title: Sex-specific trans-regulatory variation on the Drosophila melanogaster X chromosome.
abstract: The X chromosome constitutes a unique genomic environment because it is present in one copy in males, but two copies in females. This simple fact has motivated several theoretical predictions with respect to how standing genetic variation on the X chromosome should differ from the autosomes. Unmasked expression of deleterious mutations in males and a lower census size are expected to reduce variation, while allelic variants with sexually antagonistic effects, and potentially those with a sex-specific effect, could accumulate on the X chromosome and contribute to increased genetic variation. In addition, incomplete dosage compensation of the X chromosome could potentially dampen the male-specific effects of random mutations, and promote the accumulation of X-linked alleles with sexually dimorphic phenotypic effects. Here we test both the amount and the type of genetic variation on the X chromosome within a population of Drosophila melanogaster, by comparing the proportion of X linked and autosomal trans-regulatory SNPs with a sexually concordant and discordant effect on gene expression. We find that the X chromosome is depleted for SNPs with a sexually concordant effect, but hosts comparatively more SNPs with a sexually discordant effect. Interestingly, the contrasting results for SNPs with sexually concordant and discordant effects are driven by SNPs with a larger influence on expression in females than expression in males. Furthermore, the distribution of these SNPs is shifted towards regions where dosage compensation is predicted to be less complete. These results suggest that intrinsic properties of dosage compensation influence either the accumulation of different types of trans-factors and/or their propensity to accumulate mutations. Our findings document a potential mechanistic basis for sex-specific genetic variation, and identify the X as a reservoir for sexually dimorphic phenotypic variation. These results have general implications for X chromosome evolution, as well as the genetic basis of sex-specific evolutionary change.
authors: Department of Animal and Plant Sciences, University of Sheffield, Sheffield, United Kingdom; Department of Plant Ecology and Evolution, Uppsala University, Uppsala, Sweden.
authors: Michael
authors: M
authors: Stocks
authors: Department of Evolutionary Biology, Uppsala University, Uppsala, Sweden; Department of Genetics, Evolution and Environment, University College London, London, United Kingdom.
authors: Rebecca
authors: R
authors: Dean
authors: Department of Animal Ecology, Uppsala University, Uppsala, Sweden; Department of Zoology, Stockholm University, Stockholm, Sweden.
authors: Björn
authors: B
authors: Rogell
authors: Department of Evolutionary Biology, Uppsala University, Uppsala, Sweden; IFM Biology, AVIAN Behaviour and Genomics group, Linköping University, Linköping, Sweden.
authors: Urban
authors: U
authors: Friberg
mesh_terms: D000483:Alleles; D000818:Animals; D004303:Dosage Compensation, Genetic; D004331:Drosophila melanogaster / Q000235:genetics*; D019143:Evolution, Molecular; D005260:Female; D018507:Gene Expression Regulation, Developmental; D050172:Genes, X-Linked; D008297:Male; D009154:Mutation; D020641:Polymorphism, Single Nucleotide; D012727:Sex Characteristics; D014960:X Chromosome / Q000235:genetics*