Support for Y-compensation of mother’s curse affecting lifespan in Drosophila melanogaster

Mother’s curse refers to male-biased deleterious mutations that may accumulate on the mitochondria due to its strict maternal inheritance. If these mutations persist, males should ideally compensate through mutations on the Y-chromosome given its strict paternal inheritance. Previous work has addressed this hypothesis by comparing coevolved and non-coevolved Y-mitochondria pairs placed alongside foreign autosomal backgrounds, expecting males with coevolved pairs to exhibit greater fitness due to Y-compensation. To date, no evidence of Y-compensation has been found. Such an experimental design assumes that Y-chromosomes compensate via direct interaction with mitochondria and/or is independent of autosome evolutionary history. If Y-chromosomes instead compensate by modifying autosomal targets, then this design could obscure Y-compensation by disrupting Y-autosome or mitochondria-autosome coadaptation. Here we address whether Y-chromosomes could ameliorate mitochondrial mutations affecting male lifespan in Drosophila melanogaster. Using three disparate populations we compared lifespan among males with coevolved and non-coevolved Y-mitochondria pairs placed alongside autosomal backgrounds coevolved with mitochondria. We found coevolved pairs exhibited a lower mortality risk relative to non-coevolved pairs. No such pattern was observed when coevolved and non-coevolved pairs were placed alongside non-coevolved autosomes, as with previous studies. These data are consistent with Y-compensation and highlight the importance of autosomes in this capacity. We cannot however exclude the possibility that Y-autosomal coevolution independent of mitochondrial mutations contributed to our results. Regardless, modern practices in medicine, conservation, and agriculture that introduce foreign Y-chromosomes into non-coevolved genetic backgrounds should be used with caution, as they may disrupt Y-autosome coadaptation and/or inadvertently unbridle mother’s curse.