No evidence for heritability of extra-pair mating behavior in a cooperatively breeding bird

While extra-pair mating prevails among socially monogamous birds, it does not occur in all individuals within a population. Then, what underlies this variability? A poorly explored mechanism is the genetic contribution to the behavioral trait, especially for cooperatively breeding species where promiscuity may potentially conflict with the acquisition of indirect benefits to altruistic helpers. We addressed the gap through a quantitative genetic approach with 8 years of data from an individually marked population of Tibetan ground tits (Pseudopodoces humilis). Extra-pair mating was observed in 33.2% of nests, and cooperative breeding occurred in 39.5% of nests. Animal models demonstrated no significant genetic component contributing to the variance in extra-pair mating both during a specific year and over an individual's lifetime. Consequently, the heritabilities were not significantly different from zero. The lack of heritable variation in extra-pair mating can be accounted for by Fisher's fundamental theorem of natural selection, which suggests that genotypes associated with this behavior facilitating reproductive success should have become widespread within the population. Furthermore, the fitness benefits derived from promiscuity were greater for breeders than those from receiving help; for helpers, the fitness benefits from extra-pair mating outweighed the indirect genetic benefits obtained from providing help. This may explain why extra-pair mating and cooperative breeding can coexist in the same population. Our findings imply that individual variation in performing extra-pair mating behavior is more likely to be influenced by environmental factors.