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ADAPTATION and NATURAL SELECTION a Critique of Some Current Evolutionary Thought This Page Intentionally Left Blank ADAPTATION AND NATURAL SELECTION A Critique of Some Current Evolutionary Thought This Page Intentionally Left Blank Some images in the original version of this book are not available for inclusion in the eBook. Published by Princeton University Press, 41 William Street, Princeton, New Jersey 08540 In the United Kingdom: Princeton University Press, Chichester, West Sussex Copyright © 1966 by Princeton University Press Copyright © renewed 1992 Preface to the Princeton Science Library edition copyright © 1996 by Princeton University Press All Rights Reserved Library of Congress Card: 65-17164 ISBN 0-691026-157 The paper used in this publication meets the minimum requirements of ANSI/NISO Z39.48-1992 (R1997) (Permanence of Paper) First Princeton Paperback printing, 1974 Eighth paperback printing, and first printing for the Princeton Science Library, with new preface, 1996 http://pup.princeton.edu This Page Intentionally Left Blank Contents PREFACE (1996) ix PREFACE xv 1. INTRODUCTION 3 Evolutionary adaptation is a special and onerous con- cept that should not be used unnecessarily, and an effect should not be called a function unless it is clearly produced by design and not by chance. When recog- nized, adaptation should be attributed to no higher a level of organization than is demanded by the evidence. Natural selection is the only acceptable explanation for the genesis and maintenance of adaptation. 2. NATURAL SELECTION, ADAPTATION, AND PROGRESS 20 Natural selection can be effective only where there are certain quantitative relationships among sampling er- rors, selection coefficients, and rates of random change. The selection of alternative alleles in Mendelian popula- tions meets the requirements. Other conceivable kinds of selection do not. Selection of alternative alleles works only with an immediate better-vs.-worse among individ- uals in a population, and the question of population survival is irrelevant. Once a certain level of complexity is evolved, selection will maintain adaptation by occa- sionally substituting one adaptive character for another, but this will not result in any of the kinds of cumulative progress that have been envisioned. V CONTENTS 3. NATURAL SELECTION, ECOLOGY, AND MORPHOGENESIS 56 The gene is selected through a complex interaction with its environment, which can usefully be considered to include several levels: the genetic, the somatic, and the ecological. The ecological has many aspects, one of which, the "demographic," is given special treatment. Age-specific birth rates and death rates are important factors in the selection of developmental rates and other aspects of life cycles. The importance of genetic assimi- lation as a creative factor is minimized. 4. GROUP SELECTION 92 Selection at the genie level can produce adaptive organ- ization of individuals and family groups. Any adaptive organization of a population must be attributed to the selection of alternative populations. Reasons are ad- vanced for doubting, a priori, the effectiveness of such group selection. Organic adaptations, which function to maximize the genetic survival of individuals, are distin- guished from biotic adaptations, which would be de- signed to perpetuate a population or more inclusive group. 5. ADAPTATIONS OF THE GENETIC SYSTEM 125 Phenomena relating to the genetic system, such as dominance, diploidy, sex-determining mechanisms, and the distribution of sexual and asexual reproduction in life cycles are easily explained as short-term organic adaptations. The survival and evolution of groups are fortuitous consequences of these adaptations and of their occasional malfunctioning, as in mutation and introgression. There is no respectable evidence of mech- anisms for maintaining evolutionary plasticity or of any other biotic adaptations of the genetic system. vi CONTENTS 6. REPRODUCTIVE PHYSIOLOGY AND BEHAVIOR 158 Variations in the intensity of reproductive effort, and in the manner in which it is expended, seem designed to maximize the reproductive success of the reproduc- ing individuals. Attention is given to the evolution of fecundity, viviparity, gregarious reproduction, and dif- ferences between the sexes in reproductive behavior. These phenomena support the conclusion that the goal of an individual's reproduction is not to perpetuate the population or species, but to maximize the representa- tion of its own germ plasm, relative to that of others in the same population. 7. SOCIAL ADAPTATIONS 193 Selection within a population can lead to cooperative relations among closely related individuals, because the benefits of cooperation would go mainly to individuals with the genetic basis of cooperation, rather than to those of alternative genetic makeup. Selection at the genie level thus explains insect societies and analogous developments in other organisms. Other apparent ex- amples of altruism are explained as misplaced parental behavior. They represent imperfections in the mecha- nisms that normally regulate the timing and execution of parental behavior. Benefits to groups often arise as in- cidental statistical consequences of individual activi- ties, just as harmful effects may accumulate in the same way. 8. OTHER SUPPOSEDLY GROUP-RELATED ADAPTATIONS 221 Various supposed biotic adaptations, such as poisonous flesh, senescence, and genetically heterogeneous somata, are examined and found to be spurious or inconclusive. The regulation of population size is shown to arise from individual adaptations or purely physical principles rather than as an adaptive organization of the group. vii CONTENTS Similar arguments are used against the concept of an adaptive organization of ecological communities or more inclusive entities. 9. THE SCIENTIFIC STUDY OF ADAPTATION 251 For a given biological mechanism there are no estab- lished principles and procedures for answering the question, "What is its function?" Objectively deter- mined answers to such questions would facilitate prog- ress in many fields of biology, but they must await de- velopment of special concepts for the study of adapta- tion as a general principle. Teleonomy is a suitable name for this special field of study. LITERATURE CITED 275 INDEX 291 vii i Preface (1996) MY FIRST AWARENESS of a motive for Adaptation and Natu- ral Selection came during the 1954-55 academic year while on a teaching fellowship at the University of Chi- cago. The triggering event may have been a lecture by A. E. Emerson, a renowned ecologist and termite special- ist. The lecture dealt with what Emerson termed benefi- cial death, an idea that included August Weismann' theory that senescence was evolved to cull the old and impaired from populations so that fitter youthful individuals could take their places. My reaction was that if Emerson's pre- sentation was acceptable biology, I would prefer another calling. Walking home from the lecture with my wife, Doris, I regaled her with my unhappiness about the lec- ture and proposed the obvious idea that selection among individuals in any population would be biased in favor of the young, as long as the likelihood of living to age x was greater than to age x + 1. A broader dissatisfaction arose from what seemed to be a pervasive inconsistency in the use of the theory of natural selection. Formal presentations of this theory dealt with genetic variation among individuals in a population. Whatever features assisted individuals in their efforts to survive and reproduce would come to characterize the population. No other factor that could produce adaptive change was ever proposed. Yet the adaptations recog- nized by professional biologists—Emerson, for example— often related to the group as such, and often required ix PREFACE (1996) individual members to jeopardize their own interests for group welfare. Emerson's proposal that individuals adaptively died for the benefit of the population was a typical example. The simple textbook form of the theory of natural se- lection was not in fact the only version available. Emerson himself had proposed that selection must operate not only among the individuals of a population, but also among alternative populations (Allee et al., 1948: 664). Others had made the same suggestion, but these were rare ex- ceptions that I had never encountered. I doubt that many of the biologists proposing that there were adaptations for the benefit of the species had them in mind. Two publications that I read that year were also of great importance to me, and may have deterred me from some alternative career. One was Shaw and Mohler's brief article on sex ratio (1953). The other was David Lack's chapter in Huxley, Hardy, and Ford (1954). Shaw and Mohler's superb work went largely unnoticed until it was discovered by Charnov (1982), who made the Shaw- Mohler equation a focal concept for his broad treatment of sex allocation. Shaw and Mohler led me to Shaw's Ph.D. dissertation, which elaborated the key ideas more fully, and which I cited in the book. Right from its open- ing paragraph, Lack's "The Evolution of Reproductive Rates" was a sublime encouragement. I had found a bi- ologist who believed, as decisively as I did, that natural selection is a real scientific theory. It logically predicts that there are certain sorts of properties that organisms must have, and others, such as adaptations for the "benefit to the species" (Fisher, 1958: 49-50) that they could not possibly have. When I was writing the manuscript in the early 1960s, I was convinced of the validity of my position, else why would I have taken the trouble? I was
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