The role of genetic constraints and social environment in explaining female extra-pair mating

Why do females of socially monogamous species engage in extra-pair copulations? This long-standing question remains a puzzle, because the benefits of female promiscuous behavior often do not seem to outweigh the costs. Genetic constraint models offer an answer by proposing that female promiscuity emerges through selection favoring alleles that are either beneficial for male reproductive success (intersexual pleiotropy hypothesis) or beneficial for female fecundity (intrasexual pleiotropy hypothesis). A previous quantitative genetic study on captive zebra finches, Taeniopygia guttata, reported support for the first, but not for the second hypothesis. Here, we re-examine both hypotheses based on data from lines selected for high and low male courtship rate. In contrast to previous conclusions, our new analyses clearly reject the hypothesis that male and female promiscuity are genetically homologous traits. We find some support for a positive genetic correlation between female promiscuity and fecundity. This study also shows that the behavioral outcome of extra-pair courtships primarily depends on individual-specific female preferences and not on the “attractiveness” of the social mate. In contrast, patterns of paternity are strongly influenced by the social partner and the pair bond, presumably reflecting variation in copulation behavior, fertility, or sperm competitiveness.