Download Ecological Developmental Biology: Integrating Epigenetics

Integrating
Epigenetics,
Medicine,
and Evolution
Scott F. Gilbert
David Epel
Swarthmore College
Hopkins Marine Station,
Stanford University
Sinauer Associates, Inc. • Publishers
Sunderland, Massachusetts U.S.A.
© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured
or disseminated in any form without express written permission from the publisher.
Brief Contents
PART 1 Environmental Signals and Normal Development
CHAPTER 1 The Environment as a Normal Agent in Producing Phenotypes 3
CHAPTER 2 How Agents in the Environment Effect Molecular Changes in Development 37
CHAPTER 3 Developmental Symbiosis: Co-Development as a Strategy for Life 79
CHAPTER 4 Embryonic Defenses: Survival in a Hostile World 119
PART 2 Ecological Developmental Biology and Disease States
CHAPTER 5 Teratogenesis: Environmental Assaults on Development 167
CHAPTER 6 Endocrine Disruptors 197
CHAPTER 7 The Epigenetic Origin of Adult Diseases 245
PART 3 Toward a Developmental Evolutionary Synthesis
CHAPTER 8 The Modern Synthesis: Natural Selection of Allelic Variation 289
CHAPTER 9 Evolution through Developmental Regulatory Genes 323
CHAPTER 10 Environment, Development, and Evolution: Toward a New Synthesis 369
CODA Philosophical Concerns Raised by Ecological Developmental Biology 403
APPENDIX A Lysenko, Kammerer, and the Truncated Tradition of Ecological Developmental Biology 421
APPENDIX B The Molecular Mechanisms of Epigenetic Change 433
APPENDIX C Writing Development Out of the Modern Synthesis 441
APPENDIX D Epigenetic Inheritance Systems: The Inheritance of Environmentally Induced Traits 447
© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured
or disseminated in any form without express written permission from the publisher.
Contents
PART 1 Environmental Signals and Normal Development
CHAPTER 1 The Environment as a
CHAPTER 2 How Agents in the
Normal Agent in Producing Phenotypes 3
Environment Effect Molecular Changes
in Development 37
Plasticity Is a Normal Part of Development 6
BONELLIA VIRIDIS: WHEN THE ENVIRONMENT
DETERMINES SEX 6
A century of studies 7
A contextually integrated view of life 8
“Eco-Devo” and Developmental Plasticity 9
Reaction norms and polyphenisms 11
Epigenetics 12
Agents of developmental plasticity 13
Temperature-Dependent Phenotypes 13
Enzyme activity as a function of temperature 13
Seasonal polyphenism in butterflies 16
Temperature and sex 17
Nutritional Polyphenism: What You Eat Becomes
You 20
Royal jelly and egg-laying queens 20
Horn length in the male dung beetle 21
Gravity and Pressure 23
Predator-Induced Polyphenisms 26
Predator-induced polyphenism in invertebrates 27
Predator-induced polyphenism in
vertebrates 27
The Presence of Conspecifics: It’s Who You
Know 29
A swarm of locusts: Polyphenism through
touch 30
POLYPHENISMS AND CONSERVATION BIOLOGY 31
Sexual polyphenism by the community
environment 32
Convergence on Favorable Phenotypes 32
Summary 32
References 33
Regulation of Gene Transcription 38
Differential gene expression 38
DNA methylation 42
Environmental agents and direct DNA
methylation 43
The effects of maternal behavior on gene
methylation 44
Signal Transduction from Environment to
Genome via the Neuroendocrine System 46
VERNALIZATION: TEMPERATURE-DEPENDENT
CHROMATIN CHANGES 47
Neuroendocrine regulation of temperaturedependent polyphenism in insects 49
Neuroendocrine regulation of sex determination 51
SEX, AROMATASE, AND CONSERVATION BIOLOGY 54
An extreme phenotype for extreme times:
Stress and cannibalism 57
“We will pump you up”: Muscle hypertrophy 59
ANABOLIC STEROIDS 62
Signal Transmission from Environment to
Genome through Direct Induction 64
Microbial induction of gene expression in
vertebrate intestines 64
Microbial induction of the vertebrate immune
response 65
Transgenerational Effects 67
Transgenerational polyphenism in locusts 68
Transgenerational predator-induced
polyphenisms 68
Methylation and transgenerational continuity:
Toadflax 70
Methylation and transgenerational continuity:
Mice and rats 71
Summary 74
References 74
© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured
or disseminated in any form without express written permission from the publisher.
viii
Contents
CHAPTER 3 Developmental Symbiosis:
CHAPTER 4 Embryonic Defenses: Survival
Co-Development as a Strategy for Life 79
in a Hostile World 119
Symbiosis: An Overview 80
The “Grand” Symbioses 81
Characteristics of Embryo Defense 122
Nitrogen-fixing nodules 81
ENDOPHYTES 83
Mycorrhizae 83
Life Cycle Symbioses 85
THE LARGE BLUE BUTTERFLY 86
Getting Symbionts Together with Their Hosts 87
The Squid and the Microbe: A Paradigm of
Symbiont Influence 89
Evolution of the Symbiotic Regulation of
Development: Wolbachia 91
Sex determination by infection 92
Evolution of dependence on Wolbachia for sexual development 95
MUTUALISTIC CONSORTIA 97
The Mutualistic Bacteria of the Mammalian Gut
98
Introduction to the gut microbiota 98
Maintaining the gut microbial community: The
biofilm model 99
Inheritance of the gut bacteria 100
Gut Bacteria and Normal Mammalian
Development 101
An important role for symbiotic bacteria in the
normal development of the host’s gut:
Angiogenesis induction 101
The impact of symbiotic gut bacteria on the
development of the host immune system:
Antimicrobial secretions 103
IMMUNITY THROUGH DEVELOPMENTAL SYMBIOSIS
104
B lymphocytes and the GALT 105
IMMUNE SYSTEM CELL TYPES 105
Gut Bacteria Symbiosis and Human Health 107
Bacterial regulation of the immune response
107
The role of the gut bacteria in fat storage:
Implications for human obesity 110
Further implications of the enteric gut bacteria
for human health 112
Developmental robustness: A necessary but
paradoxical defense 122
Early embryonic cells differ from adult cells
125
SPECULATIONS ON CELL DEFENSES IN EARLY
DEVELOPMENT 127
Strategies for Embryo Defense 129
Strategy 1: Induced polyphenism 129
Strategy 2: Parental protection 129
Strategy 3: Dormancy and diapause 130
THE DAUERLARVA OF C. ELEGANS 132
Strategy 4: Defense physiologies 133
A general strategy: “Be prepared” 134
Mechanisms of Embryo Defense 134
Protection against Toxic Substances 135
The general plan: “Bouncers,” “chemists,” and
“policemen” 135
Toxic metals 138
Problems with metal detoxification 140
Protection against Physical Damage 141
Shells and extracellular coats 141
Cytoplasmic sealing 145
Protection against Oxidative Damage 147
Protection against Damage to DNA 150
Sunscreens prevent DNA damage 150
Repairing damaged DNA 153
Protection against Pathogens 154
Parental behavior 155
Chemical protection 155
Embryonic immune responses 155
Symbiosis and protection from fungi 156
Protection from Predation 158
Summary 160
References 161
Summary 114
References 115
© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured
or disseminated in any form without express written permission from the publisher.
Contents
ix
PART 2 Ecological Developmental Biology and Disease States
CHAPTER 5 Teratogenesis: Environmental
Assaults on Development 167
Medical Embryology and Teratology 168
Wilson’s principles of teratology 169
Thalidomide and the window of
susceptibility 170
Teratogenic Agents 172
Chemical teratogens: Industrial mercury and
Minamata disease 172
Alcohol as a teratogen 173
Retinoic acid 180
TERATOGENS AND COGNITIVE FUNCTION 182
Other teratogenic agents 183
Natural Killers: Teratogens from Plants 185
Veratrum alkaloids 185
Plant juvenile hormones 187
Deformed Frogs: A Teratological Enigma 189
A combination of factors 189
The radiation hypothesis 190
Pesticides and herbicides 190
CONSERVATION BIOLOGY: SAVING THE FROGS 191
Summary 191
References 192
CHAPTER 6 Endocrine Disruptors 197
The Nature of Endocrine Disruptors 198
The endocrine disruptor hypothesis 199
DDT: The start of it all 200
ESTABLISHING A CHAIN OF CAUSATION 202
Estrogen and Endocrine Disruptors 203
The structure and mechanisms of estrogen
receptors 204
Diethylstilbestrol 206
Mechanisms of DES action 208
Soy estrogens 212
Declining sperm counts and testicular dysgenesis syndrome 213
Pesticides and infertility in males 215
SENSITIVITY TO DISRUPTION: A GENETIC
COMPONENT 216
Plastics and Plasticity 220
Bisphenol A 221
The dose-response curve of BPA action 225
The molecular biology of the BPA effect 226
Epigenetic effects of BPA 228
Polychlorinated biphenyls 229
Possible mechanisms for the effects of PCBs 230
Transgenerational Effects of Endocrine
Disruptors 230
Summary 233
REGULATORY AND POLICY DECISIONS ON BPA
AND OTHER ENDOCRINE DISRUPTORS 234
References 237
CHAPTER 7 The Epigenetic Origin of
Adult Diseases 245
The Developmental Origins of Health and
Disease 246
Instructing the Fetus 247
Maternal-fetal co-development 248
Fetal plasticity in humans 250
Gene methylation and the fetal phenotype 253
Predictive Adaptive Responses 256
The environmental mismatch hypothesis 260
Environment-genotype interactions in
diabetes 263
PATERNAL EPIGENETIC EFFECTS 264
Developmental Plasticity and Public Health 266
Aging and Cancer as Diseases of Epigenesis 267
Epigenetic Methylation, Disease, and Aging 267
Evidence from identical twins 268
Aging and random epigenetic drift 270
Epigenetic Origins of Cancer 273
Cancer as caused by altered epigenetic methylation 274
The reciprocity of epigenetic and genetic causation in cancer 277
The tissue organization field hypothesis 278
Summary 283
References 283
Atrazine, again 217
© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured
or disseminated in any form without express written permission from the publisher.
x
Contents
PART 3 Toward a Developmental Evolutionary Synthesis
CHAPTER 8 The Modern Synthesis:
Natural Selection of Allelic Variation 289
Charles Darwin’s Synthesis 291
Classical Darwinism: Natural selection 292
SELECTION FOR HERITABLE PLASTICITY 299
Embryology and Darwin’s synthesis 299
The failure of developmental morphology to
explain evolution 303
The Modern Synthesis 304
STURTEVANT ON SNAILS 305
The Triumph of the Modern Synthesis: The
Globin Paradigm 310
Hemoglobin S and sickle-cell disease 311
MALARIA AND EVOLUTION 312
Favism 316
Summary 318
References 320
CHAPTER 9 Evolution through Develop-
mental Regulatory Genes 323
The Origins of Evolutionary Developmental
Biology 324
Molecular Parsimony: “Toolkit Genes” 326
Duplication and divergence: The Hox genes
327
Homologous pathways of development 332
Toolkit genes and evolution: A summary 334
Modularity: Divergence through Dissociation
336
Enhancer modularity 337
Malaria, again 341
Mechanisms of Macroevolutionary Change 342
Heterotopy 342
Heterochrony 344
Heterometry 345
Heterotypy 350
Speciation 354
Speciation in the Modern Synthesis 354
Regulatory RNAs may help make us human
356
Developmental Constraints on Evolution 358
Physical constraints 358
Morphogenetic constraints 359
Phylogenetic constraints 359
REACTION-DIFFUSION MODELS 360
Summary 362
References 363
CHAPTER 10 Environment, Development,
and Evolution: Toward a New Synthesis
369
Epigenetic Inheritance Systems 370
Heterocyberny: Plasticity-Driven Adaptation 372
Phenocopies and Ecotypes 373
Genetic Assimilation 375
Genetic assimilation in the laboratory 377
Genetic assimilation in nature: Mechanisms,
models, and inferences 379
THRESHOLDS OF GENETIC ASSIMILATION 380
Genetic assimilation and natural selection 381
EPIGENETIC ASSIMILATION: ANOTHER HSP90 STORY
383
Genetic Accommodation 384
Phenotypic Accommodation 386
Evolutionary considerations 387
Developmental mechanisms of phenotypic
accommodation 389
Reciprocal accommodation 390
Niche Construction 391
Summary: Eco-Evo-Devo 395
References 398
© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured
or disseminated in any form without express written permission from the publisher.
Contents
CODA Philosophical Concerns Raised by
Ecological Developmental Biology 403
Ontology 404
What is an “individual” in terms of its
developmental and ecological history? 404
What is an “individual” in terms of its
developmental and evolutionary history? 405
Integrative philosophical traditions 408
Emergence 410
Pedagogy 411
Epistemology and Methodology 412
How we study development 412
How we study evolution and ecology 414
xi
APPENDIX A Lysenko, Kammerer, and the
Truncated Tradition of Ecological
Developmental Biology 421
APPENDIX B The Molecular Mechanisms of
Epigenetic Change 433
APPENDIX C Writing Development Out of the
Modern Synthesis 441
APPENDIX D Epigenetic Inheritance Systems:
The Inheritance of Environmentally Induced
Traits 447
Opening Plate Credits 460
Index 462
Ethics and Policy 415
Ethics for the Anthropocene 417
References 418
© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured
or disseminated in any form without express written permission from the publisher.