Handbook of Parenting: Volume 2: Biology and Ecology of Parenting, Third Edition [3 ed.] 1138228699, 9781138228696

Table of contents :
Cover
Half Title
Title
Copyright
Dedication
Contents
Preface to the Third Edition
About the Editor
About the Contributors
Part I Biology of Parenting
1 The Evolution of Parenting and Evolutionary Approaches to Childrearing
2 Psychobiology of Maternal Behavior in Nonhuman Mammals
3 Parenting in Nonhuman Primates
4 Genetics and Parenting
5 Prenatal Parenting
6 The Social Neuroendocrinology of Human Parenting
7 Neurobiology of Human Parenting
Part II Ecology of Parenting
8 Ancient History of Parenting
9 Modern History of Parenting
10 Epidemiology of Parenting
11 Neighborhoods and Parenting
12 Parent Education Attainment and Parenting
13 Socioeconomic Status and Parenting
14 Culture and Parenting
15 Environment and Parenting
Index

Citation preview

HANDBOOK OF PARENTING

This highly anticipated third edition of the Handbook of Parenting brings together an array of fieldleading experts who have worked in different ways toward understanding the many diverse aspects of parenting. Contributors to the Handbook look to the most recent research and thinking to shed light on topics every parent, professional, and policy maker wonders about. Parenting is a perennially “hot” topic. After all, everyone who has ever lived has been parented, and the vast majority of people become parents themselves. No wonder bookstores house shelves of “how-to” parenting books, and magazine racks in pharmacies and airports overflow with periodicals that feature parenting advice. However, almost none of these is evidence-based. The Handbook of Parenting is. Period. Each chapter has been written to be read and absorbed in a single sitting, and includes historical considerations of the topic, a discussion of central issues and theory, a review of classical and modern research, and forecasts of future directions of theory and research. Together, the five volumes in the Handbook cover Children and Parenting, the Biology and Ecology of Parenting, Being and Becoming a Parent, Social Conditions and Applied Parenting, and the Practice of Parenting. Volume 2, Biology and Ecology of Parenting, relates parenting to its biological roots and sets parenting in its ecological framework. Some aspects of parenting are influenced by the organic makeup of human beings, and the chapters in Part I, on the Biology of Parenting, examine the evolution of parenting, the psychobiological determinants of parenting in nonhumans, and primate parenting, as well as the genetic, prenatal, neuroendocrinological, and neurobiological bases of human parenting. A deep understanding of what it means to parent also depends on the ecologies in which parenting takes place. Beyond the nuclear family, parents are embedded in, influence, and are themselves affected by larger social systems. The chapters in Part II, on the Ecology of Parenting, examine the ancient and modern histories of parenting as well as epidemiology, neighborhoods, educational attainment, socioeconomic status, culture, and environment to provide an overarching relational developmental contextual systems perspective on parenting. Marc H. Bornstein holds a BA from Columbia College, MS and PhD degrees from Yale University, and honorary doctorates from the University of Padua and University of Trento. Bornstein is President of the Society for Research in Child Development and has held faculty positions at Princeton University and New York University as well as academic appointments in Munich, London, Paris, New York, Tokyo, Bamenda, Seoul, Trento, Santiago, Bristol, and Oxford. Bornstein is author of several children’s books, videos, and puzzles in The Child’s World and Baby Explorer series, Editor Emeritus of Child Development and founding Editor of Parenting: Science and Practice, and consultant for governments, foundations, universities, publishers, scientific journals, the media, and UNICEF. He has published widely in experimental, methodological, comparative, developmental, and cultural science as well as neuroscience, pediatrics, and aesthetics.

HANDBOOK OF PARENTING Volume 2: Biology and Ecology of Parenting Third Edition

Edited by Marc H. Bornstein

Third edition published 2019 by Routledge 52 Vanderbilt Avenue, New York, NY 10017 and by Routledge 2 Park Square, Milton Park, Abingdon, Oxon, OX14 4RN Routledge is an imprint of the Taylor & Francis Group, an informa business © 2019 Taylor & Francis The right of Marc H. Bornstein to be identified as the author of the editorial material, and of the authors for their individual chapters, has been asserted in accordance with sections 77 and 78 of the Copyright, Designs and Patents Act 1988. All rights reserved. No part of this book may be reprinted or reproduced or utilised in any form or by any electronic, mechanical, or other means, now known or hereafter invented, including photocopying and recording, or in any information storage or retrieval system, without permission in writing from the publishers. Trademark notice: Product or corporate names may be trademarks or registered trademarks, and are used only for identification and explanation without intent to infringe. First edition published by Laurence Erlbaum Associates 1995 Second edition published by Taylor & Francis 2002 Library of Congress Cataloging-in-Publication Data A catalog record for this book has been requested ISBN: 978-1-138-22868-9 (hbk) ISBN: 978-1-138-22869-6 (pbk) ISBN: 978-0-429-40145-9 (ebk) Typeset in Bembo by Apex CoVantage, LLC

For Marian and Harold Sackrowitz

CONTENTS

Preface to the Third Edition About the Editor About the Contributors

ix xiv xvi

PART I

Biology of Parenting

1

  1 The Evolution of Parenting and Evolutionary Approaches to Childrearing David F. Bjorklund and Alyson J. Myers

3

  2 Psychobiology of Maternal Behavior in Nonhuman Mammals Aya Dudin, Patrick O. McGowan, Ruiyong Wu, Alison S. Fleming, and Ming Li

30

  3 Parenting in Nonhuman Primates Kim A. Bard

78

  4 Genetics and Parenting Amanda V. Broderick and Jenae M. Neiderhiser

123

  5 Prenatal Parenting David A. Coall, Anna C. Callan, Julie Sartori, and James S. Chisholm

166

  6 The Social Neuroendocrinology of Human Parenting Ruth Feldman

220

  7 Neurobiology of Human Parenting Eloise A. Stark, Alan Stein, Katherine S. Young, Christine E. Parsons, and Morten L. Kringelbach

250

vii

Contents PART II

Ecology of Parenting

285

  8 Ancient History of Parenting Valerie French

287

  9 Modern History of Parenting Peter N. Stearns

320

10 Epidemiology of Parenting Rebecca M. Pearson, Miguel Cordero, and Priya Rajyaguru

349

11 Neighborhoods and Parenting Elizabeth A. Shuey and Tama Leventhal

371

12 Parent Education Attainment and Parenting Pamela E. Davis-Kean, Sandra Tang, and Nicholas E. Waters

400

13 Socioeconomic Status and Parenting Erika Hoff and Brett Laursen

421

14 Culture and Parenting Xinyin Chen, Rui Fu, and Wai Ying Vivien Yiu

448

15 Environment and Parenting Robert H. Bradley

474

Index519

viii

PREFACE TO THE THIRD EDITION

Previous editions of the Handbook of Parenting have been called the “who’s who of the what’s what.” This third edition of this Handbook appears at a time that is momentous in the history of parenting. The family generally, and parenting specifically, are today in a greater state of flux, question, and re-definition than perhaps ever before. We are witnessing the emergence of striking permutations on the theme of parenting: blended families, lesbian and gay parents, teen versus fifties first-time moms and dads, genetic versus social parents. One cannot but be awed on the biological front by technology that now renders postmenopausal women capable of childbearing and with the possibility of parents designing their babies. Similarly, on the sociological front, single parenthood is a modern-day fact of life, adult child dependency is on the rise, and even in the face of rising institutional demands to take increasing responsibility for their offspring parents are ever less certain of their roles and responsibilities. The Handbook of Parenting is concerned with all these facets of parenting . . . and more. Most people become parents, and everyone who ever lived has had parents, still parenting remains a mystifying subject. Who is ultimately responsible for parenting? Does parenting come naturally, or must parenting be learned? How do parents conceive of parenting? of childhood? What does it mean to parent a preterm baby, twins, or a child on the autistic spectrum? to be an older parent, or one who is divorced, disabled, or drug abusing? What do theories (psychoanalysis, personality theory, attachment, and behavior genetics, for example) contribute to our understanding of parenting? What are the goals parents have for themselves? for their children? What functions do parents’ cognitions serve? What are the aims of parents’ practices? What accounts for parents believing or behaving in similar ways? Why do so many attitudes and actions of parents differ so? How do children influence their parents? How do personality, knowledge, and worldview affect parenting? How do social class, culture, environment, and history shape parenthood? How can parents effectively relate to child care, schools, and their children’s pediatricians? These are many of the questions addressed in this third edition of the Handbook of Parenting . . . for this is an evidenced-based volume set on how to parent as much as it is one on what being a parent is all about. Put succinctly, parents create people. They are entrusted with preparing their offspring for the physical, psychosocial, and economic conditions in which their children eventually will fare and hopefully will flourish. Amid the many influences on each next generation, parents are the “final common pathway” to children’s development and stature, adjustment and success. Human social inquiry—antedating even Athenian interest in Spartan childrearing practices—has always, as a matter of course, included reports of parenting. Freud opined that childrearing is one of three “impossible ix

Preface to the Third Edition

professions”—the other two being governing nations and psychoanalysis. One encounters as many views as the number of people one asks about the relative merits of being an at-home or a working mother, about what mix of day care, family care, or parent care is best for a child, about whether good parenting reflects intuition or experience. The Handbook of Parenting concerns itself with different types of parents—mothers and fathers, single, adolescent, and adoptive parents; with basic characteristics of parenting—knowledge, beliefs, and expectations about parenting—as well as the practice of parenting; with forces that shape ­parenting—employment, social class, culture, environment, and history; with problems faced by ­parents—­handicap, marital difficulties, drug addiction; and with practical concerns of parenting— how to promote children’s health, foster social adjustment and cognitive competence, and interact with educational, legal, and religious institutions. Contributors to the Handbook of Parenting have worked in different ways toward understanding all these diverse aspects of parenting, and all look to the most recent research and thinking in the field to shed light on many topics every parent, professional, and policy maker wonders about. Parenthood is a job whose primary object of attention and action is the child. But parenting also has consequences for parents. Parenthood is giving and responsibility, and parenting has its own intrinsic pleasures, privileges, and profits as well as frustrations, fears, and failures. Parenthood can enhance psychological development, self-confidence, and sense of well-being, and parenthood also affords opportunities to confront new challenges and to test and display diverse competencies. Parents can derive considerable and continuing pleasure in their relationships and activities with their children. But parenting is also fraught with small and large stresses and disappointments. The transition to parenthood is daunting, and the onrush of new stages of parenthood is relentless. In the final analysis, however, parents receive a great deal “in kind” for the hard work of parenting—they can be recipients of unconditional love, they can gain skills, and they can even pretend to immortality. This third edition of the Handbook of Parenting reveals the many positives that accompany parenting and offers resolutions for its many challenges. The Handbook of Parenting encompasses the broad themes of who are parents, whom parents parent, the scope of parenting and its many effects, the determinants of parenting, and the nature, structure, and meaning of parenthood for parents. The third edition of the Handbook of Parenting is divided into five volumes, each with two parts: CHILDREN AND PARENTING is Volume 1 of the Handbook. Parenthood is, perhaps first and foremost, a functional status in the life cycle: Parents issue as well as protect, nurture, and teach their progeny even if human development is too subtle and dynamic to admit that parental caregiving alone determines the developmental course and outcome of ontogeny. Volume 1 of the Handbook of Parenting begins with chapters concerned with how children influence parenting. Notable are their more obvious characteristics, like child age or developmental stage; but more subtle ones, like child gender, physical state, temperament, mental ability, and other individual differences factors, are also instrumental. The chapters in Part I, on Parenting Across the Lifespan, discuss the unique rewards and special demands of parenting children of different ages and stages—infants, toddlers, youngsters in middle childhood, and adolescents— as well as the modern notion of parent-child relationships in emerging adulthood and adulthood and old age. The chapters in Part II, on Parenting Children of Varying Status, discuss common issues associated with parenting children of different genders and temperaments as well as unique situations of parenting adopted and foster children and children with a variety of special needs, such as those with extreme talent, born preterm, who are socially withdrawn or aggressive, or who fall on the autistic spectrum, manifest intellectual disabilities, or suffer a chronic health condition.

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Preface to the Third Edition

BIOLOGY AND ECOLOGY OF PARENTING is Volume 2 of the Handbook. For parenting to be understood as a whole, biological and ecological determinants of parenting need to be brought into the picture. Volume 2 of the Handbook relates parenting to its biological roots and sets parenting in its ecological framework. Some aspects of parenting are influenced by the organic makeup of human beings, and the chapters in Part I, on the Biology of Parenting, examine the evolution of parenting, the psychobiological determinants of parenting in nonhumans, and primate parenting and then the genetic, prenatal, neuroendocrinological, and neurobiological bases of human parenting. A deep understanding of what it means to parent also depends on the ecologies in which parenting takes place. Beyond the nuclear family, parents are embedded in, influence, and are themselves affected by larger social systems. The chapters in Part II, on the Ecology of Parenting, examine the ancient and modern histories of parenting as well as epidemiology, neighborhoods, educational attainment, socioeconomic status, culture, and environment to provide an overarching relational developmental contextual systems perspective on parenting. BEING AND BECOMING A PARENT is Volume 3 of the Handbook. A large cast of characters is responsible for parenting, each has her or his own customs and agenda, and the psychological characteristics and social interests of those individuals are revealing of what parenting is. Chapters in Part I, on The Parent, show just how rich and multifaceted is the constellation of children’s caregivers. Considered first are family systems and then successively mothers and fathers, coparenting and gatekeeping between parents, adolescent parenting, grandparenting, and single parenthood, divorced and remarried parenting, lesbian and gay parents, and finally sibling caregivers and nonparental caregiving. Parenting also draws on transient and enduring physical, personality, and intellectual characteristics of the individual. The chapters in Part II, on Becoming and Being a Parent, consider the intergenerational transmission of parenting, parenting and contemporary reproductive technologies, the transition to parenthood, and stages of parental development, and then chapters turn to parents’ well-being, emotions, self-efficacy, cognitions, attributions, as well as socialization, personality in parenting, and psychoanalytic theory. These features of parents serve many functions: They generate and shape parental practices, mediate the effectiveness of parenting, and help to organize parenting. SOCIAL CONDITIONS AND APPLIED PARENTING is Volume 4 of the Handbook. Parenting is not uniform across communities, groups, or cultures; rather parenting is subject to wide variation. Volume 4 of the Handbook describes socially defined groups of parents and social conditions that promote variation in parenting. The chapters in Part I, on Social and Cultural Conditions of Parenting, start with a relational developmental systems perspective on parenting and move to considerations of ethnic and minority parenting among Latino and Latin Americans, African Americans, Asians and Asian Americans, Indigenous parents, and immigrant parents. The section concludes with the roles of employment and of poverty on parenting. Parents are ordinarily the most consistent and caring people in children’s lives. However, parenting does not always go right or well. Information, education, and support programs can remedy potential ills. The chapters in Part II, on Applied Issues in Parenting, begin with how parenting is measured and follow with examinations of maternal deprivation, attachment, and acceptance/rejection in parenting. Serious challenges to parenting—some common, such as stress, depression, and disability, and some less common, such as substance abuse, psychopathology, maltreatment, incarceration—are addressed as are parenting interventions intended to redress these trials. THE PRACTICE OF PARENTING is Volume 5 of the Handbook. Parents meet the biological, physical, and health requirements of children. Parents interact with children socially.

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Preface to the Third Edition

Parents stimulate children to engage and understand the environment and to enter the world of learning. Parents provision, organize, and arrange their children’s home and local environments and the media to which children are exposed. Parents also manage child development vis-à-vis childcare, school, the circles of medicine and law, as well as other social institutions through their active citizenship. Volume 5 of the Handbook addresses the nuts-and-bolts of parenting as well as the promotion of positive parenting practices. The chapters in Part I, on Practical Parenting, review the ethics of parenting, parenting and the development of children’s self-regulation, discipline, prosocial and moral development, and resilience as well as children’s language, play, cognitive, and academic achievement and children’s peer relationships. Many caregiving principles and practices have direct effects on children. Parents indirectly influence children as well, for example, through relations they have with their local or larger communities. The chapters in Part II, on Parents and Social Institutions, explore parents and their children’s childcare, activities, media, schools, and healthcare and examine relations between parenthood and the law, public policy, and religion and spirituality. Each chapter in the third edition of the Handbook of Parenting addresses a different but central topic in parenting; each is rooted in current thinking and theory as well as classical and modern research on a topic; each is written to be read and absorbed in a single sitting. Each chapter in this new Handbook follows a standard organization, including an introduction to the chapter as a whole, followed by historical considerations of the topic, a discussion of central issues and theory, a review of classical and modern research, forecasts of future directions of theory and research, and a set of evidence-based conclusions. Of course, each chapter considers contributors’ own convictions and findings, but contributions to this third edition of the Handbook of Parenting attempt to present all major points of view and central lines of inquiry and interpret them broadly. The Handbook of Parenting is intended to be both comprehensive and state-of-the-art. To assert that parenting is complex is to understate the obvious. As the expanded scope of this third edition of the Handbook of Parenting also amply attests, parenting is naturally and intensely interdisciplinary. The Handbook of Parenting is concerned principally with the nature and scope of parenting per se and secondarily with child outcomes of parenting. Beyond an impressive range of information, readers will find passim typologies of parenting (e.g., authoritarian-autocratic, indulgent-permissive, indifferent-uninvolved, authoritative-reciprocal), theories of parenting (e.g., ecological, psychoanalytic, behavior genetic, ethological, behavioral, sociobiological), conditions of parenting (e.g., gender, culture, content), recurrent themes in parenting studies (e.g., attachment, transaction, systems), and even aphorisms (e.g., “A child should have strict discipline in order to develop a fine, strong character,” “The child is father to the man”). Each chapter in the Handbook of Parenting lays out the meanings and implications of a contribution and a perspective on parenting. Once upon a time, parenting was a seemingly simple thing: Mothers mothered. Fathers fathered. Today, parenting has many motives, many meanings, and many manifestations. Contemporary parenting is viewed as immensely time consuming and effortful. The perfect mother or father or family is a figment of false cultural memory. Modern society recognizes “subdivisions” of the call: genetic mother, gestational mother, biological mother, birth mother, social mother. For some, the individual sacrifices that mark parenting arise for the sole and selfish purpose of passing one’s genes on to succeeding generations. For others, a second child may be conceived to save the life of a first child. A multitude of factors influences the unrelenting advance of events and decisions that surround parenting—biopsychosocial, dyadic, contextual, historical. Recognizing this complexity is important to informing people’s thinking about parenting, especially informationhungry parents themselves. This third edition of the Handbook of Parenting explores all these motives, meanings, and manifestations of parenting.

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Preface to the Third Edition

Each day more than three-quarters of a million adults around the world experience the rewards and challenges, as well as the joys and heartaches, of becoming parents. The human race succeeds because of parenting. From the start, parenting is a “24/7” job. Parenting formally begins before pregnancy and can continue throughout the life span: Practically speaking for most, once a parent, always a parent. Parenting is a subject about which people hold strong opinions, and about which too little solid information or considered reflection exists. Parenting has never come with a Handbook . . . until now. —Marc H. Bornstein

xiii

ABOUT THE EDITOR

Marc H. Bornstein holds a BA from Columbia College, MS and PhD degrees from Yale University, and honorary doctorates from the University of Padua and University of Trento. Bornstein was a J. S. Guggenheim Foundation Fellow and he received a Research Career Development Award from the National Institute of Child Health and Human Development. He also received the C. S. Ford Cross-Cultural Research Award from the Human Relations Area Files, the B. R. McCandless Young Scientist Award and the G. Stanley Hall Award from the American Psychological Association, a U.S. PHS Superior Service Award and an Award of Merit from the National Institutes of Health, two Japan Society for the Promotion of Science Fellowships, four Awards for Excellence from the American Mensa Education & Research Foundation, the Arnold Gesell Prize from the Theodor Hellbrügge Foundation, the Distinguished Scientist Award from the International Society for the Study of Behavioral Development, and both the Distinguished International Contributions to Child Development Award and the Distinguished Scientific Contributions to Child Development Award from the Society for Research in Child Development. Bornstein is President of the Society for Research in Child Development and a past member of the SRCD Governing Council and Executive Committee of the International Congress of Infancy Studies. Bornstein has held faculty positions at Princeton University and New York University as well as academic appointments as Visiting Scientist at the Max-Planck-Institut für Psychiatrie in Munich; Visiting Fellow at University College London; Professeur Invité at the Laboratoire de Psychologie Expérimentale in the Université René Descartes in Paris; Child Clinical Fellow at the Institute for Behavior Therapy in New York; Visiting Professor at the University of Tokyo; Professeur Invité at the Laboratoire de Psychologie du Développement et de l’Éducation de l’Enfant in the Sorbonne in Paris; Visiting Fellow of the British Psychological Society; Visiting Scientist at the Human Development Resource Centre in Bamenda, Cameroon; Visiting Scholar at the Institute of Psychology in Seoul National University in Seoul, South Korea; Visiting Professor at the Faculty of Cognitive Science in the University of Trento, Italy; Profesor Visitante at the Pontificia Universidad Católica de Chile in Santiago, Chile; Institute for Advanced Studies Benjamin Meaker Visiting Professor, University of Bristol; Jacobs Foundation Scholar-in-Residence, Marbach, Germany; Honorary Fellow, Department of Psychiatry, Oxford University; Adjunct Academic Member of the Council of the Department of Cognitive Sciences, University of Trento, Italy; and International Research Fellow at the Institute for Fiscal Studies, London.

xiv

About the Editor

Bornstein is coauthor of The Architecture of the Child Mind: g, Fs, and the Hierarchical Model of Intelligence, Gender in Low- and Middle-Income Countries, Development in Infancy (5 editions), Development: Infancy through Adolescence, Lifespan Development, Genitorialità: Fattori Biologici E Culturali Dell’essere Genitori, and Perceiving Similarity and Comprehending Metaphor. He is general editor of The Crosscurrents in Contemporary Psychology Series, including Psychological Development from Infancy, Comparative Methods in Psychology, Psychology and Its Allied Disciplines (Vols. I–III), Sensitive Periods in Development, Interaction in Human Development, Cultural Approaches to Parenting, Child Development and Behavioral Pediatrics, and Well-Being: Positive Development Across the Life Course, and general editor of the Monographs in Parenting series, including his own Socioeconomic Status, Parenting, and Child Development and Acculturation and Parent-Child Relationships. He edited Maternal Responsiveness: Characteristics and Consequences, the Handbook of Parenting (Vols. I–V, 3 editions), and the Handbook of Cultural Developmental Science (Parts 1 and 2), and is Editor-in-Chief of the SAGE Encyclopedia of Lifespan Human Development. He also coedited Developmental Science: An Advanced Textbook (7 editions), Stability and Continuity in Mental Development, Contemporary Constructions of the Child, Early Child Development in the French Tradition, The Role of Play in the Development of Thought, Acculturation and Parent-Child Relationships, Immigrant Families in Contemporary Society, The Developing Infant Mind: Origins of the Social Brain, and Ecological Settings and Processes in Developmental Systems (Volume 4 of the Handbook of Child Psychology and Developmental Science). He is author of several children’s books, videos, and puzzles in The Child’s World and Baby Explorer series. Bornstein is Editor Emeritus of Child Development and founding Editor of Parenting: Science and Practice. He has administered both Federal and Foundation grants, sits on the editorial boards of several professional journals, is a member of scholarly societies in a variety of disciplines, and consults for governments, foundations, universities, publishers, scientific journals, the media, and UNICEF. He has published widely in experimental, methodological, comparative, developmental, and cultural science as well as neuroscience, pediatrics, and aesthetics. Bornstein was named to the Top 20 Authors for Productivity in Developmental Science by the American Educational Research Association.

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ABOUT THE CONTRIBUTORS

Kim A. Bard is a Professor of Comparative Developmental Psychology in the Department of Psychology, University of Portsmouth, UK. She was educated at Wheaton College, Massachusetts (BA with Honors) and Georgia State University (MA and PhD in Comparative/Developmental Psychology). She was employed previously at Emory University as a Research Scientist at the Yerkes Regional Primate Research Center and at the Clinical Developmental and Applied Research Program of the Human Genetics Laboratory, and as a Research Fellow in the Department of Psychology. Bard is an Associate Fellow of the British Psychological Society and Past President of the Primate Society of Great Britain and European Federation for Primatology. Currently, she sits on the Advisory Board of Primates, is an Associate Editor for Animal Cognition, and sits on the Editorial Boards of American Journal of Primatology, Child Development Perspectives, and Emotion Review. Bard is the author of Responsive Care: Behavioral Intervention for Nursery-Reared Chimpanzees and a co-editor of The Cultural Nature of Attachment: Contextualizing Relationships and Development. David F. Bjorklund is Professor of Psychology at Florida Atlantic University. He received a BA in Psychology from the University of Massachusetts, an MA in Psychology from the University of Dayton, and a PhD in Developmental Psychology from the University of North Carolina at Chapel Hill. He is the author of Children’s Thinking: Cognitive Development and Individual Differences, Why Youth Is Not Wasted on the Young, co-author of Looking at Children: An Introduction to Child Development, Parents Book of Discipline, Applied Child Study and The Origins of Human Nature: Evolutionary Developmental Psychology, Child and Adolescent Development: An Integrative Approach, and the General Psychology; he is also editor of several books. He served as Associate Editor of Child Development and the Journal of Experimental Child Psychology and is Editor of the Journal of Experimental Child Psychology. Bjorklund is a contributing editor to Parents Magazine. His research interests include children’s cognitive development and evolutionary developmental psychology. Robert H. Bradley is Professor of Psychology and Director of the Center for Child and Family Success at Arizona State University. Bradley was a faculty member at the University of Arkansas at Little Rock. He served as associate editor for Child Development and Early Childhood Research Quarterly and chaired the Biobehavioral and Behavioral Research subcommittee at NIH. Bradley is one of the developers of the HOME Inventory. He was an investigator in the NICHD Study of Early Child Care and Youth Development and the Early Head Start Research and Evaluation Study.

xvi

About the Contributors

Amanda V. Broderick is a PhD student studying Child Clinical Psychology at The Pennsylvania State University. Broderick earned her BA in psychology with a minor in applied statistics at the University of Michigan and her MA at The Pennsylvania State University. Broderick uses complementary research designs to understand interparental and parent-child relationships as conduits through which risk for maladaptive child development is mitigated or conferred. Anna C. Callan is Senior Lecturer in the School of Medical and Health Sciences at Edith Cowan University, Perth, Western Australia. Callan was awarded her PhD from the University of Manchester, where she was subsequently employed as a Research Associate, before working at the Telethon Kids Institute and Edith Cowan University. Callan has expertise in the field of environmental epidemiology, with a particular interest in the health impacts of prenatal and early life exposures to substances including persistent chemicals, plasticizers, and perfluoroalkyl acids. Xinyin Chen is Professor of Psychology at the Graduate School of Education, the University of Pennsylvania. He holds a BA from East China Normal University and MA and PhD from the University of Waterloo. He received a Scholars Award from the William T. Grant Foundation and several other awards for his scientific work. He served as the President of the International Society for the Study of Behavioral Development. His research interest is mainly in children’s and adolescents’ socioemotional functioning, social relationships, and family socialization processes with a focus on cross-cultural issues in Brazil, Canada, China, Italy, and the United States. He has edited or co-edited Peer Relationships in Cultural Context, Social Change and Human Development, Socioemotional Development in Cultural Context, and Values, Religion, and Culture in Adolescent Development. James S. Chisholm is Emeritus Professor in the School of Anatomy, Physiology, and Human Biology at the University of Western Australia in Perth. He received his BA from Wesleyan University and MPhil and PhD from Rutgers University. He has conducted fieldwork among the Navajo and Aboriginal people in Arnhem Land and taught at the University of New Mexico, the University of California, Davis, and the University of Western Australia. He is the author of Navajo Infancy: An Ethological Study of Child Development and Death, Hope and Sex: Steps to an Evolutionary Ecology of Mind and Morality. David A. Coall is a Senior Lecturer in the School of Medical and Health Sciences at Edith Cowan University and Adjunct Research Fellow in the School of Medicine, The University of Western Australia. He completed his PhD at The University of Western Australia and a Postdoctoral Research Fellowship in the Institute of Psychology, University of Basel, Switzerland. His research focuses on intergenerational influences on health, such as the influence the mother’s environment has on placental development and pregnancy outcomes and the influence grandparents have in the lives of grandchildren. Coall has authored publications in evolutionary anthropology, pediatrics, cognitive science, mental health, and maternal and child health. Miguel Cordero is a child clinical psychologist with a MA in Behavioural Neurosciences at the University of Chile. He was a consultant in perinatal and pediatric mental health at Dr. Sotero del Rio Hospital in Santiago, Chile in charge of the implementation of Chile Crece Contigo at the Ministry of Health, a large-scale policy to reduce early childhood development inequalities. He was also responsible for implementing a large multi-center randomized trial to assess the impacts of implementing “Nobody’s Perfect Parenting Program” in primary health clinics from Chile. Currently, he is a PhD student at the Population Health Sciences Institute at the Bristol Medical School.

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About the Contributors

Pamela E. Davis-Kean is a Professor of Psychology and Research Professor of the Institute for Social Research at the University of Michigan where she is the Program Director of the Population, Neurodevelopment, and Genetics program. She received her BA from Florida State University and her MA and PhD from Vanderbilt University. Davis-Kean is a Fellow of the Association of Psychological Science. She is an Associate Editor of Advances in Methods and Practices in Psychological Science. Davis-Kean’s primary research focus is on parental educational attainment and how it can influence the development of the home environment throughout childhood, adolescence, and the transition to adulthood. Davis-Kean is co-editor of Socializing Children through Language. Aya Dudin is a PhD student in the McMaster Integrative Neuroscience Discovery and Study program. Dudin completed an HBSc in Behavior Genetics and Neurobiology from the University of Toronto. She is interested in understanding the underlying neurobiology of maternal behavior in mammals. Aya has co-authored work in Social Neuroscience as well as Depression and Anxiety. Ruth Feldman is the Simms-Mann Professor and Director of the Center for Developmental and Social Neuroscience at the Interdisciplinary Center, Herzlia, with a joint appointment at Yale University Child Study Center. Her research focuses on the neurobiology of affiliation, biobehavioral synchrony, longitudinal follow-up of high-risk infants, and the effects of touch-based interventions. She studies the role of oxytocin in human bonding, the parental brain, kangaroo contact, the neurobiology of conflict resolution, the effects of maternal depression, and the development of targeted interventions. Alison S. Fleming is a Professor Emerita of Psychology at the University of Toronto. Fleming received her PhD from The Institute of Animal Behavior, Rutgers University. Fleming focused her research efforts on understanding what makes a mother want to mother and what influences how she does so. This work has been taken to multiple levels of explanation in both rodent and humans, ranging from the role of hormones, odors, and other sensory cues from the young, past and present history and experiences, the brain, and the underlying genetic and neurochemical mechanisms. Fleming is the recipient of the University of Toronto Excellence in Research Award and was inducted into the Royal Society of Canada. She was awarded a Canada Research Chair in Neurobiology, and she received the Daniel S. Lehrman Lifetime Achievement Award from the Society of Behavioral Neuroendocrinology. Valerie French was Associate Professor of History at the American University. She was active in professional organizations on women’s and minority issues. She published extensively on ancient childhood, women in antiquity, Alexander the Great, and Greek historiography. French coauthored Historians and the Living Past: The Theory and Practice of Historical Study. Rui Fu is a PhD candidate in the program of Human Development and Quantitative Methods at the University of Pennsylvania. Her research interests focus on children’s and adolescents’ academic, social, and psychological functioning from a cross-cultural perspective. She also serves as an Early Career Scholar Representative of the SRCD Asian Caucus. Erika Hoff is Professor of Psychology at Florida Atlantic University. Hoff earned an AB Ed from the University of Michigan, an MS from Rutgers–The State University of New Jersey, and a PhD from the University of Michigan. Her research addresses the relations among properties of children’s early environments, their language experience, and their language development. She has studied effects of maternal education and effects of dual language exposure on children’s language growth.

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About the Contributors

She is a member of the U.S. Bridging the Word Gap Research network, which focuses on interventions to remedy SES-related disparities in children’s early experience and language skills. She has been associate editor of the Journal of Child Language and Child Development. She is currently associate editor of the Journal of Experimental Child Psychology. She is editor of multiple books on early language development, including Research Methods in Child Language and Childhood Bilingualism: Research on Infancy Through School Age. Morten L. Kringelbach is a Professor of Neuroscience at the University of Oxford, UK, and University of Aarhus, Denmark. His research uses neuroimaging and whole-brain computational models of hedonia (pleasure) linked to infants, taste, and music to discover how to increase eudaimonia (the life well-lived). He has published 14 books. He is a fellow of The Queen’s College, Oxford, of the Association for Psychological Science, is on the advisory board of Scientific American, and is a board member of the world’s first Empathy Museum. Brett Laursen is Professor of Psychology and Director of Graduate Training at Florida Atlantic University. He is also Docent Professor of Social Developmental Psychology at the University of Jyväskylä, Finland. Laursen received his PhD and MA from the Institute of Child Development at the University of Minnesota, and his BA from Nebraska Wesleyan University. He is a Fellow of the American Psychology Association (Division 7, Developmental), a Fellow and Charter Member of the Association for Psychological Sciences, and the recipient of an Honorary Doctorate from Örebro University, Sweden. He is currently the Editor-in-Chief of the International Journal of Behavioral Development. Laursen’s research focuses on parent-child and peer relationships during childhood and adolescence and their influence on individual social and academic adjustment. His edited books include Handbook of Developmental Research Methods and Handbook of Peer Interactions, Relationships and Groups. Tama Leventhal is Professor in the Eliot-Pearson Department of Child Study and Human Development at Tufts University. She received her PhD from Teachers College, Columbia University and was previously affiliated with Johns Hopkins University. Her primary research focus is the role of neighborhood contexts in the lives of children, youth, and families. Leventhal was formerly a U.S. Department of Housing and Urban Development Postdoctoral Urban Scholar, a William T. Grant Scholar, and a Foundation for Child Development Changing Faces of America’s Children Young Scholar. She was Co-director of the MacArthur Network on Housing and Families with Children and is currently Co-director of the Housing and Children’s Healthy Development study. She is Associate Editor of the Journal of Research on Adolescence and Applied Developmental Science, Co-editor of the Handbook of Child Psychology and Developmental Science: Volume 4: Ecological Settings and Processes in Developmental Systems, Steering Committee Chair of the University-Based Child and Family Policy Consortium, and Board of Directors of the Council on Contemporary Families. Ming Li is Professor of Psychology at the University of Nebraska-Lincoln. Li was educated at the Peking University and University of Toronto. He is a Fellow of Divisions 6 and 28 of the American Psychological Association. He is a co‑editor of The Neuropsychopathology of Schizophrenia: Molecules, Brain Systems, Motivation, and Cognition. Patrick O. McGowan is Associate Professor of Biological Sciences at the University of Toronto Scarborough, where he is Principal Investigator of the Laboratory of Environmental Epigenetics and Development. He also holds faculty appointments in the departments of Cell and Systems Biology, Psychology and Physiology at the University of Toronto. He received his PhD at Duke University and was Sackler Postdoctoral fellow in Psychiatry at McGill University. He is an associate editor of

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About the Contributors

Frontiers in Epigenomics and Epigenetics. McGowan’s research focuses on biological mechanisms linking exposures to stressors, particularly early in life, with the programming of health and disease. Alyson J. Myers is a PhD candidate in Developmental Psychology at Florida Atlantic University. Myers received her MA at Florida Atlantic University and is affiliated with Denise Herzing and the Wild Dolphin Project. She studies wild Atlantic spotted dolphin (Stenella frontalis) behavior, specifically synchrony and its development in juveniles. Her interests include ethology, evolutionary developmental psychology, and cognitive development. Jenae M. Neiderhiser is a Distinguished Professor of Psychology and Human Development and Family Studies at Pennsylvania State University. She is co-director of the Gene-Environment Research Initiative and is a faculty affiliate of the Social Sciences Research Institute and the Child Study Center at Pennsylvania State. She received her BS in Psychology from the University of Pittsburgh and her PhD in Human Development and Family Studies from Pennsylvania State University and was previously on the faculty of the Center for Family Research, in the Department of Psychiatry and Behavioral Science at The George Washington University. Neiderhiser’s work focuses on how genes and environments work together throughout the lifespan and the role of the prenatal environment. She has been Associate Editor of the Journal of Research on Adolescence, is on the editorial board of several developmental psychology journals, is currently Associate Editor for Frontiers in Behavioral and Psychiatric Genetics, and is on the Scientific Advisory Board of the TwinLife project. Christine E. Parsons is an Associate Professor at the Interacting Minds Centre, Department of Clinical Medicine, Aarhus University. She completed her PhD in Psychology at Maynooth University, Ireland and did her postdoctoral training in the Department of Psychiatry, University of Oxford. She has held positions as college lecturer in Psychology at Harris Manchester College, University of Oxford, and as Assistant Professor at the Center of Functionally Integrative Neuroscience, Aarhus University. Her research focuses on understanding the human parental brain using different brain imaging and behavioral methods. Rebecca M. Pearson is Lecturer Psychiatric Epidemiology, Based at the Centre for Academic Mental Health, University of Bristol. Pearson received a first degree in Applied Psychology from Cardiff University and a PhD in Psychiatric Epidemiology from the University of Bristol. Pearson is currently leading an EU-funded research program investigating intergenerational transmission of mental health problems through parenting. Priya Rajyaguru is an Academic Clinical Fellow in Psychiatry working clinically in psychiatric medicine and academically at the University of Bristol. Rajyaguru graduated from Cardiff University with a MBBCh in Medicine and BSc in Psychological Medicine. Julie Sartori is a PhD candidate with a background in nursing, as a Research Assistant with the Placenta Project, RAINE Study, and the Australian Fathers Study. She completed her BSc, taught Medical Science units, and worked in the public and private health sectors. Her research framework examines maternal, paternal, fetal, and placental factors that affect the growth and development of the placenta with a focus on morning sickness. Elizabeth A. Shuey is a Policy Analyst at the Organisation for Economic Co-operation and Development where she works on issues related to early childhood, well-being of Indigenous students, and development of social and emotional skills across international contexts. She was formerly a xx

About the Contributors

Society for Research in Child Development Policy Fellow in the Office of Planning, Research and Evaluation in the Administration for Children and Families within the U.S. Department of Health and Human Services as well as a Doris Duke Fellow for the Promotion of Child Well-Being. Shuey received her PhD from the Eliot-Pearson Department of Child Study and Human Development at Tufts University and was recognized with the Society for Child and Family Policy and Practice Dissertation Award. Eloise A. Stark is currently reading for a DPhil in Psychiatry at Somerville College, University of Oxford. Her research concerns the neural, attentional, and behavioral mechanisms underlying parent-infant interaction. She completed her undergraduate degree in Experimental Psychology at Harris Manchester College, University of Oxford. Stark is a member of the British Psychological Society and has written for The Conversation and The Psychologist magazine. Peter N. Stearns is Professor of History and Provost Emeritus at George Mason University. Stearns has written widely on world and emotions history. His books include A History of Shame, The Industrial Turn in World History, Guiding the American University: Challenges and Choices, Doing Emotions History, Gender in World History, Satisfaction Not Guaranteed: Dilemmas of Progress in Modern Society, Childhood in World History, and American Fear: The Causes and Consequences of High Anxiety. He also edited the Encyclopedia of World History. Stearns taught at the University of Chicago, Rutgers University, and Carnegie Mellon University. He served as vice president of the American Historical Association, Teaching Division, and he founded and edited the Journal of Social History. Alan Stein is Professor of Child and Adolescent Psychiatry at the University of Oxford. He also holds an Honorary Professorship in the School of Public Health, University of the Witwatersrand, South Africa, and is an Honorary Fellow of the Child, Youth, Family and Social Development Programme of the HSRC, South Africa. He received his medical training at the University of the Witwatersrand, Johannesburg, South Africa. He was previously affiliated with the University of Cambridge, the Royal Free and University College London Medical School, and the Tavistock Centre. His main area of research concerns the development of young children in the face of adversity; the ultimate aim of this work is to develop interventions to enhance children’s early development and support their families. He is an authority on early child development, especially perinatal mental health and its effect on parenting and later child development and health. He jointly led the Lancet perinatal mental health series. Sandra Tang is a Research Investigator at the Institute for Social Research at the University of Michigan. She earned a PhD in Applied Developmental and Educational Psychology from the Lynch School of Education at Boston College. Her research program focuses on the role of the family in shaping children’s educational success, especially for those children who grow up in risky contexts. She is co-editor of Socializing Children through Language. Nicholas E. Waters is a PhD candidate in Developmental Psychology at the University of Michigan and an NICHD Fellow in Interdisciplinary Science. He received his BA from the University of Michigan in Psychology. His research focuses on children’s cognitive and academic skill developments and the neurobiological and contextual factors that contribute to different developmental trajectories. Ruiyong Wu is an associate professor at the Yangzhou University, China. He received his MS and PhD degrees from College of Life Science at Shaanxi Normal University. His research focuses on the behavioral and neurochemical mechanisms underlying maternal behavior. xxi

About the Contributors

Wai Ying Vivien Yiu received her BA from the University of California, Los Angeles, and  is currently a PhD student at the Graduate School of Education, the University of Pennsylvania. Her research interests include the influence of culture, social change, parenting, and children’s socioemotional development. Katherine S. Young is a Postdoctoral Researcher at the Anxiety and Depression Research Center, Department of Psychology, University of California, Los Angeles. She completed a DPhil in Psychiatry at the University of Oxford investigating the neurobiological basis of adults’ responsiveness to infant vocalizations and how this might be disrupted in depression. Her current research focuses on investigating responsiveness to social cues among young adults at risk for anxiety and depression as well as studying the effects of treatment for social anxiety disorder on activity and functional connectivity in the brain.

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PART I

Biology of Parenting

1 THE EVOLUTION OF PARENTING AND EVOLUTIONARY APPROACHES TO CHILDREARING David F. Bjorklund and Alyson J. Myers Introduction Child and developmental psychologists, sociologists, educators, and policy makers have long viewed parenting and the family as the most significant influence on the developing child. As such, parenting has traditionally been viewed as an important source of “environmental” variability in the long debated (and still controversial) nature/nurture dichotomy. At one level, of course, parenting is a potent part of a child’s environment. An infant’s very survival depends on parents. There is nothing in the external world so critical to a child’s success in life as her or his parents. Yet, parenting also straddles the nature side of the traditional continuum. Parenting is not only important to humans, but it is central to the survival of many species of animals, including all mammals and many birds (Rosenblatt, 2002). Evolutionary biologists have long recognized this fact, arguing that, in order for individuals to get their genes into the next generation, they must make investments in mating and, following conception, parenting (Hamilton, 1964; Trivers, 1972). How much is invested in mating versus parenting will vary among species and between females and males within a species, depending on characteristics of the developing offspring and ecological conditions. But parenting—the care and nurturing of offspring between conception and independence—is universal among mammals and, depending on the species-typical pattern of such investment, influences how offspring are reared. Homo sapiens, however, have taken parenting to new heights, not simply because of our use of language, advanced cognition, cultural transmission of knowledge, or societal institutions, but also because of the extended period of immaturity of our young. As all mammals, human children are conceived within their mothers’ bodies, fed after birth with mother-produced milk, and eventually mature to be able to fend for themselves. But the period of immaturity and dependency is extended in humans relative to other primates. This prolonged period of youth is seemingly necessitated by the intellectual demands of human society; children cannot learn enough in a decade of life to function effectively in any human group. This intellectual immaturity is accompanied by physical immaturity of offspring that puts extraordinary demands on human parents, surpassing those of any other land mammal. Such pressures have shaped how parents around the world treat children, the structure of the human family, and relationships between women and men. In this chapter, we provide an evolutionary view of human parenting. In a first section, we review briefly the basic tenets of evolution by natural selection and some of the major ideas of the field of evolutionary psychology, particularly evolutionary developmental psychology. We then review a more specific evolutionary theory, Trivers’s (1972) parental investment theory, which accounts for the 3

David F. Bjorklund and Alyson J. Myers

amount of investment females and males put into parenting (all actions related to rearing an offspring to reproductive age) versus mating (including the seeking, attaining, and maintaining of a mate). We next examine some of the selection pressures that produced our species, and how those pressures led to patterns of parenting and the structure of the family that characterize our species today. We then take a closer look at some of the factors influencing the decisions parents and other people make for investing in children. The final major section of the chapter examines some of the evolved psychological mechanisms—genetically coded “messages” that, following epigenetic rules, interact with the environment over time to produce behavior—associated with infant-mother attachment, evolved mechanisms underlying neglect, abuse, and infanticide, and how an evolutionary perspective questions the very concept of “parenting” as conventionally defined. In all, we argue that an evolutionary perspective not only tells us where patterns of childrearing came from, but where they may head in the future as ecological conditions change, and how many problems of contemporary parenting can be understood, and perhaps solved.

Principles of Evolution and Evolutionary Developmental Science Evolution by Natural Selection The basic ideas behind Charles Darwin’s (1859) great theory of “descent with modification” are surprisingly simple yet frequently misunderstood, particularly when applied to human behavior. The core of evolutionary theory is the concept of natural selection, which, simply stated, refers to individuals who are well suited to their environment leaving more progeny than less well-suited (or less fit) individuals. Natural selection works because there is variation among members of a generation; that is, there are different combinations of physical and behavioral traits among individuals within a species. Critically, these traits, as well as individual differences in these traits, are heritable. Characteristics that result in an individual surviving and reproducing are passed down from one generation to the next, whereas characteristics that are associated with early death or low levels of reproduction decrease in frequency in the population. Characteristics of the individual interact with features of the local ecology, and it is this interaction that is responsible for increases and decreases in characteristics over time. This is the process of selection, and through this process, adaptive changes in individuals, and eventually species, are brought about. Natural selection is a highly interactive process, involving an active organism’s response to a sometimes changing environment. Evolutionary theorists often use phrases such as “the trait was selected by the environment” as a shorthand to refer to this complex interaction among an organism, heritable traits of that organism, and the environment. However, the term “selection” does not imply some deliberate or foresighted process (e.g., selecting for more “advanced” individuals). Natural selection, and thus evolution, is blind to the future; individuals who fit well with a current environment survive, and those who fit less well die. Nevertheless, the process, although blind, is an active one, reflecting the bidirectional relation between an organism with heritable traits and the environment. Darwin used the term reproductive fitness to refer to the likelihood that an individual will become a parent and a grandparent. Contemporary evolutionary theorists, taking advantage of the scientific advances in genetics that have occurred since Darwin’s time, use the concept of inclusive fitness (Hamilton, 1964) to take into consideration the influence that an individual may have in getting additional copies of her or his genes into subsequent generations. For example, a child possesses 50% of a parent’s genes. Thus, it is in the parent’s best genetic interest to see that an offspring survives so that copies of the parent’s genes are passed on to grandchildren (each of whom will possess 25% of a grandparent’s genes). A person can further benefit the transmission of her or his genes by helping relatives, who share a smaller percentage of genes. For example, by helping to rear a sister’s four children, each of whom shares, on average, 25% of her genes, a woman can further increase her genetic 4

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contribution to the next generation, thereby increasing her inclusive fitness. Of course, none of this happens intentionally or consciously. After all, people do not walk around calculating exactly how related they are to one another before deciding to act altruistically. Rather, the underlying mechanisms are in terms of unconscious evolved “strategies.” Moreover, such patterns are observed in nonhuman mammals, birds, and social insects, indicating that self-awareness is not ordinarily involved.

Principles of Evolutionary Developmental Science Although the principles of evolution should be the same for physical, behavioral, or cognitive characteristics, psychologists investigating the evolution of behavior or cognition, particularly human behavior or cognition, have made explicit some of these principles. Moreover, developmentalists have added to or modified slightly some of these principles to achieve a better understanding of the role of evolution in contemporary human behavior (e.g., Bjorklund and Ellis, 2014; Bjorklund, Hernández Blasi, and Ellis, 2016; Bjorklund and Pellegrini, 2000, 2002; Geary and Bjorklund, 2000), and we examine briefly some of these principles here. First, an evolutionary account of behavioral or cognitive characteristics does not imply genetic determinism. Certainly, evolutionary change implies change in the frequency of genes within a population; but evolutionary psychologists argue that behavioral change occurs as a result of a transactional relation between an organism and its environment and that the eventual behavioral phenotype of an organism is not predetermined by its genes. From this perspective, development involves the expression of evolved, epigenetic programs, from conception through old age, as described by the developmental systems approach (e.g., Bjorklund, Ellis, and Rosenberg, 2007; Gottlieb, 2007; Gottlieb, Wahlsten, and Lickliter, 1998). Development occurs as a result of the bidirectional relations between all levels of biological and experiential factors, from the genetic through the cultural. “Experience,” from this perspective, involves not only exogenous events but also self-produced activity, as reflected by the firing of a nerve cell in response to solely endogenous factors. Functioning at one level (e.g., the genetic) influences functioning at adjacent levels (e.g., neuronal) with constant feedback between levels. Because the experiences of each individual are unique, there should be substantial plasticity in development. Yet, there is much that is universal about humans (or any species), and this seeming discrepancy is resolved when one recognizes that infants of a species, beginning at conception, inherit not only a species-typical genome but also a species-typical environment. To the extent that individuals grow up in environments similar to those of their ancestors, development should follow a species-typical pattern. From the developmental systems perspective, there are no simple cases of either genetic or environmental determinism. Infants are not born as blank slates; evolution has prepared them to “expect” certain types of environments and to process some types of information more readily than others (Bjorklund, 2015). Yet, it is the constant and bidirectional interaction between various levels of organization, which changes over the course of development, that produces behavior. For example, differences in the quality and quantity of parental investment affect children’s development and influence their subsequent reproductive and childcare strategies (e.g., Belsky, Steinberg, and Draper, 1991; Ellis et al., 2012, see discussion to follow). Second, there is a need for an extended childhood to learn the complexities of human communities. Homo sapiens spend a disproportionate amount of time as prereproductives. From an evolutionary perspective, the benefits associated with an extended period of immaturity must have outweighed the costs. We believe that the most important and difficult things children need to learn are related to the social complexity of human groups (e.g., Alexander, 1989; Bjorklund and Pellegrini, 2002; Dunbar, 2010), although the time to master tool use and food acquisition techniques (e.g., Kaplan and Gangestad, 2005; Kaplan, Hill, Lancaster, and Hurtado, 2000) would also require an extended juvenile period. 5

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Third, many aspects of childhood serve as preparations for adulthood and were selected over the course of evolution. Many sex differences in social and cognitive abilities are good examples (Geary, 2010). Evolutionary psychologists have often focused on sex differences (Hyde, 2014), proposing that women and men have different self-interests and thus have evolved different psychologies. This focus is reflected especially in sex differences with regard to mating, childrearing, and intra-sex competition. However, these behaviors, dispositions, and cognitions do not appear with the first blast of pubertal hormones or on hearing the cries of one’s newborn infant, but have developmental histories, with children adapting their gender-specific behavior to local norms, based on evolved predispositions. Such sex differences should not be viewed as a form of biological determinism, destining women and men to narrow and unchanging roles. Rather, girls and boys are biased toward different environments and experiences via evolved epigenetic rules, and, to the extent that one’s environment supports those biases, children will develop in a species-typical fashion. Although these epigenetic rules may be necessary, they are not sufficient to produce a particular developmental pattern (Bjorklund, 2015; Bjorklund et al., 2007). Human behavior is highly flexible, and although some outcomes are more likely than others, all require environmental support to be realized. Fourth, different selection pressures operate on organisms at different times in ontogeny. Although some aspects of infancy and childhood can be seen as preparations for adulthood, other features have been selected in evolution to serve an adaptive function at that time in development only and not to prepare the child for later life (Bjorklund, 1997, 2007). For example, some aspects of infancy may serve to foster the attachment between an infant and mother to increase the chances of survival at that time in ontogeny, and not only to prepare the child for later adult relationships. Evolution, we propose, has endowed children (and the juveniles of other species) with many characteristics that adapt them well to their immediate environments and not solely to prepare them for a future one. Fifth, simply because some social, behavioral, or cognitive tendency was adaptive for our ancestors, does not mean that it continues to be adaptive for modern humans. Similarly, just because some tendencies (such as violence among young adult males) are “natural” based on evolutionary examination, does not mean that they are morally “good,” excusable, or inevitable. For example, humans’ penchant for sweet and fatty foods can be seen as a formerly adaptive disposition that, in modern environments with grocery stores and Ben and Jerry’s Rocky Road Ice Cream, produces increased risk of obesity and heart attacks. Similarly, formal schooling represents a situation in which many of children’s evolved tendencies do not fit well with the demands of modern society. From the perspective of evolutionary psychology, much of what we teach children in school is “unnatural,” in that teaching involves tasks never encountered by our ancestors (see papers in Geary and Berch, 2016). Many other aspects of social and childrearing behavior, perhaps adaptive for small groups of hunters and gatherers living on the brink of survival, may not be adaptive for modern people living in nation-state societies. Although not all developmentalists have embraced the evolutionary principles described here (e.g., Witherington and Lickliter, 2016), evolutionary thinking has increasingly permeated theorizing in developmental science and is well on its way to becoming a metatheory—a common set of broad, overarching assumptions and principles—for developmental psychology (Bjorklund, 2016, 2018). Evolutionary theory has been particularly influential for researchers studying cognitive and social-cognitive development (e.g., Geary, 2005; Tomasello, 2016). However, the greatest impact of evolutionary theory as it relates to developmental science has likely been to parenting, dating back to the theorizing of John Bowlby (1969) on attachment and, especially, to Robert Trivers’s (1972) parental investment theory, and we describe Trivers’s influential theory in the following section.

Parental Investment Theory Human parents, particularly mothers, devote substantial time, resources, and energy to rearing their children. Given humans’ extended period of youth, there is likely no other species that devotes as 6

The Evolution of Parenting

much time and energy to their offspring from conception to adulthood as Homo sapiens. To try to make sense of exactly why parents are so involved in a child’s life, it is important to understand the evolutionary reasons why selection would act to produce parents who invest so much in their children. First, children are a parent’s most direct route to genetic immortality. Although a person can serve her or his inclusive fitness by helping rear nieces, nephews, and younger siblings, reproductive fitness is most directly served by having children who grow up to become reproductive members of the community. From this perspective, evolution should operate to select parents who provide the means by which their offspring attain maturity, and later, carry on the parents’ reproductive lineage. Parents should provide not only the physical means necessary for their children’s survival (e.g., food, shelter), but also the means by which children develop competencies in the social groups in which humans live. At first glance it may seem as if both females and males should be equally likely to invest in their children, but this is not the case. For most species, including humans, females invest more heavily in their offspring than males. This observation and the theory developed around it known as parental investment theory, was first postulated by Trivers (1972). Trivers based his ideas on Darwin’s (1871) theory of sexual selection. Sexual selection refers to members of one sex displaying preferences for certain characteristics of individuals of the other sex, for example peahens showing a preference for the elaborate tails of peacocks. Darwin believed that sexual selection would occur for two reasons: First, there would be competition within one sex for access to the other and, second, there would be differential choice of mate selection by members of one sex for members of the other. Generally, sexual selection takes the form of males competing with one another for access to females, whereas females choose among males, often based upon signs of a male’s genetic fitness, successful domination over competing males, and the likelihood of his providing resources to her and her offspring. But why is this pattern, with males competing and females choosing, found so clearly both crossculturally and across species? The answer, Trivers theorized, lies in the amount of parental investment each parent typically contributes to an offspring. Differential amounts of parental investment actually occur before the child is even conceived. For mammals, this is due to the fact that females produce a finite number of eggs that are large and immobile. Males, in contrast, produce an unlimited number of small, mobile sperm throughout their lifetimes. This difference in sex-cell size causes females’ eggs to be more costly metabolically, and thus a limited resource, relative to sperm. Furthermore, the fact that her eggs are immobile means that conception will happen inside the female’s body, and she will then carry the child through the gestational period, and usually, be primarily responsible for lactation and care of the infant after birth. Male investment can theoretically end following copulation. As such, males have higher potential reproductive rates, in that, following insemination of a female, they can seek additional mating opportunities; in contrast, once conception has occurred, females’ mating opportunities end (at least temporarily) and their parenting efforts begin. The end result is that male mammals typically invest more in mating than parenting, whereas the reverse pattern is found for females. This greater initial investment by females, Trivers argued, is what sets in motion two differing strategies as to how to go about finding and maintaining a mate and rearing subsequent offspring. Depending on the requirements of the young, there are substantial species differences in the amount of post-copulatory investment males provide to their offspring. Males of some species contribute literally no support to their progeny or the mother, whereas others may spend considerable time and energy garnering resources for their offspring, and even spend time in “childcare.” However, in greater than 95% of mammals, males provide little or no postnatal investment to their offspring (Clutton-Brock, 1991). Human males are an exception to the typical mammalian pattern. But despite the well-known role of fathers as providers (“bringing home the bacon”), and to a lesser extent as caregivers, women in all cultures provide more support and engage their children more frequently than men (Barnard and Solchany, 2002; Parke, 2002). This pattern is observed in traditional cultures (Lancy, 2015), in 7

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industrialized societies (Whiting and Whiting, 1975), and persists in modern societies in which women work outside the home (Hetherington, Henderson, and Reiss, 1999). There were changes in Western cultures over the 20th century, with many fathers spending significant time with their children, sometimes approaching the time investment made by mothers. However, in these same societies, the number of children living in homes headed by females increased fourfold since 1960 (see Cabrera, Tamis-LeMonda, Bradley, Hofferth, and Lamb, 2000). Thus, social forces in today’s world influence degree of paternal investment, but the overall pattern is still women devoting more of their time in childcare than men, even in the most enlightened families. The consequences of such differential investment in offspring have important implications for sex differences in behavior. For women, sexual intercourse brings with it possible conception and pregnancy. Until recently, infants required breast milk to survive, and this could be provided only by the mother or other lactating females. Fathers in generations past could not take the 3 a.m. feeding; the responsibility for feeding infants fell solely to mothers, making postnatal parental investment for women obligatory (as it is for females of other mammalian species). Men’s minimum required investment is today, and surely was in the ancient past, substantially less. As a direct result of this differential minimum investment between women and men, women tend to be more cautious in assenting to sex than men (Oliver and Hyde, 1993). Women must not only evaluate the physical qualities of a potential mate (is he healthy, strong, fertile, and so forth), but they also must evaluate his access to resources (is he wealthy, of high status, or otherwise capable of supporting a family) and the likelihood of his sharing them with her and her offspring. In contrast, men are less concerned with the resources of a future mate or her likelihood of sharing. His greater interest lies with her genetic fitness (is she healthy?) and her ability to conceive, give birth, and care for a child. These are not necessarily conscious concerns of either sex, for they are reflected in the behavior of nonhuman animals as well (Clutton-Brock, 1991; Trivers, 1972, 1985). Members of the less investing sex compete with one another for access to the more investing sex. In many mammals, the result of such competition is a physically larger male. Increased size and strength afford males a competitive edge with other males and are associated, in many species, with higher social status and greater access to females (Geary, 2000, 2010). (High-status or otherwise successful males do not simply “take” females as mates; rather, by being successful in competition with other males, they possess traits that females, over evolutionary time, have come to prefer.) Females, of course, also compete with one another over males (Smuts, 1995), but female-female competition is rarely as physically fierce as that between males and is much less apt to result in injury or death (Campbell, 1999, 2013). Moreover, most females will eventually find a mate, even if an undesirable one; in contrast, some males will be have no access to females, “shut out” of the Darwinian game altogether. Finally, whereas maternity is always certain, paternity never is. It is within the women’s body that the child is conceived and carried to term, making maternity a sure thing. Males, in contrast, have no such assurance. A man could spend time, energy, and other resources investing in another man’s biological child, which would not be adaptive from an evolutionary (reproductive fitness) perspective. As a result, men are apt to question the paternity of their children and may be less likely to invest in a child when that child’s paternity is in question. In general, males may be more likely to invest minimally in their offspring because they know that females will continue to invest in their child, even if the male invests little, or even deserts her completely. In sum, evolutionary theory predicts that mothers will be more likely than fathers to invest heavily in their offspring. This phenomenon is seen both cross-culturally and in many species of mammals (as well as most sexually reproducing species). When fathers do invest, they are most likely to do so when they are sure that the child is genetically their own, and they are sure that the child is healthy enough to reach reproductive age. This pattern is prevalent in humans today, but it is widely assumed that it is an old one that has evolved in our species over the past 5 million years. 8

The Evolution of Parenting

The Environment of Evolutionary Adaptedness Depending on how one defines modern humans, animals identifiable as Homo sapiens appear in the fossil record as long ago as 300,000 years before present in the form of Archaic Homo sapiens, or as late as 35,000 years ago, when the first unambiguous evidence of artistic expression is seen. Anatomically modern humans are found in fossil records dating back about 100,000 years (see Tattersall, 2013). But human-like creatures, termed collectively hominins to refer to bipedal (upward walking) apes including humans and our ancient ancestors, date back 5 to 7 million years ago (mya). Hominins include members of the Homo genus, but also members of the Australopithecus and Ardipithecus genera. Although determining with certainty the species to which any fossil belongs is difficult, it is nonetheless certain that many physically and presumably behaviorally different species of hominins have existed over the past 7 million years, with several different species of hominins living at the same time. Homo sapiens are the only living member of this group, all others becoming extinct. Homo sapiens is a relatively young species that has not changed much over the past 100,000 years, at least physically, and certainly little at all over the past 35,000 years or so. But humans’ physical conservatism belies a behavioral and cognitive flexibility that has resulted in a radical change in how we live as a species. The advent of agriculture and a sedentary lifestyle beginning about 12,000 years ago changed drastically how most human beings lived. For most of the history of Homo sapiens and its immediate forbears, individuals lived in small, nomadic groups, living off the land, gathering fruits and vegetables (mostly the work of women), scavenging from the kills made by other animals, and hunting (mostly the work of men). In one form or another, it was in such hunter/gathering/ scavenging environments in which the modern human mind evolved. Although life has changed substantially for most members of our species since the advent of agriculture and sedentary lifestyles, there has not been sufficient time for our brains, and the evolved psychological mechanisms within them, to evolve. Basically, modern humans possess brains and minds adapted for life in a very different environment than they find themselves living today. This ancient environment is often referred to as the environment of evolutionary adaptedness. What was this environment like, how did our ancestors behave, and what pressures were there that resulted in the modern human mind, and, importantly for this chapter, how did these pressures lead to the human way of rearing children? It is impossible to specify exactly what the environment of evolutionary adaptedness was like, in part because it is impossible to define precisely what time period this term represents. On the one hand, humans share an evolutionary history with all extant primates and mammals. Thus, historical environments in which these ancestral mammals and, later primates, evolved are also relevant to modern humans. If we take as our starting point, however, the period in which the genetic line that would eventually lead to Homo sapiens separated from the line that would lead to modern chimpanzees, we find a period of about 5 to 7 million years, beginning in the forests and savannas of Africa. Because of the dearth of fossil and archeological evidence for periods much before 2 mya, it is difficult to say anything with confidence about the lifestyles of the various species of australopithecines. However, based on what fossil evidence we do have and on the way in which chimpanzees live today, it is highly likely that hominins were always social species. Based again on limited fossil evidence, the organization of chimpanzee and bonobo troops, and the lifestyles of contemporary hunter-gatherers, it is likely that the size of most social groups during the Pleistocene was relatively small (probably between 30 and 60 people), consisting of both closely related and unrelated individuals, who interacted on a regular basis. As in all societies today and for the vast majority of mammals, mothers were the primary caregivers to their children. Fathers likely provided protection to their mates and offspring and support in the form of food and other tangible resources (Kaplan et al., 2000), but likely spent relatively little time in direct childcare. Some males surely had several mates, meaning that some females shared the resources and attention of a single male and that some males had no access to reproductive females. 9

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Females probably reached puberty relatively late (late teens, early twenties), and gave birth every 3 to 5 years, with pregnancy often following the cessation of nursing a previous child (Kaplan et al., 2000; Konner, 2010). Infant mortality was surely high, and, even for those who did survive to adulthood, life was relatively brief by contemporary standards, with few people living past 40 years (Austad, 1997). However, if contemporary hunter-gatherer societies are any indication, it is likely that there were always some “old” people (i.e., beyond 60 or 70 years) in every group (Hill and Hurtado, 1991; Kaplan et al., 2000). Although hominin groups were usually small, social relationships, especially among large-brained members of the Homo genus, were surely complex. Humans in all societies around the world cooperate and compete with one another and with people from outside groups. Trade among different social groups is universal to humans, as is warfare. We are aware of no other mammal that engages in trade, and only the chimpanzee displays anything similar to war parties, attacking and killing members of another group of their own species (Goodall, 1986). All species, as all individuals, have histories, and what happened in the past influences what happens now and what will happen in the future. Although humans do not have imprinted in their brains in any simple way the experiences of their ancestors, the environments of ancient Homo sapiens shaped our ancestors’ social and cognitive evolution, with modern children and adults inheriting essentially the same brains as our hunter-gatherer forebears, designed by natural selection to solve recurrent problems of survival. In the next section, we examine some of the selection pressures that led to the evolution of human intelligence and the human family.

What Were the Selection Pressures that Led to the Modern Human Mind and the Human Family? There have been many hypotheses about the “causes” of human evolution. Selection pressures related to hunting, tool use, navigating large environments, coping with variable environments, diet, and dealing with conspecifics have all been suggested (among others) as the principal “cause” of human evolution. There is, of course, no single cause for the evolution of any species, including humans. Rather, evolution surely proceeded as the result of a confluence of interacting factors, with no single one being identified as a simple “cause” or “consequence” of another. This does not mean, however, that some hypotheses of human evolution are not better than others, and the one we prefer, which, we believe accounts well for humans’ unique cognitive abilities and style of childrearing, focuses on three interrelated factors: an enlarged brain and the accompanying cognitive abilities, increased social organization and the need to better cooperate and compete with conspecifics, and an extended juvenile period (Bjorklund and Bering, 2003; Bjorklund and Pellegrini, 2002). Each of these factors in concert with the others contributed to changes in what it took for infants to survive and to grow up to become reproductive members of their group. We describe briefly here the role of social intelligence and “big brains” in the human evolution story, and focus on how these factors may have contributed to a prolonged juvenile period, necessitating increased parental investment.

The Significance of Social Intelligence A number of theorists have proposed that the single most important selection pressure in the evolution of human intelligence was sociality—interacting, competing, and cooperating with other members of the species (e.g., Alexander, 1989; Bjorklund and Pellegrini, 2002; Byrne and Whiten, 1988; Dunbar, 2010; Hare, 2011; Humphrey, 1976; Tomasello, 2014). As hominin groups became more complex, a greater social intelligence was required to maneuver the often stormy waters within small groups of long-lived conspecifics. Individuals who could reflect on their own knowledge,

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The Evolution of Parenting

intentions, and desires, and, importantly, the knowledge, intentions, and desires of others (theory of mind), would have been at an advantage in cooperating and competing with others both within and outside their immediate group. As social cohesion became more important in primate and hominin groups, the need to control sexual and aggressive responses also increased in importance (Bjorklund and Harnishfeger, 1995). This need to control sexual and aggressive urges may have been particularly true for early humans, attributed, in part, to changes in females’ receptivity to sex. In many primates, there is considerable competition between males for access to estrus females. The receptivity of females to sexual advances varies across species, with female chimpanzees, bonobos, and some monkeys being receptive for a period of time beyond the period of estrus, resulting in extended competition among males. In contrast to the other great apes, human females do not show any (obvious) outward signs of ovulation, and, unlike other mammals, they present permanently swollen mammaries, whether nursing or not, which have become constant sexual signals for males, despite their unreliability in predicting sexual receptivity or ovulation. Thus, sexual receptivity in both human females and males cannot be determined by physical body signs, such as swollen genitals in apes. Moreover, both females and males are, in theory, continually receptive sexually, with their willingness to copulate being primarily under the control of social and not hormonal factors. These changes in female sexual behavior (potentially receptive even when not ovulating) and appearances (no outward sign of sexual receptivity or ovulation) may have contributed significantly, along with other factors, to human pair bonding. For a male hominin, whose investment is required if his long-dependent offspring is to survive, it is critical that he be confident that his resources are going to his genetic progeny and not to the offspring of another male. But being certain of paternity can be problematic in a species in which ovulation, and thus fertility, cannot be known by the male, and when females, as well as males, are potentially sexually receptive at all times. To counteract this dilemma, males may resort to some form of mate guarding, in which they hover near their mates during her fertile time, preventing her access to other males. But males cannot guard their mates all of the time. And, although it may seem to be to the female’s advantage to have as many options in terms of potential mates as she can, mating with a large number of males would do her little good if none of them contributed significantly to the support of her offspring, which seems to have been, if not necessary at least highly desirable, in hominins (Geary, 2010). One solution to these problems may have been the “invention” of neurochemical systems (opioids and oxytocin) that fostered strong emotional bonds between a female and male, producing marginally (and temporary) monogamous behavior in the pair, long enough so that children can reach an age so that they can care for themselves (Fisher, 1992). As we have suggested, one condition necessary for substantial paternal investment to evolve would be a high degree of paternity certainty. This seems to have been achieved in contemporary humans. Studies from a broad range of countries have estimated the degree of paternity discrepancy (in which the domestic father is not the genetic father) to be between 7% and 15% (see Bellis and Baker, 1990; Lerner and von Eye, 1992), although more recent studies put the rate at between 1% and 2% (Larmuseau et al., 2013). Thus, although women clearly engage in extra-mate copulations (surely enough for men to have evolved mechanisms to guard against cuckoldry), they apparently do not frequently make cuckolds of their mates. The result is a male who can be relatively confident of the paternity of his offspring, a female who obtains resources for herself and her offspring from her mate, and an offspring who survives past infancy. Inhibitory abilities necessary for increasing the control of sexual and aggressive behaviors would require increased neural capacity, and they may have been part of the selective pressures that led to enhanced brain size, particularly of the neocortex, in the hominin line. Alternately, other factors may have been primarily responsible for the increase in brain size seen in hominins over the past 5 million

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years, with greater inhibitory abilities being a by-product of this increase, co-opting neural circuits that had been selected for other purposes. Nonetheless, once inhibitory abilities did increase, the behaviors they produced were subject to natural selection. And whether they were primarily a cause or a consequence of increased brain power, what is undeniable is that brain size did increase, and, for better or worse, Homo sapiens’ large brain and resulting cognitive processes define us, more than any other feature, as a species.

Large Brains Humans have disproportionately large brains relative to their body size ( Jerison, 1973, 2002). Brains are very expensive in terms of the calories they consume, so that having “more brain” than needed to control the body must have substantial benefits for survival. Homo sapiens’ large cranium did not materialize out of thin air, however. Primates in general have larger brains than expected by their body size (represented by the encephalization quotient, or EQ, which reflects brain size relative to the expected brain size for an animal of a specified body size; Jerison, 1973); humans merely reflect an extension of a pattern already observed in primates. Figure 1.1 shows the EQ for chimpanzees and for several hominin species. (An EQ of 1.0 is the “expected” value, with EQs greater than 1.0 reflecting “more brain” than predicted for an animal of a specified size.) As can be seen, the encephalization quotient for Australopithecus afarensis was only slightly greater than that of modern chimpanzees. From this point on in evolution, brain weight relative to body weight increased at a rapid rate. One set of factors responsible for this change was related to the increased social complexity of hominin groups, although changes in diet, technology, and responses to modifications in climate all likely played interacting and contributory roles. But regardless of the reasons (i.e., selective pressures) for increased brain size, there must be some mechanisms within the organism for achieving this change. One important mechanism, we believe, can be found in alterations of patterns of development, which, in turn, would provide additional changes that must pass through the sieve of natural selection.

8

Encephaliztion Quotient

7 6 5 4 3 2 1

P. troglodytes

A. afarensis

H. habilis

H. erectus

H. sapiens

Figure 1.1 Encephalization quotients for chimpanzees (Pan troglodytes) and four hominid species (data for chimpanzees from Jerison, 1973; data for hominids from Tobias, 1987). An EQ of 1.0 is the “expected” value, with EQs greater than 1.0 reflecting “more brain” than predicted for an animal of a specified size.

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The Consequences of Delaying Development Although humans’ brains are bigger than those of their ancestors, somewhat ironically, one mechanism by which brains increased in size was the process of delayed development. Some evolutionary changes can be brought about by changing patterns of development. Genetic-based differences in developmental rate have been referred to as heterochrony (de Beer, 1958; Gould, 1977). For simplicity sake, we will talk about only two general forms of heterochrony, acceleration, in which the rate of development (ontogeny) in an individual is accelerated or extended relative to one’s ancestors, and retardation, in which development is slowed down or delayed in comparison to ancestral patterns. In one sense, big brains are a good example of accelerated development. The development of the brain of Homo sapiens is clearly extended beyond that of its progenitors. Yet, to achieve that extension required the delaying of a pattern of growth rate typical of the prenatal period to postnatal life. The primate brain develops rapidly in comparison to the overall size of the body (Bonner, 1988). For chimpanzees, macaque monkeys, and other primates, brain growth slows quickly after birth; this is much less so for humans. Rather, the rate of prenatal brain growth for humans continues over the first 2 years of life (Gould, 1977). By 2 years of age, the human brain has attained 50% of its eventual adult weight; in contrast, total body weight is only about 20% of what it will eventually be (Tanner, 1978). Increasing the time the brain grows increases the number of neurons that are produced (Finlay, Darlington, and Nicastro, 2001) and also results in the extension of dendritic and synaptic growth, so that the human brain has more neurons and more interconnections among neurons than the brains of other primates (Finlay et al., 2001; Gibson, 1991). Although most parts of the brain have undergone enlargement in human evolution, the effects are most pronounced on the neocortex, the so-called “thinking” portion of the brain. The extension of embryonic growth rates for the brain into the second year of life was necessitated by some physical limitations of human females. Big brains require big skulls, and if a human newborn’s skull were as large as “expected” given the eventual adult size (and given the standard primate rate of pre- and postnatal brain development), the infant’s head would be too large to fit through the birth canal. The size of women’s hips (which determine the size of the birth canal) are limited by the need for bipedality. A woman with hips large enough to give birth to an infant having the cranium the size of a contemporary 2-year-old child would not be able to walk. Thus, evolutionary pressures that resulted in an enlarged brain required that pregnancy be extended only to the point where the infant skull would fit through the birth canal. The result is a physically immature infant, motorically and perceptually far behind the sophistication of other primate infants (see Antinucci, 1989; Gibson, 1991). Along these lines, Piantadosi and Kidd (2016) proposed the evolving relation between brain size and parental care was the driver for human evolution. Humans are physically immature at birth (altricial), being born early enough to accommodate for their large brain size. However, due to this early birth, newborns are rather helpless and require extensive caregiving to survive. This extensive caregiving requires more intelligence, which, according to Piantadosi and Kidd, led to larger brains. Piantadosi and Kidd proposed a model illustrating that remarkably large brains and high intelligence are due to runaway selection associated with caring for physically immature and helpless infants. This runaway selection is similar to the runaway dynamics that are seen in sexual selection, where, for example, female preference may cause selection to run out of control and result in males having traits that are not beneficial for survival. If a longer tail helps a bird to fly more quickly, aiding survival, females will prefer the longer-tailed males. However, this selection may run out of control, as females choose even longer tails over time, resulting in plumage that is large and detrimental to avoiding predators, as seen in peacocks. The current model examines birth age, adult head/brain size, and an individual’s intelligence, all of which are subject to selection pressures. Piantadosi and Kidd’s results suggest that there were strong effects of infant altriciality on primate intelligence. 13

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The researchers suggested that humans’ advanced means of reading social intentions may have evolved to care for helpless neonates and that these demands may also be associated with the rise of social systems of cooperative breeding, in which mothers receive assistance from mainly female kin in rearing offspring (Hrdy, 2009). As a result, human brain and cognitive development soon became accelerated relative to their primate cousins, due in large part to the retention of fetal brain-growth rate (Langer, 1998; Parker and McKinney, 1999). Rate of brain development is not the only aspect of ontogeny that is delayed. As a species, humans spend a disproportionate amount of time as prereproductives. Worldwide today, the average age of menarche is between 12.5 and 13.5 years. However, for both girls and boys, there is typically a period of low fertility, extending the nonreproductive years even further (Bogin, 1999; Tanner, 1978). Based on historical data and data from traditional cultures (Hill and Hurtado, 1996; Kaplan et al., 2000), it is likely that our ancient ancestors were closer to 18 to 20 years of age before being fully reproductive. Such delayed reproduction is all the more impressive when one considers that the likely life expectancy of our hominin forebears was substantially less than ours today, meaning that many children would die before reaching reproductive age, and that many others would have only a limited number of reproductive years (Volk and Atkinson, 2013). Many women, for example, surely died in childbirth. When looked upon in hindsight, our delayed maturation had substantial risks. Given these risks, the selective pressures for this delayed maturation must have been derived from strong compensatory advantages of the immature state, most notably increased flexibility of learning. Human development is different from that of other primates not only in quantitative terms (i.e., being slow and extended), but also in qualitative terms. For example, Bogin (1999) proposed five stages of development for Homo sapiens: infancy, childhood, juvenility, adolescence, and adulthood, two of which (childhood and adolescence) are not observed in any other species. Infancy ends with the cessation of nursing and is followed in other mammals by the juvenile period, in which the young animal is no longer dependent on its parents but is not yet sexually mature. In contrast, weaning in humans occurs between 2 and 5 years of age, but it is another several years before children can eat an adult diet and otherwise fend for themselves. The juvenile period in humans (often referred to as middle childhood) is followed by adolescence, with its characteristic growth spurt, and continues until sexual maturity, typically in the late teen years. No other species displays this rapid growth spurt before adulthood, although chimpanzees and bonobos also apparently have a post-menarche period of infertility (Bogin, 1999). Based on fossil evidence, Bogin (1999) estimated that the life stages of our australopithecine ancestors were similar to that of chimpanzees (Pan troglodytes), consisting of a period of infancy lasting 5 or 6 years, followed by a juvenile period with adulthood beginning about 12 years of age. According to Bogin, it is only with the beginning of the Homo line that a period of childhood is seen, and only in modern Homo sapiens is there evidence for a period of adolescence. In addition to the emergence of childhood and adolescence, the length of juvenility and adulthood is longer in humans than in other primates and is almost certainly longer than for our hominin ancestors. There is also evidence from fossil dental and cranial development that brain development in Neanderthals was much faster than in modern humans (e.g., Akazawa, Muhesen, Dodo, Kondo, and Mizouguchi, 1995; Dean, Stringer, and Bromage, 1986; Zollikofer, Ponce de León, Martin, and Stucki, 1995). Mithen (1996) used this evidence to suggest that the modern human mind, with the ability to communicate between different cognitive modules, required an extended juvenile period, and Nielsen (2012) proposed that the emergence of fantasy play and imitation during childhood were necessary components for the evolution of human intelligence. There are many possible reasons for the extension of developmental periods in humans (Bogin, 1999), but the very fact of this developmental extension indicates than ancient members of the Homo line were able to keep children alive long enough to reach an age at which they could reproduce themselves. Note also that the extended developmental period is associated with an enlarged brain. 14

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We, and others (Bogin, 1999; Dunbar, 2010), believe that the extended period of youth and an enlarged brain was necessitated to master the increasing complexity of the social environment. In fact, research showing relations among large brains, an extended immaturity, and social complexity was reported by Joffe (1997), who compared aspects of brain size with length of the prereproductive period and aspects of social complexity for 27 primates, including humans. Joffe reported that the proportion of the lifespan spent as a juvenile was positively correlated with group size and the relative size of the nonvisual neocortex. This is the part of the primate brain that is associated with complex problem solving, including memory. Joffe argued that social complexity exerted selection pressures for increased nonvisual neocortex in primates and an extension of the juvenile period. Extended childhoods would also be useful for mastering other important skills in addition to social intelligence. For example, Kaplan et al. (2000) proposed that it was ancient humans’ shift to a higher-quality diet that necessitated greater cognitive skills and thus an extended childhood to learn. Chimpanzees, for example, rely primarily on a diet of easily extracted fruit and plants with low nutrition density. Such foods, when available, can be obtained relatively easily even by juveniles. Chimpanzees obtain only a small portion of their diet via hunting, which provides foods of high nutrition density. Hunting, however, is engaged in mainly by adults, and takes considerable time to learn. Kaplan et al. (2000) examined food-gathering procedures in contemporary hunter-gatherer societies and noted that, similar to chimpanzees, children often forage for low-density, easily accessible foods, such as ripe fruit, at young ages and become relatively adept at the task. Extracting foods of higher nutrition density, such as roots and tubers or vertebrate meat through hunting, is performed effectively only by older individuals and require many years to master. What does all this have to do with the formation of the human family and patterns of parenting? First, the enlargement of the Homo brain required that much of brain growth continues postnatally, due to restrictions of the female anatomy. This extended physical dependency was coupled with an extended childhood due to the need to learn the complexity of one’s social environment (or possibly, in addition, to learn the mechanisms for processing high-quality food), which further extended the time children spend as prereproductives. Humans’ extended period of immaturity necessitated that adults, particularly mothers, be disposed to care for their long-dependent offspring. Although natural selection may have increased the probability that parents are disposed to care for their children, ancestral parents could not invest indiscriminately in offspring. Rather, parents and other adults responsible for the care of children, must evaluate how best to devote their time, effort, and material resources to children, a topic we turn to in the following section.

Investing in Children If children are to grow to become sexually mature and economically productive members of their community, they require substantial support from their parents. Parents allocate effort and resources to their offspring that could otherwise be devoted to mating effort or spent on their own physical development and acquisition of resources. Yet, allocating resources to an infant not only limits one’s own ontogeny and mating efforts, but also compromises opportunities to invest in other offspring, both those born and unborn (Keller, 2000). Although it may seem obvious that parents, particularly mothers, will do anything to enhance the survival of their children, there are factors, in both contemporary and ancient environments, that affect how much mothers are willing to invest. These factors include the health of a child, the conditions of the local economy/ecology, the presence of additional children, the age and reproductive status of the parents (particularly the mother), and the amount of social support available to help rear a child, among other factors (Bornstein, 2015). We focus here on the issue of social support. Human mothers likely have never reared a child “alone.” Because of the extended dependency of their offspring, human mothers must spend more time caring for their offspring than mothers of other mammals, leaving less time for activities that 15

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would be important for their own growth and that of their other offspring. This extended dependency of offspring made it necessary for a mother to receive assistance from others, including resources and some childcare from the father, but also support from members in the community. In this section, we discuss briefly the two most likely sources of support for a mother and her offspring: fathers and children’s grandparents.

The Importance of Paternal Investment The long period of offspring dependency meant that a male’s genetic success could not be measured just by how many children he sired. His inclusive fitness would depend on how many of his offspring reached sexual maturity, assuring him of becoming (at least) a grandfather. To increase the odds of this happening, his help in rearing his children would be needed. Human males devote more time to “parenting” than the vast majority of mammals (Clutton-Brock, 1991) and, in most contemporary hunter-gatherer societies, provide the majority of calories consumed by both their offspring and their mates (Kaplan et al., 2000). Increased paternal investment permitted human females to rear multiple dependent offspring and to cut the childhood mortality rate in half in comparison to other primates and group-hunting carnivores (Lancaster and Lancaster, 1987). The significance to survival and success of paternal investment is not just speculative, but is supported by evidence from modern societies, contemporary hunter-gatherers, and historical records (see Geary, 2000, 2010, for reviews). For all types of data sets, children’s mortality rates are higher and their social status is lower when fathers are absent. Moreover, in contemporary U.S. America, the quality of a father’s active and supportive involvement in his children’s lives is positively associated with emotional regulation, academic achievement, and social competence (Cabrera et al., 2000; Lamb, 1997).

Grandparental Support Although fathers may be the most important source of support to a mother and her children, in all societies, support also comes from related kin, most often from the child’s grandparents. The conditions under which grandparents are apt to provide support are similar to the conditions under which fathers are likely to make investments—when genetic relatedness is high. Maternal grandparents, like the mothers themselves, can be quite confident that the baby is related to them, whereas paternal grandparents, as fathers, can never be 100% certain of paternity. As such, evolutionary theory predicts that, on average, maternal grandparents will invest more in their grandchildren than will paternal grandparents, and the research literature has consistently confirmed this relation (Smith and Drew, 2002). Studies from a variety of countries have shown that maternal grandparents have more contact with and show greater solicitude toward their grandchildren than paternal grandparents, even after controlling for the distance the grandparents live from their grandchildren (Smith and Drew, 2002). Moreover, maternal grandfathers are viewed as devoting more care to their grandchildren than paternal grandmothers, despite the greater childcare role that women play in all cultures (e.g., Danielsbacka and Tanskanen, 2012; Euler and Weitzel, 1996). A similar pattern of investment has been found for maternal versus paternal aunts and uncles (Gaulin, McBurney, and Brakeman-Wartell, 1997; Pashos and McBurney, 2008). Consistent with these findings, child survival is increased by the presence of a maternal grandmother. For example, based on 150 years of German birth/death records, Beise and Voland (2002) reported that children with living maternal grandmothers were more likely to survive than children without living maternal grandmothers, and, in rural Ethiopia, help provided by a mother’s mother was associated with lower child mortality (Gibson and Mace, 2005). Other research has shown that the presence of a maternal grandmother was associated with higher fertility and 16

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survival rates for Canadian and Finnish farm families (Lahdenperä, Lummaa, Helle, Tremblay, and Russell, 2004). Grandparents who contribute to the success of their adult offspring and their grandoffspring can serve to decrease infant morbidity and mortality rates, which increases their inclusive fitness. Some have even speculated that such grandparental investment has contributed significantly to Homo sapiens’ longevity (e.g., Hawkes, O’Connell, and Blurton Jones, 1997; O’Connell, Hawkes, and Blurton Jones, 1999). Characteristics associated with longevity can be selected for if older people continue to reproduce. That is, long-lived individuals can pass these characteristics directly to their offspring. However, most human females in traditional societies have their last children 20 or 30 years before they die. Thus, both women who live long lives and those who live shorter lives are likely to have reproduced before natural selection will have had an effect on genes associated with longevity. But genes for longevity can be selected for if long-lived (but nonreproducing) individuals foster their grandchildren’s survival. There is evidence from a variety of species for the “grandmother hypothesis” (because it is primarily grandmothers and not grandfathers who provide support to their grandchildren). Vervet monkeys, baboons, lions, and humans in traditional societies all benefit from the presence of a grandmother (Hawkes, 2004; Hawkes et al., 1997; Packer, Tatar, and Collins, 1998). For example, research with the Hadza, a small group of foragers living in Africa’s Rift Valley, found that older women’s foraging was particularly important for the nutrition of young children who had been weaned but who were not yet prepared to eat adult food (O’Connell et al., 1999). Hawkes et al. (1997) reported that, in families in which mothers were nursing, the nutritional status of weaned children was related to the foraging efforts of their grandmothers rather than their mothers. If this pattern reflects ancestral populations, the result would have been to increase fertility by permitting mothers to wean a child earlier and become pregnant again sooner. Without grandmother support for weaned children, nursing would likely continue for several more years, reducing the total number of children a female could expect to have. Although most mammal mothers have sole responsibility for the care of their infants, this is not the case for humans. Unlike the vast majority of male mammals, human fathers in all societies provide some childcare and/or resources to their children, with additional care being provided by a host of alloparents, people other than the genetic parents who help care for a child (Hrdy, 2009). In many cultures, maternal grandmothers are the most frequent alloparents, contributing to the health, survival, and perhaps even longevity of their grandoffspring. Yet, natural selection not only provides clues to parents and others about whom to invest in (e.g., genetically related children), but also provides psychological mechanisms to increase the chances that investment will indeed be made, a topic we turn to in the next section.

Evolutionary Perspectives on Attachment and Parenting Evolutionary theory can provide some insights into how patterns of human parenting came to be, but does an evolutionary approach to parenting provide anything more than an interesting historical perspective? We argue that it does, that looking at parenting through the lens of evolutionary theory can be useful for understanding important aspects of childrearing relevant to people in contemporary societies (Bjorklund and Ellis, 2014; Bjorklund and Pellegrini, 2002; Keller, 2000). Perhaps the most empirical research related to parenting from an evolutionary perspective concerns attachment and the consequences that styles of attachment have for subsequent development. This is due, in part, to the fact that Bowlby (1969), the founder of modern attachment theory, saw attachment from an ethological (as well as psychoanalytic) perspective, believing that attachment served an adaptive function to infants in the environment of evolutionary adaptedness. In the following sections, after a brief discussion of evolutionary developmental models of attachment, we look at how evolutionary 17

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explanations can be helpful in understanding the possible psychological mechanisms in play when parenting “goes wrong,” resulting in the neglect, abuse, or even the death of children at the hands of their parents.

Evolutionary Adaptations that Promote Attachment It is one thing to say that adults are biased toward caring for their helpless offspring, but it is quite another to propose mechanisms for such behavior. We have argued previously that infants (and their parents) have evolved low-level perceptual biases that, in interaction with species-typical experiences, result in species-typical behavior (Bjorklund, 2015; Bjorklund and Ellis, 2014; Bjorklund et al., 2007). For example, human infants are biased to attend to displays of biological motion (e.g., Bardi, Regolin, and Simion, 2011, 2014) and to face-like stimuli (e.g., Easterbrook, Kisilevsky, Hains, and Muir, 1999; Mondloch et al., 1999), and to match certain facial gestures of adult models, such as tongue protrusion (neonatal imitation; Meltzoff and Moore, 1977; but see Oostenbroek et al., 2016), each of which serves to foster social relationships (i.e., attachment) with their caregivers. Adults also possess evolved mechanisms, increasing the likelihood that they will form attachments to their helpless wards. In fact, Bowlby (1969) proposed that infants evolved certain signals and abilities to promote social relationships with their parents (see also Goetz, Keltner, and Simon-Thomas, 2010). Such cues can be physical (e.g., baby-schema features described by Lorenz, 1943, including a rounded and large head relative to body size, fat cheeks, a flat nose, big eyes located below the middle of the face profile, and short and broad extremities), behavioral (e.g., smiling, clumsy movements; Bowlby, 1969), or vocal (e.g., infants’ crying as cues to health; DeVries, 1984; Kringelbach, Stark, Alexander, Bornstein, and Stein, 2016; Soltis, 2004). In recent years, research has focused on the effects that baby-like faces, as described by Lorenz’s baby-schema, have on adults’ attitudes and behavior toward infants. Research has consistently reported that adults rate baby-faced infants as cuter, more attractive, friendlier, and more helpless and powerless than infants and older children with more mature faces (e.g., Alley, 1981; Leibenluft, Gobbini, Harrison, and Haxby, 2004; Senese et al., 2013); such immature physical features are also associated with enhanced motivation for caregiving, and even a higher likelihood of making a favorable adoption decision (e.g., Glocker et al., 2009; Waller, Volk, and Quinsey, 2004). Adults continue to view young faces positively until about 4.5 years of age, after which adults’ ratings of likeability and attractiveness of infant faces are similar to ratings of adult faces (Luo, Li, and Lee, 2011). Although faces may no longer serve as powerful cues promoting caregiving for young children, adults respond positively to some aspects of preschool-age children’s verbal expressions of cognitive immaturity (e.g., “The sun’s not out because it’s mad”), with children expressing such statements being rated more highly on items reflecting positive affect (e.g., likeable, cute) and helplessness, and lower on items reflecting negative affect (e.g., sneaky, feel more irritated with) than children expressing more mature cognition (e.g., “The sun’s not out because a cloud moved in front of it”; Bjorklund, Hernández Blasi, and Periss, 2010; Hernández Blasi, Bjorklund, and Ruiz Soler, 2015). Some research has shown that this positive bias for immature faces (Fullard and Reiling, 1976; Gross, 1997; but see Borgi, Cogliati-Dezza, Brelsford, Meints, and Cirulli, 2014) and immature cognition (Hernández Blasi and Bjorklund, 2018; Periss, Hernández Blasi, and Bjorklund, 2012) is not observed until later adolescence, beginning about 15 years of age, suggesting that the bias may be related to the possible onset of parenthood. These biases of infants to attend to social cues and of adults to be positively disposed to immature features of infants and children serve to promote the survival of helpless, dependent offspring, primarily through the development of attachment. Infant-mother attachment is common throughout the animal world, particularly in mammals and birds. According to Del Giudice (2009), attachment is a biologically based motivational system that evolved to protect children from danger while motivating caregivers to provide care. Bowlby (1969) believed that, although all but the most deprived 18

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of infants become attached to their mothers or mother figures, there were measurable differences in the quality of attachment, with some forms of attachment (notably secure) being associated with better psychological outcomes than others (notably insecure). Moreover, it was behaviors of mothers that served to establish and maintain style of attachment. Research by Ainsworth and her colleagues (e.g., Ainsworth, Blehar, Waters, and Wall, 1978; Ainsworth and Wittig, 1969) over the past 50 years has generally supported Bowlby’s contention. For example, securely attached infants are likely to have mothers (or other caregivers) who respond to them contingently and who are responsive to their signals of physical and social need (e.g., Harrist and Waugh, 2002; Isabella and Belsky, 1991); and longitudinal research has demonstrated that children and adolescents who were classified as securely attached as infants and toddlers display better social and cognitive functioning than those who had been classified as insecurely attached (Thompson, 2006). These relatively robust patterns led many to the conclusion, consistent with Bowlby’s original proclamation, that secure attachment represents the most adaptive style, with aspects of insecure attachment being predictive of poor adjustment and psychopathology (see Thompson, 2006). Other theorists, however, speculated that attachment systems are flexible and evolved to adapt individuals to subsequent environments (e.g., Belsky et al., 1991). From this perspective, different patterns of attachment should develop as a function of the ecological conditions of a child’s local environment (including amount of parental investment). Moreover, attachment classifications should reflect adjustments to contemporary environments and should not necessarily be stable over time when ecological conditions vary (Lewis, Feiring, and Rosenthal, 2000). The evolutionary-based theory that has generated the most research and controversy in this area is that of Belsky et al. (1991). Belsky et al. (1991) formulated psychosocial acceleration theory that links childhood experience, psychological development, somatic development, and reproductive strategies. They proposed that aspects of children’s environments affect their attachment style and also important aspects of later reproductive strategies. According to Belsky et al. (1991, p. 650), a principal evolutionary function of early experience—the first 5 to 7 years—is to induce in the child an understanding of the availability and predictability of resources (broadly defined) in the environment, of the trustworthiness of others, and of the enduringness of close interpersonal relationships, all of which will affect how the developing person apportions reproductive effort. Rather than viewing secure attachment as being the “best strategy” for a child to follow, they proposed that humans have evolved mechanisms that are sensitive to features of the early childhood environment that induce rate of pubertal maturation (especially in girls) and influence reproductive strategies. Specifically, they suggested that children from homes characterized by high stress, insecure attachment, and father absence, attain physical maturity early, are sexually promiscuous, and form unstable pair bonds. This pattern contrasts to children from low-stress, secure attachment, and fatherpresent homes, who reach puberty later, delay sexual activity, and form more stable pair bonds. The former strategy may be adaptive for children growing up in harsh and unpredictable environments with little expectation of social support. In such cases, both females and males invest relatively more in mating than parenting, taking a “quantity over quality” perspective. In the latter case, in which children receive social support in a low-stress, adequately resourced environment, they invest relatively more in parenting than mating, taking a “quality over quantity” perspective. In other words, Belsky and his colleagues proposed that children follow alternate reproductive strategies, depending on the availability of resources in their rearing environment, which results in differential investment in the next generation. Although it is beyond the scope of this chapter to review the literature that has accumulated on this issue, the hypothesis has generally been supported by the research literature (see Belsky et al., 19

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2007; Ellis, 2004; Ellis, Figueredo, Brumbach, and Schlomer, 2009). Children from high-stress, fatherabsent homes who experience harsh and unpredictable early environments participate in more risky and aggressive behavior, have earlier pubertal maturation (especially females) and sexual debut, form unstable pair bonds, become pregnant earlier, and will provide less investment to their offspring than children who experience less harsh and more predictable environments (e.g., Ellis, 2004; Ellis et al., 2009; Nettle, 2010; Nettle and Cockerill, 2010; Placek and Quinlan, 2012). Similar effects have been observed in some nonhuman mammals. For example, male rats reared in heightened environmental stress conditions showed more adolescent play-fighting behavior (Parent and Meaney, 2008) and adult aggressive behavior (Menard and Hakvoort, 2007), whereas female rats shifted to an earlier reproductive strategy (Meaney, 2007). This sex difference of enhanced effects for females makes sense, given the differential investment in offspring by females and males. Because females’ investment in any conception is greater than that of males, they should be more sensitive to environmental factors that may affect the rearing of offspring (such as malnutrition, stress, lack of resources) than males.

Evolved Mechanisms Underlying Neglect, Abuse, and Infanticide It seems a given that all parents want the best for their children—that children are parents’ route to immortality. From a Darwinian perspective, reproduction is the sine qua non of success, making situations in which parents do not act in the best interests of their children paradoxical. These situations become a bit easier to understand, however, when one considers that any given child is only one of potentially many offspring, some of whom may be better candidates for continuing a parent’s genetic heritage than others. Differential parental investment. Parents often choose to invest differentially in their offspring, investing the most in those who have the greatest chance of reaching reproductive age and thus carrying forth the parents’ genes. Parents must balance costs associated with care of a specific child against resources that can be used for other children, both those born and yet born, and for the parents themselves. Differential investment in offspring is most apparent in the behaviors of mothers. In ages past, it seems likely that mothers who were skilled at identifying cues to a child’s future reproductive success could invest more time, energy, and resources in those children, influencing substantially the likely survival of her various offspring. Mothers who were less proficient at making these discriminations or less reluctant to act on perceived differences, were likely to squander scarce resources on a child who may not make it to adulthood, no matter the degree of investment made. From this perspective, evolution has selected mothers who are skillful at identifying which children, as well as which circumstances, are best suited to rearing a child to reproductive years (Hrdy, 1999, 2009). Reduced maternal investment can take many forms. Children may be neglected, receiving less attention, medical care, and food than they might need; they may be abused, wet-nursed, fostered out with relatives or even strangers, or left in the custody of a religious institution. Infants and children in some cultures have been sold into slavery, or at the extreme, put to death (Hrdy, 1999). Under what conditions would parents, particularly mothers, decide to reduce investment in children? One set of salient cues comes directly from infants themselves. Sickly babies may be a bad investment, particularly if caring for a sickly child means devoting fewer resources to healthier children or postponing becoming pregnant again with the chance of having a healthy baby who is more likely to survive and thrive. Although our society places a high value on the life of even the most sickly infants, this is not universal. For example, anthropological data indicate that the killing of a deformed or seriously ill infant was sanctioned in about one-third of the traditional cultures studied (Daly and Wilson, 1984). In our own society, children with intellectual impairment or those who have other congenital defects, such as Down syndrome, spina bifida, cystic fibrosis, or cleft palate, are abused at rates 2 to 10 times higher than unaffected children (see Daly and Wilson, 1981 for review);

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and when these children are institutionalized, parental interest rapidly decreases, and many are not visited ever (Daly and Wilson, 1988). Differential investment in sickly infants is often less severe, as exemplified by Mann (1992), who examined the interaction between mothers and their premature and extremely low-birth weight twins. Although there were few differences in the interaction patterns between mothers and each of their twins at 4 months of age, by 8 months all mothers in the study showed more positive behavior toward the healthier of the two twins. That is, maternal preferences were clearly linked to the baby’s health, mediated, quite surely, by the differential behavior and appearance of the two siblings (Sameroff and Suomi, 1996). Other factors that influence maternal investment include the child’s age, such that older children (who, by living as long as they have, demonstrate viability) often receive more investment than younger children, particularly in times of high stress and low resources (Daly and Wilson, 1988); mother’s reproductive status, with younger mothers being more likely to neglect, abuse, or kill their infants than older mothers (Daly and Wilson, 1988; Lee and George, 1999), presumably because younger mothers have greater opportunity for having more children than older mothers; and social support, with mothers who have little social support being more likely to abandon an infant than mothers with greater social support (Daly and Wilson, 1988; Lancaster, 1989). We have provided evidence of neglect, abuse, and infanticide to illustrate the extremes that parents sometimes go in making decisions about parental investment. From a broader perspective, human parents are generally supportive of their children, with abuse and infanticide being relatively rare phenomena. However, the circumstances under which humans abandon their infants are similar to those seen for many other species. Hrdy (1999) suggested that mothers may kill their own infants when other means of birth control are unavailable and they were unwilling or unable to commit themselves to further care of the infant. However, with notable exceptions, mothers rarely plan to kill their babies. To quote Hrdy (1999, p. 297): Rather, abandonment is at one extreme of a continuum that ranges between termination of investment and the total commitment of a mother carrying her baby everywhere and nursing on demand. Abandonment is, you might say, the default mode for a mother terminating investment. Infanticide occurs when circumstances (including fear of discovery) prevent a mother from abandoning it. Although legally and morally there is a difference, biologically the two phenomena are inseparable. Stepparent investment. Incidence of neglect, abuse, and even death, although still rare, are more likely to occur at the hands of stepparents than biological parents. From a strictly inclusive fitness perspective, any resource a stepparent provides to stepchildren will not benefit that parent’s fitness. The stepchild possesses none of the stepparent’s genes, and presumably the adult’s resources could be better spent supporting her or his own genetic offspring. Yet, stepparenting is widespread throughout the world and through recorded history, and despite the myths and realities of the fate of children at the hands of stepparents, the vast majority of stepparents love and care for their children (Hetherington and Stanley-Hagan, 2002). Perhaps the first question we should ask is, “Why should a stepparent provide any resources to a stepchild?” Most evolutionary psychologists have suggested that parental investment from a stepparent is actually investment in mating, not investment in parenting (e.g., Anderson, Kaplan, and Lancaster, 1999). For example, a stepfather provides support to his wife’s children from a previous mating to maintain her companionship and for the children he will father with her. Women with children from a previous male select men who will not only provide support for themselves and their future offspring, but also for their children from previous matings.

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But stepparents rarely provide the same level of support to their stepchildren as they do to their natural children. Research from a wide range of cultures indicates that the amount of financial resources parents provide, and the amount of time spent interacting with stepchildren, is significantly less than for natural children (e.g., Flinn, Leone, and Quinlan, 1999; Marlowe, 1999). For example, Anderson and his colleagues (1999) found that the amount of financial resources children in the United States are likely to receive for their college education was considerably less for families that consisted of a stepfather and a biological mother than for families consisting of two biological parents. In an observational study of the Hazda, biological fathers communicated, played with, and nurtured (held, fed, pacified, cleaned) more their natural children than their stepchildren (Marlowe, 1999), despite adults’ claims of equal feelings and care for natural and stepchildren. Not providing as much money for college for a stepchild as for a biological child, or playing more with a natural child than with a stepchild, reflects pancultural differences in the amount of parental investment made to biological versus nonbiological offspring, consistent with the tenets of parental investment theory. But having a smaller college fund than a biological offspring is far from stepchild abuse. Yet, all cultures appear to have their own versions of Cinderella. Such folklore, unfortunately, has a basis in reality. Child abuse and homicide are both more likely when a child lives with a stepparent than with two biological parents (Daly and Wilson, 1988, 1996). In a Canadian study, Daly and Wilson (1985) reported that children were 40 times more likely to be abused if they lived with a stepparent than with two natural parents. Differences remained substantial even after potentially confounding factors such as poverty, mother’s age, and family size were statistically controlled. Perhaps even more disturbing are findings for child homicide, a crime that, unlike child abuse, is almost always reported to authorities. Daly and Wilson (1988) examined the results of several surveys of crime data from around the world and reported a similar pattern independent of country: Children were more likely to be killed by a stepparent than by a genetic parent, with this difference being particularly large for children under 2 years of age. Rates of child homicide were sometimes more than 100 times larger for stepchildren than for biological children. Even the risk of unintentional death (e.g., drowning) is greater in stepfamilies than in biologically intact families. For example, in one Australian study preschool children’s unintentional deaths were significantly higher for children from stepfamilies than for children from intact or single-parent families (Tooley, Karakis, Stokes, and Ozanne-Smith, 2006). Murder of one’s stepchildren, of course, is not sanctioned by modern societies. (Although in some contemporary hunter-gatherer societies, when a man marries a woman with children, it is acceptable for her young children be put to death; see Daly and Wilson, 1988). Men who kill their stepchildren are inevitably convicted and incarcerated, so there is no adaptive value to killing a stepchild. Yet, the fact that abuse and murder of stepchildren are enormously greater than for natural children suggests that the restraints against acting violently toward nonrelated children are much less than the restraints involved with one’s genetic children. The love and affection that parents “naturally” feel toward their biological children must be nurtured, often with substantial effort, to be felt for stepchildren. We are not suggesting that killing stepchildren, or unrelated children in general, was once adaptive in our evolutionary past, and that the higher rates of abuse and homicide observed for stepchildren than for natural children represent the activation of these atavistic mechanisms. Rather, we argue that in high-stress situations in which violence is apt to occur, the evolved tendencies that inhibit aggressing against one’s biological children are not as easily activated for one’s stepchildren.

Is “Parenting” the Right Concept to Describe Human Childrearing? From what we have presented to this point, as well as from a common-sense perspective, there should be no debate that parents play a key role in their children’s development. However, the “parenting” model that most U.S. Americans seem to adopt—with parents (and teachers) actively teaching 22

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their children the skills and values of their culture—may be at odds with how our forechildren were treated and developed. For example, anthropologists have reported that parents in traditional societies, including hunter–gatherer societies, rarely explicitly teach their children; rather, children acquire the skills and norms of their culture through observation and during play with mixed-age peers (e.g., Konner, 2010; Lancy, 2015). A similar point was made by Scarr (1992, 1993) more than 25 years ago (quite controversial at the time, see Baumrind, 1993; Jackson, 1993), who proposed that “ordinary differences between families have little effect on children’s development, unless the family is outside of a normal, developmental range. Good enough, ordinary parents probably have the same effects on their children’s development as culturally defined super-parents” (Scarr, 1992, p. 15). In other words, “superparenting” is not required to rear a successful adult; rather, children adapt to variations in childrearing, which, claimed Scarr, is a product of natural selection. A species such as Homo sapiens, that lives in varied environments and under a broad array of cultural traditions, must be flexible to the vagaries of “ordinary” parenting if the species is to continue. More recently, Gopnik (2016) has made a similar argument, proposing that the popular term “parenting” implies shaping children’s lives with the goal of creating successful adults. Gopnik likens this method to being a carpenter, where one shapes the material into a product of your choice. According to Gopnik, the stress for parents trying to shape their children into successful adults is high and the expectations set by parents can cause undue stress in their children. Gopnik (2016) suggests a different metaphor for parenting, that of the gardener. Instead of trying to shape children into successful adults, parents should provide a caring environment in which children can grow and develop, just as gardeners do with their plants. She argues children have evolved to develop in this way; it was the way our ancestors developed, and it is still relevant for our modern world. As previously discussed, humans are unique in that we have a prolonged juvenile period that includes childhood and adolescence. This prolonged period of immaturity allows for children to explore their surroundings, and they are intrinsically motivated to do so. Children learn about their environment and how the world works through their exploration, skills that will help them to successfully navigate adulthood. Play is also an essential aspect of childhood; children engage in pretend or fantasy play, which helps them learn about interacting with others and provides practice for dealing with hypothetical situations and symbols. Gopnik argues that, consistent with the way children evolved to learn as reflected by the childhoods of hunter-gatherers (Konner, 2010; Lancy, 2015), parents should not tell their children how to play or shape them into what they desire or consider successful, but instead to provide an environment that is safe, nurturing, and stable to allow them to explore the world’s possibilities.

Conclusions Ever since Darwin, there has been the recognition of continuity in cognitive and social functioning among different species. Homo sapiens share a heritage with other primates and mammals, and evolutionary theory provides the means of assessing that heritage. In many ways, when it comes to parenting, humans are just another mammal. They invest substantially in their offspring, with females investing disproportionately more than males; they consider the availability of resource and the likelihood of a “payoff ” when devoting resources to their children; males’ and grandparents’ investment is based partly on degree of genetic certainty; and the sex differential in parental investment dictates, to a substantial degree, the ways females and males relate to one another. Yet, in other ways, human parenting is different from that of other mammals, and such differences are also predicted from evolutionary theory. Because of the confluence of a number of factors, including a big brain and the cognitive ability that accompanies it, increased social complexity, and, most critically we believe, an extended period of youth, human children require greater investment to reach maturity than the young of other primates. This period of prolonged youth means that fathers must contribute more to their offspring if they are to be successful than is the case for the vast majority of males from other 23

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mammalian species. This has led directly to the formation of the human family, which, although taking many specific forms, is universal in our species. Evolutionary theory provides the “big picture” for how the human family and our particular way of parenting has come about. It is a fascinating story, we believe, but it is more than just history; it also provides a perspective that helps us understand important issues of parenting in contemporary societies. Many people unfamiliar with evolutionary theory assume that it is concerned only with species universals—traits that characterize all normal members of the species (or all members of one sex). Individual differences, the argument goes, are ignored or handled poorly by evolutionary theory. As the examples provided earlier in the application of parental investment theory to the phenomenon of child abuse and to quality of attachment indicate, this depiction of evolutionary theory is inaccurate. Evolutionary psychological approaches consider how evolved mechanisms become expressed over development as a function of local ecological conditions. Although evolutionary psychology certainly proposes there are universal mechanisms characterizing members of a species, this is not equivalent to proposing hard-wired “instincts,” impervious to environmental variations. Just as an individual inherits a species-typical genome, she or he also inherits a species-typical environment. Both genome and environment are constrained, in that there can be only so much variation to still produce a viable organism. But that variation can be substantial, and evolutionary theory can be useful in predicting and explaining individual differences in important social, emotional, and cognitive realms, and possibly suggesting means to deal with persistent societal problems.

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2 PSYCHOBIOLOGY OF MATERNAL BEHAVIOR IN NONHUMAN MAMMALS Aya Dudin, Patrick O. McGowan, Ruiyong Wu, Alison S. Fleming, and Ming Li Introduction Mammalian mothers of different species may differ in the extent to which physiological and psychological factors contribute to the postpartum expression of their nurturant behavior. In all species that have been studied, however, the physiological determinants are only realized in individuals that have had certain developmental histories and that are psychologically “prepared” by their physical and psychological environments (Rosenblatt and Snowdon, 1996). In many mammalian species the hormonal changes associated with late pregnancy and parturition predispose the newly parturient female to be nurturant with her offspring, to nurse, clean, and protect them. However, whether these nurturant behaviors in fact occur at the appropriate time and in the appropriate way depends on a host of psychological and environmental factors. Enhanced morbidity or mortality of young or reduced responsiveness by mammalian mothers occurs if mothers are stressed during pregnancy or parturition, severely food deprived, or are placed in low-resourced environments (Lyons, Kim, Schatzberg, and Levine, 1998), if ambient temperature precipitously rises, if pups are sickly, or if the nesting area is inadequate (Herskin, Jensen, and Thodberg, 1998; Kinsley, 1990; Leon, Coopersmith, Beasley, and Sullivan, 1990). However, mothers are also robust; to eliminate maternal behavior entirely, environmental restrictions or debilitations experienced by mothers have to be extreme and depend on the animal’s background and genetics (Aubert, Goodall, Dantzer, and Gheusi, 1997; Jenkins, McGowan, and Knafo-Noam, 2016; McGuire, Pachon, Butler, and Rasmussen, 1995; MilevaSeitz, Bakermans-Kranenburg, and van IJzendoorn, 2016; Stolzenberg and Champagne, 2016b). In nonhuman primates, examples of the importance of interactive influences of early experiences and hormones on mothering are still more pronounced. Harlow’s “motherless” monkeys raised in social isolation and on wire mothers, or monkeys who are young and inexperienced, neglected or battered their own (usually first) offspring, despite having apparently normal pregnancies and childbirths (Brett, Humphreys, Fleming, Kraemer, and Drury, 2015; Coe, 1990; Harlow, 1963; Ruppenthal, Arling, Harlow, Sackett, and Suomi, 1976). In human beings, a host of background and psychological factors increases risk of mothering disorders, including poverty, low education, social isolation, lack of supports, and immaturity, being themselves victims of abuse (Agrati and Lonstein, 2016b; Barrett and Fleming, 2011; Britton, 2008; Brummelte and Galea, 2016; Correia and Linhares, 2007; Daly, 1990; Dennis, Heaman, and Vigod, 2012; Di Florio et al., 2013; Eisenberg, 1990; Lancaster, Gold, Flynn, and Yoo, 2010; Lomanowska, Boivin, Hertzman, and Fleming, 2017; Milgrom et al., 2008; O’Hara

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and Swain, 1996; van Bussel, Spitz, and Demyttenaere, 2009; Vesga-López et al., 2008; Viguera et al., 2011) and their genetics (Mileva-Seitz et al., 2016). Even in “lower” species and situations where hormones exert clear and powerful influences on maternal behavior, the behaviors will not occur or will be masked by competing responses given dysfunctional past or present experiences. Conversely, in primates and human beings, in particular, the clear importance of these background and situational factors may seem to mask the role of biological factors in early mothering; however, a variety of approaches help to unmask contributions of these biological influences (see Fleming, Lonstein, and Lévy, 2016). This chapter provides a summary of the interaction between psychological and physiological influences in the expression of maternal behavior in nonhuman mammalian mothers. We first briefly discuss sensory, experiential, and other psychological factors that regulate maternal behavior in selected nonprimate mammals (including altricial species with litters: primarily rats and mice, and also precocial species with one or two young: e.g., sheep). We then summarize neural bases, neurochemical mechanisms, and genetics of maternal behavior, focusing on research on the roles of dopamine and serotonin in the limbic and hypothalamic regions and in their related genes. The specific approach adopted here assumes that maternal behavior is not regulated in a unitary fashion, but depends for its expression on activation of a variety of behavioral systems, mediated by multiple neurochemical and neuranatomical substrates. It assumes further that hormones and associated neurochemicals do not automatically trigger behavior, but instead act on substrates whose activation is influenced by the animal’s social/psychological and physical environments, both past and present. The interaction between newborn and the mother alters the basic mechanism of behavioral expression in both. In this chapter, the maternal behavior of rodents receives considerably more attention than maternal behavior in other nonprimate mammals. This orientation is based on a number of considerations. First, comparisons among rat and other nonprimate mammals (where appropriate data exist) show many similarities in physiological regulation of parenting (Lonstein, Levy, and Fleming, 2015). In addition, most research on mechanisms of maternal behavior focuses on Rattus norvegicus mothers, and as a result, understanding of this species is more complete. Finally, despite large differences in behavioral organization between the rat and human maternal behavior, the rat has proven to be a productive model for the analysis of human maternal behavior and has provided insights into possible mechanisms at work in human beings (Corter and Fleming, 1990; Fleming, Ruble, Krieger, and Wong, 1997; Fleming, Steiner, and Corter, 1997; Lonstein et al., 2015; Tombeau Cost et al., 2016). However, because of the extensiveness of research on rodent maternal behavior, this review does not attempt to be complete or exhaustive (Bridges, 2016b; Numan and Young, 2016; Olazábal et al., 2013a, 2013b). Its approach reflects most strongly the views and work of the authors. The chapter is divided into a number of sections. The first section describes the basic techniques used in the study of maternal behavior in rodents. The second section discusses the effects of the maternal hormones on maternal behavior and on other behaviors that undergo change when a female gives birth. This section also describes the transition that occurs in the regulation of maternal behavior after the initial period of hormonal priming and emphasizes factors regulating the longterm maintenance of maternal behavior. In this section the roles of learning, memory, and reinforcement are considered. The third section of the chapter considers the role of sensory factors in the onset and maintenance of maternal behavior, with particular attention to olfactory and somatosensory input during mother-litter interactions. The fourth and fifth sections of the chapter describe in considerable detail what is known about the neurochemistry and neuroanatomy of maternal behavior and of other behaviors that co-occur with maternal behavior in the postpartum animal. The sixth section briefly describes work on the genetic and epigenetic bases of maternal behavior.

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The final section of the chapter summarizes some of the main themes raised in the chapter and issues yet to be explored.

Methodological Issues in the Study of Rodent Maternal Behavior The popularity of the rodent (mouse and rat) as the animal of choice in the analysis of the physiology of parenting is based on both practical and scientific considerations. The laboratory rodent is an easy animal to breed, care for, and test. Its use permits the application of experimental manipulations providing greater control over physiological or psychobiological variables that is not possible with nonlaboratory animals, primate models, or human beings. For instance, to understand the role of hormones in the regulation of parenting we can analyze the behavior before and after the removal of the gland that produces the suspected hormone or before and after the administration (by injection or capsule) of the suspected hormone. Using a similar “extirpation and replacement” paradigm, we can evaluate the involvement of different sensory systems or different neural circuits in behavioral regulation by observing behavior before and after the destruction of specific neuronal cell groups within the brain by a variety of lesioning techniques (Afonso, Sison, Lovic, and Fleming, 2007; Li and Fleming, 2003a, 2003b) or by the use of psychoactive drugs (Li, 2015) that either block or enhance the functioning of specific neurotransmitters in the brain. Conversely, we can attempt to augment or facilitate the expression of the behavior in initially nonmaternal animals by the application of electrical (Morgan, Watchus, Milgram, and Fleming, 1999b), hormonal (Fleming, Cheung, Myhal, and Kessler, 1989a), or drug stimulation (Kinsley et al., 1994; Wu, Gao, Chou, Davis, and Li, 2016) that mimics the action of naturally occurring neurotransmitters. In some cases, when a longitudinal design is impractical, different groups sustaining different experimental and control conditions are compared. Thus, for instance, we might test the behavior of a group of animals which have been injected with a particular hormone or chemical that we suspect is normally released when animals become maternal at parturition and compare their maternal behavior with the behavior shown by a control group of animals which have received injections containing a related but biologically inert substance (i.e., placebo). Convergent with these invasive experimental approaches, we can also undertake correlational, rather than experimental, analyses and relate changes in physiology with changes in ongoing behavior; thus we can explore electrical events or hormonal or neurochemical changes that occur when an animal expresses maternal behavior. For instance, we can use microdialysis plus high performance liquid chromatography (HPLC) techniques to measure neurotransmitters that are released during ongoing behavior (Afonso, Shams, Jin, and Fleming, 2013). Alternatively, by means of immunocytochemical staining techniques we can determine whether particular proteins, neuropeptides, or other brain chemicals are produced in the mother’s brain in response to interactions with offspring (Numan and Numan, 1994; Zhao and Li, 2012). The role of early experiences in the development of the behavior can be studied by comparing the adult behavior and neurobiology of animals that have been raised under different early environmental conditions, with or without a mother or siblings or with and without certain nest-related cues (Rees, Akbari, Steiner, and Fleming, 2008; Rees, Steiner, and Fleming, 2006). Effects of adverse early experiences prenatally as well as postnatally can be assessed by evaluating the adult behavior of offspring of mothers who are stressed, malnourished, or who are administered agents or toxins, like antipsychotics, cocaine, or alcohol (Francis and Kuhar, 2008; Li, 2015). The effects of genotype and these maternal effects can then be partialled out by comparing animals that have been raised by their own mothers and those raised by foster mothers. Least well formulated are the technologies associated with establishing which genes or gene complexes regulate adult maternal behavior (Akbari et al., 2013). Strategies that have been employed to study heredity and genetic factors in the regulation of maternal behavior include comparison of different strains, cross-fostering within and between strains (Gomez-Serrano, Tonelli, Listwak, 32

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Sternberg, and Riley, 2001), the analysis of transgenic mice mutants that lack specific genes (so called “knockout” mice) that underlie the production of specific proteins and receptors in brain that are involved in the expression of maternal behavior (Caldwell, Aulino, Freeman, Miller, and Witchey, 2016), and use of molecular techniques that assess the animal’s genetic profile and activation of particular genes during ongoing behavior (Ribeiro, Agmo, Musatov, and Pfaff, 2016). As well, the use of functional magnetic resonance imaging techniques in awake rats allows a delineation of the functional neural circuitry and exploration of roles of neuropeptides, such as oxytocin and vasopressin, in the maternal brain (Febo, 2011; Febo, Felix-Ortiz, and Johnson, 2010; Febo and Ferris, 2014). Finally, newer techniques that have not yet been adequately utilized in the study of maternal behavior include optogenetics, which would permit the specific manipulation of individual neurons within the maternal neural circuit (Wu, Autry, Bergan, Watabe-Uchida, and Dulac, 2014). In the discussion that follows, many of the techniques, strategies, or approaches described above have been adopted to augment our understanding of the physiology of parenting. To facilitate navigation through the somewhat more technical portions of this chapter we provide a brief description of the relevant terminologies and techniques at the beginning of some of the more technical sections.

Description of Maternal Behavior at Parturition Although the study of maternal behavior in rodents has generated a smaller literature than has the study of many other species-typical behaviors, it is by no means a new area of interest. In fact, some of the most detailed and informative descriptions of the rat mother-litter interactions were provided by Wiesner and Sheard in their seminal book Maternal Behavior in the Rat, published in 1933. Based on this long history of research, we have a relatively complete picture of the phenomenology of rat maternal behavior. The new mother rat is maternally responsive to newborn pups as soon as they emerge from the birth canal (Hudson, Cruz, Lucio, Ninomiya, and Martinez-Gomez, 1999; Rosenblatt, Lehrman, and Rheingold, 1963). At parturition, she pulls off the amniotic sac, eats the placentas, and cleans off the pups (Hudson et al., 1999; Kristal, Thompson, Heller, and Komisaruk, 1986). Within the first 30 minutes after parturition, she gathers all the pups together, retrieves them to a nest site, mouthes and licks them, and adopts a nursing posture over them; she does all this without prior experience interacting with pups (Fleming and Rosenblatt, 1974a). When a female interacts with her litter after the birth, she engages in many proximal interactions. After the nest has been constructed and the pups have been retrieved into it, the dam spends a considerable proportion of her time mouthing and licking the pups, especially their anogenital regions (Moore, 1990), a behavior that functions to promote urination and elimination by the offspring and to maintain the dam’s fluid balance (Friedman, Bruno, and Alberts, 1981). The dam also gathers the young underneath her ventrum, permitting pups to gain access to her teats and suckle (Stern, 1989). Once the pups begin to suckle, the dam usually adopts a high arch crouch posture over them and becomes immobile for a period (Stern, 1989, 1990; Stern, Dix, Bellomo, and Thramann, 1992). The high motivational state of the new mother is illustrated by observations that, if new mothers are prevented from actively exhibiting these proactive maternal behaviors (by application of a muzzle over their snouts), they nevertheless spend considerable time nudging and pushing at the pups and manipulating them with their forepaws (Stern and Keer, 1999). In addition, they will overcome their anxiety to retrieve pups from the open arms of an elevated plus maze into the closed arms (Yang et al., 2015). The virgin animal, by contrast, is not maternally responsive when first presented with newborn foster pups (Rosenblatt, 1967; Wiesner and Sheard, 1933), and she does not retrieve pups on the elevated plus maze (Yang et al., 2015). In fact, initially she moves away from pups and actively avoids them (Fleming and Luebke, 1981b; Terkel and Rosenblatt, 1971). However, within 1 to 2 days of continuous pup stimulation, the virgin becomes habituated to pups and is willing to lie down in close proximity to them (Fleming and Luebke, 1981b; Fleming and Rosenblatt, 1974a; Terkel 33

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and Rosenblatt, 1971); after 5 to 10 days of continuous contact with foster pups, the virgin begins to respond maternally (Rosenblatt, 1967), showing a pattern of behavior that resembles that of the new mother, but also showing some differences (Lonstein and De Vries, 1999). This experimental procedure has come to be known as “pup-induction” or “pup-sensitization”, and is useful to study the influences of parturitional hormones on maternal behavior. Associated with changes in actual responses to pups, new mothers undergo changes in multiple psychological states which contribute to these responses. These changes are in the realms of mothers’ cognition, memory, executive functions, impulsivity, emotion regulation, and anxiety (Lonstein et al., 2015). Changes in these functions are reflected, either immediately after parturition or later in the postpartum period, in the pattern of interactions with the young. They are, in turn, regulated by neural and neurochemical systems that intersect with mechanisms more directly implicated in mothering per se. Similar psychological changes occur in species ranging from rats to humans (Barrett and Fleming, 2011; Lomanowska et al., 2017; Lomanowska and Melo, 2016; Lonstein et al., 2015).

Hormonal Effects on the Onset of Maternal Behaviors Although early endocrine studies (Beach and Wilson, 1963; Lott and Fuchs, 1962; Riddle, Lahr, and Bates, 1935) did not provide conclusive evidence for endocrine involvement in the regulation of maternal behavior, those studies provided an approach to the analysis of the hormonal control of behavior, using extirpation and replacement strategies. There is now substantial evidence that the hormones associated with late pregnancy and the parturitional period acting on brain receptors (Bridges, 2016b) account for the rapid activation of maternal responsiveness seen at parturition (Terkel and Rosenblatt, 1972). These include the steroid hormones, estradiol and progesterone, which are synthesized by the ovaries and released into the circulatory system and the protein hormones, vasopressin, prolactin, and oxytocin, which are released within the brain and from cells or nerve terminals within the “master” endocrine organ, the pituitary gland (Beery, McEwen, MacIsaac, Francis, and Kobor, 2016b; Bridges, 1990; Bridges, 2016a; Feldman, 2016; Insel, 1990; Numan, 1994; Numan and Young, 2016; Olazábal and Alsina-Llanes, 2016; Rosenblatt, 1990; Rosenblatt and Snowdon, 1996; Stolzenberg and Champagne, 2016a). Other important neurotransmitters in regulation of mothering include dopamine, norepinephrine, serotonin, GABA, and endorphins (Afonso, King, Novakov, Burton, and Fleming, 2011; Afonso, Grella, Chatterjee, and Fleming, 2008; Afonso, King, Chatterjee, and Fleming, 2009; Afonso et al., 2013; Blass, 1996; Chen et al., 2014; Gao, Wu, Davis, and Li, submitted; Hansen, Bergvall, and Nyiredi, 1993; Kendrick, Keverne, Chapman, and Baldwin, 1988; Keverne, 1988; Numan and Young, 2016; Smith, Piasecki, Weera, Olszewicz, and Lonstein, 2013; Wu, Gao, Chou, Davis, and Li, 2016). These hormones and neurochemicals serve multiple functions. They prepare the prospective mother physiologically, by acting on mammary tissue prior to the initiation of lactation (Tucker, 1994) and by acting on the uteri, first to maintain the integrity of the implanted conceptus, and then to promote uterine contractions and parturition as well as analgesia during the birth process (Hodgen and Itskovitz, 1988; Kristal et al., 1986). These hormones also contribute to elevated maternal responsiveness and reduced anxiety shown by the newly parturient mother (Bridges, 1990; Ferreira, Pereira, Agrati, Uriarte, and Fernandez-Guasti, 2002; Insel, 1990; Lonstein, 2007a; Pereira and Ferreira, 2016; Rosenblatt, 1990). A regimen of hormones designed to simulate these pregnancy and parturitional changes administered to maternally inexperienced virgins can induce a very rapid onset of retrieval, crouching, and licking in response to foster pups (Bridges, 1990; Insel, 1990; Rosenblatt, 1990). Although the “parturitional” hormones might seem to activate maternal behavior in a unitary fashion, in fact the different hormones and neurochemicals probably exert somewhat different behavioral effects, and any one hormone or neurochemical probably exerts multiple effects. Moreover, their varied effects probably result from their action on a variety of different neural pathways. 34

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Figure 2.1 Functional neuroanatomy mediating maternal and related psychological processes in mammals. Neuroanatomical structures include olfactory bulbs, amygdala, nucleus accumbens, bed nucleus of stria terminalis (BNST), medial preoptic area (MPOA), ventromedial hypothalamus (VMH), anterior hypothalamic nucleus (AHN), ventral pallidum (VP), prefrontal cortex (PFC), ventral tegmental area (VTA), doral and median raphe (DR and MR), and parietal cortex. Relevant neurochemistry include catecholamines, serotonin (5-HT), dopamine (DA), the neuropeptides, and opioids. Source: Adapted from Fleming, O’Day, and Kraemer (1999).

For instance, the hormones progesterone and estradiol might facilitate the expression of maternal behavior by altering a number of behavioral propensities, and these alterations provide the behavioral environment in which maternal responses can be most easily expressed (Fleming, 1987; Fleming and Corter, 1988). Specifically, as schematized in Figure 2.1, these hormones promote changes in the female’s attraction to the odors of pups, reduce her fearfulness in their presence, and facilitate the ease with which she learns about their characteristics, possibly by augmenting the pups’ reinforcing value. Together, these hormonal effects are seen to indirectly augment maternal responsiveness during the periparturitional period by reducing the competing effects of alternative nonmaternal behaviors and by insuring that dams will continue to respond to pups when the period of hormonal priming ends (Fleming et al., 2016; Lonstein et al., 2015). Thus, as shown in the following discussion, postpartum animals differ from virgins on a number of psychological dimensions because of the action of hormones.

Emotional and Anxiety Changes in the New Mother Naturally parturient females are less avoidant when presented with pups than are virgin animals. More generally, they are less neophobic, being more willing to approach an unfamiliar intruder and to enter and explore a novel environment (Fleming and Luebke, 1981a; Lonstein, 2007a; Lonstein et al., 2015; Pawluski, Lonstein, and Fleming, 2017). In postpartum laboratory rats, these emotional changes can be found using many paradigms within 24 hours after parturition, last for about one week, and require recent physical contact with the litter although suckling per se is unnecessary (Lonstein, 2005, 2007; Ragan and Lonstein, 2014). In fact, some reduction in neophobia, fear, and anxiety even accompanies the maternal state in 35

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sensitized nulliparous female rats (Agrati, Zuluaga, Fernandez-Guasti, Meikle, and Ferreira, 2008 Ferreira et al., 2002 Pereira, Uriarte, Agrati, Zuluaga, and Ferreira, 2005). However, the relation between anxiety and mothering is not linear. It has also been suggested that in genetically “unselected” animals, a moderate level of anxiety that is neither too high (rendering dams over-reactive to threat) nor too low (rendering them naively under-reactive) is optimal for maternal ability to focus attention on the needs of the pups despite threats in the environment (Ragan and Lonstein, 2014). Anxiety effects also depend on the context. Studies of the relation between natural variation in anxiety and mothering in laboratory rodents find no significant relation when tested under relatively benign conditions (Curley, Jensen, Franks, and Champagne, 2012), but mother rats genetically selected for high anxiety are more effective mothers under challenging conditions compared to low-anxiety dams (Neumann, Krömer, and Bosch, 2005). Thus, maternal anxiety state becomes most influential for rats in risky environments that could disrupt maternal motivation to remain with the pups and provide them care. However the relation is complex, as work by Bosch (2011) shows that high-anxiety mother rats spend more time in the nest, retrieve pups faster, and show enhanced maternal aggression in comparison to low-anxiety rats. This seems to suggest that under some circumstances elevated anxiety is positively correlated with enhanced maternal performance (Bosch, 2011). These emotionality differences between postpartum and virgin females appear to be hormonally and/or neurochemically mediated (Agrati and Lonstein, 2016a; Fleming, 1986; Fleming et al., 1989a; Lonstein, 2005; Lonstein, 2007b; Pereira and Ferreira, 2016). The regimen of progesterone and estradiol that facilitates the onset of maternal behavior in the virgin rat also reduces pup-avoidance and measures of timidity in an open-field apparatus (Fleming, Cheung, Myhal, and Kessler, 1989b). At a brain level, the postpartum reduction in postpartum anxiety is likely maintained by neurochemicals released in the brain when mothers physically interact with the litter; removing the ovaries, or adrenal or pituitary glands, does not affect the anxiety-related behavior of postpartum rats, whereas preventing the physical contact with pups before testing results in increases the dams’ anxiety-like behaviors (Agrati and Lonstein, 2016b). Among the neuropeptides implicated in postpartum anxiety are vasopressin, oxytocin, and GABA (Lonstein et al., 2015; Pawluski et al., 2017). Moreover, lactating animals show marked hyporesponsiveness of the stress system and differences between virgin and lactating females in their hypothalamic-pituitary-adrenal responses to stressors; in comparison to mothers, virgins show enhanced stressor-induced release of hypothalamic-pituitaryadrenal (HPA) related hormones (corticosterone, adrenocorticotropic hormone [ACTH]), as well as enhanced baseline corticotrophin-releasing factor (CRF) in the paraventricular nucleus (PVN) region of the hypothalamus (Neumann et al., 1998; Windle et al., 1997). These HPA differences are associated with differences on a variety of emotionality tasks (Hard and Hansen, 1985; Neumann, 2001; Neumann, 2003; Neumann et al., 1998; Neumann, Torner, and Wigger, 2000; Silva, Bernardi, Nasello, and Felicio, 1997b). Finally, the assumption that reduced timidity contributes to elevated maternal responsiveness is supported by findings that manipulations that reduce the animals’ timidity or anxiety, like benzodiazepines (Hansen, Ferreira, and Selart, 1985) or early handling (Mayer, 1983), also facilitate maternal responding. Panesar and Fleming (Panesar, Rees, and Fleming, 2000) found that high concentrations of glucocorticoids injected into an adrenalectomized virgin animal inhibits the expression of many components of pup-induced maternal behavior, whereas the same high concentration facilitates maternal behavior in the postpartum animal.

Sensory Changes in the New Mother In addition to their effects on dams’ affective state, parturitional hormones also alter their responsiveness to pup-related cues. In the following discussion we first describe hormonal effects on olfactorymediated responses and then on their somatosensory processing. 36

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Odor Cues The study of the sensory control of maternal behavior was pioneered by Beach and Jaynes in 1956; it involved observing maternal behavior in experienced mother rats after the systematic removal of the different sensory systems, either singly or in combination (Beach and Jaynes, 1956a, 1956b). This early study suggested that no single sensory system is essential for the expression of the behavior but that their combined removal produces additive deficits, leading Beach and Jaynes to conclude that maternal behavior is under multisensory control. Although these results seem to apply quite well to animals that have had maternal experience, we now know that single denervations of a number of sensory systems can have profound effects on the expression of maternal behavior in the maternally inexperienced animal (Fleming and Rosenblatt, 1974a; Stern, 1989) and that specific sensory cues from the pups play important roles both in motivating responsiveness and in guiding ongoing behavior. In comparison to virgins, new mothers without direct experience with pups prefer nest material taken from the nest of a new mother and her pups to material taken from a virgin’s nest or clean material. Virgins show no such preference (Bauer, 1983; Fleming et al., 1989b). Moreover, virgins treated with a regimen of hormones designed to mimic the parturitional changes in progesterone and estradiol also exhibit a preference for pup-related odors (Fleming et al., 1989b); the additional observation that injections of morphine can induce an aversion to pup odors (Bridges, 1990; Kinsley and Bridges, 1988; Kinsley, Morse, Zoumas, Corl, and Billack, 1995) suggests that, at the time of parturition, low concentrations of this neurochemical in relevant parts of the brain heightens attraction to pup-related odors. Experience with these odors can facilitate maternal responding; adult virgin rats show more rapid maternal inductions if they have been preexposed to pup odors and vocalizations during their early development (Gray and Chesley, 1984; Moretto, Paclik, and Fleming, 1986). Although difficult to demonstrate, it seems that preexposure to pup cues at a distance (primarily odors and vocalizations) in adulthood also facilitates maternal responding, at least among females whose responsiveness is high to begin with. Thus, a higher proportion of animals exhibits immediate maternal behavior during maternal tests if they have been preexposed to pup odors than if they have not been (Orpen and Fleming, 1987). Finally, if virgins are rendered unable to smell pups by olfactory bulb removal, which mediates the sense of smell, they are not avoidant with pups, but instead exhibit a very rapid onset of maternal behavior, as though the pups’ odors in the context of other pup cues are aversive (Fleming and Rosenblatt, 1974b, 1974c; Fleming, Vaccarino, Tambosso, and Chee, 1979). New mothers develop an attraction to pup-related odors and are guided by them. However, in rats neither the main (airborne) nor the accessory (where activating molecules are transmitted normally by means of an aqueous medium) olfactory systems are essential for mothering behavior to be expressed. Following destruction of the olfactory mucosa, a normal latency to onset of maternal behavior occurs in primiparous females (Benuck and Rowe, 1975; Jirik-Babb, Manaker, Tucker, and Hofer, 1984; Kolunie and Stern, 1995), even though retrieval may be delayed because dams who cannot detect odors (anosmic) take longer to locate pups at a distance (Benuck and Rowe, 1975; Kolunie and Stern, 1995). Similarly, no deficit in maternal behavior is observed after removing the vomeronasal organ (VNO) or cutting the vomeronasal nerves, which eliminate input from the accessory olfactory system (Fleming, Gavarth, and Sarker, 1992; Jirik-Babb et al., 1984; Kolunie and Stern, 1995). Latency to retrieve is unaffected in these VNO-operated females, suggesting that the accessory olfactory system is not critical for even locating pups. Inconsistent results on maternal behaviors have been reported using bilateral removal of the olfactory bulbs (bulbectomy) which eliminates both main and accessory olfactory input. These effects range from profound disturbances and/or cannibalism (Benuck and Rowe, 1975; Fleming and Rosenblatt, 1974b; Kolunie and Stern, 1995; Schwartz and Rowe, 1976) to no reported deficits at all (Beach and Jaynes, 1956b; Fleming, Kuchera, 37

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Lee, and Winocur, 1994); however, peripherally induced anosmia by zinc sulfate reduces licking by new mother rats (Fleming and Rosenblatt, 1974c). In contrast to rats, mice mothers depend on olfaction for the regulation of their maternal behavior. In the laboratory mouse, removal of the olfactory bulb (olfactory bulbectomy) prevents nest building, reduces nursing, and induces cannibalism (Gandelman, Zarrow, and Denenberg, 1971; Gandelman, Zarrow, Denenberg, and Myers, 1971; Sato, Nakagawasai, Tan-No, Onogi, Niijima, and Tadano, 2010b; Vandenbergh, 1973). Moreover, the deletion of genes involved in olfactory signal transduction (SCN9A or Cnga2) in the main olfactory epithelium results in deficits in pup retrieval (Fraser and Shah, 2014; Weiss et al., 2011). However, removing accessory olfactory functioning or deleting Trpc2 (gene coding for ion channels in the vomeronasal organ) does not interfere with the expression of maternal behavior in mice (Fraser and Shah, 2014; Lepri, Wysocki, and Vandenbergh, 1985). The importance of main olfactory cues for mouse mothering is diminished in experienced mothers, who can apparently compensate for a loss of olfactory function by using other sensory information (Dickinson and Keverne, 1988; Seegal and Denenberg, 1974). In contrast to rats also, maternally discriminating species, like some ungulates that recognize their young and allow them to suckle while rejecting others, olfaction is key (Lévy et al., 1995; Pitcher, Harcourt, and Charrier, 2010; Romeyer et al., 1993). Inducing anosmia in sheep mothers (ewes) before parturition prevents recognition of their own lambs and so any young is accepted to suckle (Baldwin and Shillito, 1974; Bouissou, 1968; Lévy et al., 1995; Poindron, 1976; Romeyer, Poindron, and Orgeur, 1994). In this case, the main, but not the accessory olfactory system is involved (Lévy et al., 1995). Primiparous ewes rendered anosmic before parturition show reduced maternal behavior. By contrast, females with lesions of the accessory olfactory system show little disturbance in maternal care (Lévy et al., 1995). The olfactory cues that attract ewes to any newborn lamb are linked to amniotic fluid. Removing amniotic fluid from the neonate’s coat reduces maternal licking and, in primiparous ewes, prevents acceptance behavior while increasing aggression (Lévy and Poindron, 1987). In experienced mothers, coating lambs in amniotic fluid alone is sufficient to induce maternal acceptance (Basiouni and Gonyou, 1988; Lévy and Poindron, 1984). Thus, olfactory cues provided by amniotic fluid ensure appropriate maternal behavior at parturition in sheep, especially in inexperienced mothers (Corona and Lévy, 2015).

Olfactory Cues Have Inhibitory Effects In contrast to postpartum rats, in virgin rats the induction of anosmia disinhibits the expression of maternal behavior. That is, olfactory cues associated with birth and pups prevent nulliparous female rats from being maternal. Virgin or nonpregnant female rats are simply repelled by placenta, amniotic fluid, and pup odor (Kristal, 1980), but anosmia eliminates these aversive properties and a rapid onset of maternal behavior results (Carretero, Segovia, Gomez, and Del Cerro, 2003; Fleming and Rosenblatt, 1974b; Fleming et al., 1979). These inhibitory effects seem to be mediated by both the main and accessory systems and in a number of different species (rat: Fleming et al., 1979; rabbit: González-Mariscal, Chirino, Beyer, and Rosenblatt, 2004; Chirino, Beyer, and González-Mariscal, 2007; hamsters: Marques, 1979), although of course this not the case in many strains of mice, which may require olfaction for dam maternal behavior. In rats, we have no idea which specific pup or pup-related odors influence the dam’s attraction to pups, although evidence suggests that pup anogenital licking by the mother is facilitated by secretions from the pup preputial glands (glands around the anal region; Brouette-Lahlou, Vernet-Maury, and Chanel, 1991). Moreover, the relevant component in the secretion seems to be a pheromone-like compound called dodecyl propionate (Brouette-Lahlou, Amouroux, et al., 1991). It appears likely that, because rats do not become attached to individual offspring or even individual litters—although they respond differentially to pups based on sex (Cavigelli, Ragan, Barrett, and Michael, 2010; Moore 38

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and Morelli, 1979)—the odor of individual pups or litters is less relevant than is the odor that characterizes the developmental age of the pups and/or the mother’s postpartum stage. These odors could derive from many sources in addition to preputial glands, including uterine fluids, mother’s milk, maternal diet, and maternal excretory products. Mother rats will consistently lick some pups over others in a litter; however, whether actual “attachment” occurs and/or the reasons for this differential behavior is unknown (Beery, McEwen, MacIsaac, Francis, and Kobor, 2016a; Pan, Fleming, Lawson, Jenkins, and McGowan, 2014; Ragan, Harding, and Lonstein, 2016a). In mice, for instance, Doane and Porter (1978) found that dams could discriminate pups being nursed by females fed the same diet as themselves from those nursed by mothers fed a different diet. The existence of nest-specific odors is also suggested by the work of Bauer (1983), Kinsley and Bridges (1988), Kinsley (1990), and Leon (1978). In sheep, there is considerable evidence that at parturition the ewe develops an attraction to amniotic fluids, which had been aversive prior to birth, and this attraction begins to fade by 2 hours postpartum (Lévy, Poindron, and Le Neindre, 1983; Poindron and Lévy, 1990). This attraction is apparently induced by the synergistic action of prepartum estrogen, genital stimulation, and oxytocin release associated with the parturition (Poindron and Lévy, 1990) and functions to enhance the ewe’s maternal licking and grooming and willingness to accept the neonatal lamb (Lévy and Poindron, 1984, 1987). Finally, olfactory input clearly constitutes the initial basis of the ewe’s selective bond with her lamb. As indicated above, ewes that are unable to smell their lambs exhibit enhanced maternal behavior to all lambs and do not develop a selective bond with any one lamb (Corona and Lévy, 2015; Keller, Meurisse, and Lévy, 2004).

Touch Cues Hormones exert their effects on multiple sensory systems. We now discuss effects on somatosensory function. Rat mothering involves physical interactions with pups which activate the mothers’ somatosensory systems. When mothers mouthe, lick, and retrieve pups they receive tactile input to the very sensitive mouth (perioral) region. Work by Kenyon, Cronin, and Keeble (1983) and by Stern (Stern, 1990; Stern and Johnson, 1989; Stern and Kolunie, 1989) indicates that this stimulation of the mouth region is essential to the complete expression of maternal behavior during the early postpartum period. Stern and her colleagues (Stern and Johnson, 1989; Stern and Kolunie, 1989) found that, if the mouth region is desensitized through use of a muzzle, anesthesia injected into the cheek region, or transection of the nerves in this region, mother rats will not exhibit normal crouching behavior. If anesthetized and transected, they also do not retrieve or lick pups. In fact, tactile stimulation of the mouth area seems to be necessary for activation of the pronounced nursing posture (ventroflexion) necessary for successful suckling by young (Stern, 1990, 1996). Given the clear importance of tactile sensation of the mouth and cheek regions, it is interesting that estradiol also enlarges the area of responsiveness of this facial area (Bereiter and Barker, 1975, 1980; Bereiter, Stanford, and Barker, 1980), presumably heightening maternal sensitivity to pup-generated touch cues. The ventral trunk region with its teats is obviously another important contributor to somatostimulation. When dams crouch over and nurse pups, they receive tactile input through touch receptors in the ventral skin surface and teat stimulation by suckling pups. The importance of suckling stimulation for the release of prolactin, glucocorticoids, and oxytocin (the hormones of lactation) and activation of the milk-ejection or “letdown” reflex is well known (Wakerly, Clarke, and Sumerlee, 1988). However, the fact that thelectomized females (with teats removed), or females whose individual teats have been anesthetized, engage in motivated maternal behavior suggests that teat stimulation by suckling young is not necessary for the retrieval, licking, or hovering over pups, although teat stimulation is clearly necessary for the occurrence of the high crouch involved in nursing behavior (Stern et al., 1992; Stern, Dix, Pointek, and Thramann, 1990). Similarly, insufficient ventral stimulation due 39

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to the presence of too few pups, chilled pups, or pups prevented from suckling fails to elicit the high arch crouch in dams (Stern and Johnson, 1989). Although teat stimulation may not be necessary for the expression of most maternal behaviors, the ventral surface surrounding the nipples may be. If a dam is given a local anaesthetic that desensitizes the ventrum (Stern and Johnson, 1989) or wears a specially devised spandex jacket covering the ventrum (Morgan, Fleming, and Stern, 1992), pups do not gather under the mother’s ventrum and attach to the teats but instead gravitate to her exposed neck region, where the fur presumably has the right tactile, temperature, and odor characteristics (Magnusson and Fleming, 1995; Morgan et al., 1992). Under these conditions, licking and a variety of other maternal behaviors are considerably distorted. Although such systematic experiments have not been performed in other mammals, studies in sheep indicate that preventing nursing but not licking, by placing the newborn lamb in a wire mesh cage with its lid open for either 4 or 12 hours, has little consequence on maternal behavior even in primiparae (Otal et al., 2009; Poindron and Le Neindre, 1980). Moreover, there is no indication that preventing only nursing impairs the recognition of one’s own lamb in primiparous or multiparous mothers (Otal et al., 2009). By contrast, deprivation of all physical contact with the newborn lamb has a drastic impact on the development of maternal responsiveness and selectivity in both sheep (Otal et al., 2009) and goats (Bordi et al., 1994; Romeyer et al., 1993). Whether these effects are caused by the lack of perioral stimulation, or by the absence of ingesting amniotic fluids and the impairment of some perception of olfactory cues from the young, is unknown. The latter possibility is likely, given the important role of olfaction in maternal behavior of these ungulates.

Auditory and Visual Cues Although somatosensory (touch), thermal (temperature), and olfactory (odor) cues are probably most important for the regulation of maternal behavior, other cues may also contribute to the proximal control of behavior and may be influenced by hormones. For instance, ultrasonic calls, above the range of human hearing, emitted by pups when they are in distress, cold, or out of the nest result in the mother’s locating them from a distance and retrieving them back into the nest (Allin and Banks, 1972; Brewster and Leon, 1980); such directional orientation to pup ultrasounds is facilitated by associated pup odor cues (Farrell and Alberts, 2002; Smotherman, Bell, Starzec, Elias, and Zachman, 1974). In fact, Brouette-Lahlou, Godinot, and Vernet-Maury (1999) reported that pup ultrasounds stimulate the initiation of maternal anogenital licking of pups, which is then facilitated or patterned by pup preputial secretions acting on the maternal vomeronasal system (Brouette-Lahlou et al., 1999; Brouette-Lahlou, Vernet-Maury, Godinot, and Chanel, 1992). That ultrasonic calls may acquire motivational properties is suggested by the observation that virgin animals do not awaken in response to these calls, whereas postpartum mothers do. The brain neuropeptide oxytocin plays an important role in the mediation of pup retrieval behavior in female mice acting by enhancing auditory cortical pup ultrasonic distress calls (Marlin, Mitre, D’Amour, Chao, and Froemke, 2015). They found that pup retrieval behavior was accelerated by oxytocin in the left auditory cortex, and oxytocin receptors were preferentially expressed in the left auditory cortex. Visual cues may also contribute to maternal responsiveness, although their role must be restricted to proximal interactions and distances over which the dam can see (newborn pups are more effective at eliciting retrieval in the newly parturient dam than are older pups; Peters and Kristal, 1983; Stern, 1985). That said, neither sight nor hearing is necessary for the expression of maternal behavior. In the absence of both, maternally experienced dams show normal interactions with pups (Beach and Jaynes, 1956a, 1956b; Herrenkohl and Rosenberg, 1972). Taken together, hormones reduce pup-avoidance, augment the dam’s attraction to pup-related odorants and ultrasonic vocalizations, and sensitize the mother to tactile cues that promote a rapid onset of maternal behavior at parturition. 40

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Experiential Effects on the Maintenance and Retention of Maternal Behaviors Processes regulating the long-term maintenance of maternal behavior differ from those involved in its onset. The female first undergoes a transition period during which hormones interact with environmental and experiential processes in the regulation of behavior. However, once this transition period is over, by the end of the first postpartum week, behavior is maintained primarily by sensory influences and processes of learning and reinforcement. Hormonal effects on maternal behavior at this time are minimal (Lonstein et al., 2015).

Behavioral Changes From Birth to Weaning Mothers respond to their offspring for a considerable period after parturition, although the quality of responsiveness changes as the young grow and mature. In general, young are weaned at about 20 to 25 days, and although mothers continue nursing young over this period, nursing bouts become shorter, inter-bout intervals become longer, and dams spend increasing time away from their young (Leon, Croskerry, and Smith, 1978). In fact, once the young are mobile, by 12 to 15 days of age, the mother increasingly distances herself from the pups; she rarely retrieves them, her nest becomes matted, and she terminates nursing bouts before the infants have had their fill (Fleming and Blass, 1994). By 15 to 20 days of age, pups begin to supplement their diet with solid food, which they first encounter in the mother’s milk, then as particles of food in the mother’s saliva or on the mothers body (mouth, head, and fur), and then when they follow their mother to the food source (Alberts and Cramer, 1988; Galef, 1989; Galef and Beck, 1990). At a more proximal level, after the first few postpartum days, mothers and litter develop a rhythm of interaction in which the dam alternates between being in the nest and nursing the young and leaving the nest, out of litter contact. Leon and his colleagues (Leon et al., 1990) showed that the duration of the long nursing nest bouts is regulated by an interaction of hormonal factors and the thermal characteristics of the nest, the huddle of pups, and the mother. Dams experience a rise in body temperature when nursing and get off the pups when they experience acute hyperthermia (Leon et al., 1978). In comparison to nonlactating animals, dams have a chronically elevated core temperature, making them more vulnerable to hyperthermia ( Jans and Leon, 1983a, 1983b). Moreover, endocrine changes associated with suckling and lactation contribute to the elevated core body temperature. The developing pups induce their mothers to release both prolactin and ACTH, which provoke the release of progesterone and corticosterone, respectively. Progesterone then elevates the maternal thermal set point, and corticosterone increases maternal heat production and possibly heat retention. The resulting chronic increase in maternal heat load makes mothers vulnerable to a further acute increase in their heat load, eventually driving up maternal brain temperature and forcing the interruption of pup contact (Leon et al., 1990). Although many hormones are associated with lactation, the primary ones are the peptides, prolactin, adrenocortical hormone, and oxytocin as well as adrenal steroids but not the “parturitional” hormones known to be associated with the onset of responsiveness. Although both prolactin and oxytocin have been implicated in the onset of maternal responsiveness (Bridges, 1990; Insel, 1990), there is no evidence that these “lactational” hormones contribute directly to the dam’s motivation to continue to respond nurturantly during the lactational period or are directly involved in the longterm effects of experience seen in differences between first time mothers and multiparous mothers.

Parity and Effects of Postpartum Experiences The importance of postpartum experience is reflected both in the short term, during the first postpartum week, and in the long-term maintenance of behavior of the primiparous female and across 41

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subsequent births. The latter, expressed as the parity effect, is extensively and thoroughly described by Bridges (2016b) who describes the multiple behavioral and physiological differences between primiparous and multiparous mothers. Bridges (2016b) reported for instance that in the rat with a regular estrous cycle, levels of prolactin, estrogen, and corticosterone are lower in multiparous than in primiparous females and some of these differences persist also as a function of prior parity in the pregnant animal (Bridges, 2016b). Hence, with experience, lower levels of hormones are necessary to produce the same effects; that is, multiparous animals are more sensitive to the effects on brain and/or behavior of hormones than are primiparous animals. Consistent with this idea, multiparous animals are more responsive to pup stimulation than primiparous animals in terms of their dopamine release into the nucleus accumbens (NA) with presentation of pups (Afonso et al., 2008). Parity-induced differences in the sensitivity of receptor activation have also been reported—some consistent with the idea that multiparous mothers are more sensitive, and some counter to this conceptualization (Bridges, 2016b). In terms of the nature of the relevant experience associated with parity effects, considerable work has focused on the initial few postpartum days when new mothers first encounter their young and interact with them. This interaction is laid down in memory and becomes rapidly consolidated (Bridges, 2016b; Lonstein et al., 2015). Once animals initiate responsiveness to young at parturition, whether as first time mothers or multiparous mothers, the continued expression of maternal behavior after 4 to 5 days post-parturition seems no longer to be based on hormones but is, instead, based both on experiences acquired by the mother when she interacts with pups under the influence of hormones and on experiences acquired during the lactational period (Bridges, 2016b; Fleming, Morgan, and Walsh, 1996). Thus, processes of learning and memory sustain the behavior beyond the period of hormonal priming and into the next parity (Li and Fleming, 2003a). If pups are removed from newly parturient (or cesearan-delivered) females before dams have had the opportunity to interact with the pups, maternal responsiveness declines over the next 3 to 5 days and reaches low virgin levels by day 10, by which time animals have usually reinitiated their estrous cycles (Orpen, Furman, Wong, and Fleming, 1987). However, if females give birth (or are C-sectioned) and within 24 to 36 hours are permitted to interact with pups for as little as a half hour before separation, dams continue to be maternal in tests undertaken 10 days later (Orpen and Fleming, 1987). Not surprisingly, a longer interactive exposure period results in a longer retention of responsiveness (Bridges, 1975, 1977; Cohen and Bridges, 1981; Fleming and Sarker, 1990). This long-term change in behavior as a result of experience interacting with pups has come to be known as the “maternal experience effect” or “maternal memory” and has now been demonstrated in other species (e.g., rabbit; González-Mariscal et al., 1998). Parturitional hormones influence the robustness of maternal learning and memory. Animals which acquire maternal experience under the influence of the parturitional hormones (whether postpartum animals or virgins treated with hormones) exhibit better retention of maternal behavior 30 days later than do animals who are not being stimulated with hormones at the time of the maternal experience (virgins or nonparous but experienced animals). Moreover, the optimal condition for the expression of maternal behavior occurs when both the initial experience and the test occur during a period of hormonal priming (Fleming and Sarker, 1990). There is considerable evidence that multiparous animals (which have experienced a previous pregnancy, parturition, and period of pup-rearing) are less disturbed than primiparous mothers by a variety of experimental manipulations including C-section (Moltz, Robbins, and Parks, 1966), endocrine manipulations (Moltz, Levin, and Leon, 1969; Moltz and Wiener, 1966), morphine administration (Bridges, 1990; Kinsley and Bridges, 1988), and brain lesions (Fleming and Rosenblatt, 1974b; Franz, Leo, Steuer, and Kristal, 1986; Numan, 1994; Schlein, Zarrow, Cohen, Denenberg, and Johnson, 1972) that could disrupt maternal behavior. In addition, pup cues, which are initially ineffective in eliciting maternal behavior 42

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in first-time mothers, come to be effective in multiparous animals (Noirot, 1972). Finally, among ewes, exogenous hormones are most effective in enhancing responsiveness in experienced animals (Poindron and Le Neindre, 1980). Although most work in this area has focused on mother’s learning about her offspring, this enhanced learning ability seems not to be specific to the maternal context; in comparison to virgins or nonmothers, new mothers during the postpartum period also show enhanced learning in other contexts, involving other forms of social learning (Fleming, Kuchera, et al., 1994), as well as spatial learning and hunting (Bodensteiner, Cain, Ray, and Hamula, 2006; Gatewood et al., 2005; Kinsley et al., 2014; Kinsley and Lambert, 2008; Kinsley et al., 1999; Lemaire et al., 2006; Love et al., 2005; Pawluski, Vanderbyl, Ragan, and Galea, 2006; Pawluski, Walker, and Galea, 2006; for opposite results see Bodensteiner et al., 2006; Darnaudéry et al., 2007). Early postpartum learning also occurs in sheep, and this learning maintains their maternal responsiveness beyond the peri-parturitional period (Lévy and Keller, 2008). However, maternal responsiveness fades rapidly. A 36- to 72-hour separation period that follows 4 hours of contact after parturition induces rejection of the familiar lamb (Keller, Meurisse, and Lévy, 2005; Lévy et al., 1991). This decline in maternal responsiveness cannot be compensated for by increasing initial motheryoung because the rejection is also observed when the separation is performed after a week of postpartum interaction (Keller et al., 2005). Maternal selectivity can, however, be strengthened over time. Although selective mothers exposed to the lamb for 4 hours just after birth are not able to retain selectivity after 24 or 36 hours of separation, memory of the lamb is maintained if ewes and their lambs have been in contact a week (Keller et al., 2005; Lévy et al., 1991). Hence, offspring recognition memory is labile and has a short duration during the initial postpartum period, whereas maternal selectivity strengthens over time, suggesting the involvement of consolidation processes for emergence of the latter. Taken together, these studies indicate that experiences acquired under hormones are also more easily activated by a combination of hormones and exposure to relevant pup stimuli in the absence of hormones. There are a number of ways hormones could act to promote these robust experience effects. They could increase the salience of associative cues, most likely unconditioned pup cues (e.g., proximal tactile or olfactory) during the learning phase; they could act to facilitate or strengthen the association between the conditioned and unconditioned pup-associated cues; finally, they could produce internal cues that themselves act as conditioned stimuli, a mechanism that could explain the apparent state dependency of the maternal-hormone interactions described above. Research has not yet identified which of these hormone mechanisms are most important.

Sensory Mechanisms Involved in Maternal Experience Although it is clear that interactive experience is important for the long-term retention of behavior, which aspect of the experience is important is not known. In this section, we consider different sensory experiences the animal acquires while interacting with pups. As will become apparent, both somatosensory and chemosensory inputs are important for the long-term retention of maternal behavior. During early interactions with pups, the dam is multiply stimulated by distal visual and auditory cues and by more proximal tactual, chemosensory and, possibly, thermal cues, and these may well be important aspects of the maternal experience (Stern, 1989). The significance of somatosensory and chemosensory stimulation for the maintenance of maternal responding is well established; if the mother is prevented from crouching over her young during the postpartum period, but receives other distal inputs, her responsiveness declines more rapidly with earlier weaning ( Jakubowski and Terkel, 1986; Stern, 1983). Moreover, Orpen and Fleming (1987) found that, if mothers were separated from their litters by a wire mesh floor during the 1-hour postpartum exposure phase, so that they could see, hear, 43

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and distally smell pups, but received no tactile or proximal chemosensory input, on tests 10 days later they showed no long-term benefit of maternal experience, but instead responded to pups as virgins do. These data indicate that ventral stimulation is probably an essential feature of the maternal experience. The additional findings that dams need to receive somatosensory perioral input from the mouth region to exhibit normal maternal licking and crouching (Stern and Johnson, 1989; Stern and Kolunie, 1989), and that licking during exposure is correlated with responsiveness during test (Morgan et al., 1992), point also to the importance of chemosensory and somatosensory stimulation for the maternal experience effect (Morgan et al., 1992). However, olfactory learning in this context is clearly paramount. During interactions with pups, dams learn about specific olfactory and chemosensory features of the pups. If pups are scented with an artificial odorant during the exposure phase, on test 10 days later dams respond more rapidly to pups labeled with the same scent than to those labeled with a discrepant scent. That this effect depends on the association of the odors with the pups is shown by the additional observation that preexposure to the odor on its own (in the absence of pups) does not result in the same facilitation of responsiveness to similarly scented pups (Malenfant, Barry, and Fleming, 1991). Moreover, how dams respond to pup-associated scents depends on the quality of their interactions with pups during the initial pup-odor pairings. If mothers interact proximally with pups during the pairing, and spend time sniffing and licking them, they develop a strong long-term preference for that scent over a novel scent; however, if during the pairing mothers do not respond maternally, and remain at a distance from pups, then the dams do not develop a preference for the paired scent (Fleming, unpublished observation). Although pup-associated scents can be learned, olfactory input is apparently not necessary for a maternal experience. Olfactory and accessory olfactory denervations prior to an experience does not block the long-term influence of pup-associated odors (Fleming et al., 1992; Mayer and Rosenblatt, 1977).

Long-Term Effects of Maternal Experience and Parity on Maternal Affect Parity differences in anxiety. Postpartum and virgin animals differ in the number of respects, one difference is in the effects of a maternal experience on anxiety levels. Postpartum rats are often less anxious than virgin females, as indicated by group differences in the elevated plus maze test (Lonstein, 2007a; Silva, Bernardi, Nasello, and Felicio, 1997a), the open field test, and light-dark box test (Fleming et al., 1989a; Miller, Piasecki, and Lonstein, 2011). This reduced anxiety in dams persists well into later adulthood (Bridges, 2016a; Byrnes and Bridges, 2006), as nonlactating primiparous rats exhibit reduced anxiety levels on the elevated plus maze and open field test than their age-matched nulliparous controls tested during the proestrus phase. Estrogens, possible estrogen receptor alpha (ERα), may play a role in this parity-induced shift in anxiety (Byrnes, Casey, and Bridges, 2012). Treatment of nonlactating, primiparous females with an Erα agonist increased time spent in the open arms (Agrati and Lonstein, 2016b), and altered the “stress” peptide, corticotropin releasing hormone (CRH) mRNA expression in both hypothalamus and amygdala in a parity-dependent fashion. These findings indicate that reproductive experience can alter the Erα-mediated limbic systems that mediate emotional responses. Parity differences in pup reinforcement. Despite these parity differences in general olfactory learning and emotion regulation, the primary reason the postpartum animal expresses such a robust maternal experience is because rat pups are highly reinforcing for the maternal animal (Fleming, Korsmit, and Deller, 1994a; Wansaw, Pereira, and Morrell, 2008). In a series of studies addressing this issue, Fleming and colleagues (Fleming, Korsmit, et al., 1994; Lee, Clancy, and Fleming, 2000) compared postpartum and virgin animals under a variety of different temporal, hormonal, experiential, deprivation, and stimulus conditions on a conditioned place preference (CPP) paradigm or in an operant box using either rat pups or food as the reinforcing stimulus. CPP tests showed that dams spend more time in the pup-associated side of the CPP apparatus than the food associated side, whereas 44

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virgins spend more time in the food associated side than the pup-associated side. Hence, pups are more reinforcing than food to postpartum animals, whereas food is more reinforcing than pups to the virgins. Subsequent work by Morrell and her colleagues shows that dams in early (days 4–8) postpartum period find pups more reinforcing than those in late (days 12–16) postpartum (Wansaw et al., 2008), and young pups are even more reinforcing than cocaine for early postpartum females (Mattson, Williams, Rosenblatt, and Morrell, 2001). When virgins are induced to become maternal as a result of extensive experience with pups, pups take on heightened reinforcing properties in the absence of the parturitional hormones. The fact that pups are more reinforcing to the maternal postpartum animal than to the “maternal” virgin suggests, however, that hormones augment the salience of the pup stimulus ( Fleming, Korsmit, et al., 1994). Consistent with this interpretation, in the virgin parturitional hormones enhance the reinforcing effects of pups, but only if the hormones also activate the expression of maternal behavior in virgins. Hormones had no effect on the reinforcing properties of food stimuli. In a second test of pup-reinforcement, Lee et al. (2000) found that during pregnancy females will not bar-press for pups although they will bar-press for food, but that after the birth of the litter, bar-pressing for pups increases tenfold. Again hormones augment this effect but are not necessary for it, because animals commence bar-pressing outside the postpartum period, as soon as they begin showing maternal responses in the home cage. That pups are the relevant reinforcing stimulus, maintaining responses is indicated by the observations that, if pups are removed, the barpress response extinguishes almost immediately. These studies indicate that for animals to respond maternally to pups during the initial encounters, pups do not have to be strongly reinforcing. Presumably the attraction to pups induced by hormones is adequate to insure the mother will respond nurturantly. However, for maternal responsiveness to be sustained in the absence of hormones, females must gain experience interacting with pups, which in general occurs in the presence of hormones; as a result of this experience pups acquire strongly reinforcing properties. Reinforcing characteristics of the mother-litter interaction. To determine precisely what aspects or features of pups are reinforcing to the maternal animal, Magnusson and Fleming (1995) tested the relative contributions of chemosensory and somatosensory stimulation during maternal interactions on the development of a conditioned place preference. They found that pups do not acquire reinforcing properties as readily if dams are exposed to pups placed in a Plexiglas cube, permitting visual, auditory, and olfactory stimulation, but preventing the proximal somatosensory and chemosensory input normally associated with mouthing, licking, retrieving, and crouching. Thus, for pups to be reinforcing they must provide proximal stimulation to the dam, and especially of her ventral and mouth regions. Finally, the reinforcing properties of pups also depend on their ages and odor characteristics. Younger pups are generally more reinforcing than older ones (Wansaw et al., 2008), possibly because they provide more sensory stimulation to dams. Pups will not sustain a conditioned place preference if dams are rendered anosmic. Thus, both tactile and olfactory pup input contribute to the reinforcing properties of pups. Taken together, these studies show that maternal learning is a robust phenomenon that is based on activation of both chemosensory and somatosensory systems during mother-litter interactions. Although the new mother seems primed to respond to certain cues over others by the action of hormones, the primary effect of the maternal hormones is to activate maternal behavior. Once maternal behavior has been exhibited, general mechanisms of learning and memory are utilized to further consolidate experiences acquired during mother-litter interactions. These experiences include the activation in the mother of both chemosensory and somatosensory systems.

Neuroanatomy of Maternal Behavior Although there is substantial evidence that some of the parturitional hormones exert their effects on maternal responsiveness by acting on neural substrates in the brain, which hormones exert central 45

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effects, what brain systems are implicated, and by what specific behavioral mechanisms, are not totally understood. Of interest also is whether the systems that mediate the onset of maternal behavior and the maternal experience effect are the same, different, or overlapping. As can be seen in Figure 2.1, the neural systems that are most important include the olfactory systems, the limbic system, and the hypothalamus (Numan, 1994; Numan and Sheehan, 1997). The olfactory system mediates the sense of smell and is composed of two parts: The main olfactory system detects odor molecules in the air that activate the olfactory receptors in the nose when an animal sniffs an object, and the accessory olfactory system detects molecules in a liquid medium that activate receptors in the vomeronasal organ, also situated in the nose, when an animal touches an object with its snout. The limbic system involves groups of neurons and their axons which have been implicated in the regulation of emotional behavior, reward, and memory processes, as well as species-characteristic behaviors. Brain regions included in this system are the hypothalamus, the amygdala, the nucleus accumbens (NA), the hippocampus and medial prefrontal cortex. The hypothalamus sits at the base of the brain above the pituitary gland, consists of different groups of cells involved in the control of a variety of reproductive behaviors and the release of hormones such as oxytocin and vasopressin from the pituitary gland, and is responsive through specialized receptors to hormones that activate maternal behavior. Two important nuclear groups within this region are the medial preoptic area (MPOA), which is situated somewhat anterior to the hypothalamus and the ventral part of the bed nucleus of the stria terminalis (vBNST), which sits adjacent and dorsal to the MPOA. Also within the hypothalamus are the ventromedial hypothalamic nucleus (VMH) and paraventricular nucleus (PVN), which are positioned close to the midline, but posterior to the MPOA, closer to the pituitary. All four hypothalamic structures respond to environmental stimuli and to circulating hormones. These different brain areas are interconnected by a series of neural pathways. For instance, the two olfactory systems (main and accessory) have direct connections with the limbic system (especially the amygdala) and the hypothalamus by means of the lateral olfactory tract. The amygdala, in turn, is interconnected with the nucleus accumbens, and both are connected with the hypothalamus. Prior to Numan (1974), little was known about the neuroanatomy of maternal behavior. The early work by Beach (1937) focused on neocortical structures and suggested no one area of the cortex is crucial to the expression of maternal behavior. However, the greater the cortical mass removed, the greater the deficits in behavior. Subsequent to these early studies on neocortex, other studies focused on the midline cortex and associated limbic structures, the hippocampus, and septum (Fleischer and Slotnick, 1978; Slotnick, 1967; Stamm, 1955; Terlecki and Sainsbury, 1978; Wilsoncroft, 1963). Although small lesions of these regions disrupt maternal behavior, the deficits were primarily related to motor sequencing and patterning, not to maternal motivation. Thus, animals with these forebrain lesions continued to respond to pups but in a disorganized fashion (Slotnick, 1967; Stamm, 1955).

Maternal “Core”: Two Antagonistic Neural Systems The neural bases involved in the regulation of maternal behavior expression at the time of parturition are well understood. There are at least two basic antagonistic neural systems governing the expression of maternal behavior—referred to as the maternal core. One is the excitatory neural system that deals with the activation of maternal responses towards pups; the other is an inhibitory neural system that may regulate avoidance and aversive responses to pups or pup-related stimuli. The balance between these two systems determines whether maternal behavior will be expressed at the time of parturition. The combination of sensory cues, parturitional hormones, and experiential factors exerts effects on the excitatory system to bring animals close to pups by increasing the attractive quality of pups or pup-related stimuli, and initiate and maintain maternal care; these factors exert effects on the inhibitory system to inhibit animals’ naturally fearful responses toward novel pups (Rosenblatt, 1990; Schneirla, 1959). 46

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The excitatory system. The excitatory system is controlled primarily by neurons in the medial preoptic area (MPOA) and ventral part of the bed nucleus of the stria terminalis (vBNST) and their efferent projections to the brainstem, such as the ventral tegmental area (VTA) (Numan, 1988, 1994; Numan and Sheehan, 1997). Lesions of MPOA/vBNST cell bodies, or knife cuts transecting their lateral projections completely abolish maternal behavior (Numan, Corodimas, Numan, Factor, and Piers, 1988; Numan, McSparren, and Numan, 1990; Numan and Numan, 1996) in the new mother or maternal virgin, whereas “kindling-like” electrical stimulation of this site facilitates maternal responding (Morgan, Watchus, Milgram, and Fleming, 1999a). Hormones that activate maternal behavior act on receptors in the MPOA; implants into MPOA of either estradiol, prolactin, or oxytocin (albeit under somewhat different conditions) facilitate maternal responding (Bridges, Numan, Ronsheim, Mann, and Lupini, 1990; Insel, 1990; Numan, Rosenblatt, and Komisaruk, 1977), whereas the infusion of oxytocin antagonists or morphine or β-endorphin in the MPOA impair maternal behavior (Mann and Bridges, 1992; Pedersen, Caldwell, Walker, Ayers, and Mason, 1994; Rubin and Bridges, 1984). Implants of antiestrogen in the MPOA also delay the onset of maternal behavior (Ahdieh, Mayer, and Rosenblatt, 1987; Numan and Insel, 2003; Numan and Young, 2016). Another line of evidence supporting the importance of MPOA/vBNST neurons in the control of maternal expression comes from studies using c-fos immunohistochemistry. The proto-oncogene c-fos is one of a class of genes (known as immediate early genes) which are expressed in response to a variety of stimulus conditions (Sagar, Sharp, and Curran, 1988) by producing a protein called Fos protein. Fos expression is often used as a marker for detection of neuronal activation. Several studies have demonstrated that a population of neurons in the MPOA/vBNST is involved in regulating maternal responsiveness independent of sensory input. For example, Fleming, Suh, Korsmit, and Rusak (1994) found that postpartum rats exposed to pups had higher numbers of cells showing Fos within the MPOA nuclei than did those exposed to adult conspecifics or left alone. Numan and Numan (1994) also found postpartum rats exposed to pups had more Fos-labeled neurons in the MPOA and vBNST than did postpartum control females exposed to candy. These effects require that the animal is actively maternal and crouches over pups; however, they do not depend on activation by many of the pup-associated sensory inputs. Heightened MPOA c-fos expression persists in maternally active animals even after animals are rendered anosmic (unable to smell), anaptic (unable to feel touch sensations around the muzzle) or after temporary anaesthetization of the ventral nipple area (Numan and Numan, 1995; Walsh, Fleming, Lee, and Magnusson, 1996). To understand the function of the MPOA/vBNST in maternal behavior, Numan and colleagues investigated the MPOA/vBNST projections implicated in maternal responding (see Numan and Sheehan, 1997). By combining the c-fos immunohistochemistry technique with the neural tract-tracing technique, Numan and Numan (1997) found that “maternal” neurons (visualized by Fos-labeling) in the MPOA mainly project to the lateral septum (LS), ventromedial nucleus of the hypothalamus (VMH), and the periaqueductal gray (PAG), whereas “maternal” neurons in the vBNST project to the retrorubral field, PAG, and VTA. The activation of these projections in the control of maternal behavior is consistent with the involvement of these regions in maternal behavior. For instance, the LS has been implicated in the control of the sequential organization of the maternal pattern (Fleischer and Slotnick, 1978); the VTA has been linked to the motivational aspect of maternal behavior (Hansen, Harthon, Wallin, Löfberg, and Svensson, 1991b); the VMH is involved in the control of aversive reactions toward pups (Bridges, Mann, and Coppeta, 1999; Sheehan and Numan, 1997); and the PAG specifically for the regulation of the upright nursing posture and maternal aggression (Lonstein and De Vries, 1999; Lonstein, Simmons, and Stern, 1998). These projections may contribute to different aspects of maternal behavior control. As stated by Numan and Sheehan (1997, p. 105),“the hormonally primed preoptic area projects to some regions to facilitate the appetitive aspects of maternal behavior, projects to other regions to potentiate consummatory components, and projects to still other neuronal groups to depress aversive reactions to pup stimuli”. 47

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The inhibitory systems. The MPOA/vBNST not only projects to the midbrain and motor system involved in the expression of maternal behavior, these nuclear groups also receive input from other parts of the brain, in particular the olfactory and limbic systems (see Figure 2.1), which exert inhibitory influences on the functions of the MPOA/vBNST (Fleming, 1987; Numan, 1988). For instance, a major input to the MPOA comes from the amygdala which in turn receives input from the main and accessory olfactory bulbs (Fleming, 1987). Thus, removal of main or accessory olfactory input facilitates the expression of the maternal complex in nonresponsive virgin animals, while at the same time reducing certain olfactory-mediated components (like licking) in both virgins and postpartum animals who are maximally responsive. These data are consistent with the observation that pup odors within the context of other pup cues are aversive to virgin animals but attractive to the postpartum dams (Fleming et al., 1989b; Fleming and Rosenblatt, 1974b, 1974c; Fleming et al., 1979). The findings that infusions of oxytocin into the olfactory bulb facilitate the expression of maternal behavior, whereas infusions of oxytocin antagonist markedly delay all components of maternal behavior suggest that the olfactory bulb is one such site where parturitional hormones act to antagonize the inhibitory control on maternal behavior (Yu et al., 1996). Behavioral inhibition is also exerted by sites that receive chemosensory projections and that project to the MPOA, such as the medial and cortical nuclei of the amygdala and the VMH, and the anterior hypothalamic nucleus (AHN). The amygdala receives inputs from both olfactory systems and AHN/VMH and projects directly to the MPOA and the AHN/VMH (Canteras, Simerly, and Swanson, 1995). Activation of the olfactory systems increases medial amygdala neuronal activity, whereas electrical stimulation of the medial amygdala predominantly inhibits MPOA neurons as well as the onset of maternal behavior (Gardner and Phillips, 1977; Morgan et al., 1999a). Lesions of the medial amygdala, the stria terminalis (the major efferent pathway from the medial amygdala), the BNST, or the AHN/VMH all result in the disinhibition of maternal retrieving and crouching in virgin animals exposed to foster pups (Bridges et al., 1999; Fleming, 1987; Fleming et al., 1992; Fleming, Vaccarino, and Luebke, 1980; Fleming et al., 1979; Numan, Numan, and English, 1993). The facilitation of maternal behavior produced by amygdala lesions is abolished by lesions of the MPOA, confirming that the input from amygdala acts through MPOA to exert its inhibitory role on maternal behavior (Fleming, Miceli, and Moretto, 1983). Komisaruk and colleagues (2000) provided support for the notion of an active inhibitory system in the regulation of maternal behavior. They combined 14C-2-deoxyglucose (2-DG) autoradiographic method with c-fos immunocytochemistry to visualize the neural activities in specific brain regions under different maternal conditions. The 2-DG method provides information about the metabolic activity of neuronal input. By contrast, c-fos immunocytochemistry detects post-synaptic neuronal activity, therefore it indicates the metabolic activity level of neuronal output. Information from the combined methods can reveal input-output relations in certain brain areas. They found that in parturient and hormonally primed maternal animals, there were elevated 2-DG and c-fos activities in the MPOA and in sites that receive accessory olfactory bulb input (e.g., medial amygdala), indicating an increase in the input and output activity of these areas. In contrast, maternal virgin animals showed a decrease of 2-DG activity but an increase of c-fos activity in the medial amygdala (ME), indicating a decreased input but increased output activity. These results suggest that for the virgin animals to become maternal through pup-induction, the input activity in the vomeronasal nuclei must be decreased, which in turn, disinhibits the output neurons to stimulate the neurons in the MPOA and, in so doing, activates the whole excitatory system. The amygdala, especially the medial part, has an inhibitory influence on the onset of maternal behavior. The inhibitory circuits consist of olfactory systems-to-amygdala-to-MPOA/vBNST and olfactory systems-to-amygdala-to-AHN/VMH-to-MPOA/vBNST (also the downstream periaqueductal grey, PAG; Numan, 2015). Because it has been demonstrated that virgins sustaining amygdala lesions differ from controls in not withdrawing from pups and in maintaining closer proximity to them, and they are less fearful in a series of emotionality tests (Fleming et al., 1980), it is proposed 48

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that these circuits “depress[es] maternal behavior by activating a central aversion system” (Numan and Sheehan, 1997). These effects of amygdala lesions on the animal’s affect are consistent with an extensive literature relating the amygdala to emotional behavior within other contexts (Davis, 1992; Everitt and Robbins, 1992; LeDoux, 1992). One interesting feature of these olfactory limbic structures is that a number of these sites contain receptors for estradiol (Pfaff and Keiner, 1973), progesterone (Numan et al., 1999), and oxytocin (Brinton, Wamsley, Gee, Wan, and Yamamura, 1984), as well as opiates (Bridges, 1990; Hammer, 1984), and therefore constitute likely sites for the hormonal and neurochemical alteration of maternal affect. However, no studies to date have been published showing that maternal hormones or neurotransmitters act on these limbic sites to influence maternal affect in general or maternal behavior specifically. Maternal behavior is under the joint control by two antagonistic neural systems: the excitatory system, which mainly consists of the efferents from MPOA/vBNST neurons to various brain areas, and the inhibitory system, which mainly refers to the projections from medial amygdala to the MPOA/vBNST and VMH. These systems may coordinately regulate neuroendocrine, sensory, and autonomic components necessary for the elaboration of maternal behavior. This circuitry is the “core” system mediating the expression of maternal behavior. They are likely modulated by other higher cortical regions, such as the auditory cortex (Afonso et al., 2007; Febo et al., 2010; Marlin et al., 2015; Pereira and Ferreira, 2016; Wu et al., 2016), possibly via its projections to the “core” system of maternal behavior. This core system also does not incorporate other brain structures known to be involved in maternal behavior, such as the lateral habenula (LH; Corodimas, Rosenblatt, Canfield, and Morrell, 1993; Corodimas, Rosenblatt, and Morrell, 1992; Felton, Linton, Rosenblatt, and Morrell, 1999; Matthews-Felton, Corodimas, Rosenblatt, and Morrell, 1995), and the nucleus accumbens (Li and Fleming, 2003a, 2003b).

Neurochemistry of Maternal Behavior The Mesolimbic and Mesocortical Dopamine Systems and Maternal Motivation Maternal behavior is a robust, goal-directed, motivated behavior, and pups are reinforcing stimuli for the maternal animal (Fleming, Korsmit, et al., 1994; Fleming, Suh, et al., 1994; Lee et al., 2000; Nissen, 1930; Stern and Mackinnon, 1976; Wilsoncroft, 1968). Most studies on maternal motivation have focused on pup retrieval, because it is the most dramatic behavior and is very easy to quantify. By looking at pup retrieval latency and the number of pups retrieved during a certain test period, one can assess an animal’s interest in pups and the intensity of her “motivation” to be in proximity to them. Besides the “core” MPOA/vBNST excitatory neural system in the regulation of specific maternal motivation, the other important system in the regulation of maternal “motivation” is the mesocorticolimbic dopamine system, which originates in the midbrain VTA and releases the neurotransmitter, dopamine, in the nucleus accumbens and the medial prefrontal cortex (mPFC). The current view is that the mesolimbic and mesocortical dopamine systems are part of a nonspecific or general motivational system which serves to increase an organism’s responsiveness to a wide variety of biologically significant stimuli, including pups (Numan, 2007; Numan and Young, 2016; Olazábal et al., 2013a, 2013b).

In Vivo Dopamine and Enhanced Maternal Motivation Hansen et al. (1993) were the first to demonstrate increased dopaminergic activity in the ventral striatum (nucleus accumbens) of mother rats when they were reunited with their newborns after an overnight separation. Building on the early work of Hansen et al. (1993), Fleming and her colleagues 49

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undertook a series of studies of the role of extracellular dopamine in the nucleus accumbens. In these studies the authors provided evidence for the relation between DA and (1) hormonal profiles associated with late pregnancy, parturition, and parity and (2) salience of pup stimulation. Dopamine and hormones. When provided with rat pups, postpartum females show large and sustained elevations in DA in the NA. These elevations occur against a background of a hormonally mediated suppression in basal tonic DA release (Afonso et al., 2009). In the absence of any prior pupexperience, ovariectomized rats treated with progesterone and estrogen (which induces maternal responsiveness to foster pups) display a similar reduction in basal DA responses as postpartum intact mothers and a similar initial increase in response to pup presentation (Afonso et al., 2009). The more rapidly a rat becomes maternal under the influence of hormones, the lower basal DA prior to pup exposure. Thus, hormones that facilitate maternal responsiveness in the absence of previous maternal experience have the same effects on NA DA functioning as in the intact postpartum experienced female, and this hormone-induced basal suppression is related to heightened maternal responsiveness. It can be argued that basal DA suppression aids the rapid expression of maternal behavior through a reduction in the DA noise in the absence of other stimuli. In this way, it might serve as a mechanism for sharpening the DA signal in response to pup stimuli and augmenting the pup saliency to develops. Impairments to basal suppression (e.g., by manipulations of the early environment; Afonso et al., 2011) would be expected to result in a consequent DA signal decrease and a reduction in pup salience, culminating in impaired mother-pup interaction. Dopamine and stimulus specificity. Does this signal-to-noise mechanism result in sharpened DA signals to all stimuli, or only to pup stimuli, in postpartum females? In subsequent studies Afonso et al. (2009) compared the behavioral and DA profiles of female rats when exposed to pups and to palatable food (sweet cereal). Both nulliparous and parous females showed increased DA responses when ingesting the sweet treat. However, only postpartum females showed pup-evoked DA responses greater than the food-evoked DA responses; a finding not observed in cycling females even after pup-experience. The enhanced DA responsiveness to pups in postpartum females is sustained even when the dams are exposed to pups in a perforated box at a distance and cannot interact with them (Afonso et al., 2013). In summary, microdialysis studies suggest that, with maternal suppressed basal DA, pups take on robust saliency to hormonally primed or postpartum females, as reflected in larger increased pup-evoked DA release, even in the absence of actual interactions with pups. In the absence of the hormones of parturition, DA release also occurs in response to pups in maternal animals but not in nonmaternal animals; however, this elevation is not preceded by a reduction in the baseline characteristic of the hormonally primed animal and is sustained for a shorter duration. There is, nevertheless an additive effect of maternal experience on DA release. DA therefore likely mediates pup salience brought about through exposure to hormones or to sustained pup exposure and thereby contributes to the expression of maternal behavior. Pereira et al. (2011) also found a robust DA increase in NA core associated with pup-seeking behavior (presentation of pups behind a screen). Such DA release was further augmented during active (but not passive) maternal interaction with pups. Although the pattern of DA release in relation to maternal behavior was similar in late postpartum females, the magnitude of release was considerably attenuated in late, compared to early, postpartum females behaving maternally (Pereira et al., 2011). DA transients (spike-dependent fast increases in DA; Grace, 1995) during mother-offspring interaction have been investigated using in vivo voltammetry. Champagne et al. (2004) found increased DA signal in the NA in mothers that showed heightened licking and grooming of their newborns; however, the onset of the DA signal preceded the behavior. DA transients were also analyzed by Robinson et al. (Robinson, Zitzman, and Williams, 2011) during pup investigation, and immediately before or during retrieval. The major transient DA signaling was found while the mother was 50

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investigating the cage and newborns prior to retrieving them, and during the first retrieval; subsequent retrievals were not associated with DA transients. Thus, Robinson et al. (2011) proposed that DA transients might play a role in facilitating initiation and maintenance of seeking and appetitive aspects of maternal behavior. However, as the authors also suggest series of studies in a more naturalistic environment could contribute to our understanding of the role of DA transients in the NA prior to and during mother-offspring interaction, and in the transitions among the different behavioral components (retrieving, licking, nest building, hovering over the pups, and nursing). It might also be interesting to determine if those transients of DA change across lactation. In addition to seeing changes in extracellular dopamine or dopamine transients associated with measures of mothering, the injection of certain dopamine receptor agonists (e.g., apomorphine) or antagonists (e.g., haloperidol or raclopride) disrupts various maternal responses, including pup licking, pup retrieval, and nest-building and/or nursing behavior (Giordano, Johnson, and Rosenblatt, 1990; Li, Davidson, Budin, Kapur, and Fleming, 2004; Stern and Protomastro, 2000). In all these studies, the drug-treated animals generally have longer latencies to retrieve pups and retrieve fewer pups than vehicle-treated animals, although at lower drug doses they show only minimal motor deficits. That these effects reflect motivational deficits is reflected in similar effects of dopamine antagonists on many types of “approach” behaviors. For instance, if new mother rats are fitted with a muzzle so they cannot retrieve pups, they will push pups with their snouts and paws. Dopamine antagonists also block this response, at concentrations that are too low to affect actual pup retrieval (Stern and Keer, 1999). That dopamine function within the nucleus accumbens and mPFC is important for these effects is suggested by studies that show that, if dopamine containing cells within the nucleus accumbens or the midbrain (VTA) are destroyed with a neurotoxin (6-OHDA) or by lesions or if dopamine antagonists or GABA agonists are infused into the nucleus accumbens or mPFC, new mother rats retrieve pups more slowly (Febo et al., 2010; Hansen, Harthon, Wallin, Löfberg, and Svensson, 1991a; Hansen et al., 1991b; Keer and Stern, 1999b). In contrast, pup nursing is elevated by dopamine blockade (Keer and Stern, 1999a), indicating that it is the motivation rather than consummatory behavior that is affected by the activity in the mesocorticolimbic dopamine pathways. This idea is further supported by results showing that dopamine antagonists, administered to new mother rats, also block the formation of a conditioned place preference for an environment that was previously paired with rat pups (Fleming, Korsmit, et al., 1994). The fact that these maternal deficits only occur if mothers have recently interacted with pups, but not if they have experienced a period of separation from them, suggests that blocking brain dopamine primarily affects motivation to retrieve and not the motor mechanisms of retrieval. What happens behaviorally when an animal experiences a deficit in dopamine function is an open question. Many behavioral mechanisms can be invoked. Disruption of DA function might (1) produce a general anhedonia, where pups are no longer experienced as pleasurable stimuli (Wise, 1985; Wise, Spindler, and Gerberg, 1978); (2) dampen animals’ incentive motivation to approach pups (Bindra, 1978; Bolles, 1972); or (3) inhibit flexible approach responses towards pups by impairing the behavioral invigoration processes induced by pups (Ikemoto and Panksepp, 1999). The mesolimbic system controls maternal motivation, and the integrity of this system is required for animals to exhibit normal motivated behavior. This conclusion is consistent with a large body of evidence that has implicated the mesolimbic dopamine system in other motivated behaviors, including feeding (Bassareo and Di Chiara, 1999; Wilson, Nomikos, Collu, and Fibiger, 1995), foodforaging (Whishaw and Kornelsen, 1993), drinking (Miyazaki, Mogi, Araki, and Matsumoto, 1998), drug-seeking (Di Chiara, 1998; Wise, 1998), and sex (Everitt, 1990; Mitchell and Gratton, 1994). Dopamine and the maternal “core”. We hypothesize that the mesolimbic and mesocortical dopamine systems exert their influence on maternal motivation by interacting with the MPOA and vBNST. First, the mesolimbic and cortical systems have reciprocal neural connections with MPOA and 51

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vBNST at both the nucleus accumbens and VTA (Stolzenberg and Numan, 2011). Thus, in response to pup cues, the MPOA may cause an increase in dopamine release into the ventral striatum via its action on the VTA, possibly via the oxytocin-expressing projecton neurons (Hansen et al., 1993; Hansen et al., 1991a; Shahrokh, Zhang, Diorio, Gratton, and Meaney, 2010; Stolzenberg and Numan, 2011). The increased dopamine in the nucleus accumbens acts to suppress the accumbal GABAergic inhibitory input to the ventral pallidum (VP), allowing VP efferents to promote active maternal responses. This idea is consistent with observations that bilateral inactivation of the VP disrupts rat maternal behavior, as does the unilateral inactivation of VP paired with a contralateral depression of MPOA activity (Numan et al., 2005). Second, the nucleus accumbens has long been regarded as the limbic-motor interface and is responsible for converting information from the limbic systems (hippocampus, amygdalal and prefrontal cortex, and so forth) into motor actions (Willner and ScheelKruger, 1991). It is interesting to speculate that the function of the MPOA/vBNST in the control of maternal motivation is to provide specific “maternal” information and pass it to the dopamine systems, which in turn, activate the “motivation” and “motor” control systems (extrapyramidal motor system) to execute the motor outputs. The mesolimbic and mesocortical systems may also feed back to the MPOA/vBNST to regulate the appetitive component of maternal behavior (Numan and Young, 2016).

The Serotonin Systems in Maternal Aggression and Maternal Performance Serotonin is a neurotransmitter implicated in many psychological processes relevant to maternal behavior, such as anxiety, depression, affiliation, impulsivity and aggression (Cools, Roberts, and Robbins, 2008; Graeff, Guimaraes, De Andrade, and Deakin, 1996). It also innervates several maternal brain regions, including the MPOA, BNST, olfactory bulb, hippocampus, and amygdala (AngoaPerez et al., 2014; Steinbusch, 1981), and influences the release of parturitional hormones (Bagdy, 1996; Barofsky, Taylor, Tizabi, Kumar, and Jones-Quartey, 1983). There are surprisingly few studies focusing on 5-HT in maternal behavior, possibly due to several earlier studies showing that disruption of 5-HT neurotransmission only causes a transient and nonspecific deficit (Barofsky, Taylor, and Massari, 1983). However, genetic work on mutant mice mothers suggests that genetic mutants lacking full synthesis of 5-HT display impaired pup retrieval, nursing, and nest building (Alenina et al. 2009). Other mouse mutants with impaired 5-HT metabolism also showed reduced reproductive fitness and abnormal maternal behaviors (Girirajan and Elsea, 2009). Because these 5-HT related genes are critical for natural brain maturation and homeostatic modulation of neural circuits, lack of these genes throughout the lifetime may disrupt the development of the neural circuits governing maternal behavior. Work focusing on the roles of specific 5-HT receptor subtypes (>14 known 5-HT receptors in the brain) demonstrates the distinct functions of serotonin receptors in the mediation of maternal behavior. De Almeida and Lucion (1994) first reported that acute administration of a 5-HT1A receptor agonist (8-OH-DPAT) into brain ventricles or into some brain regions (median raphe, periaqueductal gray, and corticomedial amygdala) reduced maternal aggression, whereas later studies showed that, when the same receptor agonist was infused into other brain regions (medial septum and dorsal raphe nuclei), it increased maternal aggression (da Veiga, Miczek, Lucion, and de Almeida, 2011; De Almeida and Lucion, 1997). These data suggest that the 5-HT1A receptors located in different brain regions play different roles in maternal aggression. Similar work also shows that activation of 5-HT2A/2C receptors in the brain decrease maternal aggression (De Almeida and Lucion, 1994) as well as affect other aspects of maternal care. For instance, atypical antipsychotic drugs like clozapine (CLZ), all possessing a strong antagonistic action

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against 5-HT2A/2C receptors, disrupt active components of maternal behavior (e.g., pup retrieval, licking, and nest building) in a dose-dependent fashion (Li, Budin, Fleming, and Kapur, 2005; Li et al., 2004). The involvement of these 5-HT2A/2C receptors in clozapine-induced maternal deficits is supported by the finding that pretreatment with DOI (a selective 5-HT2A/2C agonist) dose-dependently reverses the clozapine-induced disruption of pup retrieval (Zhao and Li, 2009). Furthermore, administration of DOI alone is able to disrupt maternal performance (Zhao and Li, 2010). Because both 5-HT2A/2C receptor antagonist CLZ and agonist DOI disrupt maternal behavior, this study suggests that balanced 5-HT2 neurotransmission is critical for the normal expression of maternal behavior. Too little or too much 5-HT signaling via 5-HT2A/2C receptors could lead to maternal disruptions. Because both atypical antipsychotics and DOI are nonselective for 5-HT2A versus 5-HT2C receptors, their relative contributions in the regulation of maternal behavior have been the focus of a series studies conducted by Li and his colleagues. Using highly selective agonists and antagonists against 5-HT2A and 5-HT2C, Chen et al. (2014) and Wu et al. (2016) demonstrated that activation of either 5-HT2A or 5-HT2C receptor causes a disruption of maternal behavior, although blockade of them has little impact. Although activations of 5-HT2A and 5-HT2C receptor cause a similar disruption of maternal behavior, they may do so through different behavioral mechanisms. Wu et al. (2016) provided evidence showing that pharmacologic activation of the 5-HT2C receptor disrupts maternal behavior via its suppression of mother rats’ motivation to take care of the young, whereas activation of 5-HT2A receptors likely exerts its disrupting maternal behavior by disrupt the well-programmed sequential order of behavioral acts, and not by affecting the incentive (“liking”) or instrumental (“wanting”) value of pups (Chen et al., 2014; Wu et al., 2016). To identify the brain regions where 5-HT2A and 5-HT2C receptors might be involved in maternal behavior, Gao et al. (submitted) used c-Fos immunocytochemistry and found that acute pharmacologic activation of 5-HT2A receptors increases neural activation (c-Fos expression) in the ventral bed nucleus of stria terminalis (vBNST), central amygdala (CeA), and dorsal raphe (DR), whereas Wu et al. (2016) reported that acute activation of 5-HT2C receptors decreases c-Fos expression in the ventral part of lateral septal nucleus (LSv), MPOA, dentate gyrus (DG), and dorsal raphe (DR), and increases it in the central amygdala (CeA). Furthermore, after microinjection of the 5-HT2c agonist (TCB-2) into two brain regions important for the normal expression of maternal behavior: the mPFC and mPOA. Only acute intra-mPFC infusion suppressed pup retrieval, whereas intra-mPOA infusion had no effect. These findings suggest that the 5-HT2A receptor in the mPFC and possibly in the vBNST, DR and CeA, and the 5-HT2C receptor in the LSv, MPOA, DG, and possibly CeA may be required for the normal expression of maternal behavior. Based on the available data, three neural systems where 5-HT2A and 5-HT2C receptors may achieve their maternal effects are proposed. First, the 5-HT2A and 5-HT2C receptors in the VTA and NA may modulate the neuronal activity of dopamine neurons and dopamine release (Alex and Pehek, 2007; Bailey et al., 2016) to affect incentive aspects of maternal care (Li and Fleming, 2003b; Numan, 2007). The observation that reunion with pups increases the concentration of both the metabolite of 5-HT as well as the concentrations of dopamine (DA) and DA metabolites in the ventral striatum is consistent with the DA × 5-HT interaction idea (Hansen et al., 1993). Second, the 5-HT2A and 5-HT2C receptors in the mPFC could modulate the glutamatergic and GABAergic neurotransmission and regulate impulsivity and motivation (Dalley, Mar, Economidou, and Robbins, 2008; Liu, Bubar, Lanfranco, Hillman, and Cunningham, 2007; Pentkowski et al., 2010). Finally, the 5-HT2A and 5-HT2C receptors in the lateral septum (LSv), central amygdala (CeA), and median and dorsal raphe may interact with other subcortical structures (e.g., medial preoptic area) to alter maternal behavior. Apparently, more work is needed to pinpoint the exact neural circuitry through which these two 5-HT2 receptors influence maternal behavior.

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Maternal Learning and Experience Effects In this section, we discuss the neural and chemical controls of the maternal experience effect. Maternal behavior beyond one week after parturition is maintained primarily by sensory influences and processes of learning and reinforcement. Thus, the neuroanatomical and neurochemical substrates of maternal experience effect may not be the same as those underlying the expression of maternal behavior. Brain sites, which are involved in the control of sensory processing and learning and memory processes, may be involved.

Neurochemical Bases of Maternal Experience Because maternal experiences at parturition result in a long-term facilitation of behavior, similar to other forms of learning, there must occur within the brain mediating structural (i.e., synaptic) or functional (i.e., neurotransmitter, receptor) changes. One approach to understanding neuromolecular changes associated with maternal experience was adopted by (Fleming, Cheung, and Barry, 1990) who asked whether maternal memory requires the synthesis of proteins in the brain in the same way as do other more traditional forms of memory (Davis and Squire, 1984). In their investigations of the maternal experience effect (Fleming et al., 1990) and (Malenfant et al., 1991) found that, if a drug that inhibits protein synthesis was injected into dams immediately after a 1-hour exposure, the longterm retention of maternal behavior was blocked and at test animals behaved like inexperienced virgin animals. Moreover, the consolidation of a specifically olfactory experience acquired during the exposure phase was also blocked by drugs that inhibit protein synthesis. Later work showed that the new protein synthesis in the NA shell, rather than in the NA core or MPOA, may be more critical for the maternal experience effect (Li and Fleming, 2003a), as microinjection of a drug that inhibits protein synthesis (cycloheximide at a high dose) into the NA shell immediately after 1 hour of maternal experience disrupted maternal memory, whereas infusions in the MPOA had no effect. It is unclear how these synthesis-blocking drugs interfere with the retention of the maternal experience. One possibility is the noradrenergic system. Moffat, Suh, and Fleming (1993) injected noradrenergic antagonists or agonists into dams immediately after a brief maternal experience and tested them 10 days later for the retention of maternal behavior. Animals receiving the adrenergic blocker exhibited reduced responsiveness, whereas those receiving the agonist exhibited elevated responsiveness during subsequent induction tests. However, more than one neurochemical system is probably involved in maternal memory acquisition and/or retention. Possible other candidates include the cholinergic system (Ferreira, Gervais, Durkin, and Levy, 1999) and the neuromodulators oxytocin (Amico, Thomas, and Hollingshead, 1997; Broad et al., 1999; Pedersen et al., 1995) and the endorphins and opiates (Bridges and Hammer, 1992; Byrnes and Bridges, 2000; Mann and Bridges, 1992). These peptides are present at parturition, influence maternal behavior, and have been shown in other contexts to influence learning and/or memory formation (Martinez and Kesner, 1991). Hatton demonstrated that maternal rats, either real mothers or virgins induced to be maternal by continuous exposure of pups, have profound morphological and physiological changes in their oxytocinergic neurons in the supraoptic nucleus (SON), one of the major sites responsible for oxytocin synthesis and release. These changes include increases in multiple synapses and electrical synapses and decreases in astrocytic processes (Hatton and Tweedle, 1982; Hatton, Yang, and Cobbett, 1987; Perlmutter, Tweedle, and Hatton, 1984; Theodosis and Poulain, 1984; Yang and Hatton, 1988). Another neurochemical candidate that synthesis-blocking drugs may interfere with the retention of the maternal experience is the dopaminergic system (Byrnes, Rigero, and Bridges, 2002). These drugs may interfere with the dopamine D1 and the D2 receptor subtypes, especially those in the NA to disrupt the consolidation of maternal memory (Parada, King, Li, and Fleming, 2008). Behaviorally, 54

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dopamine in the NA shell may act on both receptor subtypes to alter the motivational salience of pup stimulation (Afonso et al., 2008), as maternally experienced female rats show increased dopamine levels in the nucleus accumbens when they are re-exposed to pups. More importantly, the more experience a female has with pups, the greater is the dopamine response. Neurochemically, dopamine may interact with oxytocin in the nucleus accumbens shell to facilitate the consolidation of maternal memory (D’Cunha, King, Fleming, and Levy, 2011). Both dopamine and oxytocin are implicated in the regulation of the salience of social cues, including pups (Shamay-Tsoory and Abu-Akel, 2016). Thus, both can facilitate maternal memory by enhancing the salience of maternal experience. Indeed, oxytocin plays a role in the consolidation of maternal memory (D’Cunha et al., 2011). Taken together, it is clear that changes in multiple systems are probably involved in maternal memory acquisition and/or retention. The possible interactions of neural dopamine, oxytocin and opioid systems in maternal memory are an important topic for future research.

Neuroanatomical Bases of Maternal Experience Which specific brain sites are involved in the formation of a maternal memory has been the focus of a number of immunocytochemical and lesion studies. A number of structures within the maternal circuit are implicated in the formation of a long-term maternal experience. Besides the NA, the MPOA and the amygdala might also be involved. In a series of lesion studies we investigated experimentally which brain sites are implicated in the formation of consolidation of the experience (Lee, Li, Watchus, and Fleming, 1999). We were interested to know whether lesions in neural sites that have been implicated either in the actual expression of maternal behavior or in the formation of memories within other behavioral contexts would disrupt the long-term experience-based retention of maternal behavior. Of all the sites lesioned, only lesions to the NA (especially the shell region) prevented the formation of a long-term maternal experience effect. Animals receiving NA lesions either before or immediately after a maternal experience did not show the faciliatory effects of the experience when tested 10 days later. Instead, they responded to pups in much the same way as did the totally inexperienced animals, with long maternal onset latencies. The involvement of the NA in maternal memory is consistent with its role in the consolidation of other forms (e.g., spatial) of memory (Setlow and McGaugh, 1998; Setlow, Roozendaal, and McGaugh, 2000; Winnicka, 1999). Because the NA has long been implicated in the mediation of reward-related processes (Ikemoto and Panksepp, 1999) and is reciprocally connected with both the MPOA and amygdala (Everitt et al., 1999; Holland and Soedjono, 1981), it is possible that the NA in combination with these structures mediates the formation of maternal memory through its role in both reinforcement and associative processes.

Effects of Mothering and Its Absence on the Development of Maternal Behavior Many factors influence a new mother’s responses to her offspring. Some are situational; others are physiological. These factors exert effects by acting on an organism that has a genotype and a developmental history. Adult characteristics and sensitivities do not emerge de novo, but come about as a result of a host of earlier influences acting in relation to a genetic background, which include influences exerted during the earliest stages of development, during the prenatal period; influences exerted in the nest during the neonatal period; and influences during development through the juvenile and adolescent periods. These influences also take many forms; they include various forms of physical stimulation (associated with variations in temperature, nutritional factors, endocrine factors, and so forth) and include social influences experienced in the nest with mother and litter-mates, and with litter-mates and conspecifics during later periods of development. 55

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There is now good evidence from a number of species that earlier experiences during preweaning life can exert profound effects on the quality and intensity of mothering the new mother provides to her offspring postpartum (Fairbanks, 1996; Fleming et al., 1999). Moreover, based on research with rat and monkey, it seems that these earlier experiences exert their effects throughout development via multiple routes to alter the neurobiology of the juvenile animal and of the adult animal (Fleming et al., 1999; Francis, Caldji, Champagne, Plotsky, and Meaney, 1999; Francis and Meaney, 1999; Gonzalez, Lovic, Ward, Wainwright, and Fleming, 2001; Kraemer, 1992; Suomi and Ripp, 1983). Due to space constraints we do not review the ever-growing literature on the effects of early experience on the development of the neurobiology of mothering. For more on this topic, see Agrati and Lonstein (2016a); Brett et al. (2015); Lomanowska et al. (2017); Lomanowska and Melo (2016); Pawluski et al. (2017); and Ragan, Harding, and Lonstein (2016b).

Genetics of Maternal Behavior The role of genetic factors in the expression of maternal behavior is poorly understood. There have been attempts by geneticists to uncover quantitative trait loci corresponding to features of maternal behavior (Sauce, de Brito, and Peripato, 2012). For example, a study using a cross-fostering approach with genetically defined male and female founders identified a number of loci on offspring chromosomes 5 and 7 in mice that modify maternal behavior (Ashbrook, Gini, and Hager, 2015). The study went on to show that genetic variation in the mother can influence offspring development independent of offspring genotype. That is, genetic variation associated with maternal provisioning of care was found to be independent of genetic variation associated with the solicitation of maternal care by offspring. Many more studies using animal models have examined the interaction between specific genes of interest and the expression of maternal behavior, using gene knockout approaches. Knockout approaches involve specific genes of interest which are removed or mutated, leading to loss of function. For instance, deficits in maternal behavior have been reported for mice deficient in the Peg3 gene (Li et al., 1999; Li, Szeto, Cattanach, Ishino, and Surani, 2000), the Peg 1 (Mest) gene (Lefebvre et al., 1998a), the dopamine beta hydroxylase (Dbh) gene (Thomas and Palmiter, 1997), the Fos B gene (Brown et al., 1996), the 5-HT1B receptor gene (Brunner, Buhot, Hen, and Hofer, 1999), and the prolactin (PRLR) receptor gene (Lucas, Ormandy, Binart, Bridges, and Kelly, 1998), to name a few. In some cases the knockout involves a gene that regulates the synthesis of one of the “maternally relevant” hormones, neurotransmitters, or their receptors. When this is the case, the expected deficits in maternal behavior often occur, as with the PRLR receptor knockout (Lucas et al., 1998); however, sometimes the expected deficits do not occur, as with the oxytocin knockouts which continue to show robust maternal behavior (Young et al., 1997), despite the fact that oxytocin release occurs at parturition and during lactation and has been implicated in the regulation of maternal behavior in a wide range of mammalian species (Bell, Erickson, and Carter, 2014; Noonan et al., 1994; Pedersen et al., 1994). In the case of oxytocin knockouts, only the synthesis of the hormone was eliminated, not the oxytocin receptors which could theoretically be activated by other neurochemicals, such as ligands (Gimpl and Fahrenholz, 2001). Other deficits in maternal behavior seen in the knockouts may be due to the absence of genes that regulate activity and inhibition or ability to learn (Brunner et al., 1999). These deficits that affect more than only maternal behavior itself illustrate a central problem in interpreting the results of these classic gene manipulation studies. The deficit may occur as a result of deficits in a number of core behavioral or physical features, and may therefore not inform about the neurobiology of maternal care per se, but may relate to associated behaviors. Where deficits do not occur, this may reflect either redundancy in neural systems mediating maternal care or compensation as a direct result of the genetic manipulation. The interpretation of both deficits or lack of deficits are particularly problematic with genetic approaches that affect germ cells, 56

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as the manipulation could exert its impacts throughout all stages of life. Newer techniques involving antibiotic- or chemical-sensitive transgenes used to control the temporal specificity of expression, coupled with tissue-specific inducers of expression such as the CRE-LoxP recombination system, can be used to overcome some of these limitations (Gierut, Jacks, and Haigis, 2014). Other approaches have used optogenetic methods to identify highly specific neural circuitry involved in the expression of maternal care. These techniques involve hijacking specific genetically defined neural circuits to express light-sensitive ion channels and thus control neural activity using laser stimulation. These genetic methods thus enable exquisite temporal and spatial precision of neural activity in circuits hypothesized to underlie aspects of maternal behavior. The technique was used to show that the stimulation of oxytocin neurons projecting from the periventricular nucleus of the hypothalamus to the left auditory cortex can produce maternal retrieval in virgin mice (Marlin et al., 2015). Importantly, these studies contrast with traditional pharmacological approaches in their selective modulation of highly specified neural circuitry, as other maternal behaviors known to be responsive to changes in oxytocin are unaffected. New research has shown that a number of genes can also influence maternal care in a nonMendelian fashion. In these cases, the estimation of the influence of some genes on maternal behaviors depends on whether the genes originate from the maternal allele or the paternal allele. These special genes, termed imprinted, rely on DNA methylation to silence one or the other allele, while the other remains unmethylated and hence is expressed. DNA methylation is a form of epigenetic modification, constituting a heritable mark on the DNA itself that does not change the underlying DNA sequence. As a result, gene mutations in imprinted genes can have profound consequences, because only one allele is expressed and, if mutated, cannot be compensated by the activity of the other allele. Examples of imprinted genes that affect maternal behavior are the aforementioned Peg3 and Mest genes, where mutations of these paternal alleles lead to poor maternal care and impaired milk letdown (Curley, Barton, Surani, and Keverne, 2004; Lefebvre et al., 1998b). The potential of imprinted genes on maternal behavior has recently become more complex, as parental biases in the expression of imprinted genes have been detected in dozens of genes, particularly those expressed in the brain (Perez et al., 2015). These data indicate that the expression of imprinted genes may shift between monoallelic expression to biallelic expression depending on tissue type and developmental age. The role for parental bias in gene expression on maternal behaviors and ultimately offspring fitness is currently unknown but an important question for future research in epigenetics. While epigenetic modifications (of imprinted genes) can alter maternal behavior as a result of genetic differences, environmental factors are also associated with modifications of epigenetic mechanisms relevant for maternal care. Work by Champagne and Meaney has revealed that relative differences in levels of care provided to pups is associated with modifications of the epigenome in female offspring (Champagne and Curley, 2008). Specifically, they found that the promoter region of the estrogen receptor alpha (ERα) gene in the medial preoptic area of the hypothalamus was hypermethylated and expression reduced in adult female offspring that had received low levels of care compared to those receiving high levels of care relative to the mean of the cohort of dams examined (Champagne et al., 2006). In females, ERα plays a major role in reproductive behavior and also in maternal behavior, as evidenced by increased c-fos in ERα-positive cells during the postpartum period (Cameron et al., 2008; Lonstein, Greco, De Vries, Stern, and Blaustein, 2000). These findings are of potential importance for maternal care in light of the fact that levels of maternal care of female offspring in adulthood are highly correlated with those of their mothers (Champagne, Francis, Mar, and Meaney, 2003). Curiously, epigenetic modifications as a function of differences in maternal care received during the first week of life emerge at weaning on postnatal day 21, indicating that other mechanisms are likely involved in programing ERα activity in early life (Pena, Neugut, and Champagne, 2013). Nevertheless, these experiments showed by cross-fostering that these effects depend on the care received by the foster mother, not the birth mother. These findings indicate that the 57

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mechanism of transmission of the epigenetic modifications was behavioral rather than by gametic inheritance. The above research underlines that complex interplay between genes and environment in influencing maternal behavior. It is perhaps obvious, then, that a more complete understanding of the role of genotype in maternal care will depend on understanding the biological mechanisms that mediate gene and environment interactions to affect mothering.

Conclusions Despite the extent of our knowledge of the control of maternal behavior in nonhuman rodents, there is much still to learn. We know a great deal about the role of hormones in the onset of maternal behavior, but very little about their role in its long-term maintenance. We know that the parturitional hormones exert multiple effects on behavior, but we have very little understanding of where they act in the brain to effect their behavioral changes; hormone-binding sites outside the MPOA must surely be involved. We know that the MPOA/vBNST is a critical part of the neural circuitry, but we do not really understand its precise function; it seems not to function as a sensory integrator or a motivational “center”; the MPOA/vBNST may simply function as part of the effector mechanism. Similarly, we have learned a great deal about the multiple limbic and cortical systems that interface with the core hypothalamic, midbrain systems, but precisely how they interact online is not known. Despite our increasing knowledge about the role of individual neuropeptides and neurotransmitters in the regulation of maternal behavior, we have limited information on how these neurochemicals interact in the behaving animal. Our understanding of the sensory regulation of maternal behavior is somewhat more complete, but even in this area there is some debate regarding the extent to which single versus multiple modalities are involved in the onset and in the maintenance of maternal behavior. We know that even very brief experiences acquired when the mother interacts with the young can have robust long-term effects, profoundly altering the dam’s response to subsequent external stimulation and to hormones. However, our understanding of where these long-term effects are encoded in the brain and by what mechanism(s) is still not complete. Finally, our knowledge of the genetics of maternal behavior and of the interactive effects of genes and the developmental environment in which the young grow on adult maternal behavior is in its infancy. The importance of epigenetic mechanisms in the regulation of maternal behavior is clear and yet surprisingly few studies have demonstrated such effects. This area is wide-open for further study. An additional set of issues, not touched on in this review, but which would be extremely fruitful to pursue, is a consideration of the natural history and social factors in the regulation of both maternal behavior and its physiological underpinnings. Many of the animals discussed, and rodents in particular, live in social groups in a natural environment characterized by seasonal variations in temperature, food sources, and photoperiod. All these factors could substantially constrain the maternal system. Although maternal behavior in the rat has a specific, quite stereotyped, species-characteristic pattern, its expression depends on the activation of general processes that are stimulated in a variety of diverse contexts. The onset of maternal behavior involves a hormonally mediated change in the dam’s affective state and in the salience of pup-related olfactory and somatosensory cues. These changes increase the likelihood that the dam will approach and maintain proximal contact with pups, thereby creating the possibility for pup stimuli to elicit the specific maternal responses. Once maternal behavior is expressed, other processes become activated to insure that the behavior will be sustained beyond the period of hormonal priming. Once again, these other processes are not specific to the maternal system, but occur within other functional contexts. For instance, when the mother interacts with the young, pups acquire heightened reinforcing properties and through perceptual learning and/or other associative processes, the mother sustains responsiveness to them until weaning commences. All these processes occur in the adult animal that has had numerous experiences earlier 58

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in its life—experiences being mothered. This expression in turns affects the subsequent development of offspring and how they, in turn, will respond to their own offspring. Moreover, the general nature of many behavioral processes activated in the maternal animal is accomplished through the mediation of physiological mechanisms that are recruited in a variety of functional and stimulus contexts and that have had a particular developmental history. Thus, olfactory, limbic, and hypothalamic systems and their associated neurotransmitters, known to influence the expression and maintenance of maternal behavior, are also activated during the acquisition and/or consolidation of learned behaviors within aversive, feeding, and sexual contexts. Finally, it appears that many of these general processes also play a role in the regulation of maternal behavior in other mammalian species (Pryce, 1992), including human beings (Barrett and Fleming, 2011; Fleming et al., 2016; Lonstein et al., 2015). As a result, our understanding of the control of different species-characteristic patterns may be enhanced by understanding some of these more general processes, with the rat model providing a useful heuristic for their analysis.

Acknowledgments Many thanks to all the lab technicians, animal care workers, undergraduate and graduate students who made many of the studies reported herein possible. They know who they are. Thanks also to our families who have patiently withstood the absences necessitated by work reflected in this chapter. Short portions of the text contained herein are based on other review papers on which the authors were co-authors, especially Lonstein et al., 2015; Olazábal et al., 2013a, 2013b. Work reported in this chapter was supported by National Sciences Engineering Research Council (NSERC), Canadian Institutes for Health Research (CIHR), and National Institute of Mental Health (R01MH097718).

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3 PARENTING IN NONHUMAN PRIMATES Kim A. Bard

Introduction Conceptual and practical issues associated with parenting in nonhuman primates and with maternal competence in chimpanzees, specifically, are addressed in this chapter. An important aspect of parenting, emphasized here, is that caregiving differs across ontogeny in primates. There are both short-term and long-term consequences of different parenting experiences, some of which differ across primate species. Although we might like to know universally what makes a good primate parent, the answer must be considered separately for different species. For some species, it seems evident that there are specific behaviors that must be learned to be a competent parent (for example for chimpanzees: Bard, 1994a, 1994b, 1995a, 2002), however, the need for learning parenting behaviors may not be true for all nonhuman primate species. In addition, the influence of early experience on maternal capability remains an unknown factor. These central questions of parenting in primates have been asked for close to 50 years and still have not been satisfactorily answered (Rogers and Davenport, 1970). The foundation of basic knowledge, provided by field studies of the 1920s to 1960s (Altmann, 1967; Bingham, 1932; Carpenter, 1964; Dolhinow, 1972; Hall, 1962; Itani, 1959; Jay, 1962; Jolly, 1966; Kummer, 1967; Morris, 1967; Nishida, 1968; Nissen, 1931; Reynolds, 1967; Schaller, 1963; van Lawick Goodall, 1968; Zuckerman, 1932), allowed specific issues to be addressed, such as the following: (1) the genetic and evolutionary bases of parental care (Trivers, 1974), attachment (Chisholm, 2017), and male-infant relationships (Deag and Crook, 1971; Strum, 1984; Whitten, 1987); (2) the functions served by nonparents providing infant care (Hrdy, 1976, 2009; Lancaster, 1971; McKenna, 1979; Quiatt, 1979; Rowell, Hinde, and Spencer-Booth, 1964); (3) explanations for infanticide (Hausfater and Hrdy, 1984; Hrdy, 1976; Nicolson, 1987; Quiatt, 1979); (4) explanations for disruptions/dysfunctions in parental care (Bard, 1994a; Maestripieri and Carroll, 1998, 2000; Nadler, 1980; Reite and Caine, 1983); and (5) the manner in which social systems influence patterns of parental care (Chisholm, 2017; Hawkes et al., 2017; Hinde and Spencer-Booth, 1967; Maestripieri, 1994). Investigating these central issues has raised more specific questions. For instance, what are the major factors that influence the evolution of cooperative care? It was thought that males would provide care when paternity was certain, so monogamy was considered to be the best predictor of cooperative care. When types of care were compared across monogamous primates, some did have cooperative care but others did not (Wright, 1990). The ratio of infant(s) weight to mother’s weight was also considered to be a predictor of cooperative care, but it was also found to be a poor candidate 78

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(Gursky, 2000). Cooperative care of infants is associated with increased vigilance and defense against predators (Caine, 1993; Snowden, 1996). Comparing humans to other primates, the presence of post-reproductive alloparents (i.e., grandmothers) may be an evolutionary driver for cooperative care (Hawkes et al., 2017; Hrdy, 2009). Comparing primates to other mammals, however, shows that most primate mothers receive some type of help in the care of their offspring (Isler and van Schaik, 2012). Additionally, modern humans, across many small-scale societies, as well as those living in urban industrialized communities, have short interbirth intervals, with infants weaned while still in early infancy (Dettwyler, 2004; Hawkes et al., 2017; Sellen, 2001). A perennial issue is how nonhuman primate parenting relates to human parenting. This chapter is concerned with describing parenting behavior in primates. There are many different social and ecological environments and parenting behaviors experienced by primate subadults: “behavioral plasticity is the very hallmark of primates” (Hawkes et al., 2017, p. 71). Chimpanzees are used as the basis for comparison with other primate species. Chimpanzees are our closest evolutionary relatives, sharing over 90% similarity in genetic material (King and Wilson, 1975), and provide important information relevant to human behavior. The majority of research on primate parenting has been conducted in a relatively limited number of primate species, even though our knowledge of different primate species has expanded across the decades. This chapter, as a product of our limited knowledge, focuses on the well-studied species. Parenting behaviors in chimpanzees are described in detail and explicit comparisons are made in parenting behavior between chimpanzees and other primates. This chapter contains two main parts, descriptions of species-typical parental behaviors and longer-term consequences of infant experiences of parenting (or their lack). The section describing species-typical parental behavior is further divided by taxonomic divisions and by offspring age beginning with parental behaviors directed toward newborn chimpanzees and ending with parental behaviors directed toward adolescent prosimians. Social dynamics may also influence parenting styles (Maestripieri, 1994), but are not discussed in detail here. This perspective provides insights on primate parenting because the focus is on different parenting behaviors that are required for offspring of different ages for different primate species.

Parenting Behaviors in Nonhuman Primates Different skills are required for parental care of infants of different ages (Tardif, Harrison, and Simek, 1993). The age of individuals within each period differs between the species due to different rates of development (Table 3.1). Parenting behaviors are discussed separately for newborns, infants, juveniles, and adolescents. The newborn period is defined in humans as the initial 28 days after birth during which the infant is most vulnerable and at risk. It is unclear whether there are objective markers of this period, in humans or other primates (Bard and Nagy, 2017). Infancy is the period when the offspring is physically dependent on the mother’s milk. Weaning marks the end of the infancy period. The juvenile period, between the end of weaning and the beginning of sexual maturity, is distinguished by longer times spent further away from the parent(s), and sometimes accompanying changes in coat color. The adolescent period begins at puberty and ends at the time when effective reproduction occurs (Walters, 1987). The age estimates for weaning (the end of the infancy period), puberty (the beginning of adolescence), and attaining adulthood (first birth for females, and full adult size for males) are summarized in Table 3.1. The skills necessary for parenting offspring at each developmental period may have different developmental histories. Therefore, both the skills and their ontogeny are discussed within each age period separately. Parenting behaviors are additionally presented within sections by order (see Figure 3.1). There are major differences between species in the skills required for maternal competence. For many species of monkey, infants are motorically capable soon after birth. Maternal competence in 79

Kim A. Bard Table 3.1 Estimates of parenting life history variables from wild primate populations Weaning

Sexual maturity Females

Full adult size Males

Great and Small Apes Chimpanzees Gorilla Orangutan Gibbon

~5 yrs ~3 yrs ~5 yrs ~2 yrs

~9 yrs ~6.5 yrs ~10 yrs

Old World Monkeys Baboon Vervet Blue monkey Rhesus

~12 mos ~12 mos ~12 mos ~12 mos

~5 yrs ~4 yrs 6.7 yrs ~3 yrs

New World Monkeys Howler Spider Squirrel Capuchin Tamarin Marmoset

~9 mos ~15 mos ~4–18 mos ~16 mos ~3 mos ~2 mos

~3 yrs

Prosimians Ring-tailed lemur Lesser galago Gray mouse lemur

~3 mos ~1.5 mos 4–6 wks

~10 yrs ~9 yrs ~14 yrs ~6.5 yrs ~5 yrs ~5 yrs ~3 yrs

~4 yrs ~4.5 yrs ~2.5 yrs ~3.5 yrs ~4 yrs ~4.5 yrs ~1.2 yrs ~14 mos ~3 yrs ~9–10 mos ~3 mos

Females

Males

~14.5 yrs ~10 yrs ~14.5 yrs ~11 yrs

~18 yrs ~15 yrs ~17 yrs ~13 yrs

~7 yrs ~5 yrs ~6.5–10 yrs ~4 yrs

~7.5 yrs ~6 yrs ~8–10 yrs ~8 yrs

~4.5 yrs

~7 yrs ~7.5 yrs

~3 yrs ~4 yrs

~8 yrs ~4.5 yrs ~3.5 yrs ~1.5 yrs ~3 yrs ~1.1 yrs ~3 mos

References: Chapman and Chapman, 1990; Cords and Chowdhury, 2010; Castanet et al., 2004; Cords (pers comm)

many monkeys, therefore, involves only acceptance of the infant (i.e., allowing the infant to cling). For example, rhesus infants at birth are able to cling, climb on the mother’s body, and suckle. In other words, rhesus infants can survive as a result of their own behavior, as long as the mother does not actively reject them (i.e., pull them off her body and prevent them from clinging). In contrast, for chimpanzees as in humans, maternal competence requires active cradling and nurturing. Newborn chimpanzees are as helpless to survive without maternal support as are human newborns. As described in Bard (1995a, 2002), Winston, Barbara’s newborn baby, could not move into her arms; Barbara needed to take the active role and to pick him up—but this was one of the behavioral skills that she lacked. Maternal competence in chimpanzees therefore requires the mother to take positive action, including picking up the helpless newborn. Competence in all species is defined broadly as the ability to raise offspring to adulthood. This section of the chapter concentrates on parenting during infancy for a number of reasons. Primarily, parenting responsibilities are greatest during infancy when offspring are least capable of coping on their own. The second reason is that there are already good reviews on juveniles (Pereira and Fairbanks, 1993) and adolescents (Bernstein, Ruehlmann, Judge, Lindquist, and Weed, 1991; Caine, 1986), although little is known about those parenting behaviors specifically directed to juveniles and adolescents. Adolescence is typically the time when emigration occurs, and offspring may permanently leave the family group. In most primate species, it is the sons that leave, and the daughters that remain in the natal group with their mothers. Although parental status within the group may be crucial to the long-term outcome for an adolescent, observable parent-offspring interactions are minimal. 80

Marmosets Tamarins Capuchins

New World monkeys

Squirrel monkeys Night monkeys Howler monkeys Wooly monkeys and spider monkeys Uakaris, sakis, and titi monkeys

SIMIANS

Macaques Mandrills Baboons Vervets and guenons Colobus monkeys Langurs, proboscis, and leaf monkeys Gibbons Orangutans Great Apes

CATARRHINES

Old World monkeys

Chimpanzees Bonobos Humans Gorillas

Ruffed lemurs Aye-ayes Indris and sifakas Mouse lemurs and dwarf lemurs Galagos (Bushbabies) Lorises

Figure 3.1 Classification of living primates frequently mentioned in this chapter. Source: Reprinted with permission (Myowa and Butler, 2017, p. 54).

PROSIMIANS

Tarsiers Lemurs

Kim A. Bard

Great Apes and Small Apes Chimpanzee Demographics Captive chimpanzee mothers are approximately 11 to 12 years old when they first give birth (Fragaszy and Bard, 1997; Roof, Hopkins, Izard, Hook, and Schapiro, 2005). If they care for their infant, the subsequent infant will be born 3 to 4 years later (interbirth interval), and they will have approximately 4 babies in their lifetime (Fragaszy and Bard, 1997; Roof et al., 2005). In the wild, chimpanzee mothers are approximately 11 to 17 years old when they have their first baby (Goodall, 1986; Nishida et al., 2003; Sugiyama, 2004), although at some field sites, such as Mahale, many first babies die or are victims of infanticide (Nishida, 2012). At most field sites, female chimpanzees transfer out of their natal group before giving birth (Roof et al., 2005) and may be younger when first giving birth than those who stay in their natal group (Nishida et al., 2003). The interbirth interval in wild chimpanzees whose infants survived was 5 to 7 years, but there is substantial variation by site (e.g., 5.2 years at Budongo; 5.3 years at Bossou; 5.6 years at Gombe; 6 years at Mahale; 6.6 years at Kibale; Emery Thompson et al., 2007), and by sex at some sites (e.g., 5.5 years following birth of daughters versus 6 years following birth of sons at Mahale; Nishida et al., 2003). Wild chimpanzees have approximately three babies in their lifetime (Emery Thompson et al., 2007; Potts, 2013). There is some variation in these life history parameters across different field sites and between chimpanzees and bonobos. Bonobo mothers in the wild first give birth when they are 14 years old, and their interbirth interval is between 4.5 years at Wamba and 8 years at Lomako (Wich et al., 2004). The oldest wild chimpanzee females to give birth to surviving infants varied from 40 years at Bossou to 55 years at Kibale (Emery Thompson et al., 2007). Data on the birth of three chimpanzee infants found strong similarities in the delivery compared with human newborns (Hirata, Fuwa, Sugama, Kusunoki, and Takeshita, 2011). Specifically, the chimpanzee infants emerge from the birth canal facing away from the mother, as is found in humans. There are considerable changes in orientation through the birth canal, as the head and body subsequently rotated, before dropping to the floor (two cases) or being gathered by the mother (one case). This orientation at birth was previously thought to be unique to humans and was proposed as the evolutionary basis for the use of midwives (Hirata et al., 2011). It appears that, among all the nonhuman primates, chimpanzees share the most similarities to humans in lifespan characteristics.

Parenting Newborn Chimpanzees and Apes The newborn period is defined as the initial period after birth during which the infant is unable to survive without parental support. For some primate species, there is really no clearly definable neonatal period subsequent to the minutes after birth; for others the period lasts through the first 30 days as is true for human newborns (Bard, Brent, Lester, Worobey, and Suomi, 2011; Bard and Nagy, 2017; Brazelton, 1984). This section discusses those special parental skills applied to newborns, distinct from the parental behaviors to infants. The term infants refer to nonhuman primate infants: Human infants are distinguished explicitly. Field studies of free-living chimpanzees do not richly describe newborn chimpanzee behavior in part because the very small neonate is difficult to detect on the body of the mother (weighing 1.5 kg, on average: Fragaszy and Bard, 1997) and in part because new mothers appear to be very cautious or wary and are not often observed (Goodall, 1986; Plooij, 1984; van Lawick-Goodall, 1967). Newborn chimpanzees do not have any distinctive coloration, although their skin is lighter in color during infancy than the skin of adults (Nishida, 2012). The chimpanzee newborn and mother are in constant ventral-ventral contact during the first 30 days of life (van Lawick-Goodall, 1968). Newborn chimpanzees are as helpless to survive without 82

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maternal support, as are human newborns. Although both newborn chimpanzees and newborn humans have a strong grasping reflex (Bard, Hopkins, and Fort, 1990), this reflex is insufficient to support the infant for more than a few seconds at a time. Unlike most primates, chimpanzees are unable to support their own weight independently for at least the first two months of life (Bard, Platzman, Lester, and Suomi, 1992; van Lawick-Goodall, 1968; Nishida, 2012; Plooij, 1984; RijtPlooij and Plooij, 1987). Mothers provide the majority of physical support during this time although they seldom help neonates to suckle. Feedings are short in duration and irregularly spaced (Brown and Pieper, 1973; Dienske and Vreeswijk, 1987; Plooij, 1984). Detailed observations of newborn chimpanzees with their mothers are possible in laboratory settings, such as at the Yerkes Research Center of Emory University and the Primate Research Institute of Kyoto University. In captive settings, nuzzling, rooting, and nursing account for approximately 20% of the chimpanzee infant’s waking time during the first month of life (Bard, Platzman, and Coffman, 1989), but appears to account for only 2%–4% of infant’s time in field settings (Lonsdorf et al., 2014). Infants nuzzle and root to find the nipple, typically without any assistance by the mother. Suckling begins within the first day or two after birth, and averages 1 to 2 minutes every hour during the day and night (Bard, 2002; Mizuno, Takeshita, and Matsuzawa, 2006; Nishida, 2012). Newborn chimpanzees sleep during approximately 50% of observation time throughout the first 30 days of life. During sleep, EEG reveals brain wave patterns (REM sleep, deep sleep, etc.) in chimpanzee newborns that are similar to those of human newborns (Balsamo, Bradley, Bradley, Pegram, and Rhodes, 1972). Behavioral observations reveal that newborns are in REM sleep ~35% of the nighttime and in deep sleep ~35% of the nighttime (and awake at night, ~30%: Mizuno et al., 2006). The newborn is alert and quiet for considerable periods, especially on the first day of life and increasingly through the first month, an average of 25% of the time. Active alert states are apparent but account for less than 10% of observation time during the first month of life. Newborn chimpanzees raised by their mothers do cry and fuss, but these periods of moderate to mild distress are infrequent and brief (Bard, 2000). The vast majority of maternal behavior with newborn chimpanzees is simply cradling, providing the support they need to remain in physical contact (over 80% of the time; Bard, 1994a; Goodall, 1967; Nishida, 2012). Other maternal activities, in addition to cradling, occur for an average of 10 minutes per hour. These additional activities include grooming the infant (6%), playing with the infant and eliciting some smiles (3%), examining the infant (2.5%), assessing the behavioral and physical state of the newborn (2%), and encouraging the infant’s motor development with physical exercises (1%) (Bard, 1994a; Bard et al., 2005). Chimpanzees are responsive to their social environment, even as newborns. Bard et al. (2011) conducted tests of the neurobehavioral integrity of newborn chimpanzees raised in one of three different nursery environments and compared their performance with those raised with their mothers in another captive setting (mother-raised data originally reported in Hallock, Worobey, and Self, 1989). These environments differed in the degree of exposure to humans and degree of cradling contact. At 2 days of age, newborn chimpanzees significantly differed in the domains of Orientation (both to social and inanimate stimuli) and State Regulation (especially self-quieting skills) as a function of rearing environment. By 30 days of age, almost all of the items and clusters (all 7 items of the Orientation cluster, 4 of 5 items of the Motor cluster, 4 of 4 items of the Range cluster, and all 3 items of the Regulation cluster) showed significant differences among the chimpanzee rearing groups. In both the early part of the newborn period (2 days of age) and the latter part of the newborn period (30 days of age), the largest differences were found when comparing the newborns which were raised with their chimpanzee mothers to those raised in nurseries by human caregivers (19 items and clusters from a possible 24 showed significant differences at 30 days of age). But there were numerous significant differences among the different nursery chimpanzee groups as well (7 of 24 possible differences between the Southwest Foundation and the Yerkes Standard care nursery groups, and 2 differences between the Responsive Care Intervention and Yerkes Standard care 83

Kim A. Bard

nursery groups). Surprisingly, the chimpanzees raised by their mother appeared to have lower levels of neurobehavioral integrity in several domains (e.g., Orientation, Motor Performance, State Regulation) compared to the human group and the Standard care nursery group at 30 days of age (Bard et al., 2011). These lower scores are probably due to the fact that the mother-raised environment is more protective and restrictive of the newborn infant than are nursery environments, with less exposure to humans and human artifacts, and greater experience with constant cradling contact. Gaze is an important aspect of primate behavior, and mutual gaze is an important aspect of human mother-infant interaction (Trevarthen, 1979; Tronick, Als, and Adamson, 1979). On average, chimpanzee mothers at Yerkes spend 12 minutes an hour looking at their newborn infants (Bard, 1994a). Half of that time is spent looking at the infants’ face, which occurs during maternal activities of assessing, examining, playing, and grooming. Newborn infants also gaze at the face of their mother (Goodall, 1986, p. 86). Numerous instances of mutual gaze occur between mother and newborn infant, 10 times in an hour on the average (Bard, 1994a; Bard et al., 2005). Newborn chimpanzees, like human newborns, can mimic facial movements of their caregivers (Bard, 2007; Bard and Russell, 1999; Myowa-Yamakoshi, Tomonaga, Tanaka, and Matsuzawa, 2004). Chimpanzee newborns appear to imitate mouth openings, tongue protrusions, and sequences of mouth actions, including making sounds, such as a tongue click (Bard, 2007). Neonatal imitation, therefore, is one mechanism by which parents can directly influence the behavior of their offspring, during face-to-face interactions, especially when they are communicative (Bard, 2007). However, there are additional influences on newborn behavior that may be more indirect or subtle, such as via amount of cradling contact or degree of exposure to culture-specific practices, such as eye gaze patterns or nurturing style of caregivers, for example (Bard, 2017; Bard et al., 2005, 2011). These early interactions can have long-lasting consequences. For instance, the amount of nurturing experienced by chimpanzees in the first month of life was found to be correlated with structural co-variation in the gray matter of the basal forebrain (e.g., reward circuit) in adult chimpanzees (Bard and Hopkins, 2018). Chimpanzees have a neonatal period that appears to be as distinct as is the human neonatal period (Bard and Nagy, 2017). Newborn chimpanzees are very responsive to different parenting practices, some of which have long-term consequences (see the following and Bard and Hopkins, 2018).

Parenting Newborn Gorillas, Orangutans, and Small Apes The social structures of orangutans and gorillas differ from that of chimpanzees, and one might expect differences in parenting, even parenting newborns. Orangutans are the most solitary of the great apes (although orangutan mothers seem to spend as much time alone as do chimpanzee mothers: Galdikas and Teleki, 1981). Wild orangutan mothers give birth when they are approximately 15 years old and have the longest interbirth interval among the great apes, at 9.3 years at Ketambe (Sumatran subspecies), 7.7 years at Tanjung Puting, and 7.0 years at Gunung Palung and at Tuanan (Bornean subspecies; van Noordwijk, Willems, Atmoko, Kuzawa, and van Schaik, 2013; Wich et al., 2004). Gorilla groups consist of a dominant male silverback and five to seven unrelated females (i.e., harem). Mountain gorilla females first give birth when they are 10 years old, and their interbirth interval is 4 years (Wich et al., 2004). Newborn orangutans and gorillas appear more capable motorically compared with chimpanzees (Figure 4.2 in Bard, 2002). Orangutan mothers with newborns do not travel far or quickly, and they rest frequently (Galdikas, 1982). Maternal support of the infant may be minimal even on the first day of life, and the placenta may or may not be eaten (Fossey, 1979; Galdikas, 1982). Gorilla mothers with newborns are given preferential proximity to the father, the silverback male. Newborn gorillas can cling, unsupported by the mother, for up to three minutes (Fossey, 1979). In gorillas, the social group is important for the maintenance of maternal competence, perhaps heightening protective 84

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responses (Nadler, 1983). In captive settings, new gorilla mothers isolated from the group typically exhibit abusive behavior ( Joines, 1977; Nadler, 1983). The small apes, gibbons and siamangs, have long been thought to be exclusively monogamous and territorial, but several species regularly include more than two adults, and females engage in copulations outside of their “pair-bond” (Hawkes et al., 2017; Sommer and Reichard, 2000). Interbirth interval is 2 to 3 years in siamangs (Lappan, 2008). As expected the males engage in paternal care (mostly carrying) when offspring are older, but in the newborn and infancy periods, mothers provide exclusive care in the small apes (Lappan, 2008). Gibbon mothers provide cradling support to newborns and reposition the infants to a safer spot on the mother’s body, for example, prior to leaping between trees (Carpenter, 1964). The first weeks after birth has been identified as the newborn period for gorillas, orangutans, bonobos, and the small apes (gibbons and siamangs). Although it is not clear whether this is a distinct developmental period, it appears that caregivers do attend with extra care to the newborn.

Parenting Chimpanzee Infants Infancy is the period when the offspring is physically dependent on the mother’s milk. The infancy period is often differentiated into an early period, during which no independent locomotion occurs, and a later period, during which there is some independent locomotion although the infant remains close to the parent(s) during the day and night. Great apes (chimpanzees, orangutans, bonobos and gorillas) remain in infancy for 4 to 6 years. Goodall (1986) classified infancy in chimpanzees as the period from birth to the time of weaning (and cessation of travel on the mother’s body), which occurs at approximately four to five years of age in the wild (Clark, 1977; Nishida, 2012) but weaning occurs earlier, around 3.5 years, in captive settings (Fragaszy and Bard, 1997). The early infancy period is characterized by almost constant physical contact. The first break in contact is typically initiated by the 3- or 4-month-old laboratory infant (Miller and Nadler, 1981; van Lawick-Goodall, 1968). By 3 months the amount of maternal restraint of infant movement has increased fivefold to about 15% of the maternal interactive time (Bard, 1994a; Bard et al., 2005), indicating how active the infant has become and that the mother is responsible for maintaining the infant’s proximity to her at this age. In the first 3 months, chimpanzee mothers (with good maternal competence) engage their infants in a variety of interactions (Bard, 1994a; Goodall, 1967; Plooij, 1984), although the majority of maternal time is still spent simply cradling their young infants (71% at Yerkes, but less at PRI ~40%: Bard et al., 2005). In captive settings, mothers spend almost 30% of their interactive time grooming 3-month-old infants, and 14% of their interactive time playing with their 3-month-old infants (Figure 3.2). Although there is variation across captive settings, when their infants are 4 months old, caregivers encourage a variety of species-typical skills at a rate of 7 to 11 minutes per hour (Bard, Bakeman, Boysen, and Leavens, 2014), and nurture social communicative skills, in particular, at a rate of 2 to 3 minutes per hour (Bard, Dunbar et al., 2014). Infant motor development is stimulated through maternal maneuvers, such as standing infants while holding their hands. Mothers repeatedly and alternatively stimulate their infants to hold their weight with legs and then with arms. At 3 months, there was significantly more exercising of infants at PRI (33% of noncradling time) compared with at Yerkes (7%; Bard et al., 2005). Encouragement of early crawling is accomplished in a similar way. Because mother-infant contact is rarely broken in these early months, these stimulating exercises are typically performed on mother’s body. “Sooner or later every mother encourages and variously aids her baby to learn to creep, stand erect, climb, and finally to walk and run” (Yerkes and Tomilin, 1935, p. 333). Early mother-infant communication in chimpanzees is often accomplished with touch (Plooij, 1979) and can be accompanied by vision and audition. Mothers monitor their infant’s behavioral 85

Kim A. Bard

Figure 3.2 Mother and 3-month-old infant chimpanzees, Pan troglodytes, engage in mutual gaze 10 times per hour, on an average, at the Yerkes National Primate Research Center Field Station, Atlanta, Georgia (Bard et al., 2005). Source: Photo credit: Joshua A. Schneider.

state by stretching and moving infants’ toes, fingers, arms, and legs and sometimes just by looking at them. Chimpanzee infants smile with a playface, which consists of very little lip corner withdrawal, but lots of jaw dropping with an open mouth (Figure 3.1 in Bard et al., 1992). During play, human infant smiles are sometimes “marked” as critical features by the mother with an emphasized touch (Adamson and Bakeman, 1984). When the chimpanzee infant smiles in response to a tickle in the neck or groin, the chimpanzee mother may place her index finger on the infant’s lower gums and exaggerate the smile by pushing gently on the lower gums, “marking” it in a similar way as do some human mothers. In a responsive care nursery program for abandoned chimpanzee infants, human researchers used this technique to highlight the importance of different skills as they emerged in young chimpanzee infants (Bard, Dunbar et al., 2014). Previous reports indicated very limited episodes of mutual gaze in mother-infant great apes (Papousek, Papousek, Suomi, and Rahn, 1991; Plooij, 1979; Rijt-Plooij and Plooij, 1987). Chimpanzee mothers spend considerable amounts of their time gazing at their young infants’ body (~14% of observation time) and gazing at the infant’s face (~11% of observation time). Chimpanzee infants gaze at their mothers’ faces. Very young infant chimpanzees appear to have a greater visual acuity at 30 cm than 15 cm but see quite comparably to human infants at 15 cm (Bard, Street, McCrary, and Booth, 1995). Early social environments influence the expression of behavior in chimpanzees and humans, and eye gaze patterns between mother and infant vary during the first 3 months of life (Bard, 1994b; Bard 1992; Bard et al., 2005). At Yerkes, mothers appeared to be sensitive to infants’ eye gaze and shifted their own gaze away whenever mutual eye gaze was attained (Bard, 1994a), in striking contrast to the extended mutual gaze encouraged by some human mothers (Trevarthen, 1979; 86

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Tronick et al., 1979), or when humans are interacting with infant chimpanzees (Bard, 1998b; Bard et al., 1992). However, some captive and wild chimpanzee mothers actually encouraged extended durations of mutual gaze by lifting the infants chin to establish and maintain mutual gaze (Bard et al., 2005; van Lawick-Goodall, 1967). Chimpanzees at the Primate Research Institute, Kyoto University, had an average of 27 bouts of mutual gaze per hour with their 3-month-old infants, a rate that is very similar to that of Western human mothers with their 3-month-old infants (Bard et al., 2005). For infant chimpanzees, as well as infant humans, these differences in eye gaze patterns tend to accompany differences in proximal versus distal caregiving patterns (Bard et al., 2005; Keller, 2007). When caregiving is more proximal, with extensive cradling contact (as in Yerkes chimpanzees and many subsistence rural human communities), there is less mutual gaze, whereas when caregiving is more distal (as at PRI laboratory and in middle-class Western human communities) then mutual gaze is more extensive (Bard et al., 2005). Thus, it may be that one of the early behaviors that is “culturally” regulated in chimpanzees (and humans) is eye gaze (Bard, 2017; Bard and Gardner, 1996: Bard et al., 2005; Figure 3.2). Independent quadrupedal steps and climbing appear as early as 4 months of age in field settings (Rijt-Plooij and Plooij, 1987), and independent quadrupedal location is common by 5 months in captive settings (Bard, 1996). In wild settings, in the first 6 months, infants spend about 12% of observation time clinging to the mother’s belly or chest while she travels (i.e., riding ventrally; Lonsdorf et al., 2014). From 5 to 7 months, wild chimpanzee infants begin to ride on the mother’s back (males ~4%; females ~1% of observation time; van Lawick-Goodall, 1968; Lonsdorf et al., 2014). Male infants make the shift to more dorsal than ventral riding earlier (~1 year) than do female infants (~1.5 years; Lonsdorf et al., 2014). Typically, it is not until 1.5 years of age that infant chimpanzees reliably respond to the mother’s communicative signals to “climb aboard” (van Lawick-Goodall, 1968). One mother was explicitly observed to teach her young infant to climb on her back when she displayed a hunched posture while looking over the shoulder, which constitutes a communicative signal (Rijt-Plooij and Plooij, 1987). From 5 or 6 months, the mother places the infant on her back or repositions the infant from ventral to dorsal position. Some argue that mothers act roughly to attain dorsal riding and breaks in contact, but careful reading suggests that typical maternal behavior at Gombe is determined, rather than aggressive (Rijt-Plooij and Plooij, 1987). Observations of 19 chimpanzee infants from the Kanyawara community in Kibale National Park, and the Tai South community in Tai National Park, provide details about the subtle and frequent gestures employed by mothers and infants in coordinating joint travel (Frohlich, Wittig, and Pika, 2016a). Mothers used an average of 10 gestures and four actions to initiate carrying of 10- to 12-month-old infants, including multimodal signals, such as uttering a soft “hoo” vocalization while presenting their back for the infant to climb on or while reaching their arm to the infant (Frohlich et al., 2016a). Infants used an average of two or three gestures, and two actions, to initiate maternal carrying. As infants develop, they change from using whimpering alone, for example, to using more visual gestures, such as a reach, either alone or in multimodal combinations. Thus, chimpanzee mothers provide both physical support and encouragement for their young infants’ motor developments (Bard, 1994a; Frohlich et al., 2016a; Goodall, 1967; Yerkes and Tomilin, 1935). The responsive care nursery program at Yerkes used these infant motor milestones and maternal encouragement behaviors to design a program to encourage 5-month-old chimpanzees, for example, to engage in dorsal riding (Bard, 1996). The subtle communication between mother and infant is documented in “meshing”. Rijt-Plooij and Plooij (1987) discussed meshing only in the locomotor context and defined it as maternal anticipation of and coordination with the infant’s contact behavior. Meshing occurs from 8 to 24 months but monthly levels rise and fall in correspondence with the infants’ responsibility for contact maintenance. “It is the mother’s role to (force) teach the infant how to use newly emerged abilities it might not, or not fully, have used otherwise” (Rijt-Plooij and Plooij, 1987, p. 72). 87

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From 8 months, infants and mothers are comfortable out of physical contact and within arm’s reach, but infants whimper when mothers move too far away (Rijt-Plooij and Plooij, 1987). It is perhaps no different from increased separation anxiety observed in human infants from 7 to 9 months, when human infant’s developing cognitive processing allows them to distinguish novel from familiar, and they show wariness of strangers (Ainsworth and Bell, 1970; Bard and Gardner, 1996; Bowlby, 1969, 1973; Fritz and Fritz, 1985; Plooij, 1984; Rijt-Plooij and Plooij, 1987; van IJzendoorn, Willems, Atmoko, Kuzawa, and van Schaik, 2009). A reasonable conclusion from Rijt-Plooij’s descriptive data is that between 8 and 11 months the infant becomes more responsible for maintaining contact and proximity with the mother, in contrast to the earlier ages when the mother is mostly insisting on proximity with the infant. From 12 months to 18 months infants return to being comfortable within their mothers’ arm reach. By 18 months, dorsal riding becomes the predominant mode of joint travel (~8% of the time; Lonsdorf et al., 2014). By 2 years of age, infants are spending time outside of arm’s reach (between 1 and 1.5 meters away), and as they get older they spend increasing amounts of time more distant from the mother. By 3.5 years of age, sons move further away than daughters (3 meters versus 2 meters: Lonsdorf et al., 2014). By 4.5 years, older infant chimpanzees spend less than 1% of their time riding dorsally on their mothers, spend between 5% (females) and 10% (males) of their day traveling independently, and move up to 4.5 meters (males) and 2.5 meters (females) away from their mother (Lonsdorf et al., 2014). Social skills such as greeting social partners and using communicative signals to initiate play or grooming, develop first in interaction with the mother and then are used in interaction with others, first older siblings and peers, and then older unrelated individuals (Bard, Dunbar et al., 2014; Nishida, 2012). In the second month of life, infant chimpanzees respond to mothers’ tickles with smiles and very quiet laughter (Bard, 1998b; Bard, Dunbar et al., 2014; Plooij, 1979). In the third month, infants reach, with a smile, to initiate tickle games with the mother and sometimes with older siblings (Bard, Dunbar et al., 2014; van Lawick Goodall, 1968; Plooij, 1979). In the first 6 months, the primary social partner for infants is their mother (Goodall, 1967, 1986; Nishida, 2012). Mothers, however, can be more, or less gregarious in exposing their infants to potential future social partners. Although there are individual differences, on average, mothers with sons spend more time with both kin and nonkin, including more time with adult males, than do mothers with daughters (Murray et al., 2014). Infant chimpanzees, in the wild, play on their own, up to 20% of the time at 1 to 1.5 years of age, and engage in social play, with peak levels at ~15% for males when they are 2 to 2.5 years, and at peak levels at 20% for females when they are 3 to 3.5 years old (Lonsdorf et al., 2014). In a captive setting, 12- to 15-month-old infants played during 55% of observation time and spent only 34% of that time in social play (Ross, Bard, and Matsuzawa, 2014). Tickle play was not observed with peers, but only between infants and their mothers (and other older individuals). Mothers monitor their infants’ interactions with others and can rush to pick them up at the first sign of the infant becoming distressed. Older play partners engage in “self-handicapping” behaviors, such as laying supine, or lowering the intensity of play, when they engage with infants in play, thereby increasing the chance that the infant will play with them and lowering the likelihood that the mother will intervene (Frohlich, Wittig, and Pika, 2016b). In the second half year of life, infants may initiate social interactions with others by approaching them with vocal greetings. Nishida (2012) argued that infants first learn the appropriate greetings by imitating their mothers when they encounter others. Imitation of greetings, in this case, is a type of co-action, which is easy as the infant is riding on the mother’s belly which moves as the mother utters her vocal greeting. Knowing whom to greet may be accomplished when the infant rides on the mother’s back, as it is easy for the infant to see whom the mother greets. Infant chimpanzees learn a great deal of social communicative signals in the first two years of life. Communicative signals constitute all the ways that social partners negotiate social interactions. Some 88

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might label these communicative signals the natural “language” of chimpanzees. Chimpanzee infants may learn communicative signals through co-constructed interactions (Bard, Dunbar et al., 2014), in social negotiations (Frohlich et al., 2016a, 2016b), or mutual shaping (King and Shanker, 2003), although there is continued discussion about developmental processes (Call and Tomasello, 2007) and the role of genetics (Hobaiter and Byrne, 2011). Because young chimpanzee infants interact primarily with their mother (in the wild and some captive settings) or with a caregiver (in some captive settings), the caregiver plays an important role in communicative learning. Infants might learn greeting vocalizations by uttering greetings at the same time, with the same intensity as the mother, when she directs greetings to a particular individual (Nishida, 2012). Grooming gestures can be learned as early as the first year of life in a captive setting (Bard, Dunbar et al., 2014), but typically are seen in the 2- to 3-year-old wild chimpanzee. The grooming hand clasp, observed originally at Mahale, was observed in older infants/young juveniles (at least 4 to 6 years of age), and sometimes appears to be molded or scaffolded by the mother (Nakamura and Nishida, 2013; Nishida, 2012; Wood, Bruner, and Ross, 1976). This social custom, more accurately called high-arm grooming, occurs in many, but not all wild communities, and can take many forms, including palm-to-palm grasping, wrist-to-wrist, and others (Wrangham et al., 2016). The mother has a major influence on the form learned by her offspring. The form used by adult chimpanzees does not conform to that used by the social group, but rather individuals retain the form they learned with their mothers (Wrangham et al., 2016). The sharing of food is a negotiated event that involves communicative signals (Bard, Dunbar et al., 2014) and occurs regularly between infants and caregivers in chimpanzees (Goodall, 1986) and in orangutans (Bard, 1992: Jaeggi, van Noordwijk, and van Schaik, 2008). Mothers typically allow young infants, around 4 or 5 months, to take some food from her mouth or hand, but by 9 to 12 months, infants typically use communicative gestures to request the sharing of food (Bard, Dunbar et al., 2014; Plooij, 1984; van Lawick Goodall, 1968). It appears that chimpanzee mothers selectively share the more difficult to process or difficult to obtain foods as the infant matures (Nishida, 2012; Silk, 1978, 1979). Food sharing between mother and infant typically ends when the infant transitions to juvenile status, around six or seven years of age. The same food begging gestures observed in infants, however, are used by older individuals to request the sharing of meat from adult males after a hunt (Boesch, 2012; Goodall, 1986; Nishida, 2012). Data from a large sample of wild chimpanzees (Lonsdorf et al., 2014) show that infant chimpanzees spend between 2% and 4% of their time nursing, approximately 1.5 to 2 minutes per hour (Nishida, 2012). Although the level of nursing does not change substantially throughout the infancy period, eating solid food increases from ~5% at 6 to 12 months, to 20% of the time from 1.5 to 2.5 years, ~33% from 2.5 to 4.5 years, and almost 50% at 4.5 to 5 years (Lonsdorf et al., 2014). In captive settings, however, suckling changes with age, with approximately 3%–17% of time spent nursing in the first 4 months of life (Mizuno et al., 2006), and suckling tending to stop altogether within 2 to 4 years, much earlier than in the wild (Goodall, 1986; Nicolson, 1987; Nishida, 2012). From 9 months, wild and captive infant chimpanzees request food from their mother, typically with a cupped hand, held underneath the mother’s chin (Bard, Dunbar et al., 2014; Plooij, 1978, 1984; van Lawick-Goodall,1968). Ueno and Matsuzawa (2004) found, in an experimental setting consisting of giving the chimpanzee mother food items, that these captive mothers sometimes spontaneously offered food to their young infants. However, these offers were often the unpalatable parts of the food items. Nishida (2012) reported that mother chimpanzees at Mahale never spontaneously offer food to infants, but that infants, through their own initiative, develop their mother’s food repertoire based on eating those food items being eaten by their mothers, through both “food retrieval” and successful food sharing (Goodall, 1986). From 2 to 5 years there is much to be learned about food, food processing, traveling, and hunting. Chimpanzee mothers monitor what infants eat and prevent them from manipulating or eating undesirable objects, in an example of what Nishida (2012) labels “education by discouragement”. Mothers 89

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serve as models for older infants to learn termite fishing (Goodall, 1986), ant fishing (Nishida, 2012), tool manufacture (Wright, 1972), plant foraging (McGrew, 1974, 1977), food processing (Lefebvre, 1985), and locomotory behaviors (Bard, 1993, 1995b). Many food processing skills are thought to be learned via “education by master-apprenticeship” as Matsuzawa et al. (2001) described for nut cracking. Lonsdorf (2005, 2006) found that the amount of time mothers spend termite fishing alone with her offspring predicts the number of critical elements acquired by the offspring, but only at 2.5 years. Proficiency in termite fishing requires mastering five critical elements: identifying termite holes, manipulating tools, modifying tool material, inserting tools into the hole, and the crucial element of extracting termites. No maternal characteristics predicted the offsprings’ overall proficiency in termite fishing (Lonsdorf, 2006). Daughters were more proficient than sons, and daughters spent more time watching others engage in termite fishing, and more closely matched maternal termite fishing techniques (selecting similar lengths of tool; Lonsdorf, 2005, 2006). Lonsdorf (2005) suggested that female offspring actually imitate some aspects of maternal termite fishing, but all offspring use goal emulation (a social learning process involving copying the end result, but not imitating the means) to develop understanding that using a tool achieves acquiring termites. The five critical elements were mastered at different ages: identifying termite holes was mastered around 1.5 years of age, manipulating tools began around 2.5 years, modifying tool material began around 3.5 years, inserting tools into the hole was mastered by all offspring by 4.5 years, and extracting termites was not mastered by all offspring until 5.5 years of age. However, there is a great deal of individual trial-and-error learning involved in mastering the final critical element of extracting termites (Lonsdorf, 2006). There is an increasing amount of evidence that Great Ape mothers actively instruct their infants under some, perhaps limited circumstances. Boesch (1991) argued that chimpanzee mothers “take an active part in the apprenticeship of their female offspring” (Boesch and Boesch, 1981, p. 592) to crack nuts with a hammer tool. Chimpanzee mothers facilitate arboreal locomotory behavior by “bridging” gaps between trees allowing the young infant to cross the gap on her body and allowing older infants to cross the gap on branches that she holds close together (Goodall, 1986). It is likely that adult male chimpanzees play a teaching role in the apprenticeship of male offspring in cooperative hunting (Boesch and Boesch, 1989, 2000). Much of the teaching found in small scale huntergatherer communities with human infants involves demonstrations, giving infants tasks to perform, scaffolding, redirecting, and providing positive or negative feedback (totaling over 10 times per hour), rather than verbal instruction (less than once per hour) or ostensive cues that provide information to infants (four times per hour; Hewlett and Roulette, 2016). Chimpanzee males are remarkably tolerant when infants attempt to interfere with mating, and males may reassure uneasy infants with a touch. The tolerance of infant behavior appears to continue as long as the infant retains the “tail tuff ”, long white hairs at the base of the spine (Goodall, 1986). Chimpanzee males in captivity engage in play with infants showing there is a capability (Bingham, 1927; Taub and Redican, 1984). The difference between gorilla and chimpanzee fathers may be that paternity in chimpanzees is usually not known either by observers or apparently by the chimpanzees (Gagneux, Woodruff, and Boesch, 1997; Goodall, 1986), but in gorilla harems paternity is certain. Male orangutans rarely engage in interactions with infants. Clark (1977, p. 235) described the 2-year gradual weaning process in 2- to 4-year-old chimpanzees at Gombe as a period when infants may “display many elements of depression”. It begins with mothers preventing access to the breast by holding the infant away, pushing the infant away, or physically blocking access with an arm or knee pressed firmly against their own chest. Mothers often distract the infant with play or grooming when they attempt to suckle, and mothers may move away from the infant as the infant approaches to suckle. It was extremely rare for any mother to exhibit aggressive behavior in relation to weaning her infant. Similar tactics were observed in chimpanzee mothers in a captive setting (Horvat and Kraemer, 1982). In response to these tactics infants whimper and become physically more intrusive in their attempt to access the nipple. As the infant grows 90

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older and weaning is more strictly enforced, temper tantrums ensue at Gombe but not in the captive setting. But as weaning progresses elements of depressive response are seen in the wild, including decrease in play, loss of appetite, huddled posture, and resumption of infantile behavior with the mother including ventral riding and increased contact (Yoshida, Norikoshi, and Kitahara, 1991). In the wild, all 4- to 5-year-old infants exhibit distress when the mother’s milk is no longer available and within months make no further attempts to suckle. Clark (1977) noted that all mothers appear “remarkably tolerant and gentle with the infants during the weaning period” (p. 252) and increased their attentiveness to the infant through grooming and waiting for them in traveling. Infants, however, appear depressed through the period of the birth of younger siblings. Their depression is exhibited in lethargic movements, lack of positive emotions, and sometimes decreased appetite and moderate weight loss. Although weaning occurs at an earlier age in captive chimpanzees (~2 to 4 years of age compared to 4 to 6 years in the wild), captive chimpanzees appear less affected, as there is less distress related to the cessation of suckling and no signs of depression (Horvat and Kraemer, 1982), probably due to the abundant availability of food in captive settings.

Parenting Infant Orangutans Orangutan infants, younger than 2 years, are less frequently out of contact with the mother compared with chimpanzee infants (Figure 3.3; Bard, 1993, 1995b). Mothers may tolerate relatively close proximity with other mothers in order to allow their infants to play, but fewer peers are available for socialization in orangutans (compared with chimpanzees) during the entire infancy period (Bard, personal observation). In the wild food context, mothers respond positively to their infants’ goaldirected behaviors most often when directed toward herself (rather than directed to the food), and

Figure 3.3 Orangutan mother and 9-month-old infant, Pongo pygmaeus, at Camp Leakey, in the Tanjung Puting National Park, Kalimantan Tengah, Indonesia. Source: Photo credit: Kim A. Bard.

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when infants request food with a gesture directed toward the mother, around 3.5 years of age (Bard, 1992; Jaeggi et al., 2008). In captive settings, gestures appear to emerge at earlier ages, and orangutans (compared to chimpanzees, bonobos, and gorillas) gesture more often in the food context than other contexts (Schneider, Call, and Liebal, 2012). Mothers provide support for infants developing foraging skills. In the wild, it is likely that the initial maternal influence for infants is akin to stimulus enhancement, supporting infant’s learning of what to eat (co-feeding in the same patch occurred during 90% of bouts; Jaeggi et al., 2010). Infants watched mothers while they extracted embedded foods, providing observational learning experiences about how to process foods. Infants were more successful in food sharing if they timed their solicitations for when the mother was finished processing the food and had already taken a bite (Bard, 1992). Additionally, mothers allowed infants to scrounge discarded and partially processed pieces ( Jaeggi et al., 2010; Russon, 2006). Analyzing the complexity of infant’s object manipulations, Bard (1995b) found that more complex manipulations were used in locomotion compared with foraging. More direct maternal assistance was found in locomotor, compared to the foraging, contexts in wild orangutans. Basic assistance is provided by mother orangutans in arboreal traveling, by the infant clinging to the mother while she travels 85% of time (in contrast to 50% for juveniles; Bard, 1995b). For infant orangutans, a large proportion of the nonclinging traveling events consisted of maternal assistance provided to infants in crossing a gap between trees. Infants climbed across on the mother’s body while she held two trees to bridge a gap or rode in the tree that the mother swayed to cross a gap (Bard, 1995b). Bard (1995b) suggested that these maternal behaviors could be considered a form of tuition or scaffolding for young infants, as older infants and juveniles appeared to contribute their weight to maternal swayings, prior to learning to sway trees independently. Orangutan infants are weaned between 4 and 8 years of age (Bard, 1993; Galdikas, 1979), but can continue suckling until the next offspring is born (van Noordwijk et al., 2013).

Parenting Infant Gorillas The gorilla in early infancy is motorically more advanced than chimpanzees, chewing food items in the first 2 months of life, and clinging to the mother’s hair without support by 2 months, and reaching for objects earlier. Mothers spend time grooming the infant and begin to rebuff suckling attempts before infants’ first birthdays. Gorilla infants play very little with their mothers or with silverbacks, even in captivity, but choose to play alone primarily in the first year, and with same-aged peers, preferring male partners through the next 2 years (Maestripieri and Ross, 2004). Mothers do not seem to encourage any social activities of their infants, although they occasionally discourage them, especially when infants are young (Maestripieri and Ross, 2004). One study found that communicative competence was scaffolded for infant gorillas by all older social partners (Luef and Liebal, 2012). Juveniles, adolescents, and adult gorillas modified their gestural communication when directed to infants, through using more repetition and higher rates of sequences with a tactile component, in a type of communicative “motherese” (Luef and Liebal, 2012) or scaffolding (Wood et al., 1976). Mothers share food when infants request it with communicative gestures (Maestripieri, Ross, and Megna, 2002). In captive settings, lowland gorilla mothers encourage the development of infant locomotor skills in a manner similar to that of chimpanzees, and infants show interest in maternal activities, especially food processing, and appear to “create opportunities for their own social learning” (Maestripieri et al., 2002, p. 225; Whiten, 1999). By 2 years of age, mountain gorilla infants travel primarily independently but they retain the white tail tuff that indicates their infant status through part of the third year (Fossey, 1979). Male gorillas undoubtedly play an important role as protector for infant gorillas, as paternity is usually known (Stewart, 2001). One function of adult males may be as a “social magnet”, being the focal point for the gathering of many infants and juveniles (Figure 4.5 in Bard, 2002; Stewart, 2001). 92

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In some wild settings, gorilla infants and their fathers play frequently, in contrast to chimpanzees (Figure 3.4), but in other captive settings, infant play is almost exclusive with peers, although male infants play more than female (Maestripieri and Ross, 2004). In addition, gorilla fathers carry some young infants (Tilford and Nadler, 1978). Some gorilla infants spend more time near or interacting with their father than with their mother (Fossey, 1979, 1983; Harcourt, 1979). “Gorilla males often groom, cuddle, and nest with their 3- and 4-year old offspring” (Whitten, 1987, p. 346). The father also monitors play between infants and stops it before it becomes too rough (Fossey, 1979). Gorilla fathers, through these early interactions, appear to form a particularly close relationship with at least one male infant. This preferred infant will grow up to remain in the father’s group (Harcourt and Stewart, 1981; Tilford and Nadler, 1978).

Parenting Infant Gibbons and Siamangs: Small Ape Infants Infancy in the small apes lasts 12 to 19 months (Chivers, 1976; Fox, 1977). When the gibbon mother rests, 6-week-old infants begin to move a little distance from her. Infant gibbons in the first weeks of life may eat some solid food and engage in locomotor play (Carpenter, 1964), but continue to nurse for 2 years (Figure 3.5). One of the most striking behaviors exhibited by gibbon parents is their vocal duet, songs are given morning and evening. “Infants often squeal during a mother’s great call” (Leighton, 1987, p. 140). As older infants travel independently, they sometimes are unable to

Figure 3.4 Among the great apes, gorilla (Gorilla gorilla) fathers spend the most time interacting with infants. Source: Photo retrieved from iStock.com/omersukrugoksu.

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Figure 3.5 A white-handed gibbon mother, Hylobates lar, cradles her 8-month-old infant while she eats figs in the Khao Yai National Park, Thailand. The group’s unrelated adolescent male sits nearby. Source: Photo credit: Ulrich H. Reichard.

cross gaps between trees, and they “cry” until the mother retrieves them (Carpenter, 1964). Mother siamangs do almost all of the carrying of infants younger than 8 months. In the second year of life, fathers carry gibbon and siamang infants (up to 20% of the time) and spend some small amounts of time grooming and playing with them (Lappan, 2008). Paternal care in the small apes can be as high as 78% of the day (Whitten, 1987); the infant returns to the mother to nurse and to sleep at night (Alberts, 1987). For the siamangs, living in the Way Canguk Research Area in Sumatra, male care replaced female care, and the amount of care by males differed as a function of whether the group was socially monogamous or not (Lappan, 2008). These siamang infants began to travel independently around 1 year of age, were weaned between 10 and 15 months of age, and spent most of their time traveling independently by 21 months of age (suggesting an early emergence of the juvenile period; Lappan, 2008). Older siamang infants still rely on adults to facilitate their travel under difficult traveling conditions—“across gaps, at high speeds, or when fatigued” (p. 1311).

Parenting Juvenile Chimpanzees and Apes In chimpanzees, the end of infancy is indicated by cessation of nursing (weaning) and the disappearance of the white tail tuft (Nishida, 2012; van Lawick Goodall, 1968). The juvenile period is distinguished by longer times spent further away from the parent(s). Attention turns from mothers to peers in the juvenile period (Horvat and Kraemer, 1981). Maternal responsibilities in terms of providing milk and transportation diminish or cease, and responsibility for offspring to become fully independent increases. It is when offspring reach this period of semi-independence that chimpanzee 94

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mothers facilitate learning of travel techniques (Goodall, 1986), of food processing (McGrew, 1977; including tool use; Boesch, 1991), and of socialization. Puberty marks the end of the juvenile period. After juvenile chimpanzees are weaned, they remain in close association with their mothers, traveling with the mother but not being carried by her. Mothers are still the primary grooming partners for juvenile chimpanzees, but daughters more often groom family members compared with sons (Preuschoft, Chivers, Brockelman, and Creel, 1984). Juvenile sons and daughters play, groom, and carry younger infants who may or may not be siblings (Nishida, 1983). All juveniles exhibit submissive behaviors to adult males, for example presenting their hindquarters and pant grunting. Occasionally juveniles display and attack adolescent females, but this level of aggression only occurs when the mother joins to support her son or daughter (Pusey, 1990). During the juvenile period, chimpanzees, gorillas, and orangutans eat the full range of food items found in the diet of adults. The mother is the main source of information about what to eat, how to eat, and when to eat different foods, and for chimpanzees this information includes learning about tool use for termite fishing and nutcracking (Boesch, 2012; Lonsdorf, 2006). Many of these skills are exhibited during the late infancy period, but adult-like success is not attained until the juvenile or even adolescent periods in chimpanzees and orangutans (Russon, 2006). Gorilla juveniles receive most grooming from their mothers (Watts and Pusey, 1993), but the rate of grooming appears to be much less than found in chimpanzees. Similarly, there are few bouts of grooming in mother-offspring orangutans (Galdikas, 1995). Siamang juveniles spend most of their time traveling independently by 21 months of age (Lappan, 2008), but remain with their family group. Juveniles (2 to 4 years of age) begin to receive aggressive behaviors from their parents: typically, mothers harass daughters and fathers harass sons (Preuschoft et al., 1984). Fights ensue most often over access to food (Leighton, 1987). Juvenile gibbons and siamangs may join in singing the duet with their parents. The song tends to be sex-appropriate but imperfect (Leighton, 1987). During the juvenile period, mother gibbons initiate co-singing episodes with their daughters, but later, adolescents begin co-singing episodes (Koda et al., 2013).

Parenting Adolescent Chimpanzees and Apes The adolescent period begins at puberty and ends at the time when effective reproduction occurs (Walters, 1987). The beginning of adolescence, signaled in female chimpanzees with small sexual swellings, occurs around eight to nine years of age in wild chimpanzees (Nishida, 1988; Watts and Pusey, 1993), and orangutans (Galdikas, 1979) and 5.5 years in the laboratory (Sarah Phythyon, personal communication, 1993). Menarche and full sexual swellings occur when a chimpanzee is 11 to 12 years of age in the wild and 8 to 10 years in the laboratory. The adolescent period includes the time when offspring travel independently throughout days and nights, sometimes engaging in sexual activity and reproductive behavior, but the individual is neither fully socially or physically adult. Adolescence lasts from the age of 9 to 14 years in wild female chimpanzees (Nishida, 1988), until 15 years in male chimpanzees (Nishida, 1988), 16 years in gorillas (Watts and Pusey, 1993), and until 21 years in male orangutans (Galdikas, 1979). Mothers now have a more general influence on their offspring. For example, maternal rank significantly influences the age of their daughter’s first full sexual swelling. There is as much as a 4-year difference between the ages for daughters of high versus low ranking mothers (Pusey, Williams, and Goodall, 1997). Some physical changes that characterize the adult status include coat color (e.g., silver-colored hair on the backs in the dominant male gorilla), secondary sexual characteristics (e.g., cheek flanges in male orangutans), and attainment of full growth (e.g., canines, testes, and general body size). At adolescence, there are striking differences between chimpanzee daughters’ and sons’ behavior in whom they groom, and with whom they spend their time. Sons are more often in the company of adult males than daughters. Mothers provide support to their daughters in agonistic encounters, 95

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whereas sons solicit and receive support from older brothers. The behavior of adolescent males is molded by adult males who touch to quiet adolescent males during boundary patrols (Pusey, 1990) and guide adolescent males in assuming complementary and cooperative roles while hunting colobus monkeys (Boesch and Boesch, 1989, 2000). It is during mid-adolescence, when female chimpanzees exhibit adult-sized, sexual swellings that daughters may leave their mothers by joining a new group, and then are solicited and protected by adult males (Pusey, 1990). Adolescent orangutans (7 to 8 years to 10 to 15 years: Wich et al., 2004) are relatively sociable, traveling in mixed-gender groups (Galdikas, 1995). Females preferentially consort with adult males but continue to spend some time with mothers as well, before settling into a home range than will overlap, or be nearby the mother’s (Bard, 1995b; Galdikas, 1979; Watts and Pusey, 1993). During adolescence in the small apes (6 to 8 years in gibbons: Koda et al., 2013), fighting occurs over breeding access and adolescents leave (or may be evicted) from the family. Male adolescent gibbons appear to be inhibited from singing with their parents but females emit great calls simultaneously with their mother. The calls of the daughter are acoustically similar to those of the mother, and it appears that the mother adjusts her calls when her daughter sings along (Koda et al., 2013). Thus, mother gibbons have flexibility in their calls, and they play an important role in the “acoustic learning” of their daughters (Koda et al., 2013). Call rates of daughters decrease during the adolescent period with their increasing independence and become more adult-like in vocal structure. The call rates of daughters predict when they leave the family group to begin their own family (Koda et al., 2013). Fathers and adolescent sons may form a coalition in territorial defense against intruders. Fathers may facilitate the process of their sons establishing their own territory, either by joining the sons to usurp a neighbor’s territory or by expanding the home territory and then leaving the son in the new area (Leighton, 1987). Young adult male gibbons sing solo apparently to attract unmated females, but unmated females rarely sing alone (Leighton, 1987).

Summary Apes spend 10 to 18 years in subadult states (Table 3.1). Apes both require longer periods of parental care, and benefit from parenting for the longest periods of time. Among nonhuman primates, parenting in the apes most closely approximates that seen in humans, as parents nurture the development of many social, communicative, and motor skills in their offspring.

Old World Monkeys Parenting Newborn Old World Monkeys Macaques (e.g., rhesus, cynomologus, pigtails, and bonnets) have a strong crawling and grasping reflex that may aid in the birth process (Rosenblum, 1971; Tinklepaugh and Hartman, 1932). Their “strong righting reflexes and negative geotropism . . . function to produce the proper orientation” to emerge from the birth canal (Rosenblum, 1971, p. 324). Mothers must provide a supportive base when expelling the newborn, especially important when the mother is in an arboreal environment, or else the infant may not initially get a grasp of the mother’s hair (Rosenblum, 1971; Timmermans, 1992). Little attention is paid to the newborn in many species, but in some, particularly those with allomaternal care, newborns are of great interest to other adult females, for example in vervet monkeys (Fairbanks, 1990; Lancaster, 1971) and to large juvenile females, for example in blue monkeys (Forster and Cords, 2005). The placenta is eaten by some mothers during the initial birthing period. This period is followed by a period of intense grooming of the infant. Mothers may gaze at their newborn infants and infants may gaze at their mother’s face (Higley and Suomi, 1986). Newborn macaques, through reflexive behaviors, suckle without maternal aid. Nipple contact is maintained over 80% of 96

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the time during the first month of life in captive rhesus macaques (Higley and Suomi, 1986), and over 50% of the time in wild blue monkeys (Föster and Cords, 2002), both are in striking contrast to the 20% nipple contact of chimpanzees. New findings demonstrate that there is a short time window, or maybe a sensitive period (Bornstein, 1989), during which rhesus monkey newborns imitate lip smacking and tongue protrusion (Ferrari et al., 2006). Mother and newborn rhesus monkeys can show a great deal of reciprocal affectionate and affiliative face-to-face behavior, including mutual gaze and lip smacking (Ferrari, Paukner, Ionica, and Suomi, 2009). Paternal behaviors toward newborns varies by species but generally ranges within the indifferent category. Mothers with newborns may stay in close proximity to adult males in baboons (Papio anubis; Hrdy, 1976). One-week-old Barbary macaques are carried by adult males as well as by juvenile and subadult males (Deag and Crook, 1971), and there is a report of the dominant male holding an infant four times on the day it was born (Burton, 1972, cited in Hrdy, 1976).

Parenting Infant Old World Monkeys Most macaques remain in infancy for only 1 to 1.5 years. Baboon infants have black hair and pink skin in contrast to the light hair and black skin of adults and have a new sibling when 1.5 to 2 years of age, so are weaned at 1 to 1.5 years of age (Altmann, 1980; Strum, 1987). Macaque infants, and blue monkey infants, mature quickly and begin to crawl and climb, respectively, within a few days after birth (Förster and Cords, 2002). In the first few weeks, mother blue monkeys restrict their infants from moving out of contact. When these infants are older, mothers move away more, although they monitor the infant and remain ready to retrieve and protect the infant (Figure 3.6; Förster and Cords, 2002). In contrast, mothers of some terrestrial species encourage infant locomotion (in pigtails; Bolwig, 1980; Hinde and Simpson, 1975; Ransom and Rowell, 1972; in macaques; Ehardt and Blount,1984; Ferrari et al., 2009 [supplemental material]; Maestripieri, 1996). Macaque infants typically engage in independent excursions in the third and fourth weeks of life. The mother provides a “secure base” from which the infant travels (Harlow and Harlow, 1965) and a “safe haven” of comfort to return to when distressed (Maestripieri and Roney, 2006). “Mothers now become psychologically more than physically important for their infants” (Higley and Suomi, 1986, p. 160). However, during this time mothers are providing kinesthetic and vestibular stimulation through grooming and physical contact while traveling, and contingent responsive stimulation in their social interactions (Ferrari et al., 2009). Mothers respond to infant cries and seem to respond selectively, or at least differentially, in positive, negative, or neutral manners to all infant social communicative signals. It is this type of selective and contingent social responsiveness that mothers, in particular, provide to infants that peers do not. However, it is rare that macaque mothers engage in extended play with their infants (Suomi, 1979). Play in macaques is primarily a peer activity. Paternal behavior in Old World monkeys varies considerably among species. Mothers stay close to adult males in baboon species, and male langurs may respond to infants in distress with protection and rescue (Hrdy, 1976). Young mangabeys spend most of their time with an adult male rather than their mothers. Intensive caregiving by males is found in one species of Old World Monkeys, the Barbary macaque. Adult males “groom, nuzzle, and mouth infants, lick and smell them, manipulate their genitalia, and teeth chatter at them” (Whitten, 1987, p. 345), engaging in interactions analogous to those of mothers (Taub, 1984). Males may temporarily foster an infant or permanently adopt an orphaned infant (anubis baboon: DeVore, 1963; Japanese macaque: Itani, 1959; or hamadryas baboon: Kummer, 1967). In fact, Kummer (1968) reported that motherless infant hamadryas are invariably adopted by young adult males. But males in each of these species, and in langurs and vervets, also use infants as an “agonistic buffer”, which puts the infant at risk for injury or death. Males carry an infant to or near another male: the presence of the infant inhibits aggression and the males interact 97

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Figure 3.6 Mother and 6-month-old infant blue monkey, Cercopithecus mitis stuhlmanni, in the Kakamega Forest, western Kenya. Source: Photo credit: Marina Cords.

in a less tense environment. Cases of infanticide in langurs and rhesus by adult males typically involve nonfathers and appear to be cases whereby the adult male is maximizing his inclusive fitness (Trivers, 1974), whereas cases of infant care, play, and other affiliative interactions are by dominant males who are likely fathers (Hrdy, 1976). Infants are used by adult males as agonistic buffers regardless of genetic relatedness (Whitten, 1987). Infants in some Old World monkey species experience considerable care from nonmothers (up to 10% of the time). Nonmaternal handling of infants is common in blue monkeys, as well as vervets, patas, and langurs. In blue monkeys, for example, during the first months of life, older juvenile females attempt to kidnap infants, but by the time they are 3 to 4 months of age, allomothers act much like biological mothers, providing a secure base and a safe haven, and protecting infants from aggression and providing comfort when distressed (Förster and Cords, 2005). Infant blue monkeys receive more grooming from nonmothers than from their mother. Maternal “style” is the term used to differentiate both species differences and individual differences in maternal behaviors toward older infants that reflect the balance between permissive and restrictive rearing (Hinde and Simpson, 1975). Maternal style in early infancy is reflected by how 98

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contact and proximity are regulated and how much contact the infant is allowed with others. In rhesus and pigtail macaques, and baboon species, none may touch the newborn infant for many weeks. In contrast, colobus and langur mothers may allow others to carry away their newborns (Bennett, 1988; Fimbel, 1992). Bonnet macaque mothers allow their infants to interact in a limited fashion with others in the social group but not immediately after birth. It is common, however, to allow older siblings limited access to infants. Mothers exhibit consistent rejection rates with each of their offspring and across the development of each offspring. Moreover, there is consistency in maternal style across generations. So, it appears conclusive that maternal style is a characteristic of the mother, and not the mother-infant bond, in rhesus (Berman, 1990) and vervet monkeys (Fairbanks, 1989). Maternal “style” is also apparent at weaning. Frequency of rejection and punishment have been documented to be stable maternal characteristics in rhesus monkeys (Berman, 1990). Rejection and punishment as a weaning style clearly differentiate species; rhesus have high rejection rates compared with bonnets for instance (Rosenblum, 1971). By the end of the first year of life, weaning is complete in Old World monkeys. Baboon mothers hit, push, grab, and bite at infants. Individual differences between mothers occur, but by the time that infants are 5 months of age they have experienced maternal aggression at least once (Altmann, 1980). Weaning occurs between 4 and 6 months. Weaning begins somewhat later in Hanuman langurs, and different responses are noted from male and female offspring, but all mothers are harsh, punitive, or indifferent (Rajpurohit and Mahnot, 1991). Baboon mothers encourage independent locomotor behavior when infants are 7 months of age. The mother may descend from sleeping trees without carrying the infant. Infants “protest” with whimpers. Sometimes mothers return halfway up the tree still requiring that the infant descend part of the way independently. Mothers always monitor the tree, even if they do not facilitate any of the travel, until the infant travels down. Typically, the infant immediately runs to the mother and nurses. By the end of 1 month of these “lessons”, the 8- or 9-month-old infants descend from the sleeping tree independently. Competing theories have suggested either that punishment/rejection facilitates, if not causes, independence (Hansen, 1966; Hinde and Spencer-Booth, 1967), or that high levels of punishment/ rejection cause increased dependence and delays in the attainment of independence (Kaufman and Rosenblum, 1969; Rosenblum and Harlow, 1963). In experiments on cross-fostered rhesus monkeys, Suomi (1987) evaluated the independent contributions of inherited reactivity, foster caregiver reactivity, and foster caregiver style on infant reactivity. Foster caregiving “style” is a better index of infants’ behavioral reactivity than inherited temperament, or caregiver temperament, under stable environmental conditions. However, when presented with environmental challenges, such as a brief separation from the caregiver, infants’ reactivity was best predicted by inherited reactivity. When initially returned to the foster mother, then the caregivers’ reactivity best predicted the infants’ behavior (Suomi, 1987).

Parenting Juvenile Old World Monkeys In rhesus macaques, baboons, and Japanese macaques, the age of menarche is 5.5 years on the average but can be influenced by hierarchical dominance status (Pereira and Fairbanks, 1993). Male testes descend in baboons around 5.5 years of age (Altmann, Altmann, Hausfater, and McCuskey, 1977). Infants and juvenile baboons are given the preferential center location during group travel. Mother macaques allow juvenile daughters to handle infant siblings and juvenile sons to play with infant siblings. Mothers also allow unrelated juvenile females access to infants. Sometimes mothers are intimidated by juveniles of high-ranking matrilines and their infants are kidnapped (Hrdy, 1976; Maestripieri, 1994). In agonistic encounters the entire matriline will support their kin. Juveniles begin to acquire ranks similar to their mothers and exercise dominance toward all females that are subordinate to their mother. 99

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In Hamadryas baboons, adult males form “special relationships” with juvenile females. These begin as friendships but grow to be consortships. Juvenile males may have strong affiliative bonds with an adult male or with male peers, which develop into coalitions later in life (Kummer, 1967, 1968; Walters, 1987).

Parenting Adolescent Old World Monkeys There is a great deal of variance in the age of adolescence in Old World Monkeys. In baboons, full adult size is reached in females around 7 years of age, and full secondary sexual characteristics are developed by 10 years in males (Altmann et al., 1977). In vervets, breeding is seen at 3 years, but females are not adult in size until 4 years and males not before 5 years (Fairbanks, 1990). Rhesus monkeys are in early adolescence between 2.5 and 4.5 years (Bernstein, Judge, and Ruehlmann, 1993) but may remain in adolescence for 4 years or more (Bernstein et al., 1991). In rhesus, the males leave the birth group during adolescence. Few specifics on parenting are known to account for the large differences between male and female behavior. Female rhesus spend significantly more time grooming, and males spend more time with male peers. The result of these differences in behavior is a loosening of the sons’ bonds with mother and sisters, and a strengthening of the daughters’ bonds with mother and sisters. The role played by the mother during the process is unspecified. “Male macaques and vervets frequently emigrate in the company of brothers or natal group peers” (Walters, 1987, p. 365). In hamadryas baboons, the alpha male acts aggressively toward subadult males, eventually evicting them from the natal group (Caine, 1986). It is the adolescent females in red colobus groups, however, that migrate as adolescents (Caine, 1986).

Summary Old World monkeys spend 5 to 8 years as subadults. Parenting in Old World monkeys is less about nurturing skills (a characteristic of parenting in apes) and more about exerting an influence on their path of development. This influence takes many forms that differ across species, from adherence with strict dominance hierarchies to experiencing extensive alloparental interactions. There is good evidence in many Old World monkey species, that parents continue to have an influence on their offspring, even after they become adult.

New World Monkeys Parenting Newborn New World Monkeys New World monkeys are arboreal and forest dwelling. The newborn period has not been defined for New World monkeys but is likely to consist of only the first day or so after birth. Care of newborns is different for the species that are pair-bonded (e.g., marmosets, tamarins, titi monkeys) and for the species that live in large social groups (e.g., squirrel monkeys, howler monkeys, and capuchins). Newborn capuchin monkeys can cling to the mother unaided, but the mother supports the infant while moving from ventrum to her back (Fragaszy, 1990). Squirrel monkey newborns can move independently from the ventral position used in nursing, to the dorsal position used in travel. Early field studies of newborn howlers documented that mothers regularly restrained and pulled the infants as they continually climbed up the mother’s ventrum (Carpenter, 1964). Although newborn New World Monkeys have the physical strength to support their weight with their tails, it appears that newborns are uncoordinated with their tails (Carpenter, 1964: Fragaszy and Bard, 1997). From the day of birth, squirrel monkey infants respond visually and vocally to the communication of others. Adult females and juveniles are allowed to touch newborn squirrel monkeys but many 100

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mothers avoid adult males or prevent them from touching the newborns (Hopf, 1967). Adults vocalize “caregiver calls” to newborns, and newborns vocalize responsively (Biben, 1994). These vocal exchanges occur when infants and adults are engaged in mutual gaze. It is noteworthy that these communicative exchanges are not between infant and mother but rather between infants and other adult members of the group. Marmosets, tamarins, and titi monkeys are monogamous species, that typically give birth to twins (80% for marmosets and tamarins); triplets are as common as single births. In marmosets and cebus, mothers are primarily responsible for carrying, and totally responsible for feeding newborns (Box, 1977; Rothe, Darms, Koenig, Radespiel, and Juenemann, 1993; Wamboldt, Gelhard, and Insel, 1988). Specialized behavior has developed to cope with twin births (fraternal twinning is typical: Tardif, Carson, and Gangaware, 1992), specifically “helpers” to carry the infants which includes fathers. Experienced fathers are highly motivated to pick up infants, even if the infant is not their own and are hormonally responsive to the scent of their infants (Ziegler, Prudom, and Zahed, 2009). The amount of maternal care relative to paternal care varies among the species as does the amount of care by nonparents, however, in all these species there are substantial amounts of infant care by individuals other than the mother (Goldizen, 1987). Helpers become an important factor after the newborn period. Systematic research indicates that helpers of specific age, gender, and experience levels participate in care of infants of different ages (Price, 1992). In marmosets, fathers are allowed to carry newborns (Ziegler et al., 2009). In titi monkeys, the mother and father work as a team from birth. From the first week of life, the father carries the infant more than 70% of the time (Mason and Mendoza, 1998).

Parenting Infant New World Monkeys The infancy period in many species of New World Monkeys is relatively short (approximately five months). Infant capuchins and howlers first break contact with their mother in the second month of life (Figure 3.7) and spend 50% of their time off the mother when they are 5 months of age (Fragaszy, 1990; Pavé, Kowalewski, Zunino, and Leigh, 2016). In wild settings, howler monkey infants begin eating solid food around five weeks of age and are weaned around nine months of age (Pavé et al., 2016). Infant capuchin monkeys explore their environment and spend much of the time off of their mother, directing visual attention to the activities of the mother (Fragaszy et al., 1991; O’Malley and Fedigan, 2005). Squirrel monkeys are weaned within the first 3 months of life (Biben,1994) as are capuchins (Wamboldt et al., 1988). Marmoset and tamarins, however, appear to be weaned around six months of age. Both adult and adolescent squirrel monkey females carry and play with infants, and mothers groom their infants regularly (Robinson and Janson, 1987). Cebus infants, 2 months old or older, are occasionally left with the dominant male who either huddles with them or is tolerant of their play (Robinson and Janson, 1987). Many primatologists emphasize the commonalties in infant care patterns within cooperatively breeding species of New World Monkeys, but “variation and flexibility emerged as major themes” when considering parenting in cooperatively breeding species, such as tamarins, marmosets, and tit monkeys (Snowden, 1996, p. 682). In some monogamous species, mothers have primary responsibility for infant care at birth. For these species, however, maternal cradling of newborns does not occur. In fact, New World monkey infants, even at birth, have sufficient strength and motor maturity to support their own weight and to maneuver to the nipple. However, the survival rate of infants born to first-time tamarin mothers is quite low (i.e., 10%, Snowden, 1996). This high mortality rate appears to be due to the first-time tamarin mother doing most of the carrying of her twins: experienced mothers typically carry their infants only 50% of the time during their first week of life. The infant is able to crawl ventrally to nurse and otherwise rides on the mother’s back. In some monogamous species, such as marmosets, fathers have primary responsibility for the infant from 101

Figure 3.7 Mother and nursing month-old infant capuchin, Cebus capucinus, in the Refugio de Vida Silvestre Curú, Costa Rica. Source: Photo credit: Mary Baker.

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shortly after birth (Figure 3.8). In titi and night monkeys, fathers carry the infant up to 90% of the time and the infant forms a strong attachment to the father (Spence-Aizenberg, DiFiore, and ­Fernandez-Duque, 2016; Wright, 1990). In these species, mothers only hold infants for nursing. Fathers, not mothers, groom, play, and share food with their infants. These observations of parental care in the wild mirror those reported from captive settings (Spence-Aizenberg et al., 2016). Infants transfer to other carriers for the majority of their time. Initially, the infant’s transfer is facilitated by the helper by adopting a different posture, “including extension of the arms toward the infant and direction of the infant’s crawling motions” (Tardif et al., 1992, p. 156). Infants can be actively rejected by mothers who have insufficient prior experience ( Johnson, Petto, and Sehgal, 1991; Tardif, Richter, and Carson, 1984), and these mothers show some fear and avoidance of the newborn presumably due to the lack of prior experience (Pryce, Abbott, Hodges, and Martin, 1988). Although deaths of newborns occur due to lack of sustenance, most early deaths appear to be due to falls (i.e., skull fractures found in autopsies of newborn squirrel monkeys; Hopf, 1981). Tamarin, marmoset, squirrel monkey, and capuchin mothers actively reject an infant by rubbing the infant off their body. It is for this reason that the presence of helpers is crucial, as they can collect and carry newborns, or even take the infant before the mother tries to remove it. Both male and female nonparents act as helpers with equal frequency in cotton-top tamarins, but which gender helps may be constrained by age. Female subadults carry more than male subadults, but as adults, males carry more than females. Very young infants are carried more often by adults compared with subadults, but subadults carry more than juveniles (Yamomato, Box, Albuquerque, and Arruda, 1996). In some species (red-bellied tamarins) younger, less experienced helpers are not allowed access to very young infants (Pryce et al., 1988). Weaning is accomplished by the eighth

Figure 3.8 Marmoset fathers (Callithrix jacchus) carry young offspring on their back. The mother sits nearby. Source: Photo credit: Judith Peterson, with permission by Toni Ziegler, and reprinted with permission from Myowa and Butler (2017).

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month of life, when mothers have been observed to act aggressively toward infants who attempted to nurse (Snowden, 1996). The squirrel monkey pattern of mutual gaze and responsive vocalizing, which occurs between newborns and reproductively active females, becomes a characteristic pattern between the squirrel monkey infant and mother when the infant begins to leave mother in independent forays in the third or fourth week of life (Biben,1994). Infant position, riding on the mothers’ back, influences the infant’s ability to engage in eye contact with the mother. Constant physical contact in the early days of life also makes it unlikely that contact-resuming vocalizations will be directed at the mother. Perhaps these vocal exchanges or dialogues serve socialization purposes, acquainting infants with the sounds of group members (Biben, 1994). In captive capuchins, Weaver and de Waal (2002) were able to classify the quality of attachment between mother and infant capuchins. There were significant consequences in the behavior of infants and juveniles as observed through longitudinal study (Weaver and de Waal, 2003). Infants and weanlings initiated more reconciliations than they received from adults. Infants with an insecure relationship with their mothers (i.e., above-average amounts of agonistic behavior relative to affiliative behavior) were highly aroused by conflict with adults, exhibiting distress vocalizations, and found reconciliation to be comforting. Infants with a secure relationship with their mother (i.e., above-average ratios of affiliative relative to mildly agonistic behavior) exhibit a more appeasing style of reconciliation, imbued with positive friendly overtures to adults that previously aggressed against them. Thus, infants developed characteristic styles of reconciliation, labeled homeostatic regulation styles since they involved ways in which infants resolved the distress emerging from social conflict. Weaver and de Waal (2003) speculated that the attachment relationship facilitated the development of infant’s homeostatic regulation style, supporting interpretations of a strong biological and physiological influence on infant behaviors (Maestripieri et al., 2009). A noticeable aspect of paternal care in tamarins, Cebus apella, and Ateles is food sharing. In some species of tamarins and marmosets, food is shared with infants through both active offering and tolerated taking. The possessor vocalizes and extends their hand holding the food while maintaining eye contact with a particular infant, or infants are allowed to take food from the hands or mouth of the possessor (Feistner and McGrew, 1989). Some males, in some species, are reported to initiate food sharing with specific vocalizations (Brown and Mack, 1978), but primarily it is the infant who begs. Older siblings also participate in sharing food with infants. Food sharing is primarily directed at weanlings. In golden lion tamarins, for instance, up to 90% of the food eaten by infants is obtained from social partners (Brown and Mack, 1978). But, as in wild chimpanzees, meat is shared equally across all social partners in wild capuchins (Perry and Rose, 1994). Fathers will defend infants against intruders and rescue them, at some risk to their own welfare. Typically, parental caregiving of this sort is given only to very young infants—until infants can locomote independently (Whitten, 1987). Titi and night monkey fathers, however, are reported to guard their infants for their first full year of life (Wright, 1990). Adult male howler monkeys may carry and play with infants for short periods of time (Vogt, 1984).

Parenting Juvenile New World Monkeys In tamarins, marmosets, and squirrel monkeys, the juvenile period begins around five months and ends at puberty, around 14 months of age (Tardif et al., 1992). In some of these callitrichid species, the presence of the mother inhibits their daughter’s sexual development (Walters, 1987). In cotton-top tamarins, juveniles, 6.5 to 15 months of age, react with stress to the birth of new infants. Parents and juveniles were seen to be more often in conflict. Initially, it was thought that this conflict was due to competition for parental resources (that is, conflict between the juveniles and the infants). But, when the parents were not carrying the new infants there was no conflict, so it was clear that the conflict 104

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was due to competition for the infants. When juveniles were allowed to carry the infants, about four to six weeks after they were born, all conflicts ceased. Juveniles take more responsibility for learning and for maintaining the relationship with their parents. In wild titi monkeys, juveniles, not the parents, are responsible for maintaining proximity with their parents (Spence-Aizenberg et al., 2016). Juvenile capuchins, more than subadults or adults, spend the most time watching others process food. Although there is no evidence that they learn food processing techniques, they may benefit from learning what can and what cannot be eaten. Experimental studies find that capuchins can learn how different parts of a “plastic food” can be manipulated or the way in which different parts move (Custance, Whiten, and Fredman, 1999). In cases where prey was eaten, observation by juveniles preceded begging or scrounging (O’Malley and Fedigan, 2005).

Parenting Adolescent New World Monkeys Adolescents play less than juveniles do, and when the newest set of twins is born then adolescent behaviors become more adult-like (Caine, 1986). Adolescent sons and daughters help with infant care by grooming and caring for younger siblings. For marmosets and tamarins, adolescence appears to end at approximately three years (Santos, French, and Otta, 1997). Prior to achieving adult stature, however, both males and females leave the family. In squirrel monkeys for example, primiparous females give birth around three years of age (Hopf, 1981), but males are not fully mature before 5 years (Biben, 1992). Adolescent squirrel monkeys continue to play, but play takes on sexual elements (Caine, 1986). It appears that adult females actively reject adolescent males who are forced to the periphery of the group (Caine, 1986).

Summary New World monkeys spend 3 to 5 years as subadults. In some species, there is extensive paternal involvement and cooperation among family members in carrying offspring and sharing food with them.

Prosimians Parenting Newborn Prosimians Some prosimian newborns cling and are carried ventrally (without support) by mothers. In some species transport of infants is by mouth, and infants are left unattended in nests or left “parked”, meaning grasping on tree branches (Higley and Suomi, 1986; Klopfer and Boskoff, 1979). In some prosimian species, mothers may leave their infants unattended for up to 12 hours. Mothers may scent mark the infants for identification, an indicator that mothers do not visually identify their infants as individuals (Niemitz, 1979). Prosimians are the most quickly maturing of primate species and reach sexual maturity by 1 year of age.

Parenting Infant Prosimians Infant prosimians may ride dorsally on the mother. This is accomplished by 2 weeks of age in ringtailed lemurs (Lemur catta) and by 4 weeks in the brown lemur (Lemur fulvus). In the ruffed lemur (Varecia variegate), however, infants engage in independent excursions away from the mother by 3 weeks of age (Klopfer and Boskoff, 1979). Mothers groom their infants frequently. In contrast to monkeys, but like chimpanzees, prosimian mothers may play for extended periods of time with their infants (Charles-Dominique, 1977; Niemitz, 1979). Prosimians, which are the most evolutionarily 105

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distant from humans, are weaned by 2, 3, or 4 months depending on the species ( Jolly, 1985; Klopfer and Boskoff, 1979). The most distant ancestral primate is considered to be the gray mouse lemur, which lives in Madagascar in mixed sex social groups and is nocturnal. Mothers give birth to one or more infants (Figure 3.9), and may form sleeping groups with one or two closely related females (Eberle and Kappeler, 2006). Lactating females nurse cooperatively within these sleeping groups. During the night, mothers carry their own infants and park them nearby while they forage, mostly solitarily. In the first 4 to 6 weeks of life, mother carry their infants in their mouth (Eberle and Kappeler, 2006). Infants emit at least three different vocalizations that appear to be specific to different contexts. Infant gray mouse lemurs purr when being groomed, emit whistle vocalizations when separated from their mother, and tend to emit tsak and whistle vocations when they are threatened while alone (Scheumann, Zimmermann, and Deichsel, 2007). Scheumann et al (2007) suggest that the vocalizations of gray mouse lemur infants convey both infant emotion and a communicative message to the mother: “the mother should perceive purrs as cohesion calls, whistles as attraction calls, and tsaks as aversive calls” (p. 716). Additionally, infants and mothers engage in greeting calls, for example, when mothers return to the sleeping box after a period of time away (Scheumann, Linn, and Zimmermann, 2017). Prosimian fathers tend not to participate at all in infant care (Vogt, 1984). The involvement of male ring-tailed lemurs in parenting tends to be limited to occasional grooming or sniffing of the infant, but if the mother is removed from the group the amount of time that the infant spends in contact with the male increases (Vogt, 1984). If the gray mouse lemur mother dies, then a close maternal relative from the sleeping groups may adopt the infant (Eberle and Kappeler, 2006).

Figure 3.9 Littermate gray mouse lemurs, Microcebus murinus, at 5 days of age, have not fully opened their eyes. Source: Photo credit: Marina Scheumann, Institute of Zoology, University of Veterinary Medicine, Hannover.

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Parenting Juvenile and Adolescent Prosimians Very little is known about parental influence on older prosimian offspring. Dispersal by sons appears to be voluntary. Immature male bushbabies may leave by following an adult male when he travels through the mother’s home range. Daughters remain close to their mothers; even as adults, daughters sleep close to mothers at night (Charles-Dominique, 1977).

Summary Prosimians mature most quickly among primates, and many reach full maturity in less than one year (Table 3.1). Offspring are weaned in 3 to 12 weeks and can have relatively few interactions with their mother during waking hours as they are often parked in nests while mothers forage. Some species have extensive reciprocal vocal interactions between mothers and offspring. As adults, they may adopt a home range that overlaps with that of their mothers.

Long-Term Consequences of Early Experiences Effects of Responsive Care Intervention for Nursery-Raised Chimpanzees Two studies have documented long-term consequences of differential early rearing in chimpanzees. Whether nursery-raised chimpanzees had developed an attachment relationship with a human caregiver was assessed at 1 year of age (van IJzendoorn et al., 2009). Years later, when these chimpanzees were adults, their health, behavior, and well-being were assessed (Clay et al., 2015). Chimpanzee infants that did not possess an organized attachment system were found to have more respiratory ill-health events into adulthood, more stereotyped rocking behavior, and an average level of wellbeing, compared to those with an organized attachment system that had fewer adverse health events, significantly less rocking, and above-average levels of well-being as adults. The second study investigated differences in the structural connectivity of the gray matter in adult chimpanzees’ brains based on their early experiences (Bard and Hopkins, 2018), and followed the advice of Krasnegor and Bridges (1990) to look more closely at how the brain changes in response to parenting behavior. At birth, chimpanzees were raised by the biological mothers, or, if their mothers had insufficient maternal behavior (Bard, 1994a, 2002), they were placed in a nursery. Most were given standard nursery care that provided all essential care to meet the infants’ physical needs and provided same-aged peers to provide for the infants’ social needs. A responsive care intervention was given to some nursery-raised individuals, however, for 4 hours per weekday, that included focused efforts on nurturing chimpanzee species-typical motor, social, emotional, and communicative skills from birth through the first year of life in a sort of intuitive parenting paradigm (Bard, 1994a, 1996; Bard, Dunbar, et al., 2014). Chimpanzee mothers act responsively, contingently, and nurture development in their infants. Of special significance are the intuitive parenting behaviors utilized to support development in motor skills and in communicative behaviors (Bard, 1994a, 1996; Bard, Dunbar, et al., 2014; Rijt-Plooij and Plooij, 1987). Intuitive parenting consists of a psychobiological preadaptedness to stimulate infants’ integrative development (Papousek and Papousek, 1987). The behaviors are neither reflexive nor based on rational thought, but they appear to require prior experience with infants. Intuitive parenting of locomotor skills in monkeys, for example, may have evolutionary benefits, including early cessation of infant carrying, early weaning, and thus, increased likelihood of a shorter interval to the next birth (Maestripieri, 1995). Providing positive emotional responsiveness to infant chimpanzees, through intuitive parenting processes, for as little as four hours per day, had dramatic effects on joint attention, cooperation, organized attachment (van IJzendoorn et al., 2009), communication (Bard, Dunbar, et al., 2014), 107

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and emotional expressiveness (increasing positive affect: Bard, Bakeman, et al., 2014). In contrast, early stress had equally dramatic effects but on different systems—early stress caused deficits in attention span, goal-directed efforts, emotional expressiveness (increasing fearful responses: Bard and Gardner, 1996), and impacted the development of lateralized behavior (Bard, 1998a; Bard, Hopkins, and Fort, 1990; Hopkins and Bard, 1993, 2000). There has been a great deal of research on the effects of stress and fear, but scientists have not spent equivalent energy in investigating the effects of positive emotions and attachment relationships (Bennett et al., 2017; Panksepp, 1986; Sheridan and Bard, 2017). Standard institutional nursery care for chimpanzees appeared to cause connectivity deficits in the gray matter of the basal forebrain, dopamine-rich brain regions that in humans involves reward circuits, and these deficits were prevented with a responsive care intervention (Bard and Hopkins, 2018). The lack of nurturing care of the standard nursery resulted in gray matter volume in the basal forebrain that was greater than that of the responsive care intervention or the mother-raised group. A possible cause for larger gray matter volumes would be a concentration of cell bodies related to relatively fewer dendritic connections. A special focus of the Bard and Hopkins (2018) study is the impact of the responsive care intervention on brain structures. There were no brain components in which the Responsive Care Intervention differed from the mother-raised chimpanzees. The Responsive Care Intervention, given to chimpanzee newborns and infants through the first year of life at the Yerkes Primate Center (Bard, 1996), appeared to provide the experiences necessary to prevent the deleterious effects of atypical rearing on structural connectivity evident in the brains of the Standard Care group. The nurturing experiences of chimpanzee infants were measured for the responsive care intervention group, the standard care nursery group, and for those raised by their chimpanzee mother, and were found to differ (Bard and Hopkins, 2018). Nurturing motor development has been observed in behaviors called “exercising” (Yerkes and Tomilin, 1935), which occur for up to 20% of the time while mothers are engaged with their very young infants (Bard, 1994a). In addition to nurturing motor skills, chimpanzee mothers also nurture the development of social and communicative skills (Bard et al., 2014; Bard, 2017; van Lawick Goodall, 1968). It was surprising to find that the rate of nurturing experienced by 1-month-old chimpanzees predicted the structural connectivity in the basal forebrain of their adult brain (Bard and Hopkins, 2018). Thus, the Responsive Care Intervention was an effective intervention that prevents the deleterious effects of atypical rearing on structural connectivity in the chimpanzee brain.

Long-Term Consequences of Early Separations of Offspring From Conspecific Caregiving Rhesus monkeys have most often been the subjects for longitudinal studies, in which early rearing experiences are linked with outcomes in adulthood. Many of these studies can be conceived as investigating the long-term consequences of stress or adversity early in life (Parker and Maestripieri, 2011). These primate models have often used the lack of parenting or temporary separations from caregivers as the stressor. Not surprising, these manipulations result in long-term behavioral, physiological, immunological, and neurological consequences (reviewed in Parker and Maestripieri, 2011; Suomi, 2004). When infant rhesus monkeys are permanently separated from their mother under experimental conditions, they can become hyperaggressive adults, and females do not provide adequate care for their infants (Harlow, 1958). In rhesus, early separations in infancy can compromise adult immunological responses (e.g., to simian immunodeficiency virus [related to HIV] challenges, Capitanio and Lerche, 1991). In pigtailed macaques, separations lasting only 10 days in infancy can result in juveniles and adolescents being deficient in the ability to develop close friendships and social networks (Capitanio and Reite, 1984). 108

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Whereas isolation-rearing for the first months of life produces severe deficits in behavior, compromised physiology, and permanent changes in neuroanatomy, peer-rearing can have persistent but less severe effects in rhesus monkeys, but can include problems in maternal behavior in adulthood (Champoux, Byrne, DeLizio, and Suomi, 1992). It is common, however, for peer-rearing paradigms to consist of an initial period of isolation (e.g., for the first 30 days of life, perhaps with a surrogate and blanket provided at day 15) and peer interactions provided after day 30. This type of peer-­rearing, for instance, appears to cause a lowering of the physiological stress set-point (that can be upregulated by greater peer exposure; Capitanio, Mendoza, Mason, and Maninger, 2005), decrements in the development of the serotonin system (found as early as 14 days of age and lasting at least through 150 days of age; Shannon et al., 2005), and structural changes in the brain that last, at least, into the late juvenile period (Spinelli et al., 2009). It is worth noting, however, that these long-term consequences may not be found in other primate species or may not be found if social interaction experiences are given in the first 30 days. Pigtailed macaques, for instance, given nursery rearing with extensive infant handling by humans, showed no long-term behavioral or social deficits as juveniles or adolescents (Sackett, Ruppenthal, and Davis, 2002). Even when separations from caregivers during infancy are more limited in scope, there can still be long-term consequences. Early separation experiences cause changes in immunology in rhesus monkeys. Separation experiences in marmosets, involving daily separations from both parents in the first month of life, result in changes in physiology, impairments in cognitive functioning, and behavioral inhibition (Pryce et al., 2005), and impairments in the function of genes in the hippocampus related to synaptic plasticity (Parker and Maestripieri, 2011). It is noteworthy that separations from the mother later in life, especially around the ages when offspring are normally becoming independent, can serve to enhance resilience, at least in squirrel monkeys (Parker et al., 2004). Maternal abuse has clear immediate and short-term consequences for the primate infant, ranging from distress to injury and death. Abused infants cry more as a direct consequence of abuse, and they cry more than nonabused infants, even when they are not being abused (Parker and Maestripieri, 2011). Abuse increases the infant’s tendency to cling to the mother, which may paradoxically cause more abuse. Abused infants are developmentally delayed in initiating play with peers, and they play less (Maestripieri and Carroll, 2000; Reite, 1987). Stress experienced early in life may induces changes in emotional reactions to stress, and these changed responses may last a lifetime (Suomi and Levine, 1998). Emotional behavior, mediated by the limbic system, results in emotional reactions that are easily transferred to other individuals and to the next generation (e.g., phobic reactions; Mineka et al., 1984). The magnitude of long-term disturbance in adults could be related to the magnitude of the stress response in infancy. Many separation paradigms involve both the loss of caregiving behaviors and distress caused by that loss; thus, the independent contribution of each variable is difficult to determine. One advantage of investigations into the consequences of normal variation in maternal behaviors is that it might disentangle these variables. Long-term consequences for infants and juveniles of being raised with different “maternal styles” have been studied. In general, protectiveness is thought to prevent potential dangers, including harassment from others (Maestripieri, 1994). Infant and juvenile vervet monkeys with more protective mothers are more cautious in response to novelty (Fairbanks and McGuire, 1993). Although these infants do have less risk from predation, they appear to be less able to cope with stressors, such as the loss of the mother (Hinde, 1987). Maternal style can include differences in abuse or rough handling, typically reflected in how often offspring experience “rejection”. Rejecting vervet mothers have infants that show more enterprise (if they survive): The infants develop independence at an earlier age and are more resourceful (Fairbanks, 1996). Rhesus macaques that experienced more maternal rejection early in life were more socially avoidant as adolescents (Maestripieri et al., 2006). Adolescent male vervets with more rejecting mothers were bolder with adult male strangers (Fairbanks, 109

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1996). For daughters, it appears that the mothers’ maternal style is the best predictor of their own maternal style with their offspring (Berman, 1990: Fairbanks, 1996). Variability in maternal style has long-lasting consequences in the social behavior and physiology of offspring (for more details see review by Parker and Maestripieri, 2011). Infant temperament and the maternal style experienced early in life interact in the attainment of dominance status, which is a measure of social success. High-reactive rhesus monkey infants raised with nurturant mothers attain high status in an adolescent peer group, whereas high-reactive rhesus monkey infants raised with punitive mothers are lowest in dominance status (Scanlan, 1986). Schneider (1984) found that high-reactive nursery-reared rhesus infants and low-reactive mother-reared infants score highest on cognitive assessments when tested as juveniles even though there were no overall group differences based on rearing or on reactivity. In chimpanzees of the Tai Forest of Côte d’Ivoire, West Africa, there appears to be differential maternal investment in sons and daughters, based in part on maternal dominance rank (Boesch, 2012). Mothers of high rank have a longer period of time between the birth of a son and the next offspring—which decreases the mortality of sons of high-ranking mothers, whereas mother chimpanzees of low rank tend to invest more in their daughters (Boesch and Boesch-Achermann, 2000). Moreover, through their continuing support, mother chimpanzees of high status aid their sons in achieving high dominance status as well (Boesch and Boesch-Achermann, 2000).

Conclusions There is no single “primate pattern” of parenting. Diversity, variability, and flexibility are among the most important characteristics of primate parenting (Hawkes et al., 2017). There is a strong genetic basis for maternal behavior, but an equally strong influence of experience. It would be a mistake to expect any single variable to have an exclusive determination for parenting: “Maternal behavior is obviously so important to the survival of a species that it has been ‘overdetermined’—that is, driven by multiple behavioral and physiological systems” (Coe, 1990, p. 178). There is a danger in drawing explicit comparisons between a particular primate species and a particular human society (Myowa and Butler, 2017). Perhaps every facet of human parenting can be found to occur in some other primate species, yet clearly no one other primate species exhibits a complete repertoire of human parenting. Maternal competence in chimpanzees, expressed in interaction even with very young infants, reflects sensitive responsivity during which the mother engages in contingent behavior and encourages development of infant capacities (Bard, 1994a). These behaviors parallel those observed in intuitive parenting in humans (Papousek and Papousek, 1987). For chimpanzees, being raised with their biological mother provides a myriad of benefits, some of which can be provided by humans with a focus on nurturing the development of species-typical skills (Bard, 1996; Bard and Hopkins, 2018; Clay et al., 2015; van IJzendoorn et al., 2009). There is not a single theoretical account, barring evolutionary theory, that can explain the diversity of parenting patterns in primates (Hawkes et al., 2017). Moreover, there is not a single theoretical account that explains or predicts the diversity of patterns of infant interactions with individuals other than the mother (Caine, 1993; Chism, 2000; Maestripieri, 1994; Manson, 1999; Paul, 1999; Ross and MacLarnon, 2000; Silk, 1999; Snowden, 1996; Wright, 1990). It is likely that there will not be a single theoretical account that explains the ontogeny of maternal competence in primates, because there is a similar pattern of diversity in maternal behavior across species. For some species, such as tamarins, mothers must learn to let others help in infant care. Rhesus mothers must learn to allow infants to cling to their hair. Chimpanzee mothers must learn to provide support for the infant, and nurture their physical, emotional, and communicative development. Parenting in primates is diverse. Some Prosimian mothers park their infants in nests, carry them in their mouth, and let them nurse and otherwise do not engage with their infants. In contrast, 110

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chimpanzee mothers provide cradling support and spend up to 15 minutes each waking hour interacting socially, communicatively, or didactically with their infants. Some New World monkey fathers play an important role in parenting infants, as do gorilla fathers. Consideration of the influence of monogamy or living in a harem illuminates the manner in which social organization contributes to behavioral expressions of parenting. Cognitive influences on parenting, especially evident in the Great Apes, typically provide for flexibility and richness in parenting behaviors, making great ape parenting more similar to human parenting than that of other primates. The evolutionary risks, however, include greater dysfunction in parental behavior when learning environments are altered. The continuing influence of parents on older offspring, especially adolescents, requires more focused study. The manner in which independence is achieved is also an important consideration. Evidence of teaching complex locomotor behaviors, tool use, hunting, and subtle food searching patterns suggests that primate parents, at least of some species, continue to influence offspring throughout development (Boesch, 2012; Goodall, 1986; Lonsdorf, 2006). As we develop new primate models of parenting, it will be important to consider emotional components of parenting with an emphasis on the positive aspects of bonding and attachment (Keller and Bard, 2017), and on investigations of the mechanisms underlying the reinforcing qualities of parenting (Panksepp, 1998). There is much that remains to be learned.

Acknowledgments Funding was provided by NIH Grant RR-00165 to the Yerkes Regional Primate Research Center of Emory University, NIH Grant RR-03591 to R. B. Swenson of the Yerkes Center, NICHD Intramural Research Program funds through the Laboratory of Comparative Ethology and S. J. Suomi, a Max-Planck Society stipend in cooperation with the Developmental Psychobiology project directed by H. Papousek at the Max-Planck Institute for Psychiatry, NICHD-NRSA Research Fellowship HD-07105 to K. A. Bard, and NIH Grant RR-06158 to K. A. Bard. The Yerkes Center is fully accredited by the American Association for Accreditation of Laboratory Animal Care. I thank my research assistants, especially Kelly McDonald, Yvette Veira, Kathy Gardner, and Josh Schneider, for all their work with the chimpanzees, students at the University of Portsmouth, including Chris Brindle, Nadja Dreschler, Kriztina Ivan, and Judit Barta, and I thank Ms. N. Johns, my friend and Librarian of the Yerkes Research Center. Special appreciation is extended to Marc H. Bornstein, Steve Suomi, David Leavens, Mechthild Papousek, and to the memory of Hanus Papousek for their intellectual contributions to this chapter.

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Kim A. Bard Whitten, D. L. (1987). Infants and adult males. In B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, and T. T. Shruhsaker (Eds.), Primate societies (pp. 343–357). Chicago, IL: University of Chicago Press. Wich, S. A., Utami-Atmoko, S. S., Mitrai Setia, T., Rijksen, H. D., Schurmann, C., van Hooff, J. A. R. A. M., and van Schaik, C. P. (2004). Life history of wild Sumatran orangutan (Pongo abelii). Journal of Human Evolution, 47, 385–398. Wood, D., Bruner, J., and Ross, G. (1976). The role of tutoring in problem-solving. Journal of Child Psychology and Psychiatry, 17, 89–100. Wrangham, R. W., Koops, K., Machanda, Z. P., Worthington, S., Bernard, A. B., Brazeau, N. F., Donovan, R., Rosen, J., Wilke, C., Otali, E., and Muller, M. N. (2016). Distribution of a chimpanzee social custom is explained by matrilineal relationship rather than conformity. Current Biology, 26, 3033–3037. Wright, P. C. (1990). Patterns of parental care in primates. International Journal of Primatology, 11, 89–102. Wright, R. (1972). Imitative learning of a flaked stone technology—The case of an orangutan. Mankind, 8, 296–306. Yamomato, M. E., Box, H. O., Albuquerque, F. S., and Arruda, M. de F. (1996). Carrying behavior in captive and wild marmosets (Callithrix jacchus): A comparison between two colonies and a field site. Primates, 37, 297–304. Yerkes, R. M., and Tomilin, M. I. (1935). Mother-infant relations in chimpanzees. Journal of Comparative Psychology, 20, 321–348. Yoshida, H., Norikoshi, K., and Kitahara, T. (1991). A study of the mother- infant relationships in chimpanzees (Pan troglodytes) during the first four years of infancy in Tama Zoological Park. The Japanese Journal of Animal Psychology, 41–42, 88–99. Ziegler, T. E., Prudom, S. L., and Zahed, S. R. (2009). Variations in male parenting behavior and physiology in the common marmoset. American Journal of Human Biology, 21, 739–744. Zuckerman, S. (1932). The social life of monkeys and apes. London: Routledge.

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4 GENETICS AND PARENTING Amanda V. Broderick and Jenae M. Neiderhiser

Introduction Parenting is a dynamic, multiply determined process that is influenced by a range of extra-familial (e.g., cultural context) and intra-familial factors (e.g., interparental relationships) (Bornstein, 2016). Generally, researchers have been interested in parenting as the means by which the environment shapes the developing child. A number of theoretical models of how parents influence their children (e.g., socialization, modeling) have been generated, with these models typically assuming that parenting operates via social transmission of behaviors. Yet, the ability of children to shape their own environments has been understood for nearly five decades (Bell, 1968), and within biologically related families, parents have not only an environmental influence, but a genetic one as well. Thus, unless explicitly modeled, associations between parenting and child outcomes may be due, in part, to confounds from unmeasured heritable influences. It may be, for instance, that children’s heritable characteristics evoke certain types of parenting, such as when parents respond negatively to adolescents’ aggression (Narusyte, Andershed, Neiderhiser, and Lichtenstein, 2007). Alternatively, relations between parenting and child outcomes may be due to shared genetics between parents and children. For example, parents who are high in irritability may be more likely to use harsh parenting strategies and to have children who are also irritable (Prinzie et al., 2004). The aim of this chapter is to discuss the “genetics” of parenting by outlining how genetically informed designs can provide important information for parenting research. Genetically informed designs refer to a class of designs that measure genetic influences either by assessing family members of varying relatedness (e.g., twins, full siblings, adoptive parents and adopted children) and explicitly modeling relatedness or by directly collecting DNA. These designs (e.g., twin studies, adoption studies) allow us to test an assumption underlying many theoretical models of parenting—that associations between parent and child characteristics are due to environmental influences as opposed to heritable influences, facilitating the further refinement of existing theories and ultimately informing intervention efforts (Harold, Leve, and Sellers, 2017; Leve et al., 2017). Moreover, some genetically informed approaches are beginning to identify how children evoke parenting at the level of the gene (Elam et al., 2017). We begin with a review of the significant changes that have occurred over the past century to make behavioral genetics the field that it is today—one that includes examination of parenting. Next, we describe various genetically informed research designs and discuss the utility of each. Then, we summarize extant literature of the genetics of parenting during infancy and early childhood (ages

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birth–6 years), middle childhood (ages 6–10 years), and adolescence (ages 10–18 years). We end with a discussion of the ways in which the work of developmental scientists can inform that of behavioral geneticists and vice versa.

Historical Considerations in Genetics and Parenting The field of behavioral genetics has seen rapid growth since the middle of the 20th century, especially in regard to the types of constructs examined (Knopik, Neiderhiser, DeFries, and Plomin, 2017). Broadly, behavioral genetics research can be categorized into family-based approaches, which capitalize on varying degrees of genetic relatedness within families to quantify relative contributions of heritable and environmental influences on traits, and molecular genetic approaches, which aim to identify the specific genetic underpinning of behavioral traits. Family-based genetic studies include twin, extended family, and adoption designs and allow for heritable and environmental influences to be disentangled by estimating heritability as well as shared environmental (i.e., nongenetic influences that account for similarity among family members) and nonshared environmental influences (i.e., nongenetic influences that account for differences among family members). All of these designs, as well as combinations of the designs, can also help to clarify gene-environment interplay such as gene-environment correlations (rGE) and gene by environment interactions (GxE). Although we will discuss each of these aspects of gene-environment interplay in detail in the sections that follow, it is important to note that genes and environments can systematically co-occur (as in rGE) and can moderate one another (as in GxE) because it has implications for understanding the processes involved in development. Molecular genetics studies use approaches such as candidate gene, genome-wide association studies (GWAS), and polygenic risk scores (PRS) to pinpoint a gene or set of genes that explain variance within a phenotype. These studies can also examine gene-environment interplay, although GxE is more commonly examined within molecular genetic frameworks than is rGE. Although humans have been thinking about genetics for centuries, in 1960, Fuller and Thompson published Behavior Genetics, which was effectively the first comprehensive handbook of the study of the genetic basis of behavioral traits. At that point, genetics research had largely focused on Mendelian inheritance. During the 19th century, Gregor Mendel studied pea plants and showed that both members of the parent generation of pea plants provide a component (later called a gene) to the offspring (Knopik et al., 2017). He measured observable traits (i.e., phenotypes) of the plants, such as whether the seeds were wrinkled or smooth, and noticed that variation in offspring phenotypes could be reliably predicted based on the parent generation. In other words, a single gene determined these characteristics, and this work provided the basis of heredity, which refers to the degree to which

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Figure 4.1 Historical timeline of notable behavioral genetics and developmental events.

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Plomin & Bergemen’s GE interplay paper

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differences within a population on a phenotype can be attributed to differences on a genotype. Some human behaviors or diseases, like Huntington’s disease or phenylketonuria, are caused by single genes, but complex human behavioral traits (e.g., personality, psychopathology) are not attributable to any single gene (Knopik et al., 2017). Complex traits can be better understood by studying the degree to which they are explained by genetics. Even in 1960, when contemporary scientists rejected the notion that biology played any role in human behavior, behavioral geneticists acknowledged that behavior is not influenced by purely genetic or environmental factors (i.e., “the Nature-Nurture Problem”), but instead, results from complex processes that involve both genetic and environmental factors (Fuller and Thompson, 1960). In a seminal adoption study, Heston and Denney (1968) compared adopted offspring whose birth mothers had been diagnosed with schizophrenia with adopted offspring who had no maternal history of schizophrenia. Schizophrenia was only found in the offspring of biological mothers with schizophrenia, lending evidence to genetic causes of schizophrenia. Previously, psychologists believed that poor parenting caused schizophrenia (Fromm-Reichmann, 1948). Subsequent adoption studies, such as the Texas Adoption Project (TAP; Horn, 1983; Horn, Loehlin, and Willerman, 1979) and the Colorado Adoption Project (CAP; DeFries, Plomin, Vandenberg, and Kuse, 1981; Plomin and DeFries, 1983) expanded both the parent and offspring characteristics studied. For instance, TAP examined children ages 3 through 16 years and found that children’s intelligence was more similar to their birth mothers than to their adoptive parents (suggesting heritable influences; Horn, 1983), and CAP extended those findings downward to infancy, identifying genetic contributions to infant intelligence and communicative competence, and provided preliminary evidence that the association between maternal responsivity and infant intelligence is due to both heritable and environmental influences (Plomin and DeFries, 1983). The decades following the publication of Behavioral Genetics saw growth in both theory and methodology. Researchers who were interested in human behavioral genetics at the time Behavioral Genetics was published were limited by the methodological and statistical techniques available. Geneticists who studied nonhuman populations had the benefit of experimental designs to test the effects of manipulating genetic or environmental parameters, whereas the field of human behavioral genetics relied heavily on correlational research designs that consisted of family members of varying degrees of genetic relatedness. Advanced statistical tools, such as structural equation modeling, were developed and subsequently applied to genetically informed designs, enabling scientists to estimate the relative heritable and environmental variance underlying the covariation of multiple phenotypes (Eaves and Gale, 1974; Martin and Eaves, 1977). During the late 1970s and early 1980s, researchers began thinking about gene-environment interplay. Two early twin studies found heritable effects on adolescent twins’ reports of accepting and rejecting parenting—a construct that had been previously assumed to be a measure of the environment (Rowe, 1981, 1983). Rather than considering heredity and environment as wholly independent forces, the study of gene-environment (GE) interplay is based on the assumption that, under certain circumstances, heritable and environmental factors are systematically related due to rGE and GxE (Plomin, DeFries, and Loehlin, 1977). In other words, heritable factors can control, at least in part, which environments are experienced and how responsive an individual is to an environment (Scarr, 1992; Scarr and McCartney, 1983). Passive rGE is present when children are exposed to certain environments because of their parents’ inherited characteristics, such as a child of anxious parents being exposed to more overprotective parenting. Evocative (also called reactive) rGE occurs when children’s heritable characteristics evoke reactions from their environment, such as an anxious child eliciting more over-protective parenting in stressful situations. Active rGE refers to children choosing their environments based on inherited characteristics, such as an inhibited child partaking in more solitary activities. Conceptually, evocative and active rGE are distinct, but in extant research designs, they are difficult to differentiate. Additionally, rGE does not account for the entirety of the 125

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variance in a phenotype, but rather is one possible explanation for links between parent and child characteristics. In contrast to rGE, GxE refers to processes in which the effects of the environment vary as a function of genetics or instances in which the environment modulates the expression of an individual’s genotype. An example of GxE is a child with a predisposition for surgency who thrives in the context of appropriately structured parenting but struggles in the context of overly permissive parenting. GxE can be thought of in different ways based on whether the environmental construct under consideration is conceptualized as negative/risky or positive/protective (Burt, 2011). When the environment is risky, an inherited vulnerability may be amplified or activated (Burt, 2011). For instance, at increasing levels of paternal punitive discipline, heritable influences on adolescent externalizing behaviors increase (Button, Lau, Maughan, and Eley, 2008). Also when the environment is risky, an inherited vulnerability may be diminished, which is known as the bioecological interaction model (Burt, 2011; Pennington et al., 2009). A finding consistent with this model is that heritable influences on adolescent aggression are lower, and shared environmental influences are higher, in disadvantaged neighborhoods compared to advantaged ones (Tuvblad, Grann, and Lichtenstein, 2006). Finally, when the environment is protective, the effects of an inherited vulnerability may be diminished, as in the compensation by social context model (Burt, 2011). For instance, at increasing levels of parental warmth, heritable influences on adolescent antisocial behaviors are diminished (Feinberg, Button, Neiderhiser, Reiss, and Hetherington, 2007). Notably, GxE can occur in the context of rGE although consideration of these two types of GE interplay simultaneously is rare ( Jaffee, 2016; Jaffee and Price, 2007; Price and Jaffee, 2008). In light of evidence that parenting constructs are themselves subject to heritable influences (Rowe, 1981, 1983), Plomin and Bergeman (1991) argued that genetic influences on measures that had historically been considered “environmental”—such as parenting or family climate—do not necessarily mean that environments themselves are heritable. Instead, they suggested that such measures capture something about the individual’s relations with the environment that are due to unmeasured, heritable characteristics. Parenting, then, could be considered a phenotype that is influenced by both parents’ and children’s genetically influenced characteristics. More than a decade after Plomin and Bergeman (1991) put forth this idea, Rutter (2005) pushed the field to engage in more rigorous testing of purported environmental mechanisms of risk. In the intervening years, a number of “environmental” risk factors (e.g., harsh parenting) had been explored using genetically informed designs, but Rutter highlighted a number of steps required to strengthen the case that these are causal mechanisms. In particular, he stressed the importance of longitudinal designs that include precise measures of purported risk factors (and outcomes), that allow for testing of competing hypotheses, and that explicitly test the theoretical limitations of the specific design (e.g., equal environments assumption for twin studies, restricted range of environments for adoption designs). In many ways, he argued for the field of behavioral genetics to adopt practices that were already in place in typical developmental research, while encouraging developmental researchers to incorporate methodology practiced by behavioral geneticists. This theoretical shift that began in the early 1980s necessitated changes in research strategies and methodological advances to allow the investigation of specific developmental processes of GE interplay. For one, more fine-grained assessments of family processes were included in family-based genetic designs. Parent-offspring adoption studies, by design, are well-suited to test GxE, but the available data from some early studies were generally too vague to specify the inherited “risk” that was being captured, due in part to the fact that many early studies examined adult adoptees. Methodologically, GxE in parent-offspring adoption designs can be tested by statistically modeling the interaction between constructs of birth parents (genetic influences) and constructs of adoptive parents (environmental influences) to predict the offspring outcome of interest. One example of this strategy was implemented by Cadoret, Yates, Troughton, Woodworth, and Stewart (1995) who used 126

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hospital and prison records to diagnose the biological parents of adopted adults and also assessed the adoptive family for marital, psychiatric, and legal problems. Adoptive family problems were related to increased adoptee aggression, but only if the biological parent exhibited antisocial personality disorder. This study and others helped to establish evidence of GxE (Cadoret, Troughton, O’Gorman, and Heywood, 1986; Wahlberg et al., 1997), but the mechanistic processes remained unexplored. Registry data continue to be used and are critically important because studies using registry data are able to examine the large sample sizes needed to detect small effect sizes; to understand the mechanisms of effects, in-depth assessment of family process is also necessary. We describe findings from parent-offspring adoption studies that have collected more in-depth assessments of family processes thus helping to clarify processes by which parents and children influence one another. A second important change involved methodological advances that provided straightforward strategies for examining GxE within the context of both twin designs and molecular genetic designs (Purcell, 2002; Purcell and Sham, 2002). Prior to the early 2000s, two approaches were used to test GxE within a twin study. One required samples of twins in which co-twins were discordant on exposure to discrete environmental constructs (e.g., adult twins discordant on marital status). For instance, twins discordant on marital status were compared, and evidence suggested that being married mitigated genetic liability for depression (Heath, Eaves, and Martin, 1998). The other approach required instances in which co-twins (or whole samples) were exposed to vastly different levels of a continuous environmental construct (e.g., twins who experienced high versus low levels of life stress). Using this approach, Heath and colleagues (1985) compared twins who were educated prior to the institution of liberal educational policies in Norway with those who were educated following policy changes. The first cohort showed little evidence of heritability for educational attainment, whereas following these policy changes, heritable factors played a substantial role in educational attainment. Thus, until the early 2000s, researchers using twin designs to investigate GxE were relegated to examining characteristics or experiences that were discrete or allowed for the creation of distinct groups. This design is reasonable for discrete factors pertinent to the study of parenting (e.g., parental divorce, daycare attendance), but many other relevant factors are continuous (e.g., socioeconomic status, parental hostility). Furthermore, many statistical models of GxE assume that the latent genetic factors are independent of measured environmental constructs—an assumption that is violated in the context of rGE ( Jaffee and Price, 2007). To address this limitation, Purcell (2002) developed a method to test GxE in twin samples if the moderator is continuous, and subsequently revised the method to test GxE in the presence of rGE (Purcell and Sham, 2002), sparking a number of analyses that would not have been possible previously. Now, continuous moderators, such as those indexing parenting and broader family characteristics, could be tested in a twin GxE framework, providing more information about developmental processes. One subsequent report found that, for example, as family dysfunction increases, genetic contributions to conduct disorder decrease, while shared and nonshared environmental influences increase (Button, Scourfield, Martin, Purcell, and McGuffin, 2005). It is important to note that the model developed by Purcell (2002) and used in hundreds of studies since is not purely a strategy for testing GxE, but is rather more general. Specifically, this model tests for moderation of heritable, shared environmental, and nonshared environmental influences by a continuous variable, most often an “environmental” variable like parenting or socioeconomic status. We would argue, however, that moderation of the shared and nonshared environmental estimates is equally informative as moderation of heritability, especially when the focus is on understanding the mechanisms of gene-environment interplay. For example, using an twin/sibling design, adolescent temperament moderated heritable and shared environmental influences on parental negativity (Ganiban, Ulbricht, Saudino, Reiss, and Neiderhiser, 2011). The heritable influences on parental negativity were greatest at higher levels of adolescent negative emotionality, and both shared and nonshared 127

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environmental influences were smallest. In other words, as adolescents exhibit more temperamental negative emotionality, the child-based effects on parental negativity increase resulting in less-similar parental negativity in sibling pairs. Concomitant to advances in family-based approaches, the field of molecular genetics experienced rapid growth with major initiatives such as the Human Genome Project (Collins and Mansoura, 2001), the International HapMap Project (Gibbs et al., 2003), and the 1000 Genomes Project (Siva, 2008) that have begun to characterize the human genome. The proliferation of research in psychiatric molecular genetics is reflected in the rapid increase in human molecular genetic publications, from about 2,000 published between 2000 and 2004 to 9,400 published between 2010 and 2014 (Ayorech et al., 2016). Arguably, a catalyst of this growth was the publication of two early studies demonstrating candidate gene-by-environment interaction (cGxE). The first found that adults who were maltreated as children were likely to develop antisocial behavior as adults but only if they were carriers of the neurotransmitter-metabolizing enzyme monoamine oxidase A (MAOA) gene coding for low expression (Caspi et al., 2002). The second concluded that stressful life events were more strongly linked to depression for carriers of two short alleles of serotonin-transporter-linked polymorphic region (5-HTTLPR) (Caspi et al., 2003). This methodological approach made genetic work more accessible to nongeneticists and allowed for theories like diathesis-stress and differential susceptibility to be tested in a molecular genetic framework. However, subsequent attempts at replication of those particular findings have been inconsistent (Culverhouse et al., 2017), and general concern has been raised about the validity of published cGxE studies (Dick et al., 2015). Multiple meta-analyses (Culverhouse et al., 2017; Karg, Burmeister, Shedden, and Sen, 2011; Munafò, Durrant, Lewis, and Flint, 2009; Risch et al., 2009; Sharpley, Palanisamy, Glyde, Dillingham, and Agnew, 2014) testing the initial cGxE interaction between 5-HTTLPR and life stress on depression have themselves produced conflicting results, with some finding no evidence of an interaction and concluding that if one exists, it is likely a small effect that is not generalizable across groups (Culverhouse et al., 2017). The 5-HTTLPR and life stress interaction is an illustrative example of the challenges posed by widespread interest in cGxE work, but it is by no means unique. To address these problems, the field needs to adopt standards and practices that increase the methodological rigor of cGxE work (Dick et al., 2015). As we have reviewed, the field of behavioral genetics has seen major growth in theory and method since the publication of the field’s namesake text in 1960. We next describe contemporary approaches for studying parenting from a behavioral genetics perspective.

Research Designs and Methodology in Genetics and Parenting We first describe the logic of family-based genetic designs (e.g., twin, adoption studies) before discussing molecular genetic methodology. The foundation of family-based genetic approaches is heritability, which refers to the extent that individual differences on a phenotype are attributable to inherited differences. Estimates of heritability can be obtained by comparing the phenotypes (i.e., measured behaviors) of individuals who vary in degree of genetic relatedness but provides no information about phenotypes at the individual level or about the specific inherited factors that influence a phenotype. For instance, heritability estimates of parental warmth range from 34% to 37%, indicating that 34%–37% of the population variance in parental warmth is due to heritable influences (Kendler and Baker, 2007). By combining evidence from multiple research designs, we can better understand GE interplay and the mechanisms of effects on child development. Below, we further describe the most commonly used family-based behavioral genetic designs (twin, adoption, extended family, and combination), outline the basic assumptions and limitations of these designs and clarify how each can inform our understanding of GE interplay. We discuss family-based genetic approaches before turning to a discussion of molecular genetic approaches. 128

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Twin Designs Twin studies, as shown in Figure 4.2, compare monozygotic twins (MZ) with dizygotic twins (DZ) and are particularly well-suited for detecting heritable effects. MZ twins share 100% of their segregating genes, while DZ twins share, on average, 50% (like any full sibling pair). Twins are also the same age and often the same sex (DZ twins can also be different sex, although many twin studies use only same-sex twin pairs). Thus, if MZ twins are more similar to each other on a particular construct than DZ twins, the best explanation for this similarity is that the construct is heritable. To illustrate, within a sample of 8-year-old twin children, the intraclass twin correlations for child-rated anxiety symptoms are .72 for MZ twins and .20 for DZ twins. Because the DZ twin correlations are less than half that of the MZ twin correlations, heritable influences on child anxiety are indicated (Eley, Napolitano, Lau, and Gregory, 2010). Beyond identifying the heritability of a trait, genetically informed designs allow variance of a phenotype to be partitioned into additive genetic (A), shared environmental (C), and nonshared environmental (E) influences. Shared environmental influences refer to nongenetic influences that account for similarity among family members, such as residing in the same home. Nonshared environmental influences refer to nongenetic influences that account for differences among family members, such as having separate peer groups or differential parenting, and also include measurement error. This approach does not allow for identification of the specific environmental influences acting on parenting but highlights the importance of both heritable and environmental factors. Multivariate analyses go a step further by incorporating multiple phenotypes. Particularly relevant to twin studies is the assumption of equal environments, which states that the effects of the environments on MZ twins and DZ twins are equivalent with respect to the construct under study. It could be violated, perhaps, if parents of MZ twins systematically treat their children more similarly than do parents of DZ twins and this more similar treatment results in greater MZ twin similarity for the construct under study. This assumption has been empirically tested and supported (Conley, Rauscher, Dawes, Magnusson, and Siegal, 2013; Eaves, Foley, and Silberg, 2003); however, if it

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A = Influence of child’s genecally influenced characteriscs on parents’ parenng. Interpreted as evocave rGE

A = Influence of parents’ genecally influenced characteriscs on parenng. Interpreted as passive rGE

C = Influence of children’s shared environmental characteriscs on parenng. Interpreted as passive rGE

C = Influence of parents’ shared environmental characteriscs on parenng. E = Influence of parents’ unique environmental characteriscs on parenng.

E = Influence of child’s unique environmental characteriscs on parenng.

Figure 4.2 Child and parent-based twin designs and gene-environment correlation.

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were to be violated, genetic estimates would be inflated. An early study used a small sample of “misclassified” twins (i.e., MZ twins whose parents believed them to be DZ twins and vice versa) to investigate this assumption (Scarr, 1968). If parental beliefs about zygosity impact similarity of treatment, misclassified MZ twin correlations would resemble those of correctly classified DZ twins and misclassified DZ twin correlations would resemble those of correctly classified MZ twins. By contrast, if genetic relatedness impacts similarity of treatment, misclassified MZ twin correlations would resemble those of correctly classified MZ twins, and misclassified DZ twin correlations would resemble correctly classified DZ twins. The latter was found for all examined measures, including maternal report of twins’ current behaviors, temperament and personality characteristics, and developmental milestones. In other words, parents’ similar treatment of their children is attributable to actual genetic similarity rather than parents’ perception of twin similarity. This finding strengthens the conclusion that, when twin studies find parenting of MZ twins to be systematically more similar than DZ twins, it is not a violation of the equal environments assumption but a reflection of heritable influences on parenting. Finally, it is important to keep in mind, that the equal environments assumption is relevant only in relation to how MZ twins’ more similar experiences influence the construct being examined. Twin designs can be used to investigate GE interplay and particularly, by using combinations of twins-as-parents and twins-as-children designs, it is possible to disentangle passive and evocative/ active rGE. The distinction between these two types of twin designs in regard to parenting is important because they lead to different interpretations of heritable influences on parenting. Parent-based designs (in which the twins are parents) answer the question how do parents’ genotypes influence their parenting? Studies using these designs that find heritable influences on parenting constructs can be inferred as passive rGE, even when child constructs are not explicitly modeled because passive rGE occurs when parents’ inherited characteristics influence their parenting. Within child-based designs (in which the twins are children/adolescents), shared environmental influences refer to nongenetic factors that account for siblings’ similarity, including parents’ heritable influences on their parenting. Taken together, when there is evidence of heritability for parenting within a parent-based design and shared environmental influences within a child-based design, the case for passive rGE is strengthened. Child-based designs, by contrast, are focused on how children’s genotypes influence their parents’ behavior. When twins are children, heritability on measures of parenting suggest that parents are responding to their children’s inherited characteristics (evocative rGE). Different research designs, then, can provide complementary information about GE processes operating within families.

Adoption Designs Adoption studies are particularly useful for testing parenting as an environmental mechanism because similarities between adopted children and nonbiological adoptive parents cannot be due to shared genes (Haugaard and Hazan, 2003) especially when the child is placed in the adoptive home at or near birth. The basic adoption design is displayed in Figure 4.3 and includes data collected from birth parents, adoptive parents, and adopted children and compares correlations between biological parents and adopted children with correlations between adoptive parents and adopted children. If the adopted child and biological parent(s) correlate for a given phenotype, heritable effects are indicated, but if the adopted child correlates with adoptive parent(s) or with the rearing environment, there is evidence of environmental influences (Haugaard and Hazan, 2003). As Figure 4.3 shows, birth mothers provide children with both their prenatal environment and half of their genes, so by including birth fathers, prenatal influences can be disentangled from genetic influences (Loehlin, 2016). Beyond comparing correlations, the adoption design has been used with more complex modeling techniques (e.g., structural equation modeling) to study evocative rGE. When birth parent characteristics are related to adoptive parent parenting, there is initial evidence for evocative rGE because the child is presumably the factor linking the two (Ge et al., 1996; Leve et al., 2007). By subsequently testing child factors as 130

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Genec Influences

Environmental Influences

Birth Father

Adoptive Father

Birth Mother

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Figure 4.3 Traditional adoption design.

potential mediators between birth parent and adoptive parent characteristics (Harold, Leve, Barrett, et al., 2013), the mechanisms by which evocative rGE is operating can be more clearly specified. One criticism of adoption studies is that adoptive families are not generally representative of all families and therefore may represent a selected range of environments (Stoolmiller, 1999). Because adoptive families are screened prior to adoption, adoptive parents typically are older and better educated than nonadoptive parents and consequently may have higher incomes and more education. In other words, there are concerns that adoptive families are systematically different from nonadoptive families and that these differences reduce the generalizability of findings from these studies. If this were the case, the restricted range could increase the likelihood that shared environmental effects will be underestimated. However, comparisons of adoptive and nonadoptive families have not supported this criticism and have shown that factors like parental anxiety and depression, family functioning, and peer group exposure are roughly equivalent for adoptive and nonadoptive families (Leve et al., 2007; McGue et al., 2007). In addition, for the constructs that do differ for adoptive and nonadoptive families (e.g., socioeconomic status [SES], parental antisocial personality disorder, and substance dependence), those differences are not related to child behavioral outcomes (McGue et al., 2007; Stoolmiller, 1999). A second possible limitation of adoption studies is that, if children are placed with adoptive parents based on certain characteristics (e.g., parental education), correlations between adoptive parents and adopted children could be inflated and consequently misinterpreted as environmentally mediated. This phenomenon is referred to as “selective placement” and can be empirically tested by correlating birth parent characteristics with adoptive parent characteristics; if they are uncorrelated, there is no evidence of selective placement. Selective placement has been assessed in adoption studies on the basis of characteristics such as personality, temperament, cognitive ability, 131

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and financial needs, and no evidence of systemic selective placement has been found (DeFries et al., 1981; Leve et al., 2013).

Combination Designs Although twin and parent-offspring adoption designs are the backbone of family-based genetic research, variations on these strategies help to refine the questions that can be addressed or increase the generalizability and/or power of the approaches. Sibling designs can be used in much the same way as twin designs (D’Onofrio, Lahey, Turkheimer, and Lichtenstein, 2013). Specifically, full siblings (i.e., children who have the same biological mother and father) are as genetically similar as DZ twins, sharing 50% of their segregating genes on average, although they are different ages and did not share their intrauterine environment. Half-siblings, who share 25% of their segregating genes, and stepsiblings, who share none of their segregating genes, are often present in families, especially because of the incidence of divorce and remarriage. In the same way that twin studies compare correlations between MZ and DZ siblings, sibling designs compare correlations between sibling pairs (e.g., full, half, and biologically unrelated siblings). Similarly, sibling adoption designs can be used in two different ways. More commonly, genetically unrelated siblings living in the same homes can be examined. These genetically unrelated siblings may be the result of two unrelated children being adopted into the home or of one child being adopted and another biological to the parents. A second type of sibling adoption design comprises genetically related (full or half ) siblings living in separate homes. In other words, one sibling is adopted, and the other child is parented by the biological parent(s). If correlations for biologically unrelated siblings reared in the same home are significant, researchers can conclude that shared environmental influences are operating (Deater-Deckard, Petrill, and Wilkerson, 2003), whereas correlations for biologically related siblings reared apart would bolster conclusions that genetic influences are at play (D’Onofrio et al., 2013). Children-of-Twins (COT) studies provide strong tests of causality between parent and offspring phenotypes by including data from twin parents and the offspring of both twins (D’Onofrio et al., 2003; McAdams et al., 2014). Children of MZ twin pairs share exactly 50% of their genes with their parent (Twin 1) and with their aunt or uncle (Twin 2), while children of DZ twins share just 25% of their genes with their aunt or uncle, like any other avuncular relationship. Yet the rearing environment of children of MZ twins is not shared as it is provided by different individuals. Similarly, the children of MZ twins share 25% of their genes with their cousin (like half-siblings), whereas children of DZ twins share 12.5% of their genes with their cousin, like any other cousin pair. This extended family design provides many combinations of family member correlations that can be compared to test specific hypotheses about genetic and environmental influences. Pertinent to the study of parenting, however, is that COT designs control for genetic and environmental factors that make biologically related family members living in the same household similar. Thus, by comparing parent-offspring correlations with avuncular correlations (i.e., the correlation between aunts/uncles and nieces/nephews) for MZ and DZ twin families, COT designs can test the extent to which parent-offspring associations are attributable to shared genetic influences (passive rGE) or withinfamily environmental influences. In other words, if there is greater similarity for children of MZ twins than children of DZ twins and the parent-offspring correlations are similar to the avuncular correlations for MZ twin families, then passive rGE would be indicated. If parent-offspring correlations are greater than avuncular correlations, associations between parent and child phenotypes are attributable to rearing environmental factors. An Extended Children-of-Twins (ECOT) design can more clearly distinguish among the effects of passive rGE, evocative rGE, and direct environmental influences because it can test bidirectional effects between parents and children (Narusyte et al., 2008). As shown in Figure 4.4, ECOT models add a child-as-twin design to the parent-as-twin design of a COT, essentially combining two separate 132

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but compatible samples (comparable on key demographic characteristics) to increase the power to detect child-specific genetic effects (McAdams et al., 2014). The COT portion of the design measures the parenting of twin parents and therefore can model the effects from parents to offspring (i.e., passive rGE or direct environmental), and the child-twin portion of the design measures comparable constructs from parents of twin children and can model the effects from offspring to parent (i.e., evocative rGE; Narusyte et al., 2008). To date, this powerful design is the only one in which passive rGE, evocative rGE, and direct environmental influences between parenting and offspring phenotypes can all be modeled simultaneously.

Summary Together, family-based genetic approaches rely on the varying degrees of genetic relatedness and shared rearing environment (or lack of a shared rearing environment) between individuals that naturally occur within families. Beyond identifying whether traits are heritable, these designs can identify and/or control for confounding genetic influences that account for similarity among biologically related family members to provide strong tests of environmental causation. Child- and parent-based designs (including twin and extended family designs) can provide evidence for passive and evocative rGE, adoption designs are well-suited for detecting evocative rGE and environmental influences, and more complex models parse passive rGE from environmental influences (COT) and passive and evocative rGE from direct environmental influences (ECOT). Therefore, the use of multiple genetically informed designs allows for stronger conclusions to be reached about links between parenting and child characteristics both in regard to how genes and environments may work together and for the role of environmental effects “free” from the effects of heredity.

Molecular Genetic Approaches Although molecular geneticists use a number of approaches (e.g., linkage association, candidate gene, and genome-wide association studies), we limit our discussion to approaches that have been used 133

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to study parenting, namely, candidate gene and polygenic risk score approaches. These approaches incorporate genotypic data known interchangeably as genetic variants or genetic markers, referred to here as variants. Genetic variants are selected because they index known or purported functional segments of the gene that may be causally related to the phenotype of interest. When these segments vary across individuals, they are referred to as polymorphisms. Genetic variants include single nucleotide polymorphisms (SNPs; variation in a single nucleotide base pair), variable number tandem repeats (VNTRs; variation in the number of repeated base pairs) in addition to other, less common genetic variants that will not be discussed here (Griffin, Schlomer, Cleveland, and Vandenbergh, in press). To illustrate, a study that helped launch widespread interest in candidate genes examined 5-HTTLPR, known colloquially as the serotonin transporter polymorphism (Caspi et al., 2003). The 5-HTTLPR polymorphism is a well-studied VNTR in the promoter region of the SLC6A4 gene. This variant exists as two alleles, long and short (16 and 14 repeats, respectively; Lesch et al., 1996), and the short allele causes low expression of the serotonin transporter (Bradley, Dodelzon, Sandhu, and Philibert, 2005). Individuals with at least one copy of the 5-HTTLPR short allele (s/s and s/l, known as “short carriers”) are compared to homozygous long individuals (l/l). The basic approach of candidate gene-by-environment interactions (cGxE) involves genotyping individuals and statistically testing the interaction between selected genetic markers and measured environmental characteristics on a phenotype of interest (Dick et al., 2015). This method has been employed to test child DNA as a marker of vulnerability or susceptibility to particular parenting behaviors. However, cGxE studies face a number of criticisms and have been difficult to replicate (Duncan and Keller, 2011). cGxE work requires large (i.e., greater than 1000) sample sizes to be sufficiently powered and studies have to failed to replicate previous research that used small to moderate sample sizes (Duncan and Keller, 2011; Karg et al., 2011; Risch et al., 2009). Furthermore, many published cGxE studies omit rGE entirely. Much like family-based genetic approaches, molecular genetics designs can be used to assess gene-environment interplay including rGE and GxE ( Jaffee and Price, 2007). When parents’ genetic markers are related to their parenting behaviors, it suggests passive rGE, whereas when child genetic markers are systematically related to parenting behaviors via child behaviors, researchers can infer evocative rGE. Certain genotypes may be linked with increased exposure to certain environments and significant cGxE findings may, in reality, be capturing rGE processes. The presence of rGE can be assessed by testing the direct association between genotype and environment; if they are correlated, methods must be employed to control for rGE before testing for GxE (Dick et al., 2015). One criticism of candidate gene work is that, ultimately, any single genetic variant accounts for only a tiny fraction of the variance in a complex phenotype. To address this criticism studies have used polygenic risk scores, which are sums of multiple genetic markers used to index genetic liability. To identify genetic variants of interest, both biologically based and data-driven approaches are used (Dudbridge, 2013; Griffin et al., in press; Nikolova, Ferrell, Manuck, and Hariri, 2011). Biologically based scores rely on extant literature to inform the selection of genes relevant to neurotransmitters (e.g., dopamine and serotonin) and biochemical pathways. Data-driven approaches like GWAS employ large sample sizes to identify genetic markers associated with the phenotype of interest. Polygenic risk scores have been used to test for evocative rGE at the molecular genetic level while controlling for passive rGE and as we review below, and suggest that, for the same PRS, there is evidence of both passive and evocative rGE depending on the parenting constructs examined (Elam et al., 2016, 2017). Molecular genetic approaches have been used to study correlates of parenting at the level of the gene. Candidate gene studies of parenting aim to identify genetic variants associated with parenting behaviors or, when genes are measured from the child, to identify individual differences in susceptibility to environmental factors, such as parenting. Early candidate gene work sparked widespread attention from genetic and nongenetic researchers, but concerns about the validity of 134

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these studies have followed difficulty with replicability, culminating in a number of journals, such as Behavior Genetics, Drug and Alcohol Dependence, and the Journal of Abnormal Child Psychology, establishing stringent criteria for the publication of such studies (Hewitt, 2012; Johnston, Lahey, and Matthys, 2013; Munafò and Gage, 2013). Another response to this issue has been the development of novel approaches, such as polygenic risk scores, that include multiple genetic variants used to disentangle passive and evocative rGE in a way that is complementary to statistical genetic approaches used in family-based genetic research. In the sections that follow, we review literature that uses the genetically informed designs outlined above to better understand the etiology of parenting. We segment this discussion by developmental period (i.e., infancy and early childhood, middle childhood, and adolescence). Within each section, we first discuss work on the heritability of parenting, then review findings about the genetic influences underlying links between parenting and child behaviors (“genetics on associations between parenting and child outcomes”), and finally examine evidence of GxE. While much of the extant literature relies on family-based genetic approaches, relevant findings from molecular genetic research are interspersed throughout the discussion.

Parenting During Infancy and Early Childhood Developmental studies of infancy and early childhood (birth–6 years) have typically highlighted characteristics such as parental sensitivity, hostility, and secure parent-child attachment as crucial for shaping children’s development. To date, very few twin studies have examined parenting in infancy. The Leiden and London Twin Studies consisted of infant twins and their families recruited from a twin registry in the Netherlands (Leiden) and from hospitals in the United Kingdom (London). Both studies measured parenting when infants were approximately nine months old and found that maternal sensitivity was explained by shared environment, with little evidence of heritability (Fearon et al., 2006). The same general pattern was found in the Quebec Newborn Twin Study (QNTS), which recruited a representative sample of families living in the greater Montreal area and assessed twins beginning at 5 months of age (Boivin et al., 2005). When the infants were 5 months old, mothers’ self-efficacy, perceived parental impact, and overreaction were all attributable to large shared environmental influences. Only mothers’ hostile cognitions towards their infants were heritable when assessed when the infants were 5 months old and again when the twins were 30 months old (Forget-Dubois et al., 2007). Together, these studies suggest that, for parents of infants, positive parenting characteristics may be less due to child-driven heritable effects. There is, however, a need for more research on parenting of infants using genetically informed designs, especially that including negative parenting of infants. During early childhood, twin and family studies have found evidence for heritability in some aspects of parenting with positive parenting constructs tending to be less heritable than negative parenting constructs. The Twin’s Early Development Study (TEDS) is a representative sample of twins in the United Kingdom who were assessed repeatedly beginning at age 2 (Oliver and Plomin, 2007). Findings from TEDS have shown that parental positivity is modestly heritable when twins are 3 and 4 years old with the bulk of variance explained by shared environmental influences. Parental negativity was explained primarily by heritable influences, with the rest of the variance explained by both shared and nonshared environmental influences (Alemany, Rijsdijk, Haworth, Fañanás, and Plomin, 2013; Knafo and Plomin, 2006; Larsson, Viding, Rijsdijk, and Plomin, 2008). In contrast, a study using data from 4-year-old children and their next oldest sibling (including full, half, and stepsiblings) participating in the Avon Longitudinal Study of Parents and Children (ALSPAC) found no heritability for maternal negativity with variance due only to equal amounts of shared and nonshared environmental influences, whereas mother report of their partners’ negativity toward the children was mainly heritable with some significant shared environmental influences (Deater-Deckard, Dunn, 135

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O’Connor, Davies, and Golding, 2003). The differences in findings for these two studies could be due to differences in measurement or to differences in the samples. For example, twin studies like TEDS are especially powerful for detecting heritable effects, while studies that include step or adoptive siblings like ALSPAC provide additional power for detecting shared environmental effects but are limited in their power to detect heritable effects due to the absence of MZ twins. Studies that measure parenting of young children observationally as well as via parent reports have shown that estimates of heritable and environmental influences also vary based on the method of measurement—generally, observational measures are less heritable than parent-reports, and estimates of shared environmental influences tend to be higher when parenting is measured observationally than when assessed via parent-report. For example, the TRACKS twin study, a study of 3-year-old twins and their primary caregivers who were recruited from central and southern England, explored the heritability of observed maternal behaviors and mother-reported parenting (Deater-Deckard, 2000). Overall, variance in observed parenting behaviors (i.e., positive and negative affect, harsh discipline, positive and negative control, and responsiveness) was primarily attributable to shared environmental influences with heritability estimates essentially zero. In comparison, maternal report of parenting (i.e., positive and negative affect) was largely heritable with some variance due to shared environmental influences. The Early Childhood Longitudinal Study–Birth cohort (ECLS-B), a nationally representative sample of same-sex twin pairs from the United States who were recruited at 9 months of age (Bethel, Green, Kalton, and Nord, 2005) has shown that variance in observed parenting supportiveness when twins were 24 months old was largely explained by shared and nonshared environmental influences (Roisman and Fraley, 2008). These findings may reflect that various measurement approaches capture different aspects of parenting. For example, in child-based designs, shared environmental influences on observed parenting may be due to shared rearing environment accounting for twin/sibling similarity, but it may also suggest passive rGE (i.e., parent’s genes influencing their parenting behavior). A handful of child-based twin studies has generally found that variation in mother-infant attachment is largely explained by shared environmental influences, suggesting passive rGE. This was the case for twins in the Leiden and London Twin Studies assessed in infancy with the Strange Situation, as well as twins from the ECLS-B assessed at 24 months of age with an attachment Q-Sort (Bakermans-Kranenburg, van IJzendoorn, Bokhorst, and Schuengel, 2004; Fearon et al., 2006; Roisman and Fraley, 2008). However, data from the Louisville Twin Study, a longitudinal study of infant twins who were assessed beginning in the 1970s, did not find shared environmental influences to be important for their measure of attachment. In this case, archival videos recorded when the twins were 24 months old were coded using a measure of security that is similar to the Strange Situation. The heritability estimate for attachment security was 25%, and the rest of the variance was attributable to nonshared environmental influences (Finkel and Matheny, 2000). This difference may be due to measurement differences, in that the Louisville Twin Study used a procedure in which co-twins were in the room for much of the procedure and were occupied with an activity during the separations. Moreover, Fearon and colleagues (2006) observed mothers from the Leiden and London Twin Studies interacting with their infants and found that the covariation between maternal sensitivity and infant attachment security was attributable to shared environmental influences. The same pattern was found for families in the ECLS-B; the covariance between attachment and parenting quality was explained by shared environmental influences (Roisman and Fraley, 2008). Using a candidate gene approach, some studies have investigated whether maternal genotype is associated with mothers’ sensitive behaviors towards their young children. Together, two ­dopamine-related genes, catechol-O-methyltransferase (COMT), dopamine D4 receptor (DRD4), and daily hassles each independently explained variance in maternal sensitivity (van IJzendoorn, Bakermans-Kranenburg, and Mesman, 2008). In the same sample, maternal oxytocin receptor (OXTR) and 5-HTTLPR were also associated with maternal sensitivity (Bakermans-Kranenburg and van 136

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IJzendoorn, 2008). However, a separate study found no association between maternal dopamine receptor D2 (DRD2) and maternal sensitivity (Mills-Koonce et al., 2007). These studies are subject to some of the criticisms of candidate gene work that we highlighted above, including a reliance on small sample size.

Summary of Genetic and Environmental Influences on Parenting During Infancy and Early Childhood The paucity of twin studies examining parenting during this developmental period which is characterized by rapid developmental changes, means that there is no clear consensus about the relative importance of heritable, shared, and nonshared environmental influences in infancy and early childhood. However, some conclusions can be drawn. First, negative aspects of parenting tend to be more heritable than positive aspects. Second, parenting assessed via observational measures tends to show evidence of shared environmental influences, whereas self-report parenting measures are typically heritable. Third, studies of parent-infant attachment generally detect shared environmental influences, which could be interpreted as passive rGE. Finally, candidate gene research has begun to explore whether parents’ genetic variants are associated with maternal sensitivity during this period.

Associations Between Parenting and Child Characteristics A surprising number of genetically informed designs have been used to explore links between parenting and infant and early childhood characteristics. As such, a breadth and depth of evidence have been amassed, with evidence for passive and evocative rGE as well as support that parenting is associated with child outcomes above and beyond shared heritability. Family-based designs have demonstrated that positive parenting qualities (e.g., positivity, warmth, reinforcement) are related to child behaviors via both heritable and nonheritable pathways (Boeldt et al., 2012). Within the TEDS sample, for instance, longitudinal associations across early childhood between parental positivity and child prosocial behavior were attributable to shared environmental influences (Knafo and Plomin, 2006). Data from the TRACKS study has shown that preschoolers’ cognitive ability and task orientation were related via shared environmental influences, which were mediated via SES and maternal warmth. Specifically, children from affluent families experienced increased maternal warmth, which in turn was linked to better cognitive ability and task orientation (Petrill and Deater-Deckard, 2004). Another form of positive parenting behavior, facilitative reading, was examined in the Northeast-Northwest Collaborative Adoption Project (N2CAP). N2CAP is a national survey of adoptive families and an in-depth assessment of a subsample of families, with a focus on socioemotional and cognitive development (Deater-Deckard et al., 2003). Within this study, adoptive parents’ reading behaviors with their children (e.g., time spent on books) were related to child literacy skills, suggesting that parents’ reading-related behaviors (i.e., shared environment) facilitates literacy independent of heritable influences on literacy which were not estimated in this study (Petrill, Deater-Deckard, Schatschneider, and Davis, 2005). Much of the information about parenting and its correlates in infancy and early childhood has emerged from a parent-offspring adoption study, the Early Growth and Development Study (EGDS; Leve et al., 2007, 2013). EGDS is a longitudinal, prospective parent-offspring adoption design that includes adoptive and birth families who were first assessed when adopted children were infants. EGDS is well-suited to test evocative rGE and GxE. For example, positive parenting behaviors have been linked to child outcomes across early childhood in a way consistent with a social transmission model. In one example, adoptive parents were observed interacting with their toddlers using a clean-up task at child age 18 and 27 months (Natsuaki et al., 2013). Bidirectional longitudinal effects between parenting and child social wariness indicated more directive behavioral commands (i.e., 137

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structured parenting) from adoptive fathers at age 18 months were associated with a decline in child social wariness from 18 to 27 months. In different reports using the same sample, adoptive parents’ use of structured parenting and maternal reports of higher levels of warmth were associated with fewer behavior problems in children (Leve et al., 2009; Reuben et al., 2016). Finally, adoptive mothers who were observed using positive reinforcement during a clean-up task had toddlers who later exhibited lower levels of callous-unemotional behaviors (Hyde et al., 2016). Taken together, findings from EGDS support rearing environment having a positive impact on child social and emotional development. Across infancy and early childhood, negative parenting characteristics have generally been studied more than positive parenting in behavioral genetic research. Rather than investigating GE interplay as discussed above, some studies have used an MZ twin differences approach to control for genetic confounds within families, enabling them to test whether parenting and early childhood characteristics are associated within families for nongenetic reasons. In an MZ twin differences approach the focus is on differences between the twins within the twin pair. This allows for direct estimation of nonshared environmental influences for MZ twins who were reared together. Therefore, if within MZ twin pairs, the twin who receives higher levels of negative parenting also exhibits higher levels of the child construct of interest (e.g., externalizing behavior) than the co-twin and if this occurs systematically across families, one can conclude that nonshared environmental factors influence the association between parenting and child characteristics. Using this method with a subsample of twins from the kindergarten cohort of the ECLS study (ECLS-K), parental withdrawal was related to lower child self-control (Wright and Beaver, 2005). This approach has also been employed with the Environmental Risk Longitudinal Twin Study (E-RISK), a child-based study of twins recruited from England and Wales when the twins were 5 years old that is notably one of the few twin studies oversampled to include high-risk families (based on maternal age at twins’ birth). Within families, differences in maternal negativity directed towards each twin were linked to differences in behavior problems (Caspi et al., 2004). In other words, differences within twin pairs’ environmental experiences explained the association between maternal negativity and child behavioral problems. The twin-difference method was also used with Japanese preschool-aged twins recruited from the Tokyo Twin Cohort Project (Ando et al., 2013). Twins were assessed longitudinally at 42 and 48 months and the best-fitting model indicated that differences in authoritative parenting were associated with differences in child peer problems at each time of assessment, but not longitudinally (Yamagata et al., 2013). Thus, within families, children who received more authoritative parenting had fewer peer problems at each time and this was not attributable to heritable characteristics. Family-based studies that explicitly model heritable and environmental influences have shown that negative parenting and child characteristics are linked via passive and evocative rGE. Within the QNTS, the covariation between maternal hostile cognitions and infant difficultness was explained by genetic influences with no evidence of shared or nonshared environmental contributions to this covariation (Boivin et al., 2005). Similarly, the covariation between parenting negativity and child behavioral and emotional problems was explained by common heritable influences for ALSPAC families (Deater-Deckard, et al., 2003) and for TEDS twins (Alemany et al., 2013) with no evidence for shared or nonshared environmental contributions to the covariation. Because these are heritable effects within a child-based design, these findings can be interpreted as evocative rGE. The TRACKS twin study of preschoolers found that parental negative affect and control were linked to child externalizing behavior problems (Deater-Deckard, 2000) with different patterns of heritable and environmental contributions to the covariance as a function of reporter. For observed measures, parenting and child behaviors were associated via shared environmental influences, whereas heritable influences explained these associations for parent-report (Deater-Deckard, 2000). Data from N2CAP and the TRACKS twin study, Deater-Deckard, Ivy, and Petrill (2006) demonstrated that, for children ages 3–8 years, associations between maternal harsh discipline and child 138

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externalizing behaviors was moderated by maternal warmth. The inclusion of both study samples allowed the researchers to test for passive rGE by comparing results in biologically related and adoptive families. Passive rGE would be indicated if harsh discipline and child externalizing behaviors were more strongly linked for biologically related mother-child pairs. Because this was not the case, the authors concluded that passive rGE was not at play, but this design does not allow for evocative rGE and direct environmental causes to be disentangled. A separate study found the covariation between parents’ use of corporal punishment and oppositional behavior in children was primarily due to heritable influences (suggesting evocative rGE) in the E-RISK sample ( Jaffee et al., 2004). However, the same was not true for the association between oppositional behavior and maltreatment; this link was primarily explained by shared and nonshared environmental influences. Thus, children’s heritable characteristics appear to evoke negative punishment, but child maltreatment does not appear to be elicited or evoked by the child’s heritable characteristics. A separate report of E-RISK families found that when fathers were engaged in caregiving during early childhood and exhibited high levels of antisocial behavior themselves, their children had the highest levels of behavioral problems; this was independent of the heritable risk of antisocial behavior ( Jaffee, Moffitt, Caspi, and Taylor, 2003). In other words, antisocial fathers’ presence in their children’s lives is an environmental influence that contributes to child behavior problems above inherited risk. A series of papers has examined parenting and child behavior longitudinally in TEDS. Knafo and Plomin (2006), for instance, found that heritable influences explained the longitudinal association between parental negativity and child prosocial behavior from preschool into middle childhood. Follow-up cross-lagged approaches have shown that, after controlling for stability over time, there is evidence for bidirectional effects between parenting and child behaviors that are attributable to both heritable and environmental effects (Lysenko, Barker, and Jaffee, 2013). For instance, “parent-driven” effects from parental negativity towards preschoolers to middle childhood antisocial behavior were primarily environmentally mediated, but the opposite “child-driven” cross-lagged effects between preschoolers’ antisocial behavior and parental negativity measured in middle childhood were mediated through heritable influences (Larsson et al., 2008). Similarly, parental negativity in the preschool years was linked to adolescent behavior problems, which was due to both heritable and shared environmental factors (Alemany et al., 2013). There were also effects of preschool child behavior problems on increased parental negativity when twins were adolescents, and this was attributable to heritable factors. Longitudinal work in EGDS has shown that negative parenting behaviors are associated with children’s heritable characteristics, suggesting evocative rGE. For example, infants whose birth parents had elevated psychiatric symptoms or higher levels of reward dependence evoked more negative parenting from both adoptive mothers and fathers (Fearon et al., 2015; Hajal et al., 2015). Elam and colleagues (2014) found that birth mother low social motivation was related to child low social motivation, and, in turn, those children experienced more hostility from their adoptive parents, suggesting evocative rGE. Similarly, toddlers whose birth mothers had more antisocial behavior symptoms had adoptive fathers whose negative parenting increased from 18 to 27 months (Klahr et al., 2017). Finally, birth mother and adopted child attention deficit hyperactivity disorder (ADHD) symptoms were indirectly associated via hostile parenting (Harold, Leve, Barrett, et al., 2013). Specifically, children with an inherited “risk” for ADHD symptoms were more impulsive which evoked adoptive mothers’ hostile parenting. In turn, hostile parenting was associated with later child ADHD symptoms. Because adoptive mothers and children are not biologically related, these paths are interpreted as evidence of evocative rGE. Other reports from the EGDS have demonstrated that parenting behaviors are related to changes in child characteristics, for what appear to be rearing environmental reasons. Lipscomb and colleagues (2011) found a main effect of adoptive parents’ overreactive parenting on child negative emotionality at 9 months of age and on increases in negative emotionality between 9 and 27 months. 139

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Similarly, there were direct links between adoptive parents’ harsh parenting at 9 months and toddler anger and frustration at 18 months, and adoptive parents’ hostile parenting was related to changes in toddler’s aggressive behavior from 18 to 27 months and from 27 months to 4.5 years (Rhoades et al., 2011; Stover et al., 2012, 2016). During the infant and toddler period, parents have direct environmental influences on child emotional development. Some candidate gene research has examined preschoolers’ characteristics as mediators between their genetic variants and the parenting they receive. In an innovative approach of candidate gene work within a child-twin design, Pener-Tessler and colleagues (2013) observed mothers interacting with their preschoolers, collected genetic data from both mothers and children, and asked mothers to rate their children’s self-control. The authors examined the serotonin transporter gene polymorphism and the inclusion of the twin design allowed them to test within- and between-family effects. There were only significant results for families with male twins. Within families, 5-HTTLPR genotype was related to both self-control and positive parenting. Short allele carriers exhibited more self-control and experienced more positive parenting, which is somewhat inconsistent with prior work that showed that the short allele is related to lower self-control under certain circumstances (Beaver, Ratchford, and Ferguson, 2009). Between families, the maternal 5-HTTLPR genotype was only related to positive parenting (short allele carriers exhibited lower levels of positive parenting) and when maternal genotype was added to the full model, child genotype remained a significant predictor of self-control. In other words, because child genotype was linked to self-control even when maternal genotype was accounted for, it strengthened the authors’ conclusion that evocative, rather than passive, rGE was operating. Competing models were tested to evaluate whether child self-control statistically mediated the relation between genotype and positive parenting or whether parenting mediated the relation between genotype and child self-control. The first model (child self-control mediating the link of child 5-HTTLPR to positive parenting), but not the second (positive parenting mediating link of child 5-HTTLPR to child self-control), was supported. Thus, for preschool boys, self-control appears to be a heritable behavior that evokes differential positive parenting within families (Pener-Tessler et al., 2013). Other work in singleton preschoolers suggests that child negativity mediates the relation between child OXTR and parent confidence (Kryski, Smith, Sheikh, Singh, and Hayden, 2014) and between child DRD2 and parental support (Hayden et al., 2010).

Summary of Associations Between Parenting and Infancy and Early Childhood Characteristics Child-based designs have shown that parenting during this developmental period is linked to child characteristics via a number of pathways. Positive parenting and young children’s behavior has received less attention than negative parenting but appears to be linked via both passive rGE processes and direct environmental paths. Links between negative parenting and child characteristics have been attributed to both passive and evocative rGE, as well as to nonheritable sources. Notably, multiple methodological approaches have been used to examine this developmental period and the findings bolster the assertion that parenting and child characteristics are associated for nonheritable reasons, suggesting causality. Within a longitudinal adoption design, for instance, positive parenting behaviors have been systematically linked to decreases in maladaptive child behaviors, whereas negative parenting behaviors have been associated with increases in maladaptive child behaviors, suggesting direct effects whereby parenting can “dampen” or amplify the effects of heritable risks. Other longitudinal, cross-lagged work has shown that negative parenting behaviors are related to child outcomes many years later via environmentally mediated pathways, whereas child behaviors are linked to later parenting via heritable pathways. Finally, research in molecular genetics explores child behaviors as mediators between children’s genetic variants and the parenting they receive. 140

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Gene x Environment Interaction Evidence of GxE using family-based genetic designs in infancy and early childhood has almost exclusively come from the EGDS. First, there are instances of inherited risk (as measured by birth parent characteristics) related to child characteristics but only in the context of parenting. Birth mother sociability was only related to adopted child social competence in middle childhood when adoptive mother responsiveness during toddlerhood was low (Van Ryzin et al., 2015). In the same vein, only at low levels of observerrated adoptive mother positive reinforcement during toddlerhood was birth mother antisocial behavior related to adopted child callous-unemotional traits measured 9 months later (Hyde et al., 2016). In other words, inherited risk indexed by birth mother antisocial behavior is linked to child callous-unemotional traits only for children who experience low levels of adoptive mother positive reinforcement. The EGDS has also found evidence that some adoptive parenting characteristics are related to child outcomes only in the context of inherited risk. Infants who experienced low adoptive mother responsivity exhibited higher levels of toddler fussiness, but only if their birth mother had a history of major depression (Natsuaki et al., 2010). Children whose birth mother reported higher negative affect exhibited greater levels of negative emotionality as toddlers when they experienced low adoptive parent overreactive parenting in infancy (Lipscomb et al., 2012). Fathers’ child-centered parenting in infancy is related to higher levels of toddler social inhibition, but only for children whose birth parents experience more anxiety symptoms (Brooker et al., 2016). For children whose birth mother had a history of social phobia, adoptive mother responsiveness in toddlerhood was linked to lower levels of toddler anxiety symptoms measured 9 months later, when the children were 27 months old (Natsuaki et al., 2013). Finally, Leve and colleagues (2009) found evidence of an interaction in which structured parenting during infancy buffered the effects of birth mother psychopathology on toddler behavior problems but amplified child behavior problems in the context of low levels of birth mother psychopathology. cGxE work in young children has largely focused on genetic markers purportedly associated with children’s sensitivity to environmental inputs. One of those markers, DRD2, has received such attention as a moderator of the relation between parenting and child outcomes. For instance, children who carried the DRD2 A+ allele and had mothers who were more sensitive exhibited fewer affective problems (Mills-Koonce et al., 2007). The same pattern was found for the link between parental intrusiveness and preschoolers’ clinical symptoms (e.g., anxiety, depression; Hayden et al., 2010). DRD2 has also been shown to moderate the association between parenting and the development of children’s physiologic responses. Propper and colleagues (2008) assessed infants’ respiratory sinus arrhythmia (RSA) withdrawal—an indicator of stress regulation—at three occasions over their first year of life. For A+ allele carriers only, high maternal sensitivity was linked to more change in RSA withdrawal over time, suggesting better regulation (Propper et al., 2008).

Summary of Gene x Environment Interaction During Infancy and Early Childhood For this age range, family-based GxE work has primarily used the EGDS. Findings from that study have supported models in which parenting can activate or amplify inherited risks as well as models in which parenting is linked to maladaptive child behaviors but only for children with particular inherited vulnerabilities. From a molecular genetic viewpoint, certain genetic variants are associated with child sensitivity to parenting “inputs”.

Summary of Parenting During Infancy and Early Childhood Family-based genetic studies of parenting during infancy and early childhood have primarily used child-twin or adoption designs. Evidence has accumulated to show that many aspects of parenting 141

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are influenced by their own heritable characteristics and that children’s heritable characteristics also evoke certain parenting behaviors, together underscoring the importance of controlling for familylevel heritable confounds when studying the effects of parenting. However, parenting and child characteristics are also linked via nonheritable pathways, strengthening the case of key assumptions of developmental theories that parenting causally impacts child development. A separate line of work has shown that certain combinations of inherited risk and experienced parenting characteristics lead to different developmental outcomes, highlighting that parenting has the potential to amplify inherited risk and that inherited risk may make children particularly susceptible to negative parenting. Molecular genetic studies have taken a few different approaches to examining links between genetic variants and parenting. Researchers have begun to explore mothers’ genetic variants that are associated with their own parenting sensitivity and have identified some candidate genes that may warrant further study (e.g., COMT, DRD4, OXTR, and 5-HTTLPR). Other work has examined children’s genetic variants (e.g., 5-HTTLPR) that may underlie behavioral qualities (e.g., self-­ control) that in turn evoke particular parental responses. Finally, cGxE work with young children has examined DRD2 as a marker of children’s sensitivity to their environment and has shown that A+ allele carriers show adaptive outcomes in the presence of sensitive parenting compared to noncarriers. At present, polygenic risk scores have not been incorporated into studies of parenting during this developmental period.

Parenting During Middle Childhood For parents of children in middle childhood (roughly ages 6–10 years), developmentalists have highlighted qualities like warmth and control as relevant for children’s development. Much like infancy and early childhood, most studies of parenting have used child-based designs and have given more attention to negative parenting behaviors. In one of the few parent-twin studies of parenting during middle childhood, twins who were parents of children under the age of 8 reported on their own positive and negative parenting (Losoya, Callor, Rowe, and Goldsmith, 1997). Positive support was mostly explained by heritable influences with the remaining variance due to nonshared environmental influences, while negative control was explained by moderate heritable influences and modest shared environmental influences. Heritability estimates in a parent-based design are evidence of passive rGE or of parents’ heritable characteristics influencing the way they parent. The Twins, Adoptees, Peers, and Siblings (TAPS) study takes a unique approach to understanding parenting in middle childhood by including “virtual twins”—same-aged siblings who are biologically unrelated (McGuire, Segal, and Hershberger, 2012). In this extension of the family-based design, five types of dyads were included (MZ, DZ, virtual twins, full siblings, and unrelated friend pairs), and both child-rated and parent-rated warmth were found to be significantly heritable, indicating evocative rGE. In contrast, a subset of adoptive and nonadoptive families from CAP who participated in the Colorado Sibling Study (CSS) with a school-aged child and a younger sibling were videotaped interacting with and without their mothers. The authors found primarily shared environmental influences on maternal affection, attention, and responsiveness, and heritable influences on observed maternal control of children, suggesting evocative rGE for maternal control (Rende, Slomkowski, Stocker, Fulker, and Plomin, 1992). In this age range, evocative rGE seems to be particularly relevant for negative parenting characteristics. In the TEDS sample, parental negativity at age 7 was explained by heritable shared and nonshared environmental influences, whereas at age 9 parental negativity was only explained by heritable and shared environmental influences (Larsson et al., 2008; Oliver, Trzaskowski, and Plomin, 2014). Moreover, at age 9 nearly half the variance in parental negativity was heritable, whereas heritability was only modest for parental warmth (Oliver et al., 2014). For a subset of 8-year-old twins from the TEDS using observational coding of an one-on-one cooperative task with their mothers, large heritable influences were found on observed maternal “extreme” control (coded when mothers 142

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interfered with their child’s turn in the task; Eley et al., 2010). A similar interaction procedure was used in the Twin Study of Behavioral and Emotional Development in Children (TBED-C; Burt and Klump, 2013), which consists of 6- to 10-year-old twins and their families. Maternal warmth rated continuously throughout the interaction was explained only by shared and nonshared environmental influences, whereas maternal control was explained by heritable, shared, and nonshared environmental influences (Klahr, Thomas, Hopwood, Klump, and Burt, 2013).

Summary of Genetic and Environmental Influences on Parenting During Middle Childhood Much like in infancy and early childhood, most parenting constructs measured during middle childhood show heritable influences. Because primarily child-based designs have been used during this developmental period, there is substantial evidence for evocative rGE. Shared environmental influences appear to play a larger role for positive parenting characteristics, such as warmth, than for negative parenting characteristics, such as control, indicating that positive parenting may also be subject to passive rGE or is influenced by other, nonheritable characteristics that are shared among families.

Associations Between Parenting and Child Characteristics Child-based twin designs have found that evocative rGE accounts, in part, for the association between negative parenting and child characteristics during middle childhood. For example, using data from the TBED-C children, the correlation between negative parenting and child aggression was explained by heritable influences (Klahr, Klump, and Burt, 2014). In other words, for negative parenting, evocative rGE was specific to child aggression, not rule breaking. In contrast, the covariation between negative parenting and child rule breaking was explained by shared environmental influences, indicating that there was no role for rGE in this association. Also within this sample, observed maternal control and child control during a cooperative interaction was explained by overlapping heritable influences, suggesting evocative rGE (Klahr et al., 2013). Evocative rGE was also suggested for the association between observed maternal extreme control during a cooperative task and child anxiety in 8-year-old twins participating in TEDS (Eley et al., 2010). Studies using the TEDS have systematically explored associations between negative parenting and child characteristics using a variety of approaches to clarify the role of heritable and environmental influences on associations between parenting and child behavior. Common heritable effects were found between negative parenting and children’s antisocial behavior when the TEDS twins were 7 years old (Larsson et al., 2008). A cross-lagged approach in TEDS compared MZ twins within families and found that differences in maladaptive parenting were related to differences in child selfcontrol longitudinally (Cecil, Barker, Jaffee, and Viding, 2012). In other words, because only MZ twins were included, the authors controlled for shared genetics and shared environmental effects, thereby examining only differences in parenting across the twins (nonshared environment). Moreover, longitudinal associations extended beyond middle childhood; differences in harsh parenting (but not differences in negative parental feelings) in middle childhood were related to within-twin pair differences in adolescent conduct problems. Finally, parental negativity (rated both by parents and children in TEDS) during middle childhood was related to child depressive symptoms in adolescence, and this was explained by common heritable influences, indicating evocative rGE (Wilkinson, Trzaskowski, Haworth, and Eley, 2013). Adoption designs have also examined associations between parenting and child behavioral outcomes during middle childhood. For families in the EGDS, marital hostility was associated with child externalizing problems via hostile parenting (Harold, Leve, Elam, et al., 2013). Because the adoptive parents and their child in the EGDS are not biologically related, this association can be interpreted as 143

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evidence of social transmission from parenting to child behavior problems. Across middle childhood and into adolescence, adopted children in CAP who were classified as “at risk” (based on birth parent antisocial behavior) experienced more negative control from adoptive parents compared to children with no birth parent antisocial behavior “risk”. This was the case only for negative parenting, not for warmth or inconsistency, and was interpreted as evocative rGE (O’Connor, Deater-Deckard, Fulker, Rutter, and Plomin, 1998).

Summary of Associations Between Parenting and Middle Childhood Characteristics Child-based twin designs during middle childhood have shown that children’s heritable characteristics, such as aggression and anxiety, can evoke negative parenting. However, this is not the case for all child characteristics, and certain parenting qualities, such as hostility, appear to impact child behaviors via nonheritable pathways. Notably, very little attention has been paid to whether positive parenting is related to child characteristics via rGE or nonheritable processes.

Gene x Environment Interaction Only a few studies have examined parenting within the context of GxE during middle childhood. One such study using the EGDS found that birth mother processing speed moderated adoptive mother uninvolved parenting. Specifically, uninvolved parenting was associated with school-aged children’s membership in an internalizing-only symptom group (as opposed to low-symptom group) only for children who lacked an inherited “risk” (birth mother slow processing speed; Roos et al., 2016). A second study using the TEDS sample found that negative parenting in middle childhood moderated heritable effects on adolescent depressive symptoms with larger heritable effects for children who experienced more negative parenting during middle childhood (Wilkinson et al., 2013). Finally, hyperactivity and inattention problems moderated the shared environmental influences between child conduct problems and negative parenting in 6-year-old twins assessed through the Tokyo Twin Cohort Project and the Tokyo Twin Cross-Sectional Survey (Fujisawa, Yamagata, Ozaki, and Ando, 2012). Shared environmental influences explained a larger proportion of the covariation between conduct problems and negative parenting for children with high levels of hyperactivity and inattention problems as compared to children with low levels. A possible interpretation of this finding is that within families, parents respond consistently to conduct problems when both children are highly hyperactive or inattentive, whereas parents respond less consistently to conduct problems when both children exhibit low levels of hyperactivity or inattention.

Summary of Gene x Environment Interactions During Middle Childhood GxE during middle childhood remains an area ready for investigation. To date, there is some evidence suggesting that negative parenting during this time may amplify inherited risk for psychopathology symptoms but may also lead to symptoms in the absence of inherited risk. One study suggests that parenting during middle childhood may have effects on child behavior longitudinally, at least into adolescence. Thus, middle childhood may be a particularly important developmental period for identifying early GxE that may have additional implications for adolescent functioning.

Summary of Parenting During Middle Childhood Middle childhood has received the least attention from behavioral geneticists who study parenting, but the literature in this developmental period strongly indicates that children are not passive 144

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recipients of parenting. Rather, most parenting constructs studied during this middle childhood show heritable influences in child-based designs, suggesting that children’s heritable characteristics evoke the parenting they receive. Moreover, while many findings from studies examining covariation between parenting and child characteristics support the importance of evocative rGE, there is specificity in which child characteristics operate via evocative rGE processes. Notably, during middle childhood, children can report on the parenting they experience with some studies including child reports of parenting and of child behaviors. As we review in the next section, estimates of heritable and environmental influences often vary by reporter, and thus including middle childhood reports of parenting may be one avenue for researchers to further pursue. Additionally, parenting during middle childhood has not yet received much attention from researchers interested in GxE and has been largely omitted from molecular genetics research.

Parenting During Adolescence In addition to the parenting qualities studied in other developmental periods, such as warmth and conflict, qualities that are relevant to adolescents’ increasing agency and the social world, such as autonomy granting and parental monitoring, have been examined in genetically informed designs. A few studies using parent-based designs have examined various parenting characteristics during adolescence and generally find significant heritable and nonshared environmental influences. For instance, adult twins reported on their own use of physical discipline and limit setting towards their children. There were modest heritable influences and large nonshared environmental influences on both physical discipline and limit setting, with no evidence of shared environmental influences (Wade and Kendler, 2000). German twin parents reported on their overprotective, authoritarian, supportive/indulgent, and rejecting parenting with all domains showing significant nonshared environmental influences (Spinath and O’Connor, 2003). In addition, individual differences in overprotective, authoritarian, and supportive/indulgent parenting were also due to moderate heritable influences, while the remaining variance in rejecting parenting was due only to shared environmental influences. Findings of significant shared environmental influences are notable because they reflect experiences common to family members, such as shared rearing experiences, which for adult twin parents are likely distal or diffuse experiences. In other words, shared environmental influences that continue to be important for adult twins could include family-of-origin rearing environment during childhood or less distal influences like current contact with their co-twin (or among family-of-origin members more generally). A separate study in which twin parents reported on their own care and overprotection behaviors found differences for mothers and fathers, with heritable influences on both parenting constructs greater for mothers than for fathers, whereas nonshared environmental influences were greater for fathers than for mothers (Pérusse, Neale, Heath, and Eaves, 1994). Shared environmental influences did not significantly explain variance in parenting in this report. Finally, parenting has been explored in the Twin/Offspring Study in Sweden (TOSS; Neiderhiser and Lichtenstein, 2008), a parent-based twin design that consists of families in which parents are twins and offspring are adolescents range from 11 to 22 years. Findings from this study are discussed in more detail below. Child-based designs have consistently found that both positive (e.g., positivity, monitoring) and negative (e.g., negativity, conflict, punitive discipline) parenting qualities during adolescence are heritable (Button et al., 2008; Elkins, McGue, and Iacono, 1997; Latendresse et al., 2010; Plomin, Reiss, Hetherington, and Howe, 1994; Reiss, Neiderhiser, Hetherington, and Plomin, 2000). For instance, in the population-based FinnTwin cohort of Finnish MZ and DZ twins, autonomy granting, knowledge, and warmth were all heritable (Latendresse et al., 2010). Likewise, within the MFTS, parenting qualities such as warmth, involvement, parent-child regard, and conflict have been found to be heritable with estimates greater for older adolescents relative to younger adolescents (Elkins et al., 1997; McGue, Elkins, Walden, and Iacono, 2005). Relative to positive parenting, negative parenting 145

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characteristics tend to show higher estimates of heritability (Button et al., 2008; Neiderhiser et al., 2004, Neiderhiser, Reiss, Lichtenstein, Spotts, and Ganiban, 2007; Reiss et al., 2000). For example, in the G1219 cohort of twins and siblings living in the United Kingdom, heritability was higher for punitive discipline than for constructive discipline (Lau, Rijsdijk, and Eley, 2006). Adolescents in the E-RISK study reported on their experiences of victimization between the ages of 12 and 18 years. In contrast to reports from the same twins at earlier ages that found no evocative effects ( Jaffee et al., 2004), there were substantial heritable influences and smaller but significant nonshared influences on maltreatment (Fisher et al., 2015). Together, this accumulation of evidence of heritability of parenting in child-based designs can be interpreted as evocative rGE. Much behavioral genetic research on parenting in adolescence comes from the Nonshared Environment in Adolescent Development (NEAD) study (Neiderhiser, Reiss, and Hetherington, 2007; Reiss et al., 2000). NEAD is a study of nondivorced and stepfamilies with same-sex adolescent twin or sibling pairs who were within 4 years of age of one another. Nondivorced families included, MZ, DZ, and full siblings, and stepfamilies included full, half, and genetically unrelated (step) siblings. Data from NEAD show that parents’ positivity, negativity, and monitoring were all explained by heritable influences, but that environmental estimates varied by reporter or assessment method (Plomin et al., 1994; Reiss et al., 2000). Parents’ reports of these constructs were also explained by substantial shared environmental influences, whereas adolescents’ reports were explained by modest shared environmental influences and large nonshared environmental influences. Observer ratings were primarily explained by shared and nonshared environmental influences; and heritability estimates were negligible (Neiderhiser et al., 2004). Similar patterns were found in an ethnically diverse sample of adolescent twins participating in the Texas Twin Project who reported on the parenting they received (Patterson, Cheung, Mann, Tucker-Drob, and Harden, 2017). For warmth and control, there were modest heritable effects, moderate shared environmental effects, and substantial nonshared environmental effects. In contrast to data from NEAD, however, there were no heritable influences on monitoring, which was primarily attributable to shared and nonshared environmental influences. One approach to clarifying if passive or evocative rGE (or both) are present is to assess the same constructs in parent- and child-based twin samples and compare the findings. Using this approach, data from NEAD (child-based) were matched with data from TOSS (parent-based). This comparison analysis showed five general patterns of findings that varied based on construct, parent assessed (i.e., mother or father), and reporter (i.e., parent, child, or observer) (Neiderhiser et al., 2004; Neiderhiser, Reiss, Lichtenstein, et al., 2007). First, a single construct, maternal monitoring, showed evidence of only passive rGE for both parent and child reports. Second, three constructs, maternal negativity, maternal control, and paternal control, showed evidence of only evocative rGE for both parent and child reports. Third, three constructs, maternal positivity, paternal monitoring, and paternal negativity, showed evidence of passive and evocative rGE for both parent and child reports. Fourth, interpretations for paternal positivity differed by reporter; father report showed evidence of only evocative rGE, whereas adolescent report showed evidence of both passive and evocative rGE. Finally, observer ratings of maternal positivity, negativity, and control showed no evidence of rGE. Taken together, for most constructs examined, parent and adolescent perceptions of parenting appear to operate under the same etiologic processes. Moreover, most parenting characteristics examined in this study suggest that both parents’ and children’s heritable characteristics impact parenting.

Summary of Genetic and Environmental Influences on Parenting During Adolescence Most parenting characteristics studied in adolescence show significant heritable influences, regardless of whether they were examined in a parent-based design or a child-based design. Because heritable influences have different interpretations depending on the type of design used, this suggests that for 146

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many characteristics during adolescence, both passive and evocative rGE are operating. For three out of four constructs, there was evidence of both passive and evocative rGE when systematically examined in both types of designs, with a caveat that conclusions depend on reporter and the parent being assessed.

Associations Between Parenting and Adolescent Characteristics Findings from NEAD suggest that both mother and father positive parenting are associated with adolescent outcomes such as antisocial behavior, cognitive agency, sociability, autonomy, social responsibility, and self-worth (Reiss et al., 2000). Moreover, the associations between these parenting constructs and adolescent outcomes are best explained by common heritable influences. Compared to positivity, parental knowledge of the child was less heritable in general and correlations with the adolescent outcomes listed above were somewhat weaker. However, the majority of the covariance between parental knowledge and adolescent outcomes was best explained by heritable influences. Particularly notable was that all of the heritable influences on fathers’ knowledge was also correlated with heritable influences on adolescent antisocial behavior and social responsibility. In contrast, when adolescent drinking frequency was examined in association with parental knowledge in the FinnTwin study the association between these constructs was predominantly explained by shared environmental influences (Latendresse et al., 2010). Differences between FinnTwin and NEAD may stem from different measurement approaches; the FinnTwin study used a combined measure of adolescents’ perceptions of both parents, whereas NEAD used a multi-rater approach and considered mothers’ and fathers’ parenting separately. Similar to earlier ages, much more attention has been given the role of negative parenting in adolescent outcomes. There is consistent evidence in multiple samples using a variety of research designs that negative parenting is associated with heritable adolescent characteristics, such as negative emotionality, antisocial behaviors, and depressive symptoms (Ganiban et al., 2011; Ge et al., 1996; Narusyte et al., 2007). Findings from the NEAD study indicate that maternal and paternal negativity are both associated with adolescent antisocial behavior, depressive symptoms, cognitive agency, and social responsibility, and that these associations can largely be explained by overlapping heritable influences (Reiss et al., 2000). One exception to this overall pattern of findings is adolescent self-worth; for both maternal and paternal negativity, inverse correlations with self-worth were best explained by nonshared environmental influences (Reiss et al., 2000). However, the overall pattern that negative parenting characteristics and adolescent outcomes are due to covarying heritable influences is consistent; within the G1219 cohort, for instance, heritable influences on maternal negativity were completely explained by heritable influences on oppositionality, delinquency, depression, and anxiety (McAdams, Gregory, and Eley, 2013) and overlap between punitive discipline and externalizing behaviors was attributable to heritable effects (Button et al., 2008). Generally, longitudinal work has further bolstered the claim that both evocative and passive rGE are at play in the parental negativity-adolescent outcome association. For instance, NEAD families were assessed twice during adolescence, 3 years apart. Cross-lagged models indicated that for both mothers and fathers, after controlling for stability and within-time associations, changes between parent negativity and adolescent antisocial behavior and depressive symptoms were due to heritable factors, indicating evocative rGE (Neiderhiser, Reiss, Hetherington, and Plomin, 1999). In a similar approach, a cross-lagged model using data from the MFTS collected when twins were 11 and 14 years old found bidirectional effects between parent-child conflict and adolescent externalizing behaviors. Unlike the findings from NEAD, both cross-lagged pathways were explained by approximately equal estimates of heritable, shared, and nonshared environmental influences (Burt, McGue, Krueger, and Iacono, 2005). It is possible that these differences are attributable to the shorter age range of MFTS adolescents. Finally, Moberg, Lichtenstein, Forsman, and Larsson (2011) measured 147

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parental emotional overinvolvement and adolescent internalizing symptoms repeatedly in the Twin Study of Child and Adolescent Development (TCHAD; Lichtenstein, Tuvblad, Larsson, and Carlström, 2007), a representative sample of adolescent twins living in Sweden. Using a cross-lagged design, they found that parental emotional overinvolvement was not linked to increases in internalizing symptoms later in adolescence, but that girls’ internalizing symptoms increased parental emotional overinvolvement. Moreover, this child-driven effect was attributable to significant heritable influences, suggesting evocative rGE. Two studies suggest that passive rGE is also important for associations between parenting and adolescent behavior. In the aforementioned QNTS, when twins were assessed at ages 13 and 14, initial maternal negativity was related to increased adolescent delinquency within a nongenetic model (i.e., one that included one randomly selected co-twin per family), but when these models were re-run including both twin members, the link between maternal negativity and later adolescent delinquency became nonsignificant (Guimond et al., 2016). In other words, once child heritable influences were controlled, maternal negativity was no longer associated with adolescent delinquency, suggesting a passive rGE process in which mothers who have an inherited predisposition to negativity towards their children have children who engage in more delinquent behavior. Similarly, a cross-lagged approach with MZ twins from the MFTS found that overall increases in parent-child conflict over time were not related to concomitant increases in adolescent externalizing problems, but for a subset of twin pairs with the most extreme differences in parent-child conflict, the co-twin with the worse parent-child conflict also had higher externalizing behaviors in mid-adolescence. This link was not due to evocative factors—in other words, those co-twins with the worse parent-child conflict did not have more initial externalizing behaviors. Therefore the authors concluded that there is evidence of an environmental effect between initial parent-child conflict and later externalizing behaviors (Burt, McGue, Iacono, and Krueger, 2006). The few COT and ECOT studies of parenting of adolescents confirm what the studies summarized above suggest—that parenting during adolescence can be evoked by adolescents’ heritable characteristics—but also support the assumption that some parenting characteristics are causally related to child characteristics for environmental reasons. For instance, a COT design using twin parents participating in the Australian Twin Registry examined whether twin parents who were discordant on their use of harsh punishment (i.e., use of more extreme physical discipline) had children who exhibited more behavioral problems (Lynch et al., 2006). This design controlled for family-level confounding factors and found that use of harsh punishment was associated with greater externalizing and substance use problems, strengthening conclusions of causality within the rearing environment. All other COT and ECOT studies of parenting have exclusively relied on data from the parent-based TOSS and either NEAD or TCHAD. In the first published ECOT study, Narusyte and colleagues (2008) combined TOSS and TCHAD data and found that adolescent internalizing symptoms evoked maternal emotional over-involvement and that this effect was via heritable, not environmental, pathways. Similarly, an ECOT design using TOSS and NEAD data found that adolescent externalizing behavior evokes parental negativity, indicating evocative rGE (Marceau et al., 2013). These findings can both be interpreted as evocative rGE. Different parenting constructs examined in those same studies appear to be causally related to adolescent characteristics. TOSS and TCHAD data, for instance, have been combined in an ECOT design that found differential effects for mothers’ and fathers’ criticism with adolescent externalizing behavior (Narusyte et al., 2011). For mothers, evocative rGE was present, such that adolescents’ heritable externalizing behavior evoked maternal criticism; that was not the case for fathers. For fathers, there was no evidence of rGE, but instead results indicated a direct environmental association between paternal criticism and adolescent externalizing behavior. In a different report (also using TOSS/TCHAD data), parental criticism was associated with adolescent somatic symptoms via environmental pathways, rather than rGE for both mothers and fathers (Horwitz et al., 2015). Similarly, an ECOT using TOSS 148

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and NEAD demonstrated that parental knowledge was related to decreased adolescent externalizing behaviors, not via heritable pathways but through mechanisms that suggest social transmission (Marceau et al., 2014). Finally, using a COT approach with the TOSS and TCHAD cohorts, Hannigan and colleagues (2017) found that the link between poor parent-child relationship quality and adolescent internalizing problems was not attributable to rGE but to environmental mechanisms. In summary, COT and ECOT designs are useful tools that demonstrate that different parenting constructs are subject to different etiological processes. Together, the few studies that have examined parenting and offspring outcomes using polygenic risk scores have found evidence for both passive and evocative rGE effects. Data from the Adolescent/Adult Family Development Project (Chassin, Rogosch, and Barrera, 1991), a multigenerational sample of families of alcoholics, sheds light on rGE processes at the measured gene level. This sample includes genotypic data from the second (mothers and fathers) and third generation (child) of study participants. Researchers created a polygenic risk score by combining genotypes (i.e., DRD1, DRD2, ANKK1, DDC, TPH2, CHRM2) that have been associated with behavioral under-control in prior literature. Both mothers’ and fathers’ polygenic risk scores were included in analyses, so the authors were able to control for passive rGE while testing for evocative rGE. There was evidence of passive rGE between parental risk score and parental monitoring but not family conflict (Elam et al., 2016, 2017). Additionally, there was evidence of evocative rGE between child risk score and parental monitoring, via child impulsivity. In the same sample, a different polygenic risk score composed of genotypes (i.e., DBH, GABA, GABRB1, PRKCE) that index adolescents’ response inhibition was created based on an independent GWAS of young adults’ Stroop Colorword performance. Higher scores were related to maternal inconsistency for boys whose parents met criteria for substance use disorder, which can be interpreted as evocative rGE (Wang, Chassin, Lee, Haller, and King, 2017). Finally, in a separate study of adolescents, Salvatore and colleagues (2015) tested whether a polygenic risk score for externalizing behavior that had been derived from a discovery sample of adults was also related to adolescent externalizing behavior. Even after controlling for parental history of externalizing symptoms, the risk score was related to adolescent externalizing symptoms. Moreover, adolescents with the highest risk scores who also experienced low parental monitoring exhibited the most externalizing problems (Salvatore et al., 2015).

Summary of Associations Between Parenting and Adolescent Characteristics In this developmental period, many parenting and adolescent characteristics are associated via heritable pathways and, particularly, are subject to evocative rGE processes. However, there are exceptions; links between some parenting and adolescent characteristics have shown significant shared and nonshared environmental influences, and longitudinal work has found evidence of passive rGE and environmental pathways. Moreover, ECOT and COT approaches have found evidence for two of the possible mechanisms (evocative rGE and environmental) linking parenting and adolescent characteristics. Externalizing symptoms appear to evoke parental negativity and maternal criticism via heritable pathways, and internalizing symptoms elicit parental emotional overinvolvement. In contrast, parental knowledge and paternal criticism are related adolescent externalizing symptoms via nonheritable pathways, as are poor parent-child relationship and adolescent internalizing symptoms. At the molecular genetic level, polygenic risk scores have been used to identify the measured genes purportedly underlying evocative rGE processes.

Gene x Environment Interaction Parenting moderates the heritability of adolescent externalizing behavior. In the FinnTwin study, parental monitoring moderated both heritable and shared environmental influences on smoking; at 149

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higher levels of parental monitoring when twins were 12 years old, heritable influences on smoking at 14 years were lower, whereas shared environmental influences were higher (Dick et al., 2007). In other words, higher levels of parental monitoring during early adolescence increased the effects of within-family similarity (shared environment) during middle adolescence at least in regard to smoking. In tandem, there was a corresponding decrease in the heritable effects on smoking. The same general pattern was found in NEAD families, but in this case, heritable, shared, and nonshared environmental influences on adolescent antisocial behavior were all moderated by parental negativity (Feinberg et al., 2007). Specifically, estimates of heritable, shared, and nonshared influences on adolescent antisocial behavior were all highest at higher levels of parental negativity. Additionally, heritable and shared environmental influences on adolescent antisocial behavior were moderated by parental warmth, such that heritability estimates were highest and shared environmental estimates were lowest at low levels of warmth. These findings indicate that, as the parent-adolescent relationship worsens, heritable influences on antisocial behavior increase. One way to interpret this moderation is that a parent-adolescent relationship characterized by low negativity or high warmth may dampen the genetically influenced propensity to engage in antisocial behavior during adolescence. These findings must be considered with caution, however, as the Feinberg et al. findings are cross-sectional. A more mixed pattern of findings was found for the G1219 cohort (Button et al., 2008). At low levels of maternal punitive discipline, there were higher heritable influences on externalizing, whereas there was the opposite for paternal punitive discipline—at high levels of paternal punitive discipline, there were greater heritable influences on externalizing (Button et al., 2008). Taken together these findings suggest that, in some cases, parenting characteristics or behaviors can buffer heritable effects on adolescent externalizing behaviors. While these studies conceptualized parenting as the moderator of the heritability of adolescent phenotypes, two studies to date have done the opposite and conceptualized adolescent phenotypes (i.e., temperament and personality) as moderators of heritability of parenting. Using the NEAD study, Ganiban and colleagues (2011) found that certain features of adolescent temperament moderated heritable and shared environmental influences on parental negativity even after taking possible rGE effects into account (Ganiban et al., 2011). For example, at higher levels of offspring negative emotionality or sociability, heritable influences on parental negativity were larger than at low levels of offspring negative emotionality. The opposite pattern was found for adolescent shyness, such that, at high levels of child shyness, there were diminished heritable influences on father negativity only. High negativity, emotionality, and shyness in the adolescent were all associated with decreased shared environmental influences on parental negativity. The authors interpreted these findings as a whole to indicate that parenting negativity becomes more child-specific when adolescents exhibit more challenging temperament characteristics. Data from the MFTS used a similar approach with a somewhat different pattern of findings. For adolescent twins, estimates of heritable, shared, and nonshared environmental influences on parental regard and conflict were moderated by adolescent personality factors (South, Krueger, Johnson, and Iacono, 2008). For instance, when adolescent positive emotionality was high, heritable influences on parental regard were highest and on parental conflict were lowest. Additionally, for parental regard, shared and nonshared environmental influences were moderated by positive emotionality, such that both were highest when adolescents exhibited low positive emotionality. It is possible that these differences are attributable to differences in constructs (temperament as opposed to personality), or that the NEAD study used parent-report whereas the MFTS used adolescent self-report and therefore the two studies capture different processes. Another published report from the NEAD study suggests that broader family characteristics, such as marital conflict about the adolescent and marital satisfaction, moderate the heritable and environmental influences on parenting (Ulbricht et al., 2013). Although there were some differences for mothers and fathers, patterns were generally consistent. When marital conflict was low, there was more variance in mothers’ negativity attributable to shared environmental influences; as 150

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levels of conflict increased, there were dramatic decreases in shared environmental influences on negativity. In contrast, when marital conflict was low, there was more variance in fathers’ negativity attributable to heritable and shared environmental influences. For both parents, at increasing levels of conflict, nonshared environmental influences increased. Marital satisfaction models showed that for mothers, at increasing levels of dissatisfaction, there were increasing heritable influences on parenting negativity. For fathers, as marital dissatisfaction increased, nonshared environmental influences on parenting negativity increased, but shared environmental influences decreased. One interpretation of this moderation is that, at higher levels of marital distress, children’s inherited characteristics impact mothers’ parenting negativity to a greater degree, while nonshared environmental factors become more important for fathers’ parenting negativity. One of the few genetically informed studies to include both parenting and culture combined data from the adult twins from the TOSS with data from the Keio Twin Project, a study of Japanese adult and adolescent twins (Shikishima, Hiraishi, Yamagata, Neiderhiser, and Ando, 2013). Twins recalled their experience of being parented before the age of 16 years for both their mothers and fathers in domains of warmth, authoritarianism, and protectiveness. Although phenotypic structures were similar for Japanese and Swedish twins, relative heritable and environmental influences differed by culture. For Japanese twins, except for maternal protectiveness (which was explained by moderate shared environmental influences), the covariation of warmth and authoritarianism was attributable to substantial heritable influences. In contrast, for Swedish twins, heritable influences on parenting were negligible and the covariation of the three parenting domains was explained by shared environmental influences. The significant heritability of parenting within the Japanese sample suggests that either parents were responding to their children’s heritable characteristics or that heritable characteristics impact the twins’ recall of parenting. Shared environmental influences on Swedish twins’ experiences of parenting suggest that within those families, parenting was not child-specific. Findings from the Child Development Project, a community sample assessed longitudinally, have reported GxE interactions at the molecular genetic level using genotypes that have been associated with alcohol dependence in adult samples. Within this cohort, there was an interaction between GABRA2 and parental monitoring on adolescent externalizing behavior trajectories. As parental monitoring decreased, the link between genotype and externalizing behavior became stronger (Dick et al., 2009). Similarly, Dick and colleagues (2011) found an interaction between several CHRM2 and parental monitoring on adolescent externalizing behaviors. Much like the previous study, as parental monitoring decreased, the link between the CHRM2 “risk” genotype and externalizing behavior increased. Two studies tested Differential Susceptibility Theory (Belsky and Pluess, 2009), namely that certain individuals are particularly sensitive to environmental inputs and fare best in positive environments and worst in negative ones due to genetic variation. Each used data from the National Longitudinal Study of Adolescent Health (Add Health; Harris et al., 2009), a nationally representative sample of adolescents in the United States, measured a compilation of purported “plasticity” genes, coded those genes based on the hypothesized effects (e.g., the genotype is associated with environmental sensitivity), and combined each genotype into a score indexing each participant’s overall genetic plasticity. In addition, both studies tested for evocative rGE prior to evaluating GxE by assessing whether each genotype was correlated with parenting. Belsky and Beaver (2011) found that for males who had higher plasticity scores across five genes (i.e., DAT1, DRD2, DRD4, 5HTTLPR, MAOA), negative maternal parenting was associated with poorer adolescent self-regulation, while positive maternal parenting was associated with better adolescent self-regulation compared to males with lower plasticity scores. The second study found that for adolescents with a high plasticity score based on four genotypes (i.e., DAT1, DRD2, DRD4, 5HTTLPR), maternal positive parenting was linked to the lowest levels of adolescent parenting stress when they themselves became parents (Beaver and Belsky, 2012) compared to individuals with low plasticity scores. Conversely, maternal negative parenting was linked to the highest levels of parental stress for adolescents with high plasticity scores. 151

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Summary of Gene x Environment Interactions During Adolescence Within the adolescent period, both family-based and molecular genetic designs have taken a variety of approaches to study parenting in a GxE framework. Some have conceptualized parenting as a moderator of the heritability of adolescent phenotypes, finding evidence that monitoring, warmth, negativity, and punitive discipline moderate heritable and environmental estimates on offspring phenotypes. Others have investigated child-level and family-level moderators of the heritability of parenting, finding evidence that etiology of parental negativity, regard, and conflict depend on child characteristics such as temperament. Finally, molecular genetic research has explored singular candidate genes as well as composites that interact with parenting to predict adolescent maladjustment.

Summary of Parenting During Adolescence The literature we have reviewed highlights that adolescents’ inherited characteristics evoke many types of parenting behaviors, lending further credence to the assertion that developmental work should take family-level confounds into account when examining links between parenting and offspring characteristics. In addition, some parenting constructs show evidence of passive rGE and direct environmental influences. Notably, innovative approaches, such as ECOT and polygenic risk scores, have only been employed with data collected within this developmental period. Findings from ECOT studies are generally consistent with other approaches used during adolescence and have found evidence of evocative and passive rGE as well as direct environmental effects, and polygenic risk score approaches have begun to examine rGE at the molecular genetic level, finding evidence of both passive and evocative rGE. Aside from some of the adoption work in infancy and early childhood, the bulk of genetically informed studies that measure fathers’ parenting has been conducted on adolescents. There are many consistencies across mothers and fathers, but studies that include both parents have elucidated some differences as well. For instance, in some parent-based designs, heritability estimates for mothers’ parenting are higher than for fathers’ parenting. Another example is evidence of environmentally mediated links between paternal criticism and adolescent externalizing behaviors, but genetically mediated links for maternal criticism and adolescent externalizing behaviors. In conjunction with findings indicating that heritable and environmental influences on some parenting constructs are differentially moderated for mothers and fathers, there is accumulating evidence that certain parenting processes, such as negativity, may differ for mothers and fathers.

Future Directions in Genetics and Parenting We conclude with a discussion of the mutual benefits that may be derived by a more thorough integration of family-based genetic research and typical developmental studies and the consequent implications for both theory and methods. Behavioral genetic designs that control for confounding genetic influences within families provide an opportunity to test crucial assumptions underlying many theories of parenting. Simultaneously, this work provides an impetus for a revision of existing theoretical models of development to incorporate findings from both areas of research (Moore and Neiderhiser, 2014). For instance, there is no clear theory to explain why there would be both direct (via child impulsivity) and indirect (via maternal hostility) evocative rGE processes between genetic predisposition for ADHD and child ADHD symptoms (Harold, Leve, Barrett, et al., 2013). Such revisions may aid in the clarification of developmental processes and may open new avenues of exploration. Critical to the future of family-based genetic research is adoption of some of the measurement used in developmental and family process research studies. Specifically, measurement of purported 152

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environmental features, such as parenting, are often assessed only using parent report in behavioral genetic designs. Studies that have used different approaches, many of them described above, show that the findings of heritable and environmental influences tend to vary as a function of the way the construct was measured, which may reflect that measures are capturing different aspects of related processes (Neiderhiser et al., 2004; Neiderhiser, Reiss, Lichtenstein, et al., 2007). Moving towards fine-grained observational assessments of parenting, as some genetically informed studies have begun to do (Klahr et al., 2013; Roben et al., 2015), may make behavioral genetics work more directly relevant to cutting-edge developmental methodology. Registry data have proven extremely useful for obtaining the large sample sizes necessary to understand low-prevalence phenotypes and to study diverse family configurations, thus providing additional and powerful support for the critical role of GE interplay in the etiology of problematic behaviors and psychopathology. However, a major drawback of studies that rely on registry data is that the level of detail one can obtain from registries tends to be limited. For instance, a series of studies using Swedish registry data has explored the link between parent and offspring psychopathology (e.g., criminal behavior, drug abuse) using complementary family-based designs (e.g., comparison of intact, step, and adoptive families) (Kendler, Ohlsson, Morris, Sundquist, and Sundquist, 2015; Kendler, Ohlsson, Sundquist, and Sundquist, 2016a; Kendler, Morris, et al., 2016). Kendler, Morris, et al. (2016) examined biologically related sibling pairs in which one sibling was reared with a biological parent at high risk for drug abuse and one was living with adoptive parents to estimate risk for drug abuse in the offspring. Compared to siblings living with their biological parent, adopted offspring had a significantly decreased risk for drug abuse. A similar pattern has been found for criminal behavior; moreover, this protective factor of adoptive environment is diminished if one of the adoptive parents had their own history of criminal behavior (Kendler et al., 2015; Kendler, Ohlsson, et al., 2016). Together, these findings suggest the rearing environment buffers a genetic liability for drug abuse or criminal behavior, but the mechanisms by which this occurs are unknown. We have limited our discussion of empirical behavioral genetics research to those that expressly measure parenting. However, parent-offspring designs have produced additional noteworthy findings relevant to parenting. For instance, Turkheimer, Haley, Waldron, D’Onofrio, and Gottesman (2003) found that SES moderated heritability estimates on children’s intelligence. For children in low-SES households, intelligence was explained by large shared environmental estimates and minimal heritable influences. For children in high-SES households, intelligence was explained by large heritable influences and minimal shared environmental influences. A possible interpretation of this is that the measure of SES is actually capturing meaningful differences in rearing environment and that these differences result in differences in how the heritable and environmental factors influence child intelligence. Similarly, an innovative and alluring finding from molecular genetics supports the concept of “genetic nurturing”—that nontransmitted alleles impact offspring via effects on the rearing environment (Kong et al., 2018). In this case, parent-offspring pairs were genotyped and a polygenic score was created based on a GWAS of educational attainment. The researchers found that parents’ nontransmitted alleles explained a significant proportion of variance in offspring educational attainment. While studies such as these offer exciting possibilities about the influence of parents on children, further work must explicitly measure parenting in order to conclude that such links are attributable to parenting. Moreover, for genetically informed designs to inform basic and applied developmental work, they need to include high-quality assessments of family processes that map onto what is being studied by developmentalists (Leve et al., 2017; Moore and Neiderhiser, 2014). Importantly, a number of studies described above have begun to do this (Boivin et al., 2005; Burt and Klump, 2013; Leve et al., 2013; Oliver and Plomin, 2007; Reiss et al., 2000). One aim for integrating the fields of behavioral genetics and developmental science is to use behavioral genetics findings to inform prevention and intervention research on child socioemotional problems (Harold et al., 2017; Leve et al., 2017). Heritability is not synonymous with immutability, 153

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and mean-level changes can occur within a phenotype without changing estimates of heritable, shared, or nonshared environmental influences (Maccoby, 2000). Applied work often relies on the assumptions that parenting is the catalyst for problematic child outcomes and that improving parenting will result in improved child outcomes. Yet, as discussed above, links between parenting and child behaviors could be under the influence of passive rGE, which would mean that interventions may target the wrong mechanism. By removing family-level confounds, it is possible to identify mechanisms to target that are more likely to be amenable to change. For instance, if evocative rGE is operating, parents could be taught skills to effectively respond to specific, relevant child characteristics (Harold et al., 2017). Leve and colleagues propose genetically informed interventions, akin to personalized medicine, that capitalize on identified GxE (Harold et al., 2017; Leve et al., 2017). Namely, interventions could be tailored to specific combinations of inherited and environmental risk (or protective) factors. In addition, by clarifying the timing of heritable or environmentally influenced developmental changes, it may be possible to identify sensitive periods particularly amenable to intervention. At the molecular genetic level, there is preliminary evidence suggesting that interventions can diminish the effects of heritable risks over time (Brody, Chen, Beach, Philibert, and Kogan, 2009), and gene-by-intervention research has suggested that genetic variants moderate the effects of intervention (Albert et al., 2015; Musci and Schlomer, 2017). Taken together, GxE findings and research can help to provide information about the characteristics that can diminish the impact of one’s risk factors or enhance the effects of one’s existing protective factors (Leve et al., 2017). While genetically informed intervention work is in its nascent stages, in practice, such an approach could involve choosing or modifying interventions based on an individual’s temperamental characteristics or genetic makeup. At present, the field of behavioral genetics could benefit from expanding the participant ages and ethnicities studied. Genetically informed studies of parenting are focused on early childhood or adolescence; GE processes specific to middle childhood are less well understood and work is just beginning to examine parenting beyond adolescence. Moreover, most of the samples comprising genetically informed designs rely on White samples (Fullerton, Yu, Crouch, Fryer-Edwards, and Burke, 2010; Knerr, Wayman, and Bonham, 2011). Because Scandinavian countries have a long history of excellent population-based record keeping, they have been the source of data for many registry-based analyses and by definition primarily include European-ancestry individuals. Furthermore, minority populations often endorse a distrust of genetic research rooted in historical mistreatment (Scharff et al., 2010). Although studies examining other psychosocial constructs have not found evidence of etiological differences based on ethnic heritage (Rowe, Vazsonyi, and Flannery, 1995), cultural contexts impact parenting and child development (Bornstein and Lansford, 2010; Kotchick and Forehand, 2002) and minority families may have systematically different sociocultural experiences that impact family functioning (Mcloyd, Cauce, Takeuchi, and Wilson, 2000) and warrant inclusion in family-based genetic research.

Conclusions In conclusion, we echo statements made by many prominent scholars about the importance of behavioral genetics for developmental science (Plomin, Owen, and McGuffin, 1994; Rutter, 2005; Scarr and McCartney, 1983). Findings from behavioral genetics have been misapplied in the past to support claims that what parents do does not matter for their children’s’ development (Harris, 1998), but we have summarized a number of studies above that highlight the bidirectional links between parents and children that exist beyond inherited characteristics. Importantly, genetically informed designs are a tool that can be used by developmental researchers to test crucial assumptions underlying many parenting theories. In other words, to conclude that parents do matter, we must adequately test the competing alternative hypothesis that they do not (Rutter, 2005). To do that, behavioral 154

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geneticists must collect measurements of parenting that are compatible with the high-quality developmental and family process approaches relevant to parenting.

Acknowledgments Research reported in this publication was supported by the Environmental influences on Child Health Outcomes (ECHO) program, Office of the Director, National Institutes of Health, under award number UG3 OD023389.

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5 PRENATAL PARENTING David A. Coall, Anna C. Callan, Julie Sartori, and James S. Chisholm

Introduction Because the factors that contribute to the development of a healthy newborn are so complex, understanding them requires insights from many disciplines. Crucial to this understanding is the role parents play. Through their behavior, psychology, and biology, parents influence the development of their children well before birth (Glover and Capron, 2017). In this chapter we review insights from evolutionary ecology that we believe help marshal what is known about prenatal influences on pregnancy, fetal development, and child outcomes into a more coherent whole. We focus in particular on the concept of maternal effects. Maternal effects are particularly influential across mammalian species where the interactions between the mother and offspring are close and over an extended duration. Humans are an extreme example due to our haemochorial placenta (Mossman, 1987). Through internal fertilization and gestation, the prenatal environment is the maternal domain, and mothers have the most profound influence on their developing offspring’s phenotype (Clutton-Brock, 1991). An individual’s phenotype is partly established through the contribution of genes from mother and father and the environment of development. Therefore, it makes sense that the paternal phenotype also influences prenatal development. This is the case in animals where the influence of the father’s phenotype is strong (Smiseth, Kölliker, and Royle, 2012). In humans the strength and consistency of paternal effects are still being established. Indeed, many of these paternal effects may work indirectly through the maternal social environment and phenotype (Figure 5.1). Therefore, in this chapter maternal effects provide a useful perspective for exploring influences of the maternal environment, parental behavior, maternal physiology, and placental and fetal growth. Maternal effects are the effects of the mother’s phenotype on her unborn child’s phenotype independent of the effects of her genotype (Figure 5.1). The mechanisms by which the maternal phenotype can affect the fetus’s phenotype include her behavior and hormone levels, nutrition, mental and physical health, and size. For example, across mammalian species smaller mothers tend to produce smaller offspring, not necessarily because of genetic inheritance but because of other constraints such as a smaller pelvic outlet or reduced nutrient supply to the fetus. Maternal effects are important for understanding fetal development and evolution, for they provide a mechanism for the nongenetic intergenerational transmission of phenotypes (Maestripieri and Mateo, 2009a, 2009b; Smiseth et al., 2012).

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Local environment Maternal development

Maternal phenotype

Maternal genotype Fetal genotype

Paternal genotype

Fetal development

Fetal phenotype

Paternal phenotype

Paternal development Local environment

Figure 5.1 Maternal effects are the effects of the mother’s phenotype on her unborn child’s phenotype independent of the effects of her genotype. This schematic incorporates the life history theory framework broadening the factors that contribute to maternal effects. The black represents the maternal effects are particularly influential in mammalian species. Source: Adapted from Cheverud and Wolf (2009).

Life history theory is the branch of evolutionary ecology devoted to the study of life cycles and how they change in response to environmental variability. Here we are concerned with the beginning of the life cycle and how the prenatal environment affects fetal growth and development and the subsequent neonatal phenotype. Like all life history traits, these prenatal traits are manifest in a “reaction norm”—the range of normal phenotypes that can develop from the same genotype in different environments. In what follows we show how a combination of maternal effects and life history theory makes sense of the abundant empirical evidence for prenatal influences. We focus on maternal psychosocial stress and nutrition, environmental toxins, and the crucial role of placental physiology and epigenetic processes in transducing these maternal effects to the fetus, subsequent postnatal growth, development, health, and potential for intergenerational, nongenetic inheritance. We aim for a multi-level synthesis, utilizing a broad evolutionary perspective to examine how organisms respond to their environment with specific physiological examples and their epigenetic regulation. We focus on one mechanism of prenatal development that embodies information about a broad range of maternal environmental factors in the fetus: the hypothalamic-pituitary-adrenal (HPA) axis (see Gunnar, Doom, and Esposito, 2015; Spencer, 2017). The HPA axis is highly conserved across vertebrate species and carefully aligns development with environmental stressors in species as distant to humans as the spadefoot toad (Denver, 1997). Stress hormones influence the expression of 10% of the genotype across metabolism, growth, repair, and reproduction (Phillips and Matthews, 2011) and

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are therefore able to adapt whole life cycles to adversity. During pregnancy, one specific mechanism involved in regulating the impact of maternal stress on the fetus is the enzyme 11beta-hydroxysteroid dehydrogenase type 2 (11β-HSD-2). This enzyme is involved in limiting the amount of maternal cortisol, a stress hormone that crosses the placenta from the mother to the fetus. Cortisol itself is involved in the epigenetic regulation of 11β-HSD-2. Moreover, during pregnancy the expression of 11β-HSD-2 is influenced by maternal stress, nutrition, hypoxia, reproductive hormones, and some toxins and pollutants. This mechanism interprets a range of maternal signals in ways that tend to ensure a more appropriate fit between the fetus and the environment into which it will be born than would otherwise be the case. We begin our review by examining the role maternal effects have in the interaction between development and evolution, culminating in modern epigenetics. The next section provides an overview of life history theory and parent-offspring conflict theory, focusing on the evolutionary consequences of environmental effects on the timing of life history stages. Then we review the impact of maternal stress and nutrition during pregnancy, two prominent maternal effects, on fetal development. The following section examines the impact of prenatal exposure to toxins on the growing fetus with focus on pollutants of emerging concern. Finally, we highlight future empirical and theoretical pathways suggested by our synthesis.

An Evolutionary-Developmental Framework: Maternal Effects, Evolution, and Epigenetics In this section we introduce evolutionary-developmental (“evo-devo”) thinking to frame our discussion of prenatal parenting and development. This perspective combines maternal effects, evolution, and phenotypic development. The evolutionary-developmental nature of prenatal parenting is illustrated through the epigenetic effects of maternal nutrition.

Maternal Effects Maternal effects are independent of the effect of maternal genes (Figure 5.1), but because they increase the intergenerational transmission of traits, and thus the fit between the offspring’s phenotype and its environment, they can provide an evolutionary advantage (Maestripieri and Mateo, 2009b; Smiseth et al., 2012). Maternal effects are particularly influential in mammalian species where the interactions between mother and offspring are close and prolonged, especially in humans. Pleistocene environments (our “environment of evolutionary adaptedness”; Bowlby, 1969, p. 50) were highly variable (Potts, 1996), but the prenatal environments our ancestral mothers provided children remained relatively constant; mothers are their unborn child’s environment (Caldji, Diorio, and Meaney, 2000; Coall, Callan, Dickins, and Chisholm, 2015). Selection is therefore expected to have favored fetal sensitivity to the effects of the maternal environment on her behavior and physiology—maternal effects. To be sure, paternal effects exist, but most operate indirectly, through the father’s effects on the mother. Some direct paternal effects have been reported, but need to be replicated with paternal age emerging as one of the best documented (Alio et al., 2012; Janecka et al., 2017). Although maternal effects have only recently been studied in humans (Bjorklund, 2006), their role in human evolution should not be underestimated. It is likely that critical characteristics of human social life evolved from maternal-offspring interactions, possibly beginning before birth, and were subsequently extended to a general system of prosocial behavior (Brazelton, Koslowski, and Main, 1974; Brown, Brown, and Preston, 2011; Cheverud and Wolf, 2009; Chisholm, 2017; Chisholm, Coall, and Atkinson, 2016; Hilbrand, Coall, Gerstorf, and Hertwig, 2017).

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Evolution Evolution results in biological change over time. Charles Darwin (1859) detailed this process with much empirical evidence and some abstract description, transforming a basic idea of gradual change over time into something very much more specific. As Godfrey-Smith (2010) noted, many scholars have tried to continue the abstraction that Darwin began in the later stages of On the Origin of the Species by Natural Selection. Here is a now-classic example: Darwin’s scheme embodies three principles: 1. Different individuals within a population have different morphologies, physiologies, and behaviors (phenotypic variation). 2. Different phenotypes have different rates of survival and reproduction in different environments (differential fitness). 3. There is a correlation between parental fitness and offspring fitness (fitness is heritable). These three principles embody the process of evolution by natural selection. While they hold, a population will undergo evolutionary change (Lewontin, 1970). Darwin’s own focus fell on evolutionary change within biological systems. Therefore, in terms of maternal effects we can see that maternal characteristics and behaviors that increase her offspring’s survival and reproduction would be selected for and increase in frequency in future generations. In the example above, the term differential fitness is used. From this point, the term inclusive fitness rather than differential fitness is adopted. Inclusive fitness is the sum of direct fitness, achieved through reproduction, and indirect fitness, achieved through the reproduction of genetic relatives. Modern evolutionary theory adopts this mid-level theoretical concept to capture life-history dynamics for individuals. The assumption is that organisms act to maximize their average lifetime inclusive fitness through a series of trade-off decisions across time. These decisions happen at all levels of biological organization and are captured by formal life history theory, which we discuss in the next section.

Phenotype From Genotype Waddington (2012) introduced the notion of the epigenotype and epigenetics to distinguish the complex set of processes that allow the formation of a phenotype from a genotype. “Epigenetics” is derived from epigenesis, and Waddington used the term to refer directly to developmental processes, as Pythagoras had before him. Waddington understood these developmental processes as being, to some extent, under genetic control. The amount of regulatory control could be referred to as the degree of buffering of an organism’s development relative to the perturbations of genetic and environmental variation. More famously, Waddington referred to developmental trajectories as more or less “canalized” as a consequence of such regulation. The discussion of development within the context of natural selection made Waddington a pioneer of evolutionary developmental biology (Haig, 2004). The information represented in a zygote’s DNA is derived from or is about the environments of its ancestors, not its current environment. Because environments change more-or-less constantly, this “old” information is not necessarily a good predictor of the zygote’s future environment. As Waddington (1969) put it, “The main issue in evolution is how populations deal with unknown futures” (p. 122). Development “buffers” the organism against unknown futures, the vicissitudes of changing environments, by enabling the developing phenotype to be affected by or to embody “new” information about the environment in which it develops. Because selection operates only on phenotypes,

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not genotypes, environmental effects on phenotypes can create novel phenotypes as targets of selection. Through canalization, genetic assimilation, epigenetic inheritance, and the many kinds of learning, novel phenotypes can become heritable. Indeed, developmental plasticity, the capacity of the phenotype to be affected by the environment in potentially adaptive ways, is an important driver of evolution (West-Eberhard, 2003).

Modern Epigenetics Evolutionary developmental biology has re-established itself within biology and more broadly within behavioral biology (Bateson and Gluckman, 2011; Jablonka and Lamb, 2005; West-Eberhard, 2003). Use of the term “epigenetics” has markedly increased (Haig, 2012). Histone modification is one mechanism that allows transcription regulation. The direct addition of a methyl group to cytosine on the DNA is another—and is most closely associated with the modern concept of epigenetics. Methylation of cytosine can prevent the binding of transcription factor and suppress transcription. Ultimately, methylation acts to silence gene expression. Specifically in terms of maternal effects, there is increasing evidence of perinatal methylation and a role for this form of regulation in parenting effects and environmental modification of behavioral phenotypes in animal models (Champagne, 2013; Youngson and Whitelaw, 2008). In this way, characteristics can be acquired or developmentally induced, and their effects transmitted to the next generation. These effects are the result of proximate epigenetic mechanisms acting to modify gene expression. In many ways, these mechanisms appear to be adaptations designed to calibrate organisms to their environment (Dickins and Rahman, 2012). There follows an illustration of epigenetic mediated calibration of an organism to the nutritional environment.

Epigenetic Effects of Maternal Nutrition Kuzawa (2005) introduced the concept of “intergenerational phenotypic inertia”. On the basis of extensive evidence that a mother’s birth weight is among the strongest predictors of her offspring’s birth weight (even more so after controlling for mothers’ gestational age at birth), Kuzawa revisited the hypothesis that the nutritional experiences of a mother when she was a fetus can affect the intrauterine nutritional environment that she provides her own offspring, especially her daughters (Ounsted, Scott, and Ounsted, 1986; Wells, Sharp, Steer, and Leon, 2013). Kuzawa noted that, among survivors of the Dutch Hunger Winter of 1944–1945 (Stein and Lumey, 2000), daughters who were exposed to their mother’s undernutrition were significantly lighter at birth than Dutch girls born between 1944 and 1946 whose mothers were not exposed to the Hunger Winter. Furthermore, individuals who were prenatally exposed to the famine showed— six decades later—less DNA methylation of a gene that regulates growth (IGF2) than their unexposed, same-sex siblings (Heijmans et al., 2008). Kuzawa’s intergenerational phenotypic inertia model provided an adaptationist rationale for expecting the effects of prenatal malnutrition or stress to last more than one generation: When environments are stochastic over time scales greater than a generation, 9 months of gestation cannot provide the fetus with enough information on which to “predict” its own, within-generation optimal growth and development (Nettle, Frankenhuis, and Rickard, 2013). Physiological adaptations to pregnancy that likely match future environments are encompassed within the “predictive adaptive response” (PAR) model. Therefore, Kuzawa argued, intergenerational phenotypic inertia provides the fetus with information, not only about the environment into which it will be born, but the environment into which its mother was born, and perhaps even its mother’s mother, and so on, back an unknown number of generations. Intergenerational phenotypic inertia “has the effect of limiting changes in growth rate in response to short-term ecologic fluctuations, and thus may allow the fetus to cut through the ecologic ‘noise’ of seasonal 170

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or other stochastic influences to read the ‘signal’ of any longer term nutritional trends in the local ecology” (Kuzawa, 2005, p. 17).

Conclusion A likely mechanism through which maternal effects work is Waddington’s view of epigenesis, now grounded in modern epigenetics. Histone modification and methylation allow a complex and varied array of alterations to gene expression, which in turn affect the phenotype. As the maternal behavior example demonstrated, methylation can occur in response to external inputs (in this case the maternal environment), not only affecting the current organism but also future generations. Moreover, the reversible nature of parental effects make them candidates for facultative (e.g., developmental) adaptations. In the following section, we present life history theory and facultative reproductive strategies as developmental trajectories that may help us organize our understanding of factors that influence prenatal development.

Evolutionary Theory and the Maternal Environment: Life History Theory and Parent-Offspring Conflict Theory A multitude of factors impact maternal and fetal phenotypes during pregnancy. No one discipline can encompass this diversity. In this section we use two evolutionary perspectives to broaden and organize our investigation of maternal effects (see Figure 5.1).

Life History Theory Life history theory is the branch of evolutionary theory devoted to the study of life cycles. It seeks to understand the evolution of the developmental processes that produce life history traits (e.g., length of gestation, number and size of offspring, interbirth interval, length of lactation, age and size at maturity, postreproductive lifespan, total lifespan; see Table 5.1). It views development as an adaptation for reproduction and life cycles as reproductive strategies—naturally selected patterns of growth

Table 5.1 The minimax and maximin reproductive strategies Reproductive strategy

Ecology Mortality rates Survivorship Population size Intra- and interspecific competition Traits favored by selection

Minimax: (r-strategy) maximize current reproduction more variable and/or unpredictable often catastrophic, nondirected, density independent low in early life more variable, nonequilibrium more variable, lax 1. rapid development 2. early reproduction 3. high reproductive rate 4. low parental investment 5. small body size 6. semelparity (large litters) 7. short lifespan

Adapted from Pianka (1970) and Reznick, Bryant, and Bashey (2002).

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Maximin: (K-strategy) maximize future reproduction more constant and/or predictable more constant, directed, density dependent high in early life more constant, equilibrium more constant, intense 1. slow development 2. delayed reproduction 3. low reproductive rate 4. high parental investment 5. large body size 6. iteroparity (small litters) 7. long lifespan

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and development for maximizing reproductive success under particular ecological conditions (Bonner, 1965; Charnov, 1993; Stearns, 1992; West-Eberhard, 2003). Maternal effects are nongenetic (Maestripieri and Mateo, 2009b), but the capacity to develop alternative reproductive strategies has a genetic basis. Reproductive success is fitness. By definition, fitness is measured in terms of an organism’s reproductive success (relative to others in its breeding population) but it consists of work—the work required to stay alive, grow and develop, and reproduce. The latter requires both the production of offspring (which increases their quantity) and rearing them (i.e., parental investment, which increases their “quality” [reproductive value; probability of producing grandchildren]). But work requires resources (e.g., energy, nutrients, time, information), which are sooner or later always limited. Because selection inexorably favors organisms with greater fitness—but greater fitness requires more resources—­ something has to give. Selection is therefore expected to favor organisms’ capacity to allocate their limited resources to the most pressing adaptive problems posed by their particular ecology—staying alive, growing and developing, producing offspring, or investing in them. Trade-offs are thus inevitable. Resources allocated to the production of offspring, for example, increases offspring quantity but reduce the amount parents can invest in each offspring, and thus reduce offspring quality. The most all-encompassing trade-off is that between current and future reproduction (Stearns, 1992). At issue is whether it would be better for an organism’s lifetime reproductive success to reproduce at a given time or to wait for another opportunity in the future. Consider a nursing mother. Would it be better for her lifetime reproductive success to continue nursing her current child, delaying future reproduction, or to wean now and have another (future) child? Continuing to nurse not only consumes maternal resources but has diminishing returns for the child’s fitness as it grows. At some point the lifetime fitness benefits accruing to the mother from continuing to nurse will be less than those she would receive if she ceased investing in her current child and had another. The trade-off between current and future reproduction will therefore be optimized according to the local environment. The major determinants of the optimal current-future trade-off are (1) the probability of death at a given age and (2) the availability of energy and other resources that determine parents’ capacity to invest in offspring. Mathematical modeling and evidence show that when environmental conditions are risky or uncertain, with high or unpredictable mortality rates and few or uncertain resources, organisms in general, including humans, tend to reproduce early and often (Coall, Tickner, McAllister, and Sheppard, 2016). Maximizing current reproduction reduces the chance of lineage extinction (by maximizing the probability that at least one offspring will survive), but it reduces the amount parents can invest in each, which only further reduces their probability of producing grandchildren. However, when conditions have been severe enough, long enough, parents have little to invest anyway, so downside risk protection against lineage extinction can be evolutionarily rational (Gillespie, 1977; Promislow and Harvey, 1990, 1991; Schaffer, 1983; Stearns, 1992). At the other end of the continuum, when environmental conditions are safe and predictable, with low and predictable mortality rates and plentiful, predictable resources, organisms tend to reproduce later and less often. Minimizing offspring number can be evolutionarily risky, but with low mortality rates this is not such a problem. By having fewer offspring parents can invest more of their relatively plentiful resources in each, thereby increasing their quality (growth and development), setting the stage for the production of grandchildren, great-grandchildren, and so forth in the future (Hill and Kaplan, 1999; Low, Hazel, Parker, and Welch, 2008; Placek and Quinlan, 2012; Promislow and Harvey, 1990, 1991). In summary, there is no a priori “best” reproductive (life history) strategy. The optimal strategy in one environment is unlikely to be optimal in another. Humans have a long evolutionary history of selection for developmental plasticity—the capacity to respond adaptively to environmental change—due to the rapid fluctuations of Pleistocene environments (Potts, 1996). Our ancestors were 172

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able to take advantage of good times by maximizing future reproduction (investing more in fewer offspring) and to cope with bad times by maximizing current reproduction (investing less in more offspring). None of this, of course, required conscious awareness, and the world’s most disadvantaged peoples still tend to reproduce early and often (Low et al., 2008).

Parent-Offspring Conflict Theory The most pressing adaptive problem for unborn mammals has always been to acquire the resources needed to grow and develop well enough to reach term. Consequently, the placenta (a fetal organ) has been under more intense selection than perhaps any other organ since it appeared in Eutherian mammals over 100 million years ago (Power and Schulkin, 2012). The consensus now is that the intensity of this selection was due to parent-offspring conflict. Fetuses would have been selected to extract more maternal resources and mothers would have been selected to resist, reserving resources for future offspring, resulting in positive feedback and a maternal-fetal “arms race” (Haig, 1993, 1996; Power and Schulkin, 2012; Wildman et al., 2006). Parent-offspring conflict theory (Trivers, 1974) holds that mothers and offspring—including unborn offspring—are naturally conflicted. Mothers share 50% of their genes with each fetus, but each fetus also shares 50% of its genes with its father, making mother-fetus conflict inevitable (i.e., the fetus shares 100% of its genes with itself ). The fetus is thus expected to seek more parental investment than would be optimal for mothers to provide because they seek to benefit themselves (copies of both parents’ genes). At the same time, mothers are expected to provide fewer resources than would be optimal for the fetus because mothers, too, seek to benefit themselves through copies of their genes in current or future offspring. Haig (1993, 1996) used parent-offspring conflict theory to model maternal-fetal interactions (see Figure 5.2). When conditions are good, mother-fetus conflict is minimal because each can afford to give a little. But when maternal resources are limited by environmental risk and uncertainty, any maternal investment in the fetus entails a trade-off. For every benefit a fetus gains from maternal resources (B in Figure 5.2), there will be a correlated cost to its existing or future siblings (C in Figure 5.2). Because the mother is equally related to all of her offspring, current and future, it is evolutionarily rational for her to invest equally in each according to their capacity to benefit from the resources invested. Therefore, mothers are expected to seek the best possible balance between the benefit to the existing fetus and the cost to its existing or future siblings. In other words, at some point (x1 in Figure 5.2), the increased benefit to the current fetus from mother’s continuing investment, will be outweighed by reducing the resources she could invest in existing or future offspring. Maternal-fetal conflict and the trade-off between offspring quantity and quality mean that fetal adaptations to the effects of environmental stress on the mother can have evolutionarily adaptive consequences for her (future reproduction) but developmentally disadvantageous effects on fetal growth and development and thus postnatal health. The intergenerational consequences may be related to the fact that, despite our species’ extraordinary reproductive success, human gestation is sensitive to the environment and characterized by high rates of early miscarriage, nausea and vomiting, and conditions such as preeclampsia, maternal hypertension, gestational diabetes, and preterm birth.

Prenatal Stress, Biological Mechanisms, and Developmental Outcomes in Offspring The prenatal period is a time of rapid cell division and differentiation. As with other periods of rapid growth, environmental insults can disrupt development. The uterus is an adaptation for supporting fetal growth and buffering the fetus against challenges that affect the mother. Here, we use the 173

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Benefit to fetus (B)

Benefit

Cost to Siblings (C)

Cost

x1 x0 Maternal investment in fetus (x) Figure 5.2 Representation of the trade-off between maternal investment in the current fetus versus existing or future siblings (x1 maternal optimum, x0 current fetus’s optimum). Source: Adapted from Haig (1996).

perspective of human evolutionary ecology to examine the impact of a range of stressors on development, including stressors in the maternal psychosocial environment, nutritional stressors, disease pressures, and exposure to toxicants in the local environment. We focus on these changes as potentially adaptive responses to environmental change that in some cases produce pathology.

Developmental Plasticity Plants and animals that develop in heterogeneous environments typically have the ability to alter their phenotypes in response to those environments (Bateson, 2017; Via and Lande, 1985). The response of an individual’s phenotype to this environmental variability is referred to as phenotypic or developmental plasticity (Stearns, 1982; West-Eberhard, 2003). Human developmental plasticity enables children to make unconscious “bio-assays” of their physical environments (Ellison, 1990, 1996) and “socio-assays” of their social environments (Chisholm, 1999a; Draper and Harpending, 1982). If these assays accurately predict the adult environment, they are likely to provide a fitness advantage (Bateson et al., 2004; Hill and Kaplan, 1999). Phenotypic changes (e.g., physiology, growth, mental health) induced by the environment are often presented as being programmed (Whimbey and Denenberg, 1967). We will use such terminology, but with caution. It is important to keep in mind that these changes are latent potentials, part of the individual’s norm of reaction, and are elicited by the environment, not created by it (Bateson, 2007). Moreover, these phenotypic changes, even in sensitive periods of development, are often modifiable (Bornstein, 1989), which ultimately keeps them open to intervention. Across multi-cellular species, an organism’s developmental environment can have consequences for its own growth, development, and reproduction and for those of its descendants (Bateson et al., 2004; Coall and Chisholm, 2010; Kuzawa, 2005; West-Eberhard, 2003). Evolutionists have focused on the intrauterine environment, the broad range of challenges that influence the uterine environment, 174

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and their consequences for fetal development and subsequent health: maternal effects on offspring phenotype (Wells, 2007). Reduced fetal growth is associated with higher rates of perinatal morbidity and mortality (Kramer, 1987) and an increased risk of developing coronary heart disease, hypertension, and diabetes in adult life (Barker, 1994, 2004). Experimentally inducing fetal growth restriction in animal models (via the administration of synthetic glucocorticoids, inducing maternal stress, controlling the maternal diet, or reducing placental function) results in cardiovascular, metabolic, and endocrine changes throughout childhood and even into adulthood (McMillen and Robinson, 2005). This burgeoning focus on the intrauterine environment has culminated in a new paradigm, the Developmental Origins of Health and Disease (DOHaD). Within the DOHaD paradigm, there has been a particular focus on birth weight, placental weight, and placental weight to fetal weight ratio (hereafter placental ratio) as indicators of the quality of the uterine environment. We examine these below.

Fetal Growth It is well known that reduced fetal growth predicts subsequent morbidity and mortality. In a review of the epidemiological literature, Kramer (1987) identified a number of maternal factors associated with intrauterine growth restriction (IUGR), including demographic and psychosocial elements of the mother’s environment, obstetric factors, nutritional status, morbidity during pregnancy, toxic exposures, and prenatal care. Placental efficiency plays an integral role in two of the three main causes of reduced fetal growth, which are (1) abnormal placental structure and/or function; (2) inadequate maternal supply of oxygen and/or nutrients due to either maternal factors or placental factors; and (3) decreased ability of the fetus to use the available supply (Brodsky and Christou, 2004). Increasingly, the role of maternal constraints on fetal growth—and even that of future generations— are receiving attention (Gluckman and Hanson, 2008; Kuzawa, 2005; Lewis, Cleal, and Hanson, 2012; Ounsted et al., 1986; Wells, 2003). For example, in a study of 513 low-risk pregnancies, Coall, Charles, and Salafia (2009) found that maternal birth weight was the only factor that consistently predicted children’s fetal and placental growth, affecting outcomes including birth weight, placental weight, placental ratio, placental surface area, and placental thickness. Birth weight is a crude measure of the quality of intrauterine environment (Salafia et al., 2008; Wilcox, 2001). From the perspective of life history theory, fetal growth is a measure of resource flow to the fetus (parental investment). A more direct measure of resource flow is provided by proportionate birth weight. Proportionate birth weight is the neonate’s birth weight as a proportion of the mother’s weight and represents the amount of parental investment made during gestation (May and Rubenstein, 1985). This characteristic remains remarkably constant at 5% across all placental mammals (Land, 1985). Proportionate birth weight has been used as a direct measure of resource flow to the fetus and, therefore, of parental investment throughout gestation (Coall and Chisholm, 2010). A range of insults have a measurable impact on the uterine environment and health in the next generation. However, much of the uterine environment is buffered against the maternal environment through placental adaptation.

Placental Weight and Placental Ratio The placenta is the common filter through which maternal effects pass. Placental growth and development are strongly correlated with the growth trajectory of the fetus and have a major influence on birth weight (Salafia et al., 2005, 2008). The placenta has evolved to provide a protected environment to support fetal growth, buffering the developing organism from maternal effects, environmental insults (Lewis et al., 2012; Wooding and Burton, 2008), and preparing it for the postnatal environment it is likely to inhabit (Gluckman, Hanson, Spencer, and Bateson, 2005). 175

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The functional efficiency of the placenta may be challenged by disturbances in the maternal environment, such as poor nutrition, obesity, illness (e.g., diabetes, hypertension), smoking, medications, and maternal stress (Sibley, Brownbill, Dilworth, and Glazier, 2010; Tegethoff, Greene, Olsen, Meyer, and Meinlschmidt, 2010). Other known modulators include maternal factors, such as country of origin, weight at birth, height, age, and parity (Kiserud et al., 2017). Although beyond the scope of this chapter, male and female placentae consistently show different physiological responses to changes in the maternal environment (Terrade, Panchenko, Juneir, and Gabory, 2015; Rosenfeld, 2015). The effect of such disturbances may create adverse intrauterine conditions resulting in adaptations (that are often under endocrine control) by the placenta (Coan et al., 2010; Myatt, 2006). The placenta, as a metabolically active tissue, also plays a role in sensing the flow of nutrients, modulating the allocation of resources between the mother and fetus to maintain pregnancy (Dimasuay, Boeuf, Powell, and Jansson, 2016). Facultative metabolism provides the placenta with the capacity to adapt to challenges, for example by increasing surface area and signaling pathways to extract more nutrients when maternal nutrient levels fall (Sibley et al., 2010). In the long term this adaptation may be associated with poorer adult health outcomes (Dimasuay et al., 2016); however, when the placenta is not able to adapt in the short term, adverse outcomes for the fetus can result (Sandman and Davis, 2010). In epidemiological studies, the role of the placenta is often extrapolated from placental weight. Placental weight is generally associated with placental function (Robinson, Owens, de Barro, Lok, and Chidzanja, 1994). Like birth weight (Godfrey, Breier, and Cooper, 1999; Harding, 2001; Wilcox, 2001), placental weight is the end product of a chain of events that include the growth and development of the placenta throughout gestation (Barker and Thornburg, 2013; Coall et al., 2009; Salafia et al., 2005). As with other aspects of biology, early beneficial adaptations that improve survival can have later costs in morbidity and shortened lives (Kirkwood and Austad, 2000). DOHaD research has shown that a high placental ratio is associated with higher blood pressure throughout childhood (Moore et al., 1996) and into adulthood (Moore, Cockington, Ryan, and Robinson, 1999) and may predispose individuals to adult illnesses, such as hypertension, glucose intolerance, blood coagulation disorders, and coronary heart disease (Barker, 1997; Barker, Bull, Osmond, and Simmonds, 1990; Forsén, Eriksson, Tuomilehto, Osmond, and Barker, 1999; Forsén et al., 1997; Law, Barker, Bull, and Osmond, 1991; Phipps et al., 1993). Some researchers, however, have found a U-shaped association between placental ratio and coronary heart disease in men (Martyn, Barker, and Osmond, 1996). Others have found an association between placental weight, but not placental ratio, and subsequent blood pressure (Blake et al., 2001; Whincup, Cook, Papacosta, and Walker, 1995; Williams, St George, and Silva, 1992), some have found sex differences (Taylor, Whincup, Cook, Papacosta, and Walker, 1997), and others have found no effects of gender (Burke et al., 2004; Leon et al., 1996; Martyn et al., 1995; Matthews, Lewis, and Bethel, 1994). It may be that a relatively large placenta does not directly cause adult disease but reflects the quality of the fetal supply line throughout gestation (Robinson et al., 1995). However, animal and human studies have both shown that placental size and placental ratio play important roles in fetal adaptation to the maternal environment (Faichney and White, 1987; Godfrey, 2002; Kingdom, 1998; Robinson et al., 2001; Steyn et al., 2001). In remarkable accord with the theoretical predictions from Haig’s (1993) application of parentoffspring conflict theory to the uterine environment, the DOHaD perspective proposed that increased placental ratio was an adaptive placental response to intrauterine growth restriction (Barker et al., 1990). Initial studies involving sheep showed that moderate dietary restrictions at various times during pregnancy were associated with increased placental weight (Faichney and White, 1987). The placental growth was interpreted as “an attempt by the fetus to compensate for the reduced supply of nutrients in the maternal blood” (Faichney and White, 1987, p. 373). This compensatory mechanism maintained fetal growth in the ewes that had their diets restricted late in pregnancy, and may actually have increased the resource flow to the fetus when the dietary restriction was removed. It must be

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recognized, however, that, although similar responses have been documented in humans, the picture is over-simplified. Importantly, the timing of dietary restriction and the previous nutritional state of the ewes are known to influence placental responses (Barker et al., 1993; Robinson et al., 2001). In a natural experiment, Lumley (1998) reported that women conceiving or in the first trimester of pregnancy during the Dutch Famine Winter of 1944–1945 had relatively heavy placentae, while birth weights remained static. Lumley interpreted this finding as compensatory placental growth in response to reduced maternal nutrition. Both animal (Robinson et al., 1994) and human models (Wheeler et al., 1994) supported this interpretation. These findings reflect the importance of the timing of maternal effects.

Environmentally Appropriate Adaptation, Not Pathology This application of evolutionary theory challenges the common perception that increased placental weight is pathological (Lao and Wong, 1999, 2001). For example, infants born at high altitudes have reduced birth weights (Mayhew, Jackson, and Haas, 1990), higher placental weights (Kruger and Arias-Stella, 1970), and show structural changes that improve the efficiency of oxygen transfer between mothers and fetuses (Mayhew et al., 1990; see review by Zamudio, 2003). This placental adaptation can improve fetal growth (Mayhew, Jackson, and Boyd, 1993). Moreover, there is evidence that increased placental size can improve fetal survival. In appropriate-for-gestational-age infants of insulin-dependent diabetic mothers, a higher placental ratio is associated with an increased likelihood of offspring survival (Evers, Nikkels, Sikkema, and Visser, 2003). Increased placental size in insulindependent diabetic pregnancies are likely to reflect the larger placenta necessary to maintain a fetus when the placenta is less efficient (Lao and Ho, 2002). More generally, placental adaptation to the uterine environment, which maintains fetal growth, is a normal process of pregnancy (Pardi, Marconi, and Cetin, 2002). Therefore, pregnancies in which the placentae show evidence of compensatory growth resulting in increased placental ratios may actually represent appropriate responses to suboptimal maternal/uterine environments of diverse origin in the short term, rather than pathology itself (Adair and Thelander, 1925; Fox, 2000; Kaplan, 2008). DOHaD, as the name suggests, is interested in this developmental plasticity because of its impact on health. Differential reproductive success, however, is what drives evolution and placental function is crucial for successful reproduction (Lewis et al., 2012). Postnatal pathology arises when the trade-offs with other components of fitness entrain developmental trajectories that increase shortterm survival at the cost of ill-health and premature mortality in the future. These costs include low birth weight, preterm birth, altered stress reactivity, rapid childhood growth, early reproductive development, and short lifespans. If these costs minimize the chance of lineage extinction—that is, if they increase the chance of reproducing at all in the harsh or unpredictable environments that cause them—they may also be evolutionarily rational (Borgerhoff Mulder, 1992; Chisholm, 1999a; Harpending, Draper, and Pennington, 1990; Stearns, 1992). In summary, life history theory views many of these changes as adaptations to environmental challenges, including maternal effects that maximize survival and, ultimately, reproduction. We turn now to the impact, first, of maternal stress on early development, second, the role of maternal nutrition, and, last, the increasingly apparent role of toxicants in the environment. We begin by discussing the meaning of “stress”.

Stress, Stressors, and Adaptive and Maladaptive Coping Environmental stress affects development and does so in potentially adaptive ways by entraining alternative reproductive strategies (Belsky, Steinberg, and Draper, 1991; Chisholm, 1993; Worthman,

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1999). “Stress” has long been a slippery concept, with considerable disagreement about its meaning (Cohen, Kessler, and Gordon, 1995; McEwen, 1995). We view stress generally as a broad range of environmental challenges, including social-emotional or psychosocial, inadequate nutrition, and toxicants. We focus first on the psychosocial stress entrained by the perception of negative life events, a fairly objective measure of environmental risk and uncertainty (Cohen et al., 1995). We refer to the other stressors as biological stressors. These are factors such as malnutrition, disease, toxicants, and material poverty and include the physiological and energetic stressors associated with them (Ellis, 2004; Ellison, 1990; Thayer and Kuzawa, 2011). Therefore, biological stress represents situations of reduced biological resource availability. It must be emphasized that, although we treat psychosocial and biological stressors as independent factors, they should not be seen as mutually exclusive because there is considerable interplay between them and they are often inseparable (Chisholm, 1999a; Coall and Chisholm, 2010). The survival, growth and development, and reproduction of all organisms always depend on biological resources (e.g., nutrition, disease), but because of our species’ reliance on cooperation, social exchange, and sharing to gain access to these resources, our life history, as with most other primates, depends on the availability of psychosocial resources. Any analysis of psychosocial stress must consider individual differences in the ability to cope with or adapt to stressors (Ellis, 2004). Paramount for our intensely social species is the social-emotional support that can dramatically enhance individual coping styles, life satisfaction, and sense of control (Compas, Slavin, Wagner, and Vannatta, 1986; Steptoe and Marmot, 2003; Suldo and Huebner, 2004; Thoits, 1982). These psychosocial resources serve as buffers against the cumulative cost of constantly adapting to environmental challenge (allostatic load; McEwen, 1995) and are known to reduce the impact of stressful life events on adult health (Compas et al., 1986; Greenberg, Seltzer, Krauss, Chou, and Hong, 2004; Kaplan, Cassel, and Gore, 1977; Patterson and McCubbin, 1984). Stress has a direct effect on adult outcomes, such as mental health, and an indirect influence via the impact it has on relationships that constitute these psychosocial resources (McEwen, 2000; Thoits, 1982). Everything else being equal, an increase in the level of psychosocial stress results in a reduced availability of psychosocial resources (Ellis, 2004; Taylor and Seeman, 1999). Therefore, psychosocial stress not only puts wear and tear on an individual’s physiology but also consumes valuable psychosocial resources. From an evolutionary perspective, coping with psychosocial stress is work, and like any other work, it requires resources, in this case, social-emotional resources. In adulthood, the social support provided by family and friends is important for adjustment to life events (Runtz and Schallow, 1997). Across cultures, social support and social networks are associated with less depressive symptomatology during pregnancy and after childbirth (Byrd-Craven and Massey, 2013; Surkan, Peterson, Hughes, and Gottlieb, 2006). Although the evidence is not conclusive (Bryce and Stanley, 1991), social support interventions during pregnancy can reduce the rate of low birth weight births (Norbeck, DeJoseph, and Smith, 1996). The association between social support and birth weight appears to operate through improved fetal growth rather than longer gestation (Feldman, Dunkel-Schetter, Sandman, and Wadhwa, 2000; Rothberg and Lits, 1991). In a study of 3,073 low-income women receiving general psychosocial services during pregnancy, social support was associated with a reduced risk of delivering low birth weight babies (Zimmer-Gembeck and Helfand, 1996). It is clear that people employ both adaptive (e.g., social support) and maladaptive (e.g., alcohol and nicotine) coping mechanisms. The interacting influence of prenatal stress and social support on fetal growth and development is mediated by poor maternal coping mechanisms that include risky health behaviors (Orr et al., 1996; Zuckerman, Amaro, Bauchner, and Cabral, 1989). Lack of social support is an important determinant of smoking (McCormick et al., 1990; Rodriguez, Bohlin, and Lindmark, 2000) and prenatal weight gain (Hickey, 2000). Maladaptive coping strategies elevate stress hormones, influence nutrition and exposure to toxins during pregnancy, and lead to poor fetal development (Sandman and Davis, 2010).

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Maternal Stress During Pregnancy and Early Development Before Barker’s work in the late 1980s, the question was whether stress during pregnancy could affect fetal or child development (Bryce and Stanley, 1991). However, because of his work and rapid progress in DOHaD, the questions now are: how does maternal stress affect the developing fetus or child, what are the mechanisms whereby these early effects might predispose poor adult health, and to what extent do these adult effects constitute evolutionarily adaptive “programming” of the fetus’ or child’s developing physiology and organ systems by the maternal environment? (Sandman, Davis, Buss, and Glynn, 2012). It is now established that across mammalian species prenatal stress affects offspring development in response to changes in maternal resource provision (Berghänel, Heistermann, Schülke, and Ostner, 2017). There is now abundant evidence that maternal psychosocial stress during pregnancy is a risk factor for abnormal pregnancy/delivery, fetal abnormalities, and poor adult health. The effects of stress on the mother include the premature rupture of membranes, preeclampsia, excessive weight gain, and preterm labor and birth (Dole et al., 2003; Newton, Webster, Binus, Maskrey, and Phillips, 1979); those on the fetus include reduced fetal growth and low birth weight (Newton and Hunt, 1984; Wadhwa, Sandman, Porto, Dunkel-Schetter, and Garite, 1993), which in turn are associated with increased infant and child morbidity and mortality, impaired psychological development, and increased morbidity in adulthood (Istvan, 1986; Tegethoff et al., 2010). Most research into the effects of maternal stress during pregnancy has used either subjective self-ratings of anxiety/depression or more objective measures of stressful life events (e.g., cortisol). Because the two measures do not predict the same outcomes, different pathophysiology pathways seem to be involved (Richardson, Zorrilla, Mandyam, and Rivier, 2006; Tegethoff et al., 2010). For this reason alone, research on prenatal influences must be multivariate, incorporating (1) objective indices of stressful life events, (2) individuals’ subjective impressions of their stressors and their meaning, (3) their own and others’ responses to these stressors, and (4) the biochemical, physiological, neuroendocrine, and immunological mechanisms involved.

Biological Mechanisms of Maternal Stress The steroid hormone cortisol is a key component of the HPA axis, the “fight or flight” response of all vertebrates. It has two evolutionary functions, one short term, the other long term. Its shortterm function is to maximize the probability of survival in the face of some immediate threat. For example, negative life events typically (but not always, as is commonly thought) activate the HPA axis that stimulates the adrenal cortex to release glucocorticoids (cortisol). This response is adaptive in the short term in that it helps to maintain homeostasis in the face of environmental (including social-emotional) challenges (Cohen et al., 1995; McEwen, 1995; Repetti, Taylor, and Seeman, 2002; Selye, 1957; Tsigos and Chrousos, 2002; Wingfield and Sapolsky, 2003). Its long-term function is developmental: Cortisol is essential for immune function, glucose metabolism, and fetal (e.g., brain) development and the maturation of fetal organs (e.g., lungs; Lupien, McEwen, Gunnar, and Heim, 2009; Reynolds, 2013). Growing up in a chronically risky or uncertain environment entails chronic threats, chronic psychosocial stress, and chronic HPA activation. In chronically risky and uncertain environments the optimal reproductive strategy is to maximize current reproduction through accelerated development and early childbearing. Chronic psychosocial stress and high levels of cortisol “predict” risky or uncertain environments and may help to entrain evolutionarily adaptive developmental responses (Finch and Rose, 1995; Worthman, 1999; Worthman and Kuzara, 2005). The stress response begins with the hypothalamus, which integrates the nervous and endocrine systems. Stress, defined as any challenge to the body’s homeostasis (McEwen, 1995; Selye, 1957),

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activates the HPA axis. In response to a stressor, the hypothalamus releases corticotrophin-releasing hormone (CRH), a peptide hormone that travels through local blood vessels and binds to receptors on the plasma membranes of cells in the anterior pituitary gland. This stimulates the production of adrenocorticotropic hormone (ACTH), which enters the blood and travels around the body, having its primary influence on the cells of the adrenal gland. ACTH acts on the cortex of the adrenal gland to stimulate production of glucocorticoids (GCs), steroid hormones that include cortisol and corticosterone (Gunnar et al., 2015; Nakamura, Sheps, and Arck, 2008). The hypothalamus also directly influences the adrenal medulla via the sympathetic nervous system. Neurons of the sympathetic nervous system from the hypothalamus synapse in the adrenal medulla and release the hormones epinephrine and norepinephrine. These hormones stimulate rapid, organism-wide responses to a stressor in the form of an elevation in heart rate, respiratory rate, and release of energy reserves in preparation for quick responses to environmental threats (Sapolsky, 1994). Because steroid hormones can cross the plasma membranes of cells, the effects of glucocorticoids are mediated by glucocorticoid receptors (GRs), which have been identified in the cells of almost all tissues within the body. GCs regulate a variety of important functions and are essential for life in adult mammals. Excessive levels of GCs, however, potentially affect many internal systems by dysregulating biological homeostasis (Nakamura et al., 2008). Fetal exposure to GCs and CRH is essential for fetal growth and development, but excess levels can be detrimental. During pregnancy, due to the elevation of maternal CRH levels, maternal GC production and secretion are increased. High levels of GC hormones are necessary due to their potent and long-term effects on cellular function in almost all organ systems, particularly in regard to cellular differentiation and homeostasis (Burton and Waddell, 1999). Later in pregnancy, exposure to GCs is essential for the maturation of fetal organs and systems (Ellman, Dunkel Schetter, Hobel, Glynn, and Sandman, 2008). Throughout pregnancy, while fetal and maternal neuroendocrine functions are largely independent, with placental barriers to most maternal hormones, they still interact (Lester, Marsit, Conradt, Bromer, and Padbury, 2012). Approximately 10%–20% of maternal GCs cross the placenta to the fetus (Seckl and Meaney, 2006). Gitau, Cameron, Fisk, and Glover (1998), examining the relation between maternal and fetal cortisol levels, showed that, while fetal levels are lower than maternal levels (indicating the metabolism of 80%–90% of maternal cortisol by the placenta), the two are correlated, but not with gestational age. Even so, a 10%–20% contribution of maternal cortisol to the fetus could still double fetal concentrations. This study also measured the amount of unmetabolized cortisol crossing the placenta at 15%. Although most cortisol is metabolized by the placenta, high maternal concentrations can affect fetal concentrations because 40%–50% of fetal cortisol is derived from the mother (Gitau et al., 1998). Cortisol also plays a central role in fetal programming of adult disease (Harris and Seckl, 2011; Reynolds, 2013; Seckl and Holmes, 2007). Circulating GCs that potentially influence the tissues of the body are regulated by the 11β-HSD enzymes: 11β-HSD-2 inactivates cortisol, converting it to the inactive cortisone; conversely, 11βHSD-1 activates cortisone back into cortisol, increasing local CG levels in tissues. In the placenta, circulating maternal GCs, including cortisol, are metabolized by 11β-HSD-2 into its inactive form, cortisone (Benediktsson, Calder, Edwards, and Seckl, 1997; Brown et al., 1996). These placental enzymes catalyze and modulate ligand access to the glucocorticoid receptor (GR). Therefore, the 11β-HSD enzymes are referred to as the feto-placental barrier to maternal GCs. Because GCs are potent and have long-lasting effects, changes in the maternal environment that increase GC exposure may persist long after the original insult, thus acting on tissue accretion, differentiation and programming of the fetal HPA axis (Fowden, Giussani, and Forhead, 2005), changing baseline levels for physiology, metabolism, and behavior (Lester et al., 2012; Seckl and Meaney, 2006).

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Edwards, Benediktsson, Lindsay, and Seckl (1993) proposed that low levels of 11β-HSD-2, and concomitant over-exposure to maternal cortisol, reduced fetal growth and programmed adult disease risk. Since then, it has been shown that overexposure of GCs to the fetus reduces fetal growth, increases the risk of developing hypertension and metabolic disorders, and inhibits fetal HPA axis development (Burton and Waddell, 1999; Seckl, 1997). Moreover, Stewart, Rogerson, and Mason (1995) showed a positive association between placental 11β-HSD-2 activity and birth weight. In humans, 11β-HSD-2 activity is inhibited by medical disorders involving increased fetal exposure to cortisol, such as pre-eclampsia, maternal asthma, and intrauterine growth restriction (O’Donnell, O’Connor, and Glover, 2009). Moreover, a deficiency in 11β-HSD-2 is associated with fetal growth restriction and increased risk of hypertension in adulthood (White, 2001). Maternal stress down regulates 11β-HSD-2 in both animal and human studies (Glover, Bergman, Sarker, and O’Connor, 2009; Mairesse et al., 2007). Thus, elevated levels of maternal stress can down regulate 11β-HSD-2 activity, allowing more maternal cortisol to cross the placenta and reduce fetal growth. Maternal environments that activate the HPA axis, thereby raising cortisol levels, can also affect CRH levels and lead to preterm birth. Questionnaire studies linking measures of perceived stress, stressful life events, racism, and domestic violence with preterm birth suggest that maternal stress shortens gestation (Istvan, 1986). Increased levels of stress hormones have also been associated with preterm birth (Wadhwa et al., 1993). Rather than involving GCs suppressing CRH, as in the hypothalamus of nonpregnant individuals, the relation between GCs and CRH during pregnancy is stimulatory, with levels of both rising throughout gestation (Ellman et al., 2008; Reynolds, 2013; Sandman and Davis, 2010). In response to maternal cortisol, the feto-placental unit activates the placental CRH gene, increasing placental CRH synthesis and secretion to the fetus. This stimulates the maternal pituitary to release ACTH, and thus cortisol from the maternal adrenals. Maternal cortisol again stimulates CRH, creating a positive feedback loop and potentially high fetal exposure to GCs. By the end of pregnancy, cortisol levels are up to three times higher than nonpregnant levels. High levels of CRH are also involved in the cascade of events resulting in uterine muscle contraction and parturition, thus preterm birth. Preterm birth is directly correlated with low birth weight and suboptimal development of the brain and other tissues and organs. Resulting adverse outcomes include structural changes in the brain, negative temperament, impaired cognition, and the developmental programming of adult pathophysiologies such as metabolic and cardiovascular diseases (Mairesse et al., 2007; Reynolds, 2013; Sandman and Davis, 2010). From our evolutionary perspective, however, maternal stress-induced preterm birth, low birth weight, and their sequelae may not represent pathology so much as the adaptive response by mother and fetus to their respective risky or uncertain environments (Ellman et al., 2008), for three reasons. First, elevated maternal stress hormones, whether due to psychosocial stress, undernutrition, or exposure to environmental toxins, may accelerate maturation of fetal organs and systems in preparation for a “predicted” shorter gestation. Second, in high-risk environments, where the probability of survival for mother and fetus is reduced, maternal-fetal competition for resources increases and maternal stress hormones may allocate resources away from the fetus to the mother, resulting in fetal growth restriction but increasing the mother’s chance for “predicted” future reproduction (Haig, 1993; Stearns, 2005). Third, mother and fetus may “versusadapt” to each other as a unit, compromising on the allocation of maternal resources (Kölliker, Royle, and Smiseth, 2012) so that nutrient flow to the fetus simply reflects maternal condition and access to resources (Coall and Chisholm, 2003; Dimasuay et al., 2016; Jansson and Powell, 2013). In all of the above, apparently detrimental maternal stress effects on the fetus might represent adaptive fetal programming for survival and growth and development in the risky and uncertain environment that caused the mother’s stress in the first place—and therefore “predict” that such risk and uncertainty will continue in the future (Gluckman et al., 2005).

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Stress During Pregnancy and Developmental Outcomes The human capacity for developmental plasticity means that maternal prenatal stress can have deleterious effects on fetal development and future health and/or evolutionarily adaptive programming effects. The nature and duration of the maternal stress, together with the timing of impact during gestation, determines the severity of fetal developmental outcomes, depending on the stages of development and the number of organs and systems affected (Fowden et al., 2005). We review below a number of factors associated with stress during pregnancy to illustrate the diverse impacts prenatal stress can have. Fetal brain development commences during the third week post-conception with structural development of the central nervous system (CNS) extending to week 20 of pregnancy, providing ample opportunity to incur insults that may result in impaired development (Kurjack, Medic, and Salihagic-Kadic, 2004; Moore, 1989). There is strong evidence that stress has an impact on fetal development of the brain and CNS, including effects on brain morphology, receptor density and sensitivity, CNS function, and the activity of the autonomic and neuroendocrine systems (Stanton, Lobel, Sears, and DeLuca, 2002). GCs play an important role in the survival and maturation of CNS neurons as different regions of the brain express GRs at different stages of development, enabling selective effects of stress throughout gestation (Lupien et al., 2009; Nyirenda, 2006; Seckl and Meaney, 2006). The fetal brain also appears to silence 11β-HSD-2 expression and activity during gestational weeks 19 to 26, indicating the role of GCs in aspects of brain development (Nyirenda, 2006). Animal studies show that excessive GC exposure in utero influences hippocampal and related complex functions, including cognition, behavior, memory, versusordination of autonomic activity, and importantly, the regulation of the endocrine systems (Seckl and Meaney, 2006). These programming effects on the hippocampus include fetal HPA axis deregulation. The HPA axis is sensitive to excessive GC exposure in utero, with repeated animal studies showing that excessive GC exposure during development permanently alters HPA axis function, accounting for exaggerated HPA axis reactivity in adulthood (Nyirenda, 2006). The hippocampus expresses both types of corticosteroid receptors (GRs). There is also evidence that increased levels of GCs are associated with decreased receptor expression in the hippocampus, resulting in hypersensitivity and increased reactivity of the HPA axis (Nyirenda, 2006; Seckl and Meaney, 2006). We turn now to the evidence that the impact of GCs on the CNS and HPA axis reactivity translates into changes in postnatal behavior, cognition, and mental health.

Behavior, Cognition, and Mental Health Mounting evidence shows that overexposure to GCs in utero leads to modifications in adult behavior in a number of species (Seckl and Meaney, 2006). In humans, prenatal exposure to elevated maternal stress hormones is associated with behavioral and emotional disturbances during both infancy and childhood (Sandman and Davis, 2010). In one of the first studies of the impact of prenatal stress on the subsequent behavioral adjustment of children, O’Connor, Heron, Golding, Beveridge, and Glover (2002) found, in a longitudinal sample of 7,448, that women who were in the highest 15% of the sample for anxiety at 18 or 32 weeks of pregnancy had children who were 2 to 3 times more likely to be 2 standard deviations above the sample mean for total behavioral and emotional problems at 4 years of age. The association between prenatal maternal anxiety and filial behavioral problems remained after controls for birth weight, potential maternal confounders (age, socioeconomic status), pregnancy related anxiety, behavioral mediators (smoking and alcohol use), and postnatal (8 weeks) depression and anxiety. This adjusted analysis suggests that, barring the potential influence of maternal weight and postnatal parenting practices, the impact of prenatal anxiety was direct (i.e., 182

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not through fetal growth, maternal behavioral modifications, or postnatal anxiety and depression). Prenatal anxiety and postnatal depression both independently predicted childhood behavioral and emotional adjustment problems, and this effect persisted to 7 years of age (O’Conner et al., 2002; O’Conner, Heron, Golding, and Glover, 2003). Unfortunately, the authors did not control for birth length, which (in a later study with the same sample) was shown to be negatively associated with total behavior difficulties, hyperactivity, and conduct problems at 7 years of age (Wiles et al., 2006). Subsequent to these studies, a veritable feast of investigations has examined these associations in detail and analyzed the physiological mechanisms involved. In a review of 32 studies, Korja and colleagues (2017) found a consistent association between maternal prenatal stress (or anxiety) and a child’s negative emotional reactivity or self-regulation before 2 years of age. A likely mechanism is re-programming of the fetal HPA axis in response to maternal stress. Maternal prenatal stress and cortisol may re-program the postnatal HPA axis, influencing adult phenotypes. Maternal cortisol levels, and by association maternal stress and nutrition levels, increase the activation of the HPA axis postnatally. In mothers and their full-term infants, Davis, Glynn, Waffarn, and Sandman (2011) found an increased cortisol reaction to the newborn heel prick test (blood draw) in the neonates of women who had higher cortisol levels during the second half of pregnancy. This association remained even after adjustment for maternal medical history, socioeconomic status, ethnicity, and sex of the child. Similarly, maternal cortisol and prenatal anxiety levels mid-pregnancy were associated with elevated cortisol levels in response to the first day of a new school year (Gutteling, de Weerth, and Buitelaar, 2005). Such resetting of the HPA axis has consequences for postnatal health; we next examine a specific example: attention deficit hyperactivity disorder (ADHD). A multitude of pre- and postnatal risk factors (e.g., low birth weight, smoking, alcohol use, stress during pregnancy, and insensitive or abusive parenting) increase the risk of ADHD and disruptive behavior disorders (DBDs; Latimer et al., 2012). Some studies have managed to examine the independent impact of maternal stress on ADHD. One of the most striking examples involves a twofold increase in ADHD symptoms in children whose mothers were pregnant during, but not exposed to, the Chernobyl disaster in 1986 (Huizink et al., 2007). Similarly, in the Avon Longitudinal Study of Parents and Children (ALSPAC), prenatal anxiety at 32 weeks of gestation was associated with an increased risk of inattention/hyperactivity at 4 years of age (O’Conner et al., 2002). And in a more recent prospective study of 1,247 Finnish children, maternal depression at 10 and 28 weeks of gestation are associated with externalizing problems on the Child Behavior Check List, while maternal postnatal factors (illness, tiredness, and anxiety) were associated with internalizing problems at 12 years of age (Pihlakoski et al., 2013). As with several other programming effects, there is intriguing evidence of sexual dimorphism in the impact of the maternal environment. For example, Rodriguez and Bohlin (2005) found that maternal stress at 10 weeks of gestation was associated with ADHD symptoms at 7 years, but only in boys. Likewise, examination of a Finnish birth cohort revealed that several measures of placental size were associated with ADHD symptoms in boys, but not girls, at 8 and 16 years (Khalife et al., 2012). These sex differences are intriguing and are consistent with animal and other human studies and may be underpinned by epigenetic mechanisms. A consistent finding in the DOHaD literature is that boys are more susceptible to environmental insults during pregnancy than girls (Barker, 2003). Male-biased effects of prenatal exposures have been found for schizophrenia, autism spectrum disorders, and anxiety (Bale, 2011). Perhaps, as the faster-growing sex, males are more vulnerable. A possible mechanism underlying the differing impact of maternal stress on the male and female postnatal phenotype is altered sensitivity to GCs. Across several species, females appear to be more resistant and males appear to be more sensitive to GC exposure (Phillips and Matthews, 2011; Seckl and Holmes, 2007). Evidence of sex differences in the activation of the HPA axis has been found in animal studies (Liu, Li, and Matthews, 2001). Detailed analyses in mice show that the male vulnerability to prenatal stress, resulting in increased emotionality 183

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postnatally, may be attributable to increased placental responsivity with an up-­regulation of placental gene expression found in the placentae of male but not female mice (Mueller and Bale, 2008). Moreover, the prenatal stress-influenced placental epigenetic processes with increased expression of DNA methyl transferases and methyl-binding proteins in the male but not female placentae. Thus, the sex-specific effects of maternal stress on postnatal phenotypes may be transduced via epigenetic processes in the placenta. What, if anything, do evolutionary models say regarding sex-specific effects? An evolutionary model, sex allocation theory (Charnov, 1982), proposed that, when maternal condition is poor, investment of resources should be allocated to the offspring sex that requires the least investment. As sons grow faster and require more resources to produce, under conditions of prenatal stress the maternal physiology may preferentially allocate resources away from male fetuses and thus increase their sensitivity to environmental insults. Crucially, for this argument, stress hormones appear to provide the link between the maternal condition and the allocation of resources. In a study of European starlings, Love, Chin, Wynne-Edwards, and Williams (2005) found that elevated maternal corticosterone levels were associated with biasing allocation of resources towards females, with males experiencing higher mortality and being lighter at hatching. Therefore, maternal condition during pregnancy may have sex-specific effects on the postnatal phenotype, including mental and physical health.

Prenatal Nutrition, Fetal Development, and the Postnatal Phenotype No discussion of prenatal development is complete without examining the impact of maternal nutrition on the fetus and its postnatal phenotype. For the vast majority of human history, the primary concern has been undernutrition. Now, with the emergence of the obesity epidemic, overnutrition is of increasing concern (Wells, 2012). Unfortunately for the developing fetus, both maternal underand overnutrition provide suboptimal environments that can affect early development and lifelong health (Ojha, Robinson, Symonds, and Budge, 2013). Even in “well nourished” populations, an imbalanced diet can affect fetal development, and, if not in the form of reduced growth during pregnancy, it can still influence postnatal health (Barker, 2003; Kind, Moore, and Davies, 2006). Below, we briefly examine two important components of the maternal diet, iron and folate, before looking at the consequences of maternal nutrition for postnatal phenotypes.

Iron Iron deficiency is the most common nutrient deficiency among pregnant women (Guilbert, 2003). The prevalence of anemia among pregnant women worldwide is estimated to be 41.8%, with iron deficiency the leading cause (McLean, Cogswell, Egli, Wojdyla, and da Benoist, 2009). Iron demands during pregnancy increase rapidly, especially late in gestation. Peak gastrointestinal iron absorption in pregnant women occurs in the third trimester (Barrett, Whittaker, Williams, and Lind, 1994), concurrent with the increased iron transfer to the fetus. In the absence of adequate maternal iron status, the placenta increases the number of transferrin receptors in order to enhance placental iron absorption in an attempt to maintain adequate iron transfer to the fetus (Cetin, Berti, Mandò, and Parisi, 2011). Maternal iron deficiency early in pregnancy is associated with an increased risk of low birth weight and preterm delivery (Chang, O’Brien, Nathanson, Mancini, and Witter, 2003; Scanlon, Yip, Schieve, and Cogswell, 2000). The relation, however, appears to be U-shaped, with high maternal hemoglobin concentrations in early to mid-gestation also associated with increased risk of adverse birth outcomes, including preterm birth and low birth weight (Chang et al., 2003; Scanlon et al., 2000). 184

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Iron is required for a number of physiological processes crucial to development, including oxygen transport, energy production, and, notably, brain development. Dietary iron deficiency during prenatal development in animal models leads to an alteration in the composition and quantity of neuronal myelin sheaths (Ortiz et al., 2004). Similarly, iron is required for the synthesis of the neurotransmitters serotonin (Martinez, Knappskog, and Haavik, 2001) and dopamine and norepinephrine (Nagatsu, 1995). Iron deficiency during infancy is associated with long-lasting effects on neurocognitive outcomes, including decreased executive function at the ages of 5, 10, and 19 (Lozoff et al., 2006). Moreover, interventions improve neurocognitive outcomes. For example, a study in rural Nepal with a high prevalence of anemia observed improved general intellectual functioning, executive function, and motor skills in 7- to 9-year-old children following maternal supplementation with iron and folic acid compared with a control group (Christian et al., 2010). While there is a paucity of data regarding the mechanism through which maternal iron deficiency impacts cognitive function in children, impaired myelination is a potential cause.

Folate Folate (folic acid) is an important factor in fetal development that is involved in a number of biological processes, including acting as a cofactor for many essential cellular reactions, such as amino acid metabolism, DNA synthesis, DNA methylation, and red blood cell production. Fetal development is a time of rapid and sustained cell division and thus the demand for folate increases during this period (McPartlin, Halligan, Scott, Darling, and Weir, 1993). In the absence of adequate dietary folate intake and/or folic acid supplementation, maternal serum and erythrocyte folate concentrations decrease from mid-pregnancy onwards and continue to decline postpartum (Qvist, Abdulla, Jagerstad, and Svensson, 1986). The implications of maternal folate nutrition on fetal growth have been investigated in a number of studies worldwide, with the clearest finding that peri-conceptual folic acid supplement use reduces the risk of neural tube defects (e.g., spina bifida) by almost three quarters (Lumley, Watson, Watson, and Bower, 2001). Based on animal models, which show the importance of adequate methyl donors, such as folate, during neural tube closure, it has been hypothesized that inadequate folate availability may increase the risk of neural tube defects in humans through reduced DNA methylation (Dunlevy et al., 2006). In a hyperhomocysteinemia rat model dietary folate intake was found to correlate with the methylation of DNA in the placenta (Kim, Hong, Lee, Lee, and Chang, 2009). Folic acid over supplementation in pregnant rats was found to modify the methylation and expression of the placental gene encoding 11β-HSD-2 in a sex-dependent manner, suggesting that maternal diet can induce sex-specific differences in physiology that may have long-term health consequences (Penailillo, Guajardo, Llanos, Hirsch, and Ronco, 2015).

Nutrition and Fetal Programming Nutrition is a key determinant of fetal growth and size at term. The initial findings by Barker, linking small size at birth and chronic adult diseases such as hypertension, diabetes, and cardiovascular disease, were thought to result from an imbalance between the maternal supply and fetal demand for nutrients during pregnancy (Phillips, 2004). This hypothesis is now supported by evidence from animal studies (Eriksson, Forsen, Tuomilehto, Osmond, and Barker, 2003) and longitudinal epidemiological investigations of diet during pregnancy in humans (Ojha et al., 2013; Phillips, 2004). Prenatal brain development is dependent on adequate nutrition (Walker, 2005). It is now apparent that the impact of maternal nutrition also extends to mental health outcomes. Prenatal exposure to the Dutch hunger winter (1944–1945) in the second or third trimester was associated with an 185

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increased risk of affective disorders in both males and females (Brown, van Os, Driessens, Hoek, and Susser, 2000). In a study of 23,020 Norwegian women, Jacka et al. (2013) found that higher intake of unhealthy foods during pregnancy was associated with increased levels of externalizing problems at 1.5, 3, and 5 years of age. This relation held after adjustment for a range of confounds, including socioeconomic status, depression during pregnancy, and children’s postnatal diet. Similarly, in a nonhuman primate model, maternal nutrient restriction during pregnancy was associated with juvenile attentional and behavioral problems (Keenan et al., 2013). Together, these studies highlight a potential role of nutrition during pregnancy for mental health disorders. The evidence that small size at birth is associated with poorer adult mental and physical health outcomes is substantial. The proximate mechanisms by which these effects could be transmitted throughout a lifespan, however, are not completely understood. A likely candidate is that maternal undernutrition, like maternal prenatal stress (see above), re-programs the HPA axis and has consequences for postnatal health (Phillips and Matthews, 2011). Undernutrition as a stressor makes sense because glucocorticoids are involved in both the stress response and the liberation of glucose for the cells of the body. In a meta-analysis of 11 studies (N = 2,311), lower birth weight was significantly associated with higher levels of cortisol during childhood (van Montfoort, Finken, le Cessie, Dekker, and Wit, 2005). Increased stress reactivity to the Stroop Test has also been detected in a study of 721 people who were exposed to the Dutch hunger winter prenatally (Painter et al., 2006). In animal models, maternal undernutrition during pregnancy has been associated with the increased expression of glucocorticoid receptor 11β-HSD-1 and the decreased expression of 11β-HSD-2 suggesting programming of gene expression related to the HPA axis (Whorwood, Firth, Budge, and Symonds, 2001). Other emerging areas of interest involve pathways such as the immune process and inflammation during pregnancy which are also crucial to reproduction, interact with the HPA axis, and contribute to human life history trade-offs (Clancy, 2013; Entringer et al., 2012; McDade, 2005). Researchers rarely consider that stress hormones may also have a behavioral effect on maternal nutrition. In humans, stressful events or administration of CRH increase the eating of comfort food, but there has been no study examining the impact of maternal stress on nutritional intake during pregnancy and child outcomes (Entringer et al., 2012). Thus, evidence supports the hypothesis that maternal nutrition influences childhood mental and physical health by re-programming the HPA axis.

Epigenetics as a Potential Organizing Mechanism Epidemiological data and evolutionary theory suggest that insults during one generation can have consequences for the growth and development of second and third generation descendants (Bateson et al., 2004; Coall and Chisholm, 2003; Kuzawa, 2005; Ounsted et al., 1986). During development in mammals, there is extensive DNA methylation. The majority of methylation occurs during the development of the germ cells (future sperm and ovum) and in the early embryonic cells forming the blastocyst (Reik, Dean, and Walter, 2001; Schaefer, Ooi, Bestor, and Bourc’his, 2007). This methylation follows periods of demethylation where the epigenetic markers are thought to be “wiped clean” and reset. The mechanisms responsible for fetal growth and intrauterine programming are regulated by placental nutrient transport. Placental inefficiency is also associated with epigenetic modifications. Jansson and Powell (2013) reported that restriction of protein in the maternal diet of rats induced epigenetic changes in specific genes, the glucocorticoid receptors in the liver of the offspring. Furthermore, genes expressed in the placenta may undergo epigenetic modification in response to disturbances in the maternal compartment due to direct exposure to maternal blood. The methylation of certain genes, such as the trophoblast genes, also results in altered placental structure and function. The effects of methylation due to maternal stressors have direct effects on placental morphology 186

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and fetal programming. In addition to modifications in methylation, epigenetic mechanisms include noncoding RNA molecules, such as microRNAs (miRNA). These short RNA fragments can provide post-translational gene expression, through the inhibition of protein translation.

Prenatal Toxins, Teratogens, and Offspring Development Research on prenatal development in human evolutionary ecology, life-course epidemiology, and the DOHaD paradigm predominately focuses on maternal stress and nutrition. Stressors often ignored in these analyses, possibly because of the disruptive rather than adaptive nature of exposure, are toxins and pollutants. Many of these substances persist in the environment and accumulate over time. Human exposure arises through multiple pathways including direct contact with soils, inhalation of particulate matter and household dust, dermal contact, and the consumption of contaminated food or drinking water. In this section we highlight some pollutants and their influence on prenatal development.

Tobacco Smoke Maternal smoking during gestation is known to result in reduced fetal growth, with a decrease of approximately 200g in infants born to smoking mothers relative to those born to nonsmokers (Rogers, 2009). Tobacco smoke contains more than 4,000 chemicals, one of which is cadmium, and hence cadmium may play a role in the reduction in birth weight. Prenatal tobacco exposure was significantly associated with ADHD in a study of 4,704 U.S. children (Braun, Kahn, Froehlich, Auinger, and Lanphear, 2006). Analysis of a nationally representative sample of 8- to 15-year-olds revealed a greater than eightfold increased risk of ADHD for children who had both prenatal environmental tobacco smoke exposure and postnatal lead exposure (Froehlich et al., 2009), demonstrating the importance of environmental exposures for this prevalent health condition. A meta-analysis of 14 studies conducted worldwide with a total of over 84,000 children aged 2 years and above revealed that maternal smoking during pregnancy was associated with an elevated risk of the offspring being overweight at the ages of 3–33 years (Oken, Levitan, and Gillman, 2008). Notably, the odd ratios were almost unchanged when adjusted for a range of factors including parental sociodemographic factors, signifying that social and behavior differences between smokers and nonsmokers were unlikely to account for the increased risk (Oken et al., 2008). Maternal smoking during pregnancy has also been associated with an increased risk of early onset of type 2 diabetes in young adults (Montgomery and Ekbom, 2002) and early onset of puberty in males (Fried, James, and Watkinson, 2001). Although discussions of prenatal exposures tend to focus on maternal exposures, onset of paternal smoking prior to puberty has been associated with an increase in body mass index (BMI) in male offspring at the age of 9 years, with the effect most pronounced if fathers started smoking when they were aged 10 years or under (Pembrey et al., 2006). The relation with early paternal smoking provides compelling evidence of a male-line transgenerational effect.

Bisphenol A Bisphenol A (BPA) is a ubiquitous chemical used in the manufacture of polycarbonate plastics and epoxy resins. It is found in a number of types of food packaging, including in the lining of tins. Biomonitoring in developed countries has indicated that exposure is widespread. BPA has been shown to transfer across the human placenta, mainly in the active unconjugated form (Balakrishnan, Henare, Thorstensen, Ponnampalam, and Mitchell, 2010; Mørck et al., 2010). BPA is known to 187

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have detrimental effects on placental cells, with low, environmentally relevant, doses of the chemical inducing apoptosis in placental trophoblasts via increased expression of tumor-necrosis factor α (TNF-α) (Benachour and Aris, 2009) as well as altering the microRNA expression in cells derived from the first trimester placenta. Therefore, BPA may alter the DNA repair capabilities of these cells (Avissar-Whiting et al., 2010). Consistent with the effects of BPA on placental cells, some studies have shown an association between prenatal BPA exposure and reduced head circumference and weight (Philippat et al., 2012; Snijder et al., 2013; Wolff et al., 2008). Because BPA concentrations in maternal urine are known to vary during pregnancy (Braun, Kalkbrenner, Calafat, Bernert, et al., 2011), exposure misclassification is possible when samples are collected at a single time point. Equally, the specific window of vulnerability to BPA exposure in terms of fetal growth outcomes is unknown. The potential relation between BPA exposure and neurobehavioral outcomes has been examined in a number of studies, with sex-dependent effects reported. In boys, prenatal BPA exposure has been associated with increased emotionally reactive and aggressive behavior at ages 3–5 years (Perera et al., 2012) and internalizing behaviors, including anxiety and depression, at 7 years (Harley et al., 2011; Roen et al., 2015), as well as a range of parent-reported problem behaviors aged 6–10 years (Evans et al., 2014). Gestational exposure to BPA has also been associated with increased risk of ADHDrelated behaviors at 4 years of age, again with stronger associations in boys (Casas et al., 2015). Conversely, one study identified increased externalizing behaviors at age 2 and higher scores for measures of anxiety, hyperactivity, emotional control, and behavioral inhibition at age 3, with stronger effects in girls at both ages (Braun et al., 2009; Braun, Kalkbrenner, Calafat, Yolton, et al., 2011). The reasons for the discrepancies in findings are unclear and may reflect methodological differences in the studies. Nonetheless, the ability for prenatal BPA exposure to modify child behavior in a sex-specific manner is apparent. In vitro experiments have shown that BPA can inhibit adiponectin release from human adipose tissue (Hugo et al., 2008), suggesting adverse affects on metabolic homeostasis. Similarly, prenatal exposure to BPA has also been associated with BMI and waist circumference in children at 4 years (Valvi et al., 2013) and fat mass index, percentage body fat, and waist circumference at age 7 (Hoepner et al., 2016).

Phthalates Phthalates are used widely in a range of consumer products. For example, the high molecular weight di(2-ethylhexyl) phthalate (DEHP) is used as a plasticizer in the manufacture of polyvinyl chloride, whereas low molecular weight phthalates, such as diethyl phthalate (DEP) and dibutyl phthalate (DBP), are used in cosmetics and other personal care products. Animal models have demonstrated that prenatal exposure to DEHP, DBP, or benzyl butyl phthalate (BzBP) has a marked effect on fetal Leydig cells, reducing the production of fetal testosterone and insulin-like growth factor 3 (Insl-3; Foster, 2006). These effects are responsible for a syndrome of male reproductive abnormalities, including shortened anogenital distance, hypospadias, cryptorchidism, and malformations of the epididymis, vas deferens, seminal vesicles, and prostate (Foster, 2006). In rats, the programming window in which androgen action is required for the normal development of the reproductive tract has been identified, corresponding to 8–14 weeks’ gestation in humans (Welsh et al., 2008). In human studies, DEHP metabolites measured in maternal urine collected during gestation (mean week 28.6) were associated with reduced anogenital distance in males (median age at assessment 12.8 months), decreased penile width and impaired testicular descent (Bustamante-Montes et al., 2013; Suzuki et al., 2010; Swan, 2008). A larger study was established to examine the association between first trimester phthalate exposures and anogenital distance in children, with the timing of sample collection matching the window of vulnerability identified in animal models (Welsh et al., 188

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2008). This study confirmed that, despite low levels of exposure, metabolites of the anti-androgenic DEHP measured in first trimester urine samples were significantly negatively associated with anogenital distance and penile width in newborn boys (Swan et al., 2015). Anogenital distance has been identified as a strong predictor of multiple semen parameters in adult men, which suggests that this measure is a good indicator of male reproductive function (Mendiola, Stahlhut, Jorgensen, Liu, and Swan, 2011). Therefore, there are possible lifelong impacts of prenatal phthalate exposure on male reproductive development at the population level, which is of concern given the ubiquitous nature of exposure. Maternal occupational exposure to phthalates (estimated by questionnaire only) was associated with decreased placental weight and also decreased fetal growth in a Dutch cohort (Snijder et al., 2012). Consistent with this indication of impaired placental development, maternal urinary phthalate concentrations were associated with placental gene expression in trophoblast differentiation and steroidogenesis pathways (Adibi et al., 2010). Increased maternal phthalate exposure in the early third trimester was correlated with decreased placental gene expression, with results more pronounced for genes of the trophoblast differentiation pathway (Adibi et al., 2010). The effect of prenatal exposure to anti-androgenic phthalates on sexual differentiation of the brain is also being explored. Concentrations of two metabolites of DBP and two metabolites of DEHP in maternal urine (mean 28.6 weeks gestation) were associated with reduced masculine play in boys aged 3–6 years (Swan et al., 2010). Prenatal phthalate exposure also influences neurobehavior in infants and children, including increased ADHD (Engel et al., 2009; Kobrosly et al., 2014; Lien et al., 2015; Whyatt et al., 2012) and autistic behaviors (Miodovnik et al., 2011), impaired mental and psychomotor development (Kim et al., 2011; Whyatt et al., 2012), and increased emotional difficulties (Whyatt et al., 2012). Prenatal phthalate exposure measured late in gestation has also been associated with decrements in children’s IQ at the age of 7 (Factor-Litvak et al., 2014). Despite some variations in the findings between studies, which may reflect differences in the gestational timing of exposure assessment and/or differences in the age of children or method of neurodevelopmental assessment, overall the literature supports the notion that prenatal phthalate exposure is associated with behavioral and cognitive impacts in children.

Perfluoroalkyl Substances Perfluoroalkyl substances (PFAS) are used extensively in a range of commercial and industrial applications. Perfluorooctanesulfonate (PFOS) and perfluorooctanoate (PFOA) are PFAS that are produced either directly or from the metabolism of other PFAS, with half-lives between 4 and 5 years (Olsen et al., 2007). These chemicals are used as industrial surfactants and may be present in a number of consumer products including nonstick pans, soft furnishings, clothes, and food packaging. PFAS have been extensively used for several decades and persist for long periods in the environment, but human exposure has only been assessed relatively recently, in part due to our previous inability to detect these chemicals with sufficient sensitivity in biological media. Although the use of PFAS was phased out in most countries in 2000, human exposure to perfluorinated compounds remains widespread with biomonitoring studies indicating that four perfluoroalkyl acids (perfluorooctanoic acid [PFOA], perfluorooctane sulfonate [PFOS], perfluorononanoic acid [PFNA], and perfluorohexane sulfonate [PFHxS]), are detectable in most blood samples. These compounds are known to cross the placental barrier and are prevalent in cord blood samples. The evidence to date regarding prenatal PFAS exposure and fetal growth is largely consistent, with decreased fetal growth reported to be associated with PFOS, PFOA, or both, in most studies (Apelberg et al., 2007; Chen et al., 2012; Fei, McLaughlin, Tarone, and Olsen, 2007; Washino et al., 2009; Whitworth et al., 2012). Prenatal exposure to PFHxS has also been associated with reduced fetal growth (Callan et al., 2016; Maisonet et al., 2012). 189

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In British girls from the ALSPAC study, weight at 20 months increased with increased prenatal exposure to PFOS, with those in the highest tertile for PFOS on average 580 g heavier than those with prenatal exposure in the lowest tertile (Maisonet et al., 2012). Prenatal PFOA concentrations have also been associated with increased BMI, waist circumference and body fat in children at 8 years of age, as well as increased gains in child BMI between the ages of 2 and 8 years (Braun et al., 2016). Most studies find that decreased birth weight is associated with prenatal PFOS exposure, suggesting a rapid early growth catch-up that may have implications for long-term child health. Furthermore, there is evidence that the effects of prenatal PFAS exposure on anthropometry persist into adulthood, with positive associations between prenatal exposure to PFOA and the prevalence of overweight and high waist circumference (>88 cm) in females, but not males, at 20 years of age in a Danish cohort (Halldorsson et al., 2012). Maternal PFOA concentrations in the third trimester were also associated with biomarkers of adiposity in female adult offspring, with positive associations with insulin, leptin, and leptin-adiponectin ratio, and negative associations with adiponectin (Halldorsson et al., 2012). To date the potential associations between prenatal PFAS exposure and the male human reproductive system have received limited attention in epidemiological studies. In a Danish study, increased maternal PFOA serum concentrations measured at week 30 in gestation were associated with lower sperm concentration and reduced total sperm count in male offspring at 19–21 years of age, with higher concentrations of luteinizing hormone and follicle-stimulating hormone detected in the blood samples of those with higher in utero PFOA exposure (Vested et al., 2013). No associations were observed between prenatal PFOS exposure and the outcomes measured. Given the widespread nature of exposure to PFOA, these decreases in semen quality in adult men following prenatal exposure could pose a significant population health issue and warrant further investigation. Of equal concern is the suggestion that prenatal exposure to PFOS is associated with reduced ­antibody-mediated immune responses to childhood immunizations at the age of 5 years and increased odds of diphtheria antibody concentrations below the protective level (Grandjean et al., 2012). Consistent with this potential immunotoxic effect, prenatal exposure to PFOS and PFHxS has been associated with increased prevalence of infectious diseases in children in the first 4 years of life (Goudarzi et al., 2017).

Conclusion and Perspectives for Future Studies Investigations into the potential health effects of prenatal exposures to environmental toxicants are essential. The main challenge in this field is to deal with a number of methodological issues to improve the accuracy of conclusions that can be made. Epidemiological, in vivo, and in vitro studies frequently examine the effects of exposure to a single toxicant, but environmental exposure involves chronic simultaneous low-level exposure to multiple toxins which may have synergistic or cumulative effects. The ability to accurately assess the health implications of exposure to multiple ubiquitous environmental pollutants and identify the pollutants most strongly associated with adverse outcomes remains a challenge. Longitudinal birth cohort studies are expensive and need to follow up participants for many years to accurately ascertain the health effects of prenatal exposure, some of which may not be manifest until the offspring reach adulthood. In addition, for most adverse health effects associated with environmental exposures a discrete window of vulnerability in the prenatal period is yet to be identified, which means that ideally such studies must collect biological samples at multiple time points throughout pregnancy. Furthermore, as increasing evidence emerges of sexspecific health implications of exposure to environmental substances, sample sizes in studies will need to increase to accommodate the statistical analysis of sexually dimorphic associations. Finally, many health outcomes assessed by longitudinal birth cohorts involve a complex interplay among multiple elements, including genetic susceptibility, maternal diet, and prenatal (and postnatal) environmental 190

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exposures. For example, an association between prenatal exposure to pesticides and autism spectrum disorders was attenuated by high folic acid supplementation early in pregnancy (Schmidt et al., 2017). If indeed such a protective effect of folic acid represents a causal relation, the mechanisms by which it could occur are yet to be elucidated, although a role for DNA methylation pathways has been speculated. Nonetheless, this study highlights the importance of including full consideration of all aspects of the prenatal environment when assessing maternal influences on offspring phenotype.

Prenatal Parenting: Future Applied, Empirical, and Theoretical Perspectives Prenatal parenting and the prenatal environment more broadly is a burgeoning field of enquiry with increasing significance for health. Our understanding of and thus potential to improve aspects of the maternal environment is progressing rapidly. In this section we explore specific issues that we believe are pertinent to future applied, empirical, and theoretical work in prenatal parenting.

Prenatal Bonding Early parent-child relationships are known to have a strong psychological influence that lasts a lifetime (Bowlby, 1969). Consequently, early relationships with parents are crucial throughout development and into adulthood. Moreover, these early experiences have a profound influence on an individual’s health and emotional well-being (DeKlyen and Greenberg, 2008; Dozier and Rutter, 2008). Insensitive, unresponsive parenting is commonly associated with more insecure attachment, which has consequences for children’s relationships, development, parenting, and the intergenerational transmission of insecure attachment (Belsky et al., 1984; Berthelot et al., 2015; Chisholm, Quinlivan, Peterson, and Coall, 2005). Prenatal mother-fetal bonding appears to be a reliable predictor of early postnatal bonding. In an Australian study, Rossen and colleagues (2016) found that prenatal bonding, as measured via the Maternal Antenatal Attachment Scale in the first, second and third trimester, predicted bonding 8 weeks postnatally. These associations remained after adjustment for a wide range of factors including age, socioeconomic status, birth weight, crying, and pregnancy complications. Moreover, a systematic review found that lower levels of prenatal bonding were associated with poorer infant developmental outcomes, such as a difficult temperament, an increased risk of colic, and delayed developmental outcomes (Branjerdporn, Meredith, Strong, and Garcia, 2017). Therefore, prenatal parenting in the form of mother-fetal bonding appears to have consequences for the postnatal phenotype. Social support buffers individuals against stressful life events and may play a role in adjustment to stressors experienced during pregnancy and neonatal outcomes. Indeed, across cultures, having two or more friends or family members available in your social network and higher levels of social support were both independently associated with lower levels of depression postnatally (Surkan et al., 2006). Consistent with this social support perspective and the proposition that humans are cooperative breeders (Hrdy, 1999), a Japanese study found that having fewer support people available during pregnancy was associated with poorer mother-fetal bonding before 25 weeks of pregnancy and 1 month postnatally (Ohara et al., 2017). Thus, consistent with life history theory interpretations of attachment (Chisholm, 1996), mounting evidence suggests the impact of a mother’s social environment is transmitted to her offspring through maternal-fetal bonding. Higher quality maternal-fetal bonding is associated with improved neonatal and infant outcomes (Branjerdporn et al., 2017) suggesting bonding is a potential intervention target. Moreover, interventions exist that have been shown to promote prenatal bonding. For example, in a study of a prenatal education course consisting of five 1-hour sessions that focused on fetal physiology, development, and perceptions through singing, dance, and massage were associated with higher levels of prenatal 191

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attachment in the third trimester (Bellieni et al., 2007). As with other species (Colombelli-Negrel and Kleindorfer, 2017), during the neonatal period the newborn seems to prefer its mother’s voice (DeCasper and Fifer, 1980) which may provide a mechanism for intervention. Therefore, antenatal care can play an important role by integrating activities into maternal care that promote maternalfetal bonding during pregnancy (Rossen et al., 2016), such as the use of singing, ultrasound, and memories of parental relationships (Branjerdporn et al., 2017).

Antenatal Care Maternal health and behavior during pregnancy clearly have consequences for offspring phenotype. Some aspects of maternal health can be modified and will benefit from antenatal care, whereas others cannot (Kramer, 1987). Maternal health is unequally distributed within and between populations and, like parenting, is a mechanism for the intergenerational transfer of risk factors for poor health that may perpetuate health inequalities across generations (Fonagy and Higgitt, 2000; Kelly et al., 2017). In developing countries antenatal care is crucial for improving maternal and child health outcomes (Lincetto, Mothebesoane-Anoh, Gomez, and Munjanja, 2006). Moreover, the introduction of or additional support for antenatal care has positive effects (Choe, Min, and Cho, 2017). In cases where antenatal care is well established, the health impact which the timing of antenatal care has (when it begins) and the number of antenatal visits are difficult to assess. Moreover, study design is difficult because women with pre-existing health conditions may be more likely to initiate antenatal care earlier and attend more often. However, the quality of antenatal care, particularly for high-risk pregnancies, appears to improve outcomes (Kramer, 1987). In an audit of maternal mortality (2009– 2012) in the Republic of Ireland and the United Kingdom, the Confidential Enquiry into Maternal Deaths and Morbidity, of the 357 women who died during pregnancy or within 6 weeks of the end of their pregnancy, only 29% had the recommended level of antenatal care and 10% received no antenatal care (Shakespeare and Knight, 2015), suggesting that antenatal care is especially important for high-risk pregnancies. Maternal care is crucial for removing or reducing any modifiable risk factors which ultimately promotes healthy pregnancy, placental development, and outcomes (Kramer, 1987). In turn, minimizing risk factors is associated with the general health of the broader population (Kloosterman, 1970). Ensuring sustainable, equal, and relatively easy access to antenatal care is the issue of concern. Thus, it is likely antenatal care that can support existing health conditions (e.g., diabetes, asthma), help make informed decisions about care (e.g., morning sickness, mental health), and modify behavior (e.g., smoking, diet) will produce favorable outcomes for maternal and fetal phenotypes (Kramer, 1987).

Resource Flow to the Fetus—Not Maternal Nutrition Our evolutionary approach to reduced fetal growth suggests that the current emphasis of the DOHaD model on maternal under- or malnutrition as the main cause of reduced fetal growth and subsequent increased risk of adult disease may be misplaced. Adverse prenatal environments definitely contribute to reduced placental function and restricted fetal growth, but the impact of maternal nutrition on fetal and placental growth is complicated (Robinson et al., 1994, 2001). The influence of maternal dietary supplementation on birth weight is small (Harding, 2001), and the outcomes depend heavily on the existing nutritional state of the population (Kind et al., 2006). Investigations of maternal nutrient intake and subsequent fetal and placental weights at birth have yielded mixed results (Godfrey, Robinson, Barker, Osmond, and Cox, 1996; Kuzawa, 2005; Mathews, Yudkin, and Neil, 1999; Moore, Davies, Willson, Woesley, and Robinson, 2004). Our model suggests that the effect of maternal nutrition on placental ratio is a consequence not only of maternal nutrient intake, but also that the flow of resources from the uterus to the fetus is “negotiated” by the mother and fetus. The 192

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model we are working with suggests that the long and vulnerable fetal supply line, not measurable maternal nutrition per se, determines the ultimate flow of resources to the fetus (Godfrey et al., 1999; Harding, 2001). As resources from the maternal diet travel along the fetal supply line, what ultimately becomes fetal nutrition is mediated by the mother’s metabolism and endocrinology, uterine blood flow, placental transport and metabolism, umbilical blood flow, and the fetus’ metabolism and endocrinology (Harding, 2001). Therefore, the allocation of resources between competing demands during pregnancy mean that maternal nutrition and fetal nutrition are not the same thing (Gillman, 2002; Harding, 2001). This allocation of resources may also partly explain the finding that maternal insults that do not necessarily affect fetal growth can still have consequences for a child’s subsequent postnatal development and health. Our evolutionary synthesis highlights an interaction between the maternal reproductive strategy and diet as a possible explanation for some of the inconsistencies in studies of maternal nutrient supplementation and fetal growth and the fetal antecedents of adult disease (Coall and Chisholm, 2010; Kramer, 2000; Kramer and Joseph, 1996).

Morning Sickness: Nutrition, Stress, Hormones, and Long-Term Outcomes A common characteristic of the maternal phenotype that includes nutritional and stress components is morning sickness. Morning sickness (nausea and vomiting in pregnancy [NVP]) is a suite of symptoms affecting up to 90% of pregnant women (Einarson, Piwko, and Koren, 2013). Symptoms may include nausea, vomiting, retching, and food avoidance or aversion (Patil et al., 2012). Typically, symptoms begin around 4 to 6 weeks of pregnancy and continue until the 16th week of pregnancy. Given its frequency, it is reasonable to say that morning sickness is a “normal” part of pregnancy that exists as a continuum, with expectant mothers experiencing no symptoms at one end and those with exacerbated symptomology at the other. Hyperemesis gravidarum (HG) occurs in up to 3% of all pregnancies (reported numbers only) and is characterized by persistent nausea, vomiting, retching, dehydration, maternal weight loss of up to 3%–5%, and electrolyte imbalances that often result in hospitalization (Goodwin, 2002; Koren, 2014). Many women find NVP stressful and debilitating which can affect physical and mental health for the entire pregnancy (Bustos, Venkataramanan, and Caritis, 2017; Lee and Saha, 2011). Morning sickness in the first trimester of pregnancy is believed to be associated with a protective role and positive birth outcomes (Profet, 1992). Food aversion in early pregnancy (in animal and human models) stimulates the growth of the placenta and reduces the risk of miscarriage, preterm birth, and low birth weight babies (Huxley, 2000). Compensatory placental growth mechanisms are believed to be responsible for the redirection of maternal resources in response to nutrient restriction. Evidence suggests morning sickness may be a direct result of adaptive placental functioning ( Jauniaux, Poston, and Burton, 2006). Women who experience no symptoms of morning sickness are reported to have larger placentas and low birth weight outcomes. Nutritive insult in the second and/or third trimester (seen with severe HG) can result in fetal growth restriction and consequent shorter gestation and lower birth weight offspring (Vandraas et al., 2013; Veenendaal et al., 2011). The impact of morning sickness extends well beyond the antenatal period (Veenendaal et al., 2011). Indeed, HG is associated with a range of mental and physical issues for the mother both before and after pregnancy (Tian, MacGibbon, Martin, Mullin, and Fejzo, 2017). Moreover, HG impacts the entire family with expectant fathers who, as principal carers, reported elevated feelings of anxiety (Sartori et al., in press). Large population-based cohort studies have investigated the maternal, birth, and neonatal outcomes after pregnancies complicated with HG. In a cohort of more than eight million pregnancies from England (1997–2012; Fiaschi et al., 2018), HG was associated with an increased risk of diseases of pregnancy (e.g., anemia, eclampsia), poor birth outcomes (e.g., preterm birth, low birth weight), and increased neonatal morbidity (e.g., neonatal intensive care). Results 193

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from a Swedish birth cohort find these risks are higher when first admission occurs in the second trimester, suggesting there may be a relation between abnormal placentation and HG (Bolin, Akerud, Cnattingius, Stephansson, and Wikström, 2013). HG also is associated with subsequent maternal morbidity and mortality, including placental dysfunction, inflammation, and autoimmune diseases (Bolin et al., 2013; Jørgensen, Nielsen, Pedersen, Jacobsen, and Frisch, 2012). A population-based cohort from Norway, however, found no increase in subsequent maternal mortality (all-cause, cardiovascular disease, external cause, or mental or behavioral disorder cause) in women who experienced HG (Fossum et al., 2017). A decreased risk of cancer, particularly tobacco-related cancers, was noted. However, the lower rates of cancers may be confounded by the fact that nicotine receptors suppress nausea via decreasing levels of estradiol and human chorionic gonadotropin (hCG) resulting in a low rate of HG in smokers (Bernstein et al., 1989). Consistent with the DOHaD paradigm, it is likely the nutritional and psychological impact of severe nausea and vomiting during pregnancy may reduce the resource supply to the fetus and result in lifelong consequences for health. To date, however, few studies have examined the long-term outcomes of children from HG pregnancies (Ayyavoo, Derraik, Hofman, and Cutfield, 2014). In a study of healthy New Zealand children (4–11 years of age), 36 exposed to HG during pregnancy, compared to 42 controls, showed reduced insulin sensitivity, higher fasting insulin levels, and lower insulin-like growth factor binding-protein 1, which are associated with an increased lifelong risk of diabetes mellitus (Ayyavoo et al., 2013). These children also had basal cortisol levels that were 22% higher than controls. Inadequate nutrition or increased prenatal stress may have reset the HPA axis, influencing postnatal development. Therefore, as a maternal effect, HG may lead to long-term adverse metabolic outcomes in exposed offspring (but see Finnish birth cohort; Koot et al., 2017).

Assisted Reproductive Technologies Thus far we have considered maternal adaptations to relatively familiar environmental challenges and their health consequences. Assisted reproductive technologies (ART), however, constitute a novel but increasingly common environmental challenge that may be usefully explored from the perspective of maternal effects (Golombok, 2019). Since the first IVF baby, Louise Brown, was born in 1978 (Steptoe and Edwards, 1978), an estimated five million children have been born worldwide through ART (Hansen, Kurinczuk, Milne, de Klerk, and Bower, 2013). The most common ART treatment involves in vitro fertilization (IVF). In industrialized societies, people who plan to have children often delay reproduction in order to accumulate resources (Hammarberg and Clarke, 2005). Unfortunately, delayed reproduction is associated with decreased fertility, leading to greater demand for ART (Oakley, Doyle, and Maconochie, 2008), to a level that most industrialized countries cannot meet (Hoorens, Gallo, Cave, and Grant, 2007). While the benefits of ART treatments to couples who are unable to conceive are patent, there are also increased risks of poorer outcomes for children conceived via ART (Fisher, Hammarberg, and Baker, 2005; Kalra and Molinaro, 2008). The higher rate of multiple births in ART pregnancies was thought to account for these differences, but studies examining singleton births confirm that babies conceived by ART are more likely to be born preterm or have low birth weight than children from unassisted conceptions (Squires and Kaplan, 2007). Placentae from ART pregnancies have not been studied extensively ( Joy, Gannon, McClure, and Cooke, 2012), but, perhaps in response to reduced fetal growth, placentae from ART pregnancies are heavier and have higher placental ratios (Daniel et al., 1999; Haavaldsen, Tanbo, and Eskild, 2012). Other placental pathologies, including low-lying placenta, placenta previa, placental abruption, and poor implantation, are more common in ART pregnancies ( Jauniaux, Englert, Vanesse, Hiden, and Wilkin, 1990). Confirming these concerns, the

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British Scientific Advisory Committee of the Royal College of Obstetricians and Gynecologists (2012) stated that the babies who emerge from IVF pregnancies are at an increased risk of adverse outcomes, such as low birth weight, small for gestational age, and premature birth. Maternal prenatal stress is another factor that may be associated with poorer pregnancy outcomes in ART. During successful IVF pregnancies, couples report higher levels of stress than in successful nonassisted pregnancies (Eugster and Vingerhoets, 1999). Moreover, the difference between ART and non-ART pregnancies is likely to be underestimated as there is some, albeit mixed, evidence that pre-existing stress is associated with the increased risk of unsuccessful IVF pregnancies (Matthiesen, Frederiksen, Ingerslev, and Zachariae, 2011; Sanders and Bruce, 1999). In a study of 837 Danish women, higher levels of negative life events in the preceding 12 months were associated with a reduced chance of falling pregnant in the first IVF cycle, independent of current perceived stress and depressive symptoms (Ebbesen et al., 2009). The associations between ART and fetal and placental growth suggest the possibility of fetal programming in these pregnancies. However, the range of factors influencing babies conceived via ART are extensive (inheritance of infertility, ART procedures, stress during pregnancy, nutrition, multiple births, preterm birth, fetal growth restriction) and must be carefully considered before the consequences of ART for child and adult health become clear (Hediger, Bell, Druschel, and Louis, 2013). There is increasing evidence that programming effects, associated particularly with adult cardiac and metabolic heath, occur in children born from ART pregnancies (see reviews by Rinaudo and Wang, 2012; Yeung and Druschel, 2013). Possibly because of the positive parenting practices found in ART families, there is no evidence that children born from ARTs have poorer cognitive or socioemotional development (see Golombok, 2019). Here, postnatal attachment relationships may moderate the impact of prenatal cortisol exposure on postnatal cognitive development (Bergman, Sarkar, Glover, and O’Connor, 2010). It is clear that a full understanding of the developmental effects of ARTs cannot be assessed until ART children become parents and grandparents themselves. Perhaps the most important consideration will be the research designs developed to examine these associations. As for all pregnancies, prenatal maternal stress and nutrition must be considered, but many factors unique to ART pregnancies must be considered as well: the underlying cause of infertility itself, the ART procedures themselves (including delayed fertilization and freezing and thawing of embryos), the medications used to induce ovulation or maintain pregnancy (Hansen, Bower, Milne, de Klerk, and Kurinczuk, 2005), and the couples’ emotional reactions to these procedures. In addition, factors known to influence ART outcomes, including the culture media used to store, grow, and protect the eggs and sperm used in some treatments, must all be taken into account (Barnes and Sato, 1980; Trounson and Gardner, 2000). As the number of babies conceived through ART continues to grow, and researchers and clinicians strive to improve maternal and neonatal outcomes, the answers to these questions become increasingly crucial.

Perceived Stress, Objective Stress, and the Biology of Stress There has been substantial debate about how subjective stress during pregnancy affects maternal physiology such that fetal growth is impaired. The problem is that, while there are many reliable and valid instruments for measuring subjective psychosocial stress, their results do not correlate very well with biological measures of stress during pregnancy (e.g., free cortisol in saliva; Voegtline et al., 2013). However, both pathways—perceived stress and maternal glucocorticoids during ­pregnancy—can influence maternal physiology and pregnancy outcomes. Experiences during pregnancy as diverse as pregnancy-specific anxiety, perceived stress, nutrient restriction, and cadmium exposure can affect maternal and placental stress hormone levels. Because both the mother and fetus

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are influenced by psychosocial and physiological stressors, the correlation between perceived stress and stress hormones is often low (Sandman et al., 2012). Similarly, the commonly found association between perceived stress and preterm birth is not always reflected in hormonal measures. For example, Kramer and colleagues (2013) found that, while maternal ACTH was associated with cortisol, which in turn enhanced placental CRH, neither maternal cortisol or CRH were associated with perceived stress, maternal distress, or preterm birth. Research is beginning to establish the independent effects of perceived stress, objective stress, and the biology of stress, suggesting that several at least partially independent pathways might have been operating on maternal physiology.

Co-adaptation: Adaptive Maternal and Fetal Programming The evidence that prenatal adversity programs fetal physiology and affects subsequent infant, child, and adult phenotypes is well-established. The focus throughout this literature is strongly on the fetus: What impact does adversity in utero have on the fetus, and how does this prepare it for a harsher postnatal environment? (Barker, 1994). A new area of research suggests that these events also program maternal physiology, potentially leading to co-adaptation of maternal and offspring physiology. Our argument throughout is that the prenatal environment is as much a maternal adaptation to her life cycle as it is for the fetus (see Berghänel et al., 2017). Although parent-offspring conflict theory is a useful perspective, there is good evidence that this conflict is tempered by parents and offspring monitoring each other and adjusting their demands according to resource availability: Co-adaptation (Bateson, 1994, 2017; Kölliker et al., 2012). Sandman et al. (2012) highlighted animal and human evidence that the structure and function of the maternal brain are also programmed in response to stress during pregnancy and that these changes persist over time. They proposed that changes in maternal stress reactivity, cognitive function, and the risk of psychopathology in response to endocrine changes throughout pregnancy prepare the mother for pregnancy, birth, and postnatal life. In the general population, CRH levels have been associated with mental health disorders, particularly depression and anxiety (Risbrough and Stein, 2006). Yim et al. (2010) examined the relation between placental CRH (pCRH) and postnatal depressive symptoms, finding that women with elevated pCRH levels at 25 weeks of pregnancy were more likely to develop depressive symptoms postnatally. This may be why problems during pregnancy, anxiety, depression, stressful life events, and low levels of social support are closely associated with postnatal depression (Beck, 2001; O’Hara and Swain, 1996; Robertson, Grace, Wallington, and Stewart, 2004). Moreover, mothers suffering from postnatal depression reduce their investment in their new baby (Hagen, 1999). Thus, maternal stress during pregnancy may signal a risky or uncertain environment to which both the mother’s and fetus’ physiology respond (Sandman et al., 2012). This dual programming ultimately improves the fit between mother, infant, and environment. Since postnatal depression affects 10% to 15% of new mothers (Hagen, 1999), this adaptive interpretation of maternal stress may have clinical significance. In early postnatal development there is a remarkable synchrony between maternal behavior and neonatal sensory perception (Brazelton et al., 1974; Trevarthen, 2012; Tronick, 2007). During the long period of slow development that is human childhood this ensures a coordinated mother-infant relationship and transduction of social environmental cues via attachment relationships, among other systems (Chisholm, 1999b, 2017). Ultimately, these “synchronized capabilities” translate to the improved probability of survival and fitness benefits for the mother and infant (Simpson and Belsky, 2008). Therefore, it makes sense that the mother’s, not only the fetus’s, behavior and physiology are adapted to the environment they share. Future research must examine the interaction between cues in different life stages, as well as intergenerational inheritance, as it is likely the best fit between an organism and its ecology is affected by many environmental cues across different time frames (Nettle et al., 2013).

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Childhood Psychosocial Stress: A Developmental Predictor of Maternal Environment The critical influence of childhood experience on subsequent growth, development, and adult health and behavior is central to many disciplines, including evolutionary ecology (Henry and Ulijaszek, 1996), evolutionary psychology (Belsky et al., 1991), ethology (Bateson and Martin, 1999), developmental health (Keating and Hertzman, 1999), developmental psychology (Repetti et al., 2002), and epidemiology (Kuh and Ben-Shlomo, 1997). In humans, as with other animal species (Meaney and Szyf, 2005), the parental developmental environment and parenting behavior have particularly strong influences on offspring physical and mental phenotypes. Life history theory predicts that the flow of resources to the fetus (parental investment) during pregnancy will vary according to the mother’s developmental environment, her reproductive strategy, her currently available material and socioemotional resources, and the resources likely to be available in the future (Chisholm, 1993, 1999b; Chisholm and Coall, 2008; Coall and Chisholm, 2003; Ellison, 2005; Gluckman, Hanson, and Beedle, 2007; Jones, 2005; Kuzawa, 2007; Walker et al., 2006; Wells, 2003; Worthman, 1999; Worthman and Kuzara, 2005). Evidence is emerging, however, that the developmental trajectories entrained by early stress may reduce the maternal allocation of resources to the fetus during pregnancy, thus limiting fetal development and increasing the risk of poor health outcomes (Coall and Chisholm, 2003, 2010). Consistent with this interpretation, women who experienced two types of childhood trauma (e.g., maltreatment, abuse, neglect) had placental CRH concentrations 25% higher than a no trauma group (Moog et al., 2015). The authors interpret this as suggesting early maternal stress may influence the offspring phenotype through placental/fetal stress reactivity. Research with the Adverse Childhood Experiences (ACE) Study demonstrates that early stress is associated with higher adult disease and mortality rates (Anda et al., 1999; Felitti et al., 1998). After adjustment for age, ethnicity, gender, and education, adverse childhood experiences (e.g., sexual abuse, domestic violence, imprisonment of a family member) are risk factors for adult diseases, such as severe obesity, smoking, physical inactivity, and poor self-rated health. Compared to those with none, individuals who experienced four or more adverse experiences are more likely to develop diseases, such as ischemic heart disease, stroke, diabetes, cancer, and chronic bronchitis (Felitti et al., 1998). Moreover, these results have been replicated in four birth cohorts from 1900 to 1978 (Dube, Anda, Felitti, Edwards, and Williamson, 2002), with the risk increasing in a dose-dependent manner in association with the number of childhood stressors experienced (Felitti et al., 1998). There is convincing (albeit retrospective) evidence that the number of adverse childhood experiences predicts increased adult mortality rates, but some early stressors seem to matter more than others. This is probably because they reflect or are symptomatic of a child’s generally risky or uncertain family environment. In particular, childhood sexual, emotional or physical abuse, and witnessing physical violence between parents, tend to be associated with other adverse experiences during childhood (Dube et al., 2002; Gladstone, Parker, Wilhelm, Mitchell, and Austen, 1999). For example, while witnessing parental violence is associated with higher levels of psychological distress and lower levels of social adjustment in adulthood, this association is mediated by the amount of parental care and warmth experienced (Henning, Leitenberg, Coffey, Bennett, and Jankowski, 1997; Henning, Leitenberg, Coffey, Turner, and Bennett, 1996). Moreover, individuals who experience adverse childhood events appear to have more negative life events and experience more anxiety and depression during pregnancy (Benedict, Paine, Paine, Brandt, and Stallings, 1999; Grimstad and Schei, 1999). The early psychosocial environment may also affect fetal development via maternal body composition. Psychosocial stressors, such as neglect, abuse, and unsupportive home environments, have been associated with childhood obesity (Strauss, 1999) and rapid weight gain during childhood. In a

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study of 5,399 Swedish school children (2,661 girls), girls with the most rapid weight gain between 7 and 10 years of age also had the highest prevalence of social, behavioral, and learning problems (Mellbin and Vuille, 1989). In a study of 756 Danish school children, those who were perceived by their teachers to receive little parental support had higher rates of obesity and were seven times more likely to be obese at 20 years of age (Lissau and Sorensen, 1994). Thus, early stress may ultimately influence fetal growth through its impact on childhood weight gain and, subsequently, maternal body composition during pregnancy. Whether the mechanism is via chronic stress or increased weight gain, it is likely that these childhood experiences are embodied (Chisholm, Burbank, Coall, and Gemmiti, 2005; Hertzman, 1999; Hertzman, Power, Matthews, and Manor, 2001; Krieger, 2001) in the form of altered stress reactivity (Bremner et al., 2003). Consistent with this evolutionary synthesis, increased stress reactivity is associated with lower birth weight (Clark et al., 1996; Ward et al., 2004), lower parental responsiveness (Haley and Stansbury, 2003; Repetti et al., 2002), earlier menarche (Boyce and Ellis, 2005; Ellis, 2004), and earlier first sexual intercourse (Brody, 2002). The resultant increased levels of glucocorticoids can reduce insulin sensitivity and increase fat deposition (Brindley and Rolland, 1989; Tsigos and Chrousos, 2002). Furthermore, psychosocial stress is a risk factor for developing the metabolic syndrome in childhood, adolescence, and adulthood (Eisenmann, 2003; Hjemdahl, 2002; Rosmond, 2005). Therefore, via the actions of stress hormones, childhood psychosocial stress may be associated with weight gain throughout the lifespan and an increased risk of adult diseases, which in turn are associated with reduced fetal growth in the next generation (Lawlor, Davey Smith, and Ebrahim, 2003).

Predicting Future Environments: Predictive Adaptive Responses Earlier, we referred only in passing to the concept of “predictive adaptive responses” (PARs) because it deserves special discussion. The concept needs clarification and analysis because it has different names in different fields, its meaning is not always made clear, and there are different ways of interpreting the concept. These are significant issues because PARs could have critical implications for understanding and reducing the prenatal origins of health and disease. As commonly understood, a PAR (in the context of this chapter) is a developmental response by the fetus to a uterine environmental cue such that—if it uses this cue to correctly anticipate or “predict” the future environment— the developmental response will be evolutionarily adaptive in its postnatal environment. Otherwise, if the fetal response does not correctly “predict” the postnatal environment, whether because the signal was not reliable, or the environment changed, there will be a maladaptive mismatch between the developmental calibration and postnatal environment (Bateson et al., 2004; Gluckman et al., 2005). PARs have stimulated extensive discussion and analysis about what information from its prenatal environment the fetus extracts and responds to. This discussion has provided great stimulus to the field but is currently unresolved. As we have emphasized throughout this chapter, the fetal environment includes information not only from the mother’s current environment, but her own developmental environment and even her mother’s and her grandmothers’ as well. Therefore, the question arises: How well can we expect 9 months of pregnancy to predict the child and adult environments of the future? ( Jones, 2005; Kuzawa, 2005; Worthman and Kuzara, 2005). Alternative (although not mutually exclusive) models of how adverse prenatal environments affect development and postnatal health have emerged. In their original form, PARs supposedly prepare organisms for future environments and provide “weather forecasts” via “fetal programming”. However, as we discussed in the context of life history theory, under harsh environments the priority is simply to survive. In this light, various models portray physiological changes during pregnancy to a challenging environment as “making the best of a bad start” (Berghänel et al., 2017; Jones, 2005;

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Rickard, Frankenhuis, and Nettle, 2014; Vitzthum, 2001). Focusing on survival is a form of downside risk protection. Individuals born into an adverse environment must change their physiology to ensure survival and avoiding lineage extinction rather than to “predict” a future environment that may never exist (Chisholm and Coall, 2008). Still other models see early adversity as a detrimental disruption no matter what its environment is like. These models are often referred to as “silver spoon” (the converse as “leaden/wooden spoon”) models (Grafen, 1988) and suggest that there is a lifelong fitness advantage or disadvantage associated with the early environments that individuals embody. Throughout this chapter, these different PAR models have been discussed in specific examples. At present, attempts to test the different predictions are underway, with some support for the silver versus leaden spoon model (Hayward and Lummaa, 2013). It is important to recognize that these models currently ignore the competing demands of the mother and fetus. Thus, the application of parentoffspring conflict theory to understanding the adaptive functions of prenatal environment may also be a fruitful area of research (Del Giudice, 2012; Gangestad, Caldwell Hooper, and Eaton, 2012). Attempts to rationalize the PAR models into manageable categories are under way (Monaghan, 2008; Nettle et al., 2013; Wells, 2012), but consensus is some way off. Some useful results have come from modeling comparing the “weather forecasting” and “leaden spoon” PAR models. Nettle et al. (2013) concluded that their model predicted (1) developmental plasticity would evolve to receive information from the maximum number of environmental cues available (especially if the cues were not highly reliable) and (2) that the reliability of cues from year to year would need to be exceptional to have adaptive value across an individual’s reproductive lifespan or even shorter durations. The relation between environmental risk and how it is embodied has been developed. Indeed, it may be useful to study the causal pathways by examining the interaction between both the environmental risk (external PAR) and how the risk is embodied physiologically (internal PAR; Hartman, Li, Nettle, and Belsky, 2017). More empirical and theoretical work is needed to turn the promising field of PARs into strategies for interventions to reduce the negative prenatal impact on offspring phenotype. We are currently at the threshold of an exciting new area of research.

Conclusions In this chapter, we have tried to make two overarching points: (1) the study of prenatal influences is no longer a “grey area” of modern science because (2) evolutionary theory—our only scientific theory of life (and development)—provides the “bio-logical” basis for coordinating the multidisciplinary evidence for prenatal influences and making sense of the patterns that emerge as maternal effects. We have endeavored to present an interdisciplinary perspective within an evolutionary, life history theory framework. Maternal stress, nutrition, and exposure to toxins all provide crucial information about the harshness of the environment into which a baby will be born. These cues provide the fetus with a guide to its optimal behavioral/physiological phenotype for survival and reproduction in its postnatal environment. When this adjustment is made during sensitive periods of development, such as prenatally, the short-term benefit of changes that ensure continued survival may be traded off against the longer-term costs of lifelong and intergenerational health.

Acknowledgments We thank Tom Dickins for valuable contributions, Toni Wain for editorial assistance, and Renee Khan-Passetti, Del Periera, Michelle Cannon, and Ruben Phillips for their invaluable research assistance. We also gratefully acknowledge support from the National Evolutionary Synthesis Center, Duke University.

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6 THE SOCIAL NEUROENDOCRINOLOGY OF HUMAN PARENTING Ruth Feldman

Introduction Nonhuman mammalian mothering is hormone-dependent; hormonal changes occurring during pregnancy and labor causally determine the expression of maternal behavior. Studies in animal models have shown that experimental manipulations on the expression of key hormones markedly alter or totally eliminate the expression of maternal care (Feldman, 2012b, 2016; Lonstein, Lévy, and Fleming, 2015; Pryce, 1996; Rosenblatt, 1994; Rosenblatt, 2003). Research in rodents describes the critical role of oxytocin (OT) and prolactin (PRL), which undergo substantial changes during late pregnancy (PRL) and surge at birth (OT), for the onset of maternal behavior. In parallel, hormones associated with the stress response, particularly corticosterone (cortisol in humans), modulate maternal vigilance and active protection of offspring (Brummelte and Galea, 2010; Mann and Bridges, 2001; Pedersen and Prange, 1985). Finally, animal studies point to the involvement of vasopressin (AVP) and testosterone (T) in the emergence of fatherhood and the expression of mammalian paternal care (Carter, 2014; Wynne-Edwards, 2001). In combination with sex-related hormones (estradiol, progesterone), these hormones establish the neuroendocrine milieu that enables rodent mothers—and fathers in the 3%–5% of mammalian species who are biparental (Braun and Champagne, 2014; Kleiman, 1977)—to parent. The hormones of parenting enable parents to recognize infants as rewarding stimuli, protect infants from harm, nurse, express species-typical parental behavior, and provide external regulation for the infant’s immature regulatory systems, including sleep organization, thermoregulation, autonomic functions, attention, and exploration (Feldman, 2016; Hofer, 1995a,b; Numan and Stolzenberg, 2009). These hormones also help parents usher their young into the social niche and accommodate its distinct features. Finally, the neuroendocrinology of parenting promotes the infant’s ability to manage life in harsh ecologies via mechanisms of endocrine fit and the effects of parental hormones on the infant’s brain maturation and social fittedness (Feldman, Monakhov, Pratt, and Ebstein, 2016). Human parenting is not hormone-dependent; however, hormonal changes during pregnancy, birth, and the postpartum period prime and accompany the expression of parenting, sculpting the development of the parent-child attachment and its long-term effects on the infant’s brain and behavior (Apter-Levi et al., 2016; Galbally, Lewis, IJzendoorn, and Permezel, 2011; Feldman, 2016, 2017; Gordon, Zagoory-Sharon, Leckman, and Feldman, 2010b, 2010c). Humans’ large associative cortex, neural plasticity, and massive limbic-cortical projections enable bottom-up, behavior-based processing so that committed parental care can trigger the hormones of parenting even without pregnancy 220

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and childbirth; for instance in primary-caregiving fathers or adoptive parents (Abraham et al., 2014; Bick, Dozier, Bernard, Grasso, and Simons, 2013). Yet, as parenting is the only social phenomenon observed across species and taxa, there is no other sociobiological process that can provide a clearer lens into evolution as it occurs and shed light on the roots of humans’ collaborative, empathic, and relational abilities (Feldman, 2015a, 2015b; Rilling and Young, 2014). Furthermore, the parent-infant interface marks the arena where Darwin (1859) has initially proposed structural and functional brain adaptations take place. The neuroendocrinology of human parental care, addressing the hormonal changes that accompany parenting and their neural, behavioral, and mental correlates, may thus afford a unique perspective on the evolution of human sociality, highlighting both its conserved and human-specific features (Feldman, 2015b, 2016). In addition to a special viewpoint on human sociality, the neuroendocrinology of parenting provides a unique angle on neural plasticity not available from other topics in neuroscience. Pregnancy and the postpartum mark the period of greatest plasticity in the adult brain (Leuner, Glasper, and Gould, 2010), and such plasticity is observed not only in the maternal but also in the paternal brain, with fathers’ investment in childrearing increasing plasticity not only in the father’s brain but also in the brain of his offspring (Braun and Champagne, 2014). Parenting, therefore, enables the investigation of endocrine systems and neural networks as they reorganize in the parent’s brain and research on how successful versus less optimal reorganization directly impacts the infant’s emerging endocrine systems and neurobiological outcomes. Furthermore, parenting is perhaps the most highly conserved social phenomenon, accompanied by similar species-typical behaviors that are triggered by the same neuroendocrine events across mammalian evolution (Feldman, 2015a, 2015b; Rilling and Young, 2014). This is particularly the case with regards to the ancient oxytocin system, which supports parenting, group cohesion, and stress management in species ranging from nematodes to humans, including birds, fish, and Caenorhabditis elegans (Feldman et al., 2016; Goodson, 2013). In comparison with the neuroscience of parenting, assessing the brain basis of emotions, memory, or categorization involves a much greater conceptual leap; these constructs are heuristic, much farther away from their biological underpinnings or evolutionary origins, and are constructed online by humans’ higher-order representations. When research on the neurobiology of parenting is coupled with detailed observations of parental behavior in the natural habitat, it provides a closer setting to that of nonhuman mammals as compared to most other domains in neuroscience. Yet, notwithstanding the similarity of human parental care with that of other mammals, human parenting is also greatly influenced by humans’ higher-order cognitive abilities and cultural construals. Thus, research on the neurobiological basis of parenting affords a unique view on the integration of mammalian-general and human-specific features on key biological processes. Because parenting is triggered by the same hormones across mammalian species, the hormonal basis of human parenting provides a scientifically plausible tool for mechanistic research as compared to other domains of inquiry (e.g., the neurobiology of psychiatric illness); hence, the neuroendocrine basis of parenting is among the few topics that offer a uniform trajectory of empirical investigation across the evolutionary ladder. The social neuroendocrinology of human parental care comprises four main lines of research. The first assesses the hormonal basis of parenting in healthy parents. Most of this line of research focuses on the hormones of motherhood; the typical hormonal changes occurring in mothers during pregnancy, the postpartum period, and across the early years. Often, these studies examine not only mean-level changes but also individual differences in hormonal levels and their links with maternal behavior, attitudes, or personality traits. To date, the hormone receiving the most research in relation to mothering is cortisol (CT), possibly due to its reliable bioassay in saliva that has been available for some time. Yet, with the development of more sensitive bioassays, studies have also looked at OT, PRL, AVP, T, salivary alpha amylase (sAA), beta endorphin, and immune biomarkers (IL-6, salivary IgA). Another area of research within this global line is the hormones of fatherhood. Fathering in general, and the neurobiology of fathering in particular, has received much less research 221

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as compared to mothering in both humans and other mammals, but the hormonal basis of fathering is a developing area of research and a growing body of literature is beginning to assess fathers’ hormones in relation to observed paternal behavior. The second line of research on parental hormones examines “endocrine fit”—the “match” or synchrony between parent and child hormonal levels. Such biological synchrony is conceptualized as one mechanism by which the parental affiliative system is transferred to the child or as a way in which parents signal environmental danger to their offspring (Feldman, 2016, 2017; Pratt et al., 2017; Bornstein, 2013). Our biobehavioral synchrony model contends that such hormonal synchrony, while genetically informed, matures in the context of coordinated social behavior and shared parent-child social experiences (Feldman, 2012c, 2015a, 2016, 2017). A third line views the neurobiology of human parenting as a global area of research, which includes the brain networks, hormonal systems, and specific behaviors that activate in mothers or fathers with the birth of an infant. Several studies in this line test associations between activations of specific brain areas in the parental brain with parenting-related hormones, including OT, AVP, CT, or T (for a review see Feldman, 2015b). It is hypothesized that the “mammalian parenting network”, the brain regions that support mammalian parenting, initiates its activation through sensitization by the hormones of pregnancy (Numan and Young, 2016), thus indicating that hormonal changes trigger neural alterations that define the neurobiology of parenting. The last area of research in the neuroendocrinology of parenting, and by no means the least abundant, addresses parental hormones under high-risk conditions, whether the risk stems from motherrelated conditions (e.g., maternal depression, anxiety), child-related conditions (prematurity, autism spectrum disorders), or contextual adversities (poverty, abuse, war exposure). Several studies of highrisk parenting compared a high-risk cohort to a typical group, whereas others use a correlational design within the high-risk sample. Of note, very few studies examine fathers’ hormones in high-risk contexts, and a smaller number of studies address the fit between high-risk parents and children. The following literature reviews the hormonal basis of human parenting keeping in mind its evolutionary origins. Due to the extensive literature on the topic, this review is by no mean comprehensive and addresses mainly parental hormones in the first years of life, with a focus on infancy, and follows the four lines of research outlined above. Consistent with the comparative approach, only studies that measure hormones in relation to observed parental behavior are reviewed. This approach accords with the view that in humans the neurobiology of parenting may trigger, not only through pregnancy and lactation, but via commitment to caregiving and active involvement in daily interactions with the child. Thus, similar to the long line of  “cooperative breeding” in primates, the human “village” (grandparents, “aunties”, male partners, adoptive parents, godparents) can rear the child through bottom-up, behavior-based activation of the neurobiology of parenting, consistent with Hrdy’s (2007) suggestion that in species such as mammals parenting is behavior (Feldman, 2012d). This conceptualization of a bottom-up activation of the neurobiological systems that support parenting via parenting behavior is consistent with findings that mother-child synchrony expresses in the brain as brain-to-brain synchrony of gamma-band oscillations, with gamma marking a distinct bottom-up, behavior-based mechanism (Levy, Goldstein, and Feldman, 2017).

Hormonal Basis of Human Mothering and Fathering in Low-Risk Contexts This section describes each hormonal system separately and addresses findings related to mothering and fathering for each hormone. Following, a section discusses endocrine fit. Overall, hormones of parenting are divided into the “affiliative hormones” module, which includes mainly OT but also AVP and PRL, hormones that support the formation of parent-infant bonding, maintain attachments, and buttress human sociality (Carter, 2014; Fleming, Ruble, Krieger, and Wong, 1997; 222

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Numan, 2006). The other group involves stress-related hormones, mainly CT but also salivary alpha amylase (sAA) or immune biomarkers (IL-6, IgA). A third group considers sex-related hormones (T, progesterone, estradiol). These three classes of hormones are not independent in their action, and studies have shown co-dependence and mutual influences of these hormones on each other, mainly in complex, nonlinear ways that require much further research (Gordon, Zagoory-Sharon, Leckman, and Feldman, 2010a; Gordon et al., 2017). Research in rodents has further shown that the expression of maternal behavior functions on both the affiliation and stress neuroendocrine systems, with maternal licking and grooming building the expression of both oxytocin receptor densities in the nucleus accumbens (Francis, Champagne, and Meaney, 2000) and glucocorticoid receptors in the hippocampus of the infant’s brain (Liu et al., 1997). Figure 6.1 describes OT and CT as the main, most well-research hormones of parenting, their mutual influences on other hormones, and their behavioral correlates.

Oxytocin Oxytocin is considered the main neuroendocrine system supporting the formation and maintenance of the parent-infant bond and a central trigger for the expression of parental behavior

Figure 6.1 Key hormones of human parenting.

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(Feldman, 2015b, 2016, 2017). It is an integrative system that provides a neuroendocrine milieu for the functioning of multiple hormones. Numerous hormones operate in concert to support parental care, but OT maintains crosstalk with other hormones in the context of parenting. We found that OT links and interacts with a range of hormones in supporting parenting behavior, including AVP (Apter-Levi, Zagoory-Sharon, and Feldman, 2014), CT (Gordon et al., 2010a), T (Gordon et al., 2017; Weisman, Zagoory-Sharon, and Feldman, 2014), beta endorphin, and IL-6 (Ulmer-Yaniv et al., 2016), highlighting the role of OT in integrating the affiliation, reward, stress, and immune systems in support of parenting. OT is a nine-amino-acid neuropeptide hormone, which presumably evolved from the ancient vasotocin molecule via gene duplication in jawed fish approximately 650 million years ago (Feldman et al., 2016). OT is implicated in sociality across vertebrate evolution and substantial research in rodents has pinpointed its role in birth, lactation, and maternal care in mammals (Carter, 2014; Feldman et al., 2016; Lee, Macbeth, Pagani, and Young, 2009; Lim and Young, 2006). Studies have examined peripheral levels of OT—in plasma, saliva, urine, and to a lesser extent in cerebrospinal fluid—in relation to human parenting, aided by the availability of new and more reliable immunoassay kits. Associations between brain OT and its peripheral indices are not fully clear, but human studies have lent support to the use of peripheral OT by demonstrating marked increase in peripheral OT when individuals inhale OT, which has shown to impact the brain’s OT system (Neumann, Maloumby, Beiderbeck, Lukas, and Landgraf, 2013; Weisman, Zagoory-Sharon, and Feldman, 2012), associations between plasma OT and more efficient variants of the oxytocin receptor gene (OXTR; Feldman et al., 2012), and correlations between plasma and salivary OT with brain activations in areas rich in oxytocin receptors, including the hypothalamus or the amygdala (Abraham et al., 2014; Atzil, Hendler, and Feldman, 2011; Strathearn, Fonagy, Amico, and Montague, 2009). The distributions of OT receptors in the brain are species-specific (Stevens, Wiesman, Feldman, Hurley, and Taber, 2013) and the nature of the relation between central and peripheral OT is a matter of ongoing debate, but an accumulating body of research has shown that variability in peripheral OT is meaningfully linked with the expression of maternal and paternal behavior in ways that are consistent with research on central OT in rodents. In the first longitudinal study of OT and parenting behavior, we followed healthy women across pregnancy and the postpartum and measured plasma OT and cortisol (CT) at three time-points; first trimester of pregnancy, third trimester, and the first postpartum month when we also observed mothers interact with their infant in the home environment. We used an in-depth interview to measure maternal thoughts, preoccupations, and attachment representations. OT levels increase in early pregnancy and stay stably high across pregnancy and the early postpartum. OT levels during the first trimester predict the expression of the human species-typical maternal behavior, suggesting a priming effect of OT in humans. In addition, OT and CT across pregnancy are unrelated at any time-point, but CT levels independently predict a decrease in the expression of maternal postpartum behavior, indicating a joint effect of the two main hormonal systems on maternal postpartum behavior similar to that found in rodents (Feldman, Weller, Zagoory-Sharon, and Levine, 2007). Another evidence for a priming effect was found when mothers with higher OT during late pregnancy reported greater bonding to their fetus (Levine, Zagoory-Sharon, Feldman, Lewis, and Weller, 2007). It has been suggested that mothers develop clear representations of their unborn child during the last weeks of pregnancy and a failure to do so, due to depression or risk for preterm delivery, impairs the emerging attachment (Hart and McMahon, 2006; Pisoni et al., 2016). OT in late pregnancy also predicts increased maternal preoccupations and more positive representations of the infant and the attachment relationship. Others found similar links between attachment representations and higher OT levels in pregnancy and the postpartum (Eapen et al., 2014). These findings, therefore, add the representational component to the priming effect in other mammals and show that in humans the higher-order cognitive dimension of parenting is similarly triggered by the oxytocinergic system. 224

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We next followed first-time mothers and fathers from the first postpartum month to 6 months postpartum and measured plasma OT in relation to maternal and paternal parenting behavior. Postpartum parents had much higher OT levels as compared to individuals who were not parents or in a romantic relationship, indicating that OT levels increase when individuals become attached. In addition, no difference was found between mothers’ and fathers’ baseline OT, even when mothers were breastfeeding. Similar to the first study, OT levels in individuals were highly stable over time, and mutual influences between partners’ OT were observed both within and across time-points (Gordon, Zagoory-Sharon, Leckman, and Feldman, 2010b). This result suggests that plasma OT may tap a “trait-like” dimension of the individual which is individually stable yet shaped by close attachment relationships (Schneiderman, Kanat-Maymon, Ebstein, and Feldman, 2014). OT levels in mother and father were related to the parent-specific behavioral repertoire (Feldman, Gordon, Schneiderman, Weisman, and Zagoory-Sharon, 2010). Maternal OT was related to the “affiliative parenting” constellation typical of mothers, including gaze to infant face, expression of positive affect, “motherese” high-pitched vocalizations, and affectionate touch, the human parallel of “licking-andgrooming” (Meaney, 2001). In contrast, fathers’ OT was linked with “stimulatory parenting”, a style typical of mammalian fathering, which included directing attention to the environment, stimulatory contact, and high, unpredictable positive arousal (Gordon et al., 2010b; Naber, van IJzendoorn, Deschamps, van Engeland, and Bakermans-Kranenburg, 2010). These findings, the first to test plasma OT in new fathers, show comparable OT levels in mothers and fathers and indicate that fathers may be just as biologically prepared to care for infants. In comparison with mothers’, fathers’ parenting style is expressed via a distinct set of behaviors that prepare infants to explore their physical environment, rather than focus on the dynamics of face-to-face relationships, and this paternal repertoire is linked with father’s OT. Finally, observing triadic family interactions between these parents and their 6-month-old infants we found that OT predicted triadic synchrony, the coordination of behavior among the three family members (Gordon et al., 2010a), highlighting the role of OT as an integrator of social behavior among affiliative units. Comparing OT in plasma, saliva, and urine in a group of mothers and fathers (not couples) and their 4- to 6-month-old infants, we found no differences in baseline OT levels in plasma, saliva, or urine between mothers and fathers. Of note, OT levels in saliva and plasma showed mid-level correlations, and similar associations were found in several other samples, but no correlations emerged between these indices and urinary OT, possibly since urinary hormone concentrations travel through a different bodily route. Both plasma and salivary OT were related to higher parent-infant synchrony (Feldman, Gordon, and Zagoory-Sharon, 2011). Similar associations obtain between mothers’ plasma OT response (change from baseline to post-interaction) and gaze coordination and gaze duration between mothers and their 7-month-old infants (Kim, Fonagy, Koos, Dorsett, and Strathearn, 2014). In contrast to plasma and salivary OT, urinary OT predicts greater parental stress and attachment anxiety, highlighting the dual role of OT in linking to both the affiliative and the anxiety/vigilance components of parenting (Feldman, Gordon, et al., 2011). These findings are consistent with data from a large cohort of women and men, both parents and nonparents, which showed that in women plasma OT levels are positively associated with measures of attachment anxiety (Weisman, ZagoorySharon, Schneiderman, Gordon, and Feldman, 2013) as well as with research in animal models pointing to the role of OT in modulating stress and anxiety (Neumann and Slattery, 2016). Urinary OT has been linked with infant caregiving behavior in cooperative-breeding marmoset monkeys (Finkenwirth, Martins, Deschner, and Burkart, 2016), and listening to mother’s voice during a stress paradigm elevated children’s urinary OT and enabled better stress management (L. J. Seltzer, Ziegler, and Pollak, 2010), validating urinary OT as a biomarker of parental care. In the first months of life, parental plasma OT levels are associated with allelic variability on the OXTR on key SNPs associated with attachment, including OXTR (rs2254298 and rs1042778) and CD38 (rs3796863), as well as with more parental touch and greater gaze synchrony, the two 225

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main features of close attachment bonds (Feldman et al., 2012). These findings are consistent with numerous studies showing associations between more functional OXTR variants with sensitive parenting and attachment security throughout life (Bakermans-Kranenburg and van IJzendoorn, 2008; Feldman et al., 2016; Raby, Cicchetti, Carlson, Egeland, and Collins, 2013). Consistent with findings on the cross-generational transmission of OT functionality in rodents, which is mediated by maternal behavior (Champagne, 2008; Champagne, Diorio, Sharma, and Meaney, 2001), parental OT in the first months of life shapes the infant’s OT system and this crossgeneration transmission is similarly moderated by synchronous parenting; links between parent and child OT are found only when parents engage in synchronous interactions, but not when minimal synchrony is observed (Feldman, Gordon, and Zagoory-Sharon, 2010). In another study, following parents and infants from the first month of life to the preschool stage, we similarly found crossgenerational transmission over time and attachment bonds. Parents’ plasma OT in the postpartum predicted child salivary OT at preschool as mediated by early parental behavior. Furthermore, parental OT and synchronous parenting shaped not only the child’s OT but also the degree of reciprocity and positive engagement during interactions with the first best friend at 3–4 years, consistent with attachment theory’s predictions that parental care shapes children’s ability to enter subsequent attachments in their lives, with friends, mentors, and romantic partners culminating in their ability to parent the next generation (Feldman, 2012b; Feldman, Gordon, Influs, Gutbir, and Ebstein, 2013). The OT response is sensitive to parental touch. Mothers and fathers were tested in the 10-minute “play and touch” paradigm, where a parent interacts with the infant freely and is instructed to “touch your infant as you normally do”. Mothers who provided abundant amounts of affectionate touch, but not those who provided little touch, showed an OT increase following the interaction. In parallel, fathers who had high levels of stimulatory contact, but not those who showed little touch, increased their OT levels (Feldman et al., 2010). Furthermore, infants as young as 4 months displayed OT increases following synchronous interactions with their parents (Feldman, Gordon, and ZagoorySharon, 2010). Like rodents, human parent-specific touch, when provided in abundance, elicits OT response in parents, which, in turn, elicits a parallel OT response from the infant, priming the infant’s OT system to respond to pleasurable social touch within future attachment relationships. Finally, animal studies have suggested that neuroendocrine changes in mothers during pregnancy and the postpartum provide a template for pair bonding, and, thus, there is continuity between hormonal processes implicated in parental and pair bonding (Numan and Young, 2016). We measured plasma OT, beta endorphin, and IL-6—biomarkers of the affiliation, reward, and immune systems— in a group of first-time parents and their 3-month-old infants, a group of new romantic partners who had been together for 3 months, and unattached singles. Synchrony between parents and infants and among new lovers was microcoded. We found that all hormonal systems underwent changes with the formation of new attachment bonds. OT increased in parents but was highest in new lovers. In contrast, both beta endorphin and IL-6 were highest in parents, lowest in singles, and at mid-level in lovers. In addition to increase, biomarkers of affiliation, reward, and stress management coalesced, and the correlations between them became tighter during periods of bond formation. Finally, the effects of beta endorphin and IL-6 on behavioral synchrony were mediated by the oxytocin system (UlmerYaniv et al., 2016). These findings, combined with the aforementioned continuity between parental and filial attachment (humans’ attachment to their close friends) highlight the integrative role of OT across human affiliative bonds, as mediated by sensitive parenting (Feldman, 2012a, 2012c). Research has also investigated the effects of intranasal OT administration on a plethora of human social functions. Several studies showed effects of OT administration on increasing fathers’ energetic and object-focused interactions with their toddlers (Naber et al., 2010) or on brain response to infant cry and laughter among nonparents (e.g., Riem et al., 2011, 2012). In the context of parental hormones and behavior, we administered OT to 35 fathers of 5-monthold infants in a double-blind placebo-controlled within-subject design, examined paternal and infant 226

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hormones, and microcoded social behavior. As expected, intranasal OT administration markedly increased fathers’ salivary OT; however, surprisingly, OT administration to parent increased the infant’s salivary OT by 30-fold, although infants were taken out of the room where fathers inhaled OT and remained outside for the 45-minute waiting period. This measurable increase in infant OT may point to mechanisms of chemosignaling between parent and child which require much further research. Under the OT condition, subtle differences in parent and child’s social behavior were observed; fathers touched infants more and gently reoriented infants back to the joint play when they averted gaze. Infants gazed at their fathers for longer durations and engaged in longer episodes of joint exploration. Autonomic signs were also higher in the OT condition, and both father and infant increased cardiac vagal tone, a biomarker of social engagement (Weisman et al., 2012). OT administration to fathers also impacted the infant’s CT levels as mediated by father-infant synchrony. Among infants experiencing high synchrony, paternal still-face increased CT production and elevated infants’ social gaze to the nonattentive parent. However, among infants experiencing low paternal synchrony, OT reduced the infant’s stress response and decreased social gaze to the father during the still-face phase (Weisman, Zagoory-Sharon, and Feldman, 2013). As OT increases the social salience of events (Shamay-Tsoory and Abu-Akel, 2016), it is possible that among infants who internalized an engaged and available paternal style, the OT condition enhanced their social attention to father’s communicative failure.

Vasopressin AVP is a structurally similar neuropeptide to OT, both originating from the ancient vasotocin molecule, and both implicated in mammalian fathering (Carter, 2014), but little research has examined peripheral AVP in relation to human parenting. Studies in rodents suggest that AVP is involved in physiological changes in AVP in fathers may mediate changes in energy balance and stress reactivity that are required for the onset of fathering (for review: Bales and Saltzman, 2016; Saltzman and Ziegler, 2014). AVP is associated with male bonding and defensive and territorial behavior (Bielsky, Hu, Ren, Terwilliger, and Young, 2005), and AVP promotes social recognition in both rodents (Caldwell, Lee, Macbeth, and Young, 2008) and human males (Guastella, Kenyon, Unkelbach, Alvares, and Hickie, 2011). Regions characterized as part of the AVP circuitry are implicated in socio-cognitive processes in both humans and rodents (Goodson and Thompson, 2010). This AVP-brain associations may represent elevated AVP-dependent vigilance, which supports father’s ability to read the intention of others to defend mother and young (Thompson, George, Walton, Orr, and Benson, 2006). In contrast, AVP supports the mother’s ability to befriend others. Thus, AVP may prompt differential social strategies in social contexts in women and men (Thompson et al., 2006). Research on AVP is predominantly male oriented as AVP has been mostly studied in the context of autism and aggression. Variability on the AVP receptor gene has been associated with observed parenting in healthy parents (Avinun, Ebstein, and Knafo, 2012) as well as the context of continuous trauma exposure (Feldman, Vengrober, and Ebstein, 2014). OT administration to males and females increases both AVP (Weisman, Schneiderman, Zagoory-Sharon, and Feldman, 2013), indicating affinity between the expression of the two neuropeptides. Only two studies, to our knowledge, measured plasma AVP levels in parents. In the first, OT and AVP were measured in relation to neural activations in the maternal and paternal brain (Atzil, Hendler, Zagoory-Sharon, Winetraub, and Feldman, 2012). AVP correlated with fathers’, but not mothers’, amygdala response to infant stimuli, supporting the links between fathering and AVP in humans. In the second study, OT and AVP levels in mothers and fathers of 4-month-old infants were measured in relation to parent-infant interactions. No mean-level differences emerged in AVP between mothers and fathers, but plasma OT and AVP were associated with distinct configurations of parental behavior. Parents with higher OT directed their infants toward a social focus, enhancing 227

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behaviors such as gaze coordination and affectionate contact, behaviors that were more prevalent in mothers. In contrast, parents with high AVP engaged in stimulatory contact and tended to increase object-salience when infants showed bids for social engagement, a behavioral profile more common in fathers. Thus, synchronous processes with mother and father within the family unit distinctly prepare children to join the larger social world (Apter-Levi et al., 2014). (Another study followed parents and infants across the first 6 years of parenthood in relation to brain activations and assessed salivary AVP and is described below in the section on hormones and the parental brain.)

Prolactin Prolactin (PRL) is a peptide hormone originating mainly in the anterior pituitary lactotroph cells (Freeman, Kanyicska, Lerant, and Nagy, 2000) that has multiple effects on reproduction and lactation and is thought to mediate the formation of affiliative bonds (Neumann, 2009). PRL is released within the hypothalamus and other limbic areas during mother-infant contact in rodents (Torner et al., 2004) and its administration stimulates maternal care in rats (Bridges, DiBiase, Loundes, and Doherty, 1985). PRL has been examined in relation to fatherhood in a number of animal species (Storey, Delahunty, McKay, Walsh, and Wilhelm, 2006; Wynne-Edwards, 2001; Ziegler, Wegner, Carlson, Lazaro-Perea, and Snowdon, 2000). In humans, studies have shown that both men and women exhibit elevated levels of plasma PRL before childbirth, and fathers who report being more affected by infant cues show higher PRL (Fleming, Corter, Stallings, and Steiner, 2002; Storey et al., 2006). Experienced fathers show greater increases in PRL when listening to infant cries as compared to first-time fathers (Fleming et al., 2002). In contrast to single men, fathers’ PRL does not decline following interaction with their toddler (Gray, Parkin, and Samms-Vaughan, 2007). Among fathers to 6-month-old children, plasma PRL correlates with OT levels and higher paternal PRL is associated with greater attention to the environment and joint father-child exploratory play (Gordon et al., 2010c). In mothers, on the second post-birth day, a rise in PRL was found 20 minutes after infant suckling ( Jonas et al., 2009). Infant stimulation of nipple induces both OT and PRL responses (McNeilly, Robinson, Houston, and Howie, 1983). Finally, between 4–6 weeks postpartum, higher PRL correlates with lower stress and better mood only among formula-feeding mothers (Groër, 2005), and following cesarean delivery OT and PRL are related to lower anxiety (Nissen, Gustavsson, Widström, and Uvnäs-Moberg, 1998). Overall, early animal studies on the neurobiology of maternal care described the contribution of both OT and PRL, but human studies have placed much greater emphasis on the role of OT, with less research devoted to the links between PRL and observed parenting.

Testosterone Testosterone is an androgenic steroid produced by the hypothalamic-pituitary-gonadal (HPG) axis that modulates reproductive behavior and plays a key role in human social behavior, particularly in behaviors associated with social status, at times in combination with aggressive behavior (Eisenegger, Haushofer, and Fehr, 2011; Mazur and Booth, 1998; Wingfield, Hegner, Dufty, and Ball, 1990). Testosterone’s involvement in parenting and pair bonding has been described in human and other mammals (Kuzawa, Gettler, Muller, McDade, and Feranil, 2009; van Anders and Goldey, 2010), and alterations in T levels in males are thought to reflect a shift between conflicting reproductive strategies, from mating efforts to parenting efforts (Gray and Anderson, 2010). Studies in more than 60 bird species support the “challenge hypothesis”, which suggests that T levels increase when males compete for food and territory and decrease when males must care for offspring (Wingfield et al., 1990). Research in biparental species shows that fathers’ T levels decrease in the presence of a dependent offspring (Wynne-Edwards, 2001). For example, marmoset males who carried infants the most had 228

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the lowest urinary T levels (Nunes, Fite, Patera, and French, 2001) as well as the greatest declines in gonadal steroids (Nunes et al., 2001), and exposure to infant scent lowered serum testosterone in father common marmosets (Prudom et al., 2008). In the monogamous and biparental California mouse (Peromyscus californicus), greater T-increase during courtship is associated with paternal cuddling and a protective repertoire towards their pups (Gleason and Marler, 2010). Similar findings have emerged in human fathers. High T was found in single and divorced men, and low T in men and women within a committed relationship as well as in new fathers (Booth and Dabbs, 1993; Burnham et al., 2003; Gettler, McDade, Feranil, and Kuzawa, 2011; Mazur and Michalek, 1998; van Anders and Goldey, 2010). During the transition to fatherhood, men decrease their T levels (Berg and Wynne-Edwards, 2001; Perini, Ditzen, Fischbacher, and Ehlert, 2012), and such decrease is associated with positive paternal behavior (Fleming et al., 2002). A study in the Philippines assessing men before and after becoming fathers showed a decline in T levels in fathers, which correlated with the degree of father involvement in childcare (Gettler, McDade, Agustin, Feranil, and Kuzawa, 2013). In our study of intranasal OT administration to fathers, we found that lower baseline paternal T was associated with more optimal father and infant social behavior, including gaze, vocalizations, and touch (Weisman et al., 2014). Furthermore, OT-induced changes in T correlate with more positive affect, social gaze, and synchrony, consistent with the perspective that neuroendocrine systems in human males evolved to support committed and flexible fathering (­Ziegler, 2000). Very few studies test T in mothers. An increases in T was found in pregnant women (Edelstein et al., 2015; Fleming et al., 1997), and mothers’ T levels were associated with infants’ physical and socioemotional health and lower maternal depression ( J. I. Cho, Carlo, Su, and McCormick, 2012; J. Cho, Su, Phillips, and Holditch-Davis, 2016). We found that across the first months of parenting, fathers’ T is associated with lower behavioral synchrony, and mothers’ T is not directly related to maternal behavior (Gordon et al., 2017). However, in the context of high T, maternal OT predicts greater mother-infant synchrony, further supporting the mutual influences of OT on T, which require much further research. Assessing diurnal T in mothers and fathers of two preschool-aged children, among fathers more diurnal variability in T was associated with more sensitivity and respect for autonomy, whereas for mothers greater diurnal variability correlated with less sensitivity, further indicating that T carries differential effects on mothering and fathering (Endendijk et al., 2016). Higher maternal testosterone and infant cortisol are associated with more positive and more frequent maternal interactive behaviors ( J. Cho, Su, Phillips, and Holditch-Davis, 2015). It thus appears that the direct and mediated effects of T on parenting, particularly mothering, requires much further research both in relation to the effects of T on behavior and the effects of T on other hormones.

Cortisol Cortisol is a steroid hormone secreted by the hypothalamic-pituitary-adrenal (HPA) axis in conditions of physical and psychological stress (Lupien, McEwen, Gunnar, and Heim, 2009). Cortisol is a key component of the stress response, and as parenting is a highly stressful evolutionarily adaptive process, research has pointed to CT’s participation in the vigilant component of parenting. A large body of research in humans and animal models links CT with the regulation of maternal behavior, and, to a lesser extent, with paternal caregiving (Fleming et al., 1997; Wynne-Edwards, 2001; Ziegler, 2000). Most research on cortisol in the context of parenting is related to maternal stress, and the vast majority of studies utilize CT as an index of stressed parenting, associated with maternal early or current life stress. The various components of the stress response are indexed in parenting research by multiple CT indices, including basal cortisol, cortisol reactivity to stressful paradigms, diurnal CT production, and hair cortisol (Levine et al., 2007). Overall, the stress response involves complex interactions between 229

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the sympathetic nervous system and the HPA axis, allowing to both prepare for danger and return to baseline once threat is removed (Laurent, Ablow, and Measelle, 2012; Lupien et al., 2009). The HPA axis comprises the hormones CRH, ACTH, and cortisol, which interact with contextual factors to shape both momentary stress reactivity and long-term stress physiology (Ellis and Essex, 2007; Romeo, 2010). Cortisol plays an important role in the stress response by preventing over-reaction of the immune system to threats and acting on the hypothalamus and pituitary gland via negative feedback loops to foster homeostasis once safety is achieved (Kudielka, Hellhammer, and Wüst, 2009; Miller, Chen, and Zhou, 2007; Smyth, Hucklebridge, Thorn, Evans, and Clow, 2013). Extant evidence in humans and animals has shown that maternal care provides social buffering of HPA axis activity in offspring (Hostinar, Sullivan, and Gunnar, 2014; Jessop and Turner-Cobb, 2008; Moriceau and Sullivan, 2006; Shionoya, Moriceau, Bradstock, and Sullivan, 2007). Beginning in infancy, when the child’s HPA system is labile, and across childhood and adolescence, sensitive parenting attenuates children’s HPA reactivity, expressed in smaller cortisol increases or quicker returns to baseline following stress (Albers et al., 2008; Blair et al., 2008; Berry et al., 2016; Feldman, Singer, and Zagoory, 2010). In contrast, insensitive parenting, expressed in intrusive, unavailable, and fragmented parental style, alters the development of children’s stress response and threat-detection neurobiological circuits (Hostinar et al., 2014) and correlates with higher CT production (Ahnert et al., 2004; Berry et al., 2016; Bosquet Enlow et al., 2014; Marceau et al., 2015) or inflexible cortisol response and reduced variability (Apter-Levi et al., 2016). Thus, a central line in the study of CT relates to how the nature of parental care shapes the development of children’s HPA axis functioning. Less research on CT in the context of parenting addresses CT in the parent, and some of these studies measures parental CT in conjunction with child CT. The bulk of this research focuses on high-risk conditions (see below), with less research assessing parental CT in low-risk samples. Thus, from the extant literature and reviews available on the cross-generational transmission of human stress physiology (for review see Bowers and Yehuda, 2016) less research has focused on CT in relation to observed parental behavior in low-risk mothers, and even less research has tested paternal CT in relation to paternal behavior in typically developing families. Regarding CT and mothering, in the newborn period, reports are mixed on the relations of CT to maternal behavior. Some found the expression of maternal behavior to correlate with higher CT (Fleming, Steiner, and Anderson, 1987), but our assessment of plasma CT across pregnancy and the postpartum month showed that CT increased in late pregnancy and higher CT predicted restricted maternal behavior (Feldman et al., 2007). Starting at 3–4 months, research has measured CT in mothers and infants in stressful paradigms, such as the “still-face”, and most studies across infancy, childhood, and adolescence describe links between higher maternal CT, expressed in higher basal levels, greater stress reactivity, and slower recovery from stress, and less optimal parenting, expressed in lower sensitivity, decrease reciprocity, and greater intrusiveness (for review, Gunnar, Talge, and Herrera, 2009). Although most studies on CT and stress-inducing paradigms focus on infant CT, few also test maternal CT. For instance, higher maternal basal cortisol and greater reactivity to the “still-face” at 6 months are related to higher intrusiveness and lower second-by-second synchrony (Feldman, Singer, and Zagoory, 2010). Similarly, mothers with higher parenting-focused mindfulness show steeper cortisol recovery slopes following the still-face at 6 months (Laurent, Duncan, Lightcap, and Khan, 2017). Maternal blunted cortisol awakening response (CAR), the typical increase in CT from wakening to 30 minutes post-wakening, during pregnancy predicts lower infant emotion regulation as mediated by maternal sensitivity (Thomas, Letourneau, Campbell, Tomfohr-Madsen, and Giesbrecht, 2017). Similarly, higher diurnal cortisol production is linked with maternal retrospective report of early life stress and predicts lower sensitivity to their 2–6 months (Gonzalez, Jenkins, Steiner, and Fleming, 2012). Of note, among mothers and infants aged 6–12 months, those of low socioeconomic status (SES) had higher diurnal CT production compared to high-SES mothers and infants, as well 230

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as lower adrenocortical synchrony (Clearfield, Carter-Rodriguez, Merali, and Shober, 2014). Overall, these studies indicate that across CT biomarkers more attuned parenting and greater maternal abilities to allocate resources to the child are associated with lower CT. In fathers, CT declines following father-toddler interaction, as does fathers’ PRL, and the decline in CT is greater in experienced, compared to first-time, fathers (Gettler, McDade, Agustin, and Kuzawa, 2011). Testing fathers of 22-month-old toddlers following father-child interactions on a day they spent several hours alone with the child prior to testing versus days without the child, it was found that CT generally declined following interaction, but a greater decline was observed when fathers spent time alone with the child (Storey, Noseworthy, Delahunty, Halfyard, and McKay, 2011). We found greater diurnal CT production in mothers of 6-month-old infants compared to fathers and both parents’ CT was negatively related to warmth and sensitivity during triadic mother-fatherinfant interaction (Gordon et al., 2010a). These studies highlight the stress-reducing function of positive father-child interaction on the father’s overall cortisol production and CT response. The use of hair cortisol analysis in humans provides a measure of more chronic aspects of the stress response (Burnard, Ralph, Hynd, Edwards, and Tilbrook, 2016; Russell, Koren, Rieder, and Van Uum, 2012; Stalder and Kirschbaum, 2012; Staufenbiel, Penninx, Spijker, Elzinga, and van Rossum, 2013). Each centimeter of hair approximates one month of cortisol secretion, thus measuring CT in hair presumably integrates free steroids over the time of growth (Russell et al., 2012; Stalder et al., 2016), and thus hair cortisol concentrations (HCC) are thought to provide a retrospective month-by-month measure of cumulative cortisol secretion and serve as a reliable biomarker of chronic stress (Hinkelmann et al., 2013; Ouellette et al., 2015; Simmons et al., 2016; Steudte et al., 2013; Vanaelst et al., 2012). HCC has been studied mainly in the context of chronic stress, trauma, and psychiatric illness, and very few studies have integrated this measure into parenting research. In children, HCC is associated with lifetime trauma (Simmons et al., 2016), fearfulness upon school entry (Groeneveld et al., 2013), the number of major childhood traumatic life events (Vanaelst et al., 2012), and lower SES, which likely involves greater chronic stress (Rippe et al., 2016; Vliegenthart et al., 2016). Higher parenting stress and greater child socioemotional difficulties are linked with children’s elevated HCC (Palmer et al., 2013). Similarly, mild perinatal adversity, such as late preterm birth, moderates the links between maternal harsh parenting and HCC in 6-year-old children (Windhorst et al., 2017). These studies suggest that, if little research has integrated hair measurement in parents, HCC may be a unique biomarker of the stress response that requires much further research in the context of low- and high-risk parenting.

Salivary Alpha Amylase Salivary alpha amylase (sAA) has been integrated into research on parenting and child outcomes an index of the sympathetic-adrenal-medullary (SAM) arm of the stress response (Hellhammer, Wüst, and Kudielka, 2009; Nater and Rohleder, 2009). The stress response involves the coordinated functioning of two major anatomically distinct systems, the SAM, which initiates the fight-or-flight response by increasing blood flow, respiration, cardiovascular activity, and the release of catecholamines (Nater and Rohleder, 2009), and the HPA system, which has a more gradual onset and is associated with physiological and behavioral withdrawal (Bauer, Quas, and Boyce, 2002; Tarullo and Gunnar, 2006). Whereas momentary stress induces immediate changes in each system, chronic stress exerts a lasting effect and may alter the balance between the functioning of the SAM and HPA systems (Wolf, Nicholls, and Chen, 2008). Salivary alpha amylase has mainly been tested in children and less commonly in parents in the context of stress, both alone and in relation to CT (Wolf et al., 2008). In children, sAA has been tested in relation to physical health (Wolf et al., 2008), negative emotional reactivity (Spinrad et al., 2009), and attachment under stress (Frigerio et al., 2009). Similar to 231

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CT, the bulk of sAA studies have been conducted in high-risk samples (see below). Lower sAA was found among maltreating mothers and reduced reactivity to infant crying compared to nonmaltreating mothers (Reijman et al., 2015). Insecure-avoidant 1-year-old infants had higher sAA levels following the strange situation paradigm and their mothers, who showed no differences in sAA, exhibited less vagal withdrawal in the reunion episode (Hill-Soderlund et al., 2008). Parent-child relationship quality predicts the associations between marital conflict and higher child sAA reactivity (Lucas-Thompson and Granger, 2014), and smoking mothers have higher salivary CT and lower sAA compared to nonsmoking mothers (Granger et al., 2007). In fathers of adolescent girls, higher interparental aggression is related to lower father sAA (Gordis, Margolin, Spies, Susman, and Granger, 2010). Overall, it appears that sAA may be a useful marker of the SAM arm of the stress response, but much further clarifications are required to integrate it as a measure of optimal versus high-risk parenting.

Summary As seen, the hormones of parenting in humans function in a comparable way to those supporting parental care in nonhuman mammals and enable the expression of the unique evolution of parental care across human societies. OT, AVP, and PRL appear to ignite the expression of parenting behavior, CT, sAA, and immune biomarkers to manage the stress involve in parenting, and T plays a special role in development of fathering.

Endocrine Fit: Synchrony in Parent and Child’s Hormones Synchrony or attunement between the parent and infant’s physiological and behavioral processes enables mammalian parents to promote sociality and regulate stress in their young. Hormonal concordance or synchrony, the match between parent and child’s hormones, is a central aspect of such biobehavioral attunement and a link between parent and child’s hormonal levels has been observed in most studies reporting on the associations between parent and child’s hormones measured concurrently. Hormonal synchrony is thought to stem from both genetic similarity and shared environment; yet research has tested the degree in such linkage in different contexts and conditions and its association to parent-child relational variables. According to our biobehavioral synchrony model (Feldman, 2012c, 2015b, 2016, 2017), biological synchrony is an important mechanism in the development of mammalian young by which the parent’s mature physiological systems externally regulate the infant’s immature system through the coordination of biological and behavioral processes during moments of social contact. We showed in multiple physiological systems, such as heart rate coupling (Feldman, Magori-Cohen, Galili, Singer, and Louzoun, 2011), brain-to-brain synchrony in neural oscillations (Levy et al., 2017), and endocrine systems (e.g., Feldman et al., 2010; Pratt et al., 2017), that synchrony in biological processes is anchored in behavioral synchrony and increases during moments of concordance in parent and child nonverbal behavior in the gaze, affect, vocal, and touch modalities. Consistent with findings in animal models (Hofer, 1995a), we found that biological synchrony operates in a system-specific manner. Thus, the following reviews the two main parenting-related hormonal systems, oxytocin and cortisol, in healthy and high-risk populations, with more empirical data available for CT compared to OT. The distinction between the two hormones as the main neuroendocrine systems supporting the affiliation and stress/vigilance components of parenting is also expressed in a distinction between the developmental goal of hormonal synchrony in OT and CT. For OT, higher parental sensitivity, synchrony, and reciprocity are associated not only with higher parental OT and higher infant OT, but in a closer match between their OT levels, which promotes more optimal social-emotional outcomes in children. In contrast, tighter cortisol synchrony

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is associated with greater child stress physiology and lower parental sensitivity and dyadic reciprocity (Pratt et al., 2017).

Parent-Child Oxytocin Synchrony Among 4- to 6-month-old infants, we found hormonal synchrony of oxytocin both prior to and following a “play and touch” paradigm, and such endocrine synchrony was observed when social synchrony was high, not when it was low (Feldman et al., 2010). The endocrine fit of parent and child’s OT only in cases of high behavioral synchrony suggests that the fit between parent and child is based on parental behavior, consistent with research in animal models. In three high-risk samples we found OT synchrony between parent and child. In a study comparing preschoolers with autism spectrum disorders (ASD) with typically developing children (TD), OT synchrony in both the ASD and TD group emerged between children with both their mothers and fathers, with no significant differences in the magnitude of OT synchrony between parents or among the two groups (Feldman, Golan, Hirschler-Guttenberg, Ostfeld-Etzion, and ZagoorySharon, 2014), despite the fact that levels of OT differed between ASD and TD preschoolers but not among their mothers or fathers (see below). Following mothers diagnosed with Axis-I depression across the child’s first 6 years of life and their children, we found that depressed mothers had lower salivary OT as did their children. Fathers in families of depressed mothers also had lower OT, and low OT was related to the diminished maternal touch and social gaze in depressed mothers (Apter-Levy, Feldman, Vakart, Ebstein, and Feldman, 2013). Lower baseline OT and attenuated OT response to mother-child interaction was also found in urinary OT in mothers and children whose urinary OT levels were correlated. As stated above, such urinary OT concordance was sensitive to stressful aspects of the interaction and correlated with greater maternal intrusiveness and higher child withdrawal. Of note, among depressed mothers, those who still had higher OT were able to transmit a functional OT system to their child, and their children’s OT differed from that of controls, highlighting the protective role of the mother’s oxytocin functionality (Pratt et al., 2015). Finally, in a group of children exposed to continuous war-related trauma, we found lower OT in war-exposed mothers and OT synchrony between mother and child. Such OT synchrony mediated the effects of war on the child so that high maternal OT led to higher mother-child behavioral synchrony leading to reduced child’s anxiety disorders by age 10 (Ulmer-Yaniv et al., 2017).

Parent-Child Adrenocortical Synchrony The coordination between parent and child cortisol production has been entitled by several terms, including cortisol coregulation, hormonal concordance, stress contagion, or adrenocortical synchrony (Atkinson et al., 2013; Mörelius, Örtenstrand, Theodorsson, and Frostell, 2015; Papp, Pendry, and Adam, 2009; Pratt et al., 2017; Ruttle, Serbin, Stack, Schwartzman, and Shirtcliff, 2011; Saxbe et al., 2014; Stenius et al., 2008). The vast majority of studies examined the coordination of CT following stress paradigms and found that, when stress is elevated in mother or child, both partners increase CT in a coordinated fashion (Atkinson et al., 2013; Hibel, Granger, Blair, and Finegood, 2015; Mörelius, Broström, Westrup, Sarman, and Örtenstrand, 2012; Mörelius, Theodorsson, and Nelson, 2009; Neu, Laudenslager, and Robinson, 2009; Ruttle et al., 2011; Sethre-Hofstad, Stansbury, and Rice, 2002). Much less research has focused on the coordination of diurnal CT patterns between mother and child (Hibel, Trumbell, and Mercado, 2014; LeMoult, Chen, Foland-Ross, Burley, and Gotlib, 2015; Papp et al., 2009; Schreiber et al., 2006; Stenius et al., 2008; Williams et al., 2013), a distinct aspect of HPA axis functioning that is often uncorrelated with CT reactivity to momentary stressors (Edwards,

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Clow, Evans, and Hucklebridge, 2001). Even fewer measured parent-child linkages between hair cortisol concentrations in mother and child have been examined, yet another dimension of HPA reactivity, typically unrelated to salivary response to stress (Halevi et al., 2017). Synchrony of diurnal CT within the family is related to the amount of shared experience (Mörelius et al., 2012, 2015; Schreiber et al., 2006; Stenius et al., 2008). For instance, preterm infants placed in family care and exposed to maternal-infant skin-to-skin contact exhibit cortisol concordance, whereas no correlations between maternal and infant CT was found among infants placed in standard incubator care (Mörelius et al., 2012, 2015). Six-month-old infants show greater diurnal adrenocortical synchrony with their mothers as compared to their fathers (Stenius et al., 2008). Among preschool-aged children mother-child morning CT levels show linkage only on nonwork days (Hibel et al., 2014); and among adolescents, shared environment is a better predictor of afternoon CT linkage than genetic factors (Schreiber et al., 2006). Synchrony in diurnal CT was found between mothers and children, above and beyond time of measurement. Mother-child reciprocity is related to lower adrenocortical synchrony, whereas father-child tension is marginally predictive of greater adrenocortical synchrony. Higher child diurnal CT production predicts a stronger linkage between maternal and child diurnal CT, suggesting that greater physiological stress may render children more susceptible to the effects of maternal stress physiology. Maternal depression, although related to attenuated child diurnal CT decline, does not affect adrenocortical synchrony. Adrenocortical synchrony may tap a unique aspect of HPA axis functioning, potentially linked with the cross-generation transfer of stress physiology. Results highlight mothering and fathering family subsystems as moderators of adrenocortical synchrony and point to the role of parent-child relational stress in shaping diurnal CT linkage. Compared to a healthy control group, synchrony in diurnal CT was found between depressed mothers and children, and the degree of mother-child reciprocity was related to lower adrenocortical synchrony. When children’s CT production during the day was higher, there was also a tighter synchrony between maternal and child CT, suggesting that greater physiological stress may render children more susceptible to the effects of maternal stress physiology. Maternal depression, although related to attenuated child diurnal CT decline, did not affect adrenocortical synchrony. These findings highlight the role of parent-child reciprocity in shaping diurnal CT linkage (Pratt et al., 2017). In a group of preschoolers with ASD compared to TD children, we found CT synchrony between children and both their mothers and their fathers at the three measurement points following the SF paradigm (Ostfeld-Etzion, Golan, Hirschler-Guttenberg, Zagoory-Sharon, and Feldman, 2015). Furthermore, father-child cortisol linkage is stronger in dyads that show less reciprocity, when fathers were less sensitive and when children showed less self-regulation. Consistent with the prior findings, mother-child linkage is stronger in dyads that show less reciprocity and lower maternal sensitivity, demonstrating that higher CT linkage is observed in less functional dyads (Saxbe et al., 2017). Finally, in the war-exposed group, early childhood adrenocortical synchrony is present in maternal and child CT levels at both baseline and reactivity to stressors in early childhood (Feldman, Vengrober, Eidelman-Rothman, and Zagoory-Sharon, 2013). In late childhood (9–11) years, adrenocortical synchrony appears in both salivary cortisol and hair cortisol concentrations, and mothers’ reduced CT in the face of chronic trauma initiates a cascade of biobehavioral synchrony, linking to lower child CT, greater behavioral synchrony, and higher child social engagement, which, in turn, decreased child externalizing and internalizing symptoms (Halevi et al., 2017). Overall, adrenocortical synchrony is thought to be a mechanism by which, beginning in utero, mothers signal to the developing fetus the amount of danger the environment will likely contain. Studies in rodents indicate that the mother’s species-typical behavior carries a unique effect on consolidation of the pup’s HPA reactivity (Gubernick and Alberts, 1983; Rosenberg, Denenberg, and Zarrow, 1970) and that mothers with lower corticosterone display more maternal behavior and their infants show lower HPA axis reactivity in adulthood (Francis and Meaney, 1999; Dong Liu et al., 234

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1997). Cross-fostering studies show that maternal behavior has epigenetic effects on pup neural and behavioral responses to stress and the effects of maternal behavior exceed those of genetic dispositions (Champagne and Meaney, 2001; Kundakovic and Champagne, 2015). These findings provide mechanistic evidence for the concordance between maternal and child HPA axis functioning and suggest that variability in maternal caregiving may play a role in shaping the infant’s cortisol production and degree of their adrenocortical synchrony (Macrì, Zoratto, and Laviola, 2011).

Parents’ Hormones and the Parental Brain Hormonal Correlates of Parent Brain Activations Research in rodents has shown that hormones of pregnancy prepare brain structures which are sensitized by childbirth and form the “mammalian caregiving network”, including the amygdala, hypothalamus (particularly the MPOA), and the dopamine-rich subcortical ventral tegmental area (VTA) (for review; Numan and Stolzenberg, 2009; Numan and Young, 2016). Imaging studies of the human parental brain, exposing parents to auditory, visual, or multimodal stimuli of their infants, have revealed that the same network activates, in addition to other cortical networks implicated in empathy, interoception, embodied simulation, mentalizing, and emotion regulation to form the “global human caregiving network” (for Review, Feldman, 2015b; Swain and Ho, 2017). Work on the parental brain points to associations between parent’s brain activations and parents’ hormones. Regarding maternal brain-hormone relations, mothers’ plasma OT levels correlate with two nodes of the subcortical mammalian network; amygdala, mediating maternal vigilance, and Nucleus accumbens, linked with the subcortical dopamine reward system (Atzil et al., 2011). Salivary OT in mothers relates to maternal dorsal anterior cingulate cortex (dACC), a component of the empathy-embodied simulation network (Abraham et al., 2014), and to the hypothalamus and ventral tegmental area of the subcortical mammalian network (Strathearn et al., 2009). Finally, mothers showing less CT reactivity have higher brain activation to their infant cry in the PAG, insula, ACC, and OFC, areas implicated in interoception (perception of bodily milieu) and empathy (Laurent, Stevens, and Ablow, 2011). Fathers’ OT is associated with activations in the superior temporal sulcus, a key node of the social brain integrating mirror and mentalizing properties (Abraham et al., 2014). Fathers’ amygdala activity correlates with fathers’ plasma AVP levels (Atzil et al., 2012). Finally, fathers’ testosterone, known to decrease in men at the transition to fatherhood (Gettler, McDade, Feranil, et al., 2011), correlates with lower VTA activation and higher left caudate activation (Kuo, Carp, Light, and Grewen, 2012; Mascaro, Hackett, and Rilling, 2013).

Long-Term Prediction Of Parental Brain and Hormones for Children’s Social Development In several studies, we measured parental neural and hormonal response in infancy in relation to child outcomes across the first years of life. Among primary-caregiving mothers and fathers, we found that the coherence of the parent’s embodied simulation network, integrating structures implicating in mirror and empathy functions, and parental OT predicted children’s OT in the preschool stage as well as their capacity to use advanced strategies for regulating negative emotions (Abraham, Hendler, Zagoory-Sharon, and Feldman, 2016). Another study assessed parent brain response to coparental stimuli—stimuli depicting the partner as parent, in relation to observed coparental behavior, hormones, and child outcomes. Coparental stimuli activated the caudate, a critical node in supporting motivational goal-directed social behavior. Caudate-ventromedial prefrontal cortex (vmPFC) vmPFC connectivity, linking caudate with the 235

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prefrontal area implicated in intersubjectivity, mentalization, and affect sharing, is associated with collaborative coparenting and the link between caudate-vmPFC connectivity and reduced child behavior problem at 6 years was mediated by the parent’s OT. Caudate connectivity with the dACC, which has been linked with pain perception, envy, and vigilant monitoring of social and aggressive response, predicts undermining coparenting across time and is linked with AVP (Abraham, Gilam, et al., 2017). Greater functional connectivity between the two empathy networks in the parental brain, the embodied simulation and mentalizing networks, predicts lower child CT reactivity and better emotion regulation at preschool (Abraham, Raz, Zagoory-Sharon, and Feldman, 2018).

Parental Hormones in High-Risk Conditions A comprehensive review of parental hormones in high-risk populations is beyond the scope of a single chapter. The following reviews studies on OT and CT in high-risk populations, focusing mainly on two systems—OT and the affiliative system and CT and indices of the stress response.

Oxytocin and Affiliative Biomarkers Markers Postpartum Depression Several studies have addressed OT functionality in mothers suffering from depression, with few studies addressing mothers with clinically diagnosed Axis-I depression, not just self-reported depressive symptoms. Lower OT during pregnancy and the postpartum goes with greater depressive symptomatology in the neonatal period and less maternal behavior (Feldman et al., 2007). Similar findings were reported by Skrundz, Bolten, Nast, Hellhammer, and Meinlschmidt (2011), who showed that higher depressive symptoms during pregnancy predict lower plasma OT in the postpartum. A longitudinal study followed a community cohort of depressed mothers and their families from birth across the first decade of life. At 6 years, depressed mothers, their husbands, and their children had lower salivary OT levels and greater prevalence of the more evolutionary-recent protective A allele on the OXTR. Lower OT was linked with reduced maternal touch and sensitive parenting (Apter-Levy et al., 2013). Measuring OT in urine in mother and child showed that in both depressed mothers and their children there was lower baseline OT and lower OT response to mother-child interactions. Such reduced urinary OT was related to higher maternal intrusiveness and child withdrawal (Pratt et al., 2015). At 10 years, depressed mothers and children as a group no longer had lower salivary OT, but child OT mediated links between maternal depression and child externalizing and internalizing symptoms as well as child lower empathy as measured by two home-based paradigms (Priel et al., 2018). Administration of OT to postnatally depressed mothers did not increase the level of sensitive parenting (Mah, van IJzendoorn, Smith, and Bakermans-Kranenburg, 2013) nor improve depressive symptoms, but increased their protective behavior to infants in the presence of an intrusive stranger (Mah, Bakermans-Kranenburg, van IJzendoorn, and Smith, 2015). With regards to other hormones of the affiliation system, plasma prolactin levels are significantly lower in depressed mothers who were breastfeeding (Harris et al., 1989). Similarly, depressed mothers show lower serum prolactin levels (Groer and Morgan, 2007). To date, no study has tested maternal AVP in the context of depression.

Stress and Trauma Following a cohort of children exposed to repeated wartime trauma and their mothers from early childhood to adolescence, we found that by 9–11 years war-exposed mothers had lower OT, but children as a group did not have lower OT, only those with PTSD. These mothers also had much 236

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higher prevalence of psychiatric disorders, particularly anxiety disorders, PTSD, and depression, their children had higher levels of anxiety symptoms as well as greater prevalence of psychiatric diagnosis. War-exposed mothers also exhibited lower sensitivity and empathy, and their children displayed less social engagement, which was related to lower maternal OT (Ulmer-Yaniv et al., 2017). Children with ASD exhibit lower baseline OT levels, which are momentary normalized during parent-child contact (Feldman et al., 2014). There is evidence that OT increases during skin-to-skin contact between parents and premature infants (Cong et al., 2015), findings which are consistent with the links between maternal proximity and licking-and-grooming with the oxytocin system in animal models.

Cortisol and Stress Biomarkers Within the family of stress-related biomarkers, numerous studies assess diurnal or reactive cortisol as well as other stress biomarkers in relation to high-risk parenting. Most studies on CT and high-risk parenting address the effects of maternal stress, trauma, depression, or premature birth on the infant’s CT, but few studies also measure maternal hormones. Importantly, there are studies following children from birth to adolescence demonstrating that maternal postpartum depression or perinatal stress alter various aspects of children’s HPA axis functioning including baseline levels, diurnal patterns, and variability (e.g., Halligan, Herbert, Goodyer, and Murray, 2007).

Postpartum Depression During pregnancy and 3 months postpartum, higher depressive symptoms are associated with lower cortisol awakening response and flatter diurnal patterns (Scheyer and Urizar, 2016). In one study, at 8 weeks postpartum, breastfeeding mothers underwent a social stressor while breastfeeding. Among depressed mothers, the surge of OT during nursing was reduced and CT levels were higher, suggesting that depression attenuates the anxiolytic effects of breastfeeding on the maternal stress response (Cox et al., 2015). Mothers with a history of major depression combined with child abuse showed steeper CT decline and their infants had lower baseline CT, and more maternal comorbid conditions on top of the depression, such as abuse history or PTSD, augmented the disruptions to HPA functioning (Brand et al., 2010). At 4–6 weeks postpartum, depressed mothers show downregulated HPA functioning, expressed as lower salivary CT (Groer and Morgan, 2007). In contrast, both clinically depressed and clinically anxious mothers at 9 months have higher CT, augmented CT response to stress, and slower CT recovery, and these alterations in CT production were associated with their diminished sensitivity and lower infant social engagement (Feldman et al., 2009). Following the cohort of depressed mothers and their children from birth to 10 years, we found that at 6 years, mothers and children did not have altered cortisol levels—both diurnal and reactive, but had diminished CT variability in daily patterns and in response to stress (Apter-Levi et al., 2016; Pratt et al., 2017). Similar findings emerged at 10 years of age (Priel et al., 2018), with less flexible CT patterns (lower AUCi index) at both ages associated with less optimal mothering, including maternal intrusiveness and diminished sensitivity, and greater child social withdrawal.

Trauma Mothers with a history of early trauma show less positive affect and flatter cortisol patterns during a home visit at 6 months ( Juul et al., 2016). In a longitudinal study of children exposed to war-related trauma, we found in early childhood that, compared to nonexposed controls, children exposed to trauma since birth had reduced CT variability in response to stress. However, exposed children with PTSD had low and flat CT patterns, suggesting a “shut down” response, but exposed children who 237

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were more resilient had elevated nonflexible levels, indicating high arousal of the system. These differential patterns were related to differences in maternal depression, anxiety, and PTSD symptoms, which were higher in mothers of PTSD children, and greater proximity-seeking behavior in the more resilient exposed child group. Mothers and children also manifest altered patterns of salivary alpha amylase, and for both CT and sAA there were close links between maternal and child’s hormonal levels (Feldman, Vengrober, et al., 2013). These findings—which differentiate trauma survivors or trauma-exposed individuals with and without PTSD—are consistent across several samples and various traumas, such as survivors of the 9/11 attack, the Holocaust, and abuse (Yehuda and Bierer, 2007). At 10 years of age, we measured both hair cortisol and salivary CT response from mothers and children in the same sample. Mothers who lived in a war zone for over a decade had higher hair CT, indicating greater chronic stress, as well as greater salivary CT production during a home visit. These altered maternal patterns impacted the child’s pattern via mechanisms of cortisol linkage, charting a pathway from trauma exposure to higher psychopathology in children (Halevi et al., 2017).

Autism Spectrum Disorders Mothering children with ASD involves high levels of stress, yet few studies have assessed maternal CT in the context of ASD, and even fewer compared CT levels with observed parenting. Mothers and fathers of children with ASD have lower morning cortisol levels, indicating effects of the increased stress on daily stress response (Foody, James, and Leader, 2015). Similarly, 89% of mothers of ASD children display a blunted diurnal CT response, indicating decreased flexibility of the system (Dykens and Lambert, 2013), and another study reported lower CT production throughout the day in mothers of adolescents with ASD (Seltzer et al., 2010). We assessed CT production in 3- to 6-year-old children during a home visit with mother and a parallel home visit with father, where they faced the same experimental stress manipulations (emotion regulation tasks and “still face”). We found no differences between the CT response of mothers and fathers to children with ASD as compared to control parents; however, children with ASD showed blunted CT responses during interaction with mothers, but typical responses during the visit with father. We interpreted the findings in terms of fathers’ pushing children to act more in age-appropriate ways and mothers providing social buffering to children’s stress response in a similar manner to mammalian neonates (Ostfeld-Etzion et al., 2015).

Prematurity Kangaroo care (KC), or skin-to-skin contact, is an intervention aimed to reduce maternal-newborn separation and enhance contact among infants born preterm. Skin-to-skin contact decreases maternal CT following premature birth ( Janevski, Vujičić, and Đukić, 2016). Another study showed reduction of infant CT in a group receiving kangaroo care and linkage between maternal and infant CT at 4 months only in the KC group (Mörelius et al., 2015). Reduced CT levels across the first month following birth were also observed in a full-term sample (Bigelow, Power, MacLellan-Peters, Alex, and McDonald, 2012). In our study of kangaroo care and its long-term impact, by 10 years of age children who received kangaroo care as neonates had attenuated CT responses to social stressors (the TSST-C) and their mothers similarly had lower CT production (Feldman, Rosenthal, and Eidelman, 2014). Hormones of parenting provide biomarkers for stressed or high-risk parenting, hormonal levels are associated with the parent psychological state, history, psychiatric condition, and observed behavior, and hormones demonstrate the utility of using neuroendocrine measures to expand our understanding of at-risk parenting.

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Conclusions Individual variations in hormones play a key role in the development of parenting and are meaningfully associated with variations in maternal and paternal behavior. There is much we do not know which requires future research. First, there are currently no normed curves for hormones across pregnancy and the first year following childbirth. With the growing incorporation of hormones into parenting research, there is a critical need for large-scale studies that can define normative curves across multiple cultures for future research. Second, changing role of fathers and the growing involvement of fathers in childcare prompts much research to understand the neuroendocrinological basis of fatherhood. Third, much research is needed to compare hormonal profiles across a variety of high-risk conditions and to tease apart single from multiple risk, for instance maternal depression in the context of low-risk environment, from maternal depression occurring in the context of poverty, premature birth, or child abuse. Finally, much more research and theory-building are needed to test the hormones of parenting within a global bio-psycho-social theory of parenting that investigates endocrine systems from a comparative perspective and across levels of analysis, incorporating studies of the cellular, genetic, and neural levels with behavioral and representational levels, into a theoretical frame that can define more precisely how hormones of parenting contribute to the successful rearing of human children.

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7 NEUROBIOLOGY OF HUMAN PARENTING Eloise A. Stark, Alan Stein, Katherine S. Young, Christine E. Parsons, and Morten L. Kringelbach

Introduction Human infants need prolonged, intensive caregiving to survive and thrive. Human infants’ dependency is unlike many other newborn animals that are mobile shortly after birth, allowing them a much larger degree of independence from their parents. Early experiences have a lasting effect on our later cognitive and emotional development (Shonkoff, Boyce, and McEwen, 2009). Parenting our young represents one of our greatest social and practical challenges, helping to strengthen lifelong learning and facilitating our advanced cognitive flexibility (Bornstein et al., 2010; Konner, 2010). The pleasures of social interaction with infants are arguably some of our strongest motivators (Parsons, Young, Murray, Stein, and Kringelbach, 2010). As such the parent-infant relationship reflects a biological necessity, ultimately to ensure the survival of the species (Darwin, 1872). Indeed, the systems motivating parental behavior appear to be largely conserved across mammalian species (Numan and Insel, 2003). Here we review the emerging evidence for the way that underlying human brain systems support the parent-infant relationship. Starting with the earliest elements of the parent-infant relationship, orienting to infant cues, we demonstrate how the human brain is optimized to perceive cues across multiple sensory modalities rapidly and efficiently. This “parental instinct” in response to infant cues appears to be present for nonparents as well as parents, demonstrating how our parental capacities are well substantiated in the brain prior to parenthood. We also show how the expertise gained through parenting experience changes the structural and functional properties of the brain in ways that may optimize future caregiving. An infant possesses a large range of communicative cues prior to becoming verbal. From the cry of a distressed infant, their irresistible smell, to the cuteness of a happy smiling face, infants’ emotional expressions overwhelmingly draw our attention. Responding to infant communicative cues in a prompt and sensitive manner is a key parenting capacity (Ainsworth, Bell, and Stayton, 1974). A large body of behavioral and neuroimaging research across species has identified core brain networks that regulate parenting behavior in mammals (Barrett and Fleming, 2011; Swain, Lorberbaum, Kose, and Strathearn, 2007). However, studying the human parental brain presents a specific challenge, as numerous features are unique to human infancy, one example being the prolonged dependency on parents or caregivers (Konner, 2010). Direct cross-species comparisons are therefore difficult, despite a wealth of knowledge of maternal behavior and neurobiology in other mammals (Fleming, 2006). It is known that the quality of caregiving has a profound impact on child development (Bornstein, 250

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Hahn, and Haynes, 2011; Feldman, 2015; Parsons et al., 2010; Parsons, Young, Rochat, Kringelbach, and Stein, 2012). Furthermore, the sensitivity of caregiver responses to infant cues can have a lasting effect on a child’s cognitive and socioemotional development (Stein et al., 2013; Stein et al., 2014a). We have previously described a behavioral framework to characterize the parent-infant relationship in terms of early interactions (Parsons et al., 2010). As the postnatal period advances, interactions between a parent and infant become increasingly intricate and refined. What begins as a simple orienting to infant cues may culminate in prolonged and complex interactions such as play or conversation. Our behavioral framework covers the first 18 months of an infant’s life, and describes six major components of the parent-infant relationship: (1) orienting system; (2) recognition system; (3) intuitive parenting; (4) attachment relationships; (5) intersubjectivity; and (6) higher socioemotional and cognitive functions. The orienting system is the first interface between caregiver and infant, with early interactions characterized by an immediate propensity for each partner to seek contact with one another. Orienting to one another serves to instigate close proximity, thereby facilitating subsequent interaction. Parents demonstrate a basic attraction to infant cues, which helps secure parental attentiveness, for example, the allure of an infant’s smell, the magnetism of “cute” facial features, and “auditory cuteness” such as infant laughter and babbles (Darwin, 1872; Kringelbach, Stark, Alexander, Bornstein, and Stein, 2016). These multimodal infant cues serve to orient adults to infants rapidly. Infants show a remarkable predisposition to orient to fellow humans. Newborn infants show a readiness to track face-like patterns with their gaze, but not matched nonface forms ( Johnson, Dziurawiec, Ellis, and Morton, 1991) despite having minimal perceptual experience of faces. Newborns also prefer speech compared to nonspeech sounds matched for pitch and intensity (Vouloumanos and Werker, 2004) which helps them to orient to adults within their proximity. A more selective recognition system supersedes the general orienting response. By learning to recognize each other, parents and their infants are able to actively pursue interpersonal contact, and this process therefore happens rapidly following birth. Mothers can accurately recognize their own infant early in the postpartum on the basis of single nonvisual cues, such as smell, cry, or touch (Cismaresco and Montagner, 1990; Kaitz, Lapidot, Bronner, and Eidelman, 1992; Porter, Cernoch, and McLaughlin, 1983; Russell, Mendelson, and Peeke, 1983). Within the first few days and weeks of life, infants demonstrate preference for their mother’s face (Bushnell, 2001), voice (DeCasper and Fifer, 1980), and even breast milk smell (Macfarlane, 1975). It is therefore crucial to view the infant as a dynamic partner in the parent-infant relationship, with a wide array of communicative cues, and growing social perceptual capacities. As part of this developmental trajectory, by about 6 weeks old, infants show a remarkable sensitivity to the qualities of adult communication (Brazelton, Koslowski, and Main, 1974; Papousek and Papousek, 1975). They actively pursue social interaction with caregivers, and react in striking ways if such interactions are not forthcoming (Cohn and Tronick, 1983; Field et al., 1988). Therefore, the reciprocal recognition system functions to ensure prolonged and intricate parent and infant interaction. The third element in our behavioral framework is intuitive parenting. The processes underlying parental orienting and recognition have been conceptualized as instinctive or intuitive, forming a distinct class of social behavior (Papousek, 2000; Papousek and Papousek, 1987). These behaviors include altering speech, establishing eye contact, and mirroring infant expressions. They are argued to occur largely in the absence of conscious intent, and are therefore referred to as “intuitive” (Parsons, Young, Stein, and Kringelbach (2017), for review). We suggest that intuitive behaviors include and follow from orienting and recognition capacities. For instance, adults’ intuitive behavior also drives interpersonal contact between caregivers and infants. For example, by attempting to stay within the middle of the infant’s visual field at an optimal distance of approximately 30 cm (Von Hofsten et al., 2014) and by making direct eye contact with the infant. When eye contact is achieved, the adult may respond with vocalizations of greeting, often 251

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in a manner known as “infant-directed speech” or “motherese”, which entails high pitch and exaggerated intonation, and is preferred by infants to adult-directed speech (Fernald, 1985). Adults may also make exaggerated facial expressions (Papousek and Papousek, 1983). Within days following birth, parents and their infants also unconsciously mirror each other’s emotional expressions (Meltzoff and Moore, 1977; Trevarthen, 1977). These intuitive, preverbal interactions form the foundation of a socioemotional understanding on which complex attachment relationships can be built (Bowlby, 1982; Trevarthen and Aitken, 2001). In this chapter we focus on the initial aspects of the parent-infant relationship: orienting and recognition. Studying the first point of parent-infant interaction allows us to explore how intuitive parenting behaviors emerge and evolve. Understanding these early points of interaction may also inform us about attachment, intersubjectivity, and higher-order caregiving capacities. For example, behavioral sensitivity, generally defined as parental availability and appropriate, prompt, responsiveness to infant cues, has been shown in two meta-analyses to be a key predictor of attachment outcomes (Bakermans-Kranenburg, van IJzendoorn, and Juffer, 2003; De Wolff and van IJzendoorn, 1997), although the “transmission gap” should be noted—the gap between what can and cannot be explained about the determinants of attachment security in infancy (Belsky, 2002; Verhage et al., 2016). Recent and expanding evidence has suggested that the human parental brain is a distributed network with precise temporal involvement of subcortical and cortical regions. Of crucial importance is the orbitofrontal cortex (OFC) in the frontal lobes, which appears to be implicated in different phases of caregiving behavior (Lorberbaum et al., 2002; Parsons, Young, Mohseni, et al., 2013). Given the region’s role as a nexus of reward-related processing (Kringelbach, 2005b; Rakic, 2009; Zald and Rauch, 2006), and the often inherently rewarding nature of the parent-infant relationship, such a key role in the human parental brain is consistent with current understanding of OFC function. As well as delineating the brain regions involved in the human parental brain, we are getting closer to understanding the involvement of different regions over time. A temporal understanding complements our structural understanding, and offers a greater insight into the driving forces within preferential processing of infant cues, as well as allowing us to separate brain processes into fast, instinctive processes, and slower, more deliberative efforts. A comprehensive understanding of the neurobiology of parenting requires us to recognize how parenting may alter the brain, both structurally and functionally and allows us to explore psychiatric disorders where parenting behavior can be disrupted, which in turn raises the risk for behavioral, emotional, and cognitive difficulties in the children. The potential for new neuroscientific methods such as whole-brain computational modeling, offers great potential to explore the human parental brain in more depth than ever before.

Historical Considerations in Understanding the Neurobiology of Parenting Given the relative novelty of methods to explore the neurobiology of the human parental brain, such as functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG), the history of research in this field is relatively sparse. However, several key scientists, such as Charles Darwin, paved the way for our current understanding, and certain cultural and familial factors play an everincreasing role in understanding the neurobiology of human parenting.

Darwin In The Expression of the Emotions in Man and Animals, Darwin (1872) extolled the virtues of studying animals alongside humans for clues to our rich experiences. For Darwin, emotions had an

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evolutionary history that could be traced through cultures and across species. Darwin proposed that observing infants is a good starting point for understanding facial expressions, as infants exhibit many emotions in a “pure” form. In addition, he wrote of the strength of maternal love, and how such strong emotions can lead to instinctive behavior: No emotion is stronger than maternal love; but a mother may feel the deepest love for her helpless infant, and yet not show it by any outward sign; or only by slight caressing movements, with a gentle smile and tender eyes. But let any one intentionally injure her infant, and see what a change! how she starts up with threatening aspect, how her eyes sparkle and her face reddens, how her bosom heaves, nostrils dilate, and heart beats; for anger, and not maternal love, has habitually led to action. (Darwin, 1872) Darwin was also fascinated by the visceral cries of hungry, pained, or discomforted infants. He noted the corresponding facial expression that co-occurs with crying: firmly closed eyes, wrinkled skin around the eyes, forehead contracted into a frown, widely opened mouth with retracted lips. He collected and documented images of crying infants as he believed the photographs best showed the “instantaneous process” of crying. Darwin also wrote about smiling and laughter as examples of early emotional expressions in infants, such as the instinctive peals of laughter that ensue from being tickled. In many ways, Darwin was one of the first scientists to explore infant communicative cues and how they attracted instinctive adult behaviors, paving the way for what we know today about the human parental brain.

Lorenz and Kindchenschema Pioneers of the study of infant cues and behavioral responsivity were Nobel Prize winners and founding fathers of ethology, Konrad Lorenz and Niko Tinbergen. They focused on visual cues, proposing that infantile facial and bodily features, such as chubby cheeks, big round eyes, a small nose and ears, form a “Kindchenschema” or “infant schema” (Lorenz, 1943). They further suggested that the Kindchenschema is a prime example of an “innate releasing mechanism” that naturally attracts adults and motivates the provision of care through instinctual behaviors. The duo provided a larger ethological program, including four goals, to define how we should approach the biological study of behavior. They involved defining the physiology, the survival value, evolution, and development of behavior (Burkhardt, 2014; Tinbergen, 1963). These goals are still at the forefront of ethological research, however there does exist debate about the nature of “instincts” and the concept of “innate releasers” (Hinde, 1966, 1982; Lehrman, 1953). It may be said that infant visual cues promote caregiving, but do not determine it. This early theoretical account provided a lasting legacy in terms of how to conceptualize the impact of infant visual cues on caregiver behavior. Lorenz focused on visual cues, and other researchers focused on cues in the auditory domain. Early accounts of infant vocalizations suggested a range of motivations for promoting caregiving behavior, including terminating an aversive stimulus, empathic responding to reduce another’s distress, or evolutionarily driven responding ensuring the well-being of offspring (Murray, 1985, for overview). Later, Murray proposed a model that considered infant acoustic cues as “motivational entities”, promoting the likelihood of initiating behavioral responses in listeners (Murray, 1979, 1985). The motivational entity model states that the specific acoustic structure of an infant cry alerts the listener rapidly and universally, whereas other factors such as the context of care or cognitive appraisal have an impact on the selection of specific caregiving behavior.

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Bowlby and Attachment Bowlby (1969) proposed attachment theory, which asserts that humans are born with a psychobiological system that motivates them to seek proximity to a significant other (he focused on the mother), with the principal aim of ensuring survival. Attachment theory provides an explanation of how the parent-infant relationship emerges and influences subsequent development. An infant needs a secure relationship with one primary caregiver for the child’s successful social and emotional development, and especially for learning affective regulation. The primary caregiver should provide a secure base from which the child may face the external world, and to which he or she may return to be comforted if distressed or reassured if frightened. Alongside the infant’s propensity to form an attachment, Bowlby also proposed that caregiving is the result of an organized behavioral system. This caregiving system has the goal of promoting proximity and comfort in the event that the child is stressed by internal or external cues. Bowlby’s attachment theory remains a strong influence on current research into parenting, and evidence for the “caregiving system” may be substantiated within the neurobiological networks in the human parental brain.

Cultural Differences Parenting is a complex behavior that varies across cultures (Bornstein, 2012). Cross-cultural differences have not been well addressed in terms of the neurobiology of parenting, but we could assume that orienting, recognition and intuitive parenting capacities remain similar across cultures, while higher socioemotional functions may show greater variation. For example, the alterations that parents make to their speech when directed at infants (“infant-directed speech” or “motherese”; Kuhl, 2004) involve high pitch and exaggerated variations. Such infant-directed speech is common across cultures that differ widely in adult-directed speech (Broesch and Bryant, 2014), which suggests that early engagement with infants may follow very similar neurobiological mechanisms across cultures. Contrastingly, play is an area where cultural differences may abound, as it is fostered through their social relationships (Bornstein, 2007; Sutton-Smith, 1998). It seems that the further we travel from the initial infant-parent contact, the greater the scope for variations in interaction driven by culture.

Theoretical Perspectives on the Neurobiology Underlying Parenting The Pleasure Cycle Interactions with infants can be intrinsically rewarding, and the parent-infant relationship provides many pleasurable moments. Indeed, the typical adult response to an infant is a smile, the most conspicuous of pleasure responses (Hildebrandt and Fitzgerald, 1979). Adaptive pleasures that ensure species survival include food, sex, and social interaction (Kringelbach and Berridge, 2009a). Social interaction, including parent-infant interaction, can be examined within the framework of a complex set of processes, each involving distinguishable neurobiological mechanisms (Kringelbach and Berridge, 2009b; Leknes and Tracey, 2008). The “Pleasure Cycle” includes at least three psychological components, named “wanting”, “liking”, and “learning” (Figure 7.1). “Liking” represents the hedonic impact of a reward, whereas “wanting” promotes the approach towards and consumption of the reward, sometimes called incentive motivation. “Learning” involves adapting expectations about rewards and their future consumption. Once reward-related cues are learned, the brain is able to represent predictive associations and cognitions, underpinned by prediction-error monitoring in the orbitofrontal cortex (OFC). Each component has conscious and subconscious subcomponents. In the context of social interaction, the initial “wanting” for a reward (i.e., the inherent pleasure of 254

Figure 7.1 The pleasure cycle and pleasure network. A. The pleasure cycle for social interaction. Fundamental (i.e., rewards associated with behavior necessary for species survival) and higher order pleasures are associated with a cyclical time course. Typically, rewarding experiences go through a phase of expectation or wanting for a reward. This may or may not lead to a phase of consummation or liking of the reward, which may reach a peak of pleasure (e.g., eliciting a laugh from your child). This period of consummation is followed by a satiety or learning phase, during which the individual learns and updates predictions for the reward to guide future behavior. Learning can also take place throughout the cycle. B. The core affect elicited by infant cues such as facial cuteness or laughter is generated by the pleasure network in the human brain (shown here in one hemisphere only) with the nucleus accumbens and ventral pallidum and other main pleasure-coding regions. Clockwise views (from bottom left) are from the top, front, side, and 3D perspective. The connections indicate the tentative functional networks mediating hedonic ‘liking’ reactions and subjective pleasure ratings. C. Schematic diagram of the human “parental brain”—networks of regions typically recruited in response to infant cues.

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interacting with your child) often results in behavior to obtain the reward (i.e., holding the infant and initiating conversation), which is subsequently “liked” and learned from.

Fast and Slow Thinking In Thinking Fast and Slow, Kahneman (2011) suggested that the human mind consists of two competing systems. His central hypothesis posits a dichotomy between two modes of thought: System 1 is fast, instinctive and emotional; System 2 is slower, effortful, more deliberative, conscious, and more logical. To illustrate the two, imagine you see a baby pass you in a pram—you may react instinctively by smiling. This is an example of the “fast” system. Our brains are hardwired to respond quickly to certain cues in the environment, and this helps us to survive. Yet there are many situations when our brains take longer to complete tasks—using Kahneman’s “slow” system. For instance, you may be holding a crying infant and not know why he or she is crying. You probably really have to think through the options for why the infant is crying and work out a plan to soothe the infant and address his or her needs—that is your “slow” system which allows you to process more tricky situations. Fast responses are important for survival, and slow responses are a vital aspect of caregiving and its constituent processes. In accord with the concept of fast and slow thinking, Murray’s motivational entity model (Murray, 1979, 1985) has since been broadly substantiated within general neuroscientific and conceptual models of emotional processing, which outline a rapid emotional reaction (“core-affect”), which can be modulated by contextual factors, attentional states, and cognitive appraisal (Barrett, Mesquita, Ochsner, and Gross, 2007). This two-stage model also describes the neural hardware supporting emotional responses, with rapid, imprecise processing recruiting primarily subcortical regions, and slower, more detailed analyses occurring in sensory and higher-order cortical regions (Barrett and Bar, 2009; LeDoux, 2000; Rolls, 2000). The orbitofrontal cortex (OFC) is considered to be a central hub within the dual streams model of emotional processing, providing an interface between the fast and slow processing routes (Barrett and Bar, 2009). Caregiving can also be viewed in a stratified way based on fast or slow systems. While instinctive, rapid processes exist, such as orienting to infant cues and recognition of an infant, there also exists slower caregiving responses, such as prolonged interactions in play.

Classical and Modern Research in the Neurobiology of Parenting The Social Brain and the Parental Brain The human parental brain, by which we mean the neural networks controlling parental behavior and cognitions, must be viewed within the context of the social brain, as the parent-infant relationship provides the template for all social relationships. Social cognition has been considered to be of such fundamental importance to human functioning that some have argued it may even represent the “default mode” of cognition (Schilbach et al., 2006). It is evident that, as an evolutionary necessity, we would require continuous attunement to the social environment to prioritize attention to biologically relevant stimuli, such as a family member, an infant, or a threatening face in a crowd. Some major brain structures involved in social cognition include the superior temporal gyrus and fusiform gyrus, superior colliculus, and primary sensory cortices; premotor cortex, OFC, amygdala, and ventral striatum; the anterior cingulate cortex, as well as prefrontal regions involved in higherlevel processes, such as social reasoning, theory of mind, empathy, and moral cognition (for reviews see Adolphs, 2003; Eslinger, 1998; Fiske and Taylor, 2008; Frith and Frith, 2010; Frith, 2007; Lieberman, 2007; Moll and de Oliveira-Souza, 2007).

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The “parental brain” can be conceptualized as the network of regions that support caregiving behavior in humans. Adult responses to infant vocalizations and visual cues, in association with functional neuroimaging, have defined this network. The parental brain incorporates both responses in nonparents (the so-called parental “instinct”, which transcends the biological relationship between adult and infant) alongside parental responses that develop as a result of experience. Functional magnetic resonance imaging (fMRI) has revealed a network of regions active in response to infant facial and vocal cues, which overlap extensively with the “social brain”. These findings reflect activity in the frontal lobe (anterior cingulate, prefrontal, orbitofrontal, and insular cortices), the temporal lobe (middle temporal gyrus, superior temporal gyrus/sulcus, and inferior temporal gyrus/sulcus), motor areas (motor cortex, premotor cortex, and supplementary motor area), and in subcortical areas (basal ganglia, periaqueductal gray, and amygdala). Temporal regions, such as the middle temporal gyrus and superior temporal gyrus/sulcus, and the amygdala are involved in the initial processing of affect in vocal cues (Belin, Fecteau, and Bedard, 2004; Ethofer et al., 2006; Frühholz, Trost, and Grandjean, 2014; Yovel and Belin, 2013), and occipital and different temporal regions such as the fusiform gyrus, are predominantly recruited for the visual processing of facial expressions (Fusar-Poli, Placentino, Carletti, Landi, and Abbamonte, 2009). In these regions, stimuli may be concurrently represented and processed by frontal regions, such as the OFC (Bar et al., 2006), and latterly processed by frontal, limbic, and motor regions for higher-order processing and to initiate behavioral responses.

Infant Faces The unique and instantly recognizable facial configuration of infants is pleasing and rewarding, and an instinctive reaction of adults on seeing an infant is to smile (Hildebrandt and Fitzgerald, 1978). Such features are often referred to as “cuteness” and are instantly recognizable (Figure 7.2). This facial configuration is believed to attract attention and evoke caregiving in adults. The preference for juvenile facial features appears spontaneously and universally, transcending the biological relationship between an adult and an infant, and also seems to be conserved across multiple species (Sato, Koda, Lemasson, Nagumo, and Masataka, 2012). Adults present a general aesthetic appreciation of the infant face (“liking”), measured by explicit ratings of stimulus attractiveness. Adults also display a greater incentive salience to view infant stimuli (“wanting”) compared to images of adults (Parsons, Young, Kumari, Stein, and Kringelbach, 2011). This hedonic stratification is important to consider when assessing the responsivity to infant cues, as it brings together the different elements of the parental orienting response (such as affect and behavior). The attentional magnetism of the infant schema and “cute” infant attributes has become a mainstay of Japanese popular culture, known as kawaii. In this context, neoteny, the process of giving human or nonhuman stimuli childlike, juvenile features, has been used to alter toys, cartoon characters, entertainment, and fashion. The popular cartoon character Mickey Mouse has been demonstrated to have become “cuter” and more childlike during the 20th century in parallel with his rise in popularity (Gould, 1979). Items with “cute” or “kawaii” attributes have similarly been shown to afford an advantage on tasks involving focused attention for completion (Nittono, Fukushima, Yano, and Moriya, 2012), led by heightened approach motivation and systematic processing. Infantile characteristics in “baby-faced” men also preferentially activate reward systems in the human brain, and induce positive affect in viewers (Zebrowitz, Luevano, Bronstad, and Aharon, 2009). The effects of baby-faced adults upon brain activity and mood point to the capacity of the baby schema to guide attention, motivation, and behavior at early stages of visual and affective processing (Kringelbach et al., 2008). Neural evidence of responsivity to infant faces and visual cues has provided an important level of explanation for the field, as visual cues form an important aspect of parent-infant contact. Greater

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Figure 7.2 Behavioural effects of cuteness. A. The proportions of the features of the face can be used to provide objective measurements of cuteness in infants and adults (Glocker, Langleben, Ruparel, Loughead, Gur, et al., 2009). B. Adult men and women (who are not yet parents) differ in their liking ratings, but not in the amount of effort they expend on viewing natural images of infants with varying levels of objective cuteness (Parsons, Young, Kumari, Stein, and Kringelbach, 2011). C. Artificially changing the proportions of the faces of humans, dogs, and cats can change their perceived cuteness, although questions have been raised over the ecological validity of such non-ecological image manipulations. D. Five-year-old children find the young significantly cuter than the adults of different species (Borgi, CogliatiDezza, Brelsford, Meints, and Cirulli, 2014). Source: Panels C and D are reproduced from Borgi et al. (2014).

activity within the OFC in response to infant faces compared to adult faces has been recognized across multiple neuroimaging methods, including: electroencephalography (EEG; Proverbio, Riva, Zani, and Martin, 2011), magnetoencephalography (MEG; Kringelbach et al., 2008; Parsons, Young, Mohseni, et al., 2013), and functional magnetic resonance imaging (fMRI; Baeken et al., 2009; Glocker, Langleben, Ruparel, Loughead, Valdez, et al., 2009; Leibenluft, Gobbini, Harrison, and Haxby, 2004; Montoya et al., 2012; Nitschke et al., 2004; Ranote et al., 2004; Strathearn, Li, Fonagy, and Montague, 2008). In addition, fMRI studies of the human parental brain have found differential activity in response to infant facial expressions in the temporal lobe, frontal lobe, motor cortex, and subcortical regions (Figure 7.3, and Table 7.1 for studies). A strict test of the power of the infant facial configuration to elicit specialized processing in adults comes from circumstances where the infant face is naturally altered. It is also possible to measure 258

Figure 7.3 Infant cues elicit fast responses in the human brain. A. Infant faces are examples of cute stimuli that have been shown to elicit fast brain responses (~130ms) in the orbitofrontal cortex (OFC), at the same time as responses in the fusiform face region (Kringelbach et al., 2008). B. Artificially manipulating the cuteness of infant faces has been shown to correlate with changes in the BOLD signal in the nucleus accumbens, part of the pleasure system (Glocker, Langleben, Ruparel, Loughead, Valdez, et al., 2009). C. Very fast neural responses (~50ms) are found in the human brainstem to both positive and negative infant vocalisations (babbling, laughter and crying) (Parsons et al., 2013). D. Similar to the fast brain response to cute visual stimuli, infant crying elicits activity in the OFC (~140ms) at the same time as activity in primary sensory cortices (Young et al., 2016). Source: Panel (A) is reproduced from Kringelbach et al. (2008); panel (B) is adapted from Glocker, Langleben, Ruparel, Loughead, Valdez, et al. (2009); panel (C) is adapted from Parsons et al. (2013); and panel (D) is adapted from Young et al. (2016).

Table 7.1 Summary of findings from fMRI studies of the “parental brain”, highlighting neural regions reactive to infant vocal and facial expressions (MTG: middle temporal gyrus; STS/G: superior temporal sulcus/gyrus; FFG: fusiform gyrus; OFC: orbitofrontal cortex; PFC: prefrontal cortex; PAG: periaqueductal gray; VTA: ventral tegmental area; SMA: supplementary motor area)

Temporal lobe MTG

STS/G

FFG

Frontal lobe OFC

Infant vocal expressions

Infant facial expressions

Montoya et al. (2012) Kim, Leckman, Mayes, Newman et al. (2010) Lorberbaum et al. (2002) Riem et al. (2011) Montoya et al. (2012) Kim, Leckman, Mayes, Newman, et al. (2010) Lorberbaum et al. (2002) Riem et al. (2011) Mascaro, Hackett, Gouzoules, Lori, and Rilling (2014) Bos, Hermans, Montoya, Ramsey, and van Honk (2010) None

Montoya et al. (2012) Ranote et al. (2004) Barrett et al. (2012) Strathearn et al. (2008) Montoya et al. (2012) Ranote et al. (2004) Barrett et al. (2012) Strathearn et al. (2008) Noriuchi et al. (2008) Bartels and Zeki (2004) Strathearn et al. (2008) Bartels and Zeki (2004) Caria et al. (2012) Nitschke et al. (2004)

Mascaro et al. (2014) Laurent and Ablow (2012)

Montoya et al. (2012) Ranote et al. (2004) Strathearn et al. (2008) Noriuchi et al. (2008) Bartels and Zeki (2004) Nitschke et al. (2004) Glocker, Langleben, Ruparel, Loughead, Gur, et al. (2009) Leibenluft et al. (2004) Baeken et al. (2009) Barrett et al. (2012) Strathearn et al. (2008) Noriuchi et al. (2008) Bartels and Zeki (2004) Caria et al. (2012) Ranote et al. (2004) Barrett et al. (2012) Strathearn et al. (2008) Noriuchi et al. (2008) Bartels and Zeki (2004) Barrett et al. (2012) Noriuchi et al. (2008) Bartels and Zeki (2004) Caria et al. (2012)

Anterior cingulate

Lorberbaum et al. (2002) Laurent and Ablow (2012)

PFC

Kim, Leckman, Mayes, Newman, et al. (2010) Lorberbaum et al. (2002) Mascaro et al. (2014) Laurent and Ablow (2012)

Insula

Mascaro et al. (2014) Kim, Leckman, Mayes, Newman, et al. (2010) Laurent and Ablow (2012)

Subcortical Basal ganglia

Lorberbaum et al. (2002) Mascaro et al. (2014) Montoya et al. (2012) Laurent and Ablow (2012)

Montoya et al. (2012) Barrett et al. (2012) Strathearn et al. (2008) Noriuchi et al. (2008) Bartels and Zeki (2004)

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Infant vocal expressions

Infant facial expressions

PAG/VTA

Laurent and Ablow (2012)

Amygdala

Riem et al. (2011) Seifritz et al. (2003)

Thalamus/ hypothalamus

Lorberbaum et al. (2002)

Strathearn et al. (2008) Noriuchi et al. (2008) Bartels and Zeki (2004) Ranote et al. (2004) Barrett et al. (2012) Strathearn et al. (2008) Strathearn and Kim (2013) Bartels and Zeki (2004) Leibenluft et al. (2004) Barrett et al. (2012) Strathearn et al. (2008) Noriuchi et al. (2008) Caria et al. (2012)

Motor Motor cortex Premotor/SMA

Kim, Leckman, Mayes, Newman et al. (2010) Montoya et al. (2012)

Strathearn et al. (2008) Caria et al. (2012)

the potential impact on parent-infant interaction in such circumstances. Perhaps the most convincing evidence for the significance of infant facial features in eliciting parental care has come from instances of facial anomaly in the case of cleft lip and palate. Cleft lip is the most common congenital condition affecting the face and cranial bones, with an incidence of 1 in 700 live births in the United Kingdom (Goodacre and Swan, 2008). It affects the nasal and mouth regions and can therefore be conceived of as a specific, local change to the typical infant schema. It is also important to note that cleft lip does not typically occur with concurrent developmental difficulties—the sole difference in these children is their facial configuration. Cleft lip in infancy has been the most studied facial abnormality with reference to adult motivational processing, and adults will typically rate infants with cleft lip as less “cute” than healthy infants, and will work less hard to view them (Parsons, Young, Parsons, et al., 2011). Nonparents have also been shown to react negatively to global changes to the infant face, in cases of fetal alcohol syndrome and prematurity (Frodi, Lamb, Leavitt, and Donovan, 1978; Waller, Volk, and Quinsey, 2004). The presence of a cleft lip disrupts typical gaze patterns, with fixations to the mouth region predominating (Rayson et al., 2016). Mothers of infants with cleft lip look at their infants for less time, and demonstrate less positive and sensitive interaction compared to mothers of healthy infants (Murray et al., 2008). These findings together show that changes to the infant facial configuration appear to compromise adult responsivity.

Infant Crying Early infant communication is primarily composed of facial and vocal cues. The newborn infant cries reflexively and communicatively, acting as a “biological siren” to alert the caregiver to the infant’s presence and needs. MacLean (1990) drew attention to the importance of the universal mammalian caregiving cue of infant vocalizations as an important indicator of how mothers and fathers respond to their infant. Infant cries portray a “falling” or “rising-falling” melody, with high and dynamic pitch (ranging between 250 and 750 Hz; Golub and Corwin, 1985). Single bursts last for between 1 and 3 seconds. Initially, infant cries are largely reflexive, indicating hunger, tiredness, pain, or separation from caregivers. Their cries may also take on more variation in acoustics over 261

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time. For instance, other vocalizations, such as babbling and laughter, emerge postnatally, as infants gain greater control of the vocal tract (Soltis, 2004). Infant cries also appear to be “graded signals” in which changes in acoustic features, such as pitch, indicate varying levels of distress (Soltis, 2004), although limited success has been found in attempts to divide infant cries into acoustically distinct categories, such as pain or hunger. A higher-pitched cry is frequently perceived as more distressed and more arousing by adult listeners, both parents and nonparents (Parsons et al., 2014; Porter, Miller, and Marshall, 1986; Young, Parsons, Stein, and Kringelbach, 2012; Zeskind and Marshall, 1988). The ability to respond to infant vocalizations, universal in mammalian species, is of fundamental importance to parental responsivity (MacLean, 1990). Hearing a distressed infant’s cry has a noticeable effect on behavior. It elicits autonomic arousal in the listener, as measured by physiological correlates such as heart rate, blood pressure, skin conductance, and handgrip force (Bakermans-Kranenburg, van IJzendoorn, Riem, Tops, and Alink, 2012; Boukydis and Burgess, 1982; Zeskind and Collins, 1987). Furthermore, parents who exhibit greater physiological arousal are more likely to respond rapidly (Del Vecchio, Walter, and O’Leary, 2009), demonstrating a link between the magnitude of physiological response and parental responsivity. These physiological responses appear to ready adults to react behaviorally to infant cries. If such physiological changes are functionally important, in response to hearing the cries of an infant, then they should translate into altered behavioral responsivity. Indeed, hearing infant cries has been shown to disturb normal performance on simple cognitive tasks (Morsbach, McCulloch, and Clark, 1986) and disrupts cognitive control (Dudek, Faress, Bornstein, and Haley, 2016). This evidence of altered behavioral responsivity could reflect the magnetism of infant cries to orient people away from less biologically salient tasks. Another study found that after listening to infant distress cries, compared to adult distress vocalizations or bird sounds, participants showed improvements in fine motor performance (Parsons, Young, Parsons, Stein, and Kringelbach, 2012). Accordingly, infant cries orient us away from distracting tasks, but they may also afford an advantage in subsequent motor movements, which may reflect a behavioral readiness to address the distressed infant (Caria et al., 2012). The ability to respond appropriately to infant cries has also been associated with the ability to respond appropriately to other infant cues (Frodi and Lamb, 1980), suggesting that responsivity is not modality-specific, but could reflect a common mechanism. Infant cries express key affective and physiological information and have been demonstrated to elicit specialized activity in an array of brain regions. As with infant faces, the OFC appears to be a key region involved in responding to infant cries (Young et al., 2016). Regions in the temporal lobe, frontal lobe, motor cortex, and subcortical regions are all also involved in processing infant cries (Table 7.1). It remains unclear how brain regions involved in the response to infant cries are sensitive to differences, such as graded acoustic information. Differential brain activity in response to infant cries must also be viewed alongside neuroendocrine system activity. For example, peripheral levels of oxytocin, the “neurohormone of attachment”, have been found to be higher in mothers who demonstrate secure attachment to their infant, compared to mothers who demonstrate unstable attachment patterns (Strathearn, Fonagy, Amico, and Montague, 2009). Crucially, mothers with higher levels of oxytocin also show correspondingly higher levels of activity in reward-related brain regions (Strathearn et al., 2009). Associating endocrine factors alongside both behavioral differences and brain activity promises to elucidate the functional properties of parenting networks by affording further variables that may moderate the parent-infant relationship.

Laughter Alternatively termed “auditory cuteness” (Kringelbach et al., 2016), laughter is another infant cue that communicates the infant’s affective state and may track other cognitive developments by presenting 262

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a sign of pleasure at cognitive mastery (Addyman and Addyman, 2013). Laughter emerges at around four months after birth (Ambrose, 1963; Darwin, 1872), and probably proceeds from smiling which becomes contingently linked to maternal talk and maternal smile by the second and third months (Lavelli and Fogel, 2002). Smiling and laughter also serve to attract adult attention, eliciting warmth and care (Bowlby, 1969). Infant distress cries have taken precedence when exploring the adult’s neural response to infant vocalizations, yet laughter is powerful and important cue in maintaining caregiver interactions and facilitating attachment. As an example, the incentive salience of infant laughter appears to be elevated by oxytocin administration in nulliparous women (Riem et al., 2012), which is argued to enhance parent-infant bonding. The valence of the infant cue (happy or sad, for example) may also modulate the neural responses (Montoya et al., 2012), suggesting that positive and negative affect in the infant may draw on different neural resources in the adult. The OFC has been implicated in both the detection and evaluation of reward valence, in addition to monitoring ongoing reward values (Kringelbach, 2005a). Particularly where a “punishment” is possible, the lateral portion of the OFC is involved in responding to counteract negative reinforcement. One fMRI study exploring the neural response to infant laughter and infant crying compared parents with nonparents. (Seifritz et al., 2003) found a significant group (parents versus nonparents) and stimulus (laughter versus crying) interaction. Differential neural responses were found in the right amygdala, the middle cingulate cortex, insula, left ventral prefrontal cortex, and the left temporoparietal junction. Parents showed stronger activity in these regions in response to infant crying, whereas nonparents showed stronger activity to infant laughter. In addition, for both parents and nonparents, the infant vocalizations compared to the control stimulus produced differential activity in the Heschl’s gyri and temporal and polar planes of the auditory cortex, representing an early stage of cortical auditory processing. These findings suggest that infant vocalizations evoke early differential cortical processing and also provide evidence for experience-dependent neural plasticity as a direct result of parenthood and exposure to infant cues. Despite this preliminary evidence, infant laughter remains an underused stimulus in studies of adult response to infant cues, and could offer great insight into the human parental brain by revealing how positive affective cues relate to specific caregiving behavior.

Touch Touch represents a further modality in research linking adult responsiveness and infant cues. A large literature explores the effect of parental touch on infant outcomes. Touch appears to have many beneficial outcomes, especially with preterm infants (Smith, 2012). There is evidence that the sense of touch is the first to develop; the fetus even appears able to respond to touch as early as the 21st week of gestation (Marx and Nagy, 2015). Both mothers and fathers can recognize their newborn infants by touch alone (Kaitz et al., 1992; Kaitz, Shiri, Danziger, Hershko, and Eidelman, 1994). Tactile stimulation often seems to be a behavioral response to infant cues from other modalities, for example, mothers across several cultures preferentially respond to their infants’ vocalizing distress by picking up and holding their infant (Bornstein et al., in press). Human parents touch their infants frequently during face-to-face interactions, with infants engaged in touching behaviors roughly 85% of the time (Moszkowski and Stack, 2007) and parental touch can regulate an infant’s physiological and behavioral arousal (Hofer, 1994). The type of touch that parents use appears to be highly adaptive in engaging and stimulating their child. Parents spontaneously give slow moving, gentle touch, which is optimized to activate a specialized system of nerve fibers called “C-tactile afferents” which are purported to underpin the rewarding sensation of touch (Pawling, Cannon, McGlone, and Walker, 2017). Despite the wealth of knowledge linking infant touch and the parent-infant relationship, little is known about the underlying neurobiology that processes such cues. This is likely to be due to 263

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practical difficulties of measuring parental responses to their own infant’s touch during neuroimaging sessions, although it should not be ruled impossible.

Olfactory Cues Olfactory cues also likely drive intuitive parental responsivity to an infant. Whereas auditory and visual cues are frequently distal infant cues, bringing the caregiver into physical contact with the infant, olfactory cues may only be effective once the infant and parent are in close proximity. Mothers demonstrate considerable success with recognizing their newborn infant by olfactory signals. Mothers have been shown to recognize their infants via smell with just 10 minutes prior contact (Kaitz, Good, Rokem, and Eidelman, 1987). Paternal recognition of their newborn infant by olfactory cues, in contrast, has yielded rather inconclusive results. Bader and Phillips (2002) asked fathers to sniff the heads of three newborn infants (all bathed identically) and then attempt to identify their own infant. Contrary to the findings with mothers, the fathers were unable to choose their newborns correctly by smell at a rate significantly greater than chance. This was found for both fathers with low exposure (1–10 minutes) and high exposure to the infant (11–810 minutes), and despite greater exposure to the infant having facilitated visual recognition within the same participant group. These findings suggest that fathers learned visual facial cues rapidly, similar to mothers, but did not rapidly learn olfactory cues related to their infant. There are disappointingly few studies concerning early olfactory recognition by parents and related caregiving behaviors. Weisfeld, Czilli, Phillips, Gall, and Lichtman (2003) explored human kin recognition by olfactory-based mechanisms. They found a very low rate of kin-nonkin confusions, suggesting a possible “family odor cue”, even when controlling for effects of familiarity. Furthermore, mothers were preferentially able to identify their biological children’s odor, but not that of their stepchildren, hinting that environmental similarity and continual association are not sufficient for olfactory recognition. Whether newborns and young infants possess a distinct olfactory cue separable from any “family odor cues” remains to be explored. It might be expected that young infants possess distinct olfactory cues, as studies with rodents suggest that the processing of olfactory cues by the amygdala may mediate avoidance of young pups by nulliparous rat females, leading to fewer maternal behaviors (Numan and Sheehan, 1997) in the same way that aversive responses to foul odors are mediated by amygdala activity (LeDoux, 1996). Therefore, although olfaction is not the dominant sensory modality for human parental care as it is for other mammals, olfactory cues may be important to initiate orienting and recognition, and promote attachment.

The Temporal Dynamics of the Human Parental Brain Studies exploring the neural response to infant cues, including infant faces, crying, laughter, and even touch and smell, have clearly defined a core set of regions that encompass the human parental brain. However, a more detailed exploration of the brain response to infant cues demands that we ascertain the temporal involvement of these regions. Early detection of infant vocalizations in the brainstem. During deep brain stimulation for chronic pain, four adults were exposed to infant vocalizations (a mixture of babbling, cries, and laughter) while electrodes measured activity in the periaqueductal gray (PAG) of the midbrain (Parsons, Young, Joensson, et al., 2013). Local field potentials (LFPs) reveal differences to infant sounds compared to natural control sounds (adult cries and animal distress sounds) as early as 49 ms after the sound onset. Although the spatial resolution of LFPs is not sufficient to conclusively differentiate PAG activity from that of neighboring regions, the PAG has been associated with maternal responsiveness in nonhuman models (Lonstein and Stern, 1997; Miranda-Paiva et al., 2007; Sukikara, Mora-Ortiz, Baldo, Felicio, and Canteras, 2010) and has a role in regulating arousal. Its extensive network of anatomical 264

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connections includes the inferior colliculus (Dujardin and Jürgens, 2005), the amygdala, and frontal lobe regions including the OFC (Cavada, Company, Tejedor, Cruz-Rizzolo, and Reinoso-Suárez, 2000). These connections may allow for rapid propagation of information regarding infant cues through a network of cortical and subcortical regions that support the human parental brain. Quick orienting to the infant may therefore be supported by a state of heightened physiological arousal initiated by the PAG. A listener’s heart rate, respiration rate, and hand grip strength have all been shown to be affected by hearing infant cries, and these peripheral psychophysiological measures may represent the heightened arousal. Early detection of salient infant cues in the brainstem may therefore constitute the first step in the initiation of rapid, effortful, caregiving behavior, and support more detailed processing of cue salience and meaning. Rapid cortical sensitivity: Modulation of the N100. The N100 component, the negative deflection peak around 100 ms after the onset of a stimulus, is an obvious target for clues about early cortical processing of infant cues. There is conflicting evidence regarding whether the N100 is sensitive to the affective content of infant cues. A recent EEG study found that the emotional expression of an infant face (happy, neutral, and distressed) can modulate the N100 in mothers (Peltola et al., 2014). However, other studies have reported no early effects due to valence (Noll, Mayes, and Rutherford, 2012; Proverbio, Brignone, Matarazzo, Del Zotto, and Zani, 2006). A further EEG study of mothers compared processing of one’s own infant’s face to an unfamiliar infant and found greater power in gamma band activity occurring before 100 ms (Esposito, Valenzi, Islam, Mash, and Bornstein, 2015). Regarding valence, the contrasting effects may be due to differing task and attentional demands, whereas directing attention to infant stimuli and their emotional valence may drive earlier processing of such cues (Malak, Crowley, Mayes, and Rutherford, 2015). Selective recognition of one’s own infant and sensitivity to the emotional content of their cues may begin at a very early stage in visual processing. The orbitofrontal cortex: a crucial role in salience detection and beyond. The OFC may be engaged in several phases of parent-infant interactions, starting with early salience detection of infant cues, and progressing to ongoing monitoring of the interaction and its social rewards, and subsequent learning about the infant cues and their corresponding reward value. The OFC occupies the ventral surface of the frontal part of the brain, receiving projections from the magnocellular medial nucleus of the mediodorsal thalamus (Fuster, 1997). It receives inputs from the five sensory modalities: visual, auditory, gustatory, olfactory, and somatosensory, plus visceral sensory information (Carmichael and Price, 1995b). It enjoys direct reciprocal connections with other key brain regions, including the amygdala (Amaral and Price, 1984; Carmichael and Price, 1995a), cingulate cortex (Öngür and Price, 2000; Van Hoesen, Morecraft, and Vogt, 1993), insula/operculum (Mesulam and Mufson, 1982), hypothalamus (Rempel-Clower and Barbas, 1998), hippocampus (Cavada et al., 2000), striatum (Eblen and Graybiel, 1995), periaqueductal gray (Rempel-Clower and Barbas, 1998), and dorsolateral prefrontal cortex (Barbas and Pandya, 1989; Carmichael and Price, 1995b). It is therefore uniquely positioned between subcortical and cortical pathways and comprises a nexus of sensory processing. The OFC has established roles in affective processing, reward, and social cognition, making it a prime target for understanding rewarding interpersonal interactions such as in the parent-infant domain. The OFC is believed to play a key role in coordinating both slow and fast responses to affective stimuli. Of note, the “affective prediction hypothesis” proposes that the OFC is implicated in “tagging” emotionally salient stimuli early in time (Barrett and Bar, 2009). This rapid salience detection is suggested to influence ongoing sensory processing and to prime rapid motor responses. There is growing evidence that the OFC is involved in the early salience detection of infant cues. Kringelbach et al. (2008) found a possible biological basis for the specific relation between an infant’s facial features and an adult’s caregiving response. They used MEG to record neuronal activity while participants viewed images of adult and infant faces. In response to the infant images, there was highly specific brain activity present within 130 ms in the medial orbitofrontal cortex (mOFC), followed by 265

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expected activity in the right fusiform “face area” (FFA) as for the adult faces at around 170 ms. For evidence of this as a marker of “intuitive parenting”, Kringelbach et al. followed the same reasoning as Papousek (2000) who had argued that parental responses of such fast latency could be considered to be instinctive or hardwired. This finding has since been replicated (Parsons, Young, Mohseni et al., 2013), is found in both men and women, and appears to be present in nonparents as well as parents. As previously mentioned, cleft lip represents a natural deviation from the typical infant facial configuration, and thus provides a strict test of the power of the infant face to elicit specific activity in the parental brain. To explore the effects of cleft lip on neural processing, specifically probing the causal relation between infant facial configuration and OFC activity, functional neuroimaging using MEG has been used to compare viewing healthy infants with images of infants with cleft lip (Parsons, Young, Mohseni, et al., 2013). In this study, the previous finding of Kringelbach and colleagues (2008) of significant medial OFC activity in response to healthy infant faces at around 130 ms was replicated. However, when presented with images of infants with a cleft lip, this medial OFC activity was diminished as in the case of adult faces. These findings suggest that early OFC responses are sensitive to the baby schema or typical infant facial configuration. Evidence for salience detection mediated by the OFC in response to infant cues is also forthcoming in other modalities. Young et al. (2016) compared the neural responses of participants listening to infant and adult cry vocalizations. They observed a peak of early activity localized in the OFC at 125–135 ms for infant cries but not adult cries, in accord with previous findings of early OFC activity for visual infant cues. They also reported a second peak of differential activity at a later time point between 190–200 ms in the OFC. Such specific brain activity in the OFC could be characterized as a potential biological basis for the “innate releasing mechanisms” initially posited by Lorenz, and the motivational entity model refined by Murray, promoting, but not necessarily determining caregiving in response to infant faces. The orbitofrontal cortex is a key brain region in the representation of reward, so could plausibly represent the especially high reward value of infant visual cues. This emotional “tagging” of the stimulus may bias further neuronal processing to garner energy and resources for providing care for the infant. Beyond this early salience detection, activity in the OFC has been demonstrated to represent the reward value of stimuli, which is a function likely to be based on more detailed processing (Kringelbach and Rolls, 2003), and crucial for higher-order processing and decision making (Berridge and Kringelbach, 2008). Orienting to infants appears fast, effortless, and spontaneous, but parenting also involves slower process of decision making, such as why the infant could be crying and what the infant needs. When making decisions, the brain must predict and evaluate the reward values of the stimuli involved, and the reward values of various behaviors involved in interacting with each stimulus (Kringelbach, 2005b; Rangel, Camerer, and Montague, 2008). The OFC is a key region in these processes as neuroimaging studies have found that the reward value, expected reward value, and even subjective pleasantness are represented in the OFC (Gottfried, O’Doherty, and Dolan, 2003; Kringelbach, O’Doherty, Rolls, and Andrews, 2003; O’Doherty et al., 2000). The OFC appears to have functional subregions that subserve different aspects of reward-related processing. The medial OFC (mOFC) has been related to monitoring, learning, and memory for reward, and the lateral OFC (lOFC) has been proposed to relate primarily to the evaluation of “punishers”, which can lead to changes in behavior (Kringelbach and Rolls, 2004). A posterior-anterior gradient in the OFC is also present, with more complex or abstract reinforcers (such as monetary gain or loss) being represented more anteriorly, and less complex sensory rewards (such as taste) being represented more posteriorly (O’Doherty, Kringelbach, Rolls, Hornak, and Andrews, 2001; Small, Zatorre, Dagher, Evans, and Jones-Gotman, 2001). Responsive and attentive caregiving is likely to draw on a range of functions mediated by the OFC, as responsivity to infants requires ongoing monitoring, learning, and memory for infant cues. It also involves the ongoing evaluation of these cues to appropriately adapt behavior. Learning about 266

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infant cues via orbitofrontal activity may form the basis of experience-dependent plasticity in the human parental brain. In addition, a region of mid-anterior OFC is believed to track changes in subjective pleasure (Kringelbach et al., 2003), and may therefore provide a neural correlate of the subjective pleasure often inherent in ongoing infant interaction. Within dynamic parent-infant contact, prediction-based learning and choice behavior in uncertain environments are likely to occur. Such processes may allow for optimization of “intuitive” parenting behaviors by learning through prediction-making and subsequent analysis of error. OFC activity in response to infant cues may exemplify how the brain coordinates a seemingly “cognitively impenetrable” orienting response to infants (Fodor, 1983). Detailed sensory processing (N170 and beyond). Following early neural responses, it is presumed that infant cues are exposed to more detailed sensory processing. The N170 is a face-sensitive ERP component that elicits a larger response at occipitotemporal electrodes for human faces compared to nonface objects. Here, there are mixed results for infant-related processing. Some studies have reported no effect of valence in infant facial expressions on N170 responses (Malak et al., 2015; Noll et al., 2012). Contrastingly, another study revealed larger N170 amplitudes to negative compared to positive infant facial expressions during focused attention in both mothers and nonmothers, as well as a main effect of valence on latency of N170 responses (Peltola et al., 2014). For later EEG components, there is greater correspondence between results. These later differences are expected to reflect slower processes, such as detailed sensory processing and cognitive appraisal. Larger N2 responses within the 250–300 ms window were found in response to infant faces, compared to pre-pubertal child faces, which also had greater responses than to adult faces (Proverbio et al., 2011). These effects were subsequently localized to the fusiform gyrus, anterior cingulate cortex, and OFC. Two further studies reported effects of the valence of infant cues on responses between 200 and 300 ms (Peltola et al., 2014; Proverbio et al., 2006). Both intensity and valence of emotional expressions affected the amplitude of the P300 response in one study (between 375 and 600 ms; Proverbio et al., 2006), although another study found no difference in a comparable time window of 300 to 450 ms (Peltola et al., 2014). Last, two studies reported modulation of the late positive potential (LPP; 500–800 ms) by valence in infant cues (Malak et al., 2015; Rodrigo et al., 2011). All of these later effects demonstrate differential processing of infant cues at later time points, possibly reflecting slower appraisal processes. The effects of infant cues on behavior: Evidence for preparatory motor responses? There is preliminary evidence that infant cues may also influence a preparatory motor response in the brain, spurring us into action. The medial portions of the OFC guide autonomic, endocrine, and behavioral responses to an object (Barbas and De Olmos, 1990; Carmichael and Price, 1995b, 1996; Ghashghaei and Barbas, 2002; Ongur, Drevets, and Price, 1998; Rempel-Clower and Barbas, 1998) and coupled with strong reciprocal connections to lateral parietal regions, the OFC is well placed to coordinate preparatory motor responses (Barrett and Bar, 2009). In concordance with the connectivity between the OFC and motor regions, premotor cortex and supplementary motor area activity in response to infant face stimuli, compared to adult face stimuli, has been found in both nonmothers (Caria et al., 2012) and mothers (Strathearn et al., 2008). Similar motor cortex activity has been found in response to auditory infant cues (Kim et al., 2011; Montoya et al., 2012). Using auditory MEG, one study observed differential activity at around 180 ms to infant cries, localized to the motor cortex (Young et al., 2016). A study using transcranial magnetic stimulation demonstrated enhanced motor evoked potentials at 100–200 ms after hearing infant cries, interpreted as reflecting an automatic audiomotor response (note that this effect may be specific to female listeners, a finding which requires further assessment, Messina et al., 2015). These findings could be suggestive of a readiness for communicative behavior with infants as well as for attachment and caregiving. A potential biological mechanism to predispose us to be responsive to our young appears to transcend the adult’s biological relationship to the infant, 267

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as motor responses in nonparents demonstrate (as was Kringelbach et al., 2008). It therefore seems that in both men and women, whether they are parents or not, there is an instinctive neural response to infant visual cues that serves as a “parental instinct” and promotes responsive caregiving behavior. Additional data show specific behavioral responses that may be initiated in response to infant cues. Behavioral data show that “cute” stimuli narrow our attentional focus (Nittono et al., 2012). Sherman, Haidt, and Coan (2009) demonstrated that, after viewing images of cute stimuli, individuals display more careful behavior on a fine motor dexterity task. Viewing cute infant stimuli may change our behavior in predictable ways that predispose us to caregiving. Paying focused attention to what we are doing and being careful are both attributes that would suit responsive caregiving. In response to infant cries, adults have also been shown to score higher on the popular arcade game “Whack-amole” requiring rapid, coordinated and effortful movement (Parsons, Young, Parsons, et al., 2012). These findings all point towards the behavioral readiness of adults in response to infant cues, which could be the result of the neural activity we see in motor regions in response to the same cues. Summary of temporal dynamics within the parental brain. As outlined in Young et al. (2017), this temporal framework explains the proposed timeline of neural activity in response to infant cues in cortical and subcortical regions of the human parental brain. To summarize, specialized processing of infant cues may originate within the periaqueductal gray of the brainstem, a key “survival structure” which may trigger adaptive physiological responses, and also act as a rapid subcortical route to engage broader cortical circuitry. From the PAG, the signal rapidly propagates to sensory cortical regions and the OFC (within 100–150 ms). These early processes are believed to support salience detection and subsequent privileged processing of infant cues. OFC activity may “tag” emotionally salient stimuli, influence ongoing sensory processing, and prime cortical motor reactivity and subsequent behavior. While sensory processing continues, the OFC may become active at later time points to represent the ongoing reward value of infant stimuli as the interaction unfolds. Through these processes, it is

Figure 7.4 The pattern of neural activity over time. Proposed timeline of neural activity in response to infant cues across subcortical and cortical regions of the human parental brain. Evidence of early detection (