Recurrent Selection on the Winters sex-ratio Genes in Drosophila simulans

Abstract

Selfish genes, such as meiotic drive elements, propagate themselves through a population without increasing the fitness of host organisms. X-linked (or Y-linked) meiotic drive elements reduce the transmission of the Y (X) chromosome and skew progeny and population sex ratios, leading to intense conflict among genomic compartments. Drosophila simulans is unusual in having a least three distinct systems of X chromosome meiotic drive. Here, we characterize naturally occurring genetic variation at the Winters sex-ratio driver (Distorter on the X or Dox), its progenitor gene (Mother of Dox or MDox), and its suppressor gene (Not Much Yang or Nmy), which have been previously mapped and characterized. We survey three North American populations as well as 13 globally distributed strains and present molecular polymorphism data at the three loci. We find that all three genes show signatures of selection in North America, judging from levels of polymorphism and skews in the site-frequency spectrum. These signatures likely result from the biased transmission of the driver and selection on the suppressor for the maintenance of equal sex ratios. Coalescent modeling indicates that the timing of selection is more recent than the age of the alleles, suggesting that the driver and suppressor are coevolving under an evolutionary ''arms race.'' None of the Winters sex-ratio genes are fixed in D. simulans, and at all loci we find ancestral alleles, which lack the gene insertions and exhibit high levels of nucleotide polymorphism compared to the derived alleles. In addition, we find several ''null'' alleles that have mutations on the derived Dox background, which result in loss of drive function. We discuss the possible causes of the maintenance of presence-absence polymorphism in the Winters sex-ratio genes.

Genome-wide patterns of natural variation reveal strong selective sweeps and ongoing genomic conflict in Drosophila mauritiana

“…5; Supplemental Fig. S2): Alleles of the paralogous genes Mother of Dox (MDox) and Dox function as drivers in a well-characterized sex-ratio meiotic drive system in D. simulans (Tao et al 2007a;Kingan et al 2010). The estimated selection coefficient s ranges from 0.12 to 0.39, depending on the parameter values used (Supplemental Table S13), which could be consistent with strong selection during genomic conflict (Curtsinger 1984).…”

“…The second selective sweep might be caused by the Winters meiotic drive system, which is well-characterized in D. simulans (Tao et al 2007a,b;Kingan et al 2010). This system consists of at least three components: the drivers MDox and Dox, the autosomal dominant suppressor Nmy, and the enhancer of Dox [E(Dox)].…”

“…In some D. simulans populations, the Dox gene shows evidence of a partial selective sweep (Kingan et al 2010), but it is difficult to distinguish highly localized selective sweeps from random fluctuations in variability due to the bottleneck associated with the out of Africa expansion (Jensen et al 2005). We further scrutinized the genomic region around Dox using Pool-seq data from African D. simulans (V Nolte and C Schlötterer, unpubl.)…”

“…Due to the preferential transmission, such elements spread in the population and can leave a characteristic trace of strongly reduced variability in the genome that resembles a selective sweep (Derome et al 2004). Population genetic analyses of segregation distortion systems in Drosophila did not find a molecular signature similar to a classic selective sweep (Derome et al 2004(Derome et al , 2008Presgraves et al 2009;Kingan et al 2010;Bastide et al 2011). The patterns of variability instead resembled partial selective sweeps, suggesting that the genetic element increased in frequency but did not reach fixation.…”

Natural variation of the Y chromosome suppresses sex ratio distortion and modulates testis-specific gene expression in Drosophila simulans

“…Males with the Winters sex-ratio also show reduced fertility (Tao et al, 2007b). Furthermore, the Winters system is polymorphic in natural populations with segregating variation that shows evidence of recent selection in both distorters and suppressors (Kingan et al, 2010). Indeed, the invasion of sex-ratio distorters sets the stage for the evolution of genetic suppressors as well as behavioral and physiological mechanisms that might alleviate the fitness cost incurred by a biased sex-ratio (Price et al, 2008).…”