The Selfish Gene (24 page)

The chances are that most of the females will agree with each other on which are the best males, since they all have the same information to go on. Therefore these few lucky males will do most of the copulating. This they are quite capable of doing, since all they must give to each female is some cheap sperms. This is presumably what has happened in elephant seals and in birds of paradise. The females are allowing just a few males to get away with the ideal selfish-exploitation strategy which all males aspire to, but they are making sure that only the best males are allowed this luxury.

From the point of view of a female trying to pick good genes with which to ally her own, what is she looking for? One thing she wants is evidence of ability to survive. Obviously any potential mate who is courting her has proved his ability to survive at least into adulthood, but he has not necessarily proved that he can survive much longer. Quite a good policy for a female might be to go for old men. Whatever their shortcomings, they have at least proved they can survive, and she is likely to be allying her genes with genes for longevity. However, there is no point in ensuring that her children live long lives if they do not also give her lots of grandchildren. Longevity is not prima facie evidence of virility. Indeed a long-lived male may have survived precisely because he does not take risks in order to reproduce. A female who selects an old male is not necessarily going to have more descendants than a rival female who chooses a young one who shows some other evidence of good genes. What other evidence? There are many possibilities. Perhaps strong muscles as evidence of ability to catch food, perhaps long legs as evidence of ability to run away from predators. A female might benefit her genes by allying them with such traits, since they might be useful qualities in both her sons and her daughters. To begin with, then, we have to imagine females choosing males on the basis of perfectly genuine labels or indicators which tend to be evidence of good underlying genes. But now here is a very interesting point realized by Darwin, and clearly enunciated by Fisher. In a society where males compete with each other to be chosen as he-men by females, one of the best things a mother can do for her genes is to make a son who will turn out in his turn to be an attractive he-man. If she can ensure that her son is one of the fortunate few males who wins most of the copulations in the society when he grows up, she will have an enormous number of grandchildren. The result of this is that one of the most desirable qualities a male can have in the eyes of a female is, quite simply, sexual attractiveness itself. A female who mates with a super-attractive he-man is more likely to have sons who are attractive to females of the next generation, and who will make lots of grandchildren for her. Originally, then, females may be thought of as selecting males on the basis of obviously useful qualities like big muscles, but once such qualities became widely accepted as attractive among the females of the species, natural selection would continue to favour them simply because they were attractive. Extravagances such as the tails of male birds of paradise may therefore have evolved by a kind of unstable, runaway process. In the early days, a slightly longer tail than usual may have been selected by females as a desirable quality in males, perhaps because it betokened a fit and healthy constitution. A short tail on a male might have been an indicator of some vitamin deficiency-evidence of poor food-getting ability. Or perhaps short-tailed males were not very good at running away from predators, and so had had their tails bitten off. Notice that we don't have to assume that the short tail was in itself genetically inherited, only that it served as an indicator of some genetic inferiority. Anyway, for whatever reason, let us suppose that females in the ancestral bird of paradise species preferentially went for males with longer than average tails. Provided there was some genetic contribution to the natural variation in male tail-length, this would in time cause the average tail-length of males in the population to increase. Females followed a simple rule: look all the males over, and go for the one with the longest tail. Any female who departed from this rule was penalized, even if tails had already become so long that they actually encumbered males possessing them. This was because any female who did not produce long-tailed sons had little chance of one of her sons being regarded as attractive. Like a fashion in women's clothes, or in American car design, the trend toward longer tails took off and gathered its own momentum. It was stopped only when tails became so grotesquely long that their manifest disadvantages started to outweigh the advantage of sexual attractiveness.

This is a hard idea to swallow, and it has attracted its sceptics ever since Darwin first proposed it, under the name of sexual selection. One person who does not believe it is A. Zahavi, whose 'Fox, fox' theory we have already met. He puts forward his own maddeningly contrary 'handicap principle' as a rival explanation. He points out that the very fact that females are trying to select for good genes among males opens the door to deception by the males. Strong muscles may be a genuinely good quality for a female to select, but then what is to stop males from growing dummy muscles with no more real substance than human padded shoulders? If it costs a male less to grow false muscles than real ones, sexual selection should favour genes for producing false muscles. It will not be long, however, before counter-selection leads to the evolution of females capable of seeing through the deception. Zahavi's basic premise is that false sexual advertisement will eventually be seen through by females. He therefore concludes that really successful males will be those who do not advertise falsely, those who palpably demonstrate that they are not deceiving. If it is strong muscles we are talking about, then males who merely assume the visual appearance of strong muscles will soon be detected by the females. But a male who demonstrates, by the equivalent of lifting weights or ostentatiously doing press-ups, that he really has strong muscles, will succeed in convincing the females. In other words Zahavi believes that a he-man must not only seem to be a good quality male: he must really be a good quality male, otherwise he will not be accepted as such by sceptical females. Displays will therefore evolve that only a genuine he-man is capable of doing.

So far so good.
Now comes the part of Zahavi's theory that really sticks in the throat. He suggests that the tails of birds of paradise and peacocks, the huge antlers of deer, and the other sexually-selected features which have always seemed paradoxical because they appear to be handicaps to their possessors, evolve precisely because they are handicaps. A male bird with a long and cumbersome tail is showing off to females that he is such a strong he-man that he can survive in spite of his tail. Think of a woman watching two men run a race. If both arrive at the finishing post at the same time, but one has deliberately encumbered himself with a sack of coal on his back, the women will naturally draw the conclusion that the man with the burden is really the faster runner.

I do not believe this theory, although I am not quite so confident in my scepticism as I was when I first heard it. I pointed out then that the logical conclusion to it should be the evolution of males with only one leg and only one eye. Zahavi, who comes from Israel, instantly retorted: 'Some of our best generals have only one eye!' Nevertheless, the problem remains that the handicap theory seems to contain a basic contradiction. If the handicap is a genuine one-and it is of the essence of the theory that it has to be a genuine one-then the handicap itself will penalize the offspring just as surely as it may attract females. It is, in any case, important that the handicap must not be passed on to daughters.

If we rephrase the handicap theory in terms of genes, we have something like this. A gene that makes males develop a handicap, such as a long tail, becomes more numerous in the gene pool because females choose males who have handicaps. Females choose males who have handicaps, because genes that make females so choose also become frequent in the gene pool. This is because females with a taste for handicapped males will automatically tend to be selecting males with good genes in other respects, since those males have survived to adulthood in spite of the handicap. These good 'other' genes will benefit the bodies of the children, which therefore survive to propagate the genes for the handicap itself, and also the genes for choosing handicapped males. Provided the genes for the handicap itself exert their effect only in sons, just as the genes for a sexual preference for the handicap affect only daughters, the theory just might be made to work. So long as it is formulated only in words, we cannot be sure whether it will work or not. We get a better idea of how feasible such a theory is when it is rephrased in terms of a mathematical model. So far mathematical geneticists who have tried to make the handicap principle into a workable model have failed. This may be because it is not a workable principle, or it may be because they are not clever enough. One of them is Maynard Smith, and my hunch favours the former possibility.

If a male can demonstrate his superiority over other males in a way that does not involve deliberately handicapping himself, nobody would doubt that he could increase his genetic success in that way. Thus elephant seals win and hold on to their harems, not by being aesthetically attractive to females, but by the simple expedient of beating up any male who tries to move in on the harem. Harem holders tend to win these fights against would-be usurpers, if only for the obvious reason that that is why they are harem-holders. Usurpers do not often win fights, because if they were capable of winning they would have done so before! Any female who mates only with a harem holder is therefore allying her genes with a male who is strong enough to beat off successive challenges from the large surplus of desperate bachelor males. With luck her sons will inherit their father's ability to hold a harem. In practice a female elephant seal does not have much option, because the harem-owner beats her up if she tries to stray. The principle remains, however, that females who choose to mate with males who win fights may benefit their genes by so doing. As we have seen, there are examples of females preferring to mate with males who hold territories and with males who have high status in the dominance hierarchy.

To sum up this chapter so far, the various different kinds of breeding system that we find among animals-monogamy, promiscuity, harems, and so on-can be understood in terms of conflicting interests between males and females. Individuals of either sex 'want' to maximize their total reproductive output during their lives. Because of a fundamental difference between the size and numbers of sperms and eggs, males are in general likely to be biased towards promiscuity and lack of paternal care. Females have two main available counter-ploys, which I have called the he-man and the domestic-bliss strategies. The ecological circumstances of a species will determine whether the females are biased towards one or the other of these counter-ploys, and will also determine how the males respond. In practice all intermediates between he-man and domestic-bliss are found and, as we have seen, there are cases in which the father does even more child-care than the mother. This book is not concerned with the details of particular animals species, so I will not discuss what might predispose a species towards one form of breeding system rather than another. Instead I will consider the differences that are commonly observed between males and females in general, and show how these may be interpreted. I shall therefore not be emphasizing those species in which the differences between the sexes are slight, these being in general the ones whose females have favoured the domestic-bliss strategy.

Firstly, it tends to be the males who go in for sexually attractive, gaudy colours, and the females who tend to be more drab. Individuals of both sexes want to avoid being eaten by predators, and there will be some evolutionary pressure on both sexes to be drably coloured. Bright colours attract predators no less than they attract sexual partners. In gene terms, this means that genes for bright colours are more likely to meet their end in the stomachs of predators than are genes for drab colours. On the other hand, genes for drab colours may be less likely than genes for bright colours to find themselves in the next generation, because drab individuals have difficulty in attracting a mate. There are therefore two conflicting selection pressures: predators tending to remove bright-colour genes from the gene pool, and sexual partners tending to remove genes for drabness. As in so many other cases, efficient survival machines can be regarded as a compromise between conflicting selection pressures. What interests us at the moment is that the optimal compromise for a male seems to be different from the optimal compromise for a female. This is of course fully compatible with our view of males as high-risk, high-reward gamblers. Because a male produces many millions of sperms to every egg produced by a female, sperms heavily outnumber eggs in the population. Any given egg is therefore much more likely to enter into sexual fusion than any given sperm is. Eggs are a relatively valuable resource, and therefore a female does not need to be so sexually attractive as a male does in order to ensure that her eggs are fertilized. A male is perfectly capable of siring all the children born to a large population of females. Even if a male has a short life because his gaudy tail attracts predators, or gets tangled in the bushes, he may have fathered a very large number of children before he dies. An unattractive or drab male may live even as long as a female, but he has few children, and his genes are not passed on. What shall it profit a male if he shall gain the whole world, and lose his immortal genes?

Another common sexual difference is that females are more fussy than males about whom they mate with. One of the reasons for fussiness by an individual of either sex is the need to avoid mating with a member of another species. Such hybridizations are a bad thing for a variety of reasons. Sometimes, as in the case of a man copulating with a sheep, the copulation does not lead to an embryo being formed, so not much is lost. When more closely related species like horses and donkeys cross-breed, however, the cost, at least to the female partner, can be considerable. An embryo mule is likely to be formed and it then clutters up her womb for eleven months. It takes a large quantity of her total parental investment, not only in the form of food absorbed through the placenta, and then later in the form of milk, but above all in time which could have been spent in rearing other children. Then when the mule reaches adulthood it turns out to be sterile. This is presumably because, although horse chromosomes and donkey chromosomes are sufficiently similar to cooperate in the building of a good strong mule body, they are not similar enough to work together properly in meiosis. Whatever the exact reason, the very considerable investment by the mother in the rearing of a mule is totally wasted from the point of view of her genes. Female horses should be very, very careful that the individual they copulate with is another horse, and not a donkey. In gene terms, any horse gene that says 'Body, if you are female, copulate with any old male, whether he is a donkey or a horse', is a gene which may next find itself in the dead-end body of a mule, and the mother's parental investment in that baby mule detracts heavily from her capacity to rear fertile horses. A male, on the other hand, has less to lose if he mates with a member of the wrong species, and, although he may have nothing to gain either, we should expect males to be less fussy in their choice of sexual partners. Where this has been looked at, it has been found to be true.