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Ecological Developmental Biology: Integrating Epigenetics, Medicine, and Evolution

Scott F. Gilbert and David Epel

December 2008

459 pages, 182 illustrations

paper

About This Title

When the molecular processes of epigenetics meet the ecological processes of phenotypic plasticity, the result is a revolutionary new field: ecological developmental biology, or “eco-devo.” This new science studies development in the “real world” of predators, pathogens, competitors, symbionts, toxic compounds, temperature changes, and nutritional differences. These environmental agents can result in changes to an individual’s phenotype, often implemented when signals from the environment elicit epigenetic changes in gene expression. Ecological developmental biology is a truly integrative biology, detailing the interactions between developing organisms and their environmental contexts.

Ecological developmental biology also provides a systems approach to the study of pathology, integrating the studies of diabetes, cancers, obesity, and the aging syndrome into the framework of an ecologically sensitive developmental biology. It looks at examples where the environment provides expected cues for normal development and where the organism develops improperly without such cues. Data from research on teratology, endocrine disruptors, and microbial symbioses, when integrated into a developmental context, may have enormous implications for human health as well as the overall health of Earth’s ecosystems.

The study of epigenetics—changes in gene expression that are not the result of changes in a gene’s DNA sequence—has recently provided startling insights not only into mechanisms of development, but also into the mechanisms and processes of evolution. The notion that epialleles (changes in chromosome structure that alter gene expression) can be induced by environmental agents and transmitted across generations has altered our notions of evolution, as have new experiments documenting the genetic fixation of environmentally induced changes in development. The widespread use of symbiosis in development provides new targets for natural selection. Ecological developmental biology integrates these new ideas into an extended evolutionary synthesis that retains and enriches the notion of evolution by natural selection.

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About the Authors

Scott F. Gilbert, the Howard A. Schneiderman Professor of Biology at Swarthmore College, teaches developmental biology, developmental genetics, and the history of biology. After receiving his B.A. from Wesleyan University, he pursued his graduate and postdoctoral research at The Johns Hopkins University and the University of Wisconsin. Dr. Gilbert is the recipient of several awards, including the first Viktor Hamburger Award for excellence in developmental biology education, the 2004 Alexander Kowalevsky Prize for evolutionary developmental biology, an honorary degree from the University of Helsinki, and the Medal of François I from the Collège de France. He is a Fellow of the American Association for the Advancement of Science, and a corresponding member of the St. Petersburg Society of Naturalists. His research is sponsored by the National Science Foundation and involves the developmental genetic mechanisms by which the turtle forms its shell.

David Epel, the Jane and Marshall Steel Jr. Professor of Biological Sciences at Stanford University’s Hopkins Marine Station, did his undergraduate studies at Wayne University and then graduate and postdoctoral studies at the University of California, Berkeley and the University of Pennsylvania. Dr. Epel has been a Guggenheim Fellow, is a Fellow of the American Association for the Advancement of Science, the California Academy of Sciences, and an Overseas Fellow of Churchill College and Life Fellow of Clare Hall at the University of Cambridge. His honors include the Cox Medal for Fostering Undergraduate Research at Stanford and the Ed Ricketts Memorial Award for Lifetime Achievement in the Marine Sciences. Epel’s research focuses on the activation of the egg at fertilization, the unique physiology of the embryo, and developing web sites and curricula highlighting early development of the sea urchin embryo to capture the imagination and interest of high school students.

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Reviews and Commentary

“The book covers vast territory, describing how the environment can influence everything from cancer in humans, to wing patterns in butterflies, to sex determination in turtles. Yet, despite the broad scope, the writing is synthetic, and the authors use clear, simple, and accessible language with beautiful, colorful, and informative illustrations throughout.… this is a must-read for graduate students interested in integrating ecology, developmental biology, and evolutionary biology.”

—Antónia Monteiro, Cell

“These are propitious and exciting times for integrating the fields of development, ecology, and evolution. Students and researchers are fortunate that (in addition to the present volume) several important books have appeared recently …. Nevertheless, we have only begun to construct an integrated framework. Gilbert and Epel acknowledge the arduous task ahead and ‘hope that college students, still relatively undifferentiated, will come up with their own connections and syntheses and that they will see patterns that we haven’t yet imagined.’ Ecological Developmental Biology will serve as an excellent guide for those interested in embarking on such a synthesis. More generally, this lucid and thought-provoking book should appeal to anyone interested in understanding how organisms are built, function, and evolve or how anthropogenic environmental change affects the health of ourselves and other organisms.”

—David W. Pfennig and Chris Ledón, Science

“The appearance of a textbook is often the culmination of a long process moving a subject from the fringes to the center of a discipline, or perhaps the coalescence of a discipline. Ecological Developmental Biologyis such a milestone.”

—Samuel M. Scheiner, Evolution

“Gilbert and Epel are to be commended for this excellent collection of material and their effort to integrate that material into a new discipline. A very worthwhile endeavor.”

—F. W. Yow, Choice

“Overall, a masterful synthesis! It’s one of those things that makes one say, ‘Damn, I wish I had written that!’”

—Fred Nijhout, Duke University

“A unique, thought-provoking, and clearly written treatment, at the molecular level, of the environment’s influence on embryonic development and the paths of evolutionary change.”

—John Gerhart, University of California, Berkeley

“This is an incredible piece of work, and something that is sorely needed, right now.”

—Mary Tyler, University of Maine

“This is an extraordinary work … first-class conceptually and pedagogically.”

—John Beatty, University of British Columbia

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Contents

PART 1. ENVIRONMENTAL SIGNALS AND NORMAL DEVELOPMENT

1. The Environment as a Normal Agent in Producing Phenotypes

• Plasticity Is a Normal Part of Development
  • A century of studies
  • A contextually integrated view of life
• “Eco-Devo” and Developmental Plasticity
  • Reaction norms and polyphenisms
  • Epigenetics
  • Agents of developmental plasticity
  • Temperature-Dependent Phenotypes
    • Enzyme activity as a function of temperature
    • Seasonal polyphenism in butterflies
    • Temperature and sex
  • Nutritional Polyphenism: What You Eat Becomes You
    • Royal jelly and egg-laying queens
    • Horn length in the male dung beetle
  • Gravity and Pressure
  • Predator-Induced Polyphenisms
    • Predator-induced polyphenism in invertebrates
    • Predator-induced polyphenism in vertebrates
  • The Presence of Conspecifics: It’s Who You Know
    • A swarm of locusts: Polyphenism through touch
    • Sexual polyphenism by the community environment
  • Convergence on Favorable Phenotypes
  • Summary
  • References

2. How Agents in the Environment Effect Molecular Changes in Development

• Regulation of Gene Transcription
  • Differential gene expression
  • DNA methylation
  • Environmental agents and direct DNA methylation
  • The effects of maternal behavior on gene methylation
• Signal Transduction from Environment to Genome via the Neuroendocrine System
  • Neuroendocrine regulation of temperature-dependent polyphenism in insects
  • Neuroendocrine regulation of sex determination
  • An extreme phenotype for extreme times: Stress and cannibalism
  • “We will pump you up”: Muscle hypertrophy
• Signal Transmission from Environment to Genome through Direct Induction
  • Microbial induction of gene expression in vertebrate intestines
  • Microbial induction of the vertebrate immune response
• Transgenerational Effects
  • Transgenerational polyphenism in locusts
  • Transgenerational predator-induced polyphenisms
  • Methylation and transgenerational continuity: Toadflax
  • Methylation and transgenerational continuity: Mice and rats
• Summary
• References

3. Developmental Symbiosis: Co-Development as a Strategy for Life

• Symbiosis: An Overview
• The “Grand” Symbioses
  • Nitrogen-fixing nodules
  • Mycorrhizae
• Life Cycle Symbioses
• Getting Symbionts Together with Their Hosts
• The Squid and the Microbe: A Paradigm of Symbiont Influence
• Evolution of the Symbiotic Regulation of Development: Wolbachia
  • Sex determination by infection
  • Evolution of dependence on Wolbachia for sexual development
• The Mutualistic Bacteria of the Mammalian Gut
  • Introduction to the gut microbiota
  • Maintaining the gut microbial community: The biofilm model
  • Inheritance of the gut bacteria
  • Functions of the microbial community
• Gut Bacteria and Normal Mammalian Development
  • An important role for symbiotic bacteria in the normal development of the host’s gut: Angiogenesis induction
  • The impact of symbiotic gut bacteria on the development of the host immune system: Antimicrobial secretions
  • B lymphocytes and the GALT
• Gut Bacteria Symbiosis and Human Health
  • Bacterial regulation of the immune response
  • The role of the gut bacteria in fat storage: Implications for human obesity
  • Further implications of the enteric gut bacteria for human health
• Summary
• References

4. Embryonic Defenses: Survival in a Hostile World

• Characteristics of Embryo Defense
  • Developmental robustness: A necessary but paradoxical defense
  • Early embryonic cells differ from adult cells
• Strategies for Embryo Defense
  • Strategy 1: Induced polyphenism
  • Strategy 2: Parental protection
  • Strategy 3: Dormancy and diapause
  • Strategy 4: Defense physiologies
• Mechanisms of Embryo Defense
  • A general strategy: “Be prepared”
• Protection against Toxic Substances
  • The general plan: “Bouncers,” “chemists,” and “policemen”
  • Toxic metals
  • Problems with metal detoxification
• Protection against Physical Damage
  • Shells and extracellular coats
  • Cytoplasmic sealing
• Protection against Oxidative Damage
• Protection against Damage to DNA
  • Sunscreens to prevent DNA damage
  • Repairing damaged DNA
• Protection against Pathogens
  • Parental behavior
  • Chemical protection
  • Embryonic immune responses
  • Symbiosis and protection from fungi
• Protection from Predation
• Summary
• References

PART 2. ECOLOGICAL DEVELOPMENTAL BIOLOGY AND DISEASE STATES

5. Teratogenesis: Environmental Assaults on Development

• Medical Embryology and Teratology
  • Wilson’s principles of teratology
  • Thalidomide and the window of susceptibility
• Teratogenic Agents
  • Chemical teratogens: Industrial mercury and Minamata disease
  • Alcohol as a teratogen
  • Retinoic acid
  • Other teratogenic agents
• Natural Killers: Teratogens from Plants
  • Veratrum alkaloids
  • Plant juvenile hormones
• Deformed Frogs: A Teratological Enigma
  • A combination of factors
  • The radiation hypothesis
  • Pesticides and herbicides
• Summary
• References

6. Endocrine Disruptors

• The Nature of Endocrine Disruptors
  • The endocrine disruptor hypothesis
  • DDT: The start of it all
• Estrogen and Endocrine Disruptors
  • The structure and mechanisms of estrogen receptors
  • Diethylstilbestrol
  • Mechanisms of DES action
  • Soy estrogens
  • Declining sperm counts and testicular dysgenesis syndrome
  • Pesticides and infertility in males
  • Atrazine, again
• Plastics and Plasticity
  • Bisphenol A
  • The dose-response curve of BPA action
  • The molecular biology of the BPA effect
  • Epigenetic effects of BPA
  • Polychlorinated biphenyls
  • Possible mechanisms for the effects of PCBs
• Transgenerational Effects of Endocrine Disruptors
• Summary
• References

7. The Epigenetic Origin of Adult Diseases

THE DEVELOPMENTAL ORIGINS OF HEALTH AND DISEASE

• Instructing the Fetus
  • Maternal–fetal co-development
  • Fetal plasticity in humans
  • Gene methylation and the fetal phenotype
• Predictive Adaptive Responses
  • The environmental mismatch hypothesis
  • Environment–genotype interactions in diabetes
• Developmental Plasticity and Public Health

AGING AND CANCER AS DISEASES OF EPIGENESIS

• Epigenetic Methylation, Disease, and Aging
  • Evidence from identical twins
  • Aging and random epigenetic drift
• Epigenetic Origins of Cancer
  • Cancer as caused by altered epigenetic methylation
  • The reciprocity of epigenetic and genetic causation in cancer
  • The tissue organization field hypothesis
• Summary
• References

PART 3. TOWARD A DEVELOPMENTAL EVOLUTIONARY SYNTHESIS

8. The Modern Synthesis: Natural Selection of Allelic Variation

• Charles Darwin’s Synthesis
  • Classical Darwinism: Natural selection
  • Embryology and Darwin’s synthesis
  • The failure of developmental morphology to explain evolution
• The Modern Synthesis
• The Triumph of the Modern Synthesis: The Globin Paradigm
  • Hemoglobin S and sickle-cell disease
  • Favism
• Summary
• References

9. Evolution through Developmental Regulatory Genes

• The Origins of Evolutionary Developmental Biology
• Molecular Parsimony: “Toolkit Genes”
  • Duplication and divergence: The Hox genes
  • Homologous pathways of development
  • Toolkit genes and evolution: A summary
• Modularity: Divergence through Dissociation
  • Enhancer modularity
  • Malaria, again
• Mechanisms of Macroevolutionary Change
  • Heterotopy
  • Heterochrony
  • Heterometry
  • Heterotypy
• Speciation
  • Speciation in the Modern Synthesis
  • Regulatory RNAs may make us human
• Developmental Constraints on Evolution
  • Physical constraints
  • Morphogenetic constraints
  • Phylogenetic constraints
• Summary
• References

10. Environment, Development, and Evolution: Toward a New Synthesis

EPIGENETIC INHERITANCE SYSTEMS

HETEROCYBERNY: PLASTICITY-DRIVEN ADAPTATION

• Phenocopies and Ecotypes
• Genetic Assimilation
  • Genetic assimilation in the laboratory
  • Genetic assimilation in nature: Mechanisms, models, and inferences
  • Genetic assimilation and natural selection
• Phenotypic Accommodation
  • Evolutionary considerations
• Genetic Accommodation
  • Developmental mechanisms of phenotypic accommodation
  • Reciprocal accommodation

NICHE CONSTRUCTION

• Summary: Eco-Evo-Devo
• References

Coda: Philosophical Concerns Raised by Ecological Developmental Biology

• Ontology
  • What is an “individual” in terms of developmental and ecological history?
  • What is an “individual” in terms of its developmental and evolutionary history?
  • Integrative philosophical traditions
  • Emergence
• Pedagogy
• Epistemology and Methodology
  • How we study development
  • How we study evolution and ecology
• Ethics and Policy
• Ethics for the Anthropocene

Appendix A. Lysenko, Kammerer, and the Truncated Tradition of Ecological Developmental Biology

Appendix B. The Molecular Mechanisms of Epigenetic Change

Appendix C. Writing Development Out of the Modern Synthesis

Appendix D. Epigenetic Inheritance Systems: The Inheritance of Environmentally Induced Traits

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