Why do females have so few extra-pair offspring?

It is generally accepted that if a female can improve her offspring’s genetics via extra-pair copulations (EPC), it is by copulating with extra-pair males whose phenotypes are more superior or whose genes are more compatible to hers than those of her bonded male. Here, we present a model that puts together uncertainties about the male genetic quality, a postcopulatory sperm bias in favor of the better or the more compatible genes, and costs that females pay by being choosy about extra-pair male quality. The model’s conclusions challenge traditional views of good genes explanations of EPC. When phenotypes give incomplete information about genotypes, a female choosing a phenotypically superior extra-pair male, may nevertheless find herself trading good genes of a bonded male for poor genes of an extra-pair male. Such “unfortunate sperm replacements” can limit the female involvement in EPC even when EPC are otherwise cost-free. The model also shows that even a female bonded to a phenotypically superior male may benefit by EPC, provided that sperm competition is biased toward sperm with more fit or more compatible genes. Furthermore, if choosiness is sufficiently costly, a female may even do best by copulating with a random extra-pair male.