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.

Sex determination through X-Y heterogamety inSalix nigra

“…We used a targeted sequence capture method to sequence a broad portion of the gene space within the S. nigra genome because funds were limited for this project, and this meant that it was only possible to discover variants at loci homologous to our probes. This method allowed us to include 48 individuals within our sample, which increased the power and accuracy to detect alleles associated with sex as well as differences in diversity and Tajima including translocations, deletions, and inversions (Furman et al, 2020).…”

Conserved sex-biased DNA methylation patterns target key developmental genes and non-recombining region of the guppy sex chromosome

“…Because of their ability to move genetic material around the genome and alter expression patterns, TEs are thought to be a potential mechanism to promote turnover of sex determining loci while simultaneously suppressing recombination (Furman et al 2020). Consistent with this hypothesis, TEs have been found at the boundaries of nonrecombining regions of recently established regions of suppressed recombination in mammals and birds (Iwase et al 2003; Xu et al 2019), and are also enriched in Stratum I in guppies (Almeida et al 2020).…”

The avian W chromosome is a refugium for endogenous retroviruses with likely effects on female-biased mutational load and genetic incompatibilities

“…Sex chromosomes generally evolve from a pair of autosomes [2] that acquire a sex-determining locus and locally suppressed recombination around that locus [3,4]. The non-recombining region may remain very small, keeping the two sex chromosomes largely homomorphic.…”