Mitochondrial genotype interacts with age and sex, but not nuclear background, to shape locomotory performance across mitonuclear strains of fruit flies

The discovery that mitochondrial genomes can harbor functional mutations despite the evolutionarily conserved role of mitochondria has spurred interest in better understanding the ecological and evolutionary consequences of such mitochondrial genetic variation. Because mitochondrial DNA (mtDNA) encodes products that must function in concert with products of the nuclear genome, and because mitochondria are largely maternally inherited, outstanding questions remain as to how, when, and why variation in mtDNA may affect phenotype. In this study, we developed a set of intraspecific “mitonuclear strains” of Drosophila melanogaster fruit flies that vary across 13 mtDNA haplotypes and 3 nuclear genetic backgrounds. We created a new apparatus called the Drop Tower to test the performance of these strains in negative geotaxis, a locomotory trait we predicted to be sensitive to variation at the level of mitochondria, across both sexes and two age classes. We found that both mitochondrial and nuclear genetic variation significantly altered how negative geotaxis performance changed with age and across the sexes, though interactions between mitochondrial and nuclear strains did not affect performance. Across most strains, male flies performed more poorly and suffered a steeper decline with age than did females, and young males appeared to vary more in performance across mitochondrial strains. In addition, we discovered a strong effect of small differences of parental age on negative geotaxis— and this effect also varied by mitochondrial strain. Collectively, the results of our study reveal that intraspecific variation in both mitochondrial and nuclear DNA can affect age- and sex-related differences in fruit fly locomotory performance. Further exploring the mechanisms linking these subtle genetic differences to locomotory phenotype and creating differences in response between the sexes will be important to understanding the evolutionary forces shaping the patterns we detected.