Brief Contents PART ONE QUESTIONS Introducing Developmental Biology 1 CHAPTER 1 Comprehending Development: Generating New Cells and Organs 5 CHAPTER 2 Differential Gene Expression in Development 31 CHAPTER 3 Cell-Cell Communication in Development 69 PART TWO SPECIFICATION Introducing Cell Commitment and Early Embryonic Development 107 CHAPTER 4 Fertilization: Beginning a New Organism 117 CHAPTER 5 Early Development: Rapid Specifi cation in Snails and Nematodes 153 CHAPTER 6 The Genetics of Axis Specifi cation in Drosophila 179 CHAPTER 7 Sea Urchins and Tunicates: Deuterostome Invertebrates 217 CHAPTER 8 Early Development in Vertebrates: Amphibians and Fish 241 CHAPTER 9 Early Development in Vertebrates: Birds and Mammals 285 PART THR EE THE STEM CELL CONCEPT Introducing Organogenesis 319 CHAPTER 10 The Emergence of the Ectoderm: Central Nervous System and Epidermis 333 CHAPTER 11 Neural Crest Cells and Axonal Specifi city 375 CHAPTER 12 Paraxial and Intermediate Mesoderm 415 CHAPTER 13 Lateral Plate Mesoderm and the Endoderm 449 CHAPTER 14 Development of the Tetrapod Limb 489 CHAPTER 15 Sex Determination 519 CHAPTER 16 Postembryonic Development: Metamorphosis, Regeneration, and Aging 549 CHAPTER 17 The Saga of the Germ Line 591 PART FOUR SYSTEMS BIOLOGY Expanding Developmental Biology to Medicine, Ecology, and Evolution 627 CHAPTER 18 Birth Defects, Endocrine Disruptors, and Cancer 635 CHAPTER 19 Ecological Developmental Biology: Biotic, Abiotic, and Symbiotic Regulation of Development 663 CHAPTER 20 Developmental Mechanisms of Evolutionary Change 689 © 2013 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 00_Gilbert10e_Frontmatter.Final.indd vi 5/16/13 2:23 PM Contents PART ONE QUESTIONS Introducing Developmental Biology 1 CHAPTER 1 SIDELIGHTS & SPECULATIONS The Basic Tools of Comprehending Development Developmental Genetics 32 Differential Gene Transcription 34 Generating New Cells and Organs 5 Anatomy of the gene: Active and repressed The Cycle of Life 6 chromatin 35 A Frog’s Life 6 Anatomy of the gene: Exons and introns 35 Gametogenesis and fertilization 6 Anatomy of the gene: Promoters and enhancers 37 Cleavage and gastrulation 7 Enhancer functioning 39 Organogenesis 10 Transcription factor function 43 Metamorphosis and gametogenesis 11 Keeping the right genes on or off 45 “How Are You?” 12 SIDELIGHTS & SPECULATIONS Reprogramming Comparative embryology 12 Cells: Changing Cell Differentiation through Epigenesis and preformation 12 Embryonic Transcription Factors 46 Naming the parts: The primary germ layers and early Mechanisms of Differential Gene Transcription 47 organs 14 Finding DNA regulatory sequences 48 The four principles of Karl Ernst von Baer 15 Differentiated proteins from high and low CpG- Keeping Track of Moving Cells: Fate Maps and content promoters 48 Cell Lineages 17 DNA methylation, another key on/off switch of Fate maps 19 transcription 49 Direct observation of living embryos 19 “Poised” chromatin 51 Dye marking 19 SIDELIGHTS & SPECULATIONS Genomic Genetic labeling 19 Imprinting and DNA Methylation 52 Transgenic DNA chimeras 23 Differential RNA Processing 53 Evolutionary Embryology 23 SIDELIGHTS & SPECULATIONS X Chromosome Embryonic homologies 25 Inactivation: Noncoding RNAs in Transcriptional Medical Embryology and Teratology 27 Gene Regulation 54 Genetic malformations and syndromes 27 Creating families of proteins through differential nRNA splicing 56 Disruptions and teratogens 27 Splicing enhancers and recognition factors 57 Control of Gene Expression at the Level of CHAPTER 2 Translation 59 Differential Gene Expression in Differential mRNA longevity 59 Development 31 Stored oocyte mRNAs: Selective inhibition of mRNA translation 59 Evidence for Genomic Equivalence 32 Ribosomal selectivity: Selective activation of mRNA translation 61 © 2013 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 00_Gilbert10e_Frontmatter.Final.indd vii 5/16/13 2:23 PM viii Contents microRNAs: Specifi c regulation of mRNA translation Paracrine Factors: Inducer Molecules 84 and transcription 61 Signal transduction cascades: The response to Control of RNA expression by cytoplasmic inducers 84 localization 64 Fibroblast growth factors and the RTK pathway 84 Posttranslational Regulation of Gene The JAK-STAT pathway 86 Expression 65 The Hedgehog family 88 Coda 65 The Wnt family 90 The TGF-β superfamily 92 CHAPTER 3 SIDELIGHTS & SPECULATIONS Cell Death Cell-Cell Communication in Pathways 94 Development 69 Other paracrine factors 96 Juxtacrine Signaling 96 Cell Adhesion 70 The Notch pathway: Juxtaposed ligands and Differential cell affi nity 70 receptors 96 The thermodynamic model of cell interactions 71 SIDELIGHTS & SPECULATIONS Juxtacrine Cadherins and cell adhesion 72 Signaling and Cell Patterning 97 SIDELIGHTS & SPECULATIONS Shape Change The Extracellular Matrix as a Source of and Epithelial Morphogenesis: “The Force Is Strong Developmental Signals 99 in You” 76 Integrins: Receptors for extracellular matrix Cell Migration 78 molecules 100 Cell Signaling 79 The Epithelial-Mesenchymal Transition 101 Induction and competence 79 The Cell Biology of Paracrine Signaling 102 Reciprocal induction 81 Coda 104 Epithelial-mesenchymal interactions 82 PART TWO SPECIFICATION Introducing Cell Commitment and Early Embryonic Development 107 Levels of Commitment 107 Morphogen Gradients and Conditional Autonomous Specifi cation 109 Specifi cation 113 Conditional Specifi cation 110 Syncytial Specifi cation 114 Summary 115 CHAPTER 4 The fast block to polyspermy 129 Fertilization The slow block to polyspermy 130 Calcium as the initiator of the cortical granule Beginning a New Organism 117 reaction 132 Structure of the Gametes 117 Activation of Egg Metabolism in Sea Urchins 134 Sperm 117 Release of intracellular calcium ions 134 Sperm anatomy 118 SIDELIGHTS & SPECULATIONS Rules of Evidence: The egg 120 “Find It, Lose It, Move It” 136 Recognition of egg and sperm 123 Effects of calcium release 137 External Fertilization in Sea Urchins 124 Fusion of Genetic Material in Sea Urchins 139 Sperm attraction: Action at a distance 124 Internal Fertilization in Mammals 140 The acrosome reaction 125 Getting the gametes into the oviduct: Translocation Recognition of the egg’s extracellular coat 126 and capacitation 141 Fusion of the egg and sperm cell membranes 128 In the vicinity of the oocyte: Hyperactivation, One egg, one sperm 128 thermotaxis, and chemotaxis 143 © 2013 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 00_Gilbert10e_Frontmatter.Final.indd viii 5/16/13 2:23 PM Contents ix The acrosome reaction and recognition at the zona GENES THAT PATTERN THE DROSOPHILA BODY pellucida 143 PLAN 185 Gamete fusion and the prevention of polyspermy 145 Primary Axis Formation during Oogenesis 186 Fusion of genetic material 146 Anterior-posterior polarity in the oocyte 186 Activation of the mammalian egg 146 Dorsal-ventral patterning in the oocyte 186 SIDELIGHTS & SPECULATIONS The Generating the Dorsal-Ventral Pattern in the Nonequivalence of Mammalian Pronuclei 148 Embryo 190 Coda 149 Dorsal, the ventral morphogen 190 Establishing a nuclear Dorsal gradient 190 CHAPTER 5 Effects of the Dorsal protein gradient 191 Early Development Rapid Specifi cation in SIDELIGHTS & SPECULATIONS The Left-Right and Inside-Out Axes 193 Snails and Nematodes 153 Segmentation and the Anterior-Posterior Body Developmental Patterns among the Metazoa 153 Plan 194 Sponges and the diploblastic animals 154 Maternal gradients: Polarity regulation by oocyte The triploblastic animals: Protostomes and cytoplasm 194 deuterostomes 155 The molecular model: Protein gradients in the early EARLY DEVELOPMENTAL PROCESSES: AN embryo 194 OVERVIEW 155 The anterior organizing center: The Bicoid and Hunchback gradients 199 Cleavage 155 The terminal gene group 201 From fertilization to cleavage 156 Summarizing early anterior-posterior axis The cytoskeletal mechanisms of mitosis 157 specifi cation in Drosophila 201 Patterns of embryonic cleavage 158 Segmentation Genes 202 Gastrulation and Axis Formation 158 Segments and parasegments 202 EARLY DEVELOPMENT IN SNAILS 161 The gap genes 203 Cleavage in Snail Embryos 161 The pair-rule genes 204 The snail fate map 164 The segment polarity genes 206 Autonomous cell specifi cation and the polar lobe 164 The Homeotic Selector Genes 209 SIDELIGHTS & SPECULATIONS Adaptation by Initiating and maintaining the patterns of homeotic Modifying Embryonic Cleavage 167 gene expression 211 Gastrulation in Snails 169 Realisator genes 211 Axes and Organ Primordia: The Cartesian THE NEMATODE C. ELEGANS 170 Coordinate Model 212 Cleavage and Axis Formation in C. elegans 171 Coda 213 Rotational cleavage of the egg 171 Anterior-posterior axis formation 171 Dorsal-ventral and right-left axis formation 172 CHAPTER 7 Control of blastomere identity 173 Sea Urchins and Tunicates Gastrulation in C. elegans 176 Deuterostome Invertebrates 217 EARLY DEVELOPMENT IN SEA URCHINS 217 CHAPTER 6 Sea Urchin Cleavage 217 The Genetics of Axis Specifi cation in Blastula formation 219 Drosophila 179 Fate maps and the determination of sea urchin blastomeres 219 EARLY DROSOPHILA DEVELOPMENT 179 Gene regulatory networks and skeletogenic Fertilization 180 mesenchyme