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 quality(1-3); however, the nature of these genetic benefits is debated(1-4). 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'(1-5). Evidence for the latter process is accumulating(2,6): matings between relatives lead to decreased reproductive success, and the individual level of inbreeding-measured as average heterozygosity-is a strong fitness predictor(7-13). Females should thus benefit from mating with genetically dissimilar males(2,14). In many birds, social monogamy restricts mate choice, but females may circumvent this by pursuing extra-pair copulations(15,16). 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.