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.