Females postpone copulation to identify signs of fidelity in males

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 courtship 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.
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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 naïve 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 naïve 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.
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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 benefit 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.