Sexual Antagonism, Temporally Fluctuating Selection, and Variable Dominance Affect a Regulatory Polymorphism in Drosophila melanogaster

• Published in: Molecular biology and evolution Vol. 38; no. 11; pp. 4891 - 4907
• Main Authors: Glaser-Schmitt, Amanda, Wittmann, Meike J, Ramnarine, Timothy J S, Parsch, John
• Format: Journal Article
• Language: English
• Published: United States Oxford University Press 27.10.2021
• Subjects: Animals; Biological diversity conservation; Biological Evolution; Discoveries; Drosophila; Drosophila melanogaster - genetics; Female; Gene expression; Gene Frequency; Genes; Genetic aspects; Genetic Variation; Humans; Male; Polymorphism, Genetic; Population genetics; Selection, Genetic; Single nucleotide polymorphisms; Sub-Saharan Africa; Germany; seasonal variation; sexual conflict; balancing selection; regulatory evolution; X chromosome; phenotypic variation
• ISSN: 0737-4038; 1537-1719
• DOI: 10.1093/molbev/msab215

Abstract Understanding how genetic variation is maintained within species is a major goal of evolutionary genetics that can shed light on the preservation of biodiversity. Here, we examined the maintenance of a regulatory single-nucleotide polymorphism (SNP) of the X-linked Drosophila melanogaster gene fezzik. The derived variant at this site is at intermediate frequency in many worldwide populations but absent in populations from the ancestral species range in sub-Saharan Africa. We collected and genotyped wild-caught individuals from a single European population biannually over a period of 5 years, which revealed an overall difference in allele frequency between the sexes and a consistent change in allele frequency across seasons in females but not in males. Modeling based on the observed allele and genotype frequencies suggested that both sexually antagonistic and temporally fluctuating selection may help maintain variation at this site. The derived variant is predicted to be female-beneficial and mostly recessive; however, there was uncertainty surrounding our dominance estimates and long-term modeling projections suggest that it is more likely to be dominant. By examining gene expression phenotypes, we found that phenotypic dominance was variable and dependent upon developmental stage and genetic background, suggesting that dominance may be variable at this locus. We further determined that fezzik expression and genotype are associated with starvation resistance in a sex-dependent manner, suggesting a potential phenotypic target of selection. By characterizing the mechanisms of selection acting on this SNP, our results improve our understanding of how selection maintains genetic and phenotypic variation in natural populations.