Testing for age- and sex- specific mitonuclear epistasis in Drosophila

The need for efficient ATP production is predicted to result in the evolution of cooperation between the mitochondrial and nuclear encoded components of the electron transport system. Novel (i.e., mismatched) mitonuclear genotype combinations are therefore predicted to result in negative fitness consequences, which may become more prevalent with ageing. Such negative fitness effects are expected to be prominent in males, since maternal inheritance of mitochondria is predicted to lead to accumulation of male-harming mutations (the mother’s curse hypothesis). To test these predictions, we measured female and male fertility traits using a genetically diverse panel of 27 mitonuclear populations of Drosophila melanogaster with matched or experimentally mismatched mitonuclear genomes at different ages. We found no overall effect of mitonuclear mismatch. In females, we found no effect of mitonuclear epistasis. In males, we found limited evidence of mitonuclear epistasis affecting fitness in old age, however, not in the direction predicted. Experimentally mismatched males sired more offspring in one comparison. Sex-specific advantages of mismatched males might arise if novel nuclear alleles compensate for deleterious mitochondrial alleles that have accumulated. If such compensatory effects of novel mitonuclear combinations increasing fitness occur in nature, they could represent a possible counterforce to the mother’s curse.