EVOLUTION NOW EVOLUTION NOW A CENTURY AFTER DARWIN EDITED BY John Maynard Smith SCHOOL OF BIOLOGICAL SCIENCES, UNIVERSITY OF SUSSEX M © Nature 1982 Softcover reprint of the hardcover 18t edition 1982 978-0-333-33595-6 All rights reserved. No part of this publication may be reproduced or transmitted, in any form or by any means, without permission. First published 1982 by NATURE in association with THE MACMILLAN PRESS LTD London and Basingstoke Companies and representatives throughout the world Typeset by Oxprint Ud, Oxford ISBN 978-0-333-33603-8 ISBN 978-1-349-86046-3 (eBook) DOI 10.1007/978-1-349-86046-3 The paperback edition of the book is sold subject to the condition that it shall not, byway of trade or otherwise, be lent, resold, hired out, or other wise circulated without the publisher's prior consent in any form of binding or cover other than that in which it is published and without a similar condition including this condition being imposed on the subsequent purchaser. CONTENTS Introduction 1 The Drigin of Life 7 The Evolution of the Genome 39 Lamarckian Inheritance and the Puzzle of Immunity 91 The Pattern of Nature 107 Evolution-Sudden or Gradual? 125 The Evolution of Behaviour 183 INTRODUCTION LUDWIG Boltzmann once wrote that the nineteenth century would be remembered as the century of Darwin. One hundred years after Darwin's death this judgement still seems perceptive. No other writer had such a profound effect on the way we see ourselves, and no other brought about so great an extension in the range of subjects which we regard as explicable by scientific theory. Here, however, I shall confine myself to his contribution to evolutionary biology, and shall forget that he was the founder of ecology and ethology, and made significant contributions to geology and psychology. It was, after all, his formulation of the theory of evolution by natural selection that was decisive. In recent years there have been daims-in the daily press, on television, and by retired cosmologists-that Darwin may have got it wrong. Some excuse can be found in the fact that Darwin has indeed been criticised by scientists working in a variety of fields-for example palaeontology, taxonomy and embryology. At least one group of scientists have daimed that a new evolu tionary paradigm is on the way. The most controversial of these issues are debated in this book. However, to see Darwinism as being under serious threat would, I think, be a false perception. The error arises because Darwin's theory is so central to modem biology that any new idea may first be seen (as Mendelian genetics was seen) as being in conflict with Darwinism. This volume presents some current controversies and recent advances in evolutionary biology, by reprinting papers published in the last few years. But let me, as a background, first give abrief history of evolutionary ideas since Darwin. In the Origin o[ Spedes, Darwin aimed to establish two things. First, he argued that evolu tion had in fact happened (that is, that all existing organisms are descended from one or a few simple ancestral forms), and, second, that the main cause of evolutionary change was the natural selec tion of variations that were in their origin non-adaptive. The main weaknesses of his position were that he had no adequate theory of genetics, and that he could give no satisfactory account 2 INTRODUCTION of the origin of the variations on which selection would later act. In genetics, Darwin was a Lamarckist. That is, he thought that if organisms acquired characteristics by use and disuse during their lifetimes, this would influence the nature of their offspring. In thinking this, he was sharing an opinion held by almost all his contemporaries. The first major advance after Darwin was made by August Weismann, who argued for the independence of the 'germ line' (the celllineage leading from the fertilized egg to the germ ceHs, egg and sperm, which form the starting point of the next genera tion) from the 'soma' (the celllineage from fertilized egg to adult body). As a boy, I acquired, from reading the preface to Shaw's Back to Methuselah, a picture of Weismann as a cruel and ignorant German pedant who cut the tails off mice to see if their offspring had tails. What a ridiculous experiment! Since the mice did not actively suppress their tails as an adaptation to their environ ment, no Lamarckist would expect the loss to be inherited. Much later, I discovered that Weismann was not as I had imagined him. His experiment on mice was performed only because, when he first put forward his theory, he was met with the objection that, (as was, it was claimed, weH known) if a dog's tail is docked, its children are often tailless-an early use of what J.B.S. Haldane once called Aunt Jobisca's theorem, 'It's a fact the whole world knows'. Much more interesting are Weismann's reasons for proposing his theory, and its implications for Darwinism. At first sight, his reasons were poor. It is often not the case (for example, in higher plants) that the germ line is a lineage distinct from the soma. Even when it is distinct, the material and energy it needs are supplied by the soma. In Weismann's day, the experimental evidence for the 'non-inheritance of acquired characters' was weak. Why, then, did he believe it? I think that the clue lies in his remark that, if one were to come across.a case of the inheritance of an acquired character, it would l-e as if one were to send a telegram to China and it arrived translated into Chinese. This is the first use known to me of the information analogy in heredity. Weismann did not accept the inheritance of acquired characters because he could not conceive of a mechanism of 'reverse translation', whereby the hypertrophied muscles of the blacksmith could be translated into genes (he called them 'ids') which could, in the next generation, cause the growth of large muscIes. If Weismann was right, this greatly strengthened Darwin's theory. Natural selection, instead. of being just one of the possible INTRODUCTION 3 proeesses leading to evolutionary adaptation, beeomes the only proeess (at least, until the evolution of organisms sufficiently intelligent to learn from their parents). The next important step was the rediseovery of Mendel's laws at the start of this eentury, and the formulation of the chromo some theory of heredity. The first impact of Mendelism on evolu tionary biology was distinctly odd. The early Mendelians saw themselves as anti-Darwinians; Darwin's banner was held aloft by the biometrie school, who concentrated on measuring the correlations between relatives, and who regarded genes as meta physical entities. The Mendelians saw the 'mutations' they studied as each being the potential starting point of new species, and the continuous variation studied by the biometricians as evolu tionarily irrelevant; the biometricians saw mutations as patho logical deviants doomed to early elimination by selection, and continuous variation as the stuff of evolution. The argument, led by Bateson on the one side, and Pearson on the other, fore shadowed the current debate between punctuationists and gradualists, discussed below. It is part of the larger debate be tween those who see the world as eontinuous and those who think it proeeeds in jerks. The debate, at least in the form in which it then presented itself, was largely settled by the work of the population geneticists, Fisher, Haldane and Wright. Two points were made clear. First, the continuous variation studied by the biometricians could be explained by alternative alleles at many loci, each by itself having a small effect on the phenotype. Second, even rather small dif ferences in fitness between genotypes are sufficient to determine the direction of evolutionary change, despite mutation being mainly in an opposite direction. The work of the population geneticists prepared the way for the 'modem synthesis' of evolutionary biology, developed in the period 1930-1950 by a group including Dobzhansky, Ford, Julian Huxley, Mayr, Muller, Rensch, Simpson and Stebbins. It is hard in a few sentences to describe what these men did. In effect, they showed that the 'neo-Darwinian' mechanism-natural selection in Mendelian populations-was sufficient to explain the evolu tionary process as it could be observed in nature. Dobzhansky, Ford and others measured genetic variability and natural selec tion in wild populations. Mayr and Rensch (for animals) and Stebbins (for plants) studied geographical variation within and between species, and discussed how new species might arise. Simpson argued that the fossil record could best be understood in 4 INTRODUCTION Darwinian terms. Most research in evolutionary biology since that time has been carried out in the framework of the modern synthesis. Particular efforts have been made in areas which, at least at first sight, seem to be difficult to explain in terms of natural selection, for example, the evolution of social behaviour and of sex and breeding systems. Since 1950, developments in molecular biology have had a growing influence on the theory of evolution. The 'central dogma' of molecular biology, according to which information can pass from nucleic acid to protein, but not from protein to nucleic acid, provides a molecular explanation for Weismann's principle, thus leaving natural selection as the only agent of adaptation. Impor tant as this is, however, two additional points should be made. First, even if 'reverse translation' of amino acid sequences into base sequences were possible, this would not provide a general mechanism for Lamarckian inheritance, because most develop mental adaptations do not involve the production of new protein sequences. Second, there are good reasons why, even if living organisms have arisen independently many times in the uni verse, Lamarckian processes should playa minor role in their evolution. Most 'acquired characters' are non-adaptive--they are the results of age, injury and disease. Therefore, a hereditary mechanism which transmitted such characters to offspring would work against the evolution of adaptation. Hence the one way flow of information from nucleic acid to protein may have been a necessary feature of an hereditary mechanism able to support evolution. In physics, the second law of thermo dynamics asserts that entropy will increase in a closed physical system. In biology, Weismann's principle, together with the principle of natural selection, makes possible the maintenance, and even the increase, of information in open biological systems. Molecular biology has had an impact on evolutionary theory in other ways. Protein electrophoresis has provided a way of measuring the genetic variability of populations; its main value may be in enabling us to discover more about the breeding structure of populations. Sequence data on proteins and nucleic acids can be used to work out the phylogenetic relationships of existing organisms. In this context, sequences have the advantage over morphological data in that they provide a means of estimating the number of genetic changes separating two forms. The in formation we are acquiring about how DNA is arranged in chromosomes may at last give us some insight into the evolu tionary significance of chromosome structure. Two questions in INTRODUCTION 5 particular are being asked. First, does the large-scale arrange ment of genes on chromosomes have any significance for de velopment, or is it merely a way of ensuring accurate gene segregation during cell division? Second, does all the DNA in the genome perform some useful function in the survival or repro duction of the organism, or is some part of it 'selfish' or 'para sitic'? The second question raises a set of problems which are logically similar to those which have been debated for some time by students of the evolution of social behaviour, that is, questions about the levels at which selection acts and the differences be tween what Dawkins has called 'replicators' and 'vehicles'. There is, however, one area of molecular biology which seems to me to lag behind the rest. This is the study of the evolution of prokaryotes (organisms such as bacteria lacking a proper cell nucleus). The modem synthesis of the 1940s was concemed with eukaryotes (organisms with a cell nucleus, usually sexual and diploid). Its essential achievement was to bring together two previously separate disciplines-the chromosome theory of heredity and the study of natural populations. The same syn thesis is now required for the prokaryotes. There is an abundant knowledge of their genetics, but as yet no adequate synthesis of that knowledge with a study of the natural history ofbacteria. For example, we have little idea of the significance of conjugation for bacterial populations; it is as if we had no idea of the significance of sexual reproduction for populations of birds or insects. Popu lation thinking has been weIl developed for fully half a century, but has yet to be adopted by microbiology. The papers printed below have been grouped under six topics, each with abrief introduction aimed at doing three things. First, I explain how the topic is related to Darwin's ideas. Second, I have tried to help non-specialists to find their way through papers which are sometimes rather technical. Some of the critical tech nical terms are defined in the introductory passages, but it is inevitable that some words will be unfamiliar to some readers. Nevertheless, I would urge readers to press on regardless; it should usually be possible to grasp the gist of the argument. Finally, I have allowed myself the indulgence of expressing my own opinion on some of the more controversial issues. The selection of papers has inevitably been somewhat arbitrary. We have not aimed at reprinting just the most important papers published in recent years. Instead, we have concentrated on the more controversial fields at the expense of others in which equally valuable work is being done. Some topics have been