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

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 gen...

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Bibliographic Details
Published in:Journal of evolutionary biology 2022-12, Vol.35 (12), p.1777-1790
Main Authors: Evans, Ben J., Mudd, Austin B., Bredeson, Jessen V., Furman, Benjamin L. S., Wasonga, Domnick Victor, Lyons, Jessica B., Harland, Richard M., Rokhsar, Dan S.
Format: Article
Language:English
Subjects:
Amphibians
Chromosome 8
Chromosomes
Degeneration
Females
Genetic diversity
Genomics
Natural populations
Natural selection
Potatoes
rapid evolution
recombination suppression
Sex
sex chromosome turnover
Sex chromosomes
W chromosomes
Xenopus
Z chromosomes
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Summary: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. In most or all frogs, sex is genetically determined but the genes that control this crucial process evolve rapidly. To understand how, we explored an example of intraspecific polymorphism in sex chromosomes in the Marsabit clawed frog throughout its range in Kenya. Genome sequences, a new chromosome‐scale genome assembly, and simulations suggest that the large sex‐linked region in east Kenya is not present in west Kenya and that most or all of the Z chromosome of the east population segregates autosomally in the west. The sex chromosomes of the west population thus may be recently evolved and/or contain a small region of sex‐linked recombination suppression. The findings illustrate how rapid evolution of genetic triggers for sex determination can have genome‐wide
ISSN:1010-061X
1420-9101
1420-9101
DOI:10.1111/jeb.14078