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PART I: CONTEXT AND FOUNDATIONS 1 1 Evolution and Embryology: A Brief History of a Complex Pas de Deux 3 Introduction: Birth of a Scientific Field 3 The Modern Synthesis and the Further BOX 1.1 CLONING HOX GENES 6 Eclipse of Embryology 24 Identifying the Paradox; Defining a Specialization within Biology 25 Framework 8 Typological versus Population-Based Thinking 25 Contemplating a History 11 Thing 25 Large versus Small Differences 25 Morphology and Embryology in the 19th Nucleus versus Cytoplasm 26 Century 13 BOX 1.2 FISHER'S ARGUMENT ON THE IMPORTANCE OF Darwin's "Revolution" 19 MUTATIONS OF SMALL VERSUS LARGE EFFECT 27 The Fractured Mirror: Biology between Personalities 28 1900 and the 1930s 22 Evolutionary Developmental Biology 31 Summary 34 2 Information Sources for Reconstructing Developmental Evolution: I. Fossils 35 Introduction: Two Kinds of Evidence 35 Identifying Changes in Developmental The Essentiality of Fossil Evidence 37 Processes: Examples from Dinosaur Evolution 51 BOX 2.1 ON GEOCHRONOLOGY AND STRATIGRAPHY 39 BOX 2.2 TERMINOLOGICAL SHIFTS IN THE MEANING OF HETEROCHRONY 54 Expanding the Known Universe of Devel- Fol Ev e ad te Eln opmental Evolutionary Events 41 opmental Evolutionary Events 41 FOssil Evidence and the Elucidation of "Novelties" 57 Phylogenetic Reconstruction 42 BOX 2.3 KEY INNOVATIONS 61 Phylogenetic Systematics 42 S Summary 64 Cladistics, Fossils, and the Mapping of Events 46 3 Information Sources for Reconstructing Developmental Evolution: II. Comparative Molecular Studies 65 Introduction: Tracing Genetic Changes in Direct Development and the Overthrow of a Development 65 Long-Held Supposition 80 Gene Evolution and Developmental Evolu- Direct Development as a Window on tion: A Complex Set of Relationships 66 Mechanisms of Early Embryogenesis 81 The Analytical Problem: Identifying Ortho- Charting the Changes in Genetic Circuitry 85 logues 67 The Craniate Head: Reconstructing the The Substantive Issue: Changing Gene Cellular and Genetic Sources of an Functions in Evolution 67 Evolutionary Novelty 87 BOX 3.1 GENE DUPLICATIONS AND GENE FAMILIES 68 Comparative Anatomical Studies 91 The Analytical Opportunity: Molecular Gene Expression Studies 91 Clocks 71 Genetic Bases of the Evolutionary Elaboration Direct Development in Sea Urchins and of Structure 96 Frogs: Mapping Evolutionary Changes Summary 98 in Early Development 71 4 Genetic Pathways and Networks in Development 99 Introduction: Developmental and Genetic Pathway Analysis: The Perils of Pathways 99 Simplicity 114 Biochemical Pathways: From Garrod to Functional Redundancy 114 Beadle and Ephrussi 101 Pleiotropy 117 Developmental Pathways: Waddington's Cautionary Notes in Thinking about Genetic Contribution 105 Pathways 118 Microbial Genetics and the Birth of Satura- From Pathways to Networks 118 tion Mutant Hunting 108 Does the Genetic Pathway Concept Apply Genetic Pathways for Pattern Formation Only to Highly Canalized Systems? 122 and Sex Determination 110 Summary 125 Conserved Genes and Functions in Animal Development 127 Introduction: Visible Diversity versus Dorso-Ventral Patterning 137 Shared Genetic Identities 127 Conservation of Genes and Gene Function Hox Genes and Antero-Posterior in the CNS 141 Patterning 129 BOX 5.1 ECTOPIC EXPRESSION 144 Gene and Cluster Size 135 Conservation of Genes and Gene Functions Cluster Number 135 in Heart and Eye Development 145 Gene Order and Content 136 Conserved Heart Development Genes 145 Developmental Roles 136 Pax6 and the Evolution of Eye Structures 148 Master Control Genes: Pax6 as a Test Case Dissociating Gene Controls and 150 Morphological Evolution: Mechanisms for Conservation of Role that The Problem of Homology 165 Permit the Acquisition of New Implications for Reconstructing the Urbilaterian Functions 155 Ancestor 168 Summary 168 PART II: CASE STUDIES IN PATHWAY EVOLUTION 171 6 Evolving Developmental Pathways: I. Sex Determination 173 Introduction: Sex Determination How Might the Drosophila Sex Determina- Systems 173 tion Pathway Have Originated? 192 BOX 6.1 THE DIVERSITY OF GSD SYSTEMS 175 Is There a Universal Downstream Control Two Hypotheses about the Evolution of Gene for Sex Determination in the Sex Determination Pathways 176 Bilaterian Metazoa? 200 Comparative Information on Sex The Rapidity of Evolution of Sex Determination Pathways 183 Determination Genes 202 Sex Determination in Mammals 183 BOX 6.3 MIGHT MINOR SECONDARY ROLES OF SEX DETERMINATION GENES CONTRIBUTE TO THEIR RAPID Sex Determination in Insects 190 MOLECULAR EVOLUTION? 203 BOX 6.2 MOLECULAR TESTS OF DIFFERENTIAL Summary 204 SPLICING 190 7 Evolving Developmental Pathways: II. Segmental Patterning in Insects 205 Introduction: Pattern and Process 205 BOX 7.1 RELATIONSHIPS BETWEEN PAIR-RULE AND EVERY-SEGMENT EXPRESSION PATTERNS 236 Developmental Biology of Segmentation in EVERY-SEGMENT EXPRESSION PATTERN 236 Drosophila 207 Extracting Some General Conclusions 240 Molecular Genetics of Segmental Pattern- The Diversity of Pair-Rule Promoter ing in Drosophila 210 Structure: Evidence of a Complex History 241 Strategy of Analysis 210 Strategy of Analysis 210 BOX 7.2 DISSECTING A COMPLEX PROMOTER INTO ITS General Features of the System 213 COMPONENT REGULATORY REGIONS 242 Matemal Gradients 216 Toward an Evolutionary Scenario for the The Zygotic Gene Expression Cascade 218 Origins of the Long Germ Band Comparative Data and the Evolutionary Ori- System 247 gins of the Drosophila System 225 Initial Considerations 247 Modes of Segmentation in the Insects and a An Evolutionary Scenario 248 Simple Evolutionary Hypothesis 225 Summary 253 Comparative Studies: Patterns of Conserva- tion and Some Significant Changes 228 8 Evolving Developmental Pathways: III. Two Organ Fields: The Nematode Vulva and the Tetrapod Limb 255 Introduction: Embryonic Fields 255 Experimental Characterization of Signaling The Nematode Vulva 258 Centers 280 Critical Gene Activities 282 Developmental and Molecular Biology of the Crial Gene Act es 282 C. elegans Vulva 258 Functional Tests 288 Signals in Vulval Cell Specification 261 Evolution of the Tetrapod Limb 292 Early Cell Fate Specification 264 Connections between the Genetic Comparative Studies of Vulval Development Architecture of Arthropod Appendages and Evolutionary nferences 266 and Vertebrate Limbs: What Do and Evolutionary 266 They Signify? 298 The Tetrapod Limb 273 They Signify? 298 The Tetrapod Limb as Evolutonary T ouc- Parallels in the Construction and Evolution The Tetrapod Limb as Evolutionary Touch- of the Nematode Vulva and the Tetra- stone 273 of the Nematode Vulva and the Tetra- ston 23 .r. , ,n , pod Limb 302 Basic Cellular and Developmental Biology of the Tetrapod Limb 278 Summary 304 PART III: CONUNDR UMS 307 9 Genetic Source Materials for Developmental Evolution 309 Introduction: Gene Recruitment 309 The Evolution of Sequence Diversity and New Categories of Genetic Variation 313 Functons within the Hox Genes 333 Primary Recruitment Events and Promoter Gene Duplication and Stabilization of Devel- Primary Recruitment Events and Promoter ^ ^ 338 Evolution 316 opmental Roles 338 Evolution 316 Polyploidy as the Extreme Version of Gene Mutation in, and Evolution of, Promoter Duplication 345 Sequences 316 Gene and Genome Duplications as Resources Examples of Enhancer Mutations that Alter for Genetic Pathway Evolution 347 Development 323 A Note on Modularity and Entrainment, or Creation of New cis-Acting Enhancer Sites for What the Classic Neo-Darwinian View Transcriptional Control 324 Missed 348 Multiplying Resources for Gene Recruitment: Hiding and Sorting Variation: Canalization Gene Duplications and the Growth of and Genetic Assimilation 350 Gene Families 327 Processes that Shape Gene Family Evolution 329 Costs and Constraints: Factors that Retard u1 and Channel Developmental Evolution 363 Introduction: The Winners' Circle 363 Enhancer Properties and Their Implications Selective Processes and Developmental for Gene Recruitment 372 Evolution 367 Partitioning the Selection Coefficient 377 Genetic Variation as a Rate-Limiting Gene Products Caught in Adaptive Conflict 379 factor in Gene Recruitment and Is There a Selective Hurdle in Initial Expression Developmental Evolution 369 of Recruited Transcription Factor Genes? 381 New Genetic Variation as Rate-Setter of Physical, Physiological, and Developmental Evolutionary Change? 369 Constraints 383 Gene Recruitment: Potential Costs and Summary 392 Barriers 371 1 1 On Growth and Form: The Developmental and Evolutionary Genetics of Morphogenesis 393 Introduction: The Influence of Physical Stage 3: Moving Into the Cell: The Cell Forces 393 Cycle 425 Physical Factors in Morphogenesis and the Stage 4: Charting the Complexity of Internal Roles of Gene Products 398 and External Controls of the Cell Cycle and of Cell Proliferation 427 From Matrix Products to Morphogenesis 398 of Cell Proiferaon 427 orps of Cl M : P Stage 5: Moving toward a Developmental Morphogenesis of Cell Masses: Physical Genetics of Growth Control 429 Factors and Genetic Influences 407cs of Growth Conol 429 Evolutionary Changes in Morphogenetic Synthesizing Morphometrics, Genetics, Evolutionary Changes in Morphogenetic Development, and Evolution 434 Processes 413 Development, and Evolution 434 Processes 413 Evolutionary Quantitative Genetics and Influences of Gene Products on Morphogenesis: Evolutionary Quantitative Genetics and Generalizing the Picture 415 Growth Control 434 From Morphometrics to Evolutionary BOX 111 QUANTITATIVE TRAIT LOC 435 Developmental Genetics 419 The Development of Teeth as a Paradigm of Morphological Evolution 436 Stage 1: Quantitative Analyses of Growth 420 Morphological Evolution 436 Stage 2: Allometry and Evolutionary Summary 439 Questions 422 712 Speciation and Developmental Evolution 441 Introduction: Two Linked Phenomena 441 Sexual Selection and Developmental Speciation, Reproductive Isolation, and Evolution 450 Developmental Change 444 Sexual Selection and Sympatric Speciation 450 The Allopatric versus Sympatric Intersecting Genetic Controls of Sex Determi- Speciation Debate and Developmental nation and Morphological Systems 455 Evolution 447 The Bateson-Dobzhansky-Muller Model The Genetic Basis of Species versus Larger of Speciation and a Recent Molecular Taxonomic Differences 462 Perspective 459 Microevolution and Macroevolution as Microevolution versus Macroevolution: Dynamic Processes 464 How Different Are They? 461 Summary 465 13 2Metazoan Origins and the Beginnings of Complex Animal Evolution 467 Introduction: A Few Rays of Light 467 The "Roundish Fatworm": A View from the Fossil Evidence on the Beginnings of Fossil Beds of the Neoproterozoic 494 Animal Life 470 Early Metazoans as Trochophore Larvae and the Origination of Set-Aside Cells: Dating the Origins of the Metazoa by and the Origination of Set-AsideCeUs: Dang Molecar Clock Methe Metzods 48 A View from Comparative Developmental Molecular Clock Methods 478 Biology 494 The New Molecular Phylogenetics of the Planula Larvae as the Evolutionary Platform Metazoa 482 for the Bilateria: A View from a Systematics Stages of Complexity Increase in Early Perspective 499 Metazoan Evolution 487 Summary 500 Thinking about the Origins of the Bilateria 494 '1 4 The Coming Evolution of Evolutionary J _Developmental Biology 503 Introduction: An Analytical Framework 503 Mapping Patterns of Total Gene Expression Genetic Pathways and Networks: How Change 512 Useful a Framework? 505 Quasi-Genetic Functional Tests 514' Three Major Questions for the Future 507 Searches for Fnctional Relationships between Molecules: The Two-Hybrid How Do Developmental Novelties Arise in Method 517 Evolution? 508 ~~Evolution? 508 ~BOX 14.1 THE "TWO-HYBRID" METHOD FOR How Do Microevolutionary Processes Differ DETECTING NEW FUNCTIONAL INTERACTIONS 518 from Macroevolutionary Processes? 509 Prospects for Applying Functional Tests to What Factors Determine Rates of Develop- Evolutionary Developmental Questions 519 mental Evolution? 509 Additional Departures 519 New Technologies and New Departures 510 Synthesizing Paleontology and Moleculr Detailed Promoter Comparisons of Ortholo- Genetic Studies 522 gous Genes with Different Functions 511 Summary 523 Appendix 1: Genetic Nomenclature 525 Glossary 533 Appendix 2: Reconstructing Phylogenetic References 541 History with Cladistics 527 Index 581 Appendix 3: Molecular Clocks 530