Rapid Rise and Fall of Selfish Sex-Ratio X Chromosomes in Drosophila simulans: Spatiotemporal Analysis of Phenotypic and Molecular Data

Sex-ratio drive, which has been documented in several Drosophila species, is induced by X-linked segregation distorters. Contrary to Mendel’s law of independent assortment, the sex-ratio chromosome (X SR ) is inherited by more than half the offspring of carrier males, resulting in a female-biased sex ratio. This segregation advantage allows X SR to spread in populations, even if it is not beneficial for the carriers. In the cosmopolitan species D. simulans, the Paris sex-ratio is caused by recently emerged selfish X SR chromosomes. These chromosomes have triggered an intragenomic conflict, and their propagation has been halted over a large area by the evolution of complete drive suppression. Previous molecular population genetics analyses revealed a selective sweep indicating that the invasion of X SR chromosomes was very recent in Madagascar (likely less than 100 years ago). Here, we show that X SR chromosomes are now declining at this location as well as in Mayotte and Kenya. Drive suppression is complete in the three populations, which display little genetic differentiation and share swept haplotypes, attesting to a common and very recent ancestry of the X SR chromosomes. Patterns of DNA sequence variation also indicate a fitness cost of the segmental duplication involved in drive. The data suggest that X SR chromosomes started declining first on the African continent, then in Mayotte, and finally in Madagascar and strongly support a scenario of rapid cycling of X chromosomes. Once drive suppression has evolved, standard X ST chromosomes locally replace costly X SR chromosomes in a few decades.