Sex differences in the genetic architecture of lifespan in a seed beetle: extreme inbreeding extends male lifespan

Abstract

Background: Sex 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.

Results: Here 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.

Conclusion: No 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.

Figure 1

Schematic design of construction of genotypes. Triplets of genotypes with three levels of inbreeding were obtained using isogenic lines. Outbred genotypes (F~0) were obtained by crossing two isogenic lines (F~0.89). Male offspring from such crosses were crossed to females from the maternal isogenic line. Offspring from this cross inherited a haploid maternal genome from their mother and a haploid genome from their father, of which half came from the maternal line. Theses individuals were therefore homozygous for approximately 44.5% of their genome. Inbred genotypes came from maternal within-line crosses. With this design, genotypes of three levels of inbreeding produced by each pair of isogenic lines shared the same maternal genome, controlling for maternal effects variation among genotypes within a line-pair.

Figure 2

Sex-specific effect of inbreeding on lifespan in Callosobruchus maculatus beetles. Lifespan (mean days, error bars = SE) of females and males in the longevity assays. (A) Assay I, testing three levels of inbreeding. (B) Assay II, testing two levels of inbreeding, (C) Combined effect of inbreeding (two levels) on lifespan. Significant differences between levels of inbreeding, by contrast analysis, are indicated by different letters.

Figure 3

Age specific mortality curves in Callosobruchus maculatus beetles, first assay. Age-specific mortality hazard (ln Ux) for outbred, intermediate and inbred cohorts of males (A) and females (B) from assay I, using pooled data across lines on daily mortality for each treatment.

Figure 4

Age specific mortality curves in Callosobruchus maculatus beetles, second assay. Age-specific mortality hazard (ln Ux) for outbred and inbred cohorts of males (A) and females (B) from assay II, using pooled data across lines on daily mortality for each treatment.