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THE GENIAL GENE Deconstructing Darwinian Selfishness By Joan Roughgarden University of California Press, 255 pages, $29.95

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The great English naturalist Charles Darwin, the bicentenary of whose birth we celebrate this year, became an evolutionist in 1837, shortly after he had returned from a five-year trip around the world on HMS Beagle. About 18 months later, he discovered his mechanism of natural selection, the survival of the fittest. It is pretty clear that Darwin was led to his mechanism by analogy from the successes of animal and plant breeders selecting for shaggier sheep, fatter pigs and leafier vegetables.

It is no surprise, therefore, that Darwin also noted that breeders of his day selected for pleasure: ever-more-savage dogs and cockerels, and beautiful and melodious birds. This led him to a secondary mechanism, sexual selection, something Darwin divided into male combat, as when stags develop large antlers to battle rivals in the rutting season, and female choice, as when peahens choose the mate with the most glorious tail feathers.

Sexual selection lay unused for many years. Then, in 1871, Darwin came to write his great work on our species, The Descent of Man and Selection in Relation to Sex. This seems an odd combination and it makes for a rather strange book, with an initial discussion of human evolution, then a massive review of sexual selection, and finally a few quick comments again on our own species.

All of this is a function of the apostasy of the co-discoverer of natural selection, Alfred Russel Wallace. During the 1860s, the decade after Darwin published his paradigm-making Origin of Species, Wallace took up spiritualism, arguing that natural causes cannot alone have produced human beings, that our hairlessness and our big brains would never have appeared without spirit forces. Appalled, although agreeing that natural selection could not do the job, Darwin turned to sexual selection, and claimed that it makes for human features, including those that separate races. Men battle for mates, females prefer winners (not just hearties but thinkers also), and so we evolved naturally.

For many years after Darwin, sexual selection was virtually ignored. Then, starting in the 1960s, it came right back to life, and today's evolutionists think it one of the most important formative features of the organic world. There have been some very celebrated studies, for instance that of English biologist Tim Clutton-Brock, who showed how Scottish red deer have been moulded by competition for mates and the consequent differential reproduction.

It seems fair to say this was all part of a general move to what Richard Dawkins brilliantly labelled "selfish gene" thinking, where one tries to understand problems from the perspective of what makes any one gene (or a package of genes, better known as an organism) a success in the struggle for life. Sexual selection does not think of people coupling for the benefits of their mates or even for their families as such. Everything one does is a matter of how will it benefit me, in the sense of getting more of my genes into the next generation.

Joan Roughgarden, who is rightly celebrated as one of the important evolutionary thinkers of our time, will have none of this. She loathes and detests sexual selection, thinking it one of the greatest biological fallacies, inadequate in theory and unsupported by evidence. As revealed by the title of her new book, The Genial Gene: Deconstructing Darwinian Selfishness, she opposes tooth and nail the underlying genetic self-centred approach of much modern evolutionary biology. She wants to replace it with a warmer, friendlier way of thinking, based on something she calls "social selection," where organisms get together for the benefit of each other rather than just for No. 1.

Much of her book, therefore, is fiery polemic against supporters of sexual selection, although as the argument gathers force, there is also much on the general satisfaction that organisms get from co-operating and why this should thus be considered the baseline, as it were, and why falling out of place - having a little extra on the side - is something that needs special explanation.

Expectedly, Clutton-Brock gets roughed up on a regular basis, and it is interesting to look at a piece that he penned in Science in 2007 (Sexual Selection in Males and Females). This was written as a counter to a preliminary airing of Roughgarden's theory in an earlier issue of the same journal.

In her new book, Roughgarden portrays this counter as a classic exercise in retreat, as Clutton-Brock gelds his thinking of any real force or interest and implicitly gives over all to social selection. Going to the article in question, all I can say is that this interpretation is probably news to Clutton-Brock, as it was certainly news to me. What I see is recognition of the fact that good ideas don't stand still, but over 150 years get extended and refined and reworked. This is not giving up. This is evolution in action. Darwin himself focused his thinking about sexual selection, in The Descent of Man putting a huge amount on the hitherto-unappreciated male choice for beauty.

More generally, it seems to me that Roughgarden just doesn't understand the function of metaphor in science. "Selfish gene" is the most brilliant metaphor of the 20th century, but it doesn't mean that either genes are literally selfish or that we are. In Dickens's Martin Chuzzlewit, Seth Pecksniff was selfish, Tom Pinch was not. It might well be the case, it usually is the case, that genuine care and compassion and warmth are far better ways of furthering our genetic interests (of which most of us are quite ignorant) than calculation and self-regard. Think of your own acquaintances and ask whom you are more ready to help, the decent, friendly chap down the corridor or the snivelling little creep who is always looking for a freebie.

In any case, being warm and friendly and co-operative because this is nicer appears no less problematic than selfishness. It is clear that genes don't think about what is in the interests of others and often organisms don't either. I doubt very much that two birds raising young at the nest have thought about the consequences for themselves or their mates. It is perfectly acceptable for Roughgarden to prefer friendliness to selfishness - I do myself (well, usually, except when it comes to that little bit of extra on the side) - but this has nothing to do with whether one approach is therefore better scientifically than the other.

In the end, as Roughgarden and her critics seem to agree, not all organisms do as well in the mating game as do others, and this is a function of the differences in abilities at playing the game. Roughgarden argues that this is for reasons other than sexual selection. Her critics say it is sexual selection and that even if her mechanisms work, they are still sexual selection. Either way, it seems appropriate to praise Darwin, who not only spotted the issues but who gave the tools to work toward a solution.

Michael Ruse is the author of many books on evolution, including Darwinism and Its Discontents. As he approaches his 70th birthday, he is glad that sexual selection will trouble him only for another 20 years.

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