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Author(s): Kenneth M. Fedorka (corresponding author) [1, 2]; Timothy A. Mousseau [1] Indirect-benefit models of sexual selection assert that females gain heritable offspring advantages through a mating bias for males [...]

Mother's curse refers to male-biased deleterious mutations that may accumulate on mitochondria due to its strict maternal inheritance. If these mutations persist, males should ideally compensate through mutations on Y-chromosomes given its strict paternal inheritance. Previous work addressed this hypothesis by comparing coevolved and non-coevolved Y-mitochondria pairs placed alongside completely foreign autosomal backgrounds, expecting males with coevolved pairs to exhibit greater fitness due to Y-compensation. To date, no evidence for Y-compensation has been found. That experimental design assumes Y-chromosomes compensate via direct interaction with mitochondria and/or coevolved autosomes are unimportant in its function or elucidation. If Y-chromosomes instead compensate by modifying autosomal targets (or its elucidation requires coevolved autosomes), then this design could fail to detect Y-compensation. Here we address if Y-chromosomes 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 lower mortality risk relative to non-coevolved pairs. In contrast, 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. However, we cannot fully 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 backgrounds should be used with caution, as they may disrupt Y-autosome coadaptation and/or inadvertently unbridle mother's curse., Competing Interests: Competing interests: The authors declare no competing interests. Ethics: The work reported in this study was conducted on an invertebrate species that required no research ethics approval or oversight., (© 2024. The Author(s), under exclusive licence to The Genetics Society.)

How natural selection facilitates sexually dimorphic evolution despite a shared genome is unclear. The patrilineal inheritance of Y-chromosomes makes them an appealing solution. However, they have largely been dismissed due to their gene-poor, heterochromatic nature and because the additive genetic variation necessary for adaptive evolution is theoretically difficult to maintain. Further, previous empirical work has revealed mostly Y-linked sign epistatic variance segregating within populations, which can often impede adaptive evolution. To assess the evolutionary impact of Y-linked variation, we established replicate populations in Drosophila simulans containing multiple Y-chromosomes (YN populations) or a single Y-chromosome variant (Y1 populations) drawn from a single population. We estimated male and female heritabilities for several traits known to be influenced by Y-chromosomes, including the number of sternopleural bristles, abdominal bristles, sex comb teeth, and tibia length. A decrease in YN heritabilities compared with Y1 would be consistent with Y-chromosome variation being sign epistatic. A decrease in Y1 heritabilities would be consistent with Y-chromosome variation being additive, though additive-by-additive epistatic variation cannot be entirely dismissed. Female heritability estimates served as controls and were not expected to differ. We found male Y1 populations exhibited lower heritabilities for all traits except tibia length; consistent with Y-linked additivity (on average YN trait heritabilities were 25% greater than Y1). Female estimates showed no difference. These data suggest Y-chromosomes should play an important role in male trait evolution and may even influence sexually dimorphic evolution by shaping traits shared by both sexes., (© 2023. The Author(s), under exclusive licence to The Genetics Society.)