A sex-ratio Meiotic Drive System in Drosophila simulans. II: An X-linked Distorter

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Abstract
The evolution of heteromorphic sex chromosomes creates a genetic condition favoring the invasion of sex-ratio meiotic drive elements, resulting in the biased transmission of one sex chromosome over the other, in violation of Mendel's first law. The molecular mechanisms of sex-ratio meiotic drive may therefore help us to understand the evolutionary forces shaping the meiotic behavior of the sex chromosomes. Here we characterize a sex-ratio distorter on the X chromosome (Dox) in Drosophila simulans by genetic and molecular means. Intriguingly, Dox has very limited coding capacity. It evolved from another X-linked gene, which also evolved de nova. Through retrotransposition, Dox also gave rise to an autosomal suppressor, not much yang (Nmy). An RNA interference mechanism seems to be involved in the suppression of the Dox distorter by the Nmy suppressor. Double mutant males of the genotype dox; nmy are normal for both sex-ratio and spermatogenesis. We postulate that recurrent bouts of sex-ratio meiotic drive and its subsequent suppression might underlie several common features observed in the heterogametic sex, including meiotic sex chromosome inactivation and achiasmy. Mendel's first law of genetics states that two alleles of a heterozygote are transmitted to the next generation at an equal ratio. The cornerstone of population genetics, this law states that the evolutionary fate of genetic variants is solely governed by their contribution to the good of their carriers. However, meiotic drive genes—which skew transmission in their own favor—can evolve under certain circumstances, even though they cause harm to the genome as a whole. Meiotic drive elements are often enriched on the two sex chromosomes (i.e., the X and the Y) because of a lack of recombination between them. Here we describe the genetic and molecular characterization of a meiotic drive distorter on the X chromosome in Drosophila simulans. This distorter apparently formed de nova from yet another new gene. To fight back against this harmful distorter, the D. simulans genome has evolved an ingenious mechanism based on DNA sequence homology. We postulate that repeated meiotic drive invasion and its suppression could be a major mechanism for genome evolution, underlying the ultimate cause for the inactivation of sex chromosome during meiosis and the occasional loss of recombination (achiasmy), which is observed only in the heterogametic (XY) sex.