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.
Even within a species, there may be reasons for fussiness. Incestuous mating, like hybridization, is likely to have damaging genetic consequences, in this case because lethal and semi-lethal recessive genes are brought out into the open. Once again, females have more to lose than males, since their investment in any particular child tends to be greater. Where incest taboos exist, we should expect females to be more rigid in their adherence to the taboos than males. If we assume that the older partner in an incestuous relationship is relatively likely to be the active initiator, we should expect that incestuous unions in which the male is older than the female should be more common than unions in which the female is older. For instance father/daughter incest should be commoner than mother/ son. Brother/sister incest should be intermediate in commonness. In general, males should tend to be more promiscuous than females. Since a female produces a limited number of eggs at a relatively slow rate, she has little to gain from having a large number of copulations with different males. A male on the other hand, who can produce millions of sperms every day, has everything to gain from as many promiscuous matings as he can snatch. Excess copulations may not actually cost a female much, other than a little lost time and energy, but they do not do her positive good. A male on the other hand can never get enough copulations with as many different females as possible: the word excess has no meaning for a male.
I have not explicitly talked about man but inevitably, when we think about evolutionary arguments such as those in this chapter, we cannot help reflecting about our own species and our own experience. Notions of females withholding copulation until a male shows some evidence of long-term fidelity may strike a familiar chord. This might suggest that human females play the domestic-bliss rather than the he-man strategy. Many human societies are indeed monogamous. In our own society, parental investment by both parents is large and not obviously unbalanced. Mothers certainly do more direct work for children than fathers do, but fathers often work hard in a more indirect sense to provide the material resources that are poured into the children. On the other hand, some human societies are promiscuous, and many are harem-based. What this astonishing variety suggests is that man's way of life is largely determined by culture rather than by genes. However, it is still possible that human males in general have a tendency towards promiscuity, and females a tendency towards monogamy, as we would predict on evolutionary grounds. Which of these two tendencies wins in particular societies depends on details of cultural circumstance, just as in different animal species it depends on ecological details.
One feature of our own society that seems decidedly anomalous is the matter of sexual advertisement. As we have seen, it is strongly to be expected on evolutionary grounds that, where the sexes differ, it should be the males that advertise and the females that are drab. Modern western man is undoubtedly exceptional in this respect. It is of course true that some men dress flamboyantly and some women dress drably but, on average, there can be no doubt that in our society the equivalent of the peacock's tail is exhibited by the female, not by the male. Women paint their faces and glue on false eyelashes. Apart from special cases, like actors, men do not. Women seem to be interested in their own personal appearance and they are encouraged in this by their magazines and journals. Men's magazines are less preoccupied with male sexual attractiveness, and a man who is unusually interested in his own dress and appearance is apt to arouse suspicion, both among men and among women. When a woman is described in conversation, it is quite likely that her sexual attractiveness, or lack of it, will be prominently mentioned. This is true, whether the speaker is a man or a woman. When a man is described, the adjectives used are much more likely to have nothing to do with sex.
Faced with these facts, a biologist would be forced to suspect that he was looking at a society in which females compete for males, rather than vice versa. In the case of birds of paradise, we decided that females are drab because they do not need to compete for males. Males are bright and ostentatious because females are in demand and can afford to be choosy. The reason female birds of paradise are in demand is that eggs are a more scarce resource than sperms. What has happened in modern western man? Has the male really become the sought-after sex, the one that is in demand, the sex that can afford to be choosy? If so, why?