STEPHEN JAY GOULD The Structure Of Evolutionary Theory ______________________________ THE BELKNAP PRESS OF HARVARD UNIVERSITY PRESS CAMBRIDGE, MASSACHUSETTS AND LONDON, ENGLAND

Copyright �� 2002 by the President and Fellows of Harvard College All rights reserved Printed in the United States of America Library of Congress Cataloging-in-Publication Data Gould, Stephen Jay. The structure of evolutionary theory / Stephen Jay Gould. p. cm. Includes bibliographical references (p. ) ISBN 0-674-00613-5 (alk. paper) 1. Evolution (Biology) 2. Punctuated equilibrium (Evolution) I. Title. QH366.2.G663 2002 576.8���dc21 2001043556 Sixth printing, 2002

__________________________________________ For Niles Eldredge and Elisabeth Vrba May we always be the Three Musketeers Prevailing with panache From our manic and scrappy inception at Dijon To our nonsatanic and happy reception at Doomsday All For One and One For All

Contents Chapter 1: Defining and Revising the Structure of Evolutionary Theory 1 Part I, Chapters 2-7 The History of Darwinian Logic and Debate 91 Segue to Part II 585 Part II, Chapters 8-12 Towards a Revised and Expanded Evolutionary Theory 593 Bibliography 1344 Illustration Credits 1388 Index 1393 vii

Expanded Contents Chapter 1: Defining and Revising the Structure of Evolutionary Theory 1 ��� Theories Need Both Essences and Histories 1 ��� The Structure of Evolutionary Theory: Revising the Three Central Features of Darwinian Logic 12 ��� Apologia Pro Vita Sua 24 A Time to Keep 24 A Personal Odyssey 33 ��� Epitomes for a Long Development 48 Levels of Potential Originality 48 An Abstract of One Long Argument 53 Part I: The History of Darwinian Logic and Debate Chapter 2: The Essence of Darwinism and the Basis of Modern Orthodoxy: An Exegesis of the Origin of Species 93 ��� A Revolution in the Small 93 ��� Darwin as a Historical Methodologist 97 One Long Argument 97 The Problem of History 99 A Fourfold Continuum of Methods for the Inference of History 103 ��� Darwin as a Philosophical Revolutionary 116 The Causes of Nature's Harmony 116 Darwin and William Paley 116 Darwin and Adam Smith 121 The First Theme: The Organism as the Agent of Selection 125 ix

x Contents The Second Theme: Natural Selection as a Creative Force 137 The Requirements for Variation 141 Copious 141 Small 143 Undirected 144 Gradualism 146 The Adaptationist Program 155 The Third Theme: The Uniformitarian Need to Extrapolate: Environment as Enabler of Change 159 ��� Judgments of Importance 163 Chapter 3: Seeds of Hierarchy 170 ��� Lamarck and the Birth of Modern Evolutionism in Two-Factor Theories 170 The Myths of Lamarck 170 Lamarck as a Source 174 Lamarck's Two-Factor Theory: Sources for the Two Parts 175 The First Set: Environment and Adaptation 176 The Second Set: Progress and Taxonomy 179 Distinctness of the Two Sets 181 Lamarck's Two-Factor Theory: The Hierarchy of Progress and Deviation 175 Antinomies of the Two-Factor Theory 189 ��� An Interlude on Darwin's Reaction 192 ��� No Allmacht without Hierarchy: Weissman on Germinal Selection 197 The Allmacht of Selection 197 Weismann's Argument on Lamarck and the Allmacht of Selection 201 The Problem of Degeneration and Weismann's Impetus for Germinal Selection 203 Some Antecedents to Hierarchy in German Evolutionary Thought 208 Haeckel's Descriptive Hierarchy in Levels of Organization 208 Roux's Theory of Intracorporeal Struggle 210 Germinal Selection as a Helpmate to Personal Selection 214 Germinal Selection as a Full Theory of Hierarchy 219 ��� Hints of Hierarchy in Supraorganismal Selection: Darwin on the Principle of Divergence 224 Divergence and the Completion of Darwin's System 224 The Genesis of Divergence 232

Contents xi Divergence as a Consequence of Natural Selection 234 The Failure of Darwin's Argument and the Need for Species Selection 236 The Calculus of Individual Success 238 The Causes of Trends 240 Species Selection Based on Propensity for Extinction 246 Postscript: Solution to the Problem of the "Delicate Arrangement" 248 ��� Coda 249 Chapter 4: Internalism and Laws of Form: Pre-Darwinian Alternatives to Functionalism 251 ��� Prologue: Darwin's Fateful Decision 251 ��� Two Ways to Glorify God in Nature 260 William Paley and British Functionalism: Praising God in the Details of Design 262 Louis Agassiz and Continental Formalism: Praising God in the Grandeur of Taxonomic Order 271 An Epilog on the Dichotomy 278 ��� Unity of Plan as the Strongest Version of Formalism: The Pre-Darwinian Debate 281 Mehr Licht on Goethe's Leaf 281 Geoffroy and Cuvier 291 Cuvier and Conditions of Existence 291 Geoffroy's Formalist Vision 298 The Debate of 1830: Foreplay and Aftermath 304 Richard Owen and English Formalism: The Archetype of Vertebrates 312 No Formalism Please, We're British 312 The Vertebrate Archetype: Constraint and Nonadaptation 316 Owen and Darwin 326 ��� Darwin's Strong but Limited Interest in Structural Constraint 330 Darwin's Debt to Both Poles of the Dichotomy 330 Darwin on Correlation of Parts 332 The "Quite Subordinate Position" of Constraint to Selection 339 Chapter 5: The Fruitful Facets of Galton's Polyhedron: Channels and Saltations in Post-Darwinian Formalism 342 ��� Galton's Polyhedron 342

xii Contents ��� Orthogenesis as a Theory of Channels and One-Way Streets: the Marginalization of Darwinism 351 Misconceptions and Relative Frequencies 351 Theodor Eimer and the Ohnmacht of Selection 355 Alpheus Hyatt: An Orthogenetic Hard Line from the World of Mollusks 365 CO. Whitman: An Orthogenetic Dove in Darwin's World of Pigeons 383 ��� Saltation as a Theory of Internal Impetus: A Second Formalist Strategy for Pushing Darwinism to a Causal Periphery 396 William Bateson: The Documentation of Inherent Discontinuity 396 Hugo de Vries: A Most Reluctant Non-Darwinian 415 Dousing the Great Party of 1909 415 The (Not So Contradictory) Sources of the Mutation Theory 418 The Mutation Theory: Origin and Central Tenets 425 Darwinism and the Mutation Theory 439 Confusing Rhetoric and the Personal Factor 439 The Logic of Darwinism and Its Different Place in de Vries' System 443 De Vries on Macroevolution 446 Richard Goldschmidt's Appropriate Role as a Formalist Embodiment of All that Pure Darwinism Must Oppose 451 Chapter 6: Pattern and Progress on the Geological Stage 467 ��� Darwin and the Fruits of Biotic Competition 467 A Geological License for Progress 467 The Predominance of Biotic Competition and Its Sequelae 470 ��� Uniformity on the Geological Stage 479 Lyell's Victory in Fact and Rhetoric 479 Catastrophism as Good Science: Cuvier's Essay 484 Darwin's Geological Need and Kelvin's Odious Spectre 492 A Question of Time (Too Little Geology) 496 A Question of Direction (Too Much Geology) 497 Chapter 7: The Modern Synthesis as a Limited Consensus 503 ��� Why Synthesis? 503 ��� Synthesis as Restriction 505 The Initial Goal of Rejecting Old Alternatives 505

Contents xiii R. A. Fisher and the Darwinian Core 508 J. B. S. Haldane and the Initial Pluralism of the Synthesis 514 J. S. Huxley: Pluralism of the Type 516 ��� Synthesis as Hardening 518 The Later Goal of Exalting Selection's Power 518 Increasing Emphasis on Selection and Adaptation between the First (1937) and Last (1951) Edition of Dobzhansky's Genetics and the Origin of Species 524 The Shift in G. G. Simpson's Explanation of "Quantum Evolution" from Drift and Nonadaptation (1944) to the Embodiment of Strict Adaptation (1953) 528 Mayr at the Inception (1942) and Codification (1963): Shifting from the "Genetic Consistency" to the "Adaptationist" Paradigm 531 Why Hardening? 541 ��� Hardening on the Other Two Legs of the Darwinian Tripod 543 Levels of Selection 544 Extrapolation into Geological Time 556 ��� From Overstressed Doubt to Overextended Certainty 566 A Tale of Two Centennials 566 All Quiet on the Textbook Front 576 Adaptation and Natural Selection 577 Reduction and Trivialization of Macroevolution 579 Segue to Part II 585 Part II: Towards a Revised and Expanded Evolutionary Theory Chapter 8: Species as Individuals in the Hierarchical Theory of Selection 595 ��� The Evolutionary Definition of Individuality 595 An Individualistic Prolegomenon 595 The Meaning of Individuality and the Expansion of the Darwinian Research Program 597 Criteria for Vernacular Individuality 602 Criteria for Evolutionary Individuality 608 ��� The Evolutionary Definition of Selective Agency and the Fallacy of Selfish Genes 613

xiv Contents A Fruitful Error of Logic 613 Hierarchical vs. Genie Selectionism 614 The Distinction of Replicators and Interactors as a Framework for Discussion 615 Faithful Replication as the Central Criterion for the Gene- Centered View of Evolution 616 Sieves, Plurifiers, and the Nature of Selection: The Rejection of Replication as a Criterion of Agency 619 Interaction as the Proper Criterion for Identifying Units of Selection 622 The Internal Incoherence of Gene Selectionism 625 Bookkeeping and Causality: The Fundamental Error of Gene Selectionism 632 Gambits of Reform and Retreat by Gene Selectionists 637 ��� Logical and Empirical Foundations for the Theory of Hierarchical Selection 644 Logical Validation and Empirical Challenges 644 R. A. Fisher and the Compelling Logic of Species Selection 644 The Classical Arguments against Efficacy of Higher-Level Selection 646 Overcoming These Classical Arguments, in Practice for Interdemic Selection, but in Principle for Species Selection 648 Emergence and the Proper Criterion for Species Selection 652 Differential Proliferation or Downward Effect? 652 Shall Emergent Characters or Emergent Fitnesses Define the Operation of Species Selection? 656 Hierarchy and the Sixfold Way 673 A Literary Prologue for the Two Major Properties of Hierarchies 673 Redressing the Tyranny of the Organism: Comments on Characteristic Features and Differences among Six Primary Levels 681 The Gene-Individual 683 Motoo Kimura and the "Neutral Theory of Molecular Evolution" 684 True Genie Selection 689 The Cell-Individual 695 The Organism-Individual 700 The Deme-Individual 701 The Species-Individual 703

Contents xv Species as Individuals 703 Species as Interactors 704 Species Selection as Potent 709 The Clade-Individual 712 ��� The Grand Analogy: A Speciational Basis for Macroevolution 714 Presentation of the Chart for Macroevolutionary Distinctiveness 714 The Particulars of Macroevolutionary Explanation 716 The Structural Basis 716 Criteria for Individuality 720 Contrasting Modalities of Change: The Basic Categories 721 Ontogenetic Drive: The Analogy of Lamarckism and Anagenesis 722 Reproductive Drive: Directional Speciation as an Important and Irreducible Macroevolutionary Mode Separate from Species Selection 724 Species Selection, Wright's Rule, and the Power of Interaction with Directional Speciation 731 Species Level Drifts as More Powerful than the Analogous Phenomena in Microevolution 735 The Scaling of External and Internal Environments 738 Summary Comments on the Strengths of Species Selection and its Interaction with Other Macroevolutionary Causes of Change 741 Chapter 9: Punctuated Equilibrium and the Validation of Macroevolutionary Theory 745 ��� What Every Paleontologist Knows 745 An Introductory Example 745 Testimonials to Common Knowledge 749 Darwinian Solutions and Paradoxes 755 The Paradox of Insulation from Disproof 758 The Paradox of Stymied Practice 761 ��� The Primary Claims of Punctuated Equilibrium 765 Data and Definitions 765 Microevolutionary Links 774 Macroevolutionary Implications 781 Tempo and the Significance of Stasis 782 Mode and the Speciational Foundation of Macroevolution 783

xvi Contents ��� The Scientific Debate on Punctuated Equilibrium: Critiques and Responses 784 Critiques Based on the Definability of Paleontological Species 784 Empirical Affirmation 784 Reasons for a Potential Systematic Underestimation of Biospecies by Paleospecies 789 Reasons for a Potential Systematic Overestimation of Biospecies by Paleospecies 792 Reasons Why an Observed Punctuational Pattern Might Not Represent Speciation 793 Critiques Based on Denying Events of Speciation as the Primary Locus of Change 796 Critiques Based on Supposed Failures of Empirical Results to Affirm Predictions of Punctuated Equilibrium 802 Claims for Empirical Refutation by Cases 802 Phenotypes 802 Genotypes 810 Empirical Tests of Conformity with Models 812 ��� Sources of Data for Testing Punctuated Equilibrium 822 Preamble 822 The Equilibrium in Punctuated Equilibrium: Quantitatively Documented Patterns of Stasis in Unbranched Segments of Lineages 824 The Punctuations of Punctuated Equilibrium: Tempo and Mode in the Origin of Paleospecies 839 The Inference of Cladogenesis by the Criterion of Ancestral Survival 840 The "Dissection" of Punctuations to Infer Both Existence and Modality 850 Time 851 Geography 852 Morphometric Mode 852 Proper and Adequate Tests of Relative Frequencies: The Strong Empirical Validation of Punctuated Equilibrium 854 The Indispensability of Data on Relative Frequencies 854 Relative Frequencies for Higher Taxa in Entire Biotas 856 Relative Frequencies for Entire Clades 866 Causal Clues from Differential Patterns of Relative Frequencies 870

Contents xvii ��� The Broader Implications of Punctuated Equilibrium for Evolutionary Theory and General Notions of Change 874 What Changes May Punctuated Equilibrium Instigate in Our Views about Evolutionary Mechanisms and the History of Life? 874 The Explanation and Broader Meaning of Stasis 874 Frequency 875 Generality 876 Causality 877 Punctuation, the Origin of New Macroevolutionary Individuals, and Resulting Implications for Evolutionary Theory 885 Trends 886 The Speciational Reformulation of Macroevolution 893 Life Itself 897 General Rules 901 Particular Cases 905 Horses as the Exemplar of "Life's Little Joke" 905 Rethinking Human Evolution 908 Ecological and Higher-Level Extensions 916 Punctuation All the Way Up and Down? The Generalization and Broader Utility of Punctuated Equilibrium (in More Than a Metaphorical Sense) at Other Levels of Evolution, and for Other Disciplines In and Outside the Natural Sciences 922 General Models for Punctuated Equilibrium 922 Punctuational Change at Other Levels and Scales of Evolution 928 A Preliminary Note on Homology and Analogy in the Conceptual Realm 928 Punctuation Below the Species Level 931 Punctuation Above the Species Level 936 Stasis Analogs: Trending and Non-Trending in the Geological History of Clades 936 Punctuational Analogs in Lineages: The Pace of Morphological Innovation 939 Punctuational Analogs in Faunas and Ecosystems 946 Punctuational Models in Other Disciplines: Towards a General Theory of Change 952 Principles for a Choice of Examples 952 Examples from the History of Human Artifacts and Cultures 952 Examples from Human Institutions and Theories about the Natural World 957

xviii Contents Two Concluding Examples, a General Statement, and a Coda 962 ��� Appendix: A Largely Sociological (and Fully Partisan) History of the Impact and Critique of Punctuated Equilibrium 972 The Entrance of Punctuated Equilibrium into Common Language and General Culture 972 An Episodic History of Punctuated Equilibrium 979 Early Stages and Future Contexts 979 Creationist Misappropriation of Punctuated Equilibrium 986 Punctuated Equilibrium in Journalism and Textbooks 990 The Personal Aspect of Professional Reaction 999 The Case Ad Hominem against Punctuated Equilibrium 1000 An Interlude on Sources of Error 1010 The Wages of Jealousy 1014 The Descent to Nastiness 1014 The Most Unkindest Cut of All 1019 The Wisdom of Agassiz's and von Baer's Threefold History of Scientific Ideas 1021 A Coda on the Kindness and Generosity of Most Colleagues 1022 Chapter 10: The Integration of Constraint and Adaptation (Structure and Function) in Ontogeny and Phylogeny: Historical Constraints and the Evolution of Development 1025 ��� Constraint as a Positive Concept 1025 Two Kinds of Positivity 1025 An Etymological Introduction 1025 The First (Empirical) Positive Meaning of Channeling 1027 The Second (Definitional) Positive Meaning of Causes outside Accepted Mechanisms 1032 Heterochrony and Allometry as the Locus Classicus of the First Positive (Empirical) Meaning. Channeled Directionality by Constraint. 1037 The Two Structural Themes of Internally Set Channels and Ease of Transformation as Potentially Synergistic with Functional Causality by Natural Selection: Increasing Shell Stability in the Gryphaea Heterochronocline 1040 Ontogenetically Channeled Allometric Constraint as a Primary Basis of Expressed Evolutionary Variation: The Full Geographic and Morphological Range of Cerion uva 1045

Contents xix The Aptive Triangle and the Second Positive Meaning: Constraint as a Theory-Bound Term for Patterns and Directions Not Built Exclusively (Or Sometimes Even at All) by Natural Selection 1051 The Model of the Aptive Triangle 1051 Distinguishing and Sharpening the Two Great Questions 1053 The Structural Vertex 1053 The Historical Vertex 1055 An Epitome for the Theory-Bound Nature of Constraint Terminology 1057 ��� Deep Homology and Pervasive Parallelism: Historical Constraint as the Primary Gatekeeper and Guardian of Morphospace 1061 A Historical and Conceptual Analysis of the Underappreciated Importance of Parallelism for Evolutionary Theory 1061 A Context for Excitement 1061 A Terminological Excursus on the Meaning of Parallelism 1069 The Nine Fateful Little Words of E. Ray Lankester 1069 The Terminological Origin and Debate about the Meaning and Utility of Parallelism 1076 A Symphony in Four Movements on the Role of Historical Constraint in Evolution: Towards the Harmonious Rebalancing of Form and Function in Evolutionary Theory 1089 Movement One, Statement: Deep Homology across Phyla: Mayr's Functional Certainty and Geoffroy's Structural Vindication 1089 Deep Homology, Archetypal Theories, and Historical Constraint 1089 Mehr Licht (More Light) on Goethe's Angiosperm Archetype 1092 Hoxology and Geoffroy's First Archetypal Theory of Segmental Homology 1095 An Epitome and Capsule History of Hoxology 1095 Vertebrate Homologs in Structure and Action 1101 Segmental Homologies of Arthropods and Vertebrates: Geoffroy's Vindication 1106 Rediscovering the Vertebrate Rhombomeres 1107 More Extensive Homologies throughout the Developing Somites 1109 Some Caveats and Tentative Conclusions 1112 Geoffrey's Second Archetypal Theory of Dorso-Ventral Inversion in the Common Bilaterian Groundplan 1117