Contentious Genes: A Commentary On The Selfish Gene By .

J. Social Biol. Struct. 1980 3, 77-81Contentious genes: a commentary onThe Selfish Gene by Richard DawkinsMartin DalyMcMaster University, Department of Psychology, 1280 Main Street West,Hamilton, Ontario LSS 4K1, CanadaIn the preface to The Selfish Gene, Richard Dawkins tells us that 'threeimaginary readers looked over my shoulder while I was writing': the layman,the student, and the expert. I recently asked Dawkins how he had fared witheach of his target readers.Lay readers, he believes, 'have been moderately enthusiastic, but have quiteoften misunderstood' the book. Students have received it very favourably. Butthe response of the expert, 'which is the one I'm most interested in', came assomething of a surprise. Dawkins thought his colleagues would agree that 'thegene' is 'the level at which selection operates' and did not expect to find himselfdebating 'individual selectionists', nor did he anticipate that the metaphor of avolitional gene would stick in so many throats.The writing style of The Selfish Gene is popular to the point of cutenessDawkins now finds himself 'positively embarrassed when students parrot thequaint anthropomorphic way of speaking'-but this probably has not greatlyinfluenced expert response. Scientific reviewers who like the contents call thestyle 'superbly readable'. Those who do not substitute 'gushing'. The popularstyle is by no means inconsequential, however. Favourable reviews in suchperiodicals as the New Yorker, the Economist, and the New York TimesReview o f Books, as well as the hundreds of letters that the author has received,attest to Dawkins's success with the public.Students truly enjoy the book. Text-book publishers, please take note.Without irrelevant photographs, coloured type-faces or any other pandering tothe alleged minimal attention spans of a television-reared generation, indeedwithout a single illustration or subdivision beyond his eleven chapters, Dawkinshas written a book which students (according to my informal survey ofinstructors in biology, psychology and anthropology) are almost unanimous inpraising.It is of course precisely because of Dawkins's success with his lay and studentreaders that expert opinion becomes important. What exactly has he popularizedand has he got it right?It must first be remarked that Dawkins is more interested in explainingtheory than in presenting evidence. Sometimes this seems particularly0140-1750/80/010077 05 02.00/0 1980 Academic Press Inc. (London) Limited

78M. Da unfortunate, as in Chapter 7, where he counters Wynne-Edwards's groupselection theory with selfish gene accounts o f each allegedly group-adaptivephenomenon. The n /ve reader would hardly suspect that Lack's theory, forexample, has inspired a great deal of empirical work and has been supportedand ret'med. Critics who brand sociobiology an armchair enterprise o f fancifulstory-weaving may be regrettably reinforced in their erroneous prejudices byDawkins's treatment. And accepting the bias toward theoretical treatment, thereare still flaws evident in retrospect: contra Dawkins, Alexander's (1974)parental manipulation theory is alive and well (see Craig, 1979; Harpending,1979), and Zahavi's ( 1 9 7 5 ) h a n d i c a p principle has been successfully modelled(Bell, 1978). But if Dawkins was occasionally too assertive (and he now regretshis 'impoliteness' to authors with whom he disagreed), he neverthelesssummarized a rapidly developing field o f theory with considerable syntheticskill and with a flair that did not displease his principle sources, W.D. Hamilton,R.L. Trivers, J. Maynard Smith and G. C. Williams.Dawkins was (and remains) in some doubt about the extent to which TheSelfish Gene might constitute an original contribution to theory. According tohis preface, 'my greatest hope is that even (the expert) will find something newhere'. To his surprise, the book thrust him into the role o f radical advocate o fa position endorsed by few sociobiologists: the view that discussions o f 'group','kin' and 'individual' selection all obfuscate the fact that 'gene selection' iswhat is really at issue (Dawkins, 1978). Critics have responded that this sorto f reductionism obscures principles o f higher structural organization, a pointmade with unusual clarity by Michael Wade:Dawkins' misconception of the role of population structure in the evolution of socialbehaviors stems from his confusion of the effects of selection with the process of selection.He reasons as follows (Chapter 3): Because evolution consists of changes in gene frequencyand because genes persist unchanged longer than chromosomes, genomes, or gene pools,the gene must therefore be the unit of selection.'Since genes reside on the chromosomes of individuals, all forces which affect genefrequencies can be reduced to increments or decrements in the fitness of individuals as amatter of mathematical convenience. This reductionist approach (employed by Hamiltonin his mathematical formulation of kinship theory), however, does not mean that allselective changes can be attributed strictly to selection at the genic level. The differentialproliferation of the various units of population structure can be the actual mechanism ofgene frequency change. And, it is the variance between the units of population structurewhich determines the relative rates of gene frequency change caused by selection at anylevel' (Wade, 1978, pp. 220-221).I believe that Wade's criticism has some validity, but the disagreement maybe more semantic than substantive. Dawkins and several o f his critics acceptas meaningful the question 'What is the unit o f selection?' and give differentanswers, without apparently differing on matters o f fact. Perhaps the questionis not valid as posed. We all might find it easier to think clearly about thesematters if we bear in mind that natural 'selection' is itself a metaphor, chosenby Darwin to parallel the artificial selection performed by breeders. 'Selectiveagents', 'selective vs. non-selective deaths' and many related concepts are notdirect descriptions o f natural phenomena. They are metaphorical models ata high level of abstraction, invoked to help understand certain statisticalproperties o f classes of natural phenomena. Like all metaphors, 'selection' asa model o f differential proliferation o f types can obscure as well as clarify.

Contentious genes79(That is why Stephen Jay Gould, 1977, is unconvincing when he claims thatthe 'fatal flaw' in Dawkins's argument is that genes lack 'direct visibility tonatural selection', evoking images o f a malevolent selective agent bashingundesirable p h e n o t y p e s as they reveal themselves.) If 'selection' meansdifferential survival and reproduction, there is no question that it occursbetween alleles. But the processes by which it occurs include (at the least)differential survival and reproduction (selection) o f individuals.The question, then, should not be whether Dawkins's particular form o freductionism is correct, but whether it is useful. Wade argues that it obscureshigher-level structure. Dawkins argues that it clarifies certain thornyevolutionary problems. Presumably, we should maintain the mental flexibilityto move back and forth. But Dawkins, perhaps pushed to an extreme positionb y critical response, has written 'The time has come to carry (Hamilton's)"selfish gene" revolution to its conclusion, and give up the habit o f speaking o fadaptation at the individual level' (Dawkins, 1978, p. 75). I do not think henoticed what a reductio ad adsurdum this sounds' even if it were desirable,such a mental leap is almost unimaginable. All the game theoretic analyses inThe Selfish Gene focus on individual strategists (hawk, dove, etc.), andDawkins's own research has always focussed upon individual decision-makingby chickens, crickets, and wasps. The individual is unquestionably anappropriate focus for the study o f adaptation and perhaps even the appropriatefocus. I will give that last word on this to Richard Alexander:It is 'almost always possible to build a better system of water balance, a better locomotorymechanism, a better extruder of toxic products, or a better temperature control device.What stops the evolutionary process at any particular point is the difficulty in building abetter organism. Any study of function which fails to take into account the reproductivestrategy of the whole organism-no matter how clear the actions and effect of chemicals,organelles, or organs may seem to be-necessarily must lack focus (Alexander, 1975,pp. 83-84).Even more surprising to Dawkins than the 'unit of selection' dispute hasbeen the response to his anthropomorphising o f the gene. He knew well enoughthat theorists who described animals as strategists striving to maximize theirinclusive fitness were in danger of being taken literally, b u t as he told me, hehad hoped to obviate misunderstanding b y "the shift of volition from a levelwhere it is plausible to one where it is manifestly absurd'. The metaphor o f awilful gene is certainly a handy rhetorical device and it may even be a usefulstimulus to theory, b u t is it also mischievous? I think it can be. CertainlyDawkins leaps from a technical definition o f gene 'selfishness' to the claim 'weare born selfish' without scrutinizing the intervening logic. And certainly, theselfish genes are sometimes potrayed as seeking novel ways to exploit theenvironment for their own replication, when it would be more consistent to saythat extant genes seek no innovation b u t instead fear being supplanted byinventive alleles. How much this sort o f thing really matters I cannot say. Itwould be a critical feat b e y o n d m y abilities to dissect each use o f the 'volitionalgene' metaphor and say when it misleads. But one example must surely beDawkins's inspirational vision o f man becoming 'emancipated' from his genes, anotion that is literally nonsensical, but which follows from attributing a will tothe genes, a will which we may then defy. I hasten to add that I can think o f no