As I showed in a paper, there is a mistake in Trivers's reasoning here. He thought that prior investment in itself committed an individual to future investment. This is fallacious economics. A business man should never say 'I have already invested so much in the Concorde airliner (for instance) that I cannot afford to scrap it now.' He should always ask instead whether it would pay him in the future, to cut his losses, and abandon the project now, even though he has already invested heavily in it. Similarly, it is no use a female forcing a male to invest heavily in her in the hope that this, on its own, will deter the male from subsequently deserting. This version of the domestic-bliss strategy depends upon one further crucial assumption. This is that a majority of the females can be relied upon to play the same game. If there are loose females in the population, prepared to welcome males who have deserted their wives, then it could pay a male to desert his wife, no matter how much he has already invested in her children.
Much therefore depends on how the majority of females behave. If we were allowed to think in terms of a conspiracy of females there would be no problem. But a conspiracy of females can no more evolve than the conspiracy of doves which we considered in Chapter 5. Instead, we must look for evolutionarily stable strategies. Let us take Maynard Smith's method of analysing aggressive contests, and apply it to sex. It will be a little bit more complicated than the case of the hawks and doves, because we shall have two female strategies and two male strategies.
As in Maynard Smith's studies, the word 'strategy' refers to a blind unconscious behaviour program. Our two female strategies will be called coy and fast, and the two male strategies will be called faithful and philanderer. The behavioural rules of the four types are as follows. Coy females will not copulate with a male until he has gone through a long and expensive courtship period lasting several weeks. Fast females will copulate immediately with anybody. Faithful males are prepared to go on courting for a long time, and after copulation they stay with the female and help her to rear the young. Philanderer males lose patience quickly if a female will not copulate with them straight away: they go off and look for another female; after copulation too they do not stay and act as good fathers, but go off in search of fresh females. As in the case of the hawks and doves, these are not the only possible strategies, but it is illuminating to study their fates nevertheless.
Like Maynard Smith, we shall use some arbitrary hypothetical values for the various costs and benefits. To be more general it can be done with algebraic symbols, but numbers are easier to understand. Suppose that the genetic pay-off gained by each parent when a child is reared successfully is +15 units. The cost of rearing one child, the cost of all its food, all the time spent looking after it, and all the risks taken on its behalf, is -20 units. The cost is expressed as negative, because it is 'paid out' by the parents. Also negative is the cost of wasting time in prolonged courtship. Let this cost be -3 units.
Imagine we have a population in which all the females are coy, and all the males are faithful. It is an ideal monogamous society. In each couple, the male and the female both get the same average pay-off. They get +15 for each child reared; they share the cost of rearing it (-20) equally between the two of them, an average of -10 each. They both pay the -3 point penalty for wasting time in prolonged courtship. The average pay-off for each is therefore + 15 - 10 - 3 = + 2.
Now suppose a single fast female enters the population. She does very well. She does not pay the cost of delay, because she does not indulge in prolonged courtship. Since all the males in the population are faithful, she can reckon on finding a good father for her children whoever she mates with. Her average pay-off per child is
+ 15 - 10 = + 5. She is 3 units better off than her coy rivals. Therefore fast genes will start to spread.
If the success of fast females is so great that they come to predominate in the population, things will start to change in the male camp too. So far, faithful males have had a monopoly. But now if a philanderer male arises in the population, he starts to do better than his faithful rivals. In a population where all the females are fast, the pickings for a philanderer male are rich indeed. He gets the +15 points if a child is successfully reared, and he pays neither of the two costs. What this lack of cost mainly means to him is that he is free to go off and mate with new females. Each of his unfortunate wives struggles on alone with the child, paying the entire -20 point cost, although she does not pay anything for wasting time in courting. The net pay-off for a fast female when she encounters a philanderer male is + 15 - 20 = -5; the pay-off to the philanderer himself is +15. In a population in which all the females are fast, philanderer genes will spread like wildfire.
If the philanderers increase so successfully that they come to dominate the male part of the population, the fast females will be in dire straits. Any coy female would have a strong advantage. If a coy female encounters a philanderer male, no business results. She insists on prolonged courtship; he refuses and goes off in search of another female. Neither partner pays the cost of wasting time. Neither gains anything either, since no child is produced. This gives a net pay-off of zero for a coy female in a population where all the males are philanderers. Zero may not seem much, but it is better than the -5 which is the average score for a fast female. Even if a fast female decided to leave her young after being deserted by a philanderer, she would still have paid the considerable cost of an egg. So, coy genes start to spread through the population again.
To complete the hypothetical cycle, when coy females increase in numbers so much that they predominate, the philanderer males, who had such an easy time with the fast females, start to feel the pinch. Female after female insists on a long and arduous courtship. The philanderers flit from female to female, and always the story is the same. The net pay-off for a philanderer male when all the females are coy is zero. Now if a single faithful male should turn up, he is the only one with whom the coy females will mate. His net pay-off is + 2, better than that of the philanderers. So, faithful genes start to increase, and we come full circle.
As in the case of the aggression analysis, I have told the story as though it was an endless oscillation. But, as in that case, it can be shown that really there would be no oscillation. The system would converge to a stable state. If you do the sums, it turns out that a population in which 5/6 of the females are coy, and 5/8 of the males are faithful, is evolutionarily stable. This is, of course, just for the particular arbitrary numbers that we started out with, but it is easy to work out what the stable ratios would be for any other arbitrary assumptions.
As in Maynard Smith's analyses, we do not have to think of there being two different sorts of male and two different sorts of female. The ESS could equally well be achieved if each male spends 5/8 of his time being faithful and the rest of his time philandering; and each female spends 5/6 of her time being coy and 1/6 of her time being fast. Whichever way we think of the ESS, what it means is this. Any tendency for members of either sex to deviate from their appropriate stable ratio will be penalized by a consequent change in the ratio of strategies of the other sex, which is, in turn, to the disadvantage of the original deviant. Therefore the ESS will be preserved.
We can conclude that it is certainly possible for a population consisting largely of coy females and faithful males to evolve. In these circumstances the domestic-bliss strategy for females really does seem to work. We do not have to think in terms of a conspiracy of coy females. Coyness can actually pay a female's selfish genes.
There are various ways in which females can put this type of strategy into practice. I have already suggested that a female might refuse to copulate with a male who has not already built her a nest, or at least helped her to build a nest. It is indeed the case that in many monogamous birds copulation does not take place until after the nest is built. The effect of this is that at the moment of conception the male has invested a good deal more in the child than just his cheap sperms.
Demanding that a prospective mate shoul
d build a nest is one effective way for a female to trap him. It might be thought that almost anything that costs the male a great deal would do in theory, even if that cost is not directly paid in the form of benefit to the unborn children. If all females of a population forced males to do some difficult and costly deed, like slaying a dragon or climbing a mountain, before they would consent to copulate with them, they could in theory be reducing the temptation for the males to desert after copulation. Any male tempted to desert his mate and try to spread more of his genes by another female, would be put off by the thought that he would have to kill another dragon. In practice, however, it is unlikely that females would impose such arbitrary tasks as dragon-killing, or Holy-Grail-seeking on their suitors. The reason is that a rival female who imposed a task no less arduous, but more useful to her and her children, would have an advantage over more romantically minded females who demanded a pointless labour of love. Building a nest may be less romantic than slaying a dragon or swimming the Hellespont, but it is much more useful.
Also useful to the female is the practice I have already mentioned of courtship feeding by the male. In birds this has usually been regarded as a kind of regression to juvenile behaviour on the part of the female. She begs from the male, using the same gestures as a young bird would use. It has been supposed that this is automatically attractive to the male, in the same way as a man finds a lisp or pouting lips attractive in an adult woman. The female bird at this time needs all the extra food she can get, for she is building up her reserves for the effort of manufacturing her enormous eggs. Courtship feeding by the male probably represents direct investment by him in the eggs themselves. It therefore has the effect of reducing the disparity between the two parents in their initial investment in the young.
Several insects and spiders also demonstrate the phenomenon of courtship feeding. Here an alternative interpretation has sometimes been only too obvious. Since, as in the case of the praying mantis, the male may be in danger of being eaten by the larger female, anything that he can do to reduce her appetite may be to his advantage. There is a macabre sense in which the unfortunate male mantis can be said to invest in his children. He is used as food to help make the eggs which will then be fertilized, posthumously, by his own stored sperms.
A female, playing the domestic-bliss strategy, who simply looks the males over and tries to recognize qualities of fidelity in advance, lays herself open to deception. Any male who can pass himself off as a good loyal domestic type, but who in reality is concealing a strong tendency towards desertion and unfaithfulness, could have a great advantage. As long as his deserted former wives have any chance of bringing up some of the children, the philanderer stands to pass on more genes than a rival male who is an honest husband and father. Genes for effective deception by males will tend to be favoured in the gene pool.
Conversely, natural selection will tend to favour females who become good at seeing through such deception. One way they can do this is to play especially hard to get when they are courted by a new male, but in successive breeding seasons to be increasingly ready to accept quickly the advances of last year's mate. This will automatically penalize young males embarking on their first breeding season, whether they are deceivers or not. The brood of naive first year females would tend to contain a relatively high proportion of genes from unfaithful fathers, but faithful fathers have the advantage in the second and subsequent years of a mother's life, for they do not have to go through the same prolonged energy-wasting and time-consuming courtship rituals. If the majority of individuals in a population are the children of experienced rather than naive mothers-a reasonable assumption in any long-lived species- genes for honest, good fatherhood will come to prevail in the gene pool.
For simplicity, I have talked as though a male were either purely honest or thoroughly deceitful. In reality it is more probable that all males, indeed all individuals, are a little bit deceitful, in that they are programmed to take advantage of opportunities to exploit their mates. Natural selection, by sharpening up the ability of each partner to detect dishonesty in the other, has kept large-scale deceit down to a fairly low level. Males have more to gain from dishonesty than females, and we must expect that, even in those species where males show considerable parental altruism, they will usually tend to do a bit less work than the females, and to be a bit more ready to abscond. In birds and mammals this is certainly normally the case.
There are species, however, in which the male actually does more work in caring for the children than the female does. Among birds and mammals these cases of paternal devotion are exceptionally rare, but they are common among fish. Why? This is a challenge for the selfish gene theory which has puzzled me for a long time. An ingenious solution was recently suggested to me in a tutorial by Miss T. R. Carlisle. She makes use of Trivers's 'cruel bind' idea, referred to above, as follows.
Many fish do not copulate, but instead simply spew out their sex cells into the water. Fertilization takes place in the open water, not inside the body of one of the partners. This is probably how sexual reproduction first began. Land animals like birds, mammals and reptiles, on the other hand, cannot afford this kind of external fertilization, because their sex cells are too vulnerable to drying-up. The gametes of one sex-the male, since sperms are mobile-are introduced into the wet interior of a member of the other sex-the female. So much is just fact. Now comes the idea. After copulation, the land-dwelling female is left in physical possession of the embryo. It is inside her body. Even if she lays the fertilized egg almost immediately, the male still has time to vanish, thereby forcing the female into Trivers's 'cruel bind'. The male is inevitably provided with an opportunity to take the prior decision to desert, closing the female's options, and forcing her to decide whether to leave the young to certain death, or whether to stay with it and rear it. Therefore, maternal care is more common among land animals than paternal care.
But for fish and other water-dwelling animals things are very different. If the male does not physically introduce his sperms into the female's body there is no necessary sense in which the female is left 'holding the baby'. Either partner might make a quick getaway and leave the other one in possession of the newly fertilized eggs. But there is even a possible reason why it might often be the male who is most vulnerable to being deserted. It seems probable that an evolutionary battle will develop over who sheds their sex cells first. The partner who does so has the advantage that he or she can then leave the other one in possession of the new embryos. On the other hand, the partner who spawns first runs the risk that his prospective partner may subsequently fail to follow suit. Now the male is more vulnerable here, if only because sperms are lighter and more likely to diffuse than eggs. If a female spawns too early, i.e. before the male is ready, it will not greatly matter because the eggs, being relatively large and heavy, are likely to stay together as a coherent clutch for some time. Therefore a female fish can afford to take the 'risk' of spawning early. The male dare not take this risk, since if he spawns too early his sperms will have diffused away before the female is ready, and she will then not spawn herself, because it will not be worth her while to do so. Because of the diffusion problem, the male must wait until the female spawns, and then he must shed his sperms over the eggs. But she has had a precious few seconds in which to disappear, leaving the male in possession, and forcing him on to the horns of Trivers's dilemma. So this theory neatly explains why paternal care is common in water but rare on dry land.
Leaving fish, I now turn to the other main female strategy, the he-man strategy. In species where this policy is adopted the females, in effect, resign themselves to getting no help from the father of their children, and go all-out for good genes instead. Once again they use their weapon of withholding copulation. They refuse to mate with just any male, but exercise the utmost care and discrimination before they will allow a male to copulate with them. Some males undoubtedly do contain a larger number of good genes than other males, genes that would ben
efit the survival prospects of both sons and daughters. If a female can somehow detect good genes in males, using externally visible clues, she can benefit her own genes by allying them with good paternal genes. To use our analogy of the rowing crews, a female can minimize the chance that her genes will be dragged down through getting into bad company. She can try to hand-pick good crew-mates for her own genes.
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.
The Selfish Gene Page 21
