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Heterochrony the Evolution 0/ Ontogeny Heterochrony the Evolution of Ontogeny 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 M. L. McKinney, from "Jawless Fish and Hairless Apes: Ruminations from Edge of the Photic Zone" (unpublished) PREFACE In the past, the study of hetcrochrony has becn more conducive to lexicography (or even cryptography) than to improving our understanding of evolution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.
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