Mitochondrial genotypes affect thermal plasticity of longevity in Drosophila melanogaster

Sequence variation in mitochondrial DNA (mtDNA) was once considered neutral, but growing evidence indicates it can influence metabolic, physiological, and life-history traits. Two hypotheses offer explanations for this non-neutral mtDNA variation: the mitochondrial climatic adaptation hypothesis, which posits that natural selection shapes mtDNA variation to match local environments, and the mother's curse hypothesis, which predicts the accumulation of male-harming variants due to maternal inheritance. We explored these hypotheses using genetic strains of Drosophila melanogaster bearing eight mtDNA haplotypes-nested within two distinct haplogroups (A1 and B1) that segregate along an Australian latitudinal cline. We measured the longevity of flies under cool (18°C) and warm (28°C) conditions, predicting that the A1 haplogroup-which has been reported to predominate at subtropical latitudes-would confer higher longevity in warm but reduced longevity in cool temperatures relative to the B1 counterpart. We also tested whether effects of mtDNA haplotype on longevity were larger in males, as predicted under the mother's curse hypothesis. We found mtDNA haplogroup and haplotype is associated with longevity, with the magnitude of effects varying with temperature, but not in a pattern consistent with either hypothesis. Haplogroup-by-environment interactions did not align with reported spatial distributions of the haplogroups, and haplotype effects on longevity were similar across sexes. Our findings add to the growing evidence that mtDNA variation contributes to thermal plasticity in longevity, but do not provide clear insight into whether this variation is adaptive or maladaptive.