Heterochrony The Evolution 0/ Ontogeny Heterochrony The Evolution of Ontogeny

Michael L. McKinney The University 0/ Tennessee Knoxville, Tennessee and Kenneth J. McNamara Western Australian Museum Perth, Western Austra/ia Australia

Springer Science+Business Media, LLC Library of Congress Cataloging in Publidation Data

McKinney, Michael L. Heterochrony: the evolution of ontogeny I Michael L. McKinney and Kenneth J. McNamara. p. em. Includes bibliographical references (p. ) and index. ISBN 978-1-4757-0775-5 ISBN 978-1-4757-0773-1 (eBook) DOI 10.1007/978-1-4757-0773-1 I. Heterochrony (Biology). I. McNamara, Kenneth. II. Title. QH395.M34 1991 91-6371 575-dc20 CIP

ISBN 978-1-4757-0775-5 © 1991 Springer Science+Business Media New York Originally published by Plenum Press, New York in I 99 I

All rights reserved

No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher We dedicate this book to our wives, Victoria M. McKinney and Susan Radford, for sharing so much of their ontogenies with ours. Preface and Preview

Many readers will have noticed the recent trend toward quotations at the beginnings of chapters in scientijic boons. Often these quotes are sappy, dippy linIe things as if the authors of the boon were strugglingfor profundity. Perhaps they want 10 give their self-indulgent esoteric musings so me hint of relevance to the rapidly deteriorating human candition, to cast a shadow of importanee over the gray wall of clinical facts to follow. Most pathetie of all is the hopeless clod who quotes himself. He is, in eIfeet, baldly stating that he Iws, with his own mind, assembled something profound, clever, or at least amusing to his fellow primates. This kind of canceit will detract from his scientijic standing. Nor should humor be attempted, at any cast; it represents a distraction to the clear , analytical thought necessary for Scientijic Progress. M. L. McKinney, from "Jawless Fish and Hairless Apes: Ruminations from Edge of the Photic Zone" (unpublished)

PREFACE

In the past, the study of hetcrochrony has becn more conducive to lexicography (or even cryptography) than to improving our understanding of evolution and development. This book is an attempt to correct that. We have tried to say, as directly as possible, what we think heterochrony is, how it works, and what role it plays in evolution. It is written for anyone (students, colleagues in any field) who has an interest in learning more about it. Thus, we have tried to organize the book in a logical, straightforward progression, used boldfaced (for primary emphasis) and italicized (for secondary emphasis) terms, and included a glossary of terms. We have tried to keep [he style informal. Parts are bound to

vii viii PREFACE AND PREVIEW

seem e1ementary to specialists in those areas, but our purpose is to integrate a broad range of information, not excavate deeply in just one area. In part, then, the book is a primer. However, a book of this nature should not only educate but also stimulate, so that, after presenting the basics, we have tried to delve into the knotty, problematic areas. [nevitably, this grades into speculation at so me points, but this is a necessary part of scientific progress; it helps point out areas of future research, if only by irritating people. The problem of course is just where speculation StopS being creative inference and becomes irresponsible nonsense. We have tried to take a moder• ate course, but it is particularly difficult in this area of research because so litde is known about major aspects of it. Yet, if science is to tie all the loose ends together, it is going to take so me creative thought. [n any case, even the developmentally informed reader is likely to find a few heresies, and surprising twists and turns in the plot that folIows. Just remember our goal is to inform and stimulate, not assert. The number of "Ioose ends" extends far beyond the " black box" of development and genes when we consider the role of development in evolution, how development can interact with ecology (affecting life history tactics and behavior, not only size and morphology), and its ultima te role in macroevolutionary patterns. How much does devel• opment " constrain" evolution? (While acknowledging that "constraint" is an overused and misleading term; e.g., why not say that selection "constrains" development?) The role of development is one of the (perhaps "the") fastest growing and most exciting areas of inquiry in evolutionary theory. As Futuyama (1988) has discussed in his presidential address to the Society for the Study of Evolution, we gready need an understanding of the origin of variation to have a complete theory of evolution. Since Darwin, the emphasis has been on selection, yet selection can obviously only act upon variation created by genes and developmental processes. With the growth of knowledge in genetics and developmental biology, it is time to examine the other side of the dialectic: how much is directionality and rate of evolution " controlled" (or the milder word, " constrained") by the production of variation. That is , how much is "internally" controlled? While this book (and others like it) addresses this, the jury is still out. We need much more empiri• cal information, especially about the dynamics of development. [n asense, this requires a shift of focus from the genetic level to the cellular (and its collective unit: the tissue) level (e .g., Buss, 1987). Cells are the basic unit of the organism, yet clearly metazoans (and metaphytes) do not consist of or develop by freely moving groups of cells. To understand why (and in what way) they do not, is to understand the dynamics of ontogeny. In this book, such a cellular approach (especially Chapter 3) is promoted. Aside from the growth of new information on development, another stimulus to the rising interest in its role in evolution is the rise of interest among evolutionists in hierar• chies. It is easy to talk about hierarchies, but people have long known (at least implicitly) that complex phenomena have levels, each with emergent properties. It is only by learning the specifics of those emergent properties that we can create a theory of evolu• tion that will do what truly complete theory must do: und erstand the connections (or, interactions) among the levels in the hierarchy. The amactive thing to us (and, perhaps, many others) is that the "properties" of development are at an intermediate level which allows such linkage: above the genes but below the individual organism interacting with its ecosystem. PREFACE AND PREVIEW ix

PREVIEW

We begin (Chapter 1) with an overview of the history of ideas about heterochrony. This is followed (Chapter 2) bya discussion of what heterochrony is: how does one classify and analyze it? We hope that many who have been "turned off" by the past profusion of terms will be helped by our approach. In particular, we use bivariate graphs (both size-shape and size-age) as heuristic lOols; these are also useful in distinguishing be• tween age-based and size-based heterochrony. This encompasses the key relationship between allometry and heterochrony. We also consider a number of problems, such as determining ontogenetic age and dealing with noncomparable ontogenetic stages. After introducing such basic terms and ideas in Chapter 2, Chapter 3 attempts lo answer the question of what causes heterochrony. This is a much more difficult question than has often been implied. Obviously, genetic changes are the ultima te cause but concepts such as " rate" and " timing" genes have been greatly oversimplified. There are many kinds of "regulatory genes," at many levels in a regulatory hierarchy, in which not only develop• mental, but also many other kinds Ce.g., physiological) of genes and processes are regu• lated. Further, many heterochronic genes are not " programmed" lo regulate the "rate" of developmental processes but can affect them indirectly, by changing the flow of information via (e.g.) change in structural parameters. When we turn lo the cellular (tissue) levels of heterochronic causation (also Chapter 3), we find that here loo there has been much oversimplification. In particular, "heter• ochrony" in the past has been limited lo late-stage allometric (size-shape) changes in ontogeny. Because of this, heterochrony has been little more than a " taxonomy" of patterns rebting simple shape changes between ancestral and descendant ontogenies. Yet, we show [extending the earlier work of Hall (1983, 1984)J that the same kinds of rate/timing changes, when occurring earlier in ontogeny, can cause radical changes in morphology, by changing the time of tissue induction, to create new tissues, eliminate old ones, or just change tissue configuration. This kind of heterochrony we call "differ• entiative heterochrony" to denote its occurrence before differentiation. Later, more traditional kinds are called "growth heterochronies." Again, we use heuristic tools to illustrate the concepts, this time in the form of morphogenetic trees to represent develop• ment as cellular assembly with shared, then diverging, histories. In keeping with the cellular view, heterochrony in this light is redefined as change in rate or timing of cell dialogues. Thus, we spend so me time on biochemical media tors and other aspects of how cells communicate, and how changes in this communication can occur (often, not by change in the usual "rate/timing" genes, as noted). In Chapter 4, we leave the classification and mechanisms of ontogenetic change (i.e., the production of variation) and begin to examine how that variation is acted upon. We say " begin" because this is a transitional chapter in that environment is seen not only as a "sieve " selecting intrinsically produced variation, but also as acting directly upon onrogeny to cause heterochronic variation itself. This is an often neglected aspect of heterochrony (indeed of ontogenetic variation per se): that variation (e.g., ecopheno• typic plasticity) is directly " shaped" by the environment, and not totally programmed by the genes. Thus, we discuss heterochronic variation that is produced by a variety of environmental stimuli, and some different ways that development can be labile. (Indeed, x PREFACE AND PREVIEW

selection can act to favor lability itself.) Thus, there are at least three somewhat often• neglected points underlying this chapter: (1) that developmental variation can be di• rectly created by the environment, (2) that such nonprogrammed variation can be selected for, and (3) heterochronic variation is incremental. This last point is empha• sized because heterochrony has had a long (and not very rewarding) association with saltations (because of Goldschmidt and others) and many are not used to thinking in terms of intrapopulational polymorphisms being heterochronic variants (we call them "heterochronic morphotypes"). Yet, such variantsare often produced by minor rate and timing changes (e.g., sexual dimorphism as an extreme intrapopulational example that results from heterochronic differences). In Chapter 5, we turn to the broad view, that of evolutionary patterns produced by the interaction between the environment and ontogeny. Like any change, evolution has two basic parameters, direction (space) and time (rate), and we spend much of this chapter on them. After an initial section on the methods of evolutionary reconstruction (especially determining phylogenetic polarity), we show how directionality has been ("strongly" ?, a relative term for now) influenced by the " intrinsic" forces of ontogeny. At the core of this documentation is McNamara's key concept of the " heterochrono• cline," which provides some of the best direct empirie al evidence on how ontogenetic change is reflected in evolutionary patterns. We show, in a number of lineages, that ontogenetic trairs (morphologically, both "Iocal" and "global") are often modified in systematic, clinal patterns ac ross distinct environmental (spatial) and temporal vectors. We discuss a number of different types of such clines and their utility in characterizing and explaining evolutionary patterns. We then turn to the role of heterochrony in affect• ing rates, suggesting that, for the most part, heterochronic variations are minor, as already noted. But "saltations" are still areal possibility. Finally, we focus on the agents of selection on heterochronic variations of all kinds. In particular, predation seems to have been a major force driving the formation of heterochronoclines. The often problematic issue of targets of selection is the general subject of Chapter 6. Specific targets we discuss are size, shape, and life history (in Chapter 7, we discuss a fourth target: behavior) . Heterochrony affects all of these, and because rate and timing changes often change coadapted suites in the ontogeny, it is often unclear whether some traits change because they are actually under selection, or just part of a coadapted suite where selection is acting only on so me traits in the suite. for instance, how often is body size change an incidental by-product of selection for life history tactics (e.g., early maturation)? Or change in shape a result of allometric extrapolation for body size change? Such questions are really at the heart of the constraint debate because they directly ask how " easily" traits can be decoupled from one another. If they are easily decoupled, then developmental constraint is much less than if trait suites are " Iocked in" and traits are often " dragged along" in spite of neutral or even negative selection. Rhetoric about " constraints" aside, such questions are best answered by the direct methods of quantitative genetics as applied to selection response experiments in living animals [see especially Cheverud (1984) and Riska (1989) I. Also in Chapter 6, we note that targets often change through time. Heterochronically speaking, this broaches the topic of whether groups show more peramorphosis ("overdevelopment") or paedomor• phosis C'juvenilization") through time. Again, there are insufficient data to draw com- PREFACE AND PREVIEW xi

pie te conclusions, but there is strong evidence that the relative frequency of pera- to paedomorphosis varies among groups (perhaps because of differences in developmental programs) and through time within the same group. Having aseparate chap.rer, Chapter 7, on behavioral and human heterochrony may seem a little anthropocentric, this being a book written by hominids. However, there are at least two good reasons for it. One, the study of the evolution of behavior has often neglected the ontogenetic view even though it is now clear that such a view can be invaluable. Behavior, like morphology and life history, not only undergoes predictable ontogenetic change, but these changes occur as coadapted suites (of component behav• iors). Furthermore, such suites are amenable to heterochronic changes among and within the suites, so that a descendant adult may have behaviors present only in the ancestral juvenile (paedomorphosis). Yet, this approach is only just now being systemati• cally taken [lrwin's (1988) study is something of a groundbreaking workJ . A second reason for this chapter is that human heterochrony has been the locus of a great number of rtlisconceptions. Indeed, it is almost a proxy for all the gibberish gener• ated in the study of heterochrony writ large. There is far too much to go into here but the major point is that humans are not neotenie apes. That humans are neotenie is one of the most widely circulated bits of misinformation in both the seientific and popular litera• ture. Neoteny is the process of growing slower. Yet humans do not grow particularly slow (relative to either the chimp or our aneestors, as is now being diseovered with growth lines on fossil hominid teeth). What we do is delay the offset of virtually all developmen• tal events (growth phases) so that we are in each phase longer. This is hypermorphosis (we call it "sequential" hypermorphosis because a number of sequential phases are affected) . The key point is that the time spent in a growth phase is distinct from the rate of growth in it. The lack of this distinction is one of the main reasons for the confusion, sueh that people speak ofhumans having a "slowed" maturation; yet such events (or any single event) is not "slowed," it is delayed (or early, depending on the change). Another reason for this " neotenous" misconception is our superficial resemblance (as adults) to a juvenile chimp (especially the skulI). The problem here is that such a superficial, subjec• tive shape criterion is often not a good basis of ontogenetic eomparison. In this case, our " chimplike" shape results from a gready enlarged brain (via hypermorphosis, or pro• longed brain growth), eombined with a number of probably complex growth field changes in the jaw and facial area. Thus, to get the "complete" heterochronic story, investigators should look at developmental events of component growth fields . As Atch• ley (1987) has said, each organ may often be best looked at as having its own ontogeny. In shon, hypermorphosis seems to best explain most of those traits that make us human: large body size, large brain, long learning stage and life span, although there are also a number of morphologically " local" nonhypermorphic growth field "adjustments" (as expected, given the novel pressures of cultural adaptations). We also attempt to re la te heterochrony to various aspects of race, sex, and human behavior. This last is obviouslya difficult prospeet, contrary to Montagu' s (1981) attempt to "explain" dance, song, trustworthiness, and virtually everything else in terms of " neoteny. " In the penultimate chapter, Chapter 8, we take on the broad view of ontogeny in evolution. This is more than just a synthesis of the major ideas and themes of the other chapters, because still other ideas and themes emerge when these are combined (syner- xii PREFACE AND PREVIEW

gistically). After some theoretical soul-se are hing (on why development is becoming a focus of interest), we discuss the evolution of constraint. The message is that, despite all the talk about constraint in evolution, few workers explicitly point out that constraints themselves evolve. We try to show that, because evolution often "builds upon" preexist• ing ontogenies, developmental contingencies accumulate, increasing constraint through evolutionary time. [Levinton (1988) calls this the "evolutionary ratchet."J This "harden• ing" has a number of implications that we discuss at length. The major ones are that, as "hardening" increases, the role of intrinsic processes in evolutionary directionality and rates diminishes. However, this is somewhat misleading in that, as "hardening" evolves, there is a simultaneous decrease in the number of directions that evolution can go. In a sense, in accumulating the (ontogenetically and phylogenetically) early contingencies, intrinsic processes have already determined the basic trajectory of the biosphere's evo• lution. Indeed, one might say that the biosphere itselfhas become " hardened" in that, as contingencies within its components ("ontogenies") accumulated, so have the interac• tions (contingencies) among those components. More recent, mainly environmentally selected ("extrinsic") ontogenetic contingencies are mostly minor permutations on the basic architecture of the earth's biota. Superficially paradoxical is that, at the same time that directionality is diminished via "hardening," evolutionary rates are increasing. That is, there is more change (in ontogenies) going on, but the change is more minor because the accumulation of ontogenetic contingencies makes viable "jumps" less feasible. This is due to what might be called "the first law of evolving complex systems": the more parts there are, the more there are to change, but the (relatively) less important each local change is (being smaller relative to a larger whole). This kind of positive feedback has been elegantly described in DeAngelis et al. (1986). The bottom line is that, while the debate rages on over the "intrinsic versus extrin• sic" control of evolutionary directions and rates, the relative role of each has changed. Intrinsic control is diminished, but only after having "set" much of the trajectory, often via rapid rates. Incidentally, none of this requires the now-discarded process of "recapit• ulation via evolution by terminal addition." What we are pointing out is that the evolu• tion of complexity (and life) has occurred because the system has a memory, implying that earlier contingencies are conserved and built upon by later-occurring ones. This does not require that all change occur at the end of an ontogenetic process ("terminal addition "), only that earlier-occurring ones are progressively less likely to be successful land because ontogeny is a multiplicative, branching process (in many ways, not just mitosis), the odds against successful earlier changes may often go up exponentiallyJ. Obviously, all this is not to say that ontogeny has little role in directing evolution today. Even though changes in evolutionary direction and rates are not as profound as in the past, development is still more than an "on-demand parts supplier" for environmen• tal selection to operate upon. This is seen most clearly in the heterochronoclines of McNamara where heterochronic variants grade into evolutionary lineages. Perhaps the most dramatic role for development is in the origin of such lineages (and clades) where paedomorphosis and peramorphosis playa role in "innovation." (We give a number of reasons why, contrary to de Beer's assertions and "common widsom," paedomorphs do not generally have more evolutionary potential than peramorphs.) We try to work such innovation into a general theory of ontogeny and ecology by combining it with paleonto- PREFACE AND PREVIEW xiii logical observations, such as nearshore origination of most major clades, and ecological observations, such as that r-selection (e.g., nearshore, unstable regimes) may select for certain kinds of heterochrony [e .g., progenesis (early offset of growth) producing small size and early reproduction]. The subsequent diversification into more stable, offshore environments is often accompanied by larger body size, increased longevity, and other K-selected traits produced by the heterochronic mechanism ofhypermorphosis (delayed offset of growth). The attraction of such a general theory is that it not only links genes, cells, development, and ecology into an evolutionary framework, but also includes aspects of development often overlooked. Thus, aside from selection on the ontogeny of morphology (size and shape), it is able to take in the ontogeny oflife history events (e .g., maturation, death), and behavior. Whether our proposed, specific scenarios are correct is less important than that they are testable, especially by modem ecologists (e.g., Ebenman and Persson, 1988). One intriguing (and perhaps partly fanciful) notion to follow from such a theory is that heterochrony is a way of scaling the timing of intrinsic (ontogenetic) events to the tempo of extrinsic ones. This leads to a discussion of intrinsic time and, perhaps surprisingly, body size, which may often turn out to be a good esrima• tor of intrinsic rime.

READER COMMENTS AND ACKNOWLEDGMENTS

Comments

We consider this book as something of a "status report" and would greatly appreci• ate comments (positive or negative) by any readers, students, and colleagues alike. Should there be enough interest to justify a revised edition, this will help us to improve it. Chapters 1,4, 5, and 6 (except body size and some life history text) were written mainly by McNamara and comments on those might best be sent to hirn. McKinney wrote Chapters 2, 3, 7,8, and 9, (body size, life history in Chapter 6), the Glossary, and the (probably too-long) Preface and Preview.

Acknowledgments

We would like ro thank the following people (in no particular order) for kindly reading drafts of chapters (in one version or another) of this book and offering their comments: Brian Hall (Dalhousie University), Brian Shea (Northwestern University) , John Gittleman (University of Tennessee), Si mon Conway Morris (Cambridge Univer• sity), Jim Hanken (University of Colorado), Brian Tissot (Oregon State University), Neil Blackstone (Yale University), Michael Green (University of Tennessee), and Bill Calder (University of Arizona). As always, this does not mean they agree with the end product. In addition, K.j.M. wishes to thank the following: Alex Baynes for help with literature and provision of computer facilities . The Department of Geology, University of Western Australia, is thanked for computer suPPOrt, especially Drs. Nick Rock and David Haig. xiv PREFACE AND PREYlEW

Drs . William Peters (mayllies) and Alan Rayner (fungi) supplied information in their fields of expertise. Kris Brimmel of the Western Australian Museum assisted with some of the diagrams. Special thanks to Susan Radford for her encouragement and support. M.L.M. would like to thank Dan Frederick and Tony Tingle , University ofTennessee, for assistance with some figures and photography. Ken and I also thank the nice people at Plenum Publishing who helped us turn amorphous thoughts and back-of-the-envelope sketches into something fit for public consumption: Amelia McNamara, Mariclaire Cloutier, and the highly professional pro• duction staff. Finally, Ken and I would both like to thank our small children for permit• ting us to work on the book when they were at school, out playing, or otherwise had no need for uso

Michael L. McKinney Knoxville, Tennessee Contents

Chapter 1 Heterochrony: A Historical Overview

1. Introduction 2. Von Baer and the Naturalphilosophie School 2 3. Haeckel and the Biogenetic Law 4 4. Garstang. de Beer. and the Modern Heterochronic Synthesis 9

Chapter 2 Classifying and Analyzing Heterochrony 1. Introduction 13 2. Age-Based Views of Heterochrony 14 2.1. Clock Model 14 2.2. Three-Dimensional Model 16 2.3. Review of Heterochronic Terms 17 2.4. Two-Dimensional Model 18 2.5. Summary 19 3. Finer Points and Problems 21 3.1. Problem of Shape and Size 21 3.2. Trait Veccors and the Problem of Noncomparable Traits 25 3.3. Problem of Complex Growth Curves and Sequential Heterochrony 27 3.4. Problem of Determining üntogenetic Age 30 3.5. Problem of Determining Phylogeny 31 3.6. Problem of Determining Heritability of Changes 31 3.7. Nomenclatural Misconceptions 32 4. Size- Based Heterochrony 33 4.1. Bivariate Allometry 34 4.2. Relating Allometry co Heterochrony 36 4.3. Allometric Heterochrony 40 4.4. Multivariate Allometry 41

xv xvi CONTENTS

Chapter 3 Producing Heterochrony: Ontogeny and Mechanisms of Change

1. Introduction 47 1.1. Development as Self-Assembly of Cells 48 1.2. Preview and Outline of Chapter 49 2. Ontogeny: A Brief Sketch 49 3. Heterochrony: Change in Rate or Timing of Ontogeny 55 3.1. Growth Heterochronies 55 3.2. Differentiative Heterochronies 61 4. Biochemical Mediators of Heterochrony 72 4.1. Extracellular Mediators 72 4.2. Intracellular Mediation 75 4.3. Comparison of Extra- and Intracellular Mediation 76 4.4. Cell Adhesion and Heterochrony 77 5. Genetics of Heterochrony 78 5.1. A Proposed Hierarchy of Gene Regulation: Three Basic Levels 79 5.2. Genetics and Heterochronies of Mosaic Development 83 5.3. General Discussion of Genes and Heterochrony 84 6. Summary: Branching Morphogenetic Trees 86 6.1. Trees and Growth Heterochronies (Late Ontogeny) 89 6.2. Trees and Differentiative Heterochronies (Early Ontogeny) 92 6.3. Summary: Allometric and Disjunctive Heterochronies 92 7. Hierarchies and Heterochrony 95 7.1. Basic Hierarchical Principles as Applied to Ontogeny 95 7.2. Hierarchy and Process Rates 97 7.3. Hierarchy: Overview 98

Chapter 4 Heterochronic Variation and Environmental Selection

1. Introduction 99 2. The Nature of Phenotypic Variation 101 3. Extrinsic Factors Inducing Heterochronic Change 103 3.1. Phenotypic Modulation 103 3.2. Temperature as an Extrinsic Factor 106 3.3. Developmental Conversion 109 3.4. Evolutionary Significance of Extrinsic Perturbations to the Developmental Program IH 4. Selection and Intrinsically Produced Heterochrony 118 4.1. Intrinsically Produced Heterochrony 119 4.2. Selection and Heterochrony: A Case Study 122 4.3. Selection, Heterochrony, and Sexual Dimorphism 125 5. Conclusions 129 CONTENTS xvii

Chapter 5 Heterochrony in Evolution: Direction, Rates, and Agents

1. Introduction 133 2. Assessing Polarity in Heterochrony 135 2.1. Introduction 135 2.2. The Ontogenetic Method 135 2.3. The Outgroup (or Cladistic) Method 136 2.4. The Paleontological Method 139 2.5. Application of Both Outgroup and Paleontological Methods 143 3. Heterochrony and the Direction of Evolution 146 3.1. Introduction 146 3.2. Heterochrony and the Generation of Evolutionary Trends 149 3.3. Dissociated and Mosaic Heterochronoclines 157 3.4. Heterochronoclines and Environmental Gradients 161 4. Heterochrony and Rate;; of Evolution 168 4.1. Introduction 168 4.2. Morphological Saltations 169 4.3. Phyletic Gradualism 174 4.4. Macroevolution 179 5. Agents of Selection 188 5.1. Competition 188 5.2. Predation 190

Chapter 6 Heterochrony and Targets of Selection

1. Introduction 201 2. Influence of Growth Strategies 202 2.1. Differentiative versus Growth Heterochronies 202 2.2. Hierarchical Growth Strategies in Colonial Animals 204 2.3. Modular Growth Strategies in Plants 207 3. Changing Heterochronic Targets through Time 210 3.1. Intrinsic Factors Influencing Targets 210 3.2. Extrinsie Factors Influencing Heterochrony 216 4. Selection of Heterochronic Targets through Time 217 4.1. Equal Frequencies of Paedomorphosis and Peramorphosis 217 4.2. Extrinsic Factors and the Dominance of Paedomorphosis 218 4.3. Genome Size as an Intrinsic Factor in the Dominance of Paedomorphosis 220 5. Shape as a Target of Selection 225 5.1. Introduction 225 5.2. The Concept of Adaptation 230 5.3. Grades of Adaptiveness 232 xviii CONTENTS

5.4. Feeding Adaptations 235 5.5. Nonfeeding Adaptations 242 5.6. Locomotory Adaptations 251 6. Body Size as a Target of Selection 253 6.1. lntroduction 253 6.2. Size, Selection, and Trends: Distinguishing Anagenesis from Cladogenesis 256 6.3. Cope's Rule-Selection for Large Body Size 258 6.4. Adaptive Significance of Small Body Size 262 6.5. Size Change in Local Growth Fields 264 6.6. Life History Strategies 268 6.7. Fertility Selection 273

Chapter 7 Behavioral and Human Heterochrony

1. lntroduction 277 2. Heterochrony of Behavior 279 2.1. Heterochrony of "Programmed" Behavior 279 2.2. Heterochrony of Learned Behavior 283 2.3. Heterochrony and Neural Bases of Behavior 284 2.4. Behavior and Morphology 288 2.5 . Behavior, Morphology, and Life History 289 3. Human Heterochrony 291 3.1. Hypermorphosis as the Basic Human Characteristic 293 3.2. Human Life History, Brain/Behavior, and Morphology 298 3.3. lntraspecies Heterochrony: Human Races and Sexual Dimorphism 319 3.4. Selective Forces and Human Heterochrony 323 4. Coda: Heterochrony, Behavior, and Evolutionary Rates 325

Chapter 8 Epilogue and Synthesis: Ontogeny in Evolution 1. Development and Evolutionary Theory 327 1.1. A Rebirth of lnterest 327 1.2. The Possible Importance of Development in Evolution 328 1.3. Heterochrony and Those "Emergent Rules" 330 2. The Evolution of Constraint 334 2.1. Developmental lnertia and Directionality of Biosphere Evolution 334 2.2. The Evolution of Evolutionary Rates 341 2.3. Summing Up: Evolution of Constraint 343 3. Heterochrony and Clade Diversification 344 3.1. Paedomorphs: Not Necessarily the Best Ancestors 345 3.2. Small Organisms: The Most Common Ancestors 348 CONTENTS xix

3.3. Shape, Size, Life History, and Macroevolution 349 3.4. Summary: Heterochrony and Clade Origination 354 4. Developmental, Ecological, and Evolutionary Cascades 356 5. Internal and External Time 357 6. Ontogeny, Heterochrony, and Extinction 361 7. Summary of Chapter and Concluding Remarks 362 8. Some Major Points of the Book 365

Chapter 9 Latest Developments in Heterochrony

1. Introduction 369 2. Chapter 2: Classifying and Analyzing Heterochrony 369 2.1. Age-Based Heterochrony 369 2.2. Size-Based Heterochrony 370 3. Chapter 3: Producing Heterochrony 371 3.1 . Biochemical Mediators: Growth Factor Genetics 371 3.2. Genetics of Heterochrony 372 3.3. Differentiative Heterochrony: Induction Timing and Cell Fates 373 4. Chapter 4: Heterochronic Variation and Selection 373 5. Chapter 7: Behavioral and Human Heterochrony 374 6. Chapters 5, 6, and 8: Size, Life History, and Ontogenetic Evolution 375 6.1. Life History (r-K-Stress) and Ontogeny 375 6.2. Resurrecting Recapitulation 381

Glossary of Major Terms and Concepts 383

References 393

Index 421 Heterochrony The Evolution 0/ Ontogeny