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. Genotypes where mitochondrial and nuclear genomes from different geographic populations are combined (mismatched) are therefore predicted to result in negative fitness consequences. Such negative fitness effects are expected to be prominent in males, since maternal inheritance of mitochondria can lead to accumulation of male-harming mutations (the mother's curse hypothesis), and they may become more prevalent with aging. To test these predictions, we measured fertility traits of females and males at different ages using a genetically diverse panel of 27 mitonuclear populations of Drosophila melanogaster with matched or experimentally mismatched mitonuclear genomes. We found no evidence that novel mitonuclear combinations had reduced fitness in females. In males, we found limited evidence of mitonuclear interactions affecting fitness in old age, however, not in the direction predicted. Novel mitonuclear combinations were associated with males that sired more offspring. 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.