In vivo male fertility is affected by naturally occurring mitochondrial haplotypes

We harness an experimental design that enables us to completely disentangle mitochondrial from nuclear genetic effects in the fruit fly Drosophila melanogaster. Using this design, we directly link male fertility outcomes to the mitochondrial haplotype. Specifically, we show that competitive male fertility, measured in vivo, differs across naturally occurring mitochondrial haplotypes. We discuss this result in the context of recent studies that support the evolutionary hypothesis according to which maternal inheritance of mitochondria will facilitate the accumulation of male-harming mutations in the mitochondrial genome, when these same mutations are benign, beneficial or slightly deleterious in their effects on females 1, 2 and 3. We predict that at least some of the mitochondrial allelic variance affecting competitive male fertility across the sampled haplotypes will have accumulated under this evolutionary process and be male-specific in its effect on the phenotype. We suggest that the existence of male-harming mitochondrial mutations for male fertility would place strong selection on the interacting nuclear genome to evolve compensatory counter-adaptations that offset the negative effects, and we present support for this idea.