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

Abstract

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.

Testis Development and Differentiation in Amphibians

“…The most extreme example occurs in G. rugosa , in which six geographic variants with both XX/XY and ZZ/ZW sex chromosomes evolved after two independent chromosomal inversions followed by hybridization events [ 37 , 38 , 39 , 40 , 41 , 42 ]. Another example of intraspecies variation occurs in the amphibian model X. tropicalis , a species with three sex chromosomes (Y > W > Z) coexisting in laboratory strains [ 36 ] and in natural populations [ 43 ], which likely originated after the emergence of a Y chromosome from an ancestral Z chromosome [ 43 ].…”

The Diversity and Evolution of Sex Chromosomes in Frogs

“…The chromosomes (Chr9 and Chr10) that are never used as sex chromosomes are omitted. Sex chromosomes were identified from various publications [ 43 , 55 , 59 , 60 , 62 , 63 , 64 , 65 , 66 , 67 ]. The tree is obtained from , accessed on 5 February 2021 and visualized in Figtree ( , accessed on 5 February 2021).…”

“…Chr8 is probably involved in the intraspecific sex-determination system turnover in Glandirana rugosa , from an XY to ZW sex-determination system [ 61 ]. Finally, Xenopus tropicalis Chr7 is associated with multiple sex-determination system turnovers, where W, Z, and Y chromosomes occur in the same population in Ghana, and the degenerate W and Y probably evolved from the Z chromosomes [ 62 ].…”

Comparative Distribution of Repetitive Sequences in the Karyotypes of Xenopus tropicalis and Xenopus laevis (Anura, Pipidae)

“…Species of the genus Xenopus are interesting models for studying genome evolution after polyploidization, because most changes in genome size in this genus involve changes in ploidy (ranging from diploid to dodecaploid). They are also good models to study sex chromosome evolution, as sex chromosomes have evolved independently several times in this group [ 20 , 21 , 22 , 23 ]. Extant species of the genus Xenopus are restricted to Africa and can be classified into two clades [ 24 ].…”

“…Among Xenopus species, X. tropicalis is an interesting model as it is the only diploid species of the genus, with a karyotype containing 2n = 2x = 20 chromosomes [ 25 ]. Furthermore, in this species, three homomorphic sex chromosomes coexist (Y > W > Z) both in laboratory strains and in natural populations [ 20 , 21 ]. In contrast, X. laevis is a functional diploid with an allotetraploid origin.…”