Causes and consequences of sex-chromosome turnovers in Diptera

Abstract Sex-chromosome systems are highly variable across animals, but how they transition from one to another is not well understood. Diptera have undergone multiple sex-chromosome turnovers and expansions while maintaining their general chromosomal content, which makes them an ideal clade to study such transitions. We analyzed more than 100 dipteran whole-genome assemblies and identified 4 new lineages that underwent sex-chromosome turnover (in addition to the 5 previously reported). We find that the majority of turnovers happened in the group Schizophora, which tend to have fewer genes on Muller element F (the chromosome homologous to the ancestral insect X chromosome) than lower dipterans, a factor previously hypothesized to facilitate turnover. Most derived X chromosomes have higher GC content than autosomes, consistent with a high prevalence of male achiasmy in Diptera. In addition, an excess of gene movement out of the X is detected for most of these new X chromosomes, and many of these moved genes have high testis expression in Drosophila, suggesting that out-of-X gene movement contributes to the long-term demasculinization of X chromosomes.