Abstract
BackgroundSex differences in lifespan are ubiquitous throughout the animal kingdom but the causes underlying this phenomenon remain poorly understood. Several explanations based on asymmetrical inheritance patterns (sex chromosomes or mitochondrial DNA) have been proposed, but these ideas have rarely been tested experimentally. Alternatively, sexual dimorphism in lifespan could result from sex-specific selection, caused by fundamental differences in how males and females optimize their fitness by allocating resources into current and future reproduction.ResultsHere we used sex-specific responses to inbreeding to study the genetic architecture of lifespan and mortality rates in Callosobruchus maculatus, a seed beetle that shows sexual dimorphism in lifespan. Two independent assays revealed opposing sex-specific responses to inbreeding. The combined data set showed that inbred males live longer than outbred males, while females show the opposite pattern. Both sexes suffered reduced fitness measured as lifetime reproductive success as a result of inbreeding.ConclusionNo model based on asymmetrical inheritance can explain increased male lifespan in response to inbreeding. Our results are however compatible with models based on sex-specific selection on reproductive strategies. We therefore suggest that sex-specific differences in lifespan in this species primarily result from sexually divergent selection.
Highlights
Sex differences in lifespan are ubiquitous throughout the animal kingdom but the causes underlying this phenomenon remain poorly understood
The fact that several recent studies have indicated that the mitochondria plays an active role in determining lifespan and mortality rates [15,16,17], coupled with the growing body of research showing that the genome of many species is under different selection pressures in males and females makes this hypothesis interesting, it cannot account for the reversal of sex-specific mortality rates seen across taxa
Sexual dimorphism for lifespan was pronounced across all levels of inbreeding, but no main effect of inbreeding was detected across the sexes for this trait (Fig. 2A, Table 1)
Summary
Sex differences in lifespan are ubiquitous throughout the animal kingdom but the causes underlying this phenomenon remain poorly understood. X- (or Z-) linked recessive deleterious mutations will be unconditionally expressed in the heterogametic sex and cause an overall higher mortality rate This hypothesis has, as far as we are aware, never been experimentally tested, but is consistent with the reversal of sex-specific mortality rates seen across mammals (heterogametic males) and birds (heterogametic females). The fact that several recent studies have indicated that the mitochondria plays an active role in determining lifespan and mortality rates [15,16,17], coupled with the growing body of research showing that the genome of many species is under different selection pressures in males and females (as shown by sexually differential gene expression [reviewed in [18]] and intra-genomic conflict [19,20,21,22]) makes this hypothesis interesting, it cannot account for the reversal of sex-specific mortality rates seen across taxa
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