Sexy Son Hypothesis - Context

Context

Female mating preferences are widely recognized as being responsible for the rapid and divergent evolution of male secondary sexual traits. In 1976, prior to Weatherhead and Robertson's paper, Richard Dawkins had written in his book The Selfish Gene:

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.

The idea is that if females choose physically attractive males, they will tend to get physically attractive sons, and therefore more grandchildren, because choosy females will prefer their attractive, "sexy" sons. The theory will function regardless of the physical or behavioral trait a female chooses, as long as it is heritable, because it is possessing the trait that makes males attractive, and not the qualities of the trait in itself. Thus, traits culturally perceived as negative can still be seen as desirable; for example, females who stay with or are attracted to males they know to be disloyal in a monogamous relationship. If this trait is passed to any male children, they are more likely to themselves be non-monogamous, have several mates and spread the female's genes to multiple grandchildren. The sexy son hypothesis is one of several possible explanations for the highly diverse and often astonishing ornaments of animals.

Once a preference becomes established, females choosing males with elaborate secondary sexual traits will produce sons that carry alleles for the trait and daughters that carry alleles for the preference, generating genetic coupling that will drive self-reinforcing coevolution of both trait and preference, due to the mating advantage of males with the trait. Thus, the original viability benefits associated with the preference can be undermined by a Fisherian runaway sexy sons process. Similar models have been proposed for postcopulatory female preferences, such as the time at which females removed the male's sperm ampulla after mating. Sexual selection by direct and/or indirect benefits as well as sexual conflict determine the evolution of animal mating systems.

In its original context, the "narrow-sense sexy son hypothesis" of Weatherhead and Robertson refers to mating systems with care from both parents. In these mating systems, females that mate with a polygynous male normally receive less assistance than females mated with a monogamous male, and thus suffer from direct fitness consequences that have to be (at least) compensated for by the breeding successes of their sexy sons. On the other hand, a "broad-sense sexy son hypothesis" encompasses both polygyny and promiscuous mating systems, with and without care from both parents. Alatalo (1998) argues that the costs of any additional choice may be so minor that female choice for honestly signaling males, that is good genes, may evolve even if the indirect benefits on offspring quality are small. A similar argument can be made for the sexy son hypothesis if mates of attractive males do not suffer any direct fitness consequences.