Mitochondrial genotype decreases mitochondrial respiration in seed beetles: implications for male subfertility

Abstract

Evolutionary theory suggests that inheritance of mitochondria through the maternal lineage could drive the accumulation of male-harming mutations in mitochondrial genomes. Namely, due to uniparental mode of mitochondrial inheritance, natural selection is “blind” to mutations that are deleterious to males as long as they are beneficial or neutral to females. This evolutionary phenomenon is known as ‘the Mother’s Curse’. The male-specific adverse effects of mitochondrial mutations are thought to be due to the fact that males are sensitive to impairments in the function of the oxidative phosphorylation (OXPHOS) system, i.e. mitochondrial respiration. The OXPHOS system consists of five complexes whose subunits are coded by the mitochondrial and nuclear genomes. In our previous work, we identified several mitochondrial haplotypes (mitotypes) in laboratory populations of the seed beetle (Acanthoscelides obtectus). One of them, MG3b mitotype, significantly reduces male fertility compared to other mitotypes when expressed in the same nuclear environment, but has no negative effects on females. In this study, we tested whether the MG3b mitotype affects OXPHOS functioning in males compared with other, control mitotypes. Specifically, we expressed MG3b and two control mitotypes alongside the same nuclear background and measured mitochondrial respiration in males using high-resolution respirometry. Our results show that respiration linked to all OXPHOS complexes is significantly reduced in MG3b males compared with controls. This is particularly true for the complex IV, which shows mean reduction in activity of around 40%. This work provides evidence that the decrease in mitochondrial respiration is the cause of subfertility of MG3b males.