Embryos in Deep Time: The Rock Record of Biological Development 9780520952300

Table of contents :
Contents
Acknowledgments
Prologue
1. Fossils, Ontogeny, and Phylogeny
2. Evo-Devo, Plasticity, and Modules
3. Fossilized Vertebrate Ontogenies
4. Bones and Teeth under the Microscope
5. Proportions, Growth, and Taxonomy
6. Growth and Diversification Patterns
7. Fossils and Developmental Genetics
8. “Missing Links” and the Evolution of Development
9. Mammalian and Human Development
10. On Trilobites, Shells, and Bugs
Epilogue: Is There a Moral to Developmental Paleontology?
Notes
Bibliography
Index

Citation preview

Embryos in Deep Time

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Embryos in Deep Time The Rock Record of Biological Development Marcelo Sánchez

University of California Press Berkeley   Los Angeles   London

University of California Press, one of the most distinguished university presses in the United States, enriches lives around the world by advancing scholarship in the humanities, social sciences, and natural sciences. Its activities are supported by the UC Press Foundation and by philanthropic contributions from individuals and institutions. For more information, visit www.ucpress.edu. University of California Press Berkeley and Los Angeles, California University of California Press, Ltd. London, England © 2012 by The Regents of the University of California Library of Congress Cataloging-in-Publication Data Sánchez, Marcelo R.   Embryos in deep time : the rock record of biological development / Marcelo R. Sánchez.   p. cm.   Includes bibliographical references and index.   ISBN 978-0-520-27193-7 (cloth : alk. paper)   1. Paleobiology.  2. Embryos.  3. Developmental genetics.   I. Title.   QE719.8.S26 2012  560—dc23 2011034435  

Manufactured in the United States of America 21 20 19 18 17 16 15 14 13 12 10 9 8 7 6 5 4 3 2 1 The paper used in this publication meets the minimum requirements of ansi/niso z39.48–1992 (r 1997) (Permanence of Paper).  

Contents

Acknowledgments vii Prologue xi 1. Fossils, Ontogeny, and Phylogeny 1 2. Evo-Devo, Plasticity, and Modules 34 3. Fossilized Vertebrate Ontogenies 46 4. Bones and Teeth under the Microscope 66 5. Proportions, Growth, and Taxonomy 92 6. Growth and Diversification Patterns 105 7. Fossils and Developmental Genetics 126

8. “Missing Links” and the Evolution of Development 141 9. Mammalian and Human Development 158 10. On Trilobites, Shells, and Bugs 176 Epilogue: Is There a Moral to Developmental Paleontology? 195 Notes 197 Bibliography 213 Index 243

Ack nowledgm ents

I would like to thank the University of Zürich and its Faculty of Science, as well as the Institute of Paleontology, for providing an inspiring, challenging, and supportive environment in which I could write this book. I thank current and past members of my lab and close colleagues for everything I learned from them: Ingmar Werneburg, Laura Wilson, Torsten Scheyer, Christian Mitgutsch, Massimo Delfino, Jasi Hugi, Christian Kolb, Dai Koyabu, James Neenan, Fredy Carlini, Sandrine Ladevèze, Corinne Wimmer, Jan Prochel, Peter Menke, Madeleine Geiger, Katja Polachowski, Fiona Straehl, Patricia Meier, Vera Weisbecker, Fernando Galliari, Lisa Rager, Thomas Schmelzle, and Anjali Goswami. I also thank several colleagues in Zürich and abroad for discussion of ideas and for kindly providing information: Lennart Olsson, Shigeru Kuratani, Mike Richardson, Hiroshi Nagashima, Hugo Bucher, Tom Kemp, John Spice, Norberto Giannini, Johannes Müller, Rainer Schoch, Shige Kuraku, Andreas Wagner, Inés Horovitz, Orangel Aguilera, Lionel Hautier, Renaud Lebrun, vii

viii / Acknowledgments

Anjali Goswami, Norm MacLeod, Rick Madden, Martin Sander, Kathleen Smith, Paul Taylor, Rafael Jiménez, Nico Goudemand, Claude Monet, Michael Hautmann, Christian Klug, Heinz Furrer, Richard Hoffmann, Kenneth de Baets, Thomas Martin, Alexander Nützel, Claudia Hoffmann, Fredy Carlini, Karin Niffeler, and Séverine Urdy. I thank the contributors to the issue of Seminars in Cell and Developmental Biology that I edited in 2010, for helping to inspire this book: Richard Cloutier, Zerina Johanson, Moya Smith and colleagues, Louise Humphrey, Christoph Zollikofer, Marcia Ponce de León, Martin Sander, Nicole Klein, Nadia Fröbisch, Florian Witzmann, Rainer Schoch, Jennifer Olori, Torsten Scheyer, and Massimo Delfino. Rob Asher in Cambridge, England, Laura Wilson and Torsten Scheyer in Zürich, and Ann-Christin Honnen in Berlin kindly and critically read early drafts and made very useful suggestions. Three anonymous reviewers and especially Michel Laurin very generously provided critiques and suggestions that improved the clarity of this work and helped me to avoid mistakes. Torsten Scheyer, Christian Mitgutsch, James Neenan, Lisa Rager, Kevin de-Carli (Zürich) and Nigel Hughes (Riverside) kindly revised parts of the text. Torsten Scheyer and Jasi Hugi provided much-needed advice on the paleohistology chapter; Christian Mitgutsch, on ontogeny and historical matters. Zhe-Xi Luo shared information on “early mammals” with his usual collegiality and good humor. Séverine Urdy (Zürich) generously provided extensive comments and insights relevant to bugs and shells. Any infelicities or inaccuracies that remain are entirely my responsibility. For help with graphics and formatting issues, I thank Morana Mihaljevic, Kevin De-Carli, Rosi Roth, Fiona Straehl, and Torsten Scheyer. Madeleine Geiger, Katja Polachowski, and

Acknowledgments / ix

Claudia Joehl skillfully prepared some of the figures. John A. Long (Los Angeles), Matt Friedman (Oxford), Jasmina Hugi (Zürich), Joachim Haug (New Haven), Pancho Goin (La Plata), Zhe-Xi Luo (Pittsburgh), Torsten Scheyer (Zürich), Christian Klug (Zürich), Christoph Zollikofer and Marcia Ponce de León (Zürich), Loïc Costeur (Basel), and Rainer Schoch (Stuttgart) very generously made figures available. For crucial and superb assistance, I thank Heike Götzmann for administrative matters and Heini Walter for IT matters. I also thank my Institute’s director, Hugo Bucher, for his support. Lynn Meinhardt, Kate Warne, and Chuck Crumly of the University of California Press promptly answered my many questions during the editorial process and kindly provided much advice on a variety of matters, and Sheila Berg provided very useful and comprehensive editorial and stylistic remarks on the manuscript. Wolfgang Maier in Tübingen has inspired my interest in ontogeny over the years and has been a much-appreciated mentor. Peter Holzwarth in Zürich, Rob Asher in Cambridge, AnnChristin Honnen in Kiel and Berlin, and my mother, Gloria Villagra, in Puerto La Cruz/Buenos Aires provided moral support. In the past few years I have been supported primarily by the Swiss Research Council (SNF) and by the University of Zürich.

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Prologu e

The diversity of life is usually presented in evolutionary trees: A branching pattern culminates in figures of animals and plants. This is good, as trees convey the common history that organisms, including ourselves, share. But there is a limitation in this kind of representation. The organisms portrayed are static entities, usually adults with the recognizable features of their species. In reality, organisms change throughout their lives. If we wanted to portray the biology of biodiversity, we could show for each organism a high-speed film of the different phases of its life history—for a multicellular organism, from fertilization to death. The kinds and number of changes that occur over the life course are so numerous and complex that different scientific disciplines are devoted to each phase of the process. The first steps of cell division and formation of an embryo are associated with embryology. Much research in this area concerns, for example, gastrulation, the phase in which the germ layers are formed and the body plan of the mature organism is established. Developmental biologists tend to study the point of occurrence or orixi

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gin of tissues and organs. Comparative anatomists and zoologists are usually concerned with changes occurring after birth, which some biologists like to call “growth,” as opposed to development. For all these disciplines, molecular biology has offered methods and concepts to address a whole new set of questions concerning the mechanistic bases of life history evolution, also reviving old ones posed by morphologists. Individual development is a rich subject of investigation in biology. But what about the fact that most species represented on the tree of life are extinct? Some may think that developmental biology needs paleontology like a fish needs a bicycle. They might also claim that the fossil record appears to be totally silent about many aspects of developmental evolution and genetics. I do not think this is the case, and I have written this book to explain why. Of course, paleontology remains largely silent about major topics such as gastrulation. Defining the limits of what paleontology can achieve is thus important. In this context, I am reminded of the contributions of a famous fish anatomist to the discussions in the 1980s about the role of fossils versus molecules in reconstructing the tree of life. Colin Patterson (1933–98), a major figure in the study of fossils who was based for decades in the paleontology department of the Natural History Museum in London, strongly advocated the primacy of information on living species over fossils when investigating evolutionary relationships. He was severely criticized by most fellow paleontologists. Several years later his ideas became much appreciated, and in 1996 he was awarded the Romer-Simpson Medal, the highest recognition of the Society of Vertebrate Palaeontology. The role of paleontology in reconstructing the tree of life is largely recognized by most biologists, in spite of the limitations of working with fragmentary data, which contrasts greatly with the  

Prologue / xiii

large database of information (e.g., genomic) now known for an increasing number of living species. The integration of information from paleontology and embryology has a long tradition. During the Victorian era, for example, Thomas Huxley made major contributions in both fields; he was the first to suggest that birds are related to dinosaurs, for example, and he discovered major aspects of the early life history of cnidarians, the group to which corals and jellyfish belong. In fact, many researchers are continuing to make major contributions in these diverse fields. For example, Phil Donoghue, in Bristol, studies conodonts, basal vertebrate animals that have been extinct for about 200 million years, and also has a research program concerning micro RNAs and their role in morphologic diversification. Brought together, his paleontological, developmental, and molecular studies are leading to a better understanding of the history of life. In this book I examine what we may learn about development directly from the fossil record. Fossils are not just the static objects of defunct animals. With a discerning eye and the appropriate information and conceptual background we can learn much about the reproduction and development of the extinct animal. It would seem that the snapshot of some stage of development that a fossil provides is surrounded by so many unknowns that the interpretation of the often incomplete anatomy remains speculative at best. But there is a method in the study of incomplete fossils, and the inferences drawn by most paleontologists are evidence based. This book is intended for people with a general knowledge of biology and an interest in fossils and evolution. The notes and references at the back of the book may help to clarify and elaborate the diverse matters I treat here. I beg to be excused

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for the somewhat haphazard nature of the references cited, as some of the topics treated here are very encompassing and have had a long history of investigation and thoughtful contributions. Many examples are taken from my own work and that of my closest collaborators, as these are the ones I know best. Ultimately, each book presents a personal take on a matter, and this is no exception.

On e

Fossils, Ontogeny, and Phylogeny Human history is a brief spot in space, and its first lesson is modesty. Will Durant and Ariel Durant, The Lessons of History

I remember as a child being very impressed by a statement, attributed erroneously to Thomas Huxley, that claimed that if monkeys were left alone in front of typewriters, they would type by chance and, given enough time, would indeed type the entire Encyclopaedia Britannica. I had an abridged version of the Encyclopaedia in Spanish, fifteen thick volumes, so I had an idea of the extent of text involved. I read the statement for the first time in a creationism booklet, which pointed out the absurdity of the statement.1 But it made sense to me: unlikely, and yet, given infinite time, it could happen. While writing this book, I decided to investigate the matter a little and found out that this thought experiment about monkeys and typewriters has been seriously treated from philosophical and statistical perspectives and has been used in various popular accounts. In fact, this is one of the 1

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best-known thought experiments, dating to a 1913 essay by the French mathematician Émile Borel. Since then it has become a popular illustration of the mathematics of probability. Apparently the likelihood of monkeys typing the Encyclopaedia Britannica or Shakespeare’s works is infinitesimally small. What is the relevance of this to a discussion about evolution and development?2 There are two points to discuss: the length of time and the probability of evolutionary change occurring during it. Geologic time is not infinite, but it is long, very long, or deep—a good descriptor considering that it is in the depth of rocks that we can learn much about this distant past. The term deep time originated with the American writer John MacPhee’s popular account of geology titled Basin and Range. There he discussed how geologists develop a sense of the vastness of time intellectually and emotionally.3 Consideration also of the vastness of the extinct biodiversity raises a transcendent perspective, and it may be the most fundamental contribution to human understanding of the universe that geologists and paleontologists can provide. Thanks to dated fossils placed in evolutionary trees and to molecular estimates, we know that life originated at least 3.5 to 3.2 billion years ago and that multicellular life is at the very least 700 million years old.4 In the twentieth century one of the major achievements in geochemistry was the development of several methods of rock dating, based on isotopes of different chemical elements, leading to the secure establishment of an absolute time dimension of the vast history of earth and life. The evolution of biodiversity is said to have needed long periods of time. For Darwin, it was important to gather information about the antiquity of the earth and of life. He was concerned that there  

Fossils, Ontogeny, and Phylogeny   /  3

was “enough” time for truly complex structures, such as the eye, to have evolved. The later discovery of mutations and their “randomness” would at first glance seem to have made Darwin’s worries justified. Evolution is far from random, and monkeys in front of typewriters are not a good analogy for evolutionary processes. One of the main points made in recent books on evolution is the nonrandomness and predictability of evolution. This is not a theoretical conclusion but rather something shown empirically by the patterns seen in living phenotypes and genotypes and also in fossils. The fact that mutations in some genes have a high probability of being selected repeatedly in independent lineages facing similar environmental conditions is called “parallel genotypic adaptation.” This makes genetic trajectories of adaptive evolution predictable to some extent, leading to the reconstruction of molecular processes that most likely operated in extinct species in spite of the contingency of evolution. Development in extinct species can also be reconstructed thanks to principles that have been discovered to be shared by huge groups of species, even involving the the same developmental genes. And yet diversity, in terms of both species and breadth of form, is vast, like the deep time in which it evolved.

Extinction of Most Life on Earth The theory of evolution provides a rational explanation for the rich biodiversity that surrounds us. Every day across the world more and more people live in cities, but even those who are rarely confronted with nature are aware of at least some of this diversity thanks to television or a visit to a zoo. Approximately

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1.5 million species have been described, and 10 million to 100 million species are estimated to inhabit the planet. But this huge number of species is only a small fraction of the total number of species that have existed on the planet; conservative estimates suggest that as much as 99 percent of the entire diversity of life that has existed on earth is extinct.5 Most of that past diversity is largely undocumented in spite of the work of paleontologists, as remains of most of those species no longer exist or await discovery and study. The portion of this large diversity that is most directly obvious to us is vertebrates, the group of backboned animals to which we belong. There are about 59,000 living vertebrate species, but many more species have been described. Some vertebrate groups are better known paleontologically than others. Dinosaurs, for example, are known from some 550 described genera, but it is estimated that approximately 1,850 genera must have existed. Not all new genera and species of fossil organisms that are described are valid, as paleontologists continuously revise their decisions on taxonomy and new studies of variation and anatomy help to refine criteria on which to base decisions. A survey in 2003 determined that the then-valid 4,399 genera of fossil mammals represented 80 percent of the total number of genera ever described. This figure was 67 percent in 1945, as reported by the American paleontologist George Gaylord Simpson in a classic paper. More and more valid fossil genera of mammals and of other vertebrates are being named. The case of the evolution of our own genus, Homo, illustrates the controversy and diverging opinions on the taxonomy of fossil forms. Yet on many issues there is broad agreement. For example, most anthropologists acknowledge that about two million years ago, at least five different species of humans inhabited

Fossils, Ontogeny, and Phylogeny   /  5

the planet. We are the last branch of a once much richer evolutionary tree since our ancestors diverged from chimpanzees some seven million years ago. The numbers I present here serve simply to illustrate the fact that if we wish to understand the evolution of biodiversity, looking at the past is fundamental. The role of paleontology in describing extinct biodiversity is obvious, but there are many other ways besides mere description in which paleontology contributes to evolutionary biology.

The Fossil Record and What It Tells Us about Evolution The new fields of inquiry created by the emergence of molecular biology in recent decades brought about much well-founded enthusiasm. It also led in some circles to questioning the justification for continuing older disciplines such as paleontology. In the context of these discussions, many of my colleagues have reflected on the many specific aspects that paleontology alone can address to help other biological disciplines and establish an integrative research agenda. These include the following. 1. Fossils provide a time scale for evolution. The oldest representatives of groups from datable rocks provide numbers in which at least a splitting among groups of organisms must have occurred. If we have the DNA sequences of two living species and thus know how much they differ, and if we know when their forms became distinct in the fossil record, we can establish a rate of DNA change. This rate can then be used to estimate the divergence dates of other, related groups for which fossils are not yet known.

540 MY ago

490

445

416

298

251

202

146

65

Figure 1.  Main geologic eras and periods discussed in the text and their age in millions of years.

Quarternary

Paleogene

Cretaceous

Jurassic

Triassic

Permian

Carboniferous 355

Neogene

CENOZOIC

MESOZOIC Devonian

Silurian

Cambrian

Ordovician

PALEOZOIC

Fossils, Ontogeny, and Phylogeny   /  7

2. Fossils provide information on organisms’ historical distribution in space. The young Charles Darwin himself noticed this during his voyage around the world. He recorded fossil marine molluscs in the Andes, with obvious implications for the dramatic changes occurring in geologic time. The discovery of fossil platypus relatives in South America several years ago, among other discoveries, provided hard evidence of presupposed faunal connections with Australia. The distribution across Southern Continents in the Triassic of a dog-sized early mammalian relative, Lystrosaurus, and of extinct marine reptiles called mesosaurs in the Permian provided independent evidence for continental drift. Fossils document the past presence on islands of many forms greatly affected by human presence and driven in many cases to extinction in prehistoric times, as is the case for the many giant lemurs found in caves in Madagascar. The list of examples is indeed very long, and the significance of fossils in solving (and creating) biogeographic puzzles or serving to test hypotheses based on living species alone is indisputable. 3. Fossils can document the order in which a suite of features that now diagnose a modern group of organisms or a species arose. Modern mammals uniquely have, in addition to many other traits, hair, mammary glands, and two tooth generations. However, we know that these traits did not all appear at once, as documented by a rich fossil record going back some 315 million years, the minimal time established by fossils for the splitting of the mammalian and reptilian lineages from their common ancestor. 4. Fossils documenting the origin of groups of living species are crucial for testing relationships among organisms. Without the extinct theropod dinosaurs illustrating the origin

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of birds, for example, it is more difficult to understand how a chicken can be more closely related to a turtle than to a mammal. Fossils improve the accuracy of evolutionary tree reconstruction through the recognition that features can evolve in parallel, such as the constant body temperature of birds and mammals. They can also provide direct information on what the first feathers and hairs of these animals looked like early in their evolution. Fossils often document organisms with a unique mosaic of features, which is very revealing for our understanding of the origin and function of living organisms’ traits. Theropods show a unique combination of features that we would not know about just by looking at living species. Who would have guessed that creatures living in the Cretaceous, such as the terrestrial Tyrannosaurus rex, had colorful feathers?6 The fossil record, limited as it may be, should be cherished as the most important source of evidence for what really happened on large time scales involving major transitions. Fundamental questions about evolution can be addressed with paleontological studies. For example:

•



•

Does evolution proceed at a relatively constant rate, through the exponential accumulation of lineages, punctuated only by extinction events? Or does it proceed through bursts of speciations, including “adaptive radiations,” otherwise remaining relatively constant? How can a very large number of characters of a phenotype change dramatically while not losing their structural and functional integration that any viable organism must possess?

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To illustrate the importance of fossils, I referred to the origin of feathers and hair. These are considered “evolutionary novelties”: features that are very different and innovative and that somehow have led to, or are correlated with, a new chapter in evolutionary history. Another example is the evolution of hands and feet, as has been documented in the earliest representatives of the group to which land vertebrates belong. What biologists have agreed on and emphasized again and again is that to understand these innovations, you need to know how they developed in the individual history of the organism that possesses them. We recognize the human hand as a formed and flexible mixture of skeleton, muscle, skin, nerves, blood vessels, and other tissues. To address the origin of the hand you need to go back within a lifetime to our fetal period, during which its various components form. What are their connections with other parts of the body? Which genes are involved in their development? How do muscles, tendons, and bones come together? As stated by the evolutionary biologist Günter Wagner, “The explanation of evolutionary novelties is identical to the identification of the developmental changes that make the novel character possible.” There is another trip back in time we need to take in order to understand the origin of the hand, and that is a trip in geologic rather than individual time. The first fossil vertebrates with muscular hands and feet lived nearly 400 million years ago. By studying those fossils, we can learn the ecological context in which hands evolved and the combination of anatomical features those animals possessed. We know that the earliest vertebrates with hands and feet had more than five digits on each and were aquatic. Now, imagine we could go back in geologic time and then go back in the individual developmental time of the

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now-extinct animals to understand how their hands arose. This hypothetical journey epitomizes the coming together of two disciplines that at first may seem quite distinct: paleontology and developmental biology. But their relation is exceedingly close. We can go back in time in the history of these disciplines and their relations and see how the parallels between individual and transformational change, as documented by fossils, have long been recognized.

The Relation between Paleontology and the Biological Disciplines of Development Whole disciplines or ideas arise or solidify in the canon of human knowledge thanks to the efforts and accomplishments of exceptional individuals with the interest, drive, and opportunity to pursue a particular subject. This was certainly the case with Georges Cuvier, often referred to as the father of paleontology. Cuvier was educated largely in Stuttgart and lived in Paris in the late 1700s/early 1800s.7 Over the course of several decades, he documented the anatomy of hundreds of fossils, establishing the reality of extinction and change over geologic time. He lived before Darwin and was never sympathetic to the evolutionary ideas of his former teacher Jean-Baptiste Lamarck, or those of Cuvier’s peer, a person very much interested in development, Etienne Geoffroy Saint-Hilaire. Statues or busts of all these past glories of French science can be admired by any tourist in Paris visiting the wonderful Museum of Natural History and the Jardin des Plantes. Cuvier’s anatomical work was widely recognized, and his prominent political status during and after Napoleon’s reign also contributed to his visibility and to the spread of his encyclopedic work.

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Cuvier’s magnus opus, Leçons d’anatomie, was translated into German by a famous anatomist working in Halle, Johann Friedrich Meckel the younger. Meckel’s own work also concerned anatomical comparisons, but these were among embryos, and he was especially interested in malformations during development. What Cuvier did for fossils in Paris, Meckel did for embryos in Halle, as he amassed a huge collection of fetuses of many kinds of vertebrate animals. His legacy can be seen even in basic anatomical terminology: Meckel’s cartilage, a major skeletal feature of the lower jaw in embryonic humans; and Meckel’s diverticulum, a portion of the small intestine present in some people. Meckel saw his task as that of completing the work of Cuvier on anatomy by looking at embryology. With him, a long tradition of biologists studying embryos began. Meckel saw a parallel between the differences among adults of living and fossil organisms, on the one hand, and those among embryos of the same species at different time intervals during individual development, on the other. Figuring out the extent or truth or significance of this fascinating fact is what much of biology has been about for a couple of centuries. It is a pity that Cuvier and Meckel did not live to see a fossil that would have given them the chance to ponder extinction and malformations at the same time. A team of French and Chinese paleontologists working in northern China published in 2007 the discovery of a very singular specimen of a choristoderan reptile, representing a group of semiaquatic reptiles of uncertain affinities. Found in Cretaceous rocks known for yielding spectacular fossils of feathered dinosaurs and early mammals, the beautifully preserved skeleton has two heads, each connected to its own set of neck vertebrae, with the rest of the skeleton also completely preserved. The curled-up position of this and other

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similar but single-headed specimens suggests that this individual was a malformed embryo. Assignment of these fossils to the Choristodera was based mostly on the long neck vertebrae and the short limbs, two features characteristic of this group known from fairly complete and numerous adult specimens in this formation. The two heads/two necks malformation is common in living reptiles and is called axial bifurcation. This condition is not necessarily fatal, as many turtles and snakes have survived with it for many years in captivity. Obviously, choristoderes shared with living reptiles a developmental system in which this kind of developmental anomaly could occur. The opportunity to study developmental malformations in fossils is more commonly possible in the realm of invertebrates, where paleontologists collect and study hundreds if not thousands of specimens. Vertebrates are rarer and in most cases more time-consuming to prepare. The parallels between embryology and paleontology have been most commonly sought not through exceptional fossils but rather through comparisons of the two records or morphological transformation. This has been the case even for some scientists with an antievolutionary worldview, both before and after Darwin. For example, the Swiss-born naturalist Louis Agassiz, a student of Cuvier, looked for the relationships among “gradations” of taxa, developmental transformation, and geologic succession of fossils. By “gradation,” he meant that there are differences among taxa in some degree or another, so one could mentally transform one into another by examining the nature of those differences. Agassiz realized that to understand these transformations, the examination of individual development and of fossils in geologic time provided illuminating parallels, even if he did not think that evolution was the mechanism ultimately responsible. An example can be read

Fossils, Ontogeny, and Phylogeny   /  13

Figure 2.  Restoration of a late embryo or newborn choristoderan reptile from the Cretaceous of China. The two-headed condition is called anterior axial bifurcation. The total length of the animal, excluding the tail, was about 40 mm. Drawing by Madeleine Geiger; based on a paper by Buffetaut et al. 2007.

in his major work, Recherches sur les poissons fossils, published in several volumes between 1833 and 1843. Agassiz argued that the tail of adult fossil ray-finned fishes, to which almost all living fish species belong, except for the caelocanths and the lungfishes, paralleled the development of the tail of living species of the group from embryos to adults. Juveniles have a simple tail, later stages have a heterocercal tail in which the upper part is larger than the lower one, and the adult possesses both parts of the tail of similar size. This change is similar to the sequence that Agassiz recorded in fossils. That the differences but also the similarities among species were the result of common descent with modification via evolution was accepted by many other biologists after Darwin, most prominently by the German intellectual Ernst Haeckel, who was twenty-five years old when “On the Origin of Species” was

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first published in 1859. As discussed by his most recent and comprehensive biographer, more people in Europe read about evolution from Haeckel, including in England, than they did from Darwin himself or from any other author. Haeckel was the first person after 1859 to publish prominently an evolutionary tree with actual groups of organisms. Haeckel was also the person to popularize and ultimately to be held mostly responsible by later history to this day, for the notion that “ontogeny recapitulates phylogeny.”8 This maxim encapsulates the idea that the individual development somehow mirrors differences among species. This notion has a history going back even to a major teacher of Cuvier, Carl Friedrich Kielmeyer, from Tübingen, whose lectures at the university reportedly attracted crowds. The parallel between development and evolution has been a classic subject of investigation and discussion in German biology and is reflected in the German language: the same word, Entwicklung, can be used to describe both evolution and individual development.9

Parallels between Paleontological and Developmental Transformations The hand of an early human fetus looks like a paddle, resembling superficially that of our aquatic ancestors. There are many other examples of general similarities between paleontological and developmental transformations. The most celebrated one is that concerning the evolution and development of our lower jaw and our middle ear, a feature we share with all other mammals. This case is often quoted as the ultimate achievement of comparative biology and therefore is worth examining in some detail. Mammals have a single bone forming the lower jaw called

Fossils, Ontogeny, and Phylogeny   /  15

Figure 3.  Human embryos at different ages during the first three months of development as illustrated in the classic work of F. Keibel (1906), in part after the work of Wilhelm His. Not to scale.

the dentary, a fitting name since this is where teeth are located. All other vertebrates have many bones in their jaws. Mammals have three ear ossicles, whereas other vertebrates with a similar kind of ear have only one. Although we may not think that our jaws and ears are connected, they actually are. Mammals are the anatomical oddball, and we can infer based on a Darwinian understanding of evolutionary biology that our early ancestors must have been similar to other vertebrates at some point in our history. In fact, fossils show that our common ancestor with reptiles, which lived at least some 315 million years ago, had

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several jawbones and a simple middle ear with a single ear ossicle. The first fossils documenting the transformations that led to the anatomy of living mammals were found in South Africa and Russia in the 1840s, but since then fossils of the earliest mammalian precursors have been discovered from all continents. Over the course of mammalian history, jawbones other than the dentary underwent a reduction in size, and an articulation between the dentary and the skull evolved. The old jaw articulation became smaller and smaller and gradually detached from the lower jaw. The articulation persisted but with a different function, namely, the transmission of sound waves, eventually becoming specialized for high-frequency sound conduction. The original articular-quadrate jawbones in mammals are termed the malleus and incus as elements of the ear, or more colloquially, the hammer and anvil. Together with the stapes, these bones form the three mammalian middle ear ossicles. The connections among the ossicles form a lever system, with which high-frequency sound waves are transmitted to the inner ear cells and ultimately to the brain for final processing. These mammalian ear ossicles, once part of the masticatory or skull apparatus in our extinct ancestors and in our living cousins including fish, are not much larger than small pebbles. In at least some mammals, it has been documented that during early development two jaw articulations exist: the original one of jawed vertebrates and still characteristic of reptiles and the new, mammalian one, between the dentary, our single lower jawbone, and the squamosal bone of the skull. The middle ear bones are attached via Meckel’s cartilage to the inner side of the dentary bone. Some species from the late Triassic show exactly that arrangement: two simultaneous jaw articulations. The first fossil found to show this remarkable feature came from South

Fossils, Ontogeny, and Phylogeny   /  17

Secondary jaw articulation

Adult

Day 60

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Day 30

Medial view, at approximately Day 7

Day 15

Day 1

Lateral view

Figure 4.  Lower jaw and middle ear ossicle development in the marsupial mammal Monodelphis domestica. The series shows the gradual decrease in relative size of the elements that will become ear ossicles in the adult. The medial view of the pouch young illustrates the long and prominent Meckel’s cartilage, which becomes relatively smaller as the animal grows. Not to scale. Modified from Rowe 1996; and Luo 2007, 2011.

Africa and was named Diarthrognathus in 1958 by A. W. “Fuzz” Crompton of Harvard University.10 Another “early mammal” well known among paleontologists is Morganucodon, from the late Triassic/early Jurassic, which possessed the typical mammalian dentary-squamosal jaw joint alone but had visible remnants of the “old jaw anatomy.” Morganucodon was small, the size of a shrew, and although now known from Eurasia, Africa, and North America, it was originally described from localities in England and Wales. This remarkable example in the fossil record of the parallel between ontogeny and phylogeny does not mean that one can be used to fill gaps in the other. General similarities abound,

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Meckel’s element

Primary jaw articulation

Secondary jaw articulation

Meckel’s element

Primary jaw articulation

Figure 5.  The jaw joint in the “early mammal” Morganucodon. The skull is shown in ventral view and the lower jaw in medial view. The skull length is approximately 2.5 cm. Modified from a figure courtesy of Z.-X. Luo (see Luo 2007).

but deviations are also common. When present, the similarities are sometimes striking but on closer examination become superficial. Marsupial young still attached to their mothers possess a dual jaw articulation at a stage in which the skull is not yet ossified and the arrangements of muscle and soft tissue are poorly differentiated. This is quite distinct from the anatomy of the adult Diarthrognathus (with two jaw articulations), which

Fossils, Ontogeny, and Phylogeny   /  19

roamed some 200 million years ago in what is today the South African Karoo.11

Ontogeny Does Not Usually Recapitulate Phylogeny That ontogeny does not simply recapitulate phylogeny is very well accepted, even though general parallels abound. To understand what recapitulation means as defined by Haeckel analytically, we can use a simple graph. For true recapitulation to happen, an addition at the end of the original or ancestral developmental sequence or trajectory would have to occur. In figure 6 we have four species, each characterized by a common developmental trajectory consisting of the first step, M1–M1. In each species, a new stage is added at the end of the sequence. In this ideal case, the species with the most specialized condition, species “D,” contains in its ontogeny the sequence of evolutionary transformations that occurred through terminal additions. In evolution deviations from the hypothetical recapitulatory pattern occur, as Haeckel himself recognized. Changes mean that features in the sequence can move around, one or more of them can be deleted, or a whole new feature can appear. These changes are sometimes so dramatic or are considered so important that they are thought of as an evolutionary innovation, as in the origin of hair in mammals or feathers in dinosaurs. There are different kinds of deviations from recapitulation, and among them are heterochrony—changes in timing—and heterotopy— changes in spatial position in a structure. Some paleontologists have examined evolutionary transformations documented by fossils and compared them directly with ontogenetic transformations, quantifying the parallels or  

 

 

 

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Species and adult feature

Phylogeny M1 M2 M3 M4

New features terminal additions to an ontogenetic sequence

Ontogeny with recapitulation characters of developmental stages: M characters of adult: M

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Figure 6.  A consistent pattern of terminal addition in the evolution of ontogenetic sequences leads to ontogenetic recapitulation, but there are deviations from this pattern. Modified from Wägele 2005.

lack thereof. For example, the changes in the developing skull of alligator embryos are very similar to those seen in a series of fossils of early crocodiles. This similarity is not just superficial, but refers to a statistically significant correlation in the order in which discrete changes of the same features occur in both series. So, undoubtly, there are parallels between ontogeny and the fossil record of morphological change for some structures in some animals. But these are exceptions.

Evolution of Ontogenies Every window of development in the life of an organism is subject to change during evolution. This is to be expected, because organisms are exposed to environmental pressures in each stage

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of the here and now of their lives. A tadpole confronts challenges such as dealing with predators or finding food, and specializations may appear in this stage in the course of evolution. In fact, as far as frogs and other amphibians,12 such as salamanders, are concerned, a stunning diversity of embryonic morphologies and species-specific developmental features have been documented. Christian Mitgutsch, formerly in my lab in Zürich, and his Ph.D. advisor Lennart Olsson, in Jena, Germany, the place where Haeckel had his long and celebrated academic career, have shown the great diversity in early frog embryos in terms of the timing of development of the cellular precursors of many cranial structures. They have done this by tracing the movement of cells from the neural crest, which is an embryonic layer in vertebrates responsible for the development of many vertebrate-specific tissues. These tissues include, for instance, portions of teeth and many bones of the skull. The work of Mitgutsch and Olsson has produced beautiful illustrations of embryos showing streams of cells migrating at different times and in different proportions in different species (figure 7). The earliest land vertebrates that populated earth offer an excellent paleontological example of changes in diverse stages of ontogeny.. Among these animals were some of the ancestors of living frogs, salamanders, and a group of legless amphibians. The most diverse among these first “amphibians” were the Temnospondyli, a group occurring from the Lower Carboniferous, approximately 340 million years ago, through the Lower Cretaceous, around 120 million years ago. They overlapped for much of their existence with terrestrial dinosaurs. The smallest were less than about 30 centimeters, but some forms were crocodile-like and reached some 7 meters in length. Juvenile and larval specimens have been described for many temnospondyls,

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Bombina orientalis

Dendrobates azureus

Figure 7.  Different degrees of development of the segments or repeated blocks of embryonic tissue of the body (somites) at the start of neural crest cell migration in embryos of the frogs Bombina orientalis and Dendrobates azureus. Photos courtesy of Christian Mitgutsch and Lennart Olsson.

showing much diversity in larval ecologies and growth patterns. All temnospondyls raised their young in the water, but the type of aquatic environment varied. Some groups preferred or tolerated brackish or even saltwater; others restricted themselves to lakes.13 These larvae were all carnivorous, as shown by their dentition and, in some cases, powerful jaws. The other fossil fauna registered in the sites where these exceptional fossils were found, as well as detailed considerations of the masticatory anatomy or the occasional stomach content of temnospondyls, reveal that some preyed on fish while others ate various small “amphibians.” The remarkable preservation of diverse life stages in temnospondyls is explained in part by their large size, making them more likely to be preserved and also more easily visible to paleontologists working in the field.14 A related group, the lepospondyls, were, like the very earliest “amphibians,” small: in the 5- to 20-centimeter range. There is almost nothing known about the ontogeny of lepospondyls, and this poses a challenge for pale-

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ontologists trying to precisely determine their relationships and the origin of the living amphibians using developmental data. Much variation in ontogenetic pathways has been demonstrated in a newtlike group of some of the earliest vertebrates with limbs or tetrapods, the branchiosaurids. Almost all twenty species of this group kept larval features such as external gills or gill denticles in mature stages; these are neotenic characters. Some other species went through a metamorphosis and lost their larval features as adults. All members of the group were small, in contrast to other temnospondyls. Thousands of specimens of some branchiosaurids are known from sites in Germany, including one in the Thuringian Forest Basin. There Ralf Werneburg has studied fossil temnospondyls such as branchiosaurids for many years. Some branchiosaurid species have features that place them as stream types; others, with visible external gills, are described as pond types. One discussion among experts is whether in some cases the two types can occur as different ecomorphotypes of the same species, bringing ontogenetic variation one step further by presenting a case of “phenotypic plasticity,” a topic I discuss in chapter 2. As in the examples above, any stage during the development of an individual can change. This has been demonstrated empirically for many vertebrate species and their constituent stages. All stages of ontogeny and not just adults evolve, the subject of many research efforts. Many authors present data and ideas to criticize a straw man who defends the naive recapitulatory idea that ontogenetic and evolutionary transformations perfectly mirror each other. Most important, the desire to examine the fundamental aspect of how development has evolved has lead to the examination of organisms of many groups, leading to several major discoveries. For example, Mike Richardson and,

Figure 8.  Three stages of development in the shark, human, lizard, and bird. Modified from Westheide and Rieger 2009.

Fossils, Ontogeny, and Phylogeny   /  25

more recently, Ingmar Werneburg have documented the outer morphology of embryos that at a glance show, at more or less comparable windows of development, the substantial differences in proportions and shapes and size of the yolk in fish, snakes, frogs, birds, lizards, and mammals including humans. This feature is one of many that illustrate the different physiological and morphological features across individual time, across diverse species.15

Ontogeny and the Conditions of Existence If development tells a story, then it is like those ghost stories that children tell around a campfire, with each youngster adding a snippet, building on what has come before. There is no single narrator and no internal dialogue. There is what just happened, what is happening now, and what comes next. Mark S. Blumberg, Freaks of Nature

The changes in tissues that occur during individual development do so in the here and now of the living embryo. From that perspective, it appears as if adults are almost an accident, or rather just one of several snapshots of life. This does not mean that the features of a developmental stage are random; they are the results of processes we can in many cases quantify and predict—the product of well-coordinated and deterministic mechanisms wherein plasticity and chance play a major role in the outcome. There is a genetic developmental system that operates in an environmental context. This system lies behind the phenotypic unfolding of development, which is ruled by the physical and chemical laws that operate in nature. The explanation for the existence of a feature at any stage of  

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development other than the adult is usually made in terms of a future state toward which animals aim. As argued by John Reiss in his book Not by Design, the explanation for the existence of a feature should be in terms of the needs at the moment of its existence, not in terms of a future state toward which it conduces. To understand this basic tenet, it is most useful to refer to the idea of the “conditions for existence” originated by Cuvier. The “conditions” to which Cuvier referred are the features of a living being without which it could not survive. An organism cannot exist unless it satisfies its conditions for existence. This may sound tautological or trivial, but like many great truths, the idea becomes fundamental only after it has been fully appreciated. This idea has important implications for the conceptual framework we use to examine the evolution of development. For example, when considering the ecological aspects of evolutionary diversification, a “niche” is often used as if it were to exist externally and as a target towards which a group of organisms aim. As has been argued before, a niche does not exist independently of organisms, which actually create it. Throughout life, an organism affects and also is affected by its environment.16 If a new oceanic island forms, eventually, by chance, some organisms will make it there. They will not do so with a plan or goal; they will simply try to survive. Most biologists are not so naive as to think organisms have a plan, but a narrative is often built around a designed plan. Natural selection constrains what evolves by “choosing” without a plan among the many experiments that development produced in a new environmental context. Because organisms are a mosaic of characters, all integrated but some significantly more than others, development will evolve in a complex way with the action of natural selection. Evolutionary changes in island species are sometimes explained

Fossils, Ontogeny, and Phylogeny   /  27

as the result of a halt in or retardation of development, in which the island form simply resembles a juvenile stage of the ancestor. But organisms are mosaics. Each organ or part, although integrated with the rest, is governed by different rules of relative growth. An island species may have a general resemblance to a juvenile of the ancestral species, but this may be only superficial or valid for some features. The “mosaic” results over evolutionary time because of the conditions for existence that each stage of development has to fulfill. I have discussed several parallels between developmental biology and paleontology in subject and in approach. Another one is the teleological perspective, which holds that there is design behind the change, and design for the better. It is this perspective that has dominated in the two disciplines. The idea of a design and goal is associated with teleology, a term that comes from the Greek philosophers, who first discussed the issues of purpose and goal in life in different contexts. Unless one accepts the tenets of many religions or other forms of spiritual belief, teleology has no place in any scientific discussion on evolution. And yet the search for a narrative and ignorance of the self-organization principles of life led in the past to a teleological conception of life. A teleological view of life is not supported by study of fossil data. The fossil record shows numerous cases of diverse and parallel morphological patterns. Classic examples are the bushy evolutionary tree of horses going back to the beginning of the Eocene, some 55 million years ago, or that of humans, with the five species of hominids living simultaneously some two million years ago—only one of which survives today. Forms of teleological thinking that by current standards appear quite bizarre have been abundant in the history of biol 

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ogy. In many cases some sort of vitalistic force was claimed to exist that produced evolutionary change in a predetermined direction, triggered by an intrinsic property of organisms. Examples are the innate perfecting principle of Lamarck and the idea of “orthogenesis,” the latter treated at book length by the influential biologist Theodor Eimer. These ideas of vitalism and inner driving forces of life greatly influenced paleontology. Evolution via “aristogenesis,” a kind orthogenesis involving constant improvement, was advocated, for example, by Henry F. Osborn, a leading figure in American paleontology and for many years president of the American Museum of Natural History in New York, in the first decades of the twentieth century.17

Ontogeny and Phylogeny To further understand the relation between ontogeny and phylogeny some pictorial representations are instructive. I reproduce my two favorites here. The first one is by the German botanist Walter Zimmermann (1892–1980), who, in addition to his work on plant morphology, was an original and influential writer on evolutionary theory and methods for biological classification. In the version of a “Zimmermann diagram” reproduced here (figure 9), there are spirals of ontogeny containing different life stages changing over geologic time. Phylogeny is the evolution of ontogenies, in this case illustrated by the origin of birds, with the emblematic Archaeopteryx, the “reptile-bird missing link” from Bavaria, in a reconstruction a few steps below the current bird ontogeny. The entire spectrum of change in time, including phylogeny and ontogeny, Zimmermann called hologeny, a term that was never accepted into the standard terminology of my field.  

Si

lu

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To d

ay

Fossils, Ontogeny, and Phylogeny   /  29

Figure 9.  The relationship between ontogeny and phylogeny, as illustrated by Walter Zimmermann. Modified from Zimmermann 1968.

Another scheme that nicely illustrates evolution was produced by Wolfgang Maier, my former mentor at the University of Tübingen. Among his main contributions are investigations of the anatomy of mammals around the time of birth, when newborns face new environmental challenges. As Maier likes to point out, different species have evolved different anatomies around this window of development, and the same is true of all stages, from zygote to death—the entire life history. Natural selection operates at all stages, and the package of genes and structures and functions operating at diverse levels of biological organization change during evolution. In some cases this change  

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Figure 10.  The relationship between ontogeny and phylogeny, as illustrated by Wolfgang Maier. Modified from Maier 1999.

is gradual, leading cumulatively over geologic time to large evolutionary transformation. Genetic changes are transmitted to the next generations via sexual reproduction. Many variables can be used to characterize the ontogenies represented in abstract terms in these figures. Among them are embryonic and juvenile stage durations, age at maturation, condition at hatching or birth, and reproductive longevity. All comprise the life history of an animal, and each can evolve. Analogous life histories in plants also evolve. In the case of living species, the ability to relate these variables to studies of population dynamics is important for conservation issues, as they can

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inform management strategies for those organisms considered at risk. From an evolutionary perspective, knowledge of these variables can help us understand why particular groups became extinct while others became prolific or just survived. Some of these variables are also related to major anatomical innovations, such as the large brain of humans enabled in part by a long gestation period. To know when these features arose, fossils are key, even though they cannot deliver direct information on some variables such as gestation length. This is the case because large amounts of empirical data have shown a close association of some anatomical features that become fossilized with life history features. As with the early land vertebrates discussed above, to document the evolution of life histories in the geologic past, exceptional fossils are the first and most obvious subjects to study.

Ontogeny and the Reconstruction of the Tree of Life Since the pioneering work of Ernst Haeckel and with the theory of evolution as a framework, the reconstruction of the tree of life has been a major task. The history of approaches and issues is long and complex. A topic that has surfaced repeatedly in the discussions is how to incorporate ontogenetic information into the tree. The inference of relationships among species using morphology is usually done by comparing the existence and specification of diverse features. In the case of vertebrate specialists, we largely examine the bones, muscles, and nerves of adult animals. But heritable and interspecifically variable traits, the kind needed for tree-reconstruction analysis, are present at

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all stages in an animal’s life cycle, so there is no reason only adults should be the source. Ontogeny is thus important, but how exactly should it be used? Most practicing systematists, those biologists concerned with tree reconstruction and classification, would agree with the following series of statements, which aims to summarize what is largely a consensus. 1. An approach based on the study of only adult stages is more likely to be misleading in phylogenetic analysis than one that incorporates a large segment of the life history of the species being studied. This is related to adding a level of complexity to the analysis of features of organisms (characters), going beyond the extreme atomization of superficial morphological similarity.18 An example of the relevance of juvenile stages for figuring out relationships among organisms is provided by animals that were studied by Charles Darwin himself. Barnacles were long thought be molluscs because of their calcareous shell as adults. But barnacle larvae are like those of crustaceans, and the two groups are now known to be closely related. 2. Ontogeny alone cannot be used as the criterion for establishing the direction of evolutionary change in a feature. Systematists seek to discover which features are ancestral and which are specialized, the polarity of change. If evolutionary transformations would always happen through additions of steps at the end of the original ontogenetic sequence or prolongation of an ontogenetic trajectory, the ideal case illustrated above, the comparison of ontogenies would reveal the direction of transformations. But recapitulations are the exception rather than the norm. Comparisons among groups closely related to the ones of interest serve to reconstruct

Fossils, Ontogeny, and Phylogeny   /  33

the network of relationships. Once the root of the network is established, a tree of relationships through which to determine polarity is possible. 3. Not all groups of organisms are governed by similar growth processes, so the nature of the independence or of the morphometric relationships among parts is not universal. The differences I refer to are a major subject of study in the lab of my Zürich colleague Hugo Bucher, who together with Claude Monnet and others is developing new mathematical models for understanding the growth of ammonites, which are extinct molluscs. In molluscs, as for example in brachiopods or “lamp shells,” the form of the shell is produced via accretionary growth at an aperture of expanding diameter, with a series of associated curves. In contrast, in trilobites and in other arthropods molting and the addition of segments occurs. In echinoderms, which include sea stars and sea urchins, the original bilateral symmetry has been modified into a pentaradial one, leading to modifications of the growth process. As I describe in chapter 9, clearly the generation of form in ammonites, trilobites, and echinoderms is different, which must be considered when reconstructing their evolutionary histories. The complex form of organisms is usually partitioned into features (atomization) when conducting numerical studies of phylogeny or evolutionary tree reconstruction.19 However, growth must be considered in these analyses, and it is a big challenge for systematists to figure out how best to integrate this line of evidence.

T wo

Evo-Devo, Plasticity, and Modules

The discipline that brings together the fields of developmental genetics and evolution has been baptized “evo-devo.” Few if any new aspects of evolutionary biology have received as much attention from practitioners and philosophers of biology. Evodevo is purported to provide a new kind of synthesis of knowledge to understand the origin of biodiversity. For this reason, it is important to ponder how paleontology contributes to this area. The central focus of evo-devo is contested. Some see it as explaining the evolution of the capability to evolve, or evolvability. Many see it as explaining evolutionary novelties or innovations in the sense of truly new, large steps of morphological change—for example, the evolution of eyes, teeth, or limbs, or the turtle shell.1 Others see evo-devo as a “passing comet,” a discipline that will be superseded by a newer merging of fields or by a new ordering of groups of researchers and topics, perhaps dictated by the rise of genomics.2 Whatever the case, there is no denying that these discussions have brought much reflection and impulse to evolutionary studies of development.  

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The beginnings of evo-devo were very much about what many distantly related groups, such as flies and humans, or disparate features, such as teeth and limbs, have in common. That the eye of a fly and the eye of a vertebrate are formed via similar molecular mechanisms is a major discovery. That several molecules are shared in the development of teeth and limbs is also a significant achievement. But these structures, once they appear, have different shapes and colors, and that is what makes them fascinating. Evo-devo has changed the emphasis from trying to understand why organisms are so different to addressing how this disparity and diversity could have arisen given the widespread genetic conservatism characterizing these organisms. Understanding the relation between the genotype and phenotype is central in this endeavor. Many biologists in the past have assumed that there is a oneto-one relationship between genotype and phenotype, whereby a viable mutation leads directly to a new phenotype. At all levels of organization, even the molecular one, this has proven to be incorrect. Already one hundred years ago some biologists wrote about a reaction norm, the phenomenon that one and the same genotype is able to produce different phenotypes, depending on external environmental inputs.3 This idea was largely forgotten by the mainstream of evolutionary biologists but is now at the core of developmental studies of evolution. The newly baptized field of ecological developmental biology, as masterfully presented in a textbook by Scott Gilbert and David Epel, summarizes much about the interaction between the environment and individual development. Two aspects of diversity which have become central topics of evo-devo investigations are phenotypic plasticity and modularity. What these important concepts mean and how palaeontology can address them is discussed in what follows.

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Phenotypic Plasticity and Variation Development is not a river of genetic information flowing inexorably downstream toward the creation of biological form, but rather many rivers, tributaries, and eddies—a turbulent, cyclical process involving gene regulation and protein synthesis. Mark S. Blumberg, Freaks of Nature  

Nothing in variation makes sense except in the light of development. Jukka Jernvall

Variation has a nongenetic component, and phenotypic plasticity refers to that variation induced by environmental effects. Such effects can be physical factors such as temperature, or biotic factors such as interactions with other species, or stimuli such as diet. This is of course very important, as variation is what natural selection acts upon. More variation can mean more evolution and more diversification.4 Phenotypic plasticity in growth patterns coupled with environmental factors has been reported for several dinosaur species, including the prosauropod Plateosaurus. In periods of abundance or favorable climate, animals grew faster. Such kind of plasticity is not characteristic of all prosauropods; it is absent, for example, in the closely related Massospondylus. This kind of investigation can be undertaken only for those species for which large quantities of fossils are known, enough to produce growth curves using paleohistology to estimate the age of individual specimens. Phenotypic plasticity has been hypothesized for several groups of Paleozoic early land vertebrates based on careful anatomical and paleoecological studies of hundreds of specimens. Rainer Schoch in Stuttgart demonstrated with exceptional fossils of a temnospondyl that the same species was capable of alter-

Evo-Devo, Plasticity, and Modules   /  37

G

en

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Figure 11.  The old and new views of the relationship between genotype and phenotype. Based on a similar figure by Sholtis and Weiss (2005).

ing its ontogenetic strategy depending on the environmental conditions—as is known for many modern salamanders. The animal in question, Sclerocephalus, attained a maximum size of 2 meters and looked superficially like a strange crocodile. In lakes that were large and shallow, with poor food availability, Sclerocephalus truncated its development to produce small adults that ate small prey. In a more complex lake, richer in prey abundance and diversity, Sclerocephalus extended its growth phase and became larger and might even have ventured to land, although stomach contents show it was primarily an aquatic creature. In another fossil lake that preserves very large voracious sharks, only larvae have been found, suggesting that adults lived some 

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Figure 12.  Skeleton of Sclerocephalus haeuseri from the Saar-Nahe Basin, southwestern Germany, about 297 million years old. Courtesy of Rainer Schoch (Stuttgart).

where else, perhaps to avoid predators. The connection between ecological conditions and changes in ontogeny has been inferred with solid evidence in these Paleozoic vertebrates. Sclerocephalus was apparently plastic in its developmental strategy; other early land vertebrates also known from hundred of specimens and different localities were less so. Exceptional circumstances must have led to the preservation of such fossils and their discovery. Swamps and lakes are often good fossil deposits, and in some cases anoxic conditions in the muddy bottom of these waters, with not much biological recycling, led to excellent fossil preservation of the bones and even of soft tissues of the dead bodies of those animals. Because the ontogeny of an individual cannot be seen directly in these fossils as one does today with a frog or a salamander, paleontologists have to rely on careful anatomical comparisons of numerous specimens, and while the species affiliation of the different forms can be problematic, we can usually identify these animals with a high degree of confidence. Paleontologists have traditionally been interested in variation, because of the necessities of taxonomy. To set species boundaries among fossils one needs to establish the extent of morphological variation a species can maximally encompass.

Evo-Devo, Plasticity, and Modules   /  39

For that purpose assessing or measuring some features in as many individuals as possible is relevant, and comparisons with appropriate living species and consideration of ontogenetic variation are fundamental. The other necessary aspect is knowledge of the evolutionary tree in which the new species would fit, and with that a recognition of the derived features that characterize that species. The shapes and sizes of bones vary within a species and even within a population. But not all elements of the skeleton vary to the same extent. One factor that may affect the extent of variation is the developmental origin of a bone. Some bones are formed from cartilaginous precursors and are part of the core of the skeleton, in many cases highly integrated within a skeletal module, or group of bones, that evolves more or less in unison. Other bones have no cartilaginous precursors. Those that form from connective tissue such as the patella of the human knee, also present in many other species of mammals, are expected to exhibit greater size and shape variation. The patella and other bones known as sesamoids do not tightly articulate with others and are more affected by muscle and tendon function around the area in which they form. Sesamoids are thus expected to be more variable than other bones. These predictions were tested and confirmed in a study of Pleistocene mammals conducted by Kristina Raymond and Don Prothero, who measured almost two thousand bones from two fossil localities: Rancho La Brea in Los Angeles and San Josecito Cave in Nuevo León, Mexico. The bones belonged to six mammalian species: the saber-toothed cat Smilodon fatalis, the Ice Age lion Panthera atrox, the bison Bison antiquus, the horse Equus occidentalis, the camel Camelops hesternus, and the ground sloths Paramylodon harlani and Nothrotheriops shastensis. Raymond and Prothero compared statistically the variation

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in several dimensions of 989 intramembranous bones, including the patellae and other sesamoids, with that of 811 endochondral bones, primarily astragali, of comparable size. For twenty-one of twenty-seven measurements there is significantly higher variability in intramembranous bones than in endochondral ones.

Modularity and Integration The concepts of modularity and integration are central to the discourse on evolution and development. Modules are a subset of features of a given organism that are more integrated with each other than they are with the rest of features of that organism. For example, the cusps of a molar have much more to do with each other than each of them does with the shape of the canine tooth, or certainly with some other aspect of the skeletal anatomy. Darwin himself recognized the integration among parts, and he enumerated many examples of his correlations of growth in the first chapter of On the Origin of Species. All features in an organism are integrated, but some are more integrated than others; therefore, integration is not homogeneous. How we atomize the anatomy of an organism is of course related to this. A molar could be conceptualized as a single structure without portioning it into its cusps and its other parts, such as the tooth root. Independent of this subjective aspect, it is intuitively obvious that muscles and joint structures and bones in the knee region will be integrated with each other more closely than each of them will be with any structure in the neck. This integration is not directly observable and has to be inferred from statistical patterns of variation of the traits being studied. The aim is to delimit modules by quantifying the interaction among traits—so-called patterns of covariation. The  

Evo-Devo, Plasticity, and Modules   /  41

details on how this is done are diverse and contested, as this is a growing area of research. Morphological modules exist in different contexts: developmental, genetic, functional, and evolutionary. The methods for studying study them are different in each case. The first extensive quantitative examination of modularity was presented by Everett Olson and Robert Miller in their 1958 book, Morphological Integration. They defined a research agenda and presented the first statistical approaches to quantifying the correlations among traits. Olson and Miller treated fossils very prominently, for example, referring to the apparently modular evolution of dental cusps in a lineage of the Eocene mammal Hyopsodus. They observed a “progressive loss in successive species” of the paraconid, one of the small cusps in the lower teeth of mammals, which appears to be independent of other changes in dental form. Much more recent work in the lab of Jukka Jernvall in Helsinki has shown that several cusp features in the molars of mammals are highly integrated, because of the developmental connection among them. These observations have implications for the reconstruction of evolutionary trees, conducted in the case of fossil mammals based largely on dental characters assumed to be independent of each other. Several people have active research programs to study modularity, including Chris Klingenberg on a wide variety of vertebrate and invertebrate groups and Gabriel Marroig on mammals. Marroig and his colleagues have studied thousands of skulls of some groups of mammals to perform sophisticated analyses that require large samples to provide statistically relevant results. By combining their data with known genealogies of the individuals they study, and evolutionary trees in the case of whole groups, Marroig has been able to examine the relation between

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the genetic makeup of populations and their morphological skull variation. The main main discovery of this research is that the most important determinant of evolvability in a group is its range of size variation. The pattern of integration and of modules discovered in adults reflects associations that originate during development and that have genetic bases and are heritable. This means that by studying adults we can learn indirectly about development. This opens the field of investigation for paleontology. Anjali Goswami has also studied modularity in mammalian skulls but aiming at the incorporation of fossils so as to examine modularity’s significance to large-scale evolutionary patterns. In a widely cited study, she examined 105 species, eight of them fossil ones. She recorded landmark data in many points of the skull comparable (homologous) among species, such as the boundary between two bones. This three-dimensional data set was then analyzed statistically with tests that reveal which landmarks are significantly correlated with each other and change in unison. Anjali identified six skull modules: an anterior facial, one around the molars, one around the eye socket, one around the lateral side of the skull, one for the skull vault, and one for the base of the skull. Almost all the fossils Anjali examined conformed to this standard pattern of modules, including one saber-toothed species with their very specialized skulls. The extinct sabertoothed cat Smilodon fatalis shows a pattern of cranial integration different from that of any of the other species studied, in that the facial skeleton and the enlarged canines form two separate modules instead of the single anterior oral–nasal group. Why the deviation? Some aspects of the growth pattern of Smilodon are probably coupled with the novel modularity pattern. In Smilodon there is a unique timing of tooth replacement. The deciduous  

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saber erupts at a young age, most likely enabling hunting then— and affecting the pattern of correlation among parts of the skull early in its formation. The other fossil saber-toothed forms have a late appearance of the deciduous saber, resulting in the later preservation of the ancestral pattern of skull integration. Empirical evidence shows that modularity itself, as changing proportions among parts during growth (allometry), evolves. Fossils greatly expand the space of the morphologically possible or confirm the patterns derived from the study of living species alone. As vertebrate paleontologists focus by necessity on just the skeleton, many other aspects of anatomy and thus development, which may behave in a different way, are not considered. Because of modularity, anatomical regions can behave differently and independent from each other. For example, in monkeys and apes, the group of mammals to which we belong, the skeleton is generally similar among all species, whereas the digestive system is extremely variable, including adaptations for foregut and hindgut fermentation.  

Surviving Here and Now: Lost and Replaced Modules Everything in life is a matter of alternatives. It is not about the universal optimum but instead about the local best. A good example of this “principle” is self-amputation. This is the act whereby an animal severs one or more of its own appendages, for it is better to lose a tail or a limb, a module, than to lose your life—especially if you can then regenerate that appendage, as is known for many vertebrate groups except mammals. Salamanders can regenerate even limbs. Lizards, closer to us in the tree  

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of life, can regenerate the tail but are unable to regenerate their limbs. Tails are a module of the organism usually characterized by its larger degree of variation when compared to other portions of the axial region of vertebrates, as E. S. Goodrich already noted in 1913. Depending on the organism involved, tails can be very important for locomotion, fat storage, or defense against predators, among other roles. It costs energy to produce a tail, and when present it surely plays a role in the conditions for existence. But many animals can survive without one. In the case of caudal autotomy, some lizards and salamanders that are captured by the tail will shed part of it and thus be able to flee. The detached tail distracts the predator’s attention from the fleeing animal. In a skink species (Scincella lateralis) individuals that have lost a tail return to the site where they have lost it, and if they find it they ingest it to regain much of the energy lost. Lizards can partially regenerate their tails, whereby the original structure with vertebrae is replaced by a cartilaginous rod. Superficially the tail may also look different, either thinner or thicker or with a different color. The medical community is of course very interested in this phenomenon, given the importance of tissue regeneration for humans having had amputations. In contrast to the amphibian’s ample regeneration abilities, the partial abilities in lizards are a better model, presenting tissue regeneration, in the tail, versus regeneration failure, in the limb. To understand how caudal autotomy works it is helpful to understand how it evolved. Has this capacity evolved just once or many times independently? Which groups have it, and what do they have in common? These questions are still unanswered. Concerning extinct animals, it is very difficult if not impos-

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sible to tell which species were not capable of regenerating an appendage, as negative evidence is no evidence in this case. But the fossil record provides evidence of caudal autotomy. It can be inferred in fossils that preserve a particular kind of caudal fracture plane. Early in development the original embryonic segments, called somites, undergo resegmentation, with one posterior half joining the anterior half of the next segment and so on. The caudal fracture plane occurs at the boundary of the resulting structures of the two embryonic precursors that fuse early in development. As this feature can be identified in fossil tail vertebrae, it has been recorded for a variety of groups, including Permian capthorhinids and other groups of basal reptiles, maybe the marine reptiles called mesosaurs, maybe the prolacertiform Tanystropheus,5 rhynchocephalians and lizards and marine crocodiles from the Jurassic, and a lizard from the Middle Eocene of Germany. Because in regeneration the tail vertebrae are replaced by a cartilaginous rod, until recently we could only guess if regeneration occurred in fossil taxa. Helmut Tischlinger from Bavaria, who for years has specialized in the use of long-wave ultraviolet light to recognize structures in fossils, has been able to discover new aspects of fossils known for a long time, such as soft tissue impressions in the Berlin specimen of Archaeopteryx. Recently, using long-wave ultraviolet light photography that revealed a halo corresponding to the former presence of a tail made exclusively of soft tissues, he discovered that regeneration occurred among some Upper Jurassic squamates from Germany.

Three

Fossilized Vertebrate Ontogenies

Most fossil remains of vertebrates are mineralized portions of the skeleton. As the skeleton is at most only partially formed in embryos and in other juvenile stages, it is not surprising that most fossils are of adults or subadults, which are also larger than other life stages and thus more likely to be found. But fossils of embryos and of young individuals do exist. In a recent survey on reptiles, my colleague Massimo Delfino and I identified hundreds of scientific papers documenting such specimens (www.developmental-palaeontology.net), most of them concerning dinosaurs. Some fossils are interpreted as hatchlings or neonates, but considering the uncertainty surrounding these interpretations, it is best to refer to them as “near birth” or “perinatal” individuals. The identification of a fossil as an embryo is uncontested when found inside a fossil egg. More complicated is the case of viviparous species, that is, those that do not lay eggs but give birth to live young as humans do. Telling a fetus apart from a last meal can be difficult when you are dealing with fossil remains 46

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many millions of years old. A fetus is a small skeleton “inside” a larger one, and this small skeleton does not show signs of damage associated with digestion. The anatomy and size of the smaller skeleton is of course fundamental to determining if this belongs to the same species. Conflicting interpretations are not rare. Establishing the taxonomic identity of embryos and juvenile stages is also a challenge. In some cases the associations are so clear that embryos can be allocated to a particular species with confidence. In other cases assignment to a group is based on some unique feature diagnostic of that clade, but further taxonomic precision is not possible. In many cases specimens first described as representatives of different species turn out to be most likely different stages of the same species. Exceptional fossils of nonadults are snapshots of development, and we can learn the most about growth by having a series of them or being fortunate to find a critical stage, such as one around birth, that has been preserved.

Fossil Hatchlings and Newborns When studying life history around the time of birth, the perinatal period, the alternative strategies of being mature (precocial) versus immature (altricial) are of major importance. This state of development of hatchlings or newborns is correlated with many ecological and behavioral parameters. In the case of mammals, some newborns are very immature, having no hair and closed eyes, such as hamsters after a gestation period of about sixteen days. Others are more mature, born with open eyes, such as guinea pigs after sixty to seventy days of gestation. In newborn guinea pigs and other closely related rodents, teeth are already partially worn due to jaw movements that started in

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utero. Analogous extremes of varying stages of development at birth are seen in birds.1 Altricial birds include penguins, gulls, storks, birds of prey, parrots, hummingbirds, and songbirds and are highly dependent on parental care. Precocial birds are ducks, shorebirds, grouse, hoatzin, and turkeys. Diverse aspects of the anatomy at birth can be compared, such as degree of brain differentiation or some measure of physiological performance. When dealing with fossils, skeletal differentiation is the landmark of choice. Among lizards, hatching geckos are much less ossified than most other species, including legless species, tegus. With exceptional fossils of perinatal stages, paleontologists have the chance to learn much about reproductive strategy and brooding behavior. Dinosaurs have been more intensively studied in this regard than any other group of vertebrates. One example is embryos of one of the first dinosaurs ever to be described. Massospondylus, a prosauropod dinosaur from the early Jurassic, was named in 1854 by Richard Owen, who introduced the term Dinosauria. About 120 years later, eggs of this animal were found in South Africa, and decades later, in 2005, their embryos were described, the oldest dinosaur embryos ever found. Massospondylus belongs to a group most closely related to the later appearing giant sauropod dinosaurs like Diplodocus. Study of their growth pattern is of much interest, these being the largest animals ever to have walked on earth. Tiny skeletons of Massospondylus embryos are exquisitely preserved. The near-hatchlings had no teeth, suggesting they had no way of feeding independently. The four legs of the nearhatchlings were of equal length, indicating they were quadrupedal, whereas the adults are hypothesized to have been facultatively bipedal. The skull and eyes were proportionately oversized when compared to adults, as is common in other very

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young vertebrates, although the skulls of juveniles were taller and narrower. Based on the lack of teeth and other signs of anatomical “immaturity,” Robert Reisz and his collaborators speculated that postnatal care might have been necessary, a kind of behavior also reported for other dinosaurs. More about the life history of Massospondylus is known based on numerous skeletons representing different growth stages. By estimating body size change and absolute age changes using histological techniques, we know that Massospondylus grew at a rate of about 35 kilograms per year and was still growing at around fifteen years of age.2 Nicely preserved embryos in eggs of several other kinds of dinosaurs are also known, documenting a diversity of reproductive strategies. Among them are those of therizinosauroid theropods from the Upper Cretaceous of China. In contrast to the prosauropod Massospondylus, the theropod was very precocial, or mature, at hatching, as it had very advanced ossification in the vertebral column, ribs, pelvis (the hip girdle), and the lower leg, in which the two bones, the tibia and fibula, were already apparently co-ossified. The use of computer tomography (CT) scanning has greatly facilitated the study of eggs containing embryos. This technique allows us to peer inside the egg without breaking it, a handsoff look. My students and I use CT for different kinds of projects, and it is no longer rare in paleontology. One carefully lays the fossil on the platform that slides into the CT scanner, which looks like a giant doughnut with a narrow bed. Humans are normally the subject of investigation, but fossils are easier subjects: they do not move, do not suffer claustrophobia, and do not need to hold their breath while being scanned. A prime example of a CT-based study concerns fossils from the island of Madagascar of the recently extinct elephant

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bird, Aepyornis, an extraordinary animal that reached a height of approximately 4 meters and a body mass of about 400 kilograms. Its eggs exceeded 7 liters in volume, the largest of any fossil or living bird and larger than known sauropod and theropod eggs. Remains of these animals, including eggshells, are known from deposits only a few thousand years old. Elephant birds may have coexisted with Europeans occupying Madagascar in recent centuries. In adults of Aepyornis the bones of the skull are fused. In embryos at the stages usually represented by fossils, the individual bones, as well as the shape and extent of their contacts, can be more easily recognized. This is an important aspect when comparing skulls of different groups to trace morphological evolution. A striking feature of the elephant bird embryo is the robustness of its bones; hatchlings of ostriches and rheas are gracile in comparison. In the elephant bird study, my colleagues were able to reassemble the mess of bones into a reconstruction of the embryonic skull and with that solve questions about the identity of elements of the adult skull. They assessed the degree of skeletal differentiation in a late embryo: To what extent were bony elements mineralized? Were size proportions and spatial relations of bony elements of the adult already present?

Viviparity in Fossil Vertebrates There are a variety of reproductive strategies of vertebrates that have evolved many times in parallel. One example is placentation, in which there is an organ connecting the mother with the developing embryo and facilitating nutrient uptake, gas exchange, and waste elimination. Placentas are not exclusive to

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mammals but rather quite widespread across other major groups of vertebrates, except birds, turtles, and crocodiles. The independent evolution of an apparently singular feature such as placentation is also true for viviparity, the strategy whereby the embryo develops within the female and not in an egg. Ovoviviparity means that the eggs develop and hatch within the mother, also achieving protection and avoidance of reproductive waste. Viviparity evolved several times independently across most vertebrate groups, in lizards and snakes alone some eighty times.3 We and other placental mammals are viviparous, of course, as are all marsupials, the group that includes possums, kangaroos, koalas, and kin. But the platypus and echidna, those living species of a once much larger radiation of mammals distantly related to us, lay eggs. A prerequisite for the evolution of viviparity is a mechanism that enables fertilization to occur inside the body, where the embryo will eventually develop. It has been shown that males of some placoderm fish, the earliest jawed fishes, which lived in Paleozoic times, had clasperlike appendages, reminiscent of similar structures in modern sharks, suggesting they practiced internal fertilization. It is then not too suprising but also rewarding that the oldest record of viviparity, dating back to the late Devonian period, about 380 million years ago, was reported in a placoderm female, preserving a fetus one-third of its adult body size. The key fossil was so well preserved as to exhibit what must have been an umbilical cord with blood vessels, as shown by high resolution computer tomography. These and other extraordinary fossils come from the Gogo Formation in Western Australia.4 Some of the most beautiful fossils clearly documenting viviparity are known for a diverse group of marine reptiles, all highly specialized for swimming, that populated the seas in the

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Figure 13.  The placoderm fish Incisoscutum ritchiei, with clasperlike appendages (arrow) (Ahlberg et al. 2009). Courtesy of John A. Long (Los Angeles).

Mesozoic era.. The evolution of viviparity in these aquatic reptiles has been linked to the loss of the ability to lay eggs on land, parallel to large morphological modifications to secondarily live in water, as seen in whales and manatees, whose ancestors were already viviparous. Ichthyosaurs are among the most highly specialized of all Mesozoic marine reptile groups, and they looked superficially like dolphins. Mosasauroids were also marine reptiles and were probably related to snakes.5 These groups became extinct in the Cretaceous, at the end of which, some 65 million years ago, all dinosaurs except birds also became extinct. Viviparity surely occurred in ichthyosaurs and in mosasaurs where it was directly demonstrated by the presence of fetal remains within the abdominal cavity of the mother. The orientation of the embryos in ichthyosaurs and mosasaurs shows that they were born tail-first, the head emerging last, as happens in extant fully aquatic mammals, the whales and manatees. Embryos of ichthyosaurs are documented for species living in all epochs of the Mesozoic: the Triassic, the Jurassic, and the Cretaceous. Another diverse group of fossil reptiles, including largely aquatic forms, were the sauropterygians, including most promi-

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50 cm

Figure 14.  The pliosaur plesiosaur Peloneustes philarchus from the Upper Jurassic of England, showing a loose connection between the hip bones and vertebral column. Modified from Andrews 1913 and Sander 1994.

nently the long-necked and large-sized plesiosaurs. Evidence of viviparity in this group is mostly indirect, based on their skeletal morphology.6 In particular, the shape of the pelvic girdle is worth considering, as it provides evidence of the width of the birth canal. In sauropterygians, as in ichthyosaurs and mosasaurs, there is no solid connection between the hip bones and the vertebral column. This is most likely an adaptation to swimming, as this kind of construction allows sudden stops or sharp turns. It is speculated that this kind of loose joint also allowed these animals to maximize the space of the birth canal. The physiological requirements for an egg inside instead of outside the uterus are of course very different. Obtaining oxygen to grow while in a fluid or outside in the air is a major difference. It would seem that the evolution of viviparity is a difficult or unlikely evolutionary step. But not only has this reproductive strategy evolved many times independently, even evolutionary reversals are known. A molecular phylogeny of boid snakes suggests that the evolution from viviparity to oviparity must have occurred in the evolution of the Arabian sand boa Eryx jayakari.

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This species also lacks the egg tooth other oviparous snakes use to tear their way out of the egg, additional evidence that egglaying was lost and reacquired. Fossil evidence of this change is not yet known. For all the repeated evolution of viviparity among fossils, most of the few groups of living marine reptiles are oviparous. The living marine or semimarine reptiles are the marine iguana from the Galápagos, the sea turtles, the sixty-two sea snake species, and the penguins (birds are reptiles!). Galápagos iguanas are remarkable lizards that graze algae at the bottom of the cold sea, but they are otherwise largely terrestrial and oviparous. (Many people have seen documentaries of sea turtle mothers using their paddles to move on and off the beach in order to deposit eggs and cover them with sand.) On the other hand, the majority of the sea snakes are viviparous. No evidence has ever been found that viviparity occurred in dinosaurs, and although this reproductive mode cannot be excluded for this group, it seems unlikely to have occurred. Neither extant dinosaurs (birds) nor the living group most closely related to dinosaurs (crocodiles) has any viviparous representatives, not even in their respective fossil records. This provides a major puzzle for evolutionary biologists but seems to be related to the role of the eggshell in providing important minerals to the developing embryo. The puzzling absence of avian viviparity among the approximately 9,300 living species and all the fossil ones so far known cannot be explained by a lack of geological time in which this could have evolved, as the long evolutionary history of birds goes back to the Jurassic, when Archaeopteryx and other specialized theropod dinosaurs lived. Explanations for this absence of viviparity invoke morphological or physiological factors seem-

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Figure 15.  A breathing bird embryo about to hatch from its egg. Drawing by Claudi Joehl.

ingly incompatible with live-bearing reproduction. For example, birds possess highly specialized lungs with small capillaries that need much time to be filled with air after they have been occupied by the amniotic fluid of the egg during development. For that reason, most bird eggs have an air chamber into which the late embryo sticks its beak to start filling its lungs with air. A viviparous strategy would present the hatchling bird with a sudden need for air in the lungs—a physiological challenge apparently unfitted to the hatchling’s anatomy. The universal retention of oviparity in birds must reflect fundamental avian characteristics preventing what happened in many other groups so many times. Such hypothetical factors include flight, an egg with an isolating hard shell that prevents water loss, the mode of sex determination, immunological obstacles, and a special mode of lung development. There are pros and cons for each of these factors.7 The flight factor makes a great deal of sense at first. What mother would want to carry babies while flying? But none of the many and diverse groups of  

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nonflying birds ever evolved viviparity, and pregnant bats are able to fly. Perhaps no single avian feature alone is incompatible with viviparity or with the previous condition in its evolution, that of egg retention. Perhaps it is a cocktail of features that are incompatible. These must include endothermy, egg incubation and parental care, excretion of uric acid as the chief component of nitrogenous waste, primarily altricial hatchlings, and calcareous eggshells. Biologists have mathematically modeled the costs of egg retention, which include decreased frequency of producing offspring, increased maternal mortality, and decreased paternal investment, and concluded that these outweigh the potential benefits for most birds. Perhaps some of these factors also explain the lack of viviparity in dinosaurs, turtles, and crocodiles.8 The extinct ancestors of birds are also known to have laid eggs. Exceptional fossils not only document the eggs but also provide clues on the brooding associated with them.

Eggs, Parental Care, and Brooding Behavior Studies of fossil eggshells have revealed different strategies in the construction of the shell capable of providing security, maintenance of liquid, and gas exchange with the exterior.9 Differing features characterize several groups, and a nomenclatural system of classification, or parataxonomy, of eggs and eggshells has been developed based on histological types of the shell. The presence of embryos in fossil eggs opened the way for at least partially matching the egg parataxonomy with the taxonomy based on skeletal features. Matching of eggs with a particular species can also be done

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via an association of a skeleton with the eggs, providing evidence of brooding or of preying. The classic example of confusion between the two is that of Oviraptor, a dinosaur from the Cretaceous of Mongolia. The fossils were originally found by the celebrated expeditions to the Gobi Desert of the American Museum of Natural History in New York in the 1920s, an account of which is provided in Sean Carroll’s Into the Jungle’ and Mike Novacek’s Dinosaurs of the Flaming Cliffs. In 1923 the skeleton of a toothless dinosaur was found on top of a clutch of broken eggs. Subsequently, Henry Fairfield Osborn, at the time president of the Museum in New York, coined an evocative name for the new animal, Oviraptor philoceratops: ovi means “egg,” raptor “robber,” and philoceratops “fondness for ceratopsian dinosaurs.” The finding of the skull lying directly over the nest was interpreted as a sign of a culprit having been incapacitated by a sandstorm and becoming a fossil while in the very act of robbing an egg nest. Thanks to the new studies of the past two decades by Mark Norrell and colleagues from that same institution, we now know that the associations of Oviraptor adult skeletons with clutches of eggs do not mean that they were raiding them; instead they were laying them, practicing parental care. One kind of parental care is the brooding of eggs in which the parent brings its body into direct contact with the eggs for prolonged periods of time. The classic example is the familiar picture of a parent bird sitting on the eggs: the body over the nest, the hind legs folded beneath, the abdomen contacting the eggs broadly, and the forelimbs folded back along the sides of the body. There is clear evidence that some dinosaurs incubated eggs like birds. When the parent remained with the nest or eggs it most likely defended it actively against conspecifics or predators. In addition to many other dinosaur species we know, Ovi-

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Figure 16.  An articulated partial postcranial skeleton of an oviraptorid dinosaur from the late Cretaceous of Mongolia, preserved overlying a nest. Modified from Clark, Norell, and Chiappe 1999. Image courtesy of the American Museum of Natural History.

raptor took care of its eggs. Brooding influences incubation by raising the temperature of the eggs. Among living reptiles, egg brooding in a nest is known only in boid snakes and is widespread in pythons. Most snakes, when around a nest, are looking for a meal. Direct evidence of this is known from the Cretaceous of western India, where the remains of a nearly complete skeleton of the snake Sanajeh indicus were found coiled around a recently hatched egg in the nest of a sauropod dinosaur. Other snake individuals associated with egg

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clutches at the same fossil site supports the finding that feeding on young dinosaurs occurred. Such fossils are formed under very special circumstances. Apparently in this case the deposition and burial of the fine-grained sediment was unusually rapid, probably mobilized during a storm. There are other kinds of brooding besides that of eggs in a nest. Among vertebrates fish and frogs provide many diverse examples. Brooding in fish and amphibians refers to cases in which the embryos are retained somewhere on or in the body but not in the oviducts. There is a great deal of diversity concerning the location in which the brooding takes place: in the stomach, in dorsal pouches in the back, in vocal sacs, in pouches in the groin, or in the mouth.10 The temnospondyl Trimerorhachis, common in Permian rocks from Texas, most likely provides an example of a special kind of brooding in a fossil land vertebrate. Remains of very small individuals were found in the area of the pharyngeal pouches of an adult, suggesting the animal was brooding when it died and became preserved as a fossil. An alternative interpretation is cannibalistic behavior on its young. But it seems more likely that this predator with sharp teeth and powerful jaws fed on fish and other vertebrates with its mouth, not young of its own species via its gills.11

Mammalian Fossil Embryos Contrary to the celebrated cases of dinosaur and other reptilian embryos in the fossil record, mammalian fossil embryos are very rare, contested, or constitute mainly just a curiosity because of poor preservation. Embryos are rare even in localities known for

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their exquisite preservation of fossil adult mammals. Most mammals have a reproductive strategy in which they deliver altricial, immature young, making the discovery of embryos unlikely. More common are fossils of mammalian fetuses from species that have adopted the precocial young approach: longer gestation, smaller litter size, and greater adult body mass. We will probably never know the gestation length of a fossil species, but we can in many cases know the litter size. Horse embryos from an Eocene German locality suggest that mares carried only one fetus, showing that early horses had evolved the strategy of producing few offspring probably followed by intensive parental care. This is the typical strategy of gregarious ungulates and fits with the hypothesis, based on the high frequency of fossils in some localities, that Eocene horses lived in herds. In one instance a soft tissue structure surrounding the fetus has been interpreted with confidence as a placenta.12 A small litter size has also been documented in other exceptional fossil mammals. The skeleton of an oreodont from the Oligocene of South Dakota, Merycoidodon culbertsoni, an extinct relative of even-toed ungulates (Cetartiodactyla), exhibits in its pelvic region two fragile but fairly complete skulls of what were described as “twins” in the uterus. Younger fossil mammal embryos are known from some Pleistocene extinct giant ground sloths from South America and from mammoths from Siberia. Their not fully formed bones reveal anatomical details that solve questions surrounding the identity of bones that in the adult are too modified as compared with those of other species. In some cases, adult skulls, because of fusion of individual elements or changes in proportions, present unexpected parts when compared with other members of their kin, or they lack an expected element in the anatomy. For

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example, at first sight the adult human skull lacks a premaxillary bone. But, as discovered in the nineteenth century by Goethe, it is the obliteration of a suture that explains the apparent lack of a bone actually present in our skull.

An Embryo or a Last Meal? A rare glimpse into the steps of the life history evolution in a very special kind of mammal was made possible by the discovery of a 47.5-million-year-old early whale from Pakistan, Maia­ cetus inuus. The fossil was found with a smaller individual inside its body cavity. The authors of the study interpreted the smaller specimen as lying in its in vivo position within the uterus of an adult, a pregnant female about to give birth. The head-first delivery position of the alleged fetus is like that of land mammals, indicating that these animals, unlike modern whales, gave birth on land. The well-developed set of teeth in the fetus was interpreted as a sign of altriciality, or relative maturity, at birth, suggesting that Maiacetus newborns were probably active immediately after birth. Like other stem cetaceans, Maiacetus had four legs modified for foot-powered swimming but could probably support its weight on land with flipperlike limbs. But some colleagues with ample experience in cetacean anatomy argued against the case for a Maiacetus fetus: the position of the smaller individual relative to the vertebral series of the older individual is too close to the head of the purported mother, at the level of the stomach, and the absence of its tail vertebrae are more consistent with an interpretation of the smaller individual as a prey item. Whatever the outcome of this discussion, this example shows the importance of examining the fate of the corpse of dead animals as they decay and begin the process of

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fossilization. The field devoted to this kind of study, taphonomy, is becoming prominent in studies of fossil embryos and other important fossils preserving soft tissues.

Rotting Embryos and Petrified Ones Thanks to taphonomic studies we have gained an understanding of how to best interpret anatomical details of critical fossils. By examining patterns of postmortem decomposition we know how anatomical components differing in their chemical properties are lost at different stages of decay. Topographic changes of the structures can also occur that make more challenging the interpretation of seemingly complete fossils. A prominent example of this kind of study concerned the rate and sequence of decomposition for individual features of species of basal vertebrates. The aim of Robert Sansom and Mark Purnell and their colleagues in Leicester was to interpret the anatomy of purported early fossil chordates by examining living analogues after death. In the process of decay, soft-tissue structures tend to decompose, but not all features disappear at the same rate. Although this work did not concern embryos or ontogenetic features, it is mentioned here because it exemplifies the taphonomic approach and also deals with the acquisition of traits in the first, extinct representatives of a lineage, something relevant to understanding the origin of the developmental systems that produce those traits. Sanson and colleagues studied the decomposition in freshly dead amphioxus, Branchiostoma lanceolatum, and in the lamprey, Lampetra fluviatilis. Among the important features to study in the fossils are the eyes, the tail, and the precursor to a spine, known as a notochord. The bodies were left to rot inside clear plastic boxes filled with saltwater

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and incubated at 25 degrees Celsius for up to two hundred days. The researchers recorded the decay process for each anatomical feature and scored the changes according to a simple rating system. The features more resilient to decomposition were those shared by all vertebrates, such as the notochord. In contrast, the features more recently evolved rotted first. This is regrettable, as it is the latter features, which distinguish closely related animals within a lineage, that are most informative for evolutionary tree reconstruction. The study showed that whether a fossil represents a primitive chordate or a decomposed vertebrate can be addressed with careful anatomical and chemical studies. Some of the Cambrian fossils that this taphonomic study aimed at addressing may have been more closely related to vertebrates than previously thought. We will probably never be able to know, given the vagaries of taphonomic biases. Sediments around the world are full of fossils to be discovered, as are hundreds of museum cabinets, and these fossils do not present the interpretive challenge that these Cambrian forms do. Another example of taphonomic studies, this time more germane to the subject of this book, concerns the process of decomposition and taphonomy in tiny embryos. These studies were triggered by discoveries in the past two decades of Cambrian embryos of multicellular animals from China. These fossils are similar in the arrangement of cells and shape to modern marine animal embryos but are tiny and difficult to study. Therefore, even their organic nature can be disputed and indeed has been seriously questioned in some cases. The most informative studies of Cambrian developmental stages of embryos from cleavage to prehatching have involved the use of synchrotron-supported imaging, a technological

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breakthrough that permits the examination of minuscule fossils at the cellular level.13 Rocks are chemically treated in order to dissolve the calcium carbonate surrounding the tiny fossils, composed of calcium phosphate. As these fossils each measure less than half a millimeter in length, this is a laborious task. Considering these limitations and the fact that little has been done to search for such minute, cellular fossils, the taxonomic and phylogenetic coverage of fossil embryos is very limited. In fact, in most cases the kind of animals the different preserved stages represent remains an unsettled question. Some detailed studies have revealed the cleavage mode of some embryos, that is, the pattern in which cells divide to create the aggregation of cells in the first steps of development. But some of the features are difficult to discern as biological or geologic. Taphonomic studies have provided evidence of what embryological stages can be preserved and for how long and under which conditions these mostly Cambrian organisms lived. The pioneering studies were those of Elisabeth Raff and colleagues, who conducted experiments with embryos and larvae of sea urchins, a group of organisms preferred by developmental biologists because much is known about their early ontogeny. Raff and colleagues discovered that preservation of embryos was largely not size-biased and that mineralization of detailed structures, which could then be studied, was feasible in many circumstances. Some chemical conditions were more prone to lead to the preservation of accurate cellular anatomy than others. Some stages had negligible preservation potential. Similar experiments are currently being conducted on different species, but much more needs to be done before a strict or common protocol for the interpretation of tiny, complex organic structures from the distant past can be developed. Considering the developmental and taxonomic diversity

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that must have existed and the vagaries of geologic preservation, a universal method may be intractable. But at least the experimental approach with living species will inform and thus enable us to be more critical about what we can achieve with new imaging tools and a better understanding of fossilization.

F ou r

Bones and Teeth under the Microscope

As unlikely as it may seem, the most important piece of equipment for most paleontologists, besides the hammer, is the microscope. A large proportion of people studying extinct biodiversity work for the oil industry, examining the very small pollen of fossil plants or extinct foraminifera, the latter members of a group of single-celled organisms important for stratigraphic correlation between geologic sections. For paleontologists, the microscope enables also the study of the tissue microstructure of fossils, in particular the bone, which has become an important matter of investigation concerning development in extinct taxa. The study of living tissues, or histology, is a vast field, and much of it is concerned with the identification of pathologies, an important diagnostic procedure in studies of cancer for example. Comparative studies of tissues of different organisms have been a subject of investigation for centuries, made possible by technological advances in performing thin sections of delicate and often small complex structures of different consistencies and shapes. Pioneering work on tissues at a microscopic level 66

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goes back to the Swiss Wilhelm His (1831–1904), a native of Basel. His invented the microtome, a mechanical device consisting of a cleverly disposed blade used to slice thin tissue sections for microscopic examination. With this new technological development, he was able to trace the embryonic origins of different types of animal tissue. As far as I know, His did not study the microstructure of fossil bones; rather, he was concerned with embryos and soft tissues, for instance, making discoveries that led him to coin the term dendrites, the conducting projections of nerve cells. Histological sections using basically the same method that His used some 150 years ago are currently used in the study of embryos of living species that, by virtue of their size, are difficult to study by dissection.1 From quite early on, paleontologists realized that thin sections could reveal important anatomical details of fossils. The British specialist in fossil fish, William Johnson Sollas (1849– 1936), a professor of geology at Oxford, and his daughter, Igerna, pioneered this study when in 1903 they published an account on a Devonian fish of uncertain affinity. Their technical breakthrough consisted of sequentially grinding through a specimen, making drawings of the revealed sections, and translating these into a wax model, larger than the original. Sollas had initially made models of fossil brittlestars (ophiuroids) and graptolites, a group of extinct invertebrates related to acorn worms, which were exhibited at the British Association in 1901.2 Sollas made models of many fossils, but few appear to have survived Sollas’s method was later masterfully used by a school of Swedish comparative anatomists. But wax models are extremely time-consuming to produce. For example, a famous wax model of the head of an important animal for the fish/land vertebrate transition Eusthenopteron took fifteen years of two technicians’ time to  

 

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produce. A digital camera and the right hardware and software can now do the same job in days. This is technical progress on a grand scale. The next major technological advance was presented in a 1970 paper by the Frenchmen Cécile Poplin and Armand J. de Ricqlès, who invented microtome slicing for fossils. They were searching for a technique to slice fossils into sections that could be mounted onto glass, as done with standard histological methods. This was no trivial challenge, as in fossils the hard tissue is porous, breakable, brittle, more heterogeneous in composition, and less resilient to strain than extant bone. With the impregnation of resin under vacuum and pressure into the fossil bone, each slice becomes more stable. The chemistry of fossil bone is also different from that of extant taxa. The resulting sections preserve the outlines of the different structures in the fossil. Hence, even if the chemistry has changed or the original components have been replaced, the boundaries between them are preserved. This microtome technique was the first step toward replacing the serial grinding method, which sacrifices the original fossil. The newest technique for visualizing the internal structure of a fossil does not require sectioning. With powerful highresolution computer tomography, it is possible to study details of microanatomy without even cutting a fossil.

Informative Fossil Bone Sections The reason the histology of fossil bone is rich in information is that bone is a living tissue that experiences much successive resorption and reconstruction. We benefit from this fact after we have an accident in which we break a bone; we suffer from it in old age due to osteoporosis. For paleontologists, bone change

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during life means that it is possible to see much of a record of a vertebrate’s life. The key is to sort out the effect of the primary bone accretion and secondary remodeling processes on the record of growth. The most undisturbed growth record of a vertebrate skeleton is usually found in the midshaft region of long bones, such as those in the arm (humerus) or the leg (femur). Before sectioning, the bones are embedded in synthetic resin, which are then ground and polished to reach an appropriate thickness, usually 0.6–0.8 centimeter. These sections are then studied under different lighting and filtering conditions under the microscope. Isolated scraps of bones are usually the subject of study of palaeohistologists, as museum curators usually dislike the invasive kind of study involved in thin sectioning of fossils. This leads to the problem that often the exact anatomical or taxonomic provenance of a specimen is not known with certainty. In spite of this difficulty, the number of new finds made by the examination of fossil thin sections is increasing exponentially. My introduction to paleohistology came via a younger colleague who worked in my lab shortly after my arrival at the University of Zürich, Torsten Scheyer, and his former Ph.D. advisor Martin Sander from Bonn, a world leader in the field. I had attended a talk by Sander in Tübingen about sauropods, the largest dinosaurs, in which he showed how paleohistology could provide major insights into the growth patterns and bone construction in these animals. It occurred to me that this approach could be used to examine Stupendemys geographicus, the largest turtle that ever existed, a member of a Gondwanan group we had collected during my field project in Venezuela. Sander directed me to Scheyer, and we studied Stupendemys and other animals, mainly mammals and marine reptiles, as I describe below.  

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The shell of Stupendemys is among the thickest and largest turtle shells known, with one specimen reaching 3.3 meters in length. Histologically it shows a well-developed sandwichlike structure, with the outer layers comprising compact bone resisting tension, surrounding a meshwork of interior cancellous bone. This kind of structure was important for minimizing shell weight while retaining stability during growth. The record of growth marks was incomplete due to the weathering that the specimens we studied undoubtedly experienced and which characterizes the fossil site of Urumaco in Venezuela.3 However, the kind of tissue and the thickness between growth marks are comparable to those of living turtles with a “normal,” slow mode of growth. Assuming a rate of growth similar to that of most living sea turtles of comparable histological characteristics, the specimen we studied must have grown about 60 to 110 years to reach the giant carapace length. The tissue organization seen in living animals serves as a reference to understand the histological patterns observable in fossil bones. The osteoblasts are the bone-producing cells. There are spaces called lacunae, which are connected to each other via canaliculi, responsible for distributing nutrients and oxygen. These and other basic structures of bone can be observed in fossils. The osteoblasts and osteocytes, the blood vessels or vascular canals, and the collagen fibers are in most cases destroyed during fossilization, but their position and shape can be perfectly recorded.4 Several studies of living vertebrates have determined that bone tissues have different features in animals that grow fast as compared to those that grow slowly. Rapid growth is coupled with bone tissue rich in blood vessels, meaning an increased supply of oxygen and nutrients to the bone. Slow growth is correlated with less vascular bone, often interrupted by concentric

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Figure 17.  Thin section of a carapace fragment of Stupendemys geographicus from the late Miocene Urumaco Formation, Venezuela. The specimen is in the collection of the Universidad Francisco de Miranda in Coro (UNEFM–CIAPP–2002–01).

lines similar to growth rings of a tree. This discovery—that the rate of growth influences the type of tissue deposited—was published by Rodolfo Amprino of the University of Turin in 1947 and is now known as Amprino’s rule. The study of bone histology was continued after Amprino’s paper, and paleontologists followed his ideas when trying to reconstruct aspects of the physiology and life history in fossil species. In bone microstructure there are also traces that reveal information about life span, age, and maturity, the subjects of study of skeletochronology. The age estimation comes from the identification of growth marks such as annuli resulting from a decrease in growth and lines of arrested growth (LAGs) between zones of faster bone growth. In most cases one growth slowdown (annu 

 

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simple vascular canal

trabecular bone

vascular canal

primary osteons

woven bone Lamellar bone tissue

Fibro-lamellar bone tissue

Figure 18.  Schematic representation of two basic kinds bone histology. These are usually recorded for ectothermic “reptiles” (left) and endothermic birds and mammals (right). Modified from Chiappe 2007.

lus) or growth stop is deposited every year, either during a colder or drier season, affecting the nutrition and physiology of the animal, coupled with variables such as disease and reproductive cyclicity. Due to these events in the individual’s life, we know that the deposition of growth marks can be irregular. A typical deviation pattern is the existence of a short growth period between the annulus and the LAG or when two annuli (plus one LAG) are deposited in one growth cycle. In addition to minimum age, sexual maturity can be estimated from bone microstructure. A decrease in the width of the zones of fast growth and usually a change in the kind of bone tissue that is deposited can mean that sexual maturity has been reached. In the best cases, growth series can be studied, and data from different skeletal elements as opposed to just one are much better for confidently inferring the growth patterns of extinct vertebrates. The growth cycles are counted in each bone to estimate the mini-

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mum age of the animal; the size of the growth rings is analyzed to deduce the age of sexual maturity. When resorption of the bony tissue is observed in different bones of the same individual, the bone with the minimum amount of resorption and maximum number of growth cycles is used to estimate the minimum age of the individual. The breaking down and remodeling of bone is promoted by cells called osteoclasts.5 This is an intensive, energy-demanding process; therefore, bone development is tightly linked to metabolism. This is of direct interest to humans: the most recent molecular medicine studies have revealed that obesity, diabetes, and osteoporosis are all interconnected conditions.6 Experiments with laboratory mice have been important in this context. Much of what we know about the way bone grows and changes is derived primarily from reference studies that examine the bones of individual animals for which researchers know the gender, life history, living conditions, and diet. In many species of vertebrates, for example, pregnancy can lead to extensive remodeling of bone tissues.7 This has been documented for many species of reptiles, such as turtles and crocodiles. Depending on the group, some bones and not others are the source of calcium. The fibula, the thinner of the two long bones we humans also possess in the lower leg, is one of them. Osteoderms of egg-laying females function in some crocodylian species as calcium storage during oogenesis. This strategy probably characterized at least some fossil reptiles, so as a rule it is not optimal to use osteoderms for skeletochronology because remodeling occurs in them. In the case of turtles, one would think of the shell as an excellent reservoir, but so far the species studied do not show females’ use of this source. Perhaps the shell is just too important to the biomechanical integrity of the animal. Females instead use long

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bones such as the femur. This phenomenon during oogenesis is analogous to what happens in humans during pregnancy and lactation, periods characterized by the decrease of bone mineral density in females. Birds produce hard eggshells, consisting of more than 90 percent calcium carbonate crystals. In birds a special kind of ephemeral bony tissue forms before ovulation in the marrow cavities, as a calcium source to enable the mother to produce the eggshell. This type of bone is called medullary bone, and it has now been described for Tyrannosaurus rex and for other species representing the major groups of dinosaurs. This discovery has been important not only to establish the origin of birds among dinosaurs but also and more important to reconstruct with more accuracy the growth curves of many dinosaur species using a reliable marker for reproductive maturity. This coincided in dinosaurs with a transition from a phase of growth acceleration to deceleration.

Dinosaur Growth Patterns and the Origin of Birds We know a great deal about the ontogeny of bone tissues in dinosaurs and much less about that in mammal species. A major issue associated with paleohistological studies has been whether dinosaurs, in a physiological sense, more closely resembled ectothermic reptiles or endothermic birds and mammals. In the 1960s and 1970s Armand de Ricqlès and his colleagues in Paris found out that dinosaur bone is not typical reptilian bone but instead is well vascularized, like the bone of birds and mammals. Generally, this suggested that dinosaurs grew quickly and that growth was supported by a high basal metabolism. These

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discoveries contributed to changing the paradigm of dinosaurs from that of slow, dull, cold-blooded giants to colorful, dynamic, and hot-blooded creatures. However, several studies have shown that rapid growth cannot be correlated simply with endothermy or warm-bloodedness, so there has been no simple answer to the question of endothermy versus ectothermy. Instead, a rich and diverse pattern of unique growth and physiology for dinosaurs has emerged. There are many kinds of dinosaurs, and they lived over a long period, about 160 million years, and attained maximum adult sizes ranging from about 1 kilogram to 75 tons. Some dinosaurs survived and evolved into birds, and that is another major transition. De Ricqlès, Jacques Castanet, Jack Horner, and other colleagues across the world improved the sampling of different bones and comparisons with living analogues and also developed a skeletochronological method that has provided information about rates of growth. Kevin Padian and his colleagues have reported that in many dinosaur species there are different kinds of bone in the cortex, reflecting changes in growth rate; it appears that in late life growth slows down or even ceases. We know that even if the growth strategies of dinosaurs varied greatly, these animals grew at rates substantially faster than extant nonavian reptiles. Even the largest dinosaurs reached adult size in less than three decades. The long bones of large dinosaurs and pterosaurs are in most cases composed of well-vascularized fibrolamellar bone, reflecting rapid growth rates. This kind of bone tissue is seen in cows, horses, elk, and other large mammals, as well as in large birds. But early birds and many dinosaurs do not always have this kind of bone, and if they do, it is not necessarily in the entire cortex. Much paleohistological work has been done on sauro-

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pod dinosaurs. 8 A special interest in these animals is justified, as they were the largest terrestrial animals. The histological record of arm and leg bones has been used by Martin Sander and his students in Bonn to study metabolic rates and to examine if large sizes were achieved by an increase in growth rate or by an extension of growth. The large Jurassic forms, potentially endothermic, apparently grew fast, certainly faster than the earliest species of sauropods. Mamenchisaurus, a late Jurassic sauropod of China, grew at a maximum average rate of 2 tons each year, a remarkable metabolic accomplishment. Some species show developmental plasticity, and indeed different ontogenetic “stages” can be recognized based on different kinds of bone histology within a species. Using only living reptiles, with their lower metabolic rate, as reference, one estimates that it must have taken up to 120 years for the enormous Jurassic sauropod Apatosaurus to grow to its full, huge size. But by studying bone histology, we know that Apatosaurus must have reached its full size in as few as ten to twelve years, a pattern more similar to that of endothermic birds and mammals. Other kinds of dinosaurs have also been subject of paleohistological study, including of course the charismatic theropods, the group to which not only Tyrannosaurus rex belongs, but also birds. There is great interest in determining when and how the endothermic mode of growth of the birds originated. Tyrannosaurus had an adult body mass of approximately 5 tons and a maximum growth rate of 2.1 kilograms per day.9 In mass and growth rate T. rex was similar to the living African elephant. T. rex lived up to twenty-eight years and reached skeletal maturity in approximately two decades. As in other terrestrial theropods but unlike modern birds, the sexual maturity of T. rex

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occurred well before the animals had grown to their full size. As in giant sauropods, T. rex attained its huge size primarily through acceleration of growth rate when compared to its ancestors. The reductions in body size in the evolutionary transition from nonavian theropod dinosaurs to birds are documented by numerous, fairly complete fossils. By studying paleohistology, Kevin Padian and colleagues aimed at understanding the changes in the growth process underlying this size change. They concluded that the reduction of size coupled with the origin of birds involved a truncation of the rapid growth phase of the ancestors.

The Bones of the Moas Other reptiles and birds have been the subject of paleohistological investigation, especially those exhibiting extreme adaptations. Based on these, we know that prolongation of growth was the mechanism involved in the evolution of two very large, spectacular forms: the giant North American crocodylymorph Deinosuchus, from the late Cretaceous of North America, and Varanus (Megalania) priscus, from the Pleistocene of Australia, twice the size of its close relative, the Komodo dragon. Many animals living on islands present singular life history adaptations that may be elucidated by paleohistological study, among them the moa. Moas were flightless and herbivorous birds endemic to New Zealand. Of the eleven species in six genera, the two largest species, Dinornis robustus and D. novaezealandiae, reached almost 4 meters in height with neck outstretched and weighed about 230 kilograms. The moas are ratite birds, which include the African ostrich, the Australian emu, the New Zealand kiwi, and the South American rhea. Most likely affected by hunting by the Maori, moas are thought to have become extinct by 1500

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c.e. Moas exhibited an extreme “K-strategy,” meaning a long gestation and few offspring—accompanied by a long period of growth and late attainment of sexual maturity—contrary to other groups of birds, including other ratites. By studying the paleohistology of several long bones, Samuel Turvey and colleagues documented in four of six genera of moas several annual growth pauses, or lines of arrested growth, revealing that in those individuals the final adult size was achieved only after many years of discontinuous growth. But in the giant moa forms in which the females weighed over 200 kilograms and the males up to 85 kilograms, there occurs a different bone histology from that common for the other, smaller species. In the giant form growth was accelerated: the outer layers of bone are rich in blood vessels and show few if any LAGs. The Dinornis species grew within three years, whereas the smallest moa species such as those of the genus Euryapteryx did not attain adult size until nine years. The slow growth and the late attainment of sexual maturity evolved in an environment free from predators and perhaps short on resources or competition, although this is just speculation. The arrival of humans, as in other similar sad cases, soon led to the extinction of these animals whose life history was unsuitable to resist intensive predation. In current times, the kakapo in New Zealand, the world’s only flightless parrot, may be also doomed—as a result of habitat destruction and other human-caused pressures.10  

 

 

Bone Development and Locomotion in Extinct Species and in Galápagos Iguanas Every morning on the way to my office, I have the pleasure to pass by our museum exhibits, which show growth series or adults

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of complete skeletons of ichthyosaurs, placodonts, pachypleurosaurs, and plesiosaurs. These fossils are beautiful, and although they have been far from my original taxonomic expertise I have developed an interest in them. We have excellent collections of Triassic marine reptiles from the Monte San Giorgio locality of Ticino, the Italian-speaking region of southern Switzerland.11 Among the ichthyosaurs are the oldest records of viviparity in that group. The other marine reptiles belong to a clade that shows different degrees of commitment to aquatic life. Plesio­ saurs were probably viviparous and totally restricted to life in water, whereas some placodonts were at most semiaquatic. The pachypleurosaurs from Monte San Giorgio include different species that vary in their aquatic lifestyle. “Pachys” (as they are informally known) look very elegant. The head and overall body are elongated and the limbs usually preserved in the way they most likely position them during locomotion, namely, close to the body. They were most likely fish and squid eaters. Based on their shape and their bone articulations, it is obvious that they propelled themselves with undulating movements whereby the tail must have played an important role. Bone microstructure is also important for understanding the locomotion in these animals; weight and balast must play a fundamental role. Bones in pachypleurosaurs were heavy because they were compact, which served to counteract lung buoyancy and thus facilitate diving and foraging underwater. In fact, the German common name of the group is Dickrippensaurier, meaning “thick-ribbed lizard,” as does the name “pachypleurosaur,” which can also be translated as “thick pleurosaur,” or “thick- sided lizard.” A question that is of great interest is how the bones of these animals developed. Jasmina Hugi in my lab has investigated this topic by examining the histology of growth series of four species of pachypleuro­

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saurs. Jasmina found that there is a continuous mineralization of the bones after hatching, driven by three processes: 1. The calcified cartilaginous core is never entirely resorbed, so little or no medullary cavity is formed at any time. 2. Bone deposition starts simultaneously at different localities within the cartilaginous core. 3. The bone cortex grows in thickness due to continuous accretion, with minor or no resorption of the inner layer of bone forming around the main shaft, the periost. How do pachys compare to living analogues? Studies of living species are always important for interpreting fossil data. There are no living representatives of pachypleurosaurs, but their closest relatives are the group to which lizards and snakes belong to. The kind of gradual body elongation and limb reduction in the fossils has occurred many times in the evolution of lizards. Many examples of this can be found in skinks (Scincidae), the most diverse group of lizards, with about twelve hundred species, half of them viviparous. Skinks are terrestrial, but many forms that have partly or greatly reduced limbs are fossorial and live in sandy habitats where they perform a kind of locomotion that resembles swimming. This is why in my lab we investigated the skeletal development of different skink species and compared them with those of pachypleurosaurs. But we also wanted to see how bone growth in a living reptile is influenced by life in water. The only living lizard that regularly swims and forages in water is the Galápagos marine iguana, Amblyrhynchus cristatus. Among the close relatives of Amblyrhynchus are several species of terrestrial iguanas to which comparisons can be made, including the terrestrial Galápagos iguana, Conolophus subcristatus.

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Jasmina Hugi studied the Galápagos and other iguanas for her doctoral thesis in Zürich, after we managed to convince several museum curators across the world to lend us limb bones of these animals to cut. Because iguanas, like most metazoan animals, are bilateral, invasively studying one side leaves the other intact. I always remind museum curators of this fact when asking them for permission. We only take a small probe in the midshaft of the limb bones for our studies. The bones of these iguanas told us much about adaptation and the evolution of growth. The marine iguana is unique among living lizards in its bone compactness and life history. Completely terrestrial lizards show a balance of bone accretion and resorption processes, which allows the bone to grow without losing stability or strength. In the marine iguana we documented a slower growth process, by which the bones develop a higher density. A further increase in bone density is obtained by the remodeling processes, which substitute a woven fibered bone from the first years of life with denser lamellar bone later on. The marine iguana has a bone histology exhibiting high and constant accretion rates, which reflects relatively high metabolic rates compared to other iguanas. Skeletochronology, based on the counting of growth marks and growth cycles in between, provides estimates of the age at sexual maturity and the minimum age at time of death. The skeletochronological data of iguanas were congruent with the information on life history from field studies. Like other large iguanas, the marine iguana reaches sexual maturity rather late in life; females reach sexual maturity at the age of three to five years, whereas males are sexually mature at six to eight years. The bones, with their lines of arrested growth, revealed the expected pattern. It was reassuring to see the correspondence between the data from bones and the field data from ecologists.

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Figure 19.  Microstructure of the long bones of an adult male marine iguana, Amblyrhynchus cristatus (specimen from the Naturkunde Museum in Berlin, NKMB 30260). A: Diaphyseal transverse sections of the radius, showing the avascular and thick cortex. B: A group of marine iguanas basking on the shore (photo by Ursina Koller). C: Detailed section of the radius in normal transmitted light. Annual lines of arrested growth (LAGs) are marked by white arrows, whereas subannual LAGs are marked by gray arrows. D: Detailed section in polarized light. The distinct light and extinction pattern of the growth cycles is visible (dark and light gray zones). Figure courtesy of Jasmina Hugi.

We found a fundamental difference between the marine iguana and the pachypleurosaurs. In the iguana a medullary cavity is formed, and ballast is achieved by additional (periosteal) layers of ossification. In contrast, pachypleurosaurs lack a medullary cavity, and high bone compactness develops additionally a mineralized

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Figure 20.  Section of the humerus showing bone compactness and growth lines in an adult pachypleurosar, Neusticosaurus pusillus, from the Triassic of Monte San Giorgio, Switzerland (Palaeontological Institute and Museum, University of Zürich, T4178). Photo by K. Waskow, in normal transmitted light. The specimen shows six lines of arrested growth (white and gray arrows). The sexual maturity is estimated at age three to four years due to the abrupt decline in thickness of growth cycle four (single gray arrow). The two outermost LAGs are closely spaced. The medullary region is entirely filled with calcified cartilage, which is partly remodeling. Figure courtesy of Jasmina Hugi.

cartilaginous center. This comparison of the living animals with the fossils is another example of variation in developmental mechanisms, whereby this may be the result of different degrees of adaptation to the aquatic environment and different “starting points” (different conditions in the respective ancestors) in evolution.

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Bones, Cells, and Genes As unlikely as it may seem, paleohistological data can indirectly generate information about the genome of extinct vertebrates. This is because there is a strong correlation in living species between cell size and genome size. Cell size can be quantified in paleohistological thin sections of bone by measuring osteocyte lacunae, the space in life occupied by cells that were responsible for bone formation. Such estimations have been conducted on dozens of dinosaur species, in pterosaurs, and in a few other extinct saurians and Paleozoic land vertebrates. The relevance of these estimates is limited, as mere size is a very simplistic aspect of the genome but nevertheless of importance when making broad comparisons among groups. Genome size is reportedly correlated with metabolic rate in tetrapods, the muscular-limbed, near-shore or land-dwelling vertebrates. Smaller cells are more energy-efficient and permit a higher metabolic rate, which in turn is tied to homeothermy. These relationships need to be examined more thoroughly for the living relatives of the group of interest as reference, and much more about the significance of genome size needs to be understood before the full potential of paleohistology in this area is established. The relation between genome size evolution and morphological diversification is far from simple, and even gene duplications alone, once thought to be tightly correlated with morphological diversification, have no straightforward relation to overall complexity. Gene duplications are the doubling of a portion of the genome, producing additional copies of existing genes, whereby the new copies have potentials to gain new functions.12

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The Nature of Teeth Georges Cuvier boasted he could reconstruct a whole mammal with just one tooth. An exaggeration, but probably any mammalian paleontologist, if given a choice, would rather take a tooth to gain information from an extinct species than any other part of the body. Teeth are a feature of vertebrate animals that because of their high mineral content are more commonly preserved as fossils than the rest of the skeleton. Enamel is indeed the hardest substance in the mammalian body. This is so because enamel contains hydroxyapatite in larger quantities per unit of volume than bone. A series of fossils document changes in skeletal tissues at the earliest point in vertebrate evolutionary history. The origin of teeth is somewhat controversial for several reasons. One is that the evolutionary tree of the animals involved, some of the most basal vertebrates, is still unsettled, thus resulting in alternative reconstructions of the sequence of events. In fact, some authors have argued that teeth probably evolved more than once after revisions of the anatomy and the relationships of placoderms, armored jawed fishes that were very diverse in the Devonian.13 Before settling this matter, a more fundamental question needs to be addressed: what exactly is a tooth? Not surprisingly, the deeper we go into the origin of vertebrates, the blurrier the definitions become. This is because not all features, for example, the location of the teeth in the skull and the tissues involved, appeared simultaneously or in the form recorded in the living species so far studied. There is no clear pattern of distribution of dental tissues among early vertebrates. Conodonts likely possessed enamel (a not fully resolved issue), but other jawless ver-

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tebrates possessed a tissue called enameloid.14 Enameloid must have been present in the last common ancestor of jawed vertebrates, and this and other dental tissues appeared and became more complex during their evolution. Another matter is that the criteria to define teeth may be developmental or genetic or both, and these can only be inferred in fossils. Moya Smith and colleagues made an important discovery about the timing and place of expression of the gene sonic hedgehog, famous among other reasons for being a key regulator of tooth induction. Their studies of this gene in the catshark revealed that, as in mice, the expression sites correspond in time and space with the timing and position of tooth and cusp formation. The fact that there is a shared pattern in these distantly related species suggests that the last common ancestor of living jawed vertebrates had this developmental gene pattern. But things are complicated. As Jukka Jernvall and collaborators have shown, teeth are polygenic, that is, multiple gene mutations affect tooth shape. This is particularly true for mammals as exemplified by mice, the classic model of study in this regard, with over thirty gene mutations involved. The genetic mechanisms are not simple, and some differences must exist among species. These factors are impossible to study directly in fossils. A typical vertebrate tooth consists of tissues that originate from different layers or cells of the early embryo.15 Two tissues are fundamental: enamel, which originates from the ectoderm, the outermost layer of the embryo; and dentine, which derives from neural crest. Neural crest cells form in the early embryo aggregating in the dorsal midline of the neural tube in an anterior-to-posterior sequence, and from there they migrate to form many kinds of tissues, including the dentine of teeth. Tooth development starts from the interaction, folding, and differen-

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tiation of two layers in the skin, as is also the case with scales, hair, and feathers. Some aspects of the developmental anatomy of these structures are homologous by virtue of sharing some developmental and genetic patterns. These patterns must have been present in an animal that was the last common ancestor of species that possess teeth and integumentary specializations, including scales, feathers, and hairs. Teeth and Life History Fossil teeth can provide some clues to the timing of life history events in an individual. It is no accident that teeth are the preferred objects in the study of ontogeny. Tooth cusp morphology develops from the tip downward, in a kind of accretionary growth reminiscent of that of mollusc shells or the horns of ruminants (the group of even-toed ungulates that includes cows, giraffes, and deer). Dental eruption schedules are also correlated with life history events, as I discuss in chapter 8 in relation to our human ancestors. Mammalian teeth have been a rich subject of life history studies. In the late 1960s the use of layers in tooth cement and dentine to estimate age started to receive attention. These layers are deposited in regular cycles, and those related to long-term, yearly seasons can be counted to give absolute ages of individuals. Layers in the dentine and cement are visible under standard microscopy using simple histological techniques. Differences in metabolic rate, determined in part by environmental seasonality, cause the periodicity of layer deposition. Dental marks are usually in the form of thick layers deposited during a season of comparatively rapid growth (“summer”) and one of little growth and consequently thinner bands. Cement and dentine are sel-

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Figure 21.  Dental replacement (arrow) in the fossil rhinoceros Brachypotherium brachypus, from the Middle Miocene of Oerlikon, Kanton Zürich, Switzerland. Photo courtesy of the Palaeontological Museum of the University of Zürich.

dom subject to remodeling or resorption and for that reason can in many circumstances be better skeletochronological tools than bones, which are subject to considerable change and obliteration during growth.16 Numerous examples of life history studies of fossil mammals exist, some of extinct species that coexisted with humans in the not so distant past, such as mammoths and giant deer. The tusks of mastodons and mammoths, made of dentine, are built of laminated structures that like other teeth grew incrementally. Their analyses can thus provide information on age, growth rates, age at sexual maturity of individual animals, and mortality profiles for populations. This kind of work has been conducted by Dan Fisher, who has also studied the paleoenvironmental context

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using stable isotope analyses of the tusks. Information on temperature and diet at different times of the animal’s life can be gained with these methods. In a recent study the examination of dental histology of the (sadly extinct) giant deer Megaloceros established that the age at death for several individuals in a population from Ireland was eight to fourteen years. This is similar to the average age at death of most other deer species. The large size of Megaloceros, especially its large antlers, as well as its unusual degree of skull compactness, would have suggested a long life for these animals correlated with an expected prolongation of growth in comparison to their ancestors. The age estimates provided by dental studies contradict this prediction. Once again, a mosaic of speeds and patterns in the developmental evolution of the parts of an animal makes the comparative study of life history more complex and interesting.17 Tooth Wear The morphology of teeth can change radically during an individual’s lifetime, in some cases until the disappearance of cusps and the exposure of dental tissues originally covered by enamel when the individual was younger. Degree of wear can be used to determine relative age in fossils, but this approach has many disadvantages, including the variation in rates and patterns of tooth wear even within populations as well as regionally.18 There are two sources of tooth wear: abrasion, produced by food or particles that accompany it; and attrition, produced by contact between teeth. In the case of vertebrates with multiple tooth generations, simple replacement is an obvious strategy for coping with wear.

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Figure 22.  The lower tooth row in three individuals of Dremotherium feignouxi, an antlerless ruminant, from the locality of Montaigu-leBlin (Allier Basin, central France), of early Miocene age. Notice the significant changes in the shape of teeth due to wear during life. Photos courtesy of Loïc Costeur (Basel).

But mammals, characterized by a maximum of two tooth generations, evolved alternative strategies. Herbivores especially are exposed to abrasives, and tooth longevity is crucial to coping with wear. For that, the strategies of having taller and even evergrowing teeth have evolved numerous times in different groups. The study of wear patterns has a long tradition in mammalian paleontology and has been conducted to address life history and functional questions. Even some of the earliest mammals, such as Haldanodon exspectatus from the late Jurassic of Portugal, have been examined in this regard and shown to have had an abrasive diet. A singular example of an adaptation to counterbalance tooth wear has been recorded in Hyaenodon, a creodont mammal that lived for a long period of the Cenozoic and had a wide distribution over several continents. Hyaenodon was car-

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nivorous and possessed a shearing dentition in which the upper and lower carnassial teeth had to contact each other tightly to produce the cutting action. To preserve that tight fitting of teeth in spite of wear, a medial rotation of the upper teeth occurred. This took place to a great degree: the upper teeth in the oldest individuals are rotated almost ninety degrees, and the enamel crown is entirely worn off. This specialization must have helped to prolong the average life span of Hyaenodon.19 A few fossil species of some carnivorous placentals and marsupials also exhibit this specialization.

Five

Proportions, Growth, and Taxonomy

At the time when little anatomical research of microscopic structures had been done, many people thought that eggs contained fully formed, very small individuals—or homunculi—a theory known as preformism (figure 23). Analogous “animalcules” were assumed for other species. This idea seems ridiculous to us now, but at the time there were no microscopes and evolutionary transformations among organisms were not understood. What is really remarkable, and makes much less sense without a modern acquaintance with biology, is how an egg cell and a spermatozoid can collectively represent the information and capacity to survive and develop into a whole organism. We now know that early ontogeny of complex organisms involves simple cells dividing over and over again, eventually developing into a recognizable organism. It is a magnificent scientific achievement to have discovered this process and the mechanisms behind it at different levels of organization. Usually two aspects of ontogeny, from conception to death, are treated separately: development and growth. Development  

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Figure 23.  The “Homunculus,” as illustrated by Nicolas Hartsoekers (1694); the embryo is in the spermium already preformed. Drawing by Madeleine Geiger.

concerns cell differentiation and the formation of the basic body pattern, with fundamental structural changes and the first appearance of major features. It starts with conception and ends approximately with the formation of major body tissues. Growth is the later phase of ontogeny during which size increases. This phase builds on the embryonic pattern that has already been laid out during development. Because of the preservational bias of fossilization, most of what paleontology can say about ontogeny concerns growth. Indirectly, it can say much more, as I discuss in later chapters. Growth, in fossils and in living forms, involves changes in size and shape. A major area of research has dealt with grasping the mathematical laws that govern these changes. One of the earliest approaches to accomplish this was presented by the muchadmired scholar D’Arcy Thompson (1860–1948), a professor of zoology at Scotland’s University of St. Andrews. He was also an expert on mathematics and Greek who, among other accomplishments, prepared the standard translation of Aristotle’s Historia animalium. Thompson described his approach in his book On Growth and Form, first published in 1917. He presented transformation grids that were able to synthesize complex form differences in simple geometric terms. A previous and simpler version  

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Figure 24.  Shoulder girdle of the plesiosaur Cryptocleidus, in young (a) and adult (b) stages. From D’Arcy Thompson’s On Growth and Form (1917).

of these, concerning the differences in the proportions of the human face, can be found in the writings of Albrecht Dürer. Several examples that Thompson used in his transformation grid analyses involved fossils, including a series of fossil horse genera, Archeopteryx, extinct rhinoceroses, and the shoulder girdle of a plesiosaur in a juvenile and an adult. The geometric approach of Thompson drew much attention and praise and influenced other fields of knowledge.1 But it would not be widely implemented for a long time. It was only in recent decades that the proper algorithms to deal with complex geometric information have been developed. Since the 1980s the discipline of geometric morphometrics has flourished, and sophisticated methods and computer programs have been developed to compare different species and trace changes during growth, in the case of vertebrates much of it concerning skulls. In the geometric approach, one records many landmarks and quanti-

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fies how the whole is different among species or among stages in a growth series. There are different kinds of landmark-based approaches, each with a different mathematical framework, and they include deformation, superimposition, and linear distance– based methods.2 An alternative and simpler mathematical approach to Thompson’s geometric one was developed at around the same time. This approach also had a major impact on studies of growth. In 1936 Julian Huxley and Georges Teissier published simultaneously in English and French a paper presenting a simple but elegant equation that summarizes the relationship between two measured quantities. This relationship was expressed as  

y = xa

or in a logarithmic form, log y = a log x,

where a is the scaling exponent of the law. The mathematical path of growth, or ontogenetic trajectory, is usually represented as a straight line after logarithmic transformation. The direction or slope and the position or intercept with the horizontal graph’s vertical axis are the variables to be calculated. The parameters that are relevant when examining growth are rate, duration, onset, and offset. Evolution involves interruptions, changes, and rearrangements in these parameters. Growth can produce change in form, and this is caused by changes in size, which does not have a 1-to-1 relation to shape. If the relation of size to shape is constant, we have isometry. This is rarely the case, as we more often encounter size-dependent change in shape, or allometry, a term coined by Huxley and Teissier in

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Megaloceros

1250 1000 750 Length of Antler

Figure 25.  A classic example of the study of allometric growth to understand the different body proportions across species is that of the extinct giant deer, Megaloceros giganteus, which possessed seemingly huge antlers. By plotting measurements of body size versus antler size across deer species, Gould (1974) demonstrated that the giant deer falls within the same ontogenetic trajectory as the others. Thus the antler size of this “giant” is actually expected for a deer of this size. Antler length is plotted against length of one of the forearm bones.

500

250 200

300

400

Length of Radius

their 1936 paper.3 Due to allometric relationships during growth, individuals of the same species can have different shapes at different stages of growth. It also follows that species can vary in shape if each possesses different allometric relationships during growth, or if the same growth relationships prevail, but growth is truncated or extended. In ontogenetic scaling, the variation between two species can be completely attributed to differences in size, as both map onto a common growth trajectory. Differences result from the extension or truncation of growth. Conversely, a change in growth pattern can be inferred when the variation does not map onto a single common trajectory. The mathematical approach developed by Huxley and Teissier had several precursors during the late nineteenth century, but only in the twentieth century was the biological community

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ready to embrace and use the new numerical tool.4 Immediately after the publication of the growth equation that elegantly summarized the relation between two measurements, the evolution of extinct species was examined under this framework. The allometric approach was adopted enthusiastically in paleontological circles and led to many studies of evolutionary series of taxa in which the acquisition of a particular feature was seen as the result of allometric growth—such as horns in oreodonts (extinct camel relatives), rostral length in horses from the Eocene until today, head crests in the late Cretaceous dinosaur Protoceratops, and the elongated neural spines forming the sail in pelycosaurs, very distant, early mammal relatives from the late Carboniferous and early Permian of Texas. These studies claimed that simple relations and straightforward and constant allometric relationships ruled those features. Later revisions of many of these studies showed otherwise. As more fossils were discovered and well-founded evolutionary trees for the groups became known, it was realized that the allometries themselves evolved, that organisms were mosaics of features growing at different rates, and that these changes were ecologically driven. A good example of such revisions is the evolution of horns in a phylogenetic series of brontotheres, extinct distant relatives of horses and tapirs. Cranial ornaments in brontotheres have a positive allometry, as is the case in other groups of extinct vertebrates. This differential growth leads to shape changes; deviations from isometry in growth trajectories lead to major changes in proportions, which can generate novel morphologies. The gradual increase in horns over geologic time was first interpreted as a simple extension of a common growth trajectory. Later work showed that other changes were involved, such as an earlier onset of development and an acceleration in the rate of  

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50 cm

Figure 26.  The “pelycosaur” Edaphosaurus boanerges. Modified from Romer and Price 1940 and Sander 1994.

growth. These changes in growth trajectories may be responses to more massive body shapes and the increased forces to which the horns were subjected. A classic example of evolution of allometric proportions is the hornless fellows of brontotheres, the horses. The skull evolution of horses involved new growth patterns associated with new diets. These are well documented as a complex tree with numerous “side branches,” most leading to extinct species and others leading to species closely related to the modern horse. The single modern genus Equus is the last survivor of what was a highly diverse adaptive radiation over the past 55 million years that resulted in some three dozen extinct genera and a few hundred extinct species. Around 20 million years ago, horses underwent an explosive diversification in tooth morphology. Many clades evolved high-crowned teeth suitable for grazing on the extensive grasslands of more open country biomes, which spread at the time. Up to that point in geologic time, horses had estimated body sizes of between ~5 and 50 kilograms. In contrast, in the last 20 million years, horses were more diverse in body size. Some groups

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became larger, others remained relatively static in body size, and others became smaller over time. Due to these diverging evolutionary paths, the pattern of change of inferred growth patterns in horse evolution is not linear but instead diverse and bushy.5 The changes in horse skull proportions are thought to have been driven by changes in allometric growth. The proportions among adult fossil species are different and related to function, in particular, changes toward high-crowned teeth located more anteriorly in relation to the jaw joint and larger jaws to increase muscle attachment. The allometric relationships among skull variables during individual growth of the living horse are not the same as those recorded across comparisons of adult specimens of the different fossil species. Independent of the particular trend and the vertebrate group studied, whether horses, brontotheres, hippos, reptiles, amphibians, or fish, all have certain common growth patterns. The portion of the head where the brain and the sensory organs are located grows with negative allometry: they increase less in size compared to body size increase as the animal grows. The part of the anatomy related to the jaws, the muzzle, grows with positive allometry, thus becoming larger relative to body size increase during growth. This general pattern is valid also for humans; babies have relatively large eyes and a small mouth, for example. At the level of populations within a species, allometric growth can also generate morphological diversity, as among dog breeds. Canids in general, the group to which not only dogs but also foxes and wolves belong, are characterized by highly allometric skull growth. In contrast, felids exhibit skull isometry, and correspondingly cat breeds are less morphologically diverse. What is variable in one group can be constant in another.

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Fossil Growth Series and Taxonomic Issues The optimal means for studying skeletal development is a longitudinal series in which the same individual is examined during its lifetime. If this is repeated for several individuals, we gain a view of what goes on during the growth of a particular species. This kind of study is very rare in vertebrates because of the obvious logistical and technical difficulties involved. The study of a longitudinal series is of course impossible in paleontology. A growth series in fossils is just a static sample of individuals of the same species at different stages of development. These can be recognized as such based simply on size or on the degree of suture fusion in the skull or of ossification in some part of the skeleton. An independent assessment of the age or ontogenetic stage of a fossil can be provided by histological evidence (see chapter 4). It is possible to have a reliable fossil growth series and in fact an exhaustive size series for species representing most major groups of fossil vertebrates. But the identification of ontogenetic series of fossils is not trivial. It can be accomplished most easily when large numbers of individuals in a stratigraphically controlled area are available, a very rare situation. Incorrect taxonomic assessments are caused by preservational biases and lack of consideration of ontogenetic variation. There are many cases of taxa diagnosed on the basis of juveniles that later turn out to be junior synonyms of taxa previously described on the basis of adult specimens. 6 For example, a detailed morphometric study of early mammal skulls showed that specimens previously referred to four species in two genera likely represent different ontogenetic stages of a single species. In another example, measurements of specimens of different sizes of perhaps the

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4 cm

Figure 27.  Growth series of the late Devonian placoderm fish Bothriolepis canadensis from Miguasha, Canada. The cephalic and thoracic shields are preserved; the total sample of specimens is more than 6,725, with the length of the largest specimen on the right being about 20 cm. Scale bar is 4 cm. Drawing based on Cloutier 2010.

most famous fossil taxon, Archaeopteryx, were plotted and found to be in the same morphometric trajectory and thus assigned to a single species, Archaeopteryx lithographica. The same kind of approach is becoming routine in vertebrate paleontology. Other examples involve fossils of sloths, capybaras, and ichthyosaurs, among other creatures. The importance of considering growth in taxonomic decisions is relevant for the study of deer. Antlers are richly represented in the fossil record of these animals because they are sturdy and large, and people collect them. In most deer species antlers change dramatically in the course of the life span. Antlers are indeed the ultimate ontogenetic subject, for they are shed each year, followed by a growth phase leading to a complex structure. The maximum complexity of the antler increases each year of an individual’s lifetime. Now imagine antlers as fossils. What is usually found and fills many museum cabinets across the world are isolated antlers or more commonly antler

Variable

Nimbadon lavarackorum, different ages

Size

Variable

Diprotodontian marsupials, adults of different species

Size

Figure 28.  Intraspecific (top) and interspecific (bottom) allometry. The intraspecific example is that of an exceptional growth series of the fossil marsupial Nimbadon lavarackorum, a relative of the wombat (based on Black et al. 2010). The interspecific example includes adult skulls of several diprotodontian marsupial species, members of the mammalian “order” with the largest range of sizes; from about 15 g to approximately 3 tons in the extinct Diprotodon, the largest marsupial, known from the Pleistocene.

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Figure 29.  Outlines of the antlers of a reindeer at their maximum size for five consecutive years. This individual was named Wally by the keepers at the Cairngorms, Scotland. T. Smith (2006) has presented an account of the introduced population of reindeers to which this individual belonged.

pieces. A careful consideration of individual ontogenetic change and variation is needed to taxonomically allocate isolated fossil antlers. In the past many new species were named based on isolated specimens, leading to an overestimation of the number of species of fossil deer. Variation in size and shape is also recorded in teeth during the life of individuals, and paleontologists quantify this variation to make decisions on fossil taxa. For example, the largest extant rodent species, the capybara, has served as reference to evaluate the variation among fossil samples of fossil South American rodents and their taxonomy. This led to the synonymy, that is, the invalidity, of species described in the past. Teeth represent a special case in growth studies by virtue of the fact that they experience no remodeling during life, but nevertheless their change in form can be significant because of wear. The examination of bone histology is tied to the study of fossil growth series, as it can provide an independent assessment of

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the relative and sometimes even absolute age of a specimen. In the past few years it has become increasingly common to provide histological data when describing a new dinosaur species, even when a single specimen is available. This consideration of ontogenetic variation is making taxonomy a more solid and less typological practice, although it was not entirely absent among early paleontologists. The nineteenth-century American paleontologist Othniel C. Marsh, for example, used the degree of sutural closure in the skull in brontotheres to assess if an individual represented an adult or a juvenile specimen. Sutures, the boundaries between bones, become obliterated as the animal grows. The sequence in which this happens is species-specific.

Six

Growth and Diversification Patterns The most fertile ground for the expansion of the (evolutionary) synthesis probably lies in developing theory for the role of intrinsic biotic factors in setting differential origination and extinction rates, and how those fundamental macroevolutionary variables sum to net diversification. David Jablonski, “Origination Patterns and Multilevel Processes in Macroevolution”

Fossils potentially provide direct evidence on how changes in growth strategies may have affected diversification patterns in geologic time. New strategies may have allowed some species to exploit new ecological opportunities or contributed to their demise. The evolutionary patterns of groups of organisms in geologic time, commonly referred to as clade dynamics, are the subject of intense research in the sector of the paleontological community working with invertebrate animals. Work in this area involves in many cases large databases and mathematical models based on several variables. Diversification rates, meaning how fast or slow the number of 105

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species in a group changes in geologic time, traditionally have been associated with external, environmental factors. Two alternative external factors are usually advocated in explaining evolutionary events: Red Queen versus Court Jester. Whereas in the Red Queen scenario biotic interactions are the main drivers of change, in the Court Jester scenario physical or abiotic perturbations, such as climate change, are most important.1 “Intrinsic” factors, those associated with an organism’s physiology and development resulting from its evolutionary history, are also the subject of growing interest. Studies of many groups that lived at different geologic times have shown that a dichotomy between extrinsic and intrinsic factors is a false one. Life history variables evolve canalized by the internal features of the organisms involved, which modify and are also affected by the environment. An example at a major scale is the appearance of photosynthetic bacteria, which modified the atmosphere over geologic time by releasing oxygen, as documented by dated mineralogical sediments. The release of oxygen in the atmosphere also had a triggering effect at the geologic level, as oxygen plays a role in the way rocks are weathered chemically. Some of the environmental conditions that now-extinct organisms had to face in their lifetimes were utterly unlike those we have today. The amount of oxygen in the atmosphere, for example, has been much lower or much higher than today at different periods of deep time. It is worth pondering the significance of deep time for the understanding of the evolution of development in large clades. Both theoretical expectations and empirical data have shown that simple correlates for diversification patterns are the exception. The propensity to speciate or to resist extinction cannot be

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causally reduced to a single trait; in all cases consideration of life history variables is essential. Some of the environmental differences between the current world and the past concern variables that gradually changed during geologic time. Others concern sudden, catastrophic events of a magnitude never documented during human written history. Some of these events are recorded at the time of mass extinction events, such as that of dinosaurs. Exceptionally active volcanism is associated with them. The effects of the impact of the asteroid that landed in the Yucatán Peninsula are widely acknowledged. Arguably as relevant was the effect of the events that led to the Deccan traps of the Indian subcontinent, one of the greatest volcanic features on earth, where gigantic plateaus of lava were built on continental crust. The Deccan traps consist of half a million square kilometers of volcanic rock, more than ten times the area of Switzerland. The singular landscape consists of several flat levels, or “traps,” each formed by the top of a single lava flow and extending for many kilometers. The Deccan traps resulted from volcanic events of a magnitude unlike anything we are aware of during human history. Even the eruption of Mount Vesusius and its well-recorded consequences for Pompeii pale in comparison.2 Radiometric dating has shown that the eruptions leading to the Deccan traps occurred over a period of about 2 million years, some 66 million years ago. These volcanic eruptions not only covered a vast area with lava but also released large quantities of sulfur dioxide and fine dust into the atmosphere. The resulting climatic changes affected the vegetation and the seas on a large scale. The marine plankton was probably decimated, triggering a cascade of events given the connectedness character-

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istic of the ecosystem. Intricate ecological networks of interactions were very likely thrown into disarray. At the time of an even larger recorded extinction of biodiversity, at the PermianTriassic boundary, the eruption events leading to the Siberian traps lasted only about one million years and were more extensive than those associated with the Deccan traps. The resulting volcanic rocks currently cover about 2 million square kilometers, less than one-third of the estimated original area and yet roughly equal to Western Europe in land area. The changes in ocean chemistry associated with this major volcanic activity had a great global impact on life history evolution. Major extinction events have affected the history of life on earth, and the recovery of groups that did not go completely extinct is a matter of much interest and requires understanding of the environment and the kinds of organisms characterizing the postextinction world.

Ocean Acidification in the Past and Today After the end of the Permian period, when the largest ever mass extinction took place, the early Triassic was characterized by environmental instability. Based on the work of geochemists, we know that the levels of acidity in the ocean and the amount of oxygen in the atmosphere fluctuated. The various conditions affected the metabolism and ultimately the growth patterns in different groups of organisms, including those that build skeletons of calcium carbonate, such as reef corals (see chapter 10). The acidification of the ocean—a drop in its pH value—affected the growth patterns of ammonites and other molluscs, corals,  

 

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and most if not all other kinds of marine invertebrates. Recorded volcanic activity resulted in a relatively sudden methane release as well as an increase in carbon dioxide concentration not only in the atmosphere but also in the oceans. This reduced the marine calcium carbonate oversaturation and the calcification potential of organisms living at all levels of the water column (benthos, plankton)—a “biocalcification crisis” that my colleague Helmut Weissert at the ETH Zürich and many others have investigated. The investigation of fossil marine invertebrates and their life history is often studied in parallel with oceanic changes, bringing together geochemistry and paleontology. As occurred in the early Triassic, seawater worldwide today is acidifying, as oceans absorb the increasing amounts of carbon dioxide in the atmosphere. This ocean acidification is believed to be a major threat for near-future marine ecosystems. Experiments show that this change impairs the ability to reproduce and grow in at least some species of copepods, snails, sea urchins, and brittle stars. Because the change is occurring so rapidly, many species are unlikely to survive. But not all groups are equally affected. Sam Dupont and colleagues in Sweden presented experimental evidence that the larvae of the sea star Crossaster are positively affected by ocean acidification: when cultured at low pH, the larvae grow faster, with no visible effect on survival or skeletogenesis. This was the first report of a positive effect of ocean acidification on growth rate in any invertebrate. Differential effects on the life history of organisms must be responsible for the patterns of survivors and victims of extinction events and the recovery afterward. To quote Arnaud Brayard and colleagues, good genes and good luck are involved in the survival of clades.  

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Major Patterns of Larval Evolution in the Oceans Many marine invertebrate species of the sea floor have a freeliving dispersive larval stage that is morphologically and ecologically very different from the adult. One of two distinct strategies for larval development is employed by most marine invertebrates before they settle and metamorphose into juveniles. In planktotrophy, the larvae feed in the water column for a period of weeks or months. In the alternative strategy, the nonfeeding lecithotrophy larvae instead are nourished through egg yolk for the much shorter period they spend living in the water column. As already predicted by examining the distribution of these strategies on the evolutionary trees of living species, there must have been multiple shifts between them during evolution, even within specific groups. The question that drives much of the research on different invertebrates is whether these changes were randomly scattered or concentrated in specific periods of time. It is generally accepted that they were most likely driven by the ocurrence of predation in the ocean floor when new groups or predatory strategies evolved or by environmental change. In addition to an academic interest in this aspect of evolution, the aim is to understand the flux of nutrients and ecological interactions in the ocean that ultimately affect fisheries. Work on fossils can provide direct information on the past major changes of communities of organisms in the oceans associated with new life history strategies. A good example is the origin of planktotrophy at the transition from the Cambrian to the Ordovician, about 490 million years ago. This time period is very important because a drastic increase in global diversity and the establishment of all major groups of extant organisms is recorded.

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The direct evidence on larval strategy evolution comes from fossil gastropods. Back then, like today, some species were direct developers, and as in lecithotrophic larvae, their greater amount of yolk meant they had larger shells. The shells themselves are rarely preserved as fossils, because they are thin and minute (usually less than 1 mm). But natural casts of them are common. They are called Steinkerne (core stones) in German, and they are in many cases the side product of work by paleontologists who study conodonts, possibly very basal vertebrates, by etching rock with chemicals and looking at the residue. Because the size of the Steinkerne reflects the amount of yolk, we can then infer with certainty whether the animal was planktotrophic. Alexander Nützel and colleagues measured hundreds of these Steinkerne from the late Cambrian and the early Ordovician and recorded directly planktotrophic forms at the transition between these periods some 490 million years ago. The early Ordovician is characterized by the diversification of benthic suspension feeders, those attached to the bottom of the sea. Some researchers have speculated that this feature triggered the evolution of planktotrophy, as a strategy to escape predation. It is obvious that this plausible scenario requires that the nutrient supply in the world oceans was enough to sustain the swimming larvae. In fact, the tectonic events in the early Ordovician apparently affected ocean water dynamics in a way that could have had that effect. Biologists concerned with ocean life are starting to pay close attention to the work of paleontologists in this area, trying to understand the conditions organisms experienced in the past and thus predict what the effects of global change on organisms might be today. The flow of information goes both ways, as ultimately it is the careful study of life history of living species that

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will provide the most detailed understanding of evolution of larval strategies in the fossil record.

Climate Change and Mammalian Developmental Evolution The examination of diversity patterns and environmental changes over geologic time has shown that there have been episodes of climatic-driven changes in vertebrate faunas but also some in which no traces of change are recorded. At the time of climatic change in the Neogene of North America, which led to the transformation of large areas into deserts or very dry habitats, several new groups of mammals originated. It has been hypothesized that this occurred through similar ontogenetic changes in several clades simultaneously. A saltatorial kind of locomotion occurs in dry environments across the world (e.g., kangaroos in Australia). This kind of locomotion is coupled with different limb proportions, which evolve through different rates or timing in the onset of growth across species.3 This means that climatic change ultimately could have a simultaneous effect on developmental patterns in different groups that evolve similar adaptations to new kinds of environments. Climatic change can lead to evolutionary changes in size, usually coupled with life history changes. Horse species, once widespread and abundant in the North American faunas, exhibit a rapid decline in size before their extinction in the Pleistocene of Alaska. It is possible that natural selection operated on life history variables, leading to evolutionary changes in body size. The study of the growth and longevity as recorded in tooth histology can reveal such changes. Morphologically, due to allometric relations, changes in size mean in most cases changes in

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2 cm

Figure 30.  Saltatorial mammals evolved independently in many desert areas of the world around the end of the Miocene epoch. An example is the marsupial Argyrolagus scagliai from Argentina.4 The tail was probably much longer, and here only the preserved vertebrae of the specimen from the Museo Municipal de Mar del Plata are illustrated. Extant forms, and presumably saltatorial argyrolagids too, develop their great size differential in limb proportions through individual rates of skeletal differentiation. Modified from Simpson 1970.

the shape of the anatomical structures of organisms. Numerous examples of this occurred in many groups in parallel about three million years ago in Africa. Analogous phenomena probably occurred at different times in other continents. The evolution of mammals in South America is a rich subject of study in vertebrate paleontology, but only recently has the knowledge of the chronology and the sampling of faunas improved enough to allow us to examine evolutionary patterns with confidence. Pancho Goin, Fredy Carlini, and colleagues in La Plata have recently noticed a major mammalian turnover coinciding with a sudden drop in global temperatures at latest

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Eocene–early Oligocene time. They termed the event the Bisagra Patagónica, or Patagonian Hinge, which was recorded in southern Argentina. Many groups of marsupials and armadillo relatives became extinct at the end of the Eocene, and many new kinds of these animals appeared in the Oligocene.4 What is remarkable in the early Oligocene groups is their new strategy of dental ontogeny, one in which teeth are ever-growing, a condition called hypsodonty. This feature involves a new set of metabolic and life history changes and likely arose in response to the tooth wear produced mostly by volcanic ashes in foodstuffs, as is being investigated by Rick Madden. In contrast to the examples above, the significant drop in temperature that occurred in North America at the time of the Bisagra Patagónica in Argentina (at the Eocene-Oligocene boundary, about 34 million years ago) apparently had little effect on mammalian evolution. Based on excellent collections of many mammal species from the White River Group sediments in the western United States, Don Prothero and colleagues showed that the large majority of mammalian species did not change morphologically in spite of the well-recorded climatic changes. A study of the surface of the teeth revealed that changes in diet must have occurred, although tooth shape remained the same. Perhaps the mammals around that time and place in North America had evolved more phenotypic plasticity than their counterparts in South America. On the other hand, although the Eocene-Oligocene climatic change was global, its effects may have differed on a local scale, with distinct degrees of volcanism in the two continents being an important factor to consider in this regard. The impact of temperature on the evolution of development  

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Figure 31.  General pattern of extinction and diversification in several groups of marsupial mammals around the major climatic changes recorded at the Eocene–Oligocene boundary, denominated Bisagra Patagónica by Pancho Goin and colleagues. Modified from Goin, Abello, and Chornogubsky 2010.  

is well documented in many empirical studies of extant species. There are also indirect clues provided by the fossil record. In the Eocene, millions of years before the colder Oligocene, there was a diversity of fossil faunas with the same characteristics as those in today’s tropics, even in high latitudes. In present-day northeastern Colombia, the remarkable giant snake Titanoboa cerrejonensis, with an estimated body length of 13 meters and mass of 1,140 kilograms, lived about 58 million to 60 million years ago. As temperatures rose and declined over geologic time, so did

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the upper size limit of cold-blooded creatures such as snakes whose metabolism is influenced by the average temperature of the environment. Jason Head and collaborators calculated that a snake of Titanoboa’s size would have required an average annual temperature of 30oC to 34oC to survive. By comparison, the average yearly temperature of today’s Cartagena on the Colombian coast is about 28oC.

Jurassic Sharks The reproductive mode and the capacity to evolve, to adapt within few generations, can change during evolutionary time as a response to environmental changes of abiotic and biotic nature coupled with internal changes. An example is provided by the early diversification and radiation of modern sharks and rays in the early Jurassic, as studied by Jürgen Kriwet and colleagues. In the aftermath of the end-Triassic mass extinction, there was an opportunistic rapid diversification and ecological radiation of sharks and relatives coupled with, and likely caused by, small body size, short life spans, and oviparity. These life history traits enabled faster ecological innovations in body plans. In a study of living sharks, skates, rays, and chimaeras, it was shown that the risk of extinction is higher in viviparous than in oviparous species, even with proportionately higher individual and egg predation rates in the oviparity case. This is so because the evolutionary fitness of viviparous species is very low if pregnant females are killed, making them more prone to extinction. In the early Jurassic, oviparity allowed sharks and relatives to better adapt to changing environmental conditions. The long life span and the viviparity of most living shark species make them highly vulnerable to extinction.

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Survival and Diversification in the Early Mammalian Lineage Very few species of our own remote mammalian ancestors survived the Permo-Triassic extinction event about 250 million years ago. Most lineages became extinct, and most of these were carnivorous forms. A small portion of these early mammal relatives survived, and among them was Lystrosaurus, the most abundant tetrapod during the early Triassic postextinction recovery. Lystrosaurus belongs to dicynodonts, named after their specialized dentition containing two tusks. These herbivores were large, varying from rat to ox size, and diverse, with over seventy genera known. Lystrosaurus not only survived, but it also became geographically widespread and abundant during the early Triassic. From her paleohistological studies Jennifer Botha-Brink established that Lystrosaurus and other dicynodonts had high growth rates in comparison with other contemporary species. The histology of more than a hundred specimens of dicynodont bones shows enlarged channels in the microcortex that may have increased the supply of oxygen and nutrients, facilitating more efficient nutrient assimilation and increased bone growth. Lystrosaurus and its closest relatives grew more rapidly than its evolutionary cousins. An exceptional rapid growth rate probably contributed to the survival of Lystrosaurus during the end-Permian extinction and its abundance in the early Triassic, during the postextinction recovery phase. The increased growth rates of dicynodonts may have allowed them to quickly attain body sizes that provided refuge from predation. Furthermore, bone histology suggested a rapid attainment of sexual maturity, which would have given Lystrosaurus resilience to environmental perturbations. This discovery regarding life history also fits with

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the commonality of fossils of these animals, indicating high levels of abundance in rocks where the presence of few competing herbivores has been recorded.

Islands as Experiments in Life History Evolution Islands are favorite subjects of study for evolutionary biologists, as they are the closest to a natural experiment with which to test hypotheses. In a limited amount of space with well-defined boundaries it is easier to document the crucial physical and biological variables and examine how they affect the evolutionary process. Classic studies of island populations are those of the Galápagos finches, the Anolis lizards from the Caribbean, and the fruit flies from Hawaii. Lakes such as Victoria in Africa are also places where great natural experiments can be conducted, as only in each of them can some fish groups survive.5 Islands are also a rich subject of investigation into development and fossils. Many of the organisms in question became extinct recently, in the past hundreds or thousands, rather than millions, of years. In most cases, the cause of extinction was the pernicious impact of humans. There are different kinds of islands: old or young, small or large, and oceanic or continental. Continental islands are those that were formerly connected to a neighboring landmass. They generally lie on a continental shelf and could become, or have been, connected to the mainland via a land bridge. Bali, Cuba, and most Mediterranean islands are continental. An oceanic island is more the quintessential island. It has never been connected to the mainland, and it originates through some geologic process—most commonly a volcanic eruption—rising from the  

 

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ocean floor. The Galápagos, the Hawaiian Islands, Mauritius, and Réunion are all volcanic islands. What concerns me here is the isolation that occurs on islands, and with that the peculiar conditions that led to the evolution of different life histories, much of which can be documented in the fossil record. Among fossil mammals we find some of the most spectacular, or at least the best-known case studies of evolution on islands. 6 One study calculated that the rate of morphological evolution in mammals, rodents mostly, is greater for islands than for mainland populations by a factor of up to three to one.7 Accelerated changes in islands have been suspected for a long time, and quantitative studies include, for example, that of Adrian Lister concerning the red deer population on the island of Jersey. The fossil record shows numerous drastic size changes in the classic cases of pony-sized elephants, rabbit-sized mice, pig-sized hippos, and dog-sized deer. Following reproductive isolation, aberrant sizes, coupled with changes in life history, evolve. 8 Because of allometric growth, size results in different shapes of organisms. An ontogenetic perspective in the study of island mammals’ morphological evolution is thus the most intuitive one. There is a general tendency for small mammals to evolve toward larger size and for larger species to evolve toward smaller size over short periods of geologic time.9 There are many examples, such as the extinct Sicilian elephant Elephas falconeri, estimated to have reached an adult height of less than 1 meter and a body mass of 100 kilograms, only about 1 percent of the mass of its mainland ancestor. Other elephant-related examples are found in the Channel Islands, twenty miles off the coast of Southern California. Mammuthus exilis, a pygmy species derived from Mammuthus columbi, one of several mammoths that roamed North America within the past million years, evolved there.

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Dwarf elephants were common in the Mediterranean, having been found in Crete, Malta, Cyprus, and Sicily. There has been speculation that the skulls of these animals may have inspired the Greek legend of the Cyclopes: elephants’ skulls have a large hole in the forehead to which the trunk connects, which could be mistaken for a huge, single, and central eye socket. In spite of the seemingly bizarre association of the nose hole of an elephant with the single eye of the mythological creature, it is anatomical accuracy that makes the alternative source for inspiration, the cyclopic condition of a malformed infant, less likely. In the mythological creature the single eye is above the nose, but in the malformation the eye develops below it.10 The study of mammals from different islands reveals similarities in the species that inhabit them and in the adaptations they evolve. Numerous fossils document extinct elephants, deer, and hippos from numerous islands in the Pleistocene of the Mediterranean, and deer and elephants from islands in Japan and Southeast Asia. The taxonomic commonalities are most likely explained by the swimming abilities in the case of large species, or the ability to survive on natural rafts in the case of small ones. There are also ecological parallels in the conditions encountered by different mammals in different regions. Each island is unique, and naturally different selection pressures and historical contingency played a role in shaping the faunal and floral communities each time. However, the principles and mechanisms in operation appear to be universal. The ecological context of development is relevant to understanding cases of insular dwarfism and gigantism, whereby trade-offs among intertwined variables must be involved: size, longevity, age at reproduction, growth rate, available resources, competition, and metabolic needs.

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Figure 32.  The skull of the dwarf elephant Elephas falconeri from the late Pleistocene of Sicily. Based on a specimen on display at the Senckenberg Museum, Frankfurt. Drawing by Claudia Joehl.

How organisms fuel their growth depends on the rates of food consumption and energy expenditure. A fraction of the assimilated food is oxidized to fuel metabolism, and the rest is synthesized and stored as biomass. Mathematical models based on physiological measurements of metabolism and growth have been developed and have helped to establish that the same general principles of relations operate across different kinds of animals.11 This may explain why we see parallel morphological developments recorded on different islands. There are two pathways leading to the rapid evolution of size changes in islands. Late reproduction can lead to large size. This pattern is associated with few offspring. On the other hand, an

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optimization of metabolism under different conditions with a different, more limited set of resources can lead to early reproduction and small size. How did fossil mammals cope with the different, lower resource levels they encountered on islands? Again and again, fossils document considerable evolutionary plasticity in the developmental and physiological strategies of numerous groups. An example is Myotragus, a close relative of sheep and goats that became extinct some five thousand years ago. The ancestor of Myotragus probably arrived in the Balearic Islands around six million years ago, a time at which the Mediterranean was a collection of salty lakes. Myotragus most likely evolved under very different conditions from those in the mainland, with low resource levels and lack of predators. The island Myotragus became exceptionally small: the largest adult specimens reached a maximum of 45 to 50 centimeters from the ground to the shoulder and probably weighed no more than 50 to 70 kilograms. How did they grow, and what kind of energetic strategy did they have? Histological study of the long bones of Myotragus revealed lamellar zone bone throughout the cortex, a kind of bone otherwise common only among living reptiles such as crocodiles, which are ectotherms. Bone histology reveals that Myotragus grew slowly and without a uniform rate during life, and this was coupled with a significant delay in the attainment of skeletal maturity. Myotragus also had an extended life span when compared with its evolutionary cousins. Not affected by the activities of humans, Myotragus had a slow, long life on a Mediterranean island. In general, paedomorphism—retention in the adult of infantile or juvenile characters—has been claimed to describe much of the evolution of island mammals. But organisms are mosaics,

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in which each organ or part, although integrated with the rest, is governed by different rules of relative growth. So although an island form may have a general resemblance to a juvenile of the ancestor, this may be only superficial, and many features will show special adaptations to the new ecology and metabolic needs. The body proportions in the island forms cannot be explained simply as the result of a stop or retardation of development that produced a resemblance to the juvenile stage of the ancestor. The discovery of a new hominid species from the Pleistocene of the Indonesian island of Flores, the celebrated Homo floresiensis, provides a prominent example of the need to consider ontogeny when studying fossils and of the importance of “mosaic” evolution. H. floresiensis was only about one meter in height and fully bipedal, with a reconstructed chimplike brain size of 417 cubic centimeters in an approximately 30-kilogram body. This brain size was perplexing because this species made tools and lived recently, with a hominid ancestor possessing a comparatively much larger brain size, perhaps H. erectus, which had a brain volume of approximately 900 cubic centimeters. This is why some scholars argued that H. floresiensis was nothing more than a population of pygmies with a pathological condition that included microcephaly.12 But this disproven alternative aside, considering the allometric relations of brain to body size, the brain volume of H. floresiensis falls outside expectations, irrespective of which hominid species among the potential candidates is hypothesized as its ancestor. Examples of extreme brain size reduction outside the range expected given allometric considerations exist for other mammals. Eleanor Weston and Adrian Lister showed this quantitatively for fossil hippos from Madagascar. Brain tissue is met-

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abolically costly, and thus it was hypothesized that this organ becomes smaller in lineages for which it is advantageous to save energy. The lack of simple ontogenetic scaling is not rare in cases of rapid evolutionary reduction in size. For example, Meike Köhler and Salvador Moyá-Solá reported a significant reduction of the brain and sense organs in Myotragus during its geographic isolation in Majorca. In another example, Louise Roth reported in the 1980s that insular dwarf species of fossil proboscidians are not simply smaller with preserved scaling relationships (paedomorphic) in their postcranial proportions but also show deviations most likely responding to locomotory and metabolic constraints and adaptations, as has also been shown for many fossil species from Mediterranean islands. The patterns observed in hippos, in Myotragus, and probably in Homo florensiensis are paralleled in domestication, in which reduction in the size of brain and sense organs occur, as Darwin already noticed in his 1868 book on domestication. In fact, in one paper some authors mistakenly claimed that Myotragus’ morphology is the result not of adaptations to the new island environment but adaptations resulting from domestication. An example of an important life history feature that breeders tend to select for is maturity at small size. Apparently this feature has been more responsive to artificial selection than are features of relative growth or body composition.13 Insights into the factors involved in the rapid evolution documented by fossils on islands could also be gained with the examination of the effect of captivity in zoos and other places. This task would be analogous to that taken up by Darwin when he studied variation under domestication to gain insights into evolution in general. Captivity has a great impact on basic aspects of the biol-

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ogy of animals such as body size and longevity. Changes during the lifetime of an individual are of course not heritable, but one could imagine how those captivity conditions, a particular selection regime, could lead to evolutionary changes if kept for some generations. In captivity four fundamental aspects of life are different from the natural conditions: food availability, lack of predation, limited area in which to live, and less diverse or fewer different species coexisting in the habitat. These aspects differ between island and mainland populations too.

Seven

Fossils and Developmental Genetics

Ontogenies do not fossilize. But structures that do were once the result of a developmental process. Fossils of adult individuals can then be informative about development by virtue of preserving phenotypes with an immediate, clear correlation to a specific developmental process. To reconstruct such a process, it is important to consider the position of the fossil in the evolutionary tree of life, to ensure that the analyses are based on correct assumptions. This approach is called extant phylogenetic bracketing. It was introduced specifically to infer soft anatomical properties and behavioral reconstructions in fossils, but it can also be used for reconstructing extinct ontogenies. The extinct animal is compared to its nearest living relatives. One examines the distribution of a developmental feature among extant taxa that “surround” the extinct taxon on a given tree. The feature exists in extant species of a group within which the fossil of interest is placed: one can deduce that it existed in the common ancestor and therefore in the fossil. 126

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Figure 33.  Dinosaurs are phylogenetically bracketed by crocodiles and birds.

For example, dinosaurs are bracketed by birds and crocodiles. A feature found in both birds and crocodiles, such as oviparity, would likely be present in dinosaurs. On the other hand, a feature absent in both birds and crocodiles, such as metamorphosis, would most likely also be absent in dinosaurs. Things get more complicated when one of the extant relatives has the trait and the other does not. For example, crocodiles have largely lamellar bone, correlated with slow growth, whereas birds possess fibrolamellar bone and are capable of rapid growth spurs. What about dinosaurs? In these ambiguous cases, and also in order to test inferences based purely on the phylogenetic bracket, consideration of preservation of features that provide direct evidence of a trait are paramount. In the case of dinosaur growth, examining the bone histology has revealed direct, unequivocal information

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regarding fibrolamellar bone and singular growth curves with rapid phases in some lineages. One may question the scientific value of inferences made about organisms separated by several hundreds of millions of years of independent evolution. But such inferences are justified based on empirical evidence gathered from living organisms. A major discovery of the past few decades is that many developmental mechanisms and molecules are the same across disparate and phylogenetically distant taxa. It is well known that many molecular processes that control phenotypic change are much older than the group expressing those phenotypes, what Sean Carroll has called “ancestral complexity.” This conservatism is valid for very disparate and distantly related species. This leads to the fact that there are deep or fundamental levels, early in geologic and developmental time, at which structures found in the adults of organisms as distinct from one another as flies and humans can be traced back. In this case we talk of “deep homology” of those structures, meaning “sameness,” or homology, at some level of organization (molecular, cellular) and at some level of the hierarchy in the evolutionary tree of life. Using the present to infer the past, as in the phylogenetic bracket case, may seem limiting. In fact, the evolutionary biologist Mark Pagel has written that this approach “condemns the past to be like the present. Worse, perhaps, the past that we get from looking backwards is a very ordinary past, an average past.” But we have no choice, and it does not mean that we do not find significant and even surprising patterns by looking at fossils this way. And what is “ordinary” or “average” anyway? There are no living trilobites, but there is every reason to assume that the body segmentation they experienced during individual develop-

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ment was associated with the same processes as those recorded in living arthropods. In the following examples I set out to demonstrate how we can learn about developmental evolution by looking at extinct adult phenotypes.

Vertebral Numbers Complex animals consist largely of repeated parts, and vertebrates are no exception. This is not obvious at first sight, but if we examine our own or any other vertebrate skeleton, we see the serial repetition of vertebrae diverging only gradually in size and shape. The tissues surrounding these vertebrae are also repeated structures, including muscles, nerves, and vessels. These packages of structures, these segments of the whole, originate during development from building blocks, or somites. Somites form during a particular window of early embryonic development. The rate of segmentation determines, then, how many vertebrae the adult organism will have. Some snakes develop as many as three hundred segments, whereas turtles stop at around twentyfive, with a fixed number of eighteen before the sacrum (the portion of the vertebral column just anterior to the tail bones). There is a segmentation clock, and depending on the species it ticks differently. Sometimes it ticks longer or shorter within species, especially in the tail region. Our own vertebral column is easily subdivided into regions with distinctive features. We have no ribs in the neck, in the cervical region. We have a thoracic region with large ribs, coming together to join a sternum and building a cage where our heart, stomach, and other organs are nicely protected. We have no

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sternum or ribs in our belly, so we need to keep things in place there by having strong abdominal muscles in our lumbar region. Finally, some vertebrae are fused to form the sacral region, to which the pelvis or hip girdle attaches, to be followed by the caudal region, or tail. The boundaries between regions correspond to boundaries in the expression of special genes that regulate the developmental process and establish the regional identities along the body axis. These genes are members of the Hox family of regulatory genes. With this developmental background, something seemingly trivial such as the number of vertebrae in different regions of the skeleton gains a new dimension. The numbers reflect two fundamental aspects of early development: the formation of somites (somitogenesis) and Hox expression boundaries. Variations in vertebral numbers must then mean evolutionary plasticity in those mechanisms. Mammals have a conservative number of vertebrae anterior to the pelvis. Both a mouse and a giraffe have seven neck vertebrae. Both the koala and the opossum, in fact all marsupials, have twelve thoraco-lumbar vertebrae, and variation in this region is small across groups. Reptiles, which include birds, are much more diverse in this regard. A swan has about twenty-five neck vertebrae and ducks sixteen or fewer. All turtles have eighteen presacrals—eight cervicals, ten dorsals, and two sacrals—although the stem turtle Odontochelys, from the Triassic of China, reportedly has only nine dorsals. I first learned about the existence of these fixed patterns from Shigeru Kuratani.1 Kuratani-sensei, as I call him when in Kobe in my lousy attempt to integrate, had the insight of examining the issue of vertebral numbers across land vertebrates by mapping data provided in a classic study by the late Sir Richard Owen, a contemporary of Charles Darwin. With Yuichi Narita,  

 

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he discovered which clades are developmentally conserved and which are plastic. When visiting his lab in 2006 and discussing their analysis, I noticed in their work another peculiar pattern. In most mammals of all kinds, the sum of the vertebrae of the rib cage and of the belly region, the thoraco-lumbar region, is nineteen. This number is constant in both marsupials and in the egglaying monotremes and in many placental mammal groups, and was probably fixed in early mammalian evolution. But besides some other randomly distributed exceptions, a major group of placentals, the Afrotheria, shared an increased total number of thoracic and lumbar vertebrae. This pattern holds even when examining the oldest and less specialized fossil species of each of these groups. Afrotheria, a group first recognized based on molecular evidence alone, includes diverse creatures such as hyraxes, elephants, dugongs, tenrecs, and golden moles. After we noted this pattern, Rob Asher and Thomas Lehmann discovered that a delayed dental development is also diagnostic for afrotherians, fossil and living.2 The generation of vertebral numbers is associated with mechanisms that are impossible to study directly in extinct species. But there is a one-to-one correspondence in vertebral numbers with segmentation and with Hox-gene boundaries. The extant phylogenetic bracket clearly supports the assumption that these processes operate in all land vertebrates, fossil and living. The rich fossil record of land vertebrates gives us, then, the chance to examine development in extinct forms. This way we could examine the early history of mammals and reptiles to see the patterns of evolution and answer a suite of questions: When did the mammalian conservatism in vertebral numbers evolve? Which mechanism has been evolutionary more plastic, somitogenesis or Hox-gene boundary? What kind of limitations

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in developmental plasticity do ecological adaptations, such as secondary life in water as seen in whales and marine reptiles, produce? To answer these questions, together with Johannes Müller and Torsten Scheyer, I assembled a group of experts who provided current and comprehensive information on phylogeny and vertebral numbers for their groups of expertise. With this information, we conducted analyses that led us to the discovery of different degrees of developmental plasticity in the evolution of extinct groups and in the early history of all major living groups. The examination of fossils showed that increases and reductions in the overall vertebral numbers or in the boundaries between regions, keeping the overall number equal, occurred independently in several lineages. We traced back the developmental canalization or conservatism in mammalian presacral numbers to the origin of the group, about at least 315 million years ago, that had a cervical number fluctuating between five and six. Establishment of the almost constant number of seven cervical vertebrae occurred about 100 million years later, in the Jurassic. This discovery questions the previous hypothesis trying to explain the conservatism first recorded only for living mammals. Based on the high frequency of mortality of human fetuses and juveniles with abnormal neck vertebral numbers, lethal pleiotropic effects relating to mutations in the Hox regulation affecting not only axial skeleton but also cell proliferation were proposed to explain mammalian cervical number conservatism. Only mammals with a low metabolic rate show deviations from the standard cervical number, and this feature is also related to a lower incidence of cancer. However, our result puts into question this hypothesis. The earliest representatives of the evolution-

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Figure 34.  Tanystropheus longobardicus. Other restorations of this animal show it with the neck, which included thirteen vertebrae, stretching perpendicular to the main axis of the body. From Wild 1974, after modifications by Christian Klug based on Tschanz 1988.

ary line leading to mammals were already quite conservative in neck vertebral numbers, and their physiology, as seen in the paleohistological record and other anatomical markers, was reptilian. Maybe this is an example of what Thomas Huxley called “the slaying of a beautiful hypothesis by an ugly fact.” Another large pattern of vertebral number evolution we recorded is that in groups that inhabit an aquatic environment. In these groups there is a deviation from the standard developmental pattern: more presacral vertebrae evolve. This is true for all reptiles and mammals. The decrease of regionalization— that is, the differences between sections of the vertebrae disappear, become alike—seems to promote more developmental plasticity.3 But in the case of aquatic mammals, the number of neck vertebrae remains constant. This is in contrast to reptiles, in which the total number of vertebrae (via somitogenesis) also increases but also with plasticity in the number of neck vertebrae, as shown by different groups of extinct groups such as plesiosaurs, which possess many neck vertebrae, or pachypleurosaurs and Tanystropheus, which have fewer neck vertebrae. The dinosaur pattern clearly shows that the number of vertebrae and their distribution in regions are not determined by the overall size an animal reaches as an adult: sauropod embryos did not have a high rate of somitogenesis to reach their gigantic size.  

 

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On Saurichthys and Mutant Fish I have discussed largely how paleontological data can inform our understanding of the evolution of life history and developmental mechanisms. But can data on developmental evolution inform paleontologists? Can insights from molecular evolutionary developmental biology contribute to understanding diversity in extinct taxa? As nucleic acids and proteins are very rarely preserved over geologic time, the reconstruction of the molecular basis of morphological change in fossils must rest on inferences. Here I explore the bases of such inferences by examining the example of a fossil fish. Among the rich collections of middle Triassic vertebrates in Zürich is a remarkable fish. It looks superficially similar to the modern pike, with an elongated and streamlined shape, telling of a predator. Saurichthys, “lizard-fish,” is its name. This genus is positioned quite basal in the tree of bony fishes, close to the sturgeons, paddlefish, and bowfins among the living relatives. There are four species known from the Monte San Giorgio locality in Switzerland, and these are on display in Zürich, but the genus has a worldwide distribution, with more than thirty species. Those in our museum are characterized most conspicuously by different scale patterns and numbers, as had been recognized in the 1980s by Olivier Rieppel when he worked in Zürich. The hypothetical last common ancestor of the Saurichthys species radiation can be reconstructed with certainty based on several other fossils as having been covered entirely by uniform rhomboid scales with numerous, highly segmented fin rays and a larger number of dermal bones in the skull. The Saurichthys species, which can be traced back to this hypothetical ancestor, are characterized by different degrees of reduced squamation (rows

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and extent of scales); reduction in the number of fin rays and their segments; reduction in the number of dermal bones in the skull and their form, reflected in the shape of the operculum; and reduction in the robustness of teeth and jaws. In fact, novelties in evolution are in many cases associated with loss of structures. The general reduction of the exoskeleton in many lineages and the loss of the heavy armor of Silurian and Devonian fishes are good examples.4 But we do not need to go so far back in time. Scale loss or reduction in other fishes is not uncommon. For example, in sturgeons and paddlefishes (acipenseriforms) the full squamation documented in specimens from the late Cretaceous was reduced to five rows of scutes in the extant species. Scale loss evolved independently at least thirteen times in minnows and carps (cypriniforms) and several times in galaxids, noodlefishes (osmeriforms), and killifishes (cyprinodontiforms). Within some species, much variation is possible. The domesticated carps, Cyprinus carpio, exist in different varieties: leather carp, with virtually no scales; mirror carp, with few enlarged scales; and linear carp, with a single row of large scales on the flank. These patterns of variation and evolutionary change have led to an interest in deciphering the genetic mechanisms underlying scale reduction.5 Hundreds of specimens of Saurichthys are known, and some led to the discovery of viviparity in this animal. I always thought that one day I would like to learn about and work on this fish, but the way it happened was rather unexpected. Developmental genetics and a soft-spoken, polite, and retired medical doctor from Basel, Lieni Schmid, are key to the story. In recent years Lieni Schmid had joined Rudolf Stockar and colleagues in Lugano collecting Saurichthys in Triassic rocks in southern Switzerland. He had also attended evo-devo courses in

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6 rows of scales 6 rows of scales, rib-like flank scales

4 rows of scales

Fully scaled (Last common ancestor) Fully scaled, deep flank scales

2 rows of scales

Figure 35.  Sketches of the diversity in squamation patterns in Saurichthys. The last common ancestor must have been a fish covered entirely by uniform rhomboid scales. Modified from Schmid and Sánchez-Villagra 2010.

which the latest papers relating morphological evolution with developmental genetics were discussed. Among them are studies of some fish species that are well known genetically and are serving as models to understand evolutionary change. Schmid noticed a similarity in the morphological patterns shown in the developmental genetic studies of fish species and those in Saurichthys. He told me about his ideas, and we examined the matter further and wrote a paper about it, which I summarize here. A series of elegant studies, which are being included in textbooks, illustrate genetic and phenotypic changes at the population level in an ecological setting. The best-known example is the striking variation in the squamation patterns of stickleback fishes.6 Rapid morphological diversification has been documented in living species, generated by regulatory changes and interactions in genes that are expressed through changing ecological conditions. The marine threespine stickleback (Gasteros-

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Figure 36.  Specimen of Saurichthys curionii from the Triassic of Monte San Giorgio, Switzerland (Palaeontological Institute and Museum, University of Zürich).

teus aculeatus) has a row of about 36 lateral plates, modified scales, on its flanks. In freshwater, a mutation of the ectodysplasin signaling pathway (a network of interactions at the molecular level) was repeatedly selected that reduces the number of these modified scales from 36 to 0–7 when homozygous and to numbers in between when heterozygous. The molecular genetic factors causing a loss of squamation have been studied in sticklebacks in the lab and in the field, as well as in mutants of several fish species. There are other mutants of the ectodysplasin signaling pathway. In medaka (Oryzias latipes) it was demonstrated that a mutant with scale loss is due to a mutation in the receptor of this pathway. In zebrafish (Danio rerio) several mutations were identified, either in the signaling molecule ectodysplasin itself or in its receptor, which led to phenotypes with similar losses of scales. Another molecular mechanism leading to scale loss has been detected in a zebrafish mutant and the domesticated carps. A loss-of-function mutation in the fibroblast growth factor recep 

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tor-1 is the cause here. Fibroblast growth factors are known to be important in all stages of development. A viable mutant of this pathway is possible due only to gene duplication, such that lethal side effects of a mutation in one gene are compensated by the nonmutated version of the same gene, called the paralog in the terminology of genetics. Schmid and I postulated that similar genetic processes underlie phenotypic changes in Saurichthys and in the mutants of these fishes. The molecular underpinning of the morphological diversification of Saurichthys involved a mutation or a regulatory change of a signaling pathway as the key mechanism. There are good reasons to assume that these mechanisms operated in Triassic fishes as they do today. Sequence analyses of the genes coding for the components of the ectodysplasin signaling pathway show that these genes are highly conserved in vertebrates. Ectodysplasin is known to control the formation of teeth and dermal bones in jawed vertebrates, scales in fishes, feathers in birds, and hair and dermal glands in mammals. Concerning fibroblast growth factors, they are essential very early in development, and they are apparently shared at least by all vertebrate animals. These signaling pathways are examples of what has been called tool kit proteins, well conserved throughout evolution. In addition to reduction in scale number, the fish species mentioned above, by mutation in the ectodysplasin pathway or in the fibroblast growth factor pathway, show a tendency to have the remaining scales aligned in a pattern similar to that seen in the single rows of Saurichthys. Moreover, the remaining scales on the flank of the mutants are dorsoventrally elongated in a manner comparable to deep flank scales, as in the species of Saurichthys with riblike flank scales. Mutations in components

Wildtype

Mutant

Ectodysplasin pathway

Zebrafish

Medaka

Threespine stickleback

Fibroblast growth factor

Zebrafish

Carp

Figure 37.  Sketches of wild type and mutant fishes from different model species used in developmental genetic studies. Ectodysplasin pathway: zebrafish and medaka based on Harris et al. 2008; threespine stickleback based on Colosimo et al. 2005. Fibroblast growth factor pathway based on Rohner et al. 2009. Figures prepared by L. Schmid (Basel), modified from Schmid and Sánchez-Villagra 2010.

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of the ectodysplasin pathway also lead, at least in some mutants of zebrafish, to a reduction in the number and complexity of fin rays, as has been recorded in some morphological types of Saurichthys. Moreover, a loss of teeth and an alteration in the proportions of the dermal bones were reported for zebrafish mutants, again changes in organs that are modified in the diversification of Saurichthys. The features controlled by the tool kit proteins, including squamation, fin ray structure, and dentition, are particularly important for protection, predation, and nutrition and thus for adaptation in general. A change in a major developmental gene offers a good chance for sympatric speciation. The larger the phenotypic effect of a single mutation, the greater the chance of immediate reproductive isolation of the mutants, provided they are viable and successful. Changes in signaling pathways as we propose them for the diversification of Saurichthys could thus provide an explanation for rapid speciation. In contrast to a gradualistic model of evolution, a change in a major developmental gene serves as a viable explanation for the essential differences among the species of Saurichthys in the paleoecological context in which they originated. The fact that intermediate, gradually differing fossils of Saurichthys and of most other species have not been found fits well into the picture.

E ig h t

“Missing Links” and the Evolution of Development

Many people are accustomed to thinking of the evolution of life in terms of a ladderlike progression, with a different animal on each rung. In the case of vertebrate evolution, they may envisage a fish on the bottom rung, a salamander on the next, then a lizard, a mouse, and finally a human on top. Following this medieval myth, it seemed natural to suppose that “lower” animals evolved into “higher” animals. And if this were so, we should expect to see “links” between them, all the way up and down the “ladder.” This idea of the Great Chain of Being, or Scala naturae, is an image of evolution that remains common in the popular media, although scientists have long realized that such a concept is inaccurate. The ladder myth is misconceived and does not fit with evolution. Instead of resembling a ladder, the evolution of life is more similar to a branching bush. Each branch of the bush represents a distinct lineage of organisms. Places where two or more branches diverge from a single point on the bush indicate that the lineages represented by the branches must have shared a common ancestor at a particular point in their history. Each liv141

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ing species is a “missing link,” as each species is part of the tree of life, with a mosaic of both “primitive” retentions and derived features, which document transformations. From each species there is much to learn about these changes. Every one of the millions of species of animals shares an ancestor with every other one. The missing link is the ancestral species that gave rise to two modern groups, for example, humans on the one hand and chimpanzees on the other. But it is not reasonable to expect to find that critical species, for its identification would require a complete series of ancestor-descendant fossils. We can certainly trace the evolution of birds from feathered dinosaurs, but we are not sure exactly which fossil species were the direct ancestors of modern birds. Our focus in reconstructing the history of life is not to try to imagine how a chimpanzee could transform into a human, as this of course never happened. Rather, we try to discover which features chimps and humans inherited from their common ancestor and which features the lineages evolved after they diverged. Some authors correctly argue that the concept of the missing link is not only archaic, but its search is also an outmoded approach to the study of macroevolution. In current evolutionary biology, the focus of investigation has shifted from finding transitional taxa to finding transitional features shared by closely related forms with common ancestry. Many examples are well known today, and they provide information not only about anatomical transformations but also about the functional and ecological contexts of those transitions. Particularly important in this context are stem species, those that document the time and mode in which the acquisition of diagnostic features of living species evolved.1 An example is provided in our mammalian lineage. According to molecular esti-

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mates, supported by fossil evidence, the last common ancestor of all living mammals, that is, the last common ancestor of a human (a placental), a kangaroo (a marsupial), and a platypus (a monotreme), lived at least 220 million years ago. But the history of mammalian origins from our last common ancestor with reptiles goes even farther back in time, until at least 315 million years ago. These earliest 100 million years of evolutionary history are documented by the stem species of mammals. They are placed in the evolutionary tree between the last common ancestor of the living species and the last common ancestor of the next living relative, in this case the reptiles. Fossils provide for several major taxa, a fairly complete picture of the morphological transformations involved in their origin. The fossil record of many groups has changed from almost nonexistent to fairly diverse in a few decades, as in the case of Mesozoic mammals. The continuous reports on new discoveries of “transitional forms” show the large advances that have been made and are being made in the documentation of macroevolutionary steps of vertebrates since Darwin’s time. These reports also show that purpose and plan are not characteristic of organic evolution. Organisms fulfill their “conditions for existence” at each particular time in which they live—that is what counts, as I discuss below.  

Flatfish Eyes The large diversity of extant fish, about thirty thousand species, includes many forms with anatomical specializations, the origin of which is in most cases not documented by fossils. A classic example has been the group of flatfishes, to which the (sadly)

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gastronomically familiar halibut and plaice pertain, unusual in having both eyes on one side of the head. Matt Friedman from Oxford University described fossils from Eocene rocks of Italy and France about 50 million years old that show an arrangement of eyes intermediate between that of normal fishes and flatfishes: One eye is shifted toward the opposite side of the skull but does not quite make it there. The discovery of stem flatfishes with incomplete orbital migration demonstrates that the origin of the flatfish body plan occurred in a gradual, stepwise fashion. This evolutionary origin resembles the individual development of the flatfish asymmetry, with increasing degrees of orbital migration transforming a symmetrical embryo into a fully asymmetrical adult. The “intermediate” fossils were adults and not juveniles, so actually, no “fossilized ontogeny” was documented. But the singular fossils provide a beautiful comparison with the developmental data available from these animals. How these intermediate forms used half migrating eyes remains a mystery. The flatfish case touches on one of the most fundamental discussions in evolutionary biology, with roots in influential and controversial ideas, such as that of the “hopeful monster.” This term was introduced by Richard Goldschmidt (1878–1958), who with Hans Spemann and Viktor Hamburger made Germany preeminent in developmental biology. He became a professor of zoology at the University of California, Berkeley, in 1936. Goldschmidt had stressed the lack of “intermediate forms” in evolution and suggested the asymmetric skull of flatfishes as an example. Goldschmidt’s ideas were largely simplified and vilified by people arguing for gradual evolution. He became at some point the caricature of the dead-wrong scientist and remains depicted so in some simplified accounts of debates in evolutionary biology. Actually, Goldschmidt emphasized the role of development  

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Figure 38.  Heteronectes chaneti, from the Lower Eocene of Bolca, Italy. On one side (bottom), the eye socket is in its usual position, but on the other it is located much more dorsally (top), near the midline of the head. Photograph courtesy of Matt Friedman (Oxford).

in the origin of his “hopeful monsters,” arguing that they did not simply pop into existence out of a genetic mutation. His emphasis was not simply on genes, but on epigenetic systems emerging from a combination of environmental and genetic factors. From being a villain, Goldschmidt has now become sort of a hero.2 The flatfish fossils would seem to argue against Goldschmidt’s

Figure 39.  Eye migration during the development of a flatfish.

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ideas. They certainly contradict his prediction concerning these fishes and address the contested issue of the mode and tempo of evolution. But Goldschmidt’s ideas are nevertheless relevant and supported otherwise by empirical evidence. Furthermore, although we aim at generating principles, each individual evolutionary story is unique, so care must be taken not to generalize. This flatfish example, with the intermediate forms that Goldschmidt would not have thought could exist, is not a pledge for gradualism; it is just an example of how the fossil record is in some cases the only way to test an evolutionary hypothesis directly. The case of the bat is a counterexample—one in which the very silence of the fossil record may reveal a true evolutionary pattern.  

Bat Wings Much in the anatomy of bats is peculiar, such as specializations in the ears of many species that allow them to perform echolocation, the ability to hear very high frequency sounds in order to locate prey, enemies, and spatial surroundings. Fossils from the Eocene of North America and Europe show that echolocation evolved early in bat evolution, albeit after flying. Specializations for high-frequency hearing in bats probably evolved more than once within bats. Some sort of echolocation is also performed by shrews, and in a different way and medium by some whales. But the truly singular aspect about bats is their wings, which allow them to perform active flight, something that among vertebrates evolved otherwise only in birds and (since the late Cretaceous) in the extinct pterodactyls. The wing of bats is unique in that it basically consists of very elongated fingers besides the thumb and a movable skin between them. What would the forelimbs of

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a “missing link” look like? Among living species, many mammals are capable of gliding, and to do so they have a skin between their limbs. Gliding would appear to be a first step toward flying, involving locomotion through the air using a fold of skin. But the differences are otherwise huge. The ability to constantly flap the forelimbs with very large digits is something else. Comprehensive molecular studies of living mammals provide clear indication that bats are the closest relatives to ungulates such as cows and horses and with them form a group with carnivores such as dogs and cats. The relationships of bats among living mammals are thus resolved, but the question of the origin of the most singular morphological innovation of bats, active flight, still remains unanswered. Some ten million years after nonavian dinosaurs went ex­­ tinct, the radiation of the extant groups of mammals starts to be well documented by fossils. Many Eocene fossils are wonderfully complete and are undoubtedly classified among the earliest bats. Their wings are already present, so no intermediates are known in spite of extensive searching among rich deposits of well-preserved fossils. Perhaps this evolutionary innovation arose very fast. Developmental biology gives clues about the mechanisms that probably made this possible. A relatively larger forelimb than hind limb early in development of the limb bud is very common among mammals. This is at a developmental period some colleagues call phylotypic, characterized by some morphological and perhaps genetic commonalities among different taxa. From this somewhat similar starting point, bats and other mammals start to diverge. This has been thoroughly documented in some bat species and in mice. In bats, the size increase of forelimb digits is faster than that of hind limb digits, a case of allometric growth between limbs. In mice, both

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hands and feet grow at a similar rate. The developmental elongation of the bat digits is achieved via an accelerated rate of proliferation and differentiation of cartilage cells. Karen Sears and colleagues found that this process is associated with higher levels of a bone morphogenetic protein, Bmp2. Other comparative work has also revealed which molecules are involved in the persistence during development of skin between digits, leading to the wing of the adult. As early embryos we have skin between our digits, as do vertebrates with hands and feet. At some point the cells building that skin start to die, so we have our movable digits and not a paddle or wing, as in the feet of ducks or the wing of bats. In the duck’s feet and in the bat’s hand the skin does not die but persists and even grows. The mechanisms involved in the two cases are analogous, but as discovered by Scott Weatherbee and colleagues, the molecules involved are not the same. It had been known that in chicks and mice, model organisms in developmental genetics studies, bone morphogenetic proteins (Bmps), which are capable of stimulating cellular growth and differentiation, trigger cell death in the undifferentiated, loose connective tissue (mesenchyme) between the developing fingers characteristic of the embryonic paddle in the hands and feet. In the duck foot, the molecule Gremlin serves as inhibitor of that Bmp effect, leading to the webbed feet. The bat also has this mechanism, but in addition, another protein is involved, namely, the fibroblast growth factor Fgf8, also involved in different aspects of morphogenesis. The importance of these discoveries lies in providing empirical evidence of the simple mechanism involved in the developmental innovation of wings. Now a “sudden” origin of bats seems less unlikely, and the fossil evidence and lack thereof may indicate precisely that. Are there any fossil bat embryos that provide any further evidence? The only one to my knowledge comes

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Figure 40.  An embryo of the fruitbat Rousettus amplexicaudatus, scanning electron microscope image. Photo by M. Sánchez, modified from Giannini, Goswami, and Sánchez-Villagra 2006.

from the Eocene locality of Messel in Germany, famous in fact, among other things, for some of the earliest and best-preserved fossil bats. The skeleton of the fossil embryo is already formed, and the wings are more or less visible.

Turtle Shells Another peculiar body plan within the vertebrates, this time a reptile, is that of turtles. The main skeletal specializations are the

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presence of a shell, the lack of teeth, a short tail, and the anapsid condition of the skull. Turtles’ skulls lack the fenestration for muscle attachment typical of other land vertebrates. This condition is either secondary or primary; we cannot tell, mostly because we are not sure where turtles are placed in the reptilian tree of life.3 If they are at the base of the tree, their skulls are more likely to be simply the result of the retention of the primitive condition, as the earliest reptiles, well documented in the fossil record, are anapsid. If turtles are the sister group to either lizards or to crocodiles, their skulls are then fundamentally specialized. Fossils are not sufficient to solve this issue, not even some spectacular ones recently described. Maybe future fossil finds will. In 2008 Li and colleagues published the description of a new genus and species, Odontochelys semitestacea, from Chinese rocks about 220 million years old. This animal had an anapsid skull, but otherwise it exhibited many transitional features, such as presence of teeth and a long tail.4 Most important, Odontochelys serves to address what is unique about turtles, their shell. The turtle shell consists of a dorsal or back portion, a ventral or belly one, and a bridge of bone joining the two. The ventral portion is composed of expanded ventral ribs fused with some bones of the original vertebrate shoulder girdle, such as the clavicles, now very much modified.. The dorsal part of the shell is much more complicated in its origin, as it is the result of the fusion of ribs with ossifications from the skin that are analogous to the scales or osteoderms of many reptiles. Most significantly, in turtles the scapula is beneath the dorsal shell, or carapace, a unique condition; in all other reptiles and in mammals such as humans the scapula is outside the rib cage. The presence of the shell and the anatomical relations in turtles are so unique that a saltatory evolutionary change was traditionally invoked to explan its origin.

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Aiming at understanding the development of such a strange anatomy, Hiroshi Nagashima and colleagues have studied how the shell forms in relation to the scapula and to the muscles in the body. Their anatomical study showed that the novelty in the turtle shell is what my colleagues called the axial arrest of rib growth and the folding of muscles to accommodate the unusual position of the shoulder girdle. Development was examined not with a naive expectation of recapitulation but rather in order to understand the topographic position of muscles in living turtles and their development. Their work provided clues for formulation of a plausible hypothesis of morphological transformation, which fossils can test. Odontochelys, the oldest fossil turtle, is a “missing link” for understanding the shell origin, as it has a half a shell by exhibiting the belly half. On the dorsal side, the broad and short ribs of Odontochelys look like late embryonic ribs of extant turtles. In fact, the anatomy of Odontochelys fits very well the model that Nagashima and colleagues presented: The ribs are shortened so that without a shell the scapula is not above or dorsal to the ribs but instead in front of the first pair of ribs. The turtle example illustrates three fundamental points:

•



•



•

Fossils are paramount in showing in which order developmental innovations arose: ventral shell before dorsal shell. Together with embryological data fossils provide wellfounded scenarios on how evolutionary innovations originated. Fossils can be very informative about some features and silent about others. In the turtle case we learned much about the shell but much less about the skull.

scapula

Other land vertebrates

Other land vertebrates

Odontochelys

vertebra

rib

scapula

muscle plate

Modern turtles

Modern turtles

rib

muscle plate

Figure 41.  The carapace of turtles is composed of expanded ribs and vertebrae fused with skeletal tissue derived from the skin. The body plan is very different when compared to other land vertebrates, as in turtles the scapula is located inside the rib cage. Hiroshi Nagashima and colleagues speculate that in Odontochelys semitestacea, from the late Triassic of Guizhou, China, the embryonic “carapacial ridge” (broken line) may have developed only temporarily and incompletely in the embryo, inducing a partial fan-shaped growth of the ribs. The singular location of the scapula leads in turtle development to a folding of muscle plate in the shoulder region.

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Another aspect to consider in the turtle example and a saltational scenario for the origin of the turtle body plan is explaining the simultaneous “jump” to produce the highly integrated set of traits to which the shell is tied, including the musculature and its neural control, limb anatomy, and ventilation mechanisms. A plausible scenario is one that makes relatively rapid change possible but also considers the potential correlation among the different aspects of the turtle form.

Whale Legs Until the 1980s the origin of whales was poorly understood. Based on anatomical studies alone, it was difficult to sort out which group of terrestrial mammals would be closest to them. Fossil whales had been known since the nineteenth century, but these did not help to solve the puzzle, as they were of animals that were already very specialized to the physiological demands of a life in water, possessing flippers and tail flukes. A series of remarkable fossil discoveries by the international teams of Phil Gingerich and Hans Thewissen have since provided a fairly complete transformational series of fossils that document the steps that led from a fully legged terrestrial ungulate to a mammal with no hind limbs and only relicts of the pelvic girdle. Most of those fossils come from the Eocene of the Indian subcontinent and from Egypt. Parallel to the paleontological discoveries, molecular analyses placed the whales unequivocally as the closest relatives of the hippopotamus, which means that whales are to be classified within the even-toed ungulates or artiodactyls, to which cows, giraffes, deer, and pigs belong. The fossil record shows that the aquatic adaptations of whales and hippos must have evolved independently.

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The pakicetids are the most basal lineage of extinct whales. Their ear anatomy is intermediate between that of terrestrial and fully aquatic mammals, meaning it could probably function in both environments. Pakicetids were capable of running on land, as reflected by the skeletal anatomy of their limbs and vertebrae.5 Chemical analyses of oxygen isotope ratio data and studies of the rocks in which pakicetids were found suggest they lived in or near rivers and not in marine environments. The next important fossil in the sequence is Ambulocetus, which had an amphibious lifestyle. It had a long neck and tail, and the large feet in the hind legs and other features suggest that this animal swam like an otter. The remingtonocetids were similar ecologically to the living gharial crocodiles from Southeast Asia, with their long, narrow skulls, capable of rapid lateral movements to capture fish. The morphology of the ear region suggests that they were capable of underwater hearing. Several other fossils, such as Rhodocetus and Dorudon, document further morphological transformations, such as the reduction of the hind legs. What do fossil whales tell us about the evolution of development? Major evolutionary transformations, such as that of a whole new body plan adapted for life in a new environment, are especially relevant subjects for developmental studies, because the innovations we see in the fully formed adults are the result of an ontogenetic process that must have significantly changed in geologic time. Fossils show the tempo and mode in which the new features evolved. Their sequence of appearance is especially relevant. Hans Thewissen and colleagues have examined some aspects of the specialized limb developmental genetic system of a dolphin species that results in the almost total reduction of the hind limbs. In most toothed whales, or odontocetes, to which dolphins

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innominate femur

innominate femur

Baleen whales

Toothed whales

innominate femur Modern whales

Basilosauroidae Remingtonocetidae Ambulocetidae Pakicetidae

Complete loss of hindlimb and of vertebral regionalization Reduction of sonic hedgehog expression in hind limb f eo bud as tion h c p al redu u ad b Gr lim d i hn

Figure 42.  The gradual reduction of the hind limb bones during cetacean evolution, with examples from the major groups involved. Modified from Thewissen et al. 2006.

belong, the only hind limb element is the innominate, whereas the baleen whales or mysticeti generally preserved some of the most proximal hind limb bones. The study of dolphin embryos revealed that many of the molecules involved in the limb development of other mammals are also expressed in the dolphin but with a different timing or location. For example, the apical ectodermal ridge, the distal border of the limb bud where the gene fgf8 is expressed, is only a transient feature of the dolphin. Another important molecule, the sonic hedgehog, which mediates the development of a fundamental area of the limb bud in other land vertebrates, is absent. This absence was hypothesized by Thewissen and collaborators

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to be associated with the loss of distal limb elements such as the foot. The record of actual evolutionary change provided by fossils and the knowledge of the developmental genetics involved in hind limb reduction offer an explicit scenario of change. Without the fossils, one could only speculate on what the changes were like. With the fossils, the potential genetic mechanisms involved can be reconstructed.

Nine

Mammalian and Human Development

There are about 5,300 species of extant mammals. They represent only a fraction of the number of species that ever existed since the separation of the evolutionary line leading to them, at least 315 million years ago. Then the reptilian and the mammalian lineages split. The estimate based on fossils is that about 100 million years passed until the appearance of the last common ancestor of all living mammals in the Jurassic.1 Although 5,300 extant species sounds like a large number, it is not so impressive when compared with other groups: there are twice as many species of birds and five times as many bony fishes. But mammals are special when we consider their great ecomorphological diversity—locomotion in humans, kangaroos, whales, and bats; the size range between a shrew and the blue whale. What all mammals have in common is a unique life history and physiology among vertebrates, including an energetically expensive endothermy, parental care, milk production, and determinate growth. These and many other features must have characterized the last common ancestor of the living mammals. When  

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Morganucodon

Thrinaxodon

Lystrosaurus

Edaphosaurus

Figure 43.  After the divergence from reptiles no later than 315 million years ago, there was a long history of “stem mammals” until the last common ancestor of living species originated at least 220 million years ago. Representing living mammals are the echidna, a monotreme; the kangaroo, a marsupial; and the human, a placental. The stem species depicted here are all important ones mentioned in the text but are just a miniscule portion of the diversity of parallel paths of evolution that were followed in the deep time of mammalian evolution.

did these features arise since the split from reptiles? Did they do so simultaneously? If not, in what sequence? Whatever our ancestors did, at two critical times in geologic history they had good luck and good genes. I have already discussed how Lystrosaurus and its relatives survived the Permian-Triassic boundary, a time when many groups of organisms were completely wiped out. Mammals also survived the end of the Cretaceous event, when most dinosaurs became extinct.

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Several unique anatomical features of mammals are not coupled directly with life history traits, for example, the presence of three little ear ossicles as opposed to just the one in reptiles and birds. The way embryological and paleontological data document the origin of the mammalian ossicles fits wonderfully well together, their discovery being one of the greatest triumphs of comparative anatomy. As I discussed in chapter 8, Goldschmidt had stressed the lack of intermediate forms in evolution and the importance of epigenetics, and, in addition to the the eyes of flatfishes, his major example was the middle ear of mammals. Both were bad examples of an otherwise good idea. In fact, Goldschmidt would have welcomed the newest evidence that the origin of the mammalian middle ear was coupled developmentally with an increase in brain size and most likely with many other features, including changes in the masticatory apparatus. The concomitant developmental changes show that these features cannot be understood in isolation. During the ontogeny of living mammals, the growth of the neocortex is coupled with the gradual detachment of elements associated with the jaws. Some of the old jaw elements become relatively smaller and smaller as they detach and begin to form the future elements of the middle ear, an example of negative allometric growth. A gradual anatomical change similar to that of embryos is what fossils document in the stem line leading to the living mammals. These changes have been documented by Tim Rowe at the University of Texas based on the study of computer tomographic images of fossils and reconstructions of developing marsupial embryos of living species.2 Coupling, or nonindependence, during the evolutionary origin of mammals also characterizes life history features. The documentation of those evolutionary changes is restricted to the skeleton, as soft tissues, including organs such as the heart or the

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stomach, are rarely if ever preserved. Not surprisingly, most evidence derives from teeth and the bone histology. The complicated pattern of tooth occlusion in mammals, with the upper and lower molars possessing several cusps occluding with each other in a specialized way, is surely correlated with a high metabolic rate, coupled in turn with the life history traits. Whereas most reptiles with a diet consisting of other animals simply catch their prey and, at most, cut it with the teeth before swallowing it, mammals tend to chew what they eat. The salivary gland secretions are mixed with the food, thus partially processing it in the mouth before it is digested in the stomach and intestine. The evolution of lactation in mammals is coupled with dental features such as the late eruption of the first functional teeth. Mammals produce only two tooth generations, a condition called diphyodonty that includes a juvenile and an adult dentition. Lactation most likely originated when tooth replacement became diphyodont.3 This was in turn associated with determinate growth, which means that rapid juvenile development ends in a set adult size. For reptiles, in contrast, growth is basically indeterminate, meaning that a crocodile, for example, never stops growing and never stops replacing its teeth, although growth rate can slow with age. Each extant mammalian species has a specific dental formula, meaning a given number of incisors, canines, premolars, and molars. This differentiation of the dentition is mammal-specific, as is the fact that the most posterior group of teeth, the molars, are not replaced. Fossils document when this dental differentiation and replacement pattern was established. A growth series of the Triassic stem mammal Thrinaxodon shows that this animal had eight postcanine teeth at some juve-

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nile stage and four more added posteriorly as growth progressed. Sinoconodon, which lived in the late Triassic and is regarded, like Morganucodon, as one of “the first mammals,” apparently had a degree of indeterminate growth and multiple replacements of the incisors. In the Cretaceous mammal Gobiconodon the “molars” were replaced. Thanks to a combination of dental eruption pattern data and a growing paleohistological record, it is possible to trace the origin of the mammalian life history features. In paleohistological studies the detection of fibrolamellar bone is a major issue, as this indicates rapid osteogenesis and with that overall fast growth, related also to endothermy (see chapter 4). This kind of bone is detected in most, though not the earliest, members of the mammalian lineage. Our earliest mammalian ancestors were physiologically and developmentally more similar to extant reptiles than to mammals. An example is Dimetrodon, which had the characteristic indeterminate growth of basal amniotes, lacking fibrolamellar bone histology. Besides the direct record of bone histology, an indirect way to infer determinate growth is through population studies of fossils with good stratigraphic control. This requires lots of fossils of the same species from the same stratum. If in the sample all adults are of equal size, this would suggest determinate growth. This is what has been reported for a population study of Morganucodon, from the late Triassic–early Jurassic, considered by many paleontologistss to be among “the first mammals” because of the presence of a suite of anatomical features in this animal. In mammals, size is generally a good proxy for age of immature individuals, as their size is not so much affected by environmental factors such as temperature, which is the case in reptiles. In contrast to Morganucodon, Dimetrodon, as well as its close relative  

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Ophiacodon, adult animals of the same species have different sizes.4 In these earliest members of our lineage, as in reptiles, size is a poor indication of stage of development. As the anatomical information supported allocation of specimens of different sizes to the same species, this observation implies that these earliest representatives of the mammalian lineage did not have a mammalian kind of growth and thus for them size is not a good proxy for age. The timing of development in fish, amphibian, and reptile embryos is very much affected by the temperature in which they are incubated, and in many species even sex is determined by it. Depending on the temperature at which a turtle is incubated, which has an important effect on metabolic rate and thus growth, the sizes at similar “stages” of development can be very different. Mammals in turn are characterized by a more continuous inner temperature environment, a so-called homeostatic ability, by maintaining a high metabolic rate in a constant internal environment. The first mammals from the Jurassic have been characterized by reduced developmental plasticity, with more stable growth patterns than the often recorded bouts of rapid and slow growth typical of reptiles and of the earliest representatives of the mammalian lineage. The capacity to stop or reduce growth during adverse environmental conditions must have characterized, for example, Dimetrodon, as documented by the paleohistological record. Tom Kemp from Oxford University has named the integrated evolution of characters described above “correlated progression.” He thinks that this gradual and almost synergistic pattern of evolution, resembling a network of interactions changing across time, characterizes not only much of early mammalian evolution but also the origin of other major groups, such as turtles and the first vertebrates with limbs or tetrapods. The idea has considerable

164  /  Mammalian and Human Development fibro-lamellar bone tissue glands-rich skin secondary palate

lactation interlocking dental occlusion high metabolic rate

homeostatic internal environment

diphyodonty

determinate growth

Figure 44.  Illustration of the connections among several mammalian features that surely evolved in parallel and with a correlated progression pattern.

appeal. Certainly, the coordination of changes in different parts of the body is likely caused by a succession of small, incremental changes rather than by one single step. According to Kemp, changes in traits “evolve analogously to a line of people walking forwards hand in hand: any one of them can be a single pace in front of or behind the next, but no more without breaking the line.” The experimental evidence for organisms as varied as lab mice, plants, insects, turtles, and even humans serves as a re­­minder that features do not evolve in isolation; they are part of the whole organism. There are experiments in which researchers have tried to assess the degree to which shape variation has a genetic basis. In controlled breeding or pedigree information, researchers study the effect of selection experiments on a particular feature. In these cases there is usually a response to selection of other aspects of shape besides that which was originally selected for. In the origin of the mammalian life history pattern, it would be wrong to assume that one particular variable must have been primary, as all are integrated. Change in one variable has to be accompanied by changes in other variables for the organism to function, to fulfill its conditions for existence. Figure 44 represents this network idea. The pattern of correlation and inter-

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actions in evolution represented in the figure is backed up by empirical evidence. As the record of early mammal lineage evolution becomes better sampled and the studies of life history more quantitative, we should be able to refine and complete the details of this pattern. The clever idea of correlated progression remains just an idea unless supported by empirical evidence, and the only source for direct evidence is the fossil record. Mammalian life history and physiology are correlated with several anatomical features, some of which are recorded as fossils. They show us that diagnostic mammalian features did not originate simultaneously, and some evolved convergently in lineages that eventually became extinct. An example of a feature that evolved independently several times is the secondary palate. The secondary palate is the bony and soft-tissue horizontal wall our tongues can touch when moved to roof of the mouth. This feature is a separation between the oral and the nasal cavity, which allows us mammals to breathe while we eat and thus perform an efficient processing of food and energy production to support our high metabolic rate.5

Developmental Evolution at the Root of the Living Mammalian Diversity After 100 million years of evolution of our lineage separately from that of reptiles, the last common ancestor of living mammals originated and the diagnostic features of Mammalia, by definition, were established. But mammalian evolution involved further significant changes, and other major events in life history evolution took place. Perhaps the most significant involved the basic dichotomy among living mammals between the monotremes, including the platypus and the echidnas as the sole liv-

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Secondary palate Occlusion of molar teeth

Tongue Muscle of mastication

Nasal cavity Brain cavity

Tongue Secondary palate

Figure 45.  Some of the cranial features of mammals, including a large tongue. Multicusped molars occlude in a particular fashion, with coordinated action of the masticatory muscles involved. A secondary palate separates the mouth and the nose passages, facilitating chewing and breathing at the same time. Modified from Maier 1999.

ing representatives, and the marsupials and placentals. Monotremes lay eggs, whereas marsupials and placentals do not. This difference is one among many others, which together with the fossil record and molecular estimates show a deep separation of the two evolutionary lines going back to at least the Jurassic. It is useful to have monotremes around, as they allow us to examine much of what the earliest marsupials and placentals probably were like,6 although both the platypus and the echidnas are themselves highly specialized forms, as shown not only by their anatomy but also by their genome.

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The eggs of monotremes are extremely small and do not posses a hard shell, so the likelihood of their fossil preservation is extremely low. It is parsimonious to assume that the earliest, stem species of the marsupial-placental lineage also laid eggs, but we have no fossils documenting that. Along the evolutionary line leading to the last common ancestor of marsupials and placentals, viviparity evolved. Some authors have argued instead that differences in the reproductive anatomy and physiology among marsupials and placentals suggest an independent origin of viviparity in the two groups.7 A more tractable issue from the paleontological perspective concerns the difference between marsupials and placentals, because of the relation with hard-tissue features preserved in fossils. Extant marsupials are specialized in their dental development, in that only the last premolar is replaced in each jaw. Using ultra-high-resolution X-ray CT, Richard Cifelli and colleagues showed a marsupial-like pattern of tooth replacement in the Cretaceous stem species Alphadon. This mode was also recorded in the most complete stem forms of marsupials from the Paleocene, animals that lived in what is today the Bolivian Altiplano. As this mode of dental replacement has been associated with the marsupial mode of reproduction involving a short gestation length and a very altricial (immature) condition at birth, these life history traits were hypothesized to characterize the basal marsupial relatives of the Cretaceous and Paleocene.8

The Hominid Fossil Record Humans are a unique kind of mammal, and there is much that has been paleontologically documented about their origins. Fossils representing twenty species of our lineage, the hominine,

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are accepted by paleoanthropologists, and, although they show a general trend over time from apelike to humanlike features, the evolutionary tree is one with many branches, parallel patterns, and extinctions. Humans are not the pinnacle of a single constant trend. How did the features of the ancestral ape we share with chimps and bonobos that lived about seven million years ago transform into those of modern humans? When during hominine evolution did a human pattern of ontogeny arise for the first time? We know little of how fossil hominine species grew and developed from birth to death—few immature fossil specimens are sufficiently well preserved. The most iconic find was reported in 1925 by Raymond Dart of the Taung infant, an Australopithecus africanus from South Africa with an estimated age at death of three to four years. We have some information on Homo erectus based on a few specimens. There is an incomplete skull from Java of an individual estimated to have died at an age of approximately one year or four years. There are also skeletons of a Homo erectus boy from Nariokotome, Kenya, who reached an age of eight to nine years and of an adolescent from Dmanisi, Georgia, aged between eleven and thirteen years. Studies of some of these materials have shown that brain growth in Homo erectus was chimpanzee-like and unlike that of modern humans. The earliest-known hominid is Sahelanthropus tchadensis. It is represented only by adult specimens, but according to my colleagues in Zürich Christoph Zollikofer and Marcia Ponce de León, the comparative analysis of a well-preserved skull of this fossil with great ape and human ontogenetic allometries suggests that Sahelanthropus’s postnatal skull growth trajectory was likely similar to that of chimpanzees. The comparative study of humans and great apes, as well as  

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Figure 46.  Skull development in species of the human lineage, chimps and bonobos. The ontogenetic trajectory of each species is indicated by a gray arrow. Extant species and Neanderthals are represented by neonates (infants before the eruption of the first molar) and adults; earlier hominids, by those fossil specimens that best correspond to these life stages. Numbers indicate endocranial volume, a proxy for brain volume, in cubic centimeters. The vertical axis represents growth time in an individual. Notice the evolutionary trend toward short ontogenetic trajectories. Modified from a figure courtesy of Zollikofer and Ponce de León after their 2010 publication.

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of the bits and pieces of information that fossils provide, demonstrates that the species-specific morphological traits, those that allow us to distinguish the bones of one species from another, are established before birth. This is unfortunate, as fossils of prenatal individuals have never been found. On the other hand, much of what makes humans unique concerns changes in life history features, and for that the postnatal period is critical, and, fortunately, there is fossil evidence of it.

Beyond the Fetalization Hypothesis What is special about human development? When compared with our closest relatives the great apes, we humans are characterized by a series of features that include a long gestation period, helpless newborns with large brains, a long childhood, late eruption of the molar teeth, delayed body growth, late onset of reproduction, a long postreproductive life phase, and a long life span. Many anatomical features of humans, such as sparse body pelage, are reminiscent of early stages in living ape development. The shape of the skull of adult modern humans as well as Neanderthals is generally similar to that of infant chimps, bonobos, and australopithecines and to the reconstructed last common ancestor of humans and great apes. This led to the fetalization hypothesis, which claims that the adult human anatomy is similar to immature forms of the ancestral species. Formulated in the first half of the nineteenth century, this hypothesis was restated in 1977 by Stephen Jay Gould in the context of his classic study, Ontogeny and Phylogeny. Gould was interested primarily in changes in developmental timing, and humans presented an excellent case study. Following the Basel-based biologist Adolf

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Portmann among other previous authors, Gould claimed that humans are essentially “extrauterine fetuses” for the first year of life. The early postnatal life of humans consists of events that in the case of apes occur in utero. The human “premature birth” is thought to have been affected by maternal pelvic width given the infant’s larger head circumference. Neural growth in humans is claimed to be extended beyond the great ape ancestral state. The fetalization hypothesis has dominated comparative ontogenetic analyses of human evolution. But not all human features can be described with the fetalization model. Several features of the ontogeny and life history of great apes are different in humans but not always toward fetalization: in humans brain growth is very fast during the first few years of life in absolute terms but slow in terms of when a given percentage of adult brain size is reached. Another significant point is that human mothers resume reproduction long before a weaned infant becomes independent, which allows humans to produce multiple dependent offspring. This is viable because of the cooperative breeding characteristic of our species. It is very much unlike great apes. The small face and large braincase characteristic of the adult human skull results from slow skull development, combined with fast and long brain growth. The neurocranial size of newborn modern humans and Neanderthals is similar to that of adult chimps, bonobos, and Sahelanthropus, but it increases after birth to approximately four times the size of that of an adult chimpanzee. The overall pattern of human skull growth must have been present in the last common ancestor of Neanderthals and humans, which lived at least half a million years ago. But important differences among the two species since their splitting are documented in the fossil record.

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Neanderthal Babies and Growth Much about the postnatal ontogeny of Neanderthals, our closest extinct relatives, is well documented. The fossils are mostly fragmentary, distorted, and dispersed, but using computerassisted methods it is now possible to reconstruct much of the skeletal changes from birth to adulthood. The differences between human and Neanderthal skulls are already present in neonates, as is the case with chimps and bonobos. Modern humans have a small face and a globular braincase, with the chin being the only marked facial prominence. Neanderthals, on the other hand, have taller and more projecting faces and a prominent masticatory system. After birth, Neanderthals and humans follow a similar mode of cranial growth, but human cranial developmental rates are slightly lower, such that adult human crania are more similar in shape to those of adolescent Neanderthals. Work conducted at the Max Planck Institute in Leipzig has detected differences in the relative growth of some skull regions, in which humans produce a bulging in the top and the side of the head (the parietal and temporal regions), resulting in our globular brain shape.

The Timing of Life History Events An important marker of growth patterns and life history events is dental eruption schedules.9 The time of eruption of the first permanent upper molar (M1) is associated with the cessation of brain growth. In modern humans the M1 eruption mean times range between 4.74 and 7.0 years; in Homo erectus this number is about 4.5 years, closer to the typical number for wild chimpanzees, in which M1 erupts at about 4.0 years.

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As in other mammals, humans provide nutrition and immune protection to their young through lactation. This represents a major aspect of maternal investment, which also includes the delay in subsequent births. The termination of lactation and suckling, and with that the change to an adult diet, is called weaning. This enhancement of food processing abilities largely coincides with the appearance of a more permanent dentition. The eruption of the first molars, the first permanent teeth to emerge into the oral cavity in most primates, is correlated with weaning in many species. This correlation is weaker in hominoids, making it difficult to find a simple reconstruction of weaning in fossils with preserved dental eruption data. Based on the work of Adolph Schultz (1891–1976) at the University of Zürich, a relationship between the order of eruption of molars and second-generation nonmolar teeth (premolars, canines, incisors) and growth and maturation has been proposed for primates. Rapid growth, involving early sexual maturation and short life span, is correlated with early eruption of molars and late eruption of antemolars. Slow growth, on the other hand, is coupled with late eruption of the molars and early eruption of the secondary dentition. “Schultz’s rule” has been greatly scrutinized, and it has been found that exceptions abound. However, a general pattern does exist. Hominoids have lower mortality rates than the rest of the Old World monkeys. Early reproduction is common in the latter, whereas delayed reproduction into more mature ages characterizes hominoids. This basal dichotomy is reflected in the timing of dental eruption. The histology of teeth can also reveal information on the timing of life history events. This has traditionally been studied by cutting precious specimens. Today images derived from studies using synchrotron technology (a particle accelerator involving  

174  /  Mammalian and Human Development Rapidly growing mammal

Figure 47.  According to Schultz’s “rule,” fastgrowing mammals have molars that erupt early relative to the replacement teeth, whereas an early eruption of replacement teeth characterizes slow-growing mammals. Modified from Godfrey et al. 2005.

Set 1 Deciduos

Set 2 Molars

Set 3 Replacement Teeth

Time Slowly growing mammal

Set 1 Deciduos

Set 3 Replacement Teeth Set 2 Molars Time

magnetic and electric fields) can be used to reveal microscopic internal growth lines without having to use the more traditional and destructive approach of histological sectioning. By studying incremental growth lines in teeth, developmental rates and timings may be accurately established. Using this approach, it has been shown that australopithecines and early Homo possessed short growth periods, which were more similar to those of chimpanzees than to those of living humans. A main interest has been to establish when the modern condition of a relatively long childhood arose. This was addressed in the study of a fossil child from Morocco that lived about 160,000 years ago and its comparison with other fossil and living human populations. The fossil showed a degree of tooth development equivalent to living human children at the same age, about eight, and a modern human life history profile, with the modern condition of prolonged dental development. The individual development of cognition in the life of a human is another aspect fundamental to understanding our-

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selves, but unfortunately fossils provide little or no information in this area. As stated by Zollikofer and Ponce de León, “Here, the archaeological record might be more informative, as it represents a form of fossilized cognitive behaviour. Unfortunately, however, it remains tacit about the individual age of toolmakers.”

Ten

On Trilobites, Shells, and Bugs

So far I have mostly considered the evolution of vertebrate animals. There are many more living species of groups of animals other than vertebrates, and surely the same is true for extinct species. I aim in this chapter to present some of the discoveries in this area and the great potential the study of these animals has. To do justice to developmental paleontology in invertebrates, a full treatment of the subject would be necessary, and that is certainly not attempted here. The vertebrate skeleton, which is what is most commonly preserved as a fossil, is found inside the body and is thus an endoskeleton. Many other animals are characterized by an exterior exoskeleton, one that covers the soft parts. This is the case among arthropod animals such as the very species-rich insects, the lobsters and crabs, and the extinct trilobites. As I discussed before in relation to paleohistological studies, the endoskeleton of vertebrates is subject to continuing modification as the animal grows. The modification of existing parts 176

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in the endoskeleton of vertebrates is one of four fundamental kinds of growth patterns we can observe in animals. Adding layers during growth is another kind, this accretion being typical for mineralized shells. Fluctuations in the environment and life history of the individual are reflected in the rate and mode of this accretion. A pioneering study of this phenomenon led to the discovery that in the Devonian a year had about 400 days and in the Pennsylvanian some 387, as later confirmed by astronomers who found out that the earth’s rotation speed is slowing down. John Wells studied corals in the 1960s and noticed in them thin growth layers reflecting daily cycles but also thick layers reflecting annual ones. By bringing this information together, he made this amazing discovery. Another kind of growth is not via the addition of more layers but instead of more discrete parts, as when sea urchins grow a new plate in their shells or trilobites add a new body segment. The case of trilobites is particularly revealing of developmental evolution, as I discuss below. Trilobites, like other arthropods, also experienced molting. In this mode of development, the existing exoskeleton is repeatedly shed and a new one is grown. As, once formed, an exoskeleton cannot expand, the animal in question must pass through “soft-shell” stages in between replacing a smaller exoskeleton with a new, larger one. Absorbing minerals from the exoskeleton to be disposed of would be energetically sound, and it is in fact what happens in many living arthropods but apparently not in trilobites. Molting can produce fossils that can confuse even the expert. The exoskeleton can vary a great deal among stages, and for this reason many samples are needed to recognize that fossil samples of discontinuous clusters are in fact stages of the same species separated by gaps representing periods of growth.

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Trilobites! Very few groups of animals, perhaps dinosaurs and ammonites, can compete with trilobites in being the quintessential group of fossils. The exclamation point above is thus justified and refers to Richard Fortey’s book of the same title. This diverse group existed from some 526 million years ago in the Cambrian until the end of the Permian at about 252 million years ago, when the greatest mass extinction event affected the earth. The calcitic skeleton of trilobites makes good fossils. There are about 22,000 species described, and this large number of species and individual representatives offers the potential to explore developmental evolution at scales ranging from the population level to the overall history of a clade. The body plan of trilobites presents a head/trunk divide. The head bore paired antennae plus three other pairs of appendages. But it is the trunk that is the most relevant for developmental studies, as we can study the evolution of the number of trunk segments, their regionalization, and their modes of growth. There is an important trend in the evolution of trilobites’ trunk segments. In the early evolution of trilobites, during the Cambrian, there was much variation in numbers of those segments at maturity at the intraspecific, interspecific, and generic levels. Variation at these levels decreased in the later evolution of trilobites. It has been hypothesized that this change was a “hardening” of developmental systems, meaning increased constraints after canalization of development. After a time of evolutionary “experimentation,” the development became more or less fixed and must have involved Hox genes. As in vertebrates, in arthropods Hox genes are known to have an important role in the division of bodies into discrete segments, and one can assume

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that the control of segmentation and regionalization in trilobites could have been achieved similarly. The addition of segments in the body is terminal, and as a variety of molecules play similar roles in this process in insects and crustaceans, they probably also did in trilobites. In chapter 7 I examined how some groups of vertebrates have very plastic genetic mechanisms of segmentation, resulting in varied numbers of vertebrae, whereas other groups are very conservative. An analogous situation occurs in trilobites, and in fact Nigel Hughes, who has led many of the studies of their developmental evolution, has documented cases of much plasticity in segmental development in geologically younger forms. If there are constraints, they are not inviolable. Early in the evolution of trilobites there was little regionalization of the trunk—all the segments looked more or less similar. In later trilobites a change in the body plan led to increased regionalization. Different kinds of trilobites evolved independently a distinctive, segment-rich caudal plate consisting of numerous fused trunk segments, called the pygidium. This innovation had an ecological dimension: it made possible enrollment into an encapsulated defensive posture with all soft parts effectively protected. The protection against predators is likely to have been a major selective factor driving the evolution of enrollment. Segments in the new, enlarged caudal region were commonly distinctly different from the preceding trunk segments. In trilobites with this feature, the number of segments became less variable. In vertebrates an analogous situation exists. Animals with little or no regionalization in the vertebral column are more variable in their number of segments. This includes snakes and whales, both of which lack a hip girdle.  

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The difference between a stable and a variable number of segments in the trunk may seem trivial. But this is highly relevant to studies of development, as variation is the key to the potential to evolve. Plasticity in development can be a factor to consider when examining the potential risk of extinction in species or in groups of organisms. Researchers have found, for example, that trilobites showed declining plasticity across geologic time, and one wonders how this affected their evolutionary patterns, a matter of current investigation. The evolution of trilobites over time has also been studied using a different approach. Over decades numerous specialists have tried to reconstruct parts of the evolutionary tree of trilobites by examining features and comparing them among species and then conducting numerical analyses of them. For this, they use cladistic methodology, in which the distribution of features is optimized to produce the “best” evolutionary tree using the principle of parsimony. Basically that tree topology, providing the leading hypothesis of relationships, is the best possible explanation for the data, one for which the least number of assumptions need to be made (thus “parsimonious”). In coding a morphological feature for the analysis, it can be noticed that some species are constant for it. But other features may be variable within a species, cases of polymorphism. In 2007 Mark Webster published a study in which he quantified the degree of polymorphism within 982 species of trilobites across geologic time and found that older species, those closer to the base of the trilobite evolutionary tree, were more polymorphic than later, more derived species. Why does this clear pattern exist? It could have resulted from changes in the environment, which over time presented different selection pressures. Or it could be related to the “internal” tightening of the developmental system. Whatever

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caudal plate (pygidium)

Figure 48.  Two different body plans of trilobites. On the left, a case in which the whole trunk consists of more or less homogeneous segments to the end of the animal. This is Cambropallas telesto from the Middle Cambrian of Morocco. On the right, the most posterior segments are quite different and build a caudal plate, a case of regionalization. This is Zlichovaspis rugosa from the early / Middle Devonian of the Maïder region, Morocco. Photos courtesy of Christian Klug (Zürich).

the case, it is relevant that Webster discovered a pattern similar to that generally seen in segmental number over geologic time. In all these studies of evolution in geologic time, reliable species definitions are very important. In the case of the living, if species are defined based on reproductive isolation, experimental manipulation can put that isolation to test. On the other hand, species so defined are untestable in fossils. But the taxonomy of trilobites is on solid ground. Hundreds or thousands of specimens are studied, and the variation among them is measured. Consistent and reproducible criteria, which work for liv-

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ing arthropods, are used to define morphological species limits. Other invertebrate groups are also known from thousands of specimens, and studies of developmental paleontology are also possible.

Biomineralization The prolific biomineralization capabilities of several invertebrate groups make them suitable for paleontological studies, as the resulting shell has the potential for fossilization.1 Biomineralization has evolved many times independently in many kinds of organisms, and the paleontological signs of it should not be overlooked. 2 One classic example is the “Chalk” of southern England. This white Cretaceous limestone forms the white cliffs of Dover and the corresponding facing cliffs on the other side of the English Channel in France. At great magnification it can be seen that the Chalk is made up of millions of cocoliths, each a few thousandths of a millimeter across. These are produced by single-celled algae called coccolithophores. Some plants can also biomineralize. The process that produces silicates in algae, mollusc shells, and other carbonates in invertebrates is fundamentally analogous to that which produces the carbonate skeleton of vertebrates. Phosphate and carbonate salts of calcium are the most common biominerals. Organic compounds such as collagen and chitin are used in conjunction to provide structural support to bones and shells. The resulting materials have a complex architecture at the microscopic level, even at a nanoscale. These can result in outstanding wear or fracture resistance. Scientists studying materials and structures at the nanoscale have become very interested in these organic structures and are using

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sophisticated imaging techniques to reveal the structures that organisms, both fossils and living, have evolved. One aim is to obtain knowledge that can be applied in the artificial synthesis of organic-inorganic materials. At a more macro level, the evolution of biomineralization is also attracting more and more attention, as understanding it is fundamental in the study of life history evolution in vast groups of organisms that inhabit and inhabited the oceans (see chapter 6). Corals, prolific biomineralizing organisms, are of particular current interest. The increased atmospheric carbon dioxide levels increase the acidity of seawater, leading to the decalcification of carbonate skeletons. Can the resulting “naked” corals survive and resume calcification if atmospheric carbon dioxide levels decrease? What has occurred with corals in the geologic past when exposed to different selection pressures? Scleractinian corals present an example. Their ancestors were “naked,” anemone-like corals that survived the Permian mass extinction. The first scleractinians appeared in the Middle Triassic, being the first corals after the major extinction event at the end of the Permian. Until a recent discovery published by Jaroslaw Stolarski and colleagues, it had been assumed that scleractinian corals form purely aragonitic skeletons. But an exceptionally preserved fossil from the Upper Cretaceous possessed a purely calcitic skeleton. This suggests that these corals could form skeletons of different carbonate polymorphs, as do some other but not all groups of marine, calcium carbonate–producing organisms. The study of the geochemical properties of fossils has revealed unsuspected capabilities to change a biomineralization system. What determines that flexibility? As in the case of trilobites discussed above, not all groups were equally flexible, or “plastic,” developmentally. How this affected past patterns of evolution  

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and may affect the future of current marine ecosystems can be studied in shelled organisms.

On Mollusc Shells Thanks to biomineralization, the shells of molluscs make good fossils. These are known by the thousands in paleontological collections, reflecting an abundance of species and specimens and thus permitting comprehensive studies of evolutionary patterns across geologic time. To take advantage of this rich source of information, we must be able to characterize morphologically and taxonomically that diversity, by naming species and positioning them in robust phylogenetic trees on which to examine patterns of evolution. The problem is that each shell has few discrete morphological characters that serve to characterize it, and convergences in form and ornamentation are paramount in the fossil record. The comparison of different clades of molluscs, like ammonites and gastropods, for instance, has shown that common generative rules underlie the morphogenesis and growth of the shell. As the mollusc shell is developmentally highly integrated, most shell features often co-vary with others within species. This high level of integration makes it difficult if not impossible to define properties that are totally independent from others—but it also means that by developing the proper models, we could predict much about the evolution of shell shape. This has been intensively studied in the most famous fossil molluscs, the ammonoids. They constitute a completely extinct group of cephalopods, the group to which octopuses and squids belong. More distantly related to the rest is Nautilus, also a cephalopod, in fact the only living one with an external shell.  

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The ontogeny of the ammonoid shell has been intensively studied, and three basic aspects of it have been identified: secretion of shell as the soft body increases in size, secretion of additional layers in the inside surface of the body chamber, and secretion of septa at the rear of the body, thereby forming chambers. The first step in the ontogeny of ammonoids was the embryonic stage, which possessed a shell, called ammonitella. Fossils of these are little knobs found in exceptional fossils at the start of the spiral or as lost structures in the corner of a museum cabinet. As the shell grows, ornamentation, if present, grows in complexity. Ornamentation refers to a range of features, such as concentric and longitudinal ribs, spines, tubercles, and keels. Large marks in some ammonoid shells suggest that some shell resorption must have occurred, as they demarcate discontinuities that affect growth lines. Ornamentation in ammonoids has been used for taxonomic studies, but as has been known for a long time its degree is correlated with other shell features. Most ornate species are the most evolute, possessing almost circular whorls. This correlation has become known as Buckman’s law, after the author who first published about this idea (1892). Øyvind Hammer and Hugo Bucher concluded that the correlation patterns work well within species but less well among species. They showed using computer modeling the geometrical properties of the system that results in the coupling of development of ribs to shapes of the shell aperture. Understanding shell geometry, not only of ammonoids but also of molluscs in general, has occupied many paleontologists for a long time. In the 1960s, using an oscilloscope, David Raup pioneered the computer parameterization of shell coiling, a work that provided a basis for the emergence of the field of theoreti-

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Figure 49.  Computer models by Hammer and Bucher (2005) of hypothetical ammonoid shells, illustrating the correlation of features, with Buckman’s law as a case of proportionality. Lateral (top) and apertural (bottom) views. A: Laterally expanded (depressed) shell, in which the lateral ribs get proportionally stronger. B: Laterally compressed shell by scaling of the lateral axis, with corresponding weaker lateral ribs. C: Ammonoid with circular shell tube and equal amplitudes of lateral and ventral ribbing. As the ventral rib amplitude stays constant under lateral scaling, a variation in the ratio between ventral and lateral rib amplitude results. Modified from Hammer and Bucher 2005.

cal morphology. His and other early methods were mostly twodimensional and assumed the existence of a coiling axis, which does not have a real biological meaning since it emerges a posteriori as a result of accretionary growth. Also, many shells cannot be viewed as being coiled around a single coiling axis. Traditional models did not consider the ontogenetic changes of the

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A

B

0.5 mm

C

1 mm

D

5 mm

10 mm

Figure 50.  Schematic drawings of four stages in the ontogeny of the late Cretaceous ammonoid Hoploscpahites nicoletti, in lateral view. A) ammonitella; B) neanoconch, the first postembryonic time; C) juvenile; D) adult. Scale bars = 5 mm. Notice the increasing degree of ornamentation. The juvenile shell is more compressed and involute than the neanoconch. Modified from Bucher et al. 1996.

shell or the timing of growth processes. Newer approaches try to address these issues. One recent model developed by Séverine Urdy and colleagues simulates the shape of the aperture and nonlinear allometries during growth. How these allometries change can be explored by varying the parameters of the model. The aim is to understand the rules that may account for some recurrent evolutionary patterns and for intraspecific variation. The biological aspect of these studies of growth involves the close examination of the mantle, the soft and elastic tissue that secretes the shell. The mantle does not fossilize, but any studies of its properties and capabilities and phenotypic plasticity

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during the individual’s lifetime should be of interest to paleontologists. Fossils provide a huge data set of morphology that can be quantified with ever more sophisticated and realistic morphometric methods. An example is a method used by Claude Monnet (no relation to the painter) and colleagues. From the three-dimensional acquisition of images using a micro-CT scan, morphometric parameters are derived and used to describe the geometry of mollusc shells throughout their ontogeny and to make comparisons across species. A “skeletonization” of the 3-D virtual shell allows the extraction of a centerline, used as a reference to cross section the shell and analyze the shape of the tube using geometric morphometrics. With the resulting parameters ontogenetic trajectories of different individuals can be compared. Analogous methods have been used by Chris Kruszyński and colleagues to quantify morphological variation in scleractinian corals. Whatever models are developed to understand the evolution of shell shape, they should take into account the environment, as it has been shown experimentally and in natural populations that this affects growth rate. The external variables include food supply, substratum type, salinity, dissolved oxygen, turbidity, temperature, population density, and ecological interactions. For instance, living species of gastropods may slow their rate of growth in the presence of predators, turning an excess in shell material production into local shell thickening. Increase in relative shell thickness, a feature often viewed as a defense mechanism, is also induced by starvation. This is another example of the phenotypic plasticity and the range of phenotypes associated with a genotype I discussed in chapter 2. One of the basic life history parameters that is very much affected by the environment is longevity.

On Trilobites, Shells, and Bugs  /  189

Long- and Short-Lived Clams Longevity is a fundamental variable of life history. By counting annual layers derived from accretionary growth, it is possible to estimate the longevity of dead (including fossil) individuals. The study of living species has shown that longevity is generally affected by the temperature in which animals live. This other variable can also be estimated for fossil samples. Organisms that inhabit higher latitudes tend to live longer, which is related to temperature. In body temperatures at the level of the cold southern regions of the oceans chemical reactions take place at low speed. Metabolic exchanges are thus also slow, resulting in a life without stress. More or less constant water temperatures and salt content present no major challenges to the regulatory mechanisms of the cells. Any metabolic process produces side products, chemicals called radicals, in each cell, which gains its energy with the help of oxygen. Lower metabolism, in the cold, produces fewer damaging side products that need to be processed or eliminated. The less an organism has to suffer stress factors, the longer it can live. For some marine invertebrates, a cold environment can serve to avoid dangerous radicals. Many species have evolved other methods to prolong their life. For example, the ocean quahog or clam (Arctica islandica), a bivalve mollusc, digs itself into the oxygen-depleted depths of the ocean floor for a few days. There, it turns off its metabolism and its heart beats only one-tenth of its normal speed. When it comes out of this state, the mitochondria start to function normally, producing the radicals again. But at the same time some genes become active and produce enzymes that combat the dangerous new chemicals produced by high metabolism. With this strategy this bivalve mollusc can

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reach an age of more than two hundred years. Vertebrates do not have this option. Instead of decreasing the metabolism, under lower oxygen availability the mitochondria produce even more radicals. Patterns of growth and their relation to temperature have been studied in numerous fossils, for example, in the clam Cucullaea raea, from Eocene rocks of Seymour Island on the Antarctic Peninsula. During the Eocene temperatures were much warmer than the below-freezing temperatures that exist today. The clam shells grew very slowly and only during the Austral winters of total darkness. Surprisingly, they stopped growing entirely during the Austral summer, when food was more abundant, probably because they were putting all their energy and resources into reproduction. Due to their slow metabolism and growth rates, these clams were extremely long lived. Some had growth lines representing more than one hundred years. Like Arctica islandica, they lived longer than most humans.

Unusual Preservation Trace fossils are almost the only records of responses of the soft-bodied biota or of the soft parts of organisms. Luckily, just almost. Preservation of invertebrates goes beyond the usual exoskeleton or shells in some rare fossil sites: the finest details of the entire body, including eyes and appendages, are fossilized in different stages of development. Their discovery and study are difficult, as they are usually fragile and small. But with new imaging techniques and three-dimensional reconstruction computer programs, much new information is being discovered. The sites are all over the world and include the Crato Formation in the

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Cretaceous of Brazil, Solnhofen in the Jurassic of Bavaria, the Rhynie Chert in the Devonian of Scotland, and the “Orsten” Lagerstätten worldwide, best known from Sweden and expanding from the Lower Cambrian to the Lower Ordovician. The discoveries and descriptions of the ontogenetic stages of so many taxa are rapidly enriching the literature. In years to come the accumulation of this information and the synthesis and analyses of these discoveries will surely greatly influence our understanding of the earliest phases of evolution of several arthropod groups. Several international research groups, such as those of Mark Sutton and Derek Briggs, use sophisticated three-dimensional reconstruction software to study diminutive and fragile fossils containing rich morphological information. The example I mention here concerns an early crustacean from the Middle Cambrian of Sweden, Henningsmoenicaris scutula. Joachim Haug and colleagues identified ten ontogenetic stages of this animal and created what they like to call a “4-D model,” the fourth “dimension” being deep time. These stages document the timing and mode of addition of segments and their appendages. The first stage has four appendage-bearing segments; this number increases to seven, after which a differentiation of the regions of the trunk occurs. Haug and colleagues documented the development of compound eyes, first recognized in the fifth stage of the total of ten. Each of the subsequent stages documents the change from sessile to stalked eyes. The beautiful morphology gives us not only an aesthetic depiction of changes in form some 520 million years ago but also relevant data to understand the early branching events in the evolution of crustaceans and other arthropods. Which modes of development characterized the origins of major

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Figure 51.  A 4-D model of Henningsmoenicaris scutula, a stem crustacean from the Cambrian of Sweden. Figure courtesy of Joachim Haug (New Haven).

arthropod groups, including trilobites? Are shared developmental systems a sign of evolutionary relatedness, or have these evolved independently in different groups? Haug and colleagues noticed that the pattern in which posterior trunk segments fuse in Henningsmoenicaris during ontogeny is also present in trilo-

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bites: new segments appear and are conjoined to the next anterior segment, contrary to the pattern of later crustaceans. These and other aspects of relative timing of ontogenetic events can be mapped onto evolutionary trees to trace how conserved or plastic development has been in the earliest phases of multicellular animal evolution.

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Epilogu e Is There a Moral to Developmental Paleontology?

The history of life is a history of change, and much of that is recorded by fossils in deep time, in which a vast diversity of organisms originated and waned. Is there a moral message to be drawn from this? Of course not. There is no moral intrinsic to a scientific fact or hypothesis. Not so long ago our understanding of evolution, including that of humans, was dominated by the idea of the selfish gene. More recently biological anthropologists have demonstrated that we humans are cooperative great apes and that this is biologically ingrained. This new knowledge of biology does not change the moral imperative we freely choose to guide us. Since all is change and since we will sooner or later be doomed, both individually and as a species, what is the point? Or forgetting the vastness of time—since we humans are nothing else than very singular great apes, nothing else than biology—why fight against our “nature”? Albert Camus saw comfort in the drive to keep going in spite of his existentialist conception of life. Sisyphus was condemned for all time to push a boulder  

 

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uphill, one that repeatedly rolled back to where it started. Let’s enjoy the pushing. Biology teaches no existential lessons but can lead to reflection. The vastness of time and the realization that the vastness of biodiversity makes us just one species in a huge tree of life inspire modesty. The vastness of life colors and change—that greatest show on earth—inspires awe. Environment and development are intertwined. The phenotype is not simply the result of the genotype. The environment can drive change in development; even fossils, as incomplete as they are, show this if one knows how to read them. We humans represent only one branch of the huge tree of life—but one with the capacity to modify the environment with a speed that until now only major geologic events were capable of achieving. How we continue to influence the environment will determine the fate of all ontogenies around us: with modesty regarding what each of us can achieve, maybe acting locally to make a small contribution, driven by a moral imperative, independent from, or even in spite of, biology, chemistry, and physics.  

 

 

Notes

Chapter 1: Fossils, Ontogeny, and Phylogeny 1.  Metaphors analogous to the monkey typewriting concept have been used for a long time by antievolutionists. Georges Mivart, in his 1871 anti-Darwin book, On the Genesis of Species, stated: “There are improbabilities so great that the common sense of mankind treats them as impossibilities. It is not, for instance, in the strictest sense of the word, impossible that a poem and a mathematical proposition should be obtained by the process of shaking letters out of a box; but it is improbable to a degree that cannot be distinguished from impossibility” (65). 2. Sober’s Evidence and Evolution (2008) presents a discussion of evolutionary probability and the hurricane-in-a-junkyard analogy. 3.  The pre-Darwinian discovery of “deep time” was discussed by Gould in Time’s Arrow Time’s Cycle (1988). 4.  A discussion of the oldest fossils of life is presented in Brasier et al. 2002; and of the oldest multicellular life, in Lin et al. 2006 and Maloof et al. 2010. 5.  An explanation of the calculation for the estimated percentage of extinct species and other relevant figures concerning the magnitude of biodiversity can be found in Benton 2009a. 197

198  /  Notes to Chapter 1 6.  The preservation of colorful feathers is reported for some dinosaur species, including Anchiornis huxleyi (Li et al. 2010) and Sinosauropteryx prima (Zhang et al. 2010). 7.  Cuvier was born in Montbéliard, France, close to the Swiss border, which shortly before his birth belonged to Württemberg. For a comprehensive biography, see Taquet 2006. 8.  The actual quote from Ernst Haeckel (1834–1919), from 1866, is “Die Ontogenese ist eine kurze und schnelle Rekapitulation der Phylogenese, bedingt durch die physiologischen Funktionen der Verer­ bung (Fortpflanzung) und Anpassung (Ernährung) [The ontogeny is a short and rapid recapitulation of the phylogeny, determined by the physiological function of heritability (reproduction) and adaptation (feeding)].” The term Phylogenese was introduced by Haeckel, as was the German equivalent of “ecology” and other terms. Another very influential German biologist, Willi Hennig (1913–76), is known for a large body of influential terminology in systematics, the field of biology devoted to the reconstruction of evolutionary trees and classification. It is no coincidence that these and other Germans are responsible for so many of the fundamental terms used in biology today. New ideas require new terms. 9.  Richards discussed the German terms Evolution and Entwicklung in The Meaning of Evolution (1992), which provided much historical information and interpretation on the morphological tradition in Europe as it relates to evolution and development. 10.  A. W. Crompton worked in the mid-twentieth century on early mammals from the Karoo Basin in South Africa, a region known for the richest records of early mammalian origins in the world. Crompton was born in Durban in 1927 and did his studies in Stellenbosch and then Cambridge. After serving as director of the South African Museum in Cape Town for many years, he moved to the United States, where he was a professor at Yale and then Harvard. I had the chance to meet Professor Crompton in summer 1995 at a party hosted by one of my Ph.D. advisors at Duke University, Kathleen Smith, who in turn was advised by Crompton at Harvard. My other advisor at Duke, Rich Kay, has told me several times how influential Crompton’s work had been for his Ph.D. work. So on both sides Crompton is my academic grandfather.  

 

Notes to Chapter 1  /  199 11.  Comparisons between embryos and adults are tricky, and the careful study of anatomical detail very often reveals significant differences (Meng, Wang, and Li 2011). The double jaw articulation of Diarthrognathus is expressed in its name, but how exactly such a double articulation functioned is not totally clear, although well-founded speculation has been presented (Crompton and Hylander 1986). Luo et al. (2007) discussed how an ossified Meckel’s cartilage and a relatively large middle ear could have worked in Mesozoic early mammals called eutriconodonts, in particular in Yanoconodon from China. A review of this and related subjects is presented by Luo (2011). A functional undertstanding of the jaw biomechanics in a marsupial pouch young has never been attempted. 12.  I use the term amphibians to refer to any nonamniotic limbed vertebrate. I have opted to use a non-monophyletic term in this case because of the lack of a better term. For alternative views on extant amphibian origins, see Anderson et al. 2008; Marjanović and Laurin 2009; and Sigurdsen and Green 2011. 13.  For a discussion on the kinds of environments that temnospodyls inhabited, see Laurin and Soler-Gijón 2010. Many of them most likely tolerated saltwater. 14.  Concerning the size of temnospondyls, see Steyer and Damiani 2005. 15.  Richardson and colleagues have compared different kinds of vertebrates and even quantified morphological change; they found no support for either recapitulation or the idea of phylotypic stage (Bininda-Emonds, Jeffery, and Richardson 2003). Two recent works claimed that there is a kind of phylotypic stage at the genomic level of development, providing extensive data and analysis for species of the fly Drosophila (Kalinka et al. 2010) and for the zebrafish, Danio (Domazet-Lošo and Tautz 2010). These original works at the genomic level concerned closely related species, whereas the morphological work these authors used to compare their molecular findings dealt with very widely divergent taxa, such as vertebrates as a whole (as opposed to species of a genus of fly). More recently, Irie and Kuratani (2011) examined the phylotypic period issue by comparing transcriptome similarity, using four different statistical tests, in the mouse (Mus

200  /  Notes to Chapter 1 musculus), the chick (Gallus gallus), a frog (Xenopus laevis), and the zebrafish (Danio rerio). They compared the set of all RNA molecules produced in the entire population of cells at a given time, reflecting thus the genes being actively expressed at that stage. Irie and Kuratani (2011) concluded that the highest degree of similarity across species occurs at the time of the stages between neurula and pharyngula. 16.  For a somewhat dated but still current discussion of false dichotomies, relevant to understanding the concept “ecological niche” as not totally independent of the organism, see Levins and Lewontin’s 1987 The Dialectical Biologist. 17. Forms of teleological thinking dominated much of AngloAmerican post-Darwinian thought around 1900 and in the first decades of the twentieth century (Bowler 1983). 18.  Rieppel and Kearney (2002) presented a thorough discussion of the virtues of careful analysis of complex morphological features to be used in analysis of evolutionary relationships. 19.  For an aesthetic and unproblematic example of atomization, this time in novelle vague cinema, see Brigitte Bardot in the opening scene of Jean-Luc Godard’s Le Mepris (1963).

Chapter 2: Evo-Devo, Plasticity, and Modules 1.  The concept “evolutionary innovation” is treated at length by Gerd Müller and Stuart Newman (2005), who discussed their views on the importance of self-organization in the origin of form and the qualitative difference between innovations and the evolution of new features. In a recent and ambitious book, A. Wagner (2011) presented a comprehensive exposition with examples of a research program about the principles and the bases of a theory of evolutionary innovation. This book is mostly concerned with genotype networks. 2.  Duboule (2010) used the passing comet metaphor to refer to evodevo. Discussions of the goals of evo-devo can be found in one of the founding textbooks of Hall (1999) or in Raff’s The Shape of Life (1996). Hendrikse, Parsons, and Hallgrímsson (2007) proposed “evolvabil-

Notes to Chapter 3  /  201 ity” as the main subject, whereas Müller (2007) proposed evolutionary innovations. Olsson, Levit, and Hoßfeld (2010) presented a historical overview concentrating on German and Russian pioneers of evo-devo themes since the time of Ernst Haeckel. 3.  A central issue for Schmalhausen (1884–1963) was the reaction norm of Woltereck (1909), the phenomenon that one and the same genotype is able to produce different phenotypes, depending on external environmental inputs (Schoch 2009). 4.  I follow some colleagues in making a distinction between variation and variability. The observed differences constitute the variation, whereas variability is the tendency of a system to generate differences (Wagner, Booth, and Bagheri 1997). 5.  Renesto (2005) argued against Wild’s (1974) interpretation of caudal autotomy of the prolacertiform reptile Tanystropheus, pointing out the lack of evidence for fracture planes in the caudal vertebrae.  

Chapter 3: Fossilized Vertebrate Ontogenies 1.  The incubation time is highly variable among bird species and is one of the features coupled with the altriciality/precocity spectrum in these animals. The incubation length of the ostrich, Struthia, is about 42 days, whereas that of the chicken is 21. Although the kiwi, Apteryx, is the smallest closest relative of the large flightless birds, at 80 days it possesses the longest incubation of any ratite. 2.  Much about the life history of Massospondylus is known, based on numerous skeletons representing different growth stages. For information on Massospondylus, see Chinsamy-Turan 2005. 3.  It is unlikely that some of the fine aspects of reproductive plasticity of extinct vertebrates will ever be described and demonstrated on a sound basis. Extant clades of reptiles can show peculiar reproductive modes. An example is the extant lacertid lizard Zootoca vivipara, which is reproductively bimodal; even if it is generally viviparous, some populations at the southern periphery of its range were reported to be oviparous (see, e.g., Surget-Groba et al. 2006). This indicates that

202  /  Notes to Chapter 3 viviparity and oviparity are biological traits that might be related in some clades, and also within a single species, to the evolution of local ecological conditions. 4.  The placoderm fish with clasperlike appendages is Incisoscutum ritchiei (Ahlberg et al. 2009). The oldest record of viviparity was reported by Long et al. (2008) in a placoderm female of Materpiscis attenboroughi. A review of the significance and diversity of the extraordinary Gogo Formation from Western Australia is presented by Long and Trinajstic (2010). 5.  Lee (2009) conducted a comprehensive analysis of molecular and morphological data to review the affinities of snakes with other squamates and found mosasaurs to be indeed more closely related to snakes than to any group of lizard. 6.  Skeletal features have been argued to be indicative of different reproductive strategies. For example, the narrow pelvic canal and fused pubic symphysis of the Multituberculata, a large and extinct mammalian clade, is claimed to suggest they gave birth to altricial offspring rather than laying eggs. 7.  The discussion on the constraints or limits for viviparity in birds reminds me of that about the “extinction” of dinosaurs. Several hypotheses have been postulated. A role for a large asteroid hitting the earth in what is today the Yucatán Peninsula must have been a factor (Schulte et al. 2010), together with a high degree of volcanic activity, which produced dramatic climatic changes leading to a cascade of extinction-driving events over a period of years. 8.  The universality of the lack of viviparity applies also to crocodiles and turtles, and some of the explanations suggested for birds do not apply to these two other groups. Blackburn and Evans (1986) presented a critical review of the potential reasons for the lack of viviparity in birds, all pointing to basic physiological or biomechanical factors that somehow constrain or limit the potential evolution of a new reproductive strategy. 9.  The oldest papers discussing dinosaurian eggshells were published around the middle of the nineteenth century. Since then, a large body of discoveries and data on eggshell diversity and ultrastructure has accumulated (Carpenter 1999).

Notes to Chapter 4  /  203 10.  For a summary of reproductive strategies in amphibians and reptiles, see Zug, Vitt, and Caldwell 2001. For a recent review of reproductive strategies in fishes, see Cole 2010. 11.  Olson (1979) discussed evidence that Trimerorhachis most likely practiced mouth brooding. Witzmann (2009) reported on a specimen of the temnospondyl Apateon gracilis from the early Permian in Saxony with a nearly complete conspecific in its digestive tract, a case of cannibalism. 12.  Franzen (2006) reported on a pregnant specimen of the “early horse” Propalaeotherium voigti from the Middle Eocene of Eckfeld, Germany, with preserved soft tissue structures interpreted as remains of a placenta. 13.  A synchrotron “is an apparatus for imparting very high speeds to charged particles by means of a combination of a high-frequency electric field and a low-frequency magnetic field” (Merriam Webster’s Collegiate Dictionary, 10th ed.).

Chapter 4: Bones and Teeth under the Microscope 1.  Considering the importance of Wilhelm His in the invention of the microtome and the discoveries concerning animal cells, it is an odd coincidence that the study of tissues is called histology, which derives from the Greek his, meaning “tissue.” 2. Peter Forey presented a detailed account of Sollas and his method in the newsletter of the paleontology department of the Natural History Museum, London (vol. 3, no. 1 [2005]; www.nhm.ac.uk/ resources-rx/files/set-in-stone-3–1–17163.pdf). 3.  For an overview of the fossil site of Urumaco in Venezuela and information about the paleobiology of Stupendemys and many other Neogene vertebrates, see Sánchez-Villagra, Aguilera, and Carlini 2010. 4.  Collagen fibers are not always destroyed during fossilization. For example, Devonian fossils like Eusthenopteron can retain a wellpreserved collagenous matrix (Zylberberg, Meunier, and Laurin 2010). 5.  For a review of the function of osteoclasts, including the molecular level, see Witten and Huysseune 2009.  

 

204  /  Notes to Chapter 4 6.  Katsnelson (2010) summarized some recent developments in the study of the relationship between metabolism and bone growth. 7.  Much clinical and medical literature exists on the decrease in bone mineral density during pregnancy; see, e.g., www.ncbi.nlm.nih. gov/pubmed/10548640. 8.  Monty Python’s description of sauropod dinosaurs may be familiar: “thin at one end, much much thicker in the middle, and then thin again at the far end” (www.youtube.com/watch?v = cAYDiPizDIs). 9.  For a study of Tyrannosaurus, see, e.g., Erickson et al. 2004. 10.  For a popular account of the case of the kakapo, see Adams and Carwardine’s Last Chance to See (1990). 11.  Monte San Giorgio is one of the most important localities for marine reptiles in the world, one of the reasons it was listed as a UNESCO World Heritage Site in 2003. The many decades of collecting there have uncovered a diverse fauna of fishes and reptiles such as ichthyosaurs, placodonts, thalattosaurs, protorosaurs, rauisuchids, and nothosaurs (Furrer 2003). Ontogenetic series are known from mainly three groups from Monte San Giorgio, the pachypleurosaurs, the nothosaurs, and the ichthyosaurs. In the ichthyosaur Mixosaurus cornalianus prenatal and postnatal ossification patterns have been studied in some detail (Brinkmann 1996). In nothosaurs, especially in the smallsized pachypleurosaurs, embryos have been described within gravid females, as well as isolated outside of the adult female body (Sander 1988). Some of the species from Monte San Giorgio represented by exceptionally well preserved ontogenetic series have been the subject of detailed morphometric and descriptive morphological studies (e.g., Sander 1989 on Neusticosaurus peyeri). However, controversy exists about the taxonomic significance of some of the series of specimens, with debates about the validity of new species versus the alternative of ontogenetic variation (e.g., O’Keefe and Sander 1999). In cases where the evidence is less unequivocal, there is still the issue of not having an independent test of the validity of the growth series as such. Paleohistology can provide such a test (Scheyer, Klein, and Sander 2010). 12.  A correlation between gene duplications and complexity in specific regions of the body has been searched for in many groups of

Notes to Chapter 4  /  205 organisms. It has been reported for eye development and phototransduction across multicellular animals. Genes duplicated at a higher rate in the group with the greatest variety of optical designs, the Pancrustacea (Rivera et al. 2010). 13.  Zerina Johanson has made major discoveries about the developmental origin of some anatomical structures in placoderms, a group close to the basal node between jawless and jawed vertebrates. Growth stages of Cowralepis mclachlani preserve portions of the branchial skeleton, which, because of their topographic relations to hypobranchial musculature and late ontogenetic occurrence, are significant—illustrating potential embryonic origins from the neural crest and the formation of vertebral elements. The Merriganowry quarry in New South Wales contains thousands of layers in fine-grained shales with many placoderms—and the expectations for preserved ontogenies are high. 14.  Conodont elements, the “teeth” of very basal vertebrates, traditionally have been studied in biostratigraphy, and the extraction from the rock of these noncalcareous microfossils, made up of the mineral apatite, usually involves the use of an acetic acid solution. Concerning the position of conodonts in the tree of life, see Turner et al. 2010 for alternative arguments. 15.  Teeth, like many aspects of the skeletal anatomy, derive developmentally at least in part from ectomensenchymal cells. These are pluripotent cells that originate in the neural crest and migrate to a number of sites in the embryo, differentiating into a range of derivatives that include cartilage-forming cells called chondroblasts, boneforming cells called osteoblasts, odontoblasts (which produce the dentine of teeth), and cells of the connective tissue. The genetic pathways are similar, and all involve a molecule called ectodysplasin. 16.  In some clades of mammals both cement and dentine markings provide reliable estimates of age, whereas in others one of these two tissues or neither of them does. Klevezal (1996), a translation of a work originally in Russian, extensively examines technical aspects of age determination in many kinds of mammals. 17.  Azorit et al. (2004) studied the red deer Cervus elaphus and discussed methodological considerations important for a skeletochro 

 

206  /  Notes to Chapter 4 nology based on dental markings. Discrepancies in age estimates can result from seasonal nutritional fluctuations or geographic and physiological differences among species, but the most important source of discrepancy is the lack of a standardized method to count dental marks. They reported that precise age estimation was different among teeth, being more reliable in molars than in incisors and recommend that the aging procedure should be assessed for each tooth type and each species and, when possible, different populations. 18.  Anders et al. (2011) introduced a reference system of relative age classes in which to place wear stages across extant and extinct mammals. 19. The medial rotation of the upper teeth during the life of Hyaenodon was reported by Mellett (1969).

Chapter 5: Proportions, Growth, and Taxonomy 1. Thompson’s On Growth and Form greatly influenced the work of Claude Lévi-Strauss in providing one of the tenets of structuralism in anthropology, transformation (Wilcken 2010). 2.  For an introduction to morphometric methods and their use in paleontology, see the excellent series of contributions by Norm MacLeod in the Palaeontology Newsletter of the Palaeontological Association: www.palass.org/modules.php?name = palaeo_math. 3.  Gayon (2000) discussed in detail the history of the concept of allometry and the several forerunners of Huxley and Tessier in this regard. 4.  A major advance was the multivariate generalization of allometry introduced by Jolicoeur (1963). 5.  G. G. Simpson (1953: 259) already discussed the nonlinearity of the horse fossil record in his classic work, Major Features of Evolution. 6.  Consideration of ontogenetic changes has led to taxonomic revisions of several taxa, including, among many others, ground sloths (Cartelle and De Iuliis 2006), endemic ungulates from South America (Billet, de Muizon, and Quispe 2008), and ichthyosaurs (Motani and You 1998).

Notes to Chapter 6  /  207

Chapter 6: Growth and Diversification Patterns 1.  A review of the “Red Queen” versus “Court Jester” model was presented by Benton: “The Red Queen Model [Van Valen 1973] stems from Darwin, who viewed evolution as primarily a balance of biotic pressures, most notably competition, and it was characterized by the Red Queen’s statement to Alice in Through the Looking-Glass that ‘it takes all the running you can do, to keep in the same place.’ The Court Jester model [Barnosky 2001] is that evolution, speciation, and extinction rarely happen except in response to unpredictable changes in the physical environment, recalling the capricious behaviour of the licensed fool of Medieval times. Neither model was proposed as exclusive” (2009b: 728). For case studies in which the alternative models were explored, see Barnosky 2001; and Goin, Abello, and Chornogubsky 2010. 2.  For a vivid and superbly described account of the Deccan traps and vulcanism, see Fortey, Earth: An Intimate History (2004). 3.  In the lab of Karen Sears (www.life.illinois.edu/sears/Home.html) much work is being done on the developmental bases of the differences among mammalian species limbs (see also Richardson et al. 2009). 4.  For an account of the evolution of argyrolagid marsupials, see Simpson 1970 and Sánchez-Villagra et al. 2000. 5.  A popular book-length introduction to the subject of evolution on islands is Quammen’s The Song of the Dodo (1997). 6.  Van der Geer and colleagues (2010) presented a thorough survey of the evolution of island mammals in which numerous examples of rapid evolution are discussed and the original references cited. In their compendium the ecological relevance of the morphological traits of the island species is discussed in the context of paleoecological data. 7.  Millien (2006) examined the literature on the fossil record of mammals, combined her findings with data from living species, and calculated that in mammals the rates of morphological evolution are greater for islands than for mainland populations by a factor of up to 3 to 1. 8.  In some islands or island groups adaptive radiations have been documented (Losos and Ricklefs 2009). In these cases life history traits

208  /  Notes to Chapter 6 can be diverse in the clade in question. This is the case in the Madagascan tenrecs, a group of about thirty living species that are most closely related to golden moles, belonging to the mammalian clade Afrotheria. Some tenrec species reach sexual maturity at the age of only about forty days. Others mature rather slowly. Some of them produce large litters—one species can carry as many as thirty-two fetuses, an extreme number for mammals—and other species produce litters as small as one or two. Some have a very high metabolic rate, whereas some do not (Nowak 1999). 9.  Several dinosaur species are also claimed to be examples of dwarf forms that lived on islands (see references in Sander et al. 2010; Stein et al. 2010). 10.  Leroi (2003) and Blumberg (2008) explained the developmental anomaly of cyclopy in humans. 11.  For models of metabolic expenditure and growth applicable to diverse kinds of animals, see Hou et al. 2008. 12.  Jacob et al. (2006), among others, argued that Homo floresiensis is a population of pygmies with a pathological condition. Lieberman (2009) presented a general overview of the significance of H. floresiensis. 13.  Apparently mature body size is more responsive to artificial selection by livestock breeders than are many features of relative growth or body composition (Roth 1992: 281).  

 

Chapter 7: Fossils and Developmental Genetics 1.  For an account of Kuratani’s work on evolutionary morphology, including entertaining essays with personal anecdotes, see www.cdb. riken.jp/emo/clm/0706n.html. 2.  Asher and Lehmann (2008) reported on the coincidence of the supernumerary presacral numbers of afrotherian mammals with late dental eruption in that clade and the presence of a similar phenotypic suite in humans with the genetic pathology cleidocranial dysplasia. Both vertebral count and dental eruption can be studied in fossils, and the examination of well-preserved stem members of the relevant

Notes to Chapter 8  /  209 groups could reveal fundamental changes in developmental patterns in placental evolution. 3.  With increased regionalization development becomes less plastic. The same holds true for the pattern of segmental evolution in trilobites. The earliest trilobites evolved changes in the number of segments much more often than later trilobites, which showed more regionalization in their segments (Hughes 2005). 4.  Sire, Donoghue, and Vickaryous (2009) reviewed the general reduction of the exoskeleton in many lineages of Silurian and Devonian fishes. In sturgeons and paddlefishes (acipenseriforms) the full squamation documented in specimens from the late Cretaceous was reduced to five rows of scutes in the extant species (Grande and Hilton 2006). 5.  In some cases phenotypic convergence among far-related taxa is paralleled by molecular convergence (Gompel and Prud’homme 2009). 6.  Inferences on developmental genetic evolution on fossil stickleback fishes were made by Bell (2009), who has contributed to making these fishes a great model of developmental evolution.

Chapter 8: “Missing Links” and the Evolution of Development 1.  For a discussion of the importance of stem groups and a historical account of the origin of this concept, see Donoghue 2005. 2.  Blumberg (2008) provided a short but useful account of Goldschmidt and his ideas in his book on developmental abnormalities in the context of evolutionary developmental biology. In Pere Alberch’s perhaps most admired paper, “The Logic of Monsters,” published in 1989, an integrative and currently more accepted view of the topic pertaining to Goldschmidt and evolutionary innovations was presented. 3.  Hypotheses on the position of turtles within the amniote tree of life are highly contested, despite various efforts over the past century to solve this major issue in vertebrate evolution. My former Ph.D. student Ingmar Werneburg argued for a basal position of turtles within reptiles, sister group to the Archosauria/Lepidosauria clade (Werneburg and Sánchez-Villagra 2009). The analysis confirms some previous

210  /  Notes to Chapter 8 work on vertebrate phylogeny (e.g., Gauthier, Kluge, and Rowe 1988; Laurin and Reisz 1995) but stands in contrast to most but not all recent molecular studies that indicate a potential turtle-archosaur relationship. Among extinct reptilian clades, several groups have been hypothesized to be close turtle relatives (Lyson et al. 2010). 4.  One may reasonably interpret the fact that the skull of Odontochelys is anapsid as support for or at least consistent with the hypotheses that place turtles outside Diapsida. 5.  The osteosclerotic bones of pakicetids indicate that they were already at least amphibious.

Chapter 9: Mammalian and Human Development 1.  Reisz and Müller (2004) provided a review of the oldest fossils of several groups and discussed matters relating to the estimation of divergence events in evolution based on fossils and the molecular “clock.” 2.  Rowe (1996) provided embryological and paleontological evidence to show the importance of brain size increase in ontogeny and phylogeny to understand the origin of the mammalian middle ear anatomy, although the details of these correlations are complex (Meng et al. 2003). Z.-X. Luo and colleagues have documented brain size changes across early mammalian evolution, including the magnificient fossil of Hadrocodium wui, which lived during the Lower Jurassic and was merely 3.2 centimeters in length and estimated at 2 grams in weight (Luo, Crompton, and Sun 2001). Much of the increase in brain size was “driven by increased resolution in olfaction and improvements in tactile sensitivity (from body hair) and neuromuscular coordination” (Rowe, Macrini, and Luo 2011: 955). 3.  That lactation most likely originated when tooth replacement became diphyodont does not imply simple cause-and-effect. The coupling of these features and others likely evolved in a concerted and gradual manner. 4.  Brinkman (1988) described the postcranial changes for species of two basal synapsids, Ophiacodon and Dimetrodon.

Notes to Chapter 10  /  211 5.  Maier (1999) hypothesized that closure of the maxillary secondary palate evolved independently in precynodont therocephalians and in cynodonts (including mammals). 6.  To reduce the amount of terminology, I am avoiding the terms metatherians to refer to the marsupials and their stem species and eutherians for the placentals and their stem species (Rougier, Wible, and Novacek 1998). 7.  Sharman (1970) and Zeller (1999) have suggested that viviparity in marsupials and placentals evolved independently from an oviparous common ancestor. 8.  Van Nievelt and Smith (2005) showed that an alteration of the ancestral mammalian pattern of replacement similar to that of marsupials has occurred in many placental lineages, putting into question the association with reproductive strategies. 9.  Dental eruption sequences have been correlated with growth patterns not only in primates but also in other mammals (Smith 1992). This could be a fertile area of research once extensive sampling of species within a phylogenetic framework has been carried out, with consideration of the intraspecific variation and environmental factors involved. The relative timing of epiphyseal fusion of postcranial bones is reportedly later than the completion of dental eruption in mammals (Smith 1992), whereas sexual maturity can occur at any relative time when compared with dental and skeletal maturity. The overall reported pattern was summarized by Uhen (2000: 131): “Mammals that achieve sexual maturity after dental and skeletal maturity tend to live fast and die young, whereas mammals that achieve sexual maturity before dental and skeletal maturity tend to live slow and die old.”

Chapter 10: On Trilobites, Shells, and Bugs 1.  Murdock and Donoghue (2011) studied the occurrence of biomineralization across animal phylogeny, particularly the inclusion of extinct forms, and concluded that this process must have evolved several times independently. The co-option of molecular mechanisms is

212  /  Notes to Chapter 10 likely to have played a role in this repeated innovation, with the same “biomineralization tool kit” of genes being used in many independent evolutionary lines. 2.  The last common ancestor of bilaterian animals was unmineralized, and the mineralization of preexisting skeletal substrates may have played a role in the later appeareance of biomineralization (Minelli 2007).

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Index

acipenseriforms, 135, 209 adaptations, 3, 77, 81, 90, 112, 140; to aquatic environment, 83, 154; ecological, 123, 132; gut fermentation, 43; in insular species, 120–124; parallel genotypic, 3; to swimming, 53 adaptive radiations, 8, 98 Aepyornis, 50, 214 Africa, 17, 113, 118. See also South Africa Afrotheria, 131 Agassiz, Louis, 12–13 Alaska, USA, 112 algae, 182 allometry, 43, 95, 97, 98, 99, 102fig., 168, 187; growth, 96fig., 97–99, 119, 148, 160; interspecific, 102fig.; intraspecific, 102fig.; Alphadon, 167 altriciality, 47–48, 56, 60–61, 167, Amblyrhynchus, 80; histology, 82fig. American Museum of Natural History, 28, 57, 58fig.  

 

 

 

 

ammonites, 33, 108, 178, 184; ammonitella, 185, 187fig.; Buckman’s law, 186fig.; ontogeny, 185, 187fig.; ornamentation, 184–87 amniotic fluid, 55 amphibians, 21–23, 44, 59, 99, 163, 199n12. See also frogs and salamanders; legless, 21; lepospondyls, 22 Amprino, Rodolfo, 71 Amprino’s rule, 71 anapsid skull, 151 anatomy, 4, 10, 16, 40, 43, 55, 60; of bats, 147; at birth, 29, 48; ear, 155; of fetus, 47; of fossil chordates, 62; of mammalian jaw, 16–18, 18fig.; masticatory, 22; of turtle shell, 150–154, 153fig. Andes, 7 Antarctic Peninsula, 190 antlers, 89, 96fig., 101–3, 103fig. Apatosaurus, 76 apes, 43, 167–71, 169fig., 195  

 

 

 

 

 

243

244 / Index apical ectodermal ridge, 156 appendages, 43–45, 51, 52fig., 178, 190–191. See also limbs aquatic reptiles. See reptiles Arabian sand boa. See Eryx aragonitic skeletons, 183 Archaeopteryx, 28, 45, 54, 101, Arctica, 189, 190 Argentina, 114 Argyrolagus, 133fig. aristogenesis, 28 arms, 69, 79. See also limbs arthropods, 33, 129, 176–93. See also crustaceans and trilobites Asher, Rob, 131 atomization, 32, 33 Australia, 7, 51, 77, 112 Australopithecus, 168, 169fig. axial bifurcation, 12, 13fig.  

 

 

bacteria, 106 Balearic Islands, 122, 124 Bali, 118, barnacles, 32, Basel, Switzerland, 67, 135, 170 Basin and Range, 2 batoids. See chondrichthyans bats. evolution of wings, 147–50 Bavaria, Germany, 28, 45, 191 Berkeley, USA, 144, Berlin, Germany, 45, bilateral symmetry, 33, 81 biocalcification crisis, 109 biodiversity, 2, 3, 5, 34, 66, 108, 196 biomineralization, 182–84 birds, 8, 48, 50–57, 74, 127, 127fig., 130, 138, 142, 147, 158; altricial, 48; developmental stages, 24fig., ear ossicles, 160; embryo, 55fig.; flightless, 77, 78; histology, 72fig; origin of, 28, 74–77; precocial,  

 

 

 

48; ratites, 77–78. See also moas; retention of oviparity, 55; birth, 29, 30, 46, 47–50, 61, 167, 168, 170 173; in Neanderthals, 172; premature, 171 Bisagra Patagónica, 114, 115fig. Bison, 39 blood vessels. See bone microstructure Blumberg, Mark S., 25, 36 Bmp. See bone morphogenetic protein Bolivian Altiplano, 167 Bombina, 22fig. bone morphogenetic protein, 149 bone. accretion, 69, 80, 81; cancellous, 70; compact, 70; compactness, 82, 83fig.; cortex, 75, 80, 82fig., 122; deposition, 80; fibro-lamellar, 72fig., 75, 127, 128, 162, 164fig.; growth marks, 70– 72, 81; lamellar, 72fig., 81, 122, 127; medullary, 74; microstructure, 70–74, 72fig. See also histology; reconstruction, 68; remodeling, 69, 73, 81, 83fig., 88; resorption, 68, 73, 80, 81, 88; vascular, 70, 74, 75; woven fibered, 81 bones, 66–91, 104, 170, 182. See also jaws and long bones; dermal, 134, 135, 138, 140; endochondral, 40; intramembranous, 40; marrow cavities, 74, 80, 82; mineralization, 80 Bonn, 69, 76 Borel, Émile, 2 Botha-Brink, Jennifer, 117 Bothriolepis: growth series, 101fig. brachiopods, 33 Brachypotherium: dental replacement, 88fig. brain, 16, 31, 99, 123, 124, 168; dif 

 

 

 

 

Index / 245 ferentiation, 48; human, 170–72; size, 123, 160, 169fig., 171 branchiosaurids, 23 Branchiostoma, 62 Brayard, Arnaud, 109 Brazil, 191 Briggs, Derek, 191 brontotheres, 97, 98, 99, 104, brooding, 48, 56–59 Bucher, Hugo, 33, 185 Buckman’s law, 185, 186fig.  

 

caelocanths, 13 calcitic skeleton, 178, 183 calcium, 73–74; salts of 182 calcium carbonate, 64, 74, 108–9, 183 calcium phosphate, 64 Cambrian, 6, 63, 64, 110, 111, 178, 191 Cambropallas, 181fig. Camelops, 39 camels, 39 canaliculi, 70 canids, 99 cannibalism, 59 capybaras, 101, 103 Carboniferous, 6fig., 21, 97 Caribbean, 118 Carlini, Fredy, 113 carps, 135, 137, 139fig. Carroll, Sean, 57, 128 Cartagena, Colombia, 116 cartilage, 39, 58–59, 149, 205; calcified, 80, 83fig.; rod, 44–45 Castanet, Jacques, 75 cats, 148. See also Smilodon fatalis catsharks. See chondrichthyans caudal autotomy, 44–45 Cenozoic, 6fig., 90 cephalopods, 184 cetaceans. See whales and dolphins Cetartiodactyla, 60  

 

 

 

 

chalk, 182 Channel Islands, 119 chimaeras. See chondrichthyans chimpanzees, 5, 142, 168–74, 169fig. China, 11, 49, 63, 76, 130, 199 chitin, 182 chondrichthyans, 86, 116 Cifelli, Richard, 167 clade dynamics, 105 cladistic methodology, 180 clams, 189–90 classification, 28, 32, 56, 198 climatic change, 106, 107, 112–16, 115fig., 202 coccolithophores, 182 cocoliths, 182 collagen, 70, 182, 203 Colombia, 115–16 computer tomography, 49, 51, 68, 160 conodonts, 85, 111, 205 Conolophus, 80 continental drift, 7 cooperative breeding, 171 copepods, 109 corals, 108, 177, 183, 188 core stones. See Steinkerne correlated progression, 163, 164fig., 165 Court Jester scenario, 106, 207 cows, 75, 87, 148, 154 crabs, 176 cranium. See skull Crato Formation, 190 Cretaceous, 6fig., 8, 11, 21, 49, 52, 57, 58, 77, 97, 135, 147, 159, 162, 167, 182, 183, 191, 209 Crete, 120 crocodiles, 20, 45, 51, 54, 56, 73, 122, 127, 127fig., 151, 155, 161, 202 Crompton, A. W. “Fuzz”, 17, 198 Crossaster, 109  

 

 

 

246 / Index crustaceans, 32, 179, 191, 192fig., 193. See also lobsters, crabs, and Henningsmoenicaris Cryptocleidus: shoulder girdle, 94fig. CT. See computer tomography Cuba, 118 Cucullaea, 190 Cuvier, Georges, 10–11, 26, 85, 198 Cyprus, 120  

Danio. See zebrafish Dart, Raymond, 168 Darwin, Charles, 2–3, 7, 10, 14, 32, 40, 124, 207 de Ricqlés, Armand J., 68, 74–75 Deccan traps, 107–8, 207 deep homology, 128 deep time, 2–3, 106, 159fig., 191, 197 deer, 87–89, 96fig., 101, 103, 119–20, 154, 205 Deinosuchu, 77 Dendrobates, 22fig. dentary, 15–17 dentary-squamosal jaw joint, 17 dentine, 86–88, 205 developmental genetics, 34, 126– 40, 149, 157, developmental plasticity, 76, 132– 33, 163 developmental sequence, 19 developmental stages, 24fig. developmental transformation, 12, 14 Devonian, 6fig., 51, 67, 85, 135, 177, 191, 203, 209 Diarthrognathus, 17–18, 199 dicynodonts, 117 digits, 9, 148–49 Dimetrodon, 162–63, 210 Dinornis, 77–78 Dinosauria. See dinosaurs  

 

 

 

 

 

 

 

 

 

 

 

 

 

dinosaurs, 4, 46–59, 74–77, 104, 107, 127, 127fig., 133, 148, 159, 178, 202, 208. See also Oviraptor, prosauro­ pods, Protoceratops sauropods and theropods; feathered, 11, 19, 142, 198. Dinosaurs of the Flaming Cliffs, 57 diphyodonty, 161, 164fig. Diplodocus, 48 Diprotodon: growth series, 102fig. divergence dates: estimation of, 5 diversification, 26, 36, 140; morphological, 84, 98, 136, 138; patterns, 105–25, 207–8 Dmanisi, Georgia, 168 DNA, 5 dolphins, 155–56 Donoghue, Phil, xiii Dover, England, 182 Dremotherium: teeth, 90fig. ducks, 48; feet, 149; number of neck vertebrae, 130 dugongs, 131 Dupont, Sam, 109 Durant, Ariel, 1 Durant, Will, 1, Dürer, Albrecht. 94  

 

 

 

 

ear, 14–17, 17fig., 160, 199, 210; ear ossicles. See ear echidnas, 51, 159fig., 166, echinoderms, 33. See also Crossaster and sea urchins echolocation, 147 ecological developmental biology, 35 ectodysplasin, 137–38, 205; signaling pathway, 137–40, 139fig. ectothermy, 72fig., 74–75, 122 Edaphosaurus, 98fig. egg, 54–59, 92, 110, 116, 166–67 egg retention, 56  

 

 

 

 

 

Index / 247 eggshells, 50, 54, 56, 73–74, 167, 202–3 Egypt, 154 Eimer, Theodor, 28 elephant bird, 49–50 elephants, 76, 119–20, 121fig., 131 Elephas, 119, 121fig. elk, 75 embryology, 11–12 embryos, 11, 24fig., 25, 46–47, 50–51, 56, 59, 61–64, 67, 86, 93fig., 144, 149, 152, 153fig., 160, 163, 199, 204– 5; alligator, 20; bat 148–50, 150fig.; bird, 50, 55, 55fig., 55; dinosaur, 48–49, 54, 59; dolphin, 156; frog, 21, 22fig.; horse, 60; human, 11, 15fig.; ichthyosaur, 52; malformed, 11–12, 13fig.; mammalian, 59–60; marsupial, 160; sauropod, 133; sea urchin, 64 enamel, 85–86, 89, 91 enameloid, 85–86, Encyclopaedia Britannica, 1–2 endoskeletons, 176–77 endothermy, 56, 72fig., 74–76, 158, 162 England, 14, 17, 182 English Channel, 182 Eocene, 27, 41, 45, 60, 97, 114–15, 115fig., 144, 147–48, 154, 190, 203 Epel, David, 35 epigenetics, 37fig., 145, 160 epistasis, 37fig. Equus, 39, 98 Eryx, 53 ETH Zürich, 109 Eurasia, 17 Europe, 14, 108, 147, 198 Euryapteryx, 78 Eusthenopteron, 67, 203 Evo-devo, 34–45, 135, 200–201 evolutionary biology, 5, 15, 34, 142, 144  

 

 

 

 

 

 

 

 

evolutionary innovations, 19, 31, 34, 148, 152, 200, 209 evolutionary novelties, 9, 34 evolutionary reversals, 53 evolutionary tree reconstruction, 8, 31–33, 41, 63, 198 evolvability, 34, 42, 200 exoskeleton, 135, 176–77, 190, 209 eye socket, 42, 120, 145fig. eyes, 3, 34–35, 47–48, 62, 99, 120, 143–44, 146fig., 160, 190–91, 205, ; compound, 191  

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

feathers, 8–9, 19, 87, 138, 198; in dinosaurs. See dinosaurs feet, 9, 149, 155 felids, 99. See also cats and Smilodon fatalis femur, 69, 74, 156fig fetalization hypothesis, 170–71 fetuses, 11, 60, 132, 171, 208 Fgf8/fgf8. See fibroblast growth factor fibroblast growth factor, 137–38, 139fig., 149; Fgf8/fgf8 149, 156 fibula, 49, 73 fishes, 13, 16, 22, 25, 51, 59, 67, 79, 99, 118, 135, 141, 155, 158, 163, 203–4, 209. See also acipenseriforms, catsharks, chondrichthyans, carps, Eusthenopteron, flatfish, Oryzias, placoderms, Saurichthys, sticklebacks and zebrafish Fisher, Dan, 88 flatfish, 143–47, 146fig., 160 flight, 55, ; active, 147–48 flightless, 77–78, 201 Flores Island, Indonesia, 123 foraminifera, 66 Fortey, Richard, 178 foot. See feet Four 4-D model, 191, 192fig.  

 

 

 

 

 

 

248 / Index France, 144, 182 Freaks of Nature, 25, 36 Friedmann, Matt, 144 frogs, 21, 22fig., 25, 38, 59, 200

 

 

 

Galápagos, 54, 119; finches, 118; marine iguana, 54, 78–81 Gasterosteus. See sticklebacks gastropods, 111, 184, 188 gene duplication, 84, 138, 204 genome size, 84 genotypes, 3 geochemistry, 2, 109 geometric morphometrics, 94, 188. See also growth: geometric approach Georgia, 168 Germany, 21, 23, 45, 144, 150, 203 gestation, 13, 47, 60, 78, 167, 170 Gilbert, Scott, 35 gills, 23, 59 Gingerich, Phil, 154 giraffes, 87, 130, 154 Gobi Desert, 57 Gobiconodon, 162 Gogo Formation, 51, 202 Goin, Pancho, 113 golden moles, 131, 208 Goldschmidt, Richard, 144–47, 160 Gondwana, 69 Goodrich, E.S., 44 Goswami, Anjali, 42 Gould, Stephen Jay, 170–71 graptolites, 67 great apes, 168, 170–71, 195 Great Chain of Being. See Scala naturae Gremlin, 149 growth: accretionary, 33, 69, 80– 81, 87, 177, 186, 189; geometric approach, 93–95, 206; landmark 

 

 

 

 

 

based approaches, 94–95; mathematical approach, 33, 93, 95–96 growth patterns, 22, 36, 42, 48, 69, 72, 74–77, 96–99, 108, 163, 172, 177, 211 growth phase: extension of, 37, 96; truncation of, 77, 96 growth series, 72, 95; fossil, 78–79, 100–104, 161, 204 guinea pigs, 47  

 

 

Haeckel, Ernst, 13–14, 19, 21, 31, 198 hair, 7–9, 19, 47, 87, 138, 210 Haldanodon, 90 Halle, Germany, 11 Hamburger, Viktor, 144 Hammer, Øyvind, 185 hamsters, 47 hands, 14, 149; evolution of, 9–10 Harvard University, 17, 198 hatchlings 50, 55–56; fossil, 46–50 Haug, Joachim, 191–92 Hawaii, 118–19 Head, Jason, 116 Helsinki, Finland, 41 Henningsmoenicaris, 191–92, 192fig., Heterochrony, 19, 20fig. heterocercal tail, 13 Heteronectes, 145fig. Heterotropy, 19, 20fig. hip girdle. See pelvis hippopotamus, 99, 154; fossil, 119, 120, 123–24, His, Wilhelm, 67, 203 histology, 49, 56, 66–91, 104, 201, 203. See also paleohistology; of bones, 68, 69, 71, 72fig., 76–81, 82fig., 83fig. 103, 117, 122, 127, 161–62; Galápagos marine iguana, 81–82, 82fig.; minimum age estimation, 100; sections, 66–67, 69, 71fig., 83fig., 84, 133; sexual maturity  

 

 

 

 

 

 

 

 

 

 

 

 

 

Index / 249 estimation, 81, 83fig.; of teeth, 87, 89, 112, 161, 173–74. Historia animalium, 93 hoatzin. See birds: precocial hologeny, 28, 29fig. Homeothermy, 84, 163, 164fig. hominids, 27, 123. See also great apes; fossil record, 167–170, 169fig. Homininae, 167–68 Homo, 4, 123, 124, 168, 169fig.,172 ,174, 208. See also Neanderthals and humans; homology, 42, 87, 128 Homunculi, 92 Hoploscpahites, 187fig. Horner, Jack, 75 horses, 75, 97–99, 148. See also Equus; evolutionary tree, 27, 98; fossil, 27, 39, 60, 94, 97–99, 112, 203, 206 Hox genes, 130–32, 178 Hughes, Nigel, 179 Hugi, Jasmina, 79, 81 humans, 1, 4, 7, 9, 11, 27, 31, 35, 39, 44, 46, 49, 73–74, 78, 94, 99, 118, 122, 128, 141–43, 151, 195–96, 208. See also Homo; skull; 11, 61, 171– 72 development, 14, 15fig., 24fig., 25, 158–75, 159fig., 169fig., 172, 208; Taung infant, 168; vertebral column, 129, 132 humerus, 69, 83fig. Huxley, Julian, 95–96, 206 Huxley, Thomas, 1, 133 Hyaenodon, 90–91, 206 Hyopsodus, 41 hypsodonty, 114  

 

 

 

 

 

Indian subcontinent, 107, 154 Indonesia, 123 innominate. See pelvis insects, 164, 176, 179 integration, 8, 40–43, 184 internal fertilization, 51 Into the Jungle, 57 invertebrates, 12, 41, 67, 105, 109, 110, 176, 182, 189, 190. See also insects, molluscs, and echinoderms Ireland, 89 island species, 26–27, 77, 207 islands, 7, 77, 118–25, 207; continental, 118. See also Balearic Islands, Bali, Channel Islands, Cuba, Crete, Cyprus, Jersey, Malta, Mediterranean islands and Sicily; dwarfism, 119–24, 121fig., 122–23, 208; gigantism, 119–21; oceanic, 26, 118. See also Flores Island, Galápagos, Hawaii, Mauritius, and Réunion isometry, 95, 97, 99 Italy, 144  

 

 

 

 

 

 

 

 

 

 

 

 

ichthyosaurs, 52–53, 79, 101, 204, 206 Incisoscutum, 52fig., 202 India, 58

Jablonski, David, 105 Japan, 120 Jardin des Plantes, 10 jaw articulation, 16–18, 17fig., 18fig., 99, 199 jaws, 11, 14–18, 17fig., 18fig., 47, 59, 99, 135, 160, 167, 199. See also dentary Jena, Germany, 21 Jernvall, Jukka, 36, 41, 86 Jersey, UK, 119 Jurassic, 6fig., 17, 29fig., 45, 48, 52, 54, 76, 90, 116, 132, 158, 162–63, 166, 191, 210  

 

 

 

K-strategy, 78 kakapo, 78, 204 kangaroos, 5, 112, 143, 158, 159fig.

250 / Index Kemp, Tom, 163–64 Kielmeyer, Carl Friedrich, 14 Klingenberg, Chris, 41 koalas, 51, 130 Kobe, Japan, 130 Köhler, Meike, 124 Komodo dragon, 77 Kriwet, Jürgen, 116 Kruszyński, Chris, 188 Kuratani, Shigeru, 130, 199–200, 208  

 

La Plata, Argentina, 113 lactation, 74, 161, 164fig., 173, 210 lacunae, 70, 84 LAGs. See lines of arrested growth lakes, 22, 37–38, 118, 122; Victoria, 118 Lamarck, Jean-Baptiste, 10, 28 Lampetra, 62 lamprey, 62 larvae, 21–23, 32, 37, 109, 110–12; sea urchins, 64 Leçons d’anatomie, 11 Lehmann, Thomas, 131, 208 Leicester, England, 62 Leipzig, Germany, 172 legs, 48–49, 57, 61, 69, 73, 76, 154. See also limbs lemurs, 7 lepospondyls: ontogeny, 22 Lessons of History, The, 1 Li, Chun, 151 life history, 29–32, 47, 49, 61, 71, 73, 77, 78, 81, 87–89, 90, 106–19, 124, 134, 158, 160–74, 177, 183, 188, 189, 201, 207 limb reduction, 80, 155–57, 156fig. limbs, 12, 23, 34–35, 43–44, 57, 61, 79, 81, 112, 113fig., 147–48, 154–57, 163, 207. See also arms, legs, and long bones limestone, 182  

 

 

 

 

 

 

 

 

 

 

 

 

lines of arrested growth, 71–72, 78, 82fig., 83fig. Lister, Adrian, 119, 123 lizards, 24fig., 25, 43–45, 48, 51, 54, 80–81, 118, 141, 151, 201, 202 lobsters, 176 locomotion, 44, 78,-80, 112, 148, 158 long bones, 69, 73–75, 78, 82fig., 122. See also femur, fibula, humerus, and tibia long-wave ultraviolet light, 45 Los Angeles, USA, 39 Lugano, 135 Lystrosaurus, 7, 117, 159, 159fig.  

 

 

 

MacPhee, John, 2 macroevolution, 105, 142–43 Madagascar, 7, 49–50, 123 Madden, Rick, 114 Maiacetus, 61 Maier, Wolfgang, 29 malformations, 11, 12, 120 Malta, 120 Mamenchisaurus, 76 mammals, 4, 7–8, 11, 14–19, 17fig., 18fig., 29, 39, 41–43, 47, 51–52, 59–61, 85–90, 100, 102fig., 112– 14, 113fig., 115fig., 117–23, 138, 148, 151, 154–56, 165fig., 198, 202, 205– 8, 210–11. See also marsupials, monotremes, and placentals; development, 25, 158–75; diversification, 117; middle ear. See ear; eruption of teeth, 174; last common ancestor of living, 142–43; modularity of skull, 42–43; split from reptilian lineage, 158; stem mammals, 159fig., 161; unique traits, 7; vertebral numbers, 130– 33; histology, 72fig., 74–76 mammoths, 60, 88, 119 Mammuthus. See mammoths  

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Index / 251 manatees, 52 Maori, 77 marine reptiles, 7, 45, 51–52, 54, 69, 79, 132, 204. See also Amblyrhynchus, Galápagos marine iguana, ichthyosaurs, mesosaurs, mosasauroids, sauropterygians Marroig, Gabriel, 41 Marsh, Othniel C., 104 marsupials, 17fig., 18, 51, 91, 102fig., 113fig., 114, 115fig., 130–31, 143, 159fig., 160, 166–67, 199, 207, 211. See also Alphadon, opossums, kangaroos and koalas mass extinctions, 107; end-Permian, 108, 159, 178, 183; end-Triassic, 116 Massospondylus, 36, 48–49, 201 Mauritius, 119 Max Planck Institute, 172 Meckel, Johann Friedrich, 11 Meckel’s cartilage, 11, 16, 17fig., 18fig., 199 medakas. See Oryzias Mediterranean, 120, 122; island, 118, 120, 122, 124 Megaloceros, 89; allometric growth of antlers, 96fig. Merycoidodon, 60 mesenchyme, 149 mesosaurs, 7, 45 Mesozoic, 6fig., 52, 143, 199 Messel, Germany, 150 metabolic rate, 76, 81, 84, 87, 132, 161, 163, 164fig., 166, 208 metamorphosis, 23, 110, 127 Mexico, 39 mice, 73, 86, 119, 130, 141, 148–49, 164, 199 microtome, 67–68, 203 Miller, Robert, 41 missing links, 141–57, 209; bat wing  

 

 

 

 

 

 

evolution, 147–50; flatfish eye evolution, 143–47; reptile-bird, 28; turtle shell evolution,150–54; whale leg evolution, 154–57 Mitgutsch, Christian, 21 moas, 77–78 modularity, 34–45, 200; mammalian skull, 42 molecular biology, 5 molluscs, 7, 32–33, 87, 108, 182, 184– 85, 189. See also ammonites, brachiopods, cephalopods, clams, gastropods, snails, and squids Mongolia, 57 Monnet, Claude, 188 Monodelphis, 17fig. Monotremes, 131, 143, 159fig., 166–67. See also echidnas and platypus Monte San Giorgio, 79, 134, 204 Morganucodon, 17, 18fig., 159fig., 162 Morocco, 174 morphogenesis, 149, 184 Morphological Integration, 41 morphology, 12, 20, 25, 27, 28, 31–32, 34, 38, 41–43, 50–54, 84, 87, 89, 98–99, 110, 112, 114, 119, 121, 124, 134, 136, 138, 140, 143, 148, 152, 155, 170, 180, 182, 184, 186, 188, 191, 198– 200, 202, 204, 207–8 morphometrics, 33, 94, 100–101, 188, 204, 206 mosasauroids, 52–53, 202 Mount Vesusius, 107 mouse. See mice mouth, 59, 99, 161, 165fig., 166, 173, 203 Moyá-Solá, Salvador, 124 Müller, Johannes, 132, muscles, 9, 18, 31, 39–40, 129–30, 152, 153fig., 165fig. Museum of Natural History Paris, 10  

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

252 / Index mutations, 3, 35, 86, 132, 137–38, 140, 145 Myotragus, 122, 124  

123, 144, 160, 171, 172, 191; ammonites, 185–88, 187fig.; aspects of, 92; branchiosaurids, 23; fossilized vertebrate, 46–65; reconstruction, 126; temnospondyls, 21–22 Ophiacodon, 163, 210 opposum, 130 oral cavitiy. See mouth Ordovician, 6fig., 110–11, 191 oreodonts, 60, 97 Origination Patterns and Multilevel Processes in Macroevolution, 105 Orsten Lagerstätten, 191 orthogenesis, 28 Oryzias, 137 Osborn, Henry Fairfield, 28, 57 ossification, 48–49, 100, 151, 199, 204 osteoderms, 73, 151 oviparity, 53–55, 116, 127 Oviraptor, 57, 58fig. ovoviviparity, 51, Owen, Sir Richard, 48, 130 Oxford University, 144, 163 Oxford, England, 67  

 

Nagashima, Hiroshi, 152, 153fig. Nariokotome, Lake Turkana region, Kenya, 168 Narita, Yuichi, 130 nasal cavity. See nose Natural History Museum London, 203 natural selection, 26, 29, 36, 112 Nautilus, 184 Neanderthals, 169fig., 170–72, postnatal ontogeny of, 172 Neogene, 6fig., 112, 203 neural crest, 21, 22fig., 86, 205 Neusticosaurus, 83fig., 204 New York, USA, 28, 57 New Zealand, 77–78 Nimbadon, 102fig. Norrell, Mark, 57 North America, 17, 77, 112, 114, 119, 147 nose, 120, 165fig., 166 Not by design, 26 Nothrotheriops, 39 notochord, 62–63 Novacek, Mike, 57 Nuevo León, Mexico, 39 Nützel, Alexander, 111  

 

 

ocean acidification, 109 Odontochelys, 130, 151–52, 153fig.,210 Oligocene, 60, 114–15, 115fig. Olson, Everett, 41, 203 Olsson, Lennart, 21, 201 On Growth and Form, 93, 94fig., 206 On the Origin of Species, 13, 40 ontogenetic trajectory, 32, 95, 169fig. ontogeny, 1–33, 20fig., 29fig., 30fig., 37, 38, 74, 76, 87, 92, 93, 96, 100, 114,  

 

 

 

 

 

 

pachypleurosaurs, 78–82, 83fig. Padian, Kevin, 75, 77 paedomorphism, 122 Pagel, Mark, 128 Pakistan, 61 palate, 164fig., 165fig., 166 Paleocene, 167 Paleogene, 6, paleohistology, 36, 66–84; cell size quantification, 84; of dinosaur bone, 74–77; Lystrosaurus, 117–18; methods, 68; of moas, 78; Myotragus, 122; pterosaurs, 75, 84; pachypleurosaurs, 78–83, 83fig.; of Stupendemys, 69–70, 71fig. Paleozoic, 6, 36, 38, 51, 84  

 

 

 

 

 

Index / 253 Panthera, 39 parallel genotypic adaptation, 3 Paramylodon, 39 parataxonomy, 56 parental care, 48, 56–57, 60, 158 Paris, France, 10–11, 74 parsimony, 167, 180 patellae, 39–40 covariation, 40 pelvis, 49, 53, 60, 130, 154, 171, 202; innominate, 156, 156fig. Pelycosaurs, 97, 98fig. Penguins, 48, 54 Pennsylvanian, 177 pentaradial symmetry, 33 Permian, 6fig., 7, 45, 59, 97, 108, 117, 159, 178, 183, 203 phenotypes, 3, 8, 25, 35–37, 37fig., 126, 128,-29, 136–38, 140, 196, 201, 208–9 phenotypic plasticity, 23, 35–37, 114, 187–88 phylogeny, 14, 19–20, 20fig.29fig., 30fig., 31–33, 53, 64, 97, 132, 170, 184, 197–98, 210–11 ; phylogenetic bracket, 126–31, 127fig. placentals, 51, 91, 131, 143, 159fig., 166–67, 209, 211 placentation, 50–51 placoderms, 51, 52fig., 85, 101fig., 202, 205 placodonts, 79, 204 planktotrophy, 110–11 plasticity, 25, 122, 130–33, 163, 179– 80, 201. See also phenotypic plasticity Plateosaurus, 36 platypus, 7, 51, 143, 166 Pleistocene, 39, 60, 77, 112, 120, 123 plesiosaurs, 53, 53fig., 79, 94, 94fig., 133 Pompei, 170  

 

 

 

Ponce de Léon, Marcia, 168, 175 Poplin, Cécile, 68 Portmann, Adolf, 171 Portugal, 90 postextinction recovery, 108, 117 postnatal care, 49 preformism, 92, 93fig. Pregnancy, 56, 61, 73–74, 116, 203–4 preservation,, 22, 38, 43, 69–60, 64–65, 127, 167, 198; bias, 93, 100; unusual, 190–93 proboscidians, 124 prosauropods, 36, 48–49. See also Plateosaurus and Massospondylus Prothero, Don, 39, 114 Protoceratops,97 pterosaurs, 75, 84 Purnell, Mark, 62  

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Raff, Elisabeth, 67 Rancho La Brea, 39 Raup, David, 185 Raymond, Kristina, 39 rays. See chondrichthyans Recherches sur les poissons fossils, 13 Red Queen scenario, 106, 207 regionalization, 133, 156fig., 178–79, 181fig., 209 Reiss, John, 26 Reisz, Robert, 49, 210 reproductive isolation, 119, 140, 181 reproductive strategies, 49, 50, 202–3, 211. See also oviparity, oviviparity, and viviparity reptiles, 12, 15, 16, 28, 45–46, 52, 54, 58, 72fig., 73–80, 99, 122, 130– 33, 143, 150,-51, 159fig., 159–63, 201, 203–4; aquatic, 52; choristoderan, 11, 13fig.; semiaquatic, 11. See also marine reptiles Réunion, 119  

 

 

 

 

 

 

254 / Index rhinoceroses, 94 Rhynie Chert, 191 Richardson, Mike, 23, 199 Rieppel, Olivier, 134, 200 rodents, 47, 103, 119. See also hamsters, guinea pigs, and capybaras Roth, Louise, 124 Rousettus, 150fig. Rowe, Tim, 160, 210 Russia, 16

sea snakes, 54 Sears, Karen, 149, 207 Segmentation, 128–29, 131, 179. See also segments segments, 22fig., 33, 45, 129, 135, 177– 81, 181fig., 191–93, 209 self-amputation, 43 sesamoids, 39–40 Seymour Island, 190 sharks. See chondrichthyans shells: molluscs, 32–33, 87, 111, 166– 93; turtle, 34, 70, 73, 150–54; eggs. See eggshells shoulder girdle, 94fig., 94, 151–52 Siberia, 60 Siberian traps, 108 Sicily, 120 Silurian, 6fig., 29fig. Simpson, George Gaylord, 4, 206 Sinoconodon, 162 skeletochronology, 71, 73, 75, 81, 88; of Galàpagos marine iguana, 81– 82, 82fig. skinks, 44, 80. See also Scincella skulls, 16–21, 18fig., 41–43, 48–50, 57, 60–61, 85, 89, 94, 97–100, 102fig., 104, 120, 121fig., 134–35, 144, 151–52, 155, 165fig., 168–72, 169fig., 210 sloths, 39, 60, 110, 206. See also Paramylodon and Nothrotheriops Smith, Moya, 86 snails, 109 snakes, 12, 25, 51–54, 58, 80, 115–16, 129, 179, 202. See also Eryx, Sanajeh, and sea snakes soft tissue preservation, 38, 60 Sollas, Igerna Johnson, 67 Sollas, William Johnson, 67, 203 Solnhofen, 191 somites, 22fig., 45, 129, 133 sonic hedgehog, 86, 156, 156fig. South Africa, 16, 48, 168, 198  

 

 

 

 

Saar-Nahe Basin, 38fig. Saber, 43 saber-toothed cat. See Smilodon fatalis Sahelanthropus, 168, 169fig., 171 Saint-Hilaire, Etienne Geoffroy, 10 salamanders, 21, 37–38, 43–44, 141 saltwater, 22, 62, 199 San Josecito Cave, 39 Sanajeh, 58 Sander, Martin, 69, 76 Sansom, Robert, 62 Saurichthys, 134–38, 136fig., 137fig. sauropods, 48, 50, 58, 69, 75–77, 133, 204. See also Diplodocus, Mamenchisaurus, and Apatosaurus sauropterygians, 52–53. See also pachypleurosaurs, placodonts, and plesiosaurs Scala naturae, 141 scales, 87, 134–38, 136fig., 151 See also squamation Scheyer, Torsten, 69, 132 Schmid, Lieni, 135–38 Schoch, Rainer, 36 Schultz, Adolph, 173 Schultz’s rule, 173, 174fig. Scincella, 44 Sclerocephalus, 37–38 38fig. Scotland, 93, 191 sea urchins, 33, 109, 177  

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Index / 255 South African Karoo, 19, 198 South America, 7, 60, 113–14, 206 South Dakota, USA, 60 Southeast Asia, 120, 155 specializations, 21, 87, 91, 143, 147, 150 Spemann, Hans, 144 squamation, 136fig., 140, 209. See also scales squids, 79, 184 Steinkerne, 111 sticklebacks, 136–37, 139fig., 209 Stockar, Rudolf, 135 Stolarski, Jaroslaw, 183 stomach contents, 22, 37 Stupendemys, 69–71, 71fig. Stuttgart, Germany, 10, 36 Sutton, Mark, 191 Sweden, 109, 191 Switzerland, 79, 107, 134, 135 synchrotron technology, 63, 173  

 

 

tails, 13, 62, 79, 130, 155; self-amputation, 43–45; vertebrae, 61 Tanystropheus, 45, 133, 133fig. Tanzania, 168 taphonomy, 62–64 Taung infant, 168 taxonomy, 4, 38, 56, 92–104, 120, 181, 184 teeth, 7, 14–15, 22, 34, 35, 49, 59, 61, 98–99, 103, 114, 117, 135, 140, 151, 161, 173–74. See also dentine; canines, 40; cusps, 41; dental characters, 41; dental formula, 161; development, 86, 131, 138– 40, 205n15; histology, 85–89, 112; molars, 40, 170, 173, 174fig.; occlusion, 161, 164fig., 165fig.; replacement, 42, 88fig., 161, 167, 174fig.; shearing dentition, 91; wear, 47, 89–91, 114  

 

 

 

 

Teissier, Georges, 95–96 teleology, 27 temnospondyls, 21–23, 36, 59 terminal additions, 19, 20fig. tetrapods, 23, 84, 117, 163 Texas, USA, 59, 97 Texas, University of. See university theropods, 7, 8, 49, 54, 76, 77 theropods, eggs, 50 Thewissen, Hans, 154–56 Thompson, D’Arcy, 93–95 Thrinaxodon, 159fig., 161 Thuringian Forest Basin, 23 Ticino, Switzerland, 79 Tischlinger, Helmut, 45 Titanoboa, 115–16 tool kit proteins, 138, 140 Triassic, 6, 7, 16, 17, 52, 79, 108, 109, 117, 130, 134, 135, 138, 161, 162, 183 trilobites, 33, 128, 176–82, 181fig.; molting, 33 Trimerorhachis, 59 Tübingen, Germany, 14, 69 Tübingen, University of. See university turtles, 12, 51, 56, 73, 129, 130, 163, 164. See also paleohistology; evolution of shell anatomy, 34, 150–54, 153fig.; sea turtles, 54 Turvey, Samuel, 78 twins: fossil, 60 Tyrannosaurus, 8, 74, 76  

 

 

 

 

 

 

 

 

 

 

ungulates, 60, 75, 87, 88, 130, 148, 154. See also deer United States, 114 University of California, 144 University of St. Andrews, 93 University of Texas, 160 University of Tübingen, 29 University of Turin, 71, University of Zürich, 69, 173

256 / Index Urdy, Séverine, 187, Urumaco, Venezuela, 70 Varanus, 77 Venezuela, 69, 70 vertebrae, 44, 45, 61, 155; numbers, 129–33 vertebral column, 49, 53, 129; regionalization, 179, 156fig. vertebrates, 4, 9, 15, 16, 21, 23, 43, 69, 73, 84, 85, 86, 89, 94, 112, 138, 147, 176, 190; land, 9, 31, 36–38, 67; missing links, 141–57; ontogenies, 46–65; vertebral numbers, 129–33 viviparity, 50–56, 79, 80, 116, 135, 167  

Webster, Mark, 180, 181 Weissert, Helmut, 109 Wells, John, 177 Werneburg, Ingmar, 23 Werneburg, Ralf, 23 Weston, Eleanor, 123 whales, 52, 61, 132, 147, 158, 179; evolution of hindlimb, 154–57, 156fig., White River Group, 114  

Yucatán Peninsula, Mexico, 107

 

 

 

 

 

Wagner, Günter, 9 Wales, 17 weaning, 173 Weatherbee, Scott, 149

zebrafish, 137, 139fig., 140, 199n15 Zimmermann diagram, 29fig. Zimmermann, Walter, 28 Zlichovaspis, 181fig. Zollikofer, Christoph, 168, 175 Zürich, University of. See university Zürich, Switzerland, 21, 33, 69, 81, 134, 168



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