The unguarded-X and the genetic architecture of lifespan: Inbreeding results in a potentially maladaptive sex-specific reduction of female lifespan in Drosophila melanogaster

Sex differences in ageing and lifespan are ubiquitous in nature. The unguarded-X hypothesis (UXh) suggests they may be partly due to the expression of recessive mutations in the hemizygous sex chromosomes of the heterogametic sex, which could help explain sex-specific ageing in a broad array of taxa. A prediction central to the UX hypothesis is that inbreeding will decrease the lifespan of the homogametic sex more than the heterogametic sex, because only in the former does inbreeding increase the expression of recessive deleterious mutations. In this study, we test this prediction by examining the effects of inbreeding on the lifespan and fitness of male and female Drosophila melanogaster across different social environments. We found that, across social environments, inbreeding resulted in a greater reduction of female than male lifespan, and that inbreeding effects on fitness did not seem to counterbalance sex-specific effects on lifespan, suggesting the former are maladaptative. Inter- and intra-sexual correlation analyses also allowed us to identify evidence of an underlying joint genetic architecture for inbreeding effects on lifespan. We discuss these results in light of the UXh and other alternative explanations, and suggest that more attention should be paid to the possibility that the unguarded-X may play an important role in the evolution of sex-specific lifespan.