Genomic conflict drives patterns of X-linked population structure in Drosophila neotestacea.

ABSTRACT

Intragenomic conflict has the potential to cause widespread changes in patterns of genetic diversity and genome evolution. In this study, we investigate the consequences of sex-ratio (SR) drive on the population genetic patterns of the X-chromosome in Drosophila neotestacea. An SR X-chromosome prevents the maturation of Y-bearing sperm during male spermatogenesis and thus is transmitted to ~100% of the offspring, nearly all of which are daughters. Selection on the rest of the genome to suppress SR can be strong, and the resulting conflict over the offspring sex ratio can result in the accumulation of multiple loci on the X-chromosome that are necessary for the expression of drive. We surveyed variation at 12 random X-linked microsatellites across 16 populations of D. neotestacea that range in SR frequency from 0% to 30%. First, every locus was differentiated between SR and wild-type chromosomes, and this drives genetic structure at the X-chromosome. Once the association with SR is accounted for, the patterns of differentiation among populations are similar to the autosomes. Second, within wild-type chromosomes, the relative heterozygosity is reduced in populations with an increased prevalence of drive, and the heterozygosity of SR chromosomes is higher than expected based on its prevalence. The combination of the relatively high prevalence of SR drive and the structuring of polymorphism between the SR and wild-type chromosomes suggests that genetic conflict because of SR drive has had significant consequences on the patterns of X-linked polymorphism and thus also probably affects the tempo of X-chromosome evolution in D. neotestacea.