A frog with three sex chromosomes that co-mingle together in nature: Xenopus tropicalis has a degenerate W and a Y that evolved from a Z chromosome
Abstrakt
In many species, sexual differentiation is a vital prelude to reproduction, and disruption of this process can have severe fitness effects, including sterility. It is thus interesting that genetic systems governing sexual differentiation vary among-and even within-species.
To understand these systems more, we investigated a rare example of a frog with three sex chromosomes: the Western clawed frog, Xenopus tropicalis. We demonstrate that natural populations from the western and eastern edges of Ghana have a young Y chromosome, and that a male-determining factor on this Y chromosome is in a very similar genomic location as a previously known female-determining factor on the W chromosome.
Nucleotide polymorphism of expressed transcripts suggests genetic degeneration on the W chromosome, emergence of a new Y chromosome from an ancestral Z chromosome, and natural co-mingling of the W, Z, and Y chromosomes in the same population. Compared to the rest of the genome, a small sex-associated portion of the sex chromosomes has a 50-fold enrichment of transcripts with male-biased expression during early gonadal differentiation.
Additionally, X. tropicalis has sex-differences in the rates and genomic locations of recombination events during gametogenesis that are similar to at least two other Xenopus species, which suggests that sex differences in recombination are genus-wide. These findings are consistent with theoretical expectations associated with recombination suppression on sex chromosomes, demonstrate that several characteristics of old and established sex chromosomes (e.g., nucleotide divergence, sex biased expression) can arise well before sex chromosomes become cytogenetically distinguished, and show how these characteristics can have lingering consequences that are carried forward through sex chromosome turnovers.
Author summary Sex chromosomes often come in pairs (e.g., an X and a Y, or a Z and a W) and variation among species evidences widespread rapid evolutionary changes of sex chromosomes. To understand why, we examined a rare example of a frog (Xenopus tropicalis) with three sex chromosomes.
We discovered a small sex-linked sliver of the genome that has a high proportion of genes with higher expression in males than females during gonadal differentiation. Molecular variation in expressed transcripts from this genomic region suggests that this pattern stems from decreased or lost expression of alleles on the W chromosome combined with a recent origin of the Y chromosome from an ancestral Z chromosome.
These findings are consistent with theoretical expectations associated with reduced genetic recombination, and demonstrate that features of ancestral chromosomes have persistent genomic effects that bleed through sex chromosome transitions.