Sex Chromosome Evolution: So Many Exceptions to the Rules

Abstract

Genomic analysis of many nonmodel species has uncovered an incredible diversity of sex chromosome systems, making it possible to empirically test the rich body of evolutionary theory that describes each stage of sex chromosome evolution. Classic theory predicts that sex chromosomes originate from a pair of homologous autosomes and recombination between them is suppressed via inversions to resolve sexual conflict. The resulting degradation of the Y chromosome gene content creates the need for dosage compensation in the heterogametic sex. Sex chromosome theory also implies a linear process, starting from sex chromosome origin and progressing to heteromorphism. Despite many convergent genomic patterns exhibited by independently evolved sex chromosome systems, and many case studies supporting these theoretical predictions, emerging data provide numerous interesting exceptions to these long-standing theories, and suggest that the remarkable diversity of sex chromosomes is matched by a similar diversity in their evolution. For example, it is clear that sex chromosome pairs are not always derived from homologous autosomes. In addition, both the cause and the mechanism of recombination suppression between sex chromosome pairs remain unclear, and it may be that the spread of recombination suppression is a more gradual process than previously thought. It is also clear that dosage compensation can be achieved in many ways, and displays a range of efficacy in different systems. Finally, the remarkable turnover of sex chromosomes in many systems, as well as variation in the rate of sex chromosome divergence, suggest that assumptions about the inevitable linearity of sex chromosome evolution are not always empirically supported, and the drivers of the birth-death cycle of sex chromosome evolution remain to be elucidated. Here, we concentrate on how the diversity in sex chromosomes across taxa highlights an equal diversity in each stage of sex chromosome evolution.

Keywords: recombination suppression, sex determination, inversions, methylation, dosage compensation.

Fig. 1.

—Expected patterns of sex chromosome divergence following recombination suppression. (A) Stepwise progression, due to inversions or large shifts in recombination hotspots, results in large spatial blocks where the divergence between X–Y or Z–W orthologs is similar. (B) Progressive expansion (e.g., TE accumulation, methylation changes) results in a linear relationship between ortholog divergence across the range of the sex chromosome. (C) A potential problem of only sampling a few genes is that a stepwise pattern may be inferred, when it was truly progressive expansion. A similar pattern could happen if inversions, or other discrete changes, reinforce pre-existing recombination suppression soon after it is established.

Fig. 2.

—The cycle of sex chromosome evolution. A new master sex-determining locus arises on an autosome (gold chromosomes, left side), leading to sex chromosome formation (blue chromosomes, starting top left), but sex chromosome evolution is not a simple progression of accumulating divergence. After establishment and at any stage of evolution, sex chromosomes can persist at the current stage (blue arrows), progress in establishing larger areas of recombination suppression (gray region, top right chromosomes) and divergence (red region, right side chromosomes), or turnover (gold arrows) with either a new sex-determining gene evolving or moving the sex-determining gene to a new location in the genome. Each stage here is highlighted by a representative taxon that currently possesses that sex chromosome state.