Table of contents for The evolution of developmental pathways / Adam S. Wilkins.


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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