Reconstruction of female heterogamety from admixture of XX‐XY and ZZ‐ZW sex‐chromosome systems within a frog species

Abstract

Sex-determining mechanisms change repeatedly throughout evolution, and it is difficult to track this continual process. The Japanese soil-frog Glandirana rugosa is a remarkable evolutionary witness to the ongoing process of the evolution of sex-determining modes. The two geographic groups, designated XY and Neo-ZW, have homologous sex chromosomes, yet display opposite types of sex chromosomes, XX-XY and ZZ-ZW, respectively. These two groups are sympatric at the edges of their respective ranges in Central Japan. In this study, we discovered molecular evidence that the eastern part of the Neo-ZW group (Neo-ZW2 subgroup), which is found near the sympatric area, shares mitochondrial haplotypes with the XY group. By analysing single nucleotide polymorphism (SNP) loci, we have also discovered that the representative nuclear genome of the Neo-ZW2 subgroup shares allele clusters with both the XY group and another part of the Neo-ZW group (Neo-ZW1 subgroup), indicating a hybrid origin of the Neo-ZW2. Further analysis of sex-linked SNP loci revealed that the alleles on the W chromosomes of the Neo-ZW2 were derived mostly from X chromosomes, while alleles on the Z chromosomes originated from the Z chromosomes of the Neo-ZW1 subgroup and partly from the Y chromosomes of the XY group. Our study revealed that admixture of the two opposite sex-chromosome systems reconstructed a female heterogametic system by recycling the X chromosomes into new W chromosomes. This work offers an illustrative example of how de novo sex-chromosome systems can arise by recycling material from ancestral sex chromosomes.

Evolution of sex determination and heterogamety changes in section Otites of the genus Silene

“…In these models, the ancestral heterogamety is preserved, as is observed in anurans, though Glandirana rugosa (syn. Rana rugosa ) is an exception 49–51 and this is supported by the data from other vertebrates reviewed by Blaser et al . 48 .…”

Chromosome Painting Does Not Support a Sex Chromosome Turnover in Lacerta agilis Linnaeus, 1758

“…The cases of such turnovers, when a taxon "forsakes" a well-established sex chromosome system and acquires a new one, are rather rare , but known in lizards [Nielsen et al, 2019] and even in mammals [Matveevsky et al, 2017]. An intraspecific polymorphism in sex-determining systems is also possible, as in the case of the frog Glandirana rugosa [Ogata et al, 2018]. The second possibility is that one or both these identifications of the L. agilis sex chromosome are erroneous.…”

Landscape of snake’ sex chromosomes evolution spanning 85 MYR reveals ancestry of sequences despite distinct evolutionary trajectories

“…Therefore, it is plausible that transitions between homomorphic ZW and XY have occurred in the Boidae family without much substantial genotypic innovation (e.g. considering the 4th pair of boas as the putative sex chromosomes, the XY and ZW are morphologically similar), as reported in the Japanese frog Glandirana rugosa 56 . In our study, we did not detect any sex-specific pattern using intra- and interspecific CGH experiments (Figs.…”