A sex-ratio Meiotic Drive System in Drosophila simulans. I: An Autosomal Suppressor

Abstract

Sex ratio distortion (sex-ratio for short) has been reported in numerous species such as Drosophila, where distortion can readily be detected in experimental crosses, but the molecular mechanisms remain elusive. Here we characterize an autosomal sex-ratio suppressor from D. simulans that we designate as not much yang (nmy, polytene chromosome position 87F3). Nmy suppresses an X-linked sex-ratio distorter, contains a pair of near-perfect inverted repeats of 345 bp, and evidently originated through retrotransposition from the distorter itself. The suppression is likely mediated by sequence homology between the suppressor and distorter. The strength of sex-ratio is greatly enhanced by lower temperature. This temperature sensitivity was used to assign the sex-ratio etiology to the maturation process of the Y-bearing sperm, a hypothesis corroborated by both light microscope observations and ultrastructural studies. It has long been suggested that an X-linked sex-ratio distorter can evolve by exploiting loopholes in the meiotic machinery for its own transmission advantage, which may be offset by other changes in the genome that control the selfish distorter. Data obtained in this study help to understand this evolutionary mechanism in molecular detail and provide insight regarding its evolutionary impact on genomic architecture and speciation.

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

“…Y chromosomes from 78 isofemale stocks of D. simulans were introgressed into a nearly identical background (SR1227: w Dox; nt; nmy[sim1427]) (Tao et al, 2007b), using a cross scheme (Supplementary Figure S1) in which all chromosomes except the fourth were tracked with phenotypic markers. These stocks include 44 collected in the Carlson Orchards, Harvard, Massachusetts and 34 of global origin (Supplementary Table S1).…”

“…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 average expression level of 37 accessory gland-specific genes is significantly higher in males expressing more biased sex ratio (Figures 4a and b). Notably, protease inhibitors are accessory gland-specific proteins (Figure 4c) that are able to prevent the premature breakdown of the mating plug and increase sperm vitality (Park and Wolfner, 1995;Chapman, 2001), and that might function to mitigate the lower fitness incurred by sex-ratio males (Tao et al, 2007b). Although higher expression of accessory gland proteins (ACPs) might contribute to partly compensate for impaired testis-specific gene expression in males with skewed sexratio (Linklater et al, 2007;Dowling and Simmons, 2012), we cannot formally distinguish between adaptive and non-adaptive mechanisms underlying variation in ACP expression.…”

“…Sex-ratio describes a genetic phenomenon in which the offspring sex ratio deviates from the 50% female expectation. At least three sex ratio distortion systems have been uncovered in D. simulans, namely the Paris, the Durham and the Winters systems (Tao et al, 2007b). In the Paris sex-ratio system, the Y chromosome has high frequency of breakage and non-disjunction during meiosis II (Cazemajor et al, 2000).…”

“…Distortion is caused by the X-linked gene Dox (Distorter on the X; Tao et al, 2007a). In offspring sired by males in which the autosomal suppressor Nmy (not much yang) is removed, the sex ratio is strongly female biased (Tao et al, 2007b).…”