Rapid evolutionary dynamics of an expanding family of meiotic drive factors and their hpRNA suppressors

Meiotic drivers are a class of selfish genetic elements whose existence is frequently hidden due to concomitant suppressor systems. Accordingly, we know little of their evolutionary breadth and molecular mechanisms. Here, we trace the evolution of the Dox meiotic drive system in Drosophila simulans, which affects male-female balance (sex ratio). Dox emerged via stepwise mobilization and acquisition of multiple D. melanogaster gene segments including from protamine, which mediates compaction of sperm chromatin. Moreover, we reveal novel Dox homologs and massive amplification of Dox superfamily genes on X chromosomes of its closest sisters D. mauritiana and D. sechellia. Emergence of Dox loci is tightly associated with 359-class satellite repeats that flank de novo genomic copies. In concert, we find coordinated diversification of autosomal hairpin RNA-class siRNA loci that target subsets of Dox superfamily genes. Overall, we reveal fierce genetic arms races between meiotic drive factors and siRNA suppressors associated with recent speciation. The Dox meiotic drive system distorts the sex ratio in Drosophila simulans. Here, the authors reconstruct the stepwise emergence, and recent amplification of Dox superfamily genes in parallel with the emergence of autosomal hairpin RNA-class siRNA loci that target subsets of these putative drivers.

Automated summary

The study reveals the distortion of sex ratio in Drosophila simulans by the Dox meiotic drive system, as well as the stepwise emergence and recent amplification of Dox superfamily genes, along with the evolution of autosomal hairpin RNA-class siRNA loci targeting subsets of these putative drivers.