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

• Published in: Heredity Vol. 133; no. 6; pp. 418 - 425
• Main Authors: Nielsen, Tobias Møgelvang, Baldwin, Jaden, Danis, Megan, Fedorka, Kenneth M.
• Format: Journal Article
• Language: English
• Published: Cham Springer International Publishing 01.12.2024; Springer Nature B.V
• Subjects: 631/181/2474; 631/208/182; 64/24; Animals; Biomedical and Life Sciences; Biomedicine; Chromosomes; Coadaptation; Coevolution; Compensation; Cytogenetics; Design of experiments; Drosophila melanogaster; Drosophila melanogaster - genetics; Drosophila melanogaster - physiology; Ecology; Evolutionary Biology; Experimental design; Female; Fruit flies; Health risks; Human Genetics; Insects; Life span; Longevity - genetics; Male; Males; Maternal inheritance; Maternal Inheritance - genetics; Mitochondria; Mitochondria - genetics; Mortality; Mortality risk; Mutation; Plant Genetics and Genomics; Selection, Genetic; Somatic chromosomes; Target detection; Y Chromosome - genetics; Y chromosomes
• ISSN: 0018-067X; 1365-2540; 1365-2540
• DOI: 10.1038/s41437-024-00726-w

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.