Direct and indirect genetic effects of sex-specific mitonuclear epistasis on reproductive ageing

Abstract

Mitochondria are involved in ageing and their function requires coordinated action of both mitochondrial and nuclear genes. Epistasis between the two genomes can influence lifespan but whether this also holds for reproductive senescence is unclear. Maternal inheritance of mitochondria predicts sex differences in the efficacy of selection on mitonuclear genotypes that should result in differences between females and males in mitochondrial genetic effects. Mitonuclear genotype of a focal individual may also indirectly affect trait expression in the mating partner. We tested these predictions in the seed beetle Callosobruchus maculatus, using introgression lines harbouring distinct mitonuclear genotypes. Our results reveal both direct and indirect sex-specific effects of mitonuclear epistasis on reproductive ageing. Females harbouring coadapted mitonuclear genotypes showed higher lifetime fecundity due to slower senescence relative to novel mitonuclear combinations. We found no evidence for mitonuclear coadaptation in males. Mitonuclear epistasis not only affected age-specific ejaculate weight, but also influenced male age-dependent indirect effects on traits expressed by their female partners (fecundity, egg size, longevity). These results demonstrate important consequences of sex-specific mitonuclear epistasis for both mating partners, consistent with a role for mitonuclear genetic constraints upon sex-specific adaptive evolution.

Figure 1

Summary of the experimental design. We recorded data of age-specific reproductive performance and lifespan from mitonuclear introgression lines (I) and a reference population females (R) mated to the introgression line males. For the focal females, provided with a mating opportunity with four sets of reference virgin males (1–2-day-old virgin), we collected data from six age intervals. For the focal males and their reference female mates (1–2-day-old virgin), we collected data from six male age points. The symbols indicate data collected from each experimental group at each time point (open and closed symbols show which variables were recorded at a given time).

Figure 2

Daily egg-laying rate declines at a lower rate in females with a coadapted mitonuclear genotype (a), resulting in a higher lifetime reproductive success compared with females with a novel mitonuclear genotype (b). Figures show model predictions.

Figure 3

Direct mitonuclear epistatic effects on age-specific male ejaculate weight. Means represent model predictions.

Figure 4

Indirect effects of male age and mitonuclear genotype on female reproductive traits. Male age affects female fecundity but the decline over male age differs across mtDNA haplotypes (a) and depends upon an interaction between mitonuclear coadaptation and the nuclear genetic background (b). The different nuclear lineages are shown in panels. Means represent model predictions.

Figure 5

Female longevity increases with decreasing male age, but this general pattern also depends upon the male mtDNA haplotype (a) and an interaction between mitonuclear coadaptation and the nuclear genetic background (b). Means represent model predictions.