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

Mitsuaki Ogata, Max Lambert, Tariq EZAZ, Ikuo Miura

Research output: Contribution to journalArticle

1 Citation (Scopus)

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. 
Original languageEnglish
Pages (from-to)4078-4089
Number of pages12
JournalMolecular Ecology
Volume27
Issue number20
DOIs
Publication statusPublished - Oct 2018

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Sex Chromosomes
sex chromosomes
frog
Anura
frogs
chromosome
Chromosomes
W chromosome
Z chromosome
Alleles
Recycling
X Chromosome
X chromosome
alleles
single nucleotide polymorphism
recycling
Single Nucleotide Polymorphism
gender
loci
Y Chromosome

Cite this

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title = "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. ",
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author = "Mitsuaki Ogata and Max Lambert and Tariq EZAZ and Ikuo Miura",
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Reconstruction of female heterogamety from admixture of XX‐XY and ZZ‐ZW sex‐chromosome systems within a frog species. / Ogata, Mitsuaki; Lambert, Max; EZAZ, Tariq; Miura, Ikuo.

In: Molecular Ecology, Vol. 27, No. 20, 10.2018, p. 4078-4089.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Reconstruction of female heterogamety from admixture of XX‐XY and ZZ‐ZW sex‐chromosome systems within a frog species

AU - Ogata, Mitsuaki

AU - Lambert, Max

AU - EZAZ, Tariq

AU - Miura, Ikuo

PY - 2018/10

Y1 - 2018/10

N2 - 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. 

AB - 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. 

KW - W chromosome

KW - X chromosome

KW - heterogametic sex determination

KW - hybridization

KW - sex ratio

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UR - http://www.mendeley.com/research/reconstruction-female-heterogamety-admixture-xxxy-zzzw-sexchromosome-systems-within-frog-species

UR - http://purl.org/au-research/grants/arc/FT110100733

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SP - 4078

EP - 4089

JO - Molecular Biology

JF - Molecular Biology

SN - 0962-1083

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ER -