Long-Term Fragility of Y Chromosomes Is Dominated by Short-Term Resolution of Sexual Antagonism

Abstract

The evolution of heteromorphic sex chromosomes has fascinated biologists, inspiring theoretical models, experimental studies, and studies of genome structure. This work has produced a clear model, in which heteromorphic sex chromosomes result from repeated fixations of inversions (or other recombination suppression mechanisms) that tether sexually antagonistic alleles to sex-determining regions, followed by the degeneration of these regions induced by the lack of sex chromosome recombination in the heterogametic sex. However, current models do not predict if inversions are expected to preferentially accumulate on one sex-chromosome or another, and do not address if inversions can accumulate even when they cause difficulties in pairing between heteromorphic chromosomes in the heterogametic sex increasing aneuploidy or meiotic arrest. To address these questions, we developed a population genetic model in which the sex chromosome aneuploidy rate is elevated when males carry an inversion on either the X or Y chromosome. We show that inversions fix more easily when male-beneficial alleles are dominant, and that inversions on the Y chromosome fix with lower selection coefficients than comparable X chromosome inversions. We further show that sex-chromosome inversions can often invade and fix despite causing a substantial increase in the risk of aneuploidy. As sexual antagonism can lead to the fixation of inversions that increase sex chromosomes aneuploidy (which underlies genetic diseases including Klinefelter and Turner syndrome in humans) selection could subsequently favor diverse mechanisms to reduce aneuploidy-including alternative meiotic mechanisms, translocations to, and fusions with, the sex chromosomes, and sex chromosome turnover.

Keywords: Genetics of Sex; Y chromosome loss; aneuploidy; inversion; pseudoautosomal region; sex chromosome; sexual antagonism.

Figure 1

Sex chromosome inversions across a range of dominance factors and selection coefficients with a recombination distance of 0.3 and an aneuploidy rate of 0.02. The color in the plot indicates the stable frequency of the inversion. (A) Y chromosome inversion capturing a male benefit allele. (B) X chromosome inversion capturing a female benefit allele.

Figure 2

The fate of X and Y chromosome inversions across a range of dominance factors and aneuploidy rates. In (A–C) the recombination distance between the SDR and the SA locus is 0.1. In (D–F), the recombination distance between the SDR and the SA locus is 0.3. In each plot, the color in the field indicates the selection coefficient required for an inversion to invade or fix. (A) Minimum selection coefficient for Y inversion to fix. (B) Minimum selection coefficient for X inversion to fix. (C) Minimum selection coefficient for X inversion to invade. (D) Minimum selection coefficient for Y inversion to fix. (E) Minimum selection coefficient for X inversion to fix. (F) Minimum selection coefficient for X inversion to invade.

Figure 3

The effect of recombination on the fate of inversions that link a sexually antagonistic locus with the SDR while also increasing aneuploidy rate. Results are shown for the case where the male benefit allele is dominant and the female benefit allele is recessive. The shaded region indicates the selection coefficient necessary for the inversion to invade. (A) Y chromosome inversion linking the SDR and the male benefit allele. (B) X chromosome inversion linking the SDR and the female benefit allele.