Drivers of Achiasmatic Meiosis: Sexual Antagonism versus Heteromorphy-Dependent Aneuploidy across Sex-Chromosome Divergence

Abstract

Crossing over during meiosis ensures proper chromosome segregation and promotes genetic diversity. In species with chromosomal sex determination, recombination between sex chromosomes is often reduced or eliminated, yet the evolutionary forces driving this shift remain debated. One extreme outcome, achiasmatic meiosis, typically completely halts recombination in the heterogametic sex. Here, we use a population genetic model to compare two leading hypotheses for the evolution of achiasmy: (1) selection to reduce recombination load from sexually antagonistic alleles, and (2) selection to avoid aneuploidy driven by heteromorphic sex chromosomes. We analyze how mutations promoting achiasmy can invade autosomes, X chromosomes, or Y chromosomes under each selective regime. Our results reveal that the Y chromosome provides the most permissive context for invasion, due to male-limited expression and selection. Moreover, we predict a shift in the primary selective forces across the trajectory of sex chromosome divergence: sexually antagonistic selection is more likely to drive achiasmy in young, homomorphic sex chromosomes, whereas heteromorphy-dependent aneuploidy becomes the primary force in highly diverged, heteromorphic sex chromosomes. These results provide a unified framework for understanding transitions to achiasmy across diverse taxa.