Autosomal and X-Linked Additive Genetic Variation for Lifespan and Aging: Comparisons Within and Between the Sexes in Drosophila melanogaster

Robert M Griffin, Holger Schielzeth, Urban Friberg

Theory makes several predictions concerning differences in genetic variation between the X chromosome and the autosomes due to male X hemizygosity. The X chromosome should i) typically show relatively less standing genetic variation than the autosomes, ii) exhibit more variation in males compared to females because of dosage compensation, and iii) potentially be enriched with sex-specific genetic variation. Here we address each of these predictions for lifespan and aging in Drosophila melanogaster To achieve unbiased estimates of X and autosomal additive genetic variance we use 80 chromosome substitution lines; 40 for the X chromosome and 40 combining the two major autosomes, which we assay for sex-specific and cross-sex genetic (co)variation. We find significant X and autosomal additive genetic variance for both traits in both sexes (with reservation for X linked variation of aging in females), but no conclusive evidence for depletion of X linked variation (measured through females). Males display more X linked variation for lifespan than females, but it is unclear if this is due to dosage compensation since also autosomal variation is larger in males. Finally, our results suggest the X chromosome is enriched for sex-specific genetic variation in lifespan. Results were overall less conclusive for aging. Collectively these results suggest the X chromosome has reduced capacity to respond to sexually concordant selection on lifespan from standing genetic variation, while its ability to respond to sexually antagonistic selection may be augmented.