The origin and differentiation of the heteromorphic sex chromosomes Z, W, X, and Y in the frog Rana rugosa, inferred from the sequences of a sex-linked gene, ADP/ATP translocase

Miura, Ikuo; Ohtani, Hiromi; Nakamura, Masahisa; Ichikawa, Youko; Saitoh, Kazuo

doi:10.1093/oxfordjournals.molbev.a025889

Cited by 87 publications

(95 citation statements)

References 20 publications

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“…All five trees, including the tree for the Ar intron 5, were similar in that the cluster containing the Y/Z sequences was clearly distinct from the cluster containing the X/W sequences. These results were consistent with the evolutionary scenario of sex chromosome differentiation in the XY and ZW groups [7].…”

Section: (B) Estimation Of Divergence Time For the Rana Rugosa Populasupporting

confidence: 90%

“…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.…”

Section: Introductionmentioning

confidence: 99%

“…Phylogenetic tree analyses based on mitochondrial nucleotide sequences of four genetic groups in Rana rugosa. (a) The distribution of five R. rugosa genetic groups in Japan [7]. Specimens were collected from Sekigahara (1) and Hamamatsu (2) for the XY group, and from Kanazawa (3) and Niigata (4) for the ZW group.…”

Section: Introductionmentioning

confidence: 99%

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

Mawaribuchi

Ito

Ogata³

et al. 2016

Proc. R. Soc. B.

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Meiotic recombination is believed to produce greater genetic variation despite the fact that deoxyribonucleic acid (DNA)-replication errors are a major source of mutations. In some vertebrates, mutation rates are higher in males than in females, which developed the theory of male-driven evolution (male-biased mutation). However, there is little molecular evidence regarding the relationships between meiotic recombination and male-biased mutation. Here we tested the theory using the frog Rana rugosa, which has both XX/XY-and ZZ/ZW-type sex-determining systems within the species. The male-to-female mutation-rate ratio (a) was calculated from homologous sequences on the X/Y or Z/W sex chromosomes, which supported male-driven evolution. Surprisingly, each a value was notably higher in the XX/XY-type group than in the ZZ/ZW-type group, although a should have similar values within a species. Interestingly, meiotic recombination between homologous chromosomes did not occur except at terminal regions in males of this species. Then, by subdividing a into two new factors, a replication-based male-to-female mutation-rate ratio (b) and a meiotic recombination-based XX-to-XY/ZZ-to-ZW mutation-rate ratio (g), we constructed a formula describing the relationship among a nucleotide-substitution rate and the two factors, b and g. Intriguingly, the b-and g-values were larger and smaller than 1, respectively, indicating that meiotic recombination might reduce male-biased mutations.

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Section: (B) Estimation Of Divergence Time For the Rana Rugosa Populasupporting

confidence: 90%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

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

Mawaribuchi

Ito

Ogata³

et al. 2016

Proc. R. Soc. B.

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show abstract

“…Similar phenomena have been observed in salmonids and sticklebacks, suggesting that sex chromosomes have changed frequently in fish (Woram et al, 2003;Peichel et al, 2004;Phillips et al, 2007). In the Japanese frog, Rana rugosa, two distinct sex chromosome types, XX/ XY and ZZ/ZW, were observed in the same species (Miura et al, 1998). In addition, the change of heterogametic sex from male to female appears to have independently occurred twice during frog speciation (Ogata et al, 2008).…”

Section: Plasticity Of Sex Chromosomes In Lower Vertebratessupporting

confidence: 70%

Heritable artificial sex chromosomes in the medaka, Oryzias latipes

et al. 2009

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Chromosomal sex determination is widely used by vertebrates, however, only two genes have been identified as master sex-determining genes: SRY/Sry in mammals and DMY in the teleost medaka. Transfer of both genes into genetically female (XX) individuals can induce male development. However, transgenic strains have not been established in both cases because of infertility of the transgenic founders in mammals and low germline transmission rates in medaka. In this study, we used a BAC clone containing DMY in a 117 kb genomic region and two types of fluorescent marker to establish two DMY-transgenic medaka strains. In these strains, exogenous DMY is completely linked to a male phenotype and early gonadal development is not different from that of the wild-type strain. Sex-linkage analysis showed that the exogenous DMY was located on linkage group (LG) 23 in one strain and on LG 5 in the other strain, whereas the sex chromosome in medaka is on LG 1. Real-time PCR analysis indicated that these strains have multiple copies of DMY and higher DMY expression levels than the wild-type strain. These results showed that LGs 23 and 5 function as sex chromosomes in the two strains, respectively. This is not only the first example of the artificial generation of heritable sex chromosomes in vertebrates but also the first evidence showing plasticity of homomorphic sex chromosomes. This plasticity appears to be a characteristic of lower vertebrates and the underlying cause of frequent sex chromosome switching, recently reported in several fish and frog species.

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“…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.…”

Section: Introductionmentioning

confidence: 99%

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

Ogata¹,

et al. 2007

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The Japanese frog, Rana rugosa, has two distinct sex chromosome types, XX/XY and ZZ/ZW. These two types are found in localized groups, separated geographically by a boundary area predicted to lie somewhere around Lake Biwa in central Japan. To determine this precise boundary, the heterogametic sex of 18 populations around Lake Biwa was examined by genotyping sex-linked genes. Phylogenetic relationships between the populations were also analyzed using mitochondrial 12S rRNA gene. Results showed that the Suzuka-Kii mountain range located east of Lake Biwa separated the XX/XY populations from the ZZ/ZW populations. Unexpectedly, from a phylogenetic perspective, the ZZ/ZW populations around Lake Biwa belonged not to the main ZW group but to the XY group. The authors propose that the ZZ/ZW populations around Lake Biwa diverged secondarily from the XX/XY group through a change of heterogametic sex, eventually forming a new group. This group was thus named the 'Neo-ZW group'. As the main ZW group inhabiting northwestern Japan is known to have a different male heterogametic origin, this finding shows that change of heterogametic sex from male to female may have occurred twice, and independently, during the frog speciation.

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The origin and differentiation of the heteromorphic sex chromosomes Z, W, X, and Y in the frog Rana rugosa, inferred from the sequences of a sex-linked gene, ADP/ATP translocase

Cited by 87 publications

References 20 publications

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

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

Heritable artificial sex chromosomes in the medaka, Oryzias latipes

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

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