Multiple Transitions between Y Chromosome and Autosome in Tago's Brown Frog Species Complex.

Sex chromosome turnover is the transition between sex chromosomes and autosomes. Although many cases have been reported in poikilothermic vertebrates, their evolutionary causes and genetic mechanisms remain unclear. In this study, we report multiple transitions between the Y chromosome and autosome in the Japanese Tago's brown frog complex. Using chromosome banding and molecular analyses (sex-linked and autosomal single nucleotide polymorphisms, SNPs, from the nuclear genome), we investigated the frogs of geographic populations ranging from northern to southern Japan of two species, Rana tagoi and Rana sakuraii (2n = 26). Particularly, the Chiba populations of East Japan and Akita populations of North Japan in R. tagoi have been, for the first time, investigated here. As a result, we identified three different sex chromosomes, namely chromosomes 3, 7, and 13, in the populations of the two species. Furthermore, we found that the transition between the Y chromosome (chromosome 7) and autosome was repeated through hybridization between two or three different populations belonging to the two species, followed by restricted chromosome introgression. These dynamic sex chromosome turnovers represent the first such findings in vertebrates and imply that speciation associated with inter- or intraspecific hybridization plays an important role in sex chromosome turnover in frogs.

Evolution of a Multiple Sex-Chromosome System by Three-Sequential Translocations among Potential Sex-Chromosomes in the Taiwanese Frog Odorrana swinhoana.

Translocation between sex-chromosomes and autosomes generates multiple sex-chromosome systems. It happens unexpectedly, and therefore, the evolutionary meaning is not clear. The current study shows a multiple sex chromosome system comprising three different chromosome pairs in a Taiwanese brown frog (Odorrana swinhoana). The male-specific three translocations created a system of six sex-chromosomes, ♂X1Y1X2Y2X3Y3-♀X1X1X2X2X3X3. It is unique in that the translocations occurred among three out of the six members of potential sex-determining chromosomes, which are known to be involved in sex-chromosome turnover in frogs, and the two out of three include orthologs of the sex-determining genes in mammals, birds and fishes. This rare case suggests sex-specific, nonrandom translocations and thus provides a new viewpoint for the evolutionary meaning of the multiple sex chromosome system.

Evolution of Sex Chromosome Heteromorphy in Geographic Populations of the Japanese Tago's Brown Frog Complex.

The sex chromosomes of most anuran amphibians are characterized by homomorphy in both sexes, and evolution to heteromorphy rarely occurs at the species or geographic population level. Here, we report sex chromosome heteromorphy in geographic populations of the Japanese Tago's brown frog complex (2n = 26), comprising Rana sakuraii and R. tagoi. The sex chromosomes of R. sakuraii from the populations in western Japan were homomorphic in both sexes, whereas chromosome 7 from the populations in eastern Japan were heteromorphic in males. Chromosome 7 of R. tagoi, which is distributed close to R. sakuraii in eastern Japan, was highly similar in morphology to the Y chromosome of R. sakuraii. Based on this and on mitochondrial gene sequence analysis, we hypothesize that in the R. sakuraii populations from eastern Japan the XY heteromorphic sex chromosome system was established by the introduction of chromosome 7 from R. tagoi via interspecies hybridization. In contrast, chromosome 13 of R. tagoi from the 2 large islands in western Japan, Shikoku and Kyushu, showed a heteromorphic pattern of constitutive heterochromatin distribution in males, while this pattern was homomorphic in females. Our study reveals that sex chromosome heteromorphy evolved independently at the geographic lineage level in this species complex.