Females prefer the scent of outbred males: good-genes-as-heterozygosity?

Background: There is increasing interest to determine the relative importance of non-additive genetic benefits as opposed to additive ones for the evolution of mating preferences and maintenance of genetic variation in sexual ornaments. The 'good-genes-as-heterozygosity' hypothesis predicts that females should prefer to mate with more heterozygous males to gain more heterozygous (and less inbred) offspring. Heterozygosity increases males' sexual ornamentation, mating success and reproduction success, yet few experiments have tested whether females are preferentially attracted to heterozygous males, and none have tested whether females' own heterozygosity influences their preferences. Outbred females might have the luxury of being more choosey, but on the other hand, inbred females might have more to gain by mating with heterozygous males. We manipulated heterozygosity in wild-derived house mice (Mus musculus musculus) through inbreeding and tested whether the females are more attracted to the scent of outbred versus inbred males, and whether females' own inbreeding status affects their preferences. We also tested whether infecting both inbred and outbred males with Salmonella would magnify females' preferences for outbred males. Results: Females showed a significant preference for outbred males, and this preference was more pronounced among inbred females. We found no evidence that Salmonella infection increased the relative attractiveness of outbred versus inbred males; however, we found no evidence that inbreeding affected males' disease resistance in this study. Conclusion: Our findings support the idea that females are more attracted to outbred males, and they suggest that such preferences may be stronger among inbred than outbred females, which is consistent with the 'good-genes-as-heterozygosity' hypothesis. It is unclear whether this odour preference reflects females' actual mating preferences, though it suggests that future studies should consider females' as well as males' heterozygosity. Our study has implications for efforts to understand how mate choice can provide genetic benefits without eroding genetic diversity (lek paradox), and also conservation efforts to determine the fitness consequences of inbreeding and the maintenance of genetic diversity in small, inbred populations.