The prototype of sex chromosomes found in Korean populations of <i>Rana rugosa</i>

Abstract

The seventh largest chromosome in Japanese populations of the frog Rana rugosa morphologically evolved as a sex chromosome. The sex chromosome is XX/XY type in one geographic form and ZZ/ZW type in another. In contrast, the seventh chromosomes are still homomorphic between the sexes in the other two geographic forms: they are more subtelocentric in the Kanto form and subtelocentric in the western Japanese form. To identify a prototype of the sex chromosomes, we extended our investigation in this study to the Korean form, which is supposed to be close to the phylogenetic origin of this species. The karyotype, a sex-linked gene sequence, and mecha- nisms of sex determination and gonadal differentiation were all examined. In addition, phylogenetic analyses were performed based on mitochondrial gene sequences and the results of crossings between the Korean and Japanese forms. As a consequence, the more subtelocentric seventh chromosome, shared by the Korean and Japanese Kanto forms, was concluded to be the prototype of the sex chromosomes. Starting at the prototype, a whole process of morphological sex chromosome evolution was reconstructed.

An Evolutionary Witness: the Frog <i>Rana rugosa</i> Underwent Change of Heterogametic Sex from XY Male to ZW Female

“…Uninvestigated area is shown as blank. [Ogata et al, 2002]. The two forms share their origin at hybridization between the primary populations of Kanto and West Japan forms.…”

“…The central Japan form has differentiated sex chromosomes, which are the seventh-largest in the chromosomal complement (2n = 26), whereas the other two forms have undifferentiated, homomorphic chromosomes in both sexes. The male heterogametic sex determination of the latter two forms has been proved using a hormonally induced sex-reversal experiment [Nishioka et al, 1993a;Ogata et al, 2002]. The remaining ZW form (North- west Japan) has female heterogametic sex determination with differentiated sex chromosomes, which are the seventh-largest in the chromosomal complement, and are homologous to those of the XY form.…”

“…3 ). The structural change that made up the morphology of the sex chromosomes is a pericentromeric inversion, which is assumed to have occurred once on chromosome 7 during differentiation of the West Japan form, and once on chromosome 7 of the Kanto form during hybridization [Ogata et al, 2002]. This process of sex chromosome differentiation raises two unique points: first, morphological change occurred in both of the partners, and second, population dynamics (inter-population hybridization) may be a trigger for sex chromosome differentiation.…”

The ZZ/ZW sex-determining mechanism originated twice and independently during evolution of the frog, Rana rugosa

“…It has been shown in amphibians that the heterogametic sex was originally female, and subsequently changed more than once to male at certain branching points in amphibian phylogenetic evolution (Hillis and Green, 1990). In addition, there is evidence that the heterogametic sex returned to its previous female state in the frog Rana rugosa when its distribution range expanded across Japan (Miura et al, 1998;Ogata et al, 2002Ogata et al, , 2003. Therefore, it is plausible that heterogametic sex is not permanently fixed, but can change during evolution and speciation.…”

Meiotic recombination counteracts male-biased mutation (male-driven evolution)

“…In the first three groups, sex is determined by an XX/XY-type system, while the remaining two groups have a ZZ/ZW-type system (figure 1a) [7][8][9][10]. It is rare to find distinct sex-determining systems within a single species.…”