Females with attractive mates gain environmental benefits that increase lifetime and multi-generational fitness

Resolving the degree to which environmental (direct) vs. genetic (indirect) benefits shape female mate choice is a long-standing challenge, particularly for socially monogamous species where male environmental and genetic contributions are difficult to disentangle. This study combines long-term population monitoring with quantitative genetic analyses in a socially monogamous but sexually promiscuous Australian songbird to demonstrate that female mating preferences are driven by non-genetic environmental benefits that increase the fitness of both the female and her offspring. Male Red-backed Fairywrens (Malurus melanocephalus) flexibly breed in either ornamented or unornamented plumage, and females consistently prefer ornamented males. Females paired with ornamented males bred earlier and allocated more to current reproduction, yet experienced higher survival and lifetime fitness. Furthermore, these females produced more grand-offspring because their early-born sons were more likely to be ornamented and to breed successfully than the later-born sons of females with unornamented partners. Quantitative genetic models showed lifetime fitness was best explained by parental environment rather than genetic effects. Mating preferences in this system are maintained by a combination of primary environmental benefits that increase the lifetime fitness of choosy females, and secondary environmental benefits that increase the multi-generational fitness of those females through enhanced offspring quality and performance.