Fast females, slow males: accelerated ageing and reproductive senescence in Drosophila melanogaster females across diverse social environments

Females and males typically differ in lifespan, patterns of ageing, and reproduction. General explanations for variation in the magnitude of this sex-specificity remain elusive, and the role of the social environment in this context is under-explored. Sexual selection theory predicts that males should adopt a “live fast, die young” strategy, as their fitness is likely to be contingent on intense investment to achieve success in competing for potentially few matings. However, there is a growing realization that sexual selection can act on a much broader suite of “general performance” traits than only those directly related to mating competition. This, combined with frequently observed high costs of reproduction in females, makes an alternative prediction—that ageing and reproductive senescence can be high for females, and could potentially exceed what is seen in males. We tested these contrasting predictions in the fruit fly Drosophila melanogaster, using assays in which both sexes competed for reproductive opportunities over their lifetimes within varying socio-sexual environments. Females consistently exhibited “live fast, die young” life histories, whereas males had significantly longer lifespans and showed only limited declines in age-specific fitness and mating performance. We also identified new same-sex exposure effects—females housed with females exhibited faster reproductive ageing at a marginal lifespan cost, whereas corresponding males maintained higher courtship and activity with age, with no detectable effect on lifespan. The results highlight the crucial importance of social environments to the study of ageing and fitness. The possibility that rapid reproductive senescence is widespread in females is key to broadening our holistic understanding of the biology of sex differences in ageing and reproduction.