New insights into Xenopus sex chromosome genomics from the Marsabit clawed frog X. borealis

Abstract

In many groups, sex chromosomes change frequently but the drivers of their rapid evolution are varied and often poorly characterized. With an aim of further understanding sex chromosome turnover, we investigated the polymorphic sex chromosomes of the Marsabit clawed frog, Xenopus borealis, using genomic data and a new chromosome‐scale genome assembly. We confirmed previous findings that 54.1 Mb of chromosome 8L is sex‐linked in animals from east Kenya and a laboratory strain, but most (or all) of this region is not sex‐linked in natural populations from west Kenya. Previous work suggests possible degeneration of the Z chromosomes in the east population because many sex‐linked transcripts of this female heterogametic population have female‐biased expression, and we therefore expected this chromosome to not be present in the west population. In contrast, our simulations support a model where most or all of the sex‐linked portion of the Z chromosome from the east acquired autosomal segregation in the west, and where much genetic variation specific to the large sex‐linked portion of the W chromosome from the east is not present in the west. These recent changes are consistent with the hot‐potato model, wherein sex chromosome turnover is favoured by natural selection if it purges a (minimally) degenerate sex‐specific sex chromosome, but counterintuitively suggest natural selection failed to purge a Z chromosome that has signs of more advanced and possibly more ancient regulatory degeneration. These findings highlight complex evolutionary dynamics of young, rapidly evolving Xenopus sex chromosomes and set the stage for mechanistic work aimed at pinpointing additional sex‐determining genes in this group.

Unleashing diversity through flexibility: The evolutionary journey of sex chromosomes in amphibians and reptiles

“…Additionally, the genetic linkages of sex chromosomes were different among several Pipidae species (Bewick et al, 2011;Cauret et al, 2020;Evans et al, 2022;Furman & Evans, 2016;Furman et al, 2020;Mitros et al, 2019;Roco et al, 2015;Uno et al, 2008bUno et al, , 2015. These findings indicate that Dmw in X. laevis is younger than expected and that diversity in the origins of sex chromosomes results in frequent turnover of sex chromosomes and sex-determining genes, even in a single family, Pipidae.…”

“…However, genomic and cytogenetic analyses of Pipidae species revealed that Dmw was retained only in X. laevis and other closely related species (Bewick et al, 2011; Cauret et al, 2020; Furman & Evans, 2016; Roco et al, 2015; Uno et al, 2008b). Additionally, the genetic linkages of sex chromosomes were different among several Pipidae species (Bewick et al, 2011; Cauret et al, 2020; Evans et al, 2022; Furman & Evans, 2016; Furman et al, 2020; Mitros et al, 2019; Roco et al, 2015; Uno et al, 2008b, 2015). These findings indicate that Dmw in X. laevis is younger than expected and that diversity in the origins of sex chromosomes results in frequent turnover of sex chromosomes and sex‐determining genes, even in a single family, Pipidae.…”

Sex chromosome evolution: The remarkable diversity in the evolutionary rates and mechanisms

“…Depending on the questions and available genomic resources on given species/taxa, both approaches can detect sex‐determining regions and possible sex chromosome turnover events among closely related species. For instance, in this special issue: Using a combination of short‐read and long‐read sequencing, Evans et al (2022) and Duhamel et al (2022) perform a chromosome‐scale genome assembly in the Marsabit clawed frog and anther‐smut fungi, respectively. These approaches allow the study of intra‐specific variation of sex chromosome divergence in the frog and reveal independent chromosomal rearrangement in the mating‐type chromosomes of the fungi. With short‐read WGS and the help of existing reference genomes, Sigeman et al (2022) investigate the translocation nature of a novel neo‐sex chromosome in Sylvivoidea songbirds, whilst Rovatsos et al (2022) reveal a XX/XY sex determination system in a blind lizard and further identified a novel combination of homologous genes using the chicken X chromosome as reference. With short‐read whole‐genome pooled sequencing, Ansai et al (2022) and Jeffries et al (2022) investigate the sex‐determining regions and sex chromosome turnover across closely related fish taxa. With RAD‐seq, Keating et al (2022) and Meuser et al (2022) perform analysis in multiple individuals per sex to investigate possible sex‐determining regions and infer sex chromosome turnovers. …”

“…It is not uncommon to find intraspecific variation in sex chromosome differentiation (see Rodrigues et al, 2015; Jeffries et al, 2018; Ma et al, 2018 in various frogs). Evans et al (2022) confirm that a 54.1 Mb sex‐linked region on the W chromosome in the east Kenyan population of the Marsabit clawed frog is not sex‐linked in the west Kenyan populations. This highlights a complex evolutionary trajectory of little differentiated, ‘young’ sex chromosomes and suggests that future work should focus on understanding the evolutionary dynamics of sex chromosomes and detection of sex‐determining genes in various frog groups (see review by Ma & Veltsos, 2021).…”

A novel amphibian sex determination candidate gene, evolved by structural variation in the regulatory region between X and Y

“…Notably, to date, in >8,650 species of amphibians 16 , the widespread combination of poorly or undifferentiated sex chromosomes with large genome-sizes (see below) have caused a basic knowledge gap with only a single though very well-characterized amphibian master sex-determination gene known in a model species, the African clawed frog ( Xenopus laevis 11,17 ) and some related species 18 . Dm-w arose after (and perhaps in response to) tetraploidization, and has been lost secondarily in some tetraploid species 19 .…”