The sexy son hypothesis in evolutionary biology and sexual selection, proposed by Patrick J. Weatherhead and Raleigh J. Robertson of Queen's University in Kingston, Ontario in 1979, states that a female's ideal mate choice among potential mates is one whose genes will produce males with the best chance of reproductive success. This implies that other benefits the father can offer the mother or offspring are less relevant than they may appear, including his capacity as a parental caregiver, territory and any nuptial gifts. Fisher's principle means that the sex ratio (except in certain eusocial insects) is always near 1:1 between males and females, yet what matters most are her "sexy sons'" future breeding successes, more likely if they have a promiscuous father, in creating large numbers of offspring carrying copies of her genes. This sexual selection hypothesis has been researched in species such as the European pied flycatcher.
Context
Female mating preferences are widely recognized as being responsible for the rapid and divergent evolution of male secondary sex characteristics. In 1915, Ronald Fisher wrote:
Granted that while this taste and preference prevails among the females of the species, the males will grow more and more elaborate and beautiful tail feathers, the question must be answered "Why have the females this taste? Of what use is it to the species that they should select this seemingly useless ornament?" The first step to a solution lies in the fact that the success of an animal in the struggle for existence is not measured only by the number of offspring which it produces and rears, but also by the probable success of these offspring. So that in selecting a mate from a number of different competitors, it is important to select that one which is most likely to produce successful children.
In 1976, prior to Weatherhead and Robertson's paper, Richard Dawkins had written in his book The Selfish Gene:
Ronald Fisher's principle, as published in his book The Genetical Theory of Natural Selection, is one of several possible explanations for the highly diverse and often astonishing ornaments of animals. If females choose physically attractive males, they will tend to get physically attractive sons, and, thus more grandchildren, because other 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 (that is, the trait varies between individuals of the population), because it is possessing the trait that makes males attractive, and not the qualities of the trait in itself. Once a preference becomes established, females choosing males with elaborate secondary sexual traits will produce sons that carry alleles for the trait and produce 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, creating 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.