Rapid Evolution of a Y-Chromosome Heterochromatin Protein Underlies Sex Chromosome Meiotic Drive

Sex-ratio (SR) drive, known in a dozen Drosophila species, is a type of naturally-occurring meiotic drive in which X-linked segregation distorters promote their own transmission by preventing the production of Y-bearing sperm. Males carrying such distorters produce a large excess of female offspring. Their presence in populations fuels an intragenomic conflict in which resistant Y chromosomes and autosomal suppressors are selected to counteract the distorters. The recurrent evolution of distorters and suppressors may contribute to sex chromosome and genome evolution, the evolution of mating systems and the emergence of new species. However, we know very little about the actors of SR drive because the trait is usually associated with chromosomal inversions that restrict the genetic analysis.

Thanks to the lack of inversion in D. simulans, we were able to identify a gene involved in one of the three cases of cryptic SR drive reported in this species, the Paris system. This gene, HP1D2, is a young and fast-evolving member of the heterochromatin protein1 (HP1) gene family. Our findings that HP1D2 binds the heterochromatic Y chromosome prior to meiosis, and that Paris SR drive is a consequence of dysfunctional HP1D2 alleles, shed new light on the mechanism and evolution of sex-linked meiotic drivers.