Remote-control meiotic drive of sex chromosomes

Abstract

Some selfish genetic elements drive at meiosis to achieve transmission distortion, breaking the rules of Mendelian segregation to enhance their own evolutionary success. It has been shown that enhancers of drive must act in cis in order to gain the selfish benefit of drive and that suppressors of drive will be selected at unlinked loci. Here, we model the evolution of an autosomal trans-acting gene (Distorter) that causes the Y-chromosome (or even 0-chromosome) to drive without driving itself, a phenomenon we call "remote-control meiotic drive". We show that such a gene may spread in the population when linked to a second locus, Assister, whose alleles are transmitted at different frequencies through sperm as compared to eggs, for which we consider various scenarios, e.g. sexually antagonistic selection or sex-limited drive. Depending on the mechanistic details of sex-chromosome drive, Distorters spread can additionally facilitate transitions between XY and X0 sex determination. Our results provide a proof of principle that stretches the current understanding of segregation modifier and sex allocation theory. Moreover, we identify alternative evolutionary trajectories that could also lead to remote control drive, and discuss its potential applications in developing synthetic sex-ratio-distorting elements for use in e.g. pest management.