Assessing the role of mitonuclear interactions on mitochondrial function and organismal fitness in natural Drosophila populations

Abstract Mitochondrial function depends on the effective interactions between proteins and RNA encoded by the mitochondrial and nuclear genomes. Evidence suggests that both genomes respond to thermal selection and promote adaptation. However, the contribution of their epistatic interactions to life history phenotypes in the wild remains elusive. We investigated the evolutionary implications of mitonuclear interactions in a real-world scenario that sees populations adapted to different environments, altering their geographical distribution while experiencing flow and admixture. We created a Drosophila melanogaster panel with replicate native populations from the ends of the Australian east-coast cline, into which we substituted the mtDNA haplotypes that were either predominant or rare at each cline-end, thus creating putatively mitonuclear matched and mismatched populations. Our results suggest that mismatching may impact phenotype, with populations harboring the rarer mtDNA haplotype suffering a trade-off between aerobic capacity and key fitness aspects such as reproduction, growth, and survival. We discuss the significance of mitonuclear interactions as modulators of life history phenotypes in the context of future adaptation and population persistence.