Keywords: b. population variation; a. genome evolution
Meiotic drive is an infringement of the law of equal allele segregation into the gametes. In heterozygote individuals, the causal genetic elements prevent the production of gametes that do not contain it. Thus, they can spread through populations even if they are deleterious for the carriers. Because they induce sex-ratio bias, sex-linked drivers expressed in the heterogametic sex are an important source of genetic conflict, characterized by the evolution of suppressors which tends to restore a balanced sex ratio.
In Drosophila simulans, X-linked meiotic drivers disturb the segregation of the Y chromosome during male meiosis. The progeny of carrier male is mainly composed of females. The drive is caused by two X-linked elements, acting together. The first one lies within a segmental duplication, the second has been identified as the HP1D2 gene, a young and fast-evolving member of the Heterochromatin Protein 1 gene family. HP1D2 accumulates on the heterochromatic Y chromosome in spermatogonia, strongly suggesting that it controls the segregation of sister chromatids through heterochromatin modifications.
In natural populations where the drivers have spread, they are neutralized by resistant Y chromosomes. We followed the dynamics of the resistant Y chromosomes in natural populations in relation to the dynamics of the driver. We observed the replacement of sensitive by resistant Ys within a handful of years in populations invaded by the drivers. To go further in the study of Y chromosome variation in this species we sequenced 21 iso-Y lines, their Y chromosomes came from different locations around the world and have different phenotypes. We confirm the very low nucleotide diversity among Y chromosomes in this species, which could be considered as a signature of recurrent genetic conflicts. While we identified a haplotype with fixed differences between sensitive and resistant Ys. The sequence similarity between the sensitive Y chromosomes suggests that they have a recent common ancestor. We also confirm the ancestry of the resistant lineage by examining Y-linked sequences in the sister species of D. simulans, D. sechellia and D. mauritiana. All together the molecular polymorphism allows us to retrace the demographic and evolutionary history of the Y chromosome related to the one of the species. We show that intragenomic conflicts can drive astonishingly rapid evolution of Y chromosomes.