Foreword: Gilbert Gottlieb and the Developmental Point of View

Preface and Acknowledgments

Part I Introduction

1 Developmental Systems, Nature-Nurture, and the Role of Genes in Behavior and Development

The Goals of the Handbook

The Plan of this Handbook



2 Normally Occurring Environmental and Behavioral Influences on Gene Activity

Predetermined and Probabilistic Epigenesis

The Central Dogma

The Genome According to Central Dogma

Normally Occurring Environmental Influences on Gene Activity

From Central Dogma of Molecular Biology to Probabilistic Epigenesis

Importance of Behavioral and Neural Activity in Determining Gene Expression, Anatomical Structure, and Physiological Function

Summary and Conclusions




Part II Theoretical Foundations for the Developmental Study of Behavior and Genetics

3 Historical and Philosophical Perspectives on Behavioral Genetics and Developmental Science

Why is Behavioral Genetics so Controversial?

A Brief History of Traditional Behavioral Genetics and of Aspirations for a “Developmental” Behavioral Genetics

Two Conceptions of the Norm of Reaction

Two Conceptions of Gene-Environment Interaction

Two Conceptions of Genes and Gene Action




4 Development and Evolution Revisited

The Grandparent Effect and Epigenetic Inheritance

“Epigenetic” Then and Now

Gilbert Gottlieb’s Legacy

Lamarck’s Theory of Evolution

Darwin and the Neo-Darwinian Synthesis

Evolution, Development, and Heredity

The Genetic Paradigm and Neo-Darwinism

The Revival of Epigenetic Approaches Since Darwin and the Neo-Darwinian Synthesis

Waddington’s Theory of Canalization and Genetic Assimilation

Ho and Saunders’ Epigenetic Theory of Evolution

Rational Taxonomy Based on the Generative Dynamics of Biological Form

Natural Selection and Molecular Evolution

Epigenetic Complexity vs Genetic Diversity, Macroevolution vs Microevolution

The Demise of the Genetic Paradigm and Mechanistic Biology

The Vanishing Gene

Subverting and Rewriting the Genetic Text

Adaptive Mutations, When to Mutate or Not to Mutate

Heredity and Evolution in the Light of the New Genetics and Epigenetics

Genetic and Epigenetic Paradigms in the Study of Behavior

Maternal “Instinct” Deconstructed

Epigenetics of Maternal Behavior

The Epigenetic Approach and the Continuity between Development and Evolution



5 Probabilistic Epigenesis and Modern Behavioral and Neural Genetics

Gottlieb’s Influence

Developmental System Theory in the Light of Modern Genetics

The Future of Additivity Theory in Psychology


6 The Roles of Environment, Experience, and Learning in Behavioral Development

Organism-Environment Transaction in Behavioral Development

Epigenetics and Ecological Influences in Developmental Biology

The Concept of Environment

The Umwelt in Behavioral Development

The Role of Experience in Development

Learning and Behavioral Development

Environment, Experience, Learning and the Questions about Behavioral Development


7 Contemporary Ideas in Physics and Biology in Gottlieb’s Psychology

Emergence, Self-Organization, and Hierarchy



Nonlinear Dynamic Complex Systems and the Role of Genes in Behavioral Development

The Conceptual Foundations of Gene Theory

A Developmental Systems Perspective on the Role of Genes in Development

The Impasse between Genocentric and Developmental Systems Perspectives

Advances in Nonlinear Dynamic Systems Theory and their Relation to the Role of Biology in Behavioral Development

Gilbert Gottlieb, Probabilistic Epigenesis and Developmental Systems Theory


Part III Empirical Studies of Behavioral Development and Genetics

8 Behavioral Development during the Mother-Young Interaction in Placental Mammals


Mother-Young Interactions during the Suckling Period

Analysis of Suckling Development

The Mother as an Orientation Center for the Young

Huddling and Home Site Orientation

Play Behavior in Young Animals

Behavioral Development in the Evolutionary Context of the Mother-Young Relationship


9 Amnotic Fluid as an Extended Milieu Intérieur


The First Environment: The Behavioral Relevance of Amniotic Fluid

Mechanisms of AF Effects on Behavior

Blurring the Boundaries of the Organism


10 Developmental Effects of Selective Breeding for an Infant Trait


Selective Breeding for “Temperamental” Traits

Temperament in Children: Developmental Stability and Inheritance

Selective Breeding for High and Low Rates of Separation-Induced Infant Vocalizations

Early Differences in Brain Monoamine Systems

Social Behavior in Juvenile High and Low USV Line Rats

Developmental Continuity in Adult Affective Regulation in High and Low USV Lines

Autonomic Nervous System (ANS) Regulation of Heart Rates in the USV Lines

Low USV Line Male–Male Aggression

A Possible Role for Epigenetic Effects




11 Emergence and Constraint in Novel Behavioral Adaptations

Historical Precedents

A Selective Review: Ontology and Emergence of Novelty

Developmental Biologists: Coordination and Constraints

Contemporary Views of Evolutionary Change: Emergence and Epigenesis

Behavioral Novelty and Emergent Structures

Constraints as Factors Shaping Behavioral Development

Constraints and Emergence in Research Investigations

Gilbert Gottlieb: Radical Scientific Philosopher and Innovative Experimentalist (1929–2006)



12 Nonhuman Primate Research Contributions to Understanding Genetic and Environmental Influences on Phenotypic Outcomes across Development

Nonhuman Primates in Developmental Research

Environmental Manipulations in Nonhuman Primate Behavioral Genetic Research

Nonhuman Primate Model for Early Childhood Adversity

Nonhuman Primate Research on Specific Genetic Variation

Association Studies in Nonhuman Primates

Review of 5HTTLPR Findings in Macaques

Allele Frequencies and Comparative Considerations

Organization of Review of 5HTTLPR Macaque Studies

Major Findings across 5HTTLPR Macaque Studies

Other Genes

Summary and Conclusions


13 Interactive Contributions of Genes and Early Experience to Behavioral Development


Sensitive Periods of Development in Precocial Birds

Hemispheric Specializations

Sequential Changes in Hemispheric Dominance

Relevance to Other Species

Do These Epigenetic Influences Occur During Development in the Natural Environment?

Some Final Remarks



14 Trans-Generational Epigenetic Inheritance


Gene Regulation and Epigenetics

Trans-Generational Epigenetic Transmission

Implications and Conclusions


15 The Significance of Non-Replication of Gene-Phenotype Associations

The Concept of Replication

Reasons for Non-Replication from a Population Perspective

Genome-Wide Association Studies and Implications for a Population View of Replication

Non-Replication from a Probabilistic Epigenetic Perspective

Implications of Probabilistic Epigenesis for Models of Replication



16 Canalization and Malleability Reconsidered


The Rise of Evolutionary Developmental Biology

A Reformulation of Species-Typical Behavior

The Significance of Behavioral Malleability

The Illustrative Case of Filial Imprinting

Further Explorations of the Malleability of Species-Typical Behavior

The Organism–Environment System

Concluding Remarks



Part IV Applications to Development

17 Gene-Parenting Interplay in the Development of Infant Emotionality

Chapter Structure

Gene-Environment Correlation

Genetics of Infants’ Emotionality

Infant Emotionality and Physiological Responses

Parenting, Infants’ RSA Regulation, and Emotionality

G × E (Parenting) Predictors of RSA



18 Genetic Research in Psychiatry and Psychology


Family Studies

Twin Studies

Adoption Studies

Molecular Genetic Research

Summary and Conclusions




19 On the Limits of Standard Quantitative Genetic Modeling of Inter-Individual Variation


Aspects of the Standard Genetic Factor Model

Problems with the Standard Genetic Factor Model

General Problems with Analyses of Inter-Individual Variation

Genetic Decomposition of Intra-Individual Variation



20 Songs My Mother Taught Me: Gene-Environment Interactions, Brain Development and the Auditory System: Thoughts on Non-Kin Rejection

Example 1: Yeast Mating Types are Regulated by Epigenetic Mechanisms

Example 2: Hemoglobin Switching: Non-Coding DNA Sequences Specify Sites for Epigenetic Regulation

Example 3: Specification of the Auditory System

Example 4: Gamma Band Activation by Auditory Input

Example 5: Consonant Learning Involves Visual as well as Auditory Input



21 Applications of Developmental Systems Theory to Benefit Human Development

The Contemporary Features of Human Developmental Science

Gilbert Gottlieb’s View of Epigenesis

From Phylogeny to Ontogeny

Applied Developmental Science: An Overview




Author Index

Subject Index



Elaine L. Bearer, University of New Mexico

Allyson Bennett, Wake Forest University

Michelle J. Boyd, Tufts University

Susan A. Brunelli, Columbia University Medical Center

Gary Greenberg, Wichita State University

Paul E. Griffiths, University of Sydney

Carolyn Tucker Halpern, University of North Carolina at Chapel Hill

Lawrence V. Harper, University of California, Davis

Christopher Harshaw, Florida International University

Mae Wan Ho, Institute of Science in Society

Myron A. Hofer, Columbia University Medical Center

Kathryn E. Hood, The Pennsylvania State University

Jay Joseph, Licensed Psychologist

Evelyn Fox Keller, Massachusetts Institute of Technology

Megan K. Kiely, Tufts University

Richard M. Lerner, Tufts University

Robert Lickliter, Florida International University

Valeria Méndez-Gallardo, University of Iowa

George F. Michel, University of North Carolina at Greensboro

W. Roger Mills-Koonce, The University of North Carolina at Chapel Hill

Peter C. M. Molenaar, The Pennsylvania State University

Ginger A. Moore, The Pennsylvania State University

Christopher M. Napolitano, Tufts University

Ty Partridge, Wayne State University

Peter J. Pierre, Wake Forest University

Cathi B. Propper, The University of North Carolina at Chapel Hill

Scott R. Robinson, University of Iowa

Lesley J. Rogers, University of New England, Armidale

Jay S. Rosenblatt, Institute of Animal Behavior, Rutgers

Kristina L. Schmid, Tufts University

James Tabery, University of Utah

Douglas Wahlsten, University of North Carolina at Greensboro

Betty Zimmerberg, Williams College

Foreword: Gilbert Gottlieb and the Developmental Point of View

Evelyn Fox Keller

Gilbert Gottlieb is widely known for his life-long struggle against the dichotomies between nature and nurture, and more specifically, between innate and acquired, that so hobble our thinking about biological and psychological development. Development, as he so clearly recognized, is an immensely complex process that depends on ongoing interactions between whatever makes up the organism at any given time and its environment; and it simply cannot be understood in terms of separate (or separable) forces, elements, or factors. Decades of his own research on the role of experience in the emergence of animal behavior taught him just how dire was the need for a different explanatory model, and indeed, much of his theoretical work was devoted to the articulation of such an alternative – of an explanatory framework that begins with what he liked to call the “developmental point of view.”

A developmental point of view requires a “relational” (“coactive” and “bidirectional”) view of causality; an appreciation of the continuity between prenatal and postnatal, innate and acquired; the recognition that epigenesis is ongoing, multifaceted, not predetermined but highly dependent on experience (or, to use the term that Gottlieb preferred for describing this process, “probabilistic”), and top-down as well as bottom up. Finally, a developmental point of view requires us to shift our focus from population statistics to the study of individual trajectories for it is only through the study of such trajectories that one can begin to understand the dynamics of developmental change.

Gottlieb devoted his entire career to fleshing out this perspective, and there is no denying his influence. He leaves behind an impressive body of both experimental results and conceptual proposals, and perhaps most important, a host of students who were deeply inspired by his example, and who, in their own labs, continue in his tradition and carry on his mission. And yet, notwithstanding the magnitude of his influence, shortly before his death, he confessed to a former student that “getting across the developmental point of view has been the largest failure of my career” (Miller, 2007, p. 777). It is impossible for anyone who has struggled with these issues not to sympathize, or to fail to appreciate the magnitude of the obstacles facing any attempt to reconfigure the terms of our analyses.

As we know, Gottlieb was hardly the first to undertake this challenge, nor was he alone even in his own time. As he freely acknowledged, his debt to those who preceded him (especially, to Zing-Yang Kuo: (1898–1970), T. C. Schneirla (1902–1968), and Daniel S. Lehrman (1919–1972)) was immense; indeed, it was on their work that his own went on to build. He was equally appreciative of the contributions of like-minded contemporaries (e.g., Patrick Bateson, Susan Oyama, Richard M. Lerner), as he was of the contributions of a younger generation of colleagues. And I suspect that all of these authors have shared Gottlieb’s frustration, for all of them have confronted the same obstacles, inevitably giving rise to the question of why the difficulties should be quite so intractable. Daniel Lehrman (1970, pp. 18–19) suggested we look to semantic problems for an understanding:

When opposing groups of intelligent, highly educated, competent scientists continue over many years to disagree, and even to wrangle bitterly, about an issue which they regard as important, it must sooner or later become obvious that the disagreement is not a factual one, and that it cannot be resolved by calling to the attention of the members of one group … the existence of new data which will make them see the light … If this is, as I believe, the case, we ought to consider the roles played in this disagreement by semantic difficulties arising from concealed differences in the way different people use the same words, or in the way the same people use the same words at different times; [and] by differences in the concepts used by different workers. (1970, pp. 18–19)

I would go further. It is not just that we use the same words in different ways, that the language of behavioral genetics is hopelessly polysemic, but also that we seem to be trapped by the absence of adequate alternatives. Indeed, the lack of a vocabulary capable of doing justice to the developmental point of view constituted a formidable obstacle for Gottlieb, and his frequent coining of new terms suggests that he was well aware of the problem. The difficulty (as he himself clearly saw) is that introducing a new vocabulary is a far from simple task, and it requires a great deal more than the efforts of a few individuals. Language changes only when the felt need for a new vocabulary becomes truly widespread.

I am persuaded, however, that winds of change are in the air. New appreciation of many of Gottlieb’s themes – of the agency of organisms in constructing their environments (see, e.g., Odling-Smee et al., 2003), of the plasticity of development (West-Eberhard, 2003), of the role of phenotypic plasticity in the genesis of evolutionary novelty (Kirschner & Gerhart, 2005), of the deeply contextual character of biological information -- has begun to penetrate the main corridors of contemporary biology. These themes not only both echo and support many of Gottlieb’s own arguments, but also extend the “developmental point of view” into new domains. Signs of change are also evident in studies of the most primitive molecular levels of life. Recent findings in genomics have brought fundamental new challenges to the very concept of a particulate gene, leading a number of molecular geneticists (and others) to call for a more dynamic and relational discourse of genetics for the 21st century (see, e.g., Fox Keller & Harel, 2007; Kapranov et al, 2007; Pearson, 2006; Silver, 2007). I only wish that Gottlieb could have lived to see the creation of the more accommodating home for his work that will, I believe, come with the realization of these signs of change.


Fox Keller, E., & Harel, D. (2007). Beyond the gene. PLoS ONE, 2(11): e1231 doi:10.137l/journal.pone.0001231

Kapranov, P., Willingham, A. T., & Gingeras, T. R. (2007). Genome-wide transcription and the implications for genomic organization. Nature Reviews Genetics, 8, 413–423.

Kirschner, M. W., & Gerhart, J. C. (2005). The plausibility of life: Resolving Darwin’s dilemma. New Haven: Yale University Press.

Lehrman, D. S. (1970). Semantic and conceptual issues in the nature-nurture problem. In L. Aronson, E. Tobach, D. S. Lehrman, & J. S. Rosenblatt (Eds.), Development and evolution of behavior (pp. 17–52). New York: W. H. Freeman.

Miller, D. B. (2007). From nature to nurture, and back again. Developmental Psychobiology, 49, 770–779.

Odling-Smee, F. J., Laland, K., & Feldman, M. W. (2003). Niche construction: The neglected process in evolution. Princeton, NJ: Princeton University Press.

Pearson, H. (2006). What is a gene? Nature, 441, 399–401.

Silver, L. (2007). The year of miracles. Newsweek, October 15.

West-Eberhard, M. J. (2003). Developmental plasticity and evolution. New York: Oxford University Press.

Preface and Acknowledgments

The Handbook of Developmental Science, Behavior, and Genetics commemorates the historically important and profound contributions made by Gilbert Gottlieb across a scholarly career spanning more than four decades. Gottlieb was preparing this handbook when his untimely death in 2006 brought his work on this project to a halt. However, with the permission and support of the Gottlieb Family, the editors of this work have decided to complete Gottlieb’s "last book," which was designed to bring together in one place cutting-edge theory, research, and methodology affording a modern scientific understanding of the role of genes within the integrated and multi-level (or "fused") developmental system, that is, the system constituted by the levels of organization – ranging from the inner biological (e.g., genetic, hormonal, or neuronal) through the designed and natural physical ecological and historical – comprising the ecology of organism development.

Gottlieb’s career was dedicated to providing rigorous experimental evidence to bear on such an integrative approach to understanding the dynamics of organism and context relations that provides the fundamental process of development. His work, – and those of other colleagues in comparative and developmental science – for instance, Z. Y. Kuo, T. C. Schneirla, Ethel Tobach, Jay Rosenblatt, Daniel Lehrman, Howard Moltz, and George Michel – was the major scientific basis for rejecting the reductionism and counterfactual, “split” conceptions (of variables purportedly linked alone to nature- or to nurture-related processes) used in other approaches to understanding the links among genes, behavior, and development, for example, as found in behavioral genetics (or in other reductionist accounts of the role of biology in development, for example, sociobiology or evolutionary psychology).

Accordingly, the scholarship that Gottlieb envisioned having in this handbook – and the scholarship we as editors who have tried to implement his vision hope we have presented – offers readers the cutting-edge of theory and research from developmental-systems-predicated scholarship in biological, comparative, and developmental science. Together, this work underscores the usefulness of the synthetic, developmental systems approach to understanding the mutually influential relations among genes, behavior, and context that propel the development of organisms across their life spans.

Our aspiration is that the scholarship that we present in this Handbook will constitute a watershed reference work documenting the current ways in which psychological, biological, comparative, and developmental science are framed and, as well, advance a developmental systems approach to understanding the dynamics of mutually influential organism-environment relations. Represented as organism ↔ context relations, these relations constitute the basic unit of analysis in comparative and developmental science. In addition, from the theoretical and empirical approaches championed by Gottlieb, these organism ↔ context relations constitute the basis of change across the life spans of all organisms. We owe to Gilbert Gottlieb the clarity of theoretical vision and the standard for rigorous empirical work that has enabled this dynamic, developmental perspective to frame the cutting edge of contemporary scientific inquiry about the role of variables from all levels of organization, from genes through history, in constituting the fundamental, relational process involved in the development of all organisms across their respective life spans.

There are numerous other people to whom we owe enormous thanks for their contributions to this Handbook. Clearly, we are deeply grateful to the colleagues who contributed to this work, both for their superb scholarly contributions and for their commitment to working collaboratively to honor the work and memory of Gilbert Gottlieb. Without the excellent scholarship they contributed to this Handbook we could not honor the memory of Gilbert Gottlieb – as scientist, colleague, and friend – as thoughtfully, thoroughly, and richly as we are now able to do.

We also thank the two superb managing editors at the Institute for Applied Research in Youth Development – Leslie Dickinson and Jarrett Lerner – for their editorial work. Their commitment to quality and productivity, and their resilience in the face of the challenges of manuscript production, are greatly admired and deeply appreciated. Kathryn E. Hood is pleased to acknowledge the generous hospitality of the Center for Developmental Science at Chapel Hill, which long has welcomed visiting scholars such as Gilbert Gottlieb. Carolyn Halpern is grateful to her co-editors for their scholarship and insights, and to Gilbert Gottlieb for his mentorship and collaboration. Gary Greenberg is grateful to his wife Patricia Greenberg for her unstinting and continued support and encouragement and for understanding his long hours at the computer. Richard M. Lerner is grateful to the John Templeton Foundation, the National 4-H Council, the Philip Morris Smoking Prevention Department, and the Thrive Foundation for Youth for supporting his work during the development of this project.

Finally, we owe our deepest and most enduring debt to Gilbert Gottlieb, to whom we most obviously wish to dedicate this Handbook. Gilbert Gottlieb was one of the pillars of 20th century comparative psychology. His intellect, generosity, and kindness are warmly remembered and sorely missed.

Kathryn E. Hood

Carolyn Halpern

Gary Greenberg

Richard M. Lerner

Part I