Female extrapair mating behavior can evolve via indirect selection on males

Abstract

In many species that form socially monogamous pair bonds, a considerable proportion of the offspring is sired by extrapair males. This observation has remained a puzzle for evolutionary biologists: although mating outside the pair bond can obviously increase the offspring production of males, the benefits of such behavior to females are less clear, yet females are known to actively solicit extrapair copulations. For more than two decades adaptionist explanations have dominated the discussions, yet remain controversial, and genetic constraint arguments have been dismissed without much consideration. An intriguing but still untested hypothesis states that extrapair mating behavior by females may be affected by the same genetic variants (alleles) as extrapair mating behavior by males, such that the female behavior could evolve through indirect selection on the male behavior. Here we show that in the socially monogamous zebra finch, individual differences in extrapair mating behavior have a hereditary component. Intriguingly, this genetic basis is shared between the sexes, as shown by a strong genetic correlation between male and female measurements of extrapair mating behavior. Hence, positive selection on males to sire extrapair young will lead to increased extrapair mating by females as a correlated evolutionary response. This behavior leads to a fundamentally different view of female extrapair mating: it may exist even if females obtain no net benefit from it, simply because the corresponding alleles were positively selected in the male ancestors.

Fig. 1.

Genetic correlations between aspects of male and female extrapair mating behavior. (A) Average estimates of genetic correlations (± SEM) obtained from a series of five-trait animal models (Tables S3–S6). Between-sex genetic correlations (red) among traits related to extrapair mating are large and positive. For illustration, we show some of the data on which the most crucial estimates for between-sex correlations are based (B and C). (B) The average responsiveness score of 141 females when courted by an extrapair male (total n = 3,958 courtships) in relation to their estimated breeding value for male courtship rate. Breeding values are from a single-trait permanent environment model conducted in VCE (based on courtship rates from a total of 800 male relatives). Responsiveness scores vary from −1 (aggression) to +1 (solicitation). Dot size refers to the number of extrapair courtships observed for each female (range: 1–138, median: 19). A weighted regression line is shown (r = 0.33). (C) The average proportion of extrapair paternity among the eggs laid by 149 females (total n = 2,253 eggs) in relation to their estimated breeding value for male courtship rate. Dot size refers to the number of eggs laid by each female (range: 1–45, median: 14). A weighted regression line is shown (r = 0.19), suggesting a 2.9-fold increase in extrapair paternity levels over the observed range of female breeding values of male courtship rate. The large amount of scatter is because of the many other factors that influence paternity besides heritable differences in female extrapair mating behavior.