Amphidiploidy recovers the viability of hybrids of European and East Asian water frogs

Ohtani, Hiromi; Miura, Ikuo; Kondo, Yasuyuki; Uchibori, Masayuki

doi:10.1002/(sici)1097-010x(19971001)279:2<113::aid-jez1>3.0.co;2-r

Cited by 10 publications

(7 citation statements)

References 8 publications

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“…Experimental crosses between populations were performed following the method described by Ohtani, Miura, Kondo, and Uchibori (). For reciprocal crossings, we used ZZ males and ZW females of the Neo‐ZW1 subgroup from Toyono (P24) in Osaka Prefecture, and XY males and XX females from Hamamatsu in Shizuoka Prefecture (a closed circle with white outline on the map of Japan in Figure and a white circle on the right bottom map in Figure ), and Sekigahara (P2) in Gifu prefecture for the XY group (Table and Figure ).…”

Section: Methodsmentioning

confidence: 99%

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

Ogata¹,

Lambert

Ezaz

et al. 2018

Molecular Ecology

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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.

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Section: Methodsmentioning

confidence: 99%

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

Ogata¹,

Lambert

Ezaz

et al. 2018

Molecular Ecology

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“…Artificial crossing was performed between the frogs of Hiroshima population of the west Japan group and those of Hamakita population of the XY group according to the method of Ohtani et al (1997). Gynogenetic diploid embryos were produced from two females of Kyoto population using the method of Ohtani et al (1997).…”

Section: Artificial Crossing and Diploid Gynogenesismentioning

confidence: 99%

“…Gynogenetic diploid embryos were produced from two females of Kyoto population using the method of Ohtani et al (1997). Sex chromosome constitution of the gynogenetic diploids was checked on the basis of the AAT genotypes.…”

Section: Artificial Crossing and Diploid Gynogenesismentioning

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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“…Ovulation was induced in females by injection of a pituitary gland solution of the frog Pelophylax nigromaculatus or G. rugosa, and eggs were artificially inseminated with sperm from the male according to the method of Ohtani et al [17]. Sex-reversal experiments with testosterone were performed according to the method of Ogata et al [18].…”

Section: (C) Artificial Crossing and Sex Reversal With Testosteronementioning

confidence: 99%

Sex chromosome evolution from a heteromorphic to a homomorphic system by inter-population hybridization in a frog

Ogata¹,

Suzuki

Yuasa³

et al. 2021

Phil. Trans. R. Soc. B

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Sex chromosomes generally evolve from a homomorphic to heteromorphic state. Once a heteromorphic system is established, the sex chromosome system may remain stable for an extended period. Here, we show the opposite case of sex chromosome evolution from a heteromorphic to a homomorphic system in the Japanese frog Glandirana rugosa. One geographic group, Neo-ZW, has ZZ-ZW type heteromorphic sex chromosomes. We found that its western edge populations, which are geographically close to another West-Japan group with homomorphic sex chromosomes of XX-XY type, showed homozygous genotypes of sex-linked genes in both sexes. Karyologically, no heteromorphic sex chromosomes were identified. Sex-reversal experiments revealed that the males were heterogametic in sex determination. In addition, we identified another similar population around at the southwestern edge of the Neo-ZW group in the Kii Peninsula: the frogs had homomorphic sex chromosomes under male heterogamety, while shared mitochondrial haplotypes with the XY group, which is located in the east and bears heteromorphic sex chromosomes. In conclusion, our study revealed that the heteromorphic sex chromosome systems independently reversed back to or turned over to a homomorphic system around each of the western and southwestern edges of the Neo-ZW group through hybridization with the West-Japan group bearing homomorphic sex chromosomes. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.

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Amphidiploidy recovers the viability of hybrids of European and East Asian water frogs

Cited by 10 publications

References 8 publications

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

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

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

Sex chromosome evolution from a heteromorphic to a homomorphic system by inter-population hybridization in a frog

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