The Selfish Gene

by Richard Dawkins

  Males, then, seem to be pretty worthless fellows, and on simple 'good of the species' grounds, we might expect that males would become less numerous than females. Since one male can theoretically produce enough sperms to service a harem of 100 females we might suppose that females should outnumber males in animal populations by 100 to 1. Other ways of putting this are that the male is more 'expendable', and the female more 'valuable' to the species. Of course, looked at from the point of view of the species as a whole, this is perfectly true. To take an extreme example, in one study of elephant seals, 4 per cent of the males accounted for 88 per cent of all the copulations observed. In this case, and in many others, there is a large surplus of bachelor males who probably never get a chance to copulate in their whole lives. But these extra males live otherwise normal lives, and they eat up the population's food resources no less hungrily than other adults. From a 'good of the species' point of view this is horribly wasteful; the extra males might be regarded as social parasites. This is just one more example of the difficulties that the group selection theory gets into. The selfish gene theory, on the other hand, has no trouble in explaining the fact that the numbers of males and females tend to be equal, even when the males who actually reproduce may be a small fraction of the total number. The explanation was first offered by R. A. Fisher.

  The problem of how many males and how many females are born is a special case of a problem in parental strategy. Just as we discussed the optimal family size for an individual parent trying to maximize her gene survival, we can also discuss the optimal sex ratio. Is it better to entrust your precious genes to sons or to daughters? Suppose a mother invested all her resources in sons, and therefore had none left to invest in daughters: would she on average contribute more to the gene pool of the future than a rival mother who invested in daughters? Do genes for preferring sons become more or less numerous than genes for preferring daughters? What Fisher showed is that under normal circumstances the stable sex ratio is 50:50. In order to see why, we must first know a little bit about the mechanics of sex determination.

  In mammals, sex is determined genetically as follows. All eggs are capable of developing into either a male or a female. It is the sperms that carry the sex-determining chromosomes. Half the sperms produced by a man are female-producing, or X-sperms, and half are male-producing, or Y-sperms. The two sorts of sperms look alike. They differ with respect to one chromosome only. A gene for making a father have nothing but daughters could achieve its object by making him manufacture nothing but X-sperms. A gene for making a mother have nothing but daughters could work by making her secrete a selective spermicide, or by making her abort male embryos. What we seek is something equivalent to an evolutionarily stable strategy (ESS), although here, even more than in the chapter on aggression, strategy is just a figure of speech. An individual cannot literally choose the sex of his children. But genes for tending to have children of one sex or the other are possible. If we suppose that such genes, favouring unequal sex ratios, exist, are any of them likely to become more numerous in the gene pool than their rival alleles, which favour an equal sex ratio?

  Suppose that in the elephant seals mentioned above, a mutant gene arose that tended to make parents have mostly daughters. Since there is no shortage of males in the population, the daughters would have no trouble finding mates, and the daughter-manufacturing gene could spread. The sex ratio in the population might then start to shift towards a surplus of females. From the point of view of the good of the species, this would be all right, because just a few males are quite capable of providing all the sperms needed for even a huge surplus of females, as we have seen. Superficially, therefore, we might expect the daughter-producing gene to go on spreading until the sex ratio was so unbalanced that the few remaining males, working flat out, could just manage. But now, think what an enormous genetic advantage is enjoyed by those few parents who have sons. Anyone who invests in a son has a very good chance of being the grandparent of hundreds of seals. Those who are producing nothing but daughters are assured of a safe few grandchildren, but this is nothing compared to the glorious genetic possibilities that open up before anyone specializing in sons. Therefore genes for producing sons will tend to become more numerous, and the pendulum will swing back.

  For simplicity I have talked in terms of a pendulum swing. In practice the pendulum would never have been allowed to swing that far in the direction of female domination, because the pressure to have sons would have started to push it back as soon as the sex ratio became unequal. The strategy of producing equal numbers of sons and daughters is an evolutionarily stable strategy, in the sense that any gene for departing from it makes a net loss.

  I have told the story in terms of numbers of sons versus numbers of daughters. This is to make it simple, but strictly it should be worked out in terms of parental investment, meaning all the food and other resources that a parent has to offer, measured in the way discussed in the previous chapter. Parents should invest equally in sons and daughters. This usually means they should have numerically as many sons as they have daughters. But there could be unequal sex ratios that were evolutionarily stable, provided correspondingly unequal amounts of resources were invested in sons and daughters. In the case of the elephant seals, a policy of having three times as many daughters as sons, but of making each son a supermale by investing three times as much food and other resources in him, could be stable. By investing more food in a son and making him big and strong, a parent might increase his chances of winning the supreme prize of a harem. But this is a special case. Normally the amount invested in each son will roughly equal the amount invested in each daughter, and the sex ratio, in terms of numbers, is usually one to one.

  In its long journey down the generations therefore, an average gene will spend approximately half its time sitting in male bodies, and the other half sitting in female bodies. Some gene effects show themselves only in bodies of one sex. These are called sex-limited gene effects. A gene controlling penis-length expresses this effect only in male bodies, but it is carried about in female bodies too and may have some quite different effect on female bodies. There is no reason why a man should not inherit a tendency to develop a long penis from his mother.

  In whichever of the two sorts of body it finds itself, we can expect a gene to make the best use of the opportunities offered by that sort of body. These opportunities may well differ according to whether the body is male or female. As a convenient approximation, we can once again assume that each individual body is a selfish machine, trying to do the best for all its genes. The best policy for such a selfish machine will often be one thing if it is male, and quite a different thing if it is female. For brevity, we shall again use the convention of thinking of the individual as though it had a conscious purpose. As before, we shall hold in the back of our mind that this is just a figure of speech. A body is really a machine blindly programmed by its selfish genes.

  Consider again the mated pair with which we began the chapter. Both partners, as selfish machines, 'want' sons and daughters in equal numbers. To this extent they agree. Where they disagree is in who is going to bear the brunt of the cost of rearing each one of those children. Each individual wants as many surviving children as possible. The less he or she is obliged to invest in any one of those children, the more children he or she can have. The obvious way to achieve this desirable state of affairs is to induce your sexual partner to invest more than his or her fair share of resources in each child, leaving you free to have other children with other partners. This would be a desirable strategy for either sex, but it is more difficult for the female to achieve. Since she starts by investing more than the male, in the form of her large, food-rich egg, a mother is already at the moment of conception 'committed' to each child more deeply than the father is. She stands to lose more if the child dies than the father does. More to the point, she would have to invest more than the father in the future in order to bring a new substitute child up to the same level of de
velopment. If she tried the tactic of leaving the father holding the baby, while she went off with another male, the father might, at relatively small cost to himself, retaliate by abandoning the baby too. Therefore, at least in the early stages of child development, if any abandoning is going to be done, it is likely to be the father who abandons the mother rather than the other way around. Similarly, females can be expected to invest more in children than males, not only at the outset, but throughout development. So, in mammals for example, it is the female who incubates the foetus in her own body, the female who makes the milk to suckle it when it is born, the female who bears the brunt of the load of bringing it up and protecting it. The female sex is exploited, and the fundamental evolutionary basis for the exploitation is the fact that eggs are larger than sperms.

  Of course in many species the father does work hard and faithfully at looking after the young. But even so, we must expect that there will normally be some evolutionary pressure on males to invest a little bit less in each child, and to try to have more children by different wives. By this I simply mean that there will be a tendency for genes that say 'Body, if you are male leave your mate a little bit earlier than my rival allele would have you do, and look for another female', to be successful in the gene pool. The extent to which this evolutionary pressure actually prevails in practice varies greatly from species to species. In many, for example in the birds of paradise, the female receives no help at all from any male, and she rears her children on her own. Other species such as kittiwakes form monogamous pairbonds of exemplary fidelity, and both partners cooperate in the work of bringing up children. Here we must suppose that some evolutionary counter-pressure has been at work: there must be a penalty attached to the selfish mate-exploitation strategy as well as a benefit, and in kittiwakes the penalty outweighs the benefit. It will in any case only pay a father to desert his wife and child if the wife has a reasonable chance of rearing the child on her own.

  Trivers has considered the possible courses of action open to a mother who has been deserted by her mate. Best of all for her would be to try to deceive another male into adopting her child, 'thinking' it is his own. This might not be too difficult if it is still a foetus, not yet born. Of course, while the child bears half her genes, it bears no genes at all from the gullible step-father. Natural selection would severely penalize such gullibility in males and indeed would favour males who took active steps to kill any potential step-children as soon as they mated with a new wife. This is very probably the explanation of the so-called Bruce effect: male mice secrete a chemical which when smelt by a pregnant female can cause her to abort. She only aborts if the smell is different from that of her former mate. In this way. a male mouse destroys his potential step-children, and renders his new wife receptive to his own sexual advances. Ardrey, incidentally, sees the Bruce effect as a population control mechanism! A similar example is that of male lions, who, when newly arrived in a pride, sometimes murder existing cubs, presumably because these are not their own children.

  A male can achieve the same result without necessarily killing step-children. He can enforce a period of prolonged courtship before he copulates with a female, driving away all other males who approach her, and preventing her from escaping. In this way he can wait and see whether she is harbouring any little step-children in her womb, and desert her if so. We shall see below a reason why a female might want a long 'engagement' period before copulation. Here we have a reason why a male might want one too. Provided he can isolate her from all contact with other males, it helps to avoid being the unwitting benefactor of another male's children.

  Assuming then that a deserted female cannot fool a new male into adopting her child, what else can she do? Much may depend on how old the child is. If it is only just conceived, it is true that she has invested the whole of one egg in it and perhaps more, but it may still pay her to abort it and find a new mate as quickly as possible. In these circumstances it would be to the mutual advantage both of her and of the potential new husband that she should abort-since we are assuming she has no hope of fooling him into adopting the child. This could explain why the Bruce effect works from the female's point of view.

  Another option open to a deserted female is to stick it out, and try and rear the child on her own. This will especially pay her if the child is already quite old. The older he is the more has already been invested in him, and the less it will take out of her to finish the job of rearing him. Even if he is still quite young, it might yet pay her to try to salvage something from her initial investment, even if she has to work twice as hard to feed the child, now that the male has gone. It is no comfort to her that the child contains half the male's genes too, and that she could spite him by abandoning it. There is no point in spite for its own sake. The child carries half her genes, and the dilemma is now hers alone.

  Paradoxically, a reasonable policy for a female who is in danger of being deserted might be to walk out on the male before he walks out on her. This could pay her, even if she has already invested more in the child than the male has. The unpleasant truth is that in some circumstances an advantage accrues to the partner who deserts first, whether it is the father or the mother. As Trivers puts it, the partner who is left behind is placed in a cruel bind. It is a rather horrible but very subtle argument. A parent may be expected to desert, the moment it is possible for him or her to say the following: ' This child is now far enough developed that either of us could finish off rearing it on our own. Therefore it would pay me to desert now, provided I could be sure my partner would not desert as well. If I did desert now, my partner would do whatever is best for her/his genes. He/ she would be forced into making a more drastic decision than I am making now, because I would have already left. My partner would "know" that if he/she left as well, the child would surely die. Therefore, assuming that my partner will take the decision that is best for his/her own selfish genes, I conclude that my own best course of action is to desert first. This is especially so, since my partner may be "thinking" along exactly the same lines, and may seize the initiative at any minute by deserting me!' As always, the subjective soliloquy is intended for illustration only. The point is that genes for deserting first could be favourably selected simply because genes for deserting second would not be.

  We have looked at some of the things that a female might do if she has been deserted by her mate. But these all have the air of making the best of a bad job. Is there anything a female can do to reduce the extent to which her mate exploits her in the first place? She has a strong card in her hand. She can refuse to copulate. She is in demand, in a seller's market. This is because she brings the dowry of a large, nutritious egg. A male who successfully copulates gains a valuable food reserve for his offspring. The female is potentially in a position to drive a hard bargain before she copulates. Once she has copulated she has played her ace-her egg has been committed to the male. It is all very well to talk about driving hard bargains, but we know very well it is not really like that. Is there any realistic way in which something equivalent to driving a hard bargain could evolve by natural selection? I shall consider two main possibilities, called the domestic-bliss strategy, and the he-man strategy.

  The simplest version of the domestic-bliss strategy is this. The female looks the males over, and tries to spot signs of fidelity and domesticity in advance. There is bound to be variation in the population of males in their predisposition to be faithful husbands. If females could recognize such qualities in advance, they could benefit themselves by choosing males possessing them. One way for a female to do this is to play hard to get for a long time, to be coy. Any male who is not patient enough to wait until the female eventually consents to copulate is not likely to be a good bet as a faithful husband. By insisting on a long engagement period, a female weeds out casual suitors, and only finally copulates with a male who has proved his qualities of fidelity and perseverance in advance. Feminine coyness is in fact very common among animals, and so are prolonged courtsh
ip or engagement periods. As we have already seen, a long engagement can also benefit a male where there is a danger of his being duped into caring for another male's child.

  Courtship rituals often include considerable pre-copulation investment by the male. The female may refuse to copulate until the male has built her a nest. Or the male may have to feed her quite substantial amounts of food. This, of course, is very good from the female's point of view, but it also suggests another possible version of the domestic-bliss strategy. Could females force males to invest so heavily in their offspring before they allow copulation that it would no longer pay the males to desert after copulation? The idea is appealing. A male who waits for a coy female eventually to copulate with him is paying a cost: he is forgoing the chance to copulate with other females, and he is spending a lot of time and energy in courting her. By the time he is finally allowed to copulate with a particular female, he will inevitably be heavily 'committed' to her. There will be little temptation for him to desert her, if he knows that any future female he approaches will also procrastinate in the same manner before she will get down to business.