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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

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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