Mother’s curse and indirect genetic effects: do males matter to mitochondrial genome evolution?

Abstract

Maternal inheritance of mitochondrial DNA (mtDNA) was originally thought to prevent any response to selection on male phenotypic variation attributable to mtDNA, resulting in a male‐biased mtDNA mutation load (‘mother’s curse’). However, the theory underpinning this claim implicitly assumes that a male’s mtDNA has no effect on the fitness of females he comes into contact with. If such ‘mitochondrially‐encoded indirect genetics effects’ (mtIGEs) do in fact exist, and there is relatedness between the mitochondrial genomes of interacting males and females, male mtDNA‐encoded traits can undergo adaptation after all. We tested this possibility using strains of Drosophila melanogaster that differ in their mtDNA. Our experiments indicate that female fitness is influenced by the mtDNA carried by males that the females encounter, which could plausibly allow the mitochondrial genome to evolve via kin selection. We argue that mtIGEs are probably common, and that this might ameliorate or exacerbate mother’s curse.