, Oxford, pp 61–82 Datta SB, Beauchamp G (1991) Effects of group demography on dominance relationships among female primates. I. Mother-daughter and sister-sister relations. Am Nat 138:201–226 de Waal FBM (1978) Exploitative and familiarity dependent support strategies in a colony of semifree living chimpanzees. Behaviour 66:268–312 Page 18 of 27

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de Waal FBM (1982) Chimpanzee politics: sex and power among apes. Harper and Row, New York de Waal FBM (1984) Sex differences in the formation of coalitions among chimpanzees. Ethol Sociobiol 5:239–255 de Waal FBM (1997) The chimpanzee’s service economy: food for grooming. Evol Hum Behav 18:375–386 de Waal FBM (2000) Attitudinal reciprocity in food sharing among brown capuchin monkeys. Anim Behav 60:253–261 de Waal FBM, Harcourt AH (1992) Coalitions and alliances: a history of ethological research. In: Harcourt AH, de Waal FBM (eds) Coalitions and alliances in humans and other animals. Oxford University Press, Oxford, pp 1–19 de Waal FBM, Luttrell LM (1986) The similarity principle underlying social bonding among female rhesus monkeys. Folia Primatol 46:215–234 de Waal FBM, Luttrell LM (1988) Mechanisms of social reciprocity in three primate species: symmetrical relationship characteristics or cognition? Ethol Sociobiol 9:101–118 de Waal FBM, van Hooff JARAM (1981) Side-directed communication and agonistic interactions in chimpanzees. Behaviour 77:164–198 de Waal FBM, Yoshihara D (1983) Reconciliation and redirected affection in rhesus monkeys. Behaviour 85:224–241 de Waal FBM, van Hooff JARAM, Netto WJ (1976) An ethological analysis of types of agonistic interaction in a captive group of Java-monkeys (Macaca fascicularis). Primates 17:257–290 Di Bitetti MS (1997) Evidence for an important social role of allogrooming in a platyrrhine primate. Anim Behav 54:199–211 Dugatkin LA (1997) Cooperation among animals: an evolutionary perspective. Oxford University Press, Oxford Dunbar RIM (1988) Primate social systems. Croom Helm, London Dunbar RIM (1991) Functional significance of social grooming in primates. Folia Primatol 57:121–333 Dunbar RIM (1993) Coevolution of neocortical size, group size and language in humans. Behavioral and brain sciences 16:681–735 Dunbar RIM (2003) The social brain: mind, language, and society in evolutionary perspective. Annu Rev Anthropol 32:163–181 Dunbar RIM, Sharman M (1984) Is Social Grooming Altruistic? Zeitschrift fuer Tierpsychologie 64:163–173 Estrada A, Estrada, R, Ervin F (1977) Establishment of a Free-ranging Colony of Stumptail Macaques (Macaca arctoides): Social Relations I. Primates 18:647–676 Fairbanks LA (1980) Relationships among adult females in captive vervet monkeys: testing a model of rank-related attractiveness. Anim Behav 28:853–859 Fairbanks LA (1990) Reciprocal benefits of allomothering for female vervet monkeys. Anim Behav 40:553–562 Frank RE, Silk JB (2009) Grooming exchange between mothers and non-mothers: the price of natal attraction in wild baboons (Papio anubis). Behaviour 146:889–906 Franz C (1999) Allogrooming behaviour and grooming site preferences in captive bonobos (Pan paniscus): association with female dominance. Int J Primatol 20:525–546 Fruteau C, Voelkl B, van Damme E, Noe R (2009) Supply and demand determine the market value of food providers in wild vervet monkeys. Proc Natl Acad Sci USA 106:12007–12012

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Fruteau C, van de Waal E, van Damme E, Noe R (2011) Infant access and handling in sooty mangabeys and vervet monkeys. Anim Behav 81:153–161 Goldberg TL, Wrangham RW (1997) Genetic correlates of social behaviour in wild chimpanzees: evidence from mitochondrial DNA. Anim Behav 54:559–570 Goodall J (1986) The chimpanzees of Gombe: patterns of behaviour. Belknap Press of Harvard University Press, Cambridge, MA/London Goosen C (1975) After effects of allogrooming in pairs of adult stump-tailed macaques: a preliminary report. In: Kondo S, Kawai M, Ehara A (eds) Contemporary primatology (proceedings of fifth international congress primatology). Karger, Basel, pp 263–268 Goosen C (1987) Social grooming in primates. In: Mitchell G, Erwin J (eds) Comparative primate biology. Part 2: behaviour, cognition, and motivation. Alan R. Liss, Inc., New York, pp 107–131 Gouzoules S, Gouzoules H (1987) Kinship. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. Chicago University Press, Chicago, pp 299–305 Gros-Louis J, Perry S, Manson JH (2003) Violent coalitionary attacks and intraspecific killing in wild white-faced capuchin monkeys (Cebus capucinus). Primates 44:341–346 Gumert MD (2007) Payment for sex in a macaque mating market. Anim Behav 74:1655–1667 Hall KRL (1960) Social vigilance behaviour of the chacma baboon, Papio ursinus. Behaviour 16:261–294 Hamilton WD (1964) The genetical evolution of social behaviour. I. J Theor Biol 7:1–16 Harcourt AH (1988) Alliances in contests and social intelligence. In: Byrne RW, Whiten A (eds) Machiavellian intelligence: social expertise and the evolution of intellect in monkeys, apes, and humans. Clarendon, Oxford Harcourt AH, de Waal FBM (1992) Coalitions and alliances in humans and other animals. Oxford University Press, Oxford, p 531 Hare B, Tomasello M (2004) Chimpanzees are more skilful in competitive than in cooperative cognitive tasks. Anim Behav 68:571–581 Hemelrijk CK (1990a) A matrix partial correlation test used in investigations of reciprocity and other social interaction patterns at a group level. J Theor Biol 143:405–420 Hemelrijk CK (1990b) Models of, and tests for, reciprocity, unidirectional and other social interaction patterns at a group level. Anim Behav 39:1013–1029 Hemelrijk CK (1991) Interchange of ‘altruistic’ acts as an epiphenomenon. J Theor Biol 153:137–139 Hemelrijk CK (1994) Support for being groomed in long-tailed macaques, Macaca fascicularis. Anim Behav 48:479–481 Hemelrijk CK, Ek A (1991) Reciprocity and interchange of grooming and ‘support’ in captive chimpanzees. Anim Behav 41:923–935 Hemelrijk CK, Luteijn M (1998) Philopatry, male presence and grooming reciprocation among female primates: a comparative perspective. Behav Ecol Sociobiol 42:207–215 Hemelrijk CK, Puga-Gonzalez I (2012) An individual-oriented model on the emergence of support in fights, its reciprocation and exchange. PLoS ONE 7:e37271 Hemelrijk CK, Klomberg TJM, Nooitgedagt JH, van Hooff JARAM (1991) Side-directed behaviour and recruitment of support in captive chimpanzees. Behaviour 118:89–102 Hemelrijk CK, van Laere GJ, van Hooff JARAM (1992) Sexual exchange relationships in captive chimpanzees? Behav Ecol Sociobiol 30:269–275 Hemelrijk CK, Meier CM, Martin RD (1999) ‘Friendship’ for fitness in chimpanzees? Anim Behav 58:1223–1229

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Hemelrijk CK, Wantia J, Daetwyler M (2003) Female co-dominance in a virtual world: ecological, cognitive, social and sexual causes. Behaviour 140:1247–1273 Hemelrijk CK, Wantia J, Isler K (2008) Female dominance over males in primates: selforganisation and sexual dimorphism. PLoS ONE 3:e2678 Henzi SP, Barrett L (1999) The value of grooming to female primates. Primates 40:47–59 Henzi SP, Barrett L (2002) Infants as a commodity in a baboon market. Anim Behav 63:915–921 Higham JP, Maestripieri D (2010) Revolutionary coalitions in male rhesus macaques. Behaviour 147:1889–1908 Hill DA (1994) Affiliative behaviour between adult males of the genus Macaca. Behaviour 130:293–308 Hill DA (1999) Effects of provisioning on the social behaviour of Japanese and rhesus macaques: implications for socioecology. Primates 40:187–198 Hill DH, Okayasu N (1995) Absence of youngest ascendancy in the dominance relations of sisters in wild Japanese macaques (Macacafuscata yakui). Behaviour 132:367–380 Hrdy SB (1977) The langurs of Abu. Harvard University Press, Cambridge Kapsalis E, Berman CM (1996) Models of affiliative relationships among free-ranging rhesus monkeys (Macaca mulatta). 2. Testing predictions for three hypothesized organizing principles. Behaviour 133:1235–1263 Keverne EB, Martensz ND, Tuite B (1989) Beta-endorphin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships. Psychoendocrinology 14:155–161 Koenig A (2000) Competitive regimes in forest-dwelling Hanuman langur females (Semnopithecus entellus). Behav Ecol Sociobiol 48:93–109 Lancaster JB (1971) Play-mothering: the relations between juvenile females and young infants among free-ranging vervet monkeys (Cercopithecus aethiops). Folia Primatol 15:161–182 Langergraber KE, Mitani JC, Vigilant L (2007) The limited impact of kinship on cooperation in wild chimpanzees. Proc Natl Acad Sci USA 104:7786–7790 Lazaro-Perea C, Arruda MF, Snowdon CT (2004) Grooming as a reward? Social function of grooming between females in cooperatively breeding marmosets. Anim Behav 67:627–636 Maestripieri D (1993) Vigilance costs of allogrooming in Macaque mothers. Am Nat 141:744–753 Maestripieri D (2000) Determinants of affiliative interactions between adult males and lactating females in pigtail macaques (Macaca nemestrina nemestrina). Ethology 106:425–439 Majolo B, Ventura R, Koyama NF (2009) A statistical modelling approach to the occurrence and timing of reconciliation in wild Japanese macaques. Ethology 115:152–166 Manson JH, Navarrete CD, Silk JB, Perry S (2004) Time-matched grooming in female primates? New analysis from two species. Anim Behav 67:493–500 Massey A (1977) Agonistic aids and kinship in a group of pigtail macaques. Behav Ecol Sociobiol 12:31–40 Matsumura S (1996) Postconflict affiliative contacts between former opponents among wild Moor macaques (Macaca maurus). Am J Primatol 38:211–219 Matsumura S (1997) Mothers in a wild group of moor macaques (Macaca maurus) are more attractive to other group members when holding their infants. Folia Primatol 68:77–85 McGrew WC (1992) Chimpanzee material culture. Cambridge University Press, Cambridge McKenna JJ (1979) The evolution of allomothering behavior among Colobine monkeys: function and opportunism in evolution. Am Anthropol 81:818–840 Meier C, Hemelrijk CK, Martin RD (2000) Paternity determination, genetic characterization and social correlates in a captive group of chimpanzees (Pan troglodytes). Primates 41:175–183

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Michael RP, Bonsall RW, Zumpe D (1978) Consort bonding and operant behavior by female rhesus monkeys. Comp Physiol Psychol 92:837–845 Muroyama Y (1991) Mutual reciprocity of grooming in female Japanese macaques (Macaca fuscata). Behaviour 119:161–170 Muroyama Y (1994) Exchange of grooming for allomothering in female patas monkeys. Behaviour 128:103–119 Nishida T (1983) Alpha status and agonistic alliances in wild chimpanzees. Primates 24:318–336 Noe¨ R (1990) A veto game played by baboons: a challenge to the use of the prisoner’s dilemma as a paradigm for reciprocity and cooperation. Anim Behav 39:78–90 Noe¨ R (1992) Alliance formation among male baboons: shopping for profitable partners. In: Harcourt AH, de Waal FBM (eds) Coalitions and alliances in humans and other animals. Oxford University Press, Oxford, pp 285–321 Noe¨ R, Sluijter AA (1995) Which adult male Savanna baboons form coalitions? Int J Primatol 16:77–105 O’Brien TG (1993) Allogrooming behaviour among adult female wedge-capped capuchin monkeys. Anim Behav 46:499–510 Packer C (1977) Reciprocal altruism. Nature 265:441–443 Palombit RA, Seyfarth RM, Cheney DL (1997) The adaptive value of ‘friendships’ to female baboons: experimental and observational evidence. Anim Behav 54:599–614 Palombit RA, Cheney DL, Fisher J, Johnson S, Rendall D, Seyfarth R, Silk J, van Schaik CP, Janson CH (2000) Male infanticide and defense of infants in chacma baboons. In: Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 123–152 Parish AR (1994) Sex and food control in the ‘uncommon chimpanzee’: How bonobo females overcome a phylogenetic legacy of male dominance. Ethol Sociobiol 15:157–179 Parr LA, Matheson MD, Bernstein IS, De Waal FBM (1997) Grooming down the hierarchy: allogrooming in captive brown capuchin monkeys, Cebusapella. Anim Behav 54:361–367 Paxton R, Basile BM, Adachi I, Suzuki WA, Wilson ME, Hampton RR (2010) Rhesus monkeys (Macaca mulatta) rapidly learn to select dominant individuals in videos of artificial social interactions between unfamiliar conspecifics. J Comp Psychol 124:395–401 Payne HFP, Lawes MJ, Henzi SP (2003) Competition and the exchange of grooming among female samango monkeys (Cercopithecus erythrarchus). Behaviour 140:453–471 Petit O, Thierry B (1994) Aggressive and peaceful interventions in conflicts in Tonkean macaques. Anim Behav 48:1427–1436 Prud’homme J, Chapais B (1993) Rank relations among sisters in semi-free ranging Barbary macaques (Macaca sylvanus). Int J Primatol 14:405–420 Prud’homme J, Chapais B (1996) Development of intervention behaviour in Japanese macaques: testing the targeting hypothesis. Int J Primatol 17:429–443 Puga-Gonzalez I, Hildenbrandt H, Hemelrijk CK (2009) Emergent patterns of social affiliation in primates, a model. Plos Comput Biol 5:e1000630. doi:10.1371/journal.pcbi.1000630 Range F, Noe R (2005) Can simple rules account for the pattern of triadic interactions in juvenile and adult sooty mangabeys? Anim Behav 69:445–452 Rapaport LG (2001) Food transfer among adult lion tamarins: mutualism, reciprocity or one-sided relationships? Int J Primatol 22:611–629 Rhine RJ, Westland BJ (1981) Adult male positioning in baboon progressions: order and chaos revisited. Folia Primatol 35:77–116 Roberts G, Sherratt TN (1998) Development of cooperative relationships through increasing investment. Nature 394:175–179 Page 22 of 27

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Robinson JG (1988) Group size in wedge-capped capuchin monkeys Cebusolivaceus and the reproductive success of males and females. Behav Ecol Sociobiol 23:187–197 Ross C, MacLarnon A (2000) The evolution of non-maternal care in anthropoid primates: a test of the hypotheses. Folia Primatol 71:93–113 Rowell TE (1968) Grooming by adult baboons in relation to reproductive cycles. Anim Behav 16:585–588 Rowell TE, Wilson C, Cords M (1991) Reciprocity and partner preference in grooming of female blue monkeys. Int J Primatol 12:319–336 Ruiter JR (1998) Relatedness of matrilines, dispersing males and social groups in long-tailed macaques (Macaca fascicularis). Proc R Soc Lond 265:79–87 Schino G (2001) Grooming, competition and social rank among female primates: a meta-analysis. Anim Behav 62:265–271 Schino G (2007) Grooming and agonistic support: a meta-analysis of primate reciprocal altruism. Behav Ecol 18:115–120 Schino G, Aureli F (2008a) Grooming reciprocation among female primates: a meta-analysis. Biol Lett 4:9–11 Schino G, Aureli F (2008b) Trade-offs in primate grooming reciprocation: testing behavioural flexibility and correlated evolution. Biol J Linn Soc 95:439–446 Schino G, Aureli F (2009) Reciprocal altruism in primates: partner choice, cognition, and emotions. Adv Stud Behav 39:45–69 Schino G, Scucchi S, Maestripieri D, Turillazzi PG (1988) Allogrooming as a tension-reduction mechanism: a behavioral approach. Am J Primatol 16:43–50 Schino G, Ventura R, Troisi A (2003) Grooming among female Japanese macaques: distinguishing between reciprocation and interchange. Behav Ecol 14:887–891 Schino G, Tiddi B, Di Sorrentino EP (2006) Simultaneous classification by rank and kinship in Japanese macaques. Anim Behav 71:1069–1074 Schino G, di Sorrentino EP, Tiddi B (2007) Grooming and coalitions in Japanese macaques (Macaca fuscata): partner choice and the time frame of reciprocation. J Comp Psychol 121:181–188 Schino G, Di Giuseppe F, Visalberghi E (2009) Grooming, rank, and agonistic support in tufted capuchin monkeys. Am J Primatol 71:101–105. doi:10.1002/ajp.20627 Schuelke O, Bhagavatula J, Vigilant L, Ostner J (2010) Social bonds enhance reproductive success in male macaques. Curr Biol 20:2207–2210 Seyfarth RM (1976) Social relationships among adult female baboons. Anim Behav 24:917–938 Seyfarth RM (1977) A model of social grooming among adult female monkeys. J Theor Biol 65:671–798 Seyfarth RM (1978a) Social relationships among adult male and female baboons. I. Behaviour during sexual consortship. Behaviour 64:204–226 Seyfarth RM (1978b) Social relationships among adult male and female baboons. II. Behaviour throughout the female reproductive cycle. Behaviour 64:227–247 Seyfarth RM (1980) The distribution of grooming and related behaviours among adult female vervet monkeys. Anim Behav 28:798–813 Seyfarth RM, Cheney DL (1984) Grooming, alliances and reciprocal altruism in vervet monkeys. Nature 308:541–543 Shutt K, MacLarnon A, Heistermann M, Semple S (2007) Grooming in Barbary macaques: better to give than to receive? Biol Lett 3:231–233

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Silk JB (1982) Altruism among female Macaca radiata: explanations and analysis of patterns of grooming and coalition formation. Behaviour 79:162–188 Silk JB (1992a) The patterning of intervention among male bonnet macaques: reciprocity, revenge, and loyalty. Curr Anthropol 33:318–325 Silk JB (1992b) Patterns of intervention in agonistic contests among male bonnet macaques. In: Harcourt AH, Waal FBM (eds) Coalitions and alliances in humans and other animals. Oxford University Press, Oxford Silk JB (1999) Male bonnet macaques use information about third-party rank relationships to recruit allies. Anim Behav 58:45–51 Silk JB (2002) The form and function of reconciliation in primates. Ann Rev Anthropol 31:21–44 Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234 Silk JB, Alberts SC, Altmann J (2004) Patterns of coalition formation by adult female baboons in Amboseli, Kenya. Anim Behav 67:573–582 Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2009) The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proc R Soc B-Biol Sci 276:3099–3104 Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2010) Strong and consistent social bonds enhance the longevity of female baboons. Curr Biol 20:1359–1361. doi:10.1016/j.cub.2010.05.067 Slater KY, Schaffner CM, Aureli F (2007) Embraces for infant handling in spider monkeys: evidence for a biological market? Anim Behav 74:455–461 Smuts BB (1985a) Male-male competition for mates. In: Smuts BB (ed) Sex and friendship in baboons. Aldine Publishing Company, New York, pp 123–157 Smuts BB (1985b) Sex and friendship in baboons. Aldine, Hawthorne Smuts BB (1987) Sexual competition and mate choice. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. Chicago University Press, Chicago, pp 385–399 Stammbach E (1978) Social differentiation in groups of captive female hamadryas baboons. Behaviour 67:322–338 Stammbach E (1988) Group responses to specially skilled individuals in a Macaca fascicularis group. Behaviour 107:241–266 Stammbach E, Kummer H (1982) Individual contributions to a dyadic interaction: an analysis of baboon grooming. Anim Behav 30:964–971 Struhsaker TT (1976) Auditory communication among vervet monkeys (Cercopithecus aethiops). In: Altmann SA (ed) Social communication among primates. University of Chicago Press, Chicago, pp 3–14 Terry RL (1970) Primate grooming as a tension reduction mechanism. J Psychol 76:129–136 Thierry B (1990) Feedback loop between kinship and dominance: the macaque model. J Theor Biol 145:511–521 Thierry B (2000) Covariation of conflict management patterns across Macaque species. In: Aureli F, de Waal FBM (eds) Natural conflict resolution. University of California Press, Berkeley, pp 106–128 Thierry B (2004) Social epigenesis. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organisation. Cambridge University Press, Cambridge, pp 267–289

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Thierry B, Iwaniuk AN, Pellis SM (2000) The influence of phylogeny on the social behaviour of macaques (Primates: Cercopithecidae, genus Macaca). Ethology 106:713–728 Tiddi B, Aureli F, Schino G (2012) Grooming up the hierarchy: the exchange of grooming and rank-related benefits in a new world primate. PLoS ONE 7(5): e36641. doi:10.1371/journal. pone.0036641 Tomasello M, Call J, Gluckman A (1997) The comprehension of novel communicative signs by apes and human children. Child Dev 68:1067–1081 Trivers RL (1971) The evolution of reciprocal altruism. Quart Rev Biol 46:35–57 Uehara S, Hiraiwa-Hasegawa M, Hosaka K, Hamai M (1994) The fate of defeated alpha male chimpanzees in relation to their social networks. Primates 35:49–55 vanSchaik CP, Pandit SA, Vogel ER (2004) A model for within-group coalitionary aggression among males. Behav Ecol Sociobiol 57:101–109 Ventura R, Majolo B, Koyama NF, Hardie S, Schino G (2006) Reciprocation and interchange in wild Japanese macaques: grooming, cofeeding, and agonistic support. Am J Primatol 68:1138–1149 Vervaecke H, De Vries H, Van Elsacker L (2000) The pivotal role of rank in grooming and support behaviour in a captive group of bonobos (Pan paniscus). Behaviour 137:1463–1485 Walters J (1980) Interventions and the development of dominance relationships in female baboons. Folia Primatol 34:61–89 Watanabe K (1979) Alliance formation in a free-ranging troop of Japanese macaques. Primates 20:459–474 Watts DP (1994) Social relationships of immigrant and resident female mountain gorillas. 2. Relatedness, residence, and relationships between females. Am J Primatol 32:13–30 Watts DP (1995a) Post-conflict social events in wild mountain gorillas (Mammalia, Hominoidea). I. Social interactions between opponents. Ethology 100:139–157 Watts DP (1995b) Post-conflict social events in wild mountain gorillas. 2. Redirection, side direction, and consolation. Ethology 100:158–174 Watts DP (1997) Agonistic interventions in wild mountain gorilla groups. Behaviour 134:23–57 Watts DP (2000a) Grooming between male chimpanzees at Ngogo, Kibale National Park. I. Partner number and diversity and grooming reciprocity. Int J Primatol 21:189–210 Watts DP (2000b) Grooming between male chimpanzees at Ngogo, Kibale National Park. II. Influence of male rank and possible competition for partners. Int J Primatol 21:211–238 Watts DP (2002) Reciprocity and interchange in the social relationships of wild male chimpanzees. Behaviour 139:343–370 Watts DP (2004) Intracommunity coalitionary killing of an adult male chimpanzee at Ngogo, Kibale National Park, Uganda. Int J Primatol 25:507–521 Widdig A, Streich WJ, Tembrock G (2000) Coalition formation among male Barbary macaques (Macaca sylvanus). Am J Primatol 50:37–51 Widdig A, Streich W, Nuernberg P, Croucher P, Bercovitch FB, Krawczak M (2006) Paternal kin bias in the agonistic interventions of adult female rhesus macaques (Macaca mulatta). Behav Ecol Sociobiol 61:205–214 Wilkinson GS (1988) Reciprocal altruism in bats and other mammals. Ethol Sociobiol 9:85–100 Wilson ML, Wrangham RW (2003) Intergroup relations in chimpanzees. Annu Rev Anthropol 32:363–392 Wilson ML, Wallauer WR, Pusey AE (2004) New cases of intergroup violence among chimpanzees in Gombe National Park, Tanzania. Int J Primatol 25:523–549

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Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300 Wrangham RW (1999) Evolution of coalitionary killing. Yrbk Phys Anthropol 42:1–30 Zamma K (2002) Grooming site preferences determined by lice infection among Japanese macaques in Arashiyama. Primates 43:41–49

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Index Terms: Allomothers 15 Coalition 8 Communal rearing 15 Cooperation 1–2 Defense 8, 15 Grooming 2

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

Potential Hominoid Ancestors for Hominidae George D. Koufos* Laboratory of Geology and Palaeontology, Department of Geology, Aristotle University of Thessaloniki, Thessaloniki, Greece

Abstract Human origin and evolution are a prominent topic among scientists, one on which there continues to be disagreement. Each new finding raises new questions and arguments. This chapter summarizes the currently available data and hypotheses on hominid origins. The origin of the hominids may be traceable to Oligocene anthropoids such as Aegyptopithecus, which share some derived features with the early hominoids. The Latest Oligocene taxon Kamoyapithecus could be the oldest known hominoid, as it has relationships with some Miocene taxa. Proconsul is the most plausible taxon linking the hominoids to the great ape and human clades, as it preserves a mosaic of features from both groups. The Middle Miocene European hominoids seem to play an important role, and could include the possible link between more archaic hominoids and the great ape and human clades; candidates are numerous among both European and African forms. Among Late Miocene taxa, the craniodental morphology of Ouranopithecus provides the closest and most plausible link connecting the hominoids to the extant great apes and humans; its strong relationships to the australopiths and Homo put this taxon among the best candidates for this role at the moment. The Latest Miocene Sahelanthropus and Orrorin seem to be important links in the evolution of the hominids, whereas the Asian Middle-Late Miocene hominoids have strong similarities with the modern orangutans and are related to the “Pongo-lineage.”

Introduction The presence, origin, and future of man on earth are problems that have long preoccupied humans. Questions like “Who is my ancestor?”, “What was it like?”, or “Where do I come from?” were among the first for which answers were sought. Humanity’s need to find answers to these questions led, first, to origin myths, and later, after the development of science, to theories of human origins. Anthropology and biology offer answers based on the comparative anatomy, behavior, and genetics of humans and other animals. The evolutionary approach to understanding human origins seeks to identify all the characters that humans share with apes (our closest relatives) and with other animals. The ancient Greek philosopher Aristotle was among the first to recognize the affinities of man with the animals and placed man in the animal kingdom. Much later, the Swedish taxonomist Linnaeus classified humans laterally to the apes and monkeys, while the pre-Darwinian French naturalist Buffon as well laid out the view that humans have similarities with the apes, creating a link in the long chain of the beings. Paleoanthropology is the branch of paleontology that addresses the above questions based on the primate fossil record. Paleoanthropologists try to find the links between various fossil and extant taxa in order to complete the “chain” leading to humans. This is difficult and time‐consuming work, *Email: [email protected] Page 1 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

as fossils are relatively rare and widely dispersed; in most cases the remains are fragmentary, providing limited data. The discovery of new fossils over the last 50 years and the development of new methods for studying, comparing, and dating fossils, as well as for reconstructing their locomotion and paleoenvironment, have significantly increased our knowledge about the morphology and evolutionary relationships of primates. One of the main goals of paleoanthropology is to find the ancestor of humans – usually referred to as hominids – among the common stock of hominids and apes – known as hominoids. The hominoids constitute a group of African and Eurasian forms that lived during the Miocene epoch and are assumed to include the common ancestor of humans and apes. The following is a brief sketch of what we know about the hominoids. Later sections of this chapter will go into more detail on evidence from different time periods. The chapter does not answer what are still open research questions; its goal is merely to survey the available data about the potential hominoid ancestor of the hominids, providing a comprehensive overview. The first known hominoids are from Africa. The earliest possible representative of the hominoids originates in the Oligocene, the time of the genera Aegyptopithecus and Kamoyapithecus. Hominoids are more securely represented by the large set of Early Miocene proconsulids. The majority of the Early Miocene hominoids are restricted to Africa and are only found in East Africa and the Arabian Peninsula. A large number of taxa are recognized (Proconsul, Afropithecus, Heliopithecus, Nyanzapithecus, Mabokopithecus, Rangwapithecus, Turkanipithecus, Dendropithecus, Micropithecus, Simiolus, Morotopithecus, Limnopithecus, Kalepithecus), but most of them are known from only a few fragmentary fossils. Their size varied from small monkey sized (~3 kg) to large great ape sized (~80 kg), while their locomotion was quadrupedal and arboreal. The majority were fruit or leaf eaters. Kenyapithecus, who appeared at the end of the Middle Miocene (~14 Ma), was probably a hard-object feeder. The uppermost Middle Miocene and Late Miocene hominoids of Africa are rare and poorly known compared to Early/Middle Miocene forms (Kenyapithecus, Samburupithecus, Otavipithecus, Orrorin, Equatorius, Sahelanthropus). Towards the end of the Middle Miocene, the “story” of hominoid evolution continued in Eurasia, where hominoids were abundant until the Late Miocene (~7.5 Ma). Hominoids that migrated to Eurasia are represented by the taxa Griphopithecus and Kenyapithecus. After their arrival, they strongly diversified; several new taxa (Dryopithecus, Pierolapithecus, Anoiapithecus, Oreopithecus, Ouranopithecus, Sivapithecus, Ankarapithecus, Lufengpithecus) appeared between 8.0 and 13.0 Ma. The size of these taxa varies from medium to large, while their dietary type ranges from soft-object feeders, like Dryopithecus and Oreopithecus, to hard-object feeders like Ouranopithecus, Ankarapithecus, Lufengpithecus, and Gigantopithecus. Postcranial remains are relatively rare, and the available material indicates quadrupedal locomotion; however, one of these taxa, Pierolapithecus, is interpreted as an early orthograde (Moyà-Solà and Köhler 1996). The occurrence of the oldest australopithecines is dated to ~4.5 Ma, whereas the last Miocene hominoids date to the Middle Turolian (~7.5 Ma). There is thus a large gap of ~3 Ma between them. Until the beginning of the twenty-first century, no fossils were known from this time interval. The discovery in 2000 of the African hominoid Orrorin, dated to
6 Ma (Senut et al. 2001), provided the first evidence to fill the gap. One year later, the skull of Sahelanthropus, found in Chad and dated to 6.0–7.0 Ma, offered more data about this unknown time interval (Brunet et al. 2002). Most recently, some cranial remains of a hominoid from the Turolian of Turkey (Begun et al. 2003; G€uleç et al. 2007) and an isolated tooth of a hominoid possibly from the Middle Turolian of Bulgaria (Spassov et al. 2012) have added further evidence.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

Origin of the Miocene Hominoids The origin of the Miocene hominoids is to be found among the Oligocene primates. The division of the anthropoids into two main groups – the Platyrrhini (New World monkeys) and the Catarrhini (Old World monkeys) – is thought to have occurred at the Eocene/Oligocene boundary. One of the oldest and best‐known catarrhines is Aegyptopithecus (Fig. 1), from the Fayum province of Egypt, with an estimated age from 32.0 to 35.0 Ma (Tattersall et al. 1988). Since the Eocene/Oligocene boundary is estimated to be at ~35 Ma, the splitting of the catarrhines and platyrrhines coincides with the beginning of the Oligocene and bridges the gap between the Eocene Prosimii and the Miocene hominoids. Aegyptopithecus preserves some characters of the platyrrhines, such as the absence of an auditory tube in the external ear, but it has two premolars in each half of the jaw, a feature that serves to classify it within the catarrhines, being among the most primitive of them. The main morphological characters of Aegyptopithecus (Fig. 1) are an elongated skull with strong prognathism, strong postorbital constriction, large and completely enclosed orbits, weak supraorbital torus, large interorbital distance, a posteriorly developed sagittal crest, well‐developed sexual dimorphism in the canines, and broad molars with rounded and low cusps, well‐developed cingulum, and thin enamel. The braincase is small: its capacity is estimated at ~30 cm3 (Conroy 1990). The endocasts indicate morphology falling between the primitive and more derived anthropoids (Radinsky 1973). The humerus is relatively stout, with a large medial epicondyle and relatively wide trochlea. The morphology of the metapodials and phalanges suggests powerful grasping. The overall morphology of Aegyptopithecus indicates quadrupedal climbing, while the morphology of the skull and teeth suggests a soft‐object feeder. This type of diet fits well with its postcranial morphology, indicating a good climber. The presence of some derived characters in Aegyptopithecus has been interpreted in different ways. Simons (1965), focusing on features shared between Aegyptopithecus and Proconsul, suggested a close phyletic relationship between the two genera. Later, Andrews (1978) reported close similarities between the upper molars of Aegyptopithecus zeuxis and Proconsul africanus, but could not identify clearly shared derived features. The cranial proportions and the external ear showing a clear auditory tube in P. africanus are more derived features than those of Aegyptopithecus (Szalay and Delson 1979). The primitive robust postcrania of Aegyptopithecus, with less joint mobility, suggest relatively more leaping locomotion, whereas in the Miocene hominoids leaping constitutes only a small share of locomotion (Gebo 1993). Tattersall

Fig. 1 Aegyptopithecus zeuxis, sketch of the skull found in 1966. (a) Lateral and (b) frontal view (Drawn from the photo of Szalay and Delson (1979; Fig. 222)) Page 3 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

et al. (1988) suggested that Aegyptopithecus represents an early catarrhine close to the split between platyrrhines and catarrhines. Aegyptopithecus is a mosaic of primitive and derived characters, linking Eocene anthropoids to modern apes and monkeys, and could represent or be close to their common ancestor – a notion evidenced by its Greek species name zeuxis, meaning “way of connecting, bridge.” However, the available data do not fully support this view. Despite the possible link between Aegyptopithecus and the hominoids, there is no clear bridge, but in fact a 10.0 Ma gap in the fossil record between Aegyptopithecus and the first Miocene hominoids. The earliest possible representative of the hominoids is the Latest Oligocene Kamoyapithecus from Lothidok (Kenya), which is dated from 27.8 to 23.9 Ma (Leakey et al. 1995). The large size of Kamoyapithecus, although not decisive evidence, is similar to that of some early Late Miocene apes, suggesting that it could be the earliest known hominid (Leakey et al. 1995). During the Oligocene, several Afro-Arabian taxa of early catarrhines are known to have existed (Catopithecus, Oligopithecus, Moeripithecus, Propliopithecus), which could also be related to the Miocene hominoids.

The Miocene Hominoids Whereas the Eocene was the period of the prosimians and the Oligocene that of the early anthropoids, the subsequent Miocene represents the epoch of the hominoids, with many named genera and species. The taxonomic expansion is due in part to the limited material evidence allowing for differences in opinion among scientists, and in part to a tendency among paleoanthropologists to postulate new taxa. The hominoids expanded across the Old World from Spain to China and from South Africa to northern Europe (Fig. 2). During the last 40 years, extensive field campaigns carried out in the Old World by several scientific groups have brought to light numerous fossils. In addition, the revision of old material and new “discoveries” made in museum collections have increased the

Fig. 2 Geographic map indicating the most important sites with hominoids; blue square ¼ Oligocene and red circle ¼ Miocene localities Page 4 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

Miocene hominoid fossil record. This great knowledge gain of the last decades has led to the recognition of several new taxa, well defined through the application of several new methods, and to the recognition that the Miocene was an epoch of high diversification among hominoids. During the Miocene, several geotectonic movements took place in the Old World that caused geographic and environmental changes with either positive (diversification, expansion, migration) or negative (reduction or even extinction) effects on the hominoids. Many new hominoids appeared in Eurasia after their arrival from Africa during the upper part of the Middle Miocene. For a long time scientists believed that the Turolian dryness and the arrival of the cercopithecids were the main reasons for the extinction of the hominoids at the end of the Vallesian in Eurasia. This idea changed after the discovery of Turolian hominoids in Turkey and Bulgaria (G€ uleç et al 2007; Spassov et al. 2012). In Asia Gigantopithecus survived, as we know from finds in the Pleistocene of Southern China and Vietman (Kelley 2002). In Africa, hominoids existed in the Turolian as well; new discoveries during the last years have increased our estimate of their number (Kunimatsu et al. 2007; Brunet et al. 2002; Suwa et al. 2007; Senut et al. 2001). The paleogeographic and paleoclimatic changes that took place during the Miocene were strong factors contributing to the rapid evolution and diversification of the hominoids, leading to more derived and better adapted forms. Although the increasing severity of the ecological conditions eventually caused the extinction of most Miocene hominoids, for some of them the environmental pressure created an opportunity to develop comparatively more derived and evolved characters, which enabled their adaptation to the new conditions. As mentioned above, Aegyptopithecus and Kamoyapithecus might be the ancestors of the Miocene hominoids; the possible common ancestor of humans and apes, then, must be looked for among the stem Miocene hominoids. From this point of view, the hominoids are a very important and interesting group of primates. Over the last 50 years, several hominoids have been presented as possible ancestors of the hominids, but so far there is no one candidate that has clearly won out. The problem is complicated and cannot be solved easily, as the relationships among the fossil hominoids, as well as between extinct and extant members of this superfamily, are not fully known. The data for the fossil hominoids in most cases are limited and do not permit clear definitions and comparisons. The number of specimens is another problem. No fossil hominoid is known well enough to allow for complete understanding of its morphology and relationships. There are several important time gaps between the various forms, which prevent clear establishment of their relationships. When there is so much uncertainty to contend with, subjectivity of interpretation is also an issue: it can be difficult for researchers not to engage in speculation. As we proceed below to discuss the evidence for the most probable ancestors of the hominids, the Miocene hominoids, these caveats must all be borne in mind. Knowing the age of fossil hominoids is important for establishing their evolutionary relations. Yet here too lies a source of uncertainty and debate. Efforts at age determination must often confront contradictory data and give rise to differences of opinion. Nevertheless, for most hominoids satisfactory age correlation has been achieved by either biochronology, or radio-/magnetochronology, or both. The stratigraphic distribution of the main Miocene hominoids of Africa and Eurasia is given in Fig. 3. The figure also shows the European land mammal stages and zones, which are mentioned in the text. The continuous line indicates the stratigraphic distribution of the taxa, the dashed line their possible distribution, and an asterisk denotes that the taxon is known from a single site or all known material has similar age. It is quite clear from Fig. 3 that the hominoids are already well known from the Early–Middle Miocene of Africa, while in Eurasia, they are more common during the Late Miocene.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

Fig. 3 Stratigraphic distribution of the main Miocene hominoids; continuous line: stratigraphic distribution of a taxon; dashed line: possible distribution of a taxon; asterisk: taxon known from a single site or from several localities of the same age

The Early Miocene Early Miocene hominoids are known only from Africa. The best known taxon is Proconsul (Fig. 4) (Walker 1997). The oldest remains of Proconsul (P. africanus, P. major) were found in Kenya and Uganda and are dated to 19.0–20.0 Ma. Two other species (P. nyanzae and P. heseloni) are known from Kenya and dated to 17.0–18.5 Ma (Harrison 2002) (Fig. 4). Proconsul has an estimated body size that varies from that of a small monkey to that of a female gorilla. It shows sexual dimorphism in body size, as well as in the size and morphology of the canines. This sexual dimorphism is a primitive feature for Proconsul. The nasomaxillary region of Proconsul has a primitive internal structure with a large fossa incisiva. In addition, the maxillary processus palatinus is clearly lower than the premaxilla (Ward and Kimbel 1983; Ward and Pilbeam 1983). This nasomaxillary morphology (“African type,” according to the latter authors) is similar to Page 6 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

Fig. 4 Proconsul heseloni. Sketch of the first skull found in 1948 by M. Leakey on Rusinga Island, Lake Victoria (Drawn from a photo of Harrison (2002))

that of Australopithecus, Dryopithecus, Ouranopithecus, and the recent Gorilla. The skull has a moderately short and broad face compared to that of Aegyptopithecus, and a broad and relatively rhomboid-shaped nasal aperture, trapezoid orbits with rounded corners, a slight supraorbital torus with slightly swollen glabella, and a clear auditory tube like the recent cercopithecoids and hominoids (Szalay and Delson 1979; Walker 1997; Harrison 2002). The dentition of Proconsul preserves primitive features, such as relatively long and broad canines, a well-developed cingulum, asymmetric upper premolars with large paracones (buccal cusps), and the presence of a honing facet on the P3. Although the dental morphology of Proconsul, which indicates a soft fruit feeder (Kay and Ungar 1997), is well known, there are no clear synapomorphies with either the hominoids or the cercopithecoids. In many ways, it is similar to the dentition of the Oligocene Fayum catarrhines. The known postcrania of Proconsul are relatively abundant and provide a large set of characters. However, the systematic interpretation of these characters leads to contradictory results. Proconsul has anterior and posterior limbs of more or less similar length, indicating quadrupedal arboreal locomotion. The recent hominoids have a more erect posture (knuckle walking and brachiation). The robustness of the long bones of Proconsul suggests similarities to cercopithecoids, chimpanzees, and to ceboids with less elongated limbs. The distal extremity of the Proconsul humerus resembles that of small apes, while the distal extremity of the ulna is relatively straight, as in most anthropoids. The carpals indicate a climbing primate, whereas the phalangeal proportions are very close to macaques, suggesting a quadrupedal form (Walker and Pickford 1983; Ruff et al. 1989; Rose 1992, 1993). Most authors consider Proconsul to be a stem hominoid close to the origin of the Hominoidea (Hopwood 1933; Pilbeam 1969; Rose 1983, 1992, 1993; Andrews 1985; Begun et al. 1997; Kelley 1997; Ward 1997). These authors conclude that Proconsul shared derived characters with the extant hominoids. A different opinion suggests that Proconsul is a sister taxon of the recent great apes and humans (Walker and Teaford 1989; Rae 1997; Walker 1997). Neither opinion is accepted by Harrison (2002), whose detailed and critical analysis of key synapomorphies of the face, ear region, and postcrania shared by extant hominoids leads him to conclude that these are lacking in Proconsul. In contrast, Walker (1997) does refer to shared derived characters between Proconsul and more advanced hominoids, but he also recognizes possible features in the postcrania indicating a primitive catarrhine. Page 7 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

The frontal sinus in the skull of Proconsul could be a derived character – one shared with the extant hominoids and great apes (Andrews 1992). Although the frontal sinus is absent in Old World monkeys, it is clearly present in New World monkeys, which complicates the analysis of this feature. The absence of a tail is a derived character of the hominoids; the lack of a tail in Proconsul (Ward et al. 1991) thus suggests a relationship to the hominoids. The presence of six lumbar vertebrae rather than seven in Proconsul (Ward et al. 1993) also indicates a similarity to the hominoids and distinguishes it from monkeys. Several characters of the phalanges could be derived and shared with extant apes (Begun et al. 1994). The morphology of the trapezium and first metacarpal of Proconsul could be viewed as derived, with several characters shared between Proconsul and extant hominoids (Rose 1992). The relatively greater deviation of the ulna of Proconsul is, again, a derived character of the hominoids (Beard et al. 1986); in non-hominoid catarrhines the deviation of the ulna is not as strong. Rae (1997) studied a set of facial characters in the Early Miocene and modern hominoids and found that Early Miocene hominoids, including Proconsul, are linked to modern hominoids, in particular to great apes. As mentioned, Walker (1997) recognized Proconsul as a morphologically primitive hominoid, sharing several derived characters with the extant hominoids. In sum, Proconsul has a set of characters that link it with the Miocene hominoids, and even with the extant great apes and humans, but controversies remain. Future research may provide additional data, permitting more definitive conclusions about its phylogenetic relationships. In addition to Proconsul, several other taxa are known from the Early Miocene of Africa that could be related to the extant great apes and humans. It is appropriate here to give some information about the most important of them and their relationships. The genus Afropithecus was recognized in Kenya based on finds from localities dated to the early Miocene; the age of these finds is estimated between 17.0 and 18.0 Ma (Leakey and Walker 1997). Afropithecus is characterized by its relatively large size (similar to the recent chimpanzee), long and wide skull, narrow palate, large diastema, narrow and protruding premaxilla, large interorbital distance, asymmetrical orbits, slender supraorbital torus, frontal sinus extending to the glabella, lack of the superior transverse torus in the mandible, and an oblique angle between ascending ramus and mandibular corpus. The upper canine has a round basal section and deep mesial groove, while the lower canine is low crowned and laterally compressed. The upper premolars are wide and without lingual cingulum, while the cusps are moderately heteromorphic. The upper molars are narrow, with moderately developed lingual cingulum and very thick enamel. The dentition of Afropithecus thus differs clearly from that of Proconsul (Begun 2013), but the few known postcrania resemble those of P. nyanzae in size and morphology (Leakey and Leakey 1986; Leakey et al. 1988; Leakey and Walker 1997; Ward 2007). Afropithecus is a large hominoid whose facial shape resembles that of Aegyptopithecus zeuxis (Leakey et al. 1991), but whose postcrania are more derived than those of Aegyptopithecus and closer to Proconsul (Harrison 2002; Ward 2007). The teeth of Afropithecus are more derived than those of the Oligocene forms, featuring enlarged and procumbent incisors and thick canines. These characters as well as the very thickly enameled teeth suggest a hard-object eater, which places Afropithecus closer to Kenyapithecus. The lack of these characters in the dentition of Proconsul indicates a less derived feature, but its derived facial shape is closer to the later hominoids. Morotopithecus is known from Uganda from a single species, M. bishopi, which was originally described as Proconsul major. Its age is debatable: the correlation of the fauna and older K40/Ar39 datings suggest a Middle Miocene age, 17.0–15.0 Ma (Bishop et al. 1969; Pickford et al. 1999), whereas 40Ar/39Ar datings suggest an Early Miocene age at ~20.6 Ma (Gebo et al. 1997). Morotopithecus is relatively small sized, smaller than P. major. The skull is characterized by a long, high, and narrow face, short premaxilla, wide palate, narrow interorbital distance, large Page 8 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

diastema, and a primitive nasomaxillary region with a large fossa incisiva. There is strong sexual dimorphism in the upper canines. The upper premolars are broad and relatively large. The molars have bunodont cusps, wrinkled enamel, and a well-developed lingual cingulum, similar to those of P. major (Pilbeam 1969; Andrews 1978; Harrison 2002). Although Morotopithecus differs from Proconsul in several features, its cranial and dental characters suggest that it is closer to the proconsulids. The postcrania of Morotopithecus are few but provide some significant characters for the genus. The anatomy of the lumbar vertebrae shares some derived features (robust pedicles, reduced ventral keeling) with the extant hominoids. The scapula (some authors do not agree that it belongs to this genus) has a rounded and expanded upward glenoid articular surface, as in hominoids. Finally, the morphology of the femur and phalanges resembles that of Proconsul and indicates an arboreal form (Walker and Rose 1968; Gebo et al. 1997; MacLatchy et al. 2000; Harrison 2002). On the basis of its postcranial morphology, Morotopithecus could be considered as belonging to the Hominoidea (Gebo et al. 1997; Harrison 2002). However, Andrews (1992) reported that the morphology of the skull and teeth of Morotopithecus are less derived than in proconsulids, while the upper teeth share derived features with afropithecines. Thus Morotopithecus seems to belong to the Hominoidea given its postcranial morphology, but to pattern with the proconsulids in its cranial and dental characters. It is recognized as a stem hominoid (Gebo et al. 1997; MacLatchy et al. 2000; Harrison 2002). Harrison (2002) raises the question whether the derived features of the vertebral column might be an adaptation to increased orthogrady. As apparent from this overview, a great number of Early Miocene hominoid taxa are included in the proconsulids, but the majority is known from only one specimen or isolated teeth. They are referred to under various names, and as mentioned, their relationships to each other, as well as to the other extinct and extant hominoids, are questionable. Nevertheless, the ancestor of the Early/Middle Miocene hominoids is now deemed to be a member of this group. The reason is that taxa like Proconsul seem to have more similarities to the later hominoids in their various derived characters, while also retaining some primitive features. The derived characters of the face, the teeth, and the postcrania of the proconsulids allow for any one of them to have a close relationship to the younger forms.

The Middle Miocene Compared to the Early Miocene African hominoids, the Middle Miocene ones are few in number. One of the most important taxa is Kenyapithecus, known from Kenya (Leakey 1962) and dated to 14.0 Ma (Kelley and Pilbeam 1986). It is a medium-sized hominoid with clear canine fossa, highly zygomatic arches, clear sexual dimorphism, strong inferior torus, robust mandibular corpus, less asymmetric P4, large upper molars without lingual cingulum, and a P3 with a honing facet and buccal cingulum (Ward and Duren 2002). Few postcrania of Kenyapithecus are known, but those that have been found display some evolved characters, such as a posteriorly directed medial epicondyle and a wide trochlea in relation to the breadth of the capitulum of the humerus (Andrews and Walker 1976). The phylogenetic relationships of Kenyapithecus are still debated. Kenyapithecus has derived mandibular and dental characters (larger inferior than superior transverse torus, relatively short and wide corpus) that are shared with extant hominoids. Compared to the Early Miocene hominoids, it is characterized by a reduction or absence of cingulum in the molars, an increase of the enamel thickness, large upper premolars relative to the molars, and a more molarized dp3 close to that of Gorilla and Pan (McCrossin and Benefit 1997). All of these features are shared with Ouranopithecus, Sivapithecus, and Griphopithecus.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

Fig. 5 (a) Dryopithecus laietanus, Can Llobateres I, Vallès Penedès, Spain. Cast of the reconstructed skull CLI 18000; (b) Rudapithecus hungaricus, Rudabànya, Hungary. Cast of the mandible RUD-14; the casts are to me by D. Begun

Equatorius is a Middle Miocene African hominoid found in Kenya. It is dated between 15.5 and 14.0 Ma (Feibel et al. 1989; Ward et al. 1999). Equatorius is medium sized, with strong sexual dimorphism, more symmetrical upper premolars, reduced or absent lingual cingulum, less heteromorphic lower premolars, thick enamel, as well as a P3 with a honing facet and variably developed buccal cingulum. It is considered a primitive hominoid, belonging to a derived clade of Afropithecus (Ward and Duren 2002). The morphological characters of the teeth and mandible of Equatorius and Kenyapithecus wickeri suggest that there is no generic difference between the two taxa, which can be synonymized (Benefit and McCrossin 2000). Begun (2000) questioned the generic distinction between Equatorius and Griphopithecus from Europe, suggesting evidence of a biogeographic link between the two. Ward et al. (1999) and Kelley et al. (2000) reported that the incisor, canine, and maxillary morphology of K. wickeri are more derived than in Equatorius and distinguish the two genera. The robust mandible and the large inferior torus of Griphopithecus alpani (known from Paşalar and Çandir, Turkey) are similar to those of Kenyapithecus, but the upper jaw is less robust than that of Equatorius, while the dental morphology is similar (Andrews and Harrison 2005). Moreover, K. wickeri exhibits similarities to the rarely represented hominoid of the Paşalar sample, which are enough to attribute both to the same genus (Martin and Andrews 1993; Ward et al. 1999; Kelley et al. 2000) (see below). The Eurasian Middle Miocene hominoid fossil record is richer than the African one and includes several genera. Griphopithecus was originally found in the locality of Devinska Nova Ves of Slovakia (Abel 1902), and was later recognized in the localities of Klein-Hadersdorf, Austria (Steininger 1967), and Engelswies, Germany, by the species G. suessi (Heizmann 1992; Heizmann et al. 1996), as well as in Paşalar and Çandir, Turkey, by the species G. alpani (Andrews et al. 1996). The fossiliferous site Engelswies is considered the oldest in Eurasia; it is designated to the European Mammal Zone MN 5 (Mein 1999). According to Casanovas-Vilar et al. (2011), the localities of Devinska Nova Ves and Klein-Hadersdorf might be younger than 11.6 Ma, corresponding to the upper part of the European Mammal Zone MN 7 + 8 or younger. A similar uncertainty surrounds the age of the Turkish localities; they are correlated either to the European Mammal Zone MN 5 (Begun et al. 2003) or to MN 6 (Made 2003; 2005), (Fig. 3). Considering these data, it seems that the history of the hominoids in Eurasia starts at ~16.0 Ma. According to Rögl (1999) the physical connection

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

between Africa and Eurasia was gradually completed during this period. Three main migration waves are recognized to have occurred at that time, including the arrival of the hominoids in Eurasia. Griphopithecus is comparable in dental size to Pan, and has a robust mandible, strong superior and inferior transverse torus, very elongated and strongly inclined planum alveolar, and low-crowned molars with rounded cusps, thick enamel, and a buccal cingulum. The few known fragmentary postcrania indicate an arboreal adaptation (Begun 2002; Kelley 2002). Griphopithecus fossils consist mainly of isolated teeth and are difficult to use as evidence for establishing phylogenetic relationships either to the African Middle Miocene hominoids or to the Late Miocene Eurasian ones. The limited maxillary and mandibular fragments from Paşalar preserve mainly primitive hominoid characters (Andrews et al. 1996). The taxon’s relationships with the Late Miocene Eurasian hominoids are not clear. A second, rare Paşalar hominoid was described as a new species under the name Kenyapithecus kizili by Kelley et al. (2008). It shares several characters with the African K. wickeri, such as the robust and moderately deep maxillary alveolar processes, the restricted maxillary sinus, and the zygomatic process which originates almost above the alveolar margin (Kelley et al. 2008). The presence of Kenyapithecus in Paşalar is a piece of evidence linking the African and Eurasian hominoids. A rich sample of Middle Miocene hominoids has been recovered from the Vallès Penedès Basin (Spain). The material was discovered in the long section of Abocador de Can Mata. It is ascribed to three different hominoid taxa: Pierolapithecus catalaunicus, Anoiapithecus brevirostris, and Dryopithecus fontani, (Moyà-Solà et al. 2004, 2009a, b). Pierolapithecus catalaunicus is known by a partial skeleton; it is dated to the European Mammal Zone MN 7 + 8, with an estimated age of ~11.9 Ma (Moyà-Solà et al. 2004). The main characters of Pierolapithecus are a low face, flat nasals, posteriorly situated glabella, highly originated zygomatic arches situated anteriorly at the level of M1, high nasoalveolar clivus, reduced heteromorphy in the premolars, elongated molars, absence of a cingulum, large, low-crowned, and compressed upper canines, strong rib curvature, a large and robust clavicle, and short metacarpals and phalanges. The morphology of the thorax (wide and anteroposteriorly shallow), the lumbar vertebrae, and the wrists indicate suspensory, orthograde adaptations. The facial morphology displays the main derived characters of the extant great apes. Pierolapithecus retains some primitive characters, such as the short phalanges, suggesting palmigrade features. The overall facial and dental structures of Pierolapithecus indicate that it is probably close to the last common ancestor of great apes and humans (Moyà-Solà et al. 2004). The second Spanish hominoid found in Abocador de can Mata, named Anoiapithecus brevirostris, is dated at ~11. 9 Ma (Moyà-Solà et al. 2009a). Despite its primitive features (low-crowned teeth, labial and lingual flare in the cheek teeth, short roots in the canines, heteromorphic cusps in the upper premolars) and the autapomorphic facial morphology, Anoiapithecus shares some characters with the afropithecids and the Middle-Late Miocene hominoids (Moyà-Solà et al. 2009a). According to last authors the combination of some autapomorphic features of this taxon with the kenyapithecines and hominid synapomorphies, as well as the presence of both groups in Eurasia during the Middle Miocene, support the “Back to Africa” hypothesis. Among the Middle Miocene hominoids of Europe, Dryopithecus fontani is one of the oldest known from western and central Europe (Fig. 3). It was originally described from La Grive, France, and is correlated to the European Mammal Zone MN 7 + 8 (Casanovas-Vilar et al. 2011). According to Moyà-Solà et al. (2009b), the facial pattern of D. fontani resembles that of Gorilla; this resemblance could indicate an early member of the hominins or a stem hominid convergent with the lower facial pattern of Gorilla. Page 11 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

The Late Miocene African Late Miocene hominoids are rare; they are represented by few remains, the majority of which have been unearthed only recently. A maxillary fragment of a large-sized hominoid from Kenya has been known since 1982; it is referred to as Samburupithecus kiptalami and dated to 9.5 Ma (Ishida and Pickford 1997). This sole known maxillary fragment has been claimed to have similarities with the modern gorilla by some researchers (Ishida and Pickford 1997), but others have recognized primitive Proconsul features and analyzed it as a survivor of Proconsul lineage during the Late Miocene (Begun 2007). The maxilla of Samburupithecus has some similarities to the Eurasian Ouranopithecus, such as the low origin of the zygomatic arches and the thick enamel; the taxon’s relationships with the extinct and extant hominoids are unclear. A mandibular fragment with extremely worn teeth, as well as some isolated teeth of a hominoid, have been described from Nakali, Kenya as the new species Nakalipithecus nakayamae, with an age of ~9.8 Ma; the Nakali material has strong similarities to Ouranopithecus and is considered a possible ancestor of the latter (Kunimatsu et al. 2007). The isolated canine of Nakalipithecus is similar to that of Ouranopithecus; likely an unworn M3 (KNM-NA46436) from Nakali is similar to that of Ouranopithecus, differing in the more developed buccal cingulum and the slightly smaller width. Except for geographic reasons, these small differences cannot support a different genus; even their age difference is very small and falls within the error range. More and better material from Nakalipithecus will be needed to clarify its relationships to the other Late Miocene hominoids. Chororapithecus known from few isolated teeth from Ethiopia and dated to 10.5-10.0 Ma, is considered as is more closely related to African apes and the human clade than any Eurasian taxon. (Suwa et al. 2007). Although the last authors suggest similarity to the modern Gorilla, the material is very scanty for definite conclusions. Some hominoid remains from the Latest Miocene of Africa (Fig. 3) provide more interesting data about the evolution of apes and hominines. A few mandibular and postcranial remains of a hominoid named Orrorin have been found in Kenya; the locality is dated at ~6.0 Ma (Senut et al. 2001). Orrorin is characterized by jugal teeth that are smaller than those of australopiths, a small dentition relative to body size, large and not shovel‐like I1, short C, relatively deep mandibular corpus, and small M2 and M3 with thick enamel. The femur has a spherical head rotated anteriorly, an elongated neck with oval section, and a mesially salient lesser trochanter. The humerus has a vertical brachioradial crest, and the proximal manual phalanx is curved (Senut et al. 2001). Orrorin preserves some primitive ape characters (deep mandibular ramus, anterior teeth, and P4), as well as some more hominid ones (postcanine megadontia, postcranial pieces of evidence of bipedalism). According to Pickford et al. (2002), the femur of Orrorin shares some derived features with australopiths and Homo, but none with Pan or Gorilla, and among the Hominidae, it is closer to Homo than to australopiths. In 2001, a skull with some mandibular and dental remains of a Late Miocene hominoid named Sahelanthropus tchadensis were found in Chad; the associated mammal fauna indicates a Latest Miocene age, 6.0–7.0 Ma (Brunet et al. 2002). The taxon is characterized by weak prognathism, a small braincase, a long and narrow basicranium, large canine fossa, a small and narrow U-shaped dental arch, a very wide interorbital distance, a thick and continuous supraorbital torus, relatively small incisors and canines, rounded cusps in the molars, and moderate enamel thickness (Brunet et al. 2002). Sahelanthropus exhibits several primitive features, like the small braincase, the morphology of the basioccipital bone, and the position of the petrous portion of the temporal bone. But it also preserves a set of derived features, such as small apically worn canines, mediumthick enamel, a horizontally oriented and anteriorly situated foramen magnum, reduced prognathism, a large and continuous supraorbital torus, and the absence of canine diastema, which indicate Page 12 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

close relationship to the hominid clade. On the basis of the presence of this mosaic of characters and the age of Sahelanthropus, Brunet et al. (2002) suggested that it belongs to the hominid clade and is closer to the common ancestor of Homo and chimpanzees. Contrary to this opinion, Wolpoff et al. (2002) concluded that the dental, facial, and cranial characters of this skull cannot define its position among hominids. The sparse material of both Orrorin and Sahelanthropus does not permit clear definition of their phylogenetic relationships with each other and with the other hominids. Given that there is little evidence for the presence of hominoids in the time interval from ~7.5 to 4.5 Ma, these two Late Miocene African hominoids constitute a link between the Miocene and Plio-Pleistocene hominids. The Late Miocene Eurasian hominoids show impressive diversification and include the first indication of a relationship with the great apes and human clade. Different opinions have been expressed about their taxonomy and evolutionary relationships. They are classified with the pongines (Moyà-Solà and Köhler 1995, 1996), the dryopithecines (Casanovas-Vilar et al. 2011), and the hominines (Begun 2009, 2013) or, alternatively, as a dead group without relationship to the modern apes (Kunimatsu et al. 2007; Suwa et al. 2007). The earliest known Late Miocene European hominoid is Rudapithecus from Rudabanya, Hungary, with an age of ~10.0 Ma (Kordos and Begun 2002). At the same time Hispanopithecus appeared in Spain (Casanovas-Vilar et al. 2011). Two skulls of Rudapithecus are known, which are characterized by a short face, an elongated neurocranium, weak but distinct supraorbital torus, biconvex vertically directed and relatively short premaxilla, narrow nasal aperture, high and broad root of the zygomatic arches situated above the mesial half of M2, shallow canine fossa, large interorbital distance, squared-to-rounded orbits, and a reduced foramen incisivum with short incisive canal (Kordos and Begun 1997, 2001). The cranial capacity of the Rudabànya skulls is estimated at a mean 320 cm3 for RUD‐77 and 305 cm3 for RUD‐197–200 (Kordos and Begun 1998, 2001). Rudapithecus shared a significant number of craniodental characters with the great apes and hominines (Begun et al. 2012; Table 1) and could be related to the ancestor of these groups. The postcranials of Rudapithecus preserve a mixture of characters between Pongo and the great apes. The humerus, ulna, femur, and phalanges are similar to those of the great apes, while the wrist bones have mixed pongine and great ape characters (Begun 1993; Begun and Kordos 2011). Hispanopithecus is also known by a rich sample from the Vallesian of Spain (Fig. 3), including a partial face and skeleton (Moyà-Solà and Köhler 1995, 1996). The morphology of a lumbar vertebra suggests orthogrady, as in the modern great apes, while the femur and the phalanges are reminiscent of Pongo (Moyà-Solà and Köhler 1996; Almècija et al. 2007). Despite the mixed clues about their taxonomy, these early Late Miocene hominoids give strong indication of more affinities with the modern great apes and human clade than the Middle Miocene ones. They share several derived characters with the younger hominids and recent great apes, linking the Early Miocene African with the Late Miocene Eurasian hominoids. A well-known hominoid from the eastern Mediterranean region is Ouranopithecus, which is represented by the two species O. macedoniensis and O. turkae, while one P4 from Bulgaria also bears strong similarities to this genus (Bonis et al. 1973; 1990; Bonis and Koufos 1993, Koufos and Bonis 2004; Koufos 1993, 1995; G€ uleç et al. 2007; Spassov et al. 2012). The type species O. macedoniensis is known from three localities in northern Greece by numerous craniodental remains. All localities are correlated to the Late Vallesian or to European Mammal Zone MN 10. The bio- and magneto-chronology suggest an age between 9.6 and 8.7 Ma (Koufos 2006, 2013). O. macedoniensis has a large body size, in the range of variation of gorillas. There is strong sexual dimorphism expressed in the overall size of the dentition and in the size and morphology of the canines. In brief, the morphological characters of O. macedoniensis (Fig. 6) are as follows: a wellPage 13 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

developed supraorbital torus with a small glabellar depression, large interorbital distance, relatively short nasals, small, low, and quadrangular orbits, primitive nasoalveolar area with a large fossa incisiva, strong and low-rooted zygomatic arches, narrow and convex mandibular condyle, low and thick horizontal ramus, long planum alveolare with well-developed fossa genioglossa, strong superior and inferior torus, shovel-like incisors, relatively reduced canines, relatively symmetric upper premolars, low cusps in the molars, more symmetric P3 without honing facet, thick enamel, and an absent or very weak cingulum (Bonis and Melentis 1977, 1978, 1985; Bonis and Koufos 1993; Koufos 1993, 1995; Bonis et al. 1998; Koufos and Bonis 2004). The species is a hard-object feeder (Merceron et al. 2005, 2007), living in an open environment with shrubs, bushes, and small trees, and thick grass floor such as savannah woodland (Bonis et al. 1992, 1999; Koufos 1980, 2006). The phylogenetic position of O. macedoniensis among the hominids is very important, as it shares several derived characters with Australopithecus and Homo. Some of these characters are discussed in more detail below.

Fig. 6 Ouranopithecus macedoniensis, Axios Valley, Macedonia, Greece. (a) Male skull from Xirochori-1, XIR-1; (b) female mandible from Ravin de la Pluie, RPl-54, HOLOTYPE; (c) male maxilla from Ravin de la Pluie, RPl-128; (d) male mandible from Ravin de la Pluie, RPl-55 Page 14 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

The lateral outline of the upper face is a derived character, since in primitive Early–Middle Miocene hominoids it was more oblique, while in O. macedoniensis it is more vertical. The glabella–nasion–prosthion angle is 120 , while in the fossil and extant apes it reaches 140 . In Australopithecus africanus it is 115 and in A. boisei 150 , because of the flattening of the face (Bonis and Koufos 1993). The structure of the naso-alveolar area of O. macedoniensis belongs to the primitive “African pattern,” as also seen in Dryopithecus and Gorilla. It is different from that of Pongo and Sivapithecus, while it is closer to Australopithecus (Bonis and Melentis 1987; Bonis and Koufos 1994). However, it is more derived than Proconsul and Morotopithecus and less derived than Australopithecus afarensis and the recent chimpanzee. The narrow mandibular condyle of O. macedoniensis is a more hominine-like character. In the apes, the mandibular condyle is only slightly convex, while in Homo it is narrower and more convex. In A. afarensis it is more apelike (Bonis and Koufos 1997, 2001). The narrowness of the mandibular condyle can be measured by the index [cranial–caudal diameter  100/medial–lateral diameter]. In O. macedoniensis this index is 44.4, in A. robustus 33.8, in modern Homo 41.4–45.7, in Gorilla 46–56, in Pan 47–53, and in Pongo 43.3–43.9 (Bonis and Koufos 1993). Both the narrowness and the shape of the mandibular condyle are related to the form of the temporomandibular joint. The latter is large and relatively flat in apes, while in hominines its anterior part is cylindrical and followed by a mediolateral directed fossa (Picq 1990). The capitulum of the O. macedoniensis mandible could correspond to the latter kind of temporomandibular joint. The cingulum is absent or very weak in all cheek teeth of O. macedoniensis; compared to the strong cingula of Proconsul and the pliopithecids; this is a derived character. The presence of accessory cusps (cuspids) at the distal ends of the upper and lower third molars, as in Australopithecus afarensis, is a derived character for O. macedoniensis – one that is related to the function of the teeth. The enamel thickness relative to the body weight of O. macedoniensis can be compared to that of some australopiths (Paranthropus, Australopithecus africanus),but it is thicker than in Dryopithecus, Sivapithecus, Proconsul africanus, P. major, Gorilla, Pan, and Pongo (Bonis and Koufos 2001). Thus, enamel thickness could be a primitive feature relative to the recent hominoids, but derived when compared to the Early–Middle Miocene hominoids. Enamel thickness depends also upon the hardness of the food. A change to a more open environment, such as woodland or wooded savannah, is associated with harder food items. In the eastern Mediterranean an environmental change which brought about more open habitats occurred at the end of the Middle Miocene (Koufos 2006), leading to thick enamel in hominoids like Ouranopithecus and Ankarapithecus. At the same time, in western and central Europe the environment continued to be more forested (until the Middle Vallesian), and correspondingly the hominoids from those regions are thin-enameled (Dryopithecus, Rudapithecus). The morphology of the P3 in O. macedoniensis (not elongated, rounded occlusal outline, more symmetric buccal face, absence of a honing facet, less oblique protocristid) distinguishes it from the apes. The wear pattern of the crown in the P3 is similar to that in Australopithecus afarensis, as a result of the absence of a honing facet in both forms and the similar function of the tooth (Bonis and Koufos 2001). Indeed, the wear pattern of the whole dentition of O. macedoniensis is similar to that of A. afarensis (Koufos and Bonis 2006). The size of the upper canine of O. macedoniensis is a derived character. The plesiomorphic characters of the canine are the high, buccolingually flattened crown and the presence of a sharp distal crest on the buccolingual surface. This feature is present in cercopithecids, as well as in extant and Early–Middle Miocene hominoids. The shape of the canine is more rounded and in this respect very close to Australopithecus afarensis. The height of the upper canine of O. macedoniensis is Page 15 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

relatively reduced (Bonis and Koufos 1993), while its morphology is completely different from that of the primitive hominids. The height of the crown is less reduced than in Australopithecus afarensis (Johanson et al. 1982). In comparison, the canine of Proconsul is three times larger than that of O. macedoniensis. The size of the canine compared to the size of the cheek teeth is also small in O. macedoniensis, and is similar to that in Australopithecus afarensis and female Gorilla. It is much larger (more than 120) in the Early–Middle Miocene and extant hominoids (Bonis and Koufos 1993). In regards to the lower deciduous dentition, O. macedoniensis shares some derived characters with the Plio-Pleistocene hominines. The deciduous canine of O. macedoniensis is more reduced, compared to the molars, than that of Proconsul and Ardipithecus, but less reduced than that of australopiths and Homo. The lower deciduous premolars of O. macedoniensis are more derived than in Early–Middle Miocene and recent hominoids, and less derived than in australopiths and Homo (Koufos and Bonis 2004). All of these characters suggest that O. macedoniensis has strong relationships to the PlioPleistocene hominines: it shares several derived characters with them and can be considered their ancestor. A cladistic analysis of 22 derived characters of O. macedoniensis shared with the extinct and extant hominoids, as well as with Australopithecus and Homo, suggests that (i) O. macedoniensis can be included in the subfamily Homininae; (ii) the splitting of Homo and the African apes is dated at more than 9.5 Ma; and (iii) O. macedoniensis can be considered a sister group to Australopithecus and Homo (Bonis and Koufos 1997). O. macedoniensis also has several characters similar to those of australopiths; some of them are plesiomorphic (shape of symphysis, large interorbital distance, shallow or absent supratoral sulcus, large M3, development of nasomaxillary area). However, it preserves a set of apomorphic features. Some of them, such as thick-enameled teeth or canine reduction, may be homoplasies, but it would be peculiar and exceptional for all of them to be homoplasies (Bonis and Koufos 1999). There are some differences of opinion concerning this hypothesis. Begun (1992) suggests a relationship between Gorilla and O. macedoniensis and concludes that Dryopithecus has slightly more evidence (gnathic structures and positional behavior) in its favor for being ancestral to African apes and humans. But the postcranial morphology, and consequently the positional behavior of O. macedoniensis, are unknown. The two available phalanges of O. macedoniensis are different from those of all arboreal primates and closer to terrestrial forms. Begun (2002, p. 365) states that “it is not clear which taxon, Dryopithecus or Ouranopithecus, comes closer to the ancestral morphology of the African apes and humans”. Although he gives a slight precedence to Dryopithecus, he refers that the unknown positional behavior of Ouranopithecus is a disadvantage. Begun subsequently links O.macedoniensis with the dryopithecines (Dryopithecus, Hispanopithecus, Rudapithecus) “as a group that is the sister clade to African apes and humans” (Begun 2009). Earlier, Andrews et al. (1996) made the statement that O. macedoniensis “is recognized as a hominine, related to the African ape and human clade and possibly close to the ancestry of the living species of this group.” In their phylogeny of the Hominoidea, O. macedoniensis is the possible ancestor of the gorilla, chimpanzee, and humans (Andrews et al. 1996, Fig. 12-7). Benefit and McCrossin (1995) considered O. macedoniensis to be linked with the African ape and human clade, because of the presence of a supraorbital torus and the rectangular orbits. They also link Samburupithecus with Ouranopithecus, suggesting that the former may be a potential candidate for membership in the African ape and human clade. However, the dental morphology of Samburupithecus differs from that of Ouranopithecus in having more voluminous and higher cusps. Recently Clarke (2012) noted that “the one Miocene ape that does show remarkable dental similarity to the early hominid Australopithecus is Graecopithecus-Ouranopithecus macedoniensis.” Page 16 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

The first edition of this handbook (Koufos 2007, p. 23), in discussing the phylogenetic position of O. macedoniensis and the various opinions about it, stated: “But Africa is a huge region and who knows what will be discovered in the future.” Indeed, two new articles, published in the same year, described new Late Miocene hominoid material from Kenya and Ethiopia (Kunimatsu et al. 2007; Suwa et al. 2007). Despite the poor material, both samples have similarities to O. macedoniensis, especially Nakalipithecus, and might belong to the subtribe Ouranopithecina of Begun (2009), linking the Late Miocene African and Eurasian hominoids. Ouranopithecus turkae is a new species found in Turkey (G€ uleç et al. 2007); together with the sole P4 from Bulgaria (Spassov et al. 2012) they represent the Turolian evidence for hominoids in Eurasia. Its classification as Ouranopithecus has been questioned (Begun 2009), although it does have similarities with this genus, as well as with Indopithecus (Begun 2013). Another Asian Late Miocene hominoid is Ankarapithecus, found at Sinap Tepe (Turkey) and known from three cranial remains. This hominoid is dated at ~10.0 Ma (Kappelman et al. 2003) and seems to be slightly older than Ouranopithecus. It was interpreted as having relationships with hominids (Alpagut et al. 1996), but recent analysis indicates phylogenetic relationships with the Sivapithecus–Pongo clade based on shared characters (massive maxilla, broad nasal aperture, highplaced zygomatic arches, narrow interorbital distance, very elongated nasal bones, absence of real supraorbital tori) (Begun and G€ uleç 1998). Thus, Ankarapithecus seems to be closely related to Sivapithecus and recent Pongo or to the Asian hominoids. Oreopithecus is known from Italy only, where it has been found at the localities of Bacinello, Casteani, Ribolla, Montebamboli, and Fiume Santo and is in each case associated with an endemic fauna (Rook et al. 1999). The localities have been dated to the Middle–Late Turolian (Late Miocene), or at about 6.0–7.0 Ma (Harrison and Rook 1997; Steininger 1999). Oreopithecus is known by numerous cranial and postcranial remains, including a complete skeleton. It can be considered the best-represented European Late Miocene hominoid. The very small braincase, low zygomatic root, short and gracile premaxilla, long and narrow palate, narrow nasal cavity, projecting midface, and relatively high canines of Oreopithecus are primitive features distinguishing it from all great apes (Begun et al. 1997; Harrison and Rook 1997). The postcranial morphology of Oreopithecus resembles that of the hylobatids and is related to suspensory positional behavior. It is also similar to that of the hominids and is related to large body mass in suspensory quadrupeds, with powerful grasping and high joint mobility (Harrison and Rook 1997). The majority of the morphological characters of Oreopithecus indicate that it is the most primitive known great ape (Harrison 1986b; Harrison and Rook 1997). Nevertheless, some researchers instead consider it a highly derived member of the clade including all Eurasian Late Miocene hominoids (Moyà-Solà and Köhler 1995, 1997) and is situated at the base of the hominoid radiation representing ancestral hominid morphology (Harrison and Rook 1997; Begun 2002). However, it is necessary to keep in mind that Oreopithecus belongs to an endemic fauna and that some of its characters may be secondary adaptations to the local conditions. There are a number of Asian hominoids, like Sivapithecus, Indopithecus, Khoratpithecus, and Gigantopithecus (Andrews et al. 1996; Kelley 2002; Chaimanee et al. 2006; Jaeger et al. 2011), which are known from ~12.0–7.0 Ma. All these hominoids have strong relationships with the modern orangutan and are related to the Pongo clade. Besides the Middle Miocene Griphopithecus and Kenyapithecus and the late Miocene Ouranopithecus, there is another Asian hominoid, Udabnopithecus garedziensis from Georgia. The known material includes two molars; Udabnopithecus is somewhat confusingly classified either as Dryopithecus (Andrews et al. 1996; Gabunia et al. 2001) or under its original name (Lordkipanidze et al. 2008). The concentration in the most western part of Asia of these Middle–Late Miocene hominoids that are related to the great apes Page 17 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

and the human clade, while in the rest of the continent only pongines have been found, indicates that Asia Minor was a migration route from Africa to Eurasia and vice versa.

Conclusion The ancestor of the hominids and recent great apes is included in the stem of the Miocene hominoids, the common stock of hominids and apes. Despite the great expansion of the hominoid fossil record during the last decades, that fossil record is still quite poor and limits analysis and conclusions. From millions of hominoids that lived for a long time (
20 Ma), only very few and fragmentary remains are available, based on which scientists are trying to complete the chain of hominid evolution link by link. The absence of some links makes their work more difficult, and at times even the discovery of a possible link may cause more problems than it solves. The limited conclusions we can draw based on recent data and known material include the following: • Oligocene Aegyptopithecus and Kamoyapithecus could be the possible ancestor of the Miocene hominoids, as they share some derived features with the early hominoids. However, the large time gap between these taxa, and between them and the first proconsulids, is a source of uncertainty. • Among the Early Miocene hominoids, Proconsul is the most plausible link connecting the hominoids to the modern great apes and the hominines. Controversy over particulars notwithstanding, it can be said to display a mosaic of features that indicate relations to the extant great apes and humans. Several other hominoid taxa known from the Early Miocene might also represent the sought-after link; but their limited and fragmentary material prevents definite comparisons and results. • The Middle Miocene hominoids of Europe seem to be an important group, which could include a possible link. Certain Middle Miocene hominoids from Africa could also represent a link, but their poor material does not allow reliable comparisons, and their relationships to other taxa are still being discussed. • The overall cranial and dental morphology of Ouranopithecus seems to be closer to the hominids; possibly it is this taxon that constitutes the Late Miocene link connecting the hominoids to the extant great apes and humans – either as a sister group to Australopithecus and Homo (Bonis and Koufos 1997) or as a sister clade to the African apes and humans (Begun 2009). • The similarities of Sahelanthropus and Ouranopithecus (Brunet et al. 2002) indicate a close relationship between them, narrowing the gap between Ouaranopithecus and Australopithecus. • All known Asian hominoids, such as Sivapithecus, Indopithecus, Ankarapithecus, Khoratpithecus, and Lufengpithecus, are closely related to the modern orangutans. The question of human origin will preoccupy scientists for a long time. Each new discovery will add further data, but will also raise new questions and possibly controversies. Despite these challenges, it is very important that scientists continue their effort to collect more material and study all fossil and modern hominoids in systematic detail, in order to better understand their evolutionary relationships. Continued research efforts and the development of new methods will bring us ever closer to a full understanding of human origins.

Page 18 of 26

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_44-7 # Springer-Verlag Berlin Heidelberg 2013

Acknowledgments I wish to thank very much Prof. H. Henke and Prod. I. Tattersall for inviting mr to participate in the Handbook of Palaeoanthropology. I also Thank Dr I. Sylvestrou for her nice work on figures 1 and 4l.

Cross-References ▶ Fossil Record of Miocene Hominoids ▶ Hominoid Cranial Diversity and Adaptation ▶ Postcranial and Locomotor Adaptations of Hominoids ▶ Primate Life Histories ▶ Primate Origins and Supraordinal Relationships: Morphological Evidence ▶ Role of Environmental Stimuli in Hominid Origins ▶ The Biology and Evolution of Ape and Monkey Feeding ▶ The Origins of Bipedal Locomotion ▶ The Species and Diversity of Australopiths

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

Defining Hominidae Jeffrey H. Schwartz* Departments of Anthropology and History and Philosophy of Science, University of Pittsburgh, Pittsburgh, PA, USA

Abstract A array of relevant cranial, postcranial, and dental morphologies are reviewed in an attempt to delineate shared derived features that would unite a group that includes extant humans and their fossil relatives to the exclusion of other hominoids. This group is now often referred to as tribe Hominini, but systematic practicality suggests that family Hominidae be retained, since the lower rank de facto limits even current, and certainly future, recognition of subclades. Potential hominid postcranial synapomorphies include a distinct angle at L5–S1, a long pubic ramus, a superoinferiorly short ilium that is roundedly expanded posteriorly, some thickening in the region of an iliac (crest) tubercle, a well-developed and knoblike anterior inferior iliac spine that lies noticeably superior to and somewhat back over the superior acetabular rim, a defined and deep greater sciatic notch, differential distribution of cortical bone of the femoral neck, anteroposteriorly long femoral condyles, and an outwardly slanted femoral shaft. Although “a weakly defined linea aspera” and “a concave rather than convex medial tibial condylar facet that lies level with the primitively concave lateral facet with the two facets being separated by a pair of distinct tibial tubercles” have been suggested as hominid apomorphies, this appears not to be the case – unless the apelike specimens commonly taken as hominid (e.g., from Hadar) are not. The only possible cranial feature appears to be alignment in the adult of the biporionic chord and basion (on the anterior margin of the foramen magnum). Derived dental features that might unite Hominidae also characterize an orangutan clade and thus must be explained away (e.g., as homoplasies) or dismissed as phylogenetically relevant in order to justify the former group. Of further note is the presence of Pongo clade-like facial features in australopiths and various specimens of Homo. These and the dental similarities suggest that focusing on Pan alone as the out-group from which to judge hominid-defining features is comparatively too narrow and, consequently, phylogenetically misleading. Within Hominidae, various subclades can be justified, suggesting that the relationships of various specimens referred to genus Homo lie within a clade that also subsumes “australopiths.” Much work remains before clade Hominidae can be more fully defined.

Introduction By the twenty-first century, one would think that paleoanthropology would long ago have left behind the legacy of Linnaeus’ (1735) ultra-vague and systematically useless definition of our species, Homo sapiens: nosce te ipsum (know thyself). Yet, in spite of the incredible number of discoveries of fossils attributed to our clade (i.e., the clade that includes H. sapiens but excludes apes) since the mid-to-late nineteenth century – when discovery of the Feldhofer Grotto Neanderthal and ultimately *Email: [email protected] Page 1 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

the Spy Neanderthals undermined the notion that humans were not antediluvian – the history of paleoanthropology contrasts with that of the centuries-old disciplines of vertebrate and invertebrate paleontology in its increasing rejection of taxonomic and systematic rigor. Consequently, the task of defining Hominidae is not as straightforward as one might imagine it should be.

Historical Background In the first detailed attempt to support Linnaeus’ inclusion of humans within a specific group of mammals, and particularly in grouping humans with apes, Thomas Henry Huxley (1863b) sought evidence of this relationship not only in comparative hard- and some soft-tissue morphology but also in comparative development. Through ontogenetic comparison, he argued that if a monkey could be distinguished developmentally from other vertebrates as a mammal generally, and a primate more specifically, so, too, could humans. Hence, if a monkey was a primate, so, too, was a human. Huxley then turned to “man’s place in nature” within Primates. He began with the premise that humans were most similar to gorillas and then organized his comparisons first between gorillas and, when needed, other apes and then between them and monkeys. His rationale was if a morphological “gulf” existed between gorillas and monkeys, but not between gorillas and other apes, then humans could also be allied with the apes. But while Linnaeus claimed that, in essence, morphology barely distinguished humans from apes (Schwartz 1999), Huxley believed otherwise. Consequently, in spite of demonstrating that anatomies as distinctive as the human foot were basically comparable to the grasping feet of apes and monkeys, Huxley concluded that humans were still sufficiently unique to warrant their own taxonomic status apart from the great apes, all of which he relegated to a separate family. In hard-tissue morphology, Huxley remained as impressed by aspects of the postcranial skeleton as Aristotle had been of the human thumb and Johann Friedrich Blumenbach of the human pelvic girdle and foot. With his emphasis on aspects of the human postcranium and dentition, Blumenbach should be regarded as the “father of paleoanthropology” inasmuch as the criteria he used to distinguish humans from other animals eventually became those that paleoanthropologists used to decide if a fossil qualified as a “hominid” (Schwartz 1999). Indeed, in 1795, in On the Difference of Man from Other Animals, Blumenbach (1969) emphasized various aspects of “the external conformation of the human body” as paramount to defining Homo sapiens: erect posture, broad and flat pelvis, two hands, non-divergent hallux, close-set and serially related anterior teeth, and some aspects of mandibular morphology. With regard to erect posture, Blumenbach argued that, in contrast to other animals, this stance was natural and specific to H. sapiens as noted, for instance, in the ossification of tarsals before carpals. He claimed that only humans have a “true” pelvis, in which the broad and expanded ilia form a basin that cups the viscera. Like Aristotle, he regarded the human hand as special because of its long thumb. In addition, because of the uniqueness of the human foot, with its non-divergent hallux, Blumenbach believed that possession of only two “true” hands was significant. He also considered the human dentition distinctive in presenting orthally implanted lower incisors; canines not longer than, or separated from, the incisors; and molars with rounded cusps. He described the human mandible as quite short, bearing a prominent chin, and having a distinctive articulation with the skull (presumably referring to the depth of the articular fossa), which, he suggested, was correlated with human omnivory. Although he recognized that humans differ from many mammals in lacking a distinct premaxilla, Blumenbach also, but mistakenly, believed that other primates were similar in this regard – a claim Page 2 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

he then used to argue against separating humans from other primates taxonomically. [Goethe (1820) made a similar argument but did so on the incorrect belief that he could identify a premaxilla in humans.] In addition to “the external conformation of the body,” and in keeping with concerns of eighteenth-century philosophers, Blumenbach (as well as Goethe) addressed the “internal conformation” of humans, i.e., the importance of reasoning (as well as other mental attributes) as a criterion by which to distinguish humans from other animals, including other primates. Although not stated in these terms, we might point to a focus on mental attributes as underlying the later emphasis in paleoanthropology on the size and external morphology of the brain [features that also attracted the attention of the eighteenth-century naturalists Buffon and Bonaparte (Schwartz 1987)]. Blumenbach’s criteria for distinguishing humans from other animals were imported into paleoanthropology with the discovery of Homo (Pithecanthropus) erectus from Trinil, Indonesia (Schwartz 1999). This historical twist is likely due to Huxley’s (1863a) argument that the Feldhofer Grotto Neanderthal was an extinct human whose cranial features extended into the past a “perceived” continuum of racial “brutishness” from the most “civilized” to the most “brutish” of living humans. In turn, these notions of ancientness equating with primitiveness and of a continuum that proceeded from a brutish primitiveness to human modernity came to inform much of paleoanthropology (Schwartz 1999). The Trinil specimens, however, undermined Blumenbach’s H. sapiens-defining criteria. While the femur provided evidence of humanlike bipedalism (Blumenbach’s “erect posture”), the skullcap depicted an individual that had been less than fully human in its brain (and thus in its mental capacities). This unexpected combination of human and less-than-human features prompted Dubois to assign his new erectus first to the genus Anthropopithecus (the taxonomic alternative to Pan) (Dubois 1892) and then to Haeckel’s proposed genus for a hypothetical extinct, speechless human relative, Pithecanthropus (¼“ape-man”) (Dubois 1894). The implication, of course, was that the emergence of erect posture and bipedalism preceded expansion and elaboration of the brain. While lending itself to Darwin’s (1871) suggestion of a smooth transition from a semiquadrupedal African ape to an erect bipedal human, this picture – bipedalism first, brain second – appeared contradicted with the discovery in the early 1900s at Piltdown, England, of a large, thin-boned, and rounded humanlike cranium; an apelike partial mandible preserving two molars; and an apelike lower canine. Under the presumption that these specimens were associated, the Trinil-based scenario of human evolution was turned around: early human relatives became human first in their brains and then in the rest of the body (as inferred from the mandible and teeth). That is, the brain enlarged prior to the attainment of fully erect posture and bipedal locomotion. It was not until the 1950s, when the Piltdown fraud was exposed, that this alternative notion of human evolution – brain first, body second – was rejected. Before then, however, the discovery of the Taung child and, more importantly, Dart’s (1925) interpretation of the specimen continued the intellectual trajectory Blumenbach had begun. But Dart conceived his scenario in the context of Darwin’s incorrect biogeographic premise of finding fossil evidence in Africa of intermediate forms that provided evidence of a morphological continuum between African apes and humans. As Dart (1925, p. 196) summarized his overall impression of the preserved craniodental features of the Taung specimen, this individual represented “an extinct race of apes intermediate between living anthropoids and man.” Dart depicted specific features – such as the configurations of the brow, nasal bones, zygomatic regions, orbits, and upper and lower jaws as well as the inferred skull shape – as being of “delicate and humanoid character” (Dart 1925). Most central to his speculations were the size and potential details of the preserved partial endocast and also the forward position of

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

the foramen magnum (as indicated by bone adherent to the endocast). Dart (1925, p. 197) assumed the latter was proof of this “humanoid’s” erect posture and then made the following extrapolations: The improved poise of the head, and the better posture of the whole body framework which accompanied this alteration in the angle at which its dominant member was supported, is of great significance. It means that a greater reliance was being placed by this group upon the feet as organs of progression, and that the hands were being freed from their more primitive function of accessory organs of locomotion. Bipedal animals, their hands were assuming a higher evolutionary rôle not only as delicate tactual, examining organs which were adding copiously to the animal’s knowledge of its physical environment, but also as instruments of the growing intelligence in carrying out more elaborate, purposeful, and skilled movements, and as organs of offence and “defence”. The latter is rendered the more probable, in view, first of their failure to develop massive canines and hideous features, and secondly, of the fact that even living baboons and anthropoid apes can and do use sticks and stones as implements and as weapons of offence.

Regarding the Taung child’s brain (as represented by the endocast), Dart suggested that, since it was already as large as a chimpanzee’s and almost as large as a gorilla’s, it would have continued to enlarge, following a humanlike growth curve. In addition, as in humans but not apes, the Taung child’s brain was high and rounded, somewhat expanded in the temporal region, and apparently a posteriorly and inferiorly placed lunate sulcus. Believing his specimen to be more human- than apelike, Dart inferred that this “humanoid” had also been humanlike in its faculties of “associative memory and intelligent activity.” The expanded cerebral cortex (as indicated by the presumed lunate sulcus) also suggested to Dart that, in contrast to apes, the Taung “humanoid” had experienced increased sensory stimulation, both via vision (because of the forward position of the approximated orbits) and tactile sensation (because erect posture and bipedality supposedly freed the hands from involvement in locomotion). But the Taung child’s brain was not sufficiently enlarged in the temporal region for it to have reached the “necessary milestone in the acquisition of articulate speech” (Dart 1925, p. 198). For Dart, the Taung child, the name bearer of his genus and species Australopithecus africanus, displaced both Piltdown’s Eoanthropus dawsoni and Trinil’s Pithecanthropus erectus as viable “links” between humans and their apelike ancestors. Indeed, in spite of Dart’s conceiving this extinct juvenile as intermediate between humans and apes, his interpretation reflected Blumenbach’s criteria for distinguishing Homo sapiens. In 1925, then, in spite of their differences, the three scenarios regarding human ancestry embraced the notion of an evolutionary continuum that proceeded from an apelike precursor, through an unknown series of intermediates, to the most modern looking of living humans. In terms of the focus of this chapter – defining Hominidae – subsequent discoveries of potential extinct human relatives are less relevant than attempts to integrate these fossils into a systematic framework that had originally been based on living Homo sapiens. In this regard, after a decade-anda-half of successful fossil hunting in the limestone caves of South Africa and in caves and deposits in Europe and Asia, and a proliferation of genus and species names, and debates over the relationships of what I will refer to as “australopiths” (based initially on South African specimens), Clark (1940) was compelled to review the available evidence in order to determine the hominid status of any australopith. In addition to echoing Huxley and Darwin’s assumption of a linear transformation from ape to human, Clark based his conclusions on what he later called the “total morphological pattern” (Clark 1955). From this perspective, he considered a fossil as being hominid not in terms of derived features it shared with humans but whether, overall, it resembled humans more than great apes. As will become obvious, this approach complicated matters further because the great apes were then considered evolutionarily united. Thus, a feature to compare with humans or potential hominid

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

fossils could be extracted from any ape and deemed exemplary of the entire group, even if it only characterized the one ape [Gregory (1922) employed this device of “pick and choose” in arguing for an African ape-human relationship (Schwartz 2005)]. The irony of Clark’s phenetic approach is that in 1955 he made one of the clearest statements about distinguishing between primitive and derived characters in generating hypotheses of relatedness. Although Clark (1940, p. 317) concluded that australopiths were “more human than simian” especially in their teeth, his comparisons then and in subsequent publications were biased toward the African taxa. If, however, he had included Pongo, he might have been struck by the similarities between this hominoid and australopiths in many details of facial and dental morphology (Schwartz 2004a, 2005). Perhaps then he might have expanded his comparisons to include at least small-bodied hominoids and some Old World monkeys, thereby providing paleoanthropology with the precedent of a more broad-based approach to phylogenetic reconstruction. Unfortunately, he did not, thus making his efforts to define Hominidae as useless as his definition of the order Primates [i.e., being characterized by their lack rather than sharing of derived feature/s (Clark 1959)]. Mayr’s (1950) influential article on fossil hominids did not clarify the situation. Rather, on the grounds that all hominids were adaptively similar because they were bipedal, Mayr collapsed all named taxa into one genus, Homo. After claiming that because living humans are so diverse and occupy all available econiches the same had been true for all hominids (thus precluding the opportunity and prerequisite for speciation) (Mayr 1963), he subdivided his genus Homo into three time-sequential species: transvaalensis, erectus, and sapiens. Even though a much enlarged human fossil record later provoked Mayr (1953) to “accept” Australopithecus and acknowledge also Paranthropus, but as side branches that went extinct without issue, his concession did not elucidate how one determined in the first place if a specimen was hominid, especially if postcranial remains were unknown. This is, indeed, a problem. For while it may be true that some scholars (e.g., Clark, Mayr, Washburn) decided “that the most important single factor in the evolutionary emergence of the Hominidae as a separate and independent line of development was related to the specialized functions of erect bipedal locomotion” (Clark 1964, p. 14), the preponderance in the human fossil record of usually fragmentary skulls and jaws and isolated teeth makes impossible identifying a specimen as “hominid” on the basis of anatomical features believed to be reflective of bipedal locomotion. The cranial exception, of course, is the region of the foramen magnum and occipital condyles.

Toward a Definition of Hominidae The task of defining Hominidae is twofold. First is a taxonomic decision. How expansive is the classificatory net Hominidae? To chimpanzees? Chimpanzees and gorillas? All great apes? Although Clark (1955, 1964) wrote at a time when all great apes were relegated to the taxonomic family, Pongidae, his rationale for recognizing family Hominidae is, I believe, still viable and useful. Namely, Hominidae is a monophyletic group that subsumes extant humans and their fossil relatives, to the exclusion of any living relative. (It is in this sense that I use Hominidae/hominid/hominids throughout this contribution.) Accepting this proposition does not impinge on one’s preferred version of ape as closest living human relative. Further, it also allows more systematic space in which to accommodate the still taxonomically expanding human fossil record – which collapsing Pan and all hominids into genus Homo, on the grounds that this is “cladistic” (Goldberg et al. 2003), obviates. Indeed, the only thing “cladistic” about this, in the spirit of Hennig (1966), is translating

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

a preferred scheme of relationship directly into a classificatory representation of it – which is not the same as generating the theory of relationship. With this suggestion in mind, we can turn to the matter of defining Hominidae, but not from the perspective of looking for the “defining” moment in a transition from a presumed apelike condition to something seemingly hominid (either by a subtle hint of a supposed hominid trait or traces of a presumably primitive and retained feature). Rather, it seems logical and reasonable to return to Blumenbach’s list of criteria, to which other features have been added, as defining a clade that includes humans and their extinct relatives.

Defining Characters of Hominidae? Traditionally Accepted Features of “Erect Posture”

As reviewed above, Blumenbach’s emphasis on “erect posture” and “two handedness” – or, as Clark (1964, p. 14) put it, on “specialized functions of erect bipedal locomotion” – has remained central to considerations of our clade. Pilbeam (1972, p. 62), for example, summarized some of the “adaptations” apparently associated with these “specialized functions of erect bipedal locomotion”: a vertebral column with a distinct lumbar curve that is set at a sharp angle relative to the sacrum; a “carrying angle,” wherein the lateral femoral condyle is larger and more weight bearing than the medial condyle and the femoral shaft angles up and laterally away from the knee joint; a non-grasping foot with short toes and non-divergent hallux through which weight is transmitted during locomotion; and metacarpals in which the heads contact the substrate while the distal ends are elevated to form a springlike, transverse arch. We might also include Blumenbach’s description of the pelvic region as bowl shaped (i.e., broad and shallow) and having a short, potentially laterally flaring, posteriorly expanded, anteriorly truncated ilium; a somewhat forwardly oriented acetabulum (which is also reflected in the orientation of the proximal femur relative to the shaft); a defined greater sciatic notch; and a broad, short sacrum, wherein the alae are not remarkably small relative to the size of the lumbar facet (Schultz 1968). Clearly, these features distinguish living Homo sapiens from other extant primates. However, the degree to which these characteristics are expressed in what have been identified as fossil hominids, and whether the appropriate postcranial remains are known, is still up for debate. For instance, among fossil specimens attributed to “anatomically modern” Homo sapiens that probably represent this taxon (Schwartz and Tattersall 2000a, b; Schwartz and Tattersall 2003, 2010), only Qafzeh 9 is known from a fairly complete, albeit extremely crushed, postcranium. Inasmuch as distortion of its skull and mandible compromises definitive identification of a bipartite brow with a “glabellar butterfly” and a mandible with a “true” chin with an inverted “T” configuration and thickened inferior symphyseal margin (Schwartz and Tattersall 2000a, b; Schwartz and Tattersall 2003, 2010), the pelvic region appears to present H. sapiens, not Neanderthal, morphology (Rak 1990) (personal observation). Other cranial and/or mandibular specimens conventionally attributed to “anatomically modern” H. sapiens and preserving critical morphology, especially Qafzeh 6 and all from Skhul, do not present a bipartite brow or an inverted mandibular symphyseal “T” (Schwartz and Tattersall 2000a, b). Known Skhul postcranial remains are incompletely representative and so crushed and poorly reconstructed that one can only sense their conforming to the abovementioned pelvic configurations (personal observations). While Neanderthal postcranial morphology associated with bipedal locomotion differs from Homo sapiens in details of size, shape, and morphology [e.g., more posteriorly expanded ilia, superoinferiorly tall and anteroposteriorly compressed pubic symphyseal region, relatively long Page 6 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

pubic ramus (and thus very wide/obtuse subpubic angle), smoothly “hook-shaped” greater sciatic notch, smaller and differently oriented iliac auricular region, relatively large proximal and distal femoral ends, very large acetabulum, truncated calcaneus (Rak 1990; Sawyer and Maley 2005; Trinkaus 1983; Trinkaus and Howells 1979)], they conform to the basic configurations summarized above, including a femoral “carrying angle” and a lumbar curve. Known Middle Pleistocene pelvic remains from Sima de los Huesos (Arsuaga et al. 1997), Arago (Day 1982) (personal observation), and Jinniushan (Rosenberg and Lu 1997) differ from Homo sapiens in some iliac details (e.g., flare, anterior superior iliac spine) but can otherwise be accommodated by Pilbeam’s pelvic criteria. The Sima de los Huesos femora also present a carrying angle (Day 1986). According to Rose (1984), os coxae KNM-ER 1808, KNM-ER 3228, and OH 28 are generally similar to Homo sapiens and H. neanderthalensis but differ in having relatively larger anterior iliac regions. Scrutiny of OH 28 (cast) reveals, however, that this specimen contrasts with H. sapiens as H. neanderthalensis does, e.g., in asymmetry of anterior versus posterior iliac proportions and curvature, thickness and anterior position of the external iliac pillar, thickness of the ilium posteriorly, and small size of the auricular surface (personal observation) (Fig. 1). Further, although Day (1986) claimed morphological similarity between OH 28 and Arago XLIV, the latter clearly differs not only in the massiveness of its ilium but in details such as a sigmoidally symmetrical and shallow anteroposterior iliac crest curvature, deep and uniform greater sciatic notch angle, large auricular surface, and huge acetabulum (personal observation) (Fig. 1). These inconsistencies raise questions not only about the suggested similarities between the pairs previously compared OH 28-Arago XLIV, KNM-ER 1808–3229, and Nariokotome KNM-WT 15000-Gona BSN49/P27 partial os coxae, but also about similarities claimed to exist among them all (Day 1986; Simpson et al. 2008; Walker and Leakey 1993). A preliminary reassessment of the comparability of these OH, Arago, KNM, and BSN pelvic specimens based on casts and published images proves potentially interesting. For example, when

Fig. 1 Os coxae of Homo sapiens and various hominids with the ilium oriented laterally. Note differences in development of iliac pillar in H. sapiens, Arago XLIV, and OH 28, and virtual nondevelopment in “australopiths.” Also note differences in anterior and posterior iliac expression and especially in orientation of the acetabulum, which, if in the anatomical position, would reposition the ilium of all but H. sapiens posteriorly. See text for further discussion; not to scale; rev reversed (All specimens except H. sapiens and Sts 14 courtesy of the American Museum of Natural History) Page 7 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

orienting the acetabula in anatomical position, the “inner” iliac blade surfaces of all specimens face forward/anteriorly, as they do in Sts 14 and Al 288-1, and not medially, as in H. sapiens, H. neanderthalensis, and SK 50. Further, reconstructions of KNM-WT 15000 (e.g., as in the Neanderthal Museum) and the Gona pelvis, BSN49/P27 (Simpson et al. 2008), portray the respective ilia tilting laterally outward with their “inner” surfaces turning somewhat upward, albeit not as markedly as in some australopiths (see below, e.g., Sts 14, Al 288-1). Sts 14’s superoinferiorly low and squat, posteriorly rounded and expanded, and clearly anteroposteriorly long ilia incorporate a well-defined greater sciatic notch (Figs. 1 and 2). In these features, the small Hadar AL 288-1 left os coxa, juvenile Makapansgat ilia MLD 7 and 25, Malapa UW-88-133, the virtually reconstructed Ardipithecus ARA-VP-6/500, and apparently the Swartkrans right partial os coxa SK 50 are similar to Sts 14 (Kibii et al. 2011; Lovejoy et al. 2009b) (see Figs. 1 and 2). Adult ilia Sts 14, AL 288-1, and likely also SK 50 differ from earlier-discussed specimens in being oriented more laterally outward than vertically, with concomitantly greater superior exposure of the internal iliac surface and more subdued “S”-shaped iliac crests; further, these specimens bear only moderately thickened iliac (crest) tubercular regions and poorly developed iliac pillars (Day 1986; Johanson et al. 1982; Robinson 1972). The virtual reconstruction of Ardipithecus portrays a more vertically and anteriorly oriented ilium, more open and poorly delineated greater sciatic notch (especially regarding defined posterior superior and inferior iliac spines), and a longer pubic ramus than the virtual reconstruction of Al 288-1 (Lovejoy et al. 2009b). Australopith anterior ilia present a dichotomy of morphology. In the better-preserved left os coxa of Sts 14, this region appears to be roundedly expanded anteriorly (Robinson 1972), as in StW 431 (Toussaint et al. 2003) and AL 288-1 (Johanson et al. 1982). Thus, a definitive anterior superior iliac spine cannot be identified. But in SK 50, even though its iliac crest is damaged along much of its length, what is preserved continues forward to become a well-defined, beak-shaped anterior superior iliac spine that projects markedly anterior to a bluntly thickened, almost knoblike anterior inferior iliac spine (Day 1986; Robinson 1972). The smaller Makapansgat juvenile ilia (MLD 7 and 25) are

Fig. 2 Right os coxae of Homo sapiens, Sts 4, and Malapa MH1 (UW-88-133) to illustrate, e.g., differences between the former and the latter two in details of the pubic and ischial regions and especially iliac superoinferior height and lateral flare. See text for further discussion; not to scale; reproduced to same size (Cast of UW-88-133 courtesy of the American Museum of Natural History) Page 8 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

similar to SK 50 (but not to Sts 14 and AL 288-1) in having a projecting, beaklike anterior superior iliac spine (Dart 1957). Although differing from SK 50 and MLD 7 and 25 in the region of the anterior superior iliac spine, Sts 14 and AL 288-1 are similar to them in developing a knoblike anterior inferior iliac spine that lies noticeably superior to and back over the superior margin of the acetabulum, as in other potential hominids surveyed above. Although australopiths have traditionally been interpreted as postcranially intermediate between knuckle-walking great apes and Homo – as noted, for instance, in their developing a humanlike posterior iliac expansion while supposedly retaining an apelike anterior iliac distension – this scenario seems inappropriate: not all specimens present similarly configured anterior superior iliac spines. Indeed, only SK 50 and MLD 7 and 25 compare favorably with great apes in having a beaklike anterior superior iliac spine that continues forward the trajectory of the iliac crest. The rounded anterior expansion of this region in Sts 14, AL 288-1, and apparently also in Malapa UW-88-133, while absolutely and relatively large compared to Homo sapiens and other possible fossil hominids, is, nevertheless, derived in its own right. The preserved pubic rami of Sts 14 and AL 288-1 are reminiscent of this region in Neanderthals and the Jinniushan specimen in being relatively long, but the symphyseal regions of the australopith specimens are not also superoinferiorly tall and anteroposteriorly compressed (Rosenberg 1998). A superior view of the articulated Sts 14 pelvis illustrates (in contrast to Homo sapiens) the relation of the elongate pubic rami to the relatively wide pelvic canal and the relatively posterior positioning of the outwardly flared ilia (Robinson 1972). Further, while in H. sapiens (and other Pleistocene specimens surveyed above) the curve of the iliac crest positions the anterior superior iliac spine just lateral to the parasagittal plane intersecting the posterior superior iliac spine, in Sts 14, the anterior portion of the ilium would have been situated well lateral to the plane of the sacroiliac articulation (Robinson 1972). The known left os coxa of AL 288-1 was likely similar to Sts 14 (Johanson et al. 1982). Although SK 80’s iliac crest is similar to Sts 14 in not being strongly “S shaped,” when their iliac blades are oriented in the same plane, SK 80’s acetabulum is similar to H. sapiens in facing laterally and slightly downward (Robinson 1972). In contrast, the fairly vertically aligned Sts 14 acetabulum faces forward. When compared in anatomical position, the Sts 14 ilium is again more outwardly and obliquely oriented, while SK 50 is more anteroposteriorly arranged, as in H. sapiens and various other specimens attributed to Homo. Although Malapa MH1 and MH2 are presented as having medially facing and vertically oriented ilia (Kibii et al. 2011), the largely complete right Australopithecus sediba ilium UW-88-133 (cast) can reasonably be oriented with more outward lateral flare (Figs. 1 and 2). This also appears to be the case with the reconstructed os coxa of Ardipithecus ramidus ARA-VP-6/500 (Lovejoy et al. 2009b) (see below). Another feature of potential phylogenetic significance is the distance between the ischial tuberosity and the inferior acetabular lip, which is quite pronounced in great apes and apparently in catarrhines in general (Aiello and Dean 1999). The separation is marked in SK 50, shorter in Sts 14 and KNM-WT 15000, and minimal in Homo sapiens, in which a deep groove intervenes between the two structures. Perhaps further study of this region will prove enlightening, if not in defining features of clade Hominidae, perhaps in delineating a subclade/s within Hominidae. Unfortunately, many details of the vertebral column in general are unknown. Of particular note is that while the lumbar region of KNM-WT 15000 is somewhat curved and angled inward at L5-S1, unlike H. sapiens, H. neanderthalensis, and large-bodied apes, this individual had six rather than five lumbar vertebrae (Walker and Leakey 1993). Regarding femora, KNM-WT 15000, KNM-ER 1481 and 1472, Sts 34A, AL 129-1a, and UW 88-63 (casts) and D4167 (original) present carrying angles that set them apart from Sts 34B, AL Page 9 of 39

13 13

77

77

77

77

78 82

103

KNM103 ER 1472 UW-88- 103 63 TM 1513 103

LB1 Spy 1

83

97

a

7

8

12 8

13

14

See Table 2 in Tardieu and Trinkaus (1994)

Trinil 3/Pith I

82

AL 333-4 98

102 98

13

76

104

15

75

105

15

AL 333w-56 KNMER 1481 Sts 34B

75

105

Sts 34A

Medial Lateral Martin’s condyle angle condyle angle bicondylar Specimen ( ) ( ) angle ( ) Extant humans AL 110 70 20 129-1a KNM108 72 18 WT 15000 D4167 105 75 15

Table 1 Distal femur: carrying angle and morphology

9

9

13

10

15

18

Published bicondylar angle ( )a 10.5–8.5 (sexes pooled) 13 Popliteal fossa Inferior profile Narrow “V” Tall, narrow trapezoid Wide Very wide rectangle Moderately Moderately wide wide trapezoid Moderately Wide, odd wide trapezoid Narrow “V” Rounded, wide, semi-trapezoid Narrow, Wide, rectangle widens? Wide, deep Moderately tall, odd trapezoid Widens Wide, shortposteriorly angle triangle Moderately Wide trapezoid wide, deep Moderately Wide, moderate deep, wide trapezoid Narrow Tall, narrow trapezoid n.a. n.a. Deep, Moderately wide moderate trapezoid Wide, deep Very wide rectangle Narrow, Moderate deep trapezoid

Medial vs. lateral condyle height Patellar facet Shorter anteriorly Asymmetric, narrow Shorter anteriorly Asymmetric, wide Equal height Symmetric, wide

Much taller Asymmetric, anteriorly wide Shorter anteriorly Asymmetric, narrow Taller anteriorly Asymmetric, wide, shallow Much shorter Asymmetric, anteriorly moderately wide Equal Symmetric, wide, deep Taller anteriorly Asymmetric, moderately wide Much shorter Asymmetric, anteriorly wide Shorter anteriorly Asymmetric, narrow n.a. n.a. Much shorter Asymmetric, anteriorly narrow, deep Equal height Symmetric wide, shallow Shorter anteriorly Asymmetric, wide

Medial curve, lateral straighter Medial curve, lateral straighter n.a. Medial slight curve, lateral straight Medial curve, lateral straighter Medial curve, lateral straighter

Medial teardrop, lateral straight Medial curve > lateral

Medial angle > lateral

Medial A/P deeper, both curved Slight arc, parallel

Both curve

Both straight, diverge

Both curve, parallel

Medial vs. lateral condyle configuration

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

333-4, Trinil 3/Pith I, and Spy 1 (Table 1; see also Fig. 3) (Lordkipanidze et al. 2007; Walker and Leakey 1993). For the former seven specimens, medial distal femoral angles range between 103 and 110 and lateral angles between 70 and 77 ; using Martin’s bicondylar angle [measured between the axis perpendicular to the distal articular plane and the lateral angle (Martin 1928)], the range of this sample is 13–20 . In contrast, distal femoral angles of the Sts 34B et al. specimens are lower, i.e., below 103 (medial), 77 (lateral), and 13 (Martin’s scale). Further, Sts 34A and Sts 34B also differ in size and detail of condylar shape and orientation (Table 1). As tabulated by Tardieu and Trinkaus (Tardieu and Trinkaus 1994), bicondylar angles for several living human populations (males and females pooled) range between 8.5 and 10.5 (Martin’s scale). The fact that two “groups” are distinguishable on the basis of distal femoral angle – with Homo sapiens falling into, or at least not with, one of them – raises doubt about the allocation to genus Homo of specimens preserving the distal femur (especially KNM-WT 15000, KNM-ER 1481 and 1472, and D4167) as well as specimens presenting pelvic as well as vertebral and other features not covered here that have been deemed australopith-like. Indeed, as will become clearer below, these inconsistencies redound, in broad perspective, on defining genus Homo on the basis of sapiens-like “striding bipedalism” (Wood and Collard 1999) (see also chapter “▶ Defining the Genus Homo”) and, more specifically, on assuming because of similar age and/or location, that specimens (e.g., those from Dmanisi) must represent not only the same taxon but a paleodeme of it that morphological difference represents not taxi diversity but merely individual variation (Lordkipanidze et al. 2013; Margvelashvili et al. 2013). In the case of the Dmanisi specimens, if, as the skulls and mandibles have been designated, D4167 represents H. erectus, then, at least with regard to distal femoral angle, there is no basis for taxonomically discriminating between any of the specimens discussed here where similar distinctions are demonstrable (see below). As Robinson (1972) long ago recognized, the distal femur presents much morphology of potential significance (see Fig. 4). For instance, as he saw it, when viewed from below, distal femora TM 1513 (left) and Sts 34 (right distal femur, now identified as Sts 34B) are generally similar to those of largebodied apes in disparity and/or orientation of medial versus lateral condyle but differ in being deeper anteroposteriorly and more trapezoidal (mediolaterally narrower anteriorly) rather than rectangular

Fig. 3 Femora of Homo sapiens, TM 1513, Dmanisi D4167, KNM-WT 15000, and Sts 34B illustrating similarities in all but H. sapiens distally in bicondylar/carrying angle and proximally in lack of a distinct intertrochanteric line and posterior orientation of the lesser trochanter. See text for further discussion; not to scale (Copyright # J. H. Schwartz) Page 11 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

Fig. 4 Distal views of right femora of Pan troglodytes (¼Pan trog.), Sterkfontein TM 1513, Homo sapiens, AL 333–4, KNM-ER 1472, AL 288-1a, and UW 88–63 (Malapa hominid 1) and left femora of KNM-ER 1482 and KNM-WT 15000. Note differences in, e.g., anteroposterior length, orientation and relative sizes of medial and lateral condyles, and relative depth and symmetry versus asymmetry of the patellar surface. Also note specific differences between AL 333–4 and AL 129-1a in, e.g., anteroposterior length, crispness of lateral patellar surface border, lateral epicondylar morphology, and divergence posteriorly of medial and lateral condyles; although AL 129-1a is damaged anteromedially, it is likely that this region would not have projected as far anteriorly as in AL 333–4. Of further note is that UW 88–63 resembles only KNM-ER 1481 and only in degree of asymmetry of the region of the patellar surface. See text for detailed discussion; not to scale; images reproduced to similar mediolateral width; r reversed (Except for TM 1513, all casts courtesy of the American Museum of Natural History)

in outline and in having a somewhat more concave and slightly asymmetrical patellar fossae, in concert with the lateral margin being more anteriorly distended than the medial margin (in other words, when viewed from below, the lateral condyle is anteroposteriorly longer than the medial, regardless of differences in configuration). Robinson’s enthusiasm notwithstanding, study of casts of these specimens reveals that while TM 1513 displays (slight) patellar fossa and condyle asymmetry, Sts 34B’s fossa is symmetrical and its condyles equally distended anteriorly (Table 1). Also, the curvature of the medial condyle is much more severe in TM 1513 than in Sts 34B, in which (uniquely for hominids studied here) it is “teardrop” shaped (Table 1). Interestingly, Sts 34B also differs markedly from Sts 34A in overall and specific distal femoral features – which is consistent with the craniodental nonuniformity of Sterkfontein fossils (Schwartz and Tattersall 2005). Distal femora AL 129-1a and AL 333-4, of which the latter is the larger (McHenry 1986), also differ in morphological detail (Table 1). Lague (2002) acknowledges size and some morphological difference between the two specimens – especially the anterior projection of the medial margin of the patella fossa – but claims this merely reflects sexual dimorphic variation typical of extant populations of large-bodied hominoid species. If true, then a number of fossils that differ in ways similar to AL 129-1a and AL 333-4, or in other morphologies (Table 1), should be regarded as variants of the same subspecies. I am not suggesting that one ignore intraspecific variation, which includes sexually dimorphic differences. However, one can only address this topic after hypothesizing “groups” (e.g., morphs at least) within the morphological parameters of which individual variation can be assessed (Schwartz 2007b). Further, by focusing on general shape and outline, Lague overlooks differences between AL 129-1a and AL 333-4 not only in carrying/bicondylar Page 12 of 39

Large Moderately large Medium?

Parallel Parallel Slight taper Slight taper Taper

111–140 Short

H. 113–127 Short neanderthalensis D4167 113 Long

Long

120

120

120

120

120

120

120

120

OH 20

BAR 1002’00

KNM-WT 15000(R) SK 97

MAK VP1/1

AL 333-3

KNM-ER 1472

KNM-ER 1481

Moderate

Moderate

Moderate

Long Some taper Some taper Some taper

Taper

Moderately Slight long taper Long Some taper Long Taper

Long

UW 88-04/05/39 120

n.a. n.a.

H. sapiens

n.a. n.a.

n.a. n.a.

OH 28 ARA-VP-1/701

Large

Large

Large

Likely small

Medium

Moderately large Medium

n.a.

Large

n.a. n.a.

Small Small Small

STW 30A STW 30B UW 88-89

Specimen STW 25

Relative head size Small

Neck Neck Relative profile angle ( ) neck length (anterior) n.a. n.a. Likely tapered n.a. n.a. Taper n.a. n.a. Taper n.a. n.a. n.a.

Table 2 Proximal femur: neck/shaft angle and morphology

Yes

Yes

Yes

No

Yes

Slight

Yes

n.a.

Yes

Yes

Yes

Yes

n.a. n.a.

Yes Yes Some

Head extension distal No

Yes

Yes

Yes

No

Some

Slight

Yes

Likely

No

Yes

Yes

Yes

n.a. n.a.

No No Some

Head extension proximal No n.a. n.a. Slight pointy n.a. Large blunt Large blunt Large blunt Blunt

Lesser trochanter shape n.a.

MedioPointy posterior Posteromedial Blunt

Posteromedial Long?

Posteromedial Blunt

Very posterior Slight point Posteromedial Pointy

Posteromedial Likely pointy Fairly medial Long

Medioposterior Very posterior Large

Medial

Very medial

n.a. n.a. Medioposterior Posterior Fairly medial

Lesser trochanter position n.a.

Noted

Noted

Well above Some

Slight

Likely above n.a.

No

n.a.

Above

Well above Above

n.a. n.a.

n.a. n.a. n.a.

Moderate

Moderate

Faint

Faint

Distinct

n.a.

Faint

Faint

Faint

Moderate

Distinct

Distinct

n.a. n.a.

n.a. n.a. n.a.

Faint

n.a.

Absent

Visible

None

Faint

Marked

Marked

Marked

Marked

Faint

n.a. n.a.

Greater trochanter Intertrochanter Spiral height crest line n.a. n.a. n.a.

(continued)

Faint

n.a.

Faint/ damaged Faint

Faint

Faint

Faint

Marked

Marked

Marked

Stouter

n.a. n.a.

Gluteal line n.a.

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

Page 13 of 39

Long

130

130

130

130 130

130

130

AL 288-1

KNM-ER 999

AL 128-1 KNM-ER 738

OH 62

LB1

Moderate

Long

n.a. Very long

Very long

Long

Long

125

Relative neck length Short Very long

KNM-WT 15000(L) Trinil 6/Pith II

Specimen Trinil 3/Pith I KNM-ER 815

Neck angle ( ) 120 125

Table 2 (continued)

Taper Some taper Some taper Slight taper

Neck profile (anterior) Parallel Some taper Some taper Some taper? Some taper n.a. Slight

Head extension distal Some Slight?

Large

Likely small

n.a. Moderate

Probably small

Small

Yes

No

Likely yes n.a. Noted

Yes

Small–medium? n.a.

Medium

Relative head size Large Probably small

Lesser trochanter shape Pointy Pointy

Very posterior Slight point MedioNot long posterior Posteromedial Pointy

Lesser trochanter position Medial Posteromedial

Yes

No

n.a. Some

Medial

Blunt

Very posterior Long

Posteromedial Long Posterior Pointy

Likely yes Posteromedial Pointy

Yes

n.a.

Slight

Head extension proximal Some None?

Above

n.a.

Slight Some?

n.a.

Noted

n.a.

Slight

Greater trochanter height Noted n.a.

Distinct

n.a.

Faint Faint

Faint

Faint

None?

Faint

Intertrochanter crest Distinct Faint

Very lateral Faint

Faint

Faint

Gluteal line Marked Blunt

Marked Faint Moderate Faint

Very medial Faint

Faint

Faint

Spiral line Marked Faint

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

angle but also in morphological detail (Table 1), beyond which are yet-to-be studied distinctions in, e.g., condylar side, epicondylar, epicondylar line, popliteal surface, and diaphyseal cross-section configurations (personal observations). Indeed, it appears that at present geometric-morphometric analyses are not capable of capturing the morphological details required of systematic analyses (e.g., see Lordkipanidze et al. 2013; see also Ulhaas 2009). Turning to the proximal femur (Table 2), the most commonly reported “feature” is the femoral neck-shaft angle (measured inferiorly/medially at the intersection of the long central axes of the neck and shaft). As implied by DeSilva et al. (2013), Neanderthals display a moderate amount of variation and Homo sapiens considerable variation, the range of the latter encompassing virtually all other hominids. Gilligan et al. (2013) have argued that differences among sapiens populations in femoral neck-shaft angle are strongly correlated with differences in climate as well as in aspects of lifestyle, including types and use of clothing. Although neither the ontogeny of this angle nor its relation to the carrying/bicondylar angle has been studied, Gilligan et al.’s conclusion, at least with regard to the influence of lifestyle and clothing, is intriguing. For, if even partially correct, it suggests that the variability recorded for sapiens, and likely also for neanderthalensis, does not negatively impact the potential phylogenetic significance of the proximal femoral morphology of hominid species that were not geographically widespread and thus subject to disparate climates. Geographic and climatic restrictiveness also suggests that at least femoral neck-shaft angle differences are not due to climaterelated clothing, if consideration of clothing of any sort is actually relevant. In other words, morphological variability in the species Homo sapiens, as well as in the species H. neanderthalensis, does not necessarily lead to the conclusion that variability is the sole explanation for difference among hominid specimens. Thus, while White (2003, 2012) remains steadfastly and zealously critical of paleoanthropologists who are “biased” toward identifying taxic diversity in the human fossil record, he is not exempt from bias toward explaining virtually all morphological difference as variation. Both claims should be regarded as hypotheses in need of testing (see also chapter “▶ General Principles of Evolutionary Morphology”). Returning to the femoral neck-shaft angle, it is potentially noteworthy that non-sapiens/ neanderthalensis specimens commonly regarded as Homo do not cluster together (Table 2). Rather, in this sample, the angle in the majority of specimens is 120 , in two it is 125 , and in most others it is 130 . Further, no “group,” even excluding those with 125 angles, conforms to any traditionally recognized hominid taxon or clade. Interestingly, Dmanisi D4167 has the lowest angle: 113 . The paucity of complete femora limits comparisons involving femoral shaft-neck and carrying/ bicondylar angles, which, as seen, for instance, in D4167 (113 /15 ), KNM-WT 15000 (120 / 18 ), KNM-ER 1472 (120 /13 ), and Trinil 3/Pith I (120 /7 ) (Tables 1 and 2) would appear informative for both systematic and locomotory deliberations. Elsewhere, I (Schwartz 2007a) suggested that the posterior position/orientation of the lesser trochanter in South and East African “australopiths” and also KNM-WT 15000 (posterior) distinguished them not only from mammals in general but also from Homo sapiens, H. neanderthalensis, and from Orrorin, in which this structure points medially and is therefore visible when the femur is viewed anteriorly (Figs. 5, 6, and 7). Additional scrutiny of specimens (actual and casts) as well as review of the literature not only substantiates this observation but also demonstrates that, like KNM-WT 15000, many specimens allocated to Homo, including D4167 (Lordkipanidze et al. 2007), are “australopith”-like in having a somewhat-to-extremely posteriorly oriented lesser trochanter (Table 2; Fig. 6). These specimens are also “australopith”-like in presenting, for example, a relatively long, medially tapering, and somewhat anteroposteriorly compressed femoral neck; relatively small-to-moderate femoral head with little or no distension beyond the perimeter of the

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

neck, especially proximally; and a weakly developed intertrochanteric line (see Table 2 for additional features). Since, as previously pointed out (Schwartz 2007a), some features seen in H. sapiens are typical of mammals, and essentially of all primates (e.g., Fig. 5), those that differ – as in “australopiths” and “australopith-like Homo” – are plausibly interpreted as derived or clade informative. In other words,

Fig. 5 Right proximal femora of Homo sapiens, Pan, and Macaca (top row, anterior; bottom row, posterior) illustrating typical primate/mammalian features, e.g., short neck, large rounded head, medially projecting lesser trochanter, and stout intertrochanteric line (arrows). See text for further discussion; not to scale (Copyright # J. H. Schwartz)

Fig. 6 Proximal femora of various hominids: Dmanisi D4167 and casts of KNM-WT 15000, SK 97, and KNM-738 (top row, anterior; bottom row, posterior) illustrating atypical primate/mammalian features, e.g., long neck, small head, posteriorly projecting lesser trochanter (arrows), and weak intertrochanteric, spiral, and/or gluteal lines. See text for further discussion; not to scale (Copyright # J. H. Schwartz) Page 16 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

Fig. 7 Left proximal femur of Orrorin (left, anterior; right, posterior views). See text for further discussion; not to scale (Copyright # J. H. Schwartz)

such non-sapiens features would unite a group that consists of various specimens ascribed to Homo, to the exclusion of H. sapiens and sapiens-like hominids including, given preserved femoral morphology, Orrorin and Ardipithecus (see Tables 1 and 2). Consequently, because in the broad comparison “australopith”-like features emerge as derived relative to sapiens-like features, no “australopith”-like taxon (e.g., Australopithecus sediba represented by Malapa UW-88-04/05/39) should be considered “ancestral” to any specimens, and consequently taxa, that may constitute a Homo clade. Further, as noted previously (Bartsiokas and Day 1993; Day 1973; Kennedy 1983), Trinil 3/Pith I (complete) and Trinil 6/Pith II (partial proximal) femora are morphologically dissimilar. More specifically, the former specimen presents sapiens- and the latter “australopith”-like features (Table 2). However, contrary to suggestions that all non-Trinil 3 (complete) femora constitute a group (Bartsiokas and Day 1993; Day 1973; Kennedy 1983), Trinil 3/Pith I (complete), Trinil 3/Pith III (shaft), and Trinil 9/Pith IX (shaft) are distinguished in diaphyseal shape and proximal morphological detail from Trinil 6/Pith III, and Trinil 8/Pith IV (shaft), which resemble each other morphologically (personal observations). Regarding pedal morphology, foot bones attributed to Ardipithecus ramidus (Lovejoy et al. 2009c) and a specimen described as Ardipithecus-like (Haile-Selassie et al. 2012) lacked an arch, had fully opposable halluces, and did not “toe off” with this digit. Day and Napier (1964a, b) reconstructed the OH 8 foot bones with an arch and a first digit in alignment with the other digits; but restudy suggests that the hallux was probably semi-opposable and, by extension, there was an absence of an arch (Clarke and Tobias 1995). The latter two features characterized StW 573 (“Little Foot”) (Clarke and Tobias 1995). In contrast, tarsals attributed to Australopithecus afarensis (Latimer and Lovejoy 1990; Ward et al. 2011) and Au. sediba (DeSilva et al. 2013; Zipfel et al. 2011) are interpreted as presenting an arch, with other preserved pedal elements of Au. afarensis indicating a fully adducted hallux. Clearly, Pilbeam’s pedal features do not define a hominid clade. To review, some features of the os coxa and femur, in contrast to at least other catarrhines, appear to distinguish a hominoid clade that we could call “hominid,” i.e., a long pubic ramus, a superoinferiorly short ilium that is roundedly expanded posteriorly, some thickening in the region of an iliac (crest) tubercle, a well-developed and knoblike anterior inferior iliac spine that lies

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noticeably superior to and somewhat back over the superior acetabular rim, a deep greater sciatic notch, a defined linea aspera, development of an obliquely oriented femoral shaft (producing a carrying/bicondylar angle), and a concave lateral tibial facet for the femur that is at the same level as the (also but primitively concave) medial facet, with the two facets being separated by welldeveloped tubercles. Within this potential clade, a subclade appears to be distinguishable even just on features of the proximal femur – e.g., long neck, posteriorly directed lesser trochanter, poorly delineated head/neck cervical region, and weakly defined intertrochanteric line – and another, which may be a subclade of the latter, in presenting a medially tapering neck.

More Recently Suggested Postcranial Features of “Erect Posture” With the discovery at Kanapoi and Allia Bay, Kenya of specimens attributed to the species Australopithecus anamensis, Leakey et al. (1995) presented features of the proximal tibia (via right proximal tibia KNM-KP 29285A) they thought distinguished hominids from apes and, by extension, from other catarrhines. For example, in apes, the medial tibial condylar facet is convex and in posterior view situated slightly higher than the gently concave lateral condylar facet and, in frontal view, the shaft does not flare out smoothly and evenly to the margins of the proximal articular surface (i.e., the proximal articular surface extends especially medially and laterally farther than the respective margins of the shaft). Further in apes, the two condylar facets are separated by a single, blunt tubercle [see also Aiello and Dean (1999)]. In contrast, Leakey et al. suggested, in specimens attributed to “accepted” australopith taxa as well to species of Homo, both tibial condylar facets are at least somewhat concave, separated by a pair of well-defined tubercles and, in posterior view, level with one another. Further in hominids, in anterior view, the tibial shaft flares out to meet the medial and lateral margins of the proximal articular surface. Although these distinctions apply in general to apes and extant humans (in which the tubercles are actually variably distinct), they do not completely describe “australopiths” (Fig. 8).

Fig. 8 Posterior views of right proximal tibiae of Homo sapiens, AL 288-1a, AL 129-1a, AL 333x-26, and KNM-KP 28295A and left proximal tibiae of Pan troglodytes (¼Pan trog.) and KNM-ER 1481. See text for further discussion; not to scale; r reversed (Casts of AL 288-1a, AL 129-1a, AL 33x-26, and KNM-ER 1481 courtesy of the American Museum of Natural History)

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For example, in right proximal tibia AL 288-1a (cast), the lateral condylar facet is slightly convex while the medial is slightly concave; viewed from behind, medial facet lies slightly below the level of the lateral facet (Fig. 8). Further, the apically indistinct tibial tubercles are separated by and incorporated into a mediolaterally wide blunt, loph-like structure that is anteroposteriorly obliquely oriented from the medial to the lateral side. Right proximal tibia AL 129-1b (cast) is similar to Al 288-1a in overall size, concaveness versus convexity and disparity in height of the condylar facets, and in having indistinct tubercles incorporated into a loph-like structure but differs in the shapes of the facets, a more posterior placement of a taller intertubercular loph, and in a different orientation of the shaft. In the large right proximal tibia AL 333x-26 (cast), the cuplike condylar facets are markedly concave (more so than any other suspected hominid) and, as seen from behind, lie at the same level; also the tibial tubercles are symmetrically distinct at their tips and incorporated into a tall loph that is mediolaterally oriented and situated farther posteriorly. As seen in a cast of the large right proximal tibia KNM-KP 29285A, which is part of the published hypodigm of Australopithecus anamensis (Leakey et al. 1995), the lateral condylar facet is faintly while the medial facet is a bit more obviously concave; the two facets are separated by indistinct tubercles that present themselves as a single blunt, high-rising structure that is posteriorly situated on the proximal surface. From behind, the posteriorly sloping lateral condylar facet lies slightly higher than the medial facet. Finally, in left proximal tibia KNM-ER 1481 (cast), both condylar facets are somewhat concave; when viewed from behind, the medial facet lies slightly above the level of the lateral facet. In all of these tibial specimens, KNM-KP 29285A included, the medial margin of the shaft flares out toward the proximal articular region below which the profile actually swells (either slightly as in KNM-KP 292895A, AL 288-1am AL 129-1b, and H. sapiens or noticeably as KNM-ER 1481 and AL 333x26). Also in these specimens, with the notable exception of H. sapiens, the lateral border of the shaft flares out slightly before terminating below the proximodistally relatively tall, somewhat squaredoff overhang of the lateral portion of the proximal articular region with which the fibula articulates (Fig. 8). Interesting, in H. sapiens, the medial and lateral borders of the shaft fan out more or less symmetrically as they approach the proximal end with greater swelling occurring on the lateral rather than the medial side. As is evident even from this small tibial sample, the possession of a concave lateral femoral condylar facet that lies level with the medial facet, a pair of apically distinct tubercles, and a more symmetrically flared proximal shaft does not fully characterize Homo sapiens (and H. neanderthalensis), and they certainly do not a hominid make. Indeed, the only tibial feature Leakey et al. (1995) discussed that could distinguish a hominid from an ape is the flaring and swelling of the medial profile of the shaft as it converges upon the proximal articular region – which, in its more swollen state would represent a more derived configuration. Features of the proximal tibia not detailed here (e.g., symmetry/asymmetry of condylar facet shape, orientation of condylar facets, configurations of intercondylar facet depressions, height of tubercular region) are also consistent with the picture of nonuniformity not only among this sample of “australopiths” but also among specimens from Hadar, among which the distinctiveness of AL 333x-26 alone makes clear that “australopith” systematics is far from being resolved (for another perspective, see chapter “▶ The Species and Diversity of Australopiths”). Further, proximal tibial as well as femoral morphology (see above) confirms observations based on dental morphology (Schwartz and Tattersall 2005), namely, that the Hadar specimens encompass more than one taxon. At a higher taxonomic level, since various “australopiths” retain primitive tibial features – e.g., convex medial condylar facet, medial facet higher than lateral facet, indistinct tibial tubercles, and asymmetrically flared proximal shaft – features Leakey et al. put forward as defining hominids appear instead to unite a subclade or subclades within it. Page 19 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

Since tibial and femoral morphologies reflect aspects of locomotion, the differences noted here between specimens suggests, as pedal morphology has begun to indicate, that “bipedalism” was enacted differently among different species or subclades of hominid (see also chapter “▶ The Origins of Bipedal Locomotion”). Since no Hadar specimen is dentally comparable to the type specimen of Au. afarensis, Laetoli hominid (LH) 4, and all Laetoli specimens can reasonably be allocated to the same dental morph (Schwartz and Tattersall 2005), it would be interesting to know the postcranial morphology of the hominid – that is, of Au. afarensis – that left the footprints. Further, the singular degree to which the tibial condylar facets of AL 333x-26 are depressed and cuplike not only reflects a uniquely derived configuration but also likely a unique type of hominid locomotion. In their description of the Lukeino proximal femur (BAR 1002’00), Pickford et al. (2002) commented on how slight the linea aspera is compared to specimens of australopiths and Homo (because the spiral line of BAR 1002’00 does not meet the gluteal/3rd trochanteric line to form a linea aspera of high relief). I agree with this general description (personal observation; Fig. 7). They (p. 202) then suggested, because apes do not present a muscle scar descending from the region of the gluteal tuberosity, that such “a precursor of the linea aspera” is a hominid-identifying feature related to bipedalism. A review of casts of some femora identified as australopith or Homo reveals, however, a more complex picture (Table 2). For instance, KNM-WT 15000, the supposedly first humanlike striding biped, lacks a spiral line altogether. Other specimens differ in presence and degree of expression of a gluteal line (Table 2), as well as in where each line, if it is identifiable, emerges relative to the associated trochanter and side of shaft; how and where they converge to form/ not form a linea aspera; the shape and surface morphology of any supra-linea aspera triangle these lines might delineate between them; where on the shaft their merging produces a linea aspera; and the degree of development and distal course of the linea aspera (personal observation). Pickford et al. (2002) also mentioned that in BAR 1002’00 the lesser trochanter is medially projecting and, as in humans, gorillas, and Pongo, also well separated from the femoral neck. Regarding the latter feature, images in Pickford et al. as well as, for instance, in Robinson (1972), Day (1986), Johanson et al. (1982), and Walker and Leakey (1993) illustrate that while notable separation of lesser trochanter and femoral neck may describe specimens such as SK 82 and 97, Sts 14, AL 288-1, OH 62, KNM-WT 15000, and KNM-ER 738, 1503, and 1547, this configuration does not characterize Homo sapiens (or, e.g., Pan). Perhaps this disparity is due to differences in femoral neck length – which might imply that separation of lesser trochanter and femoral neck is phylogenetically significant not for, but within, the clade Hominidae. As discussed above, the medial orientation in BAR 1002’00 of the lesser trochanter, although similar to Homo sapiens, is also broadly descriptive characteristic of primates (Swindler and Wood 1973) (personal observation; see above). In contrast, in specimens such as AL 128-1, 288-1, AL 333-95, AL 333-3, Maka VP 1/1, SK 82 and 97, OH 62, KNM-WT 15000, and KNM-ER 738 and 1547, the lesser trochanter is more posteriorly than medially if not strongly posteriorly directed (Table 2). As contemplated above, interpretation of these different configurations is not straightforward. For instance, most mammals present a medially or more medially-than-posteriorly (i.e. medioposterior to posteromedial) oriented lesser trochanter. Based on commonality, the possession of this in apes and Homo sapiens could reasonably be interpreted as a primitive retention – in which case configurations to the contrary would be derived and thus potentially reflect a hominid subclade. On other hand, albeit less parsimoniously (but why should parsimony always dictate interpretation?), the apparent widespread distribution among possible hominids of a posteriorly oriented lesser trochanter (and other features as well) might be primitive within a hominid clade – which implies an “independent” development of the primitive mammalian condition in H. sapiens. Since, however, Page 20 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

postcrania definitively associated with crania and teeth are rare indeed, the former interpretation might be the more likely. Another feature that Pickford et al (Pickford et al. 2002; also Galik et al. 2004) suggested unites Orrorin via BAR 1002’00 with australopiths and at least Homo sapiens is differential distribution of femoral neck cortical bone, being thinner superiorly and thicker inferiorly (Ohman et al. 1997). Taxically broader study is required.

Non-postcranial Features of “Erect Posture” Although other postcranial features might delineate clade Hominidae, I will turn now to another skeletal region from which “erect posture” or “bipedal locomotion” has been inferred: the cranial base. For ever since Dart’s (1925) discussion of the Taung child, an anteriorly placed foramen magnum with attendant occipital condyles has been central to the identification of hominoids as bipedal hominids. With Ardipithecus ramidus (White et al. 1994) and Sahelanthropus tchadensis (Brunet et al. 2002) being promoted as potential hominids, attention to basicranial morphology is crucial. Interpretation of Ardipithecus (White et al. 1994) and Sahelanthropus (Brunet et al. 2002) as “hominid” was in part based on White et al.’s inference of bipedalism from the intersection of the bicarotid (foramen) chord and basion (¼the anthropometric landmark in the midline of the anteriormost margin of the foramen magnum). The published photograph of the crushed and distorted basicranium of Sahelanthropus reveals, however, that what appears to be the anterior margin of the foramen magnum lies posterior to the bicarotid chord. It is obvious that in the undistorted state, the preserved left petrosal and thus the bicarotid chord were situated more anteriorly. Consequently, a forward position of the foramen magnum is not indicated. Although not demonstrated, White et al.’s claim of an association between basion (i.e., the anterior margin of the foramen magnum) and the bicarotid chord, an anteriorly placed foramen magnum, and erect posture and bipedalism would seem intuitively reasonable. However, comparison of other potential fossil hominids, extant large-bodied hominoids, and various extant New and Old World monkeys, reveals a more complex picture (Schwartz 2004b). In juvenile anthropoids, including humans, basion, the bicarotid chord and the biporionic chord are essentially in alignment. This relationship is retained into adulthood in some anthropoid taxa, but, in others, during growth, the positions of basion and/or the bicarotid chord may change position relative to the biporionic chord. Consequently, it is the biporionic and not the bicarotid chord that better reflects the position of the foramen magnum. The alignment of basion and the two chords in the adult is, therefore, a neotenic feature that, while not defining clade Hominidae (Schwartz 2004b; Schwartz and Tattersall 2005), may be relevant to delineating relationships within it. More recently, in the context of comparison between an unspecified sample of extant catarrhines and extant sapiens, Kimbel et al. (2013) argued the hominid status of Ar. ramidus on the basis of reconstructing cranial base width and anterior foramen magnum position from missing basicranial elements in ARA-VP/500. Nevertheless, until the ontogeny of this general region in a diversity of anthropoids is understood, comparisons only between adult specimens are – as demonstrated above vis-à-vis ontogenetic changes – uninformative.

Proposed Craniodental Features of Being Hominid Based on isolated teeth attributed to Ardipithecus, White et al. (1994) suggested that, in lateral profile, a hominid’s permanent upper canine should present subequally long and quite divergent mesial and distal edges terminating in “shoulder-like” basal swellings that create the impression of a superoinferiorly short crown. This does not, however, describe the permanent upper canine (C\) of Page 21 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

Sahelanthropus (Brunet et al. 2002) or the majority of C1s of traditionally accepted Plio-Pleistocene and later hominids, including Homo sapiens (Schwartz and Tattersall 2005). Rather, White et al.’s description better captures the morphology of the C\s of adult female orangutans and the deciduous upper canines of juvenile orangutans and chimpanzees (Swarts 1988). White et al. (1994; also Suwa et al. 2009) also described Ardipithecus’ C1 as “incisiform” but from the belief, also shared by Brunet et al. (2002), that a C1-C1-P1 honing complex had been lost in hominids via a decrease in size and projection of these teeth (particularly the canines) in concert with closure of presumed attendant diastema. According to this scenario, as canines became less caniniform, they became associated functionally with the incisors, ultimately assuming the morphology and function of these spatulate anterior teeth. Yet, both the right C1 allocated to Ardipithecus and the C1 in the skull of Sahelanthropus, although differing in buccal profile triangularity, are apically pointed. Indeed, Sahelanthropus’ trenchant C1 would likely have occluded with a much more “caniniform”-looking C1 than the very unprimatelike isolated element identified as this tooth (Schwartz 2004b). Although it appears from teeth in situ that Sahelanthropus lacked upper diastema, their absence is only inferred for Ardipithecus from isolated teeth. Nevertheless, if Ardipithecus did not have diastema, both it and Sahelanthropus would be more derived than geologically younger (and supposedly descendent) specimens with diastema [e.g., AL 200-1a and StW 252 (Schwartz and Tattersall 2005)] as well as the maxilla from Bouri Hata allocated to Australopithecus garhi [see photographs in Asfaw et al. (1999)]. Consequently, features associated with “reduction of a canine-premolar honing complex,” while not defining clade Hominidae, may delineate subclades within it. Another approach to defining Hominidae is predicated on an a priori assumption of a humanchimpanzee relationship, which immediately constrains the hominid “out-group” to this single large-bodied hominoid. Thus, although White et al. (1994, p. 306) describe the dm1 of Ardipithecus as “apelike,” the only ape in their comparison is Pan. Yet, Hylobates and Gorilla dm1s are also very similar to Pan dm1s, while Pongo dm1s are most similar to those of traditionally accepted hominids, the major difference being more talonid cusp compression in the orangutan (Schwartz 2004b; Swarts 1988). Thus, Pongo, “australopiths,” and Homo dm1s conform best to White et al.’s (1994, p. 307) depiction of “apparently derived hominid features,” i.e., “buccolingual crown expansion, mesiolingually prominent metaconid, well-defined anterior fovea, and large talonid with well differentiated cusps” (White et al. 1994). In fact, the dm1s of Pongo and hominids1 are similarly derived relative to other extant hominoids (Schwartz 2007b; Schwartz and Tattersall 2002, 2003, 2005): e.g., the protoconid is more mesially situated; the less vertical and lingually facing anterior fovea (¼ trigonid basin) is noticeably smaller than the talonid basin and is enclosed by a distinct paracristid that courses somewhat mesially and then turns toward the lingual side; and the more horizontally oriented talonid basin is enclosed by a distinct hypocristid (Swarts 1988) (personal observation). Only if Pongo (and members of its clade for which dm1s are currently unknown but for which this description would be predicted as applicable) is not the sister taxon of a potential hominid clade would these dental features be relevant to defining only clade Hominidae. More broadly, Irish and Guatelli-Steinberg (2003) claim to have delineated features characteristic and also distinctive of the last common ancestor of clade Hominidae and also demonstrated that recent sub-Saharan Africans most closely resemble various Plio-Pleistocene hominids in these Comparison comprises juvenile Homo, including Melka Konturé MK81 GAR IV (2), and “australopiths” (e.g., Hadar AL 333-43b; Koobi Fora KNM-ER 820, 1477, and 1507; Laetoli LH2 and 3q; Omo 227; Taung; Swartkrans SK 47; Kromdraai TM1536, TM1601a, and TM1604; KB5503 and KB5223; and Sterkfontein Sts24 and StW 104 and 151). 1

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

features. Their study is based on the ASU dental trait scoring system established decades ago by Turner et al. (1991) (see chapter “▶ The Dentition of American Indians: Evolutionary Results and Demographic Implications Following Colonization from Siberia”). Although seemingly objective (e.g., in matching individual dental features of a specimen with plaques of dental casts varying degrees of expression of that trait), the Turner scoring system has no relation to the terms and descriptive protocol that inform the study and systematic interpretation of mammalian teeth. Rather, Turner’s system focuses instead on predefined minutiae and often idiosyncratically defined variation. Thus, although hominids are toothed mammals, Turner and scions have so ignored the conventions of mammalian dental terminology and description that a mammalian systematist cannot understand or even divine the morphology of the teeth subjected to the ASU scoring system. Indeed, terms such as “lower molar deflecting wrinkle” and “lower molar seventh cusp” or referring to a (huge) protostyle as an element of a “twinned hypocone” demonstrate just how far from biological/ systematic practice paleoanthropology is. In short, coding for one trait after another and their presumed degrees of expression informs neither about the relations of structures to one another nor, more importantly, about the shape of a tooth and the relative expressions of as well as the spatial relationships of the details of occlusal morphology. Further, rather than testing hypotheses of which specimens might represent which morph/taxon, these analyses begin by accepting prior taxonomic allocation of specimens [e.g., (Bailey 2002, 2004; Bailey and Wu 2010; Trinkaus et al. 2000)]. Unfortunately, the emphasis of the ASU approach on scoring individual traits with a focus on degrees of trait expression (e.g., larger, larger, small, smaller; distinct, more distinct, less distinct) rather than on their relationships informed the dental “study” of specimens identified as Australopithecus sediba (Irish et al. 2013). Although rooting their analysis in a gorilla out-group – without understanding that gorillas are unique among large-bodied hominoids in aspects dental morphology (Schwartz 1986) – Irish et al. (Irish et al. 2013) conclude that Au. sediba is dentally distinct from other “hominids” but similar in a phylogenetically meaningful way to their sample of Au. africanus and an assumed Homo habilis/heidelbergensis + H. erectus group. The latter larger grouping is based on four features, including the vague “identical LM1 cusp 7 expression.” Their conclusion, in conformity with interpretation of cranial and postcranial morphology, is that its “mosaic” of presumed primitive australopith and derived Homo features makes Au. sediba a good ancestor of genus Homo. Although the taxonomic distinctiveness of Au. sediba has been challenged on the grounds that the skull upon which the species was based is that of subadult – and thus its adult morphology could be comparable to known specimens of australopith (Strauss et al. 2012, 2013) – tooth and mandibular morphology provide less speculative clues to understanding this hominid. Indeed, comparison with all known australopiths demonstrates that Au. sediba is remarkably similar to Kromdraai TM1517b, the mandibular holotype of Paranthropus robustus (Fig. 9). For example, although the mandibular corpus of MH1 (UW-88-8) is more gracile, shorter superoinferiorly, and more swollen below the alveolar region – which may be because of its being subadult – both it and TM1571b are otherwise similar, including presenting two (top and bottom) mental foramina below P1. Further, in both specimens, the anterior root of the ramus originates below the region of M1-2, masking M3 entirely, and then swells only modestly before becoming crest-like as it ascends, inclining a bit backward. UW-88-129 presents a moderately steep postincisal plane, as also seen in TM1517b. Damage and incomplete restoration of TM1517b preclude assessing C1 orientation, but this tooth in UW-88-8 was relatively larger. Preserved alveoli in UW-88-8 suggest that the missing P1-2 were similar to TM1517b in shape: i.e., P2 was larger, especially in a distended hypocone region such that the buccal side of the tooth was mesiodistally somewhat shorter, while the buccal side of P1 was marginally but still visibly longer than the lingual Page 23 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

Fig. 9 Occlusal views (left to right) of right mandibles of Malapa hominid MH 2 (UW-88-54-128-129), Kromdraai TM1517b (type, Paranthropus robustus), and MH 1 (UW-88-8), illustrating numerous dental similarities, size being the major difference. See text for further discussion; not to scale but to relative size (Casts of MH 1 and MH 2 courtesy of the American Museum of Natural History)

side. The P2 of UW-88-129, although also smaller, is morphologically comparable to TM1517b. The M1s of the smaller UW-88-8 and TM1517b are otherwise distinctively similar, especially in the oblique orientation of the distal part of the crown, the presence of notches between buccal cusps, and a buccal cingulid on the protoconid. Further, for example, in both UW-88-8 and the TM1517b, M1-2 the hypoconids are compressed, they bear hypocristids, and their bases extend lingually across the midline of the crown, terminating approximately in the midline in a mesiodistally relatively long and internally squared-off end; also, small hypoconulids angle in toward the middle of the tooth, following the generally oblique orientation of their distal sides of the crowns. A groove on the internal face of the M1 metaconid base of TM1517b produces a “pillar-like” feature, which is seen on UW-88-8’s M2. Although the mesial part of TM1517b’s M2 is partially reconstructed, the distal extremity of a definitive protoconid buccal cingulid is clearly evident abutting the mesial side of this tooth’s hypoconid even in the presence of a notch between these two cusps. Similar morphological detail is noted in UW-88-8. Further, the M3s of TM1517b and UW-88-8 are generally similar in size and shape and also in presenting buccal cusp notches (also in UW-88-55a), distinct buccal cingulids on the distal part of the protoconid, a slight buccal enamel swelling below the hypoconulid, a distobuccally obliquely oriented metaconid base, and mesiodistally short trigonid basins confined to the inner portions of protoconid and metaconid bases. If, as appears to be the case, these specimens represent the same hominid, they should be regarded as Paranthropus robustus, with the Malapa specimens’ smaller size likely reflecting sexual dimorphism: i.e., MH1 was female, not male (Berger et al. 2010). Since, however, dentally and even in bony morphology the partial face TM 1517a is relatable to a morph that includes the Taung child, and which therefore must regarded as Australopithecus africanus (Schwartz and Tattersall 2005; Fig. 10), only the lower jaw from Kromdraai TM1517b represents the holotype of P. robustus. In this regard, future comparisons of the upper dentition of MH1 with those of other “australopiths” should prove enlightening in sorting out which specimens actually do represent this taxon. Certainly, we now know a lot about the postcranial skeleton of this hominid.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_45-3 # Springer-Verlag Berlin Heidelberg 2014

Fig. 10 Comparison of the Taung child specimen, the type of Australopithecus africanus, and a few other South African specimens that present similar facial and dental features of as well as variation within the Taung morph. Note that TM 1517a, which Broom referred to the holotype of Paranthropus robustus, compares favorably with this morph. Not to scale (Copyright # Jeffrey H. Schwartz)

Additional Defining Characters of Hominidae Although some obviously derived features when considered in isolation might delineate clade Hominidae, they are also shared with Pongo and its potential extinct relatives. Consequently, in order to claim them as strictly hominid apomorphies, and their presence in an orangutan clade as autapomorphic for it and non-synapomorphic with hominids (i.e., features seen in hominid and orangutan clades are homoplastic), one must first embrace another theory of extant large-bodied hominoid relationship and then “explain away” the phylogenetic significance of the similarities between humans and orangutans, which is often done merely by declaring them homoplastic (e.g., Collard and Wood 2000, 2007; Diogo and Wood 2011; Lockwood and Fleagle 1999; Wood and Harrison 2011) as if homoplasy were identifiable without first presuming a theory of relationship based on characters deemed synapomorphic for other taxa (see discussion in Schwartz 2008; see also chapter “▶ Homology: A Philosophical and Biological Perspective”). This, of course, is the current state of affairs in paleoanthropology, wherein the molecular similarities between Pan and Homo are taken as evidence of their close relationship (e.g., see Lockwood et al. 2004; Pilbeam 1986, 2000; Gibbs et al. 2000, 2002; Wood and Harrison 2011), even though most of the “favorable” comparisons involve only small portions of the 2–3 % coding (i.e., metabolically, not developmentally relevant) region of the genome and rarely include the orangutan and an array of other catarrhines (e.g., Grehan and Schwartz 2009; Grehan and Schwartz 2011; Schwartz 2009, 2011, 2012; Schwartz and Maresca 2006). Although Wood and Harrison (2011) assert there is also “overwhelming. . .morphological evidence for a ((Pan, Homo) Gorilla) Pongo) pattern of relationships” and that features suggesting a Pongo-Homo sister group were “selected” to do so (p. 470), neither of these statements is correct, especially, “overwhelming-morphological evidence for with regard to a ((Pan, Homo) Gorilla) Pongo) pattern of relationships.” Although Groves (1986) is consistently cited as having demonstrated a close human-chimpanzee relationship, scrutiny of his data demonstrates not only that most of the features he presented in support of this

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contention are not synapomorphic because they are found in other primates listed (Grehan and Schwartz 2009; Groves 1986; Schwartz 1988, 2005) but, more importantly, that numerous features are either ambiguously or incorrectly reported (Grehan and Schwartz 2009). Unfortunately, Groves’ work has been reiterated without question in subsequent publications claiming demonstration of a Homo-Pan relationship (e.g., see especially Lehtonen et al. 2011; Strait and Grine 2004; Collard and Wood 2000; Gibbs et al. 2000, 2002). Further, in light of Wood and Harrison’s claim of “overwhelming. . .morphological evidence for a ((Pan, Homo) Gorilla) Pongo) pattern of relationships,” Wood’s own work (Collard and Wood 2000; Gibbs et al. 2000, 2002), which was based in large part on Groves (1986), delineated essentially no hard-tissue and only a handful of soft-tissue features in support of a human-chimpanzee sister group. With regard to the criticism that features in support of a human-orangutan sister group were selected to demonstrate this, scrutiny of the relevant publications reveals that in all cases the comparative morphological, physiological, and developmental data cited was available in the literature (Grehan and Schwartz 2009; Schwartz 1983, 1988, 2004a, 2005). When new data was introduced, it was spelled out and, as with all data, presented for an array of primates, not just humans and large-bodied hominoids (Grehan and Schwartz 2009; Schwartz 1983, 1988, 2004a, 2005). In contrast to Groves’ claiming Homo-Pan synapomorphy not only in the rare instances when only these two hominoids shared features but more frequently when other primates shared features present in humans and chimpanzees, I hypothesized synapomorphy only when two taxa exclusively shared a feature. Consequently, in every publication, I presented all alternative theories of relationship, including Homo-Pan, even though they differed significantly in degree of robustness (¼ corroboration). The fact of the matter is, even if one used Groves’ data without eliminating ambiguous or incorrect data, and hypothesized synapomorphy on the basis of exclusivity of shared features, Homo-Pan emerges as the least and Homo-Pongo as the most highly supported theory of relationship (Schwartz 1988). With the addition of more features to the data base, and in the context of a broad comparison among primates, the same pattern of relationship emerges (Grehan and Schwartz 2011). If one were to cast the stone of “selectively” choosing features to support a particular human-ape theory of relationship, it would have to be toward those who maintain a Homo-Pan sister group through reiteration of faulty morphological datasets and ignore additional data that might lead to a conclusion other than their preferred conclusion. Nevertheless, even if the latter phylogenetic hypothesis were true, this does not justify using Pan alone as the referent for defining clade Hominidae or for determining character polarity within this clade (e.g., see Asfaw et al. 1999; Brunet et al. 2002; Guy et al. 2005; Lovejoy et al. 2009b, c; Suwa et al. 2009; White et al. 1994, 2006; Wood and Harrison 2011). Rather, the broad comparative approach that Le Gros Clark might have pursued remains the more reliable way in which to hypothesize features that could distinguish a hominid from other primate clades and also determine character polarity within it. And, in doing so, one must also confront instances when humans, or hominids in general, compare more favorably with primates other than Pan, as, indeed, they often do with Pongo.

Pongo-like Dental and Palatal Features of Potential Hominids

An interesting case of “interpreter’s bias” lies in analyses of molar enamel thickness. For example, although Martin (1985) has been cited as demonstrating that the last common ancestor of largebodied hominoids had thick molar enamel (which was retained in orangutan and hominid clades but secondarily reduced in African apes), he merely interpreted enamel thickness data in the context of an [orangutan (human-African ape)] theory of relatedness (Schwartz 1987). Otherwise he should, or at least could, have concluded that thick molar enamel united human and orangutan clades. Kelley Page 26 of 39

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and Pilbeam (1986) also interpreted molar enamel thickness in the context of an [orangutan (humanAfrican ape)] theory of relatedness but presented two scenarios: Martin’s and one in which the last common ancestors of separate human and orangutan clades independently developed thick molar enamel. In the latter case, thick molar enamel would be a defining feature of Hominidae. In contrast, but embracing first a human-chimpanzee relationship, Suwa et al. (2009) could claim that thin enamel was secondarily derived in Pan. More recently, Schwartz (2000) found that, while humans and orangutans both have thick molar enamel, humans have thicker enamel in some areas of their occlusal surfaces. He suggested that thick molar enamel had evolved independently in humans and orangutans (and, by implication, in the last common ancestors of separate human and orangutan clades) because of the demands of different diets. A more straightforward interpretation of G. Schwartz’s data is that human and orangutan clades shared a thick-molar-enameled common ancestor and that, within this clade, humans (and perhaps other hominids) are more derived. Only by accepting thick molar enamel as synapomorphic of traditionally accepted hominids can one embrace thin-enameled Ardipithecus as a sister of this clade (assuming that this relationship is based on synapomorphy). Of course, Brunet et al.’s (2002) suggestion that the thicker enameled Sahelanthropus is ancestral to Ardipithecus, and Suwa et al.’s (2009) argument based on a presumed hominid-Pan sister group that thin enamel in the latter must be secondarily derived, underscores the need for systematic rigor in paleoanthropology. For, indeed, explaining the distribution of morphology based on an already accepted theory of relationship does not substitute for the generation of that theory. If thick molar enamel does not contribute to defining Hominidae, does dental morphology? Some aspects of it might (e.g., see discussion above on dm1 morphology) but, at present, delineating more than a handful of features would be a Herculean task. This difficulty derives from the longstanding notion of the Miocene being a time of an “ape radiation,” after which “hominids” emerged. Guided by this scenario, paleoanthropologists typically identified post-5.5 ma specimens with thickenameled cheek teeth as “hominid” and pre-5.5 ma specimens as orangutan relatives. Nevertheless, study of fossils identified as hominid reveals that Pongo-like teeth have often been referred to species of Homo and Australopithecus (Grine and Franzen 1994; Schwartz 2004a; Schwartz and Tattersall 1996). Teeth allocated to Orrorin tugenensis (Senut et al. 2001), if truly thick-enameled, reinforce the question of how many Miocene “apes” are actually hominids and how many PlioPleistocene “hominids” are not. In addition, since “hominid” teeth are often worn flat, little attention has been paid to details of occlusal morphology. Thus, although most of the human fossil record has now been scrutinized at the level of morphs (Schwartz and Tattersall 2002, 2003, 2005), much work on testing these hypotheses remains before assigning specimens (other than, of course named type specimens) to specific genera and species. Were it not for their presence in, for instance, Pongo, Sivapithecus, and Ankarapithecus, other features that could “define” Hominidae are the development of a single incisive foramen (Schwartz 1983, 1997) and a posteriorly thickened palate (as seen in midline cross section) (Schwartz 2004a). With regard to the palate, if the Hadar broken palate AL 200-1a does thin posteriorly, it would be the outlier among “accepted” hominids (Schwartz 2004a; Schwartz and Tattersall 2002, 2003, 2005). As with thick molar enamel and the morphological details of dm1, the simplest phylogenetic interpretation of these features is that they characterized the last common ancestor of human and orangutan clades.

Pongo-Like Features of “Australopiths”: Implications for Defining Hominidae

Another stumbling block to defining Hominidae is the degree to which “australopiths” and specimens traditionally allocated to Homo differ from one another, especially in craniofacial morphology, Page 27 of 39

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e.g., in orbital and nasal aperture outline as well as in the configuration of the supra- and infraorbital regions; elevation of the nasoalveolar clivus above the floor of the nasal cavity; height and orientation of the subnasal region; orientation, flatness, and height of the zygomatic region; development of a “snout” with/without facial pillars (vertical or medially inclined); and a canine fossa, and in the development and configuration of a mastoid process. Thus, while one might unite all of these potential hominids via various postcranial features, craniofacial morphology seems only to delineate possible hominid subclades. This may in part explain why one approach to associating living humans with Pan is to try first to link the latter with australopiths and then to assert, since australopiths and Homo form a clade, that humans and chimpanzees are closely related (Begun 1994; Begun et al. 1997). In the latter case, the primary feature of supposed synapomorphy between (an undefined) Australopithecus and Pan – bar-like supraorbital torus with sulcus behind – describes no “australopith” (e.g., Figs. 10 and 11) and only some specimens of Homo (e.g., Fig. 13; Clarke 1987; Schwartz and Tattersall 2002, 2003, 2005). In addition, not only is the markedly inferosuperiorly tall supraorbital region of Sahelanthropus not bar-like as in African apes [i.e., it is not both superiorly and slightly anteriorly projecting and bound posteriorly by a distinct posttoral sulcus; see Schwartz (1997) for discussion], it is so unusually tall that it must represent a derived, not primitive, configuration – which, together with its distinct dental morphology and not very thick molar enamel, makes determining its relationship to any hominid (or ape) difficult indeed (Schwartz 2004b). While seeking connections between fossil hominids and African apes (especially Pan) has historical precedent (Johanson and White 1979), the most favorable comparisons are actually between Pongo (and its fossil relatives) and australopiths and some specimens attributed to Homo (Grehan and Schwartz 2009; Schwartz 2004a, 2005), e.g., rim-like superior orbital margins with a rather smooth transition into the frontal plane; often ovoid orbits; and forwardly facing, tall, and often vertical zygomatic regions (a further derived configuration, e.g., as in KNM-WT 17000, is a posteriorly tilted zygoma) (Figs. 10, 11, 12, and 13). Since the faces of Pongo, Sivapithecus, and Ankarapithecus as well as of most specimens taken as being hominid are relatively tall superoinferiorly and, even with anteriorly oriented zygomas, relatively narrow from side to side, those specimens with broad and short faces (in the orangutan clade, Lufengpithecus and among hominids,

Fig. 11 Comparison of AL 444-1 (cast of reconstruction) with Pongo and Pan illustrating lack of Pan-like supraorbital, lower facial, and zygomatic morphology, but orangutan-specific features in the hominid. See text for further discussion; not to scale (Copyright # J. H. Schwartz)

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Fig. 12 Right lateral views of Pongo, Drimolen DNH 7, and Sts 5 (top row) and Pan, StW 505, and SK 48 (bottom row) illustrating, e.g., lack of Pan-like supraorbital, lower facial, and zygomatic morphology but orangutan-specific features in the hominids. See text for further discussion; not to scale (Copyright # J. H. Schwartz)

Fig. 13 Comparison of (left column) Pongo and StW 505 with various specimens allocated to Homo illustrating especially orangutan-like facial features. See text for further discussion; not to scale (# J. H. Schwartz)

e.g., AL 444-1, SK 48, KNM-ER 406, KNM-WT 17000, KNM-ER 3883) emerge as potentially derived, which for hominids may reflect relatedness among some, if not all of them (see also Schwartz and Tattersall 2005; Fig. 14). Many australopiths are also similar to Pongo in having distinct facial pillars that emerge just above the canines and, together with a variably developed canine fossa, delineate a “snout” [Figs. 10 and 11; see also illustrations in Schwartz and Tattersall (2005)]. Interestingly, the Taung specimen has the long, slit-like single incisive foramen seen in Pongo and also preserved in Sivapithecus and Ankarapithecus (Schwartz 2005). While I am not advocating a special relationship between a Pongo clade and some or all australopiths, attention to

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Fig. 14 Comparison of various specimens of “robust australopith” to illustrate similarly derived laterally broad and superoinferiorly short faces in SK 48, KNM-ER 406, and KNM-WT 17000, which might reflect their membership in a hominid subclade that does not include specimens such as DNH 7 and OH 5. See text for further discussion; not to scale (Copyright # J. H. Schwartz)

these apparent synapomorphies is more relevant to the task of defining Hominidae, its subclades, and sister taxa than is currently appreciated. Indisputable similarities between Pongo and australopiths exist (Schwartz and Tattersall 2005) and they should be accounted for in any critical evaluation of human-ape and within-hominid relationship. Further, these similarities make even more critical for defining a hominid clade and relationships within it broadening comparisons from solely between hominids and Pan alone, or between hominids and both African apes, to include as many catarrhine taxa as possible in order to provide the best foundation for delineating shared character similarity and determining character polarity – which are critical to phylogenetic reconstruction.

Conclusions When comparing extant taxa, defining Hominidae is a simple matter. Through a curious historical twist, Homo sapiens is the only survivor of a clade whose dimensions we will never fully know. Take, for instance, the discovery of an apparent hominid from the late Pleistocene of Flores, Indonesia, best seen in LB1 (Brown et al. 2004). Its combination of morphologies would be unexpected no matter what its age. LB1 has or had a moderately globular cranium (as in some hominids); somewhat thickened and anteriorly (but not superiorly) protruding but rim-like supraorbital margins with no sulcus behind (australopiths in part and orangutans and their relatives); tall, ovoid orbits (Pongo, Sivapithecus, some “australopiths”); flat nasal bones (most hominoids, including some Homo); forwardly facing and vertical yet superoinferiorly short zygomas (australopiths and orangutans and their relatives); well-developed mastoid processes (some “australopiths” and some Homo); a thick frontal with thick diploe (autapomorphic or pathological); no frontal sinuses (most primates, including bonobos); an anterior cranial fossa that does not extend fully over the orbital cones (most primates, including some Homo); a clivus that slopes gently away from the dorsum sellae (most primates, including some Page 30 of 39

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Homo); basion and bicarotid and biporionic chords in alignment (juvenile anthropoids, some adults); a broad incisive foramen that proceeds anteriorly as a expanding groove (a few “australopiths,” e.g., OH 5); marked separation of the nasoalveolar clivus and an anteriorly thin palate (African apes, some Miocene hominoids, some “australopiths”); a smoothly but narrowly curved mandibular symphyseal region (many anthropoids); a long retromolar space (various Homo); a broadly and smoothly rounded but somewhat truncated gonial angle (some Homo); a very anteroposteriorly long sigmoid notch (some Homo); a sigmoid notch crest that is deepest near the coronoid process (autapomorphic); very large cheek teeth and apparently relatively small anterior teeth (some “australopiths”); unusually mesiodistally short upper and lower molars with large mesial and truncated distal cusps (autapomorphic); a relatively long ilium (e.g., SK 50) with a beaklike anterior superior iliac spine (great apes, SK 50, MLD 7 and 25); a poorly defined iliac pillar (australopiths); a knoblike anterior inferior iliac spine that lies noticeably superior to above and somewhat back over the supra-acetabular rim (hominids as discussed here); an arcuate line that descends well before reaching the region of the acetabulum (some hominids); no ischial spine (most primates); posterior iliac expansion that defines a greater sciatic notch (hominids as used here); a “V”-shaped greater sciatic notch (most hominids, but not Neanderthals); a large femoral head (most primates); a long and anteroposteriorly compressed femoral neck (Orrorin, “australopiths” including BOU-VP-12/1, and some Homo, e.g., OH 62, KNM-WT 15000, D4167); a well-defined intertrochanteric crest (most primates, but not KNM-WT 15000, Orrorin, and most if not all “australopiths” or OH 62); a medially facing lesser trochanter (most primates, not “australopiths” or various Homo, e.g., OH 62, KNM-WT 15000, D4167); a weakly developed linea aspera (Orrorin and various “australopiths”); a femoral “carrying angle” (“australopiths” and Homo); a tibia that is much shorter than the femur (at least apes); poorly differentiated tibial tubercles (most primates); a medial tibial condylar facet that is situated higher than the lateral (at least apes); and a convex medial tibial facet (apes and some “australopiths,” e.g., AL 288-1a, AL 129-1b) (see Brown et al. 2004). Is this Flores specimen – if the cranial and postcranial remains represent a single individual – a hominid? A gut reaction based on the external morphology of the skull is “yes,” but the internal morphologies are odd. The teeth are not necessarily hominid, the humeral shaft lacks the torque or “twist” characteristic of large-bodied hominoids (Morwood et al. 2005) and the morphology of the distal articular region is clearly not hominoid (Morwood et al. 2005; Schwartz 1986), the tibia is definitely not hominid, the femur is Orrorin-like, and the partial os coxa is somewhat “australopith”-like. So why is the composite Flores specimen considered a species of Homo when its affinities to a clade Hominidae are not entirely clear? Largely because there has been a history of allocating specimens to taxa based more on their geological age than on their morphology – which, in turn, has led to the general practice of trying to explain away “anomalous” morphologies in terms of variation (see also chapter “▶ General Principles of Evolutionary Morphology”). Methodologically, however, before one even contemplates referring a specimen to a genus and species, one should have to defend first why any specimen is a hominid and then a member of the nested subclades that subsume that species (see also chapter “▶ Principles of Taxonomy and Classification: Current Procedures for Naming and Classifying Organisms”). But in order to do so, we must have a working definition of this potential clade that is open to criticism, testing, and revision, rather than constructed in the context of a presumed theory of hominid-ape and then hominid-subclade relationship, wherein primitive features dominate the description and homoplasy assumed demonstrable (Lovejoy et al. 2009a; Wood and Harrison 2011). In this regard, there is still much work to be done.

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Cross-References ▶ Analyzing Hominin Phylogeny ▶ Defining the Genus Homo ▶ Fossil Record of the Primates from the Paleocene to the Oligocene ▶ General Principles of Evolutionary Morphology ▶ Historical Overview of Paleoanthropological Research ▶ Hominoid Cranial Diversity and Adaptation ▶ Homo ergaster and Its Contemporaries ▶ Homology: A Philosophical and Biological Perspective ▶ Later Middle Pleistocene Homo ▶ Phylogenetic Relationships (Biomolecules) ▶ Potential Hominoid Ancestors for Hominidae ▶ Principles of Taxonomy and Classification: Current Procedures for Naming and Classifying Organisms ▶ Species Concepts and Speciation: Facts and Fantasies ▶ The Earliest Putative Hominids ▶ The Origins of Bipedal Locomotion ▶ The Species and Diversity of Australopiths

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Pilbeam D (2000) Hominoid systematics: the soft evidence. Proc Natl Acad Sci U S A 97:10684–10686 Rak Y (1990) On the differences between two pelvises of Mousterian context from the Qafzeh and Kebara caves. Am J Phys Anthropol 81:323–332 Robinson JT (1972) Early hominid posture and locomotion. University of Chicago Press, Chicago Rose MD (1984) A hominine hip bone, KNM-ER 3228, from East Lake Turkana, Kenya. Am J Phys Anthropol 63:371–378 Rosenberg KR (1998) Morphological variation in west Asian postcrania. In: Akazawa T, Aoki K, Bar-Yosef O (eds) Neandertals and modern humans in Western Asia. Plenum, New York, pp 367–379 Rosenberg KR, Lu Q (1997) The pelvis of the Jinniushan specimen: an East Asian perspective on Neandertal morphology. Am J Phys Anthropol Suppl 24:199–200 Sawyer GJ, Maley B (2005) Neanderthal reconstructed. Anat Rec Part B New Anat 283B:23–31 Schultz AH (1968) The recent hominoid primates. In: Washburn SL, Jay PC (eds) Perspectives on human evolution. Holt, Rinehart and Winston, New York, pp 122–195 Schwartz JH (1983) Palatine fenestrae, the orangutan and hominoid evolution. Primates 24:231–240 Schwartz JH (1986) Primate systematics and a classification of the order. In: Swindler DR, Erwin J (eds) Comparative primate biology. Alan R. Liss, New York, pp 1–41 Schwartz JH (1987) The red ape: orangutans and human origins. Houghton Mifflin, Boston Schwartz JH (1988) History, morphology, paleontology, and evolution. In: Schwartz JH (ed) Orangutan biology. Oxford University Press, London, pp 68–85 Schwartz JH (1997) Lufengpithecus and hominoid phylogeny: problems in delineating and evaluating phylogenetically relevant characters. In: Begun DR, Ward CV, Rose MD (eds) Function, phylogeny, and fossils: Miocene hominoid evolution and adaptations. Plenum, New York, pp 363–388 Schwartz JH (1999) Sudden origins: fossils, genes, and the emergence of species. Wiley, New York Schwartz GT (2000) Taxonomic and functional aspects of the patterning of enamel thickness distribution in extant large-bodied hominoids. Am J Phys Anthropol 111:221–244 Schwartz JH (2004a) Barking up the wrong ape – australopiths and the quest for chimpanzee characters in hominid fossils. Coll Antropol 28:87–101 Schwartz JH (2004b) Issues in hominid systematics. In: Baquedano E, Rubio Jara S (eds) Miscelánea en homenaje a Emiliano Aguirre. Museo Arqueológico Regional de la Comunidad de Madrid, Madrid, pp 360–371 Schwartz JH (2005) The red ape: orangutans and human origins. Westview, Boulder Schwartz JH (2007a) Defining Hominidae. In: Henke W, Tattersall I (eds) Handbook of paleoanthropology. Springer, Berlin, pp 1379–1408 Schwartz JH (2007b) Skeleton keys: an introduction to human skeletal morphology, development, and analysis, 2nd edn. Oxford University Press, New York Schwartz JH (2008) Cladistics. In: Regal B (ed) Icons of evolution. Greenwood Press, Westport, pp 517–544 Schwartz JH (2009) Organismal innovation. In: O’Brien MJ, Shennan SJ (eds) Innovations in cultural systems: contributions from evolutionary anthropology. MIT Press, Cambridge, MA, pp 53–67 Schwartz JH (2011) Developmental biology and human evolution. Hum Orig Res 1:7–14 Schwartz JH (2012) Molecular anthropology and the subversion of paleoanthropology: an example of the ‘emperor’s clothes effect’? Hist Philos Life Sci 34:237–258

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Schwartz JH, Maresca B (2006) Do molecular clocks run at all? A critique of molecular systematics. Biol Theory 1:1–15 Schwartz JH, Tattersall I (1996) Who’s teeth? (comment on the Longgupo hominoids). Nature 381:201–202 Schwartz JH, Tattersall I (2000a) The human chin: what is it and who has it? J Hum Evol 38:367–409 Schwartz JH, Tattersall I (2000b) Variability in hominid evolution: putting the cart before the horse? In: Antunes M (ed) Últimos Neandertais em Portugal (Last Neandertals in Portugal) Odontologic and other evidence. Academia das Ciéncias de Lisboa, Lisboa, pp 367–401 Schwartz JH, Tattersall I (2002) The human fossil record, volume one, terminology and craniodental morphology of genus Homo (Europe). Wiley-Liss, New York Schwartz JH, Tattersall I (2003) The human fossil record, volume two, craniodental morphology of genus Homo (Africa and Asia). Wiley-Liss, New York Schwartz JH, Tattersall I (2005) The human fossil record, volume four: craniodental morphology of Australopithecus, Paranthropus, and Orrorin. Wiley-Liss, New York Schwartz JH, Tattersall I (2010) Fossil evidence for the origin of Homo sapiens. Yearb Phys Anthropol 53:94–121 Senut B, Pickford M, Gommery D, Mein P, Cheboi K, Coppens Y (2001) First hominid from the Miocene (Lukeino formation, Kenya). Comptes Rendue des Académie de Sci (Paris) Ser IIa 332:137–144 Simpson SW, Quade J, Levin NE, Butler R, Dupont-Nivet G, Everett M, Semaw S (2008) A female Homo erectus pelvis from Gona, Ethiopia. Science 322:1089–1092 Strait DS, Grine FE (2004) Inferring hominoid and early hominid phylogeny using craniodental characters: the role of fossil taxa. J Hum Evol 47:399–452 Strauss A, Gunz P, Spoor F (2012) Late juvenile cranial growth in hominids. Proc Eur Soc Stud Hum Evol 1:177 Strauss A, Gunz P, Benazzi S, Spoor F (2013) Late juvenile cranial growth and the diagnosis of Australopithecus sediba. Proc Eur Soc Stud Hum Evol 2:218 Suwa G, Kono RT, Simpson SW, Asfaw B, Lovejoy CO, White TD (2009) Paleobiological implications of the Ardipithecus ramidus dentition. Science 326:94–99 Swarts JD (1988) Deciduous dentition: implications for hominid phylogeny. In: Schwartz JH (ed) Orangutan biology. Oxford University Press, New York, pp 263–270 Swindler DR, Wood CD (1973) An atlas of primate gross anatomy: baboon, chimpanzee, and man. R. E. Krieger, Malabar Tardieu C, Trinkaus E (1994) Early ontogeny of the human femoral bicondylar angle. Am J Phys Anthropol 95:183–195 Toussaint M, Macho GA, Tobias PV, Partridge TC, Hughes AR (2003) The third partial skeleton of a late Pliocene hominid (Stw 431) from Sterkfontein, South Africa. S Afr J Sci 99:215–223 Trinkaus E (1983) The Shanidar Neandertals. Academic, New York Trinkaus E, Howells WW (1979) The Neanderthals. Sci Am 241:118–133 Trinkaus E, Lebel S, Bailey SE (2000) Middle Paleolithic and recent human dental remains from the Bau de l’Aubesier, Monieux (Vaucluse). Bulletin et Mémoir de la Société d’Anthropologie de Paris 12:207–226 Turner CGI, Nichol CR, Scott GR (1991) Scoring procedures for key morphological traits of the permanent dentition: the Arizona State University dental anthropology system. In: Kelly MA, Larsen CS (eds) Advances in dental anthropology. Wiley-Liss, New York, pp 13–32

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Ulhaas L (2009) Computer reconstruction: Technical aspects and applications. In: Henke W, Tattersall I (eds) Handbook of paleoanthropology. Springer, Berlin, pp 787–813 Walker AC, Leakey RF (1993) The postcranial remains. In: Walker A, Leakey R (eds) The Nariokotome Homo erectus skeleton. Harvard University Press, Cambridge, MA, pp 95–160 Ward CV, Kimbel WH, Johanson DC (2011) Complete fourth metatarsal and arches in the foot of Australopithecus afarensis. Science 331:750–753 White TD (2003) Another perspective on hominid diversity – response. Science 301:703 White T (2012) Paleoanthropology: fives a crowd in our family tree. Curr Biol 23 White TD, Suwa G, Asfaw B (1994) Australopithecus ramidus, a new species of early hominid from Aramis, Ethiopia. Nature 371:306–312 White TD, WoldeGabriel G, Asfaw B, Ambrose S, Beyene Y, Bernor RL, Boisserie J-R, Currie B, Gilbert H, Haile-Selassie Y, Hart WK, Hlusko LJ, Howell FC, Kono RT, Lehmann T, Louchart A, Lovejoy CO, Renne PR, Saegusa H, Vrba ES, Wesselman H, Suwa G (2006) Asa Issie, Aramis and the origin of Australopithecus. Nature 440:883–889 Wood BA, Collard M (1999) The changing face of the genus Homo. Evol Anthropol 8:195–207 Wood B, Harrison T (2011) The evolutionary context of the first hominins. Nature 470:347–352 Zipfel B, DeSilva JM, Kidd RS, Carlson KJ, Churchill SE, Berger LR (2011) The foot and ankle of Australopithecus sediba. Science 333:1417–1420

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Index Terms: Apomorphies 25 Ardipithecus 8, 22, 27 Australopithecus 27 Australopiths 5, 27 Bipedalism 20 Character selection 6 Dentition 2, 24 Erect posture 6 Gorilla 22–23 Hominidae 1 Homo 5, 11, 23 Morphology 23, 27, 31 Orrorin 17, 31 Pan 22, 25 Plesiomorphies 19 Pongo 22, 29 Primitive versus derived features 5 Sahelanthropus 21–22

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

Origins of Hominini and Putative Selection Pressures Acting on the Early Hominins Bogusław Pawłowski* and Wioletta Nowaczewska Department of Human Biology, University of Wroclaw, Wroclaw, Poland

Abstract One of the biggest mysteries of human evolution is the divergence of the hominin lineage from the other hominoids. This chapter addresses the problem of the selective forces that might have been behind hominin emergence and that shaped this evolutionary lineage in its early stages. To establish the selection pressures that led to hominin emergence, the following issues will be discussed: (1) The time when the human–chimpanzee split could have taken place according to paleoanthropological and molecular data. (2) The putative traits of the last common ancestor (LCA) of Hominini and extant Panini. The models for the LCA can be constructed only on the basis of the fragmentary fossils of the earliest hominins (ErH) and on the basis of the morphology and behavior of extant apes. (3) The environment in which the ErH lived and could have been exposed to some specific selection pressures. (4) The hypotheses for the selection pressures for bipedality (SPf B), which is the main diagnostic trait of the hominin clade. Some arguments for and against suggested SPf B according to different hypotheses will be presented. (5) The putative selection pressures related to the dental features of ErH. A much more difficult task is inferring behavior (including the social structure) of ErH. Since the fossils of the earliest hominins are so scarce, inferences as to their behavior are possible mainly on the basis of some features of Ardipithecus ramidus (Ar. ramidus) representatives, i.e., their overall body size, sexual dimorphism in body size, and sexual dimorphism of the canines. Finally, the future perspective (e.g., through closer integration of paleoanthropology and genetics) for determining the first appearance of derived hominin traits and the selection pressures that acted upon them is discussed.

Introduction The theory of evolution with its central tenet of Darwinian natural selection provides the scientific framework that gives the opportunity to understand the evolution of all life-forms including the hominins. Some lineage-specific phenotypic traits that can be observed in the fossil record or in living organisms ought to be explicable by certain selection forces. It is assumed that the traits that appeared and were perpetuated in some lineages were adaptive, i.e., were related to an improvement in relative reproductive success or in overall biological fitness, in relation to the specific physical or social environment. The factors that contributed to higher reproductive success of organisms that had some novel phenotypic feature are called selection pressures, and they can act either on morphology, physiology, or behavior. Natural selection is a process by which new adaptive traits (e.g., morphological, physiological, or behavioral) evolve and persist. In a population with heritable

*Email: [email protected] Page 1 of 29

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variation of traits, this can lead to phenotypic changes over consecutive generations. Although such processes as genetic drift or any other nonselective (random) forces may act on organisms and cause some lasting effects, it is mainly natural selection that produces long-term directional change (Ward 2002). In the Late Pliocene, when hominins developed Paleolithic technology and became to some extent dependent on culture, they were released from some previously effective selection pressures (e.g., stone tools and the ability to control fire could have dramatically weakened the effect of predation pressure). However, before these inventions, i.e., in the Late Miocene and for most of the Pliocene, hominins were exposed to natural selection factors in the same way as other organisms. This means that for a large part of our evolution, human ancestors were constrained and directed by similar natural pressures to those acting on other organisms. The main types of selection pressures acting on the ErH might have been related to variability in climatic conditions and change in habitat, which can be driven by climate change and is usually strongly related to the types of food available, to predation or sociosexual factors (including sexual selection), and to biomechanical or energetic constraints. In the early stages of hominin evolution, some specific features emerged that demand evolutionary explanation (e.g., bipedalism and certain dental features). There are, however, a few serious difficulties with the reconstruction of the selection pressures for hominin emergence. Reconstruction of the selection pressures that triggered the Panini–Hominini (P-H) split is today a somewhat more difficult task than it was only 15–20 years ago. This is because in the last two decades, we have gained new fossils that make the picture of human evolutionary tree more difficult to determine. What is more, some fossils attributed by their discoverers to the hominin clade are controversial in terms of the interpretation of features that may be homoplasies or retained hominoid primitive features (Wood and Harrison 2011). The most controversial of these is Sahelanthropus tchadensis, dated at over 6 Ma (Brunet et al. 2005), for which we have only craniodental material that was found ca 2,500 km west of the African Great Rift Valley (traditionally seen as the cradle of the hominins). This form exhibited small upper canines (worn at the tip) and the position of the foramen magnum suggests that this form was bipedal. These two traits were recognized as principal indicators of its hominin status (Brunet et al. 2005). Some authors, however, disagree that this form is a hominin and contest the inference, made on the basis of the position of the foramen magnum, that it was bipedal (Wolpoff et al. 2002). Less controversial the earliest hominin is Orrorin tugenensis from Lukeino Formation, dated to between 6.2 and 5.6 Ma (Senut et al. 2001; Pickford et al. 2002). Its remains include 13 specimens (fragments of hand, arm, and lower limb). The discoverers of Orrorin argued that the dental morphology of this form was “apelike” (its upper canine resembles that of a female chimpanzee) (Pickford et al. 2002). Based on morphology of its femur (BAR 1002’00), humerus, and manual phalanx, it is claimed that Orrorin possessed the adaptations both for bipedal locomotion and arboreal climbing (Senut et al. 2001; Pickford and Senut 2001; Richmond and Jungers 2008). Another genus widely attributed to the earliest hominins is Ardipithecus, containing two species: Ardipithecus kadabba (Haile-Selassie et al. 2004) from Central Awash Complex and the Western Margin, Middle Awash in Ethiopia, dated between 5.8 and 5.2 Ma, and the betterknown Ar. ramidus dated to 4.4 Ma from the Afar Rift region (northeastern Ethiopia) (White et al. 2009). A relatively complete skeleton of the latter species (ARA-VP-6/500 – Ardi) provides data for the reconstruction of the earliest stages of human evolution and allows suggesting the putative traits of LCA of the Hominini and Panini clades (White et al. 2009). The preservation state of Ardi makes possible the comprehensive study of locomotion, morphology of the teeth, body size, and even sexual dimorphism of the earliest hominins.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

The presence of the small canines and the lack of the C/P3 honing complex (characteristic of chimpanzees) in Sahelanthropus and Ardipithecus are traits they share with later hominins and are described as most indicative of their hominin status (Wood and Harrison 2011). However, as noted by Wood and Harrison (2011), the traits mentioned above are also visible in a number of Late Miocene Eurasian hominids, and they probably developed in response to dietary behavior changes, induced by ecological conditions. We cannot then reject the possibility that a similar evolutionary response also took place in African Late Miocene hominids. There is similar problem with postcranial evidence for bipedalism in the earliest hominins and in European Late Miocene Oreopithecus bambolii (Wood and Harrison 2011). All these observations indicate that recognition of the earliest unquestionable hominins is still a difficult task. One cannot exclude the possibility that the currently ascribed traits to the earliest hominins will appear to be also the features of other members of hominid lineage (e.g., chimpanzee). Only new discoveries of more complete skeletons of Miocene African hominids would help to resolve this issue. Another problem with the early stage of hominin evolution concerns methodology. Each new trait that appeared in ErH could be a real adaptation that emerged under some specific selection pressure, or it could be a trait that appeared as a side effect of some other functionally adaptive trait. If a new trait that was not under direct selection pressure later acquired some new function, it is called an exaptation. An exaptation – the term was coined by Gould and Vrba (1982) – is thus a trait that was not designed by selection. The appearance of such new by-products, nonadaptive traits, could be due to the effects of pleiotropy. When strong selection acts on a feature determined by a particular gene and if this gene is also responsible for some other feature, the latter feature can emerge irrespective of its adaptiveness and without any specific selection pressure on that particular trait. Thus, the presumption that all anatomical or behavioral traits are adaptively informative (Hlusko 2004) does not always need to be true. This also means that some morphological traits are not independent and should be analyzed as if they were dependent (Hlusko 2004) and not the effect of different selection pressures on each of the new features. We must then be aware that, the case of some derived hominin traits, one can be faced with side effects that were only later co-opted for a new function and which at the time of their evolutionary appearance were not selected specifically for the function they later acquired. All this makes the reconstruction of the selection forces that triggered the P-H split a very difficult task. To try to decipher the selection pressures that led to hominin emergence on the basis of our present knowledge, the following problems will be addressed in this chapter: 1. 2. 3. 4.

The time when the P-H split could have taken place. The putative traits of the last common ancestor of hominins and chimpanzee. The environment in which the ErH lived and was exposed to specific selection pressures. Possible hypotheses for selection pressures for bipedality, the main diagnostic trait of the hominin clade. 5. The putative selection pressures related to the dental features of ErH. 6. Whether on the bases of paleoevidence and socioecological rules, we can infer something about the behavior and social structure of the ErH (inferences from body size, sexual dimorphism in body size, and from canine size in ErH). This chapter concerns the problem of selective forces that might have been related to hominin emergence and that could have shaped this evolutionary lineage at the stage of the early hominins, i.e., before 3.0 Ma. The selection pressures for the traits that appeared in the genus Homo at the end of Pliocene or in Pleistocene will be not analyzed here (e.g., brain size increase, rate of enamel Page 3 of 29

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formation, longer development and growth time span, language or cultural inventions, including stone technology, for which the oldest evidence we have comes from ca. 2.5 to 2.9 Ma).

When Did the Hominin Lineage Diverge from the African Extant Hominoids? Early in the second half of the twentieth century, it was thought that the human lineage diverged from the lineage of living apes sometime between 10 and 15 Ma. This very early date for the origins of hominins was set in view of the strong peculiarities of humans, which were then seen as needing a long time to evolve, and because of the mistaken inclusion of the thick-enameled Miocene Asian ape Ramapithecus in the human evolutionary tree. Only in the late 1960s did pioneering molecular analyses (Wilson and Sarich 1969) reveal that the human–great ape split must have taken place at a much later date. The reassessment of Ramapithecus taxonomy and a stricter approach to all Miocene and Pliocene hominoid fossils from Africa confirmed that in fact there is no good fossil evidence of hominins before 7–5 Ma. Fossils found later and many new molecular results confirmed that dating. It now seems that there is a quite high concordance between the two kinds of evidence. Although in a range of molecular analyses the split was assessed from 3.6 (Easteal and Herbert 1997) to 13 Ma (Arnason et al. 1998), the bulk of analyses indicated either 7–5 Ma (Glazko and Nei 2003) or more extent 4–8 Ma (Wood and Harrison 2011). It is now generally held that for calculating the time of the human–great ape divergence, nuclear genes are a better guide than mtDNA. The evolutionary changes in mtDNA over time vary among different lineages, and for time estimation, we should use genes that follow a global molecular clock (Glazko and Nei 2003). Based on the results encompassing the comparison of the genome sequence of the western lowland gorilla with the genomes of the extant hominoids (including Homo sapiens), Scally et al. (2012) considered the variation in past mutation rates (10 9 mutations per bp per year in the common ancestor of great apes and possibly 0.5-0.6*10 9 afterwards) and suggested that the human–chimpanzee split was between 5.5 and 7 Ma and human–chimpanzee–gorilla speciation between 8.5 and 12 Ma. The majority of paleoanthropologists now agree that hominins appeared between 5.4 and 7.0 Ma. If the controversial Miocene taxa Sahelanthropus and Orrorin are unambiguous hominins, then this divergence would have taken place closer to 7 Ma than to 5 Ma. Molecular data also bring an interesting perspective to selection intensity in the hominin and panin clades. The hominin lineage very likely underwent a reduction in effective population size after the divergence from the chimpanzee clade (Chen and Li 2001). This would indicate that our lineage was exposed to more intensive selection pressures than other hominoids. Furthermore, comparative genetic studies also indicate that the speciation event that gave rise to hominins and chimpanzees did not involve an extended period of gene flow between the emerging species (Wakeley 2008). Thus, it is very likely that this speciation was allopatric, i.e., related to geographic isolation of these two clades. This is in contradiction to Navarro and Barton (2003), who suggested that there was a relatively long period of gene flow in collinear chromosomes and therefore hybridization between ErH and its closest contemporary African ape (the ancestral chimpanzee). The long period of genetic exchange between these lineages was also suggested by Patterson et al. (2006), who estimated that human–chimpanzee speciation occurred before 6.3 Ma. These results were, however, later contested by Wakeley (2008).

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We can tentatively conclude that knowing the estimated time of hominin emergence and the ecological circumstances of its occurrence in Africa allows reconstructing and perhaps identifying a small pool of possible selective factors that could have driven the P-H evolutionary split.

Last Common Ancestor One way to infer the nature of the selective forces that were the main causes of the emergence of the hominin lineage from the species described as the “last common ancestor” (LCA) of humans and chimpanzees would be on the basis of the best available knowledge about the morphology of LCA, about the first derived traits that appeared in the earliest hominins, and about the place and environment in which the earliest hominins and the earliest representative of the chimpanzee lineage appeared. Unfortunately, at present, remains of African Late Miocene great apes among which LCA could be found are scarce (Suwa et al. 2007). This means that it is possible to construct models for the LCA on the basis of the fragmentary ErH fossils and on the basis of behavioral ecology of extant apes. It is also possible to infer the nature of the selective forces that existed at that time, because we have some information on the biotopes in which the ErH lived. However, one must be aware that there is no certainty that ErH really emerged in the areas and in the habitats from which we have fossil evidence of these forms. Previously it was assumed that in cranial capacity, facial or dental features, as well as in postural ability, the LCA generally resembled the extant African apes. This form was described as living and foraging in the African tropical rainforest and using knuckle-walking locomotion on the ground (Richmond et al. 2001). The new specimens of the Ar. ramidus changed the views on the morphology and behavior of the LCA of human and chimpanzee lineages. The morphology of the skeleton of Ar. ramidus was not transitional between Australopithecus and its hypothetical apelike ancestor (earlier considered as similar to chimpanzee) (Lovejoy 2009; White et al. 2009). The traits exhibited by Ardipithecus indicate that the LCA probably had a low degree of sexual dimorphism, lacked specializations for knuckle-walking and suspension, had relatively thin enamel in the postcanine teeth, and had an omnivorous/frugivorous diet (Lovejoy 2009; White et al. 2009). Although currently there are more remains of Ardipithecus, there is still an inadequate number of fossils and an absence of an archaeological record which would allow scientists to determine the social structure of the LCA. To reconstruct the behavior and reproductive strategies of the LCA, both parsimony and known socioecological rules are usually used for different behavioral traits present in the extant hominoids. Some scientists claim that the LCA and ErH were behaviorally most similar to the extant chimpanzees (McGrew 2010), but others contest this assumption (Sayers et al. 2012). Taking into account Ardipithecus body size and canine size dimorphism, the chimpanzee model might not be the best for inferring the LCA social structure. In order to infer social system of LCA and to avoid the chimpanzee referential doctrine, one should consider the characteristics, present in all extant African hominoids, such as: • • • •

Male philopatry and female exogamy Male kin bonding social groups and coalitionary behavior Relatively complex interpersonal interactions Polygamy

These forms were also relatively intelligent and might have even used some rudimentary tools (view strongly supported by McGrew 2010). If the earliest hominins were sexually dimorphic in Page 5 of 29

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

body size, the dinichism of LCA could be also inferred. Females could have had smaller home ranges and a somewhat different diet, e.g., as a smaller form, they could have more frequently used trees not only to escape from predators but also as a source of food and shelter. Knowing the main evolutionary morphological adaptations that appeared in hominin evolution allows scientists to concentrate on the features that are distinctive of our close living relatives (the great apes). On the basis of this knowledge, modern Darwinian theory allows to make intriguing inferences about the selective pressures that could well have been responsible for the new (i.e., derived) traits that characterized the emergence of hominins.

Climate and Environment at the Time of Hominins’ Emergence There is a general premise that shifts in climate alter habitats and thus constitute selection pressures leading to speciation (DeMenocal 2004). It is known from many evolutionary lineages for different animals that key turnover events took place during times of climatic and ecological change (for more detail about climate influences on hominin evolution, see Vrba, Vol. 3, chapter “▶ Paleoenvironments and Hominin Evolution”). Until the late 1980s, it was assumed that the earliest hominins lived in open savanna environments and that the biotope they inhabited was a principal factor in the emergence of the hominins. The change of the east Africa environment to a more open, drier, and cooler habitat has been proposed as a main cause for the most important adaptive changes in hominins’ evolution during the Plio-Pleistocene (“savanna hypothesis”) (Vrba et al. 1989). However, with the addition of new paleoecological data from hominin fossil sites dating from the Late Miocene to the Early Pliocene, this hypothesis has been seriously undermined. We realize now that ErH lived in more mixed or wooded settings (Cerling et al. 1997; Brunet et al. 2005; Le Fur et al. 2009; WoldeGabriel et al. 2009; Blondel et al. 2010) and that the widespread expansion of more open environments in Eastern and Southern Africa took place a few million years after the emergence of bipedality (e.g., DeMenocal 2004; DeMenocal 2011). Between 4 and 1 Ma, the main faunal turnover in the Turkana Basin occurred at four main periods: 3.4–3.2, 2.8–2.6, 2.4–2.2, and 2.0–1.8 Ma (Bobe and Behrensmeyer 2004). The second and third intervals seem to coincide with the presence of Paranthropus, and the last one with grassland expansion and the first appearance of Homo ergaster. Pollen analysis also indicates that it was only after ca. 3 Ma that expansion of xeric vegetation took place (Dupont and Leroy 1995). Also, stable isotopic analyses of pedogenic carbonates from Turkana and Olduvai indicate a step-like increase in open habitats ca. 1.8 Ma (Cerling 1992). There is evidence that climatic and habitat changes triggered selection pressures that resulted in the emergence of Paranthropus and Homo and that they also triggered selection for the origin of other hominins (DeMenocal 2011). Reed (1997) reconstructed Plio-Pleistocene habitats on the basis of the analysis of mammalian fossil assemblages. She compared eight vegetative habitat types in order of tree density forests: closed woodland, woodland bushland transition, medium density woodland and bushland, open woodlands, shrubland, grasslands, and desert. It is not surprising that the percentage of arboreal locomotion decreases as these habitats progress from forest to desert. Using fossil mammals from different African sites, Reed (1997) showed the relationship between habitat type and two ecovariables (locomotor and trophic). These two variables proved to be better indicators for habit differentiation than body size. According to her analysis, the percentage of arboreality and frugivory between 3.6 and 1.8 Ma in East Africa demonstrates closed to open woodland habitats. Only later does it drop to percentages indicative of shrub and grassland. All this means that there is more

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

evidence that climatic and habitat changes triggered selection pressures that resulted in the emergence of Paranthropus and Homo than that they triggered selection for the origin of earlier hominins. Paleobotanical and faunal evidence clearly indicate that the sites bearing fossils of Orrorin (Pickford et al. 2002), Ardipithecus (WoldeGabriel et al. 2009), Au. anamensis (White et al. 2006), and Au. afarensis represent mainly tree-dominated habitats (predominantly closed woodland). Although Au. anamensis (Leakey et al. 1995) and Sahelanthropus (Vignaud et al. 2002; Le Fur et al. 2009; Blondel et al. 2010) probably lived in more mosaic environments (gallery forests at the edge of lakes and savanna and grassland away from lakes), the places where they were found are related to a lacustrine type of gallery forest. These new data displace the long-held idea that bipedalism first emerged when climate change forced our ancestors to live in open environments. The “savanna hypothesis” gained a serious opponent called the “forest hypothesis” (Rayner et al. 1993), which states that it was dense vegetation that played an important role in the evolution of early hominins. It is the forest hypothesis that explains why ErH retained upper limb morphology with the functional capacity to climb trees (see next section). Data from western and southern Africa clearly indicate that the savanna hypothesis may instead be applicable to the emergence of the Paranthropus and Homo genera and not to the divergence of hominins from other hominoids (Bobe and Behrensmeyer 2004; DeMenocal 2011). The change to more open habitat cannot, however, be completely excluded as a possible factor that triggered the acquisition of upright posture and the appearance of hominin lineage. It is possible that this bipedality emerged in the open environment in another region of Africa that is a still unknown cradle of hominin origin. Although the distribution of grassland before the Pliocene remains unclear, open habitats were present in Africa from the Middle Miocene (Retallack et al. 1990). Paleobotanical studies show that grass-dominated savanna became widespread both in west and east tropical Africa in the Late Miocene (ca. 8 Ma) (Jacobs 2004). This is documented by pollen and carbon isotopes. In the Late Miocene, Asian monsoons also influenced North and East Africa (Griffin 2002), and there was substantial environmental change from dense woodlands to grasslands or open woodlands in Asia (Barry 1995). Increased aridity around the Mediterranean and North Africa could also have led to the regional differentiation of apes. It is quite likely that such changes were not just coincidental with the rise of the hominins. Furthermore, if, as some claim (Rook et al. 1999; Wood and Harrison 2011), Oreopithecus bambolii in Europe was a biped and if this trait evolved in an open environment, then there is a strong argument that open habitat could be related to selection pressure that could have led to upright posture. All this means that there is no certainty whether the discovered fossil sites really represent the hominin cradle. They might just reflect later expansion of hominins from places with more open habitats. New studies on the stable carbon isotopes in fossil soils from hominin sites in eastern Africa (Awash and Omo-Turkana basins) showed that since ca. 7 Ma woody cover was less than 40 % at most hominin sites examined (Cerling et al. 2011). This would mean that over the past six million years in eastern Africa, open habitats predominated. This result is surprising because the carbon isotopes analysis from the teeth of several Ar. ramidus individuals showed that they consumed C3 plants in woodlands or in patches of forests (Louchart et al. 2009; White et al. 2009). Furthermore, these hominins’ bearing sites were rich in fragments of fossilized wood, and the analyses of the isotopic paleosol compositions indicate wooded conditions (WoldeGabriel et al. 2009). This might, however, be reconciled with time-frame results obtained by Cerling et al. (2011). They found that from Late Miocene to Early Pliocene (about 5.7–4.4. Ma) in Awash Valley and between 7.4 and 5.7 Ma in Omo-Turkana Basin, there was sparse wood cover. They also indicate that in this region of Africa, there was expansion of woody vegetation during the middle Pliocene. The same authors Page 7 of 29

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

suggest that open habitats were associated with presence of the earliest hominins and that Australopithecus lived in more wooded environments. If they are right, it means that the emergence of the hominin clade could be associated with the significant shift in habitat conditions occupied by ancestors of the first hominins and that the “savanna hypothesis” may be reinstated as a potential hypothesis explaining the appearance of the bipedality. Further data are needed to resolve this problem. Apart from two “habitat selection” hypotheses, there is also the “variability selection” hypothesis (Potts 1998), which is discussed in detail by Vrba. This hypothesis says that climate-driven habitat fluctuations over the last 6 Ma in Africa created disparity in adaptive conditions and caused habitatspecific adaptations to be replaced by morphological and behavioral adaptations to complex environmental changes (Potts 1998, 2012; Donges et al. 2011). It points to environmental instability as a main factor of selection among hominins for higher plasticity and new “multihabitat” adaptations. The crucial adaptations of the hominins seem to confirm that this group became adapted to variable environments. Bipedal locomotion and the retained tree climbing ability of the australopithecines made it easier to move relatively effectively both in densely forested and in open habitats. Dental traits adapted to hard and soft food, large brain volume, complex social behavior, and cultural adaptations in Homo permitted flexible responses to quite a wide diversity of climatic and habitat conditions. Although the variability hypothesis is very attractive and seems to explain the high plasticity of early hominin morphology adapted to different habitats, behavior, and later technological inventions, it is not in line with the basic selection mechanisms working in relation to the acting present environmental and social conditions. Unless environmental changes happened really fast, it is hard to believe that for organisms with a generation time of 16–20 years (and for early hominins even less: 10–14), in a period of 40–100 thousand-year cyclicity, selection would keep costly adaptations for conditions prevailing in the distant future. One could also ask how the proposed frequent periodicity worked in the lineages of any other extant taxa.

Bipedal Locomotion as the Most Difficult Trait to Explain for the Early Hominins There are many long-standing questions in paleoanthropology, but one of the most fundamental is why, in one lineage of hominids (but controversial Oreopithecus), selection promoted a new form of locomotion. Bipedalism is the hallmark trait for hominin evolution and its evolution poses a great conundrum for paleoanthropologists. The explanation of the emergence of this trait in human earliest ancestors is important, because this new locomotor pattern probably made possible (i.e., was a preadaptation to) the next great evolutionary jump, the emergence of the genus Homo, with its relatively bigger brain and with a postcranial anatomy almost indistinguishable from ours. We neither want to address here the morphological and biomechanical aspects of bipedality nor to discuss the debate on the differences in bipedal locomotion between different forms of Hominini. What we want to touch on in this chapter are the putative selection pressures for the emergence of this unusual, for primates, way of locomotion and the putative pressures for enhancing the effectiveness of this locomotion in early Homo. Many hypotheses have been put forward to explain bipedality. The first one came from Darwin, who suggested that it was the pressure for freeing the hands for the use of tools or weapons (Darwin 1871, p. 80). The problem with this, and with several later hypotheses, is that the proposed selective force could have been the consequence and not the cause of this evolutionary trait. Page 8 of 29

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

Darwin himself was already aware of the risk of feedback loops between causes and consequences and recognized the difficulties of trying to disentangle them. To think about the possible selection pressures for a new way of locomotion, it should first be considered what is already known about: 1. Locomotion of our pre-bipedal ancestors 2. Time and possible place where bipedality could have emerged 3. Climate and habitat in the areas where bipedality could have arisen (Ad 1) Two main hypotheses have been proposed earlier on the prevailing locomotion of our pre-bipedal ancestors: brachiation (hylobatid-like) and terrestrial knuckle-walking (chimpanzeelike). The newly discovered fossils of Ar. ramidus throw a new light on the problem of origin of the bipedality in the hominin clade. According to the discoverers of Ar. ramidus, these hominins moved in the trees using palmigrade clambering and walked upright on the ground in woodland habitat, but their terrestrial bipedality was more primitive than that of Australopithecus (Lovejoy 2009). Ar. ramidus skeletons lacked any traits characteristic of knuckle-walking, suspension, or vertical climbing (e.g., the hand exhibited short bones of the palm and lack of the stiff wrist joints) (Lovejoy et al. 2009a). The pelvis of Ardi was useful for climbing and walking (e.g., upper blades were shorter and broader than in extant apes) (Lovejoy et al. 2009c). The foot of these hominins with opposable big toe exhibited the traits useful for upright walking both on the ground and on branches in the trees (Lovejoy et al. 2009b). Ar. ramidus remains indicate, then, that the LCA was probably not chimpanzee-like and that Ar. ramidus inherited arboreal capabilities from the LCA (White et al. 2009). The primitive traits of the Ar. ramidus skeleton provide a new perspective on the derived postcranial characters of Australopithecus. Relative to Ar. ramidus, Au. afarensis exhibited specializations visible in hand, foot, and pelvis, indicating that this hominin abandoned locomotion in the trees probably due to the emergence of new feeding patterns. (Ad 2) There is direct evidence of bipedality from 4.4. Ma in Ar. ramidus and also from 4.2 Ma in Au. anamensis. As far as older hominins are concerned, there is still some disagreement. The foot bones fossils belonging to Ardipithecus kadabba (Haile-Selassie 2001) show mosaic morphology, and the position of the foramen magnum in Sahelanthropus is only indirect and weak evidence for bipedalism. Wolpoff et al. (2002) claim that the position of the foramen magnum excludes an upright position of the head and therefore made bipedality obligate in this form. More certain diagnostic features for habitual bipedal locomotion are found in fragments of three femora of Orrorin (Pickford et al. 2002). If the earliest known hominin forms were really bipedal, this mode of locomotion, and therefore hominins themselves, must have appeared before 6 Ma. From a more conservative point of view, it might have appeared only between 5 and 4 Ma. Fortunately, accepting the first or the second date does not greatly influence our further analysis of the putative selection forces. This is because the habitats in which all ErH were found seem to be quite similar and therefore do not greatly change the inferences about the possible natural selection factors on the emergence of bipedality. (Ad 3) The majority of the hypotheses on the SPfB are in a direct or indirect way related to the habitat in which the ErH lived. Thus, to verify all these hypotheses, we need to reconstruct the climate and habitats in which the ErH lived. On the basis of new data, some suggest that early stages of hominin evolution in Africa were related to open environments – a hypothesis that also predominated in the twentieth century. Since most evidence indicates that all forms older than 4 Ma lived in wooded habitats, currently the “woodland hypothesis” still dominates. Although those few fossil sites with Miocene and Early Pliocene forms for which there is paleoecological evidence provide quite a strong argument for a habitat in which bipedality could have emerged, this is Page 9 of 29

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

nonetheless not unquestionable proof that bipedality and hominins evolved in such a habitat. The other problem is the question of how many times could bipedality have arisen among hominoids? The majority claim that this happened only once, but there are also proponents of more than one emergence of bipedality in hominoids (Rook et al. 1999; Wood and Harrison 2011). If Oreopithecus bambolii was also a biped (as Rook et al. 1999 claim) and if this form had nothing to do with the later hominins, this would mean an independent evolution of bipedality. Having knowledge about these three points allows to narrow down the possible scenarios of selection pressures that could have been the cause of bipedality and most likely the evolution of the hominins.

Putative Selection Primers for Bipedal Locomotion We know much more about the evolutionary stages of morphological adaptation to bipedal locomotion (see ▶ Chap. 5, “The Origins of Bipedal Locomotion”) than about the selection pressures involved in this process. The first difficulty is related to the uniqueness of this adaptation among primates. There is no living nonhuman species that could be used for comparison to allow distinguishing some potential selection factors promoting such a type of locomotion. The second problem lies in the fact that Homo-type bipedality emerged not in a short period of time or as an effect of one sudden event, but rather as a more gradual process (or rather with two evolutionary steps) over a long period of time. As far as postcranial anatomy is concerned, in all pre-Homo ergaster forms of Hominini, there is some combination of human and ape features (Wood and Lonergan 2008; Pickering et al. 2011). This implies some degree of locomotor diversity and that at different stages of the elaboration of bipedal locomotion, different selection factors might have been involved. There are more plausible hypotheses regarding the pressures resulting in the changes related to the last stage of bipedalism that appeared in H. ergaster than regarding those related to the first stage. Furthermore, different selection pressures can be inferred, depending on whether all australopithecines were habitual bipeds or if they were only facultative bipeds. The evolution of bipedalism requires adaptive explanation, not only because it is unique among primates but also because in comparison to quadrupeds this mode of locomotion has certain disadvantages (e.g., reduced speed and agility) and was related to the effective enforcement of some costly but necessary morphological changes. The question “why, then, did bipedalism evolve at all?” is crucial because it is very closely related to the answer to the question of what selection process caused the evolutionary appearance of hominins. Many hypotheses have been advanced to explain the diagnostic and fundamental hominin trait of bipedality. So many concepts have been suggested that they can be divided into a few categories (Rose 1991; Niemitz 2010). Due to the limited space, and the limited plausibility of many of them, we are not going to describe all of them in detail. Some hypotheses violate the presently known temporal sequence of adaptations that appeared in our evolution; some seem to take consequences for causes; some suggest behavioral activity that can be performed as effectively when using, for instance, knuckle-walking locomotion; and still others are based on wrong presumptions about the habitat in which the earliest hominins lived. Furthermore, some hypotheses are very speculative, i.e., with no paleoanthropological evidence to support them, and some are very unlikely, e.g., due to the very weak or only very temporarily acting suggested selective pressure.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

The majority of ideas are related to various behavioral pressures, e.g.: a. b. c. d.

Increasing viewing distance above tall grass (Oakley 1954; Dart and Dennis 1959) Grass seed eating (Jolly 1970) Freeing hands for using tools or weapons (Etkin 1954; Washburn 1967) Load carrying (Preuschoft 2004) – but the same selector is also suggested only for the later Homo body proportions (Wang and Crompton 2004) – or more specifically carrying food (Hewes 1961; Isaac 1978; and in the sexual and reproductive strategy model of Lovejoy 1981) or tools and other valuable objects (e.g. unpredictably available food) Carvalho et al. 2012 e. Hunting or scavenging (Rodman and McHenry 1980) f. Bipedal threat display (Livingstone 1962; Jablonski and Chaplin 1993) or “fighting from a bipedal posture” (Carrier 2011) g. Terrestrial feeding postures when harvesting on small fruits of low, open-forest trees (Hunt 1994) h. Walking and running (Jungers 1988; Bramble and Lieberman 2004) i. Stone throwing (Fifer 1987; Dunsworth et al. 2003) On the base of current knowledge, some of these hypotheses can be excluded (or treated as only of historical interest). This is because bipedality predated the use and manufacturing of stone tools (argument against c) and probably did not evolve in an open environment as was once assumed (a, b), and it predated robust hominin dental complex (b), predated hunting (e) and social structure changes, which could be related to provisioning females with meat food (d). Because of the high energetic cost of load carriage, infant carrying was also unlikely as precursor to bipedal locomotion (Watson et al. 2008). The hunting hypothesis (Brain 1981) can be applied as a selection force only for Late Pliocene hominins. ErH were rather the hunted than the hunters, and this also means that predation pressure on ErH in Late Miocene and in most of the Pliocene could have been quite strong and therefore could have influenced hominin evolution. The main predators of our ancestors were probably the leopard (Panthera pardus), saber-tooth felids, and possibly hyenids. Only very rarely in extant apes are such behaviors as throwing objects manifest (i) or bipedal display (f); thus, these factors are a very unlikely selection pressure to posture habitual bipedalism (against (i) and (f)). Although aggressive behavior can be associated with locomotor bipedalism, it is observed mainly in male chimpanzees in captivity (Thorpe et al. 2002). The other argument against this hypothesis (f) is small dimorphism in the body size of the Ar. ramidus and therefore probably low intermale aggression in the early hominins. The cost of running for the type of bipedality used by ErH was probably higher than the cost of walking; therefore, possible selection for Homo, such as bipedal running, was rather an unlikely pressure for the emergence of bipedality. Biomechanical and energy saving hypotheses are usually proposed for the more humanlike bipedalism in Homo (Preuschoft 2004; Ruxton and Wilkinson 2011a). The analysis of relative thumb length in Au. afarensis (Alba et al. 2003), however, reveals a similar proportion to that in present-day humans. This would mean a high precision grip capability in Australopithecus and would therefore be a strong argument for the hypothesis of the evolutionary causes of bipedality under the selection for manipulative skills in these hominins. Although this would support Darwin’s proposal (c) or others related to freeing the hands (b, d, e, i), one should remember that with these particular hypotheses, there is also the problem of the possible reciprocal causation of causes and consequences. The second group of hypotheses is related to morphological, biomechanical, and/or physiological response to the physical environmental influences. One theory that in the 1980s seemed quite Page 11 of 29

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

probable was the hypothesis of the avoidance of thermal stress (by decreasing body surface exposed to the direct overhead sunlight during midday, which allowed increased daytime foraging) in open environments where there is a strong diurnal insolation. This was first suggested in 1984 and later elaborated by Peter Wheeler. Since this hypothesis is inextricably related to open habitats, it is rather unlikely explanation for the origin of bipedality in ErH (Ruxton and Wilkinson 2011a). It would rather be applicable to the new adaptations that probably appeared only in the genus Homo, e.g., fur loss and elaborate thermoregulation by eccrine glands or endurance running (Ruxton and Wilkinson 2011b). Another hypothesis is the very controversial idea of the aquatic or semiaquatic ape (Hardy 1960; Veerhaegen 1985; Morgan 1997), which states that upright posture appeared as an effect of selection for breathing air and for streamlined body shape in hominins who spent a lot of time in sea water, where they had to dive for food. This hypothesis also explains loss of body hair, brain size increase, and increase of subcutaneous fat tissue and newborn size (and even long hair on the head) as adaptations to the aquatic environment. It is a very speculative hypothesis, without fossil evidence, any similar reference within the primate order, and knowledge about the long time span sequence in the appearance of all these traits in Hominini. There is, however, also a more likely scenario that is related to littoral wading and is called “shore dweller hypothesis” (Niemitz 2010) and “waterside dweller” (Veerhaegen et al. 2007). These hypotheses are based on suggested advantages that could favor wading behavior and investment in high-quality food collection on shorelines. It also assumes that the ancestor of human clade was ecologically nonspecialized. This hypothesis is interesting and seems to be in accordance with the suggestions about omnivorous diet of LCA (Suwa et al. 2009). But whether wading behavior could stimulate our ancestor to stand up and bipedal walking, as suggested by Niemitz (2010), is still debatable. Although the data on seafood reliance by hominins (Braun et al. 2010; Steele 2010) seems to support this scenario, more evidence to connect the origin of bipedality with wading is needed. What seems to be a likelier selection force for bipedality is the hypothesis proposed by Hunt (g). Although in nonhuman primates bipedal posture or locomotion accounts only for less than 5 % of total locomotion, the majority of what is observed is related to food acquisition (Rose 1991). Studies by Stanford (2002) also provide new data on relatively frequent arboreal bipedal posture (arm assisted) by chimpanzees when foraging for small fruits (mainly figs). Although an earlier concept by Washburn (1963) was also based on the chimpanzee model and feeding adaptation in bipedal locomotion, it emphasized terrestrial (and not arboreal) bipedal posture as a preadaptation of ErH that emerged in savanna habitats. The new data on the ErH habitats and on arboreal bipedality by chimpanzees support Hunt’s hypothesis. Limb-length proportions in australopithecines indicate that their bipedality was rather related to the less energetically costly walking than running. This seems to support the view that the primary pressure could have been related to the postural feeding bipedalism and walking between clumped food sources (Rose 1984; Hunt 1994). On the basis of skeletal biology and ontogeny, it is rather unlikely that bipedality would have evolved only as a result of pressure for stationary bipedal posture. Bipedal walking must have been involved (Ward 2003), for instance, as in chimpanzee who use bipedal locomotion for transporting valuable food and objects (Carvalho et al. 2012). The other cue for solving the problem of SPfB is the body size of the ErH. The postcranial remains of Ar. ramidus indicate that these hominins were relatively small (White et al. 2009); thus, it is possible that bipedalism emerged in relatively small forms that were forced to undertake longer terrestrial or arboreal walking (McHenry 1984). If there was selection pressure for bipedal posture among small-bodied hominins in the food acquisition context, then one can postulate that this pressure must have been the strongest for young (smaller) individuals who had even more Page 12 of 29

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

difficulties in reaching the food source when it was above their heads. If they very often had to use upright posture while feeding, and if the food was relatively closely clumped (close to each other), frequent raising up of the whole trunk and the arms and stretching of the legs could have been more energetically costly than moving between these closely distributed fruits on two legs. If food acquisition pressure holds true, the costs for the behavior mentioned above must have been higher than for bipedality. Furthermore, when one arm was needed to hold and bend a branch and the second to collect food, the pressure for bipedal postural behavior and slow bipedal movement would have been even stronger. For small infants and young individuals that were already independent from mother’s milk, reaching highly positioned food could have been possible only with maximal extension of the body and arms. Together with the need to climb trees, such postural feeding would also explain why arms were not shortened and fingers were still curved at this stage of hominin evolution. According to fossil data and the molecular clock and considering how much complex rebuilding was needed to walk bipedally efficiently, we can say that natural selection acted really rapidly on the transformation of the hindlimb in the earliest stages of hominins’ evolution. The evolution of the upper limb, rib cage, or even vertebral column was, however, much slower. What may be then important in determining putative selection pressures on the bipedality is to determine whether early Hominini, apart from their upright posture, were also effective tree climbers. If arboreality was unimportant in early bipedal forms, one can assume that it was biotope change that could have influenced this dramatic change. In the case of retention of arboreal agility and parallel adaptation to both types of locomotion, i.e., until the appearance of Homo, one needs to consider different selection pressures. Australopithecines retained relatively plesiomorphic upper-limb morphology, but what is hotly debated is the adaptiveness of this ErH trait. Although it is still difficult to explain the retention of this primitive apelike character, there are only a few possible explanations for it: stabilizing selection for skilled arboreality, evolutionary inertia, pressure for a new kind of arboreality, change of diet at the time when bipedality appeared, or some specificity of ErH locomotion. The arboreal environments in which the earliest hominins lived indicate that they could have spent quite a lot of time as tree dwellers, which would seem to explain the retention of prehensility and primitive upper-limb morphology (Lovejoy et al. 2009a). The Ar. ramidus postcranium indicates palmigrade clambering in the trees and more primitive terrestrial bipedality than in Australopithecus (White et al. 2009). According to Lovejoy (2009), upright walking probably did not provide energy advantage for Ar. ramidus; thus, these hominins lacked many of the adaptations which appeared in Australopithecus. White et al. also suggest that the further musculoskeletal adaptations (visible in Australopithecus) associated with more advanced terrestrial bipedality might have been the response to carry foods, simple tools, and/or offspring. Using forelimbs for support when feeding could be a possible selection for the upright stature, as Hunt (1994) suggests. Similar to apes, an upwardly directed shoulder joint in Au. afarensis indicates that this form could have frequently directed its arms upwards (Green and Alemseged 2012; Larson 2012). All this might mean that the early hominin morphology, in effect, was a compromise for different locomotor patterns. Living in forested areas is a strong reason to have the possibility of also exploiting arboreal food resources and, therefore, of retaining the capability to climb trees. According to the basic pattern of the genetic mechanism of limb development, there is strong covariance between the morphology of the upper and lower limb. It might then be that it was strong selection for shorter toes that caused the shortening of the fingers in ErH (Hlusko 2004), and shortened fingers should not be treated as an indication of the lack of selection for arboreality in

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

these hominins. Shortened fingers would be then a side effect for bipedalism and an exaptation for tool using and manufacturing. Our grasp of the selection mechanisms that were related to the emergence of bipedality and hominins will increase as more new fossils are recovered both from the Late Miocene and Early Pliocene and with the advances in the understanding of developmental and epigenetic processes (Ward 2002; Larson 2012).

Selection Factors Inferred from the Teeth and Masticatory System of Early Hominins In addition to bipedality, the second important set of traits that seems to be connected with the appearance of the Hominini and that allows us to reconstruct the putative selection pressures that triggered the human–chimpanzee split is found in a number of features of the dentition. Teeth are not only more abundant as fossils than bones are (and especially those bones that directly indicate the mode of locomotion), but they are also easier for inferring the selection pressures which acted directly on them. Current knowledge of the adaptive meaning of relative tooth size and shape, enamel structure and thickness, microwear, and canine size is much better than of bipedality, which is not directly detectable in the earlier-known fossil record. These traits, together with the general robusticity of the masticatory system, are related not only to body size but primarily to diet (Andrews and Martin 1991). Food type and availability, and the locations in which food could have been found, probably constituted strong selection pressures on hominin evolution. The diet of the ErH can be inferred from the teeth of Ar. ramidus, Ar. kadabba, Sahelanthropus, and Orrorin. The morphology of the crown of Ar. ramidus molars was not similar to those characteristic of Pan, Gorilla, and Pongo, and the other traits of these hominins’ dentition (e.g., the incisors that were not as large as in Pan and Pongo) imply a diet different from extant apes (Suwa et al. 2009; White et al. 2009). Ar. ramidus lacked the enlarged rear teeth of Australopithecus that have been interpreted as adaptations to abrasive diet (heavy chewing) in open environments. The co-occurrence of the small canines with small molar crowns in Ar. ramidus can suggest that small canines appeared early in hominin evolution within the context of a nonspecialized diet (White et al. 2009). All hominins living before 3.5 Ma had teeth with thicker enamel than chimpanzees. From the functional point of view, this means that EH were better adapted to eat abrasive food than extant apes. The molars’ enamel of the Ar. ramidus appeared thinner from enamel exhibited by molars of earlier hominins and Australopithecus; thus, in comparison to them, Ar. ramidus diet was less abrasive. It is worth to note that the Miocene African apes, which gave rise to both living African apes and hominins, had relatively thinly enameled teeth (but thicker than in Pan) (Suwa et al. 2009). According to Sayers et al. (2012), the dentitions of the extent Pan and Gorilla are derived from that of their hypothetical LCA – e.g., Dryopithecus and all earliest hominins (including Sahelanthropus, Orrorin, and Ardi). They stressed that molars of the Ar. ramidus showed some important similarities with those of Dryopithecus and Pierolapithecus (Miocene taxa of great apes) including bunodont crowns with low cuspal relief and also greater enamel thickness than in chimpanzees (Suwa et al. 2009); thus, Ar. ramidus is more similar to ours and Pan’s LCA than chimpanzee. The reconstruction of the evolutionary history of enamel thickness in the case of Miocene apes is a very difficult task, because of the uncertainties concerning their phylogeny. Alba et al. (2010) suggest that thin enamel could have independently evolved several times in hominid phylogeny and

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

that thick enamel can be considered as the symplesiomorphy of the great apes and human clades. If they are right, it would mean that LCA had thick teeth enamel. Macro- and microscopic wear patterns in Ar. ramidus molars indicate that these hominins had less abrasive diet and did less masticatory grinding than Au. afarensis (Suwa et al. 2009). Recently, the dental microwear texture analyses of hominin cheek teeth in specimens of Au. anamensis, Au. afarensis, and Paranthropus showed that none of the Australopithecus and P. boisei teeth have surfaces indicating that these hominins were hard-object feeders. Only P. robustus had teeth specialized for a diet based on harder items (Ungar et al. 2008, 2010, 2012). The results of these studies were surprising, because although Au. anamensis and Au. afarensis were from different habitats, their teeth show similar pattern of microwear complexity. The structure (including the thickness of the enamel) and the pattern of wear of the crowns of Ar. ramidus teeth indicate that this hominin’s diet was not specialized and was less abrasive than that of later hominins (Suwa et al. 2009). It is probable that the LCA of human and chimpanzee lineages had the same nonspecialized diet as suggested for Ar. ramidus, i.e., omnivory and frugivory. The results of the isotopic analysis of Ar. ramidus tooth enamel indicate that these hominins consumed mainly C3 plants (~85–90 %) in woodland habitats and small patches of forest. Savanna woodland-dwelling chimpanzees’ intake was more than 90 % C3 plants, and Australopithecus (robust and nonrobust) consumed more than 30 % C4 plants (Suwa et al. 2009; White et al. 2009). Carbon isotope analyses, including those of hominin teeth from 4.4 to about 0.8 Ma, indicate dietary diversity and complexity. Ar. ramidus had C3 diet similar to chimpanzees and Au. africanus, P. robustus, and early Homo consumed more than 50 % C3 plants and also nearly similar quantity of C4 foods (Ungar and Sponheimer 2011). Thus, earlier ideas about the increasing dominance of hard objects in the diet of early hominins have been challenged (Ungar and Sponheimer 2011). The shift from C3-dominated diet to more middling diet (nearly the same proportions of the C3 and C4 food in diet) observed from Ar. ramidus to later hominins suggests the expansion of the Australopithecus into more open habitats. Taking into account the recent discovery at Dikika (Ethiopia) of the stone-tool-inflicted marks on animal bones older than 3.39 Ma, one cannot exclude the possibility that some species of Australopithecus (e.g., Au. afarensis) used stone tools for meat and marrow consumption (McPherron et al. 2010) and that these forms had a more expanded geographical range than the EH. The paleofauna, plant fossils, isotopic composition of soil samples and teeth all indicate that Ar. ramidus lived in woodland with patches of forest (WoldeGabriel et al. 2009). It is supposed that Ar. ramidus relied on a wider range of woodland foods than chimpanzees but did not like Australopithecus rely on open-biotope foods (White et al. 2009). All this seems clear when one look at the available fossils of Australopithecus, but inferring the putative dietary selection pressure acting on the P-H split is somewhat more complicated. Ardipithecus had still relatively thin enamel (White et al. 2009) and was forest dwelling, and these lines of evidence are against the prime-mover strong selection for a dietary change that might have triggered a P-H split. If, however, either Sahelanthropus or Orrorin was the first hominin, and both had relatively small canines and thicker enamel than Ardipithecus, then the possibility that the selection for a dietary shift was one of the causes for hominin emergence cannot be excluded. In that case, dental features would show the influence of dietary selection pressures from the very point of origin of the hominins. According to the present knowledge of the dental features of ErH and the suggested hypotheses of selection pressure for upright posture, the most likely scenario for the selection pressure that triggered the P-H split would be adaptation to more variable food, including some clumped and small fruits that were easier for ErH to reach via an upright body position in the trees (Hunt 1994) or possibly from the ground. This scenario can also be inferred on the basis of the relatively small Page 15 of 29

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

incisors in ErH (Suwa et al. 2009). This is because primates eating smaller fruits ingest them without extensive incisor preparation (Ungar 1994). Relatively longer thumbs in australopithecines (Alba et al. 2003) would support this hypothesis. However, unless more certain fossils of the ErH are found, to fully answer the question of whether selection for new diet was intimately connected with the P-H separation will not be possible.

Inferences About Behavior and Social Structure of the Early Hominins Fossil evidence provides scientists with information about the skeletal or dental morphological features that appeared in the early hominins. A much more difficult task is inferring behavior (including species-specific social or mating structures) from these very scarce fossils. This is much easier for later forms of hominins (e.g., Homo) for which there are more fossils and such archaeological records as stone tools or animal bones with cutmarks. In general, paleoanthropologists have almost the same idea about the behavior of the earliest hominins as about the behavior of the LCA. Nonetheless, they try to use all possible hints to reconstruct the behavior and social structure of the ErH. With no direct evidence of early hominin social structure and behavior, one can only propose some models that are not in disagreement with the fossils. Apart from features of locomotion and diet that probably modified ErH behavior in relation to the ancestor, other aspects of behavior and social structure do not seem to be very different. What can be inferred about behavior or the mating system of the ErH is based mainly on overall body size, sexual dimorphism in body size, and sexual dimorphism of the canines. Since fossils of the earliest hominins are so scarce, one can only infer their behavior on the basis of some features of new remains of Ar. ramidus and later Au. afarensis. Recently it was shown that Ar. ramidus exhibited less dimorphic skeletal body size than Australopithecus (White et al. 2009). This, similar to Pan, sexual dimorphism in size (SDS) in Ar. ramidus suggests a male-bonded social system. According to Sayers et al. (2012), the morphological traits of the Ardi skeleton indicate that the LCA was anatomically and behaviorally different from chimpanzees. In contrast, McGrew (2010) asserts that based on the current knowledge on chimpanzee behavior, one should infer the trait of our LCA. Below are putative selection pressures and behavioral consequences of body size and sexual dimorphism of the ErH.

Were There Any Selection Pressures on Body Size of Early Hominins? Body size is very informative about animal socioecology, life history (see Zimmermann and Radespiel, Vol. 2, “▶ Primate Life Histories”), and possible selection pressures that can act on differently sized animals. For example, smaller forms have more predators, smaller ranges, and less protection against hypothermia. The advantages of having a bigger body size are manifold: a lower predation risk, better control over the environment, higher mobility, bigger brain, longer infancy, and therefore longer time for learning and a longer lifespan. Disadvantageous consequences, however, are also present: longer gestation and infancy means longer maternal dependence, and more food and a bigger foraging area (home range size) are needed (Clutton-Brock and Harvey 1980). Without knowing the size of the LCA, it is difficult to speculate about any selection pressure for body-size change in the ErH. If they lived in a forested environment as their ancestors did, then it is rather unlikely that there was any pressure for changing body size that was independent from the pressure

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

for greater bipedal biomechanical efficiency. What it is known for sure is that a change in size did take place in the Late Pliocene, when Homo emerged. Until the relatively recent discovery of Ardi, early hominin body size and sexual size dimorphism were inferred from Au. afarensis, and the main reference fossil specimen was “Lucy” (AL-288), which had preserved ca. 40 % of the skeleton. Now these inferences can be made on the basis of most complete skeleton of the earlier and relatively small Ardi. Only minimal dimorphism in size probably characterized Ardi and indicates that the common ancestor of human and chimpanzee presumably also exhibited the same trait. If this assumption is proper, the specific selection pressures that could have acted on body size and sexual dimorphism at this stage of hominin evolution cannot be suggested.

Sexual Dimorphism and Social Structure Sexually dimorphic traits specific to hominins should also have been selected for in response to certain selection pressures. Analysis of SDS, and its changes in the hominin lineage, might then give some insight into the mating system and social structure of these forms. It is known from living primates that SDS reflects male–male competition for monopolizing the reproductive potential of females. Higher SDS is usually related to more intense male intrasexual aggression. Male body size is an investment in fighting abilities, and this investment is inversely related to the mating opportunities (Trivers 1972). Species living in a one-male group (e.g., gorilla) have the largest SDS, monogamous species (like gibbons) are monomorphic, and species living in multi-male groups (like chimpanzee) have moderate SDS. The difficulty with reconstructing the mating system in the earliest hominins is related to the lack of sufficient fossil data for the size of both sexes. Fragmentary fossils mean that sex assignment is made frequently only on the basis of size (and not on pelvic or cranial morphology). This may lead to overestimation of SDS. The problem with inferring social structure, however, becomes complicated when one also takes into consideration dimorphism in canine size (CD). This feature can also be useful for reconstructing mating systems, as CD is often positively related to SDS and therefore might also indicate a higher level of intra-male competition. If SDS and CD were both large in ErH, behavioral inferences would be relatively consistent, indicating a polygynous reproductive system in these forms. The problem appears when, contrary to SDS which suggests a high intensity of competition, CD in hypothetical ErH is small and therefore contradicts a high male–male competition for females. To solve this problem, Plavcan and van Schaik (1992) distinguished four types of male–male competition that are connected with different SDS. In order of increasing SDS: (1) low frequency and low intensity (as in monogamous gibbons), (2) high frequency and low intensity (as in chimpanzees), (3) low frequency and high intensity (as in Saimiri), and (4) high frequency and high intensity (as in Macaca mulatta, Papio hamadryas). These authors claim that the SDS of ErH hominins fits well with type 2 here. The best present model for SDS and CD and therefore social structure in the earliest hominins is Ar. ramidus. The lack of a projecting, daggerlike upper canine crown and absence of an apelike honing C/P3 complex (characteristic for chimpanzees), together with reduced canine size in Ardipithecus males, indicates a lower intensity of male–male aggression in this species than in extant chimpanzees. Although the canines of the earliest known hominins at about 6 Ma were slightly more primitive, they were similar in size to those of Ar. ramidus (Suwa et al. 2009). This indicates that male canine size was reduced by 6–4.4. Ma from an ancestral apelike condition which probably exhibited a honing C/P3 complex and a moderate chimpanzee-like difference in size between male and female canines (Suwa et al. 2009). Among other features, the big size of the upper Page 17 of 29

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

canines is important in territorial defense and in male agonistic behavior. The “feminized” shape of the male canines in Ar. ramidus and in other early hominins has been interpreted as the result of sexual selection and an occurrence of the reproductive and social behavioral changes in hominin evolution long before brain enlargement and stone tool use (Suwa et al. 2009). The dental traits and small SDS of Ar. ramidus justify ascribing to LCA minimal skull and body size dimorphism and moderate canine dimorphism, indicating male philopatry, weak competition between males, and probable male–female codominance (as in the case of P. paniscus and ateline species) (Suwa et al. 2009). The intense intermale aggression characteristics of Pan troglodytes or social structure of gorillas are then rather unlikely social models for the LCA (Lovejoy 2009; Suwa et al. 2009; White et al. 2009). High variation in body size in Australopithecus within a single site indicates high SDS and strongly undermines the hypothesis of a monogamous mating system in these forms (e.g., as suggested by Lovejoy 1981) and its possible influences on the evolution of bipedality. Gordon et al. (2008) also demonstrated that Au. afarensis showed substantial level of sexual dimorphism (most consistent with that present in gorillas and orangutans), which is in contrast with human or chimpanzee-like level of SDS in this species, as earlier suggested by some authors (e.g., Reno et al. 2005). SDS in Australopithecus was also larger than in Ar. ramidus (White et al. 2009). If the driving force behind SDS in anthropoids is sexual selection (Lindenfors and Tullberg 1998), it can be inferred on this basis that the social structure in the earliest australopithecines was not monogamous. Although smaller canines in male in these forms might indicate a lower selection pressure for fighting ability, they lived probably in multimale/multifemale groups. A new skeleton of a large-bodied Au. afarensis male (dated to 3.38 Ma) discovered in Ethiopia indicates sophisticated terrestrial bipedality (Haile-Selassie et al. 2010). It is then possible that the reduction of body size in Australopithecus females was the result of enhancing their cooperation, but male size could have increased in response to predation pressure, which became higher in more open habitats invaded by these hominins (White et al. 2009). All presented evidence and inferences about social structure face also the problem of great variation in SDS or CD within one competition type. There are a number of polygynous species with a very slight degree of dimorphism both in body and canine tooth size (Plavcan 2000). Thus, inferring social behavior from sexual dimorphism in primates has proved to be ambiguous, and this means that all speculations on the ErH social structure based on SDS or CD should be treated with caution. It cannot be also excluded that the mixture of high SDS and low CD was a consequence of male predator defense and not strong male–male competition. The primate species with higher frequency of conciliatory behavior (e.g., Tonkean macaques or bonobos in comparison to chimpanzees) have lower CD (Plavcan and van Schaik 1992). There is also a possibility that the lack of concurrence of marked SDS and CD implies a unique social system that is unknown among living primates. One possible explanation of the canine reduction observed in ErH (Ar. ramidus and Australopithecus) is the relaxation of the selection pressure favoring canine use as a weapon in an intrasexual and/or antipredatory context. Furthermore, the selective forces responsible for canine reduction probably had nothing to do with their dietary function. The later possibility of using them as functionally equivalent to incisors could have been a by-product of canine reduction selected for other reasons (Plavcan and Kelley 1996). In the opinion of Leutenegger and Shell (1987), however, the lack of CD in australopithecines could have produced the effect of “dental crowding,” which resulted from the selection for the increase of premolar and molar chewing surface area, and SDS was a result of relatively high intrasexual male competition. Unfortunately, past behaviors do not fossilize, and therefore, one cannot be certain about the mating system within the early Hominini. Page 18 of 29

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Small-bodied hominins disappear from the fossil record ca. 1.7 Ma (McHenry 1994). This suggests that there was strong selection pressure for both female and male body size to increase. However, this increase was much larger for females (McHenry 1994). Thus, it is unlikely that it was sexual selection, for example, for monogamy, that caused the decrease in SDS. If the decrease of SDS had been related to selection for monogamy, one would have expected a reduction in male–male competition and thus male body-size decrease (Lindenfors and Tullberg 1998) rather than a large increase in female body size. It is more likely, therefore, that selection pressures could have been related to locomotion efficiency (longer legs enabled walking for longer distances, which was adaptive for both sexes) or to an antipredatory strategy, thermoregulatory demands (Ruff 1991; Wheeler 1992), or to giving birth to bigger and fatter newborns (Pawlowski 1998) with larger brains.

Future Perspectives for Determining the First Appearance of Derived Hominin Traits and the Selection Pressures Acting on Them There is no doubt that the closer integration of paleoanthropology and genetics will in the future markedly advance our knowledge of the mechanism of hominin evolution. It is worth to note that the phenotypic traits described as unique to human lineage are commonly considered as the results of the selective pressures acting on human genome and the unique demographic history since the time of the divergence of the human and chimpanzee lineages (O’Bleness et al. 2012). Currently the rapid comparison of the numerous genomes within and between species is possible, and there are data on the draft genomes of several primate species including chimpanzees (Pan troglodytes), bonobo (Pan paniscus) (Pr€ ufer et al. 2012), gorillas (Scally et al. 2012), and orangutans (Locke et al. 2011). It was, for instance, determined that 25 % of human genes contain parts that appeared closely related only to one of the two Pan species (bonobo or chimpanzee). The examination of these regions can help to determine the genetic background of the phenotypic similarities between humans and Pan and to assess the time of their evolutionary appearance. There is also the genetic evidence that LCA of human and Pan lineages possessed a mosaic of the traits specific to human, chimpanzee, and bonobo (Pr€ufer et al. 2012). We are now in the “golden age” of exploration of the genetic changes and between-species differences that might contribute to the search for the emergence of the specific traits for human lineage. On the basis of the sequence changes that occurred at the rate greater than the rate of the neutral mutations, we are able to identify hypothetical evolutionary pressures. There are, however, still many challenges we face with (O’Bleness et al. 2012). Most problematic is difficulty in linking human-specific genomic change to human phenotype features. This is because to understand the genomic changes, one has mainly to rely on the observation of the variation and diseases that occur in modern humans (O’Bleness et al. 2012), although recently applied heterologous expression of human regulatory regions in mice allows detecting functions of genetic changes specific to human lineage (Prabhakar et al. 2008; McLean et al. 2011). An interesting example of using this method is the study of human accelerated noncoding region 1 (HACNS1) enhancer. This noncoding region is expressed in the anterior developing limbs of the mouse embryo, which could mean that HACNS1 might have contributed to the emergence of human bipedalism (Prabhakar et al. 2008; O’Bleness et al. 2012). It can be supposed that identification of the genes or genomic regions more directly responsible for the traits that emerged in our lineage than those suggested now will be in the future easier and much more helpful for reconstructing the fine details of our evolutionary past. Finding the time of the appearance of different gene changes will allow to put a date to the emergence of given traits and to Page 19 of 29

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

identify the particular selection pressures that were responsible for the appearance of different traits in hominin evolution. A good example of this issue is the assessment of the appearance time of the FOXP2 gene in human evolution. FOXP2 has been described as helping in learning the complex muscle movements important to speech and language in human (Enard et al. 2009), and it was suggested that the human version of this gene appeared about 500,000 years ago (Krause et al. 2007). What is abundantly clear at the beginning of the twenty-first century is that in combination with these genetic approaches, our grasp of the mechanisms of hominin evolution will radically improve through the discovery and interpretation of hominin fossils uncovered in strata of Late Miocene and Early Pliocene ages.

Conclusion The main focus of this chapter was the consideration of the main adaptive traits that appeared in the early hominins, paying particular attention to the putative selection pressures that could have triggered the hominin–chimpanzee split and then acted on the early hominins prior to the appearance

Fig. 1 The main types of data helpful in inferring the putative selection pressures acting on the early hominins. LCA last common ancestor, ErH the earliest hominins Page 20 of 29

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

of genus Homo. This task, however, is not easy. Although there is some general idea about the chronological sequence of the appearance in hominins of new (derived) morphological traits, the typically very fragmentary nature of the pre-hominin and early hominins’ fossil record limits our ability to fully account for both the selection pressures acting on derived morphological traits and even more so for behavior of the earliest hominins (Fig. 1). It is obvious that the availability of only hard-tissue fossils restricts our possible understanding of the whole biology of these extinct forms. But paleoanthropologists can also have problems with determining the evolutionary mechanisms that were responsible for the appearance of main morphological hominins’ features. There is not even a clear pattern of the main changes in the earliest stages of hominins’ evolution. The most certain trait, diagnostic for this clade, is bipedal locomotion, and this is certainly the trait for which a clear evolutionary explanation is really needed. Since it is the defining hominin trait, it is almost certain that explaining selection pressures for bipedality is concomitant with explaining the causes of the hominin–chimpanzee divergence. But unless the chronological order of the ErH is determined, the reconstruction of the main selection forces that led to the hominin–chimpanzee split will remain unclear. The reconstruction of selection pressures responsible for hominin emergence would be easier if paleoanthropologists were dealing with a complex of traits that appeared at the same time than if the derived traits appeared at different times and were independent of each other. In the latter case we would need to analyze each trait separately, and there are possibly more selective pressures to be taken into consideration. When a few traits appear at the same time, it is usually much easier to propose a selective factor (the pool of such factors would be restricted) for a complex set of dependent traits. For instance, if the ErH became bipedal and at the same time acquired new masticatory adaptations to feed on abrasive food, then the habitat change hypothesis for bipedalism would be more likely as a putative selection pressure for hominin appearance. If Orrorin and Sahelanthropus were the earliest hominins, it could be inferred that bipedality could have arisen concomitantly with a dietary shift towards more variable diet, including more abrasive foods. Since they lived in a mosaic environment, and Sahelanthropus lived far from East Africa, one cannot exclude the possibility that the cradle of the hominins was much farther to the north that was originally thought and that it was in a more open environment in which bipedality and thus the hominins first emerged. The knowledge of the sequence in which the different traits emerged is, however, not enough to exclude one selection factor for different traits. This is because the appearance of new traits can be related to a different speed of evolutionary response for the same selection pressure or can be related to different strength of the same pressure at different times. It seems unlikely that such a fundamental hominin trait as bipedality emerged a number of times independently. Other traits, such as size and body proportions, or bone and enamel thickness, seem to respond much faster to environmental selection pressure, so in our family tree, these traits might have changed in a different way in a few evolutionary lines. This notion is important because it is usually presumed that the evolutionary processes are parsimonious, which means that traits are difficult to change and evolve, and therefore, it is unlikely that one trait evolved independently in different lineages. However, such an easily evolvable trait as enamel thickening appeared under similar selection pressures, probably independently in the evolutionary lineages of at least a few Miocene hominoids. When speculating about putative selection pressures, one should also remember to distinguish causes from consequences. It is easily possible to construct scenarios which confuse them. The problem is that in many cases, they are then difficult to disentangle. The earliest stage of hominin evolution seems to be the biggest mystery and challenge of our entire evolutionary clade, and therefore, it should be no surprise that the theories of the selection Page 21 of 29

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

pressures presented here are in part inherently speculative and highly vulnerable to adjustment in the light of new evidence. There is no doubt we need more ErH remains to find out whether some ErH skeleton traits were homoplasies or symplesiomorphies. This would allow to acquire much better knowledge about the traits of LCA (Wood and Harrison 2011). We can only hope that some fresh evidence will be gained soon and that it will allow to exclude some of the more unlikely selection pressure scenarios, thereby both narrowing the debate and at the same time making it more substantial.

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McHenry HM (1984) The common ancestor. A study of the postcranium of Pan paniscus, Australopithecus and other hominoids. In: Susman RL (ed) The pygmy chimpanzee. Evolutionary biology and behavior. Plenum Press, New York, pp 201–224 McHenry HM (1994) Behavioural ecological implications of early hominid body size. J Hum Evol 27:77–87 McLean CY, Reno PL, Pollen AA, Bassan AJ, Capellini TD, Guenther C, Indjeian VB, Lim X, Menke DB, Schaar BT, Wenger AM, Bejerano G, Kingsley DM (2011) Human-specific loss of regulatory DNA and the evolution of human-specific traits. Nature 471:216–219 McPherron SP, Alemseged Z, Marean CW, Wynn JG, Reed D, Geraads D, Béarat HA (2010) Evidence for stone-tool-assisted consumption of animal tissues before 3.39 million years ago at Dikika, Ethiopia. Nature 466:857–860 Morgan E (1997) The aquatic Ape hypothesis. Souvenir Press, London Navarro A, Barton NH (2003) Chromosomal speciation and molecular divergence – accelerated evolution in rearranged chromosomes. Science 300:321–324 Niemitz C (2010) The evolution of the upright posture and gait – a review and a new synthesis. Naturwissenschaften 97:241–263 O’Bleness M, Searles VB, Varki A, Gagneux P, Sikela JM (2012) Evolution of genetic and genomic features unique to the human lineage. Nature 13:853–866 Oakley KP (1954) Skill as a human possession, chapter I. In: Singer C et al (eds) A history of technology, vol 1. Oxford Univ Press, New York/London Patterson N, Richter DJ, Gnerre S, Lander ES, Reich D (2006) Genetic evidence for complex speciation of humans and chimpanzees. Nature 441:1103–1108 Pawlowski B (1998) Why are human newborns so big and fat? Hum Evol 13:65–72 Pickering R, Dirks PHGM, Jinnah Z, de Ruiter DJ, Churchill SE, Herries AIR, Woodhead JD, Hellstrom JC, Berger R (2011) Australopithecus sediba at 1.977 Ma and implications for the origins of the genus Homo. Science 333:1421–1423 Pickford M, Senut B (2001) The geological and faunal context of Late Miocene hominid remains from Lukeino, Kenya. CR Acad Sci Paris 332:145–152 Pickford M, Senut B, Gommery D, Treil J (2002) Bipedalism in Orrorin tugenensis revealed by its femora. CR Palevol 1:191–203 Plavcan JM (2000) Inferring social behavior from sexual dimorphism in the fossil record. J Hum Evol 39:327–344 Plavcan JM, Kelley J (1996) Evaluating the “dual selection” hypothesis of canine reduction. Am J Phys Anthropol 99:379–387 Plavcan JM, van Schaik CP (1992) Intrasexual competition and canine dimorphism in anthropoid primates. Am J Phys Anthropol 87:461–477 Potts R (1998) Environmental hypotheses of hominin evolution. Yearb Phys Anthropol 41:93–136 Potts R (2012) Evolution and environmental change in early human prehistory. Annu Rev Anthropol 41:151–167 Prabhakar S, Visel A, Akiyama JA, Keith MS, Lewis D, Holt A, Plajzer-Frick I, Morrison H, FitzPatrick DR, Afzal V, Pennacchio LA, Rubin EM, Noonan JP (2008) Human-specific gain of function in a developmental enhancer. Science 321:1346–1350 Preuschoft H (2004) Mechanisms for the acquisition of habitual bipedality: are there biomechanical reasons for the acquisition of upright bipedal posture? J Anat 204:363–384 Pr€ ufer K, Munch K, Hellmann I, Akagi K, Miller JR, Walenz B, Koren S, Sutton G, Kodira C, Winer R, Knight JR, Mullikin JC, Meader SJ, Ponting CP, Lunter G, Higashino S, Hobalth A, Dutheil J, Karakoc E, Alkan C, Sajjadian S, Catacchio CR, Ventura M, Marques-Bonet T, Eichler Page 25 of 29

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Thorpe SKS, Crompton RH, Chamberlain A (2002) Bipedal behaviour in captive chimpanzees (Pan troglodytes). In: Harcourt CS, Sherwood BR (eds) New perspectives in primate evolution and behaviour. Westbury Academic and Scientific Publishing, Otley, pp 231–248 Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and descent of man 1871–1971. Heinemann, London, pp 136–179 Ungar PS (1994) Patterns of ingestive behavior and anterior tooth use differences in sympatric anthropoid primates. Am J Phys Anthropol 95:197–219 Ungar PS, Sponheimer M (2011) The diets of early hominins. Science 334:190–193 Ungar PS, Grine FE, Teaford MF (2008) Dental microwear and diet of the Plio-Pleistocene hominin Paranthropus boisei. PloS ONE 3:e2044 Ungar PS, Scott RS, Grine FE, Teaford MF (2010) Molar microwear textures and the diets of Australopithecus anamensis and Australopithecus afarensis. Philos Trans R Soc Lond B 365:3345 Ungar PS, Krueger KL, Blumenschine RJ, Njau J, Scott RS (2012) Dental microwear texture analysis of hominins recovered by the Oldovai Landscape Paleoanthropology Project, 1995–2007. J Hum Evol 63:429–437 Veerhaegen M (1985) The aquatic ape theory: evidence and a possible scenario. Med Hypotheses 16:17–21 Veerhaegen M, Munro S, Vannechoutte M, Bender-Oser N, Bender R (2007) The original econiche of the genus Homo: open plain or waterside? In: Munoz S (ed) Ecology research progress. Nova, New York, pp 155–186 Vignaud P, Duringer P, Mackaye HT, Likius A, Blondel C, Boisserie JR, de Bonis L, Eisenmann V, Etienne ME, Geraads D, Guy F, Lehmann T, Lihoreau F, Lopez-Martinez N, Mourer-Chauvire C, Otero O, Rage JC, Schuster M, Viriot L, Zazzo A, Brunet M (2002) Geology and palaeontology of the Upper Miocene Toros-Menalla hominid locality, Chad. Nature 418:152–155 Vrba ES, Denton GH, Prentice ML (1989) Climatic influences on early hominid behavior. Ossa 14:127–156 Wakeley J (2008) Complex speciation of humans and chimpanzees (2008). Nature 452:E3–E4 Wang WJ, Crompton RH (2004) The role of load-carrying in the evolution of modern body proportions. J Anat 204:417–430 Ward CV (2002) Interpreting the posture and locomotion of Australopithecus afarensis: where do we stand. Yearb Phys Anthropol 45:185–215 Ward CV (2003) The evolution of human origins. Am Anthropol 105:77–88 Washburn SL (1963) Behavior and human evolution. In: Washburn SL (ed) Classification and human evolution. Aldine, Chicago, pp 190–203 Washburn SL (1967) Behavior and the origin of man. Proc Roy Anthropol Inst 3:21–27 Watson JC, Payne RC, Chamberlain AT, Jones RK, Sellers WI (2008) The energetic costs of loadcarrying and the evolution of bipedalism. J Hum Evol 54:675–683 Wheeler PE (1992) The thermoregulatory advantages of larger body size for hominids foraging in savannah environments. J Hum Evol 23:351–362 White TD, WoldeGabriel G, Asfaw B, Ambrose S, Beyene Y, Bernor RL, Boisserie JR, Currie B, Gilbert H, Haile-Selassie Y, Hart WK, Hlusko LJ, Howell FC, Kono RT, Lehmann T, Louchart A, Lovejoy CO, Renne PR, Saegusa H, Vrba ES, Wesselman H, Suwa G (2006) Asa Issie, Aramis and the origin of Australopithecus. Nature 440:883–889 White TD, Asfaw B, Beyene Y, Haile-Selassie Y, Lovejoy CO, Suwa G, WaldeGabriel G (2009) Ardipithecus ramidus and the paleobiology of early hominids. Science 326:75–86

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Wilson AC, Sarich VM (1969) A molecular time scale for human evolution. Proc Natl Acad Sci 63:1088–1093 WoldeGabriel G, Ambrose SH, Barboni D, Bonnefille R, Bremond L, Currie B, DeGusta D, Hart WK, Murray AM, Renne PR, Jolly-Saad MC, Stewart KM, White TD (2009) The geological, isotopic, botanical, invertebrate, and lower vertebrate surroundings of Ardipithecus ramidus. Science 326:65e1–65e5 Wolpoff MH, Senut B, Pickford M, Hawks J (2002) Palaeoanthropology – Sahelanthropus or ‘Sahelpithecus’? Nature 419:581–582 Wood BA, Harrison T (2011) The evolutionary context of the first hominins. Nature 470:347–352 Wood B, Lonergan W (2008) The hominin fossil record: taxa, grades and clades. J Anat 212:354–376

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_46-6 # Springer-Verlag Berlin Heidelberg 2013

Index Terms: Bipedalism 8 Body size 16 Canine size 17 Dental features 14 Early hominines 1 Forest hypothesis 7 Hominin-chimpanzee split 20 Last common ancestor (LCA) 5 Masticatory system 14 Natural selection 1 Panini-hominini (P-H) split 2 Putative selection pressures 1 Savanna hypothesis 6 Sexual dimorphism 17 Shore dweller hypothesis 12 Variability selection hypothesis 8

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

Paleoenvironments and Hominin Evolution Elisabeth S. Vrba* Department of Geology and Geophysics, Yale University, New Haven, CT, USA

Abstract Environmental stimuli have influenced the evolution of hominins and other mammals at the levels of ontogeny, organismal adaptation, and speciation. The review refers to some agreement which has emerged – as well as to persistent debates – on the issue of environmental linkages to hominin adaptation. Current hypotheses which link physical change, adaptation, and speciation in general and in hominins in particular are discussed (including hypotheses on the role of ecological specialization and generalization, the coordinated stasis and variability selection hypotheses, habitat theory, and the turnover pulse hypothesis). Some persistent debates are revisited (such as on the current status of the savanna hypothesis and on whether or not there was mammalian species’ turnover in the Turkana Basin during the Plio-Pleistocene). The relation of hominin evolution to the recent finding of several turnover pulses coincident with global cooling trends in the 10 Ma to recent record of all African larger mammals is considered. One example of hypotheses which address issues of environmental stimuli of ontogenetic evolution is the heterochrony pulse hypothesis: the generative properties shared among lineages can result not only in coherence of morphological changes but also in a strongly nonrandom timing of heterochrony events, as diverse lineages respond in parallel by similar kinds of heterochrony to the same environmental changes. The discussion includes cases in hominins and other mammals of evolutionary increase in body size by prolongation of growth and attendant “shuffling” of body proportions including relative increase in brain volume, namely, encephalization.

Introduction It is a truism that environmental stimuli have influenced the evolution of hominins and all other life forms. The challenge is to understand the causal subcategories: what are the hypotheses and predictions that should be tested and what kinds of data can be used to best effect. This approach is based on three premises: (1) one needs to study not only the hominins but also their wider biotic and environmental contexts. (2) Given the aim of understanding hominin evolution, the theory of evolution should be accorded more prominence than has been the norm, and an expanded theoretical framework is needed. A focus on the dynamics that link the environment to selection and adaptation at the organismal level is insufficient. One also needs to consider the causal linkages from the environment to dynamics at lower and higher levels – from morphogenesis during organismal ontogeny to the macroevolutionary level of species turnover (speciation and

*Email: [email protected] Page 1 of 45

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

extinction) – and investigate the separate and combined roles in the origins of new phenotypes and species. (3) The direct influence of physical environmental stimuli on evolution at each level deserves more intensive study than it has been accorded traditionally. For much of the century following Darwin (1859), the research disciplines of geology (including climatology) and paleobiology were conducted separately. Speculations abounded on how they might link, but analyses directly integrating data from both areas remained sparse. This changed over the past decades as more refined methods led to discovery of new patterns and causal principles in paleoclimatology (e.g., the astronomical climatic cycles, Hays et al. 1976) and in the fossil record (e.g., rigorous phylogenetic hypotheses, geochemical inference of past diet, etc.). Proposals that hominins, the beginning of bipedalism, and other important human adaptations occurred in the African savanna, in response to the new selection pressures in such more open environments, are often loosely grouped under the term “savanna hypothesis.” The first such proposal is often attributed to Dart (1925) who wrote (pp 198–199), for example, that in the ancestral forest, Nature was supplying with profligate and lavish hand an easy and sluggish solution....For the production of man a different apprenticeship was needed to sharpen the wits and quicken the higher manifestations of intellect – a more open veldt country where competition was keener between swiftness and stealth, and where adroitness of thinking and movement played a preponderant role in the preservation of the species.

Later notable examples include the dietary hypotheses of Robinson (1963) and Jolly (1970). In his insightful review, Potts (1998b:107) considered that “Washburn’s [1960 and other publications] influence and interest in intrinsic accounts (as opposed to extrinsic accounts, which interpreted evolutionary events in relation to environmental change) may explain why many paleoanthropologists in the 1950s–1970s paid little attention to environmental context.” Early papers proposing physical change as a direct cause of hominin evolution concerned particular stratigraphic sequences in East and southern Africa (respectively, Coppens 1975; Vrba 1974, 1975; both compared climatic indications from mammalian change with the hominin record), the circumMediterranean area (Hsu et al. 1977 implicated the Messinian Salinity Crisis in hominin origin), and comparison of global climatic data with the hominin record (Brain 1981a). Darwin (1859) argued that the initiating causes of phenotypic change and speciation are located at the level of organisms, namely, natural selection, particularly arising from competition: “.... each new species is produced . . . by having some advantage over those with which it comes into competition . . .” (p. 320). He stressed climatic effects on competition rather than on population structure: “in so far as climate chiefly acts in reducing food, it brings on the most severe struggle between the individuals....” (p. 68). Darwin thought that an understanding of organismal selection and adaptation will also answer the question of species’ origins. Most later evolutionary studies, including those in paleoanthropology, have continued in this tradition. (See Tattersall 1997a who argued that “paleoanthropology fell completely under the sway of the evolutionary views of the [neoDarwinian] Synthesis – where it remains, for the most part, today.”) The questions which will be addressed, using theory and evidence, include how physical dynamics have influenced species’ structure and speciation, organismal ontogenetic systems, and selection and adaptation. I also consider some of the interactions among these levels. Hominini means the evolutionary group of species which are considered by most to be more closely related to humans than to chimpanzees. The term “species” is used for a sexually reproducing lineage, the members of which share a common fertilization system, and “speciation” for the divergence of the fertilization system in a daughter population to reproductive isolation from the parent species (Paterson 1982), with awareness of the difficulties involved in applying such concepts to the fossil record (Kimbel 1991; Vrba 1995a). The terms “habitat,” “specific

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

habitat,” and “habitat specificity” of an organism or species refer to the set of resources that are necessary for life; resources are any components of the environment that can be used by an organism in its metabolism and activities, including ranges of temperature, relative humidity and water availability, substrate characteristics, places for living and sheltering, and all kinds of organic foods such as plants and prey, mates, and other mutualist organisms in the same or different species (Vrba 1992). An organism’s biotic environment derives from other organisms and biotic interactions such as competition, parasitism, predation, and mutualism. “Physical change” refers to the global and local effects from extraterrestrial sources, including the astronomical climatic cycles, and from dynamics in the earth’s crust and deeper layers as manifested by topographic changes such as rifting, uplift, sea level change, and volcanism. The use of the term “savanna” follows Ratnam et al. (2011) and Cerling et al. (2011:53): “a modern ecological definition of the term savannah is comprehensive and includes structural, functional and evolutionary aspects, Ratnam et al. 2011. Because our focus is on reconstructing the physiognomic structure of palaeo-vegetation, we use a purely structural definition of savannah [quoting Ratnam et al. 2011]: “mixed treegrass systems characterized by a discontinuous tree canopy in a conspicuous grass layer.””

Physical Change, Adaptation, and Speciation: Some Current Hypotheses The traditional hypothesis follows Darwin closely and has often been called neoDarwinian. In its most conservative form, it assumes that adaptation and speciation are always driven by natural selection. The particular causes of selection are seen as very diverse, the most important being organismal interactions – such as competition and predation – that can act alone, or in combination with physical change, to initiate and complete speciation (and extinction). Under this null hypothesis, H0, selection pressures that cause speciation, differs from group to group and from one local area to the next. To explore how this model’s predictions differ from others, let us ask: what rhythm of speciation events would one expect if we could see all the events in the real world across the entire area under study (e.g., Africa) and if we plotted their frequencies against time? H0 predicts that the pattern of origination frequencies for large areas, over long time, is a random walk in time with an averagely constant probability of origination. Examples of such arguments are found in Van Valen (1973), Hoffman (1989), McKee (1993), and Foley (1994). In contrast, a number of hypotheses share the argument that physical change has an important causal role in initiating the evolution of novel adaptations and species turnover, with the consequent prediction that such evolutionary events should be nonrandomly distributed in time and in association with episodes of physical change. Several such hypotheses will be discussed after introducing some relevant theory.

Allopatric Speciation Allopatric speciation occurs in isolated populations that have been separated by vicariance or dispersal over barriers. (Vicariance is the fragmentation of a formerly continuous species’ distribution into separated populations.) Gulick (1872), who studied the Hawaiian fauna, was the first to argue that the causes of speciation are not well explained by selection among competitors, but that vicariance brought about by physical changes was seminal in initiating speciation. Mayr’s (1942, 1963) comprehensive arguments for allopatric speciation eventually resulted in widespread agreement that this mode predominates. Although there continue to appear claims of sympatric speciation, mainly in herbivorous insects and fishes, most recent such reports acknowledge that the best evidence remains circumstantial (review in Vrba 2005). It is fair to say that an expectation of predominant allopatric speciation, particularly in hominins and other large mammals, is consistent Page 3 of 45

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

with the weight of available evidence and enjoys widespread consensus. In terms of earlier concepts of hominin phylogeny, which accepted a progression from the earliest biped to Homo sapiens with minimal branching from that lineage, one might wonder whether it is worthwhile to test causal hypotheses of hominin speciation, but recent finds indicate that “any accurate view of ourselves requires recognizing Homo sapiens as merely one more twig on a great branching bush of evolutionary experimentation” (Tattersall 1999:25, 2000). That is, we need to consider seriously the question of what caused lineage branching in the hominin tree.

Physical Change as the Driver of Vicariance, Selection, and Speciation If allopatric speciation predominates, then so also must physical initiation of speciation predominate. Vicariance is nearly always produced by tectonic and climatic change. Incipient speciation initiated by dispersal over barriers also in most cases implies the causal influence of physical change (e.g., chance Drosophila fly dispersals over the ocean always occur, whether there are islands within reach or not; it took the production of the precursor islands of the Hawaiian Archipelago for the founding of those first allopatric populations of Hawaiian drosophilids, Carson et al. 1970). Thus, the chief causes of population size reduction and allopatry in the history of life have probably derived from physical changes. Although the relationship of punctuated equilibria to physical change was not explored in Eldredge and Gould (1972), the pattern they argued for implies independently that the initiation of speciation mostly comes about through physical change (Vrba 1980): if species are in equilibrium for most of their durations, what causal agency of the punctuation can one invoke other than physical change? The general consensus on the importance of allopatric speciation, together with the implications of punctuated equilibria and Paterson’s (1978) “recognition concept” of species, led to the proposal that physical change is required for most speciation (Vrba 1980). Paterson (1978, 1982) argued that change in the fertilization system, the critical evolutionary change in sexual speciation, is most likely to occur in small, isolated populations that are under selection pressure from new environmental conditions.

Ecological Specialists and Generalists This contrast is of general evolutionary interest (Stebbins 1950; Simpson 1953; Eldredge 1979; Vrba 1980, 1992) and particularly germane to mammalian evolution during the climatic instability of the late Neogene (Vrba 1987a). It has been discussed using various terminologies, such as stenotopy and eurytopy (e.g., Eldredge 1979), niche breadth (e.g., Futuyma 1979), and breadth of habitat specificity or resource use (Vrba 1987a). Specialist and generalist adaptation can be expressed in relation to different kinds of environmental variables, e.g., with respect to food intake, temperature, vegetation cover, light intensity, etc. Given the effects of the late Neogene climatic and tectonic changes in Africa (see sections “Physical Background: Climatic Change” and “Physical Background: Tectonism”), the distinction between species which are stenobiomic (restricted to a particular biome) and eurybiomic (ranging across biomes) is particularly relevant. As populations of a species encounter a new environment, beyond the ancestral biome range, they could in principle either diverge from their adaptation to the ancestral biome to become specialized on the new one or become more eurybiomic by broadening their resource use to include the new biome alongside the ancestral one (e.g., Vrba 1987a, 1989a). Evolution toward eurybiomy, which is very rare (e.g., Herna´ndez Ferna´ndez and Vrba 2005 found a large preponderance of biome specialists in living African mammals), is of special interest as it applies to Homo (Vrba 1985a, 1989a; Pickford 1991; Potts 1998a; Wood and Strait 2003). Proposals that temporal and/or spatial environmental variability, namely, life in fluctuating or unpredictable environments, can promote generalist adaptations have a long history of extensive discussion (e.g., Stevens 1989 reviewed the evolution Page 4 of 45

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

of broad climatic tolerance in high-latitude environments which have a greater range of annual and longer-term variation). Adaptations to strong seasonality range across life forms, from diatoms and other photosynthetic groups in polar waters (which each winter form resting spores in response to darkening and sink down dormant out of the plankton environment to germinate again when light returns, Kitchell et al. 1986) to the deciduous habit of many plants and hibernation and longdistance migration in animals. In advanced vertebrates, complex behaviors form an important category of such adaptations, ranging from the behavioral adjustments of animals to changing temperature and aridity (Maloyi 1972) to hominine culture. The notion of a “biome generalist species” can be subdivided as follows. The eurybiomic phenotypes can be either (A) heritable, namely, genetically based and fixed, or (B) expressed as ecophenotypes, within a broad norm of reaction, in response to varying environments (Hall 2001; West-Eberhard 2003). Case (A) has two subcases. A1: Each organism can live in more than one biome, either because each organism has the needed biomic flexibility or because each organism is a specialist on resource patches which occur across biomes. An example of the latter is the aardvark, Orycteropus afer, which is stenophagous (it eats only ants and termites), a substrate specialist (it digs burrows in sandy or clay soil), and stenophotic (it is nocturnal). Yet O. afer is eurybiomic: its specialized “resource patches” range from semidesert to dense, moist woodland across Africa. A2: There are intraspecific differences in resource use among organisms and populations; i.e., polymorphism in resource use allows the species to respond to environmental fluctuations by shifting relative abundances of the variants. An example is the African buffalo (Sinclair 1977): Syncerus caffer caffer differs in phenotype and resource use from (and lives at higher latitudes and/or altitudes with more grassland present than) the smaller, plesiomorphic phenotype S. c. nanus (in warm, forested regions). This species appears to have “rolled with the punches” of large and frequent climatic changes since the late Pliocene mainly by changes in polymorphic frequencies. All generalist adaptations first evolve in populations, thus rendering the species polymorphic. Intraspecific adaptations and polymorphisms, which become more elaborate with repeated climatic shifting, are likely to be the most frequent responses to climatic extremes (see Vrba 1992: Fig. 4c) with speciation and extinction being rarer outcomes.

Habitat Theory and the Turnover-Pulse Hypothesis The turnover-pulse hypothesis is a part of the broader “habitat theory” which focuses on species’ habitats and on the dynamic relationships between physical change, habitats, and species (Vrba 1985b, 1992). It uses the predominance of allopatric speciation and the consequence that physical change is required for most speciation. Climatic changes (from global or/and local tectonic sources) result in removal of resources from parts of the species’ former geographic distributions and therefore in vicariance. Vicariance on its own is insufficient for speciation. Many species underwent repeated episodes of geographic shifting, vicariance, and reunion of their distributions in response to the astronomical climatic oscillations, without speciation although intraspecific adaptive changes may have accumulated (Vrba 1992, 2005). For speciation to occur, physical change must be strong enough to produce population isolation, but not so severe as to result in extinction, and the isolated phase must be of sufficiently long duration for the changes which define speciation (divergence of the fertilization system) to occur. It has been suggested that most speciation requires sustained isolation or near isolation, without rapid reintegration on the Milankovitch timescale, and that shrinking populations are important in which habitat resources are dwindling and competition increases, with consequent strong selection from the changing environment (Vrba 1995b). In the absence of physical change of appropriate kind and duration,

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

although species may accumulate new adaptations, they are buffered against speciation at several levels (review in Vrba 2005). One prediction is that most lineage turnover, speciation and extinction, has occurred in pulses, varying from tiny to massive in scale, across disparate groups of organisms, and in predictable temporal association with changes in the physical environment (Vrba 1985b, 2005). If we think of origination, several possible patterns of origination frequency could result, all different from the temporally random pattern predicted under H0: (1) origination could in principle be confined to rare, large pulses in response to the largest environmental changes. Such large pulses may resemble jagged mountain crests, or dissected high plateaus, rather than simple, single peaks because the timing of turnover responses to climatic or tectonic episodes will differ among organismal groups and local areas. (2) Many, frequent, small pulses, such as in response to the 100 Ka astronomical cycle, interspersed by the less frequent, larger ones described under (1). (3) Combinations of the random null model and the turnover-pulse hypothesis suggest additional predictions such as a random background of turnover frequency punctuated by rare pulses. A comparison among turnover pulses is expected to show much heterogeneity – or “mosaic” differences. The environmental changes that trigger turnover are diverse. They vary in nature, intensity, timing – how long they endure, how much fluctuation occurs, and steepness of component changes and net trends – and in geographic emphasis and extent, from very localized to present in many parts of the earth. Topographic and latitudinal factors contribute to geographic variation in the turnover responses to a major global change. Also, the different organismal groups differ sharply in how they are affected by climatic variables (see Andrews and O’Brien 2000 for mammals). They differ in response (by speciation, extinction, intraspecific evolution, or no response at all). Lineages which do undergo turnover initiated by a given physical change may do so with different timing (in “relays,” see examples in Vrba 1995b, 1995c). Thus if a turnover pulse is detected in a data set, it is desirable to study subdivisions of those data to understand the detailed taxonomic, geographic, and temporal patterns. Additional hypotheses: (1) Under habitat theory and other concepts which invoke predominant allopatric speciation, the species should generally “start small,” namely, in geographic distributions that are more restricted than those they attain later on (Vrba and DeGusta 2004). H0 does not predict this. (2) Of two areas of similar large size, both subject over the same time to climatic cyclic extremes that remain habitable for organisms; the area that is more diverse in topography will have higher incidences of selection pressures and vicariance per species. The prediction is that the topographically more diverse area has higher rates of vicariance, speciation, and extinction (Vrba 1992). (3) During periods of strong latitudinal thermal contrasts, with ice caps on one or both poles, biomes closest to the equator are predicted to have higher speciation and extinction rates than biomes at adjacent, higher latitudes (e.g., this bias may have contributed to the high species richness in the tropics today, Vrba 1985b, 1992.). (4) Biome generalists are expected to have lower rates of vicariance, speciation, and extinction than biome specialists (Vrba 1980, 1987a, 1992). Because habitat theory stresses physically initiated vicariance and selection pressure, changes in amplitude and mean of the climatic cycles, and in which cycle predominates, are expected to affect the evolutionary outcome. The larger the amplitude, the higher the incidence of vicariance and selection pressure at any cyclic extreme, accelerating the rates of intraspecific adaptation, speciation, and extinction. Changes in cyclic dominance can affect the frequency and duration of vicariance. Large translations in the climatic mean and envelope may be especially significant for speciation and extinction (Vrba 1995b: Figs. 3.2, 3.3).

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

The Coordinated Stasis Hypothesis Brett and Baird’s (1995) hypothesis of coordinated stasis is Darwinian in a focus on organismal interactions in a community as a source of stasis. It proposes that the coevolutionary bonds during stasis are so strong that physical change is needed to disrupt them to result in turnover. Thus this model is “community based” in its theoretical assumptions (see also the hypothesis of coevolutionary disequilibrium of Graham and Lundelius 1984 and reviews in Barnosky 2001; Vrba 2005). Brett and Baird’s (1995) model predicts stasis of species, interrupted by pulses of speciation and extinction, across all communities in which a set of species occurs. Thus, their predictions are closely comparable with those of the turnover-pulse hypothesis, as acknowledged by Brett and Baird (1995:287): “The same term [coordinated stasis] could be used for the blocks of stability in Vrba’s (1985b) ‘stability-pulse’ hypothesis.”

The Variability Selection Hypothesis This hypothesis was proposed and applied to hominin evolution by Potts (1998a, 1998b, 2012; pages quoted are from the 1998a paper unless otherwise noted). It is about (1) a particular category of adaptations which he calls “variability selection adaptations” (VSAs), (2) their initial appearance and establishment, (3) their fate in the face of long-term climatic cycles, and (4) an interpretation of the theoretical implications of their evolution: 1. VSAs are “structures and behaviors responsive to complex environmental change” (p. 81), which are uniform within species “yet able to mediate secondary phenotypic traits that vary. . .” (p. 85). His examples include a locomotor system allowing a wide repertoire of movement and “a large brain or specific neurological structure that is effective in processing external data and generating complex cognitive responses” (p. 85). 2. VSAs arise first in isolated populations. Intraspecific polymorphism results with VSAs in some populations and not in others. Organismal selection from short-term variability during organismal lifetimes initially promotes such VSAs (or at least allows them to persist). 3. The long-term evolutionary outcome at Milankovitch and longer timescales is that organisms with VSAs survive climatic extremes. Therefore species, which include at least one VSAcarrying population, survive. Over time the VSAs can become more elaborate as climatic extremes recur. Thus, high climatic amplitude at timescales longer than organismal life times, notably at Milankovitch and longer timescales, causally influences the evolutionary outcome. 4. Climatic variability at the longer timescales is a selective agent of VSAs, which are “designed [by selection] to respond to novel and unpredictable adaptive settings” (p. 85). That is, these organismal adaptations are shaped by selection for the function of flexible responses to future climatic excursions of the Milankovitch cycles, and this is a new kind of selection: “variability selection” (VS). Potts regards his concept as distinct from previous concepts, notably from the (p. 82) “savanna hypothesis” and other “environmental hypotheses of hominin evolution [which focused] on a specific type of habitat.” Proposals (1), (2), and (3) are severally and jointly consistent with previous theoretical proposals (see section “Ecological Specialists and Generalists”). The sole departure is proposal (4) of a distinct type of selection, which is commented on next. The special effects which the high amplitude of climatic cycles since the late Pliocene had on the biota (e.g., that species, in which generalist adaptations for climatic tolerance evolved, survived disproportionately) has been much discussed (e.g., Stanley 1985; Vrba 1985a, 1992, 2000). No one doubts that strong Milankovitch excursions can selectively remove some populations and species Page 7 of 45

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

whose organisms are unfit under those conditions, nor that generalist adaptations of survivors can sequentially be elaborated during recurrent such episodes. But this would not be a new kind of selection. Organismal selection cannot promote adaptations to future Milankovitch extremes, although inter-demic selection (Wright 1932, 1967) or species selection (review in Vrba 1989b) could in principle occur at those longer timescales. (In fact, Potts did at one stage wonder whether his notion might represent a form of lineage or species selection, R. Potts pers. comm.). The problem is that the concept of selection and adaptation at levels higher than that of organisms is onerous (Williams 1966; Maynard Smith 1987; Vrba and Gould 1986; Vrba 1989b). Maynard Smith (1987) discussed this as follows (p. 121): “We are asking whether there are entities other than [organisms] with the properties of multiplication, heredity, and variation, and that therefore evolve adaptations by natural selection.” Considering the nature of the adaptations Potts (1998a) had in mind, one probably does not need to invoke higher level selection. Such issues on levels of selection have been extensively debated and with respect to diverse organismal case histories. An example which is of interest here, in spite of (and perhaps because of) being far removed from hominins on the tree of life, is the case in diatoms of the resting stage adaptation to polar conditions of long winter darkness (Kitchell et al. 1986): The fossil record shows that diatoms living in Arctic waters just before the Cretaceous/Tertiary (K/T) boundary already had this life cycle adaptation. Kitchell et al. (1986) documented that during the K/T mass extinction (which involved long-term global darkening), diatoms and other photosynthetic planktonic groups with resting stages had markedly lower extinction rates than groups which lacked this seasonal adaptation. They argued (correctly in my view) that these life history features, which arose by selection at the organismal level as adaptations to seasonal variability, were also fortuitously (by sheer luck) available and useful during the K/T event for weathering much longer intervals of darkness. They concluded that this sorting among species, although nonrandom, does not represent species selection but species sorting according to the effect hypothesis (Vrba 1980). The adaptation is this case could not have been selected at the organismal level for climatic variability at the timescale of mass extinction. The selective forces and character complexes which contributed to the survival of hominins and other mammals in the face of increasing climatic amplitude during the late Neogene may in principle fall into the same category.

Additional Comments on Environmental Hypotheses of Hominin Evolution In the current spirited and exciting debate on the various hypotheses (savanna, variability selection, turnover pulse, habitat theory, and more), some confusion has crept in, which is affecting the debate in a negative way to the point where sometimes the discussants are talking past each other. While Potts (2012:154) wrote that “Regarding the external drivers of human evolution, the primary alternative to Vrba’s TPH [turnover pulse hypothesis] has been the variability selection hypothesis,” the points raised here are relevant to all the hypotheses and all parts of the debate. Three such issues will be mentioned here. 1. Specific Habitats, Species-Specific Habitats, and Other Specific Notions. Consider these quotations: “The VS [variability selection] hypothesis differs from prior views of hominin evolution, which stress the consistent selective effects associated with specific habitats or directional trends (e.g., woodland, savanna expansion, cooling)” Potts (1998a:81). “Habitatspecific adaptations may entail a more limited responsiveness to environmental perturbation. . .” (Potts 1998a:155). “Over the past three decades, the environmental study of human evolution has been dominated by the search for the preferred [i.e., specific] habitat of each hominin species. This approach has led to a far more static concept of early hominin adaptation. . .” (Potts Page 8 of 45

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

1998a:161). This pits “consistent selective effects,” “specific habitats” and “habitat-specific adaptations” of “limited responsiveness,” and directional climatic trends (the not-so-good “static concept”) against variable selective effects, variable habitats, and “variability selection adaptations” and pervasive climatic oscillations and environmental complexity (the good, dynamic concept). But is this a substantive dichotomy with correct characterization of both sides? It is not, and one “culprit” is the interpretation of the word “specific.” In the present context, “specific” simply means “relating to, characterizing, or distinguishing a species,” thus neutral on breadth and changeability of adaptation, habitat, or environment in this case. The definition of the specific habitat of a species (see third paragraph in introduction of this review, which describes how many including the present author have used it) is indeed neutral on degree of variability, referring only to a list of resources and their ranges which describes where and how the species can live. In principle, the resource ranges of the specific habitat can be extremely broad. Consider an extreme and hypothetical example of a land species which can live everywhere within a temperature range of 0–100
C. Its specific habitat with respect to temperature is the range 0–100
C. A related point: the notion that each species is “specific for a particular habitat” does not equate with specificity for a particular – or single – type of environment. For example, the aardvark, while a specialist in terms of food and substrate, ranges widely across Africa from semidesert to dense, moist woodland. A species’ habitat may remain intact although it lives in strongly fluctuating environments over long time, such as the aardvark whose habitat and resources persisted as widely varying environments swept over the areas in which it lived. In other cases, habitat variability – such as variable use of food and substrate – is an integral part of the habitat specificity of the species (see 2). Unfortunately, such simple misunderstandings can spread and eventually harden. For example, deMenocal (2004:4) stated that “most environmental hypotheses of African faunal evolution are ‘habitat-specific’ (Potts 1998b) in that they consider faunal adaptations to a specific environment, most commonly the emergence of grassland savannah. . .” 2. Adaptation to Variability. Potts (1998a, 1998b, 2012) regards the VSA (variability selection adaptation) concept as distinct from previous concepts of adaptation, such as the generalist adaptations which confer eurytopy (Eldredge 1979), broad habitat specificity (Vrba 1987a), and broad climatic tolerance (Stevens 1989). He considers “habitat-specific” adaptations (e.g., Vrba 1987a) and selection pressures as different from VSAs and VS because the former in his view narrowly refer to a particular kind of environment and not to variable environments. He is wrong in these claims. Structures and behaviors that confer flexibility in the face of – and are usually ecophenotypic or genetically based adaptations to – climatic variations, and that may arise and exist as polymorphic variants in species, are well known (e.g., the resting/vegetative life cycle in diatoms noted above, hibernation, etc.) including complex behaviors in primates (e.g., the presence in some Japanese macaque populations of grass-washing behavior, Nakamishi et al. 1998). Concerning human evolution, as reviewed below, many have written about adaptation to variability (including environmental heterogeneity at any one time) and the effects of climatic cycles. As Potts (2012:154) considers habitat theory and the VS hypothesis as “primary alternatives,” any impression that previous discussions of human evolution in the light of habitat theory (e.g., Vrba 1985a, 1989a) have ignored hominin adaptation to climatic variability needs to be corrected. One hypothesis (Vrba 1989a:30) concerns culture in general: The culture of the genus Homo is a generalist adaptation. Hominine culture is an extension of the common phenomenon in other animals that use behaviour to cope with climatic conditions. . . . a special case among animal behaviors that confers an expanded use of environmental resources. In contrast, robust australopithecines

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

were more specialized on open, arid habitats. . . .[and in Homo occurred] a switch to the crucial generalist adaptations of brain and culture that have made us the least environment-dependent species on earth today (p. 37).

It turns out that Vrba’s (1989a) hypothesis that the robust australopithecines “were more specialized on open, arid habitats” is probably wrong (see review below). However, it now seems likely that the masticatory features of Paranthropus, while adaptations for consuming tough or gritty foods, had the effect of broadening, not narrowing, the range of food items consumed and allowed these forms to subsist in varied environments (Wood and Strait 2003). One hypothesis on hominin adaptation to climatic variability, which is plausible and deserving of testing, is that humans descend from deep nomadic (migratory) ancestry, at least since the onset of advanced bipedalism in Homo ca. 1.6 Ma, which falls during a time of change to more open and seasonally arid landscapes: As Baker (1978) observed, most animals are ‘migratory’ to some extent. But it is undeniable that those living in open, arid habitats, where resources tend to be patchy in space and/or time, invariably have a greater tendency to seasonal and more extensive movement. . . Did one or both of the hominin lineages that diverged during the Pliocene migrate seasonally across ecotonal margins? (Vrba 1985a:70).

If evidence of hominid nomadism in the Early Pleistocene were to be found (as it might be, for instance, by isotopic analysis of diet in conspecific hominins), one would still need to ask whether that nomadic potential was there previously or whether it evolved de novo by genetically based broadening of the norm of reaction to allow both nonmigratory and migratory behavior depending on seasonality. If the latter is true, then migratory behavior by Homo could surely be termed a good habitat-specific adaptation and a good variability selection adaptation. The use of different wording does not change the logic of that. 3. Climatic Variability. Potts (1998a, 1998b, 2012) concluded that others with versions of the savanna hypothesis that were articulated previous to his VS hypothesis, which includes me, were focusing narrowly on long-term cooling trends and failed to incorporate observations about patterns of African paleoclimatic variability from deep-sea cores and recently also from coring on the African continent (Scholz et al. 2007; Cohen et al. 2007; reviewed below). Again, the issue must be taken with this. First of all, the focus on long-term trends (e.g., Vrba 1995b) is a necessary part of the study of climatic variability in mammalian evolution: the shorter-period Milankovitch cycles modulate each other which gives rise to cycles of longer periods (and therefore to long-term cooling and warming trends) which are associated with ice sheet expansion and cooling and turn out to be important triggers of mammalian speciation and extinction (e.g., cycles with periods of ca. 1 Ma and ca. 2.4–2.5 Ma; see van Dam et al. 2006). More generally, it was the realization of the potentially enormous implications of the climatic oscillations for evolution of new form, function, and species in hominins and other mammals – of the fact that the “species specific for these . . . biomes are riding along on their ‘habitat plates’, that drift back and forth rapidly . . . over the tectonic plates that drift more slowly beneath” (Vrba 1992:11) – that prompted the organization of an interdisciplinary conference to explore those implications (Vrba et al. 1995). It was argued then (Vrba 1995a:33) that “if prolonged vicariance is important for turnover and especially for speciation, then major shifts in the mode, or periodicity pattern, of the astronomical cycles should be examined for associated turnover” (see also Vrba 1992), and a model was illustrated (Vrba 1995a:30–33), using Shackleton’s (1995: Fig. 17.3) data which records delta18O variation at 0.003 Ma interval steps for the past 6 Ma, for measuring climatic variability. Because this way of measuring climatic variability monitors the outer envelope of climate curves step by small step, it is

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

expected to detect major changes in climatic mode such as documented by deMenocal and Bloemendal (1995): a shift from dominant climatic influence occurring at 23–19 Ka periodicity prior to ca. 2.8 Ma to one at 41 Ka variance thereafter, with further increases in 100 Ka variance after 0.9 Ma (see also Ruddiman and Raymo 1988). (Some results will be compared in section “Physical Background: Climatic Change” with those of others who have measured variability in climatic curves, including Potts 1998a.) In sum, how do the turnover-pulse hypothesis (within in more general habitat theory which includes responses to climatic variability of generalists and specialists) and the variability hypothesis compare in terms of content? Readers will make up their own minds. My conclusion is that they do not differ substantively in terms of the basic processes implied. There are differences in emphasis, in terms used, and in how the terms they have in common are interpreted (particularly the term “specific habitat” of species). Is the early savanna hypothesis still alive and well? Yes, the basic hypothesis – that climatic change has caused reductions in wood: grass cover proportions which affected hominin populations and evolution – remains a good one, although it has evolved and branched out into more sophisticated versions. Cerling et al. (2011) showed that the fraction of woody cover in tropical ecosystems can be quantified using stable carbon isotopes in soils and applied the method to fossil soils from hominin sites in the Awash and Omo-Turkana basins. They concluded (p. 55) that “the combined results from two of the most significant hominid-bearing regions in eastern Africa leave the savanna hypothesis as a viable scenario for explaining the context of earliest bipedalism, as well as potentially later evolutionary innovations within the hominin clade.”

Tests Based on the Temporal Distribution of Newly Appearing Phenotypes and Species The models above all predict significant concentration in time of particular newly appearing morphologies and in the case of the coordinated stasis and turnover-pulse hypotheses also of speciation and extinction events. All of them predict that such events in the fossil record should associate significantly with climatic change. Most difficulties in testing such hypotheses have to do with errors in the chronological, physical, and biotic data and with testing at inappropriate temporal, geographic, and taxonomic scales (Barnosky 2001). There are two types of errors in such tests: inferring fossil events that are not there (i.e., erroneous rejection of H0, Type I error) and failure to detect real events (Type II error) as exemplified by Signor and Lipps (1982). Take, for example, a Type II error under the turnover-pulse or coordinated stasis hypotheses, the attempt to distinguish between H0, and real small speciation pulses that occurred at the Milankovitch timescale. Such a test using first appearance data with lower time resolution (e.g., the data for 0.5 Ma-long intervals length in Vrba and DeGusta’s 2004 study of African mammals) will fail, although major pulses might be detectable. The main bias that leads to Type I error, seeing pulses that are not there, arises from unequal fossil preservation between time intervals, areas, and groups of organisms, the “gap bias” (Vrba 2005): any given species’ fossil FAD (first appearance datum) may postdate its true, or cladistic, FAD (Kimbel 1995). Gaps have the effect that, for instance, a count of FADs in an interval is erroneously inflated by FADs of species which in reality originated (but were not detected) previously. An early version of a test that corrects for the “gap bias,” thus allowing a rigorous test of the pulse hypothesis, was applied to the African larger mammals of the past 20 Ma divided into 1 Ma-long intervals (Vrba 2000). More recently, a second, updated form was applied to the nearly 500 African species recorded over the past 10 Ma divided into 0.5 Ma-long intervals (Vrba and DeGusta 2004; Vrba 2005). Time resolution in this record is Page 11 of 45

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

sufficiently good, with more than 70 % of the site records dated by radiometric or paleomagnetic means, that any large speciation (or extinction) pulses spaced sufficiently far apart in time should be detectable. Some results will be mentioned in section “The Record of First Appearances of Mammalian Species”

Physical Change, Adaptation, Speciation: Evidence from the African Neogene Physical Background: Climatic Change Following the definitive documentation of the astronomical cycles (Hays et al. 1976), it was thought that they may have had little effect on the tropics in general (review in Burckle 1995) and on African hominin-associated environments in particular. For example, Hill (1995:187) considered that “it may be that African terrestrial vertebrate habitats were to some extent buffered from climatic changes seen elsewhere.” Hill’s caution is well taken that specific areas may “march to a local drummer” especially if that drumbeat derives from tectogenesis (see below). It now appears that much of Africa participated in global as well as more localized climatic changes over the time period of interest, namely, the late Miocene-Recent record, as the earliest hominin fossils currently date to ca.7 Ma ago (Brunet et al. 2004). For much of this time Africa has been influenced by two separate processes (deMenocal 2011): forcing from the orbital precession cycle has brought about monsoonal cycles that alternated between wet and dry conditions, and superimposed on these was a long-term trend toward increasingly more arid and more variable conditions. The Late Miocene. Changes in polar ice volume and sea level have greatly influenced African climate and human evolution as cited variously below. By the time hominins evolved, there had been large ice sheets in Antarctica since 33 Ma (following a previous time of ephemeral ice sheets), while the earliest extensive Arctic glaciation was established much later, by 2.7 Ma and contemporaneously with the first appearance of Paranthropus, the robust australopithecines, and probably also of the lineage to modern humans. Miller et al. (2005) discussed the relations of ice sheets, global climate, and sea level and considered that sea level mirrors oxygen isotope variations, reflecting ice-volume change and thus global climate on the 10,000 year–1,000,000 year timescale which applies to human evolution. They found prominent sea level falls and thus global climatic events, at 8.2 Ma, 5.7 Ma, 4.9 Ma, 4.0 Ma, 3.3 Ma, and 2.5 Ma. There was ice buildup on West Antarctica and general increase in delta18O values 7.0–5.0 Ma ago (Kennett 1995). A major cooling which started before 6 Ma and peaked shortly thereafter contributed to isolation and desiccation of the Mediterranean Basin during the Messinian low-sea level event and salinity crisis dated ca. 5.8–5.3 Ma (Haq et al. 1980; Hodell et al. 1994; Bernor and Lipscomb 1995; Aifa et al. 2003; Garcia et al. 2004). This major cooling coincides with a strong vegetation change ca. 6.3–6 Ma, with a large decrease in tree cover and increased aridity in both West and East Africa, according to Bonnefille’s (2010) overview of macrobotanical (fossil wood, leaves, and fruits) and microbotanical (mainly pollen) evidence for the past 10 Ma in tropical Africa with special reference to the hominin sites. After the Messinian followed warming and a transgressive phase started before 5 Ma and reached a maximum in the 5–4 Ma interval, according to Haq et al. (1987). Questions remain on the African effects of these late Miocene climatic events. Kingston et al. (1994) found that, in the Kenyan Tugen Hills area, a heterogeneous environment with a mix of C3 and C4 plants – and without grassland dominance – persisted over the entire past 15 Ma without any apparent local influence from global climatic change. Yet evidence from Lothagam indicates that this part of Kenya experienced strong environmental changes over the latest Miocene (Leakey et al. 1996; Leakey and Harris 2003). Further evidence comes from analyses of carbon isotope ratios in Page 12 of 45

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

soils and fossil tooth enamel. Cerling et al. (1997) studied fossil herbivores ranging over the past 22 Ma from several continents. Using the fact that low delta13C values in herbivore teeth reflect a diet of mainly C3 plants, while high values indicate feeding on C4 plants, they found that up to 8 Ma ago, mammals in Pakistan, Africa, and South and North America had C3 diets or C3dominated diets. By the late to latest Miocene, C4 plants came to dominate the diets. In Kenya, representing the lowest latitude in the sample, the transition was complete by between 8 and 6.5 Ma and in Pakistan by ca. 5 Ma. Cerling et al. (1997) interpreted their results as showing a global increase in the biomass of C4 plants 8–6 Ma ago which resulted from a decrease in atmospheric CO2. The Plio-Pleistocene. Interest in African hominin-associated climatic changes has burgeoned greatly over the past decade. Here, only a few examples are given from the large volume of evidence for the Plio-Pleistocene, from research on broader regional climatic variability, to illustrate some of the basic lines of enquiry and the diversity of approaches. Additional evidence more directly focused on hominin environments will follow below. Clemens et al. (1996) discussed how monsoon variability and evolution respond to external forcing (orbitally driven changes in solar radiation) and internal forcing (interaction among the atmosphere, oceans, land surface, and ice sheets). They examined a deep-sea sediment record spanning the past 3.5 Ma from the northwest Arabian Sea and compared diverse proxies, including abundances of Globigerina bulloides, biogenic opal content which indicates radiolaria and diatom production, and lithogenic grain size of the deep-sea sediments, all of which in this area can indicate the strength of the Asian monsoon. Clemens et al. (1996) argued that the growth of Northern Hemisphere ice sheets over the past 3.5 Ma weakened the Asian summer monsoon and increased the aridity of subtropical Asia and eastern Africa. They demonstrated that the phase relationships between the African monsoon and the glacial cycles were shifting continuously over the past 2.6 Ma, explaining why indicators of surface water such as lake levels and of vegetation, such as dust spikes, often do not covary. The authors found significant shifts in the intensity and phase of the Indian monsoon at ca. 2.6 Ma, 1.7 Ma, 1.2 Ma, and 0.6 Ma. deMenocal (2008, 2011:541) discussed the large amplitude of the African wet-dry monsoon cycles using the example of changes in the Sahara and pointed out the usefulness of sapropel layers as proxies (see also Rossignol-Strick 1985; Rossignol-Strick et al. 1998) for detecting the intensity and phase of the monsoon cycles: From 15,000 to 5,000 years ago, the modern Saharan Desert was nearly completely vegetated, with large, permanent lakes and abundant fauna. Precessional increases in summer radiation invigorated the monsoon, delivering more rainfall deeper into Africa, and enhanced Nile river runoff flooded into the eastern Mediterranean Sea. The resulting freshwater stratification created anoxic conditions and led to deposition of organic-rich sediments (sapropels) on the seafloor.

Similarly, Cole et al. (2009, 2012) found evidence for the prevalence of extensive paleolakes in the Sahara during the African humid period. The opposite extreme, “megadrought,” has also been documented. In companion papers, Scholz et al. (2007) and Cohen et al. (2007) presented results from drill cores from Lake Malawi and point out that by 2007, these were the first long and continuous, high-fidelity records of tropical climate change from the African continent itself. Their record documents periods of severe aridity between 135 Ka and 75 Ka ago, when the lake’s water volume was reduced by at least 95 %. Scholz et al. (2007:16416) wrote, “Surprisingly, these intervals of pronounced tropical African aridity in the early late-Pleistocene were much more severe than the Last Glacial Maximum, the period previously recognized as one of the most arid of the Quaternary.” According to Cohen et al. (2007:16422), “Fossil and sedimentological data show that Lake Malawi itself, currently 706 m deep, was reduced to a ca. 125 m deep saline, alkaline, well mixed lake.” Page 13 of 45

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

Among Plio-Pleistocene records that demonstrate the large effects of global climatic change on Africa, many are based on signatures from plants, algae, or other indicators of overall plant cover such as dust. Pollen cores off West Africa record the shifting of the Sahara-Sahel boundary and the earliest extensive spread of the Sahara desert ca. 2.8–2.7 Ma ago (Dupont and Leroy 1995). One of the two strongest vegetation changes found by Bonnefille (2010) across tropical Africa over the past 10 Ma occurred at 2.7 Ma (p. 391): “abrupt decline of forest pollen accompanied by an increase in grass pollen was found at 2.7 Ma, . . . accompanied by a significant increase in C-4 grass proportions, well indicated in the Turkana region and likely explained by an increase in dry season length.” Marlow et al. (2000) used an index based on the ratio of two types of alkenones (chemical compounds produced by specific species of haptophyte algae) to measure sea surface temperature (SST) in a marine core off Namibia. They presented their continuous time series of changing SST for the past 4.5 Ma, as well as estimates of paleoproductivity from the mass accumulation rates of organic carbon, diatom abundances, and diatom assemblages. Marlow et al. (2000) interpreted decreased upwelling to represent warmer conditions with wetter, more mesic periods in southern Africa and concluded that SSTs decreased markedly, in association with intensified Benguela upwelling, after 3.2 Ma, with subsequent periods of marked SST decrease and upwelling intensification near 2.0 Ma and 0.6 Ma. Another marine record from southwestern Africa, off Angola, derived from carbon isotope analyses of wind-transported terrigenous plant waxes, indicated African C4 plant abundances 1.2–0.45 Ma (Schefuss et al. 2003). The evidence showed that the African vegetation changes are linked to SST in the tropical Atlantic Ocean and that changes in atmospheric moisture content due to tropical SST changes and the strength of the African monsoon controlled African aridity and vegetation changes. Marine records off West Africa and from the Gulf of Aden have documented delta18O variations and also dust influxes from the Sahara and Sahel regions in the West and from Arabian and northeastern African areas in the Gulf of Aden (deMenocal and Bloemendal 1995; deMenocal 2004). The latter paper reported steplike shifts in the amplitude and period of eolian variability at 2.8 (0.2) Ma, 1.7 (0.1) Ma, and 1.0 (0.2) Ma. As one method to use climatic records to predict over which time intervals vicariance (population fragmentation) should be particularly concentrated, the following hypothesis was introduced with discussion on how to test it: “long-term, continuous vicariance, and long-term increases and decreases in the minimum- and maximum-value envelopes of the astronomical climatic cycles, are the kinds of allopatry and climatic change that are particularly important for speciation” (Vrba 1995b:27 and following pages). Shackleton’s (1995: Fig. 17.3) data were used, which record delta18O variation at 0.003 Ma interval steps for the past 6 Ma, to identify periods over which the largest net cooling or warming trends occurred. (Vrba 2004: take an interval tx of length x Ka, for example, t100 for x ¼ 100 Ka, and move it step by step along the time axis from early to late. At each interval step, mark the interval along the time axis if either of conditions C, for cooling, or W, for warming, is true. C: the upper [warm] envelope of the climatic curve remained continuously below the running mean of the previous 300 Ka, i.e., the interval is a t100,C, or an interval of length 100 Ka with marked cooling. W is the corresponding condition for a warming trend. A pattern of t100,C and t100,W distribution in time results, with data clusters for the most sustained trends. I here report results for separate assessments using interval lengths in Ka of x ¼ 40, 65, 100, and 140.) The following approximate intervals (in chronological sequence) emerged as times of sustained net cooling (t40,C, t65,C, t100,C, and t140,C are respectively labelled as *, **, ***, and ****, from least to most severe; time ranges in ca. Ma): 6–5.7****, 5.1–4.9*, 4.2–3.9*, 3.4–3.2***, 2.9–2.3 especially 2.7–2.5****, 2.1–2.0*, 1.8–1.65**, 0.95–0.85**, and 0.8–0.65** (and 0.8–0.6*). Intervals of net warming (similar notation as for cooling): 5.6–5.35****, 4.5–4.4*, 3.1–2.9*, 1.65–1.6*, and 0.85*. Because this method of measuring changes in climatic variability, in this case in delta18O Page 14 of 45

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

variability, monitors the outer envelope step by small step, it is expected to detect major changes in climatic mode such as documented by deMenocal and Bloemendal (1995): a shift from dominant climatic influence occurring at 23–19 Ka periodicity prior to ca. 2.8 Ma to one at 41 Ka variance thereafter, with further increases in 100 Ka variance after 0.9 Ma (see also Ruddiman and Raymo 1988). Comparison with the results in the previous paragraph shows that this way of measuring change does succeed in detecting the major dominance shifts. There are now several such approaches. For example, Potts (1998a) subtracted the lowest from highest value for each unit million year as a measure of total climatic variability for that unit year. He found that variation of 0.3–0.5 parts per million (ppm) is obtained for most of the Neogene until the 6.0–5.0 Ma interval, during which variability rose sharply. After a minor decrease during 5 to 4 Ma, there were increases during every succeeding interval with the highest one, to 1.9 ppm, during the past 1 Ma (Potts 1998a:83, Fig. 1). Donges et al. (2011) applied a nonlinear method of time series analysis, recurrence network, to records of dust flux. They found (p. 20422) three “transitions between qualitatively different types of environmental variability in North and East Africa during the (i) Middle Pliocene (3.35–3.15 Ma B. P.), (ii) Early Pleistocene (2.25–1.6 Ma B. P.), and (iii) Middle Pleistocene (1.1–0.7 Ma B. P.),” which approximately also appear among my results, as does the mode change 6.0–5.0 Ma ago found by Potts (1998a). It is worth noting the major climatic changes, including some with rough consensus on when they occurred, from the diverse sources cited above: 8.2 Ma, 7–6 Ma, and associated with the Messinian ca. 5.8–5.3 Ma, ca. 5 Ma, 4.2–3.9 Ma, 3.5–3.2 Ma, 2.9–2.3 Ma, 1.8–1.6 Ma, 1.2 Ma, and 1.0–0.6 Ma.

Physical Background: Tectonism Tectogenesis has featured less prominently than climate change in discussions of evolution, perhaps because it is mostly a slow process and the date limits for events tend to be wide. Yet it has had a primary influence on landscape and biotic evolution. This includes hominin evolution especially in rift-associated environments as recognized long ago by Coppens (1988–1989). Crustal changes influenced climate on a grand scale, e.g., the late Pliocene closure of the Isthmus of Panama may have led to the start of the modern ice age (Maier-Reimer et al. 1990; Haug et al. 2001). The uplift of western North America, the Himalayas, and the Tibetan Plateau possibly influenced the Pleistocene cooling intensification ca. 1 Ma ago (Ruddiman et al. 1986). Northward drift of Africa during the Neogene led to southward displacement and areal decrease of tropical African forests and contributed to long-term aridification (Brown 1995). Episodes of intensified African uplift since ca. 30 Ma ago, which raised the entire eastern surface higher than in the West, greatly affected the African climate (Burke 1996). Apart from the numerous localized climatic effects of tectogenesis (e.g., Feibel 1997), the topographic diversity it generates together with the superimposed climatic cycles constitutes a prime cause of spatial and temporal environmental heterogeneity, changing selection pressures, and speciation (Vrba 1992). Thus evolution of the African Rift had an especial role in some evolutionary events in hominins (Coppens 1988–1989) and other mammals (e.g., Denys et al. 1987). The present episode of rifting began in the Early Miocene (Frostick et al. 1986). Ca. 8–6 Ma ago, a general increase in African tectonic activity led to formation of the Western Rift (Ebinger 1989). A major episode of uplift coincided with the climatic changes ca. 2.5 Ma ago (Partridge and Maud 1987). After 6 Ma ago, the rift system continued to propagate to the southwest toward the Kalahari Craton (Summerfield 1996). One incipient zone of rifting, trending southwest from Lake Tanganyika, terminates in central Botswana, where faulting and tilting of the zonal margins have resulted in damming of the Okavango River to spread out as the extensive inland Okavango Delta (Scholz et al. 1976). Page 15 of 45

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

I suggest that the dynamics of the hydrological features associated with rifting – rivers redirected, lakes forming and disappearing, and especially the inland deltas spreading at the margins of incipient rift zones – have had a particular impact on the evolution of hominins and other biota. All early hominins required permanent water, and many of the eastern African hominin sequences reflect riverine and rift margin associated deltaic and lake environments (e.g., Harris et al. 1988; Brown and Feibel 1991). The significance of inland deltas is that they can form vicariated “islands” of mesic conditions – or refugia – throughout periods of aridification and even in the absence of topographic heterogeneity. The edges of such a refugium are ecologically heterogeneous with intrusions of the arid surrounding environment. (“Refugium” here means a biome refugium, e.g., a forest refugium preserves the characteristic forest vegetation physiognomy, although its detailed taxonomic composition may differ from that of the parent forest community.) The Okavango Delta provides a good example: it is a vicariant island – despite the very low relief of the area (Scholz et al. 1976) – of woodland savanna and water almost entirely surrounded by semidesert. Many of the hominin-bearing strata represent times when the areas were such inland deltaic-riverine-lacustrine refugia (Vrba 1988). This poses problems for our ability to recognize times of widespread climatic change across the larger areas because “climatic change in the larger region is recorded in a refugium only close to its ecotonal limits, by the new appearances (or disappearances) of peripheral taxa . . . that represent occasional intrusive elements from the alternative biome” (p. 410). An important implication from the evolutionary perspective is this: as climatic changes were sweeping across much of Africa at the Milankovitch scale, such inland deltas were recurrently isolated and reconnected as parts of larger continuous biomes. During the reconnected phases, migration and gene flow occurred. During the vicariant phases, there was enhanced incidence of gene pool divergence among populations, selection pressures at the refugial margins, intraspecific phenotypic diversification, and speciation. If it is true that inland deltas can in this way act as centers of phenotypic diversity and speciation and that they are particularly prevalent at the tilting margins of incipient rift zones, this would predict a late Neogene propagation of centers of increased speciation in a South-southwesterly direction as the rift evolved.

The Record of First Appearances of Mammalian Species All Larger Mammals. As noted above, a method which corrects for the “gap bias” was applied to the African larger mammal record of the past 10 Ma. Such correction is especially important in the late Neogene climatic context because open, mesic to arid areas tend to preserve vertebrate fossils better than do the more forested, wetter ones (Hare 1980). The following results emerged (largely agreeing with those in Vrba 1995c, 2000, in so far as they are comparable): over the past 8 Ma, the strongest turnover pulses, involving both origination and extinction, occurred in the 5.5–5.0 Ma and 3.0–2.5 Ma intervals. (The dating of the earlier pulse is tentative as there are no physical dates, and this event may belong to the 6.0–5.5 Ma interval; I will refer to the 5.5 Ma event.) Each of the intervals 7–6.5 Ma and 3.5–3.0 Ma had an origination pulse without an extinction pulse and 1.0–0.5 Ma ago an extinction pulse without an origination pulse. Where one can compare this set of turnover events with the strongest cooling trends, the coincidence in time and intensity is strikingly close: the strongest climatic event, cooling toward ~2.5 Ma ago, coincides with the strongest turnover pulse, while lesser cooling and turnover events are present in the intervals 3.5–3.0 Ma and 1.0–0.5 Ma. The results also showed intervals of significantly low origination and extinction, some of which overlapped with periods of high sea level with low polar ice on a warmer earth (Haq et al. 1987; Hodell and Warnke 1991). The African mammalian record and the bias-correction model which was used continue to be updated. The results do give preliminary support to the hypothesis that at least a substantial part of Page 16 of 45

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

turnover in African mammals was initiated by climatic change and that global cooling with increased aridity and increased seasonality was a more important stimulus of turnover than was global warming (Vrba 2000, 2005). Of the cooling trends, the one toward 2.5 Ma was the strongest, followed by a lesser trend starting ca. 1 Ma ago. Yet individual glacial maxima became colder after 2.5 Ma, especially after 1 Ma (Shackleton 1995). The fact that there were no further major origination pulses after 2.5 Ma suggests that most of the lineages present then were either species that had evolved during the start of the modern ice age with adaptations to the new environments or long-lasting biome generalists that survived right through that cooling trend. A related result is that of Vrba and DeGusta (2004). We studied the question of whether most species “start small,” namely, in geographic distributions that are more restricted than those they attain later on. We used the same 10 Ma-long record of the African larger mammals and the correction for the “gap bias.” The number of fossil site records from which each species is known in an interval was taken as a proxy for the magnitude of its living geographic range and abundance in that interval. We then tested H0 that the geographic spread of species remained averagely constant across successive survivorship categories, namely, from the first appearance (FAD) interval to the immediately following one, and so on. We found that the mean number of site records increased strongly from the FAD interval to the following survivorship interval, followed by a less marked although still significant increase to the next interval, with no significant changes thereafter. Thus we concluded that the average large African mammal species has indeed started its life in a relatively small population and thereafter increased in geographic range to reach its long-term equilibrium abundance by ca. 1 Ma after origin. This supports hypotheses of speciation that accord a major role to the formation of isolated populations of reduced size initiated by physical change. Not everyone has agreed that global change was a driver of evolutionary change and speciation in African hominins and other mammals. For instance, one aim of Behrensmeyer et al. (1997) was to test Vrba’s (1995c) finding of a turnover pulse in African mammals between ca. 2.8 and 2.5 Ma by examining the past 4.5 Ma in the Turkana Basin (including the northern Shungura Formation, Ethiopia, and the southwestern Nachukui and southeastern Koobi Fora Formations in Kenya). They concluded that there was “no major turnover event between 3.0 and 2.5 Ma” (p. 1591) and that this “weakens the case for rapid climatic forcing of continent-scale . . . faunal turnover” (p. 1593). I have reservations about their methods and assumptions which differed substantially from mine (Vrba 2005). A reexamination of Turkana Basin evolution over 4.0–1.0 Ma divided into 0.5 Malong intervals, using my African mammal database and the statistical “gap bias” model outlined above, showed a single significant origination pulse in the 3.0–2.5 Ma interval and no extinction pulses (Vrba 2005). Separate examination of the northern and two southern areas of the Turkana Basin indicated a strong speciation (and extinction) pulse in the North 3.0–2.5 Ma ago, but none in the combined or separate southern areas. This result is consistent with the southward spread of the Sahara Desert in the latest Pliocene (Dupont and Leroy 1995), which affected the northern basin more strongly, eliciting significant turnover, while the southern deltaic-lacustrine areas may have behaved more nearly like biome refugia. More recently, Bobe and Behrensmeyer (2004:399) found that between 4 and 1 Ma in the Turkana Basin, “episodes of relatively high faunal turnover occurred in the intervals 3.4–3.2, 2.8–2.6, 2.4–2.2, and 2.0–1.8 Ma. Paranthropus and Homo appear in the Turkana Basin during successive intervals of high turnover at 2.8–2.6 and at 2.4–2.2 Ma, while the appearance of Homo erectus is coupled to a major episode of turnover and grassland expansion after 2 Ma.” (See also Bobe’s 2011, comprehensive overview.) At least some studies show that the larger mammalian turnover pattern is also reflected in small mammals. Among micromammals of the Shungura Formation, Ethiopia (Wesselman 1995), at 2.9 Ma woodland taxa predominated and even rainforest taxa were present (e.g., the bush baby Page 17 of 45

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

Galago demidovii, a rainforest species today). These forms were displaced by new grassland-tosemidesert species by 2.4 Ma. The turnover includes terminal extinctions, immigrants from Eurasia such as a hare, Lepus, and global first appearances of species, such as a new species of Heterocephalus, the genus of desert-adapted naked mole rats, and a new species of the ground squirrel genus Xerus (Wesselman 1995). This time also marks the first African and global debuts in the record of several species of bipedal, steppe-, and desert-adapted rodents, such as the genus Jaculus of desert gerboas (Wesselman 1995) and a new springhare species, Pedetes, in South Africa. Evidence for turnover pulses has by now been found in many records from different continents and time intervals and in diverse taxa, from marine invertebrates (e.g., Lieberman 1999) to mammals in areas beyond Africa (e.g., Azanza et al. 2000; Raia et al. 2005; van Dam et al. 2006). The last study, of a dense, long (24.5–2.5 Ma) record of rodent lineages from Spain, adds an intriguing element. It showed the existence of turnover cycles with periods of 2.4–2.5 and 1.0 Ma, which van Dam et al. (2006) linked to low-frequency modulations of Milankovitch oscillations. Specifically, the pulses of turnover occur at minima of the 2.37 Ma eccentricity cycle and nodes of the 1.2 Ma yr obliquity cycle. Obliquity nodes and eccentricity minima are associated with ice sheet expansion and cooling and affect regional precipitation. As the average duration of African larger mammal species over the past 20 Ma is close to the period of the eccentricity cycle (2.33 Ma, Vrba and DeGusta 2004), the question arises: did a substantial proportion of those species originate at one eccentricity minimum, and become extinct at the next, and could hominins have been a part of that? The Hominin Record. The hominid sample is too small (15 to more than 20 species depending on which sources are consulted) to test whether most hominin species “started small” and to test for turnover pulses using the statistical methods which were applied to all larger mammals. Nevertheless it is of interest to compare the known hominin FAD record with the timing of major climatic trends and speciation pulses in all larger African mammals. The earliest appearance of hominins, Sahelanthropus from Chad (Brunet et al. 2004), is ca. 7.2–6.8 Ma according to Lebatard et al. (2008). The hominin clade originated 8–5 Ma ago based on molecular estimates (Ruvolo 1997). Thus, the first appearance of hominins in the record participates in the elevated mammalian origination toward 6.5 Ma ago, in an interval marked by increased African tectonic activity (Ebinger 1989), and ice buildup in West Antarctica with global cooling (Kennett 1995). The FAD of Orrorin tugenensis ca. 6 Ma (Senut et al. 2001; Sawada et al. 2002) occurs near the end of the strong and widespread decrease in tree cover and increased aridity over ca. 6.3 and 6 Ma reported by Bonnefille’s (2010). The genus Ardipithecus from the Middle Awash area, Ethiopia, includes two species to date: A. kadabba from the western margin in 5.7–5.2 Ma-old strata (HaileSelassie 2001; Haile-Selassie et al. 2009) and A. ramidus dated 4.4–4.2 Ma at Aramis (White et al. 1994; WoldeGabriel et al. 1994; White, Asfaw et al. 2009) and with a similar date at Gona Western Margin (bracketed 4.51–4.32 Ma, Semaw et al. 2005). Thus, the FAD of Ardipithecus is associated temporally (and possibly also causally) with the major climatic changes which accompanied the Messinian ca. 5.8–5.3 Ma ago and with the ca. 5.5 Ma turnover event in African mammals. Most African FADs of hominin species are mid-Pliocene to mid-Pleistocene in age, during which time the intervals of strongest climatic change were (see review above) 4.2–3.9 Ma, 3.5–3.2 Ma, 2.9–2.3 Ma, 1.8–1.6 Ma, 1.2 Ma, and 1.0–0.6 Ma and possibly also near 2 Ma and 4 Ma. Together, these episodes occupy ca. 40 % of the past 5 Ma. Yet most, and possibly all, of the hominin FADs either coincide with or fall very close to one of these events (chronology mostly after Wood and Richmond 2000; Wood and Leakey 2011): Australopithecus anamensis first appears at ca. 4.2 Ma and A. afarensis ca. 4.0 Ma (3.8 Ma or possibly 4 Ma according to Wood Page 18 of 45

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

and Leakey 2011); FADs of A. bahrelghazali, Kenyanthropus platyops and possibly also A. africanus are a part of the mammalian origination pulse in the 3.5–3.0 Ma interval which may be a response to the cooling trend ca. 3.5–3.2 Ma; Australopithecus garhi, Paranthropus aethiopicus, P. boisei, and possibly also Homo habilis and H. rudolfensis have FADs in the 2.8–2.3 Ma interval. The FADs of Australopithecus sediba (Berger et al. 2010; Pickering et al. 2011), H. ergaster, and H. erectus (and its migration to Eurasia) between 2.0 and 1.8 Ma may also be associated with major climatic change. While taphonomic factors and chance may have contributed to this pattern, it does leave intact the hypothesis of climatic cause of at least most hominin speciation. An important splitting event in the hominin clade was the one that led to Paranthropus on the one hand and Homo on the other. Several systematic studies have concluded that the characters of A. afarensis are consistent with it being the common ancestor of Paranthropus and Homo and possibly also of one or more additional lineages (e.g., Kimbel 1995; Asfaw et al. 1999). After enduring in apparent equilibrium since ca. 4 Ma, A. afarensis is last recorded just after 3.0 Ma (Kimbel et al. 1994), while its descendants appear variously between 2.7 Ma and 2.3 Ma. Kimbel (1995:435) concluded: “regardless of which phylogenetic hypothesis is more accurate, it is clear that a pulse of speciation occurred in the hominin lineage between 3.0 and ca. 2.7 Ma, producing at least three lineages.” The phylogenetic pattern, of an inferred ancestor ending after 2.9, with new descendants branching off between 2.9 and 2.3 Ma ago, is common in bovids (e.g., Vrba 1995c, 1998a). These concordant genealogical patterns among different mammalian groups strongly suggest the causal influence of the start of the modern ice age, namely, that common causal rules connect the climate system with evolution of different biotic groups. It remains to be seen whether additional information in the future will support these preliminary indications that major changes in the mode of the climatic pattern and the concomitant changes in African environments were important causal influences on speciation in hominins, just as they were in many other mammalian lineages.

Climate in Relation to Habitats and Adaptations of Hominins Bonnefille’s (2010) review of African vegetational evolution provides a particularly good context for this section because of its broad temporal and geographic scope, which encompasses the Cenozoic with focus on the past 10 Ma, includes the recent vegetation, and ranges right across the African tropics with emphasis on areas and sites which have yielded hominins. She discussed both the macrobotanical and the microbotanical evidence and its relationship to results from recent isotopic studies and from Atlantic and Indian Ocean deep-sea cores. Her conclusions include the following (Bonnefille 2010:409): the palaeontological hominid record so far documented appears embedded within a long evolution of tropical vegetation bracketed between two main events. These two events are the most pronounced among all of the many that occurred during the last 10 Ma. They had the strongest impact on past vegetation, at the continental scale, both in west central and eastern Africa..... The first event was a strong shift from an important forest expansion (7.5–7 Ma) to an abrupt retreat with minimum tree proportion (6.5–6 Ma) concerning the whole tropical region, half a million years before the Messinian salinity crisis. . . . The second event (2.7–2.5 Ma) was the arid shift, from forest to savanna expansion, corresponding to maximum expansion of the northern hemisphere glaciation. . . . [It involved] greater and more widespread aridity, increase in C4 grass abundance in lowlands savanna and steppe, and the relative expansions of mountain forests coincide with the appearance of the genus Homo and stone tools registered simultaneously at different sites in East Africa.

Her summation stresses how pervasive mixed vegetation types are in tropical Africa, namely, areas which include both wooded and open habitat in close geographic proximity (p. 409): “Mixed tree and grass cover are among the widely spread vegetation conditions [and have] persisted throughout the last 10 Ma.”

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I have added the bold emphasis in the last sentence because it reflects a convergent theme in early hominin environmental research over the past decade, as apparent in the following discussion of the hominin species in terms of their natural surroundings, adaptations, and habits: the vegetational and other local conditions surrounding each of the early hominin species were heterogeneous and mosaic. The earliest known hominins (or presumed members of the hominin clade; not all agree) are Sahelanthropus tchadensis (Brunet et al. 2002), ca. 7 Ma old, and Orrorin tugenensis (Senut et al. 2001) from Lukeino, Kenya, ca. 6–5.7 Ma (Sawada et al. 2002). The associated fauna of Sahelanthropus according to Brunet et al. (2005:753) “indicates a mosaic of landscapes probably resembling that of the present-day Okavango Delta (Botswana).” The Okavango Delta today “is an interlocking mosaic of habitat types” (Paterson 1976:55). These range from permanent swamp, wetlands, and seasonally inundated open areas, through higher-lying grasslands, dry scrub, woodland, to very dense woodland with high and nearly closed tree canopy and water margin forest, and many of the mammal species are virtually confined to particular parts of this mosaic (Ramberg et al. 2006). The environment of Orrorin was initially described as follows by Senut (2006:89): “It has been widely accepted that hominins (and thus bipedalism) emerged in a savannah environment. However, it is now clear that the earliest bipeds are associated with forested environments as proved by the flora and the fauna of the Lukeino Formation (Kenya, 6 Ma).” But detailed studies of the mammals indicated a more heterogeneous environment (Mein and Pickford’s 2006:183 micromammal study): The presence of galagids, fruit bats and the diversity of dendromurines (3 species) and some probably arboreal murids (possibly ancestral to Thallomys or Grammomys) indicates the presence of trees in the vicinity of the site, but some of the taxa suggest the presence of relatively open environments in the vicinity of Kapsomin at the time of deposition. A similar mixture of vegetation types is indicated by the large mammals from Lukeino.

Bonnefille (2010) linked the strong decrease in tree cover in both East and West Africa after 7 Ma to the earliest hominins as follows (p. 390): At that time, very arid conditions shown by scarce tree cover occurred over the whole tropical region. . . . Generally arid conditions coincide with the accepted timing for the chimpanzee/hominid split, and record of Sahelanthropus tchadensis in Chad and Orrorin tugenensis in Kenya, although these fossils were found under locally wooded environment.

This underlines the important point that patterns and causal actions at different hierarchical levels should not be conflated, because they are to some extent decoupled and relate only indirectly and in subtle ways: at the more inclusive climatic level “very arid conditions” and “scarce tree cover [spread] over the whole tropical region,” just as at the higher phylogenetic level of species, there were changes in population structure toward vicariance that in some cases resulted in speciation and extinction. At the more local scale were those “habitat islands,” each with its “interlocking mosaic of habitat types,” in Paterson’s (1976) words, and buffered to some extent from the larger geographic pattern of aridity and low wood cover, with the hominins and other organisms adapting to those local conditions. We still know very little about what the earliest hominids were doing. Bipedal locomotion of some kind has been claimed for both Sahelanthropus (Brunet et al. 2002) and Orrorin (Pickford et al. 2002), although doubts on that have been expressed, for example, by Harcourt-Smith and Aiello (2004), who considered that the earliest evidence for bipedalism is only arguably from Sahelanthropus, Orrorin, and the next taxon discussed here, Ardipithecus.

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Ever since the announcement of Ardipithecus ramidus as a candidate for the “long-sought potential root species for the Hominidae” (White et al. 1994:306, who described it as Australopithecus ramidus), there has been a debate about its morphology, phylogenetic position, and its habitat 4.4 Ma ago at the source site Aramis. Some of the unexpected and astonishing features and implications of this taxon, especially after subsequent discovery that more than 110 additional specimens from 4.4 Ma stratum include a partial skeleton with much of the skull, hands, feet, limbs, and pelvis, are reflected by the following statements by White, Asfaw et al. (2009:75): This hominid combined arboreal palmigrade clambering and careful climbing with a form of terrestrial bipedality more primitive than that of Australopithecus. Ar. ramidus had a reduced canine/premolar complex and a little-derived cranial morphology and consumed a predominantly C3 plant-based diet (plants using the C3 photosynthetic pathway). Its ecological habitat appears to have been largely woodland-focused. Ar. ramidus lacks any characters typical of suspension, vertical climbing, or knuckle-walking. Ar. ramidus indicates that despite the genetic similarities of living humans and chimpanzees, the ancestor we last shared probably differed substantially from any extant African ape. Hominins and extant African apes have each become highly specialized through very different evolutionary pathways.

Concerning the Aramis habitat, White, Ambrose et al. (2009) wrote (p. 87): Assessment of dental mesowear, microwear, and stable isotopes from these and a wider range of abundant associated larger mammals indicates that the local habitat at Aramis was predominantly woodland. The Ar. ramidus enamel isotope values indicate a minimal C4 vegetation component in its diet (plants using the C4 photosynthetic pathway), which is consistent with predominantly forest/woodland feeding. Although the Early Pliocene Afar included a range of environments, and the local environment at Aramis and its vicinity ranged from forests to wooded grasslands, the integration of available physical and biological evidence establishes Ar. ramidus as a denizen of the closed habitats along this continuum.

In their response to White, Ambrose et al. (2009) and also to companion papers by WoldeGabriel et al. (2009) and Louchart et al. (2009), Cerling et al. (2010) disagreed and stated that from their analysis of the stable isotopic record (p. 1105d): “we find the environmental context of Ar. ramidus at Aramis to be represented by what is commonly referred to as tree-or bush-savanna, with 25 % or less woody canopy cover,” and that “although we do not judge the validity of the savanna hypothesis, we note that from the stable isotopic record, the connection between bipedalism and C4 grass expansion starting in the late Miocene and continuing into the Pliocene remains a viable idea.” White et al. (2010) replied that Cerling et al.’s (2010) reconstruction of a predominantly open grassland environment with riparian woodland is inconsistent with a wealth of fossil, geological, and geochemical evidence. While they acknowledged that the local environment in the vicinity of Aramis ranged from dense woodland/forest to wooded grassland, White et al. (2010:1105) held firm that “in the Middle Awash, Ar. ramidus fossils are confined to the western portion of the sampled Pliocene landscape where the species is associated with woodland to grassy woodland habitat indicators.” More recently, Cerling et al. (2011) investigated the percentages of woody cover, using stable carbon isotopes, in fossil soils from hominin sites in the Awash and Omo-Turkana basins. They concluded (p. 55) that “the combined results from two of the most significant hominid-bearing regions in eastern Africa leave the savanna hypothesis as a viable scenario for explaining the context of earliest bipedalism, as well as potentially later evolutionary innovations within the hominin clade.” As coauthors of White, Ambrose et al. (2009), David DeGusta and I contributed inference of the paleohabitat based on bovid astragali (DeGusta and Vrba 2003), especially of the overwhelmingly most common species which is a tragelaphine antelope, namely, that 4 Ma ago in Aramis, A. ramidus lived in (or at least spent a lot of time in) a woodland habitat. Additional inferences from the bovids suggest that there were wetlands and water bodies nearby (thus, Louchart et al.’s

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2009:66e1, conclusion that the woodlands were “distant from large water bodies” is not one I share) and that there were also grassland areas in the vicinity. Namely, the notion that the Aramis environment was a mosaic of habitats among which A. ramidus preferred the dense woodlands seemed (and still seems) reasonable to me. I wonder whether we may find future support for the hypothesis that, since ape ancestry, Ardipithecus had already diverged toward a measure of broader use of environmental resources and the more generalized ability to live within a vegetationally mosaic environment. The results of Levin et al. (2008) give encouragement to consider this possibility seriously. They concluded (Levin et al. 2008:215) that the spectra of isotopic results from herbivores found in late Miocene Ar. kadabba and early Pliocene Ar. ramidus sites at Gona are most similar to isotopic values from extant herbivores living in bushland and grassland regions and dissimilar to those from herbivores living in closed-canopy forests, montane forests, and high-elevation grasslands. The tooth enamel isotopic data from fossil herbivores make it clear that Ardipithecus at Gona lived among a guild of animals whose diet was dominated by C4 grass, and where there is no record of closed-canopy vegetation.

However, the notion that A. ramidus at Aramis was tied to – or at least strongly preferred – woodlands (albeit situated in a mosaic of habitats) seems to be compatible with what Semaw et al. (2005:301) reported for Ardipithecus ramidus from As Duma, Gona, Ethiopia, that “the Early Pliocene As Duma sediments sample a moderate rainfall woodland and woodland/ grassland.” Kimbel et al. (2006) argued persuasively that A. anamensis and A. afarensis represent parts of an anagenetically evolving lineage or evolutionary species. In Bonnefille’s (2010) broad overview of the large-scale African changes which led to the origin and establishment of this lineage, she noted that the period from 6 to 4 Ma was marked by a progressive increase in tree cover that culminated at 3.9 Ma, during A. anamensis time and before the first appearance of A. afarensis. From their stable isotope-based diet reconstructions of Turkana Basin hominins, Cerling et al. (2013:10501) concluded that “Australopithecus anamensis derived nearly all of its diet from C3 resources . . . [while] by ca. 3.3 Ma, the later Kenyanthropus platyops had a very wide dietary range-from virtually a purely C3 resource-based diet to one dominated by C4 resources.” Bedaso et al. (2013) used carbon and oxygen isotopes of mammalian tooth enamel to reconstruct paleoenvironments of A. afarensis from the Basal Member (ca. 3.8–3.42 Ma) and the Sidi Hakoma Member (3.42–3.24 Ma) of the Hadar Formation in the Middle Pliocene locality of Dikika, Ethiopia. Their results indicate a wide range of foraging strategies, characterized by mixed C3/ C4 to C4-dominated diets in wooded grasslands to open woodlands and that (2013) the middle Pliocene habitat structure at Dikika could be as diverse as open grassland and wooded grassland, and woodland to forest in the Sidi Hakoma Member while wooded grassland, woodland to grassland are evident in the Basal Member. All habitats except closed woodland and forest are persistent through both members; however, the relative proportion of individual habitats changed through time. . . . Thus, the existence of A. afarensis throughout the middle Pliocene indicates either this species might have adapted to a wide range of habitats, or its preferred habitat was not affected by the observed environmental changes.

Kingston and Harrison (2006) used similar methods and reached similar conclusions on a heterogeneous environment for A. afarensis from the Laetoli Beds in Tanzania, much further south. While over the long term many African records show that cooling was accompanied by aridification, it is by no means an invariable association, as expected from the shifting phase relationship between the monsoon and glacial cycles. For example, pollen data from Hadar, Ethiopia, show that “Australopithecus afarensis accommodated to substantial environmental variability between 3.4 and 2.9 Ma ago. A large biome shift, up to 5
C cooling, and a 200- to

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300-mm/year rainfall increase occurred just before 3.3 Ma ago, which is consistent with a global marine delta18O isotopic shift” (Bonnefille et al. 2004:12125). Wood and Richmond (2000) considered the tibia of Australopithecus anamensis (ca. 4.2 Ma; Leakey et al. 1995) the earliest undisputed evidence of bipedalism and in thinking about the ecology of the anamensis-afarensis lineage, recall the debate on selective factors which might have promoted the inception and advancement of bipedalism. Much new evidence now clearly indicates that the relevant lineages since the late Miocene were probably all living in patchy environments, mosaics of habitat types, with patches of dense woodland and forest, light woodland, grassland, and interrupted by barriers such as volcanic deposits and watered areas including seasonally flooded wetlands. Selection pressure for traversing the barriers to reach resources on the other side (which may have been what the A. afarensis individuals who formed the Laetoli footprints were doing; Leakey and Hay 1979), or for foraging in these areas (as in a shallow delta or wetland) might have promoted the onset or, later on, elaboration of bipedality. The notion that wading in shallow water played a part (Niemitz 2000; Verhaegen et al. 2002) seems reasonable given what we know about the palaeoenvironments of many early hominid species. In such a mosaic context some additional previous hypotheses of what caused the adoption of upright posture may apply: carrying, display or warning, new feeding adaptations, control of body temperature, tools, and stone throwing. Reviews are given by McHenry (1982), who thought that hominin bipedalism “could have arisen as an energetically efficient mode of terrestrial locomotion for a small_bodied hominoid moving between arboreal feeding sites” (p. 163), and by Preuschoft (2004). Whatever the combination of selective forces, there is much healthy debate on how the postcranial anatomy of early hominins should be interpreted in terms of function, habitat use, and phylogenetic relationships. Harcourt-Smith and Aiello (2004)) reviewed some of the evidence (including the Laetoli footprints, the AL 288-1 A. afarensis skeleton, postcranial material from Koobi Fora, the Nariokotome H. ergaster skeleton, “Little Foot” [Stw 573] from Sterkfontein, South Africa, fossils of Orrorin, Ardipithecus, and Sahelanthropus) and pointed out the greater diversity in bipedalism (or putative bipedalism) in earlier hominins than previously suspected. In each of their three phylogenetic scenarios (Harcourt-Smith and Aiello 2004: Fig. 4), the postcranial diversification coincides broadly with the 3.0–2.3 Ma period of the largest Pliocene climatic trend. More recently, Haile-Selassie et al. (2012) reported a new hominin foot from a new site WoransoMille in the central Afar, Ethiopia, which further increases the diversity of Pliocene bipedal adaptations. They wrote (p. 565): Here we show that new pedal elements, dated to about 3.4 Ma ago, belong to a species that does not match the contemporaneous Australopithecus afarensis in its morphology and inferred locomotor adaptations, but instead are more similar to the earlier Ardipithecus ramidus in possessing an opposable great toe. This not only indicates the presence of more than one hominin species at the beginning of the Late Pliocene of eastern Africa, but also indicates the persistence of a species with Ar. ramidus-like locomotor adaptation into the Late Pliocene.

There has also been input from South Africa into the debate on diversity and environmental associations of hominin locomotion. Clarke and Tobias (1995) proposed that the foot bones from Sterkfontein Member 2 (STW 573, Little Foot, dated ca. 4 Ma, Partridge et al. 2003, see below) reflect a foot that had not sacrificed arboreal competence or hallucial opposability and that this suggests dense tree cover in the environment. Based on fossil pollen, it has been suggested that the preferred habitat of A. africanus at Makapansgat was subtropical forest and that selective pressures associated with densely vegetated environments played a role in the evolution of bipedalism (Cadman and Rayner 1989; Rayner et al. 1993). Potts (1998a) dubbed this the “forest hypothesis” of bipedal origin. The fossil bovids associated with A. africanus at Makapansgat and Sterkfontein do not suggest a uniform forest, although a mosaic in the greater area which includes dense and Page 23 of 45

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open woodland patches, as well as grassy patches and permanent water, could be consistent (Vrba 1974, 1980, 1987b), which agrees with Reed’s (1997) conclusions. A related insight comes from Lee-Thorp et al.’s (2010) analysis of stable isotopes in the tooth enamel of more than 40 hominin specimens, including A. africanus from Makapansgat and Sterkfontein and Paranthropus robustus from Swartkrans and Kromdraai together spanning ca. 3–1.5 Ma. They concluded (p. 3389) that among all these South African australopithecines including A. africanus and persisting over the entire time range, “these data demonstrate significant contributions to the diet of carbon originally fixed by C4 photosynthesis, consisting of C4 tropical/savannah grasses and certain sedges, and/or animals eating C4 foods. Moreover, high-resolution analysis of tooth enamel reveals strong intratooth variability in many cases, suggesting seasonal-scale dietary shifts.” (See also Sponheimer et al. 2013.) These results suggest spatial variability in vegetation cover and also seasonal variability, rather than predominant forest. Australopithecus afarensis, which persisted in place through major climatic and vegetational variability (e.g., at Hadar, Bonnefille et al. 2004; Bedaso et al. 2013), appears to have been the most generalist of all hominin species up to the Middle Pliocene. It was geographically so widespread that in the past one wondered why it was not also found among the South African hominins. The findings of Partridge et al. (2003) suggested that the anamensis-afarensis lineage may well have been present there as well: based on cosmogenic aluminum-26 and beryllium-10 burial dates of low-lying fossiliferous breccia in the Sterkfontein caves, associated hominin fossils such as skeleton STW 573 date to ca. 4 Ma, the time of the anamensis-afarensis transition in East Africa. An important splitting event in the hominin clade was the one that led to Paranthropus on the one hand and Homo on the other. Several systematic studies have concluded that the characters of A. afarensis are consistent with it being the common ancestor of Paranthropus and Homo and possibly also of one or more additional lineages (e.g., Kimbel 1995; Asfaw et al. 1999). After enduring in apparent equilibrium since ca. 4 Ma, A. afarensis is last recorded just after 3.0 Ma (Kimbel et al. 1994), while its descendants appear variously between 2.7 Ma and 2.3 Ma. Kimbel (1995:435) concluded that “regardless of which phylogenetic hypothesis is more accurate, it is clear that a pulse of speciation occurred in the hominin lineage between 3.0 and ca. 2.7 Ma, producing at least three lineages.” The phylogenetic pattern, of an inferred ancestor ending after 3.0 Ma, with new descendants branching off between that and 2.3 Ma ago, is common in bovids (e.g., Vrba 1995c, 1998a). According to Wood (1995), the first signs of the “hypermasticatory trend” occurred with an advent of Paranthropus aethiopicus ca. 2.6 Ma ago, followed by exaggeration in this trend ca. 2.3 Ma with the FAD of P. boisei, and further lesser modifications to the dentition of this species between 1.9 and 1.7 Ma. Efforts to find out what the robust australopithecines were eating, and where they lived, have been ongoing for a long time. A study which uses functional morphology of mammalian assemblages associated with early hominins to reconstruct their environs by Reed (1997) is particularly useful because it treats the East and South African Plio-Pleistocene fossil assemblages in the same analysis, comparing them with each other and with extant mammalian communities from different habitat types. Reed (1997) concluded that Paranthropus species in East and South Africa lived in both wooded and more open environments, always in habitats that include wetlands. This is compatible with our earlier findings for the relevant South African sites, based on bovid abundances (Vrba 1975) and also on the assemblages as a whole (Brain 1981b), which indicated environs of P. robustus including substantial grassland with wooded patches and permanent water indicated by water-dependent fauna. The notion that robust australopithecines, Paranthropus, were in certain senses specialists was originally proposed by Robinson (1963) based on the dentition of P. robustus. He suggested that the Page 24 of 45

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“crushing, grinding” robust vegetarian specialist lived in a somewhat wetter and more luxuriant environment than did the earlier gracile omnivore A. africanus. Prompted by the bovid evidence of change to more open vegetation in the Paranthropus- and Homo-bearing strata, compared to the earlier South African ones with only A. africanus, the question arose whether the musculature of P. robustus was massive and the molars proportionally so large “because their ‘vegetables’ were of the tough grassland type” (Vrba 1975:302) and whether, in contrast to the more generalized Homo, robust australopithecines may have been more specialized on open and relatively more arid habitats. Based on comparisons of the dental microwear of A. africanus and P. robustus, Grine (1981, 1986) concluded that the latter had probably processed tougher food items. Wood and Strait (2003) did a thorough analysis of the proposal that Paranthropus species were feeding specialists. They concluded that Paranthropus species were most likely ecological generalists (i.e., eurybiomic in being able to make a living in varied environments) and made the novel proposal that (p. 149) “. . . although the masticatory features of Paranthropus are most likely adaptations for consuming hard or gritty foods, they had the effect of broadening, not narrowing, the range of food items consumed.” I accepted their arguments because the acquisition, in response to newly encountered environments, of morphology which can perform a new specialized function but which at the same time permits the retention of functions evolved in the ancestral more uniform environment, is a recurrent theme in the evolution of generalist mammals (e.g., the impala Aepyceros melampus which, from a browsing ancestry, Vrba and Schaller 2000, evolved cranial and dental features which allow mastication of grass and other tough plant matter and also a stomach structure which undergoes reversible seasonal changes, Hofmann 1973, a rare adaptation to varied vegetational environments. As a consequence of these dental and digestive evolutionary advances, the impala is today a consummate herbivore generalist which can subsist in different environments by switching its dietary intake). A number of isotopic analyses of diet and environment have since contributed to illuminating such questions. van der Merwe et al. (2008) did isotopic dietary studies of H. habilis and P. boisei teeth from Olduvai, Tanzania, and discussed how the results compare with previous ones for the South African hominins (see citation of Lee-Thorp et al. 2010, above). They found that the two Olduvai species had very different diets, while, in contrast, the isotopic analyses of the three South African species of early hominins, A. africanus, P. robustus, and Homo sp., showed considerable variation in individual diets but no marked differences between species. For two Olduvai specimens of P. boisei, van der Merwe et al. (2008) found C4 dietary components (77 % and 81 %) that far exceeded those of the South African taxa, including P. robustus, and indeed of all other early hominins for which carbon isotope values were available by that time. They pointed out that the C4 input could come from consuming grasses, some sedges and forbs, and a variety of animals which eat C4 plants and suggested that P. boisei may have fed on papyrus or other C4 species of Cyperaceae which are perennially available near water. A similar study by Cerling et al. (2013) on hominins in the Turkana Basin showed comparable results: by ca. 2 Ma, specimens attributable to the genus Homo provide evidence for a diet with a ca. 65/35 ratio of C3- to C4-based resources, whereas P. boisei had a higher fraction of C4-based diet (ca. 25/75 ratio). Thereafter Homo sp. increased the fraction of C4-based resources in the diet through ca. 1.5 Ma, whereas P. boisei maintained its high dependency on C4-derived resources. Sponheimer et al. (2013:10513) summarized their overview of isotopic evidence of early hominin diet as follows: Before 4 Ma, hominins had diets that were dominated by C3 resources and were, in that sense, similar to extant chimpanzees. By about 3.5 Ma, multiple hominin taxa began incorporating13C-enriched [C4 or crassulacean acid metabolism (CAM)] foods in their diets and had highly variable carbon isotope compositions which are atypical for African mammals. By about 2.5 Ma, Paranthropus in eastern Africa diverged toward C4/CAM specialization

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and occupied an isotopic niche unknown in catarrhine primates, except in the fossil relations of grass-eating geladas (Theropithecus gelada). At the same time, other taxa (e. g., Australopithecus africanus) continued to have highly mixed and varied C4 diets.

Together all the available lines of evidence for species of Paranthropus support a degree of generalism in terms of the patchiness, from open to more wooded, of vegetational environments they inhabited and dietary specialization in the east African species yet not in the southern P. robustus which evidently maintained a more mixed diet in terms of the range of C3- to C4-based resources. All these leave intact the possibility raised by Wood and Strait (2003) that the evolution of the masticatory features of Paranthropus, while allowing consumption of hard or gritty foods, may have broadened their options in the soft-to-hard-and-gritty spectrum of foods, perhaps remaining within the C4/CAM range of plants in the case of P. boisei while ranging across both C3 and C4 resources in the case of the southern P. robustus. There are two species with first appearances after the last record of A. afarensis which have been assigned to Australopithecus. The specific name Australopithecus garhi reflects well the reactions of many (“garhi” means “surprise” in the Afar language) when they found out about the mosaic combination of its anatomical features relative to previously known hominins and the tantalizing associated evidence of cultural advances (which may or may not be the handiwork of this species), all at the hitherto under-represented age of 2.5 Ma (Asfaw et al. 1999; de Heinzelin et al. 1999). The cranial and dental remains, from the Hata beds, Bouri Formation, of Ethiopia’s Middle Awash, led Asfaw et al. to conclude that (p. 629) A. garhi “is descended from Australopithecus afarensis and is a candidate ancestor for early Homo. Contemporary postcranial remains feature a derived humanlike humeral/femoral ratio and an apelike upper arm-to-lower arm ratio.” The abundant vertebrate remains together with the sedimentology indicate an environment (De Heinzelin et al. 1999:626) that was “primarily lake marginal. Alcelaphine bovids are abundant and diverse. All indicators point to a broad featureless margin of a freshwater lake. Minor changes in lake level, which were brought about by fluctuating water input, would probably have maintained broad grassy plains leading to the water’s edge.” With A. garhi are found some of the earliest made stone tools with earliest evidence of the their use to butcher large mammals (p. 625): Spatially associated zooarchaeological remains show that hominins acquired meat and marrow by 2.5 Ma ago and that they are the near contemporary of Oldowan artifacts at nearby Gona. The combined evidence suggests that behavioral changes associated with Lithic technology and enhanced carnivory may have been coincident with the emergence of the Homo clade from Australopithecus afarensis in eastern Africa.

One of the specimens on which unambiguous cutmarks are visible, perhaps made during tongue removal, was identifiable to a new genus and species of a medium-sized bovid (of body size comparable to living hartebeests) in the tribe Alcelaphini, a tribe and bovid size class which are very abundant not only in this Hata Member but also were appearing in greater numbers than before all over Africa near 2.5 Ma. Looking at this earliest evidence of cutmarks made by hominins, in its faunal and environmental context, prompts one to think about the arguments of Owen-Smith (2013) who contrasted the Pleistocene large herbivore faunas of the southern continents and argued (p. 1215) that it was the African “abundance and diversity of medium-sized grazing ruminants unrivalled elsewhere . . . that facilitated the adaptive transition by early hominins from plantgatherers to meat-scavengers.” Only a few years ago, another new species of hominin was announced, Australopithecus sediba, based on two partial skeletons dated 2.0 Ma (by uranium-lead dating combined with paleomagnetic and stratigraphic analysis) from cave deposits at the Malapa site in South Africa (Berger et al. 2010; Dirks et al. 2010; Pickering et al. 2011). Berger et al. (2010:195) argue that A. sediba “is probably

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descended from Australopithecus africanus. Combined craniodental and postcranial evidence demonstrates that this new species shares more derived features with early Homo than any other australopith species and thus might help reveal the ancestor of that genus.” The faunal fossils associated with A. sediba are as yet few, but consistent in chronological and environmental implications with what was found at the other hominin-associated sites thought to date near 2 Ma in the Sterkfontein area. Near the end of the large late Pliocene cooling trend, by ca. 2.6–2.5 Ma, stone tools appeared in several other places (e.g., Semaw et al. 1997) besides the finds from Bouri, together with evidence of butchery already mentioned (de Heinzelin et al. 1999). Hatley and Kappelman (1980) proposed that the climatic change led to this behavioral advance. They showed that a high belowground plant biomass is characteristic of xeric open areas and argued that digging out of such foods, first by hand and later by digging sticks and other tools, evolved as an important feeding strategy of early hominins when the African savanna became more open and arid. Leakey (1971) noted early on that the onset of more expanded tool kits appears to overlap with the climatic change ca. 1.8–1.6 Ma ago. Another milestone dating to this time was proposed by Wood and Richmond (2000): the fact that the mandible and postcanine tooth crowns of H. ergaster (dated ca. 1.9–1.5 Ma) when scaled to body mass are no larger than those of modern humans may reflect the earliest cooking. The late Pliocene and Pleistocene behavioral and cultural advances presumably reflect reorganization and expansion of the brain. The available evidence indicates significant increase in EQ (encephalization quotient) in Homo only over the past 2 Ma, with the largest EQ increase occurring ca. 600–150 Ka ago, according to Holloway (1970, 1972, 1978) and McHenry (1982). Shultz et al. (2012) found punctuated changes in encephalization at approximately 1.8 Ma, 1 Ma, and 100 Ka, noting that brain size change at ca. 100 Ka is coincident with demographic change and the appearance of fully modern language. Holloway et al. (2003) presented evidence that brain reorganization predated brain expansion in hominin evolution. I previously suggested that the encephalization trend in Homo “evolved by progressive prolongation of ancestral, fast, early brain growth phases. It started with the modern ice age, and was fuelled by progressive intensification of cooling minima since then” (Vrba 1996:15). I suspect that we may find future indications that some of the brain modifications which came to characterize Homo – perhaps not increase in EQ but brain reorganization – were promoted by the start of the modern ice age, which would be consistent with the proliferation of stone tool finds in the record by 2.6–2.5 Ma. If the largest EQ increase did occur ca. 600–150 Ka ago (as cited above), it could be related to the end of the mid-Pleistocene strong climatic events ca. 1.0–0.6 Ma ago. Many selective scenarios for encephalization in Homo have been proposed. Falk’s (1980) review included warfare, language, tools and labor, hunting, and heat stress. Gabow (1977) emphasized population structure and culture, McHenry (1982) language, and Brain (2001) our predatory past. Vrba (1985a, 1988, 1989a) proposed that major selection pressures that led to brain and cultural evolution derived from the large-scale changes in climatic mean and amplitude during the Plio-Pleistocene and that culture and the underlying brain modifications in Homo represent adaptation to eurybiomy or “generalist adaptation. Hominine culture is an extension of the common phenomenon in other animals that use behaviour to cope with climatic conditions . . . a special case among animal behaviors that confers an expanded use of environmental resources” (Vrba 1989a:30). As cited above, Potts (1998a) made a similar proposal to explain the brain and behavioral adaptations of Homo. Others have also argued that Homo evolved toward biome generalization (e.g., Wood and Strait 2003). Morphological evidence of a commitment to long-range bipedalism (e.g., long legs, large femoral head) appeared much later, ca. 1.6 Ma, in the postcranial skeleton KNM-WT 15000 Page 27 of 45

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from Nariokotome, West Turkana (Brown et al. 1985, who assigned it to H. erectus; Wood and Richmond 2000 included it in H. ergaster). There is some agreement that the onset of advanced bipedalism in Homo ca. 1.6 Ma ago not only falls during a time of change to more open and seasonally arid landscapes (and near the advent of other novelties in hominin evolution, as noted above) but also makes sense as a selective response to these changes. Potts (1998a) pointed out that the latest Pliocene populations of Homo were increasingly mobile, for example, tool-making behavior involved long-distance transport of stones as far as 10 km. Increased mobility is reflected by the migration out of Africa by 1.8 Ma of a lineage of Homo (if the early date for H. erectus in Java, Indonesia, is correct, Swisher et al. 1994), the first of many subsequent migrations out of Africa which were associated with physical changes (Stringer 1995; Tattersall 1997b; Klein and Edgar 2002; see also Abbate and Sagri 2012, who found that the early to Middle Pleistocene Homo dispersals from Africa to Eurasia were temporally arranged into cycles of four major exodus waves (2.0–1.6 Ma, 1.4–1.2 Ma, 1.0–0.8 Ma, and 0.6–0.1 Ma) controlled by climatic and environmental changes).

Climate in Relation to the Evolution of Ontogeny Heterochrony Pulses: Parallel Developmental Responses to Common Environmental Causes The term heterochrony has been applied to both ecophenotypic and evolutionary changes in the rates and timing of ontogenetic events (Gould 1977). The same kind of heterochronic phenotype, H, commonly appears independently in different parts of a given monophyletic group in association with the same kind of environmental condition, E, and variously as an ecophenotype (i.e., reversible in later generations not faced by E) or as a phenotype, the expression of which is genetically fixed (or at least more constrained under varying conditions). An example is relative reduction of limb length in colder environments, an aspect of Allen’s Rule (Allen 1877: mammalian extremities are reduced relative to body size in cooler climates). Not only the environmental association with E but also the growth patterns tend to be similar between the independent occurrences of such a phenotype H in a clade (e.g., Gould 1977a; Wake and Larson 1987; Vrba 1998b). It appears that certain kinds of heterochrony are more likely than others under particular environmental changes. Each heterochrony response starts off from the ancestral ontogenetic trajectory for that character, and this inheritance imparts limits and direction on what can grow and evolve. To the extent that aspects of ontogeny are shared by common inheritance between related species and across larger taxonomic groups, similar kinds of heterochrony will evolve independently in related lineages faced by the same environmental change. A summary and extension of the above is given in the following two statements (Vrba 2004, 2005): 1. Similar environmental changes elicit similar heterochronies in parallel, potentially in numerous lineages across large phylogenetic groups. Such heterochrony often involves change in body size and may be accompanied by large-scale phenotypic reorganization (Arnold et al. 1989; Vrba 1998b), such that the parallel heterochronies involve concerted evolution of suites of linked characters and “shuffling” among body proportions. 2. At times of widespread climatic change, diverse lineages may show parallel changes in size and in similar kinds of heterochrony associated in time and consistently with the climatic change – a “heterochrony pulse.” “Pulse” here does not imply that the lineages responded in unison in a short time, but only that the events are significantly concentrated in time. Page 28 of 45

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I will mention one particular category of heterochrony, which is associated with body size increase by prolongation of growth and which is a common mammalian response to colder temperatures. It is of special interest in the Plio-Pleistocene context of net global cooling, and it appears to have affected many African mammals including some evolutionary changes in Homo. Cooling and Body Size Increase. Many species with FADs during times of cooling and aridification were larger than their ancestral phenotypes (as cladistically inferred). For example, Vrba (2004) tested H0 that size changes across lineages are randomly distributed in time in the Alcelaphini (wildebeests, etc.) and Reduncini (waterbuck, etc.), which together comprise 63 recorded species over the past 5 Ma with a body weight range of ca. 20–250 kg. The result of significant peaks in size increase 3.0–2.5 Ma and 1.0–0.5 Ma ago, two periods with strong cooling, is consistent with Bergmann’s Rule (1846: larger bodies are associated with colder temperature). While exceptions have been noted, in general, the predictions are upheld in living mammals (Ashton et al. 2000; Meiri and Dayan 2003) including in humans (Baker 1988) and in fossil mammals (Davis 1981; Kurten 1959; Heintz and Garutt 1965). To evaluate the claim that climateassociated heterochrony can involve extensive rearrangement – or “shuffling” – among body proportions, with parallel changes across related lineages, consider the example of Bergmann’s Rule. Bodies can become enlarged by faster growth relative to the plesiomorphic (or directly ancestral) ontogeny, by prolongation of growth time, or by a combination of both, and the influential factors may include temperature change itself or one of the attendant environmental changes (such as seasonal changes in food and water availability, e.g., Guthrie 1984; Barnosky 1986). Such changes in growth mode are expected to result in rearrangement of body proportions. This is especially true of growth prolongation which is prevalent among Bergmann cases for which there are growth studies. For instance, many African tropical ungulates have shorter growth periods to smaller size in warm lowlands, while their close relatives at higher altitudes and/or latitudes grow for longer and become larger. The example of polymorphism in the African buffalo was noted earlier: Syncerus caffer caffer is much larger (up to 810 kg), grows for longer, and lives at higher latitudes and/or altitudes always near grassland, while the smaller and plesiomorphic phenotype S. c. nanus (up to 320 kg) with a shorter growth period lives in warmer, more forested regions. Body Size Increase and “Shuffling” Among Body Proportions. Consider what is expected under the simplest way in which growth prolongation could occur: namely, if all ancestral growth phases for a character become proportionally prolonged (or extended in time by a constant factor) while maintaining the ancestral number of growth phases and the ancestral growth rates for respective phases (Vrba 1998b: Fig. 1). Let us call that simple proportional growth prolongation. Characters in the same organism have differing growth profiles, in terms of growth timing and rate in relation to age and body weight (e.g., Falkner and Tanner 1986), and character growth typically occurs in distinct phases in each of which character change is nonlinear with respect to age (Koops 1986). We can distinguish two major types of heterochrony and associated allometric growth under growth prolongation: (A) in type A heterochrony, characters which grow with net negative allometry with respect to age and body size will become reduced relative to body size in the adult stage of the prolonged descendant ontogeny (even if no other growth parameter changes) and paedomorphic in that the descendant adult resembles the ancestral juvenile. A probable example is the character evolution by Allen’s Rule (Vrba 1998b, 2004) which is upheld in modern humans (Baker 1988). The persistence of Allen’s Rule in modern biology supports the general hypothesis of similar changes in body proportions across lineages, which share inherited developmental responses to common environmental causes. (B) In type B heterochrony, characters which grow with net positive allometry become relatively enlarged. This mode, particularly by prolongation of a positively allometric late growth phase, may be how the hypermorphosed antlers of the giant Irish Page 29 of 45

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elk evolved (Gould 1974) and how exaggerated secondary sexual characters in enlarged bodies commonly evolve (Vrba 1998b). As growth trajectories become prolonged, some characters become relatively reduced and others enlarged, with potentially extensive rearrangement among body proportions and substantial evolutionary novelty (Vrba 1998b: Fig. 1). Type B heterochrony can also result from prolongation of positively allometric early growth, in which case the descendant structure is relatively enlarged and paedomorphic. An example is provided by the enlarged hind-feet of the bipedal, saltatory rodents during times of cooling (section “Climate in Relation to Habitats and Adaptations of Hominins”). If the growth of rodents, the juveniles of which in general have relatively large hind-feet (Hafner and Hafner 1988), is prolonged, a descendant adult with enlarged hind-feet is predicted. Evidence for at least some taxa is consistent with this; e.g., bipedal Kangaroo rats, Dipodomys, which inhabit semiarid to arid regions in North America, have longer growth periods and are hypermorphosed in some characters – yet paedomorphosed in others – relative to the ancestral ontogeny (Hafner and Hafner 1988). As noted earlier, the bipedal forms share suites of characters in a characteristic body plan that is today strongly associated with open, arid habitats and has appeared independently in 24 genera in 8 families (Hafner and Hafner 1988). I do not know how many of the 24 instances of parallel evolution involved growth prolongation. But I suggest that at least some of these appearances of suites of integrated character complexes exemplify coordinated morphological changes, by growth prolongation, within and between lineages in response to a common climatic cause. This case illustrates that evolution by growth prolongation, as it acts on characters with different nonlinear growth profiles in the same body plan, can result in a “shuffling” of body proportions. Substantial novelty in form can result and also in function as in these rodents which can jump to a height that is from 4 to 25 times their body length. I next discuss another example of type B heterochrony with prolongation of positively allometric early growth, namely, encephalization. Heterochrony and Brain Evolution. I applied statistical models for multiphasic growth to data on living human and common chimpanzee brain weights at ages since conception to test the hypothesis that encephalization of the human brain occurred by simple proportional growth prolongation (Vrba 1998b). Specifically, I wanted to know whether prolongation of the fetal growth phases, with strongly positive allometric growth, could account for most of the observed EQ increase. The results supported the hypothesis and imply that gross brain weight increase toward humans required change in only one growth parameter: prolongation of the nonlinear ancestral growth phases. In mammals, in general, simple growth prolongation is predicted to result in encephalization, as all mammalian brains complete a large proportion of their total growth rapidly early in ontogeny (Count 1947; Holt et al. 1975). A positive correlation of EQ with more open, seasonally cooler and drier environments has been noted in diverse mammals (Vrba 2004; e.g., in living African bovids this association is supported by comparison of the habitat preferences of the species with Oboussier’s 1979 results for their EQ variation). This raises the hypothesis that there were past “encephalization pulses,” across many mammalian lineages, in response to cooling over particular intervals (Vrba 1998b).

Conclusion Environmental stimuli have influenced the evolution of hominins and other mammals at the levels of ontogeny, organismal adaptation, and speciation. From a time a few decades ago, when any proposal that climatic change is causally linked to speciation of hominins and other mammals was subjected to much doubt and even derision, there is now substantial convergence of opinion that Page 30 of 45

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such a linkage is real. The climatic influence on hominin adaptation has received most attention, and some agreement has also emerged in this area: successive cooling trends since the late Pliocene were associated with the earliest evidence of – and probably initiated – the “hypermasticatory trend” in Paranthropus (ca. 2.6 Ma) and its later exaggeration ca 2.3 Ma, stone tools and their use to butcher carcasses (ca. 2.6–2.5 Ma), the Early Pleistocene expansion of tool kits, increased mobility by the Plio-Pleistocene interface and commitment to long-range bipedalism (ca. 1.6 Ma) in Homo, and significant brain expansion near 2 Ma and also since 600 Ka ago. There is some consensus that encephalization and culture in Homo represent generalist adaptations which conferred a more flexible and expanded use of resources (Vrba 1985a, 1988, 1989a; Potts 1998a; Wood and Strait 2004). It now seems likely that the masticatory features of Paranthropus, while adaptations for consuming tough or gritty foods, had the effect of broadening, not narrowing, the range of food items consumed and allowed these forms to subsist in varied environments (Wood and Strait 2003). There is less agreement on environmental stimuli of the onset of bipedalism, particularly on whether the vegetational habitats of the earliest bipedal hominins were forest to dense woodland or more open. I discussed why, even if the hominin ancestor and its bipedal descendant species both live(d) in forest, this does not necessarily mean that climatic change did not bring about speciation. Far less work has been done on the issue of environmental causes of hominin speciation. A brief summary of the current status is as follows: in terms of theory, the expectation that allopatric speciation predominates, particularly in hominins and other large mammals, is consistent with the weight of available evidence. It would take special pleading to argue that hominins are exceptions. If allopatric speciation predominates, then so must physical initiation of speciation predominate. Most, and possibly all, of the hominin FADs either coincide with or fall very close to one of the major cooling trends. While taphonomic factors and chance may have contributed to this pattern, it does leave intact the hypothesis of climatic cause of hominin speciation. Also, on cladistic grounds, some speciation events must be closely associated with climatic change in hominins (Kimbel 1995) and other African mammals (Vrba 1995c). Environmental stimuli of ontogenetic evolution have hardly been studied in our field. I discussed the “heterochrony pulse hypothesis”: the generative properties shared among lineages can result not only in coherence of morphological changes but also in a strongly nonrandom timing of heterochrony events, as diverse lineages respond in parallel by similar kinds of heterochrony to the same environmental changes. This has not yet been tested. Of particular interest in the present Late Neogene climatic context is heterochrony involving body enlargement by prolongation of growth, because it is associated with colder (at least seasonally colder) temperatures (Bergmann’s Rule, upheld in modern humans, Baker 1988). I have discussed some examples, including encephalization as a result of growth prolongation, in hominins and other mammals, and suggested that there were past “encephalization pulses,” across many mammalian lineages, in response to cooling trends over particular intervals, such as during the onset and later intensification of the modern ice age. In our field, one sometimes regrets (at least I do) that conclusive answers, such as those that emerge from some experiments of physical scientists, are so difficult to achieve. Hypotheses on the subject of environmental causes of hominin and other biotic evolution are difficult to test because the data come from different subdisciplines, each with its own set of biases, errors, and ambiguities. As a result, debates tend to continue interminably. While we have a long way to go, on the positive side, we can take heart in the simple fact that we are, so to speak, in a “growth industry”: while many aspects of life are deteriorating, the fossil record with its associated geological information is constantly improving. Thus, there is an excellent expectation of decisive future progress on some of the unresolved issues. In my view, the results to date already offer support for the notion that Page 31 of 45

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common rules give qualitative and temporal coherence to the evolutionary responses across many mammalian – including hominin – lineages. These common rules arise from the regularities of physical change and from attributes of organismal ontogenies and phenotypes and species that are widely shared by common inheritance. The evidence implies closer linkages between the physical and biotic dynamics on earth than has traditionally been acknowledged. This perspective contrasts with the neoDarwinian view that selection of small-step random mutations is the vastly predominant evolutionary cause, with the implication that each evolutionary advance is to a larger extent an independent piece of history. Evolution is more rule bound than that, and our evolution is no exception.

Cross-References ▶ Contribution of Stable Light Isotopes . . . ▶ Geological Background of Early Hominid Sites in Africa ▶ Paleoecology: An Adequate Window on the Past? ▶ Patterns of Diversification and Extinction ▶ Species Concepts and Speciation: Facts and Fantasies ▶ The Evolution of the Hominid Brain ▶ The Ontogeny-Phylogeny Nexus in a Nutshell . . . ▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments ▶ The Species and Diversity of Australopiths

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Shackleton NJ (1995) New data on the evolution of Pliocene climatic variability. In: Vrba ES, Denton GH, Partridge TC, Burckle LH (eds) Paleoclimate and evolution with emphasis on human origins. Yale University Press, New Haven, pp 242–248 Shultz S, Nelson E, Dunbar RIM (2012) Hominin cognitive evolution: identifying patterns and processes in the fossil and archaeological record. R Soc Phil Trans Biol Sci 367:2130–2140 Signor PW, Lipps JH (1982) Sampling bias, gradual extinction patterns and catastrophes in the fossil record. Geol Soc Am Spec Pap 190:291–296 Simpson GG (1953) The major features of evolution. Columbia University Press, New York Sinclair ARE (1977) The African Buffalo. University of Chicago Press, Chicago Sponheimer M, Alemseged Z, Cerling TE, Grine FE, Kimbel WH, Leakey MG, Lee-Thorp JA (2013) Isotopic evidence of early hominin diets. Proc Natl Acad Sci U S A 110:10513–10518 Stanley SM (1985) Climatic cooling and Plio-Pleistocene mass extinction of molluscs around margins of the Atlantic. S Afr J Sci 81:266 Stebbins L (1950) Variation and evolution in plants. Columbia University Press, New York Stevens GC (1989) The latitudinal gradient in geographical range: how so many species coexist in the tropics. Am Nat 133:240–256 Stringer CB (1995) The evolution and distribution of later Pleistocene human populations. In: Vrba ES, Denton GH, Partridge TC, Burckle LH (eds) Paleoclimate and evolution with emphasis on human origins. Yale University Press, New Haven, pp 524–531 Summerfield MA (1996) Tectonics, geology, and long-term landscape development. In: Adams WM, Goudie AS, Orme AR (eds) The physical geography of Africa. Oxford University Press, Oxford, pp 1–17 Swisher CC, Curtis GH, Jacob T, Getty AG, Suprijo A (1994) Age of the earliest known hominids in Java, Indonesia. Science 263:1118–1121 Tattersall I (1997a) Paleoanthropology and evolutionary theory. In: Ember CR, Ember M, Peregrine PN (eds) Research frontiers in anthropology, vol 3. Prentice Hall, Englewood Cliffs, pp 325–342 Tattersall I (1997b) Out of Africa again and again? Sci Am 276:46–53 Tattersall I (1999) Rethinking human evolution. Scientific American January:56–62 Tattersall I (2000) Once we were not alone. Archaeology July/August:22–25 van Dam J, Aziz HA, Sierra MAA, Hilgen FJ, Ostende LWVDH, Lourens LJ, Mein P (2006) Longperiod astronomical forcing of mammal turnover. Nature 443:687–691 van der Merwe NJ, Masao FT, Bamford MK (2008) Isotopic evidence for contrasting diets of early hominins Homo habilis and Australopithecus boisei of Tanzania. S Afr J Sci 104:153–155 Van Valen L (1973) A new evolutionary law. J Evol Theory 1:1–30 Verhaegen M, Puech PF, Munro S (2002) Aquarboreal ancestors? Trends Ecol Evol 17:212–217 Vrba ES (1974) Chronological and ecological implications of the fossil Bovidae at the Sterkfontein Australopithecine Site. Nature 256:19–23 Vrba ES (1975) Some evidence of chronology and palaeoecology of Sterkfontein, Swartkrans and Kromdraai from the fossil Bovidae. Nature 254:301–304 Vrba ES (1980) Evolution, species and fossils: how does life evolve? S Afr J Sci 76:61–84 Vrba ES (1985a) Ecological and adaptive changes associated with early hominid evolution. In: Delson E (ed) Ancestors: the hard evidence. Alan R Liss, New York, pp 63–71 Vrba ES (1985b) Environment and evolution: alternative causes of the temporal distribution of evolutionary events. S Afr J Sci 81:229–236 Vrba ES (1987a) Ecology in relation to speciation rates: some case histories of Miocene_Recent mammal clades. Evol Ecol 1:283–300 Page 41 of 45

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Vrba ES (1987b) A revision of the Bovini (Bovidae) and a preliminary revised checklist of Bovidae from Makapansgat. Palaeontol Afr 26:33–46 Vrba ES (1988) Late Pliocene climatic events and hominid evolution. In: Grine FE (ed) The evolutionary history of the Robust Australopithecines. Aldine Publishing Company, New York, pp 405–426 Vrba ES (1989a) The environmental context of the evolution of early hominids and their culture. In: Bonnichsen R, Sorg MH (eds) Bone modification. Publication of the Center for the Study of the First Americans, Orono, pp 27–42 Vrba ES (1989b) Levels of selection and sorting, with special reference to the species level. Oxf Surv Evol Biol 6:111–168 Vrba ES (1992) Mammals as a key to evolutionary theory. J Mammal 73:1–28 Vrba ES (1995a) Species as habitat specific, complex systems. In: Masters JC, Lambert DM, Spencer HG (eds) The recognition of species: speciation and the recognition concept. Johns Hopkins University Press, Baltimore, pp 3–44 Vrba ES (1995b) On the connections between paleoclimate and evolution. In: Vrba ES, Denton GH, Partridge TC, Burckle LH (eds) Paleoclimate and evolution with emphasis on human origins. Yale University Press, New Haven, pp 24–45 Vrba ES (1995c) The fossil record of African antelopes (Mammalia, Bovidae) in relation to human evolution and paleoclimate. In: Vrba ES, Denton GH, Partridge TC, Burckle LH (eds) Paleoclimate and evolution with emphasis on human origins. Yale University Press, New Haven, pp 385–424 Vrba ES (1996) Climate, heterochrony, and human evolution. J Anthropol Res 52:1–28 Vrba ES (1998a) (Monograph) New fossils of Alcelaphini and Caprinae (Bovidae, Mammalia) from Awash, Ethiopia, and phylogenetic analysis of Alcelaphini. Palaeontol Afr 34:127–198 Vrba ES (1998b) Multiphasic growth models and the evolution of prolonged growth exemplified by human brain evolution. J Theor Biol 190:227–239 Vrba ES (2000) Major features of neogene mammalian evolution in Africa. In: Partridge TC, Maud R (eds) Cenozoic geology of Southern Africa. Oxford University Press, Oxford, pp 277–304 Vrba ES (2004) Ecology, evolution, and development: perspectives from the fossil record. In: Hall BK, Pearson RD, Muller GB (eds) Environment, development, and evolution. Massachusetts Institute of Technology Press, Cambridge, pp 85–105 Vrba ES (2005) Mass turnover and heterochrony events in response to physical change. Paleobiology 31:157–174 Vrba ES, DeGusta D (2004) Do species populations really start small? New perspectives from the Late Neogene fossil record of African mammals. Phil Trans R Soc Lond B 359:285–293 Vrba ES, Gould SJ (1986) The hierarchical expansion of sorting and selection: sorting and selection cannot be equated. Paleobiology 12:217–228 Vrba ES, Schaller GB (2000) Phylogeny of Bovidae (Mammalia) based on behavior, glands and skull morphology. In: Vrba ES, Schaller GB (eds) Antelopes, deer, and relatives: fossil record, behavioral ecology, systematics, and conservation. Yale University Press, New Haven, pp 203–222 Vrba ES, Denton GH, Partridge TC, Burckle LH (eds) (1995) Paleoclimate and evolution with emphasis on human origins. Yale University Press, New Haven Wake DB, Larson A (1987) Multidimensional analysis of an evolutionary lineage. Science 238:42–48 Washburn SL (1960) Tools and human evolution. Sci Am 203:63–75

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Wesselman HB (1995) Of mice and almost-men. In: Vrba ES, Denton GH, Partridge TC, Burckle LH (eds) Paleoclimate and evolution with emphasis on human origins. Yale University Press, New Haven, pp 356–368 West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New York White TD, Suwa G, Asfaw B (1994) Australopithecus ramidus, a new species of early hominid from Aramis, Ethiopia. Nature 371:306–312 White TD, Ambrose SH, Suwa G, Su DF, DeGusta D, Bernor RL, Boisserie J-R (2009) Macrovertebrate Paleontology and the Pliocene Habitat of Ardipithecus ramidus. Science 326:87–93 White TD, Asfaw B, Beyene Y, Haile-Selassie Y, Lovejoy CO, Suwa G, WoldeGabriel G (2009) Ardipithecus ramidus and the paleobiology of early hominids. Science 326:75–86 White TD, Ambrose SH, Suwa G, WoldeGabriel G (2010) Response to comment on the paleoenvironment of Ardipithecus ramidus. Science 328:1105 Williams GC (1966) Adaptation and natural selection. Princeton University Press, Princeton WoldeGabriel G, White TD, Suwa G, Renne P, de Heinzelin J, Hart WK, Heiken G (1994) Ecological and temporal placement of early Pliocene hominids at Aramis, Ethiopia. Nature 371:330–333 WoldeGabriel G, Ambrose SH, Barboni D, Bonnefille R, Bremond L, Currie B, DeGusta D (2009) The geological, isotopic, botanical, invertebrate, and lower vertebrate surroundings of Ardipithecus ramidus. Science 326:65. doi:10.1126/science.1175817 Wood B (1995) Evolution of the early hominin masticatory system: mechanisms, events, and triggers. In: Vrba ES, Denton GH, Partridge TC, Burckle LH (eds) Paleoclimate and evolution with emphasis on human origins. Yale University Press, New Haven, pp 438–448 Wood B, Leakey M (2011) The Omo-Turkana Basin fossil hominins and their contribution to our understanding of human evolution in Africa. Evol Anthropol 20:264–292 Wood B, Richmond BG (2000) Human evolution: taxonomy and paleobiology. J Anat 197:19–60 Wood B, Strait D (2003) Patterns of resource use in early Homo and Paranthropus. J Hum Evol 46:119–162 Wright S (1932) The roles of mutation, inbreeding, crossbreeding, and a selection in evolution. Proc VIth Int Congr Genet 1:356–366 Wright S (1967) Comments on the preliminary working papers of Eden and Waddington. In: Moorehead PS, Kaplan MM (eds) Mathematical challenges to the Neo-Darwinian theory of evolution. The Wistar Institute Symposium No 5 Philadelphia, pp 117–120

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

Index Terms: Adaptation_9–10, 31 Adaptation environmental change and adaptation_9 Adaptation hominin adaptation_10, 31 Bergmann’s Rule_29 Brain_27, 30 Brain evolution_30 Brain growth prolongation_30 Brain size_27 Climatic change_8, 10 Climatic change as driver of evolution_8 Climatic change climatic variability_10 Coordinated Stasis Hypothesis_7 Delta_16 Delta inland rift margin associated deltas in relation to hominid evolution_16 Encephalization_27 Encephalization EQ in relation to climate_27 Forest hypothesis of bipedal origin_23 Generalists_4–6 Generalists and climatic variability_5 Generalists biomic generalist_5 Generalists biomic generalists_6 Generalists definition_4 Growth prolongation_29 Growth prolongation importance in hominin evolution_29 Habitat_3, 5, 8 Habitat definition_3 Habitat specificity_8 Habitat theory_5

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_47-4 # Springer-Verlag Berlin Heidelberg 2013

Heterochrony_28 Heterochrony definition_28 Heterochrony pulses_28 long-term, continuous vicariance_14 Macroevolution_1 mode_10 Ontogeny_1, 28 Physical change_3 Physical change definition_3 Physical change importance in initiating speciation and extinction_3 Punctuated equilibria_4 Savanna hypothesis_2, 11 Savanna hypothes_10 Selection_4 Selection in variable environments_4 Specialists_4 Specialists biomic specialists_4 Specialists ecological_4 Speciation_3–4 Speciation allopatric_3 Speciation recognition concept of_4 Species_2–3 Species definition_2 Species turnover_3 Turkana basins_11, 21 Turkana basins evidence for climate change in_11, 21 Turnover_5 Turnover turnover pulse hypothesis_5 Vicariance_3, 10 Vicariance definition_3 Vicariance importance of long-term vicariance as cause of speciation_10

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_48-3 # Springer-Verlag Berlin Heidelberg 2013

The Origins of Bipedal Locomotion William E. H. Harcourt-Smith* Department of Anthropology, Lehman College CUNY, Bronx, NY, USA Department of Anthropology, The Graduate Center CUNY, New York, NY, USA Department of Vertebrate Paleontology, American Museum of Natural History, New York, NY, USA

Abstract Bipedalism is a highly specialized and unusual form of primate locomotion that is found today only in modern humans. The majority of extinct taxa within the Hominini were bipedal, but the degree to which they were bipedal remains the subject of considerable debate. The significant discoveries of fossil hominin that remains in the last 40 years have resulted in this debate becoming increasingly focused on how bipedal certain fossil taxa were, rather than on the overall process. Although the early hominin fossil record remains poor, evidence points to at least two distinct adaptive shifts. First, there was a shift to habitual bipedalism, as typified by certain members of Australopithecus, but possibly including earlier genera such as Ardipithecus and Orrorin. Such taxa were bipedal, but also retained a number of significant adaptations to arboreal climbing. The second shift was to fully obligate bipedalism and coincides with the emergence of the genus Homo. By the Early Pleistocene, certain members of Homo had acquired a postcranial skeleton indicating fully humanlike striding bipedalism. The final part of this chapter reviews why bipedalism was selected for. There have been many theoretical explanations, and the most robust remain those linked to the emergence of more varied habitats. Such an environmental shift would have involved strong selection for new behavioral strategies most likely linked to the efficient procurement of food.

Introduction Bipedal locomotion sets modern humans apart from all other living primates. We are the only obligate bipeds among well over 200 extant primate species. It therefore stands to reason that this unusual and highly derived form of locomotion has attracted much attention from those who study human evolution. Current evidence points to anatomical traits strongly associated with bipedalism relatively deep in the hominin lineage (Ward et al. 2001) and well before the advent of other “traditional” human traits such as larger brains and tool use. This chapter reviews the current state of thinking on this unique form of primate locomotion. In order to understand the origins of hominin bipedalism, one first has to understand the mechanisms that make it such an efficient form of locomotion in modern humans. In the first section of this chapter, I will briefly explore the nature of the modern human walking cycle and the associated anatomical traits that facilitate it. I will then explore the fossil evidence for the origins of bipedalism and speculate on the likely locomotor behaviors that preceded it. Finally I will discuss some of the theories surrounding why bipedal locomotion was selected for.

*Email: [email protected] Page 1 of 36

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_48-3 # Springer-Verlag Berlin Heidelberg 2013

Locomotor Differences Between Modern Humans and Great Apes Modern humans are fully obligate bipeds. After the first few years of life, bipedality is the sole form of locomotion in all healthy individuals. By comparison, the great apes do not have any one form of specialized locomotion. Pongo is almost exclusively arboreal, but its locomotor behavior is taken up by clambering, vertical climbing, brachiation, terrestrial fist-walking, arboreal quadrupedalism, and even some above-branch assisted bipedalism, although orangutans are best known to have a predilection for suspensory postures (Tuttle 1968; Thorpe and Crompton 2005; Thorpe et al. 2007). Clambering, which accounts for over 50 % of observed locomotor behavior, mainly consists of forelimb suspension and hindlimb support and suspension (Tuttle 1968; Cant 1987). In nearly all respects Pongo can be considered to be an arboreal specialist. The most important aspect of the African apes is that, unlike Pongo and modern humans, their specialization lies not in their tendency to be either arboreal or terrestrial specialists but rather on having a mosaic of different locomotor modes that suit different environments and situations. Field observations have shown that all three African ape taxa spend considerable time in both the trees and on the ground. The principal form of terrestrial locomotion is fast and slow knuckle-walking, where the legs do most of the propulsive work but a significant degree of body weight is borne by the upper limbs through the knuckles (Tuttle 1970). African apes spend a small degree of time walking bipedally, but only for relatively short periods of time (Tuttle 1970; Hunt 1994). Pan also spends a proportion of its time standing bipedally, mainly to collect fruit in tall bushes, but it is important to note that, even when doing so, individuals are partially supporting themselves with their upper limbs, which are grasping onto branches (Hunt 1994; Doran and Hunt 1995). When in the trees, Pan troglodytes has a particular predilection for using knuckle-walking to move along large branches (Tuttle 1970).

The Walking Cycle The modern human walking cycle is characterized by two distinct phases: the stance phase, when the leg is on the ground, and the swing phase, when it is off the ground. The stance phase begins with the foot striking the ground, known as heel-strike. The knee is fully extended and the foot dorsiflexed, which results in the heel-striking the ground well before the rest of the foot. The foot then plantar flexes, and typically force is transmitted through to the substrate along its lateral border. The point when the body is directly over the weight-bearing foot is known as the midstance phase. The body then carries its forward momentum over the leg, at which point force moves medially over to the ball of the foot. At this point, strong muscular contraction of the plantar-flexors results in the ball of the foot pushing against the ground and eventually lifting away from it as the body continues to move forward. This action finishes with a final push-off of the big toe, known as toe-off. The leg is now off the ground and in the swing phase, with the knee and hip both bent so as to keep the leg off the ground as it swings forward to make the next heel-strike. When chimpanzees walk bipedally, there are considerable differences (Aiello and Dean 1990). The knees and hips remain bent throughout the stance phase, and the foot is less dorsiflexed at heelstrike. This results in a gait that is an awkward “shuffling” movement, with marked mediolateral swaying of the body from step to step, that is often referred to as a “bent-knee, bent-hip” (BKBH) gait. Heel-strike itself is at best weak and is often almost immediately followed by much of the rest of the foot making contact with the ground. There is little in the way of the lateral to medial shift in force transmission to the substrate during the late stance phase, and often three or more toes leave the ground at the same time (Elftman and Manter 1935).

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_48-3 # Springer-Verlag Berlin Heidelberg 2013

Associated Anatomical Differences Between Humans and Great Apes A large number of anatomical traits are functionally related to bipedal locomotion, and it is the combination of these traits that allows this to be the sole form of locomotion in modern humans. Naturally it is sometimes hard to determine which traits specifically facilitate bipedal locomotion and which are more a result of it, but in terms of determining the locomotor affinities of fossil remains, it is fair to assume that, either way, many of these traits certainly indicate bipedal locomotion to a lesser or greater degree. Table 1 summarizes the major anatomical features associated with human bipedal locomotion, but a number of them warrant further discussion. In some cases, where particular traits relate to particular fossil specimens, there is further discussion in section “Fossil Evidence.” Some of the most radical morphological adaptations in the human skeleton that relate to bipedalism are found within the pelvis and lower limb. Compared to apes, the entire lower limb complex in humans has become highly remodeled to cope with the intricate dynamics of balancing an upright trunk while efficiently moving the body forward. Balance is a particularly important factor as at any point during the walking cycle, only one limb is actually in contact with the ground and has to bear the entire weight of the body and balance it accordingly. The minimizing of mediolateral swaying of the body during walking is therefore critical, as it acts to stabilize the body over the supporting leg and to reduce energy expenditure. Consequently, many of the traits associated with bipedal locomotion relate to two major factors: balancing the body as a whole and keeping the downward transmission of force as close to the midline of the body as possible. In the skull there are two main osteological features related to bipedalism in modern humans. The semicircular canals have a larger vertical canal, which is thought to relate to more complex bipedal behaviors such as running (Spoor et al. 1994). The foramen magnum is also more anteriorly situated and horizontally orientated. This is a reflection of the more vertical positioning of the spine. Anterior positioning of the foramen magnum has recently been shown to relate to bipedalism in several lineages of mammals that have independently become bipedal (Russo and Kirk 2013). Below the neck, the spine of modern humans has a distinct “S” shape, caused by marked lordosis in the lumbar region, which helps to bring the center of the trunk’s mass anteriorly (Aiello and Dean 1990; Fleagle 1999). The lower limb is considerably longer in modern humans than in great apes. H. sapiens has a low intermembral index (72), whereas for Pan (103–106), Gorilla (115), and Pongo (139) it is far higher, reflecting their relatively shorter lower limbs and longer upper limbs. The longer lower limb in humans directly facilitates a longer stride length. The modern human pelvis is very different in shape to that of all other primates, including the great apes. The iliac blades are short and wide, the ischium extends posteriorly, and the sacrum is relatively wide. These features greatly facilitate support of the upright trunk, place the trunk’s center of gravity closer to the hip joint, and allow the lesser gluteal muscles to be positioned at the side of the pelvis (Napier 1967; Aiello and Dean 1990). This last feature is important, as contraction of these muscles during walking tilts the trunk toward the leg in contact with the ground, providing greater stability and balance. Humans also have a large acetabulum to accommodate a large femoral head, reflecting the relative increase in body weight passing through the hip during locomotion. The modern human femur has a valgus bicondylar angle, resulting in the knee being situated far closer to the midline of the body than the femoral head is. This greatly reduces the lateral deviation of body weight during walking and is argued by many to be an important feature related to habitual bipedal locomotion. However, modern humans who are unable to walk from birth do not develop a valgus bicondylar angle (Tardieu and Trinkaus 1994), and so this trait is best considered as ontogenetic even though its presence indicates habitual bipedal behavior.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_48-3 # Springer-Verlag Berlin Heidelberg 2013

Table 1 Some of the important anatomical features specifically related to bipedal locomotion in modern humans. Some descriptions adapted from Aiello and Dean (1990) Trait Foramen magnum orientation Shape of spine

Homo sapiens Perpendicular to orbital plane S curve with lumbar lordosis Intermembral index Low (72) Size of vertebral bodies Larger, especially L1-5 Shape of iliac blades Short, wide, and curved Orientation of iliac blades Mediolaterally Relative distance from hip Small to sacroiliac joints Size of acetabulum Large Anterior inferior iliac Present spine (AIIS)

African apes More vertically inclined C curve with no lumbar lordosis High (103–115) Smaller

Femoral head size Cortical bone distribution in femoral neck Bicondylar angle of femur Relative lengths of articular surfaces of femoral condyles Inclination of tibial trochlear surface Plantar tuberosity on calcaneus Longitudinal arches in foot

Large Thicker inferiorly

Small Even all around

Increase in weight transfer through hip joint Attachment site for strong iliofemoral ligament – helps maintain balance by preventing hyperextension of thigh Increase in weight transfer through hip joint Increase in weight transfer through hip joint

Valgus Similar in length

Absent/varus Lateral condyle shorter

Placement of lower leg closer to midline of body Aids medial rotation of femur and locking of knee joint at heel-strike

Perpendicular to long axis of tibia Two

More laterally inclined One

Allows perpendicular passage of leg over foot

Hallux opposability Relative tarsus length Relative lengths of rays II–V Metatarsal robusticity pattern Phalangeal curvature

Functional significance in H. sapiens Related to vertical positioning of spine More efficient balance and support of upright trunk Longer stride lengths Increased load of vertical trunk

Long, narrow, Support for vertical trunk and flat Anteroposteriorly Support for vertical trunk Large More efficient transfer of weight from spine to hip Small Absent/weak

Two present – one Absent medial and one lateral Absent Present

Facilitates stable heel-strike Acts as “shock absorber” and maintains structural rigidity in foot throughout stance phase

Facilitation of efficient toe-off and loss of arboreal grasp Long Short Increases power arm length in foot – leads to more efficient leverage in foot Short Long Decreases level arm length in foot – leads to more efficient leverage in foot 1 > 5 > 4 > 3 > 2 1 > 3 > 2 > 4 > 5 Reflects increased transfer of weight along lateral edge of foot Flat Curved Loss of arboreal grasp

The human knee has the unique ability to lock when in full extension, which greatly facilitates upright walking by keeping the leg straight and enabling the efficient downward passage of the body’s weight through to the ankle. This locking action is facilitated in humans by having long femoral condyles that are the same length as each other (in Pan they are shorter, and lateral condyle is shorter than the medial) and different femoral attachment sites for the posterior cruciate ligament (Aiello and Dean 1990). The distal tibia has a particularly important feature linked to bipedal

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locomotion worth noting. The talar articular surface is orientated perpendicular to the long axis of the bone, resulting in a less arcuate passage of the leg over the foot (Latimer et al. 1987). This allows more efficient weight transfer through to the foot. The modern human foot is particularly specialized for the requirements of bipedal locomotion. The African ape foot can be considered a grasping organ with some terrestrial adaptations, whereas that of humans is essentially a propulsive platform. Modern humans are the only living primates to have lost the ability to oppose the hallux, which is in line with the remaining toes. Human toes are relatively short and straight, and the tarsus relatively long, with an elongated calcaneal tuberosity. This allows for a more efficient lever-arm to power-arm ratio, which facilitates efficient propulsion during the stance phase. A combination of bony architecture and strong plantar ligaments results in the human foot being arched longitudinally on both the medial and lateral sides. By comparison the ape foot is weight-bearing through the midfoot, and this is reflected in the enlarged medial tuberosity on the navicular. This longitudinal arching combined with strong plantar ligaments and the unique locking morphology of the calcaneocuboid joint allows the human foot to not only act as an efficient shock absorber but also stay rigid during weight transfer to the ground.

Fossil Evidence The precise number and nature of derived traits characterizing stem hominins is increasingly difficult to determine and likely to remain so. It has recently been pointed out that, in its entirety, bipedality requires a combination of many complex anatomical traits and so cannot necessarily be classed as a dichotomous character (Haile-Selassie et al. 2004). However, it is reasonable to assume that strong evidence of bipedal locomotion is key in determining whether fossil material warrants inclusion within the hominin clade. Perhaps the best way to consider such evidence is to ask whether fossil hominin material indicates habitual or obligate bipedalism, rather than merely occasional bipedalism, which we see in most extant species of great apes (see Rose 1991). Clear evidence of a shift from occasional to habitual bipedalism is important when considering early hominin remains, as is the shift from habitual to obligate bipedalism when considering later hominin remains. In that context, when considering the hominin fossil record, this chapter will consider occasional bipeds as those animals with a bipedal component of their locomotor repertoire similar to that of modern-day chimpanzees. By contrast, habitual bipeds are considered those taxa that had a significantly increased bipedal component but were by no means exclusively bipedal and would have retained an arboreal component to their locomotor repertoire. Obligate bipeds are taxa that were exclusively bipedal and had lost all other forms of terrestrial and arboreal locomotor behaviors.

Precursors of Bipedalism There is a significant literature on the likely locomotor mode that directly preceded hominin bipedalism (see reviews by Richmond et al. 2001; Harcourt-Smith and Aiello 2004). Early models, in the absence of fossil evidence, relied heavily on observed extant primate locomotor behaviors and phylogenetic hypotheses. Arguably, the prevailing view was that a brachiating, hylobatid-like ancestor evolved into a larger-bodied African apelike ancestor capable of orthograde climbing and terrestrial knuckle-walking, which in turn evolved into a bipedal hominin (e.g. Keith 1903, 1923; Gregory 1916, 1928; Morton 1924, 1935). Minor variants of these models existed between authors, with Morton (1924, 1935) arguing for a more terrestrial “gorilloid” prehuman locomotor mode,

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while Gregory (1916, 1927) and Keith (1903, 1923) favored a more “troglodytian” hominin precursor. Others argued for a very deep tarsoid ancestry for humans and bipedalism (Wood Jones 1916, 1929) or an arboreal quadruped ancestry of monkey-like above-branch locomotion (Straus 1949). Despite the elegance of some of these early models, the central factor in understanding the evolution of bipedalism lies in the reconstruction of Late Miocene large hominoid locomotor behaviors. The advent of fossil evidence and molecular dating methods has effectively precluded some of these early theories from being likely. Based on molecular data, the last common ancestor of modern humans and chimpanzees is likely to have lived between 5 and 9 Ma (Gagneux and Varki 2000; Page and Goodman 2001; Springer et al. 2012; Steiper and Seiffert 2012; Schrago and Voloch 2013), and most Miocene hominoid remains do not show a strong adaptation to brachiation (e.g., Napier and Davis 1959; Avis 1962; Rose 1991; Moyà-Solà and Kohler 1996), although the hylobatian model is still argued by some (Tuttle 1974, 1975, 1981). In place of these earlier theories, a number of alternatives can be found in the recent literature. Perhaps the best-known recent theory today is the suggested knuckle-walking ancestry for hominins (Washburn 1967; Richmond and Strait 2000; Richmond et al. 2001), which draws heavily on the specialized knuckle-walking behavior of chimpanzees and gorillas as a model and argues for a retention of traits associated with knuckle-walking in the wrists of Au. afarensis and A. anamensis (Richmond and Strait 2000). However, this theory is also disputed by others on both paleontological and neontological grounds (e.g., Tuttle and Basmajian 1974; Dainton 1991; Lovejoy et al. 2001; Kivell and Schmitt 2009). While certain Middle and Late Miocene hominoid remains show an increased capacity for terrestriality, no large fossil hominoid taxa from this time-range show adaptations for knucklewalking behavior (Stringer and Andrews 2005). Recent work on extant primates has also shown that several traditionally accepted knuckle-walking features are not always found in Pan and Gorilla and that both genera may knuckle-walk in biomechanically distinct ways (Kivell and Schmitt 2009). This leads to the possibility that knuckle-walking may have evolved independently within hominines, although Williams (2010) argues that this may have been unlikely due to the lack of highly integrated knuckle-walking morphologies in Pan and Gorilla. Alternate contemporary theories include those suggesting an arboreal climbing ancestor (either large bodied or small bodied) (e.g., Fleagle et al. 1981; Tuttle and Basmajian 1974; Tuttle 1975, 1981; Stern 1975; Prost 1980; Hunt 1996), a terrestrial quadruped ancestor (Gebo 1992, 1996; Sarmiento 1994, 1998), a Pongo-like pronograde clambering ancestor (Crompton et al. 2003; Thorpe and Crompton 2005; Thorpe et al. 2007), and even an ancestor that practiced a type of terrestrial “tripedalism” with one limb always free to carry objects (Kelly 2001). A universal theme that links both the older and the more recent hypotheses is the choice of a single specific locomotor mode as the dominant “precursor” to hominin bipedalism. As Rose (1991) points out, most primates apart from humans usually use several different types of locomotor activity as part of their daily locomotor repertoire. Within the hominoid clade, Pongo and particularly Hylobates are traditionally considered rather derived and specialized in their locomotor behavior, while Pan and Gorilla are considered more generalized. However, the great specialization of Pan and Gorilla in fact lies in that they have a particularly mosaic and versatile locomotor repertoire, especially in the case of the smaller-bodied Pan. Both genera regularly engage in terrestrial knucklewalking, occasional bipedalism, vertical climbing, and orthograde clambering as part of their daily activities. It is quite possible that some of these behaviors, for instance, knuckle-walking, may have been independently acquired in Pan and Gorilla (e.g., Begun 2004; Kivell and Schmitt 2009). Their locomotor behavior and associated anatomy, however, combined with our current knowledge of the Middle to Late Miocene fossil record, suggest that the immediate precursors to the very first Page 6 of 36

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hominins are likely to have been rather generalized hominoids (McHenry 2002) capable of a suite of different locomotor behaviors, although perhaps with an emphasis on arboreal, predominantly orthograde locomotion (Almécija et al. 2013). In that context, it is perhaps rather limited to single out one particular locomotor mode as the likely “precursor” to habitual hominin bipedalism.

Evidence for Habitual Bipedalism Outside the Hominin Clade Although there is little current evidence to suggest that fossil hominoid taxa existing prior to the Hominini–Panini split had any significant degree of bipedalism in their locomotor repertoires, the possible locomotor affinities of one specific taxon are worth noting. There has been the suggestion that the late Miocene European hominoid, Oreopithecus bambolii, was partially bipedal (e.g., Straus 1957, 1962; Kummer 1965; H€ urzeler 1968; Köhler and Moyà Solà 1997; Rook et al. 1999). However, that assertion remains highly controversial. Although the iliac blades of Oreopithecus are reduced in length, it also has a suite of postcranial features that indicate adaptations to vertical climbing and forelimb suspension, including longer forelimbs than hindlimbs, a flexible shoulder joint, a strong grasping foot, and a lumbosacral region that is incompatible with bipedality (Harrison 1987, 1991; Russo and Shapiro 2013).

Earliest Hominin Evidence The earliest fossil evidence for potential hominin bipedalism comes from recently discovered Late Miocene cranial remains from Chad, dated to almost 7 Ma and assigned to Sahelanthropus tchadensis (Brunet et al. 2002). Virtual reconstruction of the distorted TM266 cranium is argued to show a foramen magnum that is more anteriorly positioned than in Pan and Gorilla and, more importantly, orientated almost perpendicular to the orbital plane (Zollikofer et al. 2005). This is a trait shared by modern humans and australopiths and indicates a more vertically orientated spinal column that is associated with bipedal locomotion. Currently there are no known postcranial remains of S. tchadensis, precluding any further speculation on its locomotor behavior. Fossil remains from the Lukeino formation in Kenya currently assigned to the putative hominin taxon Orrorin tugenensis (Senut et al. 2001) are also argued to indicate bipedality. The material is dated to between 5.7 and 6 Ma (Pickford and Senut 2001; Sawada et al. 2002), and it is reported that there are anatomical features on the BAR 1002’00 proximal femur that indicate habitual bipedal locomotion. The cortical bone of the inferior section of the femoral neck is argued to be relatively thick, and there is an “intertrochanteric groove” for the tendon of the obturator externus muscle on the posterior surface (Pickford et al. 2002; Galik et al. 2004). Thick cortical bone on the inferior section of the femoral neck is argued by some to imply habitual bipedalism (e.g., Pauwels 1980; Lovejoy 1988; Ohman et al. 1997), but others have noted that similar patterns of cortical distribution are found in many other primate species and that only apes and atelines differ in having relatively even distribution around the whole neck (Stern and Susman 1991; Rafferty 1998; Stern 2000). There is also debate as to whether the presence of the obturator externus tendon groove is reliable in inferring bipedalism. This feature, originally described by Day (1969), is argued to imply regular full extension of the thigh during bipedal locomotion (Day 1969; Robinson 1972; Lovejoy 1978). Others argue that it is not a diagnostic trait of habitual bipedalism (e.g., Stern and Susman 1991) and that it can even be found in quadrupedal cercopithecoids (Bacon 1997). Most recently Lovejoy et al. (2002) posit that while the trait is completely absent in large samples of Pan and Gorilla and present in australopiths and 60 % of modern humans, it does not specifically imply bipedality, but merely habitual extension of the femur. Despite these somewhat contradictory lines of evidence, more recent metrical analyses of BAR 1002’00 (Richmond and Jungers 2008; Almécija et al. 2013) seem to confirm its hominin status. These studies have found that the femur is strikingly similar to Page 7 of 36

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that of later australopiths such as Au. afarensis, indicating that Orrorin was well adapted to habitual (but not obligate) bipedalism. However, it is also clear that this taxon retained adaptations consistent with arboreality. The upper limb of O. tugenensis includes a curved proximal manual phalanx and a humeral shaft with a straight lateral crest for m. brachioradialis (Senut et al. 2001; Richmond and Jungers 2008), which are both seen as adaptations reflecting arboreal locomotor behavior (Senut 1981a, b, 1989; Stern and Susman 1983, 1991). The best-known hominin remains from the Late Miocene/Early Pliocene that indicate bipedalism belong to the genus Ardipithecus, from the Middle Awash region of Ethiopia (White et al. 1994, 1995). The oldest Ardipithecus remains (5.6–5.8 Ma) are ascribed to Ar. kadabba and include one proximal fourth pedal phalanx that is described as having strong plantar curvature, but also a dorsally inclined proximal articular surface similar to that of Au. afarensis (Haile-Selassie et al. 2004). This latter trait is argued to show that Au. afarensis could dorsiflex its foot in a similar way to modern humans (Latimer and Lovejoy 1990b). However, it has also been argued that this feature in Au. afarensis is intermediate between modern humans and great apes (Duncan et al. 1994). Until more postcranial remains of Ar. kadabba are discovered, its locomotor affinities should be treated with some caution. The 4.4 Ma Ardipithecus ramidus remains are, however, far more comprehensive. Based on a partial cranial base, this taxon was originally reported to have had an anteriorly positioned foramen magnum (White et al. 1994). Following the 2009 announcement of a partial Ar. ramidus skeleton (ARA-VP-6/500) with associated cranial and postcranial remains (White et al. 2009), this finding has been confirmed by several studies (Suwa et al. 2009; Kimbel et al. 2014). The rest of the skeleton possesses traits associated with both bipedalism and arboreal locomotor behaviors. The best evidence for bipedality rests with the pelvis. Although the original fossil is damaged and distorted, there is a prominent anterior inferior iliac spine (AIIS), and computerized reconstruction of the iliac blades suggests that they are mediolaterally flared (Lovejoy et al. 2009d). These are features found in later australopiths and indicate bipedality. However, other aspects of the pelvis are more African apelike (such as the elongated superior ischial ramus), and there is no sacrum preserved. In contrast, the relatively long upper limb of Ar. ramidus is well adapted for arboreality (Lovejoy et al. 2009b), with curved manual phalanges and a more palmarly orientated capitate head. It is important to note that the hand and wrist of ARA-VP-6/500 do not have any knuckle-walking features (Lovejoy et al. 2009b). The foot also indicates arboreality, as it has a markedly convex and abducted hallucial articular surface on the medial cuneiform, indicating a grasping hallux. Conversely, it is argued that the rather wide lateral side of the cuboid implies the presence of an os peroneum, a small sesamoid bone indicative of a powerful fibularis longus muscle that would have helped stiffen the lateral foot during the stance phase of upright walking (Lovejoy et al. 2009a). In a summary paper Lovejoy and colleagues (2009c) have interpreted Ar. ramidus as having had a locomotor repertoire made up of bipedalism on the ground and a combination of careful climbing and above-branch, pronograde quadrupedalism when in the trees. Orthograde suspensory behaviors and terrestrial knuckle-walking were definitively ruled out, and the arboreal locomotor component was argued to be somewhat similar to that suggested for the Early Miocene stem hominoid, Proconsul (Lovejoy et al. 2009c). It should be noticed that the hominin status of Ar. ramidus and its bipedality have been challenged (Harrison 2010; Sarmiento 2010; Wood and Harrison 2011) on the basis that some of the derived features reported in the taxon are found in several, non-bipedal Miocene hominoids. This has been challenged by White and colleagues, who argue that given the particular combination of features found in Ar. ramidus, the most parsimonious approach is to class it as a bipedal hominin (White et al. 2010). A preliminary morphometric analysis of the Ar. ramidus reconstructed innominate confirms the original suggestion of a derived pelvis partially adapted to Page 8 of 36

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bipedality, but also suggests that, when in the trees, Ar. ramidus was likely more similar to orthograde suspensory apes such as Pan and Gorilla (Webb et al. 2013). In summary, the rather fragmentary fossil record for early hominins allows a degree of speculation as to how bipedal these taxa were. The horizontal orientation of the Sahelanthropus tchadensis foramen magnum does certainly indicate that this taxon was likely to have spent more time engaging in bipedal behaviors than either Pan or Gorilla do, but only the discovery of postcranial remains will further strengthen this argument. The femur of O. tugenensis indicates that it was also likely to have been a biped, but its upper limb implies strong climbing. The comparatively extensive remains of Ardipithecus ramidus undoubtedly provide the best insight into the locomotion of early hominins and indicate an animal with a pelvis partially adapted to bipedalism, but a foot and upper limb clearly adapted to arboreal climbing behaviors.

The First Habitual Bipeds

Perhaps the first concrete evidence for habitual bipedalism comes with the earliest Australopithecus remains from the Kanapoi and Alia Bay localities at Lake Turkana, Kenya. Assigned to Au. anamensis, the remains include a large and well-preserved distal and proximal tibia of one individual and are dated to between 3.9 and 4.2 Ma (Leakey et al. 1995, 1998). Crucially, the distal end of the tibia has a horizontal talar surface relative to the long axis of the shaft, implying that the Au. anamensis knee would have passed directly over the foot, as in later hominins and modern humans (Ward et al. 1999, 2001). In Pan and Gorilla, the talar surface is sharply inclined, which results in the knee passing over the foot more laterally during plantigrade locomotion (Latimer et al. 1987). There are significant australopith postcranial fossil remains from the site of Woranso-Mille, Ethiopia, that at 3.8–3.6 Ma are just slightly younger than the youngest Au. anamensis specimens. They include a partial skeleton with an almost complete scapula, a partial pelvis, ribs, and wellpreserved upper and lower limb bones. Overall, these remains are argued to strongly imply committed bipedalism with little in the way of arboreal specialties (Haile-Selassie et al. 2010). As they are currently assigned to Au. afarensis, see section 5.4.3.1 for more discussion concerning this taxon. Following the Au. anamensis and Woranso-Mille remains the, record becomes richer and starts with what is arguably one of the best-known and strongest lines of evidence for early hominin bipedalism: the Laetoli footprint trail. Laetoli, Tanzania, is the type locality for Au. afarensis (see below) and has produced a number of hominin fossils assigned to this taxon. However, it is perhaps best known for its extraordinary series of preserved animal tracks, first discovered in 1976. Excavation through 1977–1979 revealed at least two (and probably three) trails of unmistakably bipedal hominin footprints preserved in a volcanic ash-fall layer that had become wet from rainfall (Leakey and Hay 1979; Leakey and Harris 1987; White and Suwa 1987). The footprints are dated between 3.5 and 3.7 Ma (Hay and Leakey 1982; Drake and Curtis 1987). The most distinctly hominid tracks are those from Site G, where there are two trails (and a possible third overprinted on the larger G-2 tracks). There is also a putative hominin track at Site A, but that has been argued by Tuttle et al. (see 1991) to have probably belonged to an ursid. Most researchers agree that the G-1 and G-2 series of tracks are very humanlike, with no evidence of any type of forelimb support. The best preserved prints show a strong heel-strike and toe-off and indicate a transmission of body weight through the stance phase of walking similar to that of modern humans. In accordance with this, there is evidence of longitudinal arching, and the hallux is in line with the remaining toes (Day and Wickens 1980; Robbins 1987; Tuttle 1987; White and Suwa 1987). Stern and Susman (1983) do argue that the footprints show a “transitional” morphology between apes and modern humans, but the prevailing view remains that they are very humanlike. Page 9 of 36

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Schmid (2004) has argued that although the prints were made by habitual bipeds, there is some evidence of increased rotational movement of the upper body reflecting a more apelike morphology of the trunk. This in turn implies an “ambling” gait-pattern inconsistent with the ability to run. More recent analyses of the prints using three-dimensional analytical techniques (e.g., Raichlen et al. 2010) have confirmed that the Laetoli hominins had a very humanlike weight transfer pattern during walking. There is much more debate over the taxonomic assignation of these trails. Most researchers accept that Au. afarensis is likely to have made them, given that the type specimen for that taxon comes from Laetoli and is roughly contemporary with the footprints. Others, principally Tuttle and colleagues (1981, 1987, 1990, 1991), have argued that the prints are so humanlike that they are incompatible with the known Au. afarensis remains from Hadar, which have long and curved pedal phalanges. They argue that another, as yet undiscovered, hominin must have made the tracks, which would have had feet far more humanlike than the Hadar Au. afarensis specimens. White and Suwa (1987) addressed this issue with a large study in which they reconstructed a hypothetical Au. afarensis foot using an amalgam of Hadar bones and the Homo habilis foot complex from Olduvai, OH 8. They argued that this reconstruction perfectly matched the Site G footprints. However, at 1.76 Ma, OH 8 is almost 2 younger million years than the Laetoli trails and has a very different combination of morphologies to the Hadar remains (Napier and Davis 1964; Kidd et al. 1996; Harcourt-Smith 2002), while a number of studies have shown that the Hadar Au. afarensis are unlikely to have had longitudinal arching in the foot, as seen in the Laetoli prints (Berillon 2000, 2003; Harcourt-Smith 2002; Harcourt-Smith and Hilton 2005; DeSilva and Throckmorton 2010). There are also a number of Hadar tarsal remains, including calcanei, two naviculars, and two tali that would be better suited to making a reconstruction of the Au. afarensis foot. Despite all this debate, what is certain is that the footprints provide an excellent temporal benchmark in terms of the origins of bipedalism. They mark a distinct behavioral event in time, which fossils can never do. In that context we can be sure that at least one line of hominins were practicing habitual bipedalism by at least 3.6 Ma, which implies that the shift from occasional to habitual bipedalism occurred sometime well before that and probably well before 4 Ma. Locomotion in Australopiths There has probably been more debate over the locomotor affinities of members of the genus Australopithecus than over any other taxa. This is partially due to the fact that there is a relatively rich postcranial record for this genus. However, the main reason is that these remains show intriguing combinations of primitive and derived traits relating to both terrestrial and arboreal locomotor behaviors. Historically the South African Au. africanus remains provided the major focus of work through to the early 1970s, perhaps culminating in Robinson’s seminal treatise “Early Hominid Posture and Locomotion” in 1972. Between the 1970s and the 1990s, the discovery in Ethiopia of extensive postcranial remains assigned to Au. afarensis, including the famous “Lucy” skeleton, has shifted the debate to East Africa and back as far as 3.4 Ma. The Au. afarensis remains are considerably older than those of Au. africanus and along with Laetoli confirm that bipedal locomotion was likely to have been selected for well before brain expansion and tool-making behavior. Most recently the exciting new Au. sediba remains from South Africa have considerably added to the locomotor variation we see within the genus. In this section we will review the morphology and associated locomotor behavior of Au. afarensis, Au. africanus, and Au. sediba in turn.

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Au. afarensis This taxon provides the first direct anatomical evidence of a true shift from occasional to habitual bipedalism. However, there has been much disagreement over the precise locomotor affinities of this taxon, most of which falls into two distinct camps. Some researchers argue that Au. afarensis was almost as proficient a biped as modern humans (e.g. Latimer 1991; Lovejoy et al. 2002; Ward 2002). Others argue that in fact this taxon had a significant number of primitive postcranial traits that must have implied an important arboreal component to its locomotor repertoire (e.g., Susman et al. 1984; Stern 2000). These views are rather polarized, and it is best to consider Au. afarensis as highly mosaic in its adaptations (see McHenry 1991, for a comprehensive review of primitive and derived traits in the Hadar hominins). The first specimen of Au. afarensis to be discovered showing evidence for bipedality was the AL 129 knee, discovered at Hadar, Ethiopia, and consisting of a well-preserved distal femur and associated proximal tibia (Taieb et al. 1974). Crucially, the morphology of the distal femur indicated a bicondylar angle even higher than that of modern humans (Johanson et al. 1976). This implied that the leg of Au. afarensis would have passed close to the midline of the body as in humans, which is an important adaptation to bipedal locomotion. Subsequent discoveries at Hadar, including the AL 288 partial skeleton (Lucy) and the extensive AL 333 assemblage, provided further evidence of a strong selection for bipedality. The AL 288 skeleton, approximately 40 % complete, included a well-preserved pelvis, ribs, vertebrae, and representative pieces of all major limb elements. In overall morphology, the pelvis of Lucy is far more similar to that of modern humans. The iliac blades are short and wide, which would have allowed the lesser gluteal muscles to be situated laterally and act as pelvic abductors. The wide sacrum, situated behind the hip joint, would also have kept the center of mass of the trunk close to the hip, allowing efficient transfer of the weight to the lower limb during walking. Finally, there is a prominent anterior inferior iliac spine, indicating the importance of the knee extensor, rectus femoris, and a strong attachment for the iliofemoral ligament which helps maintain balance by preventing hyperextension of the thigh (Aiello and Dean 1990). It is worth noting that the pelvis of AL 288 is also unique in being markedly wide, more so than in modern humans, and that its iliac blades are not orientated as anteriorly–posteriorly as they are in humans. This considerable width may well be functionally linked to the more funnel-shaped rib cage of Au. afarensis (Schmid 1983, 1991). Such a rib cage would have been relatively wider inferiorly than in humans, therefore requiring a wider pelvis to support the resulting wider trunk. However, overall the anatomy of the Au. afarensis pelvis implies that it was well suited to two of the major requirements of bipedalism: maintaining balance and efficiently transferring weight from the trunk to the leg during walking. Apart from the high bicondylar angle in Au. afarensis, it has been argued that its long femoral neck is especially adapted to bipedality. This feature may in fact have made abduction of the hip biomechanically easier than in modern humans (Lovejoy 1973; Lovejoy et al. 1973). However, it is also possible that this feature is a reflection of the wider thorax and pelvis in Au. afarensis. There are a number of other traits in the lower limb that unequivocally imply habitual bipedality. The mediolateral orientation of the talar surface of the distal tibia is horizontal relative to the long axis of the shaft. As discussed in section “Associated Anatomical Differences Between Humans and Great Apes,” this is an important feature unique to later bipedal hominins that facilitates efficient transfer of weight from the leg to the foot. In the Au. afarensis foot, the talus is very humanlike, particularly with respect to the trochlear surface (Latimer et al. 1987). The calcaneus has a lateral plantar process on the tuberosity, which greatly helps dissipate stress produced by ground reaction forces at heel-strike (Latimer and Lovejoy 1989). In general the morphology of the ankle joint and heel in Au. afarensis is extremely humanlike and would have been well suited to coping with the

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increased forces through the ankle associated with bipedal locomotion. It is also argued that the Au. afarensis foot would not have been capable of opposing its hallux (Latimer and Lovejoy 1990a). Other features present in the postcranium suggest bipedalism, but are more open to interpretation. The femoral neck in both the AL 128–1 and Maka femora has thicker cortical bone inferiorly than superiorly (Lovejoy et al. 2002). As discussed in section “Earliest Hominin Evidence,” there is disagreement concerning this trait being used to confidently imply bipedality. The femoral condyles of larger-bodied members of Au. afarensis are also more humanlike in proportions and symmetry, but this is not the case for smaller members of the species, such as AL 129 (Aiello and Dean 1990). In the foot, it has been argued that Au. afarensis had more dorsally orientated proximal articular facets on the proximal pedal phalanges, implying a human-like ability for increased dorsiflexion of this joint in bipedal walking (Latimer and Lovejoy 1990b). However, a subsequent metrical study found that the Au. afarensis angle actually falls well outside the human range of variation and between humans and the African apes (Duncan et al. 1994). The foot of Au. afarensis had also been suggested to have had strong longitudinal arching (e.g., Latimer and Lovejoy 1989; Ward et al. 2011). This assertion is partially related to the assumption that the arched footprints from Laetoli were made by Au. afarensis. As discussed in section “The First Habitual Bipeds,” this may not be the case, and when assessing the degree of arching in this taxon, it is best to assess the fossil remains directly. The markedly enlarged medial tuberosity on two navicular bones from Hadar strongly implies considerable weight-bearing in the midfoot of Au. afarensis (Sarmiento 2000; Harcourt-Smith et al. 2002; Harcourt-Smith and Hilton 2005). Such morphology is incompatible with longitudinal arching. A comprehensive architectural analysis of the Au. afarensis pedal material by Berillon (2003) also finds that this taxon was unlikely to have had a longitudinal arch, and recent work linking distal tibial morphology and arch height reached similar conclusions (DeSilva and Throckmorton 2010). However, an analysis of a well-preserved fourth metatarsal from Hadar does argue for a longitudinal arch due to humanlike torsion of the metatarsal head relative to the base (Ward et al. 2011). Drapeau and Harmon (2013) challenge these findings and point out that such torsion can only really inform on the presence of a transverse longitudinal arch, a trait many extant primates possess. They note that cercopithecoids and modern humans have similar levels of torsion for this reason, even though cercopithecoids do not have a longitudinal arch. There are also a number of more apelike traits in the Au. afarensis postcranium, some of which suggest a degree of arboreal climbing ability (see Stern 2000). Most noticeably, the manual and pedal proximal phalanges from the AL 288 and AL 333 localities, as well as from the infant Dikika specimen, are markedly curved and long and have prominent flexor ridges (Marzke 1983; Stern and Susman 1983; Susman et al. 1985; Alemseged et al. 2006). These features strongly imply an arboreal proficiency not found in later hominins. In the foot, the morphology of a partial medial cuneiform bone from AL 333 also implies that there may have been a degree of hallucial opposability (Harcourt-Smith et al. 2003), although others assert this to not be the case (Latimer and Lovejoy 1980a). Elsewhere, it has been reported that that the morphology and function of the Au. afarensis calcaneocuboid joint may have been apelike (Gomberg and Latimer 1984). Analysis of the limb proportions of the AL 288 skeleton show that the femur was relatively short (Jungers 1982; Jungers and Stern 1983), meaning that Lucy would have had much shorter stride lengths than modern humans. The morphology of the tibial plateau indicates that Au. afarensis would have had a single attachment for the lateral meniscus, as in apes (Senut and Tardieu 1985), although the phylogenetic relevance of this trait has recently been questioned (Holliday and Dugan 2003). In the upper limb, it has been argued that the distal humerus of smaller-bodied Au. afarensis specimens shows a well-developed lateral trochlear crest, an apelike trait that prevents dislocation of the elbow joint during climbing/suspension (Senut 1981a, b; Senut and Tardieu 1985) and a more cranially Page 12 of 36

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_48-3 # Springer-Verlag Berlin Heidelberg 2013

orientated glenoid in the scapula (Stern and Susman 1983). Both these features could have facilitated the arm’s being used in above-branch climbing behaviors. However, more recent finds have added to the debate over Au. afarensis shoulder function. The 3.3 Ma Dikika specimen, a presumed 3-yearold female, has a complete scapula that is most similar to its counterpart in Gorilla, something that is argued to imply arboreal locomotor behavior (Alemseged et al. 2006). Conversely, the older Woranso-Mille adult partial skeleton KSD-VP-1/1 (3.8–3.6 Ma) is argued to have a scapula with a combination of Gorilla-like and Homo-like features, but overall a total morphological pattern that was incompatible with suspensory locomotion (Haile-Selassie et al. 2010). In the wrist it has been suggested that Au. afarensis retained features consistent with a knuckle-walking ancestry (Richmond and Strait 2000, although the authors do not go so far as suggest that Au. afarensis itself had a capacity for knuckle-walking. Others disagree with this assertion (Dainton 2001; Lovejoy et al. 2001), and it is interesting to note that none of the other important morphological traits associated with knuckle-walking (e.g., transverse dorsal ridges and dorsally expanded articular surfaces on the metacarpal heads) are found in Au. afarensis specimens (Stern and Susman 1983). It has also been suggested that there is a significant degree of postcranial variation between largerbodied and smaller-bodied individuals of Au. afarensis, particularly in the knee and elbow joints as discussed above, but also in the ankle (Stern and Susman 1983; Senut and Tardieu 1985). These differences could imply locomotor differences between the sexes, as Stern and Susman have suggested (1983), but have also been interpreted as suggesting that there were two distinct species of hominin at Hadar (e.g., Senut and Tardieu 1985; Tardieu 1985; Deloison 1999). However, the prevailing view remains that the Hadar material constitutes a single species (Harcourt-Smith and Aiello 2004), although there continues to be disagreement over the degree of sexual dimorphism in Au. afarensis (e.g., Plavcan et al. 2005; contra Reno et al. 2003). The considerable debate over the locomotor behavior of Au. afarensis ultimately rests on how one views the evolutionary relationship between these traits and the process of selection (Ward 2002; Harcourt-Smith and Aiello 2004). One can argue, as Latimer (1991) does, that the derived anatomical adaptations to bipedalism seen in Au. afarensis demonstrate clear evidence of directional selection toward bipedality. Conversely one can also argue that the retention of primitive apelike traits present in Au. afarensis indicates a degree of stabilizing selection for arboreal proficiency (e.g., Stern and Susman 1983; Stern 2000), although there have also been suggestions that such features in Au. afarensis were reflective of efficient terrestrial quadrupedalism (Sarmiento 1994, 1998). Only a better understanding of the relationship between many of these traits and ontogenetic and/or epigenetic factors may help to resolve this debate (Lovejoy et al. 2002; Harcourt-Smith and Aiello 2004). Overall, the postcranial skeleton of Au. afarensis can be best considered as mosaic showing a combination of derived humanlike bipedal traits, primitive apelike climbing-related traits, and a number of traits that appear to be unique. There is no doubt that Au. afarensis was a habitual biped and would have spent a significant amounts of time engaging in bipedal locomotor behaviors, but there are enough arboreal adaptations present to imply a degree of climbing ability, and it is not unreasonable to suggest that Au. afarensis could have spent time in trees at night and for predator avoidance. The Burtele Remains In contrast to the extensive remains within the Au. afarensis hypodigm, there is one new similarly aged (3.4 Ma) partial foot from the site of Burtele in Ethiopia that appears to have been distinct to that of Au. afarensis. Although not yet taxonomically assigned, its discoverers argue that it had strong grasping abilities, with an opposable hallux (Haile-Selassie et al. 2012). The only other Page 13 of 36

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_48-3 # Springer-Verlag Berlin Heidelberg 2013

hominin with such a feature is Ar. ramidus, and the authors suggest that the Burtele hominin was similar to that taxon in its locomotor adaptations. If true this would strongly lend support to the hypothesis that multiple forms of bipedalism existed in different hominin lineages from the Late Miocene through to the Pleistocene (Harcourt-Smith and Aiello 2004). However, three-dimensional metrical analyses of the AL 333–54 hallux from Hadar have shown that it is more apelike than humanlike (Proctor et al. 2008), and further work will be needed on the Burtele foot to ascertain that it is distinct from that Au. afarensis. Au. africanus Until the discovery of the Hadar remains in the 1970s, the South African Au. africanus fossils provided the best insight into the locomotor behavior of ancient fossil hominins. This was initiated by the discovery of the Taung Child in the 1920s and Dart’s (1925) description of its foramen magnum as being in a more humanlike position, thus implying upright posture and locomotion. Since then a large number of fossils assigned to Au. africanus have been discovered, predominantly from the site of Sterkfontein. The most diagnostic specimen of bipedality is the partial skeleton, Sts 14, which includes a partial pelvis and femur and vertebral fragments and has been argued to belong to the same individual as the Sts 5 skull (Thackeray et al. 2002). The pelvis is morphologically very similar to AL 288, in having wide and short iliac blades and being predominantly more humanlike than apelike (McHenry 1986). Also like AL 288, the pelvis of Au. africanus is very wide, with laterally flaring iliac blades and a relatively smaller acetabulum and iliosacral joint. This high pelvic width is confirmed by other Au. africanus pelvic fragments, including the reconstructed Stw 431 pelvis from Member 4, Sterkfontein (Kibii and Clarke 2003). As for Au. afarensis, this is argued to have provided a distinct advantage in bipedal walking (Lovejoy 1973). Distal femora from Sterkfontein (TM 1513 and Sts 34) also indicate that Au. africanus had a high bicondylar angle, as in Au. afarensis and modern humans. More recently discovered Australopithecus postcranial remains from the Jacovec Cavern at Sterkfontein, which may be as old as 4.0 Ma, include a proximal femur (Stw 598) that has a markedly long neck and short head, as for the Paranthropus femora from Swartkrans (see below) (Partridge et al. 2003). Other aspects of Au. africanus locomotor anatomy have been argued to be more mosaic. Analysis of the relative size of the semicircular canals in the inner ear indicates that Au. africanus had canals of apelike proportions. The morphology of the semicircular canals is closely linked to locomotor behavior, and while this finding does not preclude Au. africanus from having been a biped, it is likely that it would have been less competent at complex bipedal behaviors such as running and jumping (Spoor et al. 1994). McHenry and Berger (1998a, b) argue, mainly based on analysis of the Stw 431 skeleton, that Au. africanus had relatively large upper limbs and small lower limbs, implying a more prominent climbing-related component of its locomotor repertoire. However, Stw 431 does not have any lower limb remains, only a partial pelvis with a preserved acetabulum and sacroiliac joint, and this limits the scope of their study. It is important to note that this study is often misinterpreted as stating that the limb proportions (e.g., humerofemoral index) of Au. africanus were primitive. In fact the study mainly concentrated on measurements taken from the articular surfaces at the ends of limb elements. It has also been argued that a proximal tibia from Member 4, Stw 514a, is “chimpanzee like,” in having a more rounded lateral profile of the lateral condyle, thus inferring an apelike range of motion at the knee joint (Berger and Tobias 1996). This may have been so, but it is premature to describe a structure as complex as the proximal tibia as apelike based on one feature alone, and further analysis is needed. Finally, full recovery and analysis of the well-preserved Stw 573 “Little Foot” skeleton from Member 2 (Clarke and Tobias 1995; Clarke 1998) may prove vital in helping to resolve debate surrounding the locomotion of Au. africanus. Stw 573 promises to one of the most important Page 14 of 36

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_48-3 # Springer-Verlag Berlin Heidelberg 2013

discoveries in the early hominin fossil record, as it is far more complete than that of Lucy, with a complete skull, a scapula, arm and hand bones in articulation, leg bones, foot bones, ribs, and fragments of vertebrae and the pelvis (Clarke 1999, 2002, 2013). The date of Stw 573 has been the subject of considerable debate, ranging from almost 4 to 2.2 Ma, although recent advances in dating methods and a better understanding of the complex stratigraphy of Sterkfontein have resulted in a likely range of 2.6–2.2 Ma (Herries et al. 2013). Most of these bones await removal from the breccia, but the foot bones were found separately and were initially described as showing a mosaic of adaptations, with a partially opposable hallux capable of some grasping potential, but a more humanlike ankle joint (Clarke and Tobias 1995). However, metrical analyses of these remains show that while Little Foot could not have opposed its hallux and had a navicular distinct from those at Hadar, it did have a more apelike ankle joint, implying that overall the foot was mosaic, but in a different way to that originally suggested (Harcourt-Smith 2002; Harcourt-Smith et al. 2003; Harcourt-Smith and Aiello 2004; Kidd and Oxnard 2005; McHenry and Jones 2006). It should be noted that while Stw 573 was originally argued to possibly belong to Au. africanus (Clarke and Tobias 1995), it has recently been suggested that it might instead belong to a different species of australopith (Clarke 2013). Au. sediba The discovery of the Au. sediba associated skeletons from Malapa, South Africa (Berger et al. 2010), has provided a fascinating new twist to the debate surrounding the emergence of obligate bipedalism. Dated to 1.95–1.78 Ma (Berger et al. 2010), Au. sediba is contemporary with as many as six different hominin taxa across southern and eastern Africa. When considering the locomotion of Au. sediba, analysis of the hand bones implies arboreal locomotor capabilities (Kiveell et al. 2011). This is not inconsistent with the predicted locomotor behavior for other, earlier species of Australopithecus. However, more surprising information comes from the pelvis and foot. Although some features of the pelvis are shared with other species of Australopithecus, it has many more derived, Homo-like features than not. The iliac blades are more vertically orientated and have a sinusoidal anterior border, the ischia are shortened, and the distance from the sacroiliac joint to the hip joint is reduced (Kibii et al. 2011). Given that Au. sediba has a small, australopith-sized brain, the markedly more human-like pelvis implies a level of anatomical remodeling most likely related to locomotion and challenges the hypothesis that pelvic remodeling in Plio-Pleistocene hominins was related to obstetric constraints related to increased brain size (e.g., Lovejoy et al. 1973). The foot of Au. sediba is, conversely, very mosaic. The ankle joint is humanlike, but the medial malleolus of the tibia is markedly thick mediolaterally, and the calcaneus is primitive in lacking a lateral plantar process, unlike Au. afarensis and modern humans (Zipfel et al. 2011). Combined with other features in the lower limb, including a very high lateral patella lip on the distal femur, these pedal features are argued to indicate a form of hyperpronating bipedalism in Au. sediba entirely distinct from that of other australopiths (DeSilva et al. 2013), providing further evidence of locomotor diversity in early hominins (Harcourt-Smith and Aiello 2004; McHenry and Brown 2008). Paranthropus The majority of available postcranial material from the genus Paranthropus come from the South African sites of Swartkrans and Kromdraai and are assigned to Paranthropus robustus. There are no complete long bones for P. robustus, but from Swartkrans there are a partial pelvis (SK 50), two proximal femora (SK 82 and 97), and a number of other postcrania including hand and foot bones, while from Kromdraai there is a partial talus (TM 1517). Two major studies on this postcranial material, by Napier (1964) and Robinson (1972, 1978), argued that P. robustus had a slightly less-derived postcranial skeleton than Au. africanus and would have had Page 15 of 36

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_48-3 # Springer-Verlag Berlin Heidelberg 2013

a less efficient type of bipedal gait. The main anatomical arguments for this were a more laterally facing acetabulum and longer ischium in the SK 50 pelvis, smaller femoral heads, and a more medially orientated talar neck and head, which has been sometimes linked to hallux opposability (Broom and Schepers 1946; Napier 1964; Robinson 1972). However, the SK 50 pelvis is severely distorted, and it is questionable whether there is enough well-preserved morphology for serious anatomical analysis. The Kromdraai talus, although apelike in some metrical aspects (Wood 1974), also has a relatively flat humanlike trochlear surface (Robinson 1972), and the significance of talar neck orientation to grasping potential has been brought into question by Lewis (1980, 1989). More recent finds assigned to P. robustus suggest that it was, in fact, likely to have been an efficient biped (Susman 1989). In particular, two well-preserved first metatarsals from Swartkrans show that P. robustus would have had a strong toe-off during walking, which is in concordance with efficient bipedality (Susman and Brain 1988; Susman and de Ruiter 2004). There is little in the way of confidently assigned postcranial remains of P. boisei, though a recently described partial skeleton from Olduvai Gorge, Tanzania (Domínguez-Rodrigo et al. 2013), indicates that this taxon may have had large, powerful forelimbs. Locomotor Differences and Similarities Among Australopiths The postcrania of Au. afarensis, Au. africanus, and Au. sediba all show distinct adaptations for bipedal locomotion. Particularly in Au. afarensis, however, there is also strong evidence of retained apelike traits indicating a proficiency for arboreal climbing, especially within the upper limb. There is no doubt that all these taxa were habitual bipeds, but at the same time they cannot be considered as obligate bipeds, and it is best to treat them as having had degrees of mosaicism in their locomotor repertoires. A number of studies have suggested that Au. africanus and Au. afarensis were very similar to each other in their locomotor anatomy (e.g., McHenry 1986; Dobson 2005). However, a number of other studies show that there are in fact morphologically, and this functionally, distinct. In a major analysis of the Stw 431 skeleton, Haeusler (2001) argues that there are a number of subtle but significant anatomical differences between the Stw 431 and Al 288 pelves implying that Au. africanus may have had a more humanlike type of bipedalism. Work on the tarsal bones of australopiths also shows that the putative Stw 573 Au. africanus foot may well have been mosaic (see above for details) in a different way to that of Au. afarensis (Harcourt-Smith 2002; HarcourtSmith et al. 2003). Finally, it is clear that Au. sediba is distinct from other australopiths, especially concerning its far more humanlike pelvis. Given that Au. sediba also retained more primitive features in the foot and upper limb that respectively imply a unique form of bipedalism and possibly arboreality, it seems increasingly likely that from the Early Pliocene through to the Early Pleistocene, there was perhaps a significant degree of locomotor diversity within Australopithecus. Au. afarensis, Au. sediba, and Au. africanus all show clear adaptations for bipedality, but it is entirely possible that they were achieved through different evolutionary pathways (Harcourt-Smith and Aiello 2004).

The Rise of Obligate Bipedalism

In section “Locomotion in Australopiths,” I discussed locomotor behavior within the genera Australopithecus and Paranthropus. While there may well have been some diversity in the way that different species of Australopithecus were bipedal, what is certain is that they cannot be considered as fully obligate bipeds in the way that modern humans are. Conversely, later species of Homo, such as H. erectus, H. antecessor, and H. neanderthalensis were unequivocally obligate bipeds (see Fig. 1 for a summary of which taxa there is agreement and disagreement over concerning bipedalism). There are some subtle anatomical differences in the postcranial skeletons of these taxa Page 16 of 36

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_48-3 # Springer-Verlag Berlin Heidelberg 2013

Definitely bipedal

0

Later Homo

Mosaic/Disagreement

H. erectus

Insufficient evidence

1

H. rudolfensis

P. robustus H. habilis

2

P. boisei

Au. sediba

H. ergaster

P. aethiopicus Au. africanus

Au. garhi

Ma

3 Au. bahrelghazali

Kenyanthropus platyops

Au. afarensis

4 Au. anamensis Ardipithecus ramidus

5 Ardipithecus kadabba

6

7

Orrorin tugenensis

Sahelanthropus tchadensis

Fig. 1 Temporal ranges of known hominin taxa. Solid shading indicates taxa that were unequivocally obligate bipeds. Cross-hatching indicates taxa where they are mosaic, or there is disagreement over the degree to which they were bipedal. No shading relates to those taxa where there is insufficient evidence (Adapted from Wood (2002))

when compared to modern humans, but their overall skeletal biology strongly implies fully humanlike bipedal locomotion (e.g., Trinkaus 1983; Aiello and Dean 1990; Lorenzo et al. 1999). It seems, then, that the emergence of true obligate bipedal locomotor behavior occurred between about 2.5 and 1.8 Ma. This time period is associated with the emergence of the genus Homo, with which the emergence of obligate humanlike bipedalism is likely to prove to be strongly associated. This period is also extremely complex in terms of hominin evolution and has been the subject of a very diverse range of taxonomic interpretations. At least ten widely accepted hominin species have first or last appearances within this time frame, and the fossil record implies that there was considerable overlap in the temporal and geographical distribution of many of these taxa. Determining which of these species were fully obligate bipeds, and which were not, has been hampered by a number of factors. The principle issue is a meagre postcranial fossil record, but even where there are significant numbers of postcranial elements, as at Koobi Fora (Leakey et al. 1978), there are often problems of reliable taxonomic association. However, the 1.8 Ma juvenile Homo ergaster skeleton from Nariokotome, Kenya (KNM-WT 15000), was unequivocally that of a full biped. Its postcranial skeleton is remarkably humanlike, with long legs and short arms and all of the derived postcranial traits associated with obligate bipedal locomotion (Ruff and Walker 1993). With such an advanced body plan, it is reasonable to assume that H. ergaster and possibly its direct precursors had developed obligate bipedal behavior before 2 Ma. There are a number of other postcranial remains from Koobi Fora that imply striding bipedalism. In particular the femora KNM-ER 1472 and 1481A are long and extremely humanlike. However, it is difficult to speculate whether these specimens belonged to H. rudolfensis, H. ergaster, or even P. boisei. More recently, 1.5 Ma hominin footprints

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_48-3 # Springer-Verlag Berlin Heidelberg 2013

discovered at Koobi Fora also indicate extremely humanlike bipedalism (Bennett et al. 2009). Study of the prints suggests that they are not only more humanlike than those at Laetoli, (Bennett et al. 2009) but also are compatible with body mass and height estimates for H. ergaster. However, as for many other remains at this site, they cannot confidently be assigned to any one taxon. African Early Homo Most of the debate over the locomotor affinities of early members of Homo has concentrated on postcranial remains assigned to Homo habilis from Olduvai Gorge, Tanzania. Found at site FLK NN, the holotype for this taxon, OH 7, includes a number of predominantly juvenile hand bones. These bones are argued to be mosaic in their overall morphology. The scaphoid is apelike, the proximal and intermediate phalanges are more curved than in modern humans, and the intermediate phalanges have more apelike attachments for m. flexor digitorum superficialis, a muscle associated with climbing and suspensory behavior (Susman and Creel 1979; Aiello and Dean 1990). The OH 8 ft, also found at FLK NN, is included as a paratype of H. habilis and provides the best insight into the locomotor behavior of this taxon (Day and Napier 1964; Leakey et al. 1964). Extensive analyses of these bones indicate that the foot had strong longitudinal arches, a locking calcaneocuboid joint, a metatarsal robusticity pattern similar to that of modern humans, and perhaps most importantly a hallux in line with the remaining toes that was wholly incapable of any opposability (Day and Napier 1964; Susman and Stern 1982; Berillon 1999, 2000; Harcourt-Smith and Aiello 1999). The combination of all these features points to an individual capable of efficient bipedal locomotion. However, the talus is less humanlike than the remaining foot and has a trochlea that is strongly grooved and medially sloping. This is a more-apelike morphology and is consistent more laterally arcuate passage of the leg over the foot during the stance phase (Latimer et al. 1987). The implication of this is that although the OH 8 ft is very humanlike in most critical features, its ankle joint implies less efficient weight transfer from the leg during walking. There are also the OH 35 distal tibia and fibula, which were found at site FLK (Davis 1964). These are argued to be humanlike, with a talar facet that is perpendicular to the long axis of the shaft and predominantly humanlike muscle attachments (Davis 1964; Lovejoy 1975; Susman and Stern 1982). It has been argued that OH 35 is likely to have come from the same individual as OH 8 based on morphological similarity (Susman and Stern 1982). Recent metrical comparisons contradict that assertion (Aiello et al. 1998), and it should be noted the two specimens were found 300 yards apart and in different geological horizons (Davis 1964; Dunsworth and Walker 2002). The other specimen of interest from Olduvai is the more recently discovered partial skeleton OH 62, found at site FLK and assigned to H. habilis based on associated craniodental remains (Johanson et al. 1987). Although OH 62 is extremely fragmentary, it has been argued that the intermembral proportions were more apelike and similar to that of Au. afarensis. This assertion was based on humerofemoral proportions that relied on the femoral length of OH 62 being estimated as similar to those of the considerably older Au. afarensis AL 288 (Johanson et al. 1987; Hartwig-Scherer and Martin 1991). Based on these findings, it has also been suggested that OH 62 has limb proportions as primitive as those of Au. africanus (McHenry and Berger 1998a, b). However, the OH 62 femur is incomplete, lacking a considerable part the distal end, and it is impossible to accurately estimate the correct length of this fossil (Korey 1990; Haeusler and McHenry 2004). Furthermore, an alternative reconstruction of the OH 62 femoral length, based on morphological similarity to the younger (1.15–0.8 Ma) and undescribed OH 34 femur from Bed III, yields a far more humanlike value, indicating more humanlike limb proportions (Haeusler and McHenry 2004). Given that OH 34 may have been subjected to a degree of post-depositional erosion that may have compromised its morphology (Day and Molleson 1976), this latter finding must also be treated with caution. Page 18 of 36

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However, given that the OH 35 tibia and fibula are also relatively long, it is not unreasonable to assume that the limb proportions of H. habilis could have been rather more humanlike than some have suggested. Until further material is uncovered, the evidence is not strong enough to be definitively sure of either scenario. More recently Ruff (2009) has addressed the cross-sectional properties of the OH 62 long bones and concluded that the humeral and femoral strength proportions were outside the modern human range of variation and within that of Pan, implying that H. habilis was not an obligate biped and retained some arboreal specializations. There are thus a number of things that can and cannot be said about the locomotor affinities of H. habilis. The foot, tibia, and fibula are all very humanlike in most critical aspects. There is some degree of uncertainty concerning whether the limb proportions were more human or apelike, but this issue cannot be currently resolved. The hand bones show a mosaic of humanlike and apelike morphologies that may imply some climbing activity, and this is supported by analyses of the cross-sectional properties of the long bones. Therefore, a conservative estimation of the locomotor behavior of H. habilis would place it between the habitual bipedalism of the australopiths and the obligate bipedalism of H. ergaster and later species of Homo. The ambiguity surrounding the locomotor affinities of H. habilis has been used by some to add weight to the argument that it should be transferred to the genus Australopithecus (e.g., Wood and Collard 1999). There may or may not be the case craniodentally, but it cannot yet be argued postcranially. Further fossil discoveries will undoubtedly help resolve some of these issues, but findings to date imply a type of bipedalism in H. habilis more humanlike and more efficient than that of either Au. afarensis or Au. africanus. Early Homo from Outside Africa Outside of Africa a number of postcranial remains have been discovered at the 1.8 Ma site of Dmanisi in Georgia (Lordkipanidze et al. 2007). The species-level affinities of the Dmanisi hominins are the subject of some disagreement, but there is little debate that they belong to the genus Homo. Descriptions of the material suggest that the Dmanisi hominins had a combination of derived and primitive morphologies in their postcranial skeleton (Lordkipanidze et al. 2007; Pontzer et al. 2010). There is evidence for a longitudinal arch in the foot, a humanlike ankle and an elongated lower limb. However, there is also low humeral and tibial torsion compared to modern humans. In the original description of the material (Lordkipanidze et al. 2007), it was argued that the foot of the Dmanisi hominins would have struck the ground in a more medial orientation, which is often described as being “pigeon toed” in modern humans. However, a reanalysis of the published data has clearly refuted this suggestion and shows that the variables in question fall within the ranges of modern human variation (Wallace et al. 2008). Early Homo: Summary There is likely to have been some degree of locomotor diversity between different species of early Homo. The anatomy of the Homo ergaster postcranial skeleton (mainly based on KNM-WT 15000) is extremely humanlike and derived, and it would have been an obligate biped capable of long distance travel (Wang et al. 2004). In fact it has been suggested that this would have included endurance bipedal running, something that earlier hominins are unlikely to have been able to have done (Bramble and Lieberman 2004). On the other hand there is far less certainty concerning Homo habilis. Although there is evidence of a distinct shift between the morphology and associated locomotor function of its postcranial remains and those of Australopithecus, it would not have been as efficient a biped as H. ergaster and is likely to have had a unique pattern of gait. Therefore, while it is certain that by the beginning of the Pleistocene fully obligate bipedalism had developed in Page 19 of 36

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_48-3 # Springer-Verlag Berlin Heidelberg 2013

at least one lineage of Homo, it cannot be argued that this had occurred in all species within that genus. This would suggest that different early species of Homo were perhaps ecologically distinct from each other, with different locomotor behaviors and activity patterns.

Bipedalism in Later Homo As mentioned above, nearly all later members of the genus Homo (e.g., H. antecessor, H. heidelbergensis, H. neanderthalensis) have postcranial skeletons entirely consistent with obligate bipedalism. Differences that do exist between these taxa and H. sapiens are small at best, though may have had some subtle effects on locomotor behavior. For instance, it has recently been shown that H. neanderthalensis had a slightly longer calcaneal tuber than modern humans, which would have increased its energy expenditure costs during running (Raichlen et al. 2011). The one exception is the diminutive H. floresiensis from the Middle and Late Pleistocene of Flores, Indonesia. A number of metrical analyses of the postcranium show that the wrist retained several primitive, australopith-like features (Tocheri et al. 2007), the shoulder was more like that of H. ergaster than H. sapiens (Larson et al. 2007), and the foot was markedly long compared to the leg and was unlikely to have had a longitudinal arch (Jungers et al. 2009). With such a combination of morphologies, while H. floresiensis was undoubtedly a biped, it was likely to have had a gait very different to that of modern humans.

Summary of Locomotor Behaviors Within the Hominin Clade As we have seen, there are varying degrees of fossil evidence for the origins of bipedalism. More often than not, we are faced with the problem of being unable to place skeletal remains diagnostic of bipedality within a particular taxonomic hypodigm, and those fossil specimens which are associated with a particular species often show bewildering combinations of primitive, derived, and unique characteristics. However, on the basis of existing evidence, a number of broad conclusions can be made (Fig. 2). It is possible that the earliest hominins, such as A. ramidus, O. tugenensis, and S. tchadensis, show important enough features to imply a slight shift to increased terrestrial bipedality. However, with the exception of Ar. ramidus, the evidence is extremely meagre, and further finds may show that any shift to bipedality could have been more or even less substantial. Following these taxa, there appears to have been at least two distinct shifts in the development of hominin locomotion. Firstly, between 4.5 and 3 Ma, a number of habitually bipedal hominin species emerged, as typified by the Laetoli footprints and the extensive postcranial remains from Hadar. Within this time frame it is possible that different species varied in the way that they became bipedal and that there were several different “types” of bipedalism being practiced (Harcourt-Smith and Aiello 2004; Haile-Selassie et al. 2012). The period between 2.5 and 1.8 million years heralds a second shift to fully obligate bipedalism. This period coincides with the emergence of the genus Homo, and by 1.8 Ma at least one member of this genus (H. ergaster) was a fully obligate biped with a modern human body plan. Other early species of early Homo, like H. habilis, may well have had a locomotor repertoire that was transitional between that of Australopithecus and H. ergaster. Subsequent to the advent of H. ergaster and H. erectus, all known hominins were fully obligate bipeds, although the enigmatic remains of the Middle-to-Late Pleistocene Homo floresiensis retain a number of primitive postcranial traits that would have made their gait, although bipedal, entirely distinct from that of Homo sapiens (Jungers et al. 2009).

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_48-3 # Springer-Verlag Berlin Heidelberg 2013

Obligate bipeds

Later species of Homo

1

H. erectus Au. sediba

2

Habitual bipeds

H. ergaster P. robustus H. habilis

Time (Ma)

Au. africanus

3 Au. afarensis

4

5

6

Occasional bipeds

Au. anamensis

Ardipithecus

O. tugenensis

S. tchadensis

7 Bipedality

Fig. 2 The degree of bipedality in known fossil hominins relative to time. Only taxa with documented traits relating to bipedal locomotion are included. Ardipithecus, O. tugenensis, and S. tchadensis are classed as occasional bipeds on the basis of having very few or weak traits related to bipedality. Australopithecus afarensis, africanus, and sediba are classed as habitual bipeds on the basis of major anatomical remodeling of structures functionally related to bipedality, but retention of a number of apelike climbing specializations. H. ergaster, H. erectus, and later species of Homo are classed as obligate bipeds, but there is enough debate over H. habilis to place it between habitual and obligate bipedalism

Why Was Bipedalism Selected for? As has been discussed, much contemporary debate over the origins of bipedalism rests on the locomotor affinities of particular taxa or individual specimens. This is understandable given that fossils provide concrete evidence. However, it is critical to also ponder why bipedalism was selected for and why it became such a successful form of locomotion for our species. Most early theories as to why humans became bipedal center on the “freeing of the hands” as the principal force of selection. This can be traced back to Darwin, who argued in the Descent of Man (1871) that bipedal locomotion must have evolved to allow for the construction and use of hunting weapons. Since that first explanation there has been as abundance of different theoretical explanations, ranging from the plausible to the wholly implausible. When considering these different potential selection pressures, it is important to consider that bipedal locomotion is a highly derived and unique form of primate locomotion. In that context, we have seen that the skeletal modifications associated with bipedality are considerable. It is therefore strong selection pressures that specifically required prolonged periods of upright walking that are likely to provide the key as to why bipedalism evolved (Lovejoy 1981; Rose 1991). Prior to the discovery of the Au. afarensis remains from Hadar, the orthodox view remained that tools and tool use were intrinsically involved with the emergence of habitual bipedalism. Echoing Darwin (1871), some argued that tool use itself explained the selection for bipedalism (e.g., Washburn 1960), while others suggested that behavior was a more likely explanation (e.g., Bartholomew and Birdsell 1953; Washburn 1967). Both these theories are now contradicted by the temporal sequence of events provided by the contemporary fossil and archaeological records

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(Rose 1991). Evidence of bipedal locomotion currently predates the earliest stone tools by at least 1.5 Myr and probably more, which precludes the involvement of any stone-tool-associated behavior in the origins of bipedality. More recent hypotheses have tended to be strongly linked to paleoenvironmental changes from the end of the Miocene through to the beginning of the Pleistocene. In this respect the traditional view has been that the emergence of bipedalism most likely correlated with generally cooler and dryer global conditions and an associated increase in more open grassland habitats (Van Couvering 2000), often referred to as the “savannah hypothesis.” Predominantly forested environments were gradually replaced by more mosaic environments made up of different proportions of open grassland, bushland, and open woodland (Reed 1997). To cope with these environmental changes, it was argued that hominins had to adapt a series of new behavioral strategies. Change in habitat composition would have resulted in a shift in food availability and thus necessitated a shift in food acquisition behaviors (e.g., Rose 1991; Foley and Elton 1998). Hominins would either have to have ranged further to find food or develop strategies to procure new and different types of food. In this scenario, it was therefore very likely that hominins would have had to have engaged in more terrestrial travel over more open habitats, resulting in the emergence of bipedality as an important part of the locomotor repertoire. However, the discovery of late Miocene hominins (see section “Earliest Hominin Evidence”) and the increasing complexity associated with accurately reconstructing hominin paleoenvironments (Behrensmeyer and Reed 2013) has complicated the savannah hypothesis to some degree. The paleoenvironments of the earliest hominins through to late Australopithecus have been varyingly reconstructed from very open and dry to relatively closed and forested (Behrensmeyer and Reed 2013). Coupled with recent suggestions that hominin bipedalism originated in arboreal environments (e.g., O’Higgins and Elton 2007; Thorpe et al. 2007; Almécija et al. 2013), it is possible that the classic savannah hypotheses is in need of reevaluation when considering the shift from occasional to habitual bipedalism in early hominins. For the shift from habitual to obligate bipedalism in the early Pleistocene, the hypothesis is on stronger ground, as this period coincides with an unambiguous opening up of hominin habitats (Reed 1997; Van Couvering 2000). Despite these complexities, a number of theories strongly associated with the savannah hypothesis warrant discussion. Lovejoy (1981) argues that food-carrying and procurement by males was the driving selection pressure. This would tie in with some interpretations of the fossil material from Hadar that suggests that there was a degree of locomotor sexual dimorphism in Au. afarensis (Stern and Susman 1983). Recent experimental work also supports Lovejoy’s (1980) theory in showing that introducing widely distributed “food piles” leads to an increase in chimpanzee and bonobo locomotor bipedality, mainly associated with food-carrying (Videan and McGrew 2002). Such a situation could be analogous to the more spread-out concentrations of food sources available to hominins in a more open grassland environment. Increased bipedalism in such a setting would greatly increase the ability to carry food to desired locations. Other theories argue for terrestrial foodgathering (Jolly 1970; Wrangham 1980) or even hunting (Carrier 1984; Shipman 1986; Sinclair et al. 1986). Jolly’s (1970) model uses the open-savannah gelada baboon as a modern-day analogue to suggest that early hominin bipedalism was linked to rapid seed-collecting behavior. Hunt (1990, 1994, 1996) has argued that chimpanzee postural behaviors may provide the key to our understanding of this issue. Over 80 % of chimpanzee bipedalism is related to postural feeding. Using this as a behavioral analogue, Hunt argues that early hominin postcranial adaptations in Australopithecus were related to similar postural feeding behaviors, and that true bipedal locomotion emerged with the advent of Homo (see Wood 1993). It is certainly possible that bipedal postural behavior may have preceded bipedal locomotion, but posture alone is likely to be too weak a selection pressure to have resulted in the significant anatomical remodeling seen in the Au. afarensis and Au. africanus pelvis Page 22 of 36

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_48-3 # Springer-Verlag Berlin Heidelberg 2013

and lower limb structures (Lovejoy 1981; Rose 1991). It has also been suggested that bipedal threat displays may have been an important selective precursor to bipedal locomotion (Jablonski and Chaplin 1993). One of the most interesting and widely accepted explanations of why hominins became bipedal is the thermoregulatory hypothesis suggested by Wheeler (1984, 1988, 1991, 1993, 1994). This argument rests on strong physiological explanations related to the reduction of thermal stress and directly relates to the more open habitats that hominins would have become exposed to through the Pliocene. On the open savannah, quadrupedal animals expose considerably more of their body’s surface area to the sun. By standing fully upright, Wheeler calculated that a hominin would absorb 60 % less heat at midday. Furthermore, being upright exposes the subject to any potential breeze, which would have a further cooling effect. These factors would greatly reduce the rate at which hominins would have overheated on open ground, meaning that they could have ranged further without having to have increased water intake. In a more open environment, where food sources were likely to have been more spread out, such an advantage would have greatly enhanced the ability of hominins to successfully collect food. One other physiological explanation for the development of bipedalism warrants comment. Rodman and McHenry (1980) have argued that there is a considerable energetic advantage to become bipedal. However, it has been shown that Pan and Gorilla locomotion is not any less efficient physiologically than that of modern humans (Steudel 1994). Perhaps the most interesting point relating to all the above theories is that made by Robinson (1972), who states that there is unlikely to have been one specific reason why bipedalism was selected for. It was more likely a combination of several selective factors strongly relating to feeding strategies and reproductive behavior that provided the impetus for this shift in the hominin locomotor repertoire. Furthermore, bipedalism would have provided not only the ability to range further for food and other resources; it would have exposed hominins to novel parts of the surrounding landscape, different types of predators, and new food sources. This in turn would have led to new hominin behavioral strategies to cope with such changes. It has also been argued that, on the basis of increasingly variable environmental conditions during the Late Miocene and Pliocene, associated behavioral versatility would have been a critical selective factor for early hominins (Potts 1998). If so, there is little doubt that selection for bipedality would have considerably facilitated such behavioral versatility.

Conclusion There is no doubt that the evolution of bipedalism is a critical issue in the study of human origins. However, as we have seen, there has often been a considerable degree of rather polarized debate and disagreement as to how, when, why, and in whom hominin bipedalism evolved. In particular, the emergence of so many important fossil finds in the last 40 years has resulted in the literature becoming increasingly “fossil driven” in its concentration on how bipedal a particular hominin taxon might have been. This has often clouded our understanding of the larger issues at stake surrounding the emergence of this unique form of primate locomotion. As Rose (1991) has pointed out, selection for bipedality was not an event, but rather a series of processes. In that context, what can be said about these processes? It is certain that the selection pressures for bipedality must have been strongly linked to reproductive success, and it is therefore likely that such pressures would have been related to the efficient gathering and transport of food and other resources across increasingly varied habitats. As discussed earlier in this chapter, the current fossil record points to at least one Page 23 of 36

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_48-3 # Springer-Verlag Berlin Heidelberg 2013

minor and two major steps in the emergence of obligate, humanlike bipedality. The earliest hominins were little more than occasional bipeds, while the australopiths can certainly be considered as habitual bipeds who still engaged in some arboreal locomotor behaviors. By the emergence of early Homo, certain species within that genus were unequivocally obligate bipeds much in the way that we are today. It is perhaps seductive to view such steps as punctuated events, and that may have been the case. But it is also possible that the fragmentary fossil record merely creates the illusion of such steps. Only the recovery and analysis of further fossil remains relating to bipedality, particularly from the Late Miocene hominoid record, will further our understanding of this complex and unique process.

Cross-References ▶ Defining the Genus Homo ▶ Fossil Record of Miocene Hominoids ▶ General Principles of Evolutionary Morphology ▶ Homo floresiensis ▶ Origins of Homininae and Putative Selection Pressures Acting on the Early Hominins ▶ Postcranial and Locomotor Adaptations of Hominoids ▶ Role of Environmental Stimuli in Hominid Origins ▶ The Biotic Environments of the Late Miocene Hominids ▶ The Earliest Putative Hominids ▶ The Species and Diversity of Australopiths

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Index Terms: Bipedalism 1 Hominins 5 Locomotion 1 Paranthropus 15 Walking cycle 2

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_49-2 # Springer-Verlag Berlin Heidelberg 2013

The Miocene Hominoids and the Earliest Putative Hominids Brigitte Senut* Sorbonne Universités – CR2P – MNHN, CNRS, UPMC-Paris 6, Département Histoire de la Terre, Muséum National d’Histoire Naturelle, Paris Cedex 05, France

Abstract For many years molecular studies suggested that the hominid family emerged during the Pliocene. But today we have good evidence of hominids in African Upper Miocene strata. Reconstructing our earliest history is a difficult task as the Miocene data is scanty and fragmentary. Furthermore, the tendency for anthropologists to consider the modern chimpanzee as a good model for the last common ancestor of African apes and hominids has obscured our understanding of hominid evolution because the supposed distinctive apelike features are defined on the basis of a modern animal and not on those of Miocene hominoids. Taking into account detailed studies of Miocene apes and modern hominoids, it appears that bipedalism is probably the most reliable feature for defining hominids. Of the new hominoid taxa discovered in the Upper Miocene, only Orrorin tugenensis exhibits clear evidence of adaptation to bipedalism. Bipedalism in Sahelanthropus tchadensis and Ardipithecus kadabba still needs to be demonstrated. A long-lasting idea in hominoid evolution was that hominids emerged in dry, savannah-like environments; but the data obtained from the Upper Miocene levels in Baringo (Kenya) demonstrate that the environment of the earliest hominids was more forested and humid than expected. Finally, recent discoveries of modernlooking apes made in 12.5 Ma strata at Ngorora (Kenya), 10.5 Ma strata at Nakali (Kenya), 10 Ma strata at Chorora (Ethiopia), 11–5.5 Ma strata in Niger, and 6 Ma deposits at Kapsomin and Cheboit indicate that the dichotomy between African apes and humans could be much older than generally thought. Alternatively, one or more of these hominoids could represent early stages in the lineages of modern African apes.

Introduction Identifying the earliest hominids remains a difficult task because the definition of the family varies widely from author to author. For some authors, the term hominid should be restricted to humans and their bipedal predecessors, whereas for others, it should include all extant and fossil great apes and humans; at its most extreme definition, all African apes should be included in the genus Homo (Czelusniak and Goodman 1998), or, in a slightly less extreme view, only chimpanzees and bonobos (with the exclusion of Gorilla) should be grouped with Ardipithecus, Australopithecus, and humans in this genus (Wildman et al. 2003). In the latter scenarios, the search for the oldest hominid leads to a strange situation where the quest becomes that of identifying the earliest ape rather than the earliest humans! This is definitely not what the theme of research on the origins of humans is today. The only consensus today among scientists (molecularists and anatomists) in ape evolution is that Pongo,

*Email: [email protected] Page 1 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_49-2 # Springer-Verlag Berlin Heidelberg 2013

Pan, and Gorilla do not belong to the same taxonomic group, a view that was widely accepted in the last century; the family Pongidae is now restricted to Pongo (Greenfield 1979). Homo is closely related to African apes and may be closer to Pan than to Gorilla. The modern tendency to use the term “hominines” is also misleading, as usage of the term varies: for some scientists, it gathers Pan and Homo and their ancestors, and for others, it is restricted to Homo and its forerunners. This is confusing, as the authors generally do not specify in which sense they use the term. This is why it is more appropriate to restrict the term Hominidae to humans and their fossil forerunners. Whatever systematic scheme is considered, the focus is on understanding the ancestors of humans after their split from African apes. To understand the earliest hominids and ape cousins, we need to apply a geohistorical approach. The role of Asia as well as Africa in the history of our origins cannot be dismissed out of hand. However, today it seems clear from available field data that the development of the human lineage occurred in Africa. Finally, we must consider the fact that, for the last 40 years, the history of research into the dichotomy between apes and humans has been dominated by the conflicting results obtained by paleontologists on the one hand and molecularists on the other. The debate has focused on two major aspects: chronology and the search for the closest relative. There was a heated debate in the 1970s concerning the molecular clock and its implications for hominid evolution versus paleontological evidence and geological time. But discrepancies in the time scales produced by various neontological studies have never been thoroughly debated, as pointed out by Arnason and coauthors in 2001. We have known for almost two centuries that the African apes are our closest relatives; but the research published in the last three decades has attempted to focus on the question in greater detail, and this has led to another major issue: Is the common chimpanzee the closest relative of humans? Or is it the bonobo? Or is it the group of African apes as a whole? At this point it has become widely accepted, almost without debate, that the closest human relative is the chimpanzee, frequently claimed to share 98 % or more of its genetic material with humans (or even 99.4 % for some authors such as Wildman et al. (2003)). General acceptance of these figures has occurred despite the fact that the problem is not yet definitively solved (Marks 2002). It is within this complex framework that research on our oldest ancestors has taken place during the past three decades. In addition, preconceived ideas about our earliest relatives make it even more difficult to have a dispassionate discussion. A statement such as “the common ancestor of human and chimpanzees was probably chimpanzee-like, a knuckle-walker with small thin-enamelled teeth” (Pilbeam 1996) takes us back 200 years, being no different from the quest for the missing link. This widespread preconception is probably one of the reasons why many anthropologists have used modern chimpanzees as the basic comparative material when researching hominid origins and why the reconstructed late common ancestor was depicted as a bipedal chimpanzee. This brings us to another aspect of the problem of defining the earliest hominid. Most anthropologists consider that apelike (i.e. chimpanzee-like) features are primitive and that humanlike ones are derived. However, chimpanzees are not primitive; they are in fact highly derived in their locomotor and dietary adaptations, and the use of their features as ancestral traits is a major error. Humans are also derived in their locomotion, but in a different way from chimpanzees. It is therefore not possible to define the polarity of these traits on the sole basis of some modern relict species; the Miocene apes were highly diverse, and this diversity has to be considered when reconstructing phylogenies. The neontological approach, which has been in favor in some scientific circles, turns out to be a total failure when dealing with the definition of the earliest hominids. This approach leads to a search for magic traits, such as flat face, small canines, and thick-enameled teeth, which are considered almost universally to be hominid features: for when only modern chimpanzees and humans are compared, these features seem to be obvious and clear. However, it is necessary to understand their meaning Page 2 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_49-2 # Springer-Verlag Berlin Heidelberg 2013

and their emergence before using them as a reference. When Miocene hominoids are included in the study, these same features are found to occur in many of them, suggesting that a flat face, small canines, and thick-enameled cheek teeth are plesiomorphic and that the elongated face of chimpanzees and their large canines and thin-enameled cheek teeth are apomorphies of the chimpanzee clade, rather than plesiomorphies of hominoids. Exclusion of the Miocene fossils from the comparisons of modern apes and humans erases the diversity of the past which is the raw material for understanding our evolution.

African or Eurasian Origins? Determining a place for the origin of hominids (sensu stricto) has been widely debated for several decades, and some authors have suggested that Eurasia would be a better candidate than Africa (Begun 1992, 2002; Begun et al. 2012). However, these suggestions are based on biased data concerning Africa. The fact that hominoids were highly diverse in Eurasia between 13 and 8.5 million years does not mean that Africa was devoid of them in the Middle and Late Miocene. They have been recorded in Kenya, Ethiopia, Namibia, Chad, and Niger (Figs. 1 and 2). There is thus no reason to favor Eurasia in the origins of modern African hominoids (hominids included), and the “Back to Africa” hypothesis does not appear tenable today (Senut 2011a). However, does this necessarily mean that an African origin is the correct scenario? When climatic data are taken into account, it is possible to suggest yet another scenario. Nonhuman hominoids are basically tropical animals, and all through their 25 My-long history, they inhabited tropical areas, as indicated by floral and faunal data. Taking that into consideration, the most logical idea is to consider that their ancestors inhabited tropical regions and that faunal interchanges (including hominoids) occurred between Africa and Southern Eurasia throughout the Middle and Upper Miocene (the Tethys did not act as a permanent uncrossable barrier) (Senut 2011, and references therein). In the Early Miocene most of Africa was tropical, and the distribution of hominoids was Pan-African. When the Antarctic

Fig. 1 Distribution of Late Middle Miocene and early Upper Miocene hominoids (Map modified from Begun et al. 2012) Page 3 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_49-2 # Springer-Verlag Berlin Heidelberg 2013

Fig. 2 Distribution of Upper Miocene hominoids (Modified from Begun et al. 2012)

Fig. 3 Latitudinal shifts of the climatic belts during the Neogene. Being tropical mammals, hominoids followed these changes (From Senut 2011)

ice cap expanded to cover the entire continent at about 17 Ma, the Earth’s climatic belts shifted northward such that midlatitude Eurasia became subtropical, allowing hominoids to disperse into vast areas of the Old World from Spain in the West to China in the East (Fig. 3). For several million years, faunal interchanges were possible between Eurasia and Africa, and hominoids could probably move freely between the continents in relation with paleogeography and the position of the tropical zones. This is why a precise geographic origin for African apes and humans cannot be proposed, although the paleoenvironment and paleoclimatic zone can be predicted with confidence (Fig. 4).

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_49-2 # Springer-Verlag Berlin Heidelberg 2013

Fig. 4 Distribution of hominoids during the Upper Miocene. Even though a precise geographic origin for African apes and humans cannot be proposed, the extension of the tropical area reflects the zone of possible dispersals between Europe and Africa

However, for the moment the earliest modern-looking African apes and hominids are found only in Africa. Still, the date of divergence between the different hominoids is not clear. Most biologists favor a young date for the split between humans and chimpanzees (around 6 million years); but the calibration of the so-called molecular clock is not independent, as it needs an expected divergence date for some mammal lineages. However, some geneticists had already suggested other split times for hominoids (Arnason et al. 2001). In contrast, paleontologists usually tended to support older dates of 8–10 million years, or even older, for the split. But new dates of divergence, based on comparative generation time estimates in great apes compared with humans, and then using estimated mutation rates in humans provide a new look at the issue which accords better with the dates based on fossils (Langergraber et al. 2012). The split between chimpanzees and humans is now estimated to be 7–13 Ma, and the divergence between Gorilla and the lineage leading to the ancestor of chimpanzees and humans is between 8 and 19 Ma. Modern hominoid lineages are known from the Upper Miocene, indicating that their history was probably more ancient than previously thought.

The Rise and Fall of the Ramapithecus-Kenyapithecus Group During the 1960s and 1970s, it was widely claimed that Kenyapithecus (sometimes considered to be an African relative of the Asian Ramapithecus) was a hominid, aged ca 15 Ma. This idea (Simons 1961; Simons and Pilbeam 1965; Leakey 1961/62; Andrews 1971) was questioned by some morphologists (Genet-Varcin 1969; Greenfield 1978). The divergence between apes and humans was thus considered by these authors to be very ancient (about 16 Ma or even close to 20 Ma). But in the 1970s, the development of molecular biology and the application of the molecular clock led to the notion that the dichotomy was considerably more recent, and ages of divergences for the African great apes and hominids of about 2–4 Ma were proposed (Wilson and Sarich 1969). It was in this

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_49-2 # Springer-Verlag Berlin Heidelberg 2013

context, 30 years ago, that “Lucy” and the Afar australopithecines were discovered in more than 3 Myr-old deposits (Johanson and Taieb 1976). Considered at the time to be the earliest hominid, these fossils were later named Australopithecus afarensis (Johanson et al. 1978). This major discovery was widely acclaimed: for the first time, we could examine a quasi-complete fossil skeleton from an early time; the earliest stages of bipedalism (a key feature in the definition of hominids) could be seen, and we could get information on body proportions of the earliest members of our family Hominidae. Not least, Lucy was considered by many to occur in the range of dates estimated by the famous molecular clock, which at the time suggested that the dichotomy between apes and humans took place about 4 million years ago (Wilson and Sarich 1969). Subsequently it was demonstrated that the molecular clock was not reliable, as it did not run at a constant rate in mammals and in particular in primates (Britten 1986; Pickford 1987; Stanyon 1989). In numerous papers a large variety of dates was advanced for the dichotomy between apes and humans, depending on the calibration ages accepted in the particular study and the type of protein used: these dates ranged from 2.5 Ma up to 4 Ma. But the fossils always seemed to give an earlier date. The question of an early or a late divergence was addressed by Greenfield (1980): he had already proposed that Sivapithecus (¼ Ramapithecus) brevirostris and Sivapithecus (¼ Kenyapithecus) africanus were size variants of Sivapithecus, and he suggested a late divergence for the group of Homo, Pan, and Gorilla from the pongid stock. However, the age of this dichotomy that he published (10–5 million years) was greater than the one proposed by geneticists. Following general acceptance of the molecular evidence that supported a divergence between chimpanzees and humans around 4 Ma, the matter of chronology was thus thought to be solved and neither Ramapithecus nor Kenyapithecus was subsequently considered by many authors to be hominid. By the end of the 1970s, the Kenyapithecus material had been restudied, especially in the light of sexual dimorphism in modern and fossil apes (Greenfield 1978, 1979; Pickford 1986; Pickford and Chiarelli 1986). It transpired that the group of Ramapithecines-Kenyapithecines did not belong to Hominidae, and as a result the Middle Miocene estimates for the dichotomy between apes and humans were abandoned. Eventually, a meeting organized at the Vatican in 1982 led to a consensus between paleontologists and molecularists: the divergence occurred at around 7 Ma. However, despite the fact that several isolated fossils of putative early hominid ancestors were already known at that time, such as the Lothagam mandible thought to be close to 7 million years old (Patterson et al. 1970), the 6 million year-old Lukeino lower molar (Pickford 1975), and the 4 million year-old Kanapoi humerus (Patterson 1966; Patterson and Howell 1967), these materials were too fragmentary to be taken seriously by most paleoanthropologists, and there was a tendency to avoid them in the phylogenies. Then Coppens (1983) reconsidered all the hominoids, some of which had been attributed to hominids. Taking into account environmental changes, chronology and geography, he formalized his “East Side Story.” He suggested that around 7 Ma the ancestral population to African apes and humans was divided by the formation of the Great Rift Valley, which would have led a modification in the rainfall: which remained high in the West but was reduced in the East. The apes would have survived in the West in wooded and forested environments, while hominids became adapted to wooded grasslands and more open environments in the East. He later updated the theory and suggested an age of 10 Ma for the split between apes and hominids (Coppens 1986; Senut 2006b). Until the end of the twentieth century, australopithecines were considered to be direct ancestors of humans, even though some scholars pointed out that more modern forms existed during the same period, implying that Plio-Pleistocene hominids were more diverse than expected, and that australopithecines might have been a side branch of human evolution (see Senut 1992 and Pickford 2012

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_49-2 # Springer-Verlag Berlin Heidelberg 2013

for reviews). But by the end of the twentieth century, it was widely accepted that the earliest hominid ancestor was to be found in the early Pliocene.

Bipedalism and Its Impact on the Origins of Hominidae Among living primates, facultative bipedalism is frequent; but even if most primates can sit with the back upright, stand on two feet, and walk bipedally for short distances, humans are the only ones that can move on two legs for long distances and for extended periods of time. This difference is reflected in the skeletal characters of extant humans, often defined in comparison with chimpanzees. While a suite of putatively bipedal features linked to femoral, pelvic, or sacral morphology appears to be soundly based, others are questionable. This is the case with the position of the foramen magnum. For the past 80 years, following Dart (1925), most scientists have considered that an anterior position of the foramen magnum indicates bipedality in hominids. Le Gros Clark (1950) used the anterior position of the occipital condyles to confirm the hominid nature of the australopithecines and proposed a “condylar position index,” but he noticed that in modern humans this position varied between dolichocephalic and brachycephalic individuals. Later (1972), the same author warned: “It has been assumed that the condylar-position index, by itself, is always correlated with the degree of postural erectness. The fallacy of this assumption is exposed by the fact that the index varies quite considerably even in modern H. sapiens.” However, generic, specific, and/or populational studies remained limited before 1960, despite the fact that Schultz (1955) highlighted the variability of this feature. Since then it has been shown that an anterior position of the foramen is not linked exclusively with bipedalism, but could be related to the development of the brain (Biegert 1963). Several authors demonstrated that its position relative to the cranial foramina was variable (Dean and Wood 1981, 1982; Schaeffer 1999). It is difficult to discriminate individuals on these isolated features, as there is an overlap between apes and humans. Moreover, it appears that the foramen magnum is more anteriorly displaced in australopithecines than in humans, even though they were not better bipeds than we are. This feature is more complex than usually thought, and we must be cautious when using it. Different forms of bipedalism have existed in the past. Of these, the most debated concerns Oreopithecus bambolii, discovered in the Late Miocene lignites of Tuscany (H€ urzeler 1958; Schultz 1960; Straus 1963; Tardieu 1983; Sarmiento 1983; Senut 1989 and see review in Senut 2011) and which was later demonstrated to be bipedal (Köhler and Moyà-Solà 1997; Rook et al. 1999). For the pedal features, these authors showed that this Miocene ape could move bipedally when on the ground but with a stabilization morphology that differed from those of humans and australopithecines. Oreopithecus lived in an island environment where the absence of large predators and limited trophic resources played an important role in the evolution of mammals (Köhler and Moyà-Solà 1997). The most convincing bipedal evidence from the Upper Miocene remains Orrorin (Pickford et al. 2002; Galik et al. 2004; Richmond and Jungers 2008; Almecija et al. 2013) based on the femoral anatomy and morphometrics in different independent studies. Despite the fact that Orrorin is a biped, it is still moving in the trees as shown by other postcranial elements (Senut et al. 2001; Senut 2003). This ability is probably retained from older Miocene hominoids and is still present in australopithecines. This is also supported by the paleoenvironmental studies. Bipedalism and arboreality are major factors in our origins (Senut 2006b, 2012).

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The Case of Australopithecus afarensis (¼ antiquus) At one time or another, every single fossil older than A. afarensis from Afar in Ethiopia has been considered the earliest human ancestor; and this ancestor was almost always interpreted as being in the direct line leading to the genus Homo and thence to us. However, this approach ignored or underestimated the probable diversity of Pliocene hominids. In fact, in the late 1970s, several authors had already pointed out that there might be a taxonomic problem with the species Australopithecus afarensis: was it, as claimed, a single bipedal species? Did this species include two different taxa, one of which was a combination of a climber and a terrestrial biped and the other a more advanced species which was primarily a ground-dwelling biped? (See the review of Australopithecus afarensis locomotor adaptations in Stern (2000) and in Coppens and Senut (1991).) The difficulty derived mainly from the fact that before the 1970s scientists had built their phylogenetic trees almost exclusively on the basis of dental anatomy, whereas the incorporation of locomotor traits led to a modification of these phylogenies. The picture became more complex in subsequent years, with a crop of new species of australopithecines being created; several of these had specimens also included in other hypodigms. This was especially clear with Praeanthropus africanus, Australopithecus afarensis, and Australopithecus anamensis. The use of cladistic methods did not clear up the problem (Strait et al. 1997; Strait and Grine 1999, among others), as the Praeanthropus hypodigm of these authors does not include the same fossils as those proposed by Senut in 1996. The phylogenetic approach thus became more and more confused, various scholars using the same species names in different ways without defining them. As discoveries became more and more numerous, several genera were resurrected or created: Praeanthropus, Ardipithecus, Orrorin, Sahelanthropus, and Kenyanthropus. New specimens of a Pliocene hominid, Australopithecus prometheus, were found in South Africa at Sterkfontein (Clarke 1995, 2013). But a major question remains unanswered: Is Australopithecus afarensis a direct ancestor or a side branch of our family?

The Upper Miocene Evidence The majority of scenarios concerning the dichotomy of apes and humans, with the exception of the East Side Story of Coppens (1983), failed to take into account the environment. Coppens’ hypothesis was ecogeographic in nature, the African Rift Valley constituting an ecological barrier between the apes in the West and early hominids in the East from about 7–8 Ma. But the most important elements of his hypothesis were chronological (the divergence took place between 10 and 7 Ma (Coppens 1986; Senut 2006)) and ecological (climatic change engendering modifications in regional vegetation patterns, etc.); and, despite its name, the geographic element was subsidiary in the evolutionary scenario. As soon as we began to look for early and/or putative hominids in strata older than the Pliocene, we found them. In 2000, the discovery of early hominid remains (Orrorin tugenensis) in the Upper Miocene strata of Kenya, and subsequent finds in Middle to Upper Miocene sediments of the same country, shed new light on the question of our divergence from the African apes. The Orrorin discovery was subsequently followed by finds in Ethiopia (Ardipithecus kadabba) and then Chad (Sahelanthropus tchadensis). The debate mainly focused on the C/-P/3 complex and on adaptations to bipedalism. The status of the latter in the two last-named species is still a matter of debate, as the postcranial evidence is either poor or absent. But the main disagreement lies in the fact that in most studies comparisons were made basically with modern apes and later hominids and very little with Miocene apes. As pointed out above, structures or features supposed to Page 8 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_49-2 # Springer-Verlag Berlin Heidelberg 2013

be hominid apomorphies might well be retained from older Miocene apes; and some of the modern African ape features, usually considered to be primitive, might not be so.

Ardipithecus ramidus In 1994 Australopithecus ramidus was published, and in 1995 it was attributed to the new genus Ardipithecus. This hominoid from Aramis localities 1–7 in the Middle Awash (Afar Depression in Ethiopia) (White et al. 1994, 1995) was pronounced to be the earliest-known hominid. All the specimens, except the humerus (which was found above the Daam-Aatu Basaltic Tuff), come from a level located between the Daam-Aatu Basaltic Tuff and the Gaala Vitric Tuff complex. The tuff complex, situated at the base of the section, has been dated at 4.39  0.013 Myr, and an age between 4.2 and 4.5 Ma can be estimated for the fossil hominid (WoldeGabriel et al. 1994). At the time of the discovery, these fossils were among the few supposed hominids older than 4 Ma. Recently, a few more specimens have been described from the Early Pliocene at As Duma in the Gona Western Margin (Ethiopia). Their ages have been estimated at 4.51–4.32 Ma (Semaw et al. 2005). According to its discoverers, the new genus differed from Australopithecus by the reduced megadontia of the postcanine teeth; the greater width of the upper and lower incisors compared with postcanine teeth; a narrow and obliquely elongated lower dm1 with a large protoconid and a small, distally place metaconid without an anterior fovea; a small, low talonid with reduced cuspule development; absolutely and relatively thinner canine and molar enamel; and lower and upper P3s more strongly asymmetrical, with more dominant buccal cusps. With a canine that is not mesiodistally elongated, it is distinguishable from modern African apes. However, some of the cited features – including the thin enamel in the molars, asymmetrical upper and lower third molars, and the size relationships between the incisors and jugal teeth – place Ardipithecus closer to the chimpanzee than to any of the oldest hominids known (Pickford, 2012). The first deciduous molar shows resemblances to those of bonobos. But the morphology of the canine distances Ardipithecus from apes: it is more incisiform than in the latter group. Metric comparisons of the adult teeth were made with Australopithecus afarensis and underline the diminutive size of Ardipithecus. The upper canine/lower anterior premolar complex is typical of apes and was described as being “morphologically and functionally only slightly removed from the presumed ancestral ape condition” (White et al. 1994, p. 308) (though these authors also considered the modern ape morphology plesiomorphic). However, certain features taken as support for its hominid status occur in female apes, which have a reduced canine/premolar complex compared to those of males. Its postcranial bones reveal several apelike features, but the proximal humerus is more humanlike in the shallowness of the bicipital groove. However, this character occurs not only in hominids but also in other primates such as the cautious climber Pongo (Senut 1981). The fragment of occipital preserved would suggest that the foramen magnum is placed anteriorly relative to the carotid foramen, but for the reasons given above, we must be cautious with the interpretation of this feature. At the end of 1994, a skeleton (like a roadkill, according to the authors) was found in the Aramis strata. It was published in 2009 (White et al. 2009) and claimed to be the first representative biped of the human lineage. However, the traits proposed in evidence of bipedalism are not convincing. The reconstruction of the vertebral column is based on only two fragmentary vertebrae. And whereas the femur has been reconstructed to resemble a human one, only the shaft is preserved. This is very massive and robust and has nothing to do with the more gracile, elongated human femur. The humerus, which is not preserved, has been reconstructed like a human one. The bones of the forelimb are set wide apart, rather than close as in humans, and suggest massive forearm muscles as seen in modern African apes. The thumb is short, and its distal phalanx is not hominid-like in morphology. It is elongated and narrow, as in nonhuman hominoids, and lacks the hominid morphology seen in Orrorin, australopithecines, and Homo. The pelvis is Page 9 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_49-2 # Springer-Verlag Berlin Heidelberg 2013

strongly crushed, and the reconstruction appears more hominid-like, based on comparisons with Australopithecus afarensis. Despite the numerous papers on the functional anatomy, and given such weak evidence, it is difficult to accept bipedalism in Ardipithecus ramidus. The study suggests to me that Ardipithecus might be a fossil relative of the chimpanzee. Assuming that the features exhibited in modern chimpanzees were present in its forerunners has been a widespread theme among anthropologists, the bonobo long ago being considered a good model for the hominid ancestor (Zihlman 1984), although this was already criticized at that time (Senut 1988). The idea that the discovery of Ardipithecus ramidus led to the new idea that the chimpanzee is not a good model for the ancestor of hominids (Lovejoy et al. 2009) is thus actually not new. What is more, although the hypothesis appears to be right, it is based on wrong evidence. Among other discoveries, Semaw et al. (2005) briefly described a proximal third of a pedal proximal phalanx from deposits of As Duma dated at 4.51–4.32 Ma. They wrote: “The transversely broad oval proximal facet is oriented dorsally, a character diagnostic of bipedality, and a trait also seen in Ardipithecus kadabba.” But Rose (1986) had already described the same feature in Sivapithecus from the Miocene of Pakistan, making it difficult to accept the proposed bipedalism in A. ramidus. On the basis of the fauna and the botanical and sedimentological indications, the environment of Ardipithecus ramidus at Aramis is a forested one (WoldeGabriel et al. 1994). In the Gona sites, the faunal association, carbon isotopes, and sedimentology suggest a moderate rainfall woodland and woodland/grassland (Semaw et al. 2005).

Orrorin tugenensis The discovery of Orrorin led to the elucidation of several aspects of early hominids (Senut et al. 2001). The specimens come from four sites: Cheboit, Kapsomin, Kapcheberek, and Aragai in the Lukeino Formation aged ca 6 Ma (6–5.8 Ma) (Bishop and Chapman 1970; Bishop and Pickford 1975; Chapman and Brook 1978; Kingston et al. 1994; Pickford and Senut 2001) (Fig. 5). The Lukeino Formation overlies the Kabarnet Trachyte dated by K/Ar, paleomagnetism, and biochronology at 6.1 Ma and is overlain by the Kaparaina Basalt the age of which is estimated to be 5.7 Ma (Sawada et al. 2002). In the section, Cheboit and Aragai are the oldest sites, followed by Kapsomin and then Kapcheberek which lies in the upper level of the formation. Up to now, 20 specimens of Orrorin have been found, consisting of the posterior part of a mandible in two pieces, a symphysis and several isolated teeth, as well as three femoral fragments, a partial humerus, a first phalanx, and a distal thumb phalanx. The genus is defined by its jugal teeth being smaller than those of australopithecines, an upper canine short with a shallow and narrow vertical mesial groove and a low apical height, a small triangular upper M/3, a lower p/4 with offset roots and oblique crown, small Homo-like squarish lower m/2 and m/3, thick enamel on the lower cheek teeth, a buccal notch well developed on the cheek teeth, no cingulum on the molars, a femur with a spherical head rotated anteriorly, the femoral neck elongated and oval in section, a medially salient lesser trochanter, a deep digital fossa, a humerus with a vertical brachioradialis crest, a curved proximal manual phalanx, and a dentition that is small relative to body size. Orrorin differs from Australopithecus in the morphology of the cheek teeth, which are smaller and less elongated mesiodistally. It differs from Ardipithecus by the greater thickness of enamel. It differs from both by the presence of a mesial groove on the upper canine. The upper and lower canines exhibit an apelike morphology, seen in female chimpanzees and Miocene apes; they are reduced in comparison with Pan. The apex of the upper canine is pointed and almost sectorial, and a poorly developed lingual wear facet is visible. The femurs reveal that Orrorin was bipedal (Senut et al. 2001; Pickford et al. 2002; Galik et al. 2004). However, the other postcranial bones suggest that it could climb trees. The distal Page 10 of 24

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Fig. 5 Remains attributed to Orrorin tugenensis in 2000

Fig. 6 Distal thumb phalanx of Orrorin tugensis (right) compared with an extant chimpanzee (left). (a) Dorsal view; (b) Palmar view (scale: 1 cm) (From Senut 2012)

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_49-2 # Springer-Verlag Berlin Heidelberg 2013

phalanx of the thumb exhibits features resembling hominids such as presence of a marked tuft (horseshoe shaped), deep depression for the m. pollicis longus with strongly asymmetrical edges, strongly asymmetrical basal tubercles, and a swelling at the base of the insertion of m. pollicis longus (Gommery and Senut 2006). Some features of the hominid thumb are classically (but probably erroneously) associated with the manufacture of tools; these traits could be related to grasping abilities when climbing trees (Gommery and Senut 2006) (Fig. 6). At the time of its discovery, Orrorin was the first known bipedal hominid older than 5 Ma and indicated that the dichotomy between the African apes and the hominids had to be older than 6 million years and that the classic recent dates of divergences estimated by molecular biologists did not fit with the paleontological evidence. On the other hand, the locomotor and dental features suggest that Orrorin was different from Australopithecus afarensis. It was microdont with small postcanine teeth and a rather large body size, whereas Australopithecus was megadont with large postcanine teeth and small body size. Modern humans are microdont. Some morphometric studies have suggested that Orrorin is an ancestor of later australopithecines (Richmond and Jungers 2008). However, when checked in detail, it appears that their results could be interpreted either way, as Orrorin data fall close to australopithecines and Homo. Orrorin did not live in an open environment, but in a more forested one as suggested by faunal remains that include impalas, colobines, water chevrotains, arboreal civets, fruit bats and lorisids, and floral remains that contain large leaves with drip points (Pickford and Senut 2001; Senut and Pickford 2004; Senut 2006b), from which it is concluded that, in its early stages, bipedalism was not related to dry environments (Senut 2006b). Humid conditions persisted into the Lower Pliocene (Pickford et al. 2004). Stable isotope analyses of tooth enamel carbonate of large herbivores from the Lukeino and the Mabaget Formations are consistent with the first results (Roche et al. 2013) and refine them. They show that in the Early Pliocene and the latest Miocene, conditions were more humid than in the Upper Miocene. Orrorin inhabited a mixed C3–C4 environment comprised of thicket, woodland, and forest. Fossil leaves from the Lukeino Formation indicate the presence of woodland and dry evergreen forest, but some specimens suggest a more humid forest (Bamford et al. 2013).

Ardipithecus kadabba Material discovered in Ethiopia (Haile-Selassie, 2001) from sediments aged between 5.2 and 5.7 Ma was identified as belonging to a subspecies of Ardipithecus ramidus, later raised to the specific rank Ardipithecus kadabba (Haile-Selassie et al. 2004). The material was collected at five different sites: Digiba Dora, Asa Koma, Alayla, Saitune Dora, and Amba East, from the Asa Koma Member of the Adu-Asa Formation. The first four are in the Asa Koma Member of the Adu-Asa Formation, and the deposits which have yielded the hominids are securely dated at 5.54–5.77 Myr by radiometric methods applied to underlying and overlying basalts. The Amba East material is slightly younger, being from the Kuseralee Member of the Satangole Formation dated 5.2–5.6 Ma (Renne et al. 1999). The morphology of the upper canine crown with a more rounded outline differs from Orrorin; but it also differs from Ardipithecus ramidus in the crest pattern of the same tooth as well as by a lower premolar that is more asymmetrical in outline and by the presence of a small anterior fovea. Moreover, the lingual cusps are more salient and sharp in the lower m/3 and the upper M3/ bears four cusps. The species Ardipithecus kadabba differs from extant apes in its canines, which have a tendency to be incisiform as in A. ramidus, and by the presence of a clearly defined fovea on the lower p/3 which is isolated from the mesial marginal ridge by a fold-like buccal segment. However, some of Page 12 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_49-2 # Springer-Verlag Berlin Heidelberg 2013

the Ardipithecus kadabba dental specimens could belong to Orrorin tugenensis. It is difficult to know, as the material is not available for comparisons. The postcranial morphology (Haile-Selassie 2001) indicates several similarities to African apes and selected specimens from the Hadar, but the shape of the ulnar olecranon differs from that of hominids. A proximal pedal phalanx resembles the ones from Hadar, and on the basis of the dorsal orientation of the proximal facet of the bone, it supposedly belonged to a biped. However, the curvature seen in the Ardipithecus kadabba phalanx might be linked with arboreal adaptations, as discussed by several authors (Susman et al. 1984; Stern and Susman 1983), and we must remain careful when assessing a locomotor complex on the basis of restricted material. Ardipithecus kadabba is associated with relatively wet and wooded environments as indicated by the fauna. However, the Amba East site seems to have been slightly drier (WoldeGabriel et al. 2001).

Sahelanthropus tchadensis The discovery of Sahelanthropus in Chad was published in 2002 (Brunet et al. 2002). Announced as the earliest-known hominid, this status has been the subject of debate (Wolpoff et al. 2002, 2006; Wood 2002). It was found at Toros-Menalla (Chad) in deposits supposedly dated between 6 and 7 Ma, maybe closer to 7 Ma, by faunal comparison with the Lukeino Formation and Nawata Formation (Vignaud et al. 2002). Recent Be/Al analyses performed on the levels hypothetically associated with the Sahelanthropus skull yielded a date between 7.2 and 6.8 Ma (Lebatard et al. 2008). However, some of the faunal remains found with the hominoid (discovered at the surface of the deposits), such as the Anthracotheriidae (Pickford 2008) and the fossil otters, could suggest the presence of two different biostratigraphic levels. In the latter case, data published on Dikika (Pliocene Australopithecine site in Ethiopia) (Geraads et al. 2011) based on results from Chad (Peigné et al. 2008) would suggest the presence of Pliocene fauna at Toros-Menalla. The age of the hominoid material remains uncertain. The following diagnostic features of the species have been published: orthognathic face and weak subnasal prognathism; small ape-sized braincase; long and narrow basicranium; small canines; robust supraorbital torus; absence of supratoral sulcus; marked postorbital constriction; small, posteriorly located sagittal crest and large nuchal crest; wide interorbital pillar; low-crowned jugal teeth and enamel thickness between that of Pan and Australopithecus; and anterior position of the foramen magnum. It is considered to be different from all the living great apes because of the relatively small canines, the apical wear of the canines, and a probable non-honing C/-P/3 complex. The claimed hominid status is based on the small, apically worn canine and on the structure of the face. However, when these complexes are considered among all fossil and extant hominoids, it appears that they are more frequent than believed. The maxillofacial complex in extant apes varies according to sex, just as it does in Miocene hominoids (Proconsul, Kenyapithecus, Ramapithecus). It was this combination of features that originally led to Ramapithecus being proposed as a hominid, whereas it is today considered to be the female of Sivapithecus. Bipedalism in Sahelanthropus has been inferred from the position of the foramen magnum; but again, for the reasons expressed above, this feature can be misleading. The cranial base and nuchal area of Sahelanthropus (with its strongly developed nuchal crest and the flatness of the occipital) seem more apelike to some authors (Wolpoff et al. 2002, 2006), suggesting a quadrupedal posture and locomotion despite the reconstruction proposed by Zollikofer et al. (2005), which fails to contribute more evidence to the debate. The orientation of the plan of the foramen magnum falls within the range of variation of modern apes (Pickford 2005). Whatever Sahelanthropus is, its status as a hominid is still debatable (Wood 2002), although it importantly fuels the debate on the origins of African apes and humans. Page 13 of 24

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Sahelanthropus was found in perilacustrine sandstones, and the sedimentological context suggests a mosaic of environments between lake and desert, which have been compared with the modern Okavango delta. But the geological setting is different, as Lake Chad was much deeper in the Upper Miocene than the Okavango is today.

An Earlier Dichotomy? During the past decade, several apelike fossils have been discovered in Africa that complete the data from the Samburu Hills (Ishida et al. 1984; Ishida and Pickford 1998). In the Baringo District of Kenya (Figs. 7 and 8), a lower molar in the 12.5 Ma Ngorora Formation and three fragmentary teeth from the Lukeino Formation are found in the same strata as Orrorin tugenensis (Pickford and Senut 2005); some isolated teeth at Chorora in Ethiopia are attributed to an ancestor of gorilla (Suwa et al. 2007). Also, a fragmentary mandible and isolated teeth come from Nakali (Kunimatsu et al. 2007), and a fragment of mandible of a proto-chimpanzee comes from Niger (Pickford et al. 2009). This new evidence sheds some crucial light on the dichotomy between African apes and humans.

Ngorora In 1999, a lower molar was collected at Kabarsero, Ngorora Formation, Tugen Hills (Pickford and Senut 2005) 12.5 Ma (Bishop and Pickford 1975). This tooth, probably a lower m/2 (Pickford and Senut 2005), is close in morphology to Dryopithecus (Begun 2002) and chimpanzees and distant from similarly aged Kenyapithecus and Otavipithecus (Conroy et al. 1992; Ward and Duren 2002). An upper molar had already been described from Ngorora (Bishop and Chapman 1970; Bishop and Pickford 1975; Leakey 1970), but it appears to be closer in morphology to Kenyapithecus (Ishida and Pickford 1998; Pickford and Ishida 1998; Senut 1998), and the thickness of the enamel and the more centralized cusps suggest that it belongs to a different hominoid from the lower molar. Two different kinds of hominoids would have coexisted at Kabarsero, a possibility which is also suggested in the lower (Napak) and middle (Moroto) Miocene sites of Uganda (Gommery et al. 1998, 2002). If the derived characters of the Ngorora tooth are homologous to those of chimpanzees, then it would indicate that chimpanzees were already a separate lineage by the end of the Middle Miocene, a suggestion that accords with some interpretations of the molecular data (Arnason et al. 2001) and recent genetic studies (Langergraber et al. 2012). The resemblances between the Ngorora tooth and Dryopithecus indicate that the latter genus may have originated in Africa and migrated toward Europe about 12.5 Ma.

Chorora Nine isolated teeth discovered in the Chorora area (site of Beticha) have been attributed to Chororapithecus abyssinicus (Suwa et al. 2007). They were found in the upper part of the Chorora Formation dated at around 10.7–10.1 Ma. These teeth are close in size to, and resemble, those of Gorilla gorilla. They show clearly marked crests on the teeth, suggesting that they fed on fibrous plants that they sheared; but the cusps are less high and more peripheralized. The cingulum is weaker than in Gorilla and the thick-enameled molars are slightly larger. The faunal remains, rich in primates and poor in Hipparion, indicate that the environment of Chororapithecus was humid. Sedimentation suggests that Chororapithecus was living close to a lake shore and that there were alternating humid and more open spaces. Page 14 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_49-2 # Springer-Verlag Berlin Heidelberg 2013

Fig. 7 (a) Bar 91'99, right lower molar, stereo occlusal view; (b) Pan paniscus right m/2, occlusal view; (c) Pan troglodytes, right m/2, occlusal view; (d–f) Dryopithecus brancoi lower molars from Europe, D ¼ Trochtelfingen, E ¼ Salmendingen, F ¼ Ebingen; (g) Gorilla gorilla lower m/2, occlusal view; (h–j) Bar 1757'02, Kapsomin large ape, occlusal, lingual, and oblique views; (k) Gorilla gorilla lower m/2, oblique view; (l) Australopithecus afarensis, upper m/2, occlusal view; (m) Gorilla gorilla upper M2/, occlusal view; (n) Pan troglodytes, upper M1/–M/3 occlusal view; (o) Orrorin tugenensis upper molar row, occlusal view; (p) Bar 1757'02, detail of dentine-enamel junction at hypoconulid; (q) KNM LU 335, Orrorin tugenensis, left m/3, occlusal view; (r) Praeanthropus africanus cast of upper incisor from Laetoli, lingual view; (s) BAR 1001’01, Kapsomin large ape, I1/, lingual view; (t) Gorilla gorilla upper central incisor, lingual view; (u) Praeanthropus africanus cast of upper incisor from Laetoli, distal view; (v) Bar 1001’01, Kapsomin large ape, I1/, distal view; (w) Gorilla gorilla upper central incisor, distal view

According to the authors, these teeth might represent a proto-Gorilla. If so, then, this find confirms the idea that the split between gorillas and chimpanzees and humans has to be at least 10 million years old.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_49-2 # Springer-Verlag Berlin Heidelberg 2013

Fig. 8 Hominoid right mandibular fragment (1964-27-885) from Niger. (a) Buccal view; (b) Lingual view; (c) Occlusal view (scales: 1 cm)

Nakali A few months after the discovery of the Ethiopian teeth, Kunimatsu and his team unearthed specimens belonging to another species of fossil hominoid from the Upper Miocene (9.88–9.80 Ma) at Nakali in Kenya: Nakalipithecus nakayamai (Kunimatsu et al. 2007). The reported material is composed of a posterior portion of a mandibular fragment and 11 isolated teeth. The teeth are close in size to females Gorilla or Pongo. The molars are thick-enameled, and their general morphology differs from other known hominoids in the canine and several premolar traits. It shares some similarities with the slightly younger Ouranopithecus from Greece but is more primitive. The authors suggest that it could be close to the last common ancestor to African apes and humans; but it could also belong to the lineage of the gorillas. Whatever it is, it evidences the fact that Africa was not devoid of large-bodied hominoids in the Upper Miocene.

Kapsomin In 2002, half an upper molar of a large hominoid was found at Kapsomin, Lukeino Formation, aged 5.9 Ma (Pickford and Senut 2005). This tooth is larger than those of Orrorin tugenensis and the crown morphology is different. The trigon is wide, the distal fovea is broad, the main cusps are high and less inflated, and there is a deep buccal slit. Dentine penetration is also high. Most of these features occur in Gorilla and are different from Pan. In 2000, an upper central incisor was found in the same strata as Orrorin. Originally assigned to Orrorin tugenensis, its morphology did not seem to fit with the early hominid. After a restudy of the specimen, it appears that it differs strongly from australopithecines and other hominids because of the lack of fossa on the lingual side of the tooth. Moreover, the crown is relatively low compared to root length, whereas in hominids the crown is higher with a scoop-shaped profile. In contrast, in Gorilla incisors, the lingual fossa is missing and the crown is wedge shaped as in the Kapsomin tooth. In 2003, a lower molar was found at Cheboit, near the site of discovery of the first hominid tooth from the Lukeino Formation (Pickford 1975). The morphology of the tooth is compatible with the half upper molar from Kapsomin, and the specimens probably belong to the same taxon. As for Ngorora and the Ugandan sites, two different hominoids would have coexisted at Kapsomin in the same strata, 6 million years ago.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_49-2 # Springer-Verlag Berlin Heidelberg 2013

Niger Discovered in 1964 in Niger, a right mandibular fragment with the roots of the lower M1 of a hominoid has been identified recently (Pickford et al. 2009). Comparisons with fossil and modern hominoids indicate similarities with Pan troglodytes. The faunal remains associated with the specimen suggest an Upper Miocene age between 11 and 5 million years. Furthermore, they suggest the presence of large river or a freshwater lake, indicating a more humid environment in the area than is the case today. This discovery is important, as it shows that hominoids were widespread in Africa in the Upper Miocene and it fills a gap in what is known of the distributions of African apes and their origins and sheds light on the dichotomy between humans and chimpanzees.

Conclusions The debate about our earliest origins is probably not closed and is fueled by the poverty of fossils in the time period between 12 and 4 million years ago. This is why it is necessary to continue excavation and prospecting in different areas of Africa in order to fill the gaps and extend our knowledge of variation and diversity. As a matter of fact, recent surveys in Western Uganda led to the discovery of Upper Miocene and Pliocene faunas (including mammals) in an area supposed to be of Pleistocene age (Pickford et al. 2013). In Northern Namibia, new Upper Miocene and Pliocene deposits have been identified that have yielded mammals (Miller et al. 2010). One of the most troubling aspects of the research done to date on the origins of hominids relates to the comparative samples. Most scientists still focus on modern hominoids as a good reference for primitive morphologies. However, these animals are highly derived in their cranial and postcranial anatomy. As long as Miocene apes are not properly considered in these studies, we will remain trapped in the quest for a mythical missing link. Of all the features used to define hominids, probably the least controversial is bipedalism. We know that in the past there have been several types of bipedalism, but there is definitely a basic one that is known in australopithecines, Orrorin, and Homo. In this group, adaptation to arboreality is variable: greater in some taxa, less in some others, and very little in Homo. There was probably a variety of early forms of hominids: the oldest widely accepted biped (supported by postcranial evidence) is Orrorin, and we await further data on Ardipithecus (arm, knee, and hip joints) and Sahelanthropus to clarify their status (Fig. 3). What the evidence from the Upper Miocene tells us is that we cannot continue to support an origin of the earliest hominids in dry savannah-like conditions: in contrast, they inhabited humid to forested environments. These early hominids cohabited with apes, and we are only just beginning to uncover the history of modern apes, of which we know only a small, emergent part of the iceberg: this is the challenge of the third millennium.

Cross-References ▶ Analyzing Hominin Phylogeny ▶ Defining Hominidae ▶ Fossil Record of the Primates from the Paleocene to the Oligocene ▶ Hominoid Cranial Diversity and Adaptation ▶ Modeling the Past: The Primatological Approach ▶ Patterns of Diversification and Extinction Page 17 of 24

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_49-2 # Springer-Verlag Berlin Heidelberg 2013

▶ Phylogenetic Relationships (Biomolecules) ▶ Potential Hominoid Ancestors for Hominidae ▶ Species Concepts and Speciation: Facts and Fantasies ▶ The Earliest Putative Homo Fossils ▶ The Origins of Bipedal Locomotion ▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments ▶ The Species and Diversity of Australopiths ▶ Zoogeography: Primate and Early Hominin Distribution and Migration Patterns

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Ishida H, Pickford M, Nakaya H, Nakano Y (1984) Fossil anthropoids from Nachola and Samburu Hills. African Studies Monograph, Supplementary Issue 2:73–85 Johanson D, Taieb M (1976) Plio-Pleistocene discoveries in Hadar, Ethiopia. Nature 260:293–297 Johanson DC, White TD, Coppens Y (1978) A new species of the genus Australopithecus (Primates, Hominidae) from the Pliocene of Eastern Africa. Kirtlandia 28:1–14 Kingston JD, Marino BD, Hill AP (1994) Isotopic evidence for Neogene hominid palaeoenvironments in the Kenya Rift valley. Science 264:95–959 Köhler M, Moyà-Solà S (1997) Ape-like or hominid-like? The positional behavior of Oreopithecus bambolii reconsidered. Proc Natl Acad Sci USA 94:11747–11750 Kunimatsu Y, Nakatsukasa M, Sawada Y, Sakai T, Hyodo M, Hyodo H, Itaya T, Nakaya H, Saegusa H, Mazurier A, Saneyoshi M, Tsujikawa H, Yamamoto A, Mbua E (2007) A new Late Miocene great ape from Kenya and its implications for the origins of African great apes and humans. Proc Natl Acad Sci USA 104:19220–19225 Langergraber KE, Pr€ ufer K, Rowney C, Boesch C, Crockford C, Fawcett K, Inoue E, InoueMuruyamag M, Mitani JC, Muller MN, Robbins MM, Schubert G, Stoinski TS, Viola B, Watts D, Wittig RM, Wrangham RW, Zuberb€ uhler K, Pääbo S, Vigilant L (2012) Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. Proc Natl Acad Sci USA 109(39):15716–15721 Leakey LSB (1961/1962) A new lower Pliocene fossil primate from Kenya. Ann Mag Nat Hist 13(4):689–696 Leakey LSB (1970) In: Bishop WW, Chapman D (eds) Early Pliocene sediments and fossils from Northern Kenya Rift Valley. Nature 226:914–918 Lebatard AE, Bourlès DL, Duringer P, Jolivet M, Braucher R, Carcaillet J, Schuster M, Arnaud N, Monié P, Lihoreau F, Likius A, Mackaye HT, Vignaud P, Brunet M (2008) Cosmogenic nuclide dating of Sahelanthropus tchadensis and Australopithecus bahrelghazali: Mio-Pliocene hominids from Chad. Proc Natl Acad Sci USA 105(9):3226–3231 Lovejoy OC, Suwa G, Simpson SC, Matternes JH, White T (2009) The great divides: Ardipithecus ramidus reveals the postcrania of our last common ancestors with African apes. Science 326:100–106 Marks J (2002) What does it mean to be 98 % chimpanzee? California Press, Berkeley, pp 1–312 Miller R McG, Pickford M, Senut B (2010) The geology, palaeontology and evolution of the Etosha Pan, Namibia: implications for terminal Kalahari deposition. S Afr J Geol 113:307–334 Patterson B (1966) A new locality for Early Pleistocene fossils in north-western Kenya. Nature 212:577–581 Patterson B, Howells WW (1967) Hominid humeral fragment from Early Pleistocene of Northwestern Kenya. Science 156:64–66 Patterson B, Behrensmeyer AK, Sill WD (1970) Geology and fauna of a new Pliocene locality in north-western Kenya. Nature 226:918–921 Peigné S, de Bonis L, Likius A, Mackaye HT, Vignaud P, Brunet M (2008) Late Miocene Carnivora from Chad: Lutrinae (Mustelidae). Zool J Linn Soc 152:793–846 Pickford M (1975) Late Miocene sediments and fossils from the Northern Kenya Rift Valley. Nature 256:279–284 Pickford M (1986) Sexual dimorphism in Proconsul. In: Pickford M, Chiarelli B (eds) Sexual dimorphism in primates. Il Sedicesimo, Florence, pp 133–170 Pickford M (1987) The diversity, zoogeography and geochronology of monkeys. Hum Evol 2(1):71–89

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Pickford M (2005) Orientation of the foramen magnum in Late Miocene to extant African apes and hominids. Anthropologie Brno 43(2–3):103–110 Pickford M (2008) Libycosaurus petrocchii Bonarelli, 1947, and Libycosaurus anisae (Black, 1972) (Anthracotheriidae, Mammalia): Nomenclatural and geochronological implications. Ann Paléontol 94:39–55 Pickford M (2012) Orrorin and the African ape/hominid dichotomy. In: Reynolds SC, Gallagher A (eds) African genesis – Perspectives on hominin evolution. Cambridge University Press, Cambridge, pp 99–119 Pickford M, Chiarelli B (eds) (1986) Sexual dimorphism in primates. Il Sedicesimo, Florence Pickford M, Ishida H (1998) Interpretation of Samburupithecus, an Upper Miocene hominoid from Kenya. CR Acad Sci Paris IIa 326:299–306 Pickford M, Senut B (2001) The geological and faunal context of Late Miocene hominid remains from Lukeino, Kenya. CR Acad Sci Paris 332:145–152 Pickford M, Senut B (2005) Hominoid teeth with chimpanzee- and gorilla-like features from the Miocene of Kenya: implications for the chronology of ape-human divergence and biogeography of Miocene hominoids. Anthropol Sci 113:95–102, published on line13th July 2004 Pickford M, Senut B, Gommery D, Treil J (2002) Bipedalism in Orrorin tugenensis revealed by its femora. CR Palevol 1:191–203 Pickford M, Coppens Y, Senut B, Morales J, Braga J (2009) Late Miocene hominoid from Niger. CR Palevol 8:413–425 Pickford M, Senut B, Mourer-Chauviré C (2004) Early Pliocene Tragulidae and peafowls in the Rift Valley, Kenya: evidence for rainforest in East Africa. CR Palevol 3:179–189 Pickford M, Senut B, Musalizi S, Gommery D, Ségalen L, Musiime E (2013) Miocene Vertebrates of the Packwach area, West Nile, Uganda. Geo-Pal Uganda 5:1–27 Pilbeam D (1996) Genetic and morphological records of the Hominoidea and hominid origins: a synthesis. Mol Biol Evol 5:155–168 Renne PR, WoldeGabriel G, Hart WK, Heiken G, White TD (1999) Chronostratigraphy of the Miocene-Pliocene Sagantole Formation, Middle Awash Valley, Afar Rift, Ethiopia. Geol Soc Ann Bull 111:869–885 Richmond B, Jungers WL (2008) Orrorin tugenensis femoral morphology and the evolution of Hominin bipedalism. Science 319:1662–1665. doi:10.1126/science.1154197 Roche D, Ségalen L, Senut B, Pickford M (2013) Stable isotope analyses of tooth enamel carbonate of large herbivores from the Tugen Hills deposits: Palaeoenvironmental context of the earliest Kenyan hominids. E P S L 381:39–51 Rook L, Bondioli L, Köhler M, Moyà-Solà S, Macchiarelli R (1999) Oreopithecus was a bipedal ape after all: evidence from the iliac cancellous architecture. Proc Natl Acad Sci USA 96:8795–8799 Rose M (1986) Further hominoid postcranial specimens from the Late Miocene Nagri Formation of Pakistan. J Hum Evol 15:333–367 Sarmiento E (1983) Some functional specializations in the skeleton of Oreopithecus bambolii and their phylogenetic significance. Am J Phys Anthrop 60:248–249 Sawada Y, Pickford M, Senut IT, Hyodo M, Miura T, Kashine C, Chujo T, Fuji H (2002) The age of Orrorin tugenensis, an early hominid from the Tugen Hills, Kenya. CR Palevol 1:293–303 Schaeffer MS (1999) Foramen magnum – carotid foramina relationship: is it useful for species designation? Am J Phys Anthrop 110:467–471 Schultz AH (1955) The position of the occipital condyles and of the face relative to the skull base in primates. Am J Phys Anthrop 13(1):97–120

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Schultz AH (1960) Einige Beobachtungen und Masse am Skelett von Oreopithecus. Z Morphol Anthropol 2:197–311 Semah S, Simpson SW, Quade J, Renne PR, Butler RF, McIntosh WC, Levin N, DominguezRodrigo M, Rogers MJ (2005) Early Pliocene hominids from Gona Ethiopia. Nature 433:301–305 Senut B (1981) L'humérus et ses articulations chez les Hominidés plio-pléistocènes. Cahiers de Paléontologie (Paléoanthropologie), publiés sous la direction. d'Y. Coppens, C.N.R.S, Paris Senut B (1988) The evolution of human bipedalism: general considerations. Ossa 14:33–34 Senut B (1989) Le coude des primates hominoïdes, Cahiers de Paléontologie (Paléoanthropologie). CNRS, Paris Senut B (1992) French contribution to the study of human origins: the case of Australopithecus afarensis. Hum Evol 7(4):15–24 Senut B (1996) Pliocene hominid systematics and phylogeny. S Af J Sci 92(4):165–166 Senut B (1998) Grands singes fossiles et origine des hominidés. Primatologie 1:91–134 Senut B (2003) Palaeontological approach to the evolution oh hominid bipedalism: the evidence revisited. Courrier Forschungs Senckenberg 243:125–134 Senut B (2006a) Bipédie et climat. CR Palevol 5:89–98 Senut B (2006b) The “East Side Story” twenty years later. Trans Roy Soc S Afr, Special Issue A Festschrift to H.B.S. Cooke 61(2):103–109 Senut B (2011a) Origin of hominids: European or African origin, neither or both? Estudios Geológicos 67(2):395–409 Senut B (2011b) Fifty years of debate on the origins of human bipedalism. J Biol Res 1(LXXXIV) Rubbettino-Soveria Mannelli:37–46 Senut B (2012) From hominid arboreality to hominid bipedalism. In: Reynolds SC, Gallagher A (eds) African genesis – Perspectives on hominin evolution. Cambridge University Press, Cambridge, pp 77–98 Senut B, Pickford M (2004) La dichotomie grands singes- hommes revisitée. CR Palevol 3:265–276 Senut B, Pickford M, Gommery D, Mein P, Cheboi K, Coppens Y (2001) First hominid from the Miocene (Lukeino Formation, Kenya). CR Acad Sci Paris 332:137–144 Simons EL (1961) The phyletic position of Ramapithecus. Postilla YPM 57:1–9 Simons EL, Pilbeam D (1965) A preliminary revision of Dryopithecinae (Pongidae, Anthropoidea). Folia primatol 3:81–152 Stanyon R (1989) Implications of biomolecular data for human origins with particular reference to chromosomes. In: Giacobini G (ed) Hominidae. Jaca Book, Milan, pp 35–44 Stern JT (2000) Climbing to the top: a personal Memoir of Australopithecus afarensis. Evol Anthropol 9(3):113–133 Stern JT, Susman R (1983) The locomotor anatomy of Australopithecus afarensis. Am J Phys Anthrop 60:279–317 Strait DS, Grine FE (1999) Cladistics and early hominid phylogeny. Science 285:1210 Strait DS, Grine FE, Moniz MA (1997) A reappraisal of early hominid phylogeny. J Hum Evol 32:17–82 Straus W (1963) The classification of Oreopithecus. In: Washburn SL (ed) Classification and human evolution. Aldine, Chicago, pp 146–177 Susman RL, Stern JT, Jungers WL (1984) Arboreality and bipedality in the hadar hominids. Folia Primatol 43:113–156 Suwa G, Kono RT, Katoh S, Asfaw B, Beyene Y (2007) A new species of great ape from the Late Miocene epoch in Ethiopia. Nature 448:921–924 Page 22 of 24

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Tardieu C (1983) Analyse morphofonctionnelle de l’articulation du genou chez les primates. Application aux Hominidés fossiles. Cahiers de Paléoanthropologie, CNRS, Paris Vignaud P, Duringer P, Mackaye HT, Likius A, Blondel C, Boisserie J-R, de Bonis L, Eisenmann V, Etienne M-E, Geraads D, Guy F, Lehmann T, Lihoreau F, Lopez-Martinez N, Mourer-Chauviré C, Otero O, Rage J-C, Schuster M, Viriot L, Zazzo A, Brunet M (2002) Geology and palaeontology of the Upper Miocene Toros-Menalla hominid locality, Djurab Desert. Nature 418:152–155 Ward SC, Duren DL (2002) Middle and late Miocene African hominoids. In: Hartwig WC (ed) The primate fossil record. Cambridge University Press, Cambridge, pp 385–397 White TD, Suwa G, Asfaw B (1994) Australopithecus ramidus, a new species of early hominid from Aramis, Ethiopia. Nature 371:306–312 White TD, Suwa G, Asfaw B (1995) Australopithecus ramidus, a new species of early hominid from Aramis Ethiopia: a corrigendum. Nature 375:88 White TD, Asfaw B, Beyene Y, Haile-Selassie Y, Lovejoy CO, Suwa G, WoldeGabriel G (2009) Ardipithecus ramidus and the palebiology of early hominids. Science 326:75–86 Wildman DE, Uddin M, Liu G, Grossman LI, Goodman M (2003) Implications of natural selection in shaping 99.4 % nonsynonymous DNA identity between humans and chimpanzees: enlarging genus Homo. Proc Natl Acad Sci USA 100(12):7181–7188 Wilson A, Sarich V (1969) A molecular time scale for human evolution. Proc Natl Acad Sci USA 63:1088–1093 WoldeGabriel G, White TD, Suwa G, Renne P, de Heinzelin J, Hart WK, Helken G (1994) Ecological and temporal placement of early Pliocene hominids at Aramis, Ethiopia. Nature 371:330–333 WoldeGabriel G, Haile-Selassie Y, Renne PR, Hart WK, Ambrose SH, Asfaw B, Heiken G, White T (2001) Geology and palaeontology of the Late Miocene Middle Awash valley, Ethiopia, Afar Rift, Ethiopia. Nature 412:175–181 Wolpoff MH, Senut B, Pickford M, Hawks J (2002) Sahelanthropus or Sahelpithecus? Nature 419:581–582 Wolpoff MH, Hawks J, Senut B, Pickford M, Ahern J (2006) An ape or the ape: Is the Toumaï cranium TM 266 a hominid ? Paleoanthropology 2006:36–50 Wood BA (2002) Hominid revelations from Chad. Nature 418:133–135 Zihlman A (1984) Body build and tissue composition in Pan paniscus and Pan troglodytes with comparisons to other hominoids. In: Susman RL (ed) The pygmy chimpanzee. Plenum Press, New York, pp 179–200 Zollikofer C, Ponce de Léon M, Lieberman D, Guy F, Pilbeam D, Likius A, Mackaye H, Vignaud P, Brunet M (2005) Virtual reconstruction of Sahelanthropus tchadensis. Nature 434:755–759

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_49-2 # Springer-Verlag Berlin Heidelberg 2013

Index Terms: Ardipithecus kadabba 12 Australopithecus afarensis 8 Australopithecus ramidus 9 Bipedalism 7 Hominids 1 Kapsomin 16 Kenyapithecus 5 Ngorora formation 14 Orrorin 10 Ramapithecus 5 Sahelanthropus 13

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_50-3 # Springer-Verlag Berlin Heidelberg 2014

The Species and Diversity of Australopiths William H. Kimbel* Institute of Human Origins, School of Human Evolution and Social Change, Arizona State University, Tempe, AZ, USA

Abstract In this chapter, the historical, systematic, and anatomical evidence for the diversity of the species within the australopith grade is reviewed. Given a strict evolutionary species definition, nominal taxonomic diversity and species-lineage diversity do not necessarily map onto one another in the fossil record. Species lineages entail statements of ancestry and descent that depend on the consistency of phylogenetic and stratophenetic data. The requirements for identifying species lineages in the fossil record are severe and in the early hominin record are rarely met, most often owing to small sample size, underrepresented character data, nonrepresentation of rare or short-lived taxa, poor chronological resolution, gaps in the time-stratigraphic framework, or some combination of these factors. Because hypotheses concerning the “bushiness” of the hominin phylogenetic tree depend on the identification of lineages, not phenetically based “paleospecies,” confidence with respect to this issue is not justified for the majority of the hominin fossil record. There are two cases in which an approach to this question can be attempted. In one, the evidence is consistent with the evolution of Australopithecus anamensis into A. afarensis via anagenesis. The other, the evolution of A. boisei, most likely entailed a speciation event that gave rise to southern African clade (represented by A. robustus) subsequent to the appearance of A. aethiopicus. The late Pliocene time period in which the latter events transpired (ca. 2.8–2.3 Ma) is one of substantial morphological diversity, high nominal taxonomic diversity, and high probability of synchronicity among known fossil samples. With the exception of the close phylogenetic relationship of A. africanus to A. sediba, it is not possible to connect the later Pliocene australopith taxa (A. aethiopicus, A. garhi) to particular descendants due to defects in the database. Nevertheless, this time period probably documents a previously (and subsequently) unmatched degree of lineage proliferation compared to other parts of the human evolutionary record. The challenge to paleoanthropologists is to devote resources to improving this part of the fossil record and then to create testable phylogenetic and adaptive hypotheses to explain it.

Introduction The australopiths constitute a taxonomically and adaptively diverse group of extinct hominins that are currently known to have inhabited the African continent between approximately 4.2 and 1.4 million years ago (Ma). The documented geographical distribution of this group includes presentday South Africa, Malawi, Tanzania, Kenya, Ethiopia, and Chad but certainly may have been wider. Evidence from pelvic, knee, ankle, and foot morphology and, where available, trace fossils (i.e., the Laetoli footprint trails) indicates that these hominins were terrestrial striding bipeds, more similar, if not identical, in their locomotion to living humans (and extinct representatives of the genus Homo) than to any other known primate, living or extinct. The australopiths were impressively more *Email: [email protected] Page 1 of 30

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_50-3 # Springer-Verlag Berlin Heidelberg 2014

variable in their skull and dental morphology than in their postcranial form, though the latter is poorly documented for some of the species included in the group. Our understanding of their taxonomic and adaptive diversity therefore reflects an historically important preoccupation with anatomical distinctions above the neck, particularly in the dentition and the bony structures thought to be associated with the masticatory system. Many more characters distinguish the australopith species from one another than link them together as a group. Apart from bipedality, shared australopith characteristics include: 1. An approximately ape-size brain (range ca. 375–550 cm3) 2. Inferosuperiorly short, vertical midface with massive zygomaticomaxillary region and strong subnasal prognathism 3. Short, wide basicranium with anteriorly positioned foramen magnum 4. Absolutely small, nonhoning canines 5. Large (in relation to body size) premolars and molars capped by variably thick enamel 6. Transversely thick mandibular bodies and tall ascending rami Although these traits may, in combination, identify the australopiths, they do not diagnose them as a “natural” (i.e., monophyletic) group, as none of the listed features is unique to the group (i.e., they are not autapomorphies; they are either symplesiomorphies-shared with the great ape outgroup to hominins, such as small brain size and strong subnasal prognathism, or synapomorphies-shared with one or more species in the closest sister taxon, Homo, such as bipedal locomotion, reduced canines, short cranial base, and, at least in comparison to some early species usually attributed to Homo, postcanine megadonty). As such, the australopiths most likely constitute a paraphyletic group, identified by its unique adaptive grade among the hominins (small-brained, small-canined, megadont bipeds). This idea is reflected in the entrenched tendency to use the genus Australopithecus as a “waste basket” taxon for any and all of the extinct hominin species whose skeletal and inferred behavioral characteristics fit this adaptive pattern, notwithstanding the likelihood that one or more monophyletic groups, such as the so-called “robust” australopith species (sometimes attributed to genus Paranthropus), are thus subsumed within it.

Historical Perspective on Australopith Diversity The first described australopith species was Australopithecus africanus Dart 1925, identified on the basis of a fossil juvenile skull and brain endocast from the site of the Buxton Limeworks at Taung, Orange Free State (now Free State), South Africa. During the 1930s–1940s, no fewer than four additional species (in three genera) were identified based on adult craniodental fossils recovered from brecciated sediments within collapsed and eroded karstic structures then being mined for lime in South Africa (Sterkfontein 1936; Kromdraai 1938; Makapansgat 1947; Swartkrans 1948). The early taxonomy of the australopiths was authored by paleontologist Robert Broom (1950), who conducted the excavations at Sterkfontein, Kromdraai, and Swartkrans and perceived a different species at each site (Table 1). Broom’s protégé John Robinson subsequently collapsed this taxonomy to one species within each of two genera (Table 1) based on his scenario of a dichotomous partitioning of dietary resources by these early hominins (Robinson 1954). Robinson’s simplified taxonomy and hypothesis of a morphologically specialized herbivore Paranthropus and a more generalized omnivore (and presumptively meat-eating and toolmaking) Australopithecus has had

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_50-3 # Springer-Verlag Berlin Heidelberg 2014

Table 1 The evolution of australopith taxonomy during the 1950s Site Taung Sterkfontein Makapansgat Kromdraai Swartkrans a

Broom (1950) Australopithecus africanus Dart 1925 Plesianthropus transvaalensis (Broom 1936)a Australopithecus prometheus Dart 1948 Paranthropus robustus Broom 1938 Paranthropus crassidens Broom 1949

Robinson (1954) Australopithecus africanus Australopithecus africanus Australopithecus africanus Paranthropus robustus Paranthropus robustus

Broom initially assigned the species transvaalensis to Australopithecus

a profound effect on subsequent australopith systematics. It remains the leading explanatory paradigm for the evolution of these hominins to the present day. Much of the early debate about the australopiths’ role in human evolution had less to do with their adaptations or diversity than with their suitability as human ancestors. The skepticism that greeted Dart’s claims of human ancestral status for A. africanus is well known, and despite the subsequent demonstration by Broom (1939; Broom and Schepers 1946), Gregory and Hellman (1939), Clark (1947), and others of uniquely human characteristics in adult australopith teeth, jaws, and basicrania, it was not until the identification of humanlike bipedal adaptations – and the absence of apelike quadrupedal ones – in a distal femur (TM 1513) and capitate (TM 1526) from Sterkfontein and a talus (TM 1517) from Kromdraai that the most ardent skeptics capitulated (e.g., Keith 1947, though his recantation began earlier: from Robert Broom (Broom and Schepers 1946, p. 22)) we learn that “In a letter I have recently received dated 11th May 1944, Sir Arthur writes: ‘No doubt the South African anthropoids are much more human than I had originally supposed, and I am prepared to swallow plantigrade adaptations in their limb bones’.” Although australopith fossils had lurked unidentified in east African faunal collections as early as 1935 (i.e., the BMNH M 18773 lower canine from Laetoli, Tanzania (White 1981)), it was not until the discovery of the Garusi (Laetoli) maxillary fragment in 1939 that attention was directed (albeit fleetingly) toward the East African Rift Valley as a source of early hominin fossils. The particularly apelike upper premolar and palate morphologies of the Garusi specimen were overshadowed by the powerful appeal of Robinson’s adaptive scheme in which the fossil was cast as an east African representative of A. africanus (Robinson 1953a), and thus the Garusi maxilla receded into relative obscurity until the recognition of the craniodentally plesiomorphic A. afarensis, based on new mid-Pliocene Hadar (Ethiopia) and expanded Laetoli collections in the late 1970s (Johanson et al. 1978; see below). Mary Leakey’s 1958 discovery of the megadont Zinjanthropus boisei cranium OH 5 at Olduvai Gorge, Tanzania, together with discoveries in the 1960s–1970s at Peninj, near Lake Natron in Tanzania, in the Omo River basin of southern Ethiopia, and at Koobi Fora, east of Lake Turkana, Kenya, populated the Plio-Pleistocene fossil record of eastern Africa with crania, jaws, and teeth of a hominin whose morphological pattern was easily accommodated in the adaptive mold of Robinson’s vegetarian Paranthropus (Robinson 1960). Most workers have since upheld separate species status for these hominins (as P. boisei or A. boisei) on the grounds of morphological distinction and/or geographical separation (Tobias 1967; Howell 1978; Rak 1983). The identification in 1964 of Homo habilis approximately contemporaneous with OH 5 at Olduvai Gorge (in Bed I, ca. 1.8 Ma) recalled the earlier discovery of “true man” (Telanthropus capensis) alongside Paranthropus in the pink breccia (later Member 1) at Swartkrans (Broom and Robinson 1949; Robinson 1953b; Leakey et al. 1964). Robinson (1965 et seq.) dismissed the Bed I H. habilis fossils as an east African variant of A. africanus, which he believed was ancestral to modern humans, while advocates of the “single species hypothesis” struggled to accommodate all Page 3 of 30

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southern and eastern African hominin morphological diversity within single evolving species (Brace 1967; Wolpoff 1970). However, the recovery of a cranium of Homo erectus (KNM-ER 3733) in the same radioisotopically dated horizon (ca. 1.75 Ma) of the Koobi Fora Formation (Kenya) that yielded A. boisei (e.g., KNM-ER 406) validated once and for all the idea that the pattern of early human evolution was, at least partly, the result of a process of diversification through speciation rather than a linear process of morphological advancement (Leakey and Walker 1976). The Leakeys’ argument for a geologically early appearance of genus Homo, bolstered by the 1972 recovery of the relatively large-brained, flat-faced KNM-ER 1470 (initially dated erroneously to >2.6 Ma but now known to be ca. 1.9 Myr old), strongly influenced the first interpretations of fossil hominin diversity in the collections made during the 1970s in pre-3.0-Myr-old sediments at Hadar and Laetoli. While the small Laetoli sample was thought to contain an early precursor of Homo (Leakey et al. 1976), as many as three hominin taxa, including one similar to the Laetoli form, were believed to inhabit the Hadar assemblage of teeth, jaws, and postcrania (Johanson and Taieb 1976). Such early diversity made sense given the Robinsonian view of an A. africanus-like ancestor for a geologically old Homo lineage, implying earliest Pliocene or even late Miocene hominin cladogenesis (Tobias 1973). By the late 1970s, the correct allocation of KNM-ER 1470 to the latest Pliocene and the reinterpretation of the Hadar and Laetoli fossils as representing a single species (Johanson and White 1979) had refocused discussion around two different two-lineage models, both of which featured A. afarensis at the root of mid-Pliocene hominin diversity. One, a twist on Robinson’s dietdriven diversity scenario, envisioned A. africanus as the basal taxon of a “robust” australopith clade, based on the view from the perspective of the craniodentally plesiomorphic A. afarensis of derived masticatory morphology in the hominins from Sterkfontein, Makapansgat, and Taung (White et al. 1981; Rak 1983; Kimbel et al. 1984). The other interpreted A. africanus as the better candidate for the common ancestry of Homo and “robust” australopiths by virtue of their shared derived morphology in the premolars and canines, mandible, and calvaria relative to more plesiomorphic states in A. afarensis (Kimbel et al. 1984; Skelton et al. 1986), but with implied reversals in derived states inferred to be related to heavy chewing in the transition to Homo. Underscoring an emerging consensus on the importance of cladogenesis in the early record of human evolution, homoplasy became a dominant theme in paleoanthropological writings on australopith systematics during the 1980s. These focused in particular on the likelihood of independent evolution of skeletal responses to heavy mastication (see contributions in Grine 1988), an issue highlighted by the discovery of the 2.5-Myr-old KNM-WT 17000 cranium attributed to A. aethiopicus (Walker et al. 1986), whose startlingly plesiomorphic attributes within an otherwise fairly typical “robust” australopith anatomical milieu ensured a high degree of homoplasy (in the masticatory apparatus or cranial base) in any phylogenetic hypothesis that attempted to accommodate all australopith (and early Homo) species then known (Kimbel et al. 1988). A. africanus, more than any other species, continued to occupy a place of uncertainty in hominin phylogeny, which led to musings on whether the type species of the genus may actually comprise more than one species taxon (Clarke 1988, 1994; Kimbel and White 1988; Kimbel and Rak 1993) – a view that remains in the minority, despite the uncommon degree and type of cranial and dental morphological variation within the now 700+ specimen Sterkfontein sample. The 1990s was a decade in which a great deal of paleoanthropological field work concentrated on extending the record of early hominins into the late Miocene, the period in which the evidence from DNA pinpoints the divergence of chimpanzee and human lineages. At least five hominin taxa predating A. afarensis have been recognized since 1994 (Ardipithecus kadabba, A. ramidus, Orrorin tugenensis, Sahelanthropus tchadensis, A. anamensis), aggregately spanning the period between Page 4 of 30

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ca. 4.2 and ca. 6–7 Ma. Relative to A. afarensis, all are more plesiomorphic in dental, mandibular, and cranial morphology. The youngest, A. anamensis, is by far the most similar morphologically to A. afarensis and subsequent australopiths (Leakey et al. 1995; Ward et al. 2001). For the purposes of this chapter, the australopiths will be taken to include A. anamensis as their earliest known representative. Other recently proposed taxa in the 2–4-Myr time range, including A. garhi from Ethiopia (Asfaw et al. 1999), A. bahrelghazali from Chad (Brunet et al. 1996), Kenyanthropus platyops from Kenya (Leakey et al. 2001), and a so far undiagnosed form from Member 2 at Stertkfontein, South Africa (Clarke 2002), hint at as yet poorly understood aspects of hominin diversity and geographical distribution in the early to middle Pliocene of Africa. They will be mentioned in the survey of australopith species provided below, but relatively little is known about them compared to the other species included in the group. Table 2 lists the australopith species that will be discussed in this survey.

Systematic Context of Australopith Diversity Morphological diversity, taxonomic diversity, and species-lineage diversity do not neatly map onto one another in paleontology. This is largely due to the entrenched use of a phenetic species concept in this science, which tends to endorse the recognition of lineage segments as species. But the delineation of the “actors” in evolutionary processes over geological spans of time requires that we move beyond the recognition of “paleospecies” as static phenetic constructs, useful only as a formal catalogue of diversity, to rendering them as close to the entities that underpin the notion of the genetic species as lineages evincing signs of a unique network of gene exchange (see Kimbel and Rak 1993 for discussion and references). Substantial change can in principle accrue in such lineages under a model of anagenesis – amounts that would prompt many paleontologists to recognize distinct paleospecies at widely separated temporal cross sections of a lineage – but, in the absence of cladogenesis, no actual increase in lineage diversity would have resulted from this process. Therefore, to understand the diversity of australopiths, it is one thing to identify and name morphologically distinct taxa and quite another to delineate species lineages. Although a morphologically diagnosed species and a species lineage may exactly coincide, where fossil Table 2 Australopith species diversity according to nominal taxa Taxon Australopithecus africanus Dart 1925 Australopithecus sediba Berger et al. 2010 Australopithecus robustus (Broom 1938) Australopithecus boisei (Leakey 1959) Australopithecus afarensis Johanson et al. 1978 Australopithecus aethiopicus (Arambourg and Coppens 1968) Australopithecus anamensis Leakey et al. 1995 Australopithecus garhi Asfaw et al. 1999 Kenyanthropus platyops M.G. Leakey et al. 2001

Geographical distribution South Africa South Africa South Africa Tanzania, Kenya, Ethiopia, Malawi Ethiopia, Tanzania, Kenya Ethiopia, Kenya, Tanzania Kenya Ethiopia Kenya

Known age range (Ma) ca. 3.0–2.0 ca. 2.0 ca. 1.5–2.0
2.3–1.4
3.8–3.0 ca. 2.7–2.3 4.2–4.0 2.5 3.5

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samples with different morphologies and temporal distributions are involved, the identification of species lineages entails a complex analytical process involving the comparison of phylogenetic hypotheses based on polarized morphological character states (cladistics) with data on the temporal distribution of form (stratophenetics). Where these approaches yield the same character transformations, with minimal stratigraphic gaps and no autapomorphies in temporally intermediate samples, the simplest explanation of the observed data may be the existence of a temporal sequence of samples representing ancestral and descendant populations within a single lineage (Smith 1994) even if two or more distinct nominal species are thereby joined in one evolutionary species (Simpson 1951; Wiley 1978; Krishtalka 1993). There is always the possibility that the evidence for an anagenetic lineage may mask a poorly resolved record of cladogenesis. Accordingly, a fairly densely sampled fossil record over a well-calibrated stratigraphic record and a reasonably complete sampling of taxa from the relevant time period are necessary for this kind of analysis. These requirements are rarely met in the hominin fossil record (but see Wood et al. 1994 and Kimbel et al. 2006 for exceptions). In the following survey, I examine australopith diversity as a record of nominal taxa as well as attempting to characterize it in terms of species lineages. Because I am concerned with taxonomic diversity, my review focuses on craniodental morphology.

Species Diversity of Australopiths Australopithecus anamensis (M. Leakey et al. 1995) Known temporal distribution: ca. 4.17–3.95 Ma, based on radioisotopic age determinations on tephras (Leakey et al. 1995, 1998) Known geographical distribution: Kanapoi, southwest of Lake Turkana, and Allia Bay, east of Lake Turkana, Kenya (Koobi Fora Formation); Asa Issie and Aramis sites, Middle Awash valley, Ethiopia Holotype: KNM-KP 29281, adult mandible with complete dentition and associated temporal bone fragment from Kanapoi Hypodigm: Seventy-eight catalogued fossils have come from the Kanapoi site (including the distal humerus reported by Patterson and Howells 1967); 31 specimens have come from Allia Bay (Ward et al. 2001, 2013). The combined sample comprises mostly dentognathic specimens, including, from Kanapoi, three adult mandibles, an adult maxilla, and deciduous and permanent teeth; from Allia Bay, an adult mandibular fragment, two fragmentary adult maxillae, and deciduous and permanent teeth. Postcranial material includes a distal humerus, a capitate, a proximal hand phalanx, and associated proximal and distal portions of a tibia from Kanapoi. Fragments constituting most of an adult radius from Sibilot Hill (Heinrich et al. 1993), ca. 20 km from the main fossil-bearing locality at Allia Bay, have been attributed to the species based on its inferred geological age (Ward et al. 2001). Additional teeth, a fragmentary maxilla, and a femoral shaft, representing no fewer than eight individuals, have been recovered from Asa Issie and Aramis, in the Middle Awash valley of Ethiopia (White et al. 2006). Diagnostic morphology: Craniodentally, A. anamensis differs from extant African apes and Mio-Pliocene hominins (such as Ardipithecus and Sahelanthropus) chiefly in its expanded postcanine dental battery, including occlusally more complex premolars and thicker cheek tooth enamel, characteristics that are shared with later australopiths and early Homo. In morphology and functional wear, A. anamensis canines are less apelike than those of earliest known hominins (i.e., Ardipithecus kadabba; Haile-Selassie et al. 2004). Page 6 of 30

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Differences from A. afarensis and later australopiths pervade the dentition, mostly in the anterior arcade, as well as in the symphyseal region of the mandible and the nasal region of the maxilla. The lower lateral incisors are mesiodistally expanded, as are the lower third premolars and maxillary canines. The P3 is more asymmetric in occlusal form and is uniformly single-cusped, with an incipient metaconid expressed as a tiny pyramidal expansion of the transverse crest rather than a fully developed cusp, and it usually has a relatively large, mesiolingually “open” anterior fovea. Maxillary canine crowns are symmetric in lateral view, with basally positioned mesial and distal shoulders. Although canine crown size is approximately equivalent to that of A. afarensis, the canine roots in A. anamensis are considerably larger than in this younger australopith species (Ward et al. 2010, 2013). The buccolingually compressed and occlusally simple deciduous first molar crown differs from the more fully molarized dm1 of subsequent australopiths and recalls the apelike form of this tooth in Ardipithecus. Mandibles (KNM-KP 29281, KNM-KP 29287, KNM-KP 31713) feature an externally convex anterior corpus and a strongly inclined, retreating symphyseal cross section with a “cut away” basal segment, which is manifested in a marked inferomedial inflection of the lower lateral corpus in the canine/premolar region. The lower canine crown is set lateral to the long axis of the postcanine tooth row, giving the dental arch a long, rectangular shape that is reflected in the nearly parallel-sided maxillary dental arch. However, based on what little is actually preserved of the midline cross section, the reconstructed dental arch in the maxilla KNM-KP 28283 is too narrow and posteriorly convergent as depicted in published photographs (e.g., Leakey et al. 1995, Fig. 1b; partly corrected in Ward et al. 2001, Fig. 3). In the maxilla (KNM-KP 29283 from Kanapoi, ARA-VP 14/1 from the Middle Awash), large canine roots shape the morphology around the nasal aperture. The lateral margins of the aperture are rounded, not sharp as in A. afarensis, and the inferior margin is indistinct, with the subnasal surface arching smoothly into the nasal cavity. A single fragmentary temporal bone (KNM-KP 29281) forms part of the holotype. From a small, evidently female individual, it has a flat mandibular fossa with an indistinct articular eminence and a horizontally disposed, shallow, and sagittally convex tympanic element that extends laterally to a small-diameter external auditory meatus. Although each of these features can be found individually among A. afarensis temporal bones from Hadar, their strong apelike expression in combination is not encountered in the Hadar sample. The tibia and hand phalanx from Kanapoi, and the radius from East Turkana (granting its assignment to A. anamensis), are very similar to other australopith homologues, and the tibia constitutes the earliest known skeletal evidence for australopith bipedality. The capitate (KNM-KP 31724) is distinctive, however, in the relative orientation of the distal facets for the second and third metacarpals. As in great apes, but unlike the condition in later australopiths and humans, the facet for MC II is laterally directed and set at approximately 90 to the facet for MC III, implying little or no rotational capability at the carpal/MC II joint (Leakey et al. 1998). Discussion: The A. anamensis hypodigm presents a distinctive and significantly more apelike anatomical package than those of subsequent australopith species. However, when the sample is separated into subsamples by site, a more complex picture emerges. Although the younger sample from Allia Bay is much smaller and less representative anatomically than the one from Kanapoi, in several of its morphological details, it stands out relative to conditions in the latter sample (Kimbel et al. 2006). The Allia Bay P3 (in mandible KNM-ER 20432) has an expanded posterior fovea, and its anterior fovea is partly sealed by an elevated mesial marginal ridge. The mandible corpus fragment in which this tooth is preserved does not appear to possess the inferomedial inflection of the lateral corpus under the premolars, implying a less retreating symphyseal cross section. The Allia Bay lower canines (n ¼ 2) show less development of the distal cingulum than in the Kanapoi sample Page 7 of 30

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(n ¼ 4). These distinctions of the Allia Bay sample are the most common states in A. afarensis and bridge A. anamensis to that taxon. Moreover, as suggested initially by Leakey et al. (1995), the differences between A. anamensis and A. afarensis are not as pronounced when the geologically older Laetoli sample of A. afarensis is considered separately from the younger sample from Hadar (see below, under A. afarensis). In fact, the hypothesis of anagenetic change efficiently accounts for the observed morphological transformations across the four temporally ordered site samples, implying that A. anamensis and A. afarensis constitute a single evolutionary species (Kimbel et al. 2006; see also White et al. 2006). Key references: Haile-Selassie et al. 2004; Kimbel et al. 2004, 2006; Leakey et al. 1995, 1998; Ward et al. 2001, 2013; White et al. 1994, 1995, 2006

Australopithecus afarensis (Johanson et al. 1978) Known temporal distribution: ca. 3.8–3.0 Ma based on radioisotopic age determinations on tephras, supported by biochronology and paleomagnetic polarity Known geographical distribution: Laetoli, Tanzania (upper Laetolil Beds); Hadar, Ethiopia (Sidi Hakoma, Denen Dora, and Kada Hadar Members, Hadar Formation); Dikika, Ethiopia (Basal Member and Sidi Hakoma Members, Hadar Formation), Woranso-Mille, Ethiopia, Maka, Middle Awash, Ethiopia (“Maka Sands,” Matabaietu Formation), East Turkana, Kenya (Tulu Bor Member, Koobi Fora Formation), possibly Koro Toro, Bahr-el-Ghazal, Chad Holotype: LH-4, mandible with dentition, from upper Laetoli Beds, Laetoli, Tanzania Hypodigm: Approximately 90 % of the hypodigm of A. afarensis comes from Hadar Formation sediments exposed at the Hadar site in Ethiopia (n ¼ 367 specimens). The Hadar sample includes two partial skeletons with craniodental associations (A.L. 288-1, A.L. 438-1), two nearly complete (A.L. 444-2, A.L. 822-1) and one partial (A.L. 417-1) skull, 57 adult or subadult mandibular portions, 13 adult or subadult maxillae, 12 calvarial specimens (including a partial juvenile cranium, A.L. 333-105), and a wealth of upper limb, lower limb, and axial material, the majority of which comes from the A.L. 333 locality (see descriptive papers in the March 1982 American Journal of Physical Anthropology and Latimer et al. 1987; Latimer and Lovejoy 1989, 1990a, b; Kimbel et al. 1994, 2004; Drapeau et al. 2005). The Laetoli site sample consists of the holotype mandible (LH-4), several adult or subadult jaws (Garusi I, LH-2, LH-5), a fragmentary partial skeleton of a juvenile (LH-21), and an assortment of teeth (White 1977, 1980, 1981). Trace fossils in the form of the Laetoli bipedal hominin footprint trails, presumed to have been made by A. afarensis, are part of the species’ hypodigm. From the Maka site in Ethiopia have come a proximal femur, a humerus, and several jaws, including a nearly complete mandible, at 3.4 Ma (White et al. 1993, 2000; Lovejoy et al. 2002). A partial calvaria (KNM-ER 2602; Kimbel 1988) is known from Koobi Fora. Although the 3.0–3.5-Myr-old mandible fragment (KT-12/H1) from Koro Toro, Chad, has been made the holotype of A. bahrelghazali by Brunet et al. (1996), its anatomy does not appear to distinguish it from the range of variation encompassed by the Hadar/Maka mandibular series, and so it is here tentatively interpreted to extend the geographical distribution of A. afarensis into north-central Africa. The Middle Awash frontal fragment from Belohdelie may also belong to A. afarensis, which would extend the time range of the species back to ca. 3.9 Ma (Asfaw 1987; Kimbel et al. 2004). Diagnostic morphology (Fig. 1): A. afarensis can be distinguished from A. anamensis by a more molarized, symmetric P3 crown with more frequent development of the second cusp (metaconid) and transverse orientation in the tooth row; an asymmetric upper canine with more apically positioned mesial crown shoulder; a molarized dm1 with buccolingually expanded talonid; a straighter, commonly more upright anterior corpus profile, with a “filled out” basal segment and little to no inferomedial inflection of the lower corpus beneath the canine-premolars; lower canines Page 8 of 30

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_50-3 # Springer-Verlag Berlin Heidelberg 2014

Fig. 1 Three-quarters view of the reconstructed skull of A. afarensis specimen A.L. 444-2 from Hadar, Ethiopia (Photo by W. Kimbel and Y. Rak)

set medial to postcanine row axis; a wider palate at equivalent palate lengths; a nasal aperture defined by sharp lateral margins and distinct inferior margin, with the canine jugum a distinct entity in the circumnasal topography; and a larger external auditory meatus. In all of these features, A. afarensis exhibits the derived condition for hominins. Compared to all subsequent australopiths, a distinctive, predominantly plesiomorphic, anatomy pervades the A. afarensis skull and dentition. The calvaria testifies to an extensive posterior m. temporalis origin, with posteriorly extended sagittal crests and compound temporal/nuchal crests in both large (putatively male) and small (putatively female) specimens. The nuchal plane of the occipital bone is transversely convex and set at a steep angle to the Frankfurt plane, especially in less heavily crested small and subadult individuals, and it transitions to a relatively short occipital plane. In some individuals the nuchal plane extends superiorly to a very high position on the rear of the braincase. The cranial base features a shallow mandibular fossa bounded anteriorly by a weak to moderately developed articular eminence and posteriorly by an inflated postglenoid process that sits anterior to the tympanic element. The tympanic is a horizontally inclined tube, rather than a vertically oriented plate, and it usually lacks a distinct crista petrosa. Venous blood outflow was predominantly through the occipital-marginal rather than through the transverse-sigmoid sinus system. The frontal bone features a low, flat to mildly convex squama lacking a frontal trigone, coronally oriented, laterally thickened supraorbital bars, and broad postorbital breadth relative to other facial breadth dimensions. The midfacial axis (nasion-nasospinale) is upright, in contrast to the strongly projecting, convex subnasal plane (nasospinale-prosthion), which protrudes anteriorly beyond the bicanine line (also seen in A. garhi). Interorbital and nasal aperture breadths are narrow, contrasting with the broad, flat, and massive zygomatic region. The maxilla’s zygomatic process root is located above M1 or P4-M1, and its inferior margin is moderately to strongly arched. Within the nasal cavity, an elevated platform separates the inferior nasal margin from the anterior vomeral insertion. The palate is moderately deep in narrow jaws but is shallower in wider ones, and the upper dental arch is subparallel with slight convergence to moderate divergence posteriorly. The mandible

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has a deep but relatively thin corpus at the molars, and a moderately tall ramus originating high on the corpus and separated from it by a narrow extramolar sulcus. In individuals with an associated mandible and maxilla (i.e., A.L. 417-1, A.L. 444-2, A.L. 822-1), the mandibular corpus constitutes more than two-thirds of the orbitoalveolar height in the coronal plane of the orbits. The external contour of the anterior corpus is full and transitions to a vertical lateral corpus beneath the canines and premolars. Although the symphyseal axis is more vertical than in A. anamensis, it is, on average, less vertical than in subsequent australopiths. The lower anterior dental arch is pinched in small mandibles but widens into a U-shape in larger specimens, perhaps under the influence of moderate canine dimorphism. Most of the distinctive dental features of A. afarensis are focused in the canines and premolars, which in this species are captured in evolutionary transition. Molarization of the P3 is less advanced than in subsequent australopiths: the metaconid is variably expressed, with some individuals primitively lacking a distinct second cusp (e.g., A.L. 128-23, 277-1, 288-1, 417-1), though these are not necessarily those with a more “apelike” skewed occlusal outline and oblique orientation in the tooth row. Absolute canine size overlaps that of A. africanus, though relative to postcanine size the A. afarensis canines are larger. Some canines reveal ancestral traces of shearing wear (e.g., on the elongated distal crests of the lower), which is lost almost entirely in subsequent australopith species, but this is significantly less developed than in A. anamensis and especially Ardipithecus, and occlusal wear in A. afarensis canines and premolars is predominantly apical. Nevertheless, in some mandibles canine and mesial P3 crowns stand tall even in the face of extreme occlusal molar wear, a remnant of the ancestral occlusal wear pattern. Discussion: Well-documented variation in the large A. afarensis sample from Hadar indicates high levels of cranial polymorphism. Some of this variation is due to sexual dimorphism in size and shape, while some of it is due to anagenetic trends in craniodental morphology during the younger half (3.5–3.0 Ma) of the A. anamensis to A. afarensis species lineage (Lockwood et al. 2000). The Laetoli sample (ca. 3.8–3.6 Ma) figures prominently in this discussion. Although some dental metric differences between the Laetoli and Hadar samples have been cited in the past (White 1985), it now appears that the metric and morphological differences between the hominin populations represented at these sites are phylogenetically significant. Despite limited samples, the convex, retreating form of the adult anterior mandibular corpus (LH-4), mirrored in that of a juvenile (LH-2); the influence of the canine root on the curved lateral margin; the indistinct inferior margin of the nasal aperture (Garusi I); and the mesiodistally expanded lower canine and P3 crowns recall conditions diagnostic of A. anamensis and occur in more derived states in the Hadar sample (Kimbel et al. 2006). The recently recovered sample of teeth and jaws from Woranso-Mille, dating to ca. 3.6–3.8 Ma, reinforces the hypothesis of dentognathic evolution along the A. anamensis to A. afarensis lineage (Haile Selassie et al. 2009). Later in time, in the Kada Hadar Member at Hadar (ca. 3.0–3.1 Ma), there is evidence of an anagenetic increase in hominin skull size (and perhaps body size), which drove the A. afarensis mandibular corpus and facial skeleton to sizes rarely encountered in older strata (Lockwood et al. 2000). This trend was not accompanied by especially large postcanine teeth, more robust mandibular corpora (i.e., thicker in relation to depth), or by anteriorly shifted masticatory muscle blocks that are usually thought to signal diet-related morphological specializations in subsequent species of the australopith group. The causal processes underlying the observed increase in size are presently unclear, but it does roughly correspond to a change in the Hadar mammalian faunal community to more arid-adapted taxa (e.g., among the bovids). The Burtele site, in the Woranso-Mille area of Ethiopia, has yielded a fossil partial foot skeleton from sediments contemporary with the Sidi Hakoma Member at Hadar and Dikika (ca. 3.4 Ma; Page 10 of 30

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Haile-Selassie et al. 2012). This specimen features a divergent hallux, which is universally present in arboreal catarrhines. However, derived features, including the dorsally “domed” heads of the lateral metatarsals and the anterior cant of the corresponding phalangeal bases, suggest toe off in terrestrial bipedality, as in Australopithecus and Homo. The mix of primitive and derived morphology in the Burtele foot, matching that of early Pliocene Ardipithecus ramidus, is strong evidence for a second species lineage contemporary with A. afarensis in eastern Africa (Haile-Selassie et al. 2012). Key references: Alemseged et al. 2005; Drapeau et al. 2005; Haile Selassie et al. 2009, 2012; Kimbel and Delezene 2009; Kimbel and Rak 2010; Kimbel et al. 2004, 2006; Lockwood et al. 2000; White et al. 2003; papers in American Journal of Physical Anthropology, Vol. 57, 198.

Kenyanthropus platyops (M.G. Leakey et al. 2001) Known temporal distribution: ca. 3.3–3.5 Ma based on radioisotopic dating of tephra Known geographical distribution: Lomekwi (Nachukui Formation), west of Lake Turkana, Kenya Holotype: KNM-WT 40000, a crushed and distorted cranium with partial dentition Hypodigm: In addition to the holotype, a partial maxilla with dentition (KNM-WT 38350). (Other hominin fossils, including a partial temporal bone, a mandible fragment [formerly attributed to A. afarensis by Brown et al. (1993)], and some isolated teeth, were withheld from attribution to this taxon by Leakey et al. (2001).) Diagnostic morphology: While enumeration of the diagnostic features of K. platyops is hampered by poor preservation of the holotype, taphonomy does not appear to account for all of the distinctive morphology of the type cranium relative to that of known specimens of A. afarensis, with which it was contemporary (Spoor et al. 2010). These differences reside mainly in the lower part of the face (Leakey et al. 2001) and include an anteriorly positioned root of the maxillary zygomatic process (above P3-P4, and seen in both the type specimen and KNM-WT 38350) and a transversely and sagittally flat subnasal plane with minimal projection beyond the canines. In addition, the dominant venous outflow track was via the transverse-sigmoid system, in contrast to the occipital-marginal system, which is very common in A. afarensis (though the Laetoli juvenile LH-21 also evinces the transverse-sigmoid drainage route). The size of the external auditory meatus is smaller than that of A. afarensis, despite the latter’s extensive variation in this feature (Kimbel et al. 2004), and approaches the tiny EAM of Ardipithecus ramidus and A. anamensis. The second molar in the type cranium is much smaller than that of other australopith M2s, while the M1 of KNM-WT 38350 is also very small. Discussion: Along with the Burtele foot (see above), the specimens attributed to K. platyops currently constitute the best evidence for hominin lineage diversity prior to 3.0 Ma. On the basis of published information (Leakey et al. 2001), the material attributed to K. platyops shares only primitive characteristics with A. afarensis (e.g., tubular tympanic element lacking a petrous crest, posteromedially angled temporal lines and an emphasis on posterior cranial crests, low and curved zygomaticoalveolar crest), but its facial configuration appears more derived than what is observed in the large cranial sample of that species. None of these derived characteristics are observed in the sample of one dozen adult maxillae in the Hadar sample of A. afarensis, or in the Garusi maxilla from Laetoli, which is demonstrably more primitive in the circumnasal region than the Hadar specimens (as discussed above and in greater detail in Kimbel et al. (2006)) yet is the more precise chronological match for the Kenyanthropus holotype. (KNM-WT 38350 is approximately contemporary with Hadar specimens A.L. 417-1, A.L. 200-1, and others from the middle Sidi Hakoma Member.) Therefore, K. platyops sits in phylogenetic isolation. There are no shared derived characters linking it to the A. anamensis to A. afarensis species lineage, and although favorable comparisons have been Page 11 of 30

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_50-3 # Springer-Verlag Berlin Heidelberg 2014

made directly with the lower facial morphology of Homo rudolfensis (i.e., KNM-ER 1470), at ca. 2.0 Ma (Leakey et al. 2001), it is unrealistic to link these two specimens via a meaningful phylogenetic hypothesis given 1.5 myr of no intervening data. Key references: Leakey et al. 2001; Spoor 2010

Australopithecus africanus (Dart 1925) Known temporal distribution: ca. 3.0–2.0 Ma, based on U/Pb dating, paleomagnetic polarity and biochronological correlations with radioisotopically calibrated sequences in eastern Africa (Herries et al. 2013) Known geographical distribution: Taung, Sterkfontein, and Makapansgat, South Africa Holotype: Juvenile skull, dentition, and endocast from Taung Hypodigm: In addition to the holotype, crania, jaws, teeth, and postcrania from Sterkfontein and Makapansgat. The Sterkfontein sample is by far the more extensive, consisting of some dozen nearly complete or partial crania (e.g., TM 1511, Sts 5, 17, 71, Stw 13, 505) and adult and juvenile mandibles plus hundreds of teeth, in jaws or isolated. Numerous postcranial remains are known, including at least three partial skeletons (Sts 14, Stw 431, Stw 573: Toussaint et al. 2003), but only one (Stw 573) is definitively associated with taxonomically diagnostic craniodental remains. The Makapansgat sample comprises roughly 40 specimens, including several jaws (MLD 2, 6/23, 9, 18, 40), two partial adult calvariae (MLD 1, MLD 37/38), and some fragmentary cranial and postcranial elements. Diagnostic morphology (Fig. 2): Compared to A. afarensis, A. africanus has a higher, shorter braincase with rare sagittal cresting and no compound temporonuchal cresting. The supraorbital torus thins laterally from top to bottom and is occasionally divided into distinct supraorbital and superciliary components (Lockwood and Tobias 1999). The cranial base is a bit narrower in absolute terms, but in relation of calvarial size, it is broader and shorter than in apes. The occipital plane of the occipital bone is higher and the nuchal plane is flatter and more horizontally inclined. The mandibular fossa is deeper on average, with a stronger articular eminence. The tympanic element is more vertically oriented, usually bears a distinct crista petrosa, and tapers medially to a distinctive Eustachian process. Venous drainage from the endocranium is predominantly through the transverse-sigmoid system. Prominent anterior pillars border the nasal aperture, even in young

Fig. 2 Oblique views of Sterkfontein A. africanus crania Sts. 71 (left) and Sts. 5 (right) (Photo by W. Kimbel and Y. Rak) Page 12 of 30

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_50-3 # Springer-Verlag Berlin Heidelberg 2014

individuals, and the subnasal plate is flat to slightly convex sagittally and much less projecting relative to the bicanine axis. Within the nasal cavity, the step-down to the nasal floor and anterior vomeral insertion occurs immediately posterior to nasospinale, usually without an intervening platform. The zygomatic bone features a variably prominent boss at the transition to the temporal process and a strong sagittal inflection across the frontal process/facial surface transition, which combine to create a central facial hollow in some individuals (e.g., MLD 6/23, TM 1511, Sts 71, Stw 505). Zygomatic process roots typically originate more anteriorly (above P4/M1 to P4/P3) and have a straight, superolaterally diverging inferior margin. The palate is, on average, deeper, with an inferiorly flexed premaxillary segment and posteriorly divergent tooth rows. The mandible corpus is more robust (breadth as a percentage of depth at M1) and has a more inflated lateral surface beneath the premolars and a straighter, more vertical symphyseal profile. Dentally, compared with A. afarensis, A. africanus has absolutely larger (especially broader) postcanine teeth with centrally crowded molar cusp apices in some individuals. The P3 is uniformly bicuspid, canine wear is exclusively apical, and the anterior-posterior adult occlusal wear gradient is weaker. C/P3 and I2/C diastemata are less frequent. In its moderate (though impressively variable) upper midfacial prognathism (nasion-nasospinale), occasionally patent premaxillary suture in adult faces, and less topographically complex glenoid region of the temporal bone, A. africanus remains plesiomorphic in relation to A. robustus and A. bosei (but not A. aethiopicus). The mandibular corpus is less robust compared to states observed in A. aethiopicus, A. robustus, and A. boisei, and dental size and the anterior-posterior tooth row proportions remain relatively conservative (especially those involving the premolars, which are less expanded in relation to the molars). Facial breadths are narrower as a percentage of calvarial breadths, giving the impression that the cranium is less constricted postorbitally, though the minimum frontal breadth dimension is of similar absolute magnitude. The vertex of the braincase (in specimen Sts. 5 at least) is higher in relation to the orbital roof when compared to crania of A. aethiopicus, A. robustus, and A. boisei (as well as A. afarensis and the great apes), but when sizestandardized by calvarial length, vertex height is greater only than that of the “robust” species. Discussion: The large A. africanus sample from the Sterkfontein Member 4 (“type site”) fossil assemblage is notable for its unusually extensive range of craniodental variation (e.g., basal aspect of the temporal bone, facial topography and subnasal prognathism, postcanine tooth size), which has led to proposals that more than one hominin species may be contained within it (Clarke 1988, 1994, 1998; Kimbel and White 1988; Kimbel and Rak 1993; Moggi-Cecchi et al. 1998; Lockwood and Tobias 2002). However, because dividing the sample to create overlapping cranial and dental morphs has proven difficult (while different authors tend to disagree on such divisions in the first place), these proposals have not attracted much support (see Grine 2013 for a review). Still, appeals to normal sources of variation within a single geographically delimited biological species (chiefly sexual dimorphism) do not account for the variation, as much of this does not follow patterns of dimorphism observed within extant catarrhine species (Kimbel and White 1988; Kimbel and Rak 1993). The lack of chronological control within the Member 4 faunal assemblage leaves open the possibility that the hominin sample is time-transgressive. Kimbel (1986) offered as an explanation for the Sterkfontein Member 4 variation the temporal mixing of individual organisms’ remains from morphologically distinct populations of A. africanus that had moved in and out of the Sterkfontein valley over a long period of time. Although Kuman and Clarke’s (2000) revised stratigraphy implies a long and complex depositional history for Member 4, this idea is difficult if not impossible to test and does not in any event preclude the inclusion of fossils from more than one hominin species in the Member 4 sample. The basic systematics of the type species of Australopithecus remains a vexing issue, and the likelihood of being able to discern lineages is remote. Page 13 of 30

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_50-3 # Springer-Verlag Berlin Heidelberg 2014

More recently, excavations in previously unexploited depositories in the Sterkfontein cave system have led to discoveries of hominin fossils originally said to be significantly older (ca. 4 Ma) than A. africanus of Member 4 (Clarke 1988, 2002; Partridge et al. 2003). These remains include a partial skeleton and skull (Stw 573) still being excavated in situ in the Silberberg Grotto and a small collection of specimens, including fragments of an adult cranium (Stw 578), from Jacovec Cavern. Published reports suggest general australopith affinities for these specimens. While their exact antiquity is uncertain, in part due to an extremely complex stratigraphic context, Herries et al. (2013) have presented evidence that these deposits are contemporaneous with Member 4 of the Sterkfontein site (ca. 2.0–2.6 Ma). Key references: Broom and Schepers 1946; Broom et al. 1950; Robinson 1956; White et al. 1981; Rak 1983; Clarke 1994; Lockwood and Tobias 1999, 2002; Grine 2013

Australopithecus sediba (Berger et al. 2010) Known temporal distribution: Faunal, paleomagnetic, and U/Pb dating methods combine to suggest a ca. 2.0 Ma age for the fossil-bearing sedimentary infill in the Malapa cave system, South Africa (Berger et al. 2010; Pickering et al. 2011; Herries et al. 2013) Known geographical distribution: Malapa cave system, Gauteng Province, South Africa Holotype: MH1, a subadult partial skeleton and skull thought to be male (Berger et al. 2010) Hypodigm: A subadult’s partial skeleton and skull, reportedly male (MH1, the holotype), and an adult’s partial skeleton and mandible, thought to be female (MH2). A tibia originally associated with the holotype is now said to represent a third individual (MH3) (Berger 2012). Diagnostic morphology: The MH1 individual of A. sediba is small-brained, with an estimated endocranial volume (ECV) of ca. 420 cc, which must be close to the adult value given that the M2s had achieved alveolar eruption (Carlson et al. 2011). This single value falls below the mean but within the ranges of A. afarensis and A. africanus ECV estimates (Holloway et al. 2004). Similarly, canine and postcanine tooth crown dimensions fall in the lower end of the range of size variation for these two australopith species (Berger et al. 2010). The face of MH1 is moderately prognathic with slight subnasal projection, but the latter feature, along with some other putatively diagnostic craniofacial characters, are subject to late growth-related changes. These ontogenetically labile characters include the widely spaced temporal lines, slight relative postorbital constriction, and mild relative lateral flare of the zygomatic arches (the latter two of which are expressed as a percentage of upper facial breadth in Berger et al. 2010). Thus, assessment of fully adult craniofacial shape in A. sediba would likely affect comparisons with other australopith species subtly but substantively. In several respects the MH1 facial skeleton resembles that of A. africanus specimen Sts 52a, also a subadult (M3s unerupted). This specimen departs from characteristic A. africanus craniofacial anatomy (Rak 1983) in the absence of an anterior pillar, weak subnasal projection, a pronounced canine fossa, and mild eversion of the lateral nasal aperture margins superiorly with consequent slight prominence of the nasal bridge (enhanced by a median keel) – all features observed in MH1. MH1 shares several other craniofacial features with A. africanus adults and subadults (including Sts 52a), such as a superiorly placed anterior masseter origin associated with a straight, steeply angled (in anterior view) zygomaticoalveolar crest (Rak 1983; Kimbel et al. 1984). At first glance, MH1 appears to bear a supraorbital torus separated from the frontal squama by a sulcus supratoralis, as in Homo habilis (sensu stricto; i.e., excluding fossils often attributed to H. rudolfensis). But in H. habilis the supraorbital torus is a distinct structure that bulges above the sulcus (with a topographic highpoint that divides the sulcus into lateral and medial sections on each side, as in KNM-ER 1813, OH 16 and OH 24), whereas in MH1 the squama passes onto a shelflike Page 14 of 30

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_50-3 # Springer-Verlag Berlin Heidelberg 2014

supratoral depression that extends, with little topographic disruption, directly onto the superior surface of the supraorbital structures. Perhaps this difference can be accounted for by the relative youth of MH1, although in hominoids juvenile supraorbital form is typically a good predictor of adult morphology. An alternative interpretation is that the MH1 morphology is one expression of the variable supraorbital form observed in A. africanus (as seen in the Sterkfontein Member 4 deposits). In this sample, the supraorbital elements are weakly defined topographically and are separated from the squama by a variably developed depression that ranges from virtually absent (in Sts 71, Stw 505) to mild (Sts 5) to pronounced (TM 1511, as revealed by the impression left in matrix by the specimen’s now lost frontal squama; Kimbel and Rak, pers. obs.; see also Plate IV, Fig. 16 in Broom and Schepers 1946). MH1 is similar to the adult TM 1511 in the expression of this morphology (allowing for the effects of age-related differences in temporal line incursion), which is distinct from the Homo habilis morphology. The Malapa mandibles (MH1 and MH2) are small and lightly built, but the extent to which the subadult status of MH1 and the presumptive female status of MH2 present a biased profile of mandibular size and shape variation (which is known to be considerable in other australopith taxa) can only be addressed with additional specimens. Rak et al. (in review) have concluded, however, based on the anatomy of the coronoid notch of the mandibular ramus, that the Malapa sample actually contains two hominin species, one of Australopithecus (MH1) and one of Homo (MH2) (see Rak et al. 2007). As in all other australopith species, the A. sediba skeleton presents an amalgam of ancestral and derived features. MH2 features a nearly complete hand with a distinctive character mix relative to A. afarensis, A. africanus, and H. habilis (Kivell et al. 2011). The relatively long thumb and short fingers stand out in comparison even to the anatomy of modern humans. A similarly mosaic pattern is said to be found in the pelvis (MH 1 and MH2); it is similar to other australopiths in its large interacetabular breadth and long pubis, but distinct from A. afarensis and A. africanus in having more vertically disposed iliac blades and a shortened ischium (Kibii et al. 2011). Australopith taxonomy has for decades relied chiefly on skull and dental characters (in part because of the rarity of associated craniodental and postcranial remains), so it is noteworthy that the best evidence for the taxonomic distinctiveness of A. sediba may come from the postcranium. Discussion: The case for the specific distinctiveness of the Malapa fossils has been conflated by their discoverers with arguments about its phyletic status (e.g., Berger 2012, p. 4). Neither is helped by the subadult status of the holotype and the fact that its cranium remains (at the time of this writing) partially encased in matrix, obscuring potentially informative portions of the external base (see Carlson et al. 2011). The bulk of the available craniodental evidence, however, argues for a close relationship with A. africanus as represented at Sterkfontein Member 4. The A. sediba to A. africanus relationship may constitute the best evidence for lineage continuity in the PlioPleistocene hominin record of southern Africa. If the young age (~2.6–2.0 Ma) of Sterkfontein Member 4 deposits suggested by Herries et al. (2013) is confirmed, then the age of some specimens of A. africanus (e.g., Sts 5) may fall within the error range of the age estimate for A. sediba at Malapa. Further support for chronological overlap would suggest a sister-group relationship, as opposed to an ancestor-descendant (anagenetic) relationship, between the populations represented by the two site samples. Berger et al. (2010; Berger 2012) have argued that A. sediba, at 2.0 Ma, resided at the base of the Homo lineage. But if the unique phylogenetic link between A. sediba and A. africanus is substantiated, then for this argument to work, A. africanus itself would need to be rooted as a sister taxon to the Homo clade. Yet most comprehensive phylogenetic analyses of craniodental characters find A. africanus to be basal to a strongly supported “robust” australopith-Homo clade (e.g., Strait and Page 15 of 30

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_50-3 # Springer-Verlag Berlin Heidelberg 2014

Grine 2004; Kimbel et al. 2004). The Berger argument also hinges on a dismissal (rather than evaluation) of geologically contemporaneous or older (
2.0 Ma) fossils from the genus Homo (H. habilis, H. rudolfensis, the A.L. 666-1 maxilla from Hadar, etc.) (Kimbel 2009; Spoor 2011). Key references: Berger et al. 2010; Carlson et al. 2011; Pickering et al. 2011

Australopithecus aethiopicus (Arambourg and Coppens 1968) Known temporal distribution: ca. 2.3–2.7 Ma Known geographical distribution: Omo River basin, Ethiopia (Shungura Formation, Members C–F); West Turkana, Kenya (Nachukui Formation); Laetoli, Tanzania (Ndolanya Beds) Holotype: Omo 18-1967-18, edentulous mandibular corpus (Member C, Shungura Formation, Ethiopia, ca. 2.7 Ma) Hypodigm: The mostly complete and largely edentulous cranium KNM-WT 17000 from the Nachakui Formation, West Turkana, Kenya (2.5 Ma; Walker et al. 1986; Leakey and Walker 1988) is by far the most complete and well-preserved evidence for this relatively poorly known australopith species. Suwa et al. (1996) assigned to this species some 20 lower postcanine teeth (several in mandibles) from Omo Shungura Formation Members C–F, aggregately spanning ca. 2.7–2.3 Ma. An edentulous maxilla (EP 1500/01) from the Ndolanya Beds at Laetoli has also been assigned to A. aethiopicus (Harrison 2002). Diagnostic morphology: Based on the single known cranium (KNM-WT 17000), A. aethiopicus can be distinguished from A. afarensis by its extreme midfacial prognathism (nasion-nasospinale); flat subnasal plane; smooth transition from subnasal surface to nasal cavity floor, with indistinct inferior margin of nasal aperture; anterior vomeral insertion and anterior nasal spine merged within nasal cavity; vertically thick palate; anteriorly positioned zygomatic process roots (over P3/P4); bulbous, forwardly sloping zygomatic facial surface, which leaves the nasal region in a central facial hollow; low calvarial height; frontal squama with frontal trigone delimited by strongly convergent temporal lines; vertically inclined tympanic element with distinct petrous crest; coronally aligned petrous element; and massive postcanine dentition (inferred from roots and fragmentary P4 crown; Suwa 1989). Although the KNM-WT 17000 cranium features a very high sagittal crest, its diagnostic value is doubtful, as it was produced by the juxtaposition of enlarged temporalis muscles to a very small braincase (410 cm3 cranial capacity) that may not have been typical for the species. The majority of the characters discriminating the A. aethiopicus cranium from that of A. afarensis link the former species to classical “robust” australopith masticatory configurations. In addition, the dental remains attributed to the former species testify to postcanine size expansion and molarization seen in otherwise only in A. robustus or A. boisei, though with less premolar crown specialization than in the latter taxon (Suwa 1990; Suwa et al. 1996). However, A. aethiopicus retains a number of plesiomorphic characters, such as strong midfacial prognathism, posteriorly accentuated sagittal crest and extensive compound temporonuchal crest, flat mandibular fossa with low, indistinct articular eminence, and (as inferred from roots and alveolar dimensions) relatively large incisors and/or canines. While these characters set A. aethiopicus apart from both A. robustus and A. boisei, they also effectively discriminate it from A. africanus, which in several of these respects exhibits derived morphology (cranial vault shape, crest configuration, and mandibular fossa topography). Discussion: As noted in the historical survey earlier, the discovery of the KNM-WT 17000 cranium provoked discussion about the role of homoplasy in early hominin phylogeny (see contributions in Grine 1988). The fact that aspects of this specimen’s cranial morphology are strikingly more plesiomorphic than homologous states in A. africanus, combined with its obvious “robust” australopith masticatory signal, implies a high degree of convergent evolution in the

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_50-3 # Springer-Verlag Berlin Heidelberg 2014

australopith skull, the nature of which depends to a large extent on the phyletic position accorded A. africanus. Does the temporal juxtaposition of the morphologically intermediate A. aethiopicus between A. afarensis and A. boisei support the identification of an evolving australopith lineage (evolutionary species) in the Middle to Late Pliocene of eastern Africa? Walker et al. (1986; Leakey and Walker 1988; Walker and Leakey, 1988) thought so and interpreted KNM-WT 17000 as an early, primitive, A. boisei specimen. Suwa’s (1990; Suwa et al. 1996) detailed analysis of australopith postcanine dental evolution in the Shungura Formation found that in most respects the premolars and molars from Members C–F he attributed to A. aethiopicus more closely approximate the generalized condition of A. robustus than the highly derived condition of A. boisei (e.g., Olduvai Gorge, Koobi Fora, Peninj, etc.), but that the “A. boisei morphology emerge[d] in a mosaic fashion across Member G times [i.e., sagittal chord Upper face > midface breadth Margins sharp and everted; evident nasal sill Vertical or near vertical Foreshortened Probably two-rooted premolars

An average volume of 650–675 Primitive condition

Relatively deep Orientation variable Moderate relief on external surface; rounded base Buccolingually narrowed; postcanine crowns; reduced talonid on P4; M3 reduction; mostly single-rooted mandibular premolars

Apelike Apelike Mosaic of apelike and modern humanlike features Retains climbing adaptations Australopithecine-like

Frontal lobe asymmetry Simple Torus absent Primitive condition Midface > upperface breadth Less everted margins; no nasal sill Anteriorly inclined Large Premolars three rooted; absolutely and relatively large anterior teeth Shallow Anteriorly inclined Marked relief on external surface; everted base Broad postcanine crowns; relatively large P4 talonid; no M3 reduction; twin, platelike P4 roots, and bifid, or even twin, platelike P3 roots ? ? ? Later Homo-like Later Homo-like

After Wood (1992)

Changing Taxonomy Hominid fossils have been assigned to the genus Homo if they fulfilled four main perceived criteria (Keith 1948; Tobias 1991; Wood and Collard 2001): a brain size above 600 cm3, putative ability for speech and toolmaking, and an opposable pollux. To date, the hypodigm of earliest Homo attributed to H. habilis sensu stricto and H. rudolfensis contains about 200 skeletal fragments attributable to about 40 individuals (Tables 1 and 2). Despite or maybe due to the large number of specimens, the taxonomic interpretation of earliest Homo is highly controversial (e.g., Wood 2000). Originally, the interpretation of the early Homo hand as “modern” (Leakey et al. 1964) supported the view of H. habilis as an early but “able” human as opposed to the rather “clumsy” australopithecines. However, later skeletal finds at Olduvai Gorge (OH 62) (Johanson et al. 1987)

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_52-4 # Springer-Verlag Berlin Heidelberg 2013

Table 2 Fossil remains of Homo habilis sensu stricto Homo habilis (better-preserved specimens in bold) Sites Skulls and crania Mandibles Olduvai (OH) 6, 7, 13, 14, 16, 24, 7, 13, 37, 62 52, 62 Koobi Fora (KNM-ER) Omo

807, 1478, 1805, 1813, 3735 L894-1

1501, 1502, 1506, 1805, 3734 Omo 222-2744

West Turkana

Kangaki I site (w/o number) Stw 53, SE 255, 1508, 1579, 1937, 2396; Sts 19 SK 847 (?)

–

Isolated teeth 4, 6, 15, 16, 17, 21, 27, 31, 32, 39, 40, 41, 42, 44, 45, 46, 47, 55, 56 808, 809, 1462, 1480, 1508, 1814 L28-31; L398-573, 1699; Omo 33-3282, Omo 47-47; Omo 74-18; Omo 123-5495; Omo 166-781; Omo K7-19; Omo SH1-17; P933-1 –

–

–

–

–

–

–

Sterkfontein

Swartkrans

Postcranial 7, 8, 10, 35, 43, 48, 49, 50, 62 813, 1472, 1481, 3228, 3735

–

demonstrated that the postcranial skeleton of H. habilis indeed resembled Australopithecus africanus rather than Homo. Yet the most distinctive character of H. habilis remains its relatively and absolutely higher brain volume compared to that of Australopithecus. The forehead of H. habilis is more vertical and a weak supraorbital torus is present. Whereas the morphological characters are quite uniform in the Olduvai sample, the discussion started to heat up mainly over two very distinct fragmentary skulls from Koobi Fora: KNM-ER 1470 (Fig. 3) (Leakey 1973a) and KNM-ER 1813 (Fig. 4) (Leakey 1973b). In a comprehensive character analysis of all available putative H. habilis fossils from Koobi Fora, Wood (1991) concluded that the variability exhibited by the sample was not only the result of sexual dimorphism, as was suspected at the time, but that highly significant differences exist throughout the entire skeleton. There is a mosaic of Australopithecus and Homo characters in both early species: Whereas H. rudolfensis exhibits a combination of ancestral dentition with Homo-like locomotion, H. habilis shows a progressive reduction of tooth roots and resembles great apes rather than humans postcranially. Based on the work of Wood (1991) and subsequent re-evaluation of fossils, it is evident that two distinct types can be separated. Whereas one group, represented by KNM-ER 1813, follows the original description of H. habilis from Olduvai Gorge, a new group is represented by KNM-ER 1470, for which no comparison existed in Olduvai at the time. Although the subsequent find of OH 65 at Olduvai (Blumenschine et al. 2003) showed a mixture of H. habilis sensu stricto and KNM-ER 1470 features, it is still a valid conclusion that about half the early Homo material from Koobi Fora belongs to H. habilis sensu stricto, with an age of 2.1–1.5 Ma, which includes also specimens from Koobi Fora, West Turkana, Omo, Olduvai Gorge, and southern Africa (Table 2). Hominid remains from Ubeidiya in Israel (Leakey et al. 1964) and Meganthropus palaeojavanicus from Java, Indonesia, which at one stage were tentatively assigned to H. habilis (Tobias and von Koenigswald 1964), are not considered as such today. The Koobi Fora early Homo material not assigned to H. habilis is allocated to the more recently named species H. rudolfensis, with an age of 2.5–1.8 Ma, which also includes specimens from Page 8 of 19

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_52-4 # Springer-Verlag Berlin Heidelberg 2013

Table 3 Fossil remains of Homo rudolfensis Homo rudolfensis (better-preserved specimens in bold) Skulls and Sites crania Mandibles Isolated Teeth Koobi Fora 1470, 1590, 819, 1482, – (KNM-ER) 3732, 3891 1483, 1801, 1802 Chemeron KNM-BC 1 – – Omo Omo 75-14 ? L7-279; L26-1 g; L28-30, L628-10; Omo 29-43; Omo 33-740, 5495, 5496; Omo 75i-1255; Omo 75 s-15, 16; Omo 177-4525; Omo 195-1630 West Lokalalei? – – Turkana WT 42718 Uraha (UR) – 501 1106

Postcranial –

–

– –

Chemeron, West Turkana (Prat et al. 2005), and Omo (Suwa et al. 1996; Ramirez Rozzi 1997), as well as northern Malawi (Schrenk et al. 1993) (Table 3). The species name rudolfensis was coined by Russian paleontologist Valerij Pavlovicˇ Alexeev, who in 1986 described KNM-ER 1470 as “Pithecanthropus rudolfensis,” after Lake Rudolf, the name of Lake Turkana prior to Kenyan independence in 1963.

Postcranial Skeleton The postcranial skeleton of H. habilis was characterized by Leakey et al. (1964) using a number of characteristics: the clavicle resembles that of H. sapiens, the hand shows broad terminal phalanges, and capitate and MCP articulations also resemble H. sapiens, but differ in respect to the scaphoid and trapezium, attachments of the superficial flexor tendons, and the robusticity and curvature of the phalanges. The foot bones resemble H. sapiens in the stout and adducted hallux and welldefined foot arches, but differ in shape of the talar trochlea surface and the relatively robust third metatarsal. All these features indicate an affinity toward H. sapiens and underline that the early postcranial material from Olduvai seems to be different from that of the australopiths. Functional implications based on more detailed descriptions of the foot (OH 8, OH 10) and leg (OH 35), both of which are probably from the same individual (Stern and Susman 1983), were generally more cautious (Wood 1992). According to Stern and Susman (1983), H. habilis had not reached the characteristic bipedal gait of H. sapiens, since the functional morphology of the knee joint was not well adapted for striding. Further analysis of the OH 8 foot demonstrated that some features, common in nonhuman hominoids, are also present in the foot bones (Lewis 1989). As more postcranial material was uncovered at Koobi Fora, interpretation of hind limb function of early Homo became more complex. However, some specimens, such as the femur KNM-ER-1472A and the talus KNM-ER-813, may belong to H. erectus or H. ergaster rather than to H. habilis (Tobias 1991). Although the partial skeleton OH 62 from Olduvai Gorge was interpreted as evidence for fully upright human bipedal locomotion, Haeusler and McHenry (2004) demonstrated that there is little evidence in support of ancestral body proportions with short legs and long arms in H. habilis. Their results suggest that it is more likely that earliest Homo possessed an elongation of the legs relative

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_52-4 # Springer-Verlag Berlin Heidelberg 2013

to A. africanus and A. afarensis, whereas long forearms were still retained (Johanson et al. 1987). With its upper-to-lower limb shaft length proportions, OH 62 falls within the upper range of modern humans and the lower range of chimpanzees due to the partial overlap between these taxa at small body sizes. KNM-ER 3735, the larger-bodied early Homo from Koobi Fora, falls well outside the chimpanzee range and reflects the average proportions of modern humans. Comparison of the Koobi Fora and Hadar postcranial remains has led to the interpretation that H. habilis did probably possess a modern pattern of limb shaft proportions, and the body proportions of OH 62 are in agreement with other available evidence of H. habilis postcranial material (Johanson et al. 1987), but Jungers (2009) judges OH 62 interlimb proportions as indeterminate. The change in the proportions of limb length toward the development of long legs may be indicative of longdistance terrestrial running in early Homo and probably implies a shift in hominid ecology (Bramble and Lieberman 2004).

Brain and Language A significant difference between early Homo and australopiths exists in brain size, which was larger in early Homo than in Australopithecus but smaller than H. erectus. Endocasts of H. habilis from Olduvai and Koobi Fora reveal a number of distinctive features, some of which are recognized as autapomorphies of the genus Homo. Tobias (1987) defined the principal morphological trait to distinguish H. habilis from Australopithecus as a larger mean endocranial capacity in the former (640 cm3) than in A. africanus (441 cm3), A. boisei (513 cm3), and A. robustus (530 cm3) (▶ The Evolution of the Hominid Brain; ▶ The Evolution of Speech and Language). This suggests that the evolutionary trend toward brain expansion was already well under way more than 2 Ma. The H. habilis mean (640 cm3) is close to the lower limit (647 cm3) of the 95 % population range of H. erectus but well above the upper limit of the A. africanus range (492 cm3). The brain capacity of the H. rudolfensis type specimen, originally reconstructed to give 752 cm3, is larger than the known range for H. habilis from Olduvai Gorge and Koobi Fora and falls within the lower range of H. erectus. However, the relationship between prognathism and cranial capacity in primates results in an estimate of KNM-ER 1470 cranial capacity of 625 cm3 (1 SD ¼ 49 cm3), and together with other considerations, a ca. 700 cm3 estimate is more realistic (Bromage et al. 2008). This revision is not inconsistent with other Late Pliocene Homo prior to the appearance of Early Pleistocene Homo erectus/ergaster (Holloway 1996). A prominent feature of the H. habilis brain is the bilateral transverse expansion of the cerebrum, especially in the frontal and parieto-occipital areas, and a posterior heightening. The increased bulk of cerebral frontal and parietal lobes and the sulcal and gyral patterns of the lateral frontal lobe have been interpreted as derived features for the genus Homo (Tobias 1987). The H. habilis brain showed a well-developed left superior parietal lobule and a prominent development of the inferior parietal lobule. The endocast of KNM-ER 1470 shows a left frontal lobe sulcal pattern that is associated with Broca’s area in living people (Falk 1987), a finding that has led to the conclusion that H. rudolfensis may have been capable of speech. This conclusion is in accordance with Holloway’s observation of a pronounced left-occipital-right-frontal petalia pattern in the KNM-ER-1470 endocast that may indicate functional cortical asymmetry (Holloway 1983). Surprising corroborative evidence has been provided by Toth’s analyses (▶ Overview of Paleolithic Archeology; ▶ Archeology) of stone flakes, which indicate that hominids were predominantly right-handed by 2 Ma (Toth 1985). Adjacent areas in the left frontal lobe control the speech organs and the right hand. Tobias Page 10 of 19

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_52-4 # Springer-Verlag Berlin Heidelberg 2013

(1991) stated that H. habilis is the earliest hominid to show prominent enlargement of Broca’s and Wernicke’s areas. If so, the same should be seen in H. rudolfensis. Australopithecus endocasts show Broca’s area, but not Wernicke’s region, while anthropoid apes display neither of the two. The prominent development of the two speech areas may thus be seen as an important autapomorphy of the genus Homo (Tobias 1991). Even if H. habilis and H. rudolfensis possessed the neurological bases of speech, there is no evidence that either of them used spoken language. The areas of the brain that control spoken (▶ The Evolution of the Hominid Brain) communication probably manifested themselves only when brain enlargement occurred and marked encephalization started.

Material Culture and Food Processing (▶ Archaeology; Role of Environmental Stimuli in Hominid Origins; ▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments; ▶ Analyzing Hominin Phylogeny) Around 2.5 Ma, simultaneously with an increase in drier and harder food stuffs due to increasing aridity in eastern Africa (de Menocal 2004), there occurred the first hyperrobust australopithecines (Paranthropus) and the first specimens identified as genus Homo in the fossil record (Bromage et al. 1995). This demonstrates an evolutionary alternative to the massive masticationary system of Paranthropus, which was capable of dealing with hard foods. There was a reduction in molar size in Homo rudolfensis relative to Paranthropus, but earliest Homo was nevertheless comparatively megadont, illustrating that while a larger and more possibly more cognitively complex brain may have helped early Homo to respond to changing environmental conditions, they must still have been somewhat dependent on hard and tough vegetative resources (Wood and Strait 2004). The evolutionary alternative to megadonty was the manufacturing and use of stone tools. The oldest chopper tools are known from Ethiopia (Hata, Bouri Formation) and from Tanzania, approximately 2.5 Ma (Kaiser et al. 1995). From Gona, east of Hadar in the Afar Triangle, primitive pebble tools are dated to 2.6 Ma (Harris 1986), and discoveries from west of Lake Turkana confirm the existence of an early tool culture around 2.5 Ma (Roche et al. 2003). Earliest cutmarks on bone fragments are reported from a 3.4-Ma-old site at Dikika in Ethiopia (McPherron et al. 2010) but have been interpreted as trampling marks by others (Domı´nguez-Rodrigo et al. 2010). The oldest stone tools associated with early Homo were found in the Hadar area of Ethiopia (Kimbel et al. 1996). At many sites the presence of more than one hominid species, occurring in the same horizon as early Oldowan pebbles, does not give clear evidence of who were the first toolmakers. However, distinct specialization of the skull and dental morphology in robust australopithecines and brain expansion in early Homo point to the latter as the most likely tool manufacturer (▶ Archaeology; ▶ Overview of Paleolithic Archeology). Implements are widely used by higher primates (Boesch and Boesch 1990) (▶ Great Ape Social Systems; ▶ Cooperation, Coalition, and Alliances; ▶ Theory of Mind: A Primatological Perspective). Yet during marked habitat shifts, which led to pronounced changes in food resources, it probably was the invention of stone tools which supported the origin of the genus Homo around 2.5 Ma. Increasing independence from the environment led to an increase in the dependence on culture. If early Homo utilized stone tools to prepare food, the dentition might actually reflect these behavioral changes in food acquisition. However, the morphology of early Homo teeth does not seem to suggest extensive food preparation before ingestion. The incisors are large compared to those of Australopithecus and H. erectus, and the canines are large relative to the premolar crown Page 11 of 19

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_52-4 # Springer-Verlag Berlin Heidelberg 2013

surfaces. The premolars are narrower than in Australopithecus and fall within the range of H. erectus. Molar size overlaps the ranges for Australopithecus and H. erectus. The cheek teeth of H. rudolfensis are enlarged and show affinities to Paranthropus molars. All teeth are relatively narrow buccolingually and elongated mesiodistally, especially the mandibular molars and premolars. In H. habilis we see well-developed third molars, while in H. rudolfensis, the third molar has a smaller crown than the second molar. The occlusal surface of the cheek teeth is not as broad as in australopithecine molars and indicates differences in chewing. Tobias (1987) states that the crown’s cusp relief is still present even when the teeth show advanced wear and dentine is visible. This means that the attrition of the enamel is less pronounced than in earlier hominids. Differences in tooth wear between H. rudolfensis, with megadont teeth and a more horizontal tooth abrasion, and H. habilis, with its more gracile molars and higher relief in worn teeth, are clearly visible. This indicates significant differences in diet and ecology of early H. species. H. rudolfensis and the robust australopithecines share some cranial and dental features in the morphology of the masticatory apparatus (Wood 1992), which indicates that these hominids were able to cope with hard fruits and plants. Since those features are judged as an adaptation to drier climatic conditions, they also show that H. rudolfensis was relatively conservative nutritionally and probably less versatile in his food choice than H. habilis and certainly H. erectus (Ungar et al. 2006).

Biogeographic Scenario The scenario presented here is derived mainly from hypotheses about early hominid evolution in the context of environmental change and faunal biogeography. It is thus a biogeographic perspective against which we understand the relevance to studies of early Homo systematics in general and morphology and character transformation more specifically. The behavioral inclination of the earliest hominids, distributed along the margins of the tropical rain forest, was to maintain a connection to, and remain near, the borders between broad riparian habitats and open woodlands during the ascendancy of more warm and humid times. Over short geological timescales, this typically involved a local, nondispersing tendency, but by approximately 4 Ma, several species of Australopithecus had successfully dispersed throughout the reaches of the African Rift Valley and into western Africa (Fig. 7). Over longer time frames, this included dispersal through the riparian “corridor” connecting eastern and southern Africa, permitting population dispersal into southern Africa by 3 Ma. This dispersing population maintained habitat specificities to forested environments (Rayner et al. 1993), though in more environmentally temperate climes and in relative geographical isolation at the extreme distal edge of its distribution. The dispersion along changing latitudinal circumstances covaried with its transformation into, first, a geographic variant and, subsequently, into A. africanus, joining ranks with other southern African endemic faunas. Thus, A. afarensis was essentially an eastern African endemic form, and it follows that no typical representatives are likely to be recovered from southern African deposits older than 3.5 Ma. (Figs. 6 and 7). By approximately 2.8 Ma, the initiation of cooler and drier conditions prevailed upon the African landscape, its vegetation, and its faunas, until climaxing ca. 2.5 Ma (▶ Role of Environmental Stimuli in Hominid Origins; ▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments) (Bonnefille 1980; Vrba 1985, 1988; Prentice and Denton 1988; de Menocal 2004). During this time, A. afarensis in eastern Africa and A. africanus in southern Africa were each subject to unique paleobiogeographic consequences of this global aridification, reflected in the “Habitat Theory” of Vrba (▶ Role of Environmental Stimuli in Hominid Origins) (1992). Page 12 of 19

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_52-4 # Springer-Verlag Berlin Heidelberg 2013

Fig. 6 Hominid chronology

For A. afarensis, then, the changing climate meant vicariance of its habitat and its distribution into more distant ecotonal riparian and closed lake margin environs. During the interim between ca. 2.8 and 2.5 Ma, these changing conditions engendered more extensive open habitats, comprising more resistant arid-tolerant vegetation around the remaining relatively lush but narrowed “ribbons” of tree-lined riverine forest. The selective pressures of this habitat change resulted in the increased survival of more megadont varieties capable of feeding on harder fruit and open woodland-open savannah food items. This was so for early hominid as well as numerous eastern and southern African large terrestrial vertebrate lineages ca. 2.5 Ma (Turner and Wood 1993). These pressures were likewise sufficient to result in the phyletic splitting of A. afarensis into Paranthropus and Homo lineages by ca. 2.5 Ma (Vrba 1988) (Figs. 6 and 7). Ensuing cooler and drier conditions favored a savannah vegetation composed of plant species better able to retain their moisture under such conditions. Selection favored more facially robust and large molar-toothed mammals, including early hominids, capable of efficiently processing harder, more durable vegetation of the savannah. Our evidence suggests that the tropical equatorial Page 13 of 19

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_52-4 # Springer-Verlag Berlin Heidelberg 2013

Fig. 7 Early hominid biogeography, dispersal and migration in Africa

animals, including the hominids, of eastern Africa stay in the tropical African ecological domain, while during the drying and cooling of global climates ca. 2.5 Ma, the southern and more temperate African faunas follow their northward-drifting vegetation zones. Thus, Homo and Paranthropus may have emerged in tropical Africa as a result of the ca. 2.5-Ma climatic cooling event and remained endemic to tropical latitudes during this time (Bromage et al. 1995). The eastern African tropical faunas, having habitable alternatives, remained within their biogeographic domains rather than braving the relative deterioration and paucity of habitats south of the African Rift Valley. The faunas of southern Africa were subject to a different set of environmental stimuli during the ca. 2.5-Ma cooling event. Waning of the forests and woodlands and expansion of more open arid grasslands not only invigorated evolutionary adaptations to savannah life in tropical eastern Africa but also resulted in the distribution drift northward of faunas that tracked the equatorial shift of grassland and woodland biomes into eastern Africa from the south, ca. 2.5 Ma (Bromage et al. 1995). The temperate zone ca. 2.5 Ma experienced more seasonal extremes, and many organisms unwittingly maintained their inherited preference for moderate seasonal climes and temperate vegetation by moving northward with the shrinking of this biome toward the equator, effectively transgressing the Zambezi Ecozone. Among these migrants was A. africanus which, having been adapted to a modest temperate ecology, now found its suitable habitats shifted to the north toward the East African Rift Valley. While dispersing toward the eastern African tropical domain, selection for increased behavioral flexibility was related to the habitat diversity of the tropics and the presence of other non-vegetative food resources available in their new region. This emerging taxon, H. habilis, rapidly established itself as a categorical omnivore and found that it could buffer itself more resolutely from environmental changes (Ungar et al. 2006). This enabled it

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_52-4 # Springer-Verlag Berlin Heidelberg 2013

to cross habitat boundaries more easily and also to advantage itself of more resources with its material culture. By approximately 2 Ma, Africa was rebounding from its relatively cool and dry climate to return to slightly more warm and humid conditions (Bromage et al. 1995). A phase of biome expansion ensued, which facilitated dispersions away from the equator, ending nearly 1 Myr of relative endemism dominated by tropical equatorial speciations. P. boisei dispersed southward, along reestablished ecotonal habitats, into southern Africa, became a geographic variant under more temperate conditions, and evolved into Paranthropus robustus (Fig. 6). Homo habilis expanded southward into the southern African temperate domain, but it maintained a very much broader niche and increased its distributional area as a single species. Homo rudolfensis remained endemic to the eastern African tropical domain due partly to its preference for more open habitats around the rain shadows of the African Rift Valley and partly, perhaps, to some small measure of competitive exclusion from geographic realms occupied by H. habilis. Whereas our model suggests the origin of early Homo in tropical (eastern) Africa, recent fossil discoveries from Malapa Cave South Africa (Berger et al. 2010), described as Australopithecus sediba, have been interpreted as potential evidence for a Southern African origin of Homo. The hip structure of this species seems more closely related to Homo erectus than to Homo rudolfensis or Homo habilis. However, with an age of less than 2 Ma, it seems more likely that these late australopiths were convergently adapted with rather than ancestral to the earliest Homo.

Conclusions The origin of the genus Homo is highly debated. Earliest fossil evidence dates to around 2.5 Ma and is in temporal co-existence with the appearance of Paranthropus in eastern Africa. The beginning of the Homo lineage, represented by H. rudolfensis, was an endorsement of its recency of common ancestry with A. afarensis, a distinction it shared with Paranthropus. However, while Paranthropus was principally adapted by means of a robust masticatory system to abrasive diet, early Homo exhibited an increased behavioral and dietary flexibility as its adaptation included a larger and more provoking, inquiring, and capable brain, which led to a large diversification represented by later Homo species, such as H. habilis/ergaster/erectus. This included a shift to proportionately less abrasive foodstuffs and more omnivorous habits. Increasing cultural abilities and the beginnings of a stone tool culture ameliorated the effects of changing habitats and food resources to the degree that it enabled early Homo to take advantage of diverse resources more efficiently than was ever possible before (▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments).

References Alt KW, Go¨tz H, Buitrago Tellez CH, Schrenk F, Duschner H, Henke W (2000) REM und 3D-CTAnalysen der Hominidenza¨hne von RC 911 aus Malema (Malawi/Afrika). In: Schultz M et al (eds) Internationale Anthropologie, Tagungsband des 3. Intern. Kongresses der GfA Go¨ttingen, Cuvillier-Verlag, Go¨ttingen, pp 15–19 Alexeev VP (1986) The origin of the human race. Progress Publishers, Moscow

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Berger LR, de Ruiter DJ, Churchill SE, Schmid P, Carlson KJ, Dirks PH, Kibii JM (2010) Australopithecus sediba: a new species of Homo-like australopith from South Africa. Science 328:195–204 Bermudez de Castro JM, Arsuaga JL, Carbonell E, Rosas A, Martinez I, Mosqueria M (1997) A hominid from the Lower Pleistocene of Atapuerca, Spain possible ancestor to Neanderthals and modern humans. Science 276:1392–1395 Blumenschine RJ, Peters CR, Masao FT, Clarke RJ, Deino A, Hay RL et al (2003) Late Pliocene Homo and hominid land use from western Olduvai Gorge, Tanzania. Science 299:1217–1221 Boesch C, Boesch H (1990) Tool use and tool making in wild chimpanzees. Folia Primatol 54:86–99 Bonnefille R (1980) Vegetation history of savanna in East Africa during the Pleistocene. Proc IV Int Palynol Conf Lucknow 3:75–89 Bramble DM, Lieberman DE (2004) Endurance running and the evolution of Homo. Nature 432:345–352 Bromage TG, Schrenk F, editors. Evolutionary history of the Malawi Rift. J Hum Evol 1995;28: 1–120 Bromage TG, Schrenk F, Zonneveld FW (1995b) Paleoanthropology of the Malawi Rift: an early hominid mandible from the Chiwondo Beds, northern Malawi. J Hum Evol 28:71–108 Bromage TG, McMahon JM, Thackeray JF, Kullmer O, Hogg R, Rosenberger AL, Schrenk F, Enlow DH (2008) Craniofacial architectural constraints and their importance for reconstructing the early Homo skull KNM-ER 1470, J Clinical Pediatr Dent 33(1):43–54 Curnoe D (2010) A review of early Homo in southern Africa focusing on cranial, mandibular and dental remains, with the description of a new species (Homo gautengensis sp. nov.). Homo J Comp Hum Biol 61:151–177 de Menocal PB (2004) African climate change and faunal evolution during the PliocenePleistocene. Earth Planet Sci Lett 220:3–24 Domı´nguez-Rodrigo M, Pickering TR, Bunn HT (2010) Configurational approach to identifying the earliest hominin butchers. Proc Natl Acad Sci 107(49):20929–20934 Dubois E (1892) Palaeontologische anderzoekingen op Java. Verslag van het Mijnwezen, Batavia, 3: 10–14 Falk D (1987) Hominid paleoneurology. Annu Rev Anthropol 16:13–30 Groves CP, Maza´k V (1975) An approach to the taxonomy of the Hominidae: Gracile Villafranchian hominids of Africa. Casopis pro Mineralogii A Geologii 20:225–247 Haeusler M, McHenry HM (2004) Body proportions of Homo habilis reviewed. J Hum Evol 46:433–465 Harris JWK (1986) De´couverte de materiel arche´ologique oldowayen dans le rift de l’Afar. Anthropologie 90:339–357 Henke W, Hardt T (2011) The genus Homo: origin, speciation and dispersal. In: Condemi S (ed) Continuity and discontinuity in the peopling of europe: one hundred fifty years of Neanderthal study, Vertebrate Paleobiology and Paleoanthropology. Springer, Netherlands, pp 17–43 Hill A, Ward S, Deino A, Curtis G, Drake R (1992) The earliest Homo. Nature 355:719–722 Holloway RL (1983) Human brain evolution: a search for units, models and synthesis. Can J Anthropol 3:215–230 Holloway RL (1996) Evolution of the human brain. In: Lock A, Peters C (eds) Handbook of human symbolic evolution. Oxford University Press, New York, pp 74–116 Hughes AR, Tobias PV (1977) A fossil skull probably of the genus Homo from Sterkfontein, Transvaal. Nature 265:310–312 Page 16 of 19

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Johanson DC, Masao FT, Eck GG, White TD, Walter RC, Kimbel WH, Asfaw B, Manega P, Ndessokia P, Suwa G (1987) New partial skeleton of Homo habilis from Olduvai Gorge, Tanzania. Nature 327:205–209 Jungers W (2009) Interlimb proportions in humans and fossil hominins: variability and scaling. In: Grine FE, Leakey RE, Fleagle JG (eds) The first humans: origins of the genus Homo. Springer, Dordrecht, pp 93–98 Kaiser T, Bromage TG, Schrenk F (1995) Hominid corridor research project update: new Pliocene fossil localities at Lake Manyara and putative oldest Early Stone Age occurrences at Laetoli (Upper Ndolanya Beds), northern Tanzania. J Hum Evol 28:117–120 Keith A (1948) A new theory of human evolution. CA Watts & Company, London Kimbel WH, Walter RC, Johanson DC, Red KE, Aronson JL, Assefa Z, Marean CW, Eck GG, Bobe R, Hovers E, Rak Y, Vondra C, Yemane T, York D, Chen Y, Evensen NM, Smith PEB (1996) Late Pliocene Homo and Oldowan tools from the Hadar Formation (Kada Hadar Member), Ethiopia. J Hum Evol 31:549–562 King W (1864) The reputed fossil man of the Neanderthal. Q J Sci 1:88–97 Kullmer O, Sandrock O, Abel R, Schrenk F, Bromage TG, Juwayeyi Y (1999) The first Paranthropus from the Malawi Rift. J Hum Evol 37:121–127 Kullmer O (2008) The plio-pleistocene Suids (Suidae; Artiodactyla) of the Chiwondo Beds, northern Malawi. J Vertebr Paleontol 28(1):208–216 Kullmer O, Sandrock O, Kupczik K, Frost SR, Volpato V, Bromage TG, Schrenk F (2011) New primate remains from Mwenirondo, Chiwondo Beds in northern Malawi. J Hum Evol 61:617–623 Leakey LSB (1959) A New fossil Skull from Olduvai. Nature 184:491–493 Leakey LSB (1961) The juvenile mandible from Olduvai. Nature 191:417–418 Leakey RE (1973a) Evidence for an advanced plio-pleistocene hominid from East Rudolf, Kenya. Nature 242:447–450 Leakey RE (1973b) Further evidence of Lower Pleistocene hominids from East Rudolf, north Kenya. Nature 248:653–656 Leakey LSB, Tobias PV, Napier JR (1964) A new species of the genus Homo from Olduvai Gorge. Nature 202:7–10 Lewis OJ (1989) Functional morphology of the evolving hand and foot. Oxford University Press, Oxford Linnaeus C (1758) Systema naturae. Laurentii Salvii, Stockholm Lordkipanidze D, Ponce de Leo´n MS, Margvelashvili A, Rak Y, Rightmire GP, Vekua A, Zollikofer CPE (2013) A complete skull from Dmanisi, Georgia, and the evolutionary biology of early Homo. Science 342:326–331 Mayr E (1944) On the concepts and terminology of vertical subspecies and species. Natl Res Council Bull 262:11–16 McPherron SP, Alemseged Z, Marean CW, Wynn JG, Reed D, Geraads D, Bobe R, Be´arat HA (2010) Evidence for stone-tool-assisted consumption of animal tissues before 3.39 million years ago at Dikika, Ethiopia. Nature 466:857–869 Prat S, Brugal J-P, Tiercelin J-J, Barrat J-A, Boh M, Delagnes A, Harmand S, Kimeu K, Kibunjia M, Texier P-J, Roche H (2005) First occurrence of early Homo in the Nachukui Formation (West Turkana, Kenya) at 2.3–2.4 Myr. J Hum Evol 49:230–240 Prentice ML, Denton GH (1988) The deep-sea oxygen isotope record, the global ice sheet system and hominid evolution, In: Grine FE (ed) Evolutionary History of the “Robust” Australopithecines. Aldine de Gruyter, New York, pp. 383–403 Page 17 of 19

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Ramirez Rozzi F (1997) Les hominide´s du Plio-Ple´istoce`ne de la valle´e de l’Omo. Cahiers de pale´oanthropologie CNRS e´ditions, Paris Rayner RJ, Moon BP, Masters JC (1993) The Makapansgat australopithecine environment. J Hum Evol 24:219–231 Roche H et al (2003) Les sites arche´ ologiques plioplee´istoce`nes de la formation de Nachukui, Ouest Turkana: bilan synthe´tique 1997–2001. CR Palevol 2:663–673 Schoetensack O (1908) Der Unterkiefer des Homo heidelbergensis aus den Sanden von Mauer bei Heidelberg. W Engelmann, Leipzig Schrenk F, Bromage TG, Betzler C, Ring U, Juwayeyi Y (1993) Oldest Homo and Pliocene biogeography of the Malawi Rift. Nature 365:833–836 Stern JT, Susman RL (1983) Locomotor anatomy of Australopithecus afarensis. Am J Phys Anthropol 60:279–317 Suwa G, White TD, Howell FC (1996) Mandibular postcanine dentition from the Shungura Formation, Ethiopia: crown morphology, taxonomic allocations, and Plio-Pleistocene hominid evolution. Am J Phys Anthropol 101:247–282 Tobias PV (1987) The brain of Homo habilis: a new level of organization in cerebral evolution. J Hum Evol 16:741–761 Tobias PV (1991) Olduvai Gorge: The skulls, endocasts and teeth of Homo habilis. Cambridge University Press, Cambridge, vol 4 (1–2) Tobias PV, von Koenigswald GHR (1964) A comparison between the Olduvai hominines and those of Java and some implications for hominid phylogeny. Nature 204:515–518 Toth N (1985) Archeological evidence for preferential right-handedness in the lower and middle Pleistocene, and its possible implications. J Hum Evol 14:607–614 Turner A, Wood BA (1993) Comparative palaeontological context for the evolution of the early hominid masticatory system. J Hum Evol 24:301–318 Ungar PS, Grine FE, Teaford MF (2006) Diet in early Homo: a review of the evidence and a new model of adaptive versatility. Annu Rev Anthropol 35:209ev Vrba ES (1985) Ecological and adaptive changes associated with early hominid evolution. In: Delson E (ed) Ancestors: the hard evidence. Alan R. Liss, New York, pp 63–71 Vrba ES (1988) Late Pliocene climatic events and human evolution. In: Grine FE (ed) Evolutionary history of the “Robust” Australopithecines. Aldine de Gruyter, New York, pp 405–426 Vrba ES (1992) Mammals as a key to evolutionary theory. J Mamm 73:1–28 Wood BA (1991) Koobi Fora research project, vol 4: Hominid Cranial remains. Clarendon Press, Oxford Wood BA (1992) Origin and evolution of the genus Homo. Nature 355:783–790 Wood BA (2000) The history of the genus Homo. Hum Evol 15(1–2):39–49 Wood BA, Collard M (2001) The meaning of Homo. Ludus Vitalis IX(15):63–74 Wood BA, Lonergan N (2008) The hominin fossil record: taxa, grades and clades. J Anat 212:354–376 Wood BA, Strait D (2004) Patterns of resource use in early Homo and Paranthropus. J Hum Evol 46:119–162

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Index Terms: Aridity 11 Bipedality 3, 9 Brain size 10 Broca’s area 11 Cerebrum 10 Chronospecies 2 Climate change 6, 13–14 Culture 11 Cutmarks 11 Diet 12, 15 Endocranium 10 Homo habilis 4–5, 7–8, 15 Homo rudolfensis 5–7, 9, 11, 15 Megadonty 11 Morphospecies 2 Oldowan 2 Postcranial skeleton 9 Rift Valley 12, 14 Robusticity 2, 6, 9 Savannah 1, 13–14 Stone tools 11 Wernicke’s area 11

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_53-5 # Springer-Verlag Berlin Heidelberg 2013

Homo ergaster and Its Contemporaries Ian Tattersall* Division of Anthropology, American Museum of Natural History, New York, NY, USA

Abstract On the basis of their strong morphological differences from the Javan type materials, many authorities now consider the diverse East African fossils initially classified as “African Homo erectus” to be more properly allocable to the species H. ergaster. However, while this separation at the species level of the African and Indonesian hominids is certainly justified, the species H. ergaster as thus constituted still embraces a significant morphological variety. Indeed, although this grouping of African fossils seems to form a fairly coherent clade, it also appears quite diverse. The East Turkana type mandible of H. ergaster is matched by other specimens from Kenya and Tanzania, but not by the mandible of the iconic WT 15000 skeleton, and in its turn this specimen fails to match either in its cranial construction or its upper dentition most of the other comparable specimens usually referred to H. ergaster. Clearly there is a need for a systematic reappraisal of the entire “African Homo erectus” ¼ Homo ergaster group, and equally clearly the hominid evolutionary story throughout the Old World in the Early–Middle Pleistocene was more complex than is implied by the extension of the species H. erectus to cover the entire miscellaneous assemblage of hominid fossils from this time period.

Introduction There is probably no area of paleoanthropology in which disagreement is more profound than in the systematics and taxonomy of the genus Homo in the Early to Middle Pleistocene. This discord has a long and, dare one say it, illustrious pedigree, dating right back to the initial discovery and description of the Javan species Pithecanthropus (¼Homo) erectus by Eugene Dubois in the early 1890s. At that time the only extinct hominid known was the European H. neanderthalensis, a form that, though peculiar in morphology, possessed a brain of modern human size. The new and more ancient hominid announced by Dubois as an intermediate between modern humans and apes (a status reflected in his initial choice of name, which translates as “upright ape-man”) was thus the first known human fossil relative to display a brain cavity that was significantly larger than those of modern-day great apes while lying below the range of H. sapiens. Dubois’s discovery unleashed an immediate furor. The key to Dubois’s interpretation of this specimen as a human relative (though he stopped short of placing his find in the human family Hominidae) was the association of the type Trinil skullcap with a femur whose morphology was without doubt that of an upright biped in the modern fashion. This association was immediately attacked (and has continued to be periodically

*Email: [email protected] Page 1 of 18

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_53-5 # Springer-Verlag Berlin Heidelberg 2013

questioned), initially by those who preferred to see the cranium as that of a specialized ape, maybe related to the gibbons. At the same time, many of those who accepted the association between the cranium and femur wrote off the former as deriving from an aberrant modern human (see discussion in Tattersall 1995, 2008). Still, some paleoanthropologists (Cunningham 1895) did seize immediately upon the Trinil specimen as an evolutionary intermediate between great apes and humans, and were willing to view the Javan hominid as an early member of a lineage that had given rise to H. sapiens via the Neanderthals. This interpretation rapidly gained ground (Theunissen 1988), and by early in the twentieth century, not least through the efforts of Schwalbe (1899) – and despite those of Boule (1911–1913) – the place of H. erectus as the “hominid in the middle” had effectively been secured. Given the tiny size of the hominid fossil record at that time, and that the apparent rudiments of a transformation series in brain size were present in what was known, this interpretation was hardly surprising: indeed, it was a good story that was hardly contradicted by the few facts then available. And, in the decades before the Second World War, two additional developments conspired to keep H. erectus at the front and center in scenarios of human evolution. The first of these was the discovery of the huge trove of Sinanthropus pekinensis fossils at Zhoukoudian near Beijing during the late 1920s and the 1930s, and of the similarly impressive series of H. soloensis crania at Ngandong in Java in 1931–1932. The hominids from both sites were reckoned to be very close to Javan H. erectus, if not exactly the same thing; and at a time when most hominid fossil sites produced a specimen here and there, both discoveries were overwhelming by virtue of the sheer volume of material produced. At the same time geneticists, systematists, and paleontologists in the USA and Europe were busily constructing the outlines of what came to be known as the Evolutionary Synthesis, which saw the gradual modification of continuous lineages as the central feature of the evolutionary process (see discussion in Tattersall 1995). And at midcentury, the ornithologist Ernst Mayr (1950), one of the principal architects of the Synthesis, bluntly told the paleoanthropological profession that S. pekinensis, H. soloensis, and other Middle Pleistocene hominids all belonged to H. erectus, the species that occupied the middle part of a direct and gradually transforming lineage running from H. transvaalensis (the australopiths) at the beginning to H. sapiens (which embraced the Neanderthals) at the summit. Mayr’s short article was perhaps the most influential contribution ever in paleoanthropology, and effectively set its agenda for the next half-century. The rapidly increasing size of the human fossil record eventually forced even Mayr to relent, and to admit a little more complexity into the picture; but for decades, paleoanthropologists labored steadfastly under the notion that the evolutionary history of our kind had largely involved the gradual modification through time of a central lineage that eventually culminated in H. sapiens. Of course, it was admitted that at any one point in time such a lineage, widely distributed across the Old World, would have harbored a variety of local variants (see chapter on “▶ Defining Homo erectus” by Baab); but throughout the second half of the twentieth century, the emphasis was principally on within-species variation, rather than on the question of whether a signal of systematic (species) diversity might be detectable in the variety of morphologies that emerged as the hominid fossil record steadily enlarged. Against this background, the category H. erectus became a catchall for a huge and unwieldy assortment of fossils of substantially differing morphologies. Such hominids came from widely scattered localities. First, the probably 1.0- to 0.7-million-year (myr)-old Trinil specimens from Java were joined by a steady stream of discoveries in the nearby Sangiran Dome, not far away, that probably date in the 1.5- to 1.0-myr range, most of them closer to its younger end. Then the sample was augmented by the Chinese Peking Man fossils, now thought to be probably between about 500 and 300,000 years (kyr) old, followed by the Ngandong Page 2 of 18

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_53-5 # Springer-Verlag Berlin Heidelberg 2013

specimens (which may be as young as 50–30 kyr old), and ultimately by other Javanese fossils from localities such as Sambungmacan and Ngawi, both uncertainly dated but unlikely to be more than 200 kyr old, and most probably younger. In China, later finds attributed to H. erectus came from sites including Lantian (Gongwangling and Chenjiawo, both perhaps around 1.0 myr), Hexian (maybe 400 kyr), Nanjing (ca. 350 kyr), and even Longgupo, a site that may possibly be as much as 1.8 myr old. Some European specimens in the 400–300 kyr range, such as those from Ve´rtesszo¨llo¨s (Hungary), Arago (France), and Bilzingsleben (Germany), have been referred by some authors to H. erectus, as has the 900- to 800-kyr-old calvaria from Ceprano in Italy. Further east, in the Caucasus, the 1.8-myr-old Georgian site of Dmanisi has yielded fossils that have also been attributed to H. erectus. In Africa practically anything from the earlier Middle Pleistocene, and soon many older specimens as well, found themselves identified as H. erectus, so that the species came to include such motley fossils as the 1.4-myr-old Olduvai Hominid (OH) 9 calvaria from Tanzania; the 700-kyr-old mandibles from Tighenif (Ternifine) in Algeria; the 400-kyr-old Sale´ partial braincase from Morocco; the 1.6-myr-old WT 15000 “Turkana Boy” skeleton from Nariokotome on the western side of Lake Turkana in Kenya, and several crania and mandibles in the 1.9–1.5-myr range from Koobi Fora and Ileret on the eastern side of the same lake; also from Kenya, the fragmentary Olorgesailie hominid at 1.0–0.9 myr; the 1-myr-old Daka calvaria from Ethiopia; a cranium of apparently similar age from Buia in Eritrea; and even, from South Africa, the perhaps 1.6-myr-old Swartkrans Member 1 SK 847 partial cranium. Not only do these fossils cover an enormous span of time (ca. 1.8–0.03 myr), but they also embrace a huge range of morphologies, and taken together they hardly suggest a neat chronological series of the kind the Synthesis had predicted. Clearly, there is a systematic signal of some kind in the assemblage of hominid fossils that have at one time or another been allocated to Homo erectus: a signal of diversity at the species as well as the morphological level. But it was not until the beginning of the final quarter of the twentieth century that this possibility began to be seriously investigated.

Enter Homo ergaster The existence of H. erectus as a convenient catchall for a remarkable variety of hominids certainly facilitated the telling of a relatively simple and straightforward human evolutionary story that could be told in terms of consistent long-term selection pressures for such things as more perfect thermoregulation, more efficient digestion, and above all greater intelligence. However, this story of the gradual honing over time of an ever more effective human machine was contradicted by the growing post-Synthesis realization that the evolutionary process consists of a great deal more than simple natural selection (Tattersall 1995, 1998). It also sat rather uneasily with the fact that the Pleistocene was increasingly being seen as a period of extraordinary short-term climatic oscillations as well as of longer-term fluctuations (see chapter on “▶ Quaternary Geology and Paleoenvironments” by Van Couvering). And, most significantly of all, it was not the story that the growing assemblage of Homo fossils seemed to be telling. The first shot across the bows of the all-encompassing notion of H. erectus came from work on fossils found at the classic African localities on the eastern shores of Lake Turkana. During the 1970s, several fossils, notably the partial crania KNM-ER 3733 and KNM-ER 3883, were discovered at Koobi Fora that their describers (Leakey and Walker 1976; Walker and Leakey 1978) ascribed to the species H. erectus. With cranial volumes of 848 and 804 ml respectively (these and most of the other endocranial volumes cited here come from Holloway et al. 2004), these Page 3 of 18

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Fig. 1 Lateral view of the KNM-ER 992 holotype mandible of H. ergaster. Scan of cast by Ken Mowbray

1.8- and 1.6-myr-old individuals had possessed brains almost as large as that of Dubois’s much younger (1.0–0.7 myr) Trinil type specimen of H. erectus, at about 950 ml. Another significant specimen was a well-preserved mandible, KNM-ER 992 (Fig. 1), about 1.5 myr old, which was recovered at Ileret and described simply as Homo of indeterminate species (Leakey 1972). Soon thereafter, Groves and Mazak (1975) jumped into the fray and made ER 992 the type specimen of a new species, H. ergaster. Although this innovation was disdainfully dismissed by the Koobi Fora team, and some other influential workers (Rightmire 1990) also continued to prefer the more comprehensive concept of H. erectus, this move finally opened the door to a reappraisal of the tradition of automatically assigning to H. erectus any and all African fossils with measured or assumed brain sizes in the general range of those noted above. In short, it became possible to entertain the notion that H. erectus is a terminal eastern Asian hominid species, and that hominid evolution throughout the Early and Middle Pleistocene continued in the pattern already established, with a vigorous exploration of the many different ways in which it was possible to be a hominid in the shifting and highly varied habitats of the Ice Age Old World. The next section, on “Cranial Morphologies in Homo of the Early to Middle Pleistocene,” will examine the morphological evidence for diversity within the immediate group to which both H. ergaster and H. erectus belong.

Cranial Morphologies in Homo of the Early to Middle Pleistocene General Considerations Nobody doubts that the H. erectus/H. ergaster group represents a relatively cohesive subset of the family Hominidae. The question, clearly, is whether in this group of fossils we are looking at a radiation of species or at a single hugely variable species that may or may not have evolved directionally over the entire expanse of time (about 1.9–1.8 to 0.03 myr) and space (virtually the entire habitable Old World) it occupied. The distinction here is an important one, for species (even if not greatly differentiated morphologically from their closest relatives) are historically individuated entities which can compete with one another for ecological space and become extinct without trace, whereas within species even demes that are significantly differentiated morphologically remain ephemeral entities that can disappear simply by absorption into ongoing conspecific

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Fig. 2 Lateral view of the Trinil holotype calotte of H. erectus (Photo courtesy of #Jeffrey H. Schwartz)

populations. The twin processes of speciation and genetic/morphological differentiation are not linked, so that speciation may take place in the absence of significant morphological divergence, while the latter can occur without speciation intervening. This, of course, often makes unequivocal species recognition difficult in fossil assemblages (Tattersall 1986). However, it seems generally to be the case among living primates that, where substantial osteological differences are present among populations, those populations tend to act in nature as distinct species (i.e., as effectively independent reproductive entities). If we apply this criterion very conservatively to species recognition in the fossil record, demanding that the fossil species we recognize consistently bear distinctive osteological differences from related forms, we will probably underestimate the number of species in that record. However, we will not distort its overall pattern (Tattersall 1986, 1992). It is important to bear in mind that not all “morphs” (distinctive morphological entities) that we recognize in the fossil record will necessarily correspond to species in the reproductive sense; but it is equally evident that, given the nature of the fossil record, morphology must be the starting point in our analyses of it. After all, neither geological age nor geographical provenance, the other two attributes of any fossil, is necessarily linked to species identity, while its morphology is the only feature that makes a fossil species recognizable at all. It is in this spirit that the remainder of this survey is offered, with the proviso that we will clearly not learn much that is useful about the pattern of events in hominid evolution during the Pleistocene if we do nothing more than replace the term “African Homo erectus” with the equally sweeping H. ergaster.

Eastern Asia Given the established conventions of nomenclature and systematics, when we begin to consider the mass of material that has at one time or another been allocated to H. erectus/H. ergaster we must necessarily, begin with Dubois’s holotype material (Fig. 2) from Trinil in Java (Schwartz and Tattersall 2003, 2005). It is the morphology of the Trinil skullcap that defines the species H. erectus, and the allocation of other fossils to this named entity must be done on the basis of their morphological similarities to it. The problem lies, of course, in deciding just how close those similarities should be, and it has to be admitted that there is no quantifiable answer to this question. The Trinil 2 holotype is highly derived among hominids in a number of characteristics, especially of the brow region and the rear of the skull (Schwartz and Tattersall 2000, 2005). It is a smallish, long, thin-boned calotte with a narrow, shelflike, and laterally flaring postorbital region that flows onto the long, gently sloping, and flattish frontal plane with an almost imperceptible midline keel defined by shallow depressions bilaterally. The lateral walls of the low braincase are

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_53-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 3 Lateral views of crania from Africa and Eurasia in the “Homo erectus/Homo ergaster” group. Left column, top to bottom: Sangiran S17; Koobi Fora KNM-ER 3733; Koobi Fora KNM-ER 3732; West Turkana KNM-WT 15000; Dmanisi D 2282. Right column, top to bottom: Zhoukoudian cranial reconstruction (Sawyer and Tattersall version); Koobi Fora KNM-ER 3883; Olduvai OH 9; Koobi Fora KNM-ER 1813 (scale ¼ 1 cm) (From Schwartz and Tattersall (2005). Photo courtesy of #Jeffrey H. Schwartz; Turkana fossil images courtesy of National Museums of Kenya)

short and are markedly tilted inwardly above faint, low-set temporal lines; and the rather acute nuchal angle is distended posteriorly into a well-defined horizontal torus. Although the hominid sample from the adjacent Sangiran region is quite variable, especially in robusticity, the basic Trinil braincase morphology is repeated in most of the crania, the major exception being the quite complete if somewhat distorted cranium Sangiran 17 (Fig. 3). The Sangiran sample of upper and

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_53-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 4 Occlusal views of mandibles. Top left: left side of Koobi Fora KNM-ER 992. Top right: Koobi Fora KNM-ER 3734. Middle left: Olduvai OH 22; Middle right: left side of West Turkana KNM-WT 15000. Bottom: left side of Dmanisi D 211 (scale ¼ 1 cm) (From Schwartz and Tattersall (2005). Photo courtesy of #Jeffrey H. Schwartz; Turkana fossil images courtesy of National Museums of Kenya)

lower dentitions is also heterogeneous, suggesting that a second hominid morph may be present in addition to the Trinil one. The two (now three) crania known from the Sambungmacan region, to the northeast of Sangiran, are substantially younger than the Trinil/Sangiran assemblage and share a contrasting brow structure in which the quite horizontal supraorbital tori thicken laterally and appear to be continuous across glabella. The braincase itself has the appearance of being rather better inflated than typical of the Trinil form (the two published brain volumes are 1,035 and 917 ml), and the coronal profile is tent-shaped rather than having a squat and rounded outline. The nuchal plane undercuts the occiput to produce a horizontal torus that is well defined below, but has much poorer definition above. Together these specimens, along with another calvaria from Ngawi (870 ml), produce a morph that generally resembles the Trinil type but is readily distinguishable from it. The Ngandong crania are similarly distinctive. Larger, and more robust than the others, with endocranial volumes that range from 1,015 to 1,250 ml, they differ from the Trinil form in the ways in which the Sambungmacan ones do. However, in addition they present yet more capacious braincases that have more or less vertical side walls with quite aggressively raised temporal lines; and they show a greater rearward projection than the Sambungmacan forms do of the occipital Page 7 of 18

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torus, a feature with a well-defined superior border. Nonetheless, this entire group is united, in particular, by a set of derived supraorbital and nuchal morphologies, and it presents itself as a relatively cohesive whole. Clearly, these Javan forms are part of the same eastern Asian hominid clade and, if it is not divided up (basically, at this point, a matter of taste), it is this assemblage that must provide the core identity of the species H. erectus. The hominid fossils from Locality 1 of Zhoukoudian, in China (Fig. 3), have generally been considered classic exemplars of H. erectus. But it is still worthwhile noting that as a group they do differ fairly markedly from the Trinil type material, though mostly in ways that recall the Sambungmacan/Ngandong series. The crania from this site (with brain volumes ranging from 850 to 1,140 ml) are most distinctive in their supraorbital morphology, with a low-set glabella, supraorbital tori having a strong vertical component, and a continuous posttoral sulcus. In addition, there are marked dental differences between the Zhoukoudian and Sangiran samples (Schwartz and Tattersall 2005). Chinese specimens closely resembling the Peking Man materials include the Nanjing crania (L€ u and the Tangshan Archaeological Team 1996). Other materials sometimes associated with them, such as those from Lantian, Hexian, Yunxian, and Longgupo, show a variety of differences both from Zhoukoudian and among themselves. These differences are discussed by Schwartz and Tattersall (2005) and Tattersall and Schwartz (2009).

Africa As already noted, at one time or another many African fossils in the 1- to 2-myr time range have been referred to the species H. erectus. Among them, the classic exemplars are fossils from the Turkana Basin of northern Kenya, notable among these being the cranium KNM-ER 3733 and the calvaria ER 3883 from sediments at Koobi Fora to the east of Lake Turkana, and the fairly complete skeleton KNM-WT 15000 from deposits to its west at Nariokotome. The mandible KNM-ER 992, initially allocated simply to Homo sp., comes from Ileret, to the north of Koobi Fora. All the specimens concerned date within the 1.9- to 1.5-myr range. The widely used term “African Homo erectus” was a convenient designation for these fossils and a host of others, but it disguises the fact that a substantial variety of morphologies is involved. This reality was first acknowledged in 1975 by Groves and Mazak who, as noted, made the ER 992 mandible (Figs. 1 and 4), the holotype of the new species H. ergaster (“work man”). Subsequently, many authors have begun to use the new name in place of “African Homo erectus” to the extent that it is now H. ergaster that is the standard-issue Homo of the 2- to 1-myr period. Still, all this change has achieved is to remove the assortment of Asian morphologies from the African equation, and it does nothing to address the morphological variety found within the continent in this period. In coming to grips with this, the best place to start is with the iconic example, the KNM-ER 3733 cranium (Fig. 3), which has an endocranial capacity of 848 ml. In this individual, the supraorbitals arc separately over each orbit and project forward as well as upward. There is thus a distinct posttoral sulcus in front of the quite steep frontal rise, which rapidly peaks before the profile descends more gradually rearward. Seen from behind, the braincase is rather tall compared to its breadth, and its side walls are curving. The raised temporal lines start quite far medially. It is unsurprising that these characteristics distinguish this specimen sharply from any Asian Homo; more remarkable are its differences from the ER 3883 cranium (Fig. 3), which has an endocranial volume of 804 ml. This individual has very thickened supraorbital margins that protrude outward but slightly down, overhanging nasion, and the (mostly missing) face beneath. Further, in this specimen the frontal slopes strongly up and back, reaching its maximum height rather far back. Unlike in ER 3733, the mastoid is large and protruding, and in what is preserved of

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_53-5 # Springer-Verlag Berlin Heidelberg 2013

the face the zygoma flares outward from top to bottom. That this morphology is no freak is shown by its close repetition in preserved features of the ER 3732 partial cranium (Fig. 3). Interestingly, all the specimens just mentioned are distinctly different from the skull of the KNM-WT 15000 skeleton (Fig. 3), exhaustively described in the monograph edited by Alan Walker and Richard Leakey (1993). This 1.6-myr-old skeleton is remarkable both for its degree of completeness and for being the earliest good evidence we have in the human fossil record of the arrival of essentially modern stature and postcranial proportions. Frustratingly, we cannot yet be certain that this was the case for the possessors of the ER 3733 and ER 3883 crania. The adolescent WT 15000 individual died at about 8 years of age, but was at a stage of development approximating that of a modern 12-year-old. This presumed male stood about 160 cm tall, but had he survived to adulthood, it is estimated that he would have topped 180 cm. He was long limbed and slender, with efficient heat-shedding proportions that would have served him well in the heat of the open tropical savanna. In contrast to the relatively long crania just described, the braincase of WT 15000, with a capacity of about 900 ml, was quite short and had a well-rounded profile. To the extent that it is possible to judge, the badly damaged supraorbital surfaces amounted to little more than substantial thickenings of the superior orbital margins, lacking either the aggressive projection seen in ER 3733 or the vertical thickening noted in ER 3883. The structure of the face contrasts with that seen in both ER 3733 and ER 3883; it is longer and narrower, with much more alveolar prognathism, a higher and narrower nasal aperture, and preserved portions of the nasal bones that suggest a flatter profile of the upper face. It is often claimed that these differences from the East Turkana specimens are due to the subadult status of WT 15000, but this appears rather dubious since differences of this kind would, if anything, probably have become more marked with age. Cranial differences are backed up by dental comparisons to the extent that these are possible. ER 3883 has no associated teeth, and ER 3733 has only one, an upper M2. But this tooth, though unfortunately quite heavily worn, is nonetheless distinctly different from its counterpart in WT 15000. The upper M2 of ER 3733 has smooth enamel and well-defined trigon cusps, with the paracone much larger than the metacone. The hypocone is distally placed, the cristae are sharp, and both basins are well excavated. In WT 15000, in contrast, the upper M2s are high 1/N crowned with fairly flat but wrinkled occlusal surfaces. The cusps of the trigon are subequal in size, and the basins are quite shallow. In both ER 3733 and WT 15000, the upper M2s contrast with their homologues in the best-preserved upper dentition from Java, the Sangiran 4 palate, in which there are low cusps, a massive hypocone, and a very large postprotocrista that is not a feature of either African specimen. The ER 992 type specimen of H. ergaster is a lower jaw, so comparisons to ER 3733 and ER 3883 are not possible. However, uniquely, the WT 15000 skull has a definitively associated lower jaw (Fig. 4), allowing direct comparison to ER 992. When this comparison is made, clear differences become apparent. In ER 992 (Fig. 4), the lower canines are quite high and are compressed buccolingually. In the anterior lower premolar, there are distinct anterior and posterior foveae, and the protoconid is the clearly dominant cusp. In the posterior premolar the protoconid and metaconid are subequal, and the basins are shallow. The elongated lower molars bear rounded and protruding hypoconulids, their basins are shallow, and their enamel is wrinkled. In contrast, the lower canines of WT 15000 are short crowned, with distinct mesial and distal foveae that bound a strong lingual pillar that swells out the tooth at its base. Both premolars have deep mesial and distal basins. The first molar is distended mesially, and both erupted molars have large and lingually placed hypoconulids and narrow but deep talonid basins that are surrounded by welldefined but rather bulbous cusps. Here, again, we have two distinctly different lower dental morphologies, both of which also differ from their homologues known from Sangiran. Page 9 of 18

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Morphologically, at least, the lower dentitions of ER 992 and WT 15000 are not “the same thing,” and both are at variance with Javan H. erectus (Schwartz and Tattersall 2000, 2005). Interestingly, the 1.5-myr-old ER 992 from Ileret makes a fairly good match for the mandible OH 22 (Fig. 4) from Olduvai Gorge in Tanzania, as well as for its rather older (1.9 myr) neighbor ER 3734 (Fig. 4) from Koobi Fora. As for WT 15000, its lower teeth compare quite closely with those of OH 13, one of the paratypes of H. habilis from Bed II of Olduvai Gorge, and of similar age. Both show mesially tapering premolars, with small metaconids lying opposite the protoconids, and smaller foveae in front of these cusps than behind. The degree of wear on the molars is very different, but both show an oblique groove that runs between the hypoconulid and hypoconid to the base of the metaconid; and in both the hypoconid lies buccally and the M1s taper slightly distally, while the M2s are more broadly rounded at the rear. In the cranium and upper dentition, WT 15000 shows substantial similarities with the East Turkana cranium ER 1813 (Fig. 3). Although the latter boasts a substantially smaller intracranial volume of 510 ml, both specimens share a short, high cranial vault (rather like that of OH 13) with rounded brows that arc over each orbit and a frontal that rises behind a very short posttoral plane. In both the nasal apertures are tall, are relatively narrow, and taper strongly upward, while the nasoalveolar clivuses are long and slope forward. Even more telling are upper dental similarities among WT 15000, ER 1813, and OH 13. All have a high-crowned but flat-surfaced M1, with the mesiodistally long hypocone as high as the protocone, and separated from it by a lingual notch. In all, the M2s are basically similar to the MIs, but show reduction of the metacone and a smaller notch between the hypocone and protocone. In all, M1 and M2 both have thick postcingula. In WT 15000 and ER 1813, the P2s are very similar in having a bulbous and centrally placed paracone and a continuous crista running mesially from the paracone and swinging right around the side of the tooth. Further, although it has a very worn dentition, the recently described palate OH 62 seems to present an upper dental morphology similar to those of the three specimens just described. In sum, the evidence seems to be quite compelling for the existence of an upper dental morph, most spectacularly represented by the fairly complete individual WT 15000, that is found almost a thousand kilometers away at Olduvai as well as around Lake Turkana at Koobi Fora and Nariokotome. The available name for this morph, should anyone wish to designate it a species, is H. microcranous (Ferguson 1995). Other “African Homo erectus” specimens include the 1.4-myr-old OH 9 calvaria (Fig. 3: 967 ml) from Olduvai Gorge, but it does not compare any better to the material from eastern Asia than it does to the Turkana fossils, and though it has been compared to the purportedly H. erectus Daka cranium from Ethiopia (1.0 myr, 995 ml; Asfaw et al. 2002), resemblances between the two, other than in endocranial volume and its correlates, are not particularly striking (Schwartz and Tattersall 2005). In sum, there is considerable morphological diversity among African Homo of the 2.0- to 1.0-myr period; and this diversity does seem to be organized into a number of distinctive morphs. Some of these are represented by individual fossils such as OH 9 that are clear outliers in terms of other known material; others seem to be represented by multiple individuals and even at multiple sites. Definitive systematic organization of this variety will clearly have to await a more comprehensive fossil record, but it is already evident that we are not looking here at a chronological transformation series, even one that is represented by high diversity at all time points. Somewhere in all of this there is a systematic signal, and it is evident that the blanket appellation H. ergaster, while a useful device for distinguishing the African hominid radiation of this period from the Asian one, is an inadequate expedient for describing diversity in the African record. Some paleoanthropologists are beginning implicitly to recognize this, but apparently without wishing to abandon old paradigms. Thus Spoor et al. (2007) reported new fossils from East Turkana that they concluded were evidence for two contemporaneous lineages of Homo in the Turkana Page 10 of 18

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_53-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 5 The D 2600 mandible from Dmanisi. (a) Front view, (b) left lateral, and (c) occlusal (Photos courtesy of David Lordkipanidze)

Basin at around 1.5 million years ago. One of these was the calvaria KNM-ER 42700. Spoor and colleagues cited a handful of trivial features that they claimed allied this specimen with Homo erectus; but in reality it bears none of the classic hallmarks of that species such as the long, low, posteriorly sharply angled lateral profile, the shelflike and protruding supraorbital surfaces, and the ovoid posterior profile. Indeed, in these diagnostic features the Turkana specimen is the very antithesis of the Javan type specimen. In contrast, the partial maxilla KNM-ER 42703, though hardly comparable to the calvaria, was considered to represent another lineage and was allocated to the exceedingly poorly defined species Homo habilis. Whether or not that species assignment is appropriate, or even means anything at all, the allocation of ER 42700 to Homo erectus is extremely telling. For while Spoor and colleagues evidently accept diversity among 1.5-myr-old hominids at Turkana, the assignment of the calvaria to Homo erectus only makes any sense at all in the context of the notion that Homo erectus is the middle “grade” of a single comprehensive, worldwide, variable, and gradually evolving Homo lineage.

Europe It is now fairly widely accepted that most of the western European forms that have at one time or another been described as H. erectus (see above) are better allocated to H. heidelbergensis, a move that takes these fossils out of the scope of the current discussion. And while some still view the Italian Ceprano calvaria (ca. 800–900 kyr; 1,165 ml), recently designated the holotype of H. cepranensis by Mallegni et al. (2003), as a representative of H. erectus, nobody has claimed that

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_53-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 6 Five views of the D 2700 cranium from Dmanisi (From Vekua et al. (2002), supplemental web data; Photos courtesy of David Lordkipanidze)

it represents H. ergaster. Indeed, Mounier et al. (2011) have suggested that it is a primitive Homo heidelbergensis. To the east, however, in the Caucasus at the Georgian site of Dmanisi (1.8 myr), there exists a very important and early hominid fossil assemblage with claimed African affinities (Figs. 3, 4, 5, 6, and 7). The first find, the mandible D 211 (Fig. 4) discovered in 1991, was assigned by its describers to “archaic African Homo erectus” (Gabunia and Vekua 1995). It was more generally attributed to H. erectus by Henke (1995) and also by Bra¨uer and Schultz (1996), although these latter authors remarked that, oddly, this early mandible showed “progressive” features seen in geologically younger H. erectus. These early differences in interpretation foreshadowed a fairly wild taxonomic ride. Gabunia et al. (2000) reported the discovery of two crania (D 2280 and 2282; Fig. 3) close to the original site; they considered these comparable in size and morphology to Koobi Fora H. ergaster, although cranial volumes were somewhat smaller: 780 and 650 ml, respectively. With the discovery in September 2000 of a very large and long mandible with highly worn teeth (D 2600; Fig. 5), the picture changed again. This mandible presented a marked contrast to D 211, but

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_53-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 7 The edentulous D 3444 cranium from Dmanisi. Lower left: mandible D 3900. Lower right: CT-based superimpositions by C. Zollikofer and M. Ponce de Leon of the Dmanisi skull D 3444/D 3900 on the D 2700/D 2735 and D 2282/D 211 specimens, to show contrasting silhouettes (From Lordkipanidze et al. (2005). Photos courtesy of David Lordkipanidze. Scale: 10 cm)

the Dmanisi team nonetheless concluded that all of the specimens belonged to a single highly sexually dimorphic species which they named H. georgicus, with D 2600 as its holotype (Gabounia et al. 2002). The gracile specimens D 211, D 2280, and D 2282 were considered to be female; and the robust D 2600 lower jaw was viewed as a male representative of this species. The group concluded that H. georgicus “preserves several affinities with Homo habilis and Homo rudolfensis . . . foretelling the emergence of Homo ergaster” (Gabounia et al. 2002, p. 245). But things did not stop there. Almost simultaneously, the team announced the discovery of an associated cranium and mandible, D 2700/D 2735 (Vekua et al. 2002; Fig. 6). Strikingly different from the crania discovered earlier, though also notably small-brained (600 ml), this excellently preserved specimen was said by its describers to bear resemblances to penecontemporaneous East African fossils. Page 13 of 18

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Abandoning the species H. georgicus, as well as the notion of H. ergaster as a separate entity, the Dmanisi team allocated D 2700/D 2735, and the rest of the hominid assemblage along with it, to H. erectus, while noting that they “are among the most primitive individuals so far attributed” to that expanded species (Vekua et al. 2002, p. 88). During the 2002/2004 field seasons yet another associated cranium and mandible (D 3444/D 3900) were recovered at Dmanisi. The most remarkable aspect of this aged presumed male (Fig. 7) is that he had possessed just a single tooth at death and had evidently been largely edentulous for many years (Lordkipanidze et al. 2005). Although at least one recent chimpanzee is known to have survived a long time in an edentulous state, the Dmanisi team surmised that the individual must have “survived for a lengthy period without consuming foods that required heavy chewing . . . and/ or by virtue of help from other individuals” (Lordkipanidze et al. 2005, p. 718), and suggested that this had significant implications for early hominid social structure. They also noted that the cranium had been found in close proximity to Mode 1 stone artifacts and to cut-marked animal bones. The authors refrained from commenting on the systematic implications of the new find; but in a review published soon afterward, Rightmire et al. (2006) reaffirmed their belief that the Dmanisi assemblage as a whole was a single “paleodeme” best placed within H. erectus (which to them subsumed H. ergaster), despite resemblances to H. habilis in brain volume and in some aspects of craniofacial morphology. Yet while they (Rightmire et al. 2006, p. 140) noted that, if the large D 2600 mandible could be accommodated within the rest of the Dmanisi hominid population, then “the appropriate nomen is H. erectus georgicus,” they also pointed out that should the separate species status advocated by Gabounia et al. (2002) for the large jaw be “verified by new discoveries, then a subspecies other than H. erectus georgicus will have to be selected [for the remainder of the sample].” The hoped-for new discovery, of the cranium matching the D 2600 jaw, was duly made at Dmanisi in 2005. Following a long agony of indecision, this complete and beautifully preserved specimen (D 4500) was finally published in 2013 (Lordkipanidze et al. 2013). The delay is quite understandable, for this fossil is quite unlike anything ever seen before. As one would have predicted from the large teeth and long tooth rows of the mandible, the new cranium possesses a large and highly prognathic face, which is hafted on to a remarkably small braincase with a volume of fractionally less than 550 ml. But while these attributes generally recall those of australopiths, Lordkipanidze and colleagues probably wisely refrained from associating their new specimen with any previously known early hominid taxon. Instead, they crammed it into Homo erectus, an assignment for which there is less than scant morphological justification. Declaring that the extraordinarily distinctive morphology of D 4500 “reflects variation between demes of a single evolving lineage” (Lordkipanidze et al. 2013, p. 330), the group concluded that “specimens previously attributed to H. ergaster are thus sensibly classified as a chronosubspecies, H. erectus ergaster” (Lordkipanidze et al. 2013, p. 330). And finally they took the astonishing step of reducing the entire Dmanisi hominid sample to the previously unknown status of a sub-subspecies, Homo ergaster erectus georgicus. If there is any substance whatever to this convoluted taxonomic judgment, systematists everywhere should be in mourning, because it effectively deprives morphology of any utility in systematics – and where are we left to go from there? In any event, the contorted taxonomic journey of the Dmanisi hominids reflects the unusual morphologies that make it hard to fit them into established categories. And this journey is certainly not yet at an end. Even before the initial discovery of D 4500, Schwartz and Tattersall (2005) had already noted that the morphological heterogeneity in the Dmanisi assemblage made it difficult to recognize a single consistent morph at the site, irrespective of what this might have implied about species status. What is more, the lead geologist at Dmanisi, Reid Ferring (personal Page 14 of 18

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communication), reports that accumulation of the Dmanisi hominids might have taken place over the span of as much as a few hundred years. And if this is the case, there is no compelling reason (as there might be in the case of a catastrophic assemblage) to believe that only one hominid species is necessarily implicated in the fossil assemblage. Additionally, Schwartz and Tattersall observed that none of the Dmanisi material appeared to bear very close, i.e., systematically suggestive, resemblances either to any Asian fossils that had been described as H. erectus or to any African specimens allocated to H. erectus or to H. ergaster. Exactly how much systematic variety there is in this assemblage clearly awaits more study; but although the Dmanisi hominids most plausibly represent one or possibly more early departures from Africa hard on the heels of the origin of Homo, it is hard at present to point to craniodental morphologies that specifically unite them with any latest Pliocene or earliest Pleistocene African hominids yet known. It is unknown with any certainty exactly what it was that allowed hominids to spread, for (presumably) the first time, out of the ancestral continent of Africa as far as Dmanisi. But since the Mode 1 stone tool assemblage at Dmanisi is remarkably primitive, and the brains of the hominid (s) there remained small, it seems most likely that the factor responsible was the acquisition of striding bipedality. As exemplified by WT 15000, this locomotor style was already present in Homo ergaster; and a partial postcranial skeleton from Dmanisi (putatively associated with the D 2700/D 2735) and postcranial bones from three other individuals are said to show “modernhuman-like body proportions” (Lordkipanidze et al. 2007, p. 305). Still, the scientists who described these elements also noted a “surprising mosaic of primitive and derived features” (Lordkipanidze et al. 2007, p. 305); and it is clear that the last word on the Dmanisi postcranials – and indeed, on the assemblage as a whole – has yet to be written.

Conclusions Homo ergaster is the designation of choice for the growing number of paleoanthropologists who believe that the fossils previously allocated to “African Homo erectus” are sufficiently different from the Asian type material of H. erectus to warrant assignment to a distinct species. Adoption of this nomenclature is a considerable improvement on our older understanding, certainly to the extent that it emphasizes that the Trinil fossil and others like it are quite highly autapomorphic and that Javan or at least eastern Asian H. erectus is thus most appropriately viewed as an indigenous and terminal regional species (or maybe even clade), rather than as an Old World-wide stage or grade in hominid evolution. Nonetheless, it remains true that to call the entire African rump of this Old World “Homo erectus grade” H. ergaster, is to brush a huge diversity of morphologies under the rug of one single species. Close examination of the morphologies displayed by the diversity of fossils that have at one time or another been referred to as “African Homo erectus” makes it evident that, while it is likely that all may be legitimately regarded as members of a single hominid clade, there is some diversity within it. The KNM-ER 992 holotype mandible of H. ergaster appears to be matched morphologically by the OH 22 mandible from Olduvai as well as by another mandible (ER 3734) from Koobi Fora. But there seems to be no compelling reason to match these lower jaws with any of the cranial materials available, and certainly none to associate them with the iconic KNM-WT 15000 skeleton, the lower dentition of which is distinctly different in a whole host of characteristics. Clearly, there is a need for a detailed systematic reappraisal of the entire “African Homo erectus” ¼ Homo ergaster group. Meanwhile, the recognition of a distinct H. ergaster clade at least serves to highlight the fact that the complexity of the hominid evolutionary story throughout the Old World in the Early–Middle Page 15 of 18

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Pleistocene was far greater than is implied by the inclusion of the entire group of fossils involved within the single hugely variable species H. erectus.

References Asfaw B, Gilbert WH, Bayene Y, Hart WK, Renne PR, WoldeGabriel G, Vrba ES, White TD (2002) Nature; 416:317–20. Boule M. L’homme fossile de la Chapelle-aux-Saints. Ann Pale´ontol. 1911–1913;6:1–64, 7:65–208, 8:209–79. Bra¨uer G, Schultz M (1996) The morphological affinities of the Plio-Pleistocene mandible from Dmanisi, Georgia. J Hum Evol 30:445–481 Cunningham D (1895) The place of “Pithecanthropus” on the genealogical tree. Nature 53:269 Ferguson WW (1995) A new species of the genus Homo (Primates: Hominidae) from the PlioPleistocene of Koobi Fora, in Kenya. Primates 36:69–89 Gabounia L, de Lumley M-A, Vekua A, Lordkipanidze D, de Lumley H (2002) De´couverte d’un nouvel hominide´ a` Dmanissi (Transcaucasie, Ge´orgie). C R Paleovol 1:243–253 Gabunia L, Vekua A (1995) A Plio-Pleistocene hominid from Dmanisi, East Georgia, Caucasus. Nature 373:509–512 Gabunia L, Vekua A, Lordkipanidze D, Swisher CC, Ferring R, Justus A, Nioradze M, Tvalcrelidze M, Anton S, Bosinski GC, Jo¨ris O, de Lumley MA, Majsuradze G, Mouskhelishvili A (2000) Earliest Pleistocene hominid cranial remains from Dmanisi, Republic of Georgia: taxonomy, geological setting and age. Science 288:1019–1025 Groves CP, Mazak V (1975) An approach to the taxonomy of the Hominidae: Gracile Villafranchian hominids of Africa. Cas Miner Geol 20:225–247 Henke W (1995) Qualitative and quantitative analysis of the Dmanisi mandible. In: Radlanski RJ, Renz H (eds) Proceedings of the 10th international symposium on dental morphology. Christine und Michael Br€ unae GbA, Berlin, pp 459–464 Holloway RL, Broadfield DC, Yuan MS (2004) The human fossil record. Vol. 3: brain endocasts, the paleoneurological evidence. Wiley-Liss, New York Leakey R (1972) Further evidence of lower Pleistocene hominids from East Rudolf, North Kenya. Nature 237:264–269 Leakey R, Walker A (1976) Australopithecus, Homo erectus and the single species hypothesis. Nature 261:572–574 Lordkipanidze D, Vekua A, Ferring R, Rightmire GP, Agusti J, Kiladze G, Mouskhelishvili A, Ponce de Leon M, Tappen M, Zollikofer CPE (2005) The earliest toothless hominin skull. Nature 434:717–718 Lordkipanidze D, Jashashvii T, Vekua A, Ponce de Leon M, Zollikofer CPE, Rightmire GP, Pontzer H, Ferring R, Oms O, Tappen M, Bukhsianidze M, Agusti J, Kahlke R, Kiladze G, Martinez-Navarro B, Mouskhelishvili A, Nioradze M, Rook R (2007) Postcranial evidence of early Homo from Dmanisi, Georgia. Nature 449:305–310 Lordkipanidze D, Ponce de Leon M, Margvelashvili A, Rak Y, Rightmire GP, Vekua A, Zollikofer CPE (2013) A complete skull from Dmanisi, Georgia, and evolutionary biology of early Homo. Science 342:326–331 L€u Z, The Tangshan Archaeological Team (1996) Locality of the Nanjing man fossils. Cultural Relics Publishing House, Beijing

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Mallegni F, Carnieri I, Bisconti M, Tartarelli G, Ricci S, Bidittu I, Segre AG (2003) Homo cepranensis sp. nov. and the evolution of African-European Middle Pleistocene hominids. C R Pale´ovol 2:153–159 Mayr E (1950) Taxonomic categories in fossil hominids. Cold Spring Harb Symp Quant Biol 15:109–118 Mounier A, Condemis S, Manzi G (2011) The stem species of our species: A place for the aschaic human cranium from ceprano, Italy. PLoSOne 6(4):e18821 Rightmire GP (1990) The evolution of Homo erectus: comparative anatomical studies of an extinct human species. Cambridge University Press, Cambridge Rightmire GP, Lordkipanidze D, Vekua A (2006) Anatomical descriptions, comparative studies and evolutionary significance of the hominin skulls from Dmanisi, Republic of Georgia. J Hum Evol 50:115–141 Schwalbe G (1899) Studien € uber Pithecanthropus erectus Dubois. Morphol Anthropol 1:16–228 Schwartz JH, Tattersall I (2000) What constitutes Homo erectus? Acta Anthropol Sin 19(Suppl):18–22 Schwartz JH, Tattersall I (2003) The human fossil record. Vol. 2: craniodental morphology of genus Homo, Africa and Asia. Wiley-Liss, New York Schwartz JH, Tattersall I (2005) The human fossil record. Vol. 4: craniodental morphology of early hominids (genera Australopithecus, Paranthropus, Orrorin) and overview. Wiley-Liss, New York Spoor F, Leakey MG, Gathogo PN, Brown FH, McDougall I, Kiarie C, Manthi KF, Leakey LN (2007) Implications of new early Homo fossils from Ileret, east of Lake Turkana, Kenya. Nature 448:688–691 Tattersall I (1986) Species recognition in human paleontology. J Hum Evol 15:165–175 Tattersall I (1992) Species concepts and species identification in human evolution. J Hum Evol 22:341–349 Tattersall I (1995) The fossil trail: how we know what we think we know about human evolution. Oxford University Press, New York Tattersall I (1998) Becoming human: evolution and human uniqueness. Harcourt Brace, New York Tattersall I (2008) The fossil trail: how we know what we think we know about human evolution, 2nd edn. Oxford University Press, New York Tattersall I, Schwartz JH (2009) Evolution of the genus Homo. Ann Revs Earth Planet Sci 37:67–92 Theunissen B (1988) Eugene Dubois and the ape-man from Java: the history of the missing link and its discoverer. Kluwer, Dordrecht Vekua A, Lordkipanidze D, Rightmire GP, Agusti J, Ferring R, Majsuradze G, Mouskhelishvili A, Noradze M, Ponce de Leon M, Tappen M, Tvalchrelidze M, Zollikofer C (2002) A new skull of early Homo from Dmanisi, Georgia. Science 297:85–89 Walker A, Leakey R (1978) The hominids of East Turkana. Sci Am 239(2):44–56 Walker A, Leakey R (1993) The Nariokotome Homo erectus skeleton. Harvard University Press, Cambridge

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Index Terms: Homo ergaster_3–5, 8, 11 Homo ergaster African_8 Homo ergaster Asian_5 Homo ergaster cranial morphologies_4 Homo ergaster European_11 Homo ergaster existence_3

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Later Middle Pleistocene Homo G. Philip Rightmire* Department of Human Evolutionary Biology, Harvard University, Peabody Museum, Cambridge, MA, USA

Abstract Hominin fossils are known from Middle Pleistocene localities in Africa, Europe, South Asia, and the Far East. It is recognized that these individuals display traits that are derived in comparison to the condition in H. erectus. However, the skulls retain numerous primitive features that set them apart from modern humans. Faces are massively built with strong supraorbital tori, frontals are flattened, and vaults remain low with less parietal expansion than in H. sapiens. The hominins from Bodo, Broken Hill, and Elandsfontein in Africa are quite similar to their Middle Pleistocene contemporaries in Europe. Crania and jaws from Arago Cave and Petralona, and the spectacular assemblage from Sima de los Huesos, are particularly informative. In sum, this evidence suggests a speciation event in which H. erectus gave rise to a daughter lineage. At or before the beginning of the Middle Pleistocene, new populations spread through Africa and western Eurasia and perhaps also to the Far East. How the fossils should be treated taxonomically is currently uncertain. One view emphasizes gradual anagenetic change, while others advocate speciation occurring repeatedly throughout the Pleistocene. In the perspective favored here, differences between the Middle Pleistocene hominins can be attributed to geography, time, or intragroup variation. Many, if not all, of the European and African specimens can be accommodated in one species distinct from Neanderthals and modern humans. If the Mauer mandible is included in this hypodigm, then the appropriate name is H. heidelbergensis. This species is probably ancestral to both the Neanderthals in Europe and the earliest representatives of H. sapiens in Africa.

Introduction Humans evolved in Africa and were confined to that continent for much of their early history. The first dispersals from Africa into Eurasia occurred near 2 million years ago (Ma). These migrants were probably representatives of Homo erectus (sometimes called Homo ergaster). Traces left by these hominins have been recovered from the site of ‘Ubeidiya in the central Jordan Valley and at Dmanisi in the Georgian Caucasus. Some early occupations were likely transitory and did not result in permanent settlements. However, groups of H. erectus were able to travel relatively quickly across southern Asia to the Far East, where they were established both in Java and in China by 1.7–1.6 Ma. The first penetration westward into Europe apparently came much later. There are indications that humans were moving into the Mediterranean region prior to 1 Ma, but the initial populating of Europe north of the major mountain barriers is documented only after about

*Email: [email protected] Page 1 of 20

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Fig. 1 Map giving the locations of Middle Pleistocene localities where important hominin fossils have been discovered

700 thousand years ago (Ka). The biological identity of the first Europeans is unclear, but it is agreed that these hominins differ from H. erectus. Many of the ancient fossils are presently assigned to the species H. heidelbergensis (named originally from a mandible found near Heidelberg in Germany). Homo heidelbergensis or perhaps other closely related species are known also from Middle Pleistocene localities in Asia and Africa (Fig. 1). These people seem to have been more advanced in behavior than their predecessors, and there is evidence that H. heidelbergensis was able to make relatively sophisticated stone tools, hunt larger and more dangerous game animals, and perhaps engage in cooperative social activities.

The Middle Pleistocene of Africa In Africa, fossils from the early Middle Pleistocene are clearly different from H. erectus in cranial capacity (approximately equal to brain size), width of the frontal bone, proportions of the occipital region, and anatomy of the underside of the skull. Where it is preserved, the face is still heavily constructed, but the brows, nasal profile, and bony palate more closely resemble the condition seen in later humans. In many instances, the hominins are found with stone tools that are more carefully shaped than the choppers and relatively crude hand axes associated with H. erectus. From Bodo in Ethiopia to Elandsfontein in South Africa, a shift toward the manufacture of thinner, more finely flaked bifacial tools is documented in the Middle Pleistocene, and it is reasonable to link this change in behavior to a speciation event in which H. erectus gave rise to a daughter lineage exhibiting increased relative brain size (encephalization).

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Fig. 2 Facial and oblique views of the cranium from Bodo, Ethiopia. The projecting glabellar region, wide interorbital pillar, and massive zygomatic (cheek) bones give the face an archaic appearance similar to that of H. erectus. Other traits including the vertical border of the nasal aperture are interpreted as apomorphies shared with later humans

Bodo One important specimen came to light in 1976 at Bodo, in the Middle Awash region of Ethiopia (Fig. 1). The Bodo cranium and later a broken parietal from a second individual were found in conglomerates and sands containing mammalian bones and Acheulean tools (Kalb et al. 1980; Clark and Schick 2000; Gilbert et al. 2000). Fauna from the Bodo site has been compared to that from Bed IV at Olduvai Gorge and Olorgesailie in Kenya, and an early Middle Pleistocene date is indicated. 40Ar/39Ar measurements reported by Clark et al. (1994) support this biochronology, and the evidence points to an age of about 600 Ka for the Bodo hominins. The face and the anterior part of the Bodo braincase are preserved (Fig. 2). There are some cut marks on the facial bones, and these indicate intentional postmortem defleshing, as documented by White (1986). It can be established that Bodo is like H. erectus in some features. The massive facial bones, projecting brow, low frontal with midline keeling, parietal angular torus, and thick vault give the specimen a pronounced archaic appearance. In other respects, the cranium is more specialized (derived) in its morphology. Brain size is close to 1,250 cm3 and is thus substantially greater than expected for H. erectus. Frontal bone proportions, the high-arched shape of the squamous temporal, and some traits of the cranial base are like those of more modern humans. Although the face is very broad and heavily constructed, the supraorbital tori are divided into medial and lateral segments, the margin of the nose is vertical rather than forward sloping, and the incisive canal opens into the front of the hard palate (Rightmire 1996). These are derived (apomorphic) conditions present in the face of recent Homo.

Broken Hill and Elandsfontein Another African specimen is the cranium from Broken Hill (now Kabwe) in Zambia, discovered by miners in 1921. Quarrying for lead and zinc ore had already removed most of a small hill, when the miners broke into the lower part of an extensive cavern. Published reports do not all agree on this point, but apparently the cranium was picked up by itself, not in clear association with other hominin remains. The fossil is in remarkably good condition. The face is massive, with some of the heaviest brows on record. The frontal is flattened with slight midline keeling, and the vault is low in profile. Shortly after it was found, the fossil was attributed to the (new) species H. rhodesiensis (Woodward 1921). In its overall morphology, however, Broken Hill resembles H. erectus, and Page 3 of 20

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indeed, it has been classified this way on more than one occasion. At the same time, there are apomorphic features shared with later humans. The temporal squama is high and arch shaped, and the upper scale of the occipital is expanded relative to its lower nuchal portion (where the neck muscles are attached). Several discrete characters of the temporomandibular joint region are specialized. These include a raised articular tubercle and a sphenoid spine. More changes are apparent in the face, where the lateral border of the nasal aperture is set vertically, and the palatal anatomy is like that of later people (Rightmire 2001). Another cranium quite similar to that from Broken Hill comes from the farm Elandsfontein, near Saldanha Bay on the Atlantic coast of South Africa. At Elandsfontein, there is an expanse of sandveld that has long been a focus of attention for paleontologists. Dunes migrate across this area, and in between the dunes, there are swales resulting from deflation. Whether the ancient horizons exposed in these “bays” are stratified land surfaces or simply mark the (seasonal) fluctuations of the water table is unclear. Given either of these interpretations, it is evident that during the mid-Quaternary, the region supported wetlands and water holes, with plenty of grass (Deacon 1998). Animals, many of them bovids or other large herbivores, were attracted to the water. The fauna includes numerous archaic elements such as a dirk-toothed cat, a sivathere, and a giant buffalo. Altogether, some 15 of 48 mammalian species collected at the site have no historic descendants. Comparisons conducted by Klein and Cruz-Uribe (1991) imply that the bones were accumulated between 700 and 400 Ka, but more recent sorting of the fauna suggests an older interval, between 1 Ma and 600 Ka (Klein et al. 2006). Much of the work at Elandsfontein has been surface prospecting, and it was during one such visit in 1953 that investigators picked up pieces of a human skullcap. The reconstructed Elandsfontein cranium is composed of the frontal and parietal walls and some of the occiput. The bones are cracked and heavily weathered, but the braincase is not distorted. There are some similarities to H. erectus, but certainly the better match is with Broken Hill. These two Middle Pleistocene specimens are alike not only in overall proportions but also in many anatomical details. The Elandsfontein brow is almost as thick as that of Broken Hill, and the frontal contours are the same. Radiographs show that the frontal sinus is large and complex, reaching well up into the squama in both cases (Seidler et al. 1997; Rightmire unpublished observations). The South African frontal bone gives a breadth index of 91.9 and is thus slightly less constricted than that of Broken Hill, for which the ratio of least width to greatest breadth is 83.0. Sagittal and coronal measurements of the parietal are similar in the two individuals as is the length and orientation of the upper scale of the occipital. Unfortunately, the Elandsfontein base is missing, and there is no face. These are just the regions where one would expect to find additional apomorphies setting the South African hominin apart from H. erectus.

Lake Ndutu A fourth Middle Pleistocene specimen is known from Lake Ndutu. This seasonal soda lake is located at the western end of the Main Gorge at Olduvai, in northern Tanzania. Excavations conducted near the lake margin in 1973 produced an encrusted human cranium, along with other fossils and numerous artifacts (Mturi 1976). Initially, the stone assemblage included mostly spheroids, cores, and flakes, but hand axes were picked up during later visits to the site. All of this material is thought to be derived from archaeological horizons in a greenish sandy clay, tentatively correlated with the upper Masek Beds at Olduvai. When it was found, the cranium was severely damaged and encased in a clay matrix. The process of cleaning and reconstructing the fossil has been described by Clarke (1990). These efforts were generally successful, but the face is quite incomplete, as is the frontal bone. There are gaps in the Page 4 of 20

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_55-5 # Springer-Verlag Berlin Heidelberg 2013

parietals as well. The braincase is relatively small, with a capacity of only about 1,100 cm3. Just a fragment of the supraorbital region is preserved, and the torus is projecting, if not especially thickened. Bossing of the parietals is emphasized in Clarke’s reconstruction. This has perhaps been overdone with plaster, but the walls of the vault appear to be more convex than would be the case for H. erectus. Also, the upper plane of the occiput is vertical, above the moundlike transverse torus. The morphology of this torus is in keeping with other characters suggesting that Ndutu could be female, in comparison to males such as Bodo or Broken Hill.

Florisbad Several additional fossils are more fragmentary and therefore somewhat less informative. An example is the cranium from spring deposits at Florisbad in South Africa, consisting only of facial parts, the frontal bone, and pieces of the parietals. Early studies compared the hominin to recent populations, but it is important to emphasize that Florisbad is far from modern in its morphology. Glabella (in the midline above the nasal root) is projecting, as is the brow on either side. The facial bones as repositioned by Clarke (1985) suggest that the nasal cavity is large and the cheek is flattened, without obvious infraorbital hollowing. The face is less heavily constructed than that of Broken Hill but otherwise not dissimilar. A human upper molar tooth from Florisbad has been dated by ESR to 259 Ka (Gr€ un et al. 1996).

The Omo Localities and Herto Several sites in the Omo region of southern Ethiopia, explored initially in 1967, have recently been revisited. Human remains are known from Member I of the Kibish Formation, now considered to be 200–100 Ka in age (Assefa et al. 2000). Omo 2 is an isolated surface find from PHS, lacking archaeological associations. This partial cranium is low in contour and decidedly massive in its construction, with a blunt frontal keel and a strongly angled occiput. Other likely primitive features include the shape of the deep mandibular cavity lacking any distinct articular tubercle and the absence of a sphenoid spine. Nevertheless, the vault is large overall. The frontal bone is broad and relatively unconstricted, and the parietal walls show some outward curvature (limited to the regions below the temporal lines). The supraorbital torus is extensively damaged, and none of the face is preserved. Omo 1 was excavated at the KHS site, dated to 195 Ka (McDougall et al. 2005), from which there is now a large collection of Middle Stone Age artifacts. This individual is represented by only small portions of a skull, but much more of the postcranial skeleton is present. The cranium as reconstructed by several workers is globular in form, with expanded parietals and an occipital that is more rounded than that of Omo 2. To the limited extent that these can be checked, cranial superstructures (crests and tori) are not strongly expressed. The anterior part of the mandible shows clear signs of chin formation. Given these important markers of modern morphology, there is general agreement that Omo 1 should be regarded as early H. sapiens. An important question, still not firmly resolved, is whether the Omo 1 skeleton can be grouped with the more archaic Omo 2 remains or whether these individuals should be placed in separate populations. The morphological differences between the two crania are very substantial. Indeed Omo 2 has been compared to specimens such as Broken Hill or Elandsfontein, even though the frontal is rather less narrowed behind the orbits. If the Omo fossils are approximately the same age, then there are two possibilities. Omo 2 may be a remarkably robust individual, within a highly variable but essentially modern population. Alternatively, this specimen can be regarded as representative of an archaic, late-surviving lineage, present alongside anatomically modern humans. However, if Omo 2, picked up on the surface, is actually older than implied by recent Page 5 of 20

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_55-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 3 Lateral and facial views of the cranium from Petralona, Greece. This European hominin resembles Middle Pleistocene specimens from Africa. The Petralona and Broken Hill individuals are especially similar in measurements relating to facial proportions and vault shape

dating for the PHS site, then it is easier to argue that the cranium is sampled from an earlier portion of the lineage ancestral to H. sapiens. Specimens from Herto in the Middle Awash region confirm the presence of H. sapiens in northeastern Africa late in the Middle Pleistocene. Three fossilized crania recovered in 1997 show cut marks associated with postmortem defleshing and are associated with a stone tool assemblage that can be characterized as late Acheulean or Middle Stone Age. The bones and artifacts are dated radioisotopically to between 160 and 154 Ka (Clark et al. 2003). One of the adult crania (BOU-VP-16/1) is intact, with a brain size estimated as 1,450 cm3 (White et al. 2003). This individual is ruggedly built, with a very prominent, bilaterally arched glabella, a long vault, and a distinctly flexed occipital. The parietal walls are convex rather than inward sloping, and the index of neurocranial globularity (Lieberman et al. 2002) calculated as ca. 0.54 for BOU-VP-16/1 is high enough to be within the range expected for anatomically modern humans. A second adult cranium is less complete, and there is a child estimated as 6–7 years in age. As a group, the Herto individuals are very robust but display morphologies that place them close to recent populations. White et al. (2003) have referred the fossils to a new subspecies of H. sapiens.

Middle Pleistocene Hominins from Europe Skulls very similar to those from Africa have been found in western Eurasia. Several of the principal localities lie close to the Mediterranean Sea, but it is apparent that humans were also able to reach Britain and central Europe, relatively early in the Middle Pleistocene (Fig. 1).

The Cranium from Petralona Petralona lies near the city of Thessaloniki in northern Greece. The exact provenience of the hominin fossil found within cave deposits containing the bones of numerous extinct animals is uncertain, but the Middle Pleistocene antiquity of this material is not in doubt. The cranium itself is exceptionally well preserved (Fig. 3) and would have enclosed a brain close to 1,230 cm3 in volume Page 6 of 20

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_55-5 # Springer-Verlag Berlin Heidelberg 2013

(Stringer et al. 1979). Supraorbital tori are about as massive and projecting as in Broken Hill, while CT scans show that the frontal sinuses are greatly expanded. These air cavities extend posteriorly toward bregma and also laterally, where they are separated from the sphenoid sinuses only by thin bony partitions (Seidler et al. 1997). The frontal bone itself is relatively shorter and broader than in Broken Hill. The ratio of least to greatest frontal breadths is 91.6; postorbital constriction is thus less pronounced than in Broken Hill but comparable to that estimated for the Elandsfontein specimen. Petralona also differs from Broken Hill in having a wider cranial base and a less prominent torus crossing the occipital bone. However, the two hominins are alike in many other aspects of vault shape, in orientation of the infraorbital region, and in several measures of facial projection (Rightmire 1998, 2001; Friess 2010; Harvati et al. 2010, 2011).

Arago Cave Much the same conclusion applies to the less complete cranium from Arago Cave in France dated to about 450 Ka. The partial cranium numbered Arago 21 has a face that is largely intact but damaged as a result of its long interment in compacted cave sediments. The frontal bone, interorbital pillar, nose, and cheeks show numerous cracks, and areas of localized crushing are present. The discoverers have been able to correct some of this damage in a reconstruction, but significant distortion remains. Nevertheless, it is evident that Arago 21 is somewhat smaller than Petralona or Broken Hill in brow thickness, upper facial width, and facial length. Height of the bony orbit and the subnasal part of the maxilla are especially reduced, and the nasal saddle seems to be less elevated relative to the orbital margins. Apart from these differences, Arago 21 is similar in its proportions to the Broken Hill cranium from Africa (Rightmire 2001). Some workers discern resemblances to Neanderthals. Hublin (1996) and Arsuaga et al. (1997) note that the infraorbital surface of the Arago 21 maxilla is flattened and the cheek bones are obliquely oriented, as in Neanderthals. Also, there is forward protrusion of the face at subspinale (in the midline, just below the nasal opening), and the nasal aperture is bounded inferiorly by a sharp rim. These observations must be tempered by the fact that cracking and plastic deformation make it difficult to assess key aspects of morphology. The wall of the Arago 21 maxilla is generally flattened or even inflated in the manner characteristic of Neanderthals, but the cheek is slightly hollowed laterally, below the orbit. This feature cannot be due entirely to damage. Also, it is not clear that the zygomatic bone is swept back (obliquely oriented) so noticeably as in later European populations. In facial forwardness at subspinale [as measured by the zygomaxillary angle of Howells (1973)], Arago 21 at 113 is in the Neanderthal range, and Petralona at 118 shows almost as much protrusion. But the value for Broken Hill is only 116 , so a low zygomaxillary angle does not align Arago 21 and Petralona with Neanderthals rather than with other Middle Pleistocene specimens. The sharp inferior margin of the Arago nose is indeed reminiscent of that in Neanderthals. However, there is variation in this feature. Petralona is rather less like the Neanderthals, while some later Europeans including the Sima hominins (Section “Sima de los Huesos, Atapuerca”) have a pattern of cresting on the nasal floor resembling that in Broken Hill or Bodo. In addition to the partial cranium, the cave at Arago has yielded several mandibles, of which two have been described. Arago 2 is the more complete, missing only the angle and ascending portion from the left side. This specimen has sustained damage anteriorly, where the symphysis and left corpus are cracked. Arago 13 is a large hemimandible (right side), in relatively good condition. Both specimens present a mix of archaic and more modern characters. Development of the lateral prominences, marginal tori and tubercles, and internal symphyseal buttresses is comparable to that observed in H. erectus, although the alveolar planum is steeper and less shelflike in the Arago individuals. Arago 2 displays definite incurving of the symphyseal face below the alveolar border. Page 7 of 20

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_55-5 # Springer-Verlag Berlin Heidelberg 2013

Here, the elements of a mental trigone are present, while in Arago 13, signs of “chin” formation are less clear. Both jaws have retromolar fossae. However, in Arago 13, this fossa is restricted, and the crown of M3 is partly obscured by the leading edge of the ramus when the specimen is viewed from the side. The Arago mandibles are important not only because they reveal information about a Middle Pleistocene hominin population but also because they can be compared to the jaw from Mauer, near Heidelberg in Germany. Assigned a radiometric age of 609 Ka (Wagner et al. 2010), the Mauer fossil is likely to be one of the oldest recovered in Europe. It has often been described as primitive, with a massive body and very thick symphysis lacking any mental eminence. At the same time, the broad ramus, increased symphyseal height, and moderate size of the teeth suggest a morphological pattern different from that of H. erectus. The mandible was referred to the (new) species H. heidelbergensis by Schoetensack (1908). As the Arago jaws resemble the Mauer specimen, it is possible to link the French assemblage with the same taxon. Similarities of the Arago 21 face to Petralona (or Broken Hill) in turn provide a formal basis for including other European (or African) individuals in H. heidelbergensis.

Sima de los Huesos, Atapuerca The species H. heidelbergensis is increasingly well documented by the spectacular finds from Atapuerca in northern Spain. Excavations in the Sima de los Huesos have produced hominin remains, representing virtually all parts of the skeleton, that their describers have attributed to H. heidelbergensis. In addition to skulls, there are many postcranial bones, and it is clear that at least some of the Sima (male) individuals were tall and robust (Arsuaga et al. 1999a). Somewhat surprisingly, sexual dimorphism is comparable to that expressed in recent populations. The cave also contains the bones of bears and a few other carnivores, but there are no herbivores that might represent food waste. With one exception, there are no stone artifacts. A single hand axe fashioned from red quartzite was discovered in 1998. Investigators working at the Sima have argued that the skeletons were deposited in this pit by other humans and that the unique hand axe documents symbolic behavior (Carbonell and Mosquera 2006). First application of U-series dating to a speleothem present in the lower part of the stratigraphic sequence suggested a date of >350 Ka (Bischoff et al. 2003). More recent sampling from the same speleothem points to an age for the fossils of ca. 530 Ka (Bischoff et al. 2007). Two of the Sima adults provide estimates for brain size. At close to 1,100 cm3, SH 5 is rather small, but SH 4 with a capacity of 1,390 cm3 is one of the largest of all Middle Pleistocene specimens. The crania are primitive in some respects, and the massive face of SH 5 is surmounted by a prominent browridge. Vault bones are thickened, and both sagittal keeling and an angular torus are variably developed. The braincase is broadest in the supramastoid region or just above the ear openings. As do their European and African contemporaries, the Sima hominins also exhibit derived traits in the face, shape of the squamous temporal, proportions of the occipital bone, and structure of the cranial base. An important question is the extent to which these people resemble the later Neanderthals of Europe. As described by Arsuaga et al. (1997), the midface of SH 5 seems to anticipate the distinctive morphology associated with Late Pleistocene Europeans. The infraorbital surface and the side wall of the nose meet at a shallow angle, so as to produce a slight concavity. The cheek region is thus not “inflated” in the extreme manner of Neanderthals, but it can be interpreted as intermediate in form. Also in the Sima sample, continuity of the supraorbital tori at glabella is said to be reminiscent of Neanderthals, and the broad nasal bones are set in a relatively horizontal orientation. At the rear of the cranium, the suprainiac area is large but not very depressed. This trait Page 8 of 20

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_55-5 # Springer-Verlag Berlin Heidelberg 2013

and the shape of the occipital torus may also foreshadow the Neanderthal condition. How these features are evaluated (whether any of them can be judged to be true Neanderthal apomorphies) will determine how the Sima hominins as well as Arago and Petralona are related to populations outside of Europe and how these regional paleodemes should be treated in phylogenetic schemes.

The TD6 Assemblage from Gran Dolina, Atapuerca Additional evidence bearing directly on the first peopling of Europe is accumulating from another site in the Atapuerca region. Excavations at Gran Dolina have uncovered stone core-choppers and flakes, animal bones, and human remains dating to the end of the Early Pleistocene. An age slightly in excess of 780 Ka for the TD6 level containing the fossils now seems to be established (Falgue`res et al. 1999). Cranial specimens include a juvenile face, an adult cheek bone, part of a subadult frontal with some of the brow, and a piece of the cranial base on which most of the joint cavity for the mandible is preserved. There are also broken lower jaws with teeth, along with vertebrae, ribs, and bones of the hand and foot. Arsuaga et al. (1999b) argue that the TD6 people are not H. erectus. Morphology of the hollowed cheek region, vertical orientation of the nasal aperture, features of the hard palate, form of the developing (but already substantially thickened) brow, a wide frontal, the shape of the temporal bone at the side of the vault, and the apparently modern mandibular joint all suggest that the Gran Dolina fossils are different from H. erectus and more like later humans. Also, there can be little doubt that this population is distinct from the later Neanderthals. The hollowed cheek (bearing a “canine fossa”) points toward this conclusion, and neither in the juvenile nor in the adult faces is there much sign of the specialized Neanderthal condition. One partial mandible is generalized in its morphology, while the teeth resemble those of European and African Middle Pleistocene hominins. Given this complex of traits, the Gran Dolina material may represent a new species. The name H. antecessor was proposed by Bermu´dez de Castro et al. (1997). However, the number of fossils is still quite small, and several of the craniodental remains are fragmentary and/or subadult. A fair question is whether there is presently enough evidence to separate the TD6 assemblage from other penecontemporary fossils already on record. In particular, it must be asked whether the Gran Dolina bones and teeth differ from those of other early Europeans such as Mauer, Arago, and the Sima de los Huesos. Much attention has been focused on the development of a “canine fossa” in the midface. Hollowing is indeed apparent in the cheek of the TD6 juvenile, but a fossa is less obvious in the TD6 adult. This feature is variable in its expression in other populations, and the significance of this pattern is unclear. In the mandible, teeth, and postcranial bones, there seem to be few traits that differentiate the Gran Dolina hominins from Europeans of the Middle Pleistocene.

South Asia and the Far East One South Asian locality deserving mention is the Narmada Valley in central India (Fig. 1). Part of a cranium was found there in 1982, embedded in a conglomerate containing animal bones and a scattering of Acheulean artifacts. Dates for this material are poorly constrained, but it is probably of Middle Pleistocene age (Sonakia and Biswas 1998). Unfortunately the skull is damaged and lacks most of the face. Narmada has been described by its finders as H. erectus, but it is better compared to H. heidelbergensis (Kennedy et al. 1991). In its overall morphology, the cranial vault is not very different from the African and European hominins already discussed. Early humans occupied China before 1.6 Ma (Zhu et al. 2004). This part of Asia has been a focus of research in paleoanthropology for quite a long time. Apart from the famous discoveries of Page 9 of 20

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_55-5 # Springer-Verlag Berlin Heidelberg 2013

H. erectus at Zhoukoudian, there are important sites dating to the later Middle Pleistocene. One is Dali and another is Jinniushan, both of them in northern China. The Dali cranium was found in river terrace deposits with stone flakes and fauna. The Jinniushan skeleton was recovered from cave fill containing animal bones but no artifacts. ESR and U-series dates obtained from animal teeth suggest ages of perhaps 300–200 Ka. Dali is much of a cranium, damaged on the right side and at the base. The alveolar process and palate have been crushed upward. The specimen is otherwise undistorted and carries a lot of information. It has most often been described as “archaic” H. sapiens, intermediate in form between H. erectus and recent humans. Indeed, there are similarities to erectus, and these include the heavy brow, a long low vault that is broad across the base, and the sharply angled occiput. The temporomandibular joint cavity is offset laterally, and the cranial bones are thickened. These traits are best described as primitive retentions. At the same time, Dali exhibits other advanced features that link it to later populations. There is not much postorbital constriction, and the parietal walls are vertical rather than inward sloping. Both the high temporal squama and the proportions of the occiput depart from the erectus condition. The face is particularly short and non-prognathic (Wu and Athreya 2013). The Jinniushan cranium has been reconstructed several times, and there are gaps in the face, the frontal region, and the base. The brow is somewhat less massive than in Dali, but there is an eminence behind bregma, and the occiput is flexed. In other respects, the specimen differs from H. erectus. Brain volume is close to 1,300 cm3. The border of the nasal aperture is vertical (rather than angled forward), and the nasal sill is crested. On the palate, the incisive canal opens anteriorly (just behind the incisor roots) as in recent humans. In many anatomical details, both Dali and Jinniushan are like other Middle Pleistocene hominins from Africa or Europe. Comparisons based on facial measurements show that the Chinese specimens resemble Broken Hill to about the same extent as does Arago 21 (Rightmire 2001). There are some differences relative to Broken Hill, particularly in upper facial height (reduced in Dali and Jinniushan) and flattening below the nose (more pronounced in Jinniushan). Also, the Dali cheek exhibits a “canine fossa.” This feature has been taken as a basis for regarding the Chinese fossil(s) as distinct from western populations, but in fact hollowing of the infraorbital surface can be documented for faces outside of the Far East. Finds from Gran Dolina suggest that this feature may appear in Europe at the beginning of the Middle Pleistocene (Section “The TD6 Assemblage from Gran Dolina, Atapuerca”). The recognition of such variation will make it harder to argue for isolation of the major Old World geographic provinces.

Brain Size, Encephalization, and Speciation Many of the Middle Pleistocene hominins have brains that are enlarged relative to those of H. erectus. For 10 of the more complete crania including Bodo, Broken Hill, Petralona, two of the Sima de los Huesos adults, Dali and Jinniushan, average capacity is 1,206 cm3. For 30 H. erectus individuals, the mean volume is only 973 cm3. This difference is substantial, and it can be determined that a number of the Middle Pleistocene specimens actually lie beyond the limits predicted for an average H. erectus of comparable antiquity. Apparently, the change in brain size is not simply a consequence of larger body mass (Rightmire 2004). Encephalization quotients (EQ) can also be obtained for a number of the specimens. This entails first estimating body mass from orbital height (following Aiello and Wood 1994) and then deriving EQ from the relationship of brain weight to body mass established for mammals by Martin (1981). Page 10 of 20

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_55-5 # Springer-Verlag Berlin Heidelberg 2013

Here, there are various complications. Apart from the error associated with any weight estimate, there is the fact that the regression equations of Aiello and Wood (1994) are based on several species. Because EQ is a function of body mass predicted for individuals using an interspecific equation, comparisons of the EQ values determined for fossils may be misleading (Smith 2002). In any event, six H. erectus crania from Africa and Asia are complete enough to supply the necessary measurements, and the average EQ is 3.61 (Rightmire 2004). This result is comparable to that reported by Ruff et al. (1997), who employ mean estimates of brain and postcranially based body masses to compute EQ values of 3.40 and 3.46 for temporally defined (Early Pleistocene to early Middle Pleistocene) assemblages. During the balance of the Middle Pleistocene, a rise in EQ is apparent. Bodo and Broken Hill remain within the range observed for erectus, but other individuals have higher values and the average for eight specimens is 5.26. The magnitude of this increase is greater than that determined by Ruff et al. (1997) for humans of mid-Quaternary age. These authors use unmatched brain and body weights (means for samples of disassociated crania and postcrania) as a basis for their EQ calculations, and this may account for some of the difference in results. Also, orbit height may tend to underestimate body mass in comparison to predictor variables drawn from the postcranial skeleton. Nevertheless, there is evidence for a shift in brain size at or just before the onset of the Middle Pleistocene. This increase in encephalization seems to be linked to an episode of speciation. It is generally assumed that the larger brain and accompanying changes to the vault and face distinguish H. heidelbergensis from H. erectus. Here, an important question must be raised. Differences in frontal proportions, the parietal arc, form of the temporal squama, and rounding of the occiput may be related to the expanding brain, as may the increase in cranial height. As a consequence, traits such as parietal length and occipital curvature are not independent, and it will be incorrect to claim that each of these measurements adds new information useful in phylogenetic analyses. If this is the case, it may not be reasonable to recognize one or more new species, primarily on the strength of an increase in cranial capacity. Examined critically, the morphological evidence may not justify the recognition of so many taxa within Homo (Lieberman and Bar-Yosef 2005). Correlation analysis provides information about the interactions of brain volume with vault form in Pleistocene Homo (Rightmire 2012, 2013). It can be determined that the expanding brain influences vertex height and probably also parietal sagittal length. However, brain size fails to influence vault breadth within either H. erectus or the Middle Pleistocene hominins. Instead, the cranial base has a major effect on variations in width. Endocranial volume is not associated with the frontal flattening that is so characteristic for H. erectus. In H. erectus, and in individuals such as Bodo and Petralona, the massive face seems to override the brain as a determinant of frontal form. Encephalization does not explain the occipital rounding that distinguishes Broken Hill, Omo 2, and the Sima crania. Evidently, apart from greater vertex height, few of the vault characters considered diagnostic for H. heidelbergensis can be attributed directly to changes in the brain. Traits that are independent can be used to document speciation.

Phylogenetic Hypotheses Discoveries of new fossils, reassessments of specimens found earlier, and advances in the application of dating techniques show that hominins differing from H. erectus appeared in southern Europe before 780 Ka and in Africa at about the same time. One reading of the record suggests that these European and African groups share a number of derived features of the cranial base and vault. Page 11 of 20

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_55-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 4 Alternative evolutionary trees showing the relationships among H. erectus, Middle Pleistocene hominins, Neanderthals, and modern humans. Bars depict the time range estimated for each species. Broken lines indicate likely links of ancestors with descendants. Hypothesis (a) shows H. heidelbergensis to be descended from H. erectus. This species must have dispersed widely across Africa and western Eurasia at the beginning of the Middle Pleistocene, and some populations may also have reached the Far East. Here H. heidelbergensis is depicted as the antecedent to both Neanderthals in Europe and recent humans all across the old World. In a different interpretation (b), H. antecessor is recognized as the direct descendant of H. erectus. In turn, H. antecessor evolved into European H. heidelbergensis, and this species gave rise (only) to the Neanderthals. African H. rhodesiensis is considered to be ancestral to H. sapiens

Other similarities to later humans are apparent in the facial skeleton (orientation of the nasal aperture, location of the palatal incisive canal) and perhaps the mandible (symphyseal height increased relative to the posterior corpus, incipient mental eminence). Postcranial bones known principally from the Sima de los Huesos in Spain suggest that the European hominins were heavily built, perhaps reflecting adaptation of body form to a temperate environment. In sum, the anatomical evidence can be interpreted as supporting a claim that all of the earlier Middle Pleistocene fossils belong to a single lineage (Fig. 4a). This species can be called H. heidelbergensis. Later in the Middle Pleistocene, some populations dispersed northward within Europe, where they were subject to long episodes of extreme cold. During glacial advances and retreats occurring over several hundred thousand years ago, these hominins continued to adapt to harsher (cold/dry) conditions and evolved the specialized craniofacial characters and body build of the Neanderthals. In this same interval of time, other representatives of H. heidelbergensis in Africa were becoming more like modern humans. Fossil finds from Irhoud in Morocco, the Omo in southern Ethiopia, Herto in the Middle Awash region, and Laetoli in Tanzania document this evolutionary progression toward H. sapiens. Alternatively, it can be argued that H. antecessor is the ancestor to all later humans (Fig. 4b). This species is considered to be descended from (African) H. erectus (Bermu´dez de Castro et al. 1997). Rather soon after its first appearance in Spain, H. antecessor must have given rise to H. heidelbergensis. In this scenario, the heidelbergensis lineage was confined exclusively to Europe, where its members gradually acquired the large nose, more projecting facial skeleton,

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and other morphology of the Neanderthals. This is the accretion hypothesis of Dean et al. (1998). Also, H. antecessor is presumed to have evolved an African offshoot, represented at localities such as Bodo, Broken Hill, and Elandsfontein. Although these Middle Pleistocene hominins are acknowledged as morphologically similar to (perhaps even capable of exchanging genes with) their European contemporaries, they are not assigned to H. heidelbergensis. Instead, the African fossils are lumped in a separate species, for which the nomen H. rhodesiensis is available. Whether this taxonomic view can be accepted will depend largely on the outcome of excavations that are continuing in the TD6 levels at Gran Dolina. It will be important to expand the sample of fossils documenting the earliest European settlers. Another question is whether the far eastern specimens can be accommodated within one of these systematic frameworks. The answer is a tentative yes, although the evidence is sparse. Dali and Jinniushan do share a number of apomorphic traits with the western hominins. But there are some differences, and the face has been a focus of contention. Dali has a short face, and this would be true even if damage to the maxilla were corrected. Jinniushan also has a short clivus (the subnasal portion of the maxilla), and it is oriented vertically. In Dali, there is hollowing of the cheek below the orbit, and such excavation is not present in the African crania. Much has been made of this facial morphology, but in fact there is individual variation (see Section “Brain Size, Encephalization, and Speciation”). The significance of the Dali “canine fossa” should not be overemphasized. It is possible to argue that the later Middle Pleistocene hominins of China document an eastward excursion of H. heidelbergensis, where this species is taken to be the link between H. erectus and all later humans. Dating is not very firm, but probably fossils such as Dali and Jinniushan are younger than those in Africa. This may suggest that H. heidelbergensis was a late arrival in the eastern part of Asia.

Current Debates A differing interpretation arises from ongoing analyses of the discoveries at the Sima de los Huesos. As noted above, the Sima skulls exhibit traits expected to occur (very) early in the evolution of the Neanderthal lineage (Arsuaga et al. 1997). Recently, it has been emphasized that the Sima de los Huesos teeth are remarkably like those of “typical” Neanderthals (Martino´nTorres et al. 2012). The upper incisors display conspicuous labial convexity and a distinctive shovel shape, while the upper premolars present a bulging of the buccal aspect of the crown. The M1s possess an enlarged hypocone, giving the crown a rhomboidal outline characteristic of Neanderthals. The P3s have a symmetrical contour. Here, the talonid is reduced or absent, so that the remaining cusps occupy a small area near the lingual border of the crown. This Neanderthallike morphology is more pronounced in the Sima sample than in other Middle Pleistocene hominins. Indeed, Martino´n-Torres et al. (2012) claim that the Sima specimens are “more Neanderthal” in form than the Mauer or the Arago dentitions. They suggest that the Sima may constitute a source population for Neanderthals, while Mauer and Arago document the presence of a morphologically distinct lineage. Such a conclusion is favored by Stringer (2012), who envisions two species coexisting in the European Middle Pleistocene. The second species (H. heidelbergensis) includes fossils presumed to predate the evolutionary emergence of H. neanderthalensis, as well as specimens such as Petralona from later time periods.

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Archaeology and Behavior in the Middle Pleistocene Controversy over the number of Middle Pleistocene lineages in Eurasia and Africa will likely continue. Nevertheless, it is becoming clear that the hominins were more encephalized than H. erectus. Also, there is evidence from archaeology that these people were developing new behavior. Later Acheulean artifacts are known from numerous African sites, including Bodo, Olorgesailie, Isimila, Lake Ndutu, the Cave of Hearths, Elandsfontein, and Duinefontein 2. In general, later Acheulean hand axes can be characterized as thinner, more symmetrical, and bearing many more flake scars than their earlier counterparts. In some sites, relatively small hand axes are accompanied by flake tools resembling those of the Middle Stone Age (Klein 2000). While it is dangerous to expect universal associations of Homo species with particular industrial traditions, informative patterns may be uncovered (Foley and Lahr 1997). In virtually all mid-Quaternary African contexts, where diagnostic human bones are found with later Acheulean artifacts, the maker is H. heidelbergensis (or H. rhodesiensis). One may conclude that this species was capable of producing a tool kit more sophisticated than that utilized routinely by H. erectus. In western Eurasia, hominins equipped with Acheulean tools were present by the onset of the Middle Pleistocene (780 Ka) at Gesher Benot Ya’aqov in Israel (Goren-Inbar et al. 2000). Farther to the west in Europe, there are no Acheulean sites from the beginning of the Middle Pleistocene, but Boxgrove in Britain is likely to be 500 Ka in age. This locality has yielded thin, extensively flaked flint bifaces, along with bones of horses and rhinoceroses bearing cut marks. The animals may well have been hunted and butchered. In addition, there is the shaft of a human tibia. The dimensions of this bone at midshaft are large, and the Boxgrove individual was probably quite massive. This hominin has been attributed to H. heidelbergensis by Roberts et al. (1994). Signs of later Acheulean toolmakers are known from Torralba and Ambrona in Spain, where the artifacts are again found with large herbivores, including elephants and horses (Freeman 1994). Acheulean artifacts occur also at several sites in France and Italy. At Castel di Guido in central Italy, finely flaked bifacial tools were produced from elephant bone (Villa 1991). At some other earlier Middle Pleistocene localities, including Arago Cave, the stone industries contain small chopping tools and flakes but no hand axes (De Lumley et al. 1984). The reasons for this difference are unclear, but the availability of suitable raw materials, the constraints imposed by different types of stone, and the context in which tools were manufactured must all be considered, along with the possibility that distinct cultural behaviors or styles are represented. An isolated but particularly significant example of the skills acquired by mid-Quaternary Europeans comes from Scho¨ningen in Germany. Eight carefully crafted wooden throwing spears have been uncovered near a former lake, where they are associated with flint tools and chips (Thieme 1997, 2005, 2007). Scattered through the same horizon are the remains of numerous horses. Many of the bones are cut-marked, and some of the animals must have been processed for meat and marrow extraction (Roebroeks 2001). More convincingly than other early European assemblages, the Scho¨ningen discovery points to systematic hunting of large animals. Stalking and killing of agile or dangerous prey requires experience and practice, and it is reasonable to hypothesize that the people were cooperating with one another in these efforts. Increased levels of social cooperation and exchange of knowledge would have become the norm. And if the hunters at Scho¨ningen (also at sites such as Boxgrove and Arago) were able to obtain large amounts of meat, they would likely have shared or exchanged food with other groups, perhaps at established meeting places (Roebroeks 2001). Certainly our understanding of the behavior of the early Europeans remains quite incomplete, but it is apparent that bands of H. heidelbergensis were not

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_55-5 # Springer-Verlag Berlin Heidelberg 2013

only skilled at flaking stone but also capable of interacting regularly in the pursuit of game and other social activities.

Conclusion Middle Pleistocene crania from Bodo, Broken Hill, Elandsfontein, and Lake Ndutu in Africa are quite similar to penecontemporaneous fossils from Europe. Craniodental remains and jaws from Petralona and Arago Cave are particularly informative, and the assemblage from Sima de los Huesos is spectacular. If this grouping is expanded to include the Mauer mandible, then it can be argued that H. heidelbergensis was a geographically dispersed paleospecies. A question is whether additional specimens from China can be accommodated within this taxon. Dali and Jinniushan share a number of apomorphic traits with the western hominins, but there are differences, and the face has been a focus of contention. Dali has a short face, and there is hollowing of the cheek below the orbit. Probably the significance of the Dali “canine fossa” should not be overemphasized. Later Middle Pleistocene populations of China may document an eastward excursion of H. heidelbergensis, where this species is taken to be the link between H. erectus and all later humans. Homo heidelbergensis differs from H. erectus in absolute as well as relative brain size. Correlation analysis provides information about the interactions of brain volume with vault form. It can be determined that the expanding brain influences vertex height and probably also parietal sagittal length. Traits that vary independently from brain volume have greater taxonomic utility and include anterior frontal broadening, perhaps the high, arched outline of the temporal squama, and lateral expansion of the parietal vault. Encephalization does not explain the occipital rounding that distinguishes Broken Hill, Omo 2, and the Sima crania, nor does it account for the greater elevation of the lambda-inion chord. Traits of the cranial base also serve to diagnose H. heidelbergensis in relation to H. erectus. Morphology of the temporomandibular joint generally resembles that in H. sapiens, as is the case for the tympanic and petrous portions of the temporal bone. There is no reduction in overall face size in comparison to H. erectus, and the facial skeleton seems to be “hafted” to the braincase in such a way as to accentuate anterior projection. But reorientation of the nasal aperture and forward placement of the incisive canal within the palate suggest that the face of H. heidelbergensis may be more nearly vertical, as in H. sapiens. Later Acheulean artifacts are known from many mid-Pleistocene African localities, and in general, the hand axes can be characterized as thinner and more symmetrical than earlier examples. In some sites, relatively small hand axes are accompanied by flake tools resembling those of the Middle Stone Age. While it is dangerous to expect universal associations of Homo species with particular industrial traditions, in virtually all African contexts where diagnostic human bones are found with later Acheulean artifacts, the maker is H. heidelbergensis. One may conclude that these people were more advanced in behavior than their predecessors. There is evidence that H. heidelbergensis was able to make relatively sophisticated stone tools, hunt larger and more dangerous game animals, and perhaps engage in cooperative social activities.

References Aiello LC, Wood BA (1994) Cranial variables as predictors of hominine body mass. Am J Phys Anthropol 95:409–426 Page 15 of 20

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Arsuaga JL, Martinez I, Gracia A, Lorenzo C (1997) The Sima de los Huesos crania (Sierra de Atapuerca, Spain). A comparative study. J Hum Evol 33:219–281 Arsuaga JL, Lorenzo C, Carretero JM, Gracia A, Martinez I, Gracia N, Bermu´dez de Castro JM, Carbonell E (1999a) A complete human pelvis from the Middle Pleistocene of Spain. Nature 399:255–258 Arsuaga JL, Martinez I, Lorenzo C, Gracia A, Munoz A, Alonso O, Gallego J (1999b) The human cranial remains from Gran Dolina Lower Pleistocene site (Sierra de Atapuerca, Spain). J Hum Evol 37:431–457 Assefa Z, Brown F, Passey B, Fleagle JG, Yirga S (2000) New research in the Kibish formation, southern Ethiopia. Am J Phys Anthropol 309(Suppl):100 Bermu´dez de Castro JM, Arsuaga JL, Carbonell E, Rosas A, Martinez I, Mosquera M (1997) A hominid from the Lower Pleistocene of Atapuerca, Spain: possible ancestor to Neandertals and modern humans. Science 276:1392–1395 Bischoff JL, Shamp DD, Aramburu A, Arsuaga JL, Carbonell E, Bermu´dez de Castro JM (2003) The Sima de los Huesos hominids date to beyond U/Th equilibrium (>350 kyr) and perhaps to 400–500 kyr: new radiometric dates. J Archaeol Sci 30:275–280 Bischoff JL, Williams RW, Rosenbauer RJ, Aramburu A, Arsuaga JL, Garcia N, Cuenca-Bescos G (2007) High-resolution U-series dates from the Sima de los Huesos hominids yields 600 + infinity/-66 kyrs: implications for the evolution of the early Neanderthal lineage. J Archaeol Sci 34:763–770 Carbonell E, Mosquera M (2006) The emergence of symbolic behavior: the sepultural pit of the Sima de los Huesos, Sierra Atapuerca, Burgos, Spain. C R Palevol 5:155–160 Clark JD, Schick K (2000) Acheulean archaeology of the eastern Middle Awash. In: de Heinzelin J, Clark JD, Schick K, Gilbert WH (eds) The Acheulean and the Plio-Pleistocene deposits of the Middle Awash Valley Ethiopia. Muse´e Royal de l’Afrique Centrale, Tervuren, pp 51–121 Clark JD, de Heinzelin J, Schick KD, Hart WK, White TD, Wolde Gabriel G, Walter RC, Suwa G, Asfaw B, Vrba E, H-Selassie Y (1994) African Homo erectus: old radiometric ages and young Oldowan assemblages in the Middle Awash valley, Ethiopia. Science 264:1907–1910 Clark JD, Beyene Y, Wolde Gabriel G, Hart WK, Renne PR, Gilbert H, Defleur A, Suwa G, Katoh S, Ludwig KR, Boisserie JR, Asfaw B, White TD (2003) Stratigraphic, chronological and behavioural contexts of Pleistocene Homo sapiens from Middle Awash, Ethiopia. Nature 423:747–752 Clarke RJ (1985) A new reconstruction of the Florisbad cranium, with notes on the site. In: Delson E (ed) Ancestors: the hard evidence. AR Liss, New York, pp 301–305 Clarke RJ (1990) The Ndutu cranium and the origin of Homo sapiens. J Hum Evol 19:699–736 De Lumley H, Fournier A, Park YC, Yokohama Y, Demouy A (1984) Stratigraphie du remplissage Pleistocene moyen de la Caune de l’Arago a Tautavel. Anthropologie 88:5–18 Deacon HJ (1998) Elandsfontein and Klasies River revisited. In: Ashton NM, Healy F, Pettitt PB (eds) A master of his craft: papers in stone age archaeology presented to John Wymer. Oxbow, Oxford, pp 23–28 Dean D, Hublin JJ, Holloway RL, Ziegler R (1998) On the phylogenetic position of the pre-Neandertal specimen from Reilingen, Germany. J Hum Evol 34:485–508 Falgue`res C, Bahain JJ, Yokoyama Y, Arsuaga JL, Bermu´dez de Castro JM, Carbonell E, Bischoff JL, Dolo JM (1999) Earliest humans in Europe: the age of TD6 Gran Dolina, Atapuerca, Spain. J Hum Evol 37:343–352 Foley R, Lahr MM (1997) Mode 3 technologies and the evolution of modern humans. Cam Archaeol J 7:3–36 Page 16 of 20

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Freeman LG (1994) Torralba and Ambrona: a review of discoveries. In: Corruccini RS, Ciochon RL (eds) Integrative paths to the past: paleoanthropological advances in honor of F. Clark Howell. Prentice Hall, Englewood Cliffs, pp 597–637 Friess M (2010) Calvarial shape variation among Middle Pleistocene hominins; an application of surface scanning in paleoanthropology. C R Palevol 9:435–443 Gilbert WH, Asfaw B, White T (2000) Paleontology. In: de Heinzelin J, Clark JD, Schick K, Gilbert WH (eds) The Acheulean and the Plio-Pleistocene deposits of the Middle Awash Valley Ethiopia. Muse´e Royal de l’Afrique Centrale, Tervuren, pp 183–192 Goren-Inbar N, Feibel CS, Verosub KL, Melamed Y, Kislev ME, Tchnerov E, Saragusti I (2000) Pleistocene milestones on the out-of-Africa corridor at Gesher Benot Ya’aqov, Israel. Science 289:944–947 Gr€ un R, Brink JS, Spooner NA, Taylor L, Stringer CB, Franciscus RG, Murray AS (1996) Direct dating of Florisbad hominid. Nature 382:500–501 Harvati K, Hublin JJ, Gunz P (2010) Evolution of middle-late Pleistocene human cranio-facial form: a 3-D approach. J Hum Evol 59:445–464 Harvati K, Hublin JJ, Gunz P (2011) Three dimensional evaluation of Neanderthal craniofacial features in the European and African Middle Pleistocene human fossil record (abstract). Am J Phys Anthropol 52(Suppl):157 Howells WW (1973) Cranial variation in man. A study by multivariate analysis of patterns of difference among recent human populations. Pap Peabody Mus 67:1–259 Hublin JJ (1996) The first Europeans. Archaeology 49:36–44 Kalb JE, Wood CB, Smart C, Oswald EB, Mabrate A, Tebedge S, Whitehead P (1980) Preliminary geology and palaeoecology of the Bodo d’Ar hominid site, Afar, Ethiopia. Palaeogeogr Palaeoclimatol Palaeoecol 30:107–120 Kennedy KAR, Sonakia A, Chiment J, Verma KK (1991) Is the Narmada hominid an Indian Homo erectus? Am J Phys Anthropol 86:475–496 Klein RG (2000) The earlier Stone Age of southern Africa. S Afr Archaeol Bull 55:107–122 Klein RG, Cruz-Uribe K (1991) The bovids from Elandsfontein, South Africa, and their implications for the age, palaeoenvironment and origins of the site. Afr Archaeol Rev 9:21–79 Klein RG, Avery G, Cruz-Uribe K, Steele TE (2006) The mammalian fauna associated with an archaic hominin skullcap and later Acheulean artifacts at Elandsfontein, Western Cape Province, South Africa. J Hum Evol 52:164–186 Lieberman DE, Bar-Yosef O (2005) Apples and oranges: morphological versus behavioral transitions in the Pleistocene. In: Lieberman DE, Smith RJ, Kelley J (eds) Interpreting the past: essays on human, primate and mammal evolution. Brill Academic, Boston, pp 275–296 Lieberman DE, McBratney BM, Krovitz G (2002) The evolution and development of cranial form in Homo sapiens. Proc Natl Acad Sci USA 99:1134–1139 Martin RD (1981) Relative brain size and basal metabolic rate in terrestrial vertebrates. Nature 293:57–60 Martino´n-Torres M, Bermu´dez de Castro JM, Go´mez-Robles A, Prado-Simo´n L, Arsuaga JL (2012) Morphological description and comparison of the dental remains from Atapuerca-Sima de los Huesos site (Spain). J Hum Evol 62:7–58 McDougall I, Brown FH, Fleagle JG (2005) Stratigraphic placement and age of modern humans from Kibish, Ethiopia. Nature 433:733–736 Mturi AA (1976) New hominid from Lake Ndutu, Tanzania. Nature 262:484–485 Rightmire GP (1996) The human cranium from Bodo, Ethiopia: evidence for speciation in the Middle Pleistocene? J Hum Evol 31:21–39 Page 17 of 20

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Rightmire GP (1998) Human evolution in the Middle Pleistocene: The role of Homo heidelbergensis. Evol Anthropol 6:218–227 Rightmire GP (2001) Comparison of Middle Pleistocene hominids from Africa and Asia. In: Barham L, Robson-Brown K (eds) Human roots: Africa and Asia in the Middle Pleistocene. Western Academic and Specialist Press, Bristol, pp 123–133 Rightmire GP (2004) Brain size and encephalization in early to mid-Pleistocene Homo. Am J Phys Anthropol 124:109–123 Rightmire GP (2012) The evolution of cranial form in mid-Pleistocene Homo. S Afr J Sci 108:68–77 Rightmire GP (2013) Homo erectus and Middle Pleistocene hominins: brain size, skull form, and species recognition. J Hum Evol 65:223–252 Roberts MB, Stringer CB, Parfitt SA (1994) A hominid tibia from Middle Pleistocene sediments at Boxgrove, UK. Nature 369:311–313 Roebroeks W (2001) Hominid behaviour and the earliest occupation of Europe: an exploration. J Hum Evol 41:437–461 Ruff CB, Trinkaus E, Holliday TW (1997) Body mass and encephalization in Pleistocene Homo. Nature 387:173–176 Schoetensack O (1908) Der Unterkiefer des Homo heidelbergensis aus den Sanden von Mauer bei Heidelberg. Ein Beitrag zur Pala¨ontologie des Menschen. Englemann, Leipzig Seidler H, Falk D, Stringer C, Wilfing H, Muller GB, zur Nedden D, Weber GW, Recheis W, Arsuaga JL (1997) A comparative study of stereolithographically modelled skulls of Pretralona and Broken Hill: implications for further studies of Middle Pleistocene hominid evolution. J Hum Evol 33:691–703 Smith RJ (2002) Estimation of body mass in paleontology. J Hum Evol 43:271–287 Sonakia A, Biswas S (1998) Antiquity of the Narmada Homo erectus, the early man of India. Curr Sci 75:391–393 Stringer CB (2012) The status of Homo heidelbergensis (Schoetensack 1908). Evol Anthropol 21:101–107 Stringer CB, Howell FC, Melentis JK (1979) The significance of the fossil hominid skull from Petralona, Greece. J Archaeol Sci 6:235–253 Thieme H (1997) Lower Palaeolithic hunting spears from Germany. Nature 385:807–810 Thieme H (2005) The Lower Palaeolithic art of hunting. The case of Scho¨ningen 13 II-4, Lower Saxony, Germany. In: Gamble C, Porr M (eds) The hominid individual in context. Archaeological investigations of Lower and Middle Palaeolithic landscapes, locales and artefacts. Oxford University Press, Oxford, pp 115–132 Thieme H (ed) (2007) Die Scho¨ninger Speere. Mensch und Jagd vor 400000 Jahren. Ausstellungskatalog, Stuttgart Villa P (1991) Middle Pleistocene prehistory in southwestern Europe: the state of our knowledge and ignorance. J Anthropol Res 47:193–217 Wagner GA, Krbetschek M, Dagering D, Bahain JJ, Shao Q, Falgue`res C, Voinchet P, Dolo JM, Garcı´a T, Rightmire GP (2010) Radiometric dating of the type-site for Homo heidelbergensis at Mauer, Germany. Proc Natl Acad Sci USA 107:19726–19730 White TD (1986) Cut marks on the Bodo cranium: a case of prehistoric defleshing. Am J Phys Anthropol 69:503–509 White TD, Asfaw B, de Gusta D, Gilbert H, Richards GD, Suwa G, Howell FC (2003) Pleistocene Homo sapiens from Middle Awash, Ethiopia. Nature 423:742–747 Woodward AS (1921) A new cave man from Rhodesia, South Africa. Nature 108:371–372 Page 18 of 20

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Wu X, Athreya S (2013) A description of the geological context, discrete traits, and linear morphometrics of the Middle Pleistocene hominin from Dali, Shaanxi Province, China. Am J Phys Anthropol 150:141–157 Zhu R, Potts R, Xie F, Hoffman KA, Deng CL, Shi CD, Pan YX, Wang HQ, Shi RP, Wang YC, Shi GH, Wu NQ (2004) New evidence on the earliest human presence at high northern latitudes in northeast China. Nature 431:559–562

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Index Terms: Cranium_3–10 Cranium Arago Cave_7 Cranium Bodo_3 Cranium Broken Hill_3 Cranium Dali_10 Cranium Florisbad_5 Cranium Gran Dolina_9 Cranium Lake N’dutu_4 Cranium Omo region_5 Cranium Petralona_6 Cranium Sima de los Huesos_8 Encephalization quotients (EQ)_10 Middle Pleistocene hominins_2, 6, 9–11, 14 Middle Pleistocene hominins Africa_2 Middle Pleistocene hominins archaeology_14 Middle Pleistocene hominins behavior_14 Middle Pleistocene hominins brain size_10 Middle Pleistocene hominins encephalization_10 Middle Pleistocene hominins Europe_6 Middle Pleistocene hominins locations_2 Middle Pleistocene hominins phylogenetic hypotheses_11 Middle Pleistocene hominins South Asia_9 Middle Pleistocene hominins speciation_10

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_56-3 # Springer-Verlag Berlin Heidelberg 2014

Neanderthals and Their Contemporaries Katerina Harvati* Paleoanthropology, Senckenberg Center for Human Evolution and Paleoenvironment, Eberhard Karls Universität T€ ubingen, T€ ubingen, Germany

Abstract Neanderthals are the group of fossil humans that inhabited Western Eurasia from the mid-Middle Pleistocene until ca. 40 Ka ago, when they disappeared from the fossil record, only a few millennia after the first modern humans appear in Europe. They are characterized by a suite of morphological features that in combination produce a unique morphotype. They are commonly associated with the Mousterian lithic industry, although toward the end of their tenure they are sometimes found with assemblages resembling those produced by early modern humans. Although there is still discussion over their taxonomic status and relationship with modern humans, it is now commonly recognized that they represent a distinct, Eurasian evolutionary lineage sharing a common ancestor with modern humans in the Middle Pleistocene. This lineage is thought to have been isolated from the rest of the Old World, probably due to the climatic conditions of the glacial cycles. Glacial climate conditions are often thought to have been at least in part responsible for the evolution of some of the distinctive Neanderthal morphology, although genetic drift was probably also very important. The causes of the Neanderthal extinction are not well understood. Worsening climate and competition with modern humans are implicated.

The Discovery of Neanderthals: Historical Background Although the first Neanderthal remains were discovered in the early nineteenth century (Engis child in 1830, Forbes Quarry adult in 1848), it was not until the discovery of the skeleton from the Neander Valley in 1856, roughly coinciding with the publication of Darwin’s “The Origin of Species” in 1859, that the existence of an extinct kind of archaic humans was recognized. It is this locality that lends its name to the group, and it is there that the debate surrounding the relationship of Neanderthals with modern humans began. The antiquity of the Neanderthal skeleton and its status as an archaic human was not immediately accepted. Instead, its peculiar anatomical attributes were considered the result of various pathologies, including rickets. Its antiquity was only firmly established with the eventual discovery of additional skeletons of similar morphology associated with lithic artifacts and extinct fauna. Neanderthals were assigned to the species H. neanderthalensis as early as 1864 (King 1864). However, once their status as archaic predecessors of modern humans was accepted, their relationship with modern humans, and particularly modern Europeans, began to be intensely debated. The predominant view in the 1910s and 1920s was represented by scientists like Marcellin Boule and Sir

*Email: [email protected] *Email: [email protected] Page 1 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_56-3 # Springer-Verlag Berlin Heidelberg 2014

Arthur Keith, who were among the most influential scholars of their day. They placed Neanderthals in their own species and rejected any ancestral role for them in the evolution of modern people, pointing out their “primitiveness” and presumed inferiority (Boule 1911/1913; Boule and Vallois 1957). This perception of Neanderthals began to change during the 1930s. A rearrangement and “pruning” of the tangled hominin taxonomy was undertaken in the 1940s and 1950s by Mayr, Simpson, and Dobzhansky, who placed Neanderthals and other Middle Pleistocene fossil specimens within our own species, Homo sapiens. According to this view, Neanderthals were thought to have evolved into modern people through anagenetic evolution (Trinkaus and Shipman 1992, 1993; Tattersall 2000). This view has been reexamined in more recent years, with new evidence coming from modern human and fossil genetic studies, the development of better dating techniques and new approaches to the analysis of morphology. Currently, Neanderthals are commonly viewed as a distinct, Western Eurasian evolutionary lineage, which probably did not contribute significantly to the evolution of modern people.

Chronological Distribution The earliest human skeletal remains found in Europe have been recovered from Sima del Elefante in Atapuerca, Spain, dated to ca. 1.2 Ma (Carbonell et al. 2008) and from Barranco León, with a possibly even earlier date (up to 1.4; Toro-Moyano et al. 2013; but see Muttoni et al. 2013). Human remains dated to ca. 800 Ka have been recovered from Gran Dolina (Atapuerca, Spain; Bermúdez de Castro et al. 1997; Falguères et al. 1999), and lithic artifacts dated to ca. 700 and possibly up to 950 Ka have recently been discovered in England (Parfit et al. 2005, 2010) documenting an early human presence also in Northern Europe. These early European populations are considered by some to have been ancestral to the later, Middle Pleistocene Europeans and to Neanderthals (e.g., Bermúdez de Castro et al. 1997), but may also represent unsuccessful early episodes of colonization that ended in local extinctions. A calvaria from Ceprano, Italy, previously thought to date to ca. 780–800 Ka (Manzi et al. 2001) has recently been redated to ca. 450 Ka (Muttoni et al. 2009) and is now referred to Homo heidelbergensis (Mounier et al. 2011). The first appearance of Neanderthals in the fossil record is not clear-cut. Neanderthal-like features appear for the first time in a mosaic fashion in Middle Pleistocene European humans, as, e.g., in the large assemblage from Sima de los Huesos (Atapuerca), Spain (Arsuaga et al. 1997), recently dated to between 400 and 600 Ka (Bischoff et al. 2003, 2007; Arnold et al. 2014; but see Stringer 2012 for criticisms of this age estimate). Different Neanderthal-like traits appear at different times and places and in different combinations, but their presence in the European Middle Pleistocene fossil specimens suggests that the latter were early representatives of the Neanderthal lineage (Fig. 1). A progressively stronger expression of Neanderthal morphology is perceived through time, with specimens from the late Middle Pleistocene/early Late Pleistocene (
200–100 Ka) showing clear, albeit still not fully expressed, Neanderthal morphology. The full suite of Neanderthal features appears with the “classic” Neanderthals, in the Late Pleistocene, dated from approximately 70–30 Ka. This group includes among others the famous “Old Man” of La Chapelle-aux-Saints, as well as the type specimen from the Neander Valley, Feldhofer 1. The last date of appearance of Neanderthals, and thus the potential coexistence of Neanderthals and modern humans in Europe, has also been controversial due to methodological issues affecting radiocarbon dating of this period (see Conard and Bolus 2008; Blockley et al. 2008). The radiocarbon chronology of the late Neanderthals throughout Europe has been recently extensively revised Page 2 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_56-3 # Springer-Verlag Berlin Heidelberg 2014

Fig. 1 Frontal (a) and lateral (b) views of the Middle Pleistocene cranium from Petralona, Greece, showing incipient Neanderthal morphology in its facial region (Courtesy of Eric Delson and # Eric Delson, Photo by K. Harvati)

using the latest methodological advances. Radiocarbon dates reported here are uncalibrated, unless otherwise specified. The Neanderthal specimens from Layer G1 at Vindija, Croatia, were recently directly redated to ca. 33–32 radiocarbon Ka BP through direct accelerator mass spectrometry (AMS) using collagen ultrafiltration (Higham et al. 2006), revising previously published younger dates of ca. 29 radiocarbon Ka BP (Smith et al. 1999). Two sites in France, both associated with the Châtelperronian lithic industry (see below), have been associated with Neanderthal remains. The partial skeleton from Saint-Césaire was originally dated to ca. 36 Ka BP using the thermoluminescence (TL) dating method (Mercier et al. 1991). A recent direct AMS ultrafiltration radiocarbon date on the skeleton produced a somewhat older date of ca. 36 radiocarbon Ka BP (between 41,950 and 40,660 years BP calibrated; Hublin et al. 2012). The Châtelperronian layers containing a subadult Neanderthal temporal bone (Hublin et al. 1996), as well as several Neanderthal isolated teeth (Bailey and Hublin 2006) at Arcy-sur-Cure (Grotte-duRenne), were originally dated by AMS radiocarbon to ca. 34 Ka (David et al. 2001). Hublin et al. (2012) redated the Châtelperronian and Late Châtelperronian layers at Arcy to between ca. 40 and 35.5 radiocarbon Ka BP using accelerator mass spectrometry radiocarbon dates on ultrafiltered bone collagen (calibrated to between 41,620 and 40,570 years BP). A very late direct radiocarbon date for one of the Mezmaiskaya (Russia) Neanderthal infants (
29 Ka; Ovchinnikov et al. 2000) is now thought to have resulted from modern carbon contamination. Recent work on this site has produced much older ESR dates (
70–60 Ka for the first infant and
40 Ka for the second; Skinner et al. 2005), as well as a direct 14C AMS ultrafiltration date on the second infant of ca. 39.7 Ka BP (calibrated to between 42.3 and 45.6 Ka cal BP; Pinhasi et al. 2011). Several sites in Spain have been proposed as showing late Neanderthal occupation. Zafarraya was until recently considered to be among the youngest Neanderthal sites in Europe. The Neanderthalbearing layers there had been dated to between ca. 33.4 and 28.9 Ka BP using conventional 14C and uranium series dating (Hublin et al. 1995). The age of these Neanderthal layers has most recently been revised (using ultrafiltration and AMS 14C) to be much older and close to the radiocarbon limit (Wood et al. 2013). A relatively late date for Neanderthal layers at Las Palomas (ca. 34.5 and 35 Ka BP, both AMS 14C on burnt faunal bone; Walker et al. 2008) has been criticized as unreliable due to the difficulties in dating burnt material (Wood et al. 2013). Finally an exceptionally recent date of 24 Ka BP as the date of last appearance of Neanderthals in Iberia based on redating of a Mousterian lithic assemblage (Finlayson et al. 2006) is considered questionable due to stratigraphic inconsistencies (Delson and Harvati 2006) as well as methodological concerns (Wood et al. 2013). Page 3 of 35

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Geographic Distribution Neanderthals are commonly thought of as European hominins, and Europe is often considered as their geographical area of origin, with specimens outside the continent representing later range expansions (Hublin 1998, 2000). Within Europe, Neanderthals range from Iberia to Russia and from the Mediterranean to Northern Europe. Outside of the continent, their presence has been documented in the Near East and in Western Asia as far east as Uzbekistan (Fig. 2) and Siberia (Krause et al. 2007b). Eastern Neanderthals are often juxtaposed with those from Western Europe in that their morphology is mosaic in pattern and not fully “Neanderthal” (Vandermeersch 1989; Smith 1991; Rak 1993). In some of their features, Eastern Neanderthals show conditions that have sometimes been perceived as more modern (though not all specimens show the same conditions for the same features), leading some to question the Neanderthal identity of these fossils (Arensburg and Belfer-Cohen 1998). A more widely accepted view is that the weaker expression of Neanderthal traits in these specimens reflects primitive retentions rather than affinities with modern humans (Stringer 1990). Similarly, weakly expressed Neanderthal morphology is found in early Neanderthals, such as those from Saccopastore, again interpreted as retentions of primitive morphology (Condemi 1992).

Morphology Neanderthals are characterized by a suite of distinctive cranial, mandibular, dental, and postcranial anatomical features (Figs. 3 and 4), some of which represent retentions of ancestral conditions but many of which are derived for this group. Primitive traits, shared with the common ancestor of both Neanderthals and modern humans, include their low and elongated crania, heavy brow ridges, large faces with large nasal apertures, and the lack of a chin. Neanderthals share some derived features with modern humans, including enlarged brains, reduced prognathism, a weak occipital torus, and a longer and more rounded occipital. A list of proposed deriver traits is provided in Table 1. A detailed morphological description of the various anatomical areas follows.

Cranium Face The Neanderthal face is characterized by a heavy, double-arched supraorbital torus which does not show distinct elements and grades smoothly onto the frontal squama. The orbits are large and rounded. The nasal aperture is very large and broad. The nasal cavity is voluminous and displays large medial projections and a bilevel internal nasal floor. Neanderthals show pronounced midfacial prognathism and an oblique and inflated infraorbital plate with no canine fossa, which obliquely recedes into the zygomatic bone. The inferior root of the zygomatic is oblique, and not sharply angled, and the zygomatic processes are elongated and thin. Internally, the maxillary sinuses are large, while the frontal sinus is expanded laterally to fill most of the supraorbital torus (up to midorbit) but does not extend upward into the frontal squama (Heim 1974, 1976; Stringer et al. 1984; Rak 1986; Trinkaus 1987, 2003; Schwartz and Tattersall 1996a; Arsuaga et al. 1997; Franciscus 1999, 2003). Several alternative hypotheses have been proposed to account for the distinctive Neanderthal facial morphology. The large nasal aperture and associated structures have been proposed to relate to cold-climate adaptation and to function in warming and humidifying inspired air, as well as to dissipate heat (Coon 1962; Dean 1988). Another interpretation sees the Neanderthal facial features Page 4 of 35

Fig. 2 Map of the geographic distribution of Neanderthals, showing several sites preserving Neanderthal and pre-Neanderthal skeletal remains discussed in the text

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_56-3 # Springer-Verlag Berlin Heidelberg 2014

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Fig. 3 Frontal (a) and lateral (b) views of the La Ferrassie 1 (top) and Amud 1 (bottom) Neanderthal crania (Courtesy of Eric Delson, # Musée de l’ Homme and Rockefeller Museum, Photo by C. Tarka for Ancestors)

as biomechanical consequences of intense paramasticatory behavior evidenced by the unusual anterior tooth wear pattern exhibited in this fossil group (Heim 1976; Rak 1986; Trinkaus 1987). Among recent humans, the shape of the nasal cavity has been shown to be affected by climatic factors such as temperature and humidity (Noback et al. 2011). However, large noses and nasal cavities are characteristic of warm-climate populations, although tall nasal apertures characterize arctic populations (Hubbe et al. 2009), making the climatic adaptation hypothesis difficult to evaluate. On the other hand, several studies have rejected the proposed biomechanical advantages of the Neanderthal face (Antón 1994, 1996). A third interpretation considers Neanderthal facial morphology as primarily the result of stochastic processes (Hublin 1998; Weaver et al. 2007). Vault Neanderthals show a particularly flat and elongated vault in lateral profile and an “en bombe,” rounded profile in posterior view, with the widest point at the mid-parietals. The occipital region shows a highly convex occipital scale, with a flattening above lambda, termed occipital “bun” or “chignon.” The occipital torus is weak with no external occipital protuberance. It is inferiorly undercut by the nuchal plane, but not clearly defined superiorly, and shows a pitted oval depression above it (suprainiac fossa). The temporal squama is superoinferiorly low, anteroposteriorly short, and symmetrically arched. The external auditory meatus is elevated relative to the zygomatic process and the floor of the glenoid fossa. The parietomastoid suture is relatively long and straight (Boule 1911/1913; Hublin 1978, 1988a, b, 1998; Stringer et al. 1984; Condemi 1988; Lieberman 1995; Schwartz and Tattersall 1996b; Dean et al. 1998; Harvati 2003b).

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Fig. 4 Complete Neanderthal skeleton (left) reconstructed using elements from five partial skeletons (principally La Ferrassie 1 and Kebara 2) compared to a modern human skeleton (right) (Courtesy of Ian Tattersall and Gary Sawyer, Photo by Ken Mowbray)

Neanderthal endocasts show similar features to those of modern humans (Holloway 1985), but their average cranial capacity is larger measuring approximately 1,520 cm3 (from 1,200 to 1,700 cm3). Large brains might be related to cold-climate adaptation in these hominins (Churchill 1998). Even though absolute brain size was larger on average in Neanderthals relative to modern humans, their relative brain size may have been smaller due to their greater body mass (Ruff et al. 1997). The brain enlargement characteristic of both Neanderthals and modern humans appears to have followed distinct evolutionary trajectories in the two lineages, with Neanderthals retaining an archaic endocranial shape despite larger size, and modern humans exhibiting distinct shape, as well as size, changes (Bruner et al. 2004). Modern human endocasts show enlarged parietal lobes, as well as expanded temporal lobes and enlarged cribriform plates compared to Neanderthals (Bruner et al. 2004; Bastir et al. 2011). The distinctive globular shape of the human endocast appears to be achieved early in development, through the addition of a distinct “globularization” phase (Gunz et al. 2010). Basicranium The mastoid process is small and equal in size to or smaller than the juxtamastoid eminence. It often shows a mastoid tubercle. The petrotympanic crest originates at the most inferiorly projecting part of the tympanic, and the tympanic plate is coronally oriented. The mandibular fossa is wide, shallow, and medially closed off. The foramen magnum is long, narrow, and ovoid in shape. The cranial base is relatively flattened. Recent examination of the internal morphology of the inner ear using computer tomography (CT) scans has revealed a distinctive shape for the Neanderthal bony

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_56-3 # Springer-Verlag Berlin Heidelberg 2014

Table 1 Some proposed derived Neanderthal features (Adapted from Hublin (1998)) Cranium Midfacial prognathism Medial nasal projections above a spinoturbinal crest delineating a prenasal fossa Double-arched supraorbital torus with no distinct elements Horizontally flat or convex infraorbital area, obliquely receding in alignment with the anterolateral surface of the zygomatic bone Secondarily increased relative platycephaly “En bombe” cranial shape Highly convex occipital plane (chignon or occipital “bun”) Pitted suprainiac fossa associated with a bilaterally protruding occipital torus External auditory meatus at the level of the posterior zygomatic arch, with a strong inclination of the basal groove of this process Flat mandibular fossa Long and narrow foramen magnum Laterally flattened, small mastoid process and large juxtamastoid eminence Anterior mastoid tubercle Small and inferiorly positioned posterior semicircular canal Mandible Mental foramen below the M1 Retromolar gap Asymmetric mandibular notch, coronoid process higher than the condyle Laterally expanded condyle Oval/horizontal shape of the mandibular foramen Large pterygoid tubercle Dentition Expanded anterior dentition Taurodontism Mid-trigonid crest on mandibular molars Markedly skewed upper molar crowns Asymmetric mandibular fourth premolar crown

labyrinth, most significantly characterized by an inferior placement of the posterior semicircular canal (Vallois 1969; Santa Luca 1978; Laitman and Heimbuch 1982; Trinkaus 1983; Stringer et al. 1984; Stringer 1985; Vandermeersch 1985; Hublin 1988; Condemi 1991, 1992; Elyaqtine 1995; Hublin et al. 1996; Schwartz and Tattersall 1996b; Harvati 2003b; Spoor et al. 2003).

Mandible Neanderthal mandibles show a receding symphysis resulting in the absence of a mental eminence or chin. There is a space between the third molars and the ascending ramus, termed the retromolar gap. Recent analyses have shown this trait to be related to increased size in modern humans, great apes, and Middle-Late Pleistocene European fossils, suggesting caution in the interpretation of its derived status. The Neanderthal mental foramen is positioned posteriorly below the first mandibular molar rather than the premolars, unlike modern humans. The gonial area is rounded. The mandibular (sigmoid) notch is shallow and asymmetric with a coronoid process that is higher than the condyle. The mandibular notch meets the condyle in a medial position, and the condyle is laterally expanded.

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The submandibular and pterygoid fossae are very deep, and the mandibular foramen shows an ovalhorizontal shape (Boule 1911/1913; Vandermeersch 1981; Stringer et al. 1984; Tillier et al. 1989; Condemi 1991; Franciscus and Trinkaus 1995; Hublin 1998; Rak 1998; Rosas 2001; Jabbour et al. 2002; Rak et al. 2002; Trinkaus et al. 2003; Rosas and Bastir 2004; Nicholson and Harvati 2006).

Dentition The dimensions of the Neanderthal posterior dentition completely overlap with those of modern humans. However, Neanderthal anterior teeth, and particularly the incisors, are larger. Neanderthal teeth show enlargement of the pulp chambers (taurodontism), although this trait is variable in its degree of expression and seems to be more weakly expressed in Eastern Neanderthals. Several morphological dental features appear at very high frequencies in Neanderthals compared to modern humans. These include shoveling of the incisors and the presence of a tuberculum dentale; asymmetric lower fourth premolars with transverse crests and distolingual cusps; markedly skewed upper molars; lower molars with mid-trigonid crests; and the absence of four-cusped lower third molars. Finally, the Neanderthal dentition is distinctive in its wear patterns, showing markedly greater wear anteriorly. Although this is not a heritable trait, it has been used to infer behavioral practices (Keith 1913; Trinkaus 1983; Bytnar et al. 1994; Bailey 2002, 2004; Bailey and Lynch 2005; Bailey and Hublin 2006)

Postcranium The Neanderthal postcranium (Fig. 4) is overall robust, with markedly curved shafts of the femur and radius, thick cortical bone, and strong muscle and ligament markings. Neanderthals were short relative to early modern humans and probably also to earlier H. ergaster populations. Estimated stature averages
169 cm for males and
160 cm for females. Body mass is estimated at
78 kg for males and
66 kg for females. Additional Neanderthal postcranial features include a broad and deep ribcage, with large thoracic volume, especially inferiorly; relatively short distal limb segments; large articular heads of the tibia and femur; a relatively low angle between the femoral neck and shaft; the absence of a pilaster on the femur and a more rounded (in cross section) femoral shaft; a dorsal, rather than ventral, sulcus on the axillary border of the scapula; large and round apical tufts of the manual phalanges and a relatively short proximal thumb phalanx; clavicles showing two curvatures in dorsal view; and an elongated and thin pubic ramus (Boule 1911/1913; Trinkaus 1983; Ruff 1991, 1993, 1994; Holliday 1997a, b; Ruff et al. 1997; Churchill 1998; Rosenberg 1998; Trinkaus and Ruff 1998; Pearson 2000; Voisin 2000; Niewoehner 2001; Franciscus and Churchill 2002; Weaver 2003; Sawyer and Maley 2005). Several of these traits have been linked to high activity levels and/or cold-climate adaptation. Others could represent Neanderthal-derived features, but since very little is known about their ancestral conditions, no definitive assessments can be made at present. Neanderthal body proportions are commonly viewed as “hyperarctic.” It has been suggested that the short stature and short distal limb proportions represent a cold-climate adaptation following Bergmann’s and Allen’s rules, as seen also in some modern human populations (Trinkaus 1981; Holliday 1997a, b; Steegmann et al. 2002). Overall robusticity, wide trunks, and features of the Neanderthal femur and pelvis have also been linked to climate adaptation (Ruff 1994; Pearson 2000; Weaver 2003). As improved paleoclimatic information suggests that Neanderthal ranges followed favorable climatic conditions, the designation of Neanderthals as “hyperarctic” has been challenged (Finlayson 2004). A recent estimate of the ability of the Neanderthal body shape to withstand cold temperatures showed only a small advantage over early modern humans with a less “cold-adapted” body form Page 9 of 35

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(Aiello and Wheeler 2003), indicating that Neanderthals could not have inhabited their high-latitude habitats without substantial cultural insulation.

Life History, Pathology, and Trauma Neanderthal growth seems in many ways similar to modern humans, although there are indications that some aspects of their development, including brain and dental growth, were accelerated (Dean et al. 1986, 2001; Ramírez Rozzi and Bermúdez de Castro 2004; Smith et al. 2007, 2009, 2010). The age-mortality profile observed among Neanderthals has been found to differ from that of recent human and other mammals in having a low percentage of older adults and infants and a high percentage of adolescents and prime-age adults (Trinkaus 1995). A similar pattern was found in the Atapuerca Sima de los Huesos and Krapina human assemblages (Bocquet-Appel and Arsuaga 1999). Although there are problems associated with such paleodemographic analyses, the observed mortality profile suggests very low adult life expectancy, probably associated with high levels of stress and trauma (Trinkaus 1995). Increased survivorship of adults resulting in a longer lifespan may have appeared very late in human evolution and not until the advent of early modern humans (Caspari and Lee 2004). Indications of trauma and stress are ample in the Neanderthal skeletal record, so much so that it has been remarked that posttraumatic lesions can be found on almost every well-preserved adult Neanderthal skeleton (Trinkaus 1983; Berger and Trinkaus 1995; Jelinek 1994). An analysis of traumatic lesion patterns in Neanderthals found them to be concentrated in the head and neck region, an uncommon pattern of injury that was argued to result from hunting strategies requiring proximity to large prey animals (Berger and Trinkaus 1995). On the other hand, some injuries have been argued to originate from interpersonal aggression (Trinkaus 1983; Zollikofer et al. 2002; Churchill et al. 2009). As the majority of traumatic lesions in Neanderthals are healed or partially healed, they have also been seen as evidence for social assistance in these hominins, as have the multiple incidents of highly worn or otherwise nonfunctional dentition (Trinkaus 1983, 1985; Lebel et al. 2001; Lebel and Trinkaus 2002). In addition to trauma, Neanderthal remains show elevated developmental stress (Molnar and Molnar 1985; Ogilvie et al. 1989; Jelinek 1994; Berger and Trinkaus 1995). However, the degree to which this differs from stress levels in recent foraging groups is debated (Hutchinson et al. 1997; Guattelli-Steinberg et al. 2004).

Neanderthal Genetics Neanderthals are the first extinct human species to yield genetic information. The first glimpse of their mitochondrial DNA came with the publication of the seminal article by Krings et al. (1997). These researchers were able to recover mtDNA from the Neanderthal (Feldhofer 1) type specimen and to compare it to the homologous sequence from diverse modern human populations. The Neanderthal sequence was outside the range of modern human variation and was equally dissimilar to modern human sequences from different geographic regions. It pointed to a last common ancestor for the mitochondrial genome of Neanderthals and modern humans at approximately 500 Ka (between 317 and 741 Ka). mtDNA has now been sequenced partially or in whole for several Neanderthal specimens from diverse geographic origin (Krings et al. 1997, 2000; Ovchinnikov et al. 2000; Schmitz et al. 2002; Page 10 of 35

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Serre et al. 2004; Beauval et al. 2005; Lalueza-Foz et al. 2005, 2006; Caramelli et al. 2006; Orlando et al. 2006; Krause et al. 2007a; Green et al. 2008). All have yielded similar, Neanderthal-like sequences, which group together as a distinct clade, albeit with some geographic patterning (Fabre et al. 2009). On the other hand, all of the earliest Eurasian modern human specimens so far tested have yielded only modern humanlike and no Neanderthal-like mtDNA sequences (Caramelli et al. 2003; Serre et al. 2004; Krause et al. 2010; Fu et al. 2013). A recent analysis of five Neanderthal mtDNA genomes estimated the date of divergence of the Neanderthal and modern human ancestral populations in the mid-Middle Pleistocene (starting at ca. 410–440 Ka BP; Endicott et al. 2010). More recently it has been possible to investigate also the nuclear DNA of Neanderthals. Nuclear DNA analysis has shown that Neanderthals share with modern humans the FOX P2 gene variant, one of the genes affecting language abilities, which was previously thought to be unique to modern humans (Enard et al. 2002; Krause et al. 2007a). Analysis of the nuclear DNA of an Italian Neanderthal showed that at least that individual did not share the derived allele for microcephalin with modern humans, a gene previously suggested to derive from Neanderthal ancestry (Lari et al. 2010). Ancient DNA analysis has also offered a glimpse of what Neanderthals may have looked like in the flesh: pale skin and red hair have been suggested for two Neanderthal specimens from Italy and Spain on the basis of their melanocortin 1 receptor variant (Lalueza-Fox et al. 2007). A subsequent analysis of the published genomic data from three Neanderthal individuals from Vindija, Croatia, however, indicated that they carried alleles consistent with darker skin and eyes and brown or red hair color (Cerqueira et al. 2012). These results suggest that phenotypic variability was likely high among Neanderthals. The sequencing of the Neanderthal genome has also indicated a limited contribution [1–4 % (Green et al. 2010), recently reestimated to 1.5–2.1 % (Pr€ ufer et al. 2014)] of Neanderthals to modern people from Eurasia. Admixture is thought to have likely occurred in the Near East and before the spread of early modern humans into the rest of Eurasia (Green et al. 2010), although other models have also been proposed (e.g., Currat and Excoffier 2011), in part to account for the observed higher admixture levels in Asia compared to Europe (Sankararaman et al. 2014; Vernot and Akey 2014). By measuring the extent of linkage disequilibrium among modern European genomes, Sankararaman et al. (2012) dated the last interbreeding between Neanderthals and modern Europeans to between 37,000 and 86,000 years BP and likely between 47,000 and 65,000. There is still discussion on whether the observed similarities can be at least in part explained by population substructure of the ancestral modern human population rather than by admixture (Eriksson and Manica 2012; Lowery et al. 2013). Nevertheless, it has been argued that such archaic interbreeding had important health consequences for modern humans (Abi-Rached et al. 2011; Sankararaman et al. 2014; The Sigma Type Diabetes Consortium, in press). Some of the identified Neanderthalderived alleles are connected with modern diseases, such as diabetes, lupus, Crohn’s disease, and other conditions (Sankararaman et al. 2014). Others, however, mainly alleles relating to skin and hair, appear to have been selected for in modern humans and therefore likely provided some evolutionary advantage (Sankararaman et al. 2014; Vernot and Akey 2014). Strikingly, the modern human genome is depleted from Neanderthal-derived alleles in the X chromosomes and in genes that are expressed in the testes (Sankararaman et al. 2014). This evidence strongly suggests male infertility for Neanderthal-modern human hybrids and indicates a high level of genetic incompatibility among the two sister taxa (Sankararaman et al. 2014; Vernot and Akey 2014). This finding is compatible with the high level of morphological differentiation between Neanderthals and modern humans and accounts for the very low observed levels of admixture. One of the unexpected results of the Neanderthal genome project has been the genetic identification of a hitherto unknown hominin lineage, dubbed the Denisovans (Krause et al. 2007; Reich Page 11 of 35

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et al. 2010), first recognized through the mtDNA analysis of a phalanx from Denisova cave, in the Altai Mountains, Siberia, dating to ca. 50–30 Ka BP. The mtDNA retrieved differs from that of either modern humans or Neanderthals, and appears to belong to a hominin that shared a common mtDNA ancestor with both groups at ca. 1 Ma BP (Krause et al. 2007). Reich et al. (2010) were able to retrieve nuclear DNA from the same bone, as well as to identify another fossil carrying the same mtDNA type. The genomic analysis showed that, contrary to the mtDNA results, the Denisovan individual likely represents a sister taxon to Neanderthals. Unlike Neanderthals, Denisovans seem to not have contributed genetically to all Eurasians, but instead to have admixed with modern Melanesian populations, which show Denisovan contribution of 4–6 % to their genetic material. On the basis of these results, it was suggested that this taxon was very widespread in Asia during the Late Pleistocene (Reich et al. 2010). There is little understanding of what fossil taxon may correspond to the genetically identified Denisovans. A tooth from the same cave yielded the same type of mtDNA, providing a narrow glimpse on the morphology associated with this lineage (Reich et al. 2010). This specimen is a very large upper molar, likely a third molar or possibly second molar. If considered a third molar, this specimen is outside the range of variation in its crown dimensions of any taxa of the genus Homo, except H. habilis and H. rudolfensis. If considered a second molar, its dimensions also overlap with those of H. erectus. The specimen does not present any derived Neanderthal or modern human features. This question has become even more complicated by the recent discovery of Denisovanlike mtDNA in the Sima de los Huesos material (Meyer et al. 2014). These findings suggest that the Sima population may have been related to the ancestors of both Neanderthals and Denisovans or, alternatively, that gene flow between these two lineages contributed the Denisovan-like DNA to the Sima group.

Behavior Technology Neanderthals are most commonly, though not exclusively, associated with the Mousterian lithic technology, named after the site of Le Moustier in the Dordogne, France. Typical of Mousterian industries was the use of both Levallois and discoidal flaking techniques for the production of flakes that could be converted to a wide range of shapes, including various kinds of side scrapers, retouched points, denticulates, notches, and sometimes small handaxes (Debénath and Dibble 1994; Mellars 1996; Shea and Brooks 2000). In addition to Europe, the Mousterian is found in the Caucasus, the Near East (where it is associated with both Neanderthals and early modern humans) and North Africa (where it is not associated with Neanderthals). Mousterian industries appear in Europe as early as
200–150 Ka and possibly earlier in the Near East, but most sites are dated to the interval from
130 to 30 Ka. The lithic raw material used for the production of tools in most Mousterian sites tends to be locally available. Most raw materials derive from within a 5–6 km range, and only a very small component derives from distant sources (Mellars 1996). These are mostly transported as finished tools. There is a lack of specialized use of different types of raw materials in the Mousterian, as well as a lack of specialized quarries. Very few bone tools are known (but see Soressi et al. 2013). Some points appear to have been hafted and were probably used as spear points (Mellars 1996; Shea and Brooks 2000). Wooden tools were probably also made, as is evidenced by several well-preserved wooden spears discovered in Schöningen and dated to approximately 400 Ka (Thieme 2000) and by parts of similar

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implements from Clacton-on-Sea (possibly ca. 350 Ka) and Lehringen (ca. 130–110 Ka; Mellars 1996). Neanderthal sites show relatively little structure compared to later Upper Paleolithic sites. The living areas are small and exhibit no clear focus of activity. Artificial structures are rare, although exceptions are known. Hearths are well defined and were probably central in tool production and bone processing but are not consistent in their location (Mellars 1996). Controlled use of fire appears widespread in Europe from the Middle Pleistocene Oxygen Isotope Stage (OIS) 11 (
400 Ka) onward and possibly earlier (Gowlett 2006). Until recent years, the Mousterian was commonly thought to represent a static culture. However, redating of Mousterian sites has shown changes with time in regional industries from Europe and the Near East (Shea and Brooks 2000). Additionally, reanalysis of some Mousterian sites has shown technological responses to climatic changes (Kuhn 1995; Shea and Brooks 2000). Some “transitional” Middle-Upper Paleolithic industries, like the Châtelperronian industry in France, the Uluzzian in Italy, and the Szeletian in East-Central Europe, also show strong affinities with the Mousterian. These were originally thought to have been made by early modern humans, also generally considered responsible for the Aurignacian industry. Since the Châtelperronian has been found associated with Neanderthal skeletal remains in two sites in France, St. Césaire, and Arcy-surCure (Lévêque and Vandermeersch 1980; Hublin et al. 1996), it has been widely held that at least some of these transitional industries were produced by late Neanderthal populations. This in turn has prompted intense debate over the identity of the makers of these industries, the possibility of Neanderthal acculturation by, or trade with, early modern humans, and the cognitive capacities and ability for symbolic thought in Neanderthals (d’Errico et al. 1998; Zilhão and d’Errico 1999; Mellars 1999, 2005; Klein 2000; Harvati et al. 2003; Bar-Yosef 2005; Gravina et al. 2005; Svoboda 2005; Hublin et al. 2012). Recently Benazzi et al. (2011) identified the only known human remains associated with the Uluzzian (two milk molars from Grotta del Cavallo, Italy) as representing modern human, rather than Neanderthal, children. These remains furthermore represent the earliest known modern human remains in Europe (dated to between ca. 42 and 45 Ka calibrated BP through AMS 14C dating on shell). This discovery suggests that at least the Uluzzian was produced by modern humans and further complicates our understanding of the transitional industries in Europe.

Subsistence Neanderthal sites abound in faunal remains of various taxa, indicating a high reliance on meat in their diet. Large palearctic mammals are most commonly found in these assemblages, including bison, wild cattle, horse, reindeer, red and fallow deer, ibex, wild boar, and gazelle (Shea and Brooks 2000). Sites from the high latitudes of Northern and Central Europe indicate an almost exclusive reliance on large- to medium-sized mammals, with very little small game and low diversity of animals consumed (e.g., very few bird or fish remains; Hockett and Haws 2005). Middle-latitude Neanderthal sites (Southwestern France and Northern Spain) also show low diversity and a focus on terrestrial mammals but indicate a somewhat greater reliance on medium-sized mammals. Sites from the Mediterranean region still show reliance on large- and medium-sized terrestrial mammals but also preserve evidence for consumption of other food sources, such as shellfish, birds, tortoises, and marine mammals (Stiner 1994; Barton 2000; Currant 2000; Hockett and Haws 2005; Stringer et al. 2008; Harvati et al. 2013). Plant remains in Neanderthal sites are rare, likely due to their poor preservation. Phytoliths and other vegetal remains known primarily from Mediterranean sites point to a plant component in Neanderthal diet which probably included wild legumes and grasses as well as seeds and fruit (e.g., Gale and Carruthers 2000; Madella et al. 2002; Lev et al. 2005). Recent work on dental calculus recovered from Neanderthal teeth has confirmed such strong plant Page 13 of 35

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components in Neanderthal diets and has also pointed to cooking and potentially medicinal use of plants (Henry et al. 2011; Hardy et al. 2012). In addition to direct evidence of faunal and plant remains from archaeological sites, Neanderthal diets can be assessed using the isotopic signature of the Neanderthal skeletons themselves. Analysis of the stable isotopes of carbon and nitrogen has now been undertaken for a number of Neanderthal specimens from a wide time range (
130–30 Ka) and so far has invariably indicated a very strong reliance on herbivore meat (Fizet et al. 1995; Bocherens et al. 1999, 2005; Richards et al. 2000). All Neanderthal bones so far analyzed are similar to top predators in their isotopic composition. Furthermore, some of the isotopic studies suggest a much greater reliance on very large herbivores, such as wholly rhinoceros or wholly mammoth, than had been previously thought based on the faunal archaeological evidence (Bocherens et al. 2005). The isotopic analyses agree with zooarchaeological studies in suggesting a very small component of marine foods in Neanderthal diets, in sharp contrast with later, Upper Paleolithic modern humans (Richards et al. 2001, 2005). The degree to which Neanderthals obtained meat through hunting as opposed to scavenging has been a subject of debate (Binford 1983; Chase 1986; Stiner 1990). Some have suggested that the relative significance of these two activities probably varied seasonally and from region to region (Shea and Brooks 2000). Among the arguments brought forth to support scavenging as the primary Neanderthal activity is the high proportion of cranial faunal remains in Neanderthal sites and the age profile of the remains, thought to be for the most part old individuals rather than prime-age adults (Binford 1983). However, a bias toward cranial remains may simply represent a bias in the butchering and transportation of large carcasses (Mellars 1996). The age-mortality profile is now known to vary, with several French Middle Paleolithic sites showing a catastrophic mortality profile inconsistent with hypotheses of scavenging (summarized in Mellars 1996). Further evidence in support of hunting comes from the wooden spears from Schöningen dated to 400 Ka (Thieme 2000), although there is disagreement as to whether these represent throwing or thrusting spears. Finally, the Neanderthal stable isotopic signature suggests active predation on the part of the Neanderthals and is difficult to reconcile with a subsistence strategy consisting primarily of scavenging (Richards et al. 2000).

Symbolic Thought and Language The Neanderthal ability for symbolic thought and language is hotly debated. The archaeological record shows a dearth of “symbolic” objects, such as objects of art or personal ornamentation, in Mousterian assemblages, compared not only with later Upper Paleolithic industries (Mellars 1996) but also with some penecontemporaneous African sites (McBrearty and Brooks 2000; Henshilwood et al. 2001; but see Zilhão et al. 2010; Peresani et al. 2011). The relative scarcity of such objects has been argued to indicate a lack of human cognitive abilities and language. However, it has also been pointed out that the archaeological record is a very limited and imperfect record of behavior, perhaps in this case resulting in a biased documentation (or lack thereof) of Neanderthal symbolic activities. The discovery of Neanderthal remains associated with transitional industries, and, in the case of Arcy-sur-Cure, with lavish personal ornaments, has raised tremendous discussion over the identity of the makers of these objects, as well as the processes that would have led to their association with Neanderthals (i.e., trade, acculturation, or endogenous development; see, e.g., Hublin et al. 1996, 2012; d’Errico et al. 1998; Zilhão and d’Errico 1999; Mellars 1999, 2005; Klein 2000; Harvati et al. 2003; Bar-Yosef 2005; Benazzi et al. 2011). Evidence in support for Neanderthal ability for some symbolic thought is the occurrence of ochre and manganese “crayons” in Neanderthal sites and the burial of at least some Neanderthal skeletal remains. Although the apparent Neanderthal burials have been argued to be simply the product of Page 14 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_56-3 # Springer-Verlag Berlin Heidelberg 2014

natural processes (Gargett 1999), the recovery of a number of largely complete skeletons from diverse sites found in articulation and placed in shallow pits is strongly indicative of intentional burial. Nevertheless, evidence for grave goods and other burial practices is scant and controversial (Mellars 1996; Shea and Brooks 2000). In terms of the anatomical evidence for language and cognition, Neanderthals possessed cranial capacities as large as or larger than modern humans. Their endocasts show similar features to those of modern humans and similar left-right asymmetries (Holloway 1985) although they retain an “archaic” overall shape (Bruner et al. 2004; see also Gunz et al. 2010; Bastir et al. 2011). The relatively flat Neanderthal cranial base was long considered to indicate a larynx positioned so high that it would preclude the production of certain speech sounds and particularly of vowels crucial to speech perception (Lieberman and Crelin 1971; Laitman and Heimbuch 1982; Lieberman 1989). This hypothesis was most recently tested by Barney et al. (2012) who used extensive modern human reference series and a large number of fossils to reconstruct the Neanderthal vocal tract and to simulate its articulatory potential. This study found that, although Neanderthals probably had a limited production of vowels compared to modern humans, this limitation would likely not have affected the/i/and/u/vowels that are critical for speech. A further attempt to infer language capabilities from the bony morphology focused on the hypoglossal canal, which transmits the nerves to the exceptionally large human tongue musculature. The size of the hypoglossal canal was found to be similar in Neanderthals and modern humans and larger than in earlier hominins (Kay et al. 1998), suggesting a similar function for the Neanderthal tongue in speech production. More recent work, however, has questioned this evidence (DeGusta et al. 1999). Neanderthals are also similar to modern humans and unlike earlier hominins in their enlarged thoracic vertebral canals, which could indicate an expansion of thoracic innervation (MacLarnon and Hewitt 1999). The resulting greater control of the intercostal musculature would enhance breathing control and could indicate the ability for speech. Finally, the anatomy of the outer and middle ear in the Middle Pleistocene pre-Neanderthal fossils from Sima de los Huesos (Atapuerca, Spain) was found to be similar to that of modern humans and specialized for speech perception (Martínez et al. 2004), supporting speech capabilities for Neanderthals and their ancestors.

Evolution and Classification The “Accretion Hypothesis”

The “Accretion Model” for the evolution of Neanderthals (Dean et al. 1998; Hublin 1998) accounts for the progressive appearance of Neanderthal morphology through time, beginning around 450 Ka (OIS 12). According to this hypothesis, the Neanderthal lineage became isolated in Europe due to the severe glacial conditions prevailing in the Balkans at this time, in combination with enlarged Caspian and Black seas and increased aridity in North Africa and the Levant (Stringer 2012). In these conditions of isolation, the Neanderthal morphology is thought to have become gradually fixed, partly through natural selection as an adaptation to cold-climate conditions but perhaps primarily through the process of genetic drift (Hublin 1998; Stewart and Stringer 2012). Although the accretion process of Neanderthal features is mosaic in nature, facial and mandibular features have been argued to be established first, followed by features in the occipital region and finally in the temporal bone and vault (Dean et al. 1998; Hublin 1998; Rightmire 1998). This pattern, however, is complicated by uncertainties in the chronology of the skeletal material (especially the very old ages proposed for the Sima de los Huesos remains; see Stringer 2012) and in the polarity of some of the relevant features (see Harvati et al. 2010; Freidline et al. 2012). Four broad stages of Page 15 of 35

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Neanderthal evolution have been described (Dean et al. 1998; Hublin 1998). Stage 1 includes “early pre-Neanderthals,” i.e., the Middle Pleistocene archaic specimens, such as Petralona, Arago, and Mauer, dating from before OIS 12. These hominins are considered to show incipient Neanderthal features mainly in the facial region (although some of these features may represent primitive retentions; Harvati et al. 2010). They also show strong similarities with African and Asian contemporaries (e.g., Stringer 1974; Mounier et al. 2009; Harvati et al. 2010; Schwartz and Tattersall 2010). Stage 2 (OIS 11-9) specimens are termed “pre-Neanderthals” (e.g., Steinheim, Swanscombe). They are thought to exhibit Neanderthal morphology more clearly, showing Neanderthal features also in the occipital area. Stage 3 (OIS 7-5, Biache, Krapina, Saccopastore) “early Neanderthal” specimens show most Neanderthal traits in the posterior cranium and some also in the temporal region. Finally, Stage 4 comprises the “classic Neanderthals” of OIS 4 and 3 (Neanderthal, La Chapelle-aux-Saints, Amud), showing fully expressed Neanderthal morphology.

Classification of Middle Pleistocene Humans According to the accretion hypothesis, Neanderthal evolution was an anagenetic process with no speciation event resulting in the appearance of this taxon. Within the framework of this model, Neanderthals can be viewed either as a subspecies of H. sapiens or as a full, distinct species, H. neanderthalensis. If the latter classification is accepted, then the position of the Middle Pleistocene specimens from Europe must be clarified. Traditionally, these have been included in the species H. heidelbergensis in which African Middle Pleistocene humans have also been placed, due to extensive observed morphological similarities between the European and African Middle Pleistocene human fossils (e.g., Stringer 1974; 1984; Arsuaga et al. 1997; Rightmire 1998, 2007, 2008; Harvati 2009; Mounier et al. 2009; Harvati et al. 2010). This taxon is viewed by some as ancestral to both Neanderthals and modern humans (e.g., Rightmire 1998, 2008, 2009; Stringer 2012). If the European H. heidelbergensis was exclusively ancestral to Neanderthals, this sample could be placed within the Neanderthal lineage and within the taxon H. neanderthalensis (e.g., Stringer 1995, 2012; Hublin 1998, 2009). Alternatively, the European lineage could be arbitrarily split into two paleospecies, the earlier segment retaining the nomen H. heidelbergensis and the later H. neanderthalensis (e.g., Arsuaga et al. 1997; Manzi 2004; but see Wolpoff et al. 1994; Rosas et al. 2006; Tattersall and Schwartz 2006; Bräuer 2008). In either case, the African Middle Pleistocene specimens would have to be placed into another taxon, possibly H. rhodesiensis or H. helmei (Stringer 1995, 2012). The position of the Sima de los Huesos in this scheme is crucial, as these specimens exhibit very strong Neanderthal similarities (e.g., Rak et al. 2011; Gomez-Robles et al. 2012; Martinón-Torres et al. 2012) while argued to be >530 Ka old (Bischoff et al. 2007), thus providing a very strong link between European H. heidelbergensis and later Neanderthals. Recently Stringer (2012) questioned this age estimate due to taphonomic considerations and proposed that the Sima de los Huesos specimens can be considered early Neanderthals instead of H. heidelbergensis.

Neanderthal Taxonomy and the Neanderthal Role in Modern Human Evolution Ever since their assignment to the distinct species Homo neanderthalensis (King 1864), the classification of Neanderthals and their role in human evolution have been the subject of intense discussion. Current consensus sees Neanderthals and earlier Middle Pleistocene European extinct humans as a separate evolutionary lineage, at least partly geographically isolated in Western Eurasia. What is still unclear, however, is the nature of the interaction between Neanderthals and modern humans arriving in Europe ca. 45 Ka BP (Benazzi et al. 2011; Higham et al. 2011a, b). Since the two taxa likely overlapped in Europe for some millennia, it is widely thought that they would have met at least on some occasions (although the duration of their coexistence is debated, as is contact between Page 16 of 35

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them; e.g., Finlayson 2004; Pinhasi et al. 2011, 2012). The nature of their interaction and the possibility and extent of interbreeding during these encounters are central points of discussion. Although there is no doubt that Neanderthals were our closest relatives, the magnitude of anatomical differences between Neanderthals and modern humans is such that several authors recognize the former as a distinct species under species definitions that use morphological criteria (e.g., Stringer 1974; Tattersall 1992; Stringer and Andrews 1988; Hublin 1998; Harvati 2003b; Harvati et al. 2004). The long list of uniquely derived Neanderthal features, many of which appear early in ontogeny (e.g., Maureille and Bar 1999; Ponce de León and Zollikofer 2001), points to distinct species status under the phylogenetic species concept (e.g., Hublin 1978; Santa Luca 1978; Stringer et al. 1984; Tattersall 1986, 1992, 2000; Stringer and Andrews 1988; Schwartz and Tattersall 1996a, b). Furthermore, the cranial morphological distance between Neanderthals and modern humans is more similar to interspecific than to intraspecific distances observed among primate species and their subspecies, suggesting a distinct species status as appropriate for Neanderthals (Harvati 2003a; Harvati et al. 2004). Some paleoanthropologists see evidence for admixture in the fossil record and have therefore argued for subspecific status for Neanderthals following the biological species concept. These authors have pointed out Neanderthal-like features in early modern European specimens and trends of morphological “modernization” in some late Neanderthal samples, as well as proposed individual specimens as potential hybrids (e.g., Smith 1982, 1992; Wolpoff 1989; Frayer 1992; Frayer et al. 1993; Duarte et al. 1999; Ahern et al. 2002; Trinkaus et al. 2003; Soficaru et al. 2007). However, others have rejected these claims (e.g., Lahr 1996; Bräuer and Broeg 1998; Tattersall and Schwartz 1999; Bräuer et al. 2004, 2006; Bailey 2002; Harvati 2003a, 2009; Harvati et al. 2004, 2007). From a genetic perspective, the mtDNA of Neanderthals and Upper Paleolithic Europeans shows no evidence for admixture between the two groups (Wolpoff et al. 2001; Serre et al. 2004; Green et al. 2008), although demographic modeling indicates that a small contribution of Neanderthals to the modern human gene pool is consistent with this result (9 mm), broad frontal (>125 mm), long frontal (glabella-bregma length >113 mm), or long occipital plane (>60 mm). With regard to other features used, it is unclear how they can be properly scored as present or absent without a clear scoring system. Among these are as follows: mastoidsupramastoid crests well separated, frontonasal suture arched, glabellar depression, glenoid articular surface flattened, and paramastoid crest prominent. In addition, many of the features used can hardly be regarded as distinguishing between Neanderthals and modern humans. Thus, it is not surprising that Wolpoff et al. (2001) found the most divergent numbers of differences between Mladeč 5 and two closely related early modern specimens from Skhūl, i.e., only 8 differences to Skhūl 4, but 23 to Skhūl 5. Yet there are further problems with this study, such as the morphological representativeness of using only the male specimens, the lack of relevant features, and the inappropriate method of Page 12 of 29

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pairwise difference analysis (Collard and Franchino 2002; Bräuer et al. 2004b). Thus, critical reexamination of the claimed evidence for a considerable Neanderthal contribution in the Mladeč material cannot be supported. Another early modern specimen claimed to show evidence for gene flow from Neanderthals is the mandible from Pes‚ tera cu Oase. However, according to Trinkaus et al. (2003, p. 11235), “the only feature that suggests Neandertal affinities is the lingual bridging of the mandibular foramen, a feature that is currently unknown among humans preceding Oase 1 other than the late Middle and Late Pleistocene members of the Neandertal lineage.” Yet how reliable is this so-called H-O foramen for demonstrating Neanderthal-modern gene flow? As Smith (1978, p. 327) found, there are neither individuals under 18 years of age from any modern sample examined nor any juvenile Neanderthal exhibiting the H-O type. This makes it likely that, as Smith (1978) mentioned, factors developing during the individual’s lifetime could also be responsible for the occurrence of the trait. Since the morphology at the mandibular foramen can change during a lifetime, the feature cannot be regarded as a good genetic trait (Lieberman 1995, p. 175). Moreover, its occurrence does not clearly signal continuity. According to Frayer (1992, p. 31), the H-O type appears in 10 out of 19 Neanderthals (52.6 %), in 4 out of 22 early Upper Paleolithic specimens (18.2 %), and in 2 out of 30 late Upper Paleolithic specimens (6.7 %). The four early Upper Paleolithic specimens, however, include the Neanderthal Vindija 207 and Stetten (Vogelherd) 1, which no longer belong to this group. Thus, there is no relevant occurrence of this feature in the early Upper Paleolithic. Moreover, most important in this respect is a study of terminal Pleistocene North African samples. Groves and Thorne (1999, p. 253) found the bilateral H-O foramen in 22.2 % of the Nubian material from Tushka and Jebel Sahaba, further showing that this trait is not necessarily derived from Neanderthals. Finally, the H-O foramen already occurred outside of Europe in H. erectus such as in OH 22 and Zhoukoudian H1. Thus, though it cannot be excluded, it is far from clear that this single possible Neanderthal trait present on one ramus of the Oase mandible really indicates gene flow from Neanderthals. There is also no unequivocal evidence for a Neanderthal contribution in the adolescent cranium Oase 2 that might be contemporaneous with the mandible. This specimen exhibits a whole set of derived modern features in the vault and face, combined with M3s that are unusually large and have a complex cusp pattern (Rougier et al. 2007). Specimens from two further Romanian sites have also been regarded as relevant to the gene flow debate. The mandible from the Pes‚ tera Muierii with an ultrafiltrated and calibrated AMS date of 34 Kyr bp (Higham et al. 2011) exhibits an asymmetrical mandibular notch which occurs most frequently in Neanderthals (Rak 1998; Soficaru et al. 2006). Yet it is also found in modern and recent humans as, e.g., in the Holocene Vogelherd mandible and shows great individual variability. Nevertheless, a possible indication to Neanderthal gene flow cannot be excluded here. This, however, appears less likely, regarding the nuchal morphology of the slightly younger calvaria from Cioclovina. Rather, this specimen shows a robust modern morphology and no typical Neanderthal suprainiac fossa (Bräuer 2010). Finally, the juvenile Gravettian skeleton from Lagar Velho, Portugal, has been suggested to exhibit aspects indicating Neanderthal ancestry (Zilhão and Trinkaus 2002). Yet the major feature that has been suggested to show a Neanderthal-like condition – the relatively short lower legs – is not unequivocal. It cannot be excluded that the condition also reflects some adaptation among these early modern populations to cold conditions before the Last Glacial Maximum (Stringer 2002b) or individual variation within this modern population (Tattersall and Schwartz 1999). In addition, the occurrence of Harris lines points to periods of disease or malnutrition. Moreover, if one takes the estimated adult crural index for Lagar Velho of 80.7 % and the 95 % confidence intervals (77.5–83.9) as provided by Ruff et al. (2002, p. 380), there appears to be considerable overlap with early Upper Paleolithic Europeans as well. No matter whether some Neanderthal genes were Page 13 of 29

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involved in the specimens discussed here or not, it is difficult to escape the conclusion that the hard evidence points to only small traces of interbreeding between Neanderthals and modern humans. A Neanderthal contribution to early modern Europeans of up to 50 % as assumed by Wolpoff et al. (2004) has no support. Thus, a replacement process accompanied by a small amount of gene flow as suggested by the Out-of-Africa and hybridization model appears to be in good agreement with the current evidence from Europe (Bräuer 2010; Stringer 2011).

Continuity or Discontinuity in the Far East The assumption of regional evolution in China and Australasia is mainly based on morphological features or sets of features. Weidenreich (1943) published a list of 12 so-called Mongolian traits that he regarded as clear evidence for a close relationship between Chinese H. erectus and living north Chinese. Among these are midsagittal crest and parasagittal depression, metopic suture, Inca bone, certain “Mongolian” features of the nasal bridge and cheek region of the maxilla and zygomatic bone, shovel-shaped upper lateral incisors, and horizontal course of the nasofrontal and frontomaxillary sutures. Coon (1962, p. 458) was also convinced that many common features existed between Peking Man and living northeast Asians. Finally, the multiregionalists, as well, see strong support for their model in North Asia. Accepting most of the features suggested by Weidenreich and some other authors, multiregionalists presented a rather long list of assumed regional Chinese traits (Wolpoff et al. 1984; Pope 1992; Wu 1992). Although some features are said to have changed over time, Wolpoff et al. (1984, p. 435) were convinced that “all of these characteristics have much lower frequencies and are distributed discontinuously in regions other than China.” Weidenreich (1943) also saw an evolutionary line leading from Pithecanthropus via H. soloensis to the Australian aborigines of today. Some years before, Keith (1936) had already regarded the recently discovered Solo hominins as representing the evolutionary stage linking Pithecanthropus to the Australian aborigine. Wolpoff et al. (1984, pp. 443–444) mentioned about 20 continuity features of the cranium, including flatness of the frontal in sagittal plane, distinct prebregmatic eminence, marked prognathism, persistence of the zygomaxillary ridge, eversion of the lower border of the malar, rounding of the inferolateral border of the orbit, prelambdoidal depressions, and lambdoidal protuberance. Most of the features are from Weidenreich (1943), Larnach and Macintosh (1974), and Thorne and Wolpoff (1981). Based on these assumed regional features, multiregionalists are convinced that Australasia shows a clear anatomical sequence between the earliest Indonesian H. erectus and the recent and living Australians uninterrupted by African migrants at any time (Frayer et al. 1993, p. 21). Since many of the regional features for the Far East were suggested in the first half of the twentieth century, reexaminations have been carried out by several authors over the last two decades. With regard to the suggested East Asian traits, Groves (1989, p. 279) arrived at the conclusion that there is “little evidence for special likeness of modern ‘Mongoloids’ to Homo erectus pekinensis” and identified many of the features as primitive retentions also found outside the region. According to Habgood (1992, p. 280) “none of the proposed ‘regional features’ can be said to be documenting ‘regional continuity’ in east Asia as they are commonly found on modern crania from outside of this region . . ., and are consistently found on archaic Homo sapiens and/or Homo erectus crania throughout the Old World.” In her analysis of 11 proposed East Asian continuity features, Lahr (1994) found that almost all of them occurred more frequently in recent samples from other parts of the world. Facial flatness was found to be most pronounced in final Pleistocene populations from Page 14 of 29

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Fig. 5 Archaic and early modern crania from China: (a) Dali; (b) Liujiang

Northern Africa. A later detailed study by Koesbardiati (2000) focused on the middle and upper facial regions especially regarded as showing a great number of East Asian continuity features (Pope 1992; Frayer et al. 1993). The results, however, revealed that no variable showed a distribution as would be predicted by the Multiregional Evolution model. Instead, most of the features occur more frequently or are more pronounced among population samples from Africa, Europe, and Australia than in the Chinese sample. Some of the features show the highest frequencies among the Inuit of Greenland who, however, represent a relatively young population showing adaptations to extreme conditions (Howells 1993; Lahr 1995). Also, the fossil record from China hardly supports regional continuity from H. erectus to modern people of the area. Even the problematic continuity features are lacking in archaic H. sapiens specimens. For example, the 200 Kyr old cranium from Jinniushan does not exhibit any of the following: midfacial flatness, a marked angulation of the maxilla and zygomatic bones when viewed from beneath, a flattened nasal saddle, a nondepressed nasal root, or lack of wisdom teeth. Based on further features, even Pope (1992) has raised doubts whether this hominin along with the Maba specimen fits into the picture of regional evolution in China and suggested strong genetic influence from the West into China in the terminal Middle or Late Pleistocene. Moreover, the 150–200 Kyr old cranium from Dali (Fig. 5) with its heavy supraorbital torus and other archaic features hardly reveals clear similarities to modern Chinese. Because of the discontinuity between Chinese H. erectus and this East Asian archaic H. sapiens group and the similarities of the latter to archaic H. sapiens from Europe, it has been suggested that the Dali-Maba-Jinniushan morph has its roots in the archaic sapiens of the western part of the Old World. Recent sequencing of the genome of a 40 Kyr old finger bone from the Denisova Cave in the Altai Mountains, southern Siberia, identified a new archaic hominin group that shared some of its history with Neanderthals and might have split from the Page 15 of 29

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common Preneanderthal lineage some 200–300 Ka (Reich et al. 2010). Moreover, it has been shown that these so-called Denisovans interbred with the modern ancestors of present-day Melanesians and Australians, most likely in Southeast Asia. These populations exhibit about 5 % of Denisovan DNA (Reich et al. 2010, 2011). Perhaps – but this is still a hypothesis – the Dali-Maba-Jinniushan group could belong to this archaic Denisovan lineage that lived in wide parts of East Asia. Further relevant evidence contradicting the idea of regional evolution in China comes from the earliest modern humans of the area. For a long time, the specimens from the Upper Cave at Zhoukoudian and from Liujiang in southern China were regarded to be among the earliest moderns, probably dating to ca. 25–30 Kyr bp (Hedges et al. 1995; Etler 1996). Due to more recent Uraniumseries dates, Shen et al. (2002) have argued that the Liujiang specimen could be much older (>60 Ka or 100 Ka), but there remain basic uncertainties as to the stratigraphic position of the human remains and thus to their age (Demeter et al. 2012; Keates 2010). In spite of some deviations from present-day Chinese population samples (Howells 1995; Stringer 1999), a multivariate analysis of these early modern Chinese crania (Bräuer and Mímisson 2004) demonstrated that the Upper Cave 101 specimen exhibits the closest affinities with Upper Paleolithic Europeans and also Australians and recent Europeans. For the Liujiang cranium (Fig. 5), the greatest similarity was found with recent North Africans and Europeans as well as with Upper Paleolithic Europeans, terminal Pleistocene North Africans, and sub-Saharan Africans. These similarities appear to support a more recent date for Liujiang. Yet, even if this fully modern specimen would indeed be about 100 Kyr old, it would still clearly contradict any regional evolution from the archaic Dali-MabaJinniushan group. The discussion on the date of the earliest presence of modern humans in East Asia continues, since more human remains have been reported to date between >40 and 100 Ka. These comprise an anterior mandibular fragment from Zhirendong, South China, dated to about 100 Ka (Liu et al. 2010), and a partial adult cranium from the Tam Pa Ling, a cave in Laos, with an age of ca. 46 Ka (Demeter et al. 2012). Because of extant uncertainties on the dating of Liujiang and the fully modern condition of Zhirendong, Demeter et al. (2012) regard the rather well-preserved specimen from Laos as the earliest definitively modern fossil in East Asia. Yet, even with this specimen some questions on the dating and stratigraphy exist (Pierret et al. 2012). Regarding Australasia, the central assumptions of the multiregionalists have also proven to be no longer tenable. In spite of the huge gap in time between the only H. erectus specimen with a wellpreserved face, Sangiran 17, and the earliest Australians, Wolpoff et al. (1984, p. 443) saw, especially in the face, a number of continuity features such as the marked prognathism, the maintenance of large posterior dentitions throughout the Middle and Late Pleistocene, an eversion of the lower border of the malar, the persistence of a zygomaxillary ridge, and rounding of the inferolateral border of the orbit. Yet the assumption of interregional gene flow as emphasized by multiregionalists would make it very unlikely that such combinations of features could have been maintained over a period of more than 1 Myr and during the claimed transformation process from the massive facial morphology of H. erectus toward that of modern humans (Nei 1998). In addition, Aziz et al. (1996) demonstrated that the earlier reconstruction of the Sangiran 17 cranium done by Wolpoff (Thorne and Wolpoff 1981) is incorrect in several respects. In the revised reconstruction (Fig. 6), the degree of facial prognathism is not marked, but only moderate, and there is no eversion of the lower border of the zygomatic bone, which as a whole bulges laterally. Moreover, the zygomaxillary ridge could not be detected by Aziz et al. (1996, p. 20), nor by myself, on the original. There is also no rounding of the inferolateral border of the orbit (Baba et al. 2000, p. 61). Finally, Baba et al. (2000, p. 62) demonstrated that “it does not make sense to compare the degree of facial and dental reduction between Sangiran 17 and Australians, because masticatory adaptation Page 16 of 29

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Fig. 6 Homo erectus from Indonesia and an early modern Australian: (a) Revised reconstruction of Sangiran 17 by Aziz et al. 1996 (Photo: F. Aziz/H. Baba); (b) Ngandong; (c) Lake Mungo 3

pattern is completely different from each other.” Thus, relevant continuity features which have been said to be present on Sangiran 17, dated to ca. 1.3 Ma (Antón 2003), are simply not there or are the result of incorrect reconstruction. Also, in her comprehensive analysis of 20 assumed Australasian cranial features, Lahr (1994) arrived at the conclusion that most of the traits did not show the pattern proposed by the Multiregional Evolution model and quite a number of them occur with high frequency in a robust terminal Pleistocene sample from North Africa, thereby supporting a functional interpretation of these traits. Detailed analyses of the cranial morphology of Indonesian H. erectus show a continuous gradual evolution from the early Pleistocene specimens to the late H. erectus from Ngandong (Fig. 6) and Sambungmacan, but no further evolutionary continuity to early modern Australasians (Kaifu et al. 2008). Until recently, the ages of Ngandong and of Sambungmacan, which have long been controversial, ranged between a few hundreds of thousands of years (e.g., Bartstra et al. 1988) to only 30–50 Ka (Swisher et al. 1996). New redating by Ar/Ar and ESR/U-series also arrived at divergent results that nevertheless narrow the age of the Ngandong hominins to between 140 and 540 Ka (Indriati et al. 2011). Thus, it now seems that the Ngandong erectus is older than 100 Ka and not contemporaneous with the earliest Australians, such as the fully modern skeleton Lake Mungo 3, southern Australia (Fig. 6), for which several dating approaches have yielded an age of more than 40 Kyr bp and perhaps even up to 60 Kyr bp (Thorne et al. 1999; Bowler and Magee 2000). Although no conclusive indications for a regional evolution from H. erectus to modern Australians appear to exist, the human fossil and subfossil material from Australia as a whole exhibits considerable variability with regard to robusticity. Among these anatomically modern humans, there are very robust as well as gracile specimens as, for example, present in the Kow Swamp material which dates to ca. 22–19 Kyr bp or somewhat more recent (Bräuer 1989; Stone and Cupper 2003). One of the most robust crania is WLH-50 from the Willandra Lakes, which has been absolutely dated to 14 Kyr bp (Simpson and Gr€ un 1998). The cranial vault of this specimen has also been modified by severe pathological alterations (Webb 1990). Notwithstanding the young age and pathology of WLH-50, Wolpoff et al. (2001) chose this cranium instead of the much more appropriate one from Lake Mungo in order to demonstrate regional evolution in Australasia. Page 17 of 29

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-4 # Springer-Verlag Berlin Heidelberg 2014

Fig. 7 Origin and evolution of Homo sapiens

However, their approach also suffers from fundamental problems with the characteristics used as well as their assessments (Bräuer et al. 2004b). Robust specimens also date from the early Holocene. Possible explanations for the great range of variation might be drift effects in the course of the occupation of the continent but may also include adaptation to an increasingly arid environment toward the peak of the last glacial period (Klein 1999; Baba et al. 2000). As the recent genome sequencing showed, populations of Australia and New Guinea not only exhibit up to 5 % of their DNA from the archaic Denisovans but also 1–4 % of Neanderthal DNA (Reich et al. 2011). Yet, in view of the fact that the earliest fully moderns in Australia are rather gracile, it remains controversial whether this archaic DNA component also contributed to the greater robusticity among the later terminal Pleistocene Australians.

Conclusions Over the last two and a half decades, the accumulating fossil and molecular evidence has strongly supported the “Out-of-Africa and hybridization” model. Claims by multiregionalists for a larger contribution of Neanderthals to the early modern Europeans cannot be supported by the current evidence. Instead, the most likely scenario appears to be a replacement of the Neanderthals accompanied by only a small amount of gene flow. For the Far East, it is more difficult to examine possible indications of interbreeding since the fossil record of the replacement period is rather poor.

Page 18 of 29

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-4 # Springer-Verlag Berlin Heidelberg 2014

Nevertheless, in view of the serious problems regarding the claimed continuity features for China and Australasia and the fact that the earliest modern humans in both areas are fully anatomically modern and do not fit into the concept of regional evolution, no convincing evidence can be seen for long-term regional evolution up to modern humans. The anatomical modernization process in Africa now appears to be well established by quite a number of diagnostic and reliably dated hominid specimens. To describe the obvious morphological changes of this continuously evolving lineage, three grades or groups of H. sapiens have been suggested. This evolutionary sequence led to an early emergence of anatomically modern humans nearly 200 Ka. In view of the obvious continuity from archaics to early moderns and the nearmodern morphology of the premoderns, it appears unlikely that anatomically modern humans differ from their direct ancestors on the species level (Stringer 2002a; Bräuer 2008). Instead, during the major part of the Middle Pleistocene, the African fossil record documents a diachronic increase of more derived modern-like conditions. Therefore, it appears adequate to assign the post-H. erectus humans to one biological species H. sapiens (Klein 2009; Hofreiter 2011). This view is also supported by the fact that the Preneanderthal/Neanderthal lineage which goes back to around 500 Ka bp cannot reasonably be split into different species. It might thus be in agreement with the current evidence (Fig. 7) from Africa and Europe to only assume a speciation between H. erectus and (archaic) H. sapiens at around 700 or 800 Ka in Africa. Later, early archaic sapiens populations spread into Europe evolving toward the Neanderthals. Regarding China, it appears likely that the late Middle Pleistocene humans derived from an eastward dispersal of archaic H. sapiens populations, possibly representing the Denisovan lineage, although some regional gene flow from H. erectus cannot be excluded as well. As discussed in this and other chapters, various alternative phylogenetic scenarios have been suggested to describe Middle and Late Pleistocene human evolution. H. sapiens is often restricted to modern humans, and its ancestral group (largely equivalent to late archaic H. sapiens) has been assigned either to the same species (Stringer 2002a) or to a separate species, H. helmei (McBrearty and Brooks 2000). Alternatively, H. helmei is regarded as ancestral not only to modern H. sapiens but also to H. neanderthalensis (Foley and Lahr 1997). These various possibilities, however, have their own problems. For example, the latter phylogeny does not consider that Neanderthal features had long existed in Europe prior to the hypothesized appearance of H. helmei. Moreover, suggesting several species within the continuously evolving lineages of later human evolution causes problems in delimiting the taxonomic units (Foley 2001). Such units are rather arbitrarily defined entities without any clear relation to biological species. Studies on extant primates led Jolly (2003, p. 662) to conclude that Neanderthals, Afro-Arabian “premodern” populations, and modern humans are, roughly speaking, biological subspecies, comparable to interfertile allopatric taxa or phylogenetic species of baboons. Thus, it appears well supported from different lines of evidence, including the recent results from nuclear DNA sequencing for widespread archaic-modern hybridization, to regard the European Preneanderthals/Neanderthals and the African Middle Pleistocene lineage to modern humans and the late archaic group in China as belonging to one polytypic species H. sapiens. “Speciation remains the special case, the less frequent and more elusive phenomenon, often arising by default” (Grubb 1999, p. 164).

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Serre D, Pääbo S (2006) The fate of European Neanderthals: results and perspectives from ancient DNA analyses. In: Harvati K, Harrison T (eds) Neanderthals revisited: new approaches and perspectives. Springer, Dordrecht, pp 211–219 Shen G, Wang W, Wang Q, Zhau J, Collerson K, Zhou C, Tobias PV (2002) U-Series dating of Liujiang hominid site in Guangxi, Southern China. J Hum Evol 43:817–829 Simpson JJ, Gr€ un R (1998) Non-destructive gamma spectrometric U-series dating. Quat Sci Rev 17:1009–1022 Smith FH (1978) Evolutionary significance of the mandibular foramen area in Neandertals. Am J Phys Anthropol 48:523–531 Smith FH (1982) Upper Pleistocene hominid evolution in South-Central Europe. Curr Anthropol 23:667–703 Smith FH (2002) Migrations, radiations and continuity: patterns of Middle and Late Pleistocene humans. In: Hartwig WC (ed) The primate fossil record. Cambridge University Press, Cambridge, pp 437–456 Smith FH, Falsetti AB, Donnelly SM (1989) Modern human origins. Ybk phys Anthropol 32:35–68 Smith FH, Falsetti B, Simmons T (1995) Circum-Mediterranean biological connections and the pattern of late Pleistocene human evolution. In: Ullrich H (ed) Man and environment in the Palaeolithic. ERAUL, Liège, pp 197–207 Smith FH, Trinkaus E, Pettitt PB, Karavanic I, Paunovic M (1999) Direct radiocarbon dates from Vindija G1 and Velika Pecina late Pleistocene hominid remains. Proc Natl Acad Sci U S A 96:12281–12286 Smith FH, Hutchinson VT, Jankovic I (2012) Assimilation and modern human origins in the African peripheries. In: Reynolds SC, Gallagher A (eds) African genesis: perspectives on hominin evolution. Cambridge University Press, Cambridge, pp 365–393 Soficaru A, Dobos A, Trinkaus E (2006) Early modern humans from the Pestera Muierii, Baia de Fier, Romania. Proc Natl Acad Sci U S A 103:17196–17201 Stone T, Cupper ML (2003) Last glacial maximum ages for robust humans at Kow Swamp southern Australia. J Hum Evol 45:99–111 Stringer CB (1990) British Isles. In: Orban R (ed) Hominid remains: an up-date British Isles and Eastern Germany. Université Libre de Bruxelles, Bruxelles, pp 1–40 Stringer CB (1992) Replacement, continuity and the origin of Homo sapiens. In: Bräuer G, Smith FH (eds) Continuity or replacement-controversies in Homo sapiens evolution. AA Balkema, Rotterdam, pp 9–24 Stringer CB (1999) The origin of modern humans and their regional diversity. In: recent progress in the studies of the origins of the Japanese. News Lett 9:3–5 Stringer CB (2001a) Modern human origins: distinguishing the models. Afr Archaeol Rev 18:67–75 Stringer CB (2001b) The evolution of modern humans: where are we now? Gen Anthropol 7:1–5 Stringer CB (2002a) Modern human origins: progress and prospects. Philos Trans R Soc Lond B 357:563–579 Stringer CB (2002b) New perspectives on the Neanderthals. Evol Anthropol Suppl 1:58–59 Stringer C (2011) The origin of our species. Allen Lane, London Stringer C (2012) The status of Homo heidelbergensis (Schoetensack 1908). Evol Anthropol 21:101–107 Stringer CB, Bräuer G (1994) Methods, misreading, and bias. Am Anthropol 96:416–424 Svoboda JA, van der Plicht J, Kuzelka V (2002) Upper Paleolithic and Mesolithic human fossils from Moravia and Bohemia (Czech Republic): some new 14C dates. Antiquity 76:957–962

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Swisher CC, Rink WJ, Antón SC, Schwarcz HP, Curtis GH, Suprijo A, Widiasmoro (1996) Latest Homo erectus of Java: potential contemporaneity with Homo sapiens in Southeast Asia. Science 274:1870–1874 Tattersall I, Schwartz JH (1999) Hominids and hybrids: the place of Neandertals in human evolution. Proc Natl Acad Sci U S A 96:7117–7119 Tattersall I, Schwartz JH (2000) Extinct humans. Westview Press, Boulder Terberger T, Street M, Bräuer G (2001) Der menschliche Schädelrest aus der Elbe bei Hahnöfersand und seine Bedeutung f€ ur die Steinzeit Norddeutschlands. Archäolog Korrespondenzblatt 31:521–526 Teschler-Nicola M (ed) (2006) Early modern humans at the Moravian Gate. The Mladeč Caves and their remains. Springer, Wien Thorne AG (1993) Introduction. Session: the end of Eve? Fossil evidence from Africa. Am Assoc Adv Sci 21, Abstr:173 Thorne AG, Wolpoff MH (1981) Regional continuity in Australasian Pleistocene hominid evolution. Am J Phys Anthropol 55:337–349 Thorne AG, Wolpoff MH (2003) The multiregional evolution of humans. Sci Am Spec Ed New Look Human Evol 13:46–53 Thorne AG, Gr€ un R, Mortimer G, Spooner NA, Simpson JJ, McCulloch M, Taylor L, Curnoe D (1999) Australia’s oldest human remains: age of the Lake Mungo 3 skeleton. J Hum Evol 36:591–612 Trinkaus E (1981) Evolutionary continuity among archaic Homo sapiens. In: Ronen A (ed) The transition from lower to middle Paleolithic and the origin of modern man. University of Haifa, Haifa Trinkaus E (1988) The evolutionary origins of the Neandertals, or why were there Neandertals. In: Otte M (ed) L’ Homme de Neandertal, vol 3. L’ anatomie, Liège, pp 11–29 Trinkaus E, Moldovan O, Milota S, Bilgar A, Sarcina L, Athreya S, Bailey SE, Rodrigo R, Mircea G, Higham T, Bronk Ramsey C, van der Plicht J (2003) An early modern human from the PeÅŸtera cu Oase, Romania. Proc Natl Acad Sci U S A 100:11231–11236 Turbón D (2006) La evolución humana. Editorial Ariel, Barcelona Vallois HV (1954) Neanderthals and Praesapiens. J R Anthropol Inst 84:111–130 Weaver TD (2012) Did a discrete event 200,000–100,000 years ago produce modern humans? J Hum Evol 63:121–126 Webb S (1990) Cranial thickening in an Australian hominid as a possible paleoepidemiological indicator. Am J Phys Anthropol 82:403–411 Weidenreich F (1943) The skull of Sinanthropus pekinensis: a comparative study on a primitive hominid skull. Palaeontol Sin D 10:1–485 Weidenreich F (1947) The trend of human evolution. Evolution 1:221–236 White TD, Asfaw B, DeGusta D, Gilbert H, Richards GD, Suwa G, Howell FC (2003) Pleistocene Homo sapiens from Middle Awash, Ethiopia. Nature 423:742–747 Wild EM, Teschler-Nicola M, Kutschera W, Steier P, Trinkaus E, Wanek W (2005) Direct dating of early Upper Palaeolithic human remains from Mladeč. Nature 435:332–335 Wolpoff MH (1980) Paleoanthropology, 1st edn. Knopf, New York Wolpoff MH (1992) Theories of modern human origins. In: Bräuer G, Smith FH (eds) Continuity or replacement-controversies in Homo sapiens evolution. AA Balkema, Rotterdam, pp 25–63 Wolpoff MH (1999) Paleoanthropology, 2nd edn. McGraw-Hill, Boston Wolpoff MH (2009) How Neandertals inform human variation. Am J Phys Anthropol 139:91–102 Wolpoff MH, Thorne AG (1991) The case against Eve. New Sci 130:37–41 Page 27 of 29

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Wolpoff MH, Wu X, Thorne AG (1984) Modern Homo sapiens origins: a general theory of hominid evolution involving the fossil evidence from East Asia. In: Smith FH, Spencer F (eds) The origins of modern humans: a world survey of the fossil evidence. Alan R Liss, New York, pp 411–483 Wolpoff MH, Hawks J, Frayer DW, Hunley K (2001) Modern human ancestry at the peripheries: a test of the replacement theory. Science 291:293–297 Wolpoff MH, Mannheim B, Mann A, Hawks J, Caspari R, Rosenberg KR, Frayer DW, Gill GW, Clark GA (2004) Why not the Neandertals? World Archaeol 36:527–546 Wu X (1992) The origin and dispersal of anatomically modern humans in East Asia and Southeast Asia. In: Akazawa T, Aoki K, Kimura T (eds) The evolution and dispersal of modern humans in Asia. Hokusen-Sha, Tokyo, pp 373–378 Wu X (1998) Origin of modern humans of China viewed from cranio-dental characteristics of late Homo sapiens in China. Acta Anthropol Sin 17:276–284 Zilhão J, Trinkaus E (eds) (2002) Portrait of the artist as a child: the Gravettian human skeleton from the Abrigo do Lagar Velho and its archaeological context, vol 22, Trabalhos de Arqueologia. Instituto português de arqueologia, Lisboa

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Index Terms: African emergence 4 African fossil record 8 Anatomical modernization 5 Archaic Homo sapiens 6 Assimilation model 4 Australian aborigines 14 Chinese crania 16 Denisovans 16 European Neanderthal replacement 9 H-O foramen 13 Homo heidelbergensis 8 Hybridization and replacement model 3 Multiregional evolution model 2 Occipital bun 11 Out-of-Africa model 2 Presapiens hypothesis 1 Rhodesioids 2 Suprainiac fossa 12

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-5 # Springer-Verlag Berlin Heidelberg 2015

Origin of Modern Humans Prof. G€ unter Bräuer* Abteilung f€ ur Humanbiologie, Universität Hamburg, Hamburg, Germany

Abstract In the early 1980s, a new period in the debate on modern human origins began, focusing on two alternatives: the Multiregional Evolution model and the Out-of-Africa hypothesis. Over the last few decades, new hominin discoveries, absolute dating, and other evidence have supported the latter view, which proposes a recent common origin of modern humans in Africa. The increasing evidence made the idea of long-term regional evolution up to modern humans in Europe and Asia, following the first expansion out of Africa at nearly 2 Ma, more and more unlikely. Only the African fossil record documents a continuous early modernization process. In contrast, the European evidence shows a replacement of the Neanderthals by modern humans. Also, the claimed evidence for regional continuity in China and Australasia has turned out to be unsubstantiated. Major questions in the current discussion of modern human origins refer to the fossil and molecular evidence for gene flow during the replacement period and to the number of species involved in Middle Pleistocene evolution.

Early and Current Controversies The origin of modern humans has always been a controversial topic in paleoanthropology. Already at the beginning of the twentieth century and based on a very sparse – mainly European – fossil record, alternative phylogenetic scenarios were suggested. Schwalbe (1906) proposed a unilinear concept in which Neanderthals were an intermediate form between Dubois’ Pithecanthropus and modern humans. Boule (1913), on the other hand, saw the Neanderthals as an evolutionary cul-desac postulating a parallel “presapiens” lineage to modern humans. Although the Presapiens hypothesis became widely accepted in the subsequent decades, some researchers, especially Hrdlička (1927) and Weidenreich (1943), supported unilinear concepts. Weidenreich (1943), after examining the newly discovered Chinese and Javanese hominin fossils, proposed his Polycentric Evolution Theory, which suggested different evolutionary lines in North Asia, Southeast Asia/Australasia, Europe/Near East, and eastern/southern Africa. He regarded the regional sequences as an interconnected web evolving in a single common direction. Yet Weidenreich’s (1947) explanation of orthogenesis as the driving factor of such a polycentric evolution was rejected by the new synthetic theory of evolution. In addition, Coon’s (1962) later model of largely isolated parallel evolution in different parts of the world was eventually dismissed. In the 1950s, new support emerged for the Presapiens hypothesis, in particular by the cranial remains from Fontéchevade in connection with the specimens from Swanscombe and Steinheim (Vallois 1954). However, later research on the critical presapiens specimens revealed their affinities

*Email: [email protected] Page 1 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-5 # Springer-Verlag Berlin Heidelberg 2015

to Neanderthals and Preneanderthals (Trinkaus 1981; Hublin 1982). In addition, new hominid discoveries, such as the partial crania from Arago and Biache St. Vaast, demonstrated that the idea of a separate lineage to modern humans in Europe was no longer tenable. It became clear that there was only one lineage in Europe leading to Neanderthals (Bräuer 1984a). During the 1950s, another model was proposed (Howell 1951) – the Preneanderthal hypothesis – which assumed that the lineages to Neanderthals and modern humans only split during the Eem Interglacial. Following this event, the southwest Asian “progressive” Preneanderthals evolved into modern humans, while the European Preneanderthals developed into the robust “classic” Neanderthals. However, this concept was also not supported by later research. No diachronic trends of reduction in size could be observed in the Near Eastern Neanderthals, and later dating revision revealed that early modern humans and Neanderthals were nearly contemporaneous in this region. Thus, by the late 1970s, the question of the origin of modern humans was again largely open. A few researchers such as Wolpoff (1980) continued to favor evolutionary continuity in Europe and elsewhere, whereas others like Howells (1976) assumed a recent common origin of modern humans. In the early 1980s, a new period in the controversy on modern human origins began, mainly focusing on two alternatives: the Multiregional Evolution model and the Out-of-Africa hypothesis (Fig. 1). Wolpoff et al. (1984) proposed the Multiregional Evolution model, which was largely based on Weidenreich’s theory of Polycentric Evolution. In contrast to Weidenreich’s (1947) explanation of orthogenesis, the supporters of the new multiregional concept see a balance of evolutionary forces, such as gene flow, local selection, and drift, as explanations for the assumed long-term regional continuities (Wolpoff 1992). Yet they accepted and used most of Weidenreich’s morphological observations for regional continuity that had been collected in the 1930s and 1940s (Wolpoff et al. 1984; Frayer et al. 1993). Although assuming interregional gene flow, multiregionalists have emphasized the regional pattern of evolution as stated, for example, by Frayer et al. (1993, p. 41): “Each geographic region we examined contains a wealth of information that shows the continuous evolution of Homo populations over time. We find neither specimens nor traits that could reflect an infusion of any African genes and their so-called more-modern morphology.” Frayer (1992, p. 49) considered the “Neandertals as the probable ancestors of the people in the Upper Palaeolithic,” and Thorne (1993, p. 173) is convinced that the “descendants of the Java and Peking people do not become extinct but give rise, without African influence, to the modern people of their region.” The roots of the alternative Out-of-Africa model can be traced back to the early 1970s. Although at that time practically all evidence from archaeology and paleoanthropology pointed to the presence of archaic hominins – the so-called “Rhodesioids” (named after the Kabwe cranium from Zambia) – in eastern and southern Africa from only 30 or 40 Ka (Clark 1970), new skeletal remains from Omo Kibish, Ethiopia, and new dates for the South African Border Cave specimens indicated the early presence of modern humans at about 100 Kyr bp, or even slightly earlier (Leakey et al. 1969; Protsch 1975). Yet it remained puzzling how such early moderns fit in with the much later presence of the archaic humans. Further research on the dating of the African Stone Age during the 1970s led to a drastic extension in time of the Middle and Later Stone Age and thus to older dates of the associated hominins (Clark 1979). It also turned out that the archaic “Rhodesioids” were considerably older than had been thought. In the late 1970s, I started a new analysis of the Middle and Late Pleistocene hominin material from Africa. This research provided a new framework of Homo sapiens evolution, suggesting a mosaiclike, continuous anatomical process of modernization leading to an early emergence of modern humans. Based on this framework and a review of the fossil evidence from Europe and the Far East, I proposed an Out-of-Africa model initially dubbed the “Afro-European sapiens” hypothesis (Bräuer 1982) because the best evidence for replacement came from Europe. Yet the model was Page 2 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-5 # Springer-Verlag Berlin Heidelberg 2015

Fig. 1 (a). Multiregional evolution (After Thorne and Wolpoff 2003, p. 52) and (b) Out-of-Africa models

a global one, regarding replacement as the most likely process for the Far East as well (Bräuer 1984b). The Out-of-Africa model suggested an evolution to modern humans only in Africa and subsequent dispersals into Asia and Europe that replaced the resident archaic populations, including the Neanderthals. “Replacement” was assumed to also allow for interbreeding. In fact, a “Hybridization and Replacement model” was regarded to be in best agreement with the facts (Bräuer 1984b, p. 162). It could explain possible indications of regional archaic features among

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-5 # Springer-Verlag Berlin Heidelberg 2015

early modern humans, and it upheld the widely agreed upon view that the replaced archaic and the early modern humans belonged to the same species H. sapiens. A few years later, Cann et al. (1987) provided important support for a recent common origin of modern humans in Africa based on human mitochondrial DNA (mtDNA). Although no strongly divergent mtDNA lineages could be found among extant humans, Cann (1992, p. 71) did not assume reproductive isolation between the archaic and the dispersing modern populations, but rather concluded that we are about 30 Kyr too late to see the persistence of Neanderthal maternal lineages. These and additional results from molecular biology and paleoanthropology during the 1980s supporting a Recent African Origin (RAO – a term also used for Out-of-Africa) did not lead to the dismissal of the alternative Multiregional Evolution model, but instead to a heated debate and an artificial polarization. The multiregionalists now claimed that the mtDNA results must be interpreted as excluding any gene flow and that this is an essential assumption of the Out-of-Africa model (Wolpoff and Thorne 1991). Although this view was rejected (Bräuer 1989, 1992; Stringer 1992), the multiregionalists focused on the criticism of the extreme “Eve Theory,” assuming that by excluding gene flow, any possible indication of regional continuity outside Africa would be sufficient to disprove the Out-of-Africa model (Frayer et al. 1993). This argument, however, was misleading, as the “Eve” concept is based on a particular interpretation of the mtDNA data and cannot be equated with the Out-of-Africa model, which includes the evidence from fossils and nuclear DNA as well (Stringer and Bräuer 1994, p. 416). In fact, the Out-of-Africa replacement view allows for the possibility of gene flow between archaic and modern humans and is ready to accept any convincing evidence for it that might be found in the fossil record (Bräuer and Stringer 1997; Bräuer 2001a). Although subsequent research on the mtDNA did not provide any unequivocal evidence for interbreeding (Currat and Excoffier 2004), researchers like Serre and Pääbo (2006) were cautious and did not regard the extreme interpretation of complete replacement as proven. Only as recently as 2010 was the most relevant progress on the gene flow debate made. Sequencing of more than four billion nucleotides of the Neanderthal genome and comparisons to recent human genomes suggest that between 1 % and 4 % of the genomes of the people in Eurasia are derived from Neanderthals (Green et al. 2010, p. 721). Thus, not only fossil but also the molecular evidence supports such an “Out-of-Africa and hybridization” model (Stringer 2011), as was basically suggested about three decades ago (Bräuer 1984b, 2006; Stringer 2001a). Another view on modern human origins is the so-called Assimilation model first proposed by Smith et al. (1989) that long held an intermediate position between the Out-of-Africa and Multiregional Evolution models by strongly emphasizing regional continuity in Central Europe and other peripheries (Aiello 1993; Frayer et al. 1993). More recently, this view has leaned toward the Out-of-Africa model but still assumes a more significant assimilation of the Neanderthals (Churchill and Smith 2000) than does the “Out-of-Africa and hybridization” model (Bräuer and Broeg 1998; Bräuer 2006). Most recently, the Assimilation model is said to even agree with a level of only 1–4 % of non-African contribution to extant Eurasians (Smith et al. 2012, p. 386). This would in fact mean that this latest perspective is now hardly distinguishable from the Out-of-Africa and hybridization model (Stringer 2011; Gibbons 2011). In the following paragraphs, the origin of modern humans in Africa and the controversy on the evolutionary pattern in the other parts of the Old World will be considered.

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Fig. 2 Fossil record of Homo sapiens evolution in Africa

African Emergence of Modern Humans Over the last few decades, the evolutionary framework of anatomical modernization and the early appearance of modern humans in Africa as basically suggested in the early 1980s (Bräuer 1984c) have gained increasing support (Klein 1999, 2009; Bräuer 2001b, 2012; Smith 2002; Stringer 2002a; Mbua and Bräuer 2012). Absolute dating evidence for several hominin specimens contributed to the current chronological framework of the process (Clark et al. 1994; Gr€ un et al. 1996; Bräuer et al. 1997; McDougall et al. 2005; Brown et al. 2012). The evolutionary scheme presented here (Fig. 2) is based on quite a number of diagnostic as well as absolutely dated specimens that support a mosaiclike, continuously evolving lineage from archaic to modern humans. In spite of broad agreement on the African sequence (Klein 1999, 2009), there is some controversy on whether

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-5 # Springer-Verlag Berlin Heidelberg 2015

the different evolutionary groups or morphs should be distinguished on the species or, as suggested here, on the intraspecific level (Bräuer 2008). The anatomical modernization process can be divided into three groups or grades of H. sapiens, each of which includes hominin specimens of a similar evolutionary level (Bräuer 1989, 2008, 2012). The specimens grouped within the early archaic H. sapiens category are derived relative to H. erectus, especially regarding their enlarged cranial capacity, more vertically oriented lateral walls, expanded frontal bone, less strongly angulated occipital bone, more vertically oriented upper scale of the occipital, higher temporal squama, and reduced development of the supraorbital and occipital tori. The late archaic H. sapiens is clearly more derived compared to the morphological pattern of the early archaics, especially evident in the large cranial capacity, the more reduced supraorbital torus, and the near-modern or modern face, including the canine fossa and inframalar incurvature. This grade of evolution is followed by anatomically modern H. sapiens with a fully modern morphology of vault and face. There is obvious continuity between the grades, which are best seen as a way of describing the levels of the modernization process. In this respect, the late archaics have also been designated as the transitional group (Smith 2002). This approach suggests neither anything about the underlying factors of anatomical modernization nor whether there are parts of the lineage that show more relevant changes toward the modern morphology than others. Thus, the identification of major structural elements in this process, such as neurocranial globularity and facial retraction (Lieberman et al. 2002), is relevant. Indeed, many of the features and aspects characterizing the grades are connected with such general changes (Mbua and Bräuer 2012). A key specimen of early archaic H. sapiens is the Bodo hominin from Ethiopia, dated by Ar/Ar to ca. 600 Kyr bp (Clark et al. 1994). The large cranial capacity of nearly 1,300 cm3 is associated with some parietal bossing, a coronally expanded frontal, and derived features of the temporal. The supraorbital torus even shows some division into a medial and lateral portion (see also volume 3, chapter “▶ Later Middle Pleistocene Homo”). In the still massive face, there are several characteristics shared with modern humans (Rightmire 1996). Another specimen of similar or slightly younger age (Klein 2009) is the Saldanha (or Elandsfontein) cranium from South Africa. Having an estimated cranial capacity of around 1,225 cm3, the parietals are well arched and show some bossing. Also, the frontal squama is coronally enlarged and the supraorbital torus attenuates laterally. The occipital is less angulated than generally seen in H. erectus and the transverse torus is reduced. The other well-preserved early archaic specimens, such as the crania from Kabwe, Zambia; Eyasi and Ndutu, Tanzania; and Salé, Morocco, date from the same time period between 600 and 300 Ka and exhibit similar derived sapiens-like conditions in spite of obvious individual variation (Bräuer 2008, 2012; Mbua and Bräuer 2012). The late archaic transitional group also comprises specimens spreading from northern to southern Africa. A good example of these near-moderns is the cranium KNM-ER 3884 from Ileret, East Turkana (Fig. 3) directly dated by U/Th gamma-ray spectrometry to ca. 270 Kyr bp (Bräuer et al. 1997). A previous analysis showed that most of the cranial vault falls close to the range of Holocene Africans (Bräuer et al. 1992a). However, the cranium also exhibits a continuous but moderately developed supraorbital torus that deviates from the generally rather modern impression of the specimen (Bräuer 2001b; Schwartz and Tattersall 2003). Further support for such an early presence of near-modern late archaics came from absolute dates for the Florisbad hominid from South Africa and for the Laetoli Hominid 18 from the Ngaloba Beds in Northern Tanzania (Manega 1995; Gr€ un et al. 1996). The Florisbad specimen directly dated by ESR to ca. 260 Kyr bp has a coronally greatly expanded frontal bone associated with a continuous but only slightly projecting supraorbital torus and a modern facial shape with a well-developed canine fossa. The LH 18 cranium, with an age of more than 200 up to 300 Kyr, exhibits a modern-looking face with a canine fossa and Page 6 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-5 # Springer-Verlag Berlin Heidelberg 2015

Fig. 3 Late archaic and early modern Homo sapiens: (a) KNM-ER 3884, Ileret; (b) Omo Kibish 2; (c) Omo Kibish 1; (d) BOU VP-16/1, Herto (After White et al. 2003, p. 734)

a near-modern braincase with a capacity of about 1,350 cm3, a more or less rounded occipital bone, and well-developed parietal bossing. Archaic features mainly include the flat and narrow frontal squama and the supraorbital torus (Bräuer 1989). However, the relatively thick torus shows an incipient division in the midorbital region, which might be a tendency toward the fully modern pattern. Based on its combination of ancestral and derived conditions, the cranium from Eliye Springs, West Lake Turkana, might also belong to this grade (Bräuer and Leakey 1986; Bräuer et al. 2004a). Important late archaic crania also come from Jebel Irhoud, Morocco, dated to about 170 Kyr bp (Gr€ un and Stringer 1991; Hublin 1992; Bräuer 2012). The mosaic-like transition from late archaic to early anatomically modern H. sapiens is also obvious in the available specimens from Ethiopia such as the Omo Kibish remains (Fig. 3). Recent fieldwork at the sites and Ar/Ar dating has suggested that both the Omo 1 skeleton and the Omo 2 cranium date to 195
5 Kyr bp (McDougall et al. 2005; Brown et al. 2012). Whereas the Omo 1 specimen is by most accounts fully anatomically modern and according to the new dating evidence the oldest known modern human, the Omo 2 cranium shows a mosaic of modern and archaic features. It exhibits a robust yet basically modern supraorbital morphology along with strong midsagittal keeling and an angulated occipital bone. Recently discovered cranial remains from Herto in the Middle Awash, Ethiopia, dated by Ar/Ar to ca. 154 – 160 Kyr bp, further illustrate this transitional process (White et al. 2003). The large robust Herto cranium BOU VP-16/1 (Fig. 3) apparently exhibits a modern supraorbital morphology and modern face combined with a rather angulated occipital bone similar to the condition seen in Omo 2. The variability of this occipital trait, however, is evident in the less angled condition of the more fragmentary adult specimen BOU VP-16/2 (White et al. 2003). With an age of around 150 Kyr bp, the Singa cranium from Sudan also belongs to this earliest modern human spectrum (Bräuer 2012). More early moderns come from South Africa, especially from the Klasies River Mouth Caves. Here, the oldest human remains date to ca. 120 Kyr bp. These maxillary fragments fall within the range of variation of Holocene Africans (Bräuer et al. 1992b). A nearly complete mandible with an Page 7 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-5 # Springer-Verlag Berlin Heidelberg 2015

age of about 100 Kyr is anatomically modern, as are the other slightly more recent cranial fragments from the site (Bräuer 2001b, 2008). Regarding the postcranial specimens, the conditions seen in the Klasies remains can be matched with recent population samples from southern Africa (Rightmire and Deacon 1991; Churchill et al. 1996). Some features, such as the relatively low coronoid height of the ulna, could be retained archaic features reflecting the mosaic pattern of evolution in the postcranial skeleton (Churchill et al. 1996). But it is also possible that such postcranial conditions simply belong to the range of variation of these early modern humans (Pearson 2000). Another early modern specimen from South Africa is the Border Cave 1 partial cranium, which is about 90 Kyr old or perhaps somewhat older (Gr€ un and Beaumont 2001). Considering the complete evidence from the fossil record, of which I can discuss only a few specimens here in some detail, it is obvious that there is good documentation of the modernization process in Africa. This process recently gained further support from a new analysis of the Middle Pleistocene hominins showing clear trends from early archaic up to modern H. sapiens in many metrical and nonmetrical cranial features (Mbua and Bräuer 2012). The current fossil record of the African Middle Pleistocene allows subdivision into the three suggested groups, regardless of whether they are termed “grades” of an evolving species H. sapiens or different “morphs.” Foley (2001), however, distinguishes these groups on the species level, as H. heidelbergensis, H. helmei, and H. sapiens. Yet he concedes that the derived descendant taxa of H. heidelbergensis are problematic because of the continuity that can be found between them and their presumed ancestor: These seem to be species in the sense that Simpson meant – lineages with independent trajectories – but both the details of the fossil record and the scale of the process seem to rule out any punctuated events. Indeed, continuity between them, rather than discontinuity, is the reason for the persistent problem of delimiting the taxonomic units in the later stages of human evolution and gives rise to the question of whether the species concept, which lies at the heart of macroevolutionary theory, is sufficiently fine-tuned to cope with evolution at this scale. (Foley 2001, pp. 9–10)

However, problems already exist with regard to H. heidelbergensis. Shortly after Adefris (1992) classified the Bodo cranium as “archaic Homo sapiens” based on a detailed study, Rightmire (1996) considered it more reasonable to refer to Bodo as a H. heidelbergensis. Rightmire (1998) suggested speciation between H. erectus and H. heidelbergensis in Africa at around 800 – 700 Ka, instead of a speciation between H. erectus and (archaic) H. sapiens (Bräuer 2001b). While this difference appears to mainly involve names, especially since Rightmire also favors a single polytypic species H. erectus in Asia and Africa, his scheme also suggests two further speciations: one in Europe from H. heidelbergensis to H. neanderthalensis at ca. 300 Ka and another in Africa from H. heidelbergensis to H. sapiens at ca. 150 Ka. However, due to the mosaic nature of the accretion process in Europe, it is hardly possible to define any clear divisions along the Preneanderthal/ Neanderthal lineage (Hublin 1998, p. 302; Klein 2009). Thus, there appears to be little convincing evidence for such a speciation within the European record. In Africa, there is a similar process with regard to the mosaiclike modernization, which also does not justify any subdivisions at the species level (Smith 2002; Turbón 2006; Bräuer 2008). I think it is more likely that we are dealing with one evolving biological species and several subspecies (Jolly 2003). Further splitting of the African sequence as suggested by Foley and Lahr (1997) into three species (H. heidelbergensis, H. helmei, and H. sapiens), which largely include the same African specimens as the three proposed grades, can only mean that these are artificially defined morphs or paleospecies. Yet it is problematic that Foley and Lahr (1997) also included European fossils in H. helmei, as outlined by Stringer (2002a, p. 567). First, Neanderthal characteristics were already evolving in Europe prior to the hypothesized appearance of “H. helmei,” e.g., in the Swanscombe specimen, dated to ca. 400 Kyr bp. Second, African specimens such as Florisbad and Jebel Irhoud make unparsimonious ancestors for the Page 8 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-5 # Springer-Verlag Berlin Heidelberg 2015

Neanderthals, since not only do they post-date the appearance of Neanderthal clade characters in Europe, but they appear to lack Neanderthal morphological characteristics that might be expected in a common ancestor. Recently, Weaver (2012) demonstrated that models based on theory of population and quantitative genetics are well in agreement with a lengthy process of modern human origins that lasted from the divergence of the modern human and Neanderthal evolutionary lineages more than 400 Ka to the expansion of modern humans out of Africa, without speciation events. In spite of the current discussion on the number of taxa involved (Bräuer 2008, 2012), there is nearly general agreement on a post-erectus evolutionary process in Africa leading to an early origin of modern humans during the late Middle Pleistocene. This is in agreement with the fact that in the Near East, anatomically modern humans appeared as early as about 100–130 Ka. These early moderns from Skhūl and Qafzeh might not only have an African origin but may also represent the oldest, well-documented evidence of modern humans outside of Africa. Interestingly, and not yet fully understood, these moderns might have coexisted in the Near East with Neanderthals for some tens of thousands of years until the latter disappeared at around 45 Ka. According to both morphological and the recent molecular evidence, gene flow occurred during this period of coexistence (Bräuer and Rimbach 1990; Green et al. 2010).

Replacement of European Neanderthals Largely parallel to the anatomical modernization process in Africa, the evolution of the Neanderthals took place in Europe. It is widely agreed that the development of the Neanderthal morphology mainly resulted from an accretion process, which began about 400–530 Ka (Hublin 1998; Bischoff et al. 2003; Stringer 2012). Studies on whole Neanderthal mtDNA genomes support such a long, separate evolution in Africa and Europe (Briggs et al. 2009; Endicott et al. 2010). Recent estimations of the human-chimpanzee split using generation times in great apes could also point to a somewhat earlier population split between Neanderthals and modern humans (Langergraber et al. 2012). This does not necessarily indicate that two different biological species originated since the taxonomic significance of the genetic differences is ambiguous (Hublin 1998; Jolly 2003), and as Hofreiter (2011, p. 7) put it: “. . ., given that humans and Neanderthals are large-bodied mammals with long generation times, the recent divergence time of humans and Neanderthals argues against specieslevel distinction.” In view of the increasing evidence for widespread interbreeding between modern and different archaic humans (see below), Stringer (2011, p. 261, 2012) also pointed to the possibility of abandoning the different species names and lumping all these post-erectus fossils together as H. sapiens. So, whether one prefers to regard the Neanderthals as a subspecies of H. sapiens (Turbón 2006; Bräuer 2008) or as a different species or paleospecies (Tattersall and Schwartz 2000; Harvati 2003), the Neanderthals were clearly very closely related to us (Stringer 2001b). Of special relevance in this respect is also the research on possible Neanderthal-modern differences in life history. Current evidence, however, points to great overlap between dental development in Neanderthals and modern populations from different regions of the world and to great difficulties in gauging Neanderthal life histories from dental growth (Guatelli-Steinberg 2009). Nevertheless, the long, separate evolution of the Neanderthals led to an accumulation of a large number of derived features in the skull and postcranial skeleton that are either unique or most frequent in this group (Trinkaus 1988; Hublin 1998). In spite of the numerous differences between the Neanderthal morphology and that of early modern Europeans, multiregionalists have long regarded Central Europe as a possible region of Page 9 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-5 # Springer-Verlag Berlin Heidelberg 2015

evolutionary change from Neanderthals to modern humans (Smith 1982; Frayer et al. 1993). In particular, the Neanderthal remains from Vindija, Croatia, were considered to demonstrate evolutionary continuity to early modern humans of the region, as, e.g., from Velika Pećina. However, direct AMS radiocarbon dating has shown that the frontal fragment from Velika Pećina once regarded to be ca. 34 Kyr old is only 5 Kyr old (Smith et al. 1999) and the most recent Vindija Neanderthal sample (G1) has an age of ca. 32 Kyr bp, based on a new ultrafiltration technique for bone radiocarbon samples (Higham et al. 2006). AMS dating has led to further drastic revisions regarding some presumably early modern Europeans. The frontal bone from Hahnöfersand near Hamburg, which was dated to ca. 36 Kyr bp (Berger and Protsch 1989, p. 64), has been redated to only 7,500 years bp (Terberger et al. 2001). For the fragmentary crania from Zlatý Kůn and Svitávka, Czech Republic, for which ages of at least 30 Kyr were suggested, new dates of 12,870 and 1,180 years bp, respectively, were obtained (Svoboda et al. 2002). Also, the human remains from the Vogelherd Cave in southwestern Germany, which have long been thought to derive from Aurignacian deposits, turned out to be only 5 Kyr old (Conard et al. 2004). In spite of the exclusion of several presumably early modern Europeans, there are still a number of specimens that date to more than 30,000 and even somewhat more than 40,000 radiocarbon years bp (Mellars 2011). Among these are the remains from Mladeč, Czech Republic, for which direct AMS dating on several specimens provided ages of about 31 Kyr bp, i.e., 36 Kyr bp based on new calibration curves, which are in agreement with the Aurignacian artifacts as well as previous AMS dates for associated calcite deposits (Svoboda et al. 2002; Wild et al. 2005; Higham et al. 2011). Further early modern cranial and mandibular remains have recently been discovered in the Pes‚ tera cu Oase, Romania, for which direct AMS dating of a mandible yielded ages of 34–36 Kyr bp (Trinkaus et al. 2003) and recent redating using the ultrafiltration technique resulted in a calibrated date of ca. 40 Kyr bp (Higham et al. 2011). Ultrafiltrated collagen radiocarbon dating on animal bones associated with the presumably modern maxillary fragment Kent’s Cavern 4 from England has even suggested calibrated dates between 42 and 44 Kyr bp (Higham et al. 2011; Stringer 1990). In spite of the recent use of the improved cleaning techniques of bone collagen to reduce contaminations, there is still good evidence for several thousand years of Neanderthal-modern coexistence. The question of a Neanderthal contribution to the early modern European gene pool has been strongly debated between supporters of the Multiregional Evolution, Assimilation, and Out-ofAfrica models for many years. Based on the current dates, the Mladeč remains represent the best preserved early modern material from the time at which Neanderthals were still around in Central Europe (Teschler-Nicola 2006). Thus, it is key material for examining the question of Neanderthal-modern gene flow. Multiregionalists have long used the Mladeč material to demonstrate regional evolution. Frayer (1986, p. 254) saw here “good evidence in support of a gradualist model,” and Wolpoff (1999, pp. 762–763) described the Mladeč specimens 4, 5, and 6 as Neanderthal-like. In testing the similarities of Mladeč 5 and 6 to their potential ancestors – European Neanderthals and early moderns from Skhūl/Qafzeh – Wolpoff et al. (2001, p. 293; Wolpoff 2009) even found a predominance of Neanderthal resemblances for several sets of variables, which are said to separate the Neanderthal and Skhūl/Qafzeh samples. In order to determine the hard evidence for the Neanderthal contribution to these early moderns, analyses of the Mladeč material were carried out (Bräuer and Broeg 1998; Bräuer 2006; Bräuer et al. 2006). These studies included the most relevant and well-preserved crania, the females Mladeč 1 and 2 and the males Mladeč 5 and 6 (Fig. 4) as well as the maxilla fragment, Mladeč 8. A set of nonmetrical Neanderthal features was used as well as measurements of the frontal shape and facial morphology and projection. The results were rather unexpected. Regarding the common Page 10 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-5 # Springer-Verlag Berlin Heidelberg 2015

Fig. 4 Early modern crania from Czech Republic: (a) Mladeč 1; (b) Mladeč 2; (c) Mladeč 5; (d) Mladeč 6 (Photos c, d: H. Broeg)

nonmetrical Neanderthal features studied, not a single condition could be found in the Mladeč specimens that can be said to have been unequivocally derived from Neanderthals. On the contrary, the respective regions, such as the supraorbitals, the shape of the vault, the face, the occipital, and mastoid regions, are all anatomically modern and do not exhibit any derived Neanderthal morphology. Also, the metrical analysis revealed great deviations in the frontal curvature of the Mladeč specimens from both European and Near Eastern Neanderthals. Among the Upper Paleolithic sample (n ¼ 18), Mladeč 1 and 5 show the greatest divergence from Neanderthals (n ¼ 10). No indication of a midfacial projection could be found in these early Czech specimens. Mladeč 1, 2, and 5 diverge strongly from Neanderthals with regard to their Nasofrontal Angle (NFA), and Mladeč 1, the only specimen for which the Zygomaxillary Angle (SSA) could be determined, shows a large disparity when compared to the Neanderthal range of variation. Major reasons for these contradictory results lie in the assessment as well as the selection of the features. For example, one of the commonly used features is the “occipital bun” (chignon), which exhibits a derived morphology in Neanderthals. In early modern Europeans, the occipital projections are not only placed “in the context of a rather different cranial shape” compared to that of Neanderthals (Churchill and Smith 2000, p. 97), but they also differ in a number of special details such as the extent of lambdoidal flattening, the angulation between the nuchal and occipital planes, and the height of the vertical face of the posterior occiput (Caspari 1991). These differences led Smith (1982) to suggest the term “hemibun” for the occipital projections in Upper Paleolithic specimens. Lieberman et al. (2000, p. 291) even raised the possibility that the specialized Neanderthal bun and the projections in early modern Europeans may not be homologous. In addition, these more moderate projections are rather variable and occur practically all over the world as, e.g., in Africa or East Asia (Bräuer and Broeg 1998; Wu 1998, p. 282). Thus, to label as an “occipital bun” anything different from the derived and well-defined Neanderthal bun leads to confusion, as can be well demonstrated in the case of the Mladeč specimens. Wolpoff (1999, p. 762) classifies the occipital projections in Mladeč 5 and 6 as a “Neanderthallike occipital bun,” a view shared by Frayer (1992, p. 21). However, the midsagittal curvatures of

Page 11 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-5 # Springer-Verlag Berlin Heidelberg 2015

Mladeč 5 and La Chapelle-aux-Saints are in fact more different than those of, e.g., Mladeč 5 and late Middle Pleistocene archaic H. sapiens specimens like Jebel Irhoud 1 or Laetoli H18 (Bräuer and Broeg 1998; Bräuer 2006). Smith et al. (1995, p. 201) had also emphasized that “the occipital buns in Jebel Irhoud are more similar to those in early modern Europeans (like Mladeč, Zlatý Kůn, or Predmosti) than to Neanderthals because of the greater similarity in posterior cranial vault morphology between them.” Thus, there should be little reason to suggest that the more African-like hemibuns in Mladeč were derived from European Neanderthals. However, Frayer (1992, p. 21) argued that the morphology in the early modern Europeans must have derived from Neanderthals because occipital buns are not present in the Near Eastern early moderns. Yet, in regard to the bunning in Jebel Irhoud and other circum-Mediterranean specimens, Wolpoff (1999, p. 613) considers the bunning similar to Skhūl/Qafzeh. And indeed, comparisons of the midsagittal curvatures demonstrate close similarities between the occipital profiles of Qafzeh 6 and those of all three Mladeč crania in which the occipital is preserved (Bräuer 2006). Thus, the predominant multiregionalist assessment of the bun morphology in Neanderthals and Mladeč as present and in Skhūl/Qafzeh as absent is inaccurate. Another example of problematic assessment concerns the “suprainiac fossa,” which also has a clearly defined morphology in Neanderthals. It is a generally large, wide resorptive depression which is either rectangular or triangular in shape with a horizontal base formed by the transverse occipital torus (Nara 1994; Hublin 1998). Yet, as Caspari (1991, p. 184) pointed out, “it is unclear if all resorptive pitting in this area that could be referred to as fossae (or incipient fossae) can be validly compared with the Neandertal condition. Perhaps only the Neandertal pattern should be considered true suprainiac fossae, or alternatively some intermediate forms might also be considered suprainiac fossae.” Quite obviously, not all pitting in this region can be regarded as a Neanderthal suprainiac fossa. Smaller or larger resorptive depressions that do not match the Neanderthal condition can be found in modern humans nearly everywhere in the world. They are frequently present, e.g., in terminal Pleistocene material from North Africa and occur in recent crania from New Guinea (Bräuer and Broeg 1998). These depressions normally have an inverted triangular shape with the apex pointing to the nuchal plane. Mladeč 5 shows such a small pitting, which can hardly be regarded as Neanderthal suprainiac fossa, and also Mladeč 6 exhibits a tiny non-Neanderthal-like depression. This had also been contended by Frayer (1986, p. 251), when he concluded that “neither Mladeč 6 nor 5 have a distinct suprainiac fossa.” However, later Caspari (1991) felt that there was a suprainiac fossa in Mladeč 6, and Frayer (1992, p. 22), although emphasizing the differences between the Neanderthal and Upper Paleolithic conditions, recognized the structure in Mladeč 6 as a possible exception. This example also highlights the problematic use of character states in order to support the idea of continuity. Wolpoff et al.’s (2001) finding of a great number of Neanderthal resemblances in two of the Mladeč specimens – which he recently repeated in more detail (Wolpoff 2009) – is largely based on features which are problematic with regard to both their assessment and phylogenetic relevance. Many of the nonmetrical features used are, in fact, metrical traits that were arbitrarily divided into two alternative conditions without any recognizable justification such as thick parietal at asterion (>9 mm), broad frontal (>125 mm), long frontal (glabella-bregma length >113 mm), or long occipital plane (>60 mm). With regard to other features used, it is unclear how they can be properly scored as present or absent without a clear scoring system. Among these are as follows: mastoidsupramastoid crests well separated, frontonasal suture arched, glabellar depression, glenoid articular surface flattened, and paramastoid crest prominent. In addition, many of the features used can hardly be regarded as distinguishing between Neanderthals and modern humans. Thus, it is not surprising that Wolpoff et al. (2001) found the most divergent numbers of differences between Mladeč 5 and Page 12 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-5 # Springer-Verlag Berlin Heidelberg 2015

two closely related early modern specimens from Skhūl, i.e., only 8 differences to Skhūl 4, but 23 to Skhūl 5. Yet there are further problems with this study, such as the morphological representativeness of using only the male specimens, the lack of relevant features, and the inappropriate method of pairwise difference analysis (Collard and Franchino 2002; Bräuer et al. 2004b). Thus, critical reexamination of the claimed evidence for a considerable Neanderthal contribution in the Mladeč material cannot be supported. Another early modern specimen claimed to show evidence for gene flow from Neanderthals is the mandible from Pes‚ tera cu Oase. However, according to Trinkaus et al. (2003, p. 11235), “the only feature that suggests Neandertal affinities is the lingual bridging of the mandibular foramen, a feature that is currently unknown among humans preceding Oase 1 other than the late Middle and Late Pleistocene members of the Neandertal lineage.” Yet how reliable is this so-called H-O foramen for demonstrating Neanderthal-modern gene flow? As Smith (1978, p. 327) found, there are neither individuals under 18 years of age from any modern sample examined nor any juvenile Neanderthal exhibiting the H-O type. This makes it likely that, as Smith (1978) mentioned, factors developing during the individual’s lifetime could also be responsible for the occurrence of the trait. Since the morphology at the mandibular foramen can change during a lifetime, the feature cannot be regarded as a good genetic trait (Lieberman 1995, p. 175). Moreover, its occurrence does not clearly signal continuity. According to Frayer (1992, p. 31), the H-O type appears in 10 out of 19 Neanderthals (52.6 %), in 4 out of 22 early Upper Paleolithic specimens (18.2 %), and in 2 out of 30 late Upper Paleolithic specimens (6.7 %). The four early Upper Paleolithic specimens, however, include the Neanderthal Vindija 207 and Stetten (Vogelherd) 1, which no longer belong to this group. Thus, there is no relevant occurrence of this feature in the early Upper Paleolithic. Moreover, most important in this respect is a study of terminal Pleistocene North African samples. Groves and Thorne (1999, p. 253) found the bilateral H-O foramen in 22.2 % of the Nubian material from Tushka and Jebel Sahaba, further showing that this trait is not necessarily derived from Neanderthals. Finally, the H-O foramen already occurred outside of Europe in H. erectus such as in OH 22 and Zhoukoudian H1. Thus, though it cannot be excluded, it is far from clear that this single possible Neanderthal trait present on one ramus of the Oase mandible really indicates gene flow from Neanderthals. There is also no unequivocal evidence for a Neanderthal contribution in the adolescent cranium Oase 2 that might be contemporaneous with the mandible. This specimen exhibits a whole set of derived modern features in the vault and face, combined with M3s that are unusually large and have a complex cusp pattern (Rougier et al. 2007). Specimens from two further Romanian sites have also been regarded as relevant to the gene flow debate. The mandible from the Pes‚ tera Muierii with an ultrafiltrated and calibrated AMS date of 34 Kyr bp (Higham et al. 2011) exhibits an asymmetrical mandibular notch which occurs most frequently in Neanderthals (Rak 1998; Soficaru et al. 2006). Yet it is also found in modern and recent humans as, e.g., in the Holocene Vogelherd mandible and shows great individual variability. Nevertheless, a possible indication to Neanderthal gene flow cannot be excluded here. This, however, appears less likely, regarding the nuchal morphology of the slightly younger calvaria from Cioclovina. Rather, this specimen shows a robust modern morphology and no typical Neanderthal suprainiac fossa (Bräuer 2010). Finally, the juvenile Gravettian skeleton from Lagar Velho, Portugal, has been suggested to exhibit aspects indicating Neanderthal ancestry (Zilhão and Trinkaus 2002). Yet the major feature that has been suggested to show a Neanderthal-like condition – the relatively short lower legs – is not unequivocal. It cannot be excluded that the condition also reflects some adaptation among these early modern populations to cold conditions before the Last Glacial Maximum (Stringer 2002b) or individual variation within this modern population (Tattersall and Schwartz 1999). In addition, the occurrence of Harris lines points to periods of disease or malnutrition. Moreover, if one takes the Page 13 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-5 # Springer-Verlag Berlin Heidelberg 2015

estimated adult crural index for Lagar Velho of 80.7 % and the 95 % confidence intervals (77.5–83.9) as provided by Ruff et al. (2002, p. 380), there appears to be considerable overlap with early Upper Paleolithic Europeans as well. No matter whether some Neanderthal genes were involved in the specimens discussed here or not, it is difficult to escape the conclusion that the hard evidence points to only small traces of interbreeding between Neanderthals and modern humans. A Neanderthal contribution to early modern Europeans of up to 50 % as assumed by Wolpoff et al. (2004) has no support. Thus, a replacement process accompanied by a small amount of gene flow as suggested by the Out-of-Africa and hybridization model appears to be in good agreement with the current evidence from Europe (Bräuer 2010; Stringer 2011).

Continuity or Discontinuity in the Far East The assumption of regional evolution in China and Australasia is mainly based on morphological features or sets of features. Weidenreich (1943) published a list of 12 so-called Mongolian traits that he regarded as clear evidence for a close relationship between Chinese H. erectus and living north Chinese. Among these are midsagittal crest and parasagittal depression, metopic suture, Inca bone, certain “Mongolian” features of the nasal bridge and cheek region of the maxilla and zygomatic bone, shovel-shaped upper lateral incisors, and horizontal course of the nasofrontal and frontomaxillary sutures. Coon (1962, p. 458) was also convinced that many common features existed between Peking Man and living northeast Asians. Finally, the multiregionalists, as well, see strong support for their model in North Asia. Accepting most of the features suggested by Weidenreich and some other authors, multiregionalists presented a rather long list of assumed regional Chinese traits (Wolpoff et al. 1984; Pope 1992; Wu 1992). Although some features are said to have changed over time, Wolpoff et al. (1984, p. 435) were convinced that “all of these characteristics have much lower frequencies and are distributed discontinuously in regions other than China.” Weidenreich (1943) also saw an evolutionary line leading from Pithecanthropus via H. soloensis to the Australian aborigines of today. Some years before, Keith (1936) had already regarded the recently discovered Solo hominins as representing the evolutionary stage linking Pithecanthropus to the Australian aborigine. Wolpoff et al. (1984, pp. 443–444) mentioned about 20 continuity features of the cranium, including flatness of the frontal in sagittal plane, distinct prebregmatic eminence, marked prognathism, persistence of the zygomaxillary ridge, eversion of the lower border of the malar, rounding of the inferolateral border of the orbit, prelambdoidal depressions, and lambdoidal protuberance. Most of the features are from Weidenreich (1943), Larnach and Macintosh (1974), and Thorne and Wolpoff (1981). Based on these assumed regional features, multiregionalists are convinced that Australasia shows a clear anatomical sequence between the earliest Indonesian H. erectus and the recent and living Australians uninterrupted by African migrants at any time (Frayer et al. 1993, p. 21). Since many of the regional features for the Far East were suggested in the first half of the twentieth century, reexaminations have been carried out by several authors over the last two decades. With regard to the suggested East Asian traits, Groves (1989, p. 279) arrived at the conclusion that there is “little evidence for special likeness of modern ‘Mongoloids’ to Homo erectus pekinensis” and identified many of the features as primitive retentions also found outside the region. According to Habgood (1992, p. 280) “none of the proposed ‘regional features’ can be said to be documenting ‘regional continuity’ in east Asia as they are commonly found on modern crania from outside of this region . . ., and are consistently found on archaic Homo sapiens and/or Homo erectus crania Page 14 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-5 # Springer-Verlag Berlin Heidelberg 2015

Fig. 5 Archaic and early modern crania from China: (a) Dali; (b) Liujiang

throughout the Old World.” In her analysis of 11 proposed East Asian continuity features, Lahr (1994) found that almost all of them occurred more frequently in recent samples from other parts of the world. Facial flatness was found to be most pronounced in final Pleistocene populations from Northern Africa. A later detailed study by Koesbardiati (2000) focused on the middle and upper facial regions especially regarded as showing a great number of East Asian continuity features (Pope 1992; Frayer et al. 1993). The results, however, revealed that no variable showed a distribution as would be predicted by the Multiregional Evolution model. Instead, most of the features occur more frequently or are more pronounced among population samples from Africa, Europe, and Australia than in the Chinese sample. Some of the features show the highest frequencies among the Inuit of Greenland who, however, represent a relatively young population showing adaptations to extreme conditions (Howells 1993; Lahr 1995). Also, the fossil record from China hardly supports regional continuity from H. erectus to modern people of the area. Even the problematic continuity features are lacking in archaic H. sapiens specimens. For example, the 200 Kyr old cranium from Jinniushan does not exhibit any of the following: midfacial flatness, a marked angulation of the maxilla and zygomatic bones when viewed from beneath, a flattened nasal saddle, a nondepressed nasal root, or lack of wisdom teeth. Based on further features, even Pope (1992) has raised doubts whether this hominin along with the Maba specimen fits into the picture of regional evolution in China and suggested strong genetic influence from the West into China in the terminal Middle or Late Pleistocene. Moreover, the 150–200 Kyr old cranium from Dali (Fig. 5) with its heavy supraorbital torus and other archaic features hardly reveals clear similarities to modern Chinese. Because of the discontinuity between Chinese H. erectus and this East Asian archaic H. sapiens group and the similarities of the latter to archaic H. sapiens from Europe, it has been suggested that the Dali-Maba-Jinniushan morph has its roots in the archaic Page 15 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-5 # Springer-Verlag Berlin Heidelberg 2015

sapiens of the western part of the Old World. Recent sequencing of the genome of a 40 Kyr old finger bone from the Denisova Cave in the Altai Mountains, southern Siberia, identified a new archaic hominin group that shared some of its history with Neanderthals and might have split from the common Preneanderthal lineage some 200–300 Ka (Reich et al. 2010). Moreover, it has been shown that these so-called Denisovans interbred with the modern ancestors of present-day Melanesians and Australians, most likely in Southeast Asia. These populations exhibit about 5 % of Denisovan DNA (Reich et al. 2010, 2011). Perhaps – but this is still a hypothesis – the Dali-Maba-Jinniushan group could belong to this archaic Denisovan lineage that lived in wide parts of East Asia. Further relevant evidence contradicting the idea of regional evolution in China comes from the earliest modern humans of the area. For a long time, the specimens from the Upper Cave at Zhoukoudian and from Liujiang in southern China were regarded to be among the earliest moderns, probably dating to ca. 25–30 Kyr bp (Hedges et al. 1995; Etler 1996). Due to more recent Uraniumseries dates, Shen et al. (2002) have argued that the Liujiang specimen could be much older (>60 Ka or 100 Ka), but there remain basic uncertainties as to the stratigraphic position of the human remains and thus to their age (Demeter et al. 2012; Keates 2010). In spite of some deviations from present-day Chinese population samples (Howells 1995; Stringer 1999), a multivariate analysis of these early modern Chinese crania (Bräuer and Mímisson 2004) demonstrated that the Upper Cave 101 specimen exhibits the closest affinities with Upper Paleolithic Europeans and also Australians and recent Europeans. For the Liujiang cranium (Fig. 5), the greatest similarity was found with recent North Africans and Europeans as well as with Upper Paleolithic Europeans, terminal Pleistocene North Africans, and sub-Saharan Africans. These similarities appear to support a more recent date for Liujiang. Yet, even if this fully modern specimen would indeed be about 100 Kyr old, it would still clearly contradict any regional evolution from the archaic Dali-MabaJinniushan group. The discussion on the date of the earliest presence of modern humans in East Asia continues, since more human remains have been reported to date between >40 and 100 Ka. These comprise an anterior mandibular fragment from Zhirendong, South China, dated to about 100 Ka (Liu et al. 2010), and a partial adult cranium from the Tam Pa Ling, a cave in Laos, with an age of ca. 46 Ka (Demeter et al. 2012). Because of extant uncertainties on the dating of Liujiang and the fully modern condition of Zhirendong, Demeter et al. (2012) regard the rather well-preserved specimen from Laos as the earliest definitively modern fossil in East Asia. Yet, even with this specimen some questions on the dating and stratigraphy exist (Pierret et al. 2012). Regarding Australasia, the central assumptions of the multiregionalists have also proven to be no longer tenable. In spite of the huge gap in time between the only H. erectus specimen with a wellpreserved face, Sangiran 17, and the earliest Australians, Wolpoff et al. (1984, p. 443) saw, especially in the face, a number of continuity features such as the marked prognathism, the maintenance of large posterior dentitions throughout the Middle and Late Pleistocene, an eversion of the lower border of the malar, the persistence of a zygomaxillary ridge, and rounding of the inferolateral border of the orbit. Yet the assumption of interregional gene flow as emphasized by multiregionalists would make it very unlikely that such combinations of features could have been maintained over a period of more than 1 Myr and during the claimed transformation process from the massive facial morphology of H. erectus toward that of modern humans (Nei 1998). In addition, Aziz et al. (1996) demonstrated that the earlier reconstruction of the Sangiran 17 cranium done by Wolpoff (Thorne and Wolpoff 1981) is incorrect in several respects. In the revised reconstruction (Fig. 6), the degree of facial prognathism is not marked, but only moderate, and there is no eversion of the lower border of the zygomatic bone, which as a whole bulges laterally. Moreover, the zygomaxillary ridge could not be detected by Aziz et al. (1996, p. 20), nor by myself, on the Page 16 of 28

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_57-5 # Springer-Verlag Berlin Heidelberg 2015

Fig. 6 Homo erectus from Indonesia and an early modern Australian: (a) Revised reconstruction of Sangiran 17 by Aziz et al. 1996 (Photo: F. Aziz/H. Baba); (b) Ngandong; (c) Lake Mungo 3

original. There is also no rounding of the inferolateral border of the orbit (Baba et al. 2000, p. 61). Finally, Baba et al. (2000, p. 62) demonstrated that “it does not make sense to compare the degree of facial and dental reduction between Sangiran 17 and Australians, because masticatory adaptation pattern is completely different from each other.” Thus, relevant continuity features which have been said to be present on Sangiran 17, dated to ca. 1.3 Ma (Antón 2003), are simply not there or are the result of incorrect reconstruction. Also, in her comprehensive analysis of 20 assumed Australasian cranial features, Lahr (1994) arrived at the conclusion that most of the traits did not show the pattern proposed by the Multiregional Evolution model and quite a number of them occur with high frequency in a robust terminal Pleistocene sample from North Africa, thereby supporting a functional interpretation of these traits. Detailed analyses of the cranial morphology of Indonesian H. erectus show a continuous gradual evolution from the early Pleistocene specimens to the late H. erectus from Ngandong (Fig. 6) and Sambungmacan, but no further evolutionary continuity to early modern Australasians (Kaifu et al. 2008). Until recently, the ages of Ngandong and of Sambungmacan, which have long been controversial, ranged between a few hundreds of thousands of years (e.g., Bartstra et al. 1988) to only 30–50 Ka (Swisher et al. 1996). New redating by Ar/Ar and ESR/U-series also arrived at divergent results that nevertheless narrow the age of the Ngandong hominins to between 140 and 540 Ka (Indriati et al. 2011). Thus, it now seems that the Ngandong erectus is older than 100 Ka and not contemporaneous with the earliest Australians, such as the fully modern skeleton Lake Mungo 3, southern Australia (Fig. 6), for which several dating approaches have yielded an age of more than 40 Kyr bp and perhaps even up to 60 Kyr bp (Thorne et al. 1999; Bowler and Magee 2000). Although no conclusive indications for a regional evolution from H. erectus to modern Australians appear to exist, the human fossil and subfossil material from Australia as a whole exhibits considerable variability with regard to robusticity. Among these anatomically modern humans, there are very robust as well as gracile specimens as, for example, present in the Kow Swamp material which dates to ca. 22–19 Kyr bp or somewhat more recent (Bräuer 1989; Stone and Cupper 2003). One of the most robust crania is WLH-50 from the Willandra Lakes, which has been absolutely dated to 14 Kyr bp (Simpson and Gr€ un 1998). The cranial vault of this specimen has also been Page 17 of 28

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Fig. 7 Origin and evolution of Homo sapiens

modified by severe pathological alterations (Webb 1990). Notwithstanding the young age and pathology of WLH-50, Wolpoff et al. (2001) chose this cranium instead of the much more appropriate one from Lake Mungo in order to demonstrate regional evolution in Australasia. However, their approach also suffers from fundamental problems with the characteristics used as well as their assessments (Bräuer et al. 2004b). Robust specimens also date from the early Holocene. Possible explanations for the great range of variation might be drift effects in the course of the occupation of the continent but may also include adaptation to an increasingly arid environment toward the peak of the last glacial period (Klein 1999; Baba et al. 2000). As the recent genome sequencing showed, populations of Australia and New Guinea not only exhibit up to 5 % of their DNA from the archaic Denisovans but also 1–4 % of Neanderthal DNA (Reich et al. 2011). Yet, in view of the fact that the earliest fully moderns in Australia are rather gracile, it remains controversial whether this archaic DNA component also contributed to the greater robusticity among the later terminal Pleistocene Australians.

Conclusions Over the last two and a half decades, the accumulating fossil and molecular evidence has strongly supported the “Out-of-Africa and hybridization” model. Claims by multiregionalists for a larger contribution of Neanderthals to the early modern Europeans cannot be supported by the current

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evidence. Instead, the most likely scenario appears to be a replacement of the Neanderthals accompanied by only a small amount of gene flow. For the Far East, it is more difficult to examine possible indications of interbreeding since the fossil record of the replacement period is rather poor. Nevertheless, in view of the serious problems regarding the claimed continuity features for China and Australasia and the fact that the earliest modern humans in both areas are fully anatomically modern and do not fit into the concept of regional evolution, no convincing evidence can be seen for long-term regional evolution up to modern humans. The anatomical modernization process in Africa now appears to be well established by quite a number of diagnostic and reliably dated hominid specimens. To describe the obvious morphological changes of this continuously evolving lineage, three grades or groups of H. sapiens have been suggested. This evolutionary sequence led to an early emergence of anatomically modern humans nearly 200 Ka. In view of the obvious continuity from archaics to early moderns and the nearmodern morphology of the premoderns, it appears unlikely that anatomically modern humans differ from their direct ancestors on the species level (Stringer 2002a; Bräuer 2008). Instead, during the major part of the Middle Pleistocene, the African fossil record documents a diachronic increase of more derived modern-like conditions. Therefore, it appears adequate to assign the post-H. erectus humans to one biological species H. sapiens (Klein 2009; Hofreiter 2011). This view is also supported by the fact that the Preneanderthal/Neanderthal lineage which goes back to around 500 Ka bp cannot reasonably be split into different species. It might thus be in agreement with the current evidence (Fig. 7) from Africa and Europe to only assume a speciation between H. erectus and (archaic) H. sapiens at around 700 or 800 Ka in Africa. Later, early archaic sapiens populations spread into Europe evolving toward the Neanderthals. Regarding China, it appears likely that the late Middle Pleistocene humans derived from an eastward dispersal of archaic H. sapiens populations, possibly representing the Denisovan lineage, although some regional gene flow from H. erectus cannot be excluded as well. As discussed in this and other chapters, various alternative phylogenetic scenarios have been suggested to describe Middle and Late Pleistocene human evolution. H. sapiens is often restricted to modern humans, and its ancestral group (largely equivalent to late archaic H. sapiens) has been assigned either to the same species (Stringer 2002a) or to a separate species, H. helmei (McBrearty and Brooks 2000). Alternatively, H. helmei is regarded as ancestral not only to modern H. sapiens but also to H. neanderthalensis (Foley and Lahr 1997). These various possibilities, however, have their own problems. For example, the latter phylogeny does not consider that Neanderthal features had long existed in Europe prior to the hypothesized appearance of H. helmei. Moreover, suggesting several species within the continuously evolving lineages of later human evolution causes problems in delimiting the taxonomic units (Foley 2001). Such units are rather arbitrarily defined entities without any clear relation to biological species. Studies on extant primates led Jolly (2003, p. 662) to conclude that Neanderthals, Afro-Arabian “premodern” populations, and modern humans are, roughly speaking, biological subspecies, comparable to interfertile allopatric taxa or phylogenetic species of baboons. Thus, it appears well supported from different lines of evidence, including the recent results from nuclear DNA sequencing for widespread archaic-modern hybridization, to regard the European Preneanderthals/Neanderthals and the African Middle Pleistocene lineage to modern humans and the late archaic group in China as belonging to one polytypic species H. sapiens. “Speciation remains the special case, the less frequent and more elusive phenomenon, often arising by default” (Grubb 1999, p. 164).

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Cann RL (1992) A mitochondrial perspective on replacement or continuity in human evolution. In: Bräuer G, Smith FH (eds) Continuity or replacement-controversies in Homo sapiens evolution. AA Balkema, Rotterdam, pp 65–73 Cann RL, Stoneking M, Wilson AC (1987) Mitochondrial evolution and human evolution. Nature 325:32–36 Caspari RE (1991) The evolution of the posterior cranial vault in the central European Upper Pleistocene. Ph.D. dissertation, University of Michigan, Ann Arbor Churchill SE, Smith FH (2000) Makers of the early Aurignacian of Europe. Yrbk Phys Anthropol 43:61–115 Churchill SE, Pearson OM, Grine FE, Trinkaus E, Holliday TW (1996) Morphological affinities of the proximal ulna from Klasies River Mouth Main Site: archaic or modern? J Hum Evol 31:213–237 Clark JD (1970) The prehistory of Africa. Praeger, New York Clark JD (1979) Radiocarbon dating and African archaeology. In: Berger R, Suess HE (eds) Radiocarbon dating. University of California Press, Berkeley, pp 7–31 Clark JD, de Heinzelin J, Schick K, Hart KW, White TD, Wolde-Gabriel G, Walter RC, Suwa G, Asfaw B, Vrba E, Haile-Selassie Y (1994) African Homo erectus: old radiometric ages and young Oldowan assemblages in the Middle Awash Valley, Ethiopia. Science 264:1907–1910 Collard M, Franchino N (2002) Pairwise difference analysis in modern human origins research. J Hum Evol 43:323–352 Conard NJ, Grootes PM, Smith FH (2004) Unexpectedly recent dates for human remains from Vogelherd. Nature 430:198–201 Coon CS (1962) The origin of races. Knopf, New York Currat M, Excoffier L (2004) Modern human did not admix with Neanderthals during their range expansion into Europe. PLoS Biol 2:e421 Demeter F, Shackelford LL, Bacon AM, Duringer P, Westaway K, Sayavongkhamdy T, Braga J, Sichanthongtip P, Khamdalavong P, Ponche JL, Wang H, Lundstrom C, Patole-Edoumba E, Karpoff AM (2012) Anatomically modern human in Southeast Asia (Laos) by 46ka. Proc Natl Acad Sci U S A 109:14375–14380 Endicott P, Ho SYW, Stringer C (2010) Using genetic evidence to evaluate four palaeoanthropological hypotheses for the timing of Neanderthal and modern human origins. J Hum Evol 59:87–95 Etler DA (1996) The fossil evidence for human evolution in Asia. Ann Rev Anthropol 25:275–301 Foley R (2001) In the shadow of the modern synthesis? Alternative perspectives on the last fifty years of paleoanthropology. Evol Anthropol 10:5–14 Foley R, Lahr MM (1997) Mode 3 technologies and the evolution of modern humans. Camb Archaeol J 7:3–36 Frayer DW (1986) Cranial variation at Mladeč and the relationship between Mousterian and Upper Paleolithic hominids. Anthropologie (Brno) 23:243–256 Frayer DW (1992) Evolution at the European edge: Neanderthal and Upper Palaeolithic relationships. Préhist Eur 2:9–69 Frayer DW, Wolpoff MH, Thorne AG, Smith FH, Pope G (1993) Theories of modern human origins: the paleontological test. Am Anthropol 95:14–50 Gibbons A (2011) A new view of the birth of Homo sapiens. Science 331:392–394 Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MHY, Hansen NF, Durand EY, Malaspinas AS, Jensen JD, Marques-Bonet T, Alkan C, Pr€ ufer K, Meyer M, Burbano HA, Good JM, Schultz R, Aximu-Petri A, Butthof A, Höber B, Höffner B, Page 22 of 28

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Siegemund M, Weihmann A, Nusbaum C, Lander ES, Russ C, Novod N, Affourtit J, Egholm M, Verna C, Rudan P, Brajkovic D, Kucan Z, Gusic I, Doronichev VB, Golovanova LV, LaluezaFox C, de la Rasilla M, Fortea J, Rosas A, Schmitz RW, Johnson PLF, Eichler EE, Falush D, Birney E, Mullikin JC, Slatkin M, Nielsen R, Kelso J, Lachman M, Reich D, Pääbo S (2010) A draft sequence of the Neandertal genome. Science 328:710–722 Groves CP (1989) A regional approach to the problem of the origin of modern humans in Australasia. In: Mellars P, Stringer CB (eds) The human revolution. Edinburgh University Press, Edinburgh, pp 274–285 Groves CP, Thorne A (1999) The terminal Pleistocene and early Holocene population of northern Africa. Homo 50:249–262 Grubb P (1999) Evolutionary processes implicit in distribution patterns of modern African mammals. In: Bromage TG, Schrenk F (eds) African biogeography, climate change, and human evolution. Oxford University Press, New York, pp 150–164 Gr€un R, Beaumont P (2001) Border Cave revisited: a revised ESR chronology. J Hum Evol 40:467–482 Gr€un R, Stringer CB (1991) Electron spin resonance dating and the evolution of modern humans. Archaeometry 33:153–199 Gr€un R, Brink JS, Spooner NA, Taylor L, Stringer CB, Franciscus RG, Murray AS (1996) Direct dating of Florisbad hominid. Nature 382:500–501 Guatelli-Steinberg D (2009) Recent studies of dental development in Neandertals: implications for Neandertals life histories. Evol Anthropol 18:9–20 Habgood PJ (1992) The origin of anatomically modern humans in East Asia. In: Bräuer G, Smith FH (eds) Continuity or replacement- controversies in Homo sapiens evolution. AA Balkema, Rotterdam, pp 273–288 Harvati K (2003) The Neanderthal taxonomic position: models of intra-and inter-specific craniofacial variation. J Hum Evol 44:107–132 Hedges REM, Housley RA, Bronk Ramsey C, van Klinken GJ (1995) Radiocarbon dates from the Oxford AMS system: archaeometry datelist 14. Archaeometry 34:141–159 Higham T, Bronk Ramsey C, Karavanic I, Smith FH, Trinkaus E (2006) Revised direct radiocarbon dating of the Vindija G1 Upper Paleolithic Neandertals. Proc Natl Acad Sci U S A 103:553–557 Higham T, Crompton T, Stringer C, Jacobi R, Shapiro B, Trinkaus E, Chandler B, Gröning F, Collins C, Hillson S, O’Higgins P, FitzGerald C, Fagan M (2011) The earliest evidence for anatomically modern humans in northwestern Europe. Nature 479:521–524 Hofreiter M (2011) Drafting human ancestry: what does the Neanderthal genome tell us about hominid evolution? Commentary on Green et al. (2010). Hum Biol 83:1–11 Howell FC (1951) The place of Neanderthal man in human evolution. Am J Phys Anthropol 9:379–416 Howells WW (1976) Explaining modern man: evolutionists versus migrationists. J Hum Evol 5:477–495 Howells WW (1993) Getting here. The story of human evolution. Compass Press, Washington, DC Howells WW (1995) Who’s who in skulls. Peabody museum of archaeology and ethnology. Harvard University, Cambridge Hrdlicka A (1927) The Neanderthal phase of man. J R Anthropol Inst 67:249–269 Hublin JJ (1982) Les Anténéandertaliens: Présapiens ou Prénéandertaliens. Geobios Mém Spec 6:245–357 Hublin JJ (1992) Recent human evolution in northwestern Africa. Philos Trans R Soc (Lond) B 337:243–250 Page 23 of 28

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Hublin JJ (1998) Climatic changes, paleogeography, and the evolution of the Neandertals. In: Akazawa T, Aoki K, Bar-Yosef O (eds) Neandertals and modern humans in Western Asia. Plenum Press, New York, pp 295–310 Indriati E, Swisher CC, Lepre C, Quinn RL, Suriyanto RA, Hascaryo AT, Gr€ un R, Feibel CS, Pobiner BL, Aubert M, Lees W, Antón SC (2011) The age of the 20 meter Solo River Terrace, Java, Indonesia and the survival of Homo erectus in Asia. PLoS One 6:e21562 Jolly CJ (2003) Comment to: species concepts, reticulation, and human evolution by TW Holliday. Curr Anthropol 44:662–663 Kaifu Y, Aziz F, Indriati E, Jacob T, Kurniawan I, Baba H (2008) Cranial morphology of Javanese Homo erectus: new evidence for continuous evolution, speciation and terminal extinction. J Hum Evol 55:551–580 Keates SG (2010) The chronology of Pleistocene modern humans in China, Korea and Japan. Radiocarbon 52:428–465 Keith A (1936) History from caves: a new theory of the origin of modern races of mankind. First speleological conference July 1936, British Speleological Association Klein R (1999) The human career. Human biological and cultural origins, 2nd edn. University of Chicago Press, Chicago Klein RG (2009) The human career. Human biological and cultural origins, 3rd edn. University of Chicago Press, Chicago Koesbardiati T (2000) On the relevance of the regional continuity features of the face in East Africa. Ph.D. dissertation, Hamburg Lahr MM (1994) The multiregional model of modern human origins: a reassessment of its morphological basis. J Hum Evol 26:23–56 Lahr MM (1995) Patterns of modern human diversification: implications for Amerindian origins. Yrbk Phys Anthropol 38:163–198 Langergraber KE, Pr€ ufer K, Rowney C, Boesch C, Crockford C, Fawcett K, Inoue E, InoueMuruyama M, Mitani JC, Muller MN, Robbins MM, Schubert G, Stoinski TS, Viola B, Watts D, Wittig RM, Wrangham RW, Zuberb€ uhler K, Pääbo S, Vigilant L (2012) Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great apes and human evolution. Proc Natl Acad Sci U S A 109:15716–15721 Larnach SL, Macintosh NWG (1974) A comparative study of Solo and Australian Aboriginal crania. In: Elkin AP, Macintosh NWG (eds) Grafton Elliot Smith: the man and his work. Sydney University, Sydney, pp 95–102 Leakey REF, Butzer K, Day MH (1969) Early Homo sapiens remains from the Omo River region of South-West Ethiopia. Nature 222:1132–1138 Lieberman DE (1995) Testing hypotheses about recent human evolution from skulls. Curr Anthropol 36:159–197 Lieberman DE, Pearson OM, Mowbray KM (2000) Basicranial influence on overall cranial shape. J Hum Evol 38:291–315 Lieberman DE, McBratney BM, Krovitz G (2002) The evolution and development of cranial form in Homo sapiens. Proc Natl Acad Sci U S A 99:1134–1139 Liu W, Jin CZ, Zhang YQ, Cai YJ, Xing S, Wu XJ, Cheng H, Edwards RL, Pan WS, Qin DG, An ZS, Trinkaus E, Wu XZ (2010) Human remains from Zhirendong, South China, and modern human emergence in East Asia. Proc Natl Acad Sci U S A 107:19201–19206 Manega PC (1995) New geochronological results from the Ndutu, Naisiusiu and Ngaloba Beds at Olduvai and Laetoli in Northern Tanzania: their significance for evolution of modern humans. Bellagio Conference, Italy Page 24 of 28

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Mbua E, Bräuer G (2012) Patterns of Middle Pleistocene hominin evolution in Africa and the emergence of modern humans. In: Reynolds SC, Gallagher A (eds) African genesis. Perspectives on hominin evolution. Cambridge University Press, Cambridge, pp 394–422 McBrearty S, Brooks AS (2000) The revolution that wasn’t: a new interpretation of the origin of modern human behavior. J Hum Evol 39:453–563 McDougall I, Brown F, Fleagle JG (2005) Stratigraphic placement and age of modern humans from Kibish, Ethiopia. Nature 433:733–736 Mellars P (2011) The earliest modern humans in Europe. Nature 479:483–485 Nara MT (1994) Etude de la variabilité de certains caractères métriques et morphologiques des Néandertaliens. Thèse de Docteur, Bordeaux Nei M (1998) Genetic studies on the origin of modern humans. In: Omoto K, Tobias PV (eds) The origins and past of modern humans-towards reconciliation. World Scientific, Singapore, pp 27–41 Pearson OM (2000) Postcranial remains and the origin of modern humans. Evol Anthropol 9:229–247 Pierret A, Zeitoun V, Forestier H (2012) Irreconcilable differences between stratigraphy and direct dating cast doubts upon the status of Tam Pa Ling fossil. Proc Natl Acad Sci U S A 109:E3523 Pope GG (1992) Craniofacial evidence for the origin of modern humans in China. Yrbk Phys Anthropol 35:243–298 Protsch R (1975) The absolute dating of Upper Pleistocene sub-Saharan fossil hominids and their place in human evolution. J Hum Evol 4:297–322 Rak Y (1998) Does any Mousterian cave present evidence of two hominid species? In: Akazawa T, Aoki K, Bar-Yosef O (eds) Neandertals and modern humans in Western Asia. Plenum Press, New York, pp 353–366 Reich D, Green RE, Kircher M, Krause J, Patterson N, Durand EY, Viola B, Briggs AW, Stenzel U, Johnson PL, Maricic T, Good JM, Marques-Bonet T, Alkan C, Fu Q, Mallick S, Li H, Meyer M, Eichler EE, Stoneking M, Richards M, Talamo S, Shunkov MV, Derevianko AP, Hublin JJ, Kelso J, Slatkin M, Pääbo S (2010) Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468:1053–1060 Reich D, Patterson N, Kircher M, Delfin F, Nandineni MR, Pugach I, Ko AMS, Ko YC, Jinam TA, Phipps ME, Saitou N, Wollstein A, Kayser M, Pääbo S, Stoneking M (2011) Denisova admixture and the first modern human dispersals into Southeast Asia and Oceania. Am J Hum Genet 89:516–528 Rightmire GP (1996) The human cranium from Bodo, Ethiopia: evidence for speciation in the Middle Pleistocene? J Hum Evol 31:21–39 Rightmire GP (1998) Human evolution in the Middle Pleistocene: the role of Homo heidelbergensis. Evol Anthropol 6:218–227 Rightmire GP, Deacon HJ (1991) Comparative studies of Late Pleistocene human remains from Klasies River Mouth, South Africa. J Hum Evol 20:131–156 Rougier H, Milota S, Rodrigo R, Gherase M, Sarcina L, Moldovan O, Zilhão J, Constantin S, Franciscus RG, Zollikofer CPE, Ponce de León M, Trinkaus E (2007) Peştera cu Oase 2 and the cranial morphology of early modern Europeans. Proc Natl Acad Sci U S A 104:1165–1170 Ruff CB, Trinkaus E, Holliday TW (2002) Body proportions and size. In: Zilhão J, Trinkaus E (eds) Portrait of the artist as a child: the Gravettian human skeleton from the Abrigo do Lagar Velho and its archaeological context. Trabalhos de Arqueologia 22, Lisboa, pp 365–391 Schwalbe G (1906) Studien zur Vorgeschichte des Menschen: I. Zur Frage der Abstammung des Menschen. E. Schweizerbart, Stuttgart

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Schwartz JH, Tattersall I (2003) The human fossil record. Vol. 2: craniodental morphology of Genus Homo (Africa and Asia). Wiley-Liss, Hoboken Serre D, Pääbo S (2006) The fate of European Neanderthals: results and perspectives from ancient DNA analyses. In: Harvati K, Harrison T (eds) Neanderthals revisited: new approaches and perspectives. Springer, Dordrecht, pp 211–219 Shen G, Wang W, Wang Q, Zhau J, Collerson K, Zhou C, Tobias PV (2002) U-Series dating of Liujiang hominid site in Guangxi, Southern China. J Hum Evol 43:817–829 Simpson JJ, Gr€ un R (1998) Non-destructive gamma spectrometric U-series dating. Quat Sci Rev 17:1009–1022 Smith FH (1978) Evolutionary significance of the mandibular foramen area in Neandertals. Am J Phys Anthropol 48:523–531 Smith FH (1982) Upper Pleistocene hominid evolution in South-Central Europe. Curr Anthropol 23:667–703 Smith FH (2002) Migrations, radiations and continuity: patterns of Middle and Late Pleistocene humans. In: Hartwig WC (ed) The primate fossil record. Cambridge University Press, Cambridge, pp 437–456 Smith FH, Falsetti AB, Donnelly SM (1989) Modern human origins. Ybk phys Anthropol 32:35–68 Smith FH, Falsetti B, Simmons T (1995) Circum-Mediterranean biological connections and the pattern of late Pleistocene human evolution. In: Ullrich H (ed) Man and environment in the Palaeolithic. ERAUL, Liège, pp 197–207 Smith FH, Trinkaus E, Pettitt PB, Karavanic I, Paunovic M (1999) Direct radiocarbon dates from Vindija G1 and Velika Pecina late Pleistocene hominid remains. Proc Natl Acad Sci U S A 96:12281–12286 Smith FH, Hutchinson VT, Jankovic I (2012) Assimilation and modern human origins in the African peripheries. In: Reynolds SC, Gallagher A (eds) African genesis: perspectives on hominin evolution. Cambridge University Press, Cambridge, pp 365–393 Soficaru A, Dobos A, Trinkaus E (2006) Early modern humans from the Pestera Muierii, Baia de Fier, Romania. Proc Natl Acad Sci U S A 103:17196–17201 Stone T, Cupper ML (2003) Last glacial maximum ages for robust humans at Kow Swamp southern Australia. J Hum Evol 45:99–111 Stringer CB (1990) British Isles. In: Orban R (ed) Hominid remains: an up-date British Isles and Eastern Germany. Université Libre de Bruxelles, Bruxelles, pp 1–40 Stringer CB (1992) Replacement, continuity and the origin of Homo sapiens. In: Bräuer G, Smith FH (eds) Continuity or replacement-controversies in Homo sapiens evolution. AA Balkema, Rotterdam, pp 9–24 Stringer CB (1999) The origin of modern humans and their regional diversity. In: recent progress in the studies of the origins of the Japanese. News Lett 9:3–5 Stringer CB (2001a) Modern human origins: distinguishing the models. Afr Archaeol Rev 18:67–75 Stringer CB (2001b) The evolution of modern humans: where are we now? Gen Anthropol 7:1–5 Stringer CB (2002a) Modern human origins: progress and prospects. Philos Trans R Soc Lond B 357:563–579 Stringer CB (2002b) New perspectives on the Neanderthals. Evol Anthropol Suppl 1:58–59 Stringer C (2011) The origin of our species. Allen Lane, London Stringer C (2012) The status of Homo heidelbergensis (Schoetensack 1908). Evol Anthropol 21:101–107 Stringer CB, Bräuer G (1994) Methods, misreading, and bias. Am Anthropol 96:416–424

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Svoboda JA, van der Plicht J, Kuzelka V (2002) Upper Paleolithic and Mesolithic human fossils from Moravia and Bohemia (Czech Republic): some new 14C dates. Antiquity 76:957–962 Swisher CC, Rink WJ, Antón SC, Schwarcz HP, Curtis GH, Suprijo A, Widiasmoro (1996) Latest Homo erectus of Java: potential contemporaneity with Homo sapiens in Southeast Asia. Science 274:1870–1874 Tattersall I, Schwartz JH (1999) Hominids and hybrids: the place of Neandertals in human evolution. Proc Natl Acad Sci U S A 96:7117–7119 Tattersall I, Schwartz JH (2000) Extinct humans. Westview Press, Boulder Terberger T, Street M, Bräuer G (2001) Der menschliche Schädelrest aus der Elbe bei Hahnöfersand und seine Bedeutung f€ ur die Steinzeit Norddeutschlands. Archäolog Korrespondenzblatt 31:521–526 Teschler-Nicola M (ed) (2006) Early modern humans at the Moravian Gate. The Mladeč Caves and their remains. Springer, Wien Thorne AG (1993) Introduction. Session: the end of Eve? Fossil evidence from Africa. Am Assoc Adv Sci 21, Abstr:173 Thorne AG, Wolpoff MH (1981) Regional continuity in Australasian Pleistocene hominid evolution. Am J Phys Anthropol 55:337–349 Thorne AG, Wolpoff MH (2003) The multiregional evolution of humans. Sci Am Spec Ed New Look Human Evol 13:46–53 Thorne AG, Gr€ un R, Mortimer G, Spooner NA, Simpson JJ, McCulloch M, Taylor L, Curnoe D (1999) Australia’s oldest human remains: age of the Lake Mungo 3 skeleton. J Hum Evol 36:591–612 Trinkaus E (1981) Evolutionary continuity among archaic Homo sapiens. In: Ronen A (ed) The transition from lower to middle Paleolithic and the origin of modern man. University of Haifa, Haifa Trinkaus E (1988) The evolutionary origins of the Neandertals, or why were there Neandertals. In: Otte M (ed) L’ Homme de Neandertal, vol 3. L’ anatomie, Liège, pp 11–29 Trinkaus E, Moldovan O, Milota S, Bilgar A, Sarcina L, Athreya S, Bailey SE, Rodrigo R, Mircea G, Higham T, Bronk Ramsey C, van der Plicht J (2003) An early modern human from the PeÅŸtera cu Oase, Romania. Proc Natl Acad Sci U S A 100:11231–11236 Turbón D (2006) La evolución humana. Editorial Ariel, Barcelona Vallois HV (1954) Neanderthals and Praesapiens. J R Anthropol Inst 84:111–130 Weaver TD (2012) Did a discrete event 200,000–100,000 years ago produce modern humans? J Hum Evol 63:121–126 Webb S (1990) Cranial thickening in an Australian hominid as a possible paleoepidemiological indicator. Am J Phys Anthropol 82:403–411 Weidenreich F (1943) The skull of Sinanthropus pekinensis: a comparative study on a primitive hominid skull. Palaeontol Sin D 10:1–485 Weidenreich F (1947) The trend of human evolution. Evolution 1:221–236 White TD, Asfaw B, DeGusta D, Gilbert H, Richards GD, Suwa G, Howell FC (2003) Pleistocene Homo sapiens from Middle Awash, Ethiopia. Nature 423:742–747 Wild EM, Teschler-Nicola M, Kutschera W, Steier P, Trinkaus E, Wanek W (2005) Direct dating of early Upper Palaeolithic human remains from Mladeč. Nature 435:332–335 Wolpoff MH (1980) Paleoanthropology, 1st edn. Knopf, New York Wolpoff MH (1992) Theories of modern human origins. In: Bräuer G, Smith FH (eds) Continuity or replacement-controversies in Homo sapiens evolution. AA Balkema, Rotterdam, pp 25–63 Wolpoff MH (1999) Paleoanthropology, 2nd edn. McGraw-Hill, Boston Page 27 of 28

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Wolpoff MH (2009) How Neandertals inform human variation. Am J Phys Anthropol 139:91–102 Wolpoff MH, Thorne AG (1991) The case against Eve. New Sci 130:37–41 Wolpoff MH, Wu X, Thorne AG (1984) Modern Homo sapiens origins: a general theory of hominid evolution involving the fossil evidence from East Asia. In: Smith FH, Spencer F (eds) The origins of modern humans: a world survey of the fossil evidence. Alan R Liss, New York, pp 411–483 Wolpoff MH, Hawks J, Frayer DW, Hunley K (2001) Modern human ancestry at the peripheries: a test of the replacement theory. Science 291:293–297 Wolpoff MH, Mannheim B, Mann A, Hawks J, Caspari R, Rosenberg KR, Frayer DW, Gill GW, Clark GA (2004) Why not the Neandertals? World Archaeol 36:527–546 Wu X (1992) The origin and dispersal of anatomically modern humans in East Asia and Southeast Asia. In: Akazawa T, Aoki K, Kimura T (eds) The evolution and dispersal of modern humans in Asia. Hokusen-Sha, Tokyo, pp 373–378 Wu X (1998) Origin of modern humans of China viewed from cranio-dental characteristics of late Homo sapiens in China. Acta Anthropol Sin 17:276–284 Zilhão J, Trinkaus E (eds) (2002) Portrait of the artist as a child: the Gravettian human skeleton from the Abrigo do Lagar Velho and its archaeological context, vol 22, Trabalhos de Arqueologia. Instituto português de arqueologia, Lisboa

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Analyzing Hominin Phylogeny David Straita*, Frederick E. Grineb,c and John G. Fleaglec a Department of Anthropology, University at Albany, Albany, NY, USA b Department of Anthropology, State University of New York, Stony Brook, NY, USA c Department of Anatomical Sciences, Stony Brook University, School of Medicine, Stony Brook, NY, USA

Abstract An understanding of the phylogenetic relationships among organisms is critical for evaluating the evolutionary history of their adaptations and biogeography as well as forming the basis for systematics. As the numbers of hominin fossils and hominin taxa have increased over the past 40 years, controversies over phylogeny have expanded and have become a hallmark of paleoanthropology. Concordant with the rise in taxonomic diversity, the increased use of phylogenetic systematics, or cladistics, has provided a valuable tool for reconstructing hominin phylogeny. Despite the widespread view that hominin phylogeny is a source of endless debate, there is a broad consensus regarding many aspects of hominin phylogeny.

Introduction Phylogeny is central to our understanding of virtually any aspect of an organism’s biology. An appreciation of the phylogenetic relationships of an organism not only provides a perspective on its place in the history of life and a basis for taxonomy but is also critical for evaluating biogeography as well as ecology and behavior. The adaptations of all organisms, even those as adaptively flexible as primates, are inherited, and thus any proper statistical analysis of physiological adaptations requires a consideration of phylogeny (Harvey and Pagel 1991; Purvis and Webster 1999). In paleoanthropology at the beginning of the twenty-first century, the study of phylogeny hardly needs to be justified. The first questions that are asked about any new fossil discovery are “How is it related to us?” and “What does it tell us about our evolutionary past?” Paleoanthropology has a reputation in the popular press as a discipline characterized by disagreements over phylogeny, and this is perhaps not unfair if one considers the seemingly diverse array of phylogenetic hypotheses that have been proposed in the last two decades (Delson 1986; Walker et al. 1986; Chamberlain and Wood 1987; Grine 1988; Kimbel et al. 1988, 2004; Wood 1988, 1991, 1992; Skelton and McHenry 1992, 1998; White et al. 1994; Leakey et al. 1995, 2001; Brunet et al. 1996, 2002; Lieberman et al. 1996; Strait et al. 1997; Strait and Grine 1998, 1999, 2001, 2004; Asfaw et al. 1999; Senut et al. 2001; Martino´n-Torres et al. 2007; Berger et al. 2010; Organ et al. 2011). Certainly much of the current interest in hominin phylogeny has been fueled by new paleontological discoveries. Nine new early hominid species have been described in the decades between 1994

*Email: [email protected] Page 1 of 23

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and 2014 (White et al. 1994; Leakey et al. 1995, 2001; Brunet et al. 1996, 2002; Asfaw et al. 1999; Senut et al. 2001; Haile-Selassie et al. 2004; Berger et al. 2010). Many of these discoveries have been accompanied by phylogenetic hypotheses, not all of which are compatible with each other. However, the current importance of phylogeny in paleoanthropology and the current understanding of hominin phylogeny are not just the result of new fossil discoveries. They also reflect major theoretical and methodological advances in the discipline during recent decades (Tattersall 1999). Thus, before discussing current views on hominin phylogeny, a brief history of this endeavor during the last century is provided. The term hominin is used to mean taxa that are more closely related to humans than to any other primate.

Phylogenetic Diversity in Hominin Evolution As numerous authors have emphasized, theoretical approaches to hominin phylogeny changed considerably through the course of the twentieth century (Fleagle and Jungers 1982; Tattersall 1999; Gundling 2005). In the early decades, discussions of hominin phylogeny were largely limited to evaluating whether the few fossil taxa that were known at the time – Pithecanthropus erectus from Java, Cyphanthropus rhodesiensis, or Rhodesian Man from Africa, Piltdown (Eoanthropus dawsoni) from England, Neanderthals from Europe, and, after 1925, Australopithecus and allied forms from Africa – were ancestral to living humans in their various forms. Two distinct issues dominated the literature. First, were any of the various fossil forms directly in the lineage leading to modern humans? As noted by Dobzhansky in 1944, most authorities found that all fossils had features which precluded placing them directly in human ancestry so that phylogenetic trees generally show a main trunk leading from somewhere in the primate past to modern humans, with each fossil taxon occupying a side branch leading to extinction (Fig. 1; Dobzhansky 1944; Tattersall 1999). Despite the lack of reliable estimates of the geological age of any extinct taxa, they were generally suggested to have branched from the (main) human lineage at different times, such that each documented some aspect of human ancestry. However, all discussion concerned the relationship of the extinct taxa to the main human lineage, with little discussion of the relationships among the extinct taxa themselves. The notable exception to this was Weidenreich’s trellis model of hominin evolution in which all living and extinct taxa were interconnected but with temporal and geographic differentiation (Weidenreich 1946; Smith 1997). To a large degree, these trees showing humans at the crown just reflect the fact that in the early part of the twentieth century, as today, paleoanthropology was different from other aspects of zoology in being by definition focused primarily on tracing the history of a single organism, humans, rather than on the interrelationships of a large group of more or less equally important taxa. After all, it is the human species that writes the books. However, as Gundling (2005) has argued, a related but distinct and in many cases more important issue in the first half of the twentieth century was the taxonomic issue of whether the various extinct species were hominins or apes. That is, where should the ape-human boundary be drawn? In most cases, these two approaches yielded concordant views. Fossils that were placed on the ape lineage were clearly not hominins. However, in some cases fossil taxa might be considered offshoots of the main human stem but still considered apes because they lacked the critical hominin character. This was at the heart of much of the debate regarding the place of Piltdown and Australopithecus in hominin phylogeny during the early part of the twentieth century. In general, most researchers limited the human family to modern people.

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Fig. 1 A phylogeny of Primates from Hooton (1931) showing a tree with human races at the crown and the few known fossil taxa as long side branches from the main stem

As Tattersall (1999) has so eloquently discussed, all of this changed in mid-century as paleoanthropologists began, however slowly, to adopt the tenets of the New Darwinian Synthesis. Despite a growing record of new fossils, human evolution was increasingly seen as a unilinear progression through time, with all morphological diversity consigned to intraspecific variation due to geography or sexual dimorphism (Buettner-Janusch 1966; Brace 1967). All of the divergent branches from earlier in the century were incorporated into the main stem, and human evolution was seen as one continuous chain of forms separated mainly by time. The most extreme expression of this approach was Mayr’s (1950) inclusion of all fossil hominins (including “robust” and “gracile australopithecines”) into a single genus, Homo, with three species. Certainly there were other views, for example, Robinson, following Broom, repeatedly argued that Paranthropus was a separate lineage of hominin from Australopithecus and Homo, and Louis Leakey argued from time to time that the ancestry of the human lineage was not to be found among known fossils of the time. However, for much of the discipline, there was little appreciation of phyletic diversity in human evolution (Fig. 2). This view of limited phyletic diversity was very compelling. It was supported by the leading authorities on evolutionary biology at the time, such as Mayr and Dobzhansky; it brought paleoanthropology in line with the rest of evolutionary biology; and it conformed well with what is seen in the world today: a single species of humans with considerable intraspecific variation. Moreover, there were theoretical reasons offered to justify a lack of phyletic diversity in a culture-bearing creature (Mayr 1950; Wolpoff 1971). And while extrapolating human behavior backward into the fossil record may not be totally justified, especially for the Pliocene, it is not totally unreasonable. However, by the 1970s the unilinear view of human evolution was being seriously challenged on several fronts and had become increasingly difficult or even impossible to support. There were clearly two distinct hominin lineages present in the Late Pliocene and Early Pleistocene at Olduvai

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Fig. 2 A chart of hominin evolution from a major textbook from 1966 (Buettner-Janusch 1966) showing the conservative lumper’s view on the left and the extreme splitter’s view on the right

Gorge and Koobi Fora (Leakey and Walker 1976), and there was increasing evidence that in other parts of the world modern humans had preceded or were contemporary with European Neanderthals (Leakey 1969; Stringer 1974, 1978; Howells 1975; Bra¨uer 1982). Likewise, “new” analytical approaches emphasized the view that morphological changes over the past 3 Myr or so did not follow a simple temporal pattern of increasingly modern features through time (Eldredge and Tattersall 1975). With an increasing number of contemporaneous taxa, the potential phylogenetic complexity of the hominin fossil record continued to grow and came to a head with the description of Australopithecus afarensis (hereafter called Praeanthropus afarensis) in 1978 and the ensuing debate over taxonomic diversity and phylogenetic relationships in early hominin evolution (Johanson et al. 1978; Johanson and White 1979; Tobias 1980; Olson 1981, 1985; White et al. 1981; Rak 1983; Kimbel et al. 1984; Skelton et al. 1986). The level of debate over early hominin diversity and phylogeny was heightened even further with the discovery in Kenya of the

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_58-4 # Springer-Verlag Berlin Heidelberg 2013

Black Skull (KNM-WT 17000) several years later (Delson 1986; Walker et al. 1986; Grine 1988; Kimbel et al. 1988; Wood 1988). Similarly, the debate over the timing and geography of modern human origins and the relationship between Homo sapiens, Neanderthals, and Homo erectus expanded in the 1980s and has yet to abate (Smith and Spencer 1982; Mellars and Stringer 1989; Trinkaus 1989; Stringer 2002, 2012a).

Reconstructing Phylogeny: The Rise of Cladistics The increasing evidence of taxonomic and phyletic diversity in hominin evolution during the 1970s and 1980s coincided with the increasing prominence of phylogenetic systematics or cladistics in paleoanthropology (Eldredge and Tattersall 1975; Luckett and Szalay 1975; Delson et al. 1977; Tattersall and Eldredge 1977; Delson 1985; Skelton et al. 1986; Wood et al. 1986; Grine et al. 1987; Grine 1988). The methods of phylogenetic systematics, or cladistics, were developed by the German entomologist Willi Hennig in 1950, but it was only with their publication in an English translation (Hennig 1966) that his methods became widely known and applied in morphological studies to understanding the phylogeny of all sorts of organisms. Cladistics is a method of phylogenetic reconstruction premised on the notion that not all morphological similarities are indicative of phylogeny. Rather, only those similarities that are derived (i.e., novel) and inherited from a recent common ancestor should be indicative of patterns of relatedness. In practice, it is difficult (if not impossible) to discern, a priori, such features (called synapomorphies) from other types of similarities such as primitive retentions (symplesiomorphies) or traits that have evolved convergently or in parallel (homoplasies). Thus, cladistics relies on the principle of parsimony to identify synapomorphies and, hence, to reconstruct phylogeny. In a general sense, parsimony is the idea that the simplest explanation is the best one because it makes the fewest assumptions. As applied to cladistics, parsimony dictates that the best cladogram is the one that requires the fewest number of homoplasies or independent appearances of the same feature. Parsimony analysis is conventional in evolutionary biology (Kitching et al. 1998) but is viewed with skepticism by some paleoanthropologists (Trinkaus 1990; Asfaw et al. 1999; Hawks 2005). This skepticism is misplaced because, at its core, the logic of parsimony is intuitive and not too dissimilar from that of “traditional” evolutionary systematics (e.g., Olson 1981). More significantly, it provides a replicable criterion for evaluating alternative hypotheses beyond preconceived notions of how things should be (Tattersall 1996). Consider an example in which a phylogenetic analysis is being performed on the living hominoids (Hylobates, Pongo, Gorilla, Pan, and Homo) and a fossil hominin (Australopithecus). Now consider a character with two states (knee joint valgus or varus). The nonhuman apes and various outgroup taxa (other Old World higher primates) have a varus knee, while Homo and Australopithecus have a valgus knee. Given a cladogram in which Australopithecus and Homo are sister taxa (Fig. 3a), what can be concluded about the evolution of the knee joint? There are actually many ways in which the knee joint might have evolved. It is possible that a valgus knee joint was present in all of the ancestors represented by the internal nodes of the cladogram (Fig. 3b). Such a reconstruction requires that a varus knee joint evolved in parallel in each nonhuman ape lineage. Alternatively, it is possible that a varus knee joint was present at all of the nodes of the cladogram, including the one representing the last common ancestor of hominins (Fig. 3c). This reconstruction requires that a valgus knee joint would have evolved in parallel in Homo and Australopithecus. Neither of these reconstructions is satisfying because both are needlessly complex. There is instead a much simpler (i.e., more parsimonious) explanation for the evolution of the knee joint, namely, Page 5 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_58-4 # Springer-Verlag Berlin Heidelberg 2013

Fig. 3 Principles of cladistics. (a) Cladogram depicting possible phylogenetic relationships among hominoids. (b) Pattern of character evolution in which a varus knee evolves many times in parallel in each of the nonhuman hominoids. (c) Valgus knee evolves in parallel in Homo and Australopithecus. (d) Most parsimonious pattern of character evolution in which a valgus knee evolves once in the last common ancestor of Australopithecus and Homo. (e) Cladogram depicting an alternative phylogeny. (f) Most parsimonious pattern of character evolution in the alternative cladogram. a(¼d) is preferred over (e) because it involves fewer changes, and it is therefore the most parsimonious

that a valgus knee joint evolved once in the last common ancestor of the hominins Australopithecus and Homo, who subsequently passed that trait onto its descendants (Fig. 3d). Such a reconstruction does not require any homoplasy. Now consider an alternative cladogram in which Australopithecus is the sister taxon of all of the living hominoids (Fig. 3e). In this tree, the most parsimonious reconstruction of the evolution of the knee joint is one in which a valgus knee evolved in parallel in Australopithecus and Homo (Fig. 3f). No other possible reconstruction of character evolution in the knee joint requires fewer character state changes or steps. Now consider that the two cladograms presented here (Fig. 3a and e) represent alternative interpretations of hominoid phylogeny. How can these cladograms be compared so as to select one of them as the better hypothesis of phylogeny? Parsimony states that the preferred cladogram is the one that is simplest, namely, the one that minimizes the number of homoplasies required. Fewer homoplasies are required in Fig. 3d than in Fig. 3f, so the preferred cladogram is the one in which Australopithecus and H. sapiens are sister taxa (Fig. 3a). There is nothing controversial about this example, and both cladists and noncladists would agree with the

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_58-4 # Springer-Verlag Berlin Heidelberg 2013

result. The only difference between this example and an actual cladistic analysis is that most analyses would examine many characters at once. This is a great advantage of numerical cladistic analysis over “traditional” evolutionary systematics in which only a handful of characters tends to strongly influence the shape of phylogenetic trees. Even more significant is the fact that cladistic studies make explicit assumptions and predictions so that analyses are replicable, and the results are testable.

Cladistic Analyses of Hominin Phylogeny Early Studies The first cladistic analysis of hominin evolution was by Eldredge and Tattersall (1975) who also coauthored a series of papers delineating various levels of phylogeny reconstruction from producing a cladogram, to creating a phylogenetic tree, and finally an evolutionary scenario (Delson et al. 1977; Tattersall and Eldredge 1977). In the late 1970s and early 1980s, cladistic analyses in paleoanthropology were relatively simple and often consisted of little more than producing a cladogram and identifying a few shared derived characters at each node (Olson 1978; Andrews 1984; papers in Luckett and Szalay 1975; Delson 1985; Wood et al. 1986; Grine et al. 1987). Nevertheless, this was major advance from much previous work in primate phylogeny in that there was a clear effort to distinguish shared derived features from shared primitive ones, and authors provided explicit morphological justification for phylogenetic grouping at every level. Falsifying a set of relationships based on a cladistic analysis generally requires identification of additional morphological features that produce a different cladogram when analyzed. As Tattersall (1999) has pointed out, the rise of cladistics has led to a tremendous increase in the detailed documentation and analysis of hominin morphology. The mid-1980s saw the first use of quantitative cladistic analyses in hominin evolution. By using computer algorithms researchers were able to evaluate dozens of characters and compare thousands of trees (or more), tasks that were simply unfeasible otherwise. The first efforts to evaluate hominin phylogeny using numerical methods were in an analysis of early hominin phylogeny by Chamberlain and Wood in 1987 and a study of the genus Homo by Stringer (1987). Numerous subsequent analyses of the phylogeny of hominins and many other groups of primates have used essentially the same methods (Fleagle and Kay 1987; Kay et al. 1997; Strait et al. 1997; Ross et al. 1998).

Moving Toward a Rough Consensus The 1987 study of early hominin phylogeny by Chamberlain and Wood did not include Paranthropus aethiopicus, which subsequently became the linchpin of early hominin phylogeny. The first study to include this species was that of Wood (1988), who examined the trait list provided by Walker et al. (1986) in their description of KNM-WT 17000. Wood (1988) found that Paranthropus robustus and Paranthropus boisei are sister taxa, that Homo is the sister taxon of this clade, and that Pr. afarensis, P. aethiopicus, and Australopithecus africanus branch off in sequence from the base of the hominin tree (Fig. 4a). Notably, the three “robust” species are paraphyletic. A subsequent study by Skelton and McHenry (1992), using a more extensive trait list, found an identical cladogram. Wood (1991, 1992), using a data set composed entirely of craniometric measurements, found a most parsimonious cladogram in which A. africanus is the sister taxon of Homo, H. habilis sensu stricto and H. rudolfensis are sister taxa, and P. boisei and P. robustus are monophyletic (Fig. 4b). Technically, Wood’s (1991, 1992) cladogram does not Page 7 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_58-4 # Springer-Verlag Berlin Heidelberg 2013

Fig. 4 Cladistic analyses of early hominins from various studies. (a) Cladogram of Wood (1988) and Skelton and McHenry (1992). (b) Cladogram of Wood (1991, 1992). (c) Cladogram of Lieberman et al. (1996). (d) Cladogram of Strait et al. (1997) and Kimbel et al. (2004)

include P. aethiopicus, but it is reported in the text of his analysis that this species is the sister taxon of P. boisei. Lieberman et al. (1996) found a most parsimonious tree (Fig. 4c) in which Paranthropus is paraphyletic, P. robustus and P. boisei are sister taxa, and A. africanus is nested within the Homo clade. Subsequently, Strait et al. (1997) found a cladogram in which Paranthropus is monophyletic and the sister taxon of Homo (Fig. 4d). Recently, an independent analysis by Kimbel et al. (2004) has largely corroborated Strait et al.’s (1997) results. Kimbel et al. (2004) found two equally parsimonious trees: one is equivalent to those of Strait et al. (1997) and the other differs only in placing A. africanus as the sister taxon of the Paranthropus clade. The analyses noted above appear to differ from each other, but in fact they are similar to a much greater degree than is generally acknowledged. The results of Strait et al. (1997) and Kimbel et al. (2004) differ from those of Wood (1988) and Skelton and McHenry (1992) only with respect to the relationships of P. aethiopicus. They differ from those of Wood (1991, 1992) principally with respect to the relationships of A. africanus. The most parsimonious tree of Lieberman et al. (1996) differs from that of Wood (1988) and Skelton and McHenry (1992) only with respect to A. africanus. Thus, these cladograms disagree primarily with respect to only two taxa, A. africanus and P. aethiopicus. There are also disagreements concerning the exact relationships of H. habilis and H. rudolfensis, but all analyses that include these taxa place them at the base of the Homo clade. In short, it appears as if cladistic analyses of early hominins are converging on a common set of relationships. It would be an overstatement to claim that the pattern of early hominin phylogeny is known, but insofar as repeatability is a key component of any scientific result, it would appear that the broad strokes of early hominin phylogeny are perhaps better understood than commonly acknowledged.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_58-4 # Springer-Verlag Berlin Heidelberg 2013

Phylogenetic Implications of a “Golden Age” of Discovery (1994–2004) There were many discoveries of new fossil hominin species in the decade between 1994 and 2004 (White et al. 1994; Leakey et al. 1995, 2001; Brunet et al. 1996, 2002; Asfaw et al. 1999; Senut et al. 2001; Ward et al. 2001; Haile-Selassie et al. 2004). Despite the common refrain that phylogenetic debates can be resolved by the discovery of new fossils, many of these new finds raised rather than resolved phylogenetic questions. Although most of the new discoveries were accompanied by a phylogenetic hypothesis, those hypotheses often only addressed the relationships among a few hominin taxa. Moreover, these hypotheses were potentially difficult to test using cladistic analysis because they specified ancestor-descendant relationships without specifying sister-group relationships. At the time, the remains of many of these new hominin taxa were not yet thoroughly published, and further documentation of their morphology will doubtless permit more complete analyses. However, on the basis of information available so far, one can use cladistic analysis to test many of the initial hypotheses that have been proposed because phyletic relationships imply sister-group relationships. In particular, it is an accepted principle that a species can only be an ancestor of another taxon if it is the sister species of that taxon and if its character states resemble those reconstructed as being present in the relevant internal node of a cladogram (Szalay 1977; Smith 1994; Wagner and Erwin 1995; O’Keefe and Sander 1999). Accordingly, the phyletic hypotheses that have been proposed for many recent fossil discoveries in hominin evolution can be evaluated through reconstruction of sister-group relationships (Fig. 5). Strait and Grine (2004) tested many of the hypotheses generated by these new taxa. They found that the pattern of hominin phylogeny is unbalanced such that many species branch off by themselves from the base of the tree, while the top of the tree is dominated by two multispecies clades, Homo and Paranthropus (Fig. 6). Sahelanthropus and Ardipithecus are, respectively, the first two branches of the tree, with subsequent branches successively represented by Australopithecus anamensis, Pr. afarensis, Australopithecus garhi, and A. africanus. If Kenyanthropus platyops is a valid species, then its position within the Homo + Paranthropus clade is unresolved; it is either the sister taxon of the rest of the clade or of Paranthropus. Relationships within Paranthropus are also unresolved, with P. boisei being the sister taxon of either P. aethiopicus or P. robustus. The position of H. habilis relative to H. rudolfensis is unresolved, but it is clear that one or the other is the basal branch of the Homo clade. Homo ergaster and H. sapiens are sister taxa. These results are consistent with certain of the hypotheses offered in the original descriptions and inconsistent with others. Ardipithecus ramidus At the time of its description (White et al. 1994), Ardipithecus ramidus was the oldest and most morphologically primitive hominin species then known. White et al. (1994) suggested that Ar. ramidus lies near the ancestry of all other hominins and that it may be the actual ancestor of those species. A cladogram consistent with this hypothesis would place Ar. ramidus as the sister taxon of a clade that includes all other hominin species (Fig. 5a). Strait and Grine (2004) found that Ar. ramidus is the sister taxon of all hominins except Sahelanthropus (Fig. 6). These results support the hypothesis of White et al. in a general sense insofar as Ar. ramidus branches off near the base of the hominin tree, if not necessarily at the basal node.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_58-4 # Springer-Verlag Berlin Heidelberg 2013

Fig. 5 Phylogenetic hypotheses associated with recently discovered hominins

Australopithecus anamensis The following year, Leakey et al. (1995) described Australopithecus anamensis as a species intermediate both chronologically and morphologically between Ar. ramidus and Pr. afarensis. Leakey et al. (1995) and Ward et al. (2001) have suggested that A. anamensis is more closely related to later hominins than is Ar. ramidus and may be directly ancestral to Pr. afarensis (Kimbel et al., 2006). A cladogram consistent with this hypothesis would depict A. anamensis as diverging

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_58-4 # Springer-Verlag Berlin Heidelberg 2013

Fig. 6 Early hominin cladistic relationships found by Strait and Grine (2004)

from a higher node on the hominin tree than Ar. ramidus and as the sister taxon of all later hominins (Fig. 5b). An alternative topology that might also be consistent with the phyletic hypothesis would make A. anamensis the sister taxon of Pr. afarensis. Strait and Grine’s (2004) results (Fig. 6) are consistent with the hypothesis that A. anamensis is the sister taxon of all hominins except Ardipithecus (and, presumably, Sahelanthropus). Australopithecus bahrelghazali The discovery of Australopithecus bahrelghazali was notable primarily because it represented the first early hominin species found in central Africa. Brunet et al. (1996) did not offer a detailed phylogenetic hypothesis for A. bahrelghazali but rather noted merely that the species is more derived than the contemporaneous Pr. afarensis. Not all workers accept that A. bahrelghazali and Pr. afarensis are distinct species (Kimbel et al. 2004). This species was not included in the analysis by Strait and Grine because it is known from only a few remains. Australopithecus garhi As described by Asfaw et al. (1999), Australopithecus garhi preserves an unexpected combination of cranial and dental characteristics. In particular, it has megadont molars and premolars but a relatively primitive-appearing face and neurocranium. Asfaw et al. (1999) implied that A. garhi could be a suitable ancestor for Homo, although they noted that the exact phylogenetic relationships of this species remained unresolved. They presented a cladogram in which A. garhi, A. africanus, P. robustus, P. boisei, P. aethiopicus, and Homo form a clade but in which relationships within that clade were left unresolved. However, they presented four phyletic trees, and in three of those, A. garhi was posited to be an ancestor of at least some members of the genus Homo. Moreover, they (Asfaw et al. 1999, p. 632) state that “If A. garhi proves to be the exclusive ancestor of the Homo clade, a cladistic classification would assign it to genus Homo.” Such a classification would only be valid if A. garhi and at least some of the Homo species form a monophyletic group, as in Fig. 5c. Furthermore, in reference to the morphology of A. garhi, Asfaw et al. (1999, p. 634) state that “its lack of derived robust characters leaves it as a sister taxon to Homo but absent many derived Homo characters.” Strait and Grine’s (2004) results are consistent with the hypothesis that A. garhi belongs to a clade that also includes A. africanus, Paranthropus, and Homo, insofar as A. garhi is reconstructed as the sister taxon of a clade comprising those taxa (Fig. 4). In addition, the relationships of Ardipithecus ramidus, A. anamensis, and Pr. afarensis are equivalent to those Page 11 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_58-4 # Springer-Verlag Berlin Heidelberg 2013

proposed by Asfaw et al. (1999). However, Asfaw et al. (1999) also suggested that A. garhi may be ancestral to all or part of the genus Homo. Cladistic analysis fails to find a sister-group relationship between Homo and A. garhi (Fig. 6). Moreover, A. garhi is excluded from a clade that includes only Homo, Paranthropus, A. africanus, and K. platyops. Thus, there is no support for the hypothesis that A. garhi and Homo are sister taxa, so A. garhi is unlikely to be the direct ancestor of Homo. Orrorin tugenensis Found in Late Miocene deposits (Senut et al. 2001), Orrorin tugenensis supplanted Ar. ramidus as the oldest known fossil hominin. Senut et al. (2001) claim that on the basis of dental and postcranial characters, O. tugenensis is the basal member of the Homo clade, to the exclusion of australopiths. Moreover, they suggest that Ar. ramidus is not a hominin but an ancestor of Pan. A cladogram consistent with these hypotheses (Fig. 5d) would have Orrorin and Homo as sister taxa, a clade of all australopithecines except Ardipithecus being the sister taxon of the Orrorin + Praeanthropus + Homo clade, and Ardipithecus as the sister taxon of Pan. Strait and Grine’s (2004) analysis did not include Orrorin because too few characters are preserved in that species. However, their data set can be used to examine the effect of making Ardipithecus the sister of Pan and the other australopiths monophyletic (Senut et al. 2001). The most parsimonious tree found by Strait and Grine’s data set for the hypothesis that Ardipithecus in the sister taxon of Pan is 30 steps longer than that shown in Fig. 6. Considering that Senut et al.’s (2001) hypothesis is based on only a few characters (e.g., molar size, enamel thickness, details of the proximal femur), which cannot account for so many steps, it is fair to conclude that this hypothesis is not favored by cladistic analysis. Kenyanthropus platyops The discovery of Kenyanthropus platyops was notable because it demonstrated the existence of multiple hominin lineages in the Middle Pliocene. Leakey et al. (2001) noted that Kenyanthropus platyops appeared to share several derived character states exclusively with H. rudolfensis. They posited (Lieberman 2001) that this might imply that these two species had a particularly close relationship. A cladogram consistent with this hypothesis (Fig. 5e) would have K. platyops and H. rudolfensis as sister taxa. Although the validity of the species diagnosis of Kenyanthropus platyops has been questioned by White (2003), who has implied that many of the defining features of the type specimen are artifacts of postdepositional distortion, others have found no reason to doubt its validity. The results of the analysis by Strait and Grine (2004) are inconsistent with the hypothesis that K. platyops shares especially close affinities with H. rudolfensis even to the point of removing the latter from the Homo clade. Rather, Kenyanthropus is the sister taxon of either Paranthropus or the Homo + Paranthropus clade (Fig. 6). There is no strong evidence supporting the hypothesis that H. rudolfensis and K. platyops are sister taxa, and thus the transfer of H. rudolfensis to the genus Kenyanthropus is at present unwarranted. One implication of these results is that some of the facial features shared between H. rudolfensis and K. platyops may be primitive for the Homo + Paranthropus clade, while others may be convergent. Another implication concerns the timing of early hominin cladogenic events. If K. platyops is a valid species, then its age (3.3–3.5 Ma) and cladistic relationships suggest that Homo and Paranthropus may have diverged from other hominin taxa up to 700 kyr prior to the earliest known specimens currently attributed to those genera (Suwa et al. 1996). It follows, therefore, that this divergence would not be explained by the Turnover Pulse Hypothesis (Vrba 1988) because the divergence would have predated the desiccations event that

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_58-4 # Springer-Verlag Berlin Heidelberg 2013

she postulates to have occurred in Africa between 2.7 and 2.3 Ma. These two clades may have each diversified during this period, but their origins are likely to have been earlier in the fossil record. Sahelanthropus tchadensis The title of “oldest hominin” now belongs to Sahelanthropus tchadensis (Brunet et al. 2002). Brunet et al. (2002, p. 151) note that S. tchadensis appears to be “the oldest and most primitive member of the hominin clade, close to the divergence of hominins and chimpanzees.” The authors are cautious about the precise phylogenetic relationships of the species, but note the possibility that Sahelanthropus is the sister taxon of all other hominins, including Ardipithecus. A cladogram consistent with this hypothesis would have Sahelanthropus as the basal branch of the hominin clade (Fig. 5f). Brunet et al. (2002) discuss the possibility that Sahelanthropus is the sister taxon of all known hominin species, including Ardipithecus. The Strait and Grine study is consistent with this hypothesis insofar as Sahelanthropus was found to be the basal branch of the hominin clade (Fig. 6). It also does not group with African apes as suggested by Wolpoff et al. (2002). Ardipithecus kadabba Fossils attributed to Ardipithecus kadabba were first assigned to a subspecies of Ardipithecus ramidus (Haile-Selassie 2001), but subsequent discoveries led to the elevation of this assemblage to species status (Haile-Selassie et al. 2004). The species is notable for its extremely primitive canine-premolar honing complex. Its describers imply that it is the best candidate to be the sister taxon or ancestor of all other hominins and that fossils of the other two known Miocene species, O. tugenensis and S. tchadensis, are in fact representatives of Ar. kadabba. This species was not included in the analysis of Strait and Grine (2004) because it is currently known from only a few body parts.

Discoveries Since 2004 and Implications for Early Hominin Relationships The phylogenetic relationships described above collectively represent a reasonable working hypothesis of early hominin phylogeny, but more recent discoveries and descriptions of hominin fossils may necessitate important revisions in the near future. In 2009, a relatively complete skeleton of Ar. ramidus and other fossils from this species were comprehensively described (e.g., White et al. 2009). These descriptions confirm that Ar. ramidus possesses a small number of derived cranial traits that seem to place it within and near the base of the hominin clade. However, as described, the species also seems to lack nearly all of the postcranial traits traditionally associated with bipedal locomotion, as well as most of the traits seen in living apes that are functional related to suspensory locomotion. The describers of Ar. ramidus interpret this suite of characters to mean that the earliest hominins were not descended from an ancestor possessing suspensory traits. While possible, this hypothesis appears to be wildly unparsimonious, because it also implies that many suspensory traits must have evolved in parallel in multiple ape lineages. It is difficult to imagine cladistic analysis supporting this hypothesis but formal study is needed. Indeed, in light of the new postcranial evidence, the possibility that Ar. ramidus is not a hominin warrants further investigation, even if its hominin status is ultimately upheld. In 2010, partial skeletons of a new hominin species, Australopithecus sediba, were discovered in southern Africa that similarly possess an unexpected mosaic of primitive and derived traits. The species exhibits craniodental traits that may align it with early Homo, but has postcranial characters (especially in the foot) that appear to be more primitive than those in Pr. afarensis

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_58-4 # Springer-Verlag Berlin Heidelberg 2013

Fig. 7 Hypothetical cladogram (a) and phylogenetic tree (b) of evolution within the genus Homo (Modified from Tattersall 1999)

(Berger et al. 2010; Zipfel et al. 2011). It has been hypothesized that it lies near the ancestry of Homo, but such a position might imply extensive homoplasy in hominin postcranial traits. A difficulty in assessing the phylogenetic significance of these new data is that cladistic analyses of early hominins have traditional been based on cranial rather than postcranial characters because several early hominin species lack well-associated postcranial remains. Thus, it is difficult to quantitatively evaluate how the new postcranial data will affect parsimony-based assessments of early hominin phylogeny. Clearly, a research priority of the next decade will be to formally incorporate postcranial data into cladistic analyses of early hominins.

Phylogenetic Relationships Within the Genus Homo Compared with studies of early hominin evolution in the Late Miocene and Pliocene, research on the phylogeny of Pleistocene hominins (Fig. 7) is complicated by ongoing debates on the number of species involved. The extremes range from those who, like Mayr in 1950, have argued for a single species in the genus Homo (Wolpoff et al. 1994) – thus precluding any phylogeny within the genus – to others who suggest the presence of more than 15 species (Tattersall 1999). However, the majority of researchers recognize, at least for the purposes of discussion, between seven and nine species. Homo habilis, Homo rudolfensis, Homo ergaster, Homo erectus, Homo heidelbergensis, Homo neanderthalensis, and Homo sapiens are widely recognized, with Homo antecessor and Homo floresiensis more poorly known and/or less widely accepted.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_58-4 # Springer-Verlag Berlin Heidelberg 2013

As noted above, the relationships of H. habilis and H. rudolfensis are poorly resolved. On the basis of an assessment of adaptive differences between Homo and Australopithecus, Wood and Collard (1999a, b) have argued that these taxa should be removed from the genus Homo, although their suggestion has yet to be widely adopted. Among other early Pleistocene species, there are ongoing debates over whether Homo ergaster from Africa is more closely related to later species of Homo than is the mostly Asian Homo erectus (e.g., Fig. 4b) or whether any of the early species of the genus Homo can be distinguished at all (e.g., Wood 1994; Bra¨uer 1994; Rightmire 1992; Lordkipanidze et al., 2013). Like studies of early Homo, studies of phylogenetic relationships among later species of the genus Homo are bedeviled by problems of proper taxonomic allocation of fossils to be included in any analysis. Many researchers agree that the descendant of the Early Pleistocene H. erectus (or H. ergaster?) is a Middle Pleistocene taxon usually referred to as H. heidelbergensis (Rightmire 1998), which in turn may have given rise to both Neanderthals and modern humans (Fig. 7b). However, it has also been suggested that the immediate ancestor of H. heidelbergensis is not H. erectus, but the poorly known H. antecessor from the latest Early Pleistocene of Atapuerca, Spain (Bermudez de Castro et al. 2004), and possibly Italy as well (Manzi 2004). The relationships between H. heidelbergensis, H. neanderthalensis, and H. sapiens are also uncertain. Although Neanderthals have traditionally been viewed as either a subspecies or sister taxon of H. sapiens, many authorities now argue that H. heidelbergensis and H. neanderthalensis are sister taxa or even a single anagenetic lineage with no clear break (Arsuaga et al. 1997; Hublin 1998). From this perspective, H. sapiens is the sister taxon of a H. heidelbergensis and H. neanderthalensis clade (Fig. 7a). In this scheme H. sapiens is the descendant of a distinct early Middle Pleistocene taxon from Africa, usually given the name Homo rhodesiensis. Stringer (2012b) has recently argued that reconstructions of the population history of Middle Pleistocene humans might be clarified by removing the hominins from Sima de los Huesos out of H. heidelbergensis and instead grouping them with Neanderthals. An interesting recent debate concerns the phylogenetic relationships of H. floresiensis. Although once considered to be a dwarf descendant of Homo erectus, there is tantalizing evidence from both cranial and postcranial anatomy suggesting that it may, in fact, represent a H. habilis-like hominin whose lineage pre-dates the appearance of H. erectus (Argue et al. 2009; Jungers et al. 2009). More study is needed, however, and this, again, speaks of the need to incorporate postcranial characters into cladistic analyses of hominins.

Summary It is too soon to say whether a consensus will emerge concerning the phylogenetic relationships of the hominin species described over the last two decades, not to mention those likely to be discovered in the coming years. Strait and Grine’s (2004) results on early hominin phylogeny need to be tested by other, independent cladistic analyses, and a comprehensive phylogenetic analysis of the genus Homo is long overdue. Postcranial characters need to be incorporated into future studies. New fossils of almost all of these species are badly needed in order to provide a better representation of characters and a better understanding of intraspecific variation. Improvements in techniques to assess character independence, morphological integration, and developmental modularity (McCollum 1999; Ackermann and Cheverud 2000; Strait 2001) will also greatly improve the accuracy of cladistic analysis. At the heart of all attempts to understand hominin phylogeny are unresolved issues regarding the identification of species in the fossil record Page 15 of 23

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_58-4 # Springer-Verlag Berlin Heidelberg 2013

Fig. 8 A summary of the temporal span and phylogenetic relationships among fossil hominins

(Tattersall 1986, 1992, 1996; Kimbel and Rak 1993; Plavcan and Cope 2001). This is especially critical within the genus Homo, in which genetic evidence has demonstrated that population history is perhaps more complicated than might have been expected based on a consideration of the fossil record alone (Green et al. 2010; Reich et al. 2010). Despite these caveats, a broad consensus regarding the phylogenetic relationships of many hominin taxa has emerged (Fig. 8). It is likely that disagreement will persist as to the exact relationships among S. tchadensis, Ar. kadabba, and O. tugenensis until they are known by more body parts that can be directly compared, but most workers accept that these species all lie somewhere near the base of the hominin tree. The greatest disagreement will probably focus on A. garhi and K. platyops and the relationships of these species to the genus Homo, as well as whether or not Ar. ramidus is a hominin. While there is broad general agreement about overall phylogenetic relationships in later hominin evolution, there is less consensus about the number of taxa that should be identified. The number and relationships of the early species of the genus Homo remain a source of ongoing debate (Wood and Collard 1999a, b; Wood and Lonergan 2008; Henke and Hardt 2011; Stringer 2012a), and there are various alternative interpretations concerning the few fossils from the Early and Middle Pleistocene (Tattersall 1986; Rightmire 1998; Bermudez de Castro et al. 2004; Manzi 2004). Some have argued that hominin phylogeny will never be resolved in a timely fashion because of the many gaps in the fossil record (White 2002). That view is unduly pessimistic. Of course there are gaps in the fossil record! Despite the fact that knowledge of that record is constantly expanding, it will never be complete. That is not an excuse for failing to do the best one can with the material that is available in order to evaluate phylogenetic hypotheses. There is no doubt that the fossil record samples only a portion of the organisms, including hominins, that have ever lived and that new discoveries always document new, unanticipated aspects of evolutionary diversity. This is

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_58-4 # Springer-Verlag Berlin Heidelberg 2013

why paleontology is such an exciting and rewarding field of study. Despite this serendipitous sampling of the history of life, and ongoing uncertainties regarding some taxa, cladistic analysis has led researchers toward a general consensus of the phylogenetic relationship of many of the hominin taxa that can be documented and remains the best hope for resolving future questions about hominin phylogeny.

Cross-References ▶ General Principles of Evolutionary Morphology ▶ Homo ergaster and Its Contemporaries ▶ Homo floresiensis ▶ Homology: A Philosophical and Biological Perspective ▶ Later Middle Pleistocene Homo ▶ Neanderthals and Their Contemporaries ▶ Paleoecology: An Adequate Window on the Past ▶ Quantitative Approaches to Phylogenetics ▶ Quaternary Geology and Paleoenvironments ▶ The Earliest Putative Hominids ▶ The Earliest Putative Homo Fossils ▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments ▶ The Species and Diversity of Australopiths

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Lordkipanidze D, Ponce de Leon MS, Margvelashvili A, Rak Y, Rightmire GP, Vekua A, Zollikofer PE (2013) A complete skull from Dmanisi, Georgia, and the evolutionary biology of early Homo. Science 342:326–331 Luckett WP, Szalay FS (eds) (1975) Phylogeny of the primates: a multidisciplinary approach. Plenum, New York Manzi G (2004) Human evolution at the Matuyama-Brunhes boundary. Evol Anthropol 13:11–24 Martino´n-Torres M, Bermu´dez de Castro JM, Go´mez-Robles A, Arsuaga JL, Carbonell E, Lordkipanidze D, Manzi G, Margvelashvili A (2007) Dental evidence on the hominin dispersals during the Pleistocene. Proc Natl Acad Sci U S A 104:13279–13282 Mayr E (1950) Taxonomic categories in fossil hominids. Cold Spring Harb Symp Quant Biol 15:109–118 McCollum MA (1999) The robust australopithecine face: a morphogenetic perspective. Science 284:301–305 Mellars P, Stringer C (1989) The human revolution: behavioral and biological perspectives on the origin of modern humans. Edinburgh University Press, Edinburgh O’Keefe FR, Sander PM (1999) Paleontological paradigms and inferences of phylogenetic pattern: a case study. Paleobiology 25:518–533 Olson TR (1978) Hominid phylogenetics and the existence of Homo in member I of the Swartkrans formation. S Afr J Hum Evol 7:159–178 Olson TR (1981) Basicranial morphology of the extant hominoids and Pliocene hominids: the new material from the Hadar formation, Ethiopia, and its significance in early human evolution and taxonomy. In: Stringer CB (ed) Aspects of human evolution. Taylor and Francis, London, pp 99–128 Olson TR (1985) Cranial morphology and systematics of the Hadar formation hominids and “Australopithecus” africanus. In: Delson E (ed) Ancestors: the hard evidence. Alan R Liss, Inc., New York, pp 102–119 Organ C, Nunn CL, Machanda Z, Wrangham RW (2011) Phylogenetic rate shifts in feeding time during the evolution of Homo. Proc Natl Acad Sci U S A 108:14555–14559 Plavcan JM, Cope DA (2001) Metric variation and species recognition in the fossil record. Evol Anthropol 10:204–222 Purvis A, Webster AJ (1999) Phylogenetically independent comparisons and primate phylogeny. In: Lee PC (ed) Comparative primate socioecology. Cambridge University Press, New York, pp 44–70 Rak Y (1983) The Australopithecine face. Academic, New York Reich D, Green RE, Kircher M, Krause J, Patterson N, Durand EY, Viola B, Briggs AW, Stenzel U, Johnson PLF, Maricic T, Good JM, Marques-Bonet T, Alkan C, Fu Q, Mallick S, Li H, Meyer M, Eichler EE, Stoneking M, Richards M, Talamo S, Shunkov MV, Derevianko AO, Hublin J-J, Kelso J, Slatkin M, Pa¨a¨bo S (2010) Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468:1053–1060 Rightmire GP (1992) Homo erectus: ancestor or evolutionary side branch. Evol Anthropol 1:43–49 Rightmire GP (1998) Human evolution in the Middle Pleistocene. Evol Anthropol 6:218–227 Ross CF, Williams BA, Kay RF (1998) Phylogenetic analysis of anthropoid relationships. J Hum Evol 35:221–306 Senut B, Pickford M, Gommery D, Mein P, Cheboi K, Coppens Y (2001) First hominid from the Miocene (Lukeino formation, Kenya). CR Acad Sci Paris Sci Terre Plan 332:137–144 Skelton RR, McHenry HM (1992) Evolutionary relationships among early hominids. J Hum Evol 23:309–349 Page 20 of 23

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Vrba ES (1988) Late Pliocene climatic events and hominid evolution. In: Grine FE (ed) Evolutionary history of the “robust” australopithecines. Aldine de Gruyter, New York, pp 405–426 Wagner PJ, Erwin DH (1995) Phylogenetic tests of speciation models. In: Erwin DH, Antsy RL (eds) New approaches to speciation in the fossil record. Columbia University Press, New York, pp 87–122 Walker AC, Leakey REF, Harris JM, Brown FH (1986) 2.5-Myr Australopithecus boisei from west of Lake Turkana, Kenya. Nature 322:517–522 Ward CV, Leakey MG, Walker A (2001) Morphology of Australopithecus anamensis from Kanapoi and Allia Bay, Kenya. J Hum Evol 41:255–368 Weidenreich F (1946) Apes, giants, and man. University of Chicago Press, Chicago White TD (2002) Earliest hominids. In: Hartwig WC (ed) The primate fossil record. Cambridge University Press, Cambridge UK, pp 407–417 White TD (2003) Early hominids: diversity or distortion? Science 299:1194–1197 White TD, Johanson DC, Kimbel WH (1981) Australopithecus africanus: its phyletic position reconsidered. S Afr J Sci 77:445–470 White TD, Suwa G, Asfaw B (1994) Australopithecus ramidus, a new species of early hominid from Aramis, Ethiopia. Nature 371:306–312 White TD, Asfaw B, Beyene Y, Haile-Selassie Y, Lovejoy CO, Suwa G, WoldeGabriel G (2009) Ardipithecus ramidus and the paleobiology of early hominids. Science 326:75–86 Wolpoff MH (1971) Competitive exclusion among lower Pleistocene hominids: the single species hypothesis. Man 6:601–614 Wolpoff MH, Thorne AG, Jelinek J, Yinyum Z (1994) The case for sinking Homo erectus 100 years of Pithecanthropus is enough! Cour Forsch Inst Senckenb 171:341–361 Wolpoff MH, Senut B, Pickford M, Hawks J (2002) Sahelanthropus or ‘Sahelpithecus’? Nature 419:581–582 Wood BA (1988) Are “robust” australopithecines a monophyletic group? In: Grine FE (ed) Evolutionary history of the “robust” australopithecines. Aldine de Gruyter, New York, pp 269–284 Wood BA (1991) Koobi Fora research project. vol 4: Hominid cranial remains. Clarendon, Oxford Wood BA (1992) Early hominid species and speciation. J Hum Evol 22:351–365 Wood BA (1994) Taxonomy and evolutionary relationships of Homo erectus. In: Franzen JL (ed) 100 years of Pithecanthropus; The Homo erectus problem. Cour Forusch Inst Senckenberg 171:159–165 Wood BA, Collard M (1999a) The human genus. Science 284:65–71 Wood BA, Collard M (1999b) The changing face of Genus Homo. Evol Anthropol 8:195–207 Wood B, Lonergan N (2008) The hominin fossil record: taxa, grades and clades. J Anat 212(4):354–376 Wood B, Martin LB, Andrews P (1986) Major topics in primate and human evolution. Taylor and Francis, London Zipfel B, DeSilva JM, Kidd RS, Carlson KJ, Churchill SE, Berger LR (2011) The foot and ankle of Australopithecus sediba. Science 333:1417–1420

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Index Terms: Ardipithecus 9 Australopithecus 2, 5–6, 10–11 Cladistics 5 Evolution 2 Hominin 1 Homoplasy 5, 14 Homo 5, 8, 14 Kenyanthropus 12 Orrorin 12 Paranthropus 3, 8–9, 12 Parsimony 5–6 Phylogenetic systematics 5 Sahelanthropus 13

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_59-2 # Springer-Verlag Berlin Heidelberg 2013

Phylogenetic Relationships (Biomolecules) Todd R. Disotell* Department of Anthropology, Center for the Study of Human Origins, New York University, New York, NY, USA

Abstract Biomolecules, in particular DNA, assist us in generating and testing hypotheses about human evolutionary history. Molecular analyses testing for and then utilizing a local molecular clock can inform us as to the timing of the split between different lineages or populations. When applied to the split between hominins and chimpanzees, for instance, the molecular clock estimates of their divergence date place constraints on interpretations of the growing fossil record from the Late Miocene and Early Pliocene. The pattern and distribution of modern human variation can be used to extrapolate back in time to infer when and where the modern human gene pool arose. Mitochondrial DNA and Y chromosome sequences and markers have been extensively surveyed in populations from around the world. Numerous nuclear loci and other markers, such as microsatellites and Alu insertions, have similarly been sampled and analyzed. More recently, high-throughput massively parallel sequencing technologies have allowed for the characterization of hundreds of human and nonhuman primate complete genomes. The majority of such analyses point toward a relatively recent origin for modern human diversity from a small population in Africa within the last 200 Ka, with a subsequent dispersal into Eurasia less than 100 Ka though there is some debate as to the timing of these events. While analyses of ancient mitochondrial sequences from archaic hominins strongly suggest that archaic females did not contribute to the modern human mitochondrial gene pool, whole-genome sequences of two archaic populations suggest limited interbreeding with modern humans in Eurasia but not Africa. Analyses of modern African genomes suggest that some populations also interbred with an as yet unknown archaic population or populations. Thus, while a complete replacement of archaic populations by African-derived modern humans is no longer fully tenable, only a limited amount interbreeding between anatomically modern human populations and archaic forebears is likely to have taken place.

Introduction Over 100 years ago, George Nuttall began his book, Blood Immunity and Blood Relationship, with a discussion of the classification of the order Primates stating, “The persistence of the chemical blood-relationship between the various groups of animals serves to carry us back into geological times, and I believe that we have but begun the work along these lines, and that it will lead to valuable results in the study of various problems of evolution” (Nuttal 1904, p. 4). We now know that biomolecules, in particular DNA, can inform us about phylogeny and population history, selection, and perhaps even taxonomy. Inferences drawn from molecular analyses can provide insights into at least three areas of hominin history. The first is the timing of the hominin–chimpanzee split, which in turn may provide a background for interpreting the growing Late Miocene–Early Pliocene hominin and hominid fossil record. The second is the origins of *Email: [email protected] Page 1 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_59-2 # Springer-Verlag Berlin Heidelberg 2013 H. neanderthalH. ensis Denisovans heidelberd gensis b c Homo e sapiens f H.

1

Pan

H. floresiensis H. erectus

antecessor H. habilis

2

Au. sediba

Au. garhi Au. africanus

H. ergaster

H. rudolfensis Au. bahrelghazali

3

Kenyanthropus platyops

4

P. boisei P. robustus

P. aethiopicus

Au. afarensis

Au. anamensis

Ardipithecus ramidus

5 Ardipithecus kadabba 6 7

a Sahelanthropus tchadensis

Orrorin tugenensis

Ma

Fig. 1 Time ranges of hominin species (After Wood 2010). Gray ovals represent the six places where molecular information may be informative. (a) The timing of the split between hominins and chimpanzees, (b) the origins of the modern human gene pool, (c) the diversity and origin of the Neanderthal gene pool, (d) the diversity and origin of the Denisovan gene pool, (e) the time of divergence between Neanderthals and Denisovans, and (f) the time of divergence between the common ancestor of Neanderthals and Denisovans and that of modern humans

modern human populations by extrapolating into the past by examining the pattern of modern human molecular variation. Finally, Middle to Late Pleistocene fossils such as the Neanderthals and Denisovans have now successfully yielded DNA sequence information which allows us to draw inferences back to the point at which the modern and archaic lineages originated (see Fig. 1)

History Nuttall’s research, carried out shortly after the discovery of blood groups in 1901, was based on qualitative and quantitative measures of the immunological reactions of various proteins in the blood. Immunological approaches were improved and systematically applied to questions about primate evolutionary history extensively in the 1960s through the works of Goodman (1961, 1963) and Sarich and Wilson (1966, 1967). It was also during this period that the concept of the molecular clock was first proposed (Zuckerkandl and Pauling 1962). By the 1970s, research increased directly at the DNA level, though only using approximate methods such as DNA–DNA hybridization and restriction mapping to measure the differences between species, populations, and individuals. This time period also saw the development of chromosomal banding techniques for evolutionary analysis (Chiarelli 1966; Dutrillaux 1979; Yunis and Prakash 1982). These techniques have been further developed and have helped us understand the rearrangements that are both shared and differ between humans and other primates using fluorescence in situ hybridization (FISH) and reciprocal chromosomal painting (Weinberg and Stanyon 1998). Chromosomal techniques are generally only used clinically within modern humans as our level of chromosomal variation is extremely low. Techniques that directly measure differences at the DNA sequence level have advanced greatly in the last three decades. Earlier studies of species and population differences utilized restriction endonucleases, enzymes that cut a strand of DNA at a particular short sequence pattern, to estimate either genetic distances or to provide phylogenetically informative characters between individuals in Page 2 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_59-2 # Springer-Verlag Berlin Heidelberg 2013

the sample. Until 2005, the majority of molecular information was derived using a variety of manual to semiautomated technologies that allowed DNA sequences or microsatellite allele sizes to be relatively rapidly determined. The use of the variants of the polymerase chain reaction (PCR) allowed for minute samples from a variety of biomaterials including blood, saliva, hair, feces, bones, teeth, and other biological materials to be amplified and/or sequenced from only a few molecules of DNA. Amplification was generally followed by gel or capillary electrophoresis to determine sequences or allele sizes. Practical constraints required the use of either relatively short sequences (hundreds to tens of thousands of bases) or variable markers such as retroelements, microsatellites, and SNPs. One popular class of molecular markers consists of retrotransposable elements, including short interspersed elements (SINEs) and long interspersed elements (LINEs). SINEs, particularly the Alu family, which exists in over 500,000 copies in human genomes, can vary in number and location between individuals and populations (Batzer et al. 1996). Because the absence of an Alu element at a particular location in the genome is the ancestral condition, the shared presence of an element is most likely indicative of common descent. Similarly, the longer LINE elements, which make up over 15 % of human genomes, can be used as markers of common evolutionary descent (Sheen et al. 2000; Boissinot and Furano 2005). Extremely variable short tandem repeats (STRs), also known as microsatellites, have also proven useful in individual identification and parentage assessment and to infer population relationships based on the analysis of the frequencies of different allele sizes (Bowcock et al. 1994). SNPs continue to be used to infer population relationships and evolutionary history (Yu et al. 2002). Another class of genomic DNA elements is the endogenous retroviruses, which make up a surprisingly large portion of the human genome. Their type, copy number, and positions within the genome vary between populations, so they can provide useful evolutionary markers in the same way as the retrotransposable elements mentioned above (Turner et al. 2001). Extragenomic molecular data from pathogenic and commensal organisms can also be useful in inferring human evolutionary history. Tapeworm, lice, and stomach bacteria sequences have all been used to generate and test hypotheses about human population relationships and migrations (Hoberg et al. 2001; Disotell 2003; Leo and Barker 2005). Single-nucleotide polymorphisms (SNPs) are typically characterized using DNA microarrays in which DNA probes for variants that are to be identified are usually attached to a solid surface. A DNA sample is then passed over the microarray to allow for hybridization of the source DNA to the probes which are then detected by fluorescence or chemiluminescence indicating a match. Current DNA microarrays can detect up to nearly two million SNPs, copy number variants, or other markers at once. Beginning in 2005, several new sequencing platforms were developed that generate several orders of magnitude more data than previous methods, at dramatically reduced cost (Mardis 2013). Often referred to as Next Generation (NextGen) technologies, Second Generation (2ndGen) is probably a better term as there will always be a next generation. Though multiple platforms and methods are used, they all basically share several commonalities. First, rather than cloning or amplifying the DNA in advance, different synthetic adapters are added to the source DNA depending upon the platform used, and the fragments are amplified on a solid surface, either glass or a tiny bead, to which the adapters bind. Then the bound amplified fragments are sequenced by adding nucleotides that are detected one at a time as they are incorporated into the amplified clusters. The sequencing and detection step is carried out in a massively parallel manner so that hundreds of thousands to millions of DNA fragments are sequenced simultaneously. One downside to these techniques is that they generate relatively short sequences (from 50 to 60 to a few hundred bases Page 3 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_59-2 # Springer-Verlag Berlin Heidelberg 2013

long), with a relatively high error rate. These then need to be assembled into a genome or portion of a genome usually be comparing them to a closely related reference genome. The completion of the first human genomes in 2001 by Lander et al. (2001) and Venter et al. (2001) was followed in 2005 by a complete draft of the chimpanzee and, in 2007, the macaque genomes, using conventional sequencing approaches allowing for even more sophisticated comparative analyses (Chimpanzee Sequencing and Analysis Consortium 2005; Rhesus Macaque Genome Sequencing and Analysis Consortium 2007). Second-Generation technologies were used to sequence the orangutan (Locke et al. 2011), gorilla (Scally et al. 2012), and bonobo (Pr€ufer et al. 2012) genomes. These genomes have not only allowed for far more in-depth analyses of the similarities and differences among the various ape lineages but provide information useful in inferring the polarities of molecular characters that vary among humans. Finally, molecular data are being used to investigate the differences between humans and our primate relatives through studies of copy number variation, gene expression, epigenetics, and other underlying molecular and developmental processes; but these issues are beyond the scope of this review (e.g., Enard et al. 2002; Cheng et al. 2005; Eckhardt et al. 2006; Sudmant et al. 2013; Pääbo 2014).

Hominin Origins Molecular studies have been used to draw inferences about the possible Eurasian origin of the African hominids including the ancestor of hominins, though not without controversy (Miyamoto et al. 1998; Stewart and Disotell 1998; Moyà-Solà et al. 1999; Heizmann and Begun 2001; Begun et al. 2012). However, until the discoveries of the Late Miocene hominids and/or hominins including Ardipithecus, Orrorin, and Sahelanthropus (Haile-Selassie 2001; Senut et al. 2001; Brunet et al. 2002), little could be said about origin of the hominin lineage itself. In fact, only its date, approximately 6 Ma, inferred from molecular clock estimates was available (Chen and Li 2001; Wildman et al. 2003). This date estimate is also not without controversy, though significantly older dates put forth by Arnason et al. (1996, 1998) and supported by Tavare et al. (2002) do not appear to be supported by more detailed molecular analyses (Raaum et al. 2005). Recently a new debate has broken out over estimating divergence dates with molecular data. Typically, comparisons between two lineages for which good fossil evidence provides the age of at least one of them are converted into rates of change per year. This is of course dependent not only on proper placement of a fossil but also its appearance in the record near the point of divergence. Nevertheless, multiple estimates within the catarrhines have relatively consistently suggested a rate of approximately 1.0  10 9 bp 1 year 1 (Takahata and Satta 1997; Green et al. 2010). With wholegenome analyses now common and relatively inexpensive, a direct estimation of the human mutation rate can be estimated by examining parent–offspring triads across the whole genome. With a known mutation rate and an estimate of the generation time for the taxa being investigated, divergence dates can be estimated. Coupled with new estimates of generation times for human, chimpanzees, and gorillas (Langergraber et al. 2012), an overall rate of approximately 0.5  10 9 bp 1 year 1 or about half the previous rate has been estimated (Roach et al. 2010; 1000 Genomes Project Consortium 2010; Scally and Durbin 2012). However O’Roak et al. (2012) do not find such a slow rate in their whole-genome family triad study. Ho et al. (2011) provide an excellent discussion of the discrepancy in rates of evolution determined at different timescales, at both the morphological and molecular levels.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_59-2 # Springer-Verlag Berlin Heidelberg 2013

Fu et al. (2013) provide a third way of estimating molecular rates of evolution, at least for the mitochondrial genome. By sequencing mtDNA in fossils dated to within the last 40,000 years (the reliable range of radiocarbon dating), they can measure the effect of “branch shortening” in which fossil lineages are missing the substitutions that would have occurred had they survived to the present. The number of missing substitutions coupled with the dates of the samples provided remarkably consistent rates. These rates when applied to mitochondrial trees provide divergence estimates that fall within the range of the classically accepted dates discussed below. When high enough quality whole-genome data become available, this technique will be applied to nuclear DNA as well (Green and Shapiro 2013). It should not come as a surprise that, with whole genomes of the apes available, the interpretation of when speciation occurred has become more complex. For instance, 15 % of the sequences in the western lowland gorilla genome are most similar to those in humans, and 15 % are most similar to those in chimpanzees despite the overall closer relationship of chimpanzees to humans (Scally et al. 2012). Furthermore, 3 % of the human genome is more closely related to chimpanzees or bonobos than they are to each other (Pr€ ufer et al. 2013). These differences in gene lineages from the overall pattern of speciation may be due to several phenomena. In incomplete lineage sorting, ancestral polymorphism or variation in the common ancestral population may be partitioned into descendent populations and ultimately descendent species such that individual genes do not match the species phylogeny. If there is gene flow between the ancestral populations or the incipient species, the gene phylogeny may similarly differ from the species phylogeny. Thus, care must be taken in interpreting molecular divergence dates, especially those derived from concatenated datasets and whole genomes. With the discovery of these Late Miocene fossils, numerous phylogenetic hypotheses were put forth suggesting their hominin status (Haile-Selassie 2001; Brunet et al. 2002) or that only one was an early hominin and the others were either fossil chimpanzees or gorillas or broadly ancestral to both the human and chimpanzee lineages (Senut et al. 2001). Given the vast amount of molecular data collected to assess the relationships among African apes including humans, “. . . genetic data can also give us trees that are well enough proportioned to be useful to us as paleontologists and that can provide constraints on our ‘flights of fancy,’ when calibrated by plausible paleontological or other historical data” (Pilbeam 1995). An approximately 6 Ma split between humans and chimpanzees (see Fig. 2), for instance, makes untenable the phylogenetic proposal put forth by Senut et al. (2001), in which Ardipithecus falls along the chimpanzee lineage and Orrorin falls well within the hominin lineage more than 2.5 Ma after a human–chimpanzee divergence (assumed by Senut et al. to have occurred around 8.5 Ma). On the other hand, if the purported much slower rate of evolution is applied, the human–chimpanzee split (and all others) becomes much older. Hawks (2012) points out that if older divergence dates are accepted, then fossils such as Chororapithecus at 10.5 million years old could indeed fall along the gorilla lineage as claimed by Suwa et al. (2007). The gorilla affinities of Chororapithecus have, however, been disputed by others (Gibbons 2007). Overall, given that the phylogenetic approach to estimating divergence dates and the method using missing substitutions from fossils concur and the whole-genome family triad methods give suspiciously ancient divergence estimates for many primate lineages, it is probably best to continue to use the faster rate estimates when inferring dates. An interesting proposal put forth by Wildman et al. (2003) using a combination of lineage divergence estimates based both on molecular and fossil data would substantially revise the taxonomy of all hominins and our close relatives, the chimpanzees. They propose a time-based phylogenetic classification/taxonomy linking the timing of the origin of a clade to its taxonomic level for most catarrhines. In their scheme, because chimpanzees and humans share a recent Page 5 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_59-2 # Springer-Verlag Berlin Heidelberg 2013 0

Pan

Homo

1 2

Australopithecines

3 Praeanthropus

4 Ardipithecus 5

Orrorin

6 7 8 9 10

Samburupithecus Ma

Fig. 2 Potential phylogenetic relationships of Late Miocene and Early Pliocene hominins and hominids. Black lines and ranges after Senut et al. (2001); gray line represents the molecular clock estimate of the divergence of hominins and chimpanzees (Chen and Li 2001; Wildman et al. 2003)

common ancestor at only 6 Ma, chimpanzees would be classified within the genus Homo as Homo (Pan) troglodytes and Homo (Pan) paniscus. Consequently, all genera of hominins, including Australopithecus, Paranthropus, and Kenyanthropus, would necessarily be sunk into the genus Homo. Depending on their phylogenetic positions and divergence dates, Sahelanthropus, Orrorin, and Ardipithecus might similarly be included within Homo. While the chaos and difficulty of adopting this strategy are apparent, the underlying phylogenetic logic is appealing.

Modern Human Origins Most studies of blood group allele frequencies and protein polymorphisms carried out in the 1960s and early 1970s that presented their findings in the form of a phylogenetic tree posited a basal split between Asians and an Afro-European cluster. In 1974, Nei and Roychoudury (1974) analyzed 21 blood group systems and 35 polymorphic proteins from which they inferred an initial African versus European–Asian split. In this rather prescient chapter, they extrapolated from estimated amino acid replacement rates and inferred that the basal split between Africans and Eurasians occurred approximately 120 Ka and that Europeans and Asians split around 55 Ka. Few additional studies attempting to infer modern human origins were carried out until the late 1980s. Two seminal papers published in the late 1980s by Cann et al. (1987) and Vigilant et al. (1989), both working in Allan Wilson’s laboratory at the University of California at Berkeley, inferred a less than 200 Ka African origin for all human mitochondrial DNA (mtDNA) and, by extrapolation, perhaps for all modern populations. Known by various names, the “Mitochondrial Eve” or “Out-ofAfrica” hypothesis, will hereafter be referred to as the Recent African Origin (RAO) model. This model stands in contrast to the regional continuity or multiregional (MRE) model in which local populations are thought to derive from the original groups that migrated into the various regions of the Old World over 1 Ma from Africa, with various amounts of gene flow between the different Page 6 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_59-2 # Springer-Verlag Berlin Heidelberg 2013

regions ever since (Wolpoff et al. 2000). Cann et al.’s (1987) study was based on phylogenetic inferences drawn from parsimony analysis of high-resolution restriction mapping of the whole mtDNA genome. To counter criticisms of the precision of restriction mapping, the geographical sampling, and the lack of an outgroup in Cann et al.’s original analysis, Vigilant et al. (1989) employed one of the first uses of PCR utilizing hair samples to generate nucleotide sequences in a phylogenetic analysis, followed by a sequence-based analysis with a much larger sample size (Vigilant et al. 1991). Through sequencing the D-loop or control region of the mtDNA genome, they were able to align human sequences with those of a chimpanzee in order to carry out a parsimony analysis rooted by an outgroup. The results were remarkably congruent with those of Cann et al. (1987), in inferring a similar timing and location for the origin of all contemporary human mtDNA: approximately 200 Ka in Africa. The initial papers of Cann et al. (1987) and Vigilant et al. (1989, 1991) came under criticism for an important analytical flaw. Their parsimony trees suggesting a recent African ancestry for all modern mtDNA were derived from heuristic search strategies that did not find the most parsimonious trees for their respective data sets. Other researchers were able to infer trees without African roots that were more parsimonious (Maddison et al. 1992; Templeton et al. 1992). Since no search strategy is available to guarantee the most parsimonious tree is found for such large data sets, alternative strategies were utilized to infer the root of the modern human mtDNA tree. However, Stoneking et al. (1992) and Sherry et al. (1994) demonstrated that the much greater amount of mtDNA diversity found within Africa compared to outside of it was best explained by a longer period of time for it to accumulate within Africa. Additional smaller data sets chosen to represent the most diverse human sequences possible were also analyzed, and an African origin for modern mtDNA types was inferred (Kocher and Wilson 1991). Additional molecular dating inferences also supported the approximately 200 Kyr time frame inferred to explain human mtDNA diversity (Ruvolo et al. 1994). A huge number of human complete mitochondrial genome sequences has been collected and subjected to phylogenetic and population genetic analyses. Due to the rapid rate of evolution of the mtDNA genome, short sequences such as those found in the D-loop or control region are not always useful over long timescales and may show spurious clustering due to homoplasy or multiple substitutions at the same site, including saturation of substitutions at a site. One solution when available is to characterize both the fast-evolving control region and several more slowly evolving region of the mtDNA genome to define haplogroups or related lineages of mtDNA haplotypes. In fact, sequencing the complete 16.5 kb mtDNA genome has become commonplace (Ingman et al. 2000; Herrnstadt et al. 2002). By the end of 2013, more than 20,000 complete human mitochondrial genomes had been deposited in GenBank. Such analyses show more geographic partitioning of mtDNA sequences than previous studies based on much shorter sequences revealed. Unfortunately, the nomenclature for major mtDNA lineages has developed haphazardly, mostly by time of definition and not with phylogenetic relationships in mind. In fact, most haplogroups are defined by the number of substitutions that they differ from the first complete human mtDNA sequence (a European) published (Anderson et al. 1981). A recent proposal has been put forth to redefine the mtDNA tree from its root, by inferring the common ancestral human mtDNA haplotype through analyzing 8,216 modern mitogenomes along with those from six Neanderthals (Behar et al. 2012). Seven major lineages (L0–6) have been defined for African mtDNA haplotypes, while two macro-haplogroups (M and N) contain all Eurasian lineages which are derived from African L3 (Kivisild et al. 1999; Herrnstadt et al. 2002). Sub-haplogroups of macro-haplogroup M are almost exclusively found among contemporary Asians along with a small number of individuals in Africa presumably due to back migrations (Gonzalez et al. 2007). Macro-haplogroup N contains around

Page 7 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_59-2 # Springer-Verlag Berlin Heidelberg 2013

Pre do mi na ntl y

As ia n

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A

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ly nt

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L6

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Fig. 3 Mitochondrial DNA haplogroup phylogeny with arbitrary branch lengths (Modified from Ruiz-Pesini et al. 2007 and Behar et al. 2012)

a dozen sub-haplogroups that are found predominantly in Europe with another seven that are found in Asia and the Americas (see Fig. 3). Various criticisms of using mtDNA sequence data that have been put forth include the possibility of nonmaternal inheritance, selection skewing inferences of geographic structure and rates of evolution, and the presence of recombination. To date, no firm evidence of paternal inheritance has been demonstrated in humans (Bandelt et al. 2005). Furthermore, a mechanism that destroys sperm mtDNA has been discovered, making paternal inheritance even more unlikely (Nishimura et al. 2006). Claims for selection acting strongly upon some human mtDNA lineages, especially related to humans’ entry into colder climates, have been put forth (Mishmar et al. 2003; Ruiz-Pesini et al. 2004). Others interpret the evidence for selection as mainly for purifying selection with only a restricted amount of positive selection in a small portion of the mtDNA genome (Elson et al. 2004). Eyre-Walker and Smith (1999) suggested that mtDNA genomes undergo recombination making inferences about their evolutionary history much less straightforward. The suggestion that mtDNA undergoes recombination has been amply countered by further analyses (Macaulay et al. 1999). All in all, mtDNA analyses provide a very powerful tool for inferring the evolutionary history of humans and provide a remarkably consistent story as additional data and techniques are brought to bear. Mitochondria, however, only yield a maternal history of the organisms under study. To better understand the overall evolutionary history of any group, both male-specific and biparentally inherited loci are also needed. The Y chromosome fulfills an analogous paternal role to maternally inherited mtDNA, as the majority of it does not recombine with regions of the X chromosome. This nonrecombining region (NRY) is also referred to as the male-specific portion (MSY) of the Y chromosome. While it was initially thought that little variation was present on the human Y chromosome, increasingly sophisticated molecular analytical techniques have allowed for the discovery of a wealth of variation and potential phylogenetically informative markers. Fortunately, unlike mtDNA, the naming of major lineages or haplogroups was regularized to unambiguously label the clades based upon their phylogenetic structure (The Y Chromosome Consortium 2002).

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_59-2 # Springer-Verlag Berlin Heidelberg 2013 As As mixed

As D Af

F2

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A1 A0

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L

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T

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Eu mixed

S

K P N

As Af

mixed

O As

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R mixed

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Af

Af

Af

Fig. 4 T chromosome haplogroup phylogeny with arbitrary branch lengths. Labels outside terminal nodes describe the geographic origin of the majority of the individuals represented by the haplogroup (Af Africa, Am Americas, As Asia, Eu Europe, Oc Oceania) (Modified from van Oven et al. 2014)

Early major research groups investigating human evolutionary history using Y chromosome markers inferred trees that have their deepest and next deepest roots within African populations (Underhill et al. 2000; Hammer et al. 2001; Jobling and Tyler-Smith 2003) (see Fig. 4). These studies also concurred in inferring a relatively recent African origin, around 100 Ka or younger with a more recent exodus into the rest of the Old World (Hammer et al. 1998; Underhill et al. 2000). This date is more recent than the mtDNA-derived estimate possibly because of the smaller effective population size of the human Y chromosome due to greater variation in reproductive success of males compared with females and the greater geographic structuring of Y chromosome variation. This apparent more recent common ancestry has been called into question by more recent studies involving more markers and more individuals. Cruciani et al. (2011) sequenced ~240 kb to better resolve the deeper lineages. Their study doubled the number of African-specific lineages and estimated the most recent common ancestor (MRCA) at 142 Ka. Another study of 9 mega-base pairs (Mb) from over 1,200 males which using a rate of 0.53  10 9 bp 1 year 1 (which is close to the estimates from triad de novo rates) found a MRCA of ~200 Ka (Francalacci et al. 2013). Mendez et al. (2013) discovered a new Y chromosome lineage in an African American individual that is also found in extremely low frequency in some Central Africans that they name A00. They inferred a MRCA date of 338 Ka and suggested either fundamental reassessment of the models for Y chromosome origins or the possibility of archaic hominin introgression. Elhaik et al. (2014) strongly critiqued Mendez et al.’s (2013) analyses on several grounds and recalculate the MRCA to 208 Ka. An analysis of 69 complete Y chromosome sequences estimates the MRCA between 120 and 156 Ka, in line with mtDNA estimates (Poznik et al. 2013). All these Y chromosome studies concur in the African origin of modern diversity, with the larger analyses placing the timing of this origin within the range of the estimated MRCA for mtDNA depending upon which evolutionary rates and fossil calibration points were used. Pre-Second-Generation sequencing era studies were remarkably consistent. A study of over 10,000 base pairs on a region of the X chromosome with low levels of recombination also is compatible with the mtDNA and Y chromosome results. Kaessmann et al. (1999) found an approximately 535 Ka most recent common ancestor for the alleles of this region. This is broadly consistent with the mtDNA and Y chromosome dates, given that the effective population size of the X chromosome is three times that of the other two loci, so coalescent estimates will be approximately Page 9 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_59-2 # Springer-Verlag Berlin Heidelberg 2013

three times as old as well. A 3,000 bp region of the b-globin locus on chromosome 11 yielded an estimate of 750 Ka, which is again broadly consistent with being four times older then mtDNA and Y chromosome dates (Harding et al. 1997). Nuclear loci such as the compound haplotype composed of an STR locus and an Alu deletion polymorphism on chromosome 12 at the CD4 locus demonstrate a similar pattern to the mtDNA and Y chromosome patterns of variation (Tishkoff et al. 1996). An African origin for the variation at this locus is estimated in the same time frame as that inferred from mtDNA and Y chromosome data with dramatically reduced variation found outside of Africa. Phylogenetic trees derived from numerous microsatellite (STR) loci similarly find their roots within Africa with reduced variation outside of it, though divergence date estimates cannot be easily calculated from such data (Bowcock et al. 1994). A similar pattern is found with SNPs (Yu et al. 2002) and polymorphic Alu insertions (Batzer et al. 1996). Altogether, the majority of analyses of relatively short molecular sequences and markers suggest a recent African origin for the diversity of modern human genomes (Jorde et al. 2000; Takahata et al. 2001; Excoffier 2002; Satta and Takahata 2002). However, interpretations that contradict a scenario of a recent African origin have been put forth (Harris and Hey 1999; Hawks and Wolpoff 2001; Templeton 2005). Harris and Hey (1999), for instance, interpret PDHA1 (an X chromosome locus) sequence diversity as yielding a 1.86 Ma common ancestor, which would fall outside of the range of estimates derived from the above loci. The PDHA1 analysis has been called into question, due to the probability that the locus is under selection which makes inferences as to coalescence dates difficult (Disotell 1999). Nested clade analyses (Templeton 2002, 2005) suggest more than one major exodus from Africa, an early one, approximately 1.9 Ma, one around 600–700 Ka, and a final one around 100 Ka with evidence for range expansion, long-distance dispersal, and isolation by distance complicating the picture. These analyses have generated a healthy skepticism, especially over the efficacy and accuracy of nested clade analysis (Cann 2002; Knowles and Maddison 2002; Satta and Takahata 2002; Panchal and Beaumont 2010). Another approach to understanding our evolutionary history comes from examining the particular patterns of molecular variation found throughout the world. Several studies using microsatellite or short tandem repeat (STR) markers have found patterns that are best explained by a series of serial founder effects emanating from Africa outward to other regions of the world. Both Prugnolle et al. (2005) and Ramachandran et al. (2005) find the amount of genetic variation measured in a variety of ways linearly decreases the further populations are from Africa. Analyses of the several thousandfold increase in amount of human molecular data collected with the advent of microarray SNP typing and Second-Generation (2ndGen) sequencing have corroborated most of the above findings. The Recent African Origin (RAO) model with important caveats discussed in detail below best explains the patterns of human molecular diversity observed today.

Neanderthals, Denisovans, and Other Archaic Hominins Another opportunity for biomolecules to shed light on hominin phylogeny involves the direct characterization of DNA from fossils. While the earliest analyses of ancient hominin DNA focused on mtDNA, 2ndGen technologies now allow entire genomes to be sequenced. The presence of hundreds to thousands of copies of the mtDNA genome in most cells makes it an ideal candidate for extraction from poor or degraded sources of tissue, such as teeth and bone, including fossils. Ancient DNA (aDNA) analyses are however fraught with difficulties (Cooper and Poinar 2000; Mulligan 2005). Ancient DNA, when present, even under ideal preservation conditions is likely to be Page 10 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_59-2 # Springer-Verlag Berlin Heidelberg 2013

damaged and fragmented. More importantly, it is almost certainly contaminated with modern DNA from the environment, excavators, curators, scientists who have handled the material, and molecular laboratory personnel. Extraordinary precautions and techniques need to be carried out to lower the probability of mistakenly accepting such modern contaminants as the sequences from the ancient material (Cooper and Poinar 2000; Mulligan 2005). Despite these difficulties, aDNA provides a unique and important window in the evolutionary history and processes. By the end of 2007, partial mtDNA sequences from around 18 Neanderthal individuals have been gathered (Krings et al. 1997; Ovchinnikov et al. 2000; Schmitz et al. 2002; Serre et al. 2004; Beauval et al. 2005; Lalueza-Fox et al. 2005; Caramelli et al. 2006; Lalueza-Fox et al. 2006; Orlando et al. 2006; Krause et al. 2007). These sequences form a reciprocally monophyletic clade with the thousands of modern human mtDNA sequences analyzed to date and are estimated to have diverged from modern humans somewhere between 365 and 853 Ka, with an average between 550 and 600 Ka. Even with this preliminary sampling of multiple individuals from different time periods and geographic locations, it is unlikely that a Neanderthal sequence that falls within the modern mtDNA gene pool will be discovered (Krings et al. 2000). Wolpoff (1998) suggested that because the original Feldhofer Neanderthal sequence is more similar to some modern human sequences than some other modern sequences are to other moderns, their mtDNA gene pools overlapped. This however was a misleading analysis as a cladistic analysis of the same data clearly demonstrates a complete separation of Neanderthals and moderns into reciprocally monophyletic clades (Disotell 1999). This observation has been further strengthened by all additional Neanderthal sequences and molecular analyses. These Neanderthal sequences do not cluster among modern European sequences, as might be expected if they gave rise to the Europeans or extensively interbred with the new migrants into Europe as would be predicted under the multiregional model. However, both Nordborg (1998) and Relethford (2001) point out that different amounts of crossbreeding between Neanderthals and early moderns could have still been possible with the Neanderthal mtDNA lineages having gone extinct due to normal stochastic processes over the last 30 Ka. The Neanderthal sequences do show geographic and temporal structure however. The oldest sequences and eastern-most Neanderthals cluster together to the exclusion of western European samples younger than 48 Ka. Fabre et al. (2009) and Dalén et al. (2012) suggest that the western population may have experienced a bottleneck and population replacement while the eastern populations were more stable through time. To further test hypotheses of modern human origins, several researchers have attempted to recover and sequence early modern human aDNA. One of these attempts provides a good illustration of the numerous difficulties of aDNA analysis. Adcock et al. (2001) claimed to have recovered an mtDNA sequence from an early modern human fossil skeleton from Australia, known as Lake Mungo III, then thought to date to approximately 60 Ka [this specimen has since been redated to 40 Ka (Bowler et al. 2003)]. The sequence fell outside of the range of modern human mtDNA diversity and clustered with a sequence located on chromosome 11 of the modern human genome, a known mitochondrial pseudogene (numt). Their interpretation was that early modern humans reached Australia before the most recent African exodus that gave rise to the rest of the world’s mtDNA diversity less than 100 Ka. This analysis seems deeply flawed for several reasons. First, the standard protocols suggested to avoid contamination with modern DNA (Cooper and Poinar 2000; Mulligan 2005) were not rigidly followed (Cooper et al. 2001). The sequence is most likely in fact a contaminating numt or has been damaged to yield spurious nucleotide substitutions (Cooper et al. 2001). Smith et al. (2003) point out that it is extremely unlikely for aDNA to have survived at the Lake Mungo site due to the environmental conditions present. Finally, reanalysis with additional Page 11 of 25

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Australian and African sequences yields a tree very different from that originally put forth (Cooper et al. 2001). Caramelli et al. (2003) attempted to sequence several early modern specimens from Paglicci Cave in Southern Italy. Their sequences fully fall within the range of modern human sequences. These sequences are therefore either modern contaminants, or early modern mtDNA sequences indeed fall within the range of all modern mtDNA present today. Serre et al. (2004) therefore took a different approach to investigating early modern human and Neanderthal mitochondrial diversity. They realized that demonstrating the presence of early modern mtDNA at that time was nearly impossible, so they tested five early modern fossil samples along with four Neanderthal samples for the presence of Neanderthal-specific mtDNA motifs. Included among the early human samples were fossils from Vindija, Croatia, and Mladeč (Czech Republic) that have been claimed to be transitional between Neanderthals and early moderns (Wolpoff 1999). Their reasoning was that, if interbreeding occurred between the two groups, the presence of Neanderthal mtDNA in early modern individuals would be more likely since it would not have had a great amount of time to go extinct as Nordborg (1998) and Relethford (2001) potentially proposed for the absence of Neanderthal mtDNA today. Serre et al. (2004) were able to amplify all four Neanderthal samples with “Neanderthal-specific” primers. None of the early modern human fossils yielded amplification products, though they did for more generalized “hominoid-specific” primers, suggesting DNA was present. Furthermore, faunal samples from the same sites all yielded DNA products, suggesting that the conditions at the sites were adequate for the preservation of aDNA. Currat and Excoffier (2004) carried out a simulation study to model the conditions necessary to detect Neanderthal introgression with mtDNA. They extensively modeled different scenarios of modern human expansion into Europe with competition and admixture with Neanderthals. They found the mtDNA data at the time was only compatible with a less than 0.1 % interbreeding rate that would mean fewer than 120 matings over a 12,000-year period of overlap. One of the most important components of their model demonstrated that at the leading edge of an expanding population where interbreeding is most likely acts like a wave carrying new mutations and introgressed alleles to higher and higher frequencies. This iterative founder effect phenomenon is often referred to as “surfing the wave.” With development of 2ndGen sequencing methods, the potential of retrieving archaic hominin nuclear DNA improved dramatically. The first such studies (Noonan et al. 2006; Green et al. 2006) sampled a 38 Ka specimen (Vi-80) from Vindija Cave, Croatia, whose mtDNA analysis suggested contained 98 % endogenous Neanderthal DNA and only 2 % modern human contamination. Noonan et al. (2006) directly cloned DNA from the specimen (without amplification) and generated 62 kb of Neanderthal DNA. The sequences had the particular patterns of damage usually found in ancient DNA and were thus of presumed Neanderthal origin. They estimated an average divergence time between their sequences and those of modern humans at 706 Ka with the population split at 370 Ka. Divergence time estimates for different loci within the genome will almost always be older than the population split, because nearly all populations have some level of variation within them. One test for the populations’ divergence date is to look at variants within each population. For instance, if modern humans and Neanderthals separated a long time ago, Neanderthals would only rarely have the derived version of a modern human variant because if the variant appeared only in the modern lineage, and not in the common ancestor of modern humans and Neanderthals, the derived modern variant would not be found in Neanderthals. On the other hand, if Neanderthals and modern humans split recently or were significantly admixed, then derived modern human variants should be

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_59-2 # Springer-Verlag Berlin Heidelberg 2013

common in the Neanderthal genome. With only three derived modern human variants in their Neanderthal sample, Noonan et al. (2006) concluded that little to no interbreeding had occurred. Green et al. (2006) using the same sample as Noonan et al. (2006) generated more than a million bases of sequence using a standard 2ndGen technique involving bead-based amplification. They estimated a divergence time of 516 Ka and found 30 % of the SNPs were identical to human-derived alleles. From this, they concluded significant admixture occurred. However, Wall and Kim (2007) demonstrated that much of Green et al.’s (2006) sequence was modern human contamination most likely introduced in the commercial facility utilized for the final sequencing. Thus, as of 2007, there was little evidence of any Neanderthal admixture with modern humans (Hodgson and Disotell 2008). Using 2ndGen sequencing techniques, Green et al. (2008) generated a complete mtDNA genome from a Neanderthal from Croatia (Vindija 33.16). Briggs et al. (2009) sequenced five additional complete mtDNA Neanderthal genomes including Feldhofer 1 and 2, Vindija 33.25, El Sidrón in Spain, Mezmaiskaya 1, and Mezmaiskaya 2 (only a partial mtDNA genome) using a 2ndGen approach that targeted mtDNA. The younger individuals (38–70 Ka) had only about a third of the variation found in modern humans today, while the oldest sample was most divergent. The Mezmaiskaya 2 individual, despite only being 42 Ka, clustered with the younger western Neanderthals. A complete mtDNA genome from a 30 Ka modern human sample from Kostenki, Russia, was also sequenced using these techniques (Krause et al. 2010a). It clusters inside modern human haplogroup U2, which is common in North Africa, western Asia, and Europe. With over two-dozen Neanderthal individuals sampled as of 2009, there was no evidence of mtDNA gene flow with modern humans (Currat and Excoffier 2004; Serre et al. 2004; Hodgson and Disotell 2008). With no sign of Neanderthal mtDNA in the tens of thousands of modern humans sampled to date, it was suggested that Neanderthal–human hybrids would have been rare while male hybrids might be sterile (Mason and Short 2011). According to Haldane’s rule, the heterogametic sex in interspecific hybrids will be absent, rare, or sterile (Short 1997). Improvements to 2ndGen sequencing techniques and new ways of avoiding or at least identifying contamination allowed Green et al. (2010) to successful produce a complete draft Neanderthal genome to 1.3-fold coverage. They generated 5.3 gigabases (Gb) of sequence from three Croatian female Neanderthal samples, using two different techniques that reduced microbial background and enriched the endogenous DNA present in the bones. They were able to cover about 60 % of the Neanderthal genome with less that 1 % error (Green et al. 2010). Along with the complete genomes of five diverse humans and small amounts of sequence from El Sidón, Feldhofer Cave, and Mezmaiskaya Neanderthals, they estimate the population split between humans and Neanderthals at occurred 270–440 Ka. Since modern human mtDNA coalesces around 200 Ka, the Neanderthal–human population split falls within the range of coalescence for nuclear genes (four times that of mtDNA). Therefore, it is expected that many alleles should be shared between humans and Neanderthals. Green et al. (2010) found an excess of shared alleles between Neanderthals and the genomes they sampled from a French, Han Chinese, and Papua New Guinean individual but not two Africans (San and Yoruba). This suggests that non-African populations share more ancestry than African populations with Neanderthals, indicating some level of admixture. Interestingly enough, the Chinese and Papuan individuals share as much ancestry with Neanderthals as the French individual. By examining the extended haplotypes (regions of the genome that are similar between two individuals), they noted longer haplotypes in Neanderthals and non-Africans than in Africans. This suggests that the admixture was recent, since these regions were not broken up by recombination. Page 13 of 25

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Green et al. (2010) estimated between 1 % and 4 % of non-African modern human alleles introgressed from Neanderthals. Furthermore, this gene flow was within the last 100 Kyr. They proposed two alternate scenarios to explain this admixture. Since the Neanderthal–human split occurred within the time frame in which modern human nuclear DNA diversity developed, if there was ancient substructure, the African modern human population, some African populations could be more closely related to Neanderthals than to others. If such a population or populations also later gave rise to the modern humans that exited Africa, non-Africans and Neanderthals would share more alleles than Neanderthals and other Africans. Given that only two African individuals were sampled, this could not be ruled out. Eriksson and Manica (2012) note that any analyses of potential admixture need to take such substructure into account. Yang et al. (2012) carried out simulations and compared them to data from the Complete Genomics Diversity Panel (Drmanac et al. 2010) and concluded that ancient African substructure does not explain Green et al.’s (2010) finding. Eriksson and Manica (2014) however argue that Yang et al.’s (2012) simulations were inadequate and ancient population substructure cannot be ruled out. Green et al.’s (2010) favored scenario is that admixture occurred shortly after the modern human exodus from Africa carrying Neanderthal alleles both into western Asian and Europe as well as eastern and southeast Asia. One estimate of the timing of this potential gene flow is between 37 and 80 Ka (Sankararaman et al. 2012). Hodgson et al. (2010) suggested an alternative hypothesis in which limited admixture occurred slightly earlier, when African fauna and early modern humans expanded into western Eurasia around 100 Ka before retreating back into Africa due to climatic shifts. Neanderthal alleles would then be present in low frequency in northeast Africa. Populations from there later migrated out of Africa, either through the Sinai, the Arabian Peninsula, or both, carrying these alleles with them into Eurasia several tens of thousands of years later. These alleles would have become more common due to the iterative founder effect, surfing the wave to higher and higher frequencies in Europe and Asia (Currat and Excoffier 2004, 2011). Updating their admixture models based on mtDNA (Currat and Excoffier 2004) to whole genomes, Currat and Excoffier (2011) found that under a wide variety of demographic scenarios, very low levels of interbreeding would be necessary to yield 1–4 % admixture. They further speculate that there would have been some kind of avoidance of interspecific mating or lower fitness in hybrids. They estimate that during the entire time and range of overlap, as few a few hundred matings may have occurred. Depending upon when and where those events occurred, different populations and different individuals are likely to share different Neanderthal alleles (Wills 2011). Vernot and Akey (2014) and Sankararaman et al. (2014) infer that up to 20–30 % of the Neanderthal genome is spread out among modern humans, a few nonoverlapping percent at a time. With the continuing improving methodologies to extract and manipulate ancient DNA and higher and higher throughput 2ndGen sequencing technologies, an entire mtDNA genome followed by a 1.9 coverage full genome was generated from a 50 Ka partial juvenile distal phalanx and a single molar from Denisova Cave in the Altai Mountains of southern Siberia (Krause et al. 2010b; Reich et al. 2010). Using new techniques and remaining fragments of the phalange and some of the original extracted material, Meyer et al. (2012) generated a much higher coverage (31) Denisovan genome which covers 99 % of the “mappable” genome. Despite being only 100 km from known Neanderthal sites, the Denisovan mtDNA genome is equally distantly related to both Neanderthals and modern humans, diverging around 1 Ma (Krause et al. 2010b). This date is too late to belong to Homo erectus and too early for the common ancestor of modern humans and Neanderthals. The Denisovan nuclear DNA on the other hand clusters with Neanderthals with an average divergence around 640 Ka. The discrepancy between the mtDNA and nuclear divergence dates between Denisovans and Neanderthals could have two possible explanations. The Denisovans may have hybridized with an Page 14 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_59-2 # Springer-Verlag Berlin Heidelberg 2013

as yet unknown archaic hominin that migrated out of Africa after Homo erectus but before the common ancestor of Neanderthals and modern humans. Or, if the population that gave rise to Neanderthals and humans was quite variable and included the Denisovan haplotype, that haplotype may have gone extinct in both the modern human and Neanderthal lineages. This is known as incomplete lineage sorting. To date, neither of these hypotheses can be ruled out. As interesting as the discovery of potential admixture between Neanderthals and Eurasians is the finding that up to 4.8 % Denisovan alleles are found in Melanesians (Reich et al. 2010). Along with 2.6 % Neanderthal ancestry, Melanesians may have up to 7.4 % of their genome composed of alleles found in archaic hominins. Denisovan alleles are also found in aboriginal Australians, near Oceanic, Polynesian, Fijian, and east Indonesian, but not south Asian or east Asian populations (Reich et al. 2011). Denisovans were also not very diverse, with only about 20 % of modern African and ~30 % of the variation found in Eurasians. There is also a reduced amount of admixed X chromosome alleles potentially suggesting it was mostly male-mediated gene flow. Unfortunately, all archaic genomes generated to date come from females, so we do not know what archaic Y chromosomes look like. A toe phalanx discovered in 2010 in Denisova Cave has yielded an extremely high-quality (52 coverage) genome of a female Neanderthal (Pr€ ufer et al. 2013). With two high-quality archaic genomes now available, it was possible to estimate that the common ancestor of Denisovans and Neanderthals split from the modern human lineage between 553 and 589 Ka, while the two archaic lineages split approximately 381 Ka. The Altai Neanderthal was relatively inbred and probably derived from a population that went through a severe bottleneck. The higher-quality genomic data also reduce the amount of Neanderthal DNA thought to have introgressed into Eurasians to 1.5–2.1 %. Given that the branch length of the genome derived from the toe is shorter than the one derived from the finger, it is thought to be from slightly older sediments. Further complicating the picture of admixture among the various hominins of the Middle Pleistocene is the observation that the mtDNA genome sequenced from a specimen from Sima de los Huesos in Spain is related to Denisovan mtDNA (Meyer et al. 2014). The Sima de los Huesos and Denisovan mtDNA genomes diverged around 700 Ka. The femur from which it was derived is classified as Homo heidelbergensis and is from sediments dated to over 300 Ka. Estimating the number of missing substitutions in the mtDNA genome, that is, those that would have occurred since the individual died, yields an expected age of 400 Kyr. Meyer et al. (2014) suggest that the most plausible evolutionary scenario is that the Sima de los Huesos hominins are broadly ancestral to both Denisovans and Neanderthals, which somehow maintained two deeply divergent mtDNA lineages. Multiple scenarios are thus available to explain the complex patterns of relationships among the various Middle Pleistocene hominins and modern humans. The amounts, directions, and timings of introgression events are under healthy debate. There is still the possibility that what we are calling introgression may be the result of ancient population substructure (Eriksson and Manica 2014). Even the number of lineages involved is debatable. Does the Denisovan mtDNA haplotype represent another potential lineage? Hammer et al. (2011) infer approximately 2 % admixture from an unknown archaic population into some Africans population based on modern diversity in Africa. Similarly, based on whole-genome analyses, Lachance et al. (2012) infer introgression, from an unknown archaic population or populations, into Pygmy and click-speaking Hadza and Sandawe populations. Will east Asian fossils yield more surprises if or when molecular data is generated from them? Will the Flores Island specimens yield DNA with new and improved techniques, despite poor preservation?

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_59-2 # Springer-Verlag Berlin Heidelberg 2013

Conclusions Biomolecules have many advantages over morphological characters for phylogenetic analyses. The sheer volume of data potentially available is staggering. More importantly, nontrivial hypotheses regarding homology are generally more robust than those inferred for morphological characters and systems. The independence of characters and traits is more easily achieved at the molecular level, allowing multiple independent phylogenetic hypotheses to be generated and examined for concordance. On the other hand, all molecular phylogenies are necessarily gene trees, which can have different histories from the species or populations in which they reside. With whole-genome sequencing now available, including for a limited number of fossil taxa, the complexities of evolution are more readily apparent. Homoplasy and selection are more easily detectable at the molecular level. With high-quality ancient genomes, molecularly derived estimates of the ages of fossils are now possible. Fossils, on the other hand, can test hypotheses that have been put forth and suggest novel combinations of traits that we are not clever enough to have thought possible. A combination of approaches and techniques will provide us with the best insights into our evolutionary history.

Cross-References ▶ Analyzing Hominin Phylogeny ▶ Ancient DNA ▶ Chronometric Methods in Paleoanthropology ▶ Historical Overview of Paleoanthropological Research ▶ Molecular Evidence of Primate Origins and Evolution ▶ Neanderthals and Their Contemporaries ▶ Origin of Modern Humans ▶ The Earliest Putative Hominids

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Batzer MA, Arcot SS, Phinney JW, Alegria-Hartman M, Kass DH, Millegan SM, Kimpton C, Gill P, Hochmeister M, Ioannou PA, Herrera RJ, Boudreau DA, Scheer WD, Keats BJ, Deininger PL, Stoneking M (1996) Genetic variation of recent Alu insertions in human populations. J Mol Evol 42:22–29 Beauval C, Maureille B, Lacrampe-Cuyaubere F, Serre D, Peressinotto D, Bordes JG, Cochard D, Couchoud I, Dubrasquet D, Laroulandie V, Lenoble A, Mallye JB, Pasty S, Primault J, Rohland N, Pääbo S, Trinkaus E (2005) A late Neanderthal femur from Les Rochers-deVilleneuve, France. Proc Natl Acad Sci U S A 102:7085–7090 Begun DR, Nargolwalla MC, Kordos L (2012) European Miocene hominids and the origin of the African ape and human clade. Evol Anthropol 21:10–23 Behar DM, van Oven M, Rosset S, Metspalu M, Loogväli EL, Silva NM, Kivisild T, Torroni A, Villems R (2012) A “Copernican” reassessment of the human mitochondrial DNA tree from its root. Am J Hum Genet 90:675–684 Boissinot S, Furano AV (2005) The recent evolution of human L1 retroposons. Cytogenet Genome Res 110:402–406 Bowcock A, Ruiz-Linares A, Tomfohrde J, Minch E, Kidd JR, Cavalli-Sforza LL (1994) High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368:455–457 Bowler JM, Johnston H, Olley JM, Prescott JR, Roberts RG, Shawcross W, Spooner NA (2003) New ages for human occupation and climatic change at Lake Mungo, Australia. Nature 421:837–840 Briggs AW, Good JM, Green RE, Krause J, Maricic T, Stenzel U, Lalueza-Fox C, Rudan P, Braijkovic D, Kucan Z et al (2009) Targeted retrieval and analysis of five Neanderthal mtDNA genomes. Science 325:318–321 Brunet M, Guy F, Pilbeam D, Mackaye HT, Likius A, Ahounta D, Beauvilain A, Blondel C, Bocherens H, Boisserie JR et al (2002) A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418:145–151 Cann RL (2002) Tangled genetic routes. Nature 416:32–33 Cann RL, Stoneking M, Wilson AC (1987) Mitochondrial DNA and human evolution. Nature 325:31–36 Caramelli D, Lalueza-Fox C, Vernesi C, Lari M, Casoli A, Mallegni F, Chiarelli B, Dupanloup I, Bertranpetit J, Barbujani G, Bertorelle G (2003) Evidence for a genetic discontinuity between Neanderthals and 24,000-year-old anatomically modern Europeans. Proc Natl Acad Sci USA 100:6593–6597 Caramelli D, Lalueza-Fox C, Condemi S, Longo L, Milani L, Manfredini A, de Saint Pierre M, Adoni F, Lari M, Giunti P et al (2006) A highly divergent mtDNA sequence in a Neanderthal individual from Italy. Curr Biol 16:R630–R632 Chen FC, Li WH (2001) Genomic divergences between humans and other hominoids and the effective population size of the common ancestor or humans and chimpanzees. Am J Hum Genet 68:444–456 Cheng Z, Ventura M, She X, Khaitovich P, Graves T, Osoegawa K, Church D, Dejong P, Wilson K, Pääbo S et al (2005) A genome-wide comparison of recent chimpanzee and human segmental duplications. Nature 437:88–93 Chiarelli B (1966) Caryology and taxonomy of the catarrhine monkeys. Am J Phys Anthropol 24:155–169 Chimpanzee Sequencing and Analysis Consortium (2005) Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437:69–87 Cooper A, Poinar HN (2000) Ancient DNA: do it right or not at all. Science 289:1139 Page 17 of 25

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Cooper A, Rambaut A, Macaulay V, Willerslev E, Hansen AJ, Stringer C (2001) Human origins and ancient human DNA. Science 292:1655–1656 Cruciani F, Trombetta B, Massaia A, Destro-Bisol G, Sellitto D, Scozzari R (2011) A revised root for the human Y chromosomal phylogenetic tree: the origin of patrilineal diversity in Africa. Am J Hum Genet 88:814–818 Currat M, Excoffier L (2004) Modern humans did not admix with Neanderthals during their range expansion into Europe. PLoS Biol 2:e421 Currat M, Excoffier L (2011) Strong reproductive isolation between humans and Neanderthals inferred from observed patterns of introgression. Proc Natl Acad Sci USA 108:15129–15134 Dalén L, Orlando L, Shapiro B, Brandström-Durling M, Quam R, Gilbert MT, Díez FernándezLomana JC, Willerslev E, Arsuaga JL, Götherström A (2012) Partial genetic turnover in neandertals: continuity in the East and population replacement in the West. Mol Biol Evol 29:1893– 1897 Disotell TR (1999) Human evolution: origins of modern humans still look recent. Curr Biol 9:647–650 Disotell TR (2003) Discovering human history from stomach bacteria. Genome Biol 4:213 Drmanac R, Sparks AB, Callow MJ, Halpern AL, Burns NL, Kermani BG, Carnevali P, Nazarenko I, Nilsen GB, Yeung G et al (2010) Human genome sequencing using unchained base reads on self-assembling DNA nanoarrays. Science 327:78–81 Dutrillaux B (1979) Chromosomal evolution in primates: tentative phylogeny from Microcebus murinus (Prosimian) to Man. Hum Genet 48:251–314 Eckhardt F, Lewin J, Cortese R, Rakyan VK, Attwood J, Burger M, Burton J, Cox TV, Davies R, Down TA et al (2006) DNA methylation profiling of human chromosomes 6, 20 and 22. Nat Genet 38:1378–1385 Elhaik E, Tatarinova TV, Klyosov AA, Graur D (2014) The ‘extremely ancient’ chromosome that isn’t: a forensic bioinformatic investigation of Albert Perry’s X-degenerate portion of the Y chromosome. Eur J Hum Genet (Epub ahead of print) Elson JL, Turnbull DM, Howell N (2004) Comparative genomics and the evolution of human mitochondrial DNA: assessing the effects of selection. Am J Hum Genet 74:229–238 Enard W, Khaitovich P, Klose J, Zollner S, Heissig F, Giavalisco P, Nieselt-Struwe K, Muchmore E, Varki A, Ravid R, Doxiadis GM, Bontrop RE, Pääbo S (2002) Intra- and interspecific variation in primate gene expression patterns. Science 296:340–343 Eriksson A, Manica A (2012) Effect of ancient population structure on the degree of polymorphism shared between modern human populations and ancient hominins. Proc Natl Acad Sci USA 109:13956–13960 Eriksson A, Manica A (2014) The doubly conditioned frequency spectrum does not distinguish between ancient population structure and hybridization. Mol Bio Evol 31:1618–1621 Excoffier L (2002) Human demographic history: refining the recent African origin model. Curr Opin Genet Dev 12:675–682 Eyre-Walker A, Smith NH (1999) How clonal are human mitochondria? Proc R Soc Lond B Biol Sci 266:477–483 Fabre V, Condemi S, Degionna A (2009) Genetic evidence of geographical groups among Neanderthals. PLoS One 4:e5151 Francalacci P, Morelli L, Angius A, Berutti R, Reinier F, Atzeni R, Pilu R, Busonero F, Maschio A, Zara I, Sanna D et al (2013) Low-pass DNA sequencing of 1200 Sardinian reconstructs European Y-chromosome phylogeny. Science 341:565–569

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Fu Q, Mittnik A, Johnson PL, Bos K, Lari M, Bollongino R, Sun C, Giemsch L, Schmitz R, Burger J et al (2013) A revised timescale for human evolution based on ancient mitochondrial genomes. Curr Biol 23:553–559 Gibbons A (2007) Fossil teeth from Ethiopia support early, African origin for apes. Science 317:1016–1017 Gonzalez AM, Larruga JM, Abu-Amero KK, Shi Y, Pestano J, Cabrera VM (2007) Mitochondrial lineage M1 traces an early human backflow to Africa. BMC Genomics 8:223 Goodman M (1961) The role of immunological differences in the phyletic development of human behavior. Hum Biol 33:131–162 Goodman M (1963) Serological analysis of the systematics of recent hominoids. Hum Biol 35:377–436 Green RE, Shapiro B (2013) Human evolution: turning back the clock. Curr Biol 23:R286–288 Green RE, Krause J, Ptak SE, Briggs AW, Ronan MT, Simons JF, Du L, Egholm M, Rothberg JM, Paunovic M, Pääbo S (2006) Analysis of one million base pairs of Neanderthal DNA. Nature 444:330–336 Green RE, Malaspinas AS, Krause J, Briggs A, Johnson PLF, Uhler C, Meyer M, Good JM, Maricic T, Stenzel U et al (2008) A complete Neanderthal mitochondrial genome sequence determined by high-throughput sequencing. Cell 134:416–426 Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MH et al (2010) A draft sequence of the Neanderthal genome. Science 328:710–722 Haile-Selassie Y (2001) Late Miocene hominids from the Middle Awash, Ethiopia. Nature 412:178–181 Hammer MF, Karafet T, Rasanayagam A, Wood ET, Altheide TK, Jenkins T, Griffiths RC, Templeton AR, Zegura SL (1998) Out of Africa and back again: nested cladistic analysis of human Y chromosome variation. Mol Biol Evol 15:427–441 Hammer MF, Karafet TM, Redd AJ, Jarjanazi H, Santachiara-Benerecetti S, Soodyall H, Zegura SL (2001) Hierarchical patterns of global human Y-chromosome diversity. Mol Biol Evol 18:1189–1203 Hammer MF, Woerner AE, Mendez FL, Watkins JC, Wall JD (2011) Genetic evidence for archaic admixture in Africa. Proc Natl Acad Sci USA 108:15123–15128 Harding RM, Fullerton SM, Griffiths RC, Clegg JB (1997) A gene tree for beta-globin sequence form Melanesia. J Mol Evol 44(Suppl 1):S133–S138 Harris EE, Hey J (1999) X chromosome evidence for ancient human histories. Proc Natl Acad Sci USA 96:3320–3324 Hawks J, Wolpoff MH (2001) Brief communication: paleoanthropology and the population genetics of ancient genes. Am J Phys Anthropol 114:269–272 Hawks J (2012) Longer time scale for human evolution. Proc Natl Acad Sci USA 109:15531–15532 Heizmann EP, Begun DR (2001) The oldest Eurasian hominoid. J Hum Evol 41:463–481 Herrnstadt C, Elson JL, Fahy E, Preston G, Turnbull DM, Anderson C, Ghosh SS, Olefsky JM, Beal MF, David RE, Howell N (2002) Reduced-median-network analysis of complete mitochondrial DNA coding-region sequences of the major African, Asian, and European Haplogroups. Am J Hum Genet 70:1152–1171 Ho SY, Lanfear R, Bromham L, Phillips MJ, Soubrier J, Rodrigo AG, Cooper A (2011) Timedependent rates of molecular evolution. Mol Ecol 20:3087–3101 Hoberg EP, Alkire NL, de Queiroz A, Jones A (2001) Out of Africa: origins of the Taenia tapeworms in humans. Proc Biol Sci 268:781–787

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Hodgson JA, Disotell TR (2008) No evidence of a Neanderthal contribution to modern human diversity. Genome Biol 9:206 Hodgson JA, Bergey CM, Disotell TR (2010) Neanderthal genome: the ins and outs of African genetic diversity. Curr Biol 20:R517–R519 Ingman M, Kaessmann H, Pääbo S, Gyllensten U (2000) Mitochondrial genome variation and the origin of modern humans. Nature 408:708–713 Jobling MA, Tyler-Smith C (2003) The human Y chromosome: an evolutionary marker comes of age. Nat Rev Genet 4:598–612 Jorde LB, Watkins WS, Bamshad MJ, Dixon ME, Ricker CE, Seielstad MT, Batzer MA (2000) The distribution of human genetic diversity: a comparison of mitochondrial, autosomal, and Ychromosome data. Am J Hum Genet 66:979–988 Kaessmann H, Heissig F, von Haeseler A, Pääbo S (1999) DNA sequence variation in a non- coding region of low recombination on the human X chromosome. Nat Genet 22(1):78–81 Kivisild T, Bamshad MJ, Kaldma K, Metspalu M, Metspalu E, Reidla M, Laos S, Parik J, Watkins WS, Dixon ME, Papiha SS, Mastana SS, Mir MR, Ferak V, Villems R (1999) Deep common ancestry of Indian and western Eurasian mtDNA lineages. Curr Biol 9:1331–1334 Knowles LL, Maddison WP (2002) Statistical phylogeography. Mol Ecol 11:2623–2635 Kocher TD, Wilson AC (1991) Sequence evolution of mitochondrial DNA in humans and chimpanzees: control region and a protein-coding region. In: Osawa S, Honjo T (eds) Evolution of life: fossils, molecules and culture. Springer, Tokyo, pp 391–413 Krause J, Serre D, Viola B, Pr€ ufer K, Richards MP, Hublin JJ, Derevianko AP, Pääbo S (2007) Neanderthals in central Asia and Siberia. Nature 444:902–904 Krause J, Briggs AW, Kircher M, Maricic T, Zwyns N, Derevianko A, Pääbo S (2010a) A complete mtDNA genome from an early modern human from Kostenki. Russia Curr Biol 20:231–236 Krause J, Fu Q, Good JM, Viola B, Shunkov MV, Derevianko AP, Pääbo S (2010b) The complete mitochondrial DNA genome of an unknown hominin from southern Siberia. Nature 464:894–897 Krings M, Stone A, Schmitz RW, Krainitzki H, Stoneking M, Pääbo S (1997) Neanderthal DNA sequences and the origin of modern humans. Cell 90:19–30 Krings M, Capelli C, Tschentscher F, Geisert H, Meyer S, von Haeseler A, Grosschmidt K, Possnert G, Paunovic M, Pääbo S (2000) A view of Neanderthal genetic diversity. Nat Genet 26:144–146 Lachance J, Vernot B, Elbers CC, Ferwerda B, Froment A, Bodo JM, Lema G, Fu W, Nyambo TB, Rebbeck TR, Zhang K, et al (2012) Evolutionary history andadaptation from high-coverage whole-genome sequences of diverse African hunter-gatherers. Cell 150:457–469 Lalueza-Fox C, Sampietro ML, Caramelli D, Puder Y, Lari M, Calafell F, Martinez-Maza C, Bastir M, Fortea J, de la Rasilla M, Bertranpetit J, Rosas A (2005) Neanderthal evolutionary genetics: mitochondrial data from the Iberian Peninsula. Mol Biol Evol 22:1077–1081 Lalueza-Fox C, Krause J, Caramelli D, Catalano G, Milani L, Sampietro ML, Calafell F, MartínezMaza C, Bastir M, García-Tabernero A (2006) A highly divergent mtDNA sequence in a Neanderthal individual form Italy. Curr Biol 16:R630–R632 Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921 Langergraber KE, Pr€ ufer K, Rowney C, Boesch C, Crockford C, Fawcett K, Inoue E, InoueMuruyama M, Mitani JC, Muller MN, Robbins MM et al (2012) Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. Proc Natl Acad Sci USA 109:15716–15721 Page 20 of 25

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Leo NP, Barker SC (2005) Unravelling the evolution of the head and body lice of humans. Parisitol Res 98:44–47 Locke DP, Hillier LW, Warren WC, Worley KC, Nazareth LV, Muzny DM, Yang SP, Wang Z, Chinwalla AT, Minx P (2011) Comparative and demographic analysis of orang-utan genomes. Nature 469:529–933 Macaulay V, Richards M, Sykes B (1999) Mitochondrial DNA recombination – no need to panic? Proc R Soc Lond B Biol Sci 266:2037–2039 Maddison DR, Ruvolo M, Swofford DL (1992) Geographic origins of human mitochondrial DNA: phylogenetic evidence from control region sequences. Syst Biol 41:111–124 Mardis ER (2013) Next-generation sequencing platforms. Annu Rev Anal Chem 6:287–303 Mason PH, Short RV (2011) Neanderthal-human hybrids. Hypothesis 9:1–5 Mendez FL, Krahn T, Schrack B, Krahn AM, Veeramah KR, Woerner AE, Fomine FL, Bradman N, Thomas MG, Karafet TM, Hammer MF (2013) An African American paternal lineage adds and extremely ancient root to the human Y chromosome phylogenetic tree. Am J Hum Genet 92:454–459 Meyer M, Fu Q, Aximu-Petri A, Glocke I, Nickel B, Arsuaga JL, Martínez I, Gracia A, de Castro JM, Carbonell E, Pääbo S (2014) A mitochondrial genome sequence of a hominin from Sima de los Huesos. Nature 505:403–406 Meyer M, Kircher M, Gansauge MT, Li H, Racimo F, Mallick S, Schraiber JG, Jay F, Prüfer K, de Filippo C, et al (2012) A high-coverage genome sequence from anarchaic Denisovan individual. Science 338:222–226 Mishmar D, Ruiz-Pesini E, Golik P, Macaulay V, Clark AG, Hosseini S, Brandon M, Easley K, Chen E, Brown MD, Sukernik RI, Olckers A, Wallace DC (2003) Natural selection shaped regional mtDNA variation in humans. Proc Natl Acad Sci USA 100:171–176 Miyamoto MM, Young TS, Ward C, Zihlman AL, Lowenstein JM, Groves C, Covert H, Stewart C-B, Disotell TR (1998) Primate evolution – in and out of Africa (correspondence). Curr Biol 8: R647–R650 Moyà-Solà S, Köhler M, Alba DM, Stewart C-B, Disotell TR (1999) Primate evolution–in and out of Africa (correspondence). Curr Biol 9:R547–R550 Mulligan CJ (2005) Isolation and analysis of DNA from archaeological, clinical, and natural history specimens. Methods Enzymol 395:87–103 Nei M, Roychoudury AK (1974) Genic variation within and between the three major races of Man, Caucasoids, Negroids, and Mongoloids. Am J Hum Genet 26:421–443 Nishimura Y, Yoshinari T, Naruse K, Yamada T, Sumi K, Mitani H, Higashiyama T, Kuroiwa T (2006) Active digestion of sperm mitochondrial DNA in single living sperm revealed by optical tweezers. Proc Natl Acad Sci USA 103:1382–1387 Noonan JP, Coop G, Kudaravalli S, Smith D, Krause J, Alessi J, Chen F, Platt D, Pääbo S, Pritchard JK, Rubin EM (2006) Sequencing and analysis of Neanderthal genomic DNA. Science 314:1113–1118 Nordborg M (1998) On the probability of Neanderthal ancestry. Am J Hum Genet 63:1237–1240 Nuttal GHF (1904) Blood immunity and blood relationships. Cambridge University Press, Cambridge Orlando L, Darlu P, Toussaint M, Bonjean D, Otte M, Hanni C (2006) Revisiting Neanderthal diversity with a 100,000 year old mtDNA sequence. Curr Biol 16:R400–R402 O’Roak BJ, Vives L, Girirajan S, Karakoc E, Krumm N, Coe BP, Levy R, Ko A, Lee C, Smith JD et al (2012) Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations. Nature 485:246–250 Page 21 of 25

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Ovchinnikov IV, Götherström A, Romanova GP, Kharitonov VM, Lidén K, Goodwin W (2000) Molecular analysis of Neanderthal DNA from the northern Caucasus. Nature 404:490–493 Pääbo S (2014) The human condition – a molecular approach. Cell 157:216–226 Panchal M, Beaumont MA (2010) Evaluating nested clade phylogenetic analysis under models of restricted gene flow. Syst Biol 59:415–432 Pilbeam D (1995) Genetic and morphological records of the Hominoidea and hominid origins: a synthesis. Mol Phylogenet Evol 5:155–168 Poznik GD, Henn BM, Yee MC, Sliwerska E, Euskirchen GM, Lin AA, Snyder M, QuintanaMurci L, Kidd JM, Underhill PA, Bustamante CD (2013) Sequencing Y chromosomes resolves discrepancy in time to common ancestor of males versus females. Science 341:562–565 Pr€ufer K, Langergraber KE, Pääbo S, Vigilant L (2013a) Reply to Gibb and Hills: divergence times, generation lengths and mutation rates in great apes and humans. Proc Natl Acad Sci USA 110: E612 Prüfer K, Munch K, Hellmann I, Akagi K, Miller JR, Walenz B, Koren S, Sutton G, Kodira C, Winer R, et al (2012) The bonobo genome compared with the chimpanzee and human genomes. Nature 486:527–531 Pr€ ufer K, Racimo F, Patterson N, Jay F, Sankararaman S, Sawyer S, Heinze A, Renaud G, Sudmant PH, de Filippo C et al (2013b) The complete genome sequence of a Neanderthal from the Altai Mountains. Nature 505:43–49 Prugnolle F, Manica A, Balloux F (2005) Geography predicts neutral genetic diversity of human populations. Curr Biol 15:R159–R160 Raaum RL, Sterner KN, Noviello CM, Stewart C-B, Disotell TR (2005) Catarrhine primate divergence dates estimated from complete mitochondrial genomes: concordance with fossil and nuclear DNA evidence. J Hum Evol 48:237–257 Ramachandran S, Deshpande O, Roseman CC, Rosenberg NA, Feldman MW, Cavalli-Sforza L (2005) Support from the relationship of genetic and geographic distance in human populations for a serial founder effect originating in Africa. Proc Natl Acad Sci USA 102:15942–15947 Reich D, Green RE, Kircher M, Krause J, Patterson N, Durand EY, Viola B, Briggs AW, Stenzel U, Johnson PL et al (2010) Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468:1053–1060 Reich D, Patterson N, Kircher M, Delfin F, Nandineni MR, Pugach I, Ko AM, Ko YC, Jinam TA, Phipps ME et al (2011) Denisova admixture and the first modern human dispersals into Southeast Asia and Oceania. Am J Hum Genet 89:516–528 Relethford JH (2001) Absence of regional affinities of Neanderthal DNA with living humans does not reject multiregional evolution. Am J Phys Anthropol 115:95–98 Rhesus Macaque Genome Sequencing and Analysis Consortium (2007) Evolutionary and biomedical insights from the rhesus macaque genome. Science 316:222–234 Roach JC, Glusman G, Smit AF, Huff CD, Hubley R, Shannon PT, Rowen L, Pant KP, Goodman N, Bamshad M et al (2010) Analysis of genetic inheritance in a family quartet by whole-genome sequencing. Science 328:636–639 Ruiz-Pesini E, Mishmar D, Brandon M, Procaccio V, Wallace DC (2004) Effects of purifying and adaptive selection on regional variation in human mtDNA. Science 303:223–226 Ruiz-Pesini E, Lott MT, Procaccio V, Poole J, Brandon MC, Mishmar D, Yi C, Kreuziger J, Baldi P, Wallace DC (2007) An enhanced MITOMAP with a global mutational phylogeny. Nucleic Acids Res 35(Database issue):D823–D828. http://www.mitomap.org Ruvolo M, Zehr S, von Dornum M, Pan D, Chang B, Lin J (1994) Mitochondrial COII sequences and modern human origins. Mol Biol Evol 10:1115–1135 Page 22 of 25

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Sankararaman S, Patterson N, Li H, Pääbo S, Reich D (2012) The date of interbreeding between Neandertals and modern humans. PLoS Genet 8:e1002947 Sankararaman S, Mallick S, Dannemann M, Pr€ ufer K, Kelso J, Pääbo S, Patterson N, Reich D (2014) The genomic landscape of Neanderthal ancestry in present-day humans. Nature 507:354–357 Sarich VM, Wilson AC (1966) Quantitative immunochemistry and the evolution of primate albumins. Science 154:1563–1566 Sarich VM, Wilson AC (1967) Immunological time scale for hominid evolution. Science 158:1200–1203 Satta Y, Takahata N (2002) Out of Africa with regional interbreeding? Modern human origins. Bioessays 24:871–875 Scally A, Durbin R (2012) Revising the human mutation rate: implications for understanding human evolution. Nat Rev Genet 13:745–753 Scally A, Dutheil JY, Hillier LW, Jordan GE, Goodhead I, Herrero J, Hobolth A, Lappalainen T, Mailund T, Marques-Bonet T et al (2012) Insights into hominid evolution from the gorilla genome sequence. Nature 483:169–175 Schmitz RW, Serre D, Bonani G, Feine S, Hillgruber F, Krainitzki H, Pääbo S, Smith FH (2002) The Neanderthal type site revisited: interdisciplinary investigations of skeletal remains from the Neander Valley, German. Proc Natl Acad Sci USA 99:13342–13347 Senut B, Pickford M, Gommery D, Mein P, Cheboi K, Coppens Y (2001) First hominid from the Miocene (Lukeino Formation, Kenya). CR Acad Sci Paris Ser Iia 332:137–144 Serre D, Langaney A, Chech M, Teschler-Nicola M, Paunovic M, Mennecier P, Hofreiter M, Possnert G, Pääbo S (2004) No evidence of Neanderthal mtDNA contribution to early modern humans. PLoS Biol 2:313–317 Sheen F, Sherry ST, Risch GM, Robichaux M, Nasidze I, Stoneking M, Swergold GD (2000) Reading between the LINEs: human genomic variation induced by LINE-1 retroposition. Genome Res 10:1496–1508 Sherry ST, Rogers AR, Harpending H, Soodyall H, Jenkins T, Stoneking M (1994) Mismatch distributions of mtDNA reveal recent human population expansions. Hum Biol 66:761–775 Short RV (1997) An introduction to mammalian interspecific hybrids. J Heredity 88:355–357 Smith CI, Chamberlain AT, Riley M, Stringer C, Collins MJ (2003) The thermal history of human fossils and the likelihood of successful DNA amplification. J Hum Evol 45:203–217 Stewart C-B, Disotell TR (1998) Primate evolution – in and out of Africa. Curr Biol 8:R582–R588 Stoneking M, Sherry ST, Redd AJ, Vigilant L (1992) New approaches to dating suggest a recent age for the human mtDNA ancestor. Philos Trans R Soc Lond B Biol Sci 337:167–175 Sudmant PH, Huddleston J, Catacchio CR, Malig M, Hillier LW, Baker C, Mohajeri K, Kondova I, Bontrop RE, Persengiev S et al (2013) Evolution and diversity of copy number variation in the great ape lineage. Genome Res 23:1373–1382 Suwa G, Kono RT, Katoh S, Asfaw B, Beyene Y (2007) A new species of great ape from the late Miocene epoch in Ethiopia. Nature 448:921–924 Takahata N, Satta Y (1997) Evolution of the primate lineage leading to modern humans: phylogenetic and demographic inferences from DNA sequences. Proc Natl Acad Sci USA 94:4811–4815 Takahata N, Lee S-H, Satta Y (2001) Testing multiregionality of modern human origins. Mol Biol Evol 18:172–183 Tavare S, Marshall CR, Will O, Soligo C, Martin RD (2002) Using the fossil record to estimate the age of the last common ancestor of extant primates. Nature 416:726–729 Templeton AR (2002) Out of Africa again and again. Nature 416:45–51 Templeton AR (2005) Haplotype trees and modern human origins. Yrbk Phys Anthropol 48:33–59 Page 23 of 25

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Templeton AR, Hedges SB, Kumar S, Tamura K, Stoneking M (1992) Human origins and analysis of mitochondrial DNA sequences. Science 255:737–739 Tishkoff SA, Dietzsch E, Speed W, Pakstis AJ, Kidd JR, Cheung K, Bonné-Tamir B, Santa- chiaraBenerecetti AS, Moral P, Krings M, Pääbo S, Watson E, Risch N, Jenkins T, Kidd KK (1996) Global patterns of linkage disequilibrium at the CD4 locus and modern human origins. Science 271:1380–1387 Turner G, Barbulescu M, Su M, Jensen-Seaman MI, Kidd KK, Lenz J (2001) Insertional polymorphisms of full-length endogenous retro-viruses in humans. Curr Biol 11:1531–1535 Underhill PA, Shen P, Lin AA, Jin L, Passarino G, Yang WH, Kauffman E, Bonne-Tamir B, Bertranpetit J, Francalacci P, Ibrahim M, Jenkins T, Kidd JR, Mehdi SQ, Seielstad MT, Wells RS, Piazza A, Davis RW, Felmand MW, Cavalli-Sforza LL, Oefner PJ (2000) Y chromosome sequence variation and the history of human populations. Nat Genet 26:358–361 van Oven M, Van Geystelen A, Kayser M, Decorte R, Larmuseau MHD (2014) Seeing the wood for the trees: a minimal reference phylogeny for the human Y chromosome. Hum Mutat 35:187–191 Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, Smith HO, Yandell M, Evans CA, Holt RA (2001) The sequence of the human genome. Science 291:1304–1351 Vernot B, Akey JM (2014) Resurrecting surviving Neandertal lineages from modern human genomes. Science 343:1017–1021 Vigilant L, Pennington R, Harpending H, Kocher TD, Wilson AC (1989) Mitochondrial DNA sequences in single hairs from a southern African population. Proc Natl Acad Sci USA 86:9350–9354 Vigilant L, Stoneking M, Harpending H, Hawkes K, Wilson AC (1991) African populations and the evolution of human mitochondrial DNA. Science 253:1503–1507 Wall JD, Kim SK (2007) Inconsistencies in Neanderthal genomic DNA sequences. PLoS Genet 3:1862–1866 Weinberg J, Stanyon R (1998) Comparative chromosome painting of primate genomes. ILAR J 39:77–91 Wildman DE, Uddin M, Liu G, Grossman LI, Goodman M (2003) Implications of natural selection in shaping 99.4% nonsynonymous DNA identity between humans and chimpanzees: enlarging genus Homo. Proc Natl Acad Sci USA 100:7181–7188 Wills C (2011) Genetic and phenotypic consequences of introgression between humans and Neanderthals. Adv Genet 76:27–54 Wolpoff MH (1998) Concocting a divisive theory. Evol Anthropol 7:1–3 Wolpoff MH (1999) Paleoanthropology. McGraw-Hill, Boston Wolpoff MH, Hawks J, Caspari R (2000) Multiregional, not multiple origins. Am J Phys Anthropol 112:129–136 Wood B (2010) Reconstructing human evolution: achievements, challenges, and opportunities. Proc Natl Acad Sci USA 107:8902–8909 Yang MA, Malaspinas AS, Durand EY, Slatkin M (2012) Ancient structure in Africa unlikely to explain Neanderthal and non-African genetic similarity. Mol Biol Evol 29:2987–2995 Y Chromosome Consortium (2002) A nomenclature system for the tree of human Y-chromosomal binary haplogroups. Genome Res 12:339–348

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_59-2 # Springer-Verlag Berlin Heidelberg 2013

Yu N, Chen F-C, Ota S, Jorde LB, Pamilo P, Patthy L, Ramsay M, Jenkins T, Shyue S-K, Li W-H (2002) Larger genetic differences with Africans than between Africans and Eurasians. Genetics 161:269–274 Yunis JJ, Prakash O (1982) The origin of man: a chromosomal pictorial legacy. Science 215:1525–1530 Zuckerkandl E, Pauling L (1962) Molecular disease, evolution, and genetic heterogeneity. In: Kasha M, Pullman N (eds) Horizons in biochemistry. Academic, New York

Page 25 of 25

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

Population Biology and Population Genetics of Pleistocene Hominins Alan R. Templeton* Department of Biology, Washington University in St. Louis, St. Louis, MO, USA Department of Evolutionary and Environmental Biology, University of Haifa, Haifa, Israel

Abstract The population genetics of Pleistocene hominins is deduced from three types of data: coalescent processes and haplotype trees estimated from surveys of genetic variation in present-day human populations, ancient DNA extracted from fossils, and overlays of current quantitative genetic variance/covariance matrices upon hominin fossils. The haplotype trees are subjected to nested clade phylogeographic analyses. These analyses show that there were three major expansion events of hominins out of Africa during the last 2 Myr. The first expansion event marked the original dispersal of Homo erectus out of Africa into Eurasia. The quantitative genetic analysis of hominin fossils indicates that there was relaxed selection upon at least some morphological features at this time, perhaps due to an increased use of cultural inheritance in dealing with the environment. Coalescent analyses indicate that the colonization of Eurasia was marked by strong selection at many loci, so although morphological selection may have been relaxed, adaptive processes were still proceeding as humans colonized this new geographical area. A second expansion out of Africa was marked by the spread of the Acheulean culture, implying that the spread of this culture was due to a spread of peoples and not just ideas. The expanding Acheulean populations interbred with existing Eurasian populations, and recurrent gene flow between Eurasian and African populations was established although restricted by isolation by distance after the Acheulean expansion. A third expansion out of Africa marked the spread of many anatomically modern traits that had earlier appeared in Africa. This expansion was also marked by interbreeding, so regional continuity persisted for some traits. Total replacement of Eurasian populations is rejected with a p < 10
17, under nested clade phylogeographic analysis, and this strong conclusion has been confirmed by subsequent phylogeographic analysis using Approximate Bayesian Computation after correcting for some statistical errors. Direct studies on ancient DNA also support limited admixture rather than total replacement. Coalescent studies are inconclusive and contradictory both about the size of hominin populations before this last out-of-Africa expansion and the degree of population growth during the expansion phase. Because of admixture and gene flow, humanity evolved into its modern form as a single evolutionary lineage but with geographical differentiation at any given time due to isolation by distance and local adaptation.

*Email: [email protected] Page 1 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

Introduction Population genetics is concerned with the origin, amount, and distribution of genetic variability present in populations of organisms and the fate of this variability through space and time. Variation in genes through space and time constitutes the fundamental basis of evolutionary change, so population genetics can be thought of as the science of the mechanisms responsible for evolution within a species or within a continuous lineage of species through time. The fate of genes through space and time is strongly influenced by a population’s demography, so genetic studies can also be used as a powerful tool to investigate past demography. Most population genetic studies of natural populations involve surveying a sample of individuals from one or more demes (local subpopulations), followed by analyses to infer population structure, demography, and/or the impact of various evolutionary forces such as genetic drift, gene flow, and natural selection. But how does one study the genetics and demography of populations from the distant past, such as hominin populations from the Pleistocene? The most common approach to the study of past populations arises from the subdiscipline of population genetics known as coalescent theory. Because DNA can replicate and pass on copies of itself to the next generation, contemporary DNA contains information from past generations. One can therefore genetically survey contemporary populations and then use phylogenetic techniques to estimate the pattern of past DNA replication events. A DNA replication event produces two copies of DNA from one ancestral molecule, so when looked at backward in time, a DNA replication event corresponds to two molecules of DNA coalescing into a single ancestral molecule. Our ability to infer coalescent events with phylogenetic methods depends on the descendant DNA lineages being distinguishable from one another, so the only coalescent events that can be inferred are those that are also associated with a mutation in one of the DNA lineages. The distinguishable DNA lineages are called haplotypes, and we can only reconstruct the haplotype tree of a DNA region, that is, the pattern of coalescent events marked by mutational changes. Thus, the rate of mutation in a DNA region places a limit on our ability to infer the evolutionary history of that region. Because of the Mendelian properties of genetic recombination and assortment and because different DNA regions can display different patterns of inheritance (e.g., the DNA on the Y chromosome is paternally inherited but autosomal DNA is inherited through both sexes), different regions of DNA can have different evolutionary histories and can be influenced by different subsets of past demographic events and processes. Moreover, population genetic inference requires genetic variation, so once all the contemporary copies of a gene or DNA region have coalesced back to a single ancestral molecule of DNA, all population genetic information is lost. Because different DNA regions can coalesce to their common ancestral molecule at different times in the past, different genes are informative of different time periods in the past. Natural selection can also affect the coalescent dynamics of a particular gene region, either by increasing the frequency and geographical range of a new, favored haplotype, by maintaining locally adaptive haplotypes, or favoring the maintenance of multiple DNA lineages. In this case, the haplotype tree does not just reflect the impact of past demography, but also past and ongoing natural selection. Populations generally contain much variation in their gene pools. Hence, when a population splits into two or more isolates, those isolates at first share much of their genetic variation. As time proceeds, genetic drift insures that some DNA lineages are lost, and one will eventually become the common ancestral form for a particular isolate. Because of the randomness of genetic drift, this process of DNA lineage sorting can sometimes produce haplotype trees with different topologies than the evolutionary tree of population splits. Finally, populations can differentiate under restricted gene flow, never experiencing true splits followed by isolation. Page 2 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

Indeed, if gene flow is sufficiently strong, the entire species may represent a single panmictic population. In these cases there is no evolutionary tree of populations at all, but there are still haplotype trees for specific regions of the genome. For all of these reasons, any one gene or DNA region captures only a portion of a population’s evolutionary history, and the haplotype tree of a gene or DNA region should never be equated to the evolutionary history of populations. Many different haplotype trees are required to overcome these difficulties in order to yield a reconstruction of population history. Fortunately, such multi-locus, coalescent analyses are now feasible. The coalescent approach starts in the present and looks into the past. An opposite approach is to start in the past with some set of assumed conditions and then project into the present using a detailed evolutionary model. This projection is typically accomplished through computer simulation. The parameter space of the assumed model is explored to find the set of parameters that best fits the current genetic observations. Often qualitatively different models are also simulated to find the model that best fits the current genetic observations. This approach does not require haplotype trees, but rather can be applied to wide variety of genetic data sets. One limitation of both the coalescent and simulation approaches is not easily overcome. Both types of analyses are based upon current genetic variation and therefore are limited to inferences on past populations or subpopulations that have left genetic descendants in present-day populations. Any population that left no descendants is outside the domain of coalescent analyses. DNA from fossils can overcome this limitation, so ancient DNA studies can extend coalescent and simulation analyses. But because evolution is a population process, accurate evolutionary inferences often depend upon having large sample sizes, and the number of fossils that retain useful DNA severely limits ancient DNA approaches. As a result, ancient DNA surveys usually involve limited sample sizes, even when fossils from diverse geographical locations and separated by tens of thousands of years are pooled together as a single “population.” Extremely small sample sizes often preclude precise population genetic inference. However, some population genetic inferences depend more on the number of genes sampled than the number of individuals, and since ancient DNA studies on hominins can now span the entire genome, some types of inferences can be made with a high degree of confidence. Hence, ancient DNA studies can now address at least some of the questions addressed by studies based on current variation. This allows a direct cross-validation between the present and the past. Coalescent approaches and patterns found in current genetic variation can also be used to infer the presence and type of natural selection operating upon specific genes. Hence, some aspects of adaptive evolution in hominin populations can be addressed from surveys of present-day genetic variation. Additional adaptive insights can be achieved by combining genetic surveys on living populations with ancient genomes from fossils. Another approach to studying past adaptive evolution is to use genetic studies on morphological variation in present-day populations to model the evolutionary forces that created morphological change in the fossil record. All four approaches – coalescence of haplotypes, ancient DNA, simulation, and quantitative genetics – will be considered in this chapter with respect to two major aspects of hominin evolutionary history: (1) hominin population structure and historical demographic events and (2) natural selection and adaptive evolution in past hominin populations.

Page 3 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

Hominin Population Structure and Historical Demographic Events Nested Clade Phylogeographic Analyses Nested clade phylogeographic analysis (NCPA) is a coalescent-based approach to extract information from haplotype trees to infer the qualitative nature of past population structure (patterns of gene flow among geographical areas) and historical demographic events (population range expansions, colonization events, and fragmentation events) (Templeton et al. 1995). NCPA first defines a series of hierarchically nested clades (branches within branches) from the haplotype tree using a set of explicit nesting rules (Templeton et al. 1987; Templeton and Sing 1993). Most human haplotype trees are rooted, so the oldest clade is known in any given nested category. The relative temporal orderings are used to analyze the spread of haplotypes and clades through space and time. NCPA next quantifies the spatial distribution of haplotypes and clades by measuring how widespread a clade is spatially and how far away a clade is located from those clades with which it is nested into a higher-level clade (Templeton et al. 1995). To adjust for sampling, the nested clade analysis uses a random permutation procedure to test the null hypothesis that the clades nested within a higher-level clade have no geographical associations. Because the nested clades are asymptotically independent (Templeton et al. 1995), the Bonferroni procedure is used to correct for multiple testing. All subsequent inferences are limited to those clades associated with a statistically significant rejection of the null hypothesis of no geographical association. Statistical significance tells us that geographical associations exist within the haplotype tree, but they do not tell us how to interpret those geographical associations. Indeed, no single test statistic discriminates between recurrent gene flow, past fragmentation, and past range expansion in NCPA. Rather, it is a pattern formed from several statistics that allows discrimination. Also, many different patterns can sometimes lead to the same biological conclusion, and sometimes a statistically significant pattern has no clear biological meaning because of inadequate geographical sampling or a lack of genetic resolution. Finally, NCPA searches out multiple, overlaying patterns within the same data set. In light of these complexities (which reflect the reality of evolutionary possibilities and sampling constraints), an inference key was provided as an appendix to Templeton et al. (1995), with the latest version being available at http://darwin.uvigo.es/ along with the program GEODIS for implementing the nested clade analysis. Although NCPA has many strengths, it does have limitations. In particular, inference is limited by (1) sample size and sample sites, (2) insufficient genetic resolution to detect an event or process that actually occurred, and (3) false inferences arising from the evolutionary stochasticity of the coalescent process or by the haplotype tree being skewed or otherwise altered by natural selection. In light of these limitations, the inference key has been extensively validated by applying NCPA to actual data sets with 150 a priori expectations (Templeton 2004b). The inference key did well, with the most common error being the failure to detect a known event. Only rarely did NCPA result in a false positive. The failure to detect known events was due to the fact that an appropriate mutation had not occurred in the right place and time to mark the event. This shows that no one locus or DNA region can capture the totality of a species’ population structure and evolutionary history. Concerning false positives, the processes of mutation and genetic drift, which shape the haplotype tree upon which the NCPA is based, are both random processes. Therefore, the expected pattern for a particular event or process can sometimes arise by chance alone, leading to a false biological inference. Moreover, natural selection can lead to false biological inferences by skewing the shape of the haplotype tree and the geographical distribution of certain haplotypes. The occurrence of false negatives and false positives can be reduced by performing NCPA upon many loci or gene regions (Templeton 2002). Using multiple DNA regions reduces the danger of Page 4 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

missing an event or process due to the lack of an appropriately placed mutation in time and space for any one DNA region. The chance of making a false inference is reduced by cross-validating inferences across DNA regions. Templeton (2002) used a multi-locus NCPA based on the human mitochondrial genome and nine nuclear genome regions to infer recent human evolutionary history. What was most remarkable about the cross-validated inferences in this case was the incompleteness found in any one DNA region. This illustrates that failure to detect events or processes with a single DNA region is a common phenomenon. Interestingly, most inferences that were made with one gene were cross-validated by other DNA regions, thereby indicating that false positive inferences are rare in NCPA. This is the same pattern observed when validating the inference key with real data with a priori expectations (Templeton 2004b). The power and low false positive rate of multi-locus NCPA was confirmed by the simulations of Knowles and Maddison (2002). Knowles and Maddison simulated an evolutionary history of micro-vicariance, in which each local population was a genetic isolate due to past fragmentation events. Moreover, the time between population splits was less than the expected coalescent times and the population sizes were large, thereby insuring the sharing of much ancestral polymorphism across isolates. This is a difficult inference problem, and indeed their own simulation procedures fared poorly (Knowles and Maddison 2002). Although the multi-locus version of NCPA had been published 9 months earlier (Templeton 2002), Knowles and Maddison chose to apply only the 1998 single-locus version of NCPA to their simulated data, despite the fact that micro-vicariance had been explicitly excluded from the single-locus version (Templeton et al. 1995). Accordingly, it is not surprising that single-locus NCPA fared poorly when used to analyze these simulated data sets. However, when the 2002 version of multi-locus NCPA was applied to these same simulated data sets, a 100 % accurate reconstruction of the population’s evolutionary history was made with no false inferences (Templeton 2009a). These simulations therefore demonstrate the power of multilocus NCPA to reconstruct difficult evolutionary histories even when no single locus could yield accurate inferences and the low false positive rate of multi-locus NCPA. Cross-validation in Templeton (2002) was based upon concordance across DNA regions of NCPA inferences by type and geographical location. Assessing concordance of inference type and locality is straightforward as these are categorical variables, but inferences should also be temporally concordant. Estimated times of events are quantitative variables with considerable error due to the high stochasticity associated with the coalescent process (Templeton 2004b). Therefore, Templeton (2004a) developed log-likelihood ratio tests of temporal concordance. Panchal and Beaumont (2010) performed simulations to determine the false positive rates under a variety of scenarios using this triple cross-validation of inference type, geographical location, and a formal statistical test of temporal concordance. In general, they found low rates of false positives that were below the nominal rate of 5 %. The one exception was for inferences involving gene flow. Panchal and Beaumont claimed that gene flow inference is subject to a high false positive rate “because there is no stipulation that the inferences should be concordant across time” (Panchal and Beaumont 2010, p. 418). This claim is false. Gene flow is a recurrent event, so temporal concordance does not mean that all gene flow inferences must have occurred at exactly the same time. Therefore, likelihood ratio tests were designed for temporal concordance across a time interval for gene flow (Templeton 2004a, Eq. 12; Templeton 2009b, Eq. 2). The 2009 test specifically tests the null hypothesis of no gene flow between two areas in a specific time interval. Panchal and Beaumont (2010) are correct in concluding that their reported high false positive rate for gene flow inferences was due to their failure to test for temporal concordance, but Panchal and Beaumont made an egregious misrepresentation of NCPA by claiming that such a test did not exist. Whenever Panchal and Beaumont actually implemented multi-locus NCPA, the false Page 5 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

Table 1 The times to the most recent common ancestor (TMRCA) in millions of years ago for the 24 loci subjected to NCPA Gene region Y-DNA mtDNA MAO FIX MSN/ALAS2 Xq13.3 G6PD HS571B2 APLX MC1R ECP EDN AMELX MS205 HFE TNFSF5 Hb-Beta CYP1A2 RRM2P4 PDHA1 FUT6 Lactase CCR5 FUT2

TMRCA 0.23 0.24 0.449 0.47 0.656 0.67 0.692 0.71 0.84 0.85 1.09 1.15 1.178 1.25 1.27 1.34 1.63 1.69 1.714 1.91 1.9375 2.14 2.52 5.04

positive rates were always below the nominal rate. These simulations therefore demonstrate that multi-locus NCPA is a powerful and accurate method for reconstructing past evolutionary histories from current genetic data. Because multi-locus NCPA uses haplotype trees, only those gene regions that have little to no recombination can be used. Recombination can place together in a single DNA molecule different segments that may have had different evolutionary histories, thereby undermining the very idea of an evolutionary tree of haplotypes. This is why the initial studies using NCPA for human evolution were limited to the nonrecombining molecules of mitochondrial DNA (mtDNA) and the Y chromosome (Y-DNA). However, recombination in the human genome is not evenly distributed, but rather is concentrated into hotspots with little to no recombination in many of the regions bounded by hotspots (Templeton et al. 2000a). Hence, with modern genomics it is not difficult to find many regions in the human genome that are amenable to multi-locus NCPA. These nonrecombining regions are the ones upon which human evolutionary history is most clearly and cleanly written. Multi-locus NCPA was first applied to infer recent human evolution with 10 gene regions (mitochondrial DNA, Y chromosomal DNA, and 8 nuclear gene regions) (Templeton 2002) and was later expanded to include 15 additional nuclear gene regions (Templeton 2005; Templeton 2008). The MX1 data used in Templeton (2002) was later found to contain some paralogous copies, Page 6 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

Table 2 The NCPA inferences and their estimated times (in MYA) from the 24 gene regions that yielded significant and interpretable results. Time is indicated only as “recent” for events too young to be reliably dated by phylogenetic means. Only gene flow inferences between Africa and Eurasia are shown Gene region Range expansion events mtDNA Out of Africa, t ¼ 0.1308 To N. Eurasia, recent To Siberia, recent To the Americas followed by fragmentation, recent Within the Americas, recent Y-DNA Out of Africa, t ¼ 0.0916 Out of Asia to Europe and Africa, recent CCR5 – CYP1A2 Out of Africa, t ¼ 1.43 ECP EDN FIX FUT2

– To the Americas, recent – Out of Africa, t ¼ 2.686

FUT6

Out of Africa, t ¼ 0.5

G6PD

To the Americas, recent Africa and Eurasia, origin ambiguous, t ¼ 0.625 Hb-b Out of Africa, t ¼ 0.8212 Out of Asia to Europe and Africa, recent HFE Out of Africa, t ¼ 0.169 Within Eurasia, t ¼ 0.2535 Out of Africa, t ¼ 0.5493 HS571B2 Out of Africa, t ¼ 0.1558 Lactase Out of Africa, t ¼ 0.86 Africa and Eurasia, origin ambiguous, t ¼ 1.93 MC1R Out of Africa, t ¼ 1.00 To N. Eurasia, recent MS205 Africa and Eurasia, origin ambiguous, t ¼ 1.87 To the Americas, recent To the Pacific, recent To the Pacific, recent MSN/ALAS2 – PDHA1 – RRM2P4 Out of Africa, t ¼ 0.14 TNFSF5 To the Americas, recent Xq13.3 –

Restricted gene flow between Africa and Eurasia Isolation by distance, recent

Isolation by distance, recent Isolation by distance, recent Isolation by distance, recent Isolation by distance, t ¼ 1.9844 Isolation by distance, t ¼ 0.2649 Isolation by distance, t ¼ 0.3532 Isolation by distance, t ¼ 0.5824 Isolation by distance, t ¼ 0.6912 Isolation by distance, t ¼ 0.3378 With some long-distance dispersal, recent Isolation by distance, t ¼ 0.9948 Isolation by distance, t ¼ 1.5917 With some long-distance dispersal, recent Isolation by distance, t ¼ 1.25 Isolation by distance, t ¼ 1.3 Isolation by distance, t ¼ 0.4808 Isolation by distance, t ¼ 0.4927 Isolation by distance, t ¼ 0.169 Isolation by distance, t ¼ 0.3944 – Isolation by distance, recent – Isolation by distance, recent

Isolation by distance, t ¼ 0.164 Isolation by distance, t ¼ 0.8597 With some long-distance dispersal, t ¼ 0.6 – Isolation by distance, t ¼ 0.48

Page 7 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

so it was subsequently excluded, leaving a total of 24 gene regions. Interestingly, the inferences from MX1 had already been excluded from the earlier analysis on the basis of the cross-validation procedure (Templeton 2005; Templeton 2008). Coalescent theory predicts that there will be a large variance in coalescent times to the most recent common ancestor (TMRCA) among the various gene regions, with the unisexual, haploid regions (mtDNA and Y-DNA) having an expected coalescence time of Nef generations (the long-term inbreeding effective size of humanity), the X-linked loci having an expected coalescence time of 3Nef, and the autosomal loci having an expected coalescence time of 4Nef (Templeton 2002). Table 1 gives the TMRCAs for the 24 loci used in this analysis. The average coalescence times do indeed fit the expected ranking, and there is also the large expected variance within each category. Table 1 further shows that there is a rather continuous temporal coverage up to about 2.5 Ma. Thus, with these 24 loci, events going back to around 2 Ma can be inferred with potential cross-validation, which represents a significant improvement in the informative temporal range over that of the original 10 loci (Templeton 2002). Table 2 shows the inferences made from the 24 gene regions along with their estimated times of occurrence. Some events could not be timed because there were too few or no mutations available to obtain a reliable estimate. The inferences shown in Table 2 span most of the Pleistocene. Table 2 reveals 15 different identifications of out-of-Africa range expansion events or Africa/ Eurasian range expansion events of ambiguous origin. These 15 events are concordant by type (range expansion) and geographical location (expansion events involving both African and Eurasian populations, and when geographical resolution of the origin is possible, it is always out of Africa). To test temporal concordance of these 15 inferences, their estimated times are regarded as random variables with a mean given by a standard phylogenetic estimator (Takahata et al. 2001) of the age of the youngest clade contributing in a statistically significant fashion to the inference, with a calibration point of 6 Ma for the divergence between humans and chimpanzees (Templeton 2004a). The variance of this time is given by Tajima (1983). s2 ¼

T2 ð1 þ kÞ

(1)

where T is the standard phylogenetic estimator of age and k is the pairwise divergence among present-day haplotypes as measured by the number of mutations that have accumulated in the descendants of the haplotype or node whose age is estimated to be T. Equation 1 incorporates two sources of error into the variance associated with estimator T. First, the numerator of Eq. 1 is T2, reflecting the evolutionary stochasticity of the coalescent process itself in which the variance is proportional to the square of the mean (Donnelly and Tavare 1995; Hudson 1990). The other factor that influences the variance is k, which depends upon the number of mutations that have accumulated in the DNA lineages from T to the present. This can vary considerably from locus to locus, depending upon the local substitution rates and upon the amount of DNA being sequenced. Because k is generally very small for recent events, phylogenetic dating procedures are often unreliable for recent events (Rannala and Bertorelle 2001). If the population under study has not been significantly fragmented into subpopulations and evolution is neutral, then the distribution of ti, the time of a phylogeographic event or process inferred from DNA region i, can be approximated by a gamma distribution (Kimura 1970):

Page 8 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 1 The distributions for the ages of range expansion events involving Africa and Eurasia, all of which are out-ofAfrica events when the geographical origin is unambiguous. The x-axis gives the age in millions of years before present, and the y-axis gives the gamma probability distribution f(t) that was fitted to the data from a particular locus or DNA region. Because the probability mass is so concentrated close to the y-axis for several genes, the gamma distribution was divided by 7 for mtDNA, by 4 for Y-DNA, and by 2 for HFE, HS571B2, and RRM2P4 to yield a better visual presentation. The age distributions fall into three clusters, shown by thin black lines, medium colored lines, and thick dashed lines, respectively

tki i e
ti ð1þki Þ=T i 1þki Ti Gð1 þ ki Þ 1þki

f ðti jT i , ki Þ ¼


(2)

where ki is the average pairwise nucleotide diversity among the haplotypes in DNA region i in the youngest monophyletic clade that contributed in a statistically significant fashion to the NCPA inference of interest, and Ti is the age obtained by the phylogenetic estimator (Templeton 2004a). Given that the NCPA did not reveal any cross-validated fragmentation events except perhaps very early in the Pleistocene between Africa and Eurasia (the exclusive focus of this chapter) that were subsequently mostly erased by range expansions and admixture, the gamma distribution assumption is justified for the human data. Templeton (2004a) used these gamma distributions to derive maximum-likelihood estimators of the time of an event based on multi-locus data and to derive a log-likelihood ratio test of the null hypothesis that n separate inferences of a geographically concordant event are also temporally concordant; that is, they are the same event. Figure 1 shows the gamma distributions for the 15 inferences of range expansion involving African and Eurasian populations. The log-likelihood ratio test rejects the null hypothesis that all 15 events are temporally concordant with a probability value of 3.89  10
15. Thus, the genetic evidence is overwhelming that there were multiple range expansion events out of Africa during the last 2 Myr (million years) of human evolution. An inspection of Fig. 1 reveals that the time distributions for the 15 events cluster into three distinct groupings. Accordingly, the null hypotheses of temporal concordance within each of these three groupings were tested, and in all cases there was strong concordance within (p ¼ 0.95 for the most recent expansion out of Africa, p ¼ 0.51 for the middle expansion, and p ¼ 0.62 for the oldest expansion). Pooling together the inferences from j homogeneous loci also results in a gamma distribution with mean and variance (Templeton 2004a):

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

Table 3 The estimated times and 95 % confidence limits of the NCPA inferences of out-of-Africa range expansions when multiple loci are pooled according to the results of log-likelihood ratio tests Time of expansion (Ma) 0.1304 0.6508 1.9007

More recent age limit 0.0965 0.3917 0.9937

j X

Mean ¼ T^ ¼

Older age limit 0.1693 0.9745 3.0969

ti ð1 þ ki Þ

i¼1 j X

(3) ð1 þ ki Þ

i¼1 j X

  Var T^ ¼

2

ð1 þ ki Þ Varðti Þ

i¼1 j X

!2 ¼ ð1 þ ki Þ

i¼1

j X

ð1 þ ki Þti 2

i¼1 j X

!2

(4)

ð1 þ ki Þ

i¼1

Combining Eq. 1 with Eq. 4, the effective number of informative mutations about the age of the event based on pooled data, keff, is given by keff

2 T^  
1 ¼ Var T^

(5)

The standard log-likelihood ratio test given in Templeton (2004a) can be used to test the null hypothesis that two or more times based on pooled data are the same by using Eqs. 3 and 5. The log-likelihood ratio test of temporal homogeneity of the most recent and middle out-of-Africa expansion events yields a chi-square statistic of 40.84 with 1 of freedom with a p-value of 1.66  10
10. Hence, the null hypothesis of temporal concordance is strongly rejected, and the first two clusters shown in Fig. 1 define two distinct out-of-Africa expansion events. The log-likelihood ratio test of homogeneity of the middle and oldest out-of-Africa expansion events also rejects temporal concordance with a chi-square statistic of 8.85 with 1 of freedom and a p-value of 0.0029. Hence, all three clusters shown in Fig. 1 identify separate events that are all cross-validated by multiple loci. The estimated times and 95 % confidence intervals for these three out-of-Africa range expansions are shown in Table 3. These NCPA inferences from molecular genetic data are consistent with the fossil and archaeological record. The oldest expansion, genetically dated to 1.9 Ma, corresponds well to the fossil dating of the original expansion of Homo erectus (which includes ergaster in this chapter) from Africa into southern Eurasia at 1.85 Ma (Ferring et al. 2011) and far East Asia by 1.7 Ma (Zhu et al. 2008). Dennell (2003) has argued that these early Pleistocene fossil finds in Eurasia may not have represented permanent settlement but also acknowledges the difficulty of inferring (or rejecting) regional continuity over a long-time period from temporally sporadic fossil and archaeological finds from a single geographical area. Genetics can offer an important tool that

Page 10 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

complements the fossil and archaeological data. Recall that the NCPA can only detect the genetic signatures of past populations that have made at least some genetic contribution to current populations. This statistically significant signal of an expansion into Eurasia in the late Pliocene to early Pleistocene, cross-validated by three genes, would not exist at all if these initial Eurasian colonies had not left some descendants in present-day Eurasian populations. Hence, the initial colonization of Eurasia by Homo erectus was a successful one that resulted in the permanent settlement of at least parts of Eurasia. The middle expansion out of Africa shown in Table 3 is consistent with the spread of the Acheulean stone-tool culture out of Africa and into Eurasia. Evidence for this culture is found first in Africa at 1.76 Ma (Beyene et al. 2013; Lepre et al. 2011), with the earliest non-African sites being older than 1 Ma (Pappu et al. 2011). However, Acheulean sites are not widespread in Eurasia until about 0.6–0.8 Ma, particularly eastern Asia (Hou et al. 2000). This has led to the suggestion by some that there were two Acheulean expansions out of Africa: the first at about 1.4 Ma and the second at 0.6–0.8 Ma (Aguirre and Carbonell 2001; Bar-Yosef and Belfer-Cohen 2001; GorenInbar et al. 2000). As outlined above, the current analysis indicates a statistically significant out-ofAfrica expansion at 0.65 Ma (0.3917–0.9745 Ma), which corresponds well with the second, more widespread, Acheulean expansion. However, this genetic analysis does not falsify the hypothesis that there was an earlier Acheulean expansion at 1.4 Ma. Indeed, the out-of-Africa expansion detected by CYPA2 dates to 1.43 Ma. However, because of the large variances associated with older coalescent-based estimates of age (Eq. 1), this event at 1.43 Ma could not be distinguished from the older out-of-Africa events detected by FUT2 and Lactase with the likelihood ratio tests described above. Thus, there may well have been an Acheulean expansion at 1.4 Ma, but because this event is between the original out-of-Africa expansion by Homo erectus and the much stronger (in terms of both archaeological and genetic evidence) Acheulean expansion between 0.6 and 0.8 Ma, it will take a much larger data set to achieve statistical discrimination. Another explanation is that the Acheulean expansion at 1.4 Ma may have been very limited geographically, perhaps confined to the Middle East and southern India. A limited range expansion from Africa would not be detectable by most of the loci analyzed here because of sparse geographical sampling in the Middle East and India. Finally, it is also possible that the 1.4 Ma Acheulean expansion was only a cultural expansion, in which case it would be invisible to NCPA. It is not clear from the archaeological evidence whether the 0.6–0.8 Ma Acheulean expansion was solely the diffusion of ideas from Africa or also involved movement of populations or individuals (Saragusti and Goren-Inbar 2001). Here, the genetic data can complement the archaeological data. NCPA can only detect movements of reproducing populations and individuals, not ideas. By combining NCPA with archaeology, it is likely that the 0.6–0.8 Ma Acheulean expansion represented a movement of both people and ideas. Another question that cannot be answered by the archaeological data alone is what happened when these Acheulean peoples coming out of Africa encountered the Eurasian populations? Perhaps the Acheulean peoples drove the earlier inhabitants to extinction, completely replacing them. Alternatively, the expanding Acheulean peoples could have interbred with the Eurasian populations. The Acheulean replacement hypothesis can be tested by noting that if complete replacement had occurred, there would be no genetic signatures of events or genetic processes in Eurasia that would be older than this expansion event (Templeton 2004a). This prediction stems from the simple fact that NCPA can only detect events and processes that affected past populations that left genetic descendants in present-day populations. The Acheulean replacement hypothesis can therefore be tested by testing the null hypothesis that the gamma distribution marking the Acheulean expansion has a mean time that is not significantly older than other Eurasian events or processes with older estimated times. To be conservative in the definition Page 11 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

of “older,” an event or process will only be regarded as older than the Acheulean expansion if its estimated age falls in the older 1 % tail of the pooled gamma distribution that describes the Acheulean expansion. This 1 % cutoff is calculated from the pooled Acheulean gamma distribution to be 1.0476 Ma. NCPA identified four events or processes with estimated times older than 1.0476 Ma: the first out-of-Africa expansion at 1.9 Ma and three inferences of restricted gene flow dating from 1.25 Ma to 1.9844 Ma (Table 2). The log-likelihood ratio test of the null hypothesis that these four other events and processes involving Eurasian populations are no older than the Acheulean expansion yields a chi-square of 10.37 with 4 degrees of freedom, which is significant at the 5 % level (p ¼ 0.0346). Hence, the null hypothesis of Acheulean replacement is rejected. The expansion of people from Africa about 0.6–0.8 Ma was therefore marked both by bringing a new culture to and by interbreeding with Eurasian populations. The Acheulean range expansion from Africa dated to 0.65 Ma (Table 3) is also compatible with the fossil record. After the initial expansion of Homo erectus out of Africa about 1.9 Ma (Table 3), there was little change in average brain size up to 0.7–0.6 Ma, after which cranial capacities show a substantial increase (Lepre et al. 2011; Relethford 2001b; Rightmire 2004; Ruff et al. 1997). Hence the fossil record, the archaeological record, and the genetic analysis presented here all imply that an important transition in human evolution occurred about 0.65 Ma. The final out-of-Africa expansion is genetically dated to 130,000 years ago (Table 3). Many anatomically modern traits first appeared in sub-Saharan Africa around 200,000 years ago (McDougall et al. 2005), then appeared outside of sub-Saharan Africa in northern Africa, the Arabian Peninsula, and Levant between 130,000 and 125,000 years ago (Armitage et al. 2011; Grun et al. 2005; Vanhaeren et al. 2006), and finally reached far eastern Asia no later than 110,000 years ago (Jin et al. 2009; Liu et al. 2010). Once again, the genetic date from NCPA agrees remarkably well with the fossil and archaeological records. There has been considerable controversy over whether or not this most recent out-of-Africa expansion event was also a replacement event. This recent replacement hypothesis can be tested in the same manner as the Acheulean replacement hypothesis. The older 1 % tail of the gamma distribution that describes this recent out-of-Africa expansion occurs at 0.1774 Ma. Two older out-of-Africa expansion events occurred, as previously discussed, as well as an expansion event within Eurasia dated to 0.2535 Ma (Table 2). However, this within-Eurasia expansion event is not cross-validated by any other locus, so it will be ignored in this and all subsequent analyses. In addition to the two expansion events, there are 15 inferences of restricted gene flow involving Eurasian populations that have estimated ages older than 0.1774 (Table 2). The log-likelihood ratio test of the null hypothesis that all 17 of these times are no older than the most recent out-of-Africa expansion event yields a chi-square statistic of 118.18 with 17 degrees of freedom, which yields a p-value of less than 10
17. Hence, the genetic data overwhelmingly reject the out-of-Africa replacement hypothesis. There is no doubt from NCPA that this spread of humans with many anatomically modern traits resulted in interbreeding with at least some Eurasian populations. Several more range expansions were detected by NCPA: expansions within Eurasia, including the colonization(s) of new areas in Northern Eurasia and colonizations of the Pacific and the Americas. These expansions were marked by genetic regions with too few mutations to date, but they were inferred to have occurred after the most recent out-of-Africa expansion. More extensive data on the Y chromosome has allowed the dating of an expansion originating in Eurasia to 41,000–52,000 years ago (Wei et al. 2013). As this expansion was marked by both Y-DNA and nuclear DNA in the NCPA but not mtDNA, even though mtDNA had the best sampling and genetic resolution, this Paleolithic expansion was most likely male-mediated and therefore must have involved interbreeding with previously established populations. Page 12 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 2 The distributions for the ages of the youngest clade contributing to a significant inference of restricted gene flow, primarily with isolation by distance. The x-axis gives the age in millions of years before present, and the y-axis gives the gamma probability distribution, f(t). The genes or DNA regions yielding these distributions are, as ordered by their peak values of f(t) going from left to right: Xq13.1, MSN/ALAS2, HFE, FIX, HFE, G6PD, bHb ECP, RRM2P4, EDN, PDHA1, CYP1A2, FUT2, FUT6, FUT6, FUT2, CYP1A2, CCR5, and MX1. The curve for MX1 is shown in a dashed line to emphasize its outlier status (Templeton 2002). Several other inferences of restricted gene flow that were too recent to date phylogenetically are not shown and not used in the analyses

The NCPA results indicate that expansions coupled with interbreeding or admixture were not the only source of genetic contact between African and Eurasian populations during much of the Pleistocene. Figure 2 shows the gamma distributions for all the inferences of restricted gene flow among African and Eurasian populations from Table 2. Almost all of the older inferences of gene flow indicate that it was restricted by isolation by distance, but some of the more recent inferences (often not datable by phylogenetic techniques) indicate some long-distance dispersal as well. This means that this genetic interchange was mostly due to short-distance movements to neighboring demes (other than the three major population-level expansions), but copies of genes could have spread throughout Africa and Eurasia via gene flow, using local demes as stepping stones to cross vast distances over many generations. A glance at Fig. 2 versus Fig. 1 reveals a dramatic difference; the inferences of range expansion are clustered, but the inferences of restricted gene flow form a continuum across much of the Pleistocene. The continuum defined by the genes is expected if gene flow restricted by isolation by distance were a recurrent evolutionary force throughout much of the Pleistocene, with no lengthy interruptions. Because gene flow is a recurrent evolutionary force, there is no expectation of different inferences of restricted gene flow from the various genes to be temporally concordant, in contrast to historical events such as rapid range expansions. But it is possible to test the null hypothesis of isolation (no gene flow) between two areas in the time interval l to u. In particular, if j is the number of loci that yield an inference of gene flow within the time interval l to u between the two areas of interest, the likelihood ratio test (LRT) of the null hypothesis of isolation between the two areas in the time interval l to u is

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

Fig. 3 A model of recent human evolution as inferred from NCPA. All inferences are cross-validated by two or more genes and are statistically significant at least at the 5 % level. Major expansions of human populations are indicated by arrows, and the time periods for the out of Africa are the 95 % confidence limits given in Table 3. Genetic descent is indicated by vertical lines and gene flow by diagonal lines

2 LRTðisolation in ½l; u ¼
2

j X i¼1

6 ln41


ðu

3

tki i e
ti ð1þki Þ=T i 7 dti 5
1þki Ti Gð1 þ ki Þ l 1þki

(6)

with the degrees of freedom being j (Templeton 2009a). During the early Pleistocene in the time interval between the first out-of-Africa expansion (1.9 Ma) and the Acheulean expansion (0.65 Ma), there were seven inferences of gene flow with isolation by distance between Africa and Eurasia (Table 2). The likelihood ratio test of the null hypothesis of isolation (no gene flow) between Africa and Eurasia given by Eq. 6 yields a log-likelihood ratio statistic of 11.86 with 7 degrees of freedom, which is not significant at the 5 % level. Hence, after the first expansion of Homo erectus into Eurasia, there was no significant gene flow between Eurasian and African populations up to the time of the Acheulean expansion. In the time interval between the Acheulean expansion (0.65 Ma) and the expansion of anatomically modern humans out of Africa (0.13 Ma), there are 11 inferences of gene flow between Africa and Eurasia, with Eq. 6 yielding a log-likelihood ratio statistic of 23.94 with 11 degrees of freedom, which yields a p-value of 0.013. Hence, the null hypothesis of isolation between Africa and Eurasia is rejected during this time interval. Humans by 650,000 years ago had the capability of moving both in and out of Africa and did so on a recurrent basis.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

Figure 3 summarizes the cross-validated, statistically significant conclusions from the NCPA based on 24 genes or DNA regions. The inferences in Fig. 3 of ancient and recurrent gene flow punctuated by major population movements out-of-Africa coupled with interbreeding are consistent with the fossil record. Many fossil traits display a pattern of first appearing in Africa and then spreading throughout Eurasia (Stringer 2002), whereas other traits display a pattern of regional continuity (Wolpoff et al. 2000; Wu 2004). These two patterns are often regarded as mutually exclusive alternatives, but they are not under a model of genetically interconnected populations and no total replacement. As long as there is genetic interchange among populations, the Mendelian mechanisms of recombination and assortment allow different traits influenced by different genes to have different evolutionary fates. Some traits could have spread due to the joint actions of gene flow, admixture, and natural selection, whereas other traits may not have spread as rapidly or not at all due to a lack of selection or due to local selective pressures. Recurrent gene flow and admixture therefore provide the genetic interconnections that explain all of the fossil trait patterns during this time period, as well as current distributions of genetic variation in humans (Dugoujon et al. 2004; Eller 1999; Eswaran 2002). This model of gene flow and interbreeding also explains why current genetic variation in human populations does not fit an evolutionary tree model in which different human populations are treated as distinct “branches” on an evolutionary tree. Although the human evolutionary genetic literature is filled with portrayals of human populations as branches on a tree, none of these population evolutionary trees actually fit the genetic data when tested (Templeton 1998; Templeton 2003; Templeton 2013). Instead, patterns of genetic differentiation among current human populations fit an isolation-by-distance model much better than a tree model (Eller 1999; Eller 2001; Templeton 1998; Templeton 2003; Templeton 2013).

Ancient DNA Analyses The NCPA overwhelmingly indicates that the most recent out-of-Africa range expansion event was not a total replacement event. This does not mean, however, that there was interbreeding with all Eurasian populations. The possibility of some local replacement is compatible with the NCPA, but that possibility is not testable with NCPA because its inference is limited to historical populations that have left some genetic descendants in present-day populations. One way of addressing this possibility is to extract DNA from hominin fossils. Working with ancient DNA is difficult. Because mtDNA is much more abundant than nuclear DNA, the initial ancient DNA studies focused on mtDNA (Caramelli et al. 2003; Currat and Excoffier 2004; Knight 2003; Krings et al. 2000; Serre et al. 2004). These studies revealed that Neanderthal mtDNA represents a unique mitochondrial lineage that is distinct both from presentday human mtDNA and from the mtDNA found in fossil but anatomically modern specimens from comparable time periods. This pattern has been interpreted to mean that there was no or extremely little interbreeding between Neanderthals and their more anatomically modern contemporaries. However, there are difficulties with these conclusions from ancient DNA studies. First are the technical difficulties. Ancient DNA is subject to damage over time, and resulting lesions can create artifactual substitutions (Caldararo and Gabow 2000; Hansen et al. 2001). One test for artifactual substitutions makes use of the considerable age range found in the Neanderthal fossils used as sources for DNA. If the apparent divergence is real, then the oldest Neanderthal samples should tend to be closest to current human mtDNA because they are temporally closer to the common ancestral sequence for Neanderthal and modern human mtDNA. In contrast, if DNA damage has made a large contribution to the apparent divergence, then the oldest Neanderthal sequences should be the farthest from that of modern humans. The later pattern is true (Gutierrez et al. 2002). Because the samples are small, one could argue that just by chance the oldest Page 15 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

Neanderthal sequences just happened to come from an abnormally highly divergent lineage of Neanderthal mtDNA; but these results indicate that DNA damage cannot be discounted as a significant source of error in these early studies. In addition, ancient DNA extracts induce artifactual mutations, both nucleotide substitutions and insertions/deletions, in a nonrandom fashion such that the same artifacts are independently created in controlled experiments (Pusch and Bachmann 2004). Moreover, many of the sites at which these artifacts repeatedly occur are the same sites observed in Neanderthal mtDNA divergence (Pusch and Bachmann 2004). These results indicate that great caution should be exercised in interpreting these early ancient mtDNA sequence data. Second, these initial ancient DNA studies on human fossils were confined to mtDNA, a molecule that has some unusual patterns of mutation and nucleotide substitution. Most of the analyses of Neanderthal mtDNA have ignored this fact. When the best-fitting maximum-likelihood model of mtDNA evolution is used, there is no statistically significant support for a branch separating the Neanderthal sequences from modern human sequences even when all the sequences are assumed to be completely valid (Gutierrez et al. 2002). Third, mtDNA is incapable biologically of completely reflecting a population’s evolutionary history and of rejecting the hypothesis of admixture. MtDNA is sensitive only to female-mediated gene flow and can totally miss even extensive interbreeding mediated through males. Fourth, as mentioned in the introduction, the evolutionary history of a single gene or DNA region should never be equated to the evolutionary history of a population. A glance at Fig. 3 reveals that much of humanity’s recent evolutionary history is not detected at all by mtDNA. One needs multiple loci to obtain an accurate reconstruction of evolutionary history (Wall 2000) and to protect against false inferences due to evolutionary stochasticity and natural selection skewing the results of a particular gene (Templeton 2002, 2004b). Fifth, the small sample sizes preclude the ability to dismiss significant amounts of gene flow between Neanderthals and moderns (Currat and Excoffier 2004; Nordborg 1998; Pearson 2004; Relethford 2001a; Wall 2000). Technological advances have overcome many of these problems, as it is now possible to examine much of the nuclear genome with increasing accuracy and coverage (Green et al. 2010; Mendez et al. 2012; Meyer et al. 2012; Reich et al. 2010; Skoglund and Jakobsson 2011; Wall and Slatkin 2012; Yotova et al. 2011). These newer studies on ancient DNA clearly document low levels of admixture with the two archaic populations examined so far: Neanderthals from Europe and Denisovans from Siberia. The fact that two out of two studied archaic populations have contributed to modern human genetic diversity through admixture implies that low levels of admixture between the expanding populations of modern humans with the earlier Eurasian resident populations were both spatially widespread and common. Moreover, ancient DNA studies on an anatomically modern human fossil from China dated to 40,000 years ago revealed admixture levels that were similar to those found in current human populations (Fu et al. 2013). This indicates that admixture was essentially completed before 40,000 years ago. As discussed earlier, modern human fossils are found in China by 110,000 years ago, so the admixture event or processes in China occurred in the time interval between 40,000 and 110,000 years ago. Similarly, a linkage disequilibrium analysis indicates that the last gene flow from Neanderthals into Europeans likely occurred 37,000–86,000 years ago (Sankararaman et al. 2012). These ancient DNA studies confirm the strong rejection of the out-of-Africa replacement model in favor of limited admixture with Eurasian populations made by multi-locus NCPA (Templeton 2002; Templeton 2005).

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

Demographic Inferences from Coalescent and Simulation Analyses The definitive rejection by multi-locus NCPA of the null hypothesis of the out-of-Africa replacement hypothesis in favor of a limited amount of admixture (Templeton 2002; Templeton 2005) was extremely controversial at the time because the replacement hypothesis had become the standard model of Pleistocene human evolution. The almost universal acceptance of the replacement model by geneticists was all the more remarkable because not a single genetic data set or analysis had resulted in a statistically significant hypothesis test favoring replacement (Templeton 2007). The support for replacement was not based on the standard scientific standard of hypothesis testing, but rather on the weaker argument of hypothesis compatibility with genetic data sets incapable of discriminating among the alternatives (Templeton 2007). The only analysis prior to the ancient DNA studies that claimed a statistically significant rejection of even small amounts of admixture was that of Fagundes et al. (2007) who used computer simulations of several models of human evolution followed by a comparison of how well the specific models fit the genetic data. Such simulation approaches had been frequently used to assess various models of human evolution, but the best-fitting models varied from simulation to simulation, sometimes favoring replacement and sometimes favoring other models (Templeton 2007). The basic problem with these simulations was that there was no rigorous statistical assessment of the goodness of fit, making it impossible to objectively measure how well a particular model fit the data compared to an alternative model. Fagundes et al. (2007) solved this problem by using an approach called approximate Bayesian computation (ABC). The simulation of a model of human evolution requires the specification of a large number of parameters (population sizes, times of range expansions, gene flow rates, degree of admixture, etc.). With ABC, these parameters are regarded as random variables drawn from probability distributions called “priors.” After a specific set of parameter values are drawn from the priors, the simulation is executed followed by a comparison of how close a set of summary genetic statistics calculated from the simulation are to the summary statistics calculated from the actual genetic data. This process is repeated multiple times, and from the subset of simulations that result in summary statistics closest to the observed results, it is possible to calculate a localized approximation to the “posterior” distribution of the parameters given the genetic data. Rigorous statistical inference can then be drawn from these posterior distributions. Fagundes et al. (2007) concluded that the replacement model had the highest posterior probability of 0.8 and that any model that included even small amounts of admixture had a posterior probability of only 0.001. These statistically significant results were the opposite of those arising from multi-locus NCPA and are contradictory to the findings of ancient DNA studies. Egregious statistical errors were made in the analysis by Fagundes et al. (Templeton 2010). The great strength of a Bayesian approach is that prior information can be incorporated into the prior probability distributions. However, Fagundes et al. did not just ignore prior information, they constructed priors that were contradictory to prior information. For example, as mentioned earlier, already by 2007 there were fossil and archaeological data showing that the expansion of anatomically modern humans out of sub-Saharan Africa had commenced by 125,000–130,000 years ago. Despite this prior information, Fagundes et al. used a prior that assigned zero probability to any date older than 4,000 generations (80,000 years ago assuming a generation time of 20 years), thereby ensuring a more recent estimated date then indicated by the fossil and archaeological data regardless of the genetic data. Other priors likewise were incompatible with prior studies (Templeton 2010). Much more seriously, Fagundes et al. used the posterior probabilities in a manner that violated fundamental probability measure theory. In particular, they had a parameter M that measured the degree of admixture. The model with no admixture (M ¼ 0) is a special case of the general model in which M can take on any value between 0 and 1. Hence, the Page 17 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_60-5 # Springer-Verlag Berlin Heidelberg 2013

M ¼ 0 model is nested within the general model. Fagundes et al. treated the special case and general models as if they were mutually exclusive rather than nested, resulting in posterior model probabilities that were mathematically and logically impossible (Templeton 2010). It is possible to reformulate nested models as mutually exclusive models in a Bayesian framework by performing a Jordon decomposition in which the special case is assigned an atom of probability mass, and the remaining parameter values are assigned a continuous probability measure. No such decomposition was made, so the model probabilities given by Fagundes et al. have no validity. By using a standard Bayesian procedure that treats nested models as nested models (Lindley 1965), the hypothesis of replacement is rejected in favor of the admixture model with a probability 20,000 BP) of peoples from the Old to the New World. There have been any number of archaeological claims for pre-Clovis occupation of the New World, but as Meltzer (1993) noted, the claims usually have a “shelf life” of about 5 years. Among modern physical anthropologists, several revivalists of the pre-Clovis and/or non-Mongoloid origins include Neves and Pucciarelli (1991, and several similar articles), Crawford (1992), Lahr and Haydenblit (1995), Steele and Powell (1992), and Owsley (2013). Lahr and Haydenblit (1995) proposed that Sundadonty was present in a series of South American crania from Patagonia and Tierra del Fuego. In a lengthy review article, Lahr (1995) proposed that either Sinodonty evolved in parallel in Asia and the Americas or there were two migrations ancestral to Native Americans, i.e., a Sundadont group followed by a Sinodont group. Based on a dental morphological analysis of Peruvian and Chilean samples, Sutter (2004) arrived at a similar conclusion. He notes that older samples exhibit dental morphology more in line with the simplified Sundadont pattern, while later groups exhibit the more complex features associated with Sinodonty. These proposals are inconsistent with dental observations on South Americans. The senior author has never observed a South American series or individual skull that could be considered as having the Sundadont pattern. This includes the Lagoa Santa remains housed in Brazil and those curated in Denmark, as well as Archaic samples from coastal Brazil, Chile, Ecuador, and Peru. The observations of Lahr and Haydenblit on degree of trait expression may have been impacted by dental attrition. Wear most likely caused the underscoring of crown traits that led them to propose the presence of Sundadonty (Burnett et al. 1998). Tooth wear might also have misled Powell and his associates in their observations on small Paleo-Indian samples. The observation of Stojanowski et al. (2013) that some South American samples exhibit root trait frequencies that would not be impacted by crown wear and yet are in line with the Sundadont pattern has not been fully evaluated. When Steele and Powell (1997) evaluated craniometric data of two ancient skulls from Nevada (Spirit Cave, Pyramid Lake) that dated ca. 9,500 BP, they found that they failed to cluster with any Page 5 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_63-3 # Springer-Verlag Berlin Heidelberg 2013

of 22 comparative modern populations. They felt the skulls were more closely aligned with South Asian, Pacific, and Australian populations than with North Asian and recent North American Indians. They concluded that “the studied Paleoindians arrived in the Americas prior to the establishment of the crania shape that is distinctive of recent Northern Asians and North American Indians, and that the colonization of the Americas was more complex than has previously been proposed” (Steele and Powell 1997, p. 218). This contrast was also reported by Jantz and Owsley (2001). Again using craniometric data, they concluded Paleo-Indians were more similar to Polynesians, Europeans, and East Asians than to recent American Indians. Taken altogether, the form of the Paleo-Indian skull relative to most of the comparative samples is a reflection of not only geogenetic linkages but also sedentism and its related nutritional, growth, health, and activity benefits and stresses. Thus, African samples cluster together (geogenetic linkage) despite both nomadism and sedentism being represented. The same can be said for the European, Northeastern Asian, and Oceanic sets. Given that archaeological remains of PaleoIndians strongly suggest a nomadic hunting life way, then the cranial differences between PaleoIndians and recent Native Americans should have been interpreted along economic lines as much as geogenetic. Only in the last sentence of their article do Steele and Powell (1992) remark on the possibility of “adaptational” factors contributing to the cranial differences between Paleo-Indians and recent Native Americans. All but one sentence in this article is clearly aimed at identifying possible “genomic” differences between Paleo-Indians and recent Indians. It should be noted that Steele and Powell (1992, p. 329) speak of Paleo-Indian crania as not being “classically sinodont in craniofacial appearance. Instead, it differed by appearing as much like modern southern Asians [recall they use this term to refer to Chinese, who have traditionally been classified as Mongoloids] as it did recent North American Indians and northern Asians. In this respect our findings resemble the contentions of previous scholars that the earliest recovered samples were proto-Caucasoid or proto-Mongoloid.” There has never been an analysis carried out to show if there is a relationship between craniofacial morphology and Sinodonty or Sundadonty. Steele and Powell have assumed that vaults, faces, and teeth go together like a hand in a glove. In fact, Sinodonty is found in people whose craniofacial variation includes every shape in South and North America, including robust California Indians, heavy and long-skulled Southwest US Basketmakers, and robust long-headed Archaic crania from Mexico, Brazil, and Chile, to round-headed gracile Southwest Puebloans, Chinese, Japanese, Buriats, and a long list of other long- and round-headed Northeast Asians. As for early Native Americans having been proto-Caucasoids, a notion strongly championed by Birdsell (1951), Harris and Turner (1974) showed that dental morphology was in opposition to such typological thinking.

Genetics and the Peopling of the New World During the first half of the twentieth century, scholars who investigated issues relating to the settlement of the New World came primarily from archaeology and skeletal biology. During the past 50 years, genetic data have played an increasingly important role in debates on Native American population history. Researchers have applied three different kinds of genetic data to the problem. Initially, focus was on nuclear genetic markers, from red blood cell antigens and serum proteins to red cell enzymes, immunoglobulins, and white blood cell antigens (cf. Mourant 1954; Mourant et al. 1976; Roychoudhury and Nei 1988; Cavalli-Sforza et al. 1994). In the 1980s, a new and different type of genetic marker was used, one derived from the single-stranded DNA of Page 6 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_63-3 # Springer-Verlag Berlin Heidelberg 2013

the mitochondria (mtDNA) which was transmitted, with but few exceptions, through maternal lineages (for reviews, see Cann 1988; Long 1993). Finally, in the 1990s, the Y chromosome was sequenced and a surprising variety of interesting polymorphisms emerged (cf. Hammer and Zegura 2002; Jobling et al. 2004). The literature in the field has expanded at an exponential rate during the past two decades. It is beyond the scope of this review to provide a detailed synthesis of genetic studies. The goal is to highlight some of the results from the three different sorts of genetic data to determine the extent to which the analyses of synchronic genetic data correspond with peopling models based on diachronic dental data.

Nuclear Markers Around 1950, the nascent field of human genetics started to weigh in on the issue of Native American origins. On that date, W.C. Boyd published his seminal work Genetics and the Races of Man. Therein, he utilized available data on three red cell antigen systems (ABO, Rh, MN) to set up a classification of modern human groups. He deemed Native Americans to be sufficiently distinct from other groups to warrant their own racial category. In this regard, he noted that Indians lacked the “r” allele of the Rh system and the A2 and B alleles of the ABO system, although Eskimos did have a low frequency of B. Indians also showed a relatively high frequency of the M allele and a marked dichotomy in frequencies of the A and O alleles of the ABO system. Populations south of the US-Mexico border showed essentially 100 % O alleles, while some North American groups, in particular Algonquians, Athapaskans, and Eskimo-Aleuts, exhibited high frequencies of the A allele. While similarities to Asian populations were noted (lack of r and A2), Boyd felt that the high frequency of the M allele and the very low frequency of B were sufficient to distinguish Asian and American “races.” Laughlin (1951) used blood group data along with anthropometric and osteometric comparisons to assess the affinities of Aleut populations. He felt the presence of the B allele indicated Aleuts were closer to Eskimos than Indians. Moreover, he noted that the “B present in the Eskimos is an indication of their recent Asiatic heritage” (Laughlin 1951, p. 119). Throughout his career, Laughlin (1963, 1966) adhered to the notion that there were two major groups in the Americas – American Indians and Aleut-Eskimos. After comparing Native Americans to Siberians for allele frequencies on the ABO and MN systems, Laughlin (1966, p. 473) opined that the “essential affinity of the Eskimo-Aleut stock with Asiatic Mongoloids, rather than with American Indians, is well attested.” With the development of starch gel electrophoresis in the early 1950s, there was a dramatic increase in the number of genetic surveys across the Americas and throughout the world and in the number of genetic systems that became standard markers for population profiles. By the 1970s, the original three RBC antigen standards were complemented by the addition of many more antigen systems and serum proteins (e.g., Diego, P, Duffy, Kell, Kidd, Haptoglobin, Transferrin, Albumin, etc.). By the time of their massive worldwide synthesis, Cavalli-Sforza et al. (1994) were able to tabulate data on 120 nuclear alleles. Beginning in the 1970s, Szathmary (1979, 1981, 1993, and elsewhere) played an important role in making inferences on long-term population history based on the analysis of Native American gene frequency profiles. One of her early efforts, prepared with Nancy Ossenberg, had the eyecatching title “Are the Biological Differences Between Eskimos and North American Indians Truly Profound?” (Szathmary and Ossenberg 1978). This paper developed the position that Indians and Eskimos were not as distinct as many scholars had presumed (cf. Laughlin 1963, 1966), even suggesting that the two groups might have differentiated from a common stock after their arrival in the New World. Until this time, authors had disagreed on the number of possible migrations to the Page 7 of 35

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New World, but the consensus was that the ancestors of Aleut-Eskimos constituted not only a separate migration but the last major migration across the Bering Strait. While the arguments and analysis in these works are interesting, Szathmary limited her comparisons between AleutEskimos and northern Indians of the American Subarctic, to wit Athapaskans in the west and Algonquians in the east. It is now well established that these northern groups are more similar to Eskimo-Aleuts than Indian groups from Mesoamerica, Central America, and South America (cf. Schanfield 1992; Cavalli-Sforza et al. 1994). Authors who focus on GM allotypes have proposed different migration scenarios to account for variation in immunoglobulin genetic variants. Williams et al. (1985) observed that Gm1;21 was present in “Paleo-Indians,” Na-Dene, and Eskimo-Aleut samples, while Gm1,2;21 was absent in Eskimo-Aleuts and Gm1;11,13 was absent in Paleo-Indians. Na-Dene speakers had all three allotypes. This observation led the authors to conclude that Gm data supported the three-wave model of Greenberg et al. (1986) for peopling of the New World. Also focusing on immunoglobulins, Schanfield (1992) pointed out that the work of both Szathmary (1993) and Williams et al. (1985) provided only a limited picture given their emphasis on North American native populations. When Schanfield synthesized Gm data from both North and South American populations, he found South Americans differed consistently from non-Na-Dene North American Indians, Na-Dene speakers, and Eskimo-Aleuts. He feels his data suggest that “in the peopling of the New World, at least four separate migrant groups crossed Beringia at various times” (Schanfield 1992, p. 381). He further suggested that the ancestors of South American Indians arrived before 17,000 BP while North American Indians arrived when the ice-free corridor opened up at the end of the Pleistocene. Both Eskimo-Aleuts and Na-Dene groups are thought to be later Holocene arrivals. A grand synthesis of patterns of variation in nuclear genetic markers was accomplished by Cavalli-Sforza et al. (1994) in The History and Geography of Human Genes. This worldwide analysis of 120 markers in over 40 genetic systems devoted entire chapters to populations in each major geographic region, including a chapter on the Americas. To maximize the availability of genetic data across as many loci as possible, the authors combined data sets and came up with 23 New World groups, defined primarily on linguistic grounds. Importantly, the analysis included several Eskimo, Na-Dene, Siberian, North American, and South American groupings. After conducting a variety of distance analyses and two- and three-dimensional ordinations, CavalliSforza et al. (1994, pp. 340–341) concluded: The genetic patterns in the Americas fully confirm the three waves of migration suggested by dental and linguistic evidence: Amerinds, Na-Dene, and Eskimo. Their order in time is strongly suggested by their northsouth geographical order. Further refinements may reveal that more than one entry contributed to the first wave, but the archeological information is contradictory and our understanding of the genetic pattern of Amerinds is incomplete, so that further investigations are required to settle this problem.

Going well beyond classic nuclear markers, Reich et al. (2012) addressed the issue of origins through the analysis of 364,470 single-nucleotide polymorphisms in 52 Native American, 17 Siberian, and 57 “other” populations. They found evidence for three migration streams into the New World. The initial stream, which they call “First Americans,” is comprised of American Indians from South America, Central America, Mesoamerica, and a few groups near the USMexican border. The second stream is “Eskimo-Aleut.” Significantly, Greenland Eskimos and Aleuts cluster with Northeast Siberians, in line with earlier results on genetic markers and dental morphology. The third stream is represented by a single Chipewyan (Na-Dene) sample; this group also clusters with Algonquians of the eastern Subarctic, a point also made by Scott and Turner (2006). Reich et al. (2012, p. 373) suggest their results “are consistent with a three-wave model Page 8 of 35

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proposed mostly on the basis of dental morphology and a controversial interpretation of the linguistic data.” Despite defining three distinct migration streams, they note that the second and third streams (i.e., Eskimo-Aleut, Na-Dene) are strongly admixed with First Americans. Despite this caveat, this meta-analysis supports what has long been contended on the basis of dental morphology; that is, Macro-Indians (or First Americans) from North, Central, and South America show homogeneity supporting a relatively recent common ancestor, with no evidence to suggest a second and separate ancestor for South American Indians. The analysis also revealed that Eskimo-Aleuts and Na-Dene-Algonquian represent two additional movements into the New World, a finding that is not totally obscured by later admixture with First American populations. Just as many are disparaging the three-wave model for the peopling of the Americas (cf. Stojanowski et al. 2013), Reich et al. (2012) step forward with evidence suggesting there is still life in the “dusty proposal” put forward by Greenberg et al. (1986) almost 30 years ago.

Mitochondrial DNA When geneticists first discovered that mutationally induced variation in mitochondrial DNA (mtDNA) might help unravel human evolutionary history, there were severe sampling limitations. To harvest enough mtDNA for analysis, researchers had to collect human placentas, often a formidable task. The development of PCR (polymerase chain reaction) techniques in the early 1990s allowed researchers to obtain mtDNA samples from many kinds of tissue samples, including bone. This development revolutionized the study of mtDNA, and research teams quickly pursued historical questions on every continent, among both living and earlier human populations. Although mtDNA variation has been evaluated in groups throughout the world, the geographic region that has received an inordinate amount of attention is the New World. Because of sampling limitations, the early studies were regional in scope (Ward et al. 1991, 1993; Shields et al. 1992, 1993). With improved methods, expanding sample sizes, and cooperation among research teams, groups eventually addressed bigger issues regarding the internal differentiation of New World populations and dispersal dates from ancestral Asian populations (Wallace and Torroni 1992; Torroni et al. 1993, 1994; Forster et al. 1996; Malhi et al. 2002; Eshleman et al. 2003). Mitochondrial DNA variation is studied through a combination of restriction fragment length polymorphisms (RFLPs) and direct nucleotide sequencing of the relatively short hypervariable control region (HVR-I and II). Haplogroups are distinguished by a combination of RFLPs and HVR-I and HVR-II polymorphisms (Schurr 2004a). Jobling et al. (2004, p. 291) show the worldwide distribution of the major mtDNA clades, or haplogroups. Of the 27 major clades shown (lettered A to Z), New World populations exhibit the presence of only five haplogroups – A, B, C, D, and X. Numerous articles have been devoted to the issues of (1) how these haplogroups vary within and among Native American populations, (2) whether or not they were brought by separate founding groups or differentiated after arrival in the New World, and (3) the time depth for the origin of each haplogroup. Regarding mtDNA haplogroup variation, North, Central, and South American Indians (Amerinds) all exhibit haplogroups A, B, C, and D. Eskimo-Aleuts, by contrast, have essentially no B and very little C (Schurr 2004a). Athapaskans were initially thought to lack the B haplogroup (Lorenz and Smith 1994), but it now appears to be present but infrequent in Na-Dene-speaking groups. Haplogroup X is limited to northern North American Indians from the Northwest Coast and Subarctic culture areas (Brown et al. 1998). While the pattern of mtDNA haplogroup variation is coming into focus, opinions on the meaning of this variation have yet to reach a consensus. Some early studies favored the notion that the haplogroups indicated four separate migrations into the New World (Schurr et al. 1990; Horai et al. Page 9 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_63-3 # Springer-Verlag Berlin Heidelberg 2013

1993; Lorenz and Smith 1996). Torroni et al. (1994) concluded there were three migrations: two Amerind migrations, with an early dispersal of A, C, and D, and a later migration that involved the B haplogroup. Athapaskans, with an exceptionally high frequency of the A haplogroups, were thought to constitute a third migration. Starikovskaya et al. (1998) also believed there was an early migration that carried the A, C, and D haplogroups with a later migration bringing B. Although there are several proponents of multiple migrations, the majority of researchers contend that the mitochondrial DNA variation evident among all Native Americans is best explained by a single migration event with haplogroup differentiation occurring after arrival in the Americas (Merriwether 1995, 2002; Kolman et al. 1996; Merriwether et al. 1996; Bonatto and Salzano 1997; Malhi et al. 2002; Silva et al. 2002). From the outset, geneticists have argued that mtDNA is useful not only for describing patterns of variation but also for estimating times of divergence on a branching tree. Using either coalescence or distance methods of estimation in conjunction with several assumed mutation rates, most researchers addressing the issue of the initial New World settlement have arrived at very old dates for this event (Schurr 2004b). Several authors contend the first wave of migrants arrived in the Americas more than 30,000 years ago (Bonatto and Salzano 1997; Starikovskaya et al. 1998). Other workers give dispersal estimates of between 20000 and 30,000 BP (Torroni et al. 1994; Silva et al. 2002). Starikovskaya et al. (1998) dated early Amerinds at 34,000–26,000 BP with a later migration at 16,000–13,000 BP. Torroni et al. (1994) tried to come up with an estimate that agreed with either an early entry date (30,000+ BP) or a late entry date (ca. 13,000 BP) compatible with the Clovis-first model. Instead of coming down on one side or the other of this debate, their estimate fell in the middle with a range of 22,000–29,000 years ago. Despite differing opinions on the numbers of migrations and times of dispersal, mtDNA geneticists are in fundamental agreement that Native American haplogroups are of Siberian origin. Torroni et al. (1994, p. 1162) reflect the sentiments of many when they say “We accept that all significant human entry into the Americas was by way of Siberia during periods of glaciation, when a land bridge connected Siberia and the extreme northwest of the Americas.” When haplogroup X was discovered in American Indians, this was initially thought to represent a possible migration from Europe, or at least some founding Amerinds had Caucasian ancestry (Brown et al. 1998). If so, why is there no haplogroup H in Native Americans, as this is far more common in Europeans (ca. 40 %) than haplogroup X (ca. 2 %) (Schurr 2004a)? An alternative to a direct trans-Atlantic migration of X-bearing Europeans was developed by Reidla et al. (2003) who feel that haplogroup X represents a fifth rare mtDNA clade that came into the Americas across Eurasia, originating as far west as the Near East (Reidla et al. 2003). Finally, there are no haplogroups that link modern or ancient Americans to Southeast Asian or South Pacific populations, a population source for early Americans favored by some osteologists (Neves and Pucciarelli 1991; Steele and Powell 1992, 1997; Powell and Neves 1999). Taking a somewhat unconventional approach, Perego et al. (2009) addressed the issue of migration routes into the Americas through the analysis of two rare mtDNA haplogroups: D4h3 and X2a. The distribution of D4h3 is primarily along the Pacific coast, with most samples coming from South America but also some from Mexico and California. With but one exception, this haplogroup is limited to the Americas but the exception is interesting. One individual from eastern China had the D4h3 haplogroup and control-region motif of 16301–16343 comparable to that in Native Americans. The senior author has long contended that China was a possible geographic source for Native Americans and this one small puzzle piece supports that position. The other haplogroup, X2a, is found exclusively in the Great Lakes region, Great Plains, and western Canada. It has been found only in the Americas. Perego et al. (2009) feel the divergence times for these two Page 10 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_63-3 # Springer-Verlag Berlin Heidelberg 2013

haplogroups was almost coincident at around 16,000 BP. Whether it happened before or after entry into the New World is not clear. The distribution of the two haplogroups suggests that the ancestral groups may have entered the New World along two different paths: D4h3 along the Pacific coast and X2a following an interior route (O’Rourke 2009). A combination of archaeology and genetic variation has led researchers to develop a Beringian Standstill model (Tamm et al. 2007). Although sites in Alaska do not go back beyond the late Pleistocene, Pitulko and his colleagues (2013) have excavated the Yana Rhinoceros Horn site in northern Siberia that goes back 30,000 BP. The abundant material and zoological remains at this site show that people were well adapted to the rigors of an Arctic environment during the early Upper Paleolithic. In conjunction with genetic diversity that is unique to Native Americans, the Yana site raises the possibility that groups could have entered Beringia at least 30,000 BP but could not move further into the Americas because of major physiographic barriers (i.e., ice sheets, glaciers). During the standstill (also called Beringian incubation model), the Asian progenitors of Native Americans had ample temporal and spatial opportunity to differentiate within the broad confines of Beringia. When environmental conditions improved around 15,000 BP, populations could disperse south along a Pacific coastal route and/or via an interior corridor and carry their genetic differences with them.

Y Chromosome As a complement to mtDNA, recent genetic studies that focus on the settlement of the Americas are evaluating recently discovered polymorphisms on the Y chromosome. The long neglected Y, whose strict paternal transmission complements the maternal transmission of mitochondrial DNA, exhibits two major types of polymorphisms on the nonrecombining segment (NRY) of the chromosome. First, there are point mutations that result in single-nucleotide polymorphisms (SNPs). The mutation rates for these polymorphisms are slower than for the second type of polymorphism – short tandem repeats (STRs). Taken together, researchers use SNPs and STRs to define a diverse array of haplogroups and haplotypes. As with mtDNA, Y chromosome polymorphisms have been used to estimate the number of migrations, the timing of dispersal of populations to the Americas, and the Old World sources for this peopling event. Evolving and diverse nomenclatural systems applied to Y polymorphisms make the literature on this system difficult to decode for nonspecialists. To allay confusion, workers convened a consortium in 2001 to develop a common set of standardized terms for Y chromosome binary haplogroups (Y Chromosome Consortium 2002; Hammer and Zegura 2002). Based on this new system, it appears that most Native Americans exhibit haplogroup Q, an observation that led some workers to conclude that a single founding male lineage is sufficient to account for the ancestry of all Native Americans (Tarazona-Santos and Santos 2002; Jobling et al. 2004). Haplogroup Q is, however, defined on the basis of several distinct SNPs and STRs, which other workers have interpreted as indications of multiple migrations from Asia. Lell et al. (2002) suggest that the QM3 and P-M45a Y haplogroups dispersed eastward from central Siberia along with the C and D haplogroups of mtDNA. Moreover, these authors feel that the haplogroups P-M45b and RSP4Y came from south Siberia along with a subgroup of the A haplogroup of mtDNA (control-region sequence variant 16192T and the RsaI polymorphism at np16392). Karafet et al. (1999) and RuizLinares et al. (1999) also conclude there were at least two founding Y haplogroups in the Americas. Regarding the timing of dispersal, most estimates for arrival in the New World favor the long chronology (cf. Schurr 2004b). For their two migrations, Lell et al. (2002) estimate the first wave arrived in the New World ca. 20,000–30,000 BP with the second wave arriving much later, ca. 7,000–9,500 years ago. In contrast to those who see great time depth for Y haplogroups in the Page 11 of 35

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Americas, Seielstad et al. (2003) attempted to set an upper limit for initial entry into the New World based on a mutation (M242) that occurred just before the arrival of populations in the New World. Using a mutation rate of 0.18 % per generation, the authors estimated that M242 arose around 15,000 BP. These workers, who consider 18,000 an upper limit for New World settlement, thus favor an entry into the New World that followed, rather than preceded, the Last Glacial Maximum.

Macro-Indian Dental Variation Now that contrasting models for the peopling of the New World from skeletal biology and genetics have been briefly reviewed, the case that can be made from tooth crown and root morphology will be presented in more detail. Table 1 lists the archaeologically derived Indian series used in this chapter. Altogether 3,584 individuals are represented in 17 North American groups and 11 South American groups. All the data in Table 1 were collected by the senior author. A key set of 29 largely independent, normal, age- and sex-free crown and root traits were scored for occurrence and expression using the Arizona State University dental anthropology system (Turner et al. 1991). An overwhelming number of individuals are pre-Columbian in age. Hence, there is little chance for European, African, or Oceanic admixture in this Pan-American assemblage, whose chronometric ages range from protohistoric to late Paleo-Indian. Although the exact modes of inheritance are still under investigation for these and other dental traits, it is believed that each has a substantial genetic component for occurrence and expression (Scott 1973; Harris 1977; Berry 1978; Scott and Turner 1988, 1997; Nichol 1990). Space limitations permit reviewing only a few of the 29 traits, so mainly those that distinguish Northeast Asian Sinodonty from Southeast Asian Sundadonty are presented (Turner 1983, 1987, 1990a). Figures 1 and 2 illustrate five of these traits – incisor shoveling, double shoveling, tuberculum dentale, and first and second lower molar root number

Findings American Indian dental morphological variation, assessed against the background of archaeological and linguistic information, led to the following generalizations: 1. There are three dental clusters of Macro-Indians: North America, South America, and an interregionally convergent group. 2. Dental variation is relatively low among Macro-Indians. 3. The Macro-Indian dental divisions arose by local evolution. 4. South America was colonized soon after North America. 5. Individual dental trait frequencies show only random variation. 6. Only Northeast Asian Sinodonty is present in the New World. 7. Dental variation supports the Clovis/epi-Clovis prehistory and Greenberg language migration models. Three dental clusters: Figure 3 is a dendrogram computed with Ward’s clustering method for the 106 possible pairwise mean measures of divergence, a multivariate similarity/dissimilarity statistic developed by C.A.B. Smith (Berry and Berry 1967) with widely used adjustments for sample size and determination of statistical significance (references in Turner 1985). There are three primary dental groups: North America (at the top), South America (at the bottom), and a middle group that shows interregional convergence. Page 12 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_63-3 # Springer-Verlag Berlin Heidelberg 2013

Table 1 Frequency variation in archaeological New World dental samplesa Trait, tooth break point Sample North America Archaic Canada Iroquois Canada Maryland Athapaskan California Grand Gulch, Utah Chelly and Kayenta Chavez Pass New Mexico Grasshopper Pt. Pines early Pt. Pines late Arkansas Alabama Coahuila, Mex. Cuicuilco and Tehuacan Tlatelolco No. South America Panama Ayalan, Ecuador Cotocollao, Ec. Chanduy, Ec. Santa Elena, Ecuador Paloma, Peru Peru 1 and 2 Chile Coronado, Brz. Lagoa Sta, Brz. Sambaqui, Brz. No. North America Mean Range South America Mean Range

Shovel UI1 2–7/0–7 %

Uto-Aztec UP1 1/0–1 No. %

Enamel ext. UM1 1–3/0–3 No. %

One-root UP1 1/1–3 No. %

No.

86.9 71.7 93.7 70.0 97.7 100.0

38 39 48 10 88 7

0.0 0.0 0.0 – 1.1 0.0

34 116 54 0 91 33

12.9 26.0 35.8 33.3 41.7 45.9

84 231 106 66 213 48

78.7 75.4 81.9 89.2 83.9 94.1

80 207 94 83 211 51

97.6

42

1.7

59

61.4

96 97.4

76

71.4 87.5 91.0 87.5 97.0 87.8 97.3 75.0 94.7

7 120 133 24 33 49 146 8 38

4.2 0.8 4.0 2.6 0.0 4.1 1.9 6.5 1.7

24 128 124 38 44 97 159 31 59

55.1 45.9 49.1 58.8 49.2 33.1 34.0 21.1 33.3

29 170 157 51 61 127 203 76 66

83.9 91.5 84.0 85.0 85.5 88.8 77.8 87.3 91.2

31 141 81 40 55 125 108 63 57

100.0

39 797/869

0.0

85 20/1176

50.8

122 91.0 743/1906

122 1386/1625

94.1 90.2 100.0 88.2 100.0

51 51 28 17 31

0.0 1.4 3.7 0.0 0.0

43 74 27 12 25

52.3 44.3 54.0 40.0 45.0

67 106 37 20 20

92.7 88.7 89.3 94.7 69.6

55 97 28 19 23

86.5 90.0 92.2 95.0 91.4 91.1

52 50 64 20 35 68 429/467

0.0 0.0 0.0 0.0 1.8 0.0

29 118 65 34 56 74 3/557

46.2 48.4 71.7 36.0 33.3 55.5

78 310 127 61 78 146 525/1050

88.1 86.7 96.9 90.5 83.6 84.7

101 450 128 42 73 111 992/1127

91.7 70.0–100.0

1.7 0.0–6.5

39.0 21.1–61.4

85.3 75.4–97.4

91.9 86.5–100.0

0.5 0.0–3.7

50.0 33.3–71.7

88.0 69.6–96.9 (continued)

Page 13 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_63-3 # Springer-Verlag Berlin Heidelberg 2013

The Dentition of American Indians: Evolutionary Results and Demographic Implications Following Colonization from Siberia, Table 1 (continued) Trait, tooth break Shovel UI1 point 2–7/0–7 NA/SA I¨{2 1 d.f.P 0.0160.9

Trait, tooth break point Sample North America Archaic Canada Iroquois Canada Maryland Athapaskan California Grand Gulch, Utah Chelly and Kayenta Chavez Pass New Mexico Grasshopper Pt. Pines early Pt. Pines late Arkansas Alabama Coahuila, Mex. Cuicuilco and Tehuacan Tlatelolco No. South America Panama Ayalan, Ecuador Cotocollao, Ec. Chanduy, Ec. Santa Elena, Ecuador Paloma, Peru Peru 1 and 2 Chile Coronado, Brz. Lagoa Sta, Brz. Sambaqui, Brz. No. North America Mean

Enamel ext. UM1 1–3/0–3 33.6 < 0.01

Uto-Aztec UP1 1/0–1 3.892 0.05–0.02

One-root UP1 1/1–3 4.2 0.05–.02

Cusp 6 LM1 1–5/ 0–5 %

4-cusped LM2 4/ 4–6 No. %

3-rooted LM1 3/ 1–3 No. %

Y groove LM2 Y/Y+X No. %

No.

65.2 56.6 41.8 52.4 60.0 76.9 57.1

69 8.3 152 9.2 91 8.8 21 2.7 95 5.1 13 8.3 49 10.8

84 10.5 163 7.4 102 6.0 37 9.2 197 8.2 24 2.3 74 7.2

124 230 150 76 292 43 97

5.3 13.2 11.5 12.1 12.0 3.6 3.7

76 167 96 33 184 28 82

61.5 39.4 47.3 45.9 43.6 55.7 67.7 61.5 51.9

13 94 148 37 39 79 127 26 52

25.0 8.0 17.3 16.0 13.0 8.5 3.4 7.9 2.8

20 3.8 138 4.2 104 5.9 50 4.8 54 12.3 118 5.3 178 5.1 38 5.4 72 10.1

26 167 135 63 65 150 178 56 89

18.2 8.6 17.6 3.6 8.8 12.4 7.6 12.8 7.4

22 152 119 56 57 121 170 39 81

65.2

132 683/1237

5.3

151 130/1604

5.2

173 16.9 143/2114

154 177/1637

61.9 66.2 52.2 35.7 80.0

63 11.4 68 7.8 23 12.5 14 15.8 10 5.7

70 77 40 19 35

5.6 3.7 8.8 3.6 4.7

90 108 34 28 43

43.1 61.3 42.2 64.1 54.2 60.9

51 1.5 119 8.6 45 10.7 39 16.1 48 9.5 69 6.2 316/549

55.2

8.1

1.4 3.8 7.9 5.3 3.3

72 79 38 19 30

66 2.8 197 5.1 75 7.7 56 5.4 63 16.8 113 3.1 72/811

107 7.6 217 7.9 155 8.5 56 0.0 101 3.9 161 19.5 66/1100

66 152 82 54 76 128 61/796

6.8

10.8 (continued) Page 14 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_63-3 # Springer-Verlag Berlin Heidelberg 2013

The Dentition of American Indians: Evolutionary Results and Demographic Implications Following Colonization from Siberia, Table 1 (continued) Trait, tooth break point Range South America Mean Range NA/SA I¨{2 1 d.f.P

Cusp 6 LM1 1–5/ 0–5 41.8–76.9

4-cusped LM2 4/ 4–6 2.7–25.0

3-rooted LM1 3/ 1–3 2.3–12.3

57.5 43.1–80.0 0.85 0.5–0.3

8.9 1.5–16.1 0.42 0.7–0.5

6.0 2.8–16.8 0.697 0.5–0.3

Y groove LM2 Y/Y+X 3.6–18.2 7.6 0.0–19.5 6.02 0.02–0.01

a

Individual count, sexes pooled, all prehistoric except Athapaskan sample and some Iroquois. Sample provenience and break points are detailed in Turner (1985) and elsewhere. Scoring is done with ASUDAS (Turner et al. 1991)

The Paloma sample is surely a misclassification attributable to chance. Some interregional convergence is expected given that dental microevolution (in the sense of gene frequency changes) is probably best explained as caused largely because of random changes due to founder’s effect, population structure, and local genetic drift. There is no archaeological or other evidence to believe, for example, that the Ecuadorian Santa Elena series is similar to the Alabama sample because of ancestry closer than to each sample’s respective regional relationships. Instead, the Santa Elena-Alabama similarity is most likely an example of the occasional convergences that should be expected if Macro-Indian dental evolution was mainly due to chance, not selection or gene flow. As will be discussed below, the relatively low amount of variation, despite the two main North and South American clusters, is not supportive of multiple Paleo-Indian migrations. Low dental variation: Inspection of Table 1 reveals a low amount of trait frequency variation between the 29 groups relative to that in, say, eastern Asia or even New World Arctic people (Turner 1991). This limited New World Indian dental divergence is probably what causes the rather limited “treeness” of the dendrogram in Fig. 3. This suggests either substantial gene flow throughout the Americas or a relatively recent colonization of the Americas with only minor in situ dental differentiation. Excellent “treeness” has been obtained throughout the New World (Arctic, Subarctic, non-Arctic) with these same dental traits and statistical methods (Turner 1987). Table 1 shows that upper central incisor shoveling and lower first molar root number have very different overall frequencies in the New World. The former is a high frequency trait, and the latter, a low frequency trait. Scott (1973) demonstrated that trait frequency was positively correlated with trait expression in the offspring of specific mating types, providing strong evidence for polygenic inheritance. As can be seen, shoveling is universally high (>70 %) among the groups, whereas three-rooted lower first molars are uniformly at a low frequency, averaging about 6 %. Both traits have little variation within and between North and South America. These two traits, like the other 27, show no sign of clinal variation from north to south, east to west, coastal to interior, or low to high elevation. Trait frequencies have no identifiable gross environmental correlates in the New or Old World that would suggest the effects of short-term natural selection. Dental divisions arose by local evolution: Table 1 also lists the North and South American means and ranges for eight traits, seven of which distinguish Sinodonty from Sundadonty, plus a trait found almost exclusively in Native Americans – the Uto-Aztecan premolar. The tabulation shows that there are no statistically significant differences in some traits and very little in all others except the enamel extension, between pre-Columbian North and South American Indians. None of these traits has a north-south mean difference greater than 6 % (enamel extensions). There is no tendency

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_63-3 # Springer-Verlag Berlin Heidelberg 2013

Fig. 1 Arrow 1 indicates right upper central incisor shoveling trait in a female skull from prehistoric Alabama site Lu25–425. Arrow 2 points to double shoveling. Not discussed in this report, but one of the key traits used in the multivariate analysis, arrow 3 points to canine tuberculum dentale (CGT neg. no. 6-6-80:19)

Fig. 2 Arrow 1 indicates left lower first molar with two roots in prehistoric Peruvian male from a cemetery in the Chicama Valley. Had there been a supernumerary third root, it would be out of view on the distolingual aspect. Not discussed in this report, but one of the key traits, arrow 2 points to a one-rooted lower second molar (CGT neg. no.7-380:7. Reprinted courtesy of Dental Anthropology Newsletter)

to exhibit less “Mongolization” or Sinodonty in South America than in North America, that is, there is no evidence for Sundadonty. The differences between the means appear to be mainly random. What little difference there is between North and South America is better interpreted as due to postcolonization local evolution rather than to pre-differentiated multiple migrations. Moreover, the archaeology, craniology, and odontology the senior author has personally seen and read about in Russian sources for eastern Siberia do not provide any cultural or biological basis for hypothesizing markedly differentiated source populations in Primorye, Chukotka, trans-Baikalia, or Yakutia. However, the fact that these Siberian geographic districts and their pre-Russian cultures are recognizable today and prehistorically could mean that they were also distinctive even earlier in Late Pleistocene times as well and would have served as incubator habitats for some amount of preBeringian biocultural and linguistic differentiation. No genetic bottlenecking at Panama: Because there are few dental differences between North and South American Indians relative to even smaller area of eastern Asia, it would appear that there was no meaningful Paleo-Indian genetic bottlenecking in Panama. The size of the Paleo-Indian population wave that advanced through the isthmus was large enough to contain a representative sample of the North American Indian dental gene pool. A trait-by-trait comparison of presumed North and South American Paleo-Indians (Turner 1992a) turns up no differences greater than the

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_63-3 # Springer-Verlag Berlin Heidelberg 2013

Fig. 3 Dendrogram of North and South American pre-Columbian dental relationships based on mean measures of divergence clustered with Ward’s method, 29 dental traits. Computer reference: North and South America

within-continent range of trait occurrence. However, as is well known from various studies of blood group and DNA markers (Spuhler 1979; Szathmary 1979; Shields et al. 1992), the initial Paleo-Indian gene pool probably did not contain a representative sample of Chukotka genes, let alone Pan-Northeast Asian genes. For example, allele B of the ABO system was seemingly not carried across the Bering land bridge by Paleo-Indian colonists, and the three-rooted lower first molar gene(s) was carried by only a small proportion of the first Beringian migrants. South America colonized soon after North America: In 1976, MacNeish suggested that North America was populated for some 100,000 years, while South America had been inhabited for only 25,000 years. Had this been the actual occupational history of the New World and if continuous occupation and regular postcolonization dental microevolution are assumed (Turner 1986), then the North American samples should have exhibited in Fig. 3, on the basis of time alone, about fourfold more internal dental divergence than do the samples from South America. That is, the secondary branching in North America should be much further to the left compared with South America. The dendrogram provides no support for unequal evolutionary time in North and South America, nor do the individual trait values in Table 1. Admittedly, variation in the rate of dental microevolution, connected as it must be to population structure, size, and demography, does not allow precise estimates of separation between branching populations, in this case North and South America. However, claims for 25,000–30,000 years of South American occupation are certainly pushing the envelope of credibility on the basis of both New World and Old World dental evolutionary considerations and most archaeological evidence (Lynch 1991; Haynes 2002a; Fiedel 2004). In the Old World, it is a question of the antiquity of Sinodonty, which may date to around the age for Upper Cave Zhoukoudian, sometime between 11,000 and 30,000 years BP (Chen et al. 1992). Individual dental trait frequencies show only random variation: Comparisons of the means for North and South American dental trait frequencies (Table 1) show no identifiable trends that could be attributed to multiple migrations, differential geographic selection, or some other type of localized natural selection directly affecting teeth. While these samples are not ideal for rigorously Page 17 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_63-3 # Springer-Verlag Berlin Heidelberg 2013

assessing the likelihood of selection pressure, the more obvious correlates are absent. Hence, the dental samples of the South American Pacific coastal populations of Chanduy-Valdivia, Santa Elena, Paloma, Peru, and Chile are not especially similar according to the analysis in Fig. 3. These groups might be relatively similar due to some form of coastal environmental selection, but if this were so, then they should have also incorporated the coastal Sambaqui of Brazil. Samples from upland environments are not any better correlated than the coastal groups. Mountain-plateauoriginating Grasshopper and Point of Pines 1 are linked to coastal Peru. Mountain-located Cotocollao clusters with coastal-lowland Panama. High rainfall and tropical coast Sambaqui folk are linked to low rainfall Arizona plateau Chavez Pass. The two long-lasting deep-winter Archaic Canada and Iroquois samples are joined, but their link with Coahuila from the cool winter high desert of northern Mexico does not suggest cold selection. Only city-state organization versus noncity-state seems to be a source of possible selection. Thus, Tlatelolco, a late and large central Mexican Aztec metropolis, clusters with the similarly developed Peruvian samples. Their clustering together may be the result of oral and other disease selection associated with agricultural economies and highly processed cereal and tuber foods. However, if caries selection had been responsible, then city-state-level Tlatelolco and Peru should have higher frequencies of simpler and potentially more caries-resistant teeth, such as 4-cusped lower second molars, less shoveling, and fewer first molar cusps 6, which is not the case for either sample. Still, disease selection requires further study with respect to dental morphology because caries are rare in hunters and gatherers but are very common among agriculturalists. Only Sinodonty is present in the New World. Shoveling: Figure 4 illustrates upper central incisor shoveling. Tables 1 and 2 show crown and root trait frequencies within the Americas, eastern Asia, Melanesia, Australia, and western Europe. Shoveling is very common throughout the Americas and in Northeast Asia. There is no significant difference in the shoveling frequencies of North America (91.7 %) and South America (91.9 %). It is less common in Southeast Asia and Australia, much less so in Melanesia, and very rare in western Europe. This trait alone shows that Paleo-Indians more likely originated in the north ChinaMongolia gene pool than in those of the other areas. That gene pool, in turn, had to have had its morphogenetic origin in the Sundadont dental pattern of Southeast Asia and South China – the closest dental pattern in the world to Sinodonty. Clearly, Paleo-Indians did not originate in Europe, Oceania, or Southeast Asia according to the distribution of the incisor shoveling genes. The African dental pattern is too different from that of Sinodonty to be considered relevant to Native American origins considerations (Turner 1992b). The frequency of shoveling in the earliest North and South American crania is high (ca. 90.1 %) (Turner 1992a, p. 18), nearly identical to that of recent populations (Table 1). This apparent similarity is not what would be expected for the implication that the Kennewick skeleton was not a Sinodont (Powell and Rose 1999), as well as the claim that early South American skeletons were also not Sinodonts (Lahr 1995, p. 163). Enamel extensions: Figure 5 shows the frequencies for the enamel extension polymorphism, a quasi-continuous trait found on the buccal surface of the upper first permanent molar. While shoveling might conceivably have some minor adaptive value (Mizoguchi 1985), it is difficult to imagine how selection could favor the tiny extension of enamel on the subgingival root surface. In fact, these smooth enamel extensions could have a slightly negative value because they do not provide a porous surface for periodontal tissue attachment, hence favoring the formation of periodontal disease pockets in the adjacent alveolar bone. Enamel extension variation provides essentially the same frequency picture as shoveling; namely, extensions are common in Indians and

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_63-3 # Springer-Verlag Berlin Heidelberg 2013

Fig. 4 Circum-Pacific and European frequencies of upper central incisor shoveling

Northeast Asian Sinodonts, slightly less so in Southeast Asian Sundadonts and very uncommon in Melanesians, Australians, and Europeans. One-rooted upper first premolar: Figure 6 shows the frequencies for the upper first (P3 in paleontological notation) premolar root number polymorphism, which can have one to three roots. As with the shoveling and enamel extensions, one-rooted upper first premolars are common in Northeast Asian Sinodonts and all pre-Columbian Indians, less common in Southeast Asian Sundadonts, and slightly less common in Melanesians, Australians, and western Europeans. While there is less continental Old World and South Pacific Islander occurrence of one-rooted upper first premolars, there is nothing in the data to suggest that American Indian ancestry was anything other than from Northeast Asian Sinodonts. Deflecting wrinkle: Figure 7 shows the frequencies of another tiny secondary trait, the first permanent molar deflecting wrinkle. This polymorphism is the degree of distalward deflection from none to pronounced of the medial ridge of cusp 2 (mesiolingual cusp). This feature has almost no potential for adaptation as it is usually worn off the first molar by the beginning of reproductive age. The deflecting wrinkle is common in pre-Columbian American Indians and Northeast Asian Sinodonts. It is less frequent in Sundadonts and western Europeans. Melanesians and Australians are highly variable for the deflecting wrinkle, and the present Oceanic samples have a substantial frequency, fitting the geographic expectation of an old Southeast Asian origin for the ancestors of Pacific Islanders. Three-rooted lower first molar: Figure 8 shows the frequencies for the three-rooted lower first permanent molar, another root polymorphism with one to three possible roots. Lower molar and upper premolar root numbers are statistically unrelated morphogenetic features. By far, worldwide, the two-rooted condition is most common for the lower first molar root number. The oldest known example of a three-rooted lower first molar in anatomically modern humans is the 22,000-year-old mandible fragment from the Tabon Caves site on Palawan Island in the western Philippines, excavated by Fox (1970). The fragment has three root sockets at the first molar location. Threerooted lower first molars are a Sinodont characteristic, but, like the missing B allele in living

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_63-3 # Springer-Verlag Berlin Heidelberg 2013

Table 2 World dental frequency variation for the eight distinguishing Sinodont and Sundadont morphological traitsa Trait tooth break point Arcticb Eastern USA and Canada SW USA California Mesoamerica South America North China-Mongolia Recent Japan Recent Thailand Early Malay Archipelago Melanesia Australia West Europe Trait tooth break point Arcticb Eastern USA and Canada SW USA California Mesoamerica South America North China-Mongolia Recent Japan Recent Thailand Early Malay Archipelago Melanesia Australia West Europe

Shovel UI1 2–7/0–7 78 91 91 98 94 92 84 66 37 30 9 20 2 Peg-reduced-C.A. UM3 prc/norm+prc 20 18 21 17 19 25 53 42 18 0 13 5 12

Double-shovel UI1 2–6/0–6 75 78 65 90 93 90 30 20 9 28 5 1 4 Deflecting wrinkle LM1 1–3/0–3 30 45 35 45 28 38 29 35 19 11 18 23 7

1-root UP1 1/1–3 95 80 89 84 89 87 77 75 66 68 57 58 58

Enamel extension UM1 1–3/0–3 46 31 51 42 39 49 51 55 39 18 4 9 2

3-root LM1 3/1–3 30 6 6 6 6 6 34 24 11 6 3 5 1

1-root LM2 1/1–3 31 32 29 32 29 37 42 33 31 33 5 6 27

U denotes upper, L lower, CA congenital absence Individual count, sexes pooled, historic and prehistoric native groups, sample provenience, and break points detailed in Turner (1985) and elsewhere b Unpublished new grouping contains Aleut, Eskimo, Greenland Eskimo, Alaska Peninsula, Bering Sea, Kachemak, and Kodiak (computer file name: Arctic94) a

American Indians, Paleo-Indian colonists almost failed to carry to the New World the gene(s) responsible for this accessory root on the lower first molars.

Dentition Supports Ice-Free Corridor, Epi-Clovis/Clovis-First, and Macro-Indian Models Unlike the other dental traits discussed here, three-rooted lower first molar frequency is less than that of Northeast Asian Sinodonts, and this trait is generally uncommon although uniformly present at about 5 % in pre-Columbian Indians. These characteristics imply two events. First, the initial number of Siberians to reach eastern Beringia was apparently small and not strongly representative for all genetic characters. Second, the trait’s Pan-American uniformity suggests (1) that after crossing the ecologically patchy Bering land bridge, group size increased significantly because Page 20 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_63-3 # Springer-Verlag Berlin Heidelberg 2013

Fig. 5 Circum-Pacific and European frequencies of upper first molar enamel extension

Fig. 6 Circum-Pacific and European frequencies of one-rooted upper first premolars (P3)

similar dental gene samples were carried southward to all other parts of the New World and (2) all American Indians discussed here are descended from the founding Siberian epi-Clovis migrants whose archaeological record for colonizing Alaska and Chukotka begins about 12,000 BP (Goebel et al. 2003). The demographic events of rapid population growth and widespread territorial expansion, leading to genetic stabilization in North and South America, could have occurred first in interior Alaska or later after subsequent generations reached and passed through the inhospitable and limiting corridor between the Cordilleran and Laurentide ice sheets of Canada. Unfortunately, there is nothing that can be identified in the dental data that help explain where and how the rapid Page 21 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_63-3 # Springer-Verlag Berlin Heidelberg 2013

Fig. 7 Circum-Pacific and European frequencies of lower first molar deflecting wrinkle

Fig. 8 Circum-Pacific and European frequencies of three-rooted lower first molars

expansion began, regardless of how one defines migration (i.e., wavelike, pulsed, clonal spread, chaotic drift, niche based, continuous leakage, leapfrogging, etc.), or which migration route one chooses (“ice-free corridor,” Pacific coast, ice-crossings and polar desert trek to Atlantic coast, or some combination of these). However, given the rarity of Paleo-Indian sites in Alaska, the recent Fairbanks and Brooks Range finds notwithstanding (West 1981, 1996; Powers et al. 1990; Hoffecker et al. 1993; Kunz and Reanier 1994; Yesner 2001; Yesner and Pearson 2002, others), the model favored here is that of demographic growth, related faunal extinctions (Martin 1990), and genetic drift stabilization as having explosively started at the southern exit of the western Page 22 of 35

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_63-3 # Springer-Verlag Berlin Heidelberg 2013

Canadian ice sheet corridor. The corridor entry is favored over the coastal route because of the severe boating difficulty of getting past the Late Pleistocene glacial ice mass on and around the Alaska Peninsula (Elias 2002; Turner 2002; Hoffecker and Elias 2003). In contrast to the rarity of Clovis or Clovis-like fluted points along the entire Pacific coast of North America, Carlson (1991) identified at least 40 archaeological sites in the ice-free corridor area of British Columbia and Alberta that had various types of fluted points. Elsewhere the senior author (Turner 1992a) inventoried a number of dental observations from crania that were “candidates” for Paleo-Indian chronometric status. None of these incomplete individuals deviated from the Sinodont pattern. Since then, he has examined the teeth of four other crania that are dated as Paleo-Indian or Early Archaic. These include Sulphur Springs woman, excavated in southern Arizona by Waters (1986), Horn Rock Shelter double burial near Waco, Texas, and the Wilson-Leonard female, also from Texas (Young et al. 1987; Steele 1989; Steele and Powell 1992). These four also conform to the Sinodont dental pattern as best as can be determined given the considerable amount of tooth wear they and other hunter-gatherers exhibit worldwide. Finally, some archaeologists (reviewed in Dixon 1999; for opposition, see Carlson 1991; Haynes 2002b) and geneticists (discussed previously) have argued for a Pacific coastal entry route to North and South America from Siberia despite the absence of archaeological evidence for, and Alaska Peninsula glacial evidence against, such a route (Workman 2001; Turner 2003). Moreover, MacroIndian language family distributions in the Americas, Penutian, for example (Ruhlen 2000), do not suggest Pacific coastal entry. As for dental morphology, the Pacific coast samples presented in Table 1 show no sign of meaningful differences with interior samples as would be expected, had there been an earlier more Sundadont-like migration or a fourth American variant of Sinodonty.

Concluding Discussion In assaying the different types of biological data brought to bear on the peopling of the Americas, there are disagreements on the numbers of migrations and their timing, but there are many points of agreement as well. The homogeneity among American Indians indicated by dental morphology is paralleled by mtDNA and Y chromosome haplogroup data and single-nucleotide polymorphism (SNP) arrays. The dentition shows a dichotomy between North American and South American Indians, and this is also evident in genetic markers. Several studies critique the three migration model of Greenberg et al. (1986), but these often fail to include data on Eskimo-Aleut populations. If researchers argue that mtDNA and Y chromosome data support a position that Eskimo-Aleuts differentiated from American Indians after the arrival of a common ancestor in the New World, there are serious problems with their data sets (or the interpretation thereof). On the basis of teeth, nuclear markers, and even craniometry, Eskimo-Aleuts are consistently more closely aligned with recent Asian populations than are American Indians. The placement of other northern groups, especially Na-Dene speakers, is a bit less certain than the Eskimo-Aleut case. Based on similarities in mtDNA, Shields et al. (1993) concluded that Eskimo-Aleuts and Athapaskans were very closely related, diverging from one another in the American Arctic as recently as 7,000 years ago. This same general position has long been advocated by Szathmary (1979, 1981, 1993); Szathmary and Ossenberg 1978) based on the variation in blood group and serum protein polymorphisms. Cavalli-Sforza et al. (1994) found Na-Dene groups fell between Eskimo-Aleuts and Amerinds in general. This intermediary position is also indicated by dental morphological variation (Turner 1985; Scott 1991; Scott and Turner Page 23 of 35

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1997, 2008). When ancillary fields are taken into account, especially linguistics and archaeology, it is hard to reconcile common origins for Eskimo-Aleuts and Na-Dene speakers in the Holocene. Even rare genetic markers speak against this purported tie. Albumin Algonquin (formerly Albumin Naskapi) is found in polymorphic frequencies in Athapaskans and Algonquians but not in Eskimos (Lampl and Blumberg 1979). Eskimos have the B allele and Subarctic Indians do not (Harper 1980). The Y chromosome haplogroup C-M130 has also been found exclusively in Athapaskan and Algonquian populations (Schurr 2004a). The level of genetic diversity in the Americas has led some authors to conclude that the New World was peopled long before the Last Glacial Maximum, with many estimates exceeding 30,000 years BP. To a considerable extent, this runs counter to what is known about the archaeology of Siberia and Beringia, let alone Australia whose aborigines’ biology, tools, and language have evolved so much that few resemblances remain with their Southeast Asian homeland. The New World founding population had to have been in place in Northeast Asia before any groups could start budding off to colonize the Beringian landscape. In a recent synthesis of mtDNA and Y chromosome analyses, Schurr (2004a) proposes three major peopling events from Asia to the Americas: (1) the initial founding population in the Americas came from south-central Siberia and arrived in the New World between 20,000 and 14,000 cal year BP; given the presence of ice sheets across the breadth of Canada, the route of this migration is presumed to be coastal; (2) a second migration, following an interior route, contributed to many of the populations of North and Central America; and (3) Beringian populations, including the ancestors of Aleuts, Eskimos, and Na-Dene speakers, came into New World following the Last Glacial Maximum. Although Schurr’s reconstruction parallels dental findings in a number of ways, the degree of dental differentiation in the New World still favors a late entry model, a position more in line with current archaeological knowledge (Haynes 2002a; Fiedel 2004) and some genetic studies (cf. Seielstad et al. 2003). In principle, there is no objection to an earlier date for the peopling of the New World. At present, a compelling case has not been made for this position, especially in light of archaeological success in Australia in finding very early sites by a much smaller number of archaeologists and geologists (Jelinek 1992). If a coastal migration did take place, more evidence for this event is required. For example, of all the pre-Clovis archaeological sites listed by Schurr (2004a) to support early entry, none are along the Pacific coast. Scholars will continue to find “preClovis” sites and develop molecular clocks and models of linguistic differentiation that indicate early human entry into the Americas, but the final arbiter of dispersal will come from archaeological sites that have excellent stratigraphy and no dating issues. Granted, a major problem associated with a coastal migration is the presumption that most early sites are now under water and mostly inaccessible. The dental characteristics of pre-Columbian American Indians easily fit with both the hypothesis of a rapidly expanding Clovis- or epi-Clovis first colonization event, long advocated by Martin (1990) and Haynes (1991), and the Macro-Indian language evolution model developed by Greenberg (1990). Because all prehistoric and unadmixed living Native Americans, including Na-Dene/Greater Northwest Coast and Aleut-Eskimo, only briefly discussed here, have the Sinodont dental pattern, it would seem that when a date for the emergence of full-blown Sinodonty in Asia is established with some certainty, then that will have to be the earliest possible date for the subsequent colonization of the Americas, assuming that early and late similarity actually means genetic continuity. Inasmuch as the Upper Cave crania seem to have a Sinodont dental pattern, then whatever date is finally settled on for that assemblage will provide a reasonable time estimate for the potential colonization of the Americas.

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It is necessary to focus on Upper Cave since there are only a few sites in Siberia with Late Pleistocene human remains. One site near Lake Baikal, called Mal’ta, seems to have Europeanrather than Asian-like teeth (Turner 1990b), an observation supported by aDNA which shows individuals from this site had the European haplogroup U (Willerslev 2013). Two sites west of Lake Baikal have physical anthropological signs of “Mongoloid” or Sinodonty. These are the Late Pleistocene Yenisei River sites in and near Krasnoyarsk. In the city of Afontova Gora, a fragment of a subadult frontal bone found in a river bank section was thought to have been Mongoloid because of the size and form of the adhering nasal bones (Alekseev 1998). Upstream ca. 35 km (21 mi) is Listvenka, from which came a mandible of a child whose unerupted first molar is slightly more Asian than European in overall appearance. Hence, broadly speaking, the pre-Arctic ancestral homeland of Paleo-Indians must have been in north China, Mongolia, and southern Siberia. It is easy to envision how newly evolved Sinodonts quickly expanded into northeastern Siberia, after they succeeded in domesticating the dog for hunting and hauling, perhaps drifting north out of China via the Vitim River system. Although people were in northern Siberia at 30,000 BP (Pitulko et al. 2013), population density above the Arctic Circle was likely circumscribed so the ancestral Paleo-Indian northward drift would have been rapid and with little human resistance in Beringia. Because the dental differences between the north China-Mongolia group and all unadmixed Indians are small compared with the much larger difference between Northeast and Southeast Asians, the relatively small amount of intra-trait dental variation within the New World may reflect the simple evolutionary fact that Sinodonts have been in the Americas for a relatively short period of time, less time than it took for Sinodonty to evolve out of Sundadonty. Moreover, the colonists and their dogs were so reproductively successful that the usual genetic drift cause of short-term dental trait frequency change was reduced or negated by the large population size that quickly grew south of the east Beringian Arctic steppe. This evolutionary scenario, despite years of bioarchaeological research, does not differ much from that first proposed on craniological grounds by Hrdlicˇka (1925). While some readers may find such lack of theoretical and empirical change as unthinkable in the rapidly changing world of science, others, ourselves included, recognize it as a tribute to Hrdlicˇka’s empirical orientation and one of the more probable scenarios in the complex world history of Late Pleistocene human microevolution and dispersal. For the present, MacroIndian dental variation is not supportive of a Pacific coastal entry route to North and South America, leaving the late entry ice-free corridor model as dentally most parsimonious.

Cross-References ▶ Ancient DNA ▶ Cultural Evolution in Africa and Eurasia During the Middle and Late Pleistocene ▶ General Principles of Evolutionary Morphology ▶ Overview of Paleolithic Archeology ▶ Phylogenetic Relationships (Biomolecules) ▶ Population Biology and Population Genetics of Pleistocene Hominins ▶ Species Concepts and Speciation: Facts and Fantasies

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References Alekseev VP (1979) Anthropometry of Siberian peoples. In: Laughlin WS, Harper AB (eds) The first Americans: origins, affinities and adaptations. Gustav Fischer, New York, pp 57–90 Alekseev VP (1998) The physical specificities of Paleolithic hominids in Siberia. In: Derev’anko AP, Shimkin DB, Powers WR (eds) (Laricheva IP, trans) The Paleolithic of Siberia: new discoveries and interpretations. University of Illinois Press, Urbana, pp 329–335 Berry AC (1978) Anthropological and family studies on minor variants of the dental crown. In: Butler PM, Joysey KA (eds) Development, function and evolution of teeth. Academic, New York, pp 81–98 Berry AC, Berry RJ (1967) Epigenetic variation in the human cranium. J Anat 101:361–379 Birdsell JB (1951) The problem of the early peopling of the Americas as viewed from Asia. In: Laughlin WS (ed) The physical anthropology of the American Indian. Viking Fund, New York, pp 1–69 Bonatto SL, Salzano FM (1997) Diversity and age of the four major mtDNA haplogroups, and their implications for the peopling of the New World. Am J Hum Genet 61:1413–1423 Boyd WC (1950) Genetics and the races of man. Little, Brown and Company, Boston Brace CL, Nelson AR, Seguchi N, Oe H, Sering L, Qifneg P, Yongyi L (2001) Old World sources of the first New World human inhabitants: a comparative craniofacial view. Proc Natl Acad Sci 98:10017–10022 Brown MD, Hosseini SH, Torroni A, Bandelt H-J, Allen JC, Schurr TG, Scozzari R, Cruciani F, Wallace DC (1998) mtDNA haplogroup X: an ancient link between Europe/western Asia and North America. Am J Hum Genet 63:1852–1861 Burnett SE, Irish JD, Fong MR (1998) How much is too much? Examining the effect of dental wear on studies of dental morphology. Am J Phys Anthropol 26(Suppl):115–116 Callegari-Jacques SM, Salzano FM, Constans J, Maurieres P (1993) Gm haplotype distribution in Amerindians: relationship with geography and language. Am J Phys Anthropol 90:427–444 Cann RL (1988) DNA and human origins. Annual Rev Anthropol 17:127–143 Carlson RL (1991) Clovis from the perspective of the ice-free corridor. In: Bonnichsen R, Turnmire KL (eds) Clovis: origins and adaptations. Oregon State University, Corvallis, pp 81–90, Center for the Study of the First Americans Carter GF (1957) Pleistocene man at San Diego. Johns Hopkins Press, Baltimore Cavalli-Sforza LL, Piazza A, Menozzi P, Mountain J (1988) Reconstruction of human evolution: bringing together genetic, archaeological, and linguistic data. Proc Natl Acad Sci USA 85:6002–6006 Cavalli-Sforza LL, Menozzi P, Piazza A (1994) The history and geography of human genes. Princeton University Press, Princeton Chen T, Hedges REM, Zhenxin Y (1992) The second batch of accelerator radiocarbon dates for Upper Cave site of Zhoukoudian. Acta Anthropol Sin 11:112–116 Crawford MH (1992) When two worlds collide. Hum Biol 64:271–279 Dillehay TD, Meltzer DJ (1991) The first Americans: search and research. CRC Press, Boca Raton Dixon EJ (1999) Bones, boats, and bison. University of New Mexico Press, Albuquerque Elias SA (2002) Setting the stage: environmental conditions in Beringia as people entered the New World. In: Jablonski NG (ed) The first Americans: the Pleistocene colonization of the New World. Memoirs of the California Academy of Sciences 27, San Francisco, pp 255–271

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Roberts RG, Jones R, Smith MA (1994) Beyond the radiocarbon barrier in Australia. Antiquity 68:611–616 Rogers RA, Rogers LA, Martin LD (1992) How the door opened: the peopling of the New World. Hum Biol 64:281–302 Roychoudhury AK, Nei M (1988) Human polymorphic genes: world distribution. Oxford University Press, New York Ruhlen M (2000) Some unanswered linguistic questions. In: Renfrew C (ed) America past, America present: genes and languages in the Americas and beyond. McDonald Institute for Archaeological Research, Cambridge, pp 163–175 Ruiz-Linares A, Ortiz Barrientos D, Figueroa M, Mesa N, Munera JG, Bedoya G, Velez ID, Garcia LF, Perez-Lezuan A, Bertranpetit J, Feldman MW, Goldstein DB (1999) Microsatellites provide evidence for Y chromosome diversity among the founders of the New World. Proc Natl Acad Sci USA 96:6312–6317 Schanfield MS (1992) Immunoglobulin allotypes (GM and KM) indicate multiple founding populations of Native Americans: evidence of at least four migrations to the New World. Hum Biol 64:381–402 Schurr TG (2004a) The peopling of the New World: perspectives from molecular anthropology. Annu Rev Anthropol 33:551–583 Schurr TG (2004b) Molecular genetic diversity in Siberians and Native Americans suggests an early colonization of the New World. In: Madsen DB (ed) Entering America: Northeast Asia and Beringia before the last glacial maximum. University of Utah Press, Salt Lake City, pp 187–238 Schurr TG, Ballinger W, Gan YY, Hodge JA, Merriwether DA, Lawrence DN, Knowler WC, Weiss KM, Wallace DC (1990) Amerindian mitochondrial DNAs have rare Asian mutations at high frequencies, suggesting they derived from four primary maternal lineages. Am J Hum Genet 46:613–623 Scott GR (1991) Continuity or replacement at the Uyak site, Kodiak Island, Alaska: a physical anthropological analysis of population relationships. University of Oregon Anthropological Papers 44, pp 1–56 Scott GR (1973) Dental morphology: a genetic study of American White families and variation in living Southwest Indians. Ph.D. dissertation, Department of Anthropology, Arizona State University, Tempe Scott GR, Turner CG II (1988) Dental anthropology. Annu Rev Anthropol 17:99–126 Scott GR, Turner CG II (1997) The anthropology of modern human teeth: dental morphology and its variation in recent human populations. Cambridge University Press, Cambridge Scott GR, Turner CG II (2006) Dentition. In: Ubelaker D (ed) Handbook of North American Indians. vol 3: Environment, origins, and population. Physical anthropology. Smithsonian Institution Press, Washington, DC, pp 645–660 Scott GR, Turner CG II (2008) The physical anthropological intermediacy problem of Na Dene/ Greater Northwest Coast Indians. Alaska J Anthropol 6:57–68 Scott GR, Yap Potter RH, Noss JF, Dahlberg AA, Dahlberg T (1983) The dental morphology of Pima Indians. Am J Phys Anthropol 61:13–31 Scott GR, Street SR, Dahlberg AA (1988) The dental variation of Yuman speaking groups in an American Southwest context. In: Russell DF, Santoro JP, Sigogneau-Russell D (eds) Teeth Revisited, Me´moires du Muse´um National D’Histoire Naturelle C53. Brill Academic Publisher, pp 305–319 Scott GR, Anta A, Schomberg R, de la Rua C (2013) Basque dental morphology and the “Eurodont” dental pattern. In: Scott GR, Irish JD (eds) Anthropological perspectives on tooth Page 31 of 35

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morphology: genetics, evolution, variation. Cambridge University Press, Cambridge, pp 296–318 Seielstad M, Yuldasheva NS, Underhill P, Oefner P, Shen P, Wells RS (2003) A novel Ychromosome variant puts an upper limit on the timing of first entry into the Americas. Am J Hum Genet 73:700–705 Shields GF, Hecker K, Voevoda MI, Reed JK (1992) Absence of the Asian-specific region V mitochondrial marker in native Beringians. Am J Hum Genet 50:758–765 Shields GF, Schmiechen AM, Frazier BL, Redd A, Voevoda MI, Reed JK, Ward RH (1993) MtDNA sequences suggest a recent evolutionary divergence for Beringian and northern North American populations. Am J Hum Genet 53:549–562 Silva WA Jr, Bonatto SL, Holanda AJ, Ribeiro-dos-Santos AK, Paixa˜o BM, Goldman GH, AbeSandes K, Rodriguez-Delfin L, Barbosa M, Paco´-Larson ML, Petzl-Erler ML, Valente V, Santos SEB, Zago MA (2002) Mitochondrial genome diversity of Native Americans supports a single early entry of founder populations into America. Am J Hum Genet 71:187–192 Spuhler JN (1979) Genetic distances, trees, and maps of North American Indians. In: Laughlin WS, Harper AB (eds) The first Americans: origins, affinities, and adaptations. Gustav Fischer, New York, pp 135–183 Stanford DJ, Day JS (eds) (1992) Ice age hunters of the Rockies. University Press of Colorado, Niwot Starikovskaya YB, Sukernik RI, Schurr TG, Kogelnik AM, Wallace DC (1998) MtDNA diversity in Chukchi and Siberian Eskimos: implications for the genetic history of ancient Beringia and the peopling of the New World. Am J Hum Genet 63:1473–1491 Steele DG (1989) Recently recovered Paleoindian skeletal remains from Texas and the Southwest. Am J Phys Anthropol 78:307 Steele DG, Powell JF (1992) Peopling of the Americas: paleobiological evidence. Hum Biol 64:303–336 Steele DG, Powell JF (1997) Biological affinities of the oldest recovered North Americans: the Spirit Cave and Pyramid Lakes data. Am J Phys Anthropol 24(Suppl):218 Stojanowski CM, Johnson KM, Duncan WN (2013) Sinodonty and beyond: hemispheric, regional, and intracemetery approaches to studying dental morphological variation in the New World. In: Scott GR, Irish JD (eds) Anthropological perspectives on tooth morphology: evolution, genetics, variation. Cambridge University Press, Cambridge, pp 408–452 Stone AC, Stoneking M (1993) Ancient DNA from a pre-Columbian Amerindian population. Am J Phys Anthropol 92:463–471 Sutter RC (2004) The prehistoric peopling of South America as inferred from epigenetic dental traits. Andean Past 7:183–217 Szathmary EJE (1979) Blood groups of Siberians, Eskimos, and Subarctic and Northwest Coast Indians: the problem of origins and genetic relationships. In: Laughlin WS, Harper AB (eds) The first Americans: origins, affinities, and adaptations. Gustav Fischer, New York, pp 185–209 Szathmary EJE (1981) Genetic markers in Siberian and northern North American populations. Yrbk Phys Anthropol 24:37–73 Szathmary EJE (1993) Genetics of aboriginal North Americans. Evol Anthropol 1:202–220 Szathmary EJE, Ossenberg NS (1978) Are the biological differences between North American Indians and Eskimos truly profound? Curr Anthropol 19:673–701 Tamm E, Kivisild T, Reidla M, Metspalu M, Smith DG, Mulligan CJ, Bravi CM, Rickards O, Martinez-Labarga C, Khusnutkdinova EK, Federova SA, Golubenko MV, Stepanov VA, Gubina

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MA, Zhadanov SI, Ossipova LP, Damba L, Voevoda MI, Dipierri JE, Villems R, Malhi R (2007) Beringian standstill and spread of Native American founders. Plos One 2(9):e829 Tarazona-Santos E, Santos FR (2002) The peopling of the Americas: a second major migration? Am J Hum Genet 70:1377–1380 Torroni A, Schurr GG, Yang C-C, Szathmary EJE, Williams RC, Weiss KM, Wallace DC (1992) Native American mitochondrial DNA analysis indicates that the Amerind and the Nadene populations were founded by two independent migrations. Genetics 130:153–162 Torroni A, Schurr TG, Cabell MF, Brown MD, Neel JV, Larsen M, Smith DG, Vullo CM, Wallace DC (1993) Asian affinities and continental radiation of the four founding Native American mtDNAs. Am J Hum Genet 53:563–590 Torroni A, Neel JV, Barrantes R, Schurr TG, Wallace DC (1994) Mitochondrial DNA “clock” for the Amerinds and its implications for timing their entry into North America. Proc Natl Acad Sci USA 91:1158–1162 Turner CG II (1983) Sinodonty and Sundadonty: a dental anthropological view of Mongoloid microevolution, origin, and dispersal into the Pacific Basin, Siberia, and the Americas. In: Vasilievsky RS (ed) Late Pleistocene and early Holocene cultural connections of Asia and America. U.S.S.R. Academy of Sciences, Siberian Branch, Novosibirsk, pp 72–76 [in Russian] Turner CG II (1985) The dental search for Native American origins. In: Kirk R, Szathmary E (eds) Out of Asia: peopling the Americas and the Pacific. Australian National University, Canberra, pp 31–78, Journal of Pacific History Turner CG II (1986) Dentochronological separation estimates for Pacific rim populations. Science 232:1140–1142 Turner CG II (1987) Late Pleistocene and Holocene population history of East Asia based on dental variation. Am J Phys Anthropol 73:305–321 Turner CG II (1990) The major features of Sundadonty and Sinodonty, including suggestions about East Asian microevolution, population history, and late Pleistocene relationships with Australian Aboriginals. Am J Phys Anthropol 82:295–317 Turner CG II (1991) The dentition of Arctic peoples. Garland Publishing, New York Turner CG II (1992a) New World origins: new research from the Americas and the Soviet Union. In: Stanford DJ, Day JS (eds) Ice age hunters of the Rockies. University Press of Colorado, Niwot, pp 7–50 Turner CG II (1992b) Microevolution of East Asian and European populations: a dental perspective. In: Akazawa T, Aoki K, Kimura T (eds) The evolution and dispersal of modern humans in Asia. Hokusen-Sha Pub. Co., Tokyo, pp 415–438 Turner CG II (1992c) The dental bridge between Australia and Asia: following Macintosh into the East Asian hearth of humanity. Perspect Hum Biol 2/Archaeol Ocean 27:143–152 Turner CG II (1993) Southwest Indians: prehistory through dentition. Natl Geogr Res Explor 9:32–53 Turner CG II (2003) Three ounces of sea shells and one fish bone do not a coastal migration make. Am Antiq 68:391–395 Turner CG II (2002) Teeth, needles, dogs, and Siberia: bioarchaeological evidence for the colonization of the New World. In: Jablonski NG (ed) The first Americans: the Pleistocene colonization of the New World. Memoirs of the California Academy of Sciences No. 27, San Francisco, pp 123–158 Turner CG II (1990b) Upper Paleolithic Mal’ta child (Siberia). News from the Siberian Branch of the U. S.S.R. Academy of Sciences 2:70-71 [in Russian]

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Turner CG II, Nichol CR, Scott GR (1991) Scoring procedures for key morphological traits of the permanent dentition: the Arizona State University dental anthropology system. In: Kelley MA, Larsen CS (eds) Advances in dental anthropology. Wiley-Liss, New York, pp 13–31 Tyler DE (1998) Homo americanus: an original American species. Discovery Books, Ontario Wallace DC, Torroni A (1992) American Indian prehistory as written in the mitochondrial DNA: a review. Hum Biol 64:403–416 Ward RH, Frazier BL, Dew-Jager K, Paabo S (1991) Extensive mitochondrial diversity within a single Amerindian tribe. Proc Natl Acad Sci USA 88:8720–8724 Ward RH, Redd A, Valencia D, Frazier B, Paabo S (1993) Genetic and linguistic differentiation in the Americas. Proc Natl Acad Sci USA 90:10663–10667 Waters MR (1986) Sulphur Springs woman: an early human skeleton from southeastern Arizona. Am Antiq 51:361–365 West FH (1981) The archaeology of Beringia. Columbia University Press, New York West FH (1990) Archaeology in the press: science misserved? Rev Archaeol 11:25–32 West FH (1996) American beginnings: the prehistory and palaeoecology of Beringia. University of Chicago Press, Chicago Willerslev (2013) Genetics as a means for understanding early peopling of the Americas. Paper presented at Paleoamerican Odyssey, Santa Fe NM, October 2013 Williams RC, Steinberg AG, Gershowitz H, Bennett PH, Knowler WC, Pettitt DJ, Butler W, Baird R, Dowda-Rea L, Burch TA, Morse HG, Smith CG (1985) GM allotypes in native Americans: evidence for three distinct migrations across the Bering land bridge. Am J Phys Anthropol 66:1–19 Workman WB (2001) Reflections on the utility of the coastal migration hypothesis in understanding the peopling of the New World. Paper presented at the Alaska Anthropological Association, Fairbanks, March Y Chromosome Consortium (2002) A nomenclature system for the tree of human Y-chromosomal binary haplogroups. Genome Res 12:339–348 Yesner DR (2001) Human dispersal into interior Alaska: antecedent conditions, mode of colonization, and adaptations. Quat Sci Rev 20:315–327 Yesner DR, Pearson G (2002) Microblades and migrations: ethnic and economic models in the peopling of the Americas. In: Elston G, Kuhn SL (eds) Thinking small: global perspectives on microlithization. Archeological papers of the American Anthropological Association No. 12, pp 133–161 Young D, Patrick S, Steele DG (1987) An analysis of the Paleoindian double burial from Horn Shelter No. 2, in central Texas. Plains Anthropol 32:275–298 Zoubov AA, Haldeyeva NI (1979) Ethnic odontology of the U.S.S.R. Nauka, Moscow, in Russian

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_63-3 # Springer-Verlag Berlin Heidelberg 2013

Index Terms: ABO system 7 Beringia 11, 24 Blood group antigens 7 Clovis 20 Deflecting wrinkle 19 Dental morphology 9 Dental pattern 2, 18 Enamel extension 18 Eskimo-Aleut 8, 23 Ice-free corridor 20 Incisor shoveling 12, 18–19 Macro-Indian 2, 4, 12 definition 2 dental variation 4, 12 Mitochondrial DNA (mtDNA) 9 Mongolization 16 Na Dene 8 Proto-Sundadonty 3 Serum proteins 7 Short tandem repeats (STRs) 11 Single nucleotide polymorphisms (SNPs) 11 Sinodont 2, 20 Sundadont 2, 5, 20 Three-rooted lower first permanent molar 19 Three-wave model 9 Y chromosome 11

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_64-4 # Springer-Verlag Berlin Heidelberg 2013

Overview of Paleolithic Archaeology Nicholas Toth* and Kathy Schick Stone Age Institute and Indiana University, Bloomington, IN, USA

Abstract The Paleolithic, or Old Stone Age, comprises over 99 % of human technological history and spans a time range from 2.6 Ma (the earliest recognizable stone tools and archaeological record) to 10,000 years ago (the end of the last ice age). There are three major stages of the Paleolithic: (1) The Early Paleolithic which includes the following: (a) the Oldowan, from 2.6 to about 1.0 Ma, characterized by simple core forms on cobbles and chunks (choppers, discoids, polyhedrons), battered percussors (hammerstones and spheroids), flakes and fragments, and retouched forms such as flake scrapers. Cut marks and fracture patterns on animal bones indicate meat and marrow processing, with the use of simple stone knives and hammers. This stage is associated with the later australopithecines and the earliest forms of the larger-brained genus Homo and documents the first hominid dispersal out of Africa and into Eurasia, (b) The Acheulean, which lasted from approximately 1.7 Ma to 250,000 years ago and was characterized by large bifaces such as handaxes, cleavers, and picks. The early Acheulean is associated with Homo erectus/ergaster, while the later Acheulean (by ca. 500,000 years ago) is associated with the even larger-brained Homo heidelbergensis. (2) The Middle Paleolithic/Middle Stone Age, from about 250,000 to 30,000 years ago, characterized by a focus on retouched flake tools, such as scrapers, points, and backed knives, and prepared core technologies such as the Levallois method. The controlled production and use of fire appears to be widespread for the first time. This stage is especially associated with archaic forms of Homo sapiens (having modern-size brains but more robust faces and postcranial skeletons), including the Neanderthals (see Neanderthals and Their Contemporaries) and the earliest anatomically modern humans (see Origin of Modern Humans). (3) The Late Paleolithic, from 40,000 until 10,000 years ago, characterized by blade tool industries; a proliferation of artifacts in bone, antler, and ivory; and the emergence of rich symbolic art in the form of paintings, engravings, sculpture, and personal body adornment (see Archaeology; Cultural Evolution in Africa and Eurasia During the Middle and Late Pleistocene; Dispersals of Early Humans: Adaptations, Frontiers, and New Territories). Early examples of clear architectural structures, musical instruments, and mechanical devices (spear-throwers and bows and arrows) appear during this time. This stage is especially associated with anatomically modern humans, Homo sapiens sapiens.

*Email: [email protected] Page 1 of 21

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_64-4 # Springer-Verlag Berlin Heidelberg 2013

Introduction The Paleolithic is the term applied to a very broad, early period of human prehistory beginning with the first archaeological evidence of stone toolmaking approximately 2.6 Ma, through to the end of the Pleistocene epoch about 10,000 years ago, when the last continental glaciation receded. It documents the emergence of a wide range of new technological, behavioral, and adaptive traits through time (Toth and Schick 2010). It is important to appreciate that over 99 % of human technological development took place during the Paleolithic. The Paleolithic thus constitutes the bulk of the time span of human technological development and human prehistory and documents the emergence and evolution of the genus Homo. The term is applied primarily to prehistoric developments in the Old World, as the New World’s earliest archaeological evidence appears only toward the very end of Paleolithic times, during the last phases of the terminal Pleistocene glaciation. In the New World, however, the period of Late Ice Age hunter-gatherers is often referred to as “Paleo-Indian” and is contemporaneous with the last few thousand years of the Paleolithic in the Old World. For overviews of human evolution and the Paleolithic, see also Boyd and Silk (2012), Burenhult (2003), Clark (1982), Ciochon and Fleagle (2006), Delson et al. (2000), Gamble (1986), Johanson and Edgar (1996), Jones et al. (1992), Klein (2009), Lewin and Foley (2004), Mithen (1996), Noble and Davidson (1996), Renfrew and Bahn (1996), Roberts (2011), Scarre (2013), Schick and Toth (1993), Stringer and Andrews (2005), Tattersall (1999), Tattersall and Schwartz (2000), and Toth and Schick (2010). “Paleolithic” literally means the “Old Stone” (paleo ¼ old, lithic ¼ stone) Age, as it represents the earliest phases of human technological development when the vast majority of the tools represented in the archaeological record were made of stone. At the end of the Pleistocene, the Paleolithic is followed by the later phases of the Stone Age, the Mesolithic and then the Neolithic. During the Mesolithic (in some regions referred to as the “Epipaleolithic”), stone technologies continued to evolve as stone tool-using hunter-gatherers adapted to changing environments of the current (Holocene) epoch, sometimes characterized by small (microlithic) stone tools. During the last phase of the Stone Age, often referred to as the Neolithic (or “New Stone” Age), a transition occurred from hunting-gathering to a more settled way of life based on food production (agriculture and herding), but stone continued for some time to be used for tools (such as ground axes, projectile points, and sickles). The Paleolithic is traditionally divided into three major subdivisions: (1) the Early Paleolithic (also sometimes called the Lower Paleolithic) or Early Stone Age (ca. 2.6 Ma to 250,000 years ago); (2) the Middle Paleolithic or Middle Stone Age (ca. 250,000–30,000 years ago); and the Late Paleolithic (also Upper Paleolithic) or Later Stone Age (ca. 40,000–10,000 years ago). The “Lower”/“Middle”/“Upper” designations for the Paleolithic stages were developed in Europe in the late nineteenth and earlier twentieth centuries, based primarily on diagnostic artifact types and technological patterns observed in the stratigraphic and cultural sequences in various regions of Europe. More recently, with the appreciation that other parts of the world did not follow the precise cultural-historical sequence of Europe, many researchers have put less formal emphasis on these designations in favor of the more neutral terms “Early”/“Middle”/“Late” on a worldwide scale. This latter terminology will be used here. For the first hundred years of Paleolithic research, these Paleolithic subdivisions were used to express a general chronological sequence (a relative chronology) without a firm sense of how many years ago each phase began or ended (an absolute chronology). During the past half-century, however, radiometric dating techniques have allowed the development of a more precise

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_64-4 # Springer-Verlag Berlin Heidelberg 2013

chronological framework for this Paleolithic sequence worldwide (see “▶ Chronometric Methods in Paleoanthropology”), with approximate times for the beginning and end of each phase. Change from one stage of the Paleolithic to the next, however, does not always entail an immediate or complete turnover in artifact types, though it does generally represent an obvious and perceptible shift in the types of artifacts dominating the archaeological tool assemblages and often a corresponding shift in the dominant methods used in making these tools. For instance, while modified flake tools are present at a number of Lower Paleolithic sites, they become the dominant artifact form, often with consistent or repeated shapes, at many Middle Paleolithic sites. There is also some regional variation in the absolute chronology of the sequence, with evident technological transitions in some regions occurring earlier or later than in other regions. For instance, the transition from the Middle Paleolithic/Middle Stone Age to the Late Paleolithic/Later Stone Age happens somewhat earlier in some regions than in others.

Perspectives on Early Stone Tools The earliest prehistoric archaeological record is now approximately 2.6 Myr old, based on the recognition of flaked stone artifacts in securely dated deposits in East Africa. The fossil record of bipedal hominids, however, goes back at least 6 Ma, several Myr before the first appearance of stone tools (see volume 3, Chap. 5). On the basis of modern primate analogs, especially from chimpanzees, a range of tools and tool-using behaviors might be postulated for hominid populations prior to 2.6 Ma. Such hypothetical early tool use likely involved highly perishable, organic raw materials that provide no enduring, visible archaeological record. A handful of nonhuman species have been documented to show some minimal use of tools in the wild, including sea otters, birds (such as crows, finches, and Egyptian vultures), and even mud wasps (Shumaker et al. 2011). Aside from humans, however, the only other animals showing habitual use of a variety of tools for a variety of purposes are our closest living relatives, the chimpanzees (McGrew 1992). What is more, chimpanzee toolmaking and tool-using skills appear to be learned over several years, suggesting a simple culturally transmitted system. We now know that there is variability among different chimpanzee groups in the sets of tools (see “▶ Great Ape Social Systems”; “▶ The Biology and Evolution of Ape and Monkey Feeding”; “▶ The Hunting Behavior and Carnivory of Wild Chimpanzees”; “▶ Archaeology”) they commonly use, showing cultural variation among chimpanzees in their tool kits. Modern chimpanzee tool use includes nut cracking with stone and wood hammers and anvils, termite fishing, ant dipping with sticks or grass stems, and using chewed-up wads of leaves as sponges to obtain water or for self-cleaning. Although some chimpanzee tools consist of unmodified objects used for a particular task, chimpanzees do intentionally modify or shape some of their tools, such as the sticks and grasses used for termite fishing or ant dipping and the chewed leaves used as sponges. Deliberately manufactured stone artifacts in the early archaeological record represent the earliest evidence of tool production by early hominids. As such, they reveal the development of a reliance on stone tool use in early hominid adaptation by at least 2.6 Ma. Although stone tool use may have been affected by seasonal, environmental, or other opportunities, the archaeological record reveals a consistent manufacture of stone tools that persisted from this time onward until recent times. Early stone artifacts clearly indicate a number of interesting behavioral characteristics of these early hominids: they selected stone raw materials at specific locations, transported manufactured artifacts and unmodified stone from one place to another on the paleolandscape, and discarded artifacts (and sometimes parts of animal carcasses) in distinct concentrations at many localities Page 3 of 21

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_64-4 # Springer-Verlag Berlin Heidelberg 2013

Fig. 1 Kanzi, a bonobo (Pan paniscus or “pygmy chimpanzee”), flaking stone. Kanzi learned stone tool manufacture by modeling or imitation followed by years of trial and error, and he uses his tools to cut open a container to obtain food. His stone toolmaking skills have improved since the start of this experiment in 1990. Many of his artifacts resemble those found at Oldowan sites, although overall his flakes and cores still show some important differences from those found at Early Paleolithic sites

some distance from the raw material sources. Moreover, the manufacturing process used to produce early stone artifacts is one that is not observed in any nonhuman animal, even among chimpanzees, highlighting the novelty of behavioral innovation in the early stone toolmakers. Although early stone tools are admittedly simple and do not show elaborate shaping, they represent clear evidence of a new and unusual behavior pattern: the deliberate, controlled fracture of rock through percussive blows. Technological patterns seen in early stone artifacts indicate they were produced primarily through a technique sometimes called “free hand, hard hammer percussion.” This involves hitting one rock (the hammer) against another (the core) to bring about controlled fracture of the core (called conchoidal fracture, as the shock waves can produce radiating, shell-like ripples in finergrained materials) and produce numbers of sharp pieces called flakes, a process called flaking or knapping. Experiments have shown that the main objective of early stone tool making was likely the production of such sharp flakes to use as cutting tools. Thus, a primary tool in the early hominid tool kit was likely the sharp-edged flake, and many of the cores found at early sites were likely byproducts of the toolmaking process (see “▶ Archaeology”). Early stone toolmaking hominids were consistently producing such fractured stones at a number of early site localities. Early Paleolithic sites often involve dozens of flaked cores and thousands of flake products. Analysis of early archaeological materials often reveals extensive, controlled flaking of cores, involving rotation and manipulation to produce a series of flakes from the same

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_64-4 # Springer-Verlag Berlin Heidelberg 2013

piece of stone. Such fine core manipulation and exploitation is observable at even the very earliest Stone Age sites at Gona in Ethiopia, showing consistent, controlled, and skillful flaking of cores by 2.6 Ma. With such skillful flaking observable among early hominid toolmakers on the one hand and the diverse tool-using and toolmaking cultures observable in chimpanzees (McGrew 1992) on the other, a natural question is whether the production of early stone tools represents skills beyond those seen in other apes. Wild chimpanzees are known to have ca. 40 cultural traits, which can pattern geographically (Whiten et al. 1999). At the subspecies level, chimpanzee groups in closer proximity tend to share more of these cultural traits (Toth and Schick 2009; Whiten et al. 2009). Although chimpanzees are known to use stones as hammers and anvils in nut-cracking activities in West Africa, wild chimpanzee tool manufacture does not involve the intentional percussive flaking of stone, and wild chimpanzees have not developed sharp-edged tools for cutting in their assorted tool kits. It has been possible, however, to explore through experiments how comparable toolmaking skills of early hominids are to those of apes in captivity. An essential question in such experiments is whether the toolmaking skills of early hominids represent a significant departure from an ape “substrate” of toolmaking ability and what insights we might gain regarding early hominid cognitive abilities. Do early hominid toolmakers exhibit special cognitive or biomechanical skills or abilities, or do these emerge only much later in human biological and technological evolution? (see “▶ Theory of Mind: A Primatological Perspective”) Experiments were begun in 1990 teaching a bonobo (see “▶ Great Ape Social Systems”; “▶ Primate Intelligence”) (pygmy chimpanzee), Kanzi (Savage-Rumbaugh and Lewin 1994), to make and use stone tools (Fig . 1) (Toth et al. 1993; Schick et al. 1999). The experiment involved introducing the use of a stone tool for cutting and retrieving a foodstuff, initial demonstrating (modeling) stone tool manufacture, and a subsequent period of trial-and-error learning on Kanzi’s part in both the toolmaking and tool-using operations. This experiment has clearly shown that apes can become adept at some aspects of stone toolmaking. However, after more than 15 years of this experiment, some distinct technological differences have persisted in the bonobos’ artifacts compared to artifact assemblages found at early Paleolithic sites (Toth et al. 2006; Toth and Schick 2009). Some of these differences appear to reflect lesser skill in the bonobo toolmaker, perhaps reflecting lesser cognitive appreciation of particular facets of the toolmaking process (such as flaking sharper edges of the core), although others are likely related to biomechanical differences in the hand and arm of the apes. This experiment highlights how skilled and adept early stone hominids were in their stone toolmaking by the time of the earliest known archaeological occurrences 2.6 Ma. The skillfulness reflected in the earliest stone tools might suggest that even earlier stone technologies existed, yet undiscovered and perhaps rare on the paleolandscape, whose makers were not quite as proficient in flaking stone and who did not produce such a readily recognizable product. Or it may be that hominids were “preadapted” to efficiently flaking stone because of selection for other manipulative skills that were later transferred to stone knapping when the need arose. The ape stone tool making experiments give important clues as to what technological characteristics might be found in such hypothetical “Pre-Oldowan” technologies.

Early Paleolithic The Early Paleolithic comprises a long time interval, between 2.6 Ma and approximately 250,000 years ago. It not only includes this extremely large span of human prehistory but also encompasses, Page 5 of 21

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_64-4 # Springer-Verlag Berlin Heidelberg 2013

over time, sites across huge geographical distances, from southern Africa to eastern Asia. During this period of more than 2.25 Myr, profound evolutionary changes occurred among hominids, and some marked changes are observed in the archaeological record in multiple parts of the Old World. In Africa, where the Early Paleolithic is often referred to as the Early Stone Age, two industries have been recognized: (1) The first to appear, starting 2.6 Ma, the Oldowan industry (named after Olduvai Gorge in Tanzania), consists of stone industries containing simple cores and flaked pieces, along with some battered artifacts such as hammerstones and (2) starting between 1.7 and 1.5 Ma, or approximately 1 Myr after the onset of Oldowan technology, the Acheulean industry (named after the locality of St. Acheul in France) appears, with new distinctive artifact forms in the form of relatively large bifacial tools (handaxes, cleavers, and picks).

Oldowan The Oldowan is the first recognizable archaeological record, with simple flaked and battered stone artifacts, sometimes found with cut-marked and broken animal bones, emerging around 2.6 Ma. Although similar types of simple lithic industries are found throughout time, archaeologists usually use a cutoff of around 1 Ma when referring to the Oldowan Industrial Complex. The Oldowan coexisted for several hundred thousand years with the Acheulean handaxes industries, starting about 1.76 Ma. Oldowan sites are known first from Africa and subsequently document the spread of hominids outside of Africa into parts of Eurasia, notably producing archaeological sites in the Near East, the Republic of Georgia, and eastern Asia. These sites are found especially in tropical and subtropical climatic regimes, in particular grassland/woodland environments. At Dikika, Ethiopia, it has been argued that marks on surface bovid bones believed to date to 3.3 Ma were produced by stone tool-wielding hominids, in this case the contemporary Australopithecus afarensis (McPherron et al. 2010). Others, however, have argued that these marks could be produced by crocodile teeth (Njau 2012) or by trampling (Dominguez-Rodrigo et al. 2010). No stone tools have been found at this locality. Until new evidence comes to light, the claim of stone cutting tools from this time period should be regarded as unsubstantiated. In East and North Africa, most Oldowan sites are open-air occurrences that are located along stream courses, in deltaic settings, or on lake margins. These were areas of close proximity to water and were depositional settings where sediments could build up over time. In South Africa, Oldowan artifacts are found in karstic limestone cave deposits and may have been carried there by hominids or brought in by natural forces such as slope wash or gravity. The high incidence of hominid bones in South African cave deposits (especially robust australopithecines) may be the result of predation and/or scavenging by carnivore such as leopards and hyenas. Oldowan industries are contemporaneous with a number of bipedal hominid forms, including later australopithecines (see “▶ The Species and Diversity of Australopiths”) (Australopithecus garhi, A. aethiopicus, A. robustus, and A. boisei), whose cranial capacities ranged from about 400 to 550 cm3, and early forms of the more encephalized genus Homo (see “▶ Evolution of the Primate Brain”) (H. rudolfensis, H. habilis, H. ergaster/erectus), whose cranial capacities ranged from about 600 to 850 cm3. Although it is possible that all of these hominids used stone technology to a greater or lesser extent, many anthropologists believe that the genus Homo was probably the more habitual toolmaker and tool user, as its brain size almost doubles in the first million years of the Oldowan, while its jaws and teeth tend to diminish in robusticity. By 1 Ma, only Homo ergaster/ erectus was known in the human paleontological record, while the australopithecines became extinct. Interestingly, Homo ergaster/erectus appears to have much more modern limb proportions and stature relative to earlier hominids and is the first form clearly identified outside of Africa (see

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_64-4 # Springer-Verlag Berlin Heidelberg 2013

Fig. 2 Typical Oldowan artifacts found at Early Paleolithic sites. These are examples of flaked and battered stone artifacts found at Olduvai Gorge, with their common or conventional designations (“types”) noted

“▶ Homo ergaster and Its Contemporaries”; “▶ Later Middle Pleistocene Homo”; “▶ Defining Homo erectus”). Oldowan industries are characterized by simple technologies (sometimes called Mode 1) consisting of cores made on pebbles or chunks (choppers, discoids, polyhedrons, heavy-duty scrapers, facetted spheroids), battered percussors (hammerstones and battered spheroids), debitage (flakes and fragments), and retouched pieces (scrapers, awls, etc.) (Fig . 2) (Hovers and Braun 2009; Isaac 1989; Leakey 1971; Schick and Toth 2010; Toth and Schick 2006, 2009). Common raw materials include volcanic lavas, quartz, and quartzite. The most common techniques for producing Oldowan artifacts were hard hammer percussion and bipolar technique (in which the core to be flaked is set on a stone anvil and hit with a stone hammer). At Olduvai Gorge, some technological trends have been observed through time, with later Oldowan sites showing higher frequencies of such artifact classes as scrapers and battered spheroids and lower frequencies of choppers. These sites are sometimes assigned to a “Developed Oldowan,” but this designation is more difficult to apply elsewhere. Microwear patterns on a small sample of Oldowan tools suggest that flakes were used for animal butchery, woodworking, and cutting soft plant matter. Experiments in using stone tools (Fig . 3) have shown that Oldowan flakes can be used to efficiently process the carcasses of animals from the size of small mammals to elephants (Fig . 4) and stone hammers could easily break bones for access to nutritious marrow and skulls for brain tissue. Choppers could have been used to chop branches to make spears or digging sticks, although many such Oldowan core forms were probably by-products of flake production. It is likely that a rich range of perishable organic material cultures were also used, including containers of shell, horn, skin, or bark; wooden clubs and/or throwing sticks; wooden spears or digging sticks (Fig . 5); and horn or bone fragments as digging tools. In addition, a small sample of bone specimens from South African caves are polished and striated on their pointed end, suggesting that these may have been used as opportunistic digging tools to gain access to underground vegetable resources or insects such as termites.

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_64-4 # Springer-Verlag Berlin Heidelberg 2013

Fig. 3 Potential functions of Early Paleolithic artifacts, both Oldowan and Acheulean forms, based on experiments using tool replicas for various purposes

Although evidence of fire has been found at a few Oldowan sites (in the form of reddened, baked sediments, burnt bones, or fire-cracked stone), it cannot be ruled out that natural agents, such as lightning strikes and brushfires, may have produced these fires. No clear architectural structures have been found at Oldowan sites, and it is possible that Oldowan hominids could have been sleeping in trees at night (perhaps building nests like chimpanzees) rather than on the ground, in order to avoid predation by nocturnal carnivores (see “▶ The Biology and Evolution of Ape and Monkey Feeding”; “▶ Great Ape Social Systems”; “▶ The Hunting Behavior and Carnivory of Wild Chimpanzees”). It seems clear that these Oldowan hominids were concentrating lithic material and animal bones at favored locations on the landscape (a pattern not seen in nonhuman primates today), but the precise behavioral patterns that formed these concentrations are still debated. Interpretations for these concentrations include home bases or central foraging places; favored places due to

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_64-4 # Springer-Verlag Berlin Heidelberg 2013

Fig. 4 Butchery of an elephant, the world’s largest terrestrial mammal, using simple Oldowan flakes (The elephant had died of natural causes)

proximity to shade, water, or food resources; intentional stone caches; and scavenged carnivore accumulations. It is also possible that Oldowan sites formed through more than one behavioral pattern. Cut marks and percussion marks/fractures on bones show that hominids were accessing meat and marrow resources from animal carcasses obtained through scavenging or hunting. The modified bones at Oldowan sites typically come from animals ranging in size from small mammals to those weighing hundreds of pounds. This is a scale of carnivory that is not seen in the nonhuman primate world and was most likely greatly facilitated through the use of stone tools. At present, there is debate as to whether hominids accessed larger animals through more marginal scavenging (getting the ravaged leftovers of carnivore kills) or, rather, had access to more complete carcasses through hunting or confrontational scavenging. In any case, the processing of larger animal carcasses could have significantly increased the dietary breadth (and thus survivorship and reproductive success) of Oldowan hominids, although the majority of Oldowan hominid diet was likely derived from plant foods such as fruits, berries, nuts, edible leaves, and underground storage organs (roots, tubers, corms, and rhizomes). Carrying devices may have facilitated the collection and transport of dietary items that could be consumed at a later time. Important Oldowan localities include Gona, Fejej, and the Omo Valley in Ethiopia; East and West Turkana in Kenya; Olduvai Gorge in Tanzania; Sterkfontein and Swartkrans Caves in South

Fig. 5 Sharpening a wooden branch with a simple stone flake. Such implements could have been used as spears, digging sticks, or skewers to carry meat resources Page 9 of 21

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_64-4 # Springer-Verlag Berlin Heidelberg 2013

Fig. 6 Early Acheulean tools: relatively crude handaxe (left) and cleaver (right), approximately 1.4 Myr old. These artifact forms, made on large flakes or cobbles, show definite shaping to leave a sharp working edge, especially toward the tip end of the handaxe and the bit of the cleaver, with the lower part of the tool shaped or left natural to serve as a handle. They usually show some, though relatively low, degree of symmetry in their plan view and their cross-section and were made by hard hammer percussion

Africa; Ain Hanech and El Kherba in Algeria; the lowest levels at Ubeidiya in Israel; and Dmanisi in the Republic of Georgia.

Acheulean The Acheulean Industrial Complex is characterized by the presence of large bifacial handaxes, cleavers, and picks (sometimes called Mode 2 technologies), which are found from approximately 1.76 Ma to 250,000 years ago. The earliest known Acheulean sites are Kokiselei 4, West Turkana, Kenya, dated to 1.76 million years ago (Lepre et al. 2011), and Konso in Ethiopia, dated to 1.76 million years ago (Beyene et al. 2013). At Kokiselei four large cobbles of phonolite lava were flaked into crude handaxes and picks, while at Konso-Gardula, similar large picks and bifaces and unifaces were manufactured primarily from large flakes. Such handaxe/cleaver industries are contemporaneous and sometimes regionally co-occurring with the simpler Oldowan-like (Mode 1) industries. Acheulean and contemporaneous Mode 1 industries are found throughout Africa and Eurasia, but classic handaxe and cleaver assemblages are especially characteristic of Africa, the Near East, the Indian subcontinent, and Western Europe. Elsewhere, notably Eastern Europe and most of eastern Asia, simpler Mode 1, Oldowan-like technologies are found. This was a period of major climatic change, with numerous cold/warm oscillations that would have especially affected northern latitudes of Eurasia. For most of this period, hominids would have flourished only during Page 10 of 21

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_64-4 # Springer-Verlag Berlin Heidelberg 2013

Fig. 7 Late Acheulean tools: beautifully made, highly symmetrical handaxes and cleavers typical of the latter part of the Acheulean, approximately 400,000 years old. These forms clearly show more cognitive complexity, craftsmanship, and probably an aesthetic sense hundreds of thousands of years before the first representational art

the warmer periods in these northern latitudes. Hominids extended their range from grasslands and woodlands of tropical and subtropical regions to cooler, more temperate climates during this period (Fleagle 2010; Gamble 2005; Norton and Braun 2010; Shipton and Petraglia 2010). Contemporaneous hominid forms (see “▶ Homo ergaster and Its Contemporaries”) include Homo ergaster/erectus and the later, larger-brained Homo heidelbergensis (sometimes referred to as “early archaic Homo sapiens”). Cranial capacities range from about 800 to 1,400 cm3, generally increasing over the time span of this period. In the early Acheulean, robust australopithecines (see “▶ Analyzing Hominin Phylogeny”; “▶ The Species and Diversity of Australopiths”) (A. robustus and A. boisei) still existed, but most anthropologists do not regard these forms as plausible Acheulean toolmakers, and in any case they appear to have gone extinct by 1 Ma. New elements in Acheulean industries (in addition to Mode 1, Oldowan-like artifacts that continue to be found) include handaxes, cleavers, picks, and knives (generically called “bifaces”) made either on large flakes struck from boulder cores or on larger cobbles and nodules. A range of well-made retouched tools, such as side scrapers, awls, and backed knives, are also common. Frequently used raw materials include fine-grained lavas, quartzites, and flints. Earlier, cruder bifaces were produced by hard hammer percussion (Fig . 6), while later more refined bifaces were probably finished by the soft hammer technique, in which a softer material, such as wood, bone, ivory, antler, or even soft stone, was used as a percussor, producing thinner, more invasive flakes (Fig . 7). Prepared core techniques, notably the Levallois tortoise core technique (in which a large, predetermined flake is removed from the upper surface of a discoidal core) and, more rarely, early blade production, are found in some later Acheulean industries. Sharpened wooden spears are known from later Acheulean times, as at Scho¨ningen in Germany (see “▶ Archaeology”) and Clacton in England, suggesting that more formal hunting weaponry was established as part of a regular subsistence pattern by at least this time if not earlier. Page 11 of 21

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_64-4 # Springer-Verlag Berlin Heidelberg 2013

The fact that Acheulean and contemporaneous hominids successfully occupied cooler, more temperate latitudes suggests that they were better adapted to such cooler conditions. Use-wear patterns on side scrapers indicate that many of these tools were used to scrape hides, strongly suggesting that animal skins were being used for simple clothing, blankets, and/or tent or hut coverings. Evidence of fire in the form of charcoal or ash layers is occasionally seen in later Acheulean times but is by no means widespread in the archaeological record during this period. There is no definitive evidence of architectural structures during Acheulean times, although arguments have been made in this regard. Sites are found in numerous caves and rock shelters as well as many open-air sites. Handaxes and cleavers, in particular, indicate the ability to impose bilateral symmetry on lithic materials. This clearly shows higher cognitive abilities and motor skills than are manifested in the Oldowan. Even modern humans who learn to make stone tools normally require considerable apprenticeship before they can produce well-made handaxes and cleavers. Although there is a wide range of handaxe forms through time and space, it is common that at certain Acheulean sites, there are recurrent shapes and sizes, as if there were stylistic norms of production among their makers. Presence of ocher at some sites and, occasionally, incised bone may indicate the emergence of proto-symbolic behavior as well. Important Acheulean sites/localities include Konso-Gardula, Middle Awash, Melka Kunture, and Gadeb in Ethiopia; Olduvai Gorge and Peninj in Tanzania; Olorgesailie and Isenya in Kenya; Kalambo Falls in Zambia; Elandsfontein and Montagu Cave in South Africa; Ternifine in Algeria; Ubeidiya and Gesher Benot Ya’aqov in Israel; Swanscombe, Hoxne, and Boxgrove in England; Saint-Acheul and Terra Amata in France; and Torralba and Ambrona in Spain. Important contemporaneous Mode 1 localities include Atapuerca (TD6) in Spain, Arago Cave in France, Clacton in England, Bilzingsleben and Scho¨ningen in Germany, Ve´rtesszo¨lo¨s in Hungary, Isernia in Italy, and the Nihewan Basin and Zhoukoudian (“Peking Man”) cave in China. It has recently been argued (Wilkins et al. 2012) that stone points from Kathu Pan 1, South Africa, believed to date to ca. 500,000 years ago, could have functioned as hafted spear points, based upon the morphology of the artifacts and edge damage. These artifacts are associated with a stone tool industry, often referred to as the “Fauresmith” that includes handaxes and is considered by some to be transitional between the Acheulean and the Middle Stone Age. If this argument is valid, this would put the origins of hafted technologies several hundred thousand years before the first widely accepted evidence of hafting (see “▶ Archaeology”; “▶ Cultural Evolution in Africa and Eurasia During the Middle and Late Pleistocene”; “▶ Dispersals of Early Humans: Adaptations, Frontiers, and New Territories”). Kathu Pan 1 also shows evidence of systematic blade production, another trait which tends to appear in the archaeological record in later times (Wilkins and Chazan 2012).

Middle Paleolithic/Middle Stone Age The Middle Paleolithic industries of Europe, the Near East, and North Africa (sometimes called the “Mousterian” after the site of Le Moustier in France) and Middle Stone Age industries of subSaharan Africa are found between approximately 250,000 and 30,000 years ago. They are found in tropical, subtropical, temperate, and even periglacial climatic regimes. During this time, hominids extended their ranges to most environmental zones of Africa and Eurasia except harsh deserts, the densest tropical forests, and extreme northern or arctic tundras. It appears that hominids were somehow able to cross the water between Southeast Asia and Australia and then attached to New Page 12 of 21

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_64-4 # Springer-Verlag Berlin Heidelberg 2013

Fig. 8 Middle Paleolithic tools: numerous retouched flake tools, such as side scrapers, points, and denticulates, were made on flake blanks, some struck from prepared cores. It is possible that some of these points were hafted to wooden shafts as thrusting or throwing spears

Guinea and Tasmania, by late in this period. Contemporary hominid forms include those often designated as archaic Homo sapiens (including the Neanderthals of Europe and the Near East) and anatomically modern humans. Handaxes and cleavers tend to be less common (although toward the end of the Middle Paleolithic of Western Europe, smaller, well-made handaxes are found), and the emphasis in these stone industries is on retouched forms made on flakes (such as side scrapers, denticulates, and points) that become numerous in many of these assemblages (Fig . 8). Hard hammer and soft hammer techniques were common during this period. Many of these industries exhibit prepared core methods, notably the Levallois technique for more controlled production of flakes, points, and sometimes blades. Wooden spear technology continues from the Acheulean (as seen at Lehringen, Germany, where a spear with a fire-hardened tip was associated with an elephant carcass), and stone points with tangs or thinned bases suggest that these forms may have been hafted onto spear shafts, suggesting the development of composite tools. Rare bone points are also known from this time. Fire and hearth structures are much more common during this period, although clear architectural features outlined by stones or bones are rare. Sites are numerous in caves and rock-shelters, as well as open-air sites on plateaus and along river floodplains. Occasional perforated and grooved shells and teeth at a few sites imply the emergence of some personal adornment and, along with the infrequent presence of ocher as well as a number of welldocumented burials, suggest at least some symbolic component to hominid behavior during this period of the Paleolithic (McBrearty and Brooks 2000). Important Middle Paleolithic/Middle Stone Age sites include Combe Grenal, Pech de L’Aze´, Le Moustier, La Quina, and La Ferrassie in France; Krapina in Croatia; Cueva Morin in Spain; Tabun, Skhul, Kebara, Amud, and Qafzeh in Israel; Shanidar in Iraq; Dar es-Soltan in Morocco; Bir el Ater Page 13 of 21

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_64-4 # Springer-Verlag Berlin Heidelberg 2013

Fig. 9 Late Paleolithic tools: tools made on blades struck from prepared cores were important components of these technologies, made into such forms as end scrapers, burins, and points, as were formal tools shaped from bone, antler, and ivory

in Algeria; Haua Fteah in Libya; Kharga Oasis in Egypt; Dire´-Dawa, Omo-Kibish, and Middle Awash in Ethiopia; Enkapune Ya Muto, Prospect Farm, and Kapthurin in Kenya; Kalambo Falls and Twin Rivers in Zambia; and Florisbad, Border Cave, Klasies River Mouth Cave, and Die Kelders Cave in South Africa.

Late Paleolithic The Late Paleolithic (often called Upper Paleolithic in Europe and Later Stone Age in Africa) is found between 40,000 and 10,000 years ago, at which time the last glaciation receded. This period of human prehistory overlaps and is contemporaneous with the end of the Middle Paleolithic/ Middle Stone Age in some regions. During this time, humans inhabited tropical, subtropical, temperate, desert, and arctic climates; occupied present-day Australia, New Guinea, and Tasmania after crossing significant bodies of water; and, late in this period, spread to the Americas via the Bering Straits (see “▶ The Dentition of American Indians: Evolutionary Results and Demographic Implications Following Colonization from Siberia”; “▶ Dispersals of Early Humans: Adaptations, Frontiers, and New Territories”). Late Paleolithic industries are almost always associated with anatomically modern humans (Homo sapiens sapiens), but some early Upper Paleolithic sites in Europe are also contemporaneous with the last populations of Neanderthals (see “▶ Neanderthals and Their Contemporaries”) there. Late Paleolithic stone industries are often characterized by blade technologies, elongated flakes produced by soft hammer or indirect percussion, in which a punch is placed on the edge of a blade core and struck with a percussor. These blades were then made into a variety of tool forms, including end scrapers, burins, and backed knives (Fig . 9). Some Late Paleolithic technologies emphasized bifacial points, such as the Solutrean of Spain and France and the Paleo-Indian Page 14 of 21

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_64-4 # Springer-Verlag Berlin Heidelberg 2013

Fig. 10 Examples of probable symbolic behavior in Late Paleolithic times, expressed in art, personal adornment, music, notation, burial, and possibly more formal architecture

occurrences of the New World (Clovis and Folsom) (see “▶ The Dentition of American Indians: Evolutionary Results and Demographic Implications Following Colonization from Siberia”). Such points may have been produced by soft hammer technique or by pressure flaking, in which small flakes are detached by directed pressure rather than by percussion. Some raw materials appear to have been heat treated to make them easier to work. Other Late Paleolithic technologies emphasized bladelets (small blades) and geometric microliths, which were hafted as composite tools into a range of projectiles and cutting tools. These microlithic technologies are characteristic of the Later Stone Age of Africa as well as some parts of central and eastern Asia. A diagnostic element of many Late Paleolithic industries is an emphasis on nonlithic materials for tools, including bone, antler, and ivory, made into a range of artifact forms such as points, needles, spear-throwers, shaft straighteners, and harpoons. Hooked spear-throwers are essentially mechanical devices to increase the velocity and/or distance of a projectile, and thus represent a significant advance in hunting technology or weaponry. The small size of some points and microliths toward the end of the Late Paleolithic suggest the development of bow and arrow technology, and arrows are preserved at Stellmoor, Germany. Several human sculptures from the Late Paleolithic suggest clothing such as hooded parkas, headdresses, and aprons. The development of bone and antler needles also suggests that sewed clothing was common after 20,000 years ago, and recently discovered impressions on fired clay fragments from the Czech Republic indicate woven textiles, presumably of plant material. Controlled use of fire appears to be a universal trait during this period, with hearths sometimes lined with stones. Architectural features are much more common than in earlier periods, with hut

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_64-4 # Springer-Verlag Berlin Heidelberg 2013

structures delineated by stone or bone patterns, by postholes, and sometimes with hearth structures and other apparent activity areas within (such as toolmaking or tool-using). Sites tend to be more numerous and have denser concentrations of materials, suggesting larger populations and more regular habitation of sites. Relatively late in the time span of the Late Paleolithic, the first evidence of human occupation of the Americas appears. The most widespread evidence is attributed to the Clovis culture, characterized normally by fluted spear points and often associated with mammoth remains, dating to ca. 13,500–13,000 years ago. Several sites may predate the Clovis in the Americas by several thousand years (Meltzer 2010). One of the most distinctive characteristics of the Late Paleolithic is the proliferation of symbolic expression in art and personal adornment (Fig . 10). This can be seen in the naturalistic representation of animals and, more rarely, humans in painting and sculpture as well as in the more abstract geometric designs. A variety of media were employed for artistic expression, including use of charcoal, pigment paints, antler, bone and ivory, and clay, as well as a diversity of techniques, including drawing, painting, engraving, carving, and modeling. Personal adornments are sometimes numerous, manifested in beads or pendants of shell, bone, tooth, antler, ivory, and stone. This proliferation of symbolic expression, best seen in the European Upper Paleolithic, has sometimes been referred to as the “Creative Explosion.” Some of these artistic manifestations, particularly paintings, drawings, and engravings, are located in deep, hard-to-access recesses of caves, suggesting a ritualistic and religious aspect to this symbolism. In view of the complexity of the material culture of this period and its well-developed symbolic component, it is likely that modern human language abilities were fully developed by this time, if not before. Late Paleolithic burials are more common and more elaborate than in the Middle Paleolithic. Men, women, and children were sometimes interred with rich grave goods, including stone tools, jewelry, and bone/antler/ivory artifacts. Again, this suggests an important symbolic component and a probable belief in an afterlife, in other words, something akin to a spiritual belief and a religion. Important sites include Lascaux, Pincevent, La Madeleine, Abri Pataud, Cro-Magnon, Solutre´, Chauvet, and Laugerie Haute in France; El Castillo, Altamira, and Parpallo´ in Spain; Dolnı´ Veˇstonice in the Czech Republic; Vogelherd in Germany; Ista´llo´sko¨ in Hungary; Willendorf in Austria; Kebara Cave in Israel; Ksar Akil in Lebanon; Kostienki and Sungir in Russia; Mezin and Mezhirich in Ukraine; Mal’ta in Siberia; Zhoukoudian Upper Cave in China; Lukenya Hill in Kenya; Mumba Cave in Tanzania; Nelson Bay Cave, Die Kelders, Elands Bay Cave, and Wilton, in South Africa; Haua Fteah in Libya; Lake Mungo in Australia; and Blackwater Draw in New Mexico (North America).

Conclusion The earliest evidence of hominid technology dates to between 2.6 and 2.5 Ma in the Ethiopian Rift Valley. The Oldowan, characterized by simple cobble cores, flakes, retouched flakes, and battered percussors, is associated in time with later australopithecines and early forms of larger-brained hominids assigned to the genus Homo. Cut marks on fossil mammalian bones and hammerstone fracture of long bones indicate that one aspect of these early technologies was the processing of animal carcasses. By 1.8–1.7 Ma, the prehistoric record documents the emergence of Homo ergaster/erectus and the early Acheulean, characterized by new artifact forms such as handaxes, cleavers, and picks. The Page 16 of 21

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_64-4 # Springer-Verlag Berlin Heidelberg 2013

first hominid migrations out of Africa and into Eurasia are documented at the same time. Later Acheulean sites, ca. 500–250 Ka, are often characterized by better-made and more symmetrical handaxes and cleavers and are associated with Homo heidelbergensis. Handaxe industries are known for much of Africa, the Near East, Western Europe, and the Indian subcontinent. In much of Eastern Europe and East Asia, contemporary hominid populations were producing simpler cobble cores and a range of retouched flake tools. The Middle Stone Age/Middle Paleolithic emerges around 250 Ka, usually characterized by prepared core technologies (e.g., Levallois cores, flakes, and points), side scrapers, denticulates, and retouched points. In Africa these industries are associated with larger-brained archaic forms (sometimes assigned to Homo helmeii) and early anatomically modern humans. In the Near East, such industries are associated with Neanderthals and modern humans. In Europe the Middle Paleolithic appears to be exclusively associated with Neanderthals. In East Asia during this time, the lithic industries are usually simpler core/flake/retouched flake industries, associated with archaic forms of hominids. Evidence of fire becomes very common during this period. The Late Paleolithic (Upper Paleolithic, Later Stone Age) emerges in the Old World in the last 50,000 years. Industries are often characterized by blade production, blade tools such as backed knives, end scrapers, and burins, and a range of unifacial and bifacial point styles. For the first time, materials such as bone, antler, and ivory (and presumably a very rich wood technology) became major raw materials for tools. Architectural features such as hut structures and well-made hearths became common for the first time. The first representational artwork was produced on cave walls in the forms of paintings and engravings as well as mobiliary sculpture and engraving. During the last glaciation, modern humans reached Australia by 40 Ka and the Americas by at least 15 Ka. Around the world, stone industries document a greater variability over time and space, suggesting stronger regional cultural rules regarding material culture and more innovation and technological change over time. With more complex technologies and adaptive patterns, humans were able to occupy extreme environments such as dense tropical forests, arid deserts, and frigid tundras. In a number of places in the Near East, Africa, East Asia, Oceania, and North and South America, these Paleolithic foraging societies slowly emerged as sedentary farmers, and then in some of these places, complex societies emerged as “civilizations” with urban centers. The Paleolithic lasted over two-and-a-half million years and, in terms of duration, covers well over 99 % of human technological history. It is no exaggeration to say that the human lineage is a product of its Paleolithic past and that the modern human condition, characterized by industrialization, farming, urban life, and ever-increasing networks of communication and globalization, is firmly rooted in its Stone Age past.

Cross-References ▶ Archaeology ▶ Chronometric Methods in Paleoanthropology ▶ Cultural Evolution in Africa and Eurasia During the Middle and Late Pleisto ▶ Defining Homo erectus ▶ Defining the Genus Homo ▶ Dispersals of Early Humans: Adaptations, Frontiers, and New Territories ▶ Geological Background of Early Hominid Sites in Africa ▶ Homo ergaster and Its Contemporaries ▶ Later Middle Pleistocene Homo Page 17 of 21

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▶ Neanderthals and Their Contemporaries ▶ Origin of Modern Humans ▶ Paleodemography of Extinct Hominin Populations ▶ Primate Intelligence ▶ Quaternary Deposits and Paleosites ▶ Quaternary Geology and Paleoenvironments ▶ Role of Environmental Stimuli in Hominid Origins ▶ The Earliest Putative Homo Fossils ▶ The Evolution of the Hominid Brain ▶ The Evolution of Speech and Language ▶ The Species and Diversity of Australopiths ▶ Zoogeography: Primate and Early Hominin Distribution and Migration Patterns

References Beyene Y, Katoh S, WoldeGabriel G, Hart WK, Uto K, Sudo M, Kondo M, Hyodo M, Renne PR, Suwa G, Asfaw G (2013) The characteristics and chronology of the earliest Acheulean at Konso, Ethiopia. Proc Natl Acad Sci U S A 110:1584–1591 Boyd R, Silk JB (2012) How humans evolved, 6th edn. Norton, New York Burenhult G (2003) People of the past: the illustrated history of humankind. Fog City Press, San Francisco Ciochon RL, Fleagle JG (2006) The human evolution source book, 2nd edn. Pearson/Prentice Hall, Upper Saddle River Clark JD (1982) The Cambridge history of Africa. Cambridge University Press, Cambridge Delson E, Tattersall I, Van Couvering JA, Brooks AS (2000) Encyclopedia of human evolution and prehistory, 2nd edn. Garland, New York Fleagle JG (ed) (2010) Out of Africa I: the first hominin colonization of Eurasia. Springer, New York Gamble C (1986) The Palaeolithic settlement of Europe. Cambridge University Press, Cambridge Gamble C (2005) The hominid individual in context: archaeological investigations of Lower and Middle Palaeolithic landscapes, locales and artefacts. Routledge, London Hovers E, Braun DR (eds) (2009) Interdisciplinary approaches to the Oldowan. Springer, New York Isaac G (1989) The archaeology of human origins: papers by Glynn Isaac. Cambridge University Press, Cambridge Johanson D, Edgar B (1996) From Lucy to language. Simon & Schuster, New York Jones S, Martin R, Pilbeam D (1992) The Cambridge encyclopedia of human evolution. Cambridge University Press, Cambridge Klein RG (2009) The human career: human biological and cultural origins, 3rd edn. University of Chicago Press, Chicago Leakey MD (1971) Olduvai Gorge, vol 3, Excavations in beds I and II, 1960–1963. Cambridge University Press, Cambridge Lepre CJ, Roche H, Kent DV, Harmand S, Quinn RL, Brugal J-P, Texier P-J, Lenoble A, Feibel CS (2011) An earlier origin for the Acheulian. Nature 477:82–85 Lewin R, Foley RA (2004) Principles of human evolution, 2nd edn. Blackwell, Malden

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McBrearty S, Brooks A (2000) The revolution that wasn’t: a new interpretation of the origin of modern human behavior. J Hum Evol 39:453–563 McGrew WC (1992) Chimpanzee material culture: implications for human evolution. Cambridge University Press, Cambridge Meltzer DJ (2010) First peoples in a New World: colonizing Ice Age America. University of California Press, Berkeley Mithen S (1996) The prehistory of mind: the cognitive origins of art, religion, and science. Thames and Hudson, London Noble W, Davidson I (1996) Human evolution, language and mind: a psychological and archaeological inquiry. Cambridge University Press, Cambridge Norton CJ, Braun DR (eds) (2010) Asian paleoanthropology: from Africa to China and beyond. Springer, New York Renfrew C, Bahn P (1996) Archaeology: theories methods and practice, 2nd edn. Thames and Hudson, London Roberts A (2011) Evolution: the human story. Dorling Kindersley, London Savage-Rumbaugh S, Lewin R (1994) Kanzi: the ape at the brink of the human mind. Wiley, New York Scarre C (ed) (2013) The human past: world prehistory and the development of human societies, 3rd edn. Thames and Hudson, London Schick KD, Toth N (1993) Making silent stones speak: human evolution and the dawn of technology. Simon & Schuster, New York Schick K, Toth N (eds) (2010) The cutting edge: new approaches to the archaeology of human origins. Stone Age Institute Press, Gosport Schick K, Toth N, Garufi GS, Savage-Rumbaugh ES, Rumbaugh D, Sevcik R (1999) Continuing investigations into the stone tool-making and tool-using capabilities of a bonobo (Pan paniscus). J Archaeol Sci 26:821–832 Shipton C, Petraglia MD (2010) Inter-continental variation in Acheulean bifaces. In: Norton CJ, Braun DR (eds) Asian paleoanthropology: from Africa to China and beyond. Springer, New York Shumaker RW, Walkup KR, Beck BB (2011) Animal tool behavior: the use and manufacture of tools by animals. Johns Hopkins University Press, Baltimore Stringer C, Andrews P (2005) The complete world of human evolution. Thames and Hudson, London Tattersall I (1999) Becoming human: evolution and human uniqueness. Oxford University Press, Oxford Tattersall I, Schwartz J (2000) Extinct humans. Westview, Boulder Toth N, Schick KD (eds) (2006) The Oldowan: case studies into the earliest Stone Age. Stone Age Institute Press, Gosport Toth N, Schick KD (2009) The Oldowan: the tool making of early hominins and chimpanzees compared. Annu Rev Anthropol 38:289–305 Toth N, Schick KD (2010) Hominin brain reorganization, technological change, and cognitive complexity. In: Broadfield D, Yuan M, Schick K, Toth N (eds) The human brain evolving: paleoneurological studies in honor of Ralph L Holloway. Stone Age Institute Press, Gosport, pp 293–312 Toth N, Schick K, Savage-Rumbaugh ES, Sevcik R, Rumbaugh D (1993) Investigations into the stone tool-making and tool-using capabilities o a bonobo (Pan paniscus). J Archaeol Sci 20:81–91 Page 19 of 21

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Toth N, Schick K, Semaw S (2006) A comparative study of the stone tool-making skills of Pan, Australopithecus, and Homo sapiens. In: Toth N, Schick K (eds) The Oldowan: case studies into the earliest Stone Age. Stone Age Institute Press, Gosport, pp 155–222 Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V, Yugiama Y, Tutin C, Wrangham R, Boesch C (1999) Culture in chimpanzees. Nature 399:420–435 Whiten A, Schick K, Toth N (2009) The evolution and cultural transmission of percussive technology: integrating evidence from palaeoanthropology and primatology. J Hum Evol 57:420–435 Wilkins J, Chazan M (2012) Blade production ~500 thousand years ago at Kathu Pan 1, South Africa: support for a multiple origins hypothesis for early Middle Pleistocene blade technologies. J Archaeol Sci 39:1883–1900 Wilkins J, Schoville BJ, Brown KS, Chazan M (2012) Evidence for early hafted hunting technology. Science 338:942–946

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Index Terms: Acheulean 10 Ape technology 5 Australopithecines 6 Biface technology 11 Early Homo sapiens 11 Early Paleolithic 2, 4–5 Handaxes 12, 16 Homo erectus 6, 11 Homo heidelbergensis 11, 17 Late Paleolithic 2, 14 Lithic technology 6, 12 Middle Paleolithic 2, 12 Middle Stone Age 12 Modern Homo sapiens 13–14 Oldowan 6 Paleolithic 2–3 Stone tools 3–5 Upper Paleolithic 14

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_66-2 # Springer-Verlag Berlin Heidelberg 2013

Cultural Evolution in Africa and Eurasia During the Middle and Late Pleistocene Nicholas Conard* Eberhard-Karls-Universität T€ ubingen, Institut f€ ur Ur- und Fr€uhgeschichte, Abteilung Ältere Urgeschichte und Quartärökologie, T€ ubingen, Germany

Abstract This chapter examines large-scale patterns of behavioral change that are often viewed as indicators for the advent of cultural modernity and developed symbolic communication. Using examples from Africa and Eurasia, the chapter reviews patterns of lithic and organic technology, subsistence, and settlement as potential indicators of modern behavior. These areas of research produce a mosaic picture of advanced technology and behavioral patterns that come and go during the late Middle and Late Pleistocene. Based on these data the emergence of modern behavior, as seen in the archaeologically visible material record, appears to be gradual and heterogeneous in space and time. During the early part of the Late Pleistocene, personal ornaments in the form of perforated seashells are documented in southwestern Asia and northern and southern Africa. By about 40,000 years ago (Ka), a diverse array of personal ornaments are documented across the Old World in association with Neanderthals and anatomically modern humans. These include both modified natural objects and fully formed ornaments. The timing and distribution of the appearance of figurative art, mythical imagery, and other classes of artifacts including musical instruments point to a more punctuated development of fully modern behavior during the middle of the Late Pleistocene and certainly no later than 40 Ka. Due perhaps in part to the long and intense history of research, much, but by no means all, of the relevant data come from Europe. Early figurative art from the Aurignacian of southwestern Germany, northern Italy, Austria, and southern France provides undisputed evidence for fully developed symbolic communication and behavioral modernity. This chapter also discusses some of the hypotheses for the development and spread of cultural modernity and rejects a strict monogenetic model in favor of a pattern of mosaic polycentric development. This chapter highlights the need for new refutable, regional and superregional hypotheses for the advent and spread of behavioral modernity.

Introduction The question of when in the course of human evolution hominids became like ourselves has been at the center of several decades of productive debate in paleoanthropology. Reduced to the most fundamental level, the appearance of anatomical and behavioral modernity is a question of at what time in the course of evolution hominid anatomy and behavior fall within the variability documented in recent societies. The key component of fully modern cultural behavior is communication within a symbolically organized world and the ability to manipulate symbols in diverse social and economic contexts.

*Email: [email protected] Page 1 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_66-2 # Springer-Verlag Berlin Heidelberg 2013

This chapter will not address the development of modern human anatomy; here, I consider some of the key evidences for the evolution of complex behavioral systems. While there is no consensus about when modern behavior can first be identified in the archaeological record, by no later than about 40 Ka, various finds documenting the production of diverse ornaments, musical instruments, figurative representations, and mythical imagery provide undisputed evidence for cultural modernity. These and other archaeologically visible indicators of cultural modernity point to a patchy development of complex cultural behavior and symbolic communication across the Old World. While regional patterning is becoming increasingly visible (Delporte 1998; McBrearty and Brooks 2000; Bon 2002; Conard and Bolus 2003; Hovers and Belfer-Cohen 2006; Texier et al. 2010; d’Errico and Stringer 2011; Porraz et al. 2013), the current data on this topic include an uneven distribution of evidence that has been put through a selective taphonomic filter and that reflects diverse regional histories of research. These biases hinder the location of convincing centers of origin and dispersal for many of the key features considered here. At present, we see diverse points of view regarding the origins of behavioral modernity, and current interpretations that include but are not limited to the following models are (1) gradual African origin (McBrearty and Brooks 2000), (2) coastal origin in connection with new dietary patterns during the early Late Pleistocene (Parkington 2001), (3) punctuated late African origin (Klein 1999; Klein and Edgar 2002), (4) gradual origins across multiple human taxa and multiple continents (d’Errico et al. 2003), and (5) relatively late origins among multiple human taxa, including Neanderthals’ own Upper Palaeolithic revolution (Zilhão 2001, p. 54). Here, I argue for a mosaic polycentric advent of behavioral modernity (Conard 2008). The evolution toward behavioral modernity accelerated in the middle of the Late Pleistocene, and culturally modern behavior with diverse regional signals and local innovations can be seen in many parts of Africa, Europe, Asia, and Australia between 30 and 45 Ka. While archaic and modern humans must have interacted in many regions in the context of diverse social and ecological settings, ultimately modern humans were at a demographic advantage in all regions and replaced archaic humans with relatively little interbreeding (Pr€ ufer et al. 2013; Sankararaman et al. 2014). This chapter reviews some of the evidence for advanced cultural behavior and argues for a highly variable pattern of development depending on specific historical and evolutionary contingencies. The development of modern behavior does not in my view represent a one-time-only quantum leap, but a complex pattern of innovation, spread, and local extinction of new traits through cultural selection and social reproduction. Social, technological, and linguistic reproductions through learning are fostered by the biological success of the members of societies, but are not only driven by demographic growth. Demographic trends and complex patterns of intra- and intersocietal contacts led to mosaic patterns of cultural development that result from specific historical and ecological events and processes during the Pleistocene. The current archaeological record provides glimpses of these evolutionary processes, but it would be naive to think that our current data on the fleeting material remains of the development and spread of behavioral modernity provide a one-toone indication of where and when advanced technology, highly developed patterns of settlement and subsistence, ornaments, music, and abstract and figurative representation evolved. The question of why fully modern cultural behavior evolved is still more difficult to answer, but recent years have begun to see attempts to address the thorny questions of causality (Klein 1999; Parkington 2001; Shennan 2001; Lewis-Williams 2002; Conard and Bolus 2003; Jerardino and Marean 2010; Kuhn and Hovers 2013). Much more work is needed that addresses the potential causes of cultural evolution and develops testable hypotheses. In this context, monocentric and polycentric models need to be formulated and tested explicitly.

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Turning to the more mundane aspects of archaeology, it is necessary to stress the ambiguities and problems with dating sites in excess of 40,000 years. Radiocarbon dating, the strongest tool for dating LSA and Upper Paleolithic assemblages, begins to reach its limits in the period before 40 Ka. Here, several factors come into play. In this period, in excess of seven radiocarbon half-lives, contamination becomes a serious problem. The isolation of preserved collagen in bones and similar problems related to sample preparation become more problematic than in younger periods (Higham 2011). Also, the physics of the AMS and beta counting become more challenging as minimal contamination begins to affect the results more strongly and the uncertainties related to the chemistry and instrument background become significant. Equally important is the wealth of evidence that there are major fluctuations in radiocarbon levels, probably in connection with variations in production due to magnetic excursions (Voelker et al. 2000; Beck et al. 2001; Conard and Bolus 2003; Hughen et al. 2004). These factors tend to make radiocarbon ages underestimate the calendar age of archaeological materials in excess of 30,000 years (Higham 2011; Higham et al. 2012). Other methods, including luminescence dating, have great potential for sorting out the chronology of the emergence of modern human anatomy and behavior, and the prospects for gaining improved chronological control for the later stages of human evolution are excellent (Richter et al. 2000; Jacobs et al. 2003a, b, 2008; Tribolo et al. 2013). This presentation will of necessity be brief and in no way attempts to be encyclopedic. Instead, I consider examples to illustrate the overall pattern of behavioral evolution. These examples are often drawn from regions where I have worked and know the data best. The subject matter is divided into two main sections. The first deals with the nuts and bolts of Paleolithic archaeology and focuses on lithic and organic artifacts and patterns of subsistence and settlement. The second section deals more with data that provide more direct access to the Paleolithic world of symbols, beliefs, and communication and reviews evidence for burials, ornaments, figurative and nonfigurative representation, and music as a means of defining modern cultural patterns. In general, the results from a review of the latter kinds of evidence give a better indication of the origins of behavioral modernity. My concern here is not in developing trait lists or single signatures for modernity, but rather to look at the evolutionary contexts of diverse classes of data that may help us to identify patterns of behavioral evolution. Other similar reviews of this evidence at different geographic scales can be found in a number of publications and should be consulted along with the primary references for further details (Deacon and Deacon 1999; McBrearty and Brooks 2000; d’Errico 2003; d’Errico et al. 2003; Conard 2004a; Hovers and Belfer-Cohen 2006; Klein 2009; d’Errico and Stringer 2011). Finally, many of the chapters in this volume present up-to-date information that is of central importance for defining the evolution of modern behavior.

Technology, Settlement, and Subsistence as Measures of Modernity Lithic Technology Stone artifacts are a physically robust class of artifacts and often survive the numerous potential forms of taphonomic destruction. In this regard, they are a major source of data on early human behavior. In many Paleolithic settings, stone artifacts are the most abundant class of anthropogenically altered material. These attributes of lithic artifacts make them the most important means of defining Paleolithic cultural groups. Thus, if specific lithic artifacts can be shown to provide an indication of modern cultural behavior, scholars could use such finds as indicators of modernity. Despite attempts to define linear and cladistic systems for the evolution of stone tools (Foley 1987; Foley and Lahr 2003), lithic technology is based on learned behavior and is not directly Page 3 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_66-2 # Springer-Verlag Berlin Heidelberg 2013

transmitted biologically. Thus, it comes as little surprise that new forms of lithic technology come and go over the more than two-million-year-old Paleolithic record. Oldowan technology is the most common form of flint knapping at the pyramids of Giza (Conard 2000), and this simplest of knapping approaches comes and goes throughout the Stone Age. Many other knapping technologies also come and go over the last several hundred thousands of years that are the backdrop for the development of anatomical and cultural modernity. Hand axes, Levallois technology, blade technology, and other elements of stone knapping come and go and do not provide certain indicators of behavioral modernity. Additionally, the ethnographic record points to the problems associated with viewing lithic technology as a clear indicator of levels of cultural evolution. Subrecent ethnographic sources document cases of hunter-gatherers in regions including, for example, parts of Australia and Tierra del Fuego, who used Stone Age technologies that would leave no traces of behavioral modernity. These groups were undeniably modern humans and highly developed in respect to their linguistic skills and their ability to manipulate symbols, yet the lithic technology and the archaeologically visible material culture would leave no traces of this modernity. Lithic technology provides no simple solution to the problems related to identifying modernity. Even blades, which were once seen as clear indicators for behaviorally modern Upper Paleolithic and Later Stone Age cultures, have been demonstrated in diverse contexts in Africa, the Near East, and Europe (Rust 1950; McBurney 1967; Besançon et al. 1981; Singer and Wymer 1982; Conard 1990, 2012; Révillion 1994; McBrearty and Brooks 2000; Locht 2002; Meignen 2011; Wojtczak 2011; Fig. 1). These blade-based assemblages date to the second half of the Middle Pleistocene and the Late Pleistocene and include technologies based on Upper Paleolithic platform cores and non-Levallois and Levallois blade production. Lithic assemblages document a heterogeneous pattern of development, with forms coming and going across the Old World. While in Europe there is doubtless a difference between Middle and Upper Paleolithic assemblages, many forms typically associated with the Upper Paleolithic appear in earlier periods, and it is becoming increasingly clear that the variability documented by Bordes (1961) in the Middle Paleolithic of southwestern France reflects only a small portion of the overall lithic variability. Many regions of Europe (Bosinski 1967, 1982; Conard and Fischer 2000) show a diverse pattern of cultural development that is analogous to that documented in Africa (Clark 1982, 1988; McBrearty and Brooks 2000). Also in the Near East, the early Middle Paleolithic includes

Fig. 1 Kapthurin Formation, Kenya. Late Middle Pleistocene blades ca. 250,000 years old (After McBrearty and Brooks 2000)

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lithic assemblages such as Yabrudian and Humalian, and the later Middle Paleolithic is characterized by Levalloisian assemblages that were made by both Neanderthals and anatomically modern humans (Shea 2003). The latter observation demonstrates how tenuous the link is between anatomical and cultural evolution. As Bosinski (1982), Clark (1982, 1988), and others have long pointed out, the MSA and Middle Paleolithic are marked by the growth and increased visibility of local traditions. The frequently made suggestion that lithic technology from these periods is static or even boring strikes me as incorrect. In many areas where high-quality data are available, MSA and Middle Paleolithic assemblages show considerable diversity. The development of local traditions appears to increase with time in some areas of Africa and Eurasia (Bosinski 1967; Conard and Fischer 2000; Wadley 2001; Jöris 2002; Conard et al. 2012; Porraz et al. 2013), but these trends are, to a certain extent, a reflection of the improved quality of data that results from both better chronological control and more numerous assemblages per unit time. Researchers who try to define variability must consider the quality and density of the available data. In general, early periods of the MSA and Middle Paleolithic have provided less data suitable for addressing these questions than the later phases of these periods or the LSA or Upper Paleolithic. Thus, it is not surprising that, in general, assemblages from more recent periods document more technological and typological variation than samples from earlier periods. The complexity of Middle Paleolithic and MSA lithic technology is highly variable, but at times advanced. Hafting and composite tools have been documented directly and indirectly in many regions. In Africa, we can consider the standardized-backed forms from Howiesons Poort assemblages to be strong candidates for hafting, as well as numerous point assemblages of the Late Pleistocene and perhaps the Middle Pleistocene (Singer and Wymer 1982; McBrearty and Brooks 2000; Lombard and Phillipson 2010; Fig. 2). In southwestern Asia, Shea (1988, 1993, 1998) has long argued for hafting based on patterns of damage to artifacts and use wear. Mastic attached to Middle Paleolithic artifacts at Umm el Tlel in central Syria also demonstrates the use of hafting and provides evidence for composite tools (Boëda et al. 1998). In Europe, a similar pattern is present with small-backed artifacts that almost certainly required hafting being recovered at Tönchesberg (Conard 1992). European chipped stone points would have required hafting as on other continents, and mastic has been recovered, for example, at the Middle Paleolithic sites of Königsaue (Mania and Toepfer 1973), Neumark-Nord (Mania et al. 1990; Meller 2003), Bocksteinschmiede (Wetzel and Bosinski 1969), and Inden-Altdorf (Pawlik and Thissen 2011) in Germany and Campitello Quarry in Italy (Mazza et al. 2006). The production of mastics such as birch pitch requires advanced knowledge of pyrotechnology and material sciences and provides good evidence for advanced cultural behavior (Wadley et al. 2009; Roebroeks and Villa 2010; Pawlik and Thissen 2011). Through experimental and use-wear studies, Rots has also demonstrated the hafting in multiple contexts during the Middle Paleolithic and MSA (Rots 2010, 2013; Rots et al. 2011). Lithic assemblages of the MSA and Middle Paleolithic do not provide the evidence needed to define precisely when modern patterns of human behavior developed. They do, however, clearly show a heterogeneous pattern of technological development and transmission indicating that the beginnings of the LSA and Upper Paleolithic did not see fundamental revolutionary changes in technology across the Old World. This transition saw the further development of both new and older technologies. While more advanced forms of lithic technology came into broader use in the LSA and Upper Paleolithic, most of these technologies have well-documented precursors in earlier periods.

Organic Technology The development of organic technology shows a pattern analogous to that of lithic technology. While the LSA and Upper Paleolithic are defined on the basis of new artifact forms that occur in Page 5 of 39

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Fig. 2 Klasies River Mouth, South Africa. Highly standardized lithic artifacts from the Howiesons Poort assemblage ca. 75,000 years old (After Singer and Wymer 1982)

easily detectable numbers, organic artifacts have antecedents extending into the ESA and Lower Paleolithic. Thus, the beginnings of the LSA and Upper Paleolithic reflect legitimate archaeological divisions, but the changes represent a further elaboration and intensification of technologies that in some cases existed earlier. In regard to this question, the most important information comes from the finds from Schöningen in northern Germany, where Thieme’s excavations have yielded eight wooden spears with multiple designs and other wooden tools dating to the late Lower Paleolithic about 300 Ka BP (Thieme 1997, 1999, 2007; Fig. 3). These tools are of the highest workmanship and lend support to the importance of wooden tools from Clacton-on-Sea (Oakley et al. 1977) and Lehringen (Thieme and Veil 1985). Middle Pleistocene hominins manufactured the spears and other wooden artifacts from Schöningen with great care, and their context demonstrates a high degree of planning depth, social organization, and sophisticated communication. Unless we postulate that this part of Northern Europe enjoyed a privileged position in human cultural evolution, we must conclude that organic technology and

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Fig. 3 Tönchesberg 2B, Germany. Middle Paleolithic assemblage with blades, bladelets, backed points, and backed bladelets and imported lithic materials ca. 100,000 years old (After Conard 1992)

diverse well-made wooden tool assemblages were a part of the daily life of the Lower and presumably Middle Paleolithic inhabitants of Europe. These waterlogged sites provide a highly favorable setting for preservation that cannot be matched in other sedimentary settings, but occasional finds of preserved wood in Africa and the Near East leave room for optimism that future work may uncover comparable wooden artifacts. Much has been made of the development and elaboration of bone, ivory, and antler tools in recent years (Gaudzinski 1999; d’Errico 2003; d’Errico et al. 2003; Soressi et al. 2013). MSA assemblages Page 7 of 39

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Fig. 4 Schöningen, Germany. Lower Paleolithic wooden spear and horse bones ca. 300,000 years old (Photo N.J. Conard)

from sites including Apollo 11 (Vogelsang 1998), Klasies River (Singer and Wymer 1982), Sibudu (Backwell et al. 2008), and Blombos (Henshilwood et al. 2001) have produced a wealth of bone artifacts (Fig. 4). Many examples are sharpened bones and bone splinters. Other bone tools show a series of notches or more enigmatic forms. An exceptional case is the elaborately made harpoons from Katanda in D. R. Congo (Brooks et al. 1995); these finds would be remarkable if they were indeed of early Late Pleistocene age. Certainly, by the middle of the Late Pleistocene, bone tools were widespread in the MSA. The European Lower Paleolithic also documents early examples of bone tools including carefully manufactured hand axes (Segre and Ascenzi 1984; Gatti 1993). Similarly, bone tools are well documented at Middle Paleolithic sites, including Salzgitter-Lebenstedt (Gaudzinski 1999), Große Grotte (Wagner 1983), and Vogelherd (Riek 1934). Bone tools are by no means as common or complex as those of the Upper Paleolithic, but they no doubt existed in Middle Paleolithic assemblages. Bone tools were clearly used by late Neanderthals in many settings, and they have occasionally been documented in large numbers (d’Errico et al. 2003). While research continues to document more diverse and more specialized osseous tools associated with archaic hominins, such as those from Abri Peyrony and Pech de l’Azé I (Soressi et al. 2013), tools from the Middle Paleolithic are often less elaborate than the organic tools of the Upper Paleolithic. Split base points, for example, serve as diagnostic artifacts for the early Aurignacian over much of Europe and occur in significant numbers starting around 40 Ka (Albrecht et al. 1972; Hahn 1977).

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Finally, the Late Pleistocene sees further evidence for cultural innovations that should be mentioned here. These innovations include the widespread use of grinding technology during the MSA and Middle Paleolithic of northern Africa (Wendorf et al. 1993; Van Peer et al. 2004), evidence for fire-making technology in the Swabian Aurignacian (Riek 1934, p. 161; Weiner and Floss 2004), and water transport technology in the form of perforated ostrich eggshells (Vogelsang 1998; Parkington et al. 2005; Texier et al. 2010; but see Kandel 2004). As these and other less wellstudied categories of finds and behavioral innovations become topics of more systematic research, they will play a more prominent role in the discussions about the evolution of cultural modernity.

Subsistence Patterns of subsistence vary in time and space due to changing environmental conditions and changes in technology combined with changing social and settlement strategies. Although most sites do not contain preserved botanical remains, there is every reason to assume that plants played an important part in the diet of all hominids, just as they do for all ethnographically documented societies (Ono and Owen 2005). The diet of Neanderthals as reflected in stable isotope data indicates a relatively high component of animal resources (Bocherens et al. 1999, 2001, 2011), but these results do not preclude the use of plants in the diet, and even in the harshest arctic and desert environments, plants are seasonally available and nutritionally important. This is not the place to summarize the history of research on this question, but recent decades have seen a shift from assuming that archaic and early modern humans practiced fully developed systems of hunting and food sharing, to a critical assessment and rejection of earlier interpretations by many Anglophone colleagues. More recently, many case studies have provided convincing evidence that both later archaic and anatomically modern humans practiced systematic hunting of large, medium, and small game. These data by no means suggest that patterns of subsistence are homogenous over whole continents or subcontinents, but the advocates of subsistence forms based on scavenging or ineffective forms of hunting (Binford 1989; Stiner 1990, 1994) seem to have overstated the case against the existence of reliable hunting economies within MSA and Middle Paleolithic societies (Marean and Kim 1998; Marean and Assefa 1999). In recent years faunal studies have increasingly shown a diverse array of adaptations among late archaic and early modern humans (Clark and Speth 2013), with increasing evidence for intensification and the exploitation of a broader range of taxa as hominin population densities increase and highly ranked faunal resources become less available (Stiner 2005, 2013; Speth 2010, 2013). Again in this context, the finds from Schöningen are of central importance and have redefined the discourse on Lower Paleolithic subsistence. Thieme’s (1997, 1999, 2007) team recovered eight spears from Schöningen in direct association with the bones of several dozen horses in deposits dating to ca. 300 Ka (Voormolen 2008; van Kolfschoten 2014). These discoveries from the mid-1990s brought the more extreme assessment of Lower and Middle Paleolithic subsistence based on obligate scavenging to an end, and as far as I am aware, the implications of these remarkable finds for documenting hunting of large game by archaic hominids and the implications of the recovery of a yew wood spear with the skeleton of an Eemian age forest elephant at Lehringen have not been questioned in recent years. These finds do not demonstrate that hunting large game was a universal phenomenon in the late Middle and Late Pleistocene, but they do document the existence of well-planned and successfully executed hunting of large and fast game using refined and deadly technology.

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More mundane sources of information tend to support this view. Numerous faunal assemblages indicate that late archaic and early modern humans had frequent early access to game. In most settings, the possibility of scavenging cannot be completely excluded, but active hunting is the most parsimonious explanation for the faunal assemblages at sites including, for example, SalzgitterLebenstedt (Gaudzinski and Roebroeks 2000), Tönchesberg (Conard 1992), and Wallertheim (Schmidtgen and Wagner 1929; Gaudzinski 1995; Conard and Prindiville 2000). In other contexts, in many parts of Eurasia and Africa, similar evidence for the role of mammals in the diet of Middle Paleolithic and MSA people is available (Gaudzinski 1996; Marean and Kim 1998; Marean and Assefa 1999; Burke 2000; Bocherens et al. 1991, 2001; Costamagno et al. 2006; Rendu et al. 2011, 2012; Clark and Speth 2013). Finally, it must be stressed that scavenging fresh carcasses is an attractive economic option in contemporary hunting and gathering societies (O’Connell et al. 1988). Thus, there is no reason to stigmatize Paleolithic scavenging as a premodern adaptation. In southern Africa, Klein and Parkington have developed new approaches and hypotheses for the development of subsistence practices during the MSA. Parkington (2001) stresses the key role of the exploitation of coastal resources for brain development and the origin of cultural modernity in coastal settings. He has also suggested that similar processes may have driven human evolution in other coastal environments, including the circum-Mediterranean region. Jeraldino and Marean (2010) have also emphasized the role of coastal adaptations in the later phases of human evolution in southern Africa. Klein (2009) has looked at small game such as tortoises and marine resources as playing an important role in MSA and LSA subsistence. He argues that until ca. 50 Ka, hunting was limited to comparatively easily hunted game and that people only started systematically hunting dangerous animals, including suids and buffalo in the late MSA and LSA. Klein sees this shift in subsistence as an indication of the rise of cultural modernity in connection with genetic mutations and the appearance of fully developed language. Both Parkington’s and Klein’s hypotheses have been received with considerable skepticism, but both hypotheses present entirely welcome, refutable models for the rise of cultural modernity. Given the general lack of clearly formulated models that provide causal explanations for the rise of behavioral modernity, these hypotheses, even if they are later demonstrated to be incorrect, have fostered considerable new research. This is certainly the case of the critical assessment of the early evidence for hunting by Binford and colleagues in the 1980s and 1990s. Like the other data we have considered thus far, the evidence on subsistence during the Middle and Upper Pleistocene shows a pattern of advanced adaptations at an early date. With the possible exception of Parkington’s model for increased use of marine resources in the Late Pleistocene, the data on subsistence tend to argue against a revolutionary change in economic and social behavior that defines the appearance of cultural modernity. This being said, Stiner, Speth, and other scholars have documented how intensification led to the exploitation of lower ranked and more diverse resources as over the course of the Middle and Late Pleistocene (Stiner 1999, 2005; Speth 2010, 2013; Steele and Klein 2009; Steele and Alverez-Fernandez. 2011; Conard et al. 2013). In general, hominins tend to exploit highly ranked resources when they are available, and thus, under similar conditions both archaic and modern hominins often exploited large- and medium-sized bovids, cervids, and equids when they were available (M€ unzel and Conard 2004).

Settlement Reconstructing patterns of settlement and the organization of space is one of the more elusive ways of trying to define modern patterns of behavior. This relates to the general difficulty of reconstructing Page 10 of 39

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settlement dynamics in any period and particular problems associated with Paleolithic periods, where the amount and quality of data are generally poorer than in later periods. The analysis of Paleolithic settlement in the contexts of defining modern behavioral forms has two major approaches, one intrasite and the other regional. Binford (1998), Wadley (2001), and others have argued that spatial organization within a find horizon can be used to define cultural modernity. Binford, for example, sees repetitive modular units of hearths and bedding areas in rock shelters as a hallmark of modern spatial organization. In his view, this pattern of spatial organization is not present before the LSA or Upper Paleolithic. Wadley sees a marked increase in spatial organization during the late MSA of Rose Cottage Cave in the Free State of South Africa as a further indication that the final stages of the MSA may reflect the period in which cultural modernity developed. In Europe, Kolen (1999) has pointed to the lack of clear evidence for architecture as an indication that neither Lower nor Middle Paleolithic groups regularly built shelters as centers of social and economic interaction, as are known in many later archaeological periods. Instead, archaic humans used what Kolen refers to as “nests” to provide shelter. If correct, this would indicate that settlement dynamics of archaic humans, including Neanderthals, fell outside the range of culturally modern people. Several researchers have questioned this model and suggest that even if clear architectural features other than hearths are generally lacking before the Upper Paleolithic, late Middle Paleolithic sites document spatially structured activity areas similar to those one would expect in sites of modern hunters and gatherers (Vaquero et al. 2001, 2004; Conard 2001b; Chacón Navarro et al. 2012). As with many of the criteria considered here, it is unclear to what extent taphonomic factors and the quality of data affect our interpretations. Kolen, however, is certainly correct to note that clear evidence for anthropogenic shelters and dwellings is extremely rare prior to the Upper Paleolithic. Although less effort has been invested in studying the spatial structure of MSA sites, recent work at Sibudu has demonstrated the use of bedding and regular site maintenance in multiple find horizons (Goldberg et al. 2009; Wadley et al. 2011). This kind of research promises to provide insights into the organization of space by early modern humans in southern Africa. At a larger scale of analysis, we see more tantalizing, yet largely inconclusive, evidence for the use of space and distant resources as indicators of behavioral modernity. Important works by Geneste (1988), Roebroeks et al. (1988), Floss (1994), and others examine the use of distant raw materials as a source of information on Paleolithic economic and spatial organization. Especially in the context of the continental European approaches to the study of patterns of lithic reduction and technology (Geneste 1988; Hahn 1988; Boëda et al. 1990), much research has been aimed at linking patterns of lithic technology to systems of mobility and settlement. These and other studies show the nearly universal pattern that more distant raw materials are present at sites in more reduced form than local raw materials. This applies for all Paleolithic periods. In later periods more raw materials from distant sources are transported to sites, but there is no specific moment that reflects a quantum shift from non-modern to modern patterns of behavior. Also, the “provisioning of place” (Kuhn 1995) – that is, the movement of quantities of raw material to sites for future use – is documented on sites of both modern and archaic hominids (Conard and Adler 1997). Examination of the abundance of distant raw materials as a reflection of the size of territories and long-distance economic and social relationships has also provided ambiguous results. Middle Paleolithic assemblages document the use of raw materials from 100 or more km away (Floss 1994; Féblot-Augustins 1997). Nonetheless, such long-distance transport of tools and raw materials is still more common in the Upper Paleolithic, and the difference is more one of degree than of kind. So far these kinds of data have not led researchers to devise a reliable means of distinguishing between archaic and modern behavioral forms. These lithic data also suggest mosaic, contextPage 11 of 39

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dependent systems of adaptations with considerable variability, rather than a black-and-white world of unilinear evolution, in which quantum leaps between archaic and modern behavior can be readily identified. Finally, an analysis of site types and links between sites within settlement systems shows considerable diversity in MSA and Middle Paleolithic systems of settlement, but no easily recognizable criterion for defining behavior modernity (Conard 2001c, 2004b). Here, as in other areas, I doubt whether the search for a holy grail of cultural modernity is a productive way of defining a research program. Scholars continue to struggle to identify the origins of a settlement system that reflects a symbolically mediated landscape inhabited by culturally modern people. Furthermore, if our definition of behavioral modernity includes all ethnographically documented patterns of settlement, we must concede that a nearly endless diversity of adaptations among subrecent hunters and gatherers are by definition modern and by no means easy to distinguish from hypothetical non-modern settlement dynamics as indicated by the distribution of archaeologically visible material cultural remains.

Beyond Technology, Subsistence, and Settlement As the discussion above suggests, identifying clear criteria for behavioral modernity is probably more likely in the realms of ideology and symbolic communication than in the nuts and bolts archaeology of chipped stone and faunal remains. Here, I consider several lines of argument and sets of data that lie outside the pragmatic economic concerns of day-to-day subsistence.

Burials Most of the more complete human skeletons from before the Middle Paleolithic and Middle Stone Age appear to be the result of extraordinarily favorable taphonomic contexts. Despite arguments to the contrary by Gargett (1989, 1999) and other colleagues, there are a wealth of Middle Paleolithic human skeletons that seem to have been buried deliberately (Solecki 1971; Trinkaus 1983; Defleur 1993). Such burials could be motivated by purely practical factors like the need to dispose of undesirable cadavers, but I think it is more likely that the numerous burials of Neanderthals and anatomically modern humans of the Middle Paleolithic reflect the deliberate burial of kin and are linked to personal and emotional ties between the living and the dead. Defleur (1993) has summarized much of the evidence for Middle Paleolithic burials and points to a number of convincing cases in Europe and the Levant. Debate on the presence of Middle Paleolithic burials continues with Rendu and colleagues (2013) favoring the existence of burials and Goldberg and colleagues (2013) insisting on very high standards of data to document the presence of burials in the Paleolithic record. The question of the deliberate inclusion of grave goods and the identification of specific ritual practices is perhaps still more contentious and difficult to demonstrate beyond doubt. In the Upper Paleolithic the data are unambiguous, and many burials preserve opulent grave goods that reflect the status of the individuals and the needs of the dead in the afterlife. Examples of burials from Sungir’, Dolní Vĕstonice, the Grimaldi Caves, and other sites suggest that the system of beliefs in association with death and the afterlife were much more elaborate in Upper Paleolithic than Middle Paleolithic societies. These Upper Paleolithic burials are universally accepted as indicators of cultural modernity. As far as I am aware, aside from somewhat enigmatic cases like the highly fragmented and partially burnt assemblage from Klasies River Mouth in South Africa, the MSA and early LSA have not produced sufficient data for burials to allow conclusions to be drawn about practices and beliefs in sub-Saharan Africa. Human skeletal material, for example, in the Upper Page 12 of 39

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Cave of Zhoukoudian in China is suggestive of early Upper Paleolithic burials in the Far East (Pei 1939; Wang 2005), and the burials at Lake Mungo in Australia point to the cultural sophistication of the earliest inhabitants of that continent over 40 Ka BP (Thorne et al. 1999).

Pigments In recent years, there have been a number of reports of early occurrences of pigments and discussions of the importance and meaning of the use of pigments (Barham 1998; McBrearty and Brooks 2000; d’Errico and Soressi 2002; Hovers et al. 2003; Dayet et al. 2013). On the basis of this work, it has become clear that pigments were used in some MSA contexts during the later Middle Pleistocene and in numerous MSA and Middle Paleolithic settings of the Late Pleistocene (Watts 1998). Southern Africa has yielded particularly abundant evidence for the use of pigments during the MSA. Barham’s (1998) work at Twin Rivers in Zambia is a noteworthy example of the presence of many pieces of pigments in Middle Pleistocene contexts, and numerous MSA sites dating to the Late Pleistocene including Klasies River (Singer and Wymer 1982), Diepkloof (Dayet et al. 2013), Peers Cave, Hollow Rock Shelter (Watts 2002), Hoejiespunt (Will et al. 2013), Klipdrift (Henshilwood et al. 2014), Apollo 11 (Vogelsang 1998), and Blombos (Henshilwood et al. 2001) have produced much evidence for grinding of pigments. Recent work at Blombos has documented tool kits for making and storing pigments (d’Errico and Stringer 2011). Parkington has argued that the use of pigments provides additional indications of the advent of behavioral modernity in the MSA, particularly in more coastal settings, where Howiesons Poort and Still Bay assemblages are concentrated. Watts (1998, 2002) has reviewed the evidence for the use of pigments in the MSA and concludes that they are extremely common at many MSA sites and reflect a widespread ability to structure the world into a symbolically organized whole. Watts rejects the hypothesis that pigments were primarily used for strictly utilitarian purposes, including tanning hides, while Wadley (2005; Wadley et al. 2009) emphasizes the practical uses of ground ochre. Through a program of experimental and archaeological observations, Wadley has shown that worked ochre from Sibudu, and likely elsewhere, often served as a component of mastic. In the Levant and Europe, Hovers et al. (2003) see strong evidence for the use of ochre at Middle Paleolithic sites including Qafzeh (Vandermeersch 1969). Sites including Maastricht-Belvédère (Roebroeks et al. 2012), Pech de l’Azé (Bordes 1972; d’Errico and Soressi 2002), Cueva de los Aviones, and Cueva Antón (Zilhão et al. 2010) document the use of red, yellow, and black pigments in Middle Paleolithic contexts and suggest that Neanderthals regularly used pigments. Zilhão and d’Errico emphasize that the use of symbols and complex technology evolved independently among Neanderthals and was not the product of acculturation after contact with fully modern humans as has been argued by White (2000), Hublin (2012), and Mellars (2005). The potential uses of ground ochre include body painting, rock painting, drawing, ritual, medicinal, as well as more mundane purposes. Although we rarely have reliable information on the specific use of these early occurrences of ochre, they are presumably, at least in some settings, such as in Middle Paleolithic burials, connected with religious beliefs that speak for a high level of cultural development and a significant degree of symbolic communication (Hovers et al. 2003). As with other potential indicators of advanced cultural attributes discussed above, the use of ochre does not appear to reflect a quantum leap signifying the shift from archaic to modern patterns of behavior. Both anatomically modern and archaic humans used pigments and presumably attached symbolic meaning to red, black, and perhaps other ground mineral pigments. Here, however, Wadley’s caveats against assuming that ground ochre served as primarily as pigment should be reiterated. Given the likely use of mineral pigments in the MSA and Middle Paleolithic, the use of organic pigments is likely, even if difficult to demonstrate with direct archaeological observations. Page 13 of 39

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Decorated Objects and Nonfigurative Representation There is a long history of claims for deliberate nonutilitarian modification of objects in Paleolithic contexts. These include finds from the Lower Paleolithic, such as incised bones from Bilzingsleben (Mania 1990; Steguweit 2003), and many finds from later periods. These objects are often controversial and are usually not accepted as demonstrating complex symbolic communication. Following other lines of argument, colleagues have suggested that the perfect symmetry of some hand axes indicates an advanced aesthetic development, but Wynn (1995) and Haidle (2004) argue that hand axes do not necessarily reflect symbolically based communication or language. Over the course of the Middle Paleolithic and MSA, larger numbers of enigmatic objects have been published, including the cross-incised stone and modified fragment of a mammoth tooth from Tata, Hungary (Vértes 1964), and the so-called mask from La Roche-Cotard (Lorblanchet 1999). Some researchers have included evidence for collected fossils or curated natural products as indicators of advanced aesthetic and behavioral patterns (Schäfer 1996). Particularly in recent years, the MSA has produced a number of incised objects that have been taken as evidence for symbolic communication and a high degree of cultural development. Important examples of these finds include engraved linear and crosshatched patterns on pieces of ochre from Still Bay deposits at Blombos dating to ca. 75 Ka (Henshilwood et al. 2002) and incised pieces of ochre from, for example, Peers Cave, Klein Kliphuis (Mackay and Welz. 2008), and Klasies River Cave 1 (d’Errico 2012). Current excavations at Diepkloof have produced hundreds of fragments of decorated ostrich eggshells from Howiesons Poort contexts including pieces that are interpreted as originating from decorated ostrich eggshell flasks (Parkington et al. 2005; Texier et al. 2010). Similar finds have also been recovered from MSA contexts at sites including Klipdrift (Henshilwood et al. 2014) and Apollo 11 (Vogelsang 1998). These finds are unquestionably the result of deliberate manufacture and probably reflect the desire of the craftsperson to convey symbolic content and aesthetically meaningful information to members of his or her social group. There can be little doubt that such carefully produced decorated objects and the nonfigurative representations they carry communicated specific information from the maker to people who used or saw these objects. Deciphering the specific meaning broadcast through these finds is not easy, and few specific explanations for their meaning have been presented. With increasing amounts of carefully executed fieldwork during the MSA, there is reason for optimism that contextual information will help archaeologists to develop hypotheses to explain the meaning of these finds. The concentration of these finds in southern Africa may be simply a reflection of the intensity of highquality research in this region, or perhaps an indication that this form of storing and using symbolic information was more common in this part of the world than in other geographic areas. Some colleagues accept these finds as definitive evidence of cultural modernity with fully developed symbolic communication, modern cognitive abilities including language (Henshilwood et al. 2002; d’Errico et al. 2003; Texier et al. 2010). The wealth of finds of engraved objects in the southern African MSA demonstrate that symbolic artifacts of this kind are not as exceptional as initially thought and that marked objects.

Ornament The manufacture and use of ornaments convey social information about individual identity and group affiliation. This means of projecting assertive individual style or emblematic style reflecting social affiliation within a larger demographic group (Wiessner 1983) is an important characteristic of modern behavioral patterns and has been the focus of much recent research (Vanhaeren 2002; Kölbl and Conard 2003; Vanhaeren and d’Errico 2006). The archaeological distribution of ornaments provides a clearer signal than many of the classes of information considered above. Page 14 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_66-2 # Springer-Verlag Berlin Heidelberg 2013

Fig. 5 Klasies River Mouth, South Africa. Bone artifacts from Middle Stone Age deposits ca. 75,000 years old (After Singer and Wymer 1982)

Early evidence for the use of marine shells as ornaments comes from burial contexts from Qafzeh Cave in Israel and dates to about 100 Ka (Bar-Yosef and Vandermeersch 1993). Perforated marine shells of similar age are also documented at Skhul Cave in Israel (Vanhaeran et al. 2006) and Grotte des Pigeons in Morocco (Bouzouggara et al. 2007). Slightly younger examples of perforated marine shell ornaments come from Still Bay deposits at Blombos Cave dating to about 75 Ka (Henshilwood et al. 2004) and MSA contexts at Sibudu (d’Errico et al. 2008). Starting roughly 40 Ka, personal ornaments have been documented in many parts of the Old World from multiple regions of Africa, Eurasia, and Australia. Early ornaments include ostrich eggshell beads from early LSA contexts in Enkapune Ya Muto rock shelter, Kenya, with associated radiocarbon measurements between 30 and 40 Ka (Ambrose 1998). AMS radiocarbon dates directly on ostrich eggshell beads from deposits representing the transition from the MSA to LSA at Mumba Cave in Tanzania (Fig. 5; Weiß 2000; Conard 2004a) have yielded multiple dates between 29 and 33 Ka uncalibrated radiocarbon years, or starting roughly 36 Ka cal BP, and lend support to the early dates from Enkapune Ya Muto. There is every reason to assume that these East African ornaments were made by anatomically and presumably culturally modern people. € Excavations at Ksar Akil in Lebanon (Azoury 1986) and at Uçagizli in the Hatay Province of Turkey (Kuhn et al. 1999, 2001) have produced rich assemblages of perforated marine shells from Initial Upper Paleolithic contexts dating to about 40 Ka (Fig. 6). Similar finds have been recovered from other Mediterranean early Upper Paleolithic contexts, including Riparo Mochi on the Ligurian Coast of Italy (Kuhn and Stiner 1998; Stiner 1999). Douka (2013) has recently developed new methods for dating marine shells and has repeatedly demonstrated the finds date to roughly 40 Ka

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_66-2 # Springer-Verlag Berlin Heidelberg 2013

Fig. 6 Mumba Cave, Tanzania. Ostrich eggshell beads radiocarbon dated between 29,000 and 33,000 radiocarbon years ago scale in millimeters (Photo H. Jensen)

BP. With the exceptions of late Middle Paleolithic sites of Cueva de los Aviones and Cueva Antón in Spain (Zilhão et al. 2010), the perforated shells have normally been interpreted as having been produced and used by anatomically modern humans. In Europe there is considerable evidence for a rapid spread in the use of ornaments with the beginning of the Upper Paleolithic. In addition to the Spanish examples, Neanderthals apparently created a wide range of perforated and incised ornaments in Ch^atelperronian contexts such as at Grotte du Renne at Arcy-sur-Cure (Leroi-Gourhan and Leroi-Gourhan 1964; d’Errico et al. 1998; Baffier 1999). These finds remain at the center of considerable debate about whether or not Neanderthals may have developed advanced symbolic communication. At more or less the same time, numerous examples of early Aurignacian ornaments have been recovered from several regions including the Swabian sites such as Vogelherd, Geißenklösterle, and Hohle Fels (Conard 2003a; Higham et al. 2012; Fig. 7). In addition to incised and perforated natural forms such as teeth, these artifacts include diverse ornaments made of mammoth ivory. It is noteworthy that many of the oldest forms of ornaments in Europe are not only perforated natural objects but also completely carved, three-dimensional ivory beads, pendants, and figurines in which the maker completely dictated the form of the artifact (Conard 2008, 2010). Although earlier examples of personal ornament are known, by around 40 Ka ornaments are well documented across much of the Old World. These data are consistent with the hypothesis that modern cultural behavior spread rapidly between roughly 30 and 50 Ka. Personal ornaments from the Upper Cave of Zhoukoudian, Shuidonggou Locality 2 (Gao et al. 2002), and Xiaogushan Cave (Archaeological Institute of Liaoning Province 2009) document the presence of this class of artifacts in association with flake-based lithic assemblages in northeastern China by 30 Ka (Pei 1939; Conard 2013). Shell beads from Mandu Mandu Creek Rock Shelter in Western Australia dating to more than 30 Ka (Morse 1993) suggest that the use of personal ornaments was indeed widespread at an early date. Although Australia lies outside the scope of this review, the colonization of Sahul was an event in prehistory that required crossing the vast open water of Wallacea with rafts or other forms of boats. Page 16 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_66-2 # Springer-Verlag Berlin Heidelberg 2013

€ Fig. 7 Uçagizli Cave, Turkey. Perforated marine shell ornaments dating to ca. 40,000 radiocarbon years ago (After Kuhn et al. 2001)

The best available dates for the colonization lie in the range of ca. 42–45 Ka and fit with the pattern suggesting the rapid spread of advanced behavioral patterns at about this time (O’Connell and Allen 1998, 2004).

Figurative Representations

The presence of figurative art is universally accepted as an indication of behavioral modernity. As far as I am aware, no one has disputed that figurative representations are a hallmark of modern cultural behavior. Mann (2003) has gone so far as to argue that representational art is the “gold standard” by which behavior modernity can be identified and measured. This being said, figurative representations can be viewed as documenting fully developed symbolic communication, but the lack of such artifacts in the archaeological record tells us little since many recent archaeological cultures lack figurative art. Clearly many forms of symbolic communication, including speech, stories, and song, are archaeologically nearly invisible. In Africa, the earliest figurative art is from the late MSA of Apollo 11 (Fig. 8), dating between 25,500 and 27,500 radiocarbon years ago (Vogelsang 1998). These examples of painted mobile art depict a number of animals, geometric forms, and a therianthrope. The Middle Pleistocene-aged, anthropomorphic-shaped stone from Tan-Tan, Morocco (Bednarik 2003), much like a similar object from Berekhat Ram, Israel (Goren-Inbar 1986; Goren-Inbar and Peltz 1995; d’Errico and Nowell 2000), appears to be a modified natural form rather than deliberately carved figurine. In the Levant there is little or no evidence of figurative art before 30 Ka. The situation in Europe is very different, in that several sites have provided evidence of figurative representation between 30 and 40 Ka. The earliest figurative art includes the mammoth ivory figurines from four caves in Swabia in southwestern Germany (Hahn 1986; Schmid 1989; Conard and Bolus 2003; Conard 2003b; Conard 2009; Conard et al. 2009) and several red monochrome paintings from Fumane in northern Italy (Broglio 2002; Broglio and Dalmeri 2005). The Swabian caves of Vogelherd, Hohlenstein-Stadel, Geißenklösterle, and Hohle Fels (Fig. 9a, b) have produced Page 17 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_66-2 # Springer-Verlag Berlin Heidelberg 2013

Fig. 8 Apollo 11 Cave, Namibia. Figurative painting from Middle Stone Age deposits dated with radiocarbon to ca. 27,000 years old (After Vogelsang 1998)

about 50 mostly fragmentary, very small, ivory figurines and figurative representations in bone and stone dating well in excess of 30,000 radiocarbon years, which corresponds to closer to 40 Ka in calendar years. Due to the noisy radiocarbon signal in this period and above-average 14C production, the radiocarbon ages at the Swabian caves and the similarly aged deposits from Fumane significantly underestimate the age of these artworks (Conard and Bolus 2003). The most recent calibrated radiocarbon dates place the beginning of the Swabian Aurignacian at about 42.5 Ka and at the very beginning of this cultural tradition (Higham et al. 2012). The Swabian ivory figurines include depictions of lions, mammoths (see Fig. 10), horses, bisons, bears, a water bird, a fish, numerous unidentified fragments, and three therianthropes that combine features of lions and humans (Hahn 1986; Conard 2003b; Wehrberger 2013; see Fig. 11). The depictions of mythical imagery, in the form of therianthropic representations, appear simultaneously with other more naturalistic depictions of animals and humans and provide unique insight into the system of beliefs of Paleolithic peoples (Conard 2010). These artworks from the Swabian caves are usually small and beautifully carved. The oldest of the figurines is likely a remarkable female figurine, the “Venus of Hohle Fels” (Fig. 12) that excavators found in the basal Aurignacian deposit of Hohle Fels Cave in the Ach Valley (Conard 2009). This find, and abundant ivory working debris from the basal Aurignacian at Hohle Fels and the lower Aurignacian at Geißenklösterle, demonstrates that this rich tradition of ivory carving in the region dates back to the start of the Aurignacian, the period in which modern humans initially migrated up the Danube corridor. The early figurative depictions from Swabia suggest that figurative representations evolved very quickly and reached a high level of refinement almost immediately. These finds stand in sharp stylistic contrast to the highly schematic paintings of animals, unknown forms, and a possible therianthrope from Fumane (Broglio 2002). Geißenklösterle has also produced a painted rock from this period that preserves traces of red, yellow, and black pigments (Hahn 1986). Most of the spectacular paintings from Grotte Chauvet in the Ardèche region of southern France (Fig. 13) appear to slightly postdate the examples of figurative art from Swabia and Fumane (Clottes 2001). Here, numerous depictions of animals date back as far as 32,000 radiocarbon years ago, which corresponds to roughly 36 Ka cal. The selection of animals depicted in Chauvet, with an emphasis on dangerous, strong, and large animals, shows remarkable similarities to the Aurignacian figurines from Swabia and no stylistic similarities to the simple depictions from Fumane. Page 18 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_66-2 # Springer-Verlag Berlin Heidelberg 2013

Fig. 9 (a) Sirgenstein, Bockstein Cave, Hohlenstein-Stadel, Vogelherd, Bockstein-Törle, Germany. Personal ornaments from the Aurignacian dating to ca. 36,000–30,000 radiocarbon years ago (After Conard 2003a) (b) Ivory ornaments from the Swabian Aurignacian, ca. 34 Ka radiocarbon years BP. 1–5 and 11–16 Hohle Fels; 6–10 and 17–20 Vogelherd (Photo: W. Binczik; Eberhard Karls Universität T€ubingen)

Therianthropic representations are present at these sites and, as in Swabia and at Apollo 11, suggest that depictions of mythical images have been part of the cultural repertoire of many groups of people from the beginning of artistic representation. Other important sites in this context include Stratzing

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_66-2 # Springer-Verlag Berlin Heidelberg 2013

Fig. 10 Mammoth from Vogelherd, ca. 34 Ka radiocarbon years BP (Photo: H. Jensen; Eberhard Karls Universität T€ ubingen)

Fig. 11 1 Geißenklösterle, 2 Hohle Fels, 3 Hohlenstein-Stadel, Germany. Three lionmen carved from mammoth ivory, ca. 34,000 radiocarbon years BP (Photo: 1 P. Frankenstein, H. Zwietasch; Landesmuseum W€urttemberg, Stuttgart. 2 H. Jensen; Eberhard Karls Universität T€ ubingen. 3 Y. M€uhleis; Landesamt f€ur Denkmalpflege im RP Stuttgart)

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_66-2 # Springer-Verlag Berlin Heidelberg 2013

Fig. 12 Hohle Fels, Germany. Female figurine carved from mammoth ivory, age ca. 36 Ka radiocarbon years BP (Photo: H. Jensen; Eberhard Karls Universität T€ubingen)

Fig. 13 Grotte Chauvet, France. Early Upper Paleolithic parietal art radiocarbon dated to ca. 30,000 years ago (After Clottes 2001)

in Lower Austria, where a human figurine of stone has been dated to between 30 and 32 Ka (Neugebauer-Maresch 1989). Abri Cellier, La Ferrassie, Abri Blanchard, and Abri Castanet in southwestern France have produced an impressive group of engraved representations in stone of animals and vulvas dating between ca. 30 and 34 Ka radiocarbon years ago (Leroi-Gourhan 1995; White et al. 2012). Recently paintings in Pes‚ tera Coliboaia, Romania, have been discovered dating to ca. 32 Ka that show stylistic similarities to the paintings in Grotte Chauvet and suggest that Chauvet may not stand entirely alone with respect to early parietal art (Besesek et al. 2010; Clottes et al. 2011). These figurative depictions from European contexts are the oldest known worldwide. They all date to the early Upper Paleolithic and were presumably made by modern humans; however, as far as we can tell, Neanderthals still occupied parts of Europe at this time, roughly 40 Ka. At present, there

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_66-2 # Springer-Verlag Berlin Heidelberg 2013

is no concrete evidence for a direct association between modern humans and early figurative art in Swabia. Thus, for now, the hypothesis that Neanderthals created the figurative art and other remarkable finds of the early Aurignacian, although improbable, cannot be refuted (Conard et al. 2004a). The specific context in which figurative art developed has been the subject of considerable discussion of late and will not be elaborated on here (Lewis-Williams 2002; Conard and Bolus 2003). Regardless of the specific social-cultural mechanisms that led to the development and spread of figurative art, there is a consensus among archaeologists and paleoanthropologists that the makers of these early artistic traditions were culturally modern people (Churchill and Smith 2001). While many other advanced behavioral forms have precursors in earlier periods, there is no convincing evidence for figurative depictions prior to the beginnings of the European Upper Paleolithic.

Music Perhaps because of the long research tradition and favorable taphonomic conditions, the earliest examples of musical instruments have been recovered from early Aurignacian contexts in Swabia (Hahn and M€ unzel 1995; d’Errico et al. 2003; Conard et al. 2004b, 2009). As with figurative representations, evidence for music and musical instruments can be seen as an indication of fully developed cultural forms based on symbolic communication. The assumption in this context is that where there is figurative art and music, there must have been fully developed language, by which Paleolithic people assigned specific concrete and abstract meaning to words and could efficiently communicate information about the past, present, and future. Thus, where there is figurative art and music, there must have been behaviorally modern people. While speech, song, music, and dance presumably existed still earlier, the oldest musical instruments known are two bone flutes from swan radii and one mammoth ivory flute from the Aurignacian archaeological horizon II at Geißenklösterle (Hahn and M€ unzel 1995; Conard et al. 2004b), fragments of a bone and ivory flute from Vogelherd (Conard and Malina 2006), and fragments of two ivory flutes and one nearly complete flute carved from the radius of a griffon vulture from the basal Aurignacian of Hohle Fels (Conard et al. 2009; Fig. 14). These deposits have been dated by thermoluminescence and radiocarbon to about 40–37 Ka. Reconstructions of the swan bone flutes produce a high-pitched but pleasing music. Friedrich Seeberger (2002, 2004) has recently recorded a CD of Ice Age music played on a reconstructed bone flute of the kind known from Geißenklösterle. This flute can be played without a reed and is clearly a flute rather than a reed- or trumpet-voiced instrument as suggested by d’Errico and colleagues (2003). Similarly the ivory flutes and the griffon vulture flutes can be played in similar manners and produce attractive tones and musical possibilities but have a lower register of tones due to their larger diameters. While Aurignacian musicians may have played very different-sounding music, Seeberger’s playing provides a striking impression of what this early Upper Paleolithic music may have sounded like. Interestingly, all of the flutes and fragments of flutes recovered thus far are from horizons containing a wide range of rich settlement debris from day-to-day life, suggesting that bone and ivory flutes and the music played on them formed part of the daily lives of the Aurignacian inhabitants of the Swabian Jura. Other sites, most notably Isturitz in the French Pyrenees, have produced additional flutes and indicate that wind instruments were in fairly wide use during the early Upper Paleolithic (Buisson 1990; d’Errico et al. 2003). Of course, there are countless other less conspicuous forms of percussion and wind instruments that could have existed during the early Upper Paleolithic or still earlier, yet they remain to be identified. Claims for earlier examples of Middle Paleolithic flutes have generally been met with skepticism in archaeological circles, as was the case with recent claims for a Middle

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Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_66-2 # Springer-Verlag Berlin Heidelberg 2013

Fig. 14 1 Geißenklösterle Flute 1 from a swan radius, 2 Geißenklösterle Flute 3 from mammoth ivory, and 3 Hohle Fels Flute 1 from a radius of a griffon vulture (Drawing: 1 A. Frey. 2–3 R. Ehmann. Eberhard Karls Universität T€ ubingen)

Paleolithic flute made from a cave bear bone from Divje Babe in Slovenia (Turk 1997; Albrecht et al. 1998).

Conclusions This overview has touched on some, but by no means all, of the evidence for the development of behavioral modernity. I have mentioned some of the main data sets and lines of reasoning that play a role in the discussions and debates about the origins of modern behavior. This leads to the question of by what means, where, and under what circumstances behavioral modernity arose and which of the hypotheses for its origins lies closest to the mark? The answers to these questions depend on how the evidence is weighed and interpreted. From my point of view, there can be no doubt that European Aurignacian societies by roughly 40 Ka had all of the hallmarks of modern behavior including Mann’s “gold standard” of figurative art as well as musical instruments. The best evidence for early figurative art and music comes from the caves of the Swabian Jura. While one could argue that some important Upper Paleolithic artifact forms developed in the Upper Danube drainage in the period around the time of the arrival of modern humans, naming this region as the single global center for the origin of cultural modernity would be a radical and naive interpretation. The broadly contemporary finds of figurative art from Fumane, and slightly later finds from southern France and the Wachau of Austria, indicate that the beginnings of the Upper Page 23 of 39

Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_66-2 # Springer-Verlag Berlin Heidelberg 2013

Paleolithic reflect a time in which earlier behavioral forms were replaced by behavioral forms that lie within the range of modern variability. This transition appears to have begun across much of Europe about 45 Ka when modern humans entered a continent inhabited by Neanderthals. Based on the presence of late Neanderthals in several regions of Europe (Hublin et al. 1995; Smith et al. 1999), it appears that there must have been a period in which both archaic and modern humans coexisted in Europe, and contact between the two forms of people must have occurred (Conard 2006). Given the poor chronostratigraphic resolution and scarcity of human fossil material during this key period between roughly 30 and 45 Ka, it is difficult to specify exactly how long both hominids coexisted in specific regions, but progress is being made on clarifying the regional sequences (Higham et al. 2011, 2012). Early anatomically modern humans at Skhul and Qafzeh in the Levant predate many remains of Neanderthals in southwestern Asia and point to an initially successful colonization of the region. The reappearance of Neanderthals in the Levant by roughly 60 Ka suggests that Neanderthals had more successful adaptations and demographic advantages over anatomically modern humans in interactions dating to the middle part of the Late Pleistocene. While evidence for strict contemporaneity is still lacking, this observation indicates that in some settings in which both hominins produced Middle Paleolithic artifact assemblages, Neanderthals had the upper hand (Conard 2008). However, in later encounters the situation was different. At about 45 Ka, modern humans arrived in western Eurasia with more developed cognitive skills (Lewis-Williams 2002) or behavioral advantages (Marean 2005) that led to demographic success relative to the indigenous Neanderthals. In western Eurasia, a period of dynamic equilibrium between Neanderthals and anatomically modern populations existed, in which moderns presumably profited from the knowledge and cultural practices of the “archaics” and vice versa. There is little reason to postulate a violent rapid advance of Neanderthals into the Levant replacing indigenous anatomically modern humans in the middle of the Late Pleistocene, and similarly there is little reason to assume that the arrival and spread of modern humans into Europe was either universally rapid or brutal. On the contrary, the transition from the Middle to the Upper Paleolithic and the infiltration and eventual complete dominance of Homo sapiens sapiens in Eurasia probably took on countless local ecologically and historically dictated variants in which there was give and take between archaic and modern humans. This pattern is reflected in the diverse regional signatures of the archaeological records from nearly every region that has produced relevant data for this transition. These data show very different archaeological signatures depending on the environmental and social-cultural setting encountered by incoming populations (Conard 1998; Conard and Bolus 2003). Evidence from the sites occupied by late Neanderthals indicates that they too manufactured and used ornaments (Baffier 1999), and as we have seen above, there is little that separated the patterns of technology, subsistence, and settlement reflected in Middle Paleolithic artifact assemblages from those of the MSA or early Upper Paleolithic. Still, some time presumably in the early and middle parts of the Late Pleistocene and certainly no later than 40 Ka, people began producing material cultural remains that allow us to identify behavioral modernity. This pattern of behavior was carried primarily, but perhaps not exclusively, by anatomically modern humans (Zilhão et al. 2010; d’Errico 2003). Many characteristics of modern behavior can be found across much of the Old World, and the distribution of advanced cultural traits is significantly determined by the intensity of research in different regions. The recent trend of important discoveries being made in MSA contexts in southern Africa will no doubt continue as more work is done. The data from Klasies River, Apollo 11, Rose Cottage Cave, Blombos, Sibudu, Diepkloof, the Pinnacle Point sites, and Klipdrift clearly show the enormous potential of the subcontinent. Elsewhere, a similar intensification of research would Page 24 of 39

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perhaps produce a similar increase in data relevant to the definition of cultural modernity. Although this chapter has not addressed these regions in detail, research in China and East Asia is improving the database and documenting new patterns of cultural evolution during the Late Pleistocene (Wang 2005; Conard 2013; Ono 2013). Western Eurasia also has considerable potential, but there is less reason to assume that the archaeological record will be so radically transformed by further work. Instead, important gaps will be filled and gradually a more complete picture of the highly variable behavioral patterns during the Lower, Middle, and Upper Paleolithic will emerge. With time we will be better able to develop and test new hypotheses for the evolution and spread of cultural modernity, and this problematic concept will continue to undergo debate (Henshilwood and Marean 2003; d’Errico and Stringer 2011). For example, colleagues including Shea (2011) have long argued that we should jettison the simplistic and controversial concept of behavioral modernity and instead work to gain a better understanding of behavioral variability. Researchers in T€ ubingen are developing a model for behavioral plasticity and the evolution of “hyperplasticity” to help explain how cultural complexity developed over the course of human evolution (Kandel et al. 2014). This model arises in part from the observation that, over the course of human evolution, behavioral patterns become increasingly detached from direct environmental causality, and ever more behavioral patterns and solutions to problems appear in the archaeological record. Hominins increasingly have created their own environment until they could occupy even the most inhospitable parts of the planet. This pattern continues today, and the concept of hyperplasticity offers the advantage of not reducing human evolution to a dichotomy between archaic or modern behavior. Based on the data presented above, a strict unilinear and monocentric model for the evolution of behavioral modernity appears less likely than a pattern of mosaic polycentric modernity (Conard 2008, 2010). These data suggest that MSA and Middle Paleolithic societies generally existed within regionally specialized social groups with highly variable material culture. Whether anatomically modern or archaic, these people lived at a similar level of technological and cultural development. Perhaps by the early part of the Late Pleistocene or possibly as late as 40–50 Ka, full behavioral modernity developed in Africa and in Eurasia. Most archaic humans appear not to have mastered the repertoire of new behaviors including fully developed symbolic communication. If, however, some late archaic humans, including Neanderthals, were culturally fully modern as d’Errico and Zilhão have long argued, their behavioral patterns still put them at a reproductive and demographic disadvantage in comparison with the anatomically and culturally modern social groups that propagated across the Old World. The extinction of Neanderthals and Denisovans “▶ Neanderthals and Their Contemporaries” following a small amount of interbreeding (Green et al. 2010; Krause et al. 2010; Pr€ ufer et al. 2013; Sankararaman et al. 2014) does not necessarily mean that they were not culturally modern, just as the extinction of local groups of modern Homo sapiens in recent times does not mean that they were not culturally modern. The main characteristic of Homo is that our cultural development can, and does, vary independently of our biological substrate (Conard 1990). Thus, late anatomically archaic peoples may or may not have been behaviorally modern, just as early anatomically modern humans may well have been behaviorally archaic (Zilhão 2001). Nonetheless, at the end of the day, only modern humans survived and populated all regions of the globe and outcompeted all other hominins. In the coming years, archaeologists and paleoanthropologists need to establish high-quality regional databases and specific local scenarios and hypotheses for the evolution of modern patterns of behavior (Hublin et al. 1996; Parkington 2001; Lewis-Williams 2002; Conard and Bolus 2003; Longo et al. 2011; Higham et al. 2011, 2012; Douka et al. 2012; Talamo et al. 2012). As work progresses, researchers should be able to test these hypotheses and better define these diverse regional scenarios to create new models that come closer to reflecting the evolutionary reality that Page 25 of 39

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a nuanced history of our species warrants. This work should precede using multiple analytical paradigms and shifting scales of analysis (Conard 2001a). There are certainly multiple approaches to this complex problem, and all contextually informed explanatory models for the rise of cultural modernity are welcome, regardless of whether they originate from the natural sciences, social science, or humanities. Regardless of where one positions oneself in these debates, only Paleolithic archaeologists and paleoanthropologists are able to make direct observations from the past, and thus they are in the best position to explain how our species evolved. If we accept the fundamental unity of all living people, the question of when hominins became like ourselves remains a relevant question that cannot be left to experts in other fields, who have no direct observations and data from the past. Following this line of argument, we should use our privileged position as the producers and curators of knowledge about the past to continue to refine our models of how populations of modern humans with our remarkable cultural capacities evolved.

Cross-References ▶ Archaeology ▶ Defining Homo erectus ▶ Dispersals of Early Humans: Adaptations, Frontiers, and New Territories ▶ Evolution of Religion ▶ Hominin Paleodiets: The Contribution of Stable Isotopes ▶ Homo ergaster and Its Contemporaries ▶ Homo floresiensis ▶ Later Middle Pleistocene Homo ▶ Modelling the Past: The Ethnological Approach ▶ Neanderthals and Their Contemporaries ▶ Origin of Modern Humans ▶ Overview of Paleolithic Archaeology ▶ Phylogenetic Relationships (Biomolecules) ▶ Quaternary Deposits and Paleosites ▶ The Evolution of Speech and Language ▶ The Evolution of the Hominid Brain

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