Long-term fragility of Y chromosomes is dominated by short-term resolution of sexual antagonism

Heath Blackmon, Yaniv Brandvain

Research output: Contribution to journalArticlepeer-review

13 Scopus citations

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.

Original languageEnglish (US)
Pages (from-to)1621-1629
Number of pages9
JournalGenetics
Volume207
Issue number4
DOIs
StatePublished - Dec 2017

Bibliographical note

Funding Information:
We thank Sally Otto, David Zarkower, and two anonymous reviewers for helpful comments on an earlier version of this manuscript. We also appreciate helpful discussions with the University of Minnesota EEB Theory Group and members of the Brandvain and McGaugh laboratories. This work was supported by a University of Minnesota Grand Challenges postdoctoral grant to H.B.

Publisher Copyright:
© 2017 by the Genetics Society of America.

Keywords

  • Aneuploidy
  • Genetics of sex
  • Inversion
  • Pseudoautosomal region
  • Sex chromosome
  • Sexual antagonism
  • Y chromosome loss

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