Females increase offspring heterozygosity and fitness through extra-pair matings

Females in a variety of species commonly mate with multiple males, and there is evidence that they benefit by producing offspring of higher genetic quality1,2,3; however, the nature of these genetic benefits is debated1,2,3,4. Enhanced offspring survival or quality can result from intrinsic effects of paternal genes—‘good genes’—or from interactions between the maternal and paternal genomes—‘compatible genes’1,2,3,4,5. Evidence for the latter process is accumulating2,6: matings between relatives lead to decreased reproductive success, and the individual level of inbreeding—measured as average heterozygosity—is a strong fitness predictor7,8,9,10,11,12,13. Females should thus benefit from mating with genetically dissimilar males2,14. In many birds, social monogamy restricts mate choice, but females may circumvent this by pursuing extra-pair copulations15,16. Here we show that female blue tits, Parus caeruleus, increase the heterozygosity of their progeny through extra-pair matings. Females thereby produce offspring of higher reproductive value, because less inbred individuals have increased survival chances, a more elaborate male secondary sexual trait (crown colour) and higher reproductive success. The cost of inbreeding may therefore be an important factor driving the evolution of female extra-pair mating.