Sex differences in deleterious mutational effects in Drosophila melanogaster: combining quantitative and population genetic insights. Issue 3 (2nd September 2021)

• Record Type: Journal Article
• Authors: Ruzicka, Filip; Connallon, Tim; Reuter, Max
• Editors: Wolf, J
• Is Part Of: Genetics. Volume 219:Issue 3(2021)
• Publication Date: 2021-09-02
• Subjects: sex differences -- fitness -- GWAS -- X chromosome -- autosomes -- purifying selection -- deleterious polymorphism -- dominance -- population genetics -- quantitative genetics; Genetics -- Periodicals; 576.5
• DOI: 10.1093/genetics/iyab143
• Languages: English
• ISSNs: 0016-6731

Abstract

Abstract: Fitness effects of deleterious mutations can differ between females and males due to: ( i ) sex differences in the strength of purifying selection; and ( ii ) sex differences in ploidy. Although sex differences in fitness effects have important broader implications ( e.g., for the evolution of sex and lifespan), few studies have quantified their scope. Those that have belong to one of two distinct empirical traditions: ( i ) quantitative genetics, which focusses on multi-locus genetic variances in each sex, but is largely agnostic about their genetic basis; and ( ii ) molecular population genetics, which focusses on comparing autosomal and X-linked polymorphism, but is poorly suited for inferring contemporary sex differences. Here, we combine both traditions to present a comprehensive analysis of female and male adult reproductive fitness among 202 outbred, laboratory-adapted, hemiclonal genomes of Drosophila melanogaster . While we find no clear evidence for sex differences in the strength of purifying selection, sex differences in ploidy generate multiple signals of enhanced purifying selection for X-linked loci. These signals are present in quantitative genetic metrics— i.e., a disproportionate contribution of the X to male (but not female) fitness variation—and population genetic metrics— i.e., steeper regressions of an allele's average fitness effect on its frequency, and proportionally less nonsynonymous polymorphism on the X than autosomes. Fitting our data to models for both sets of metrics, we infer that deleterious alleles are partially recessive. Given the often-large gap between quantitative and population genetic estimates of evolutionary parameters, our study showcases the benefits of combining genomic and fitness data when estimating such parameters.