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

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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. Genetic conflicts among genes happen when their modes of transmission differ. Genes in the heterogametic (XY) sex can be grouped as X-linked, Y-linked, autosomal, or cytoplasmic. Sex ratio in the progeny greatly affects the transmission advantage of each of the four types of genes, with the optimal sex ratio for each type being respectively 100%, 0%, 50%, and 100% of females. Sex ratio can often be biased from the normal 50% by genes that distort the sex ratio toward their own optimal transmission. Here we report genetic and molecular characterization of an autosomal gene that functions as a suppressor of an X-linked sex-ratio distorter. Male mutants give rise to female-biased progeny. The cause of the distortion was assigned to a failure of the Y-bearing sperm to mature. The DNA sequence of the suppressor gives clues to understanding the sex-ratio meiotic drive at the molecular level. More generally, the genetic conflict over sex ratio may be important in determining the evolutionary dynamics and the architecture of eukaryotic genomes.