Autosomally-encoded segregation distortion of sex chromosomes

Some selfish genetic elements drive at meiosis to achieve transmission
distortion, breaking the rules of Mendelian segregation to enhance their
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, Distorter’s spread can additionally facilitate
transitions between XY and X0 sex determination. Our results provide 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.