Biol. Rev. (2010), 85, pp. 829835. doi: 10.1111/j.1469-185X.2010.00128.

829

Natural selection then and now

Tim Lewens
University of Cambridge, Department of History and Philosophy of Science, Free School Lane, Cambridge, CB2 3RH, UK (Received 8 September 2009; revised 2 February 2010; accepted 3 February 2010)

ABSTRACT One often reads the following claims: (1) The modern conception of natural selection differs from Darwins own conception only with respect to incidental features; (2) Natural selection is a very simple idea with enormous explanatory power. Both claims are problematic. R.A. Fisher famously argued that given a particulate view of inheritance, selection could proceed in a powerful manner even with frequent crossing, small tness advantages and a low mutation rate. This is quite different from Darwins view, which (roughly translated into a modern idiom) insists on infrequent crossing, large tness advantages and a high mutation rate. The modern conception of natural selection is not the same as Darwins, unless we describe natural selection in the most abstract manner. When so described, the ability of natural selection to account for adaptation is questionable. Key words: blending inheritance, Charles Darwin, R. A. Fisher, Thomas Malthus, natural selection, struggle for existence. CONTENTS I. II. III. IV. V. VI. VII. VIII. IX. X. XI. XII. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Natural selection in On the Origin of Species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Changing understandings of natural selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The explanatory role of Malthusian struggle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The explanatory role of variation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Darwin and the Modern Synthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The explanatory role of unconscious selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cultural evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Darwins reputation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 829 830 830 831 832 832 833 833 834 835 835 835

I. INTRODUCTION Darwins anniversary year has elicited several evaluations of his contribution to scientic thought. Many have rhapsodised on natural selection. Richard Dawkins, for example, has recently written: Charles Darwin had a big idea, arguably the most powerful idea ever. And like all the best ideas it is beguilingly simple. In fact, it is so staggeringly elementary, so blindingly obvious that although others before him tinkered nearby, nobody thought to look for it in the right place. (Dawkins, 2008)
* Address for correspondence: E-mail: tml1000@cam.ac.uk.

Daniel Dennett admits that there really were large gaps in [Darwins] theory, that have only recently begun to be properly lled in (Dennett, 1995, p. 20), but this does not stop him from arriving at a verdict very similar to that of Dawkins: If I were to give an award for the single best idea anyone has ever had, Id give it to Darwin. (Dennett, 1995, p. 21). In this essay I want to clarify and explore what we might call the Darwins Dangerous Idea thesis, henceforth the Dangerous Thesis. I will certainly not be arguing that the modern conception of natural selection is conceptually awed, or that it is without explanatory power. I have no complaint with the thought that the modern conception of natural selection is a descendant of an idea put forward by Darwin. If the Dangerous Thesis asserts nothing more

Biological Reviews 85 (2010) 829835 2010 The Author. Biological Reviews 2010 Cambridge Philosophical Society

830 than this rather mild claim, then we should let it stand. Yet the Dangerous Thesis appears to involve two sub-claims, which I think are false. They are: (1) the modern conception of natural selection differs from Darwins own conception only with respect to incidental features; (2) natural selection is a very simple idea with enormous explanatory power. In opposition to these claims, I will argue that there are fundamental differences between our conception of natural selection and Darwins, and that natural selection needs to be made rather complex if it is to do explanatory work. Where Darwins conception and the modern conception differ is precisely with regard to those complexities that give natural selection its explanatory bite. These conclusions undermine the Dangerous Thesis, but they do nothing to undermine Darwins standing. On the contrary, Darwins efforts to lay out a rened conception of natural selection that could be linked in explanatorily novel ways to a wide range of natural historical phenomena make him an exemplar for modern biologists.

Tim Lewens
resulting in the production of such exquisite adaptations as the wing or the eye (Darwin, 1859, p. 169-70). For Darwin, natural selection is an explanatory schema, which allows us to account for adaptation in virtue of the preservation of variations that are benecial in the struggle for existence.

III. CHANGING UNDERSTANDINGS OF NATURAL SELECTION In very rough outline, Darwins understanding of natural selection is indeed the same as the modern one. Modern biologists tend to argue that natural selection occurs in virtue of heritable variation in tness. All of these terms are contentious in their interpretation. For our purposes we can take tness to measure the likely number of offspring an organism will have (although see Sober, 2001 among others for renement and discussion). Organisms need to vary in their tness for adaptation to emerge. Moreover, offspring need to resemble parents. For the moment let us simply assume that to say that some trait is heritable is to say that if parents have it, offspring will have it too. This is, of course, a thoroughly misleading assumption: heritability has a series of technical meanings in modern biology, with the result that a trait that is reliably inherited need not be heritable. Opposable thumbs are the sorts of traits that are reliably inherited in humans. But when we ask what explains population-wide variation in the presence of opposable thumbs, environmental accidents (in kitchens, with machinery, and so forth) are likely to have greater signicance than genetic variation. Opposable thumbs, therefore, will count as only weakly heritable. Let us set these worries aside, and proceed with our assumption that heritability and inheritance are roughly similar ideas. Given these assumptions, we can say that the modern understanding of natural selection thus put forward is similar to Darwins, because the requirement of variation in tness corresponds to Darwins requirement that organisms vary in terms of their suitability to the struggle for existence, while the requirement that this variation be heritable corresponds to Darwins principle of inheritance. Here, then, are the broad similarities, but differences mount up quickly when we compare Darwins work with recent evolutionary theory in more detail (see Depew & Weber 1995 for a compendious, illuminating and idiosyncratic treatment of many of these issues). What I want to focus on here, because I think it is the most instructive difference, is Darwins insistence on a Malthusian struggle for existence. If we take natural selection to occur whenever there is heritable variation in tness, then natural selection can occur when there are different rates of reproduction, regardless of whether there is the kind of scarcity of resources that a Malthusian struggle seems to demand. R.A. Fisher complained that Darwin had over-stated the importance of struggle in his account of selection: The historical fact that both Darwin and Wallace were led through reading Malthuss essay on population to appreciate the efcacy

II. NATURAL SELECTION IN ON THE ORIGIN OF SPECIES The explanation of adaptation is one of the primary goals of On the Origin of Species. As Darwin puts it, the transmutationist view (that is, the evolutionary view): . . . even if well founded, would be unsatisfactory, until it could be shown how the innumerable species inhabiting this world have been modied, so as to acquire that perfection of structure and co-adaptation which most justly excites our admiration (Darwin, 1859, p. 66). Natural selection was put forward by Darwin as an answer to this problem. Let us remind ourselves of the bare bones of his presentation. He begins by arguing that the members of all species face a struggle for existence. He follows Malthus (1798) in claiming that populations have a tendency to expand until they eventually outstrip the food supply. As a result, not all members of the population can survive. Darwin is explicit that members of a species need not literally do battle with each other. If some are better able to make use of limited resources than others, we can legitimately speak of a struggle in a large and metaphorical sense (Darwin, 1859, p. 116). Hence plants face a struggle for existence just as much as animals do. Darwin also argues that the members of a species have a tendency to vary. He concludes that some individuals in a species will be better suited to the struggle for existence than others. These individuals will live longer, and leave more offspring on average. Finally, Darwin argues that the traits which assist parents in the struggle for existence will appear in offspring, in virtue of the principle of inheritance. Favourable variations are thereby preserved, and given large stretches of time these variations can be added up,

Biological Reviews 85 (2010) 829835 2010 The Author. Biological Reviews 2010 Cambridge Philosophical Society

Natural selection then and now

of selection. . .should no longer constrain us to confuse the consequences of that principle with its foundations. (Fisher, 1930) As Elliott Sober puts it, . . . selection can modify a population even when all offspring survive. (Sober, 1984, p. 195). The claim that natural selection does not require struggle in any sense is contentious (Lewens 2009; Godfrey-Smith, 2009, pp. 48-53). Consider two herds of reindeer, one in Sweden, one in Canada. Maybe the Swedish reindeer have some trait that makes them reproduce at a faster rate than the Canadian reindeer. No biologist would say there is a selection process going on here between the members of the different herds. There might be heritable variation in tness, but the variant forms are disconnected from each other. So it seems that natural selection requires that the variants in question are in the same environment (Brandon, 1990). But what does this mean? Not, surely, that they are in the same geographical zone, but rather that they have causal interactions with each other, perhaps such that one variant prospering causes the other to do worse. If natural selection needs to be dened in this way, then while we drop the assumption that some offspring must die, we retain a notion of a struggle for existence in a large and metaphorical sense. But note that we lose the part of this metaphor that appeared to be most crucial for Darwinnamely, the fact of scarce resources, made inevitable by the geometric increase in population size unless unchecked. Darwin repeats over and over again in his presentations of natural selection the severity of the struggle for existence: . . . as more individuals are produced than can possibly survive, there must in every case be a struggle for existence. (Darwin, 1859, p. 63) Darwin regards the struggle for existence as exceptionally intenseit is the doctrine of Malthus applied with manifold force to the whole animal and vegetable kingdomswith the result that all but the best adapted will perish.

831 featured prominently in The Origins fth and sixth editions. In fact, pangenesis hardly gets a mention. Vorzimmer also notes that Jenkins review was published too late to have inuenced the content of Darwins chapter on pangenesis. Vorzimmer offers a plausible explanation for Darwins famous comments on the trouble Jenkins review gave him: on Vorzimmers reading, Darwin takes Jenkin to offer strong arguments against the possibility of selection preserving occasional sports. Darwin, Vorzimmer claims, holds that Jenkins work shows he should have been even more sceptical in earlier writings regarding the importance of rare (and dramatic) saltations: ironically, Darwin takes Jenkin to reconrm his faith in the importance of small variations commonly found in populations. These are the many slight differences which may be called individual differences, such as are known frequently to appear in the offspring from the same parents, or which may be presumed to have thus arisen, from being observed in the individuals of the same species inhabiting the same conned locality (Darwin, 1859, p. 45). Darwin perceived quite early in his career the potential obstacle which blending posed for the efcacy of selection; he did not need Jenkin to alert him to it. He was concerned while writing The Origin that the effects of blending could result in benecial variations being lost through crossing. A struggle for existence of exceptional intensity was then invoked in order to respond to this potential problem. As he puts it in The Origins rst edition: The process [of selection] will often be greatly retarded by free intercrossing. Many will exclaim that these several causes are amply sufcient wholly to stop the action of natural selection. I do not believe so (Darwin, 1859, p. 108). Darwin explains that in the case of conscious articial selection, these blending effects do not disrupt the process of improvement because breeders tend to mate the best animals with each other. A good breeder does not allow poorly adapted animals to reproduce. If the struggle for existence is exceptionally strong, then poorly adapted organisms cannot reproduce either, because they will not survive (see also Vorzimmer, 1963, p. 379). The detrimental effects of blending are (Darwin proposes) limited in nature, because all but the best adapted organisms perish, leaving only welladapted organisms to interbreed. I suggest that this aspect of Darwins theorising is partly obscured to the modern reader by his claiming that natural selection works on slight differences. It is tempting for us to understand Darwin to be arguing that natural selection can favour variations that make only a slight difference to tness. But although Darwins variations are slight in terms of their anatomical, physiological, or behavioural magnitude, the fact that natural selection is exceptionally discerning, and the fact that the struggle for existence is exceptionally intense, means that they make a very big difference to an organisms chances of surviving and reproducing. Darwins slight variations are not slight in terms of their inuence on the prospects of the

IV. THE EXPLANATORY ROLE OF MALTHUSIAN STRUGGLE The defender of the Dangerous Thesis might argue that Darwins claims about the intensity of the struggle for existence are incidental features of his presentation of natural selection. Here I show that they are essential to his explanation of adaptation, for they form part of Darwins response to the problem of blending. It has sometimes been suggested that Darwin did not appreciate the difculties posed by blending inheritance until he read Fleeming Jenkins review of The Origin (Fleeming Jenkin 1867). And some have suggested, in turn, that the hypothesis of pangenesis (Darwins provisional explanation of the phenomena of inheritance) was formulated, and subsequently presented in The Variation of Animals and Plants Under Domestication (Darwin, 1868), in order to deal with Jenkins comments. But, as Peter Vorzimmer argued many years ago (Vorzimmer 1963), this is a mistake. After all, if the hypothesis of pangenesis were really intended as a way of shoring up natural selection against Jenkins arguments, then one would expect pangenesis to have

Biological Reviews 85 (2010) 829835 2010 The Author. Biological Reviews 2010 Cambridge Philosophical Society

832 animal or plant. In Variation, Darwin considers a giraffe with a slightly longer neck. It would . . .during a dearth. . .have a slight advantage and be enabled to browse on higher twigs, and thus survive. A few mouthfuls more or less every day would make all the difference between life and death (Darwin, 1868, p. 206). Or consider elsewhere in Variation, where Darwin reminds us that in The Origin: It was there shown that all organic beings, without exception, tend to increase at so high a ratio, that no district, no station, not even the whole surface of the land of the whole ocean, would hold the progeny of a single pair after a certain number of generations. The inevitable result is an ever-recurrent Struggle for Existence. . . . [The] severe and often-recurrent struggle for existence will determine that those variations, however slight, which are favourable shall be preserved or selected, and those which are unfavourable shall be destroyed (Darwin, 1868, pp. 5-6). We have seen, then, that the notion that the struggle for existence is exceptionally severe is present in The Origins rst edition, and it is there nine years later in Variation. It is also present much earlier in the Notebooks, as in Notebook E where Darwin describes my principle as the destruction of all the less hardy ones and the preservation of accidental hardy seedlings (Barrett et al., 1987, E112). I suggest we need to read Darwin in a full-blooded manner here: the struggle for existence does not merely weed out the very worst adapted. Selection eliminates all the less hardy ones; that is, all but the very hardiest. The strength of this struggle is borne out by Darwins difculty in believing in the dreadful but quiet war of organic beings when he goes into the peaceful woods, and smiling elds. (Barrett et al., 1987, E114) Why would Darwin have such difculty if selection simply eliminated a small proportion of some population that is worst suited to its conditions of life? There is a contest and a grain of sand turns the balance (Barrett et al., 1987, E115c). Slight differences in organic structure make all the difference in the world for an organisms prospects. V. THE EXPLANATORY ROLE OF VARIATION This insistence on the severity of the struggle for existence is not the only way in which Darwin responds to the problem of blending inheritance. Vorzimmer (1963) canvasses many of Darwins strategies for coping with blending; here I shall restrict myself to just one more. Darwin often begins his presentations of natural selection by sketching circumstances in which a species environment changes in some way. This introduces his views about the causes of variation:

Tim Lewens
We have reason to believe. . .that a change in the conditions of life, by specially acting on the reproductive system, causes or increases variability. . . .and this would manifestly be favourable to natural selection, by giving a better chance of protable variations occurring (Darwin, 1859, p. 82). Now not only do changes in environment increase the tendency to vary, Darwin also regards this tendency as something that is itself inherited: . . .the tendency to variability is in itself hereditary, consequently they [the offspring] will tend to vary, and generally to vary in nearly the same manner as their parents varied (Darwin, 1859, p. 118). This helps to explain why Darwin is insistent that selection depends on what we in our ignorance call spontaneous or accidental variability (Darwin, 1868, p. 236). We say that variations are produced by chance, but these variations are not genuinely random for Darwin. Whatever the causes of variation might be, those causes are preserved from one generation to the next, and they tend to act in the same way to produce further variation. In this way, the offspring of parents that tended to increased speed will themselves tend to have offspring with yet more variations in the direction of increasing speed. So by scrupulously preserving benecial variations, and weeding out those which are inferior, natural selection also helps to ensure that further benecial variations of the same sort will appear. The result (Darwin believes) is that natural selection is again able to counteract the conservative effects of blending, by magnifying the tendency for variations of the favoured kind to be produced.

VI. DARWIN AND THE MODERN SYNTHESIS It is risky to write of the modern conception of evolution: there are different schools of thought. Yet however we understand modern evolutionary theory, it seems clear that Darwins way of understanding natural selectionhis general manner of explaining adaptation, that isrelies on a number of features that do not appear in standard modern textbook presentations of evolutionary change. On Darwins view, the struggle for existence is exceptionally severe, the tendency to vary in a particular direction is inherited, and so forth. Darwins reason for introducing these assumptions rests on his concern that the effects of crossing will otherwise swamp the effects of selection. If inheritance were to follow a blending pattern in the way Darwin suggests, then further assumptions explaining how adaptation can emerge would indeed be required. Darwin confronts this problem head-on, and supplies one set of ancillary conditions which (he believes) do the trick. By contrast, R.A. Fisher famously argued that given a particulate view of inheritance, selection could proceed in a powerful manner even with frequent crossing, small tness advantages and a low mutation rate (Fisher, 1930). This is all quite different to Darwins view, which (translated into a modern

Biological Reviews 85 (2010) 829835 2010 The Author. Biological Reviews 2010 Cambridge Philosophical Society

Natural selection then and now

idiom) effectively insists on infrequent crossing, large tness advantages and a high mutation rate. Fisher put the general point like this, demonstrating his historical understanding of what Darwin asserted in The Origin, as well as his own theoretical conception of selection: The important consequence of. . .blending is that, if not safeguarded by intense marital correlation, the heritable variance is approximately halved in every generation. To maintain a stationary variance fresh mutations must be available in each generation to supply the half of the variance lost. If variability persists, as Darwin rightly inferred, causes of new variability must continually be at work. Almost every individual of each generation must be a mutant. . . (Fisher, 1930) Without thinking in some detail about the potential interactions between systems of inheritance and the variations that promote reproductive success, the generic idea of natural selection is one whose explanatory standing is dubious. Darwin thought about these issues in detail, and gave one set of answers which typically appeal to what we would now call truncation selection, or quasi-truncation selection, of an intense form (see Crow & Kimura, 1979). Fisher thought about them and gave quite a different set of answers, which rejected Malthusian assumptions about the struggle for existence that are central to Darwins presentation of natural selection. Of course, we might say that some core notion of selection is common to both. But the common residue of selection is the very broad, and informal, notion of the preservation of favourable inherited variation. Had Darwin himself rested content with this, his contemporaries would have accused him, quite rightly, of giving a half-baked theory. It is far from clear that natural selection, construed in this way, and with no attention to the difculties presented by inheritance, is adequate to the explanation of adaptation. In response, then, to the Dangerous Thesis, we can conclude that the modern conception of natural selection is not the same as Darwins, unless we describe natural selection in the most abstract manner. But when described in this abstract manneras the preservation of favourable variations, saythe ability of natural selection to account for adaptation is questionable. VII. THE EXPLANATORY ROLE OF UNCONSCIOUS SELECTION There is another way in which Darwin tried to answer those who are sceptical of the ability of natural selection to produce adaptation. He placed considerable weight on the existence of what he called unconscious selection, a conceptual bridge between natural and articial selection. Unconscious selection is the preservation by man of the most valued, and the destruction of the least valued individuals, without any conscious intention on his part of altering the

833 breed (Darwin, 1868, p. 195). Darwin attempts to show that unconscious selection has been effective in modifying races: It is difcult to offer direct proofs of the results which follow from this kind of selection; but the indirect evidence is abundant (Darwin, 1868, p. 195). If Darwin can show this, then he also takes himself to have shown empirically that blending can be overcome without conscious efforts to mate the best animals: The different strains, just alluded to, which have been actually produced by breeders without any wish on their part to obtain such a result, afford excellent evidence of the power of unconscious selection. This form of selection has probably led to far more important results than methodical selection, and is likewise more important under a theoretical point of view from closely resembling natural selection. For during this process the best or most valued individuals are not separated and prevented from crossing with others of the same breed, but are simply preferred and preserved; yet this inevitably leads to their gradual modication and improvement; so that nally they prevail, to the exclusion of the old parent-form (Darwin, 1868, p. 420). Darwin gives us strong evidence in favour of the possibility, somehow or another, that a population can adapt even when no conscious effort is made to prevent crossing. And that, in turn, suggests that the prospect of blending need not undermine natural selection, merely in virtue of the fact that no intelligent breeder oversees matings in nature. What that means is that Darwin gave us good empirical evidence in favour of the efcacy of some principle or another that resembles his notion of natural selection. It does not mean that Darwin articulated a simple idea of great explanatory power that we still use today. VIII. CULTURAL EVOLUTION Before concluding, let me consider another potential response from the defender of the Dangerous Thesis. One might say that the explanatory power of an abstract conception of natural selection is secured by the fact that selection has been used to good effect in models of evolution outside the organic realm. Doesnt the success of cultural evolutionary theorising, for example, show us that Darwins Dangerous Idea has exceptionally broad explanatory scope? Here we enter into a vast and contentious topic. I will make only two brief points. First, the manner of approaching cultural evolution that leans most heavily on an abstract conception of natural selection is memetics. Most meme theorists have been content to explore analogies between biological and cultural evolution. And in exploring these analogies, many have found that the details of how cultural inheritance works turn out to be essential when we come to ask what explanatory

Biological Reviews 85 (2010) 829835 2010 The Author. Biological Reviews 2010 Cambridge Philosophical Society

834 role natural selection might have in this area. Moreover, it is one thing to explore the nature of an analogy, another thing to give a novel, enlightening explanation of some specic episode of cultural change. There are no clear-cut examples where the memetic approach has achieved this second goal. So we can question whether the memetic approach has had the kind of success that demonstrates the explanatory power of an abstract conception of natural selection. This leads on to my second point. There are successful evolutionary theories of culture. I regard the work of evolutionary anthropologists R. Boyd and P. Richerson as leading the way in this domain. But Boyd and Richerson reject the concept of the meme (e.g. Boyd & Richerson, 2000). They say that Population thinking is the core of the theory of culture we defend. . . (Richerson & Boyd, 2005, p. 5). Their insights come from an approach which asks what the population-level consequences might be when we model a group of interacting individuals with characteristic psychological dispositions. They see themselves as inheritors of a Darwinian tradition here, and it is true that Darwins account of the modication of species rests on the aggregrated effects of interactions of individual members of those species. Natural selection, although present in some of Boyd and Richersons models, is not their explanatory centrepiece; population thinking is. So the Dangerous Thesis gets little support from the successes of work in cultural evolution.

Tim Lewens
might account for at least some instances of adaptation. In any case, if we consider a Nineteenth Century reader of The Origin, it seems to me that scepticism about natural selection was perfectly justiable. Darwins efforts to overcome the problems of blending had not shown decisively that natural selection could promote adaptation. And the view that some other principle, which had not yet been formulated, might instead offer the right explanation, seems entirely reasonable. There is a deeper worry with this effort to defend the Dangerous Thesis. If Darwin is supposed to get credit for having formulated natural selection as an abstract explanatory principle in spite of his getting the details wrong, then one might suggest that Darwins predecessors, who also formulated abstract conceptions of selection, and who also got the details wrong, should share that credit equally. Patrick Matthew, author of On Naval Timber and Arboriculture, suggested an idea very like natural selection in 1831 (Matthew, 1831). The usual reaction of historians to the writings of Matthew and others is to point out that Darwin did not merely formulate a principle of natural selection (e.g. Bowler, 2003, p. 158; Mayr, 1982). He sought to apply it as an explanatory principle to a wide range of cases. He also sought to establish its reality by scrupulous investigation of the nature of variation, inheritance and articial selection. In so doing he gave natural selection an empirical footing that no other theorist had come close to achieving, and he made natural selection visible and inuential to natural historians. This standard response gives us all we need to cement Darwins reputation. It is also worth noting that the standard response seems to reect how both Darwin and Matthew saw things. Here is how Darwin reected on Matthews contribution in the Historical Sketch, which appeared as an introductory note to The Origins third edition of 1861: In 1831 Mr. Patrick Matthew published his work on Naval Timber and Arboriculture, in which he gives precisely the same view on the origin of species as that (presently to be alluded to) propounded by Mr. Wallace and myself in the Linnean Journal, and as that enlarged on in the present volume. . .In answer to a letter of mine (published in Gard. Chron., April 13th), fully acknowledging that Mr. Matthew had anticipated me, he with generous candour wrote a letter (Gard. Chron. May 12th) containing the following passage:To me the conception of this law of Nature came intuitively as a self-evident fact, almost without an effort of concentrated thought. Mr. Darwin here seems to have more merit in the discovery than I have had; to me it did not appear a discovery. He seems to have worked it out by inductive reason, slowly and with due caution to have made his way synthetically from fact to fact onwards; while with me it was by a general glance at the scheme of Nature that I estimated this select production of species as an a priori recognisable ` factan axiom requiring only to be pointed

IX. DARWINS REPUTATION One might worry that the preceding arguments undermine Darwins reputation, in a way that is thoroughly inappropriate as we look back on an anniversary year. It seems to show that Darwins explanation of adaptation by natural selection was mistaken when construed in ne-grained terms, and that it was vacuous when construed in the abstract. I do not think this is the moral we should draw. Before explaining why not, let me briey consider a response that defenders of the Dangerous Thesis might put forward. Richard Dawkins has argued not merely that natural selection is the correct explanation of adaptation, but that it is the only possible explanation of adaptation (Dawkins, 1983). We might say, then, that Darwins achievement lies in nding the right generic explanation, even if he got the details wrong. I do not deny that there are commonalities between Darwins notion of selection and modern conceptions. I am sceptical about the claim that natural selection is the only possible explanation of adaptation. After all, it is enough for Dawkinss campaign against intelligent design theorists that intelligent design is not the right explanation of adaptation. Few will doubt that natural selection will continue to be regarded as the correct explanation for a majority of adaptive traits. Further claims to the effect that there is no other possible explanation for adaptation are unnecessary, and future scientists might simply accuse us of a lack of imagination. There is surely no need for us to claim that it is impossible that self-organisation, or the plastic properties of some forms of organic material,

Biological Reviews 85 (2010) 829835 2010 The Author. Biological Reviews 2010 Cambridge Philosophical Society

Natural selection then and now

out to be admitted by unprejudiced minds of sufcient grasp. (Peckham, 1959, pp. 62-3). Matthew considered the principle of natural selection to be an a priori principle. And on some modern readings it does indeed have the character of a general mathematical truth, knowable a priori: if one type has a greater tendency to reproduce its kind than another, then, in the long run, we should expect the former type to replace the latter in a population. Matthewlike Dawkins and Dennettreally did conceive of natural selection as a tremendously simple, self-evident idea, which he believed had enormous explanatory power. Darwins understanding of natural selection, on the other hand, incorporates an attempt to ll out the empirical details of how inheritance works, of what sorts of environmental conditions must apply for selection to be efcacious in producing complex adaptation, and so forth. Darwin is the hero of modern evolutionary biology not because Darwin was the rst to formulate an abstract idea, but because Darwin was the rst to build a detailed explanatory system, backed by massive empirical data, ranging over the gamut of biological phenomena, with a version of natural selection at its core. Those who admire Darwin today typically aim to do something similar, albeit with a signicantly different version of natural selection. Darwin can act as an exemplar in this sense even though Darwins conception of natural selection is quite different to our own. Darwins pre-eminent status does not require that we endorse the Dangerous Thesis, except in its mildest version. X. CONCLUSIONS (1) Some commentators are tempted to think of natural selection as an exceptionally simple idea which we have inherited in a more or less unmodied version from Darwin. (2) Darwin insisted on an exceptionally strong struggle for existence because he believed it helped to counter the problem of blending inheritance. (3) Darwins conception of natural selection therefore differs from the modern conception in important respects, including respects that are essential to the explanation of adaptation. (4) If natural selection is understood in an abstract enough manner to allow us to say that Darwins conception is the same as the modern one, then the ability of natural selection to account for adaptation is dubious. (5) Darwins reputation is better understood in terms of the development of a detailed explanatory theory, rather than in terms of the articulation of a simple explanatory idea. XI. ACKNOWLEDGEMENTS

835

Versions of this paper were read to the British Society for the Philosophy of Science conference in July 2009, and at meetings in Bergamo, Paris and Riga over the course of 20082009. I am grateful to audiences there for the comments, and to the Isaac Newton Trust and the Leverhulme Trust for nancial support. I am especially grateful to Jon Hodge for advice in the early stages of this project. XII. REFERENCES
Barrett, P., Gautrey, P., Herbert, S., Kohn, D. & Smith, S. (1987). Charles Darwins Notebooks, 18361844. Cambridge: Cambridge University Press. Bowler, P. (2003). Evolution: The History of an Idea. 3rd Edition. University of California Press. Boyd, R., & Richerson, P. (2000). Memes: Universal acid or a better mousetrap? In: Darwinizing Culture (ed. R. Aunger), 143162. Oxford: Oxford University Press. Brandon, R. (1990). Adaptation and Environment. Princeton, NJ: Princeton University Press. Crow, J., & Kimura, M. (1979). Efciency of Truncation Selection PNAS 76, 396399. Darwin, C. (1859/1964). On the Origin of Species. Facsimile of the First edition, Edited by Ernst Mayr. Cambridge, MA: Harvard University Press. Darwin, C. (1868/1998). The Variation of Animals and Plants Under Domestication, Volumes One and Two. Edited by Harriet Ritvo. Johns Hopkins University Press. Dawkins, R. (1983). Universal Darwinism In: Evolution: From Molecules to Men. (ed. D. S. Bendall), 403425. Cambridge: Cambridge University Press. Dawkins, R. (2008). Why Darwin Matters Guardian, February 9th . Online: http://www.guardian.co.uk/science/2008/feb/09/darwin.dawkins1. Accessed 8th September 2009. Dennett, D. (1995). Darwins Dangerous Idea. London: Allen Lane. Depew, D. & Weber, B. (1995). Darwinism Evolving: Systems Dynamics and the Genealogy of Natural Selection. Cambridge MA: MIT Press. Fisher, R. (1930). The Genetical Theory of Natural Selection. Oxford: Clarendon Press. Fleeming Jenkin, H. (1867). Review of the Origin of Species North British Review 46, 277318. Godfrey-Smith, P. (2009). Darwinian Populations and Natural Selection. Oxford: Oxford University Press. Lewens, T. (2009). Natural Selection and Adaptation. In: Routledge Encyclopedia of Philosophy (ed. E. Craig). London: Routledge. Online: http://www.rep.routledge.com/ article/Q126. Accessed 2nd February 2010. Matthew, P. (1831). On Naval Timber and Arboriculture. Edinburgh: Black. Malthus, T. (1798/1986). An Essay on the Principle of Population. First edition, edited by Anthony Flew. London: Penguin. Mayr, E. (1982). The Growth of Biological Thought. Cambridge, MA: Harvard University Press. Peckham, M. (1959). The Origin of Species by Charles Darwin: A Variorum Text. Philadelphia: University of Pennsylvania Press. Richerson, P., & Boyd, R. (2005). Not by Genes Alone: How Culture Transformed Human Evolution. Chicago: University of Chicago Press. Sober, E. (1984). The Nature of Selection: Evolutionary Theory in Philosophical Focus. Chicago: University of Chicago Press. Sober, E. (2001). The Two Faces of Fitness, in R. Singh, C. Krimbas, D. Paul and J. Beatty (eds.) Thinking About Evolution, Cambridge: Cambridge University Press. Vorzimmer, P. (1963). Charles Darwin and Blending Inheritance Isis 54, 371390.

Biological Reviews 85 (2010) 829835 2010 The Author. Biological Reviews 2010 Cambridge Philosophical Society