Adaptive genetic complementarity in mate choice coexists with selection for elaborate sexual traits

Abstract

Choice of genetically unrelated mates is widely documented, yet it is not known how self-referential mate choice can co-occur with commonly observed directional selection on sexual displays. Across 10 breeding seasons in a wild bird population, we found strong fitness benefits of matings between genetically unrelated partners and show that self-referential choice of genetically unrelated mates alternates with sexual selection on elaborate plumage. Seasonal cycles of diminishing variation in ornamentation, caused by early pairing of the most elaborated males, and influx of increasingly genetically unrelated available mates caused by female-biased dispersal, lead to temporal fluctuations in the target of mate choice and enabled coexistence of directional selection for ornament elaboration with adaptive pairing of genetically unrelated partners.

Figure 1

Fitness consequences of offspring genetic diversity in house finches in 1995–2004. The proportion of nestlings per nest (n=117) that survived to the onset of dispersal is greater in nests with higher genetic diversity and earlier-initiated nests. Larger IR values indicate lesser genetic diversity.

Figure 2

Seasonal changes in genetic composition and sexual ornamentation in the breeding population. (a) Average pairwise relatedness of arriving females (filled circles, solid line) and males (filled triangles, dashed line) in relation to individuals of the same sex that were present in the population at the time of arrival (females: n=30, males: n=155). (b) Average pairwise relatedness of local resident, early-arriving non-local and late-arriving non-local males (filled bars) and females (open bars) in relation to unpaired mates in the population at the time of arrival. (c) Variation in sexual ornamentation of local males, early-arriving non-local and late-arriving non-local males (10 years, shown is the mean of coefficient of variation for each year+s.e.m). Numbers above the bars indicate the sample sizes.

Figure 3

Mate selection based on genetic relatedness and sexual ornamentation across the breeding season. (a) No difference in pairwise relatedness between potential partners at the time of pairing and chosen social partners early in the breeding season. Chosen extrapair males are less related to female than available males or chosen social males. Late in the breeding season, more genetically dissimilar social and extrapair mates were selected compared to all available mates. (b) Elaboration of sexual ornamentation in males available for pairing and males selected as social and extrapair mates early and late in the breeding season. Numbers above the bars indicate the sample sizes and solid lines connect groups that did not differ statistically. (c) Comparison of relatedness of individual females to their social and extrapair mates. Points below the dashed line of equal relatedness indicate that the female's extrapair male is less related to female than the female's social male.