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Range-wide sex-chromosome sequence similarity supports occasional XY recombination in European tree frogs (Hyla arborea).

Dufresnes C, Stöck M, Brelsford A, Perrin N - PLoS ONE (2014)

Bottom Line: In contrast with mammals and birds, most poikilothermic vertebrates feature structurally undifferentiated sex chromosomes, which may result either from frequent turnovers, or from occasional events of XY recombination.In contrast, populations of NW Europe, which originated from a recent postglacial expansion, show a clear pattern of XY differentiation; the X and Y gametologs of the sex-linked gene Med15 present different alleles, likely fixed by drift on the front wave of expansions, and kept differentiated since.Our results support the view that sex-chromosome homomorphy in H. arborea is maintained by occasional or historical events of recombination; whether the frequency of these events indeed differs between populations remains to be clarified.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and evolution, Biophore Building, University of Lausanne, Lausanne, Switzerland.

ABSTRACT
In contrast with mammals and birds, most poikilothermic vertebrates feature structurally undifferentiated sex chromosomes, which may result either from frequent turnovers, or from occasional events of XY recombination. The latter mechanism was recently suggested to be responsible for sex-chromosome homomorphy in European tree frogs (Hyla arborea). However, no single case of male recombination has been identified in large-scale laboratory crosses, and populations from NW Europe consistently display sex-specific allelic frequencies with male-diagnostic alleles, suggesting the absence of recombination in their recent history. To address this apparent paradox, we extended the phylogeographic scope of investigations, by analyzing the sequences of three sex-linked markers throughout the whole species distribution. Refugial populations (southern Balkans and Adriatic coast) show a mix of X and Y alleles in haplotypic networks, and no more within-individual pairwise nucleotide differences in males than in females, testifying to recurrent XY recombination. In contrast, populations of NW Europe, which originated from a recent postglacial expansion, show a clear pattern of XY differentiation; the X and Y gametologs of the sex-linked gene Med15 present different alleles, likely fixed by drift on the front wave of expansions, and kept differentiated since. Our results support the view that sex-chromosome homomorphy in H. arborea is maintained by occasional or historical events of recombination; whether the frequency of these events indeed differs between populations remains to be clarified.

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Sampling localities (a) and haplotype networks of Smarcb1 (b), Med15 (c) and Ha-A103 (d).For each allele, labels indicate locality number, followed by the sex of the individual (black for females and white for males), a sample number, and the letter a or b (discriminating two alleles of heterozygotes; written “ab” for homozygotes). The colors of haplotypes correspond to the main phylogeographic regions across H. arborea’s present distribution range (as described by Stöck et al. 2012, and Dufresnes et al. 2013), delimited by thin dashed lines on the map (orange: southeastern European refugia; violet: Pannonian basin; green: NW Europe). Arrows show post-glacial recolonization routes.
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pone-0097959-g001: Sampling localities (a) and haplotype networks of Smarcb1 (b), Med15 (c) and Ha-A103 (d).For each allele, labels indicate locality number, followed by the sex of the individual (black for females and white for males), a sample number, and the letter a or b (discriminating two alleles of heterozygotes; written “ab” for homozygotes). The colors of haplotypes correspond to the main phylogeographic regions across H. arborea’s present distribution range (as described by Stöck et al. 2012, and Dufresnes et al. 2013), delimited by thin dashed lines on the map (orange: southeastern European refugia; violet: Pannonian basin; green: NW Europe). Arrows show post-glacial recolonization routes.

Mentions: To address this apparent paradox, we decided to extend investigations on the patterns of XY differentiation to a broader phylogeographic framework. West-European populations of H. arborea are of recent origin [9], [10]. The patterns of mitochondrial and nuclear diversity testify to a post-glacial expansion from southeastern Europe, where three main haplogroups (with ∼200 ky divergence) survived in distinct refugia across the Balkan Peninsula. While two of these mitochondrial lineages remained limited to the Balkans (Adriatic coast and southern Balkans; orange area in Fig. 1a), a third one expanded after the Last Glacial Maximum (∼15 kya) to recolonize first the Pannonian Basin (violet area), then from there Western and Northern Europe (green area), losing much of its diversity during this process [10]. In the present study, we use intraspecific sequence polymorphism of three sex-linked markers to seek evidence for possible events of XY recombination during this species’ late Pleistocene history.


Range-wide sex-chromosome sequence similarity supports occasional XY recombination in European tree frogs (Hyla arborea).

Dufresnes C, Stöck M, Brelsford A, Perrin N - PLoS ONE (2014)

Sampling localities (a) and haplotype networks of Smarcb1 (b), Med15 (c) and Ha-A103 (d).For each allele, labels indicate locality number, followed by the sex of the individual (black for females and white for males), a sample number, and the letter a or b (discriminating two alleles of heterozygotes; written “ab” for homozygotes). The colors of haplotypes correspond to the main phylogeographic regions across H. arborea’s present distribution range (as described by Stöck et al. 2012, and Dufresnes et al. 2013), delimited by thin dashed lines on the map (orange: southeastern European refugia; violet: Pannonian basin; green: NW Europe). Arrows show post-glacial recolonization routes.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4043726&req=5

pone-0097959-g001: Sampling localities (a) and haplotype networks of Smarcb1 (b), Med15 (c) and Ha-A103 (d).For each allele, labels indicate locality number, followed by the sex of the individual (black for females and white for males), a sample number, and the letter a or b (discriminating two alleles of heterozygotes; written “ab” for homozygotes). The colors of haplotypes correspond to the main phylogeographic regions across H. arborea’s present distribution range (as described by Stöck et al. 2012, and Dufresnes et al. 2013), delimited by thin dashed lines on the map (orange: southeastern European refugia; violet: Pannonian basin; green: NW Europe). Arrows show post-glacial recolonization routes.
Mentions: To address this apparent paradox, we decided to extend investigations on the patterns of XY differentiation to a broader phylogeographic framework. West-European populations of H. arborea are of recent origin [9], [10]. The patterns of mitochondrial and nuclear diversity testify to a post-glacial expansion from southeastern Europe, where three main haplogroups (with ∼200 ky divergence) survived in distinct refugia across the Balkan Peninsula. While two of these mitochondrial lineages remained limited to the Balkans (Adriatic coast and southern Balkans; orange area in Fig. 1a), a third one expanded after the Last Glacial Maximum (∼15 kya) to recolonize first the Pannonian Basin (violet area), then from there Western and Northern Europe (green area), losing much of its diversity during this process [10]. In the present study, we use intraspecific sequence polymorphism of three sex-linked markers to seek evidence for possible events of XY recombination during this species’ late Pleistocene history.

Bottom Line: In contrast with mammals and birds, most poikilothermic vertebrates feature structurally undifferentiated sex chromosomes, which may result either from frequent turnovers, or from occasional events of XY recombination.In contrast, populations of NW Europe, which originated from a recent postglacial expansion, show a clear pattern of XY differentiation; the X and Y gametologs of the sex-linked gene Med15 present different alleles, likely fixed by drift on the front wave of expansions, and kept differentiated since.Our results support the view that sex-chromosome homomorphy in H. arborea is maintained by occasional or historical events of recombination; whether the frequency of these events indeed differs between populations remains to be clarified.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and evolution, Biophore Building, University of Lausanne, Lausanne, Switzerland.

ABSTRACT
In contrast with mammals and birds, most poikilothermic vertebrates feature structurally undifferentiated sex chromosomes, which may result either from frequent turnovers, or from occasional events of XY recombination. The latter mechanism was recently suggested to be responsible for sex-chromosome homomorphy in European tree frogs (Hyla arborea). However, no single case of male recombination has been identified in large-scale laboratory crosses, and populations from NW Europe consistently display sex-specific allelic frequencies with male-diagnostic alleles, suggesting the absence of recombination in their recent history. To address this apparent paradox, we extended the phylogeographic scope of investigations, by analyzing the sequences of three sex-linked markers throughout the whole species distribution. Refugial populations (southern Balkans and Adriatic coast) show a mix of X and Y alleles in haplotypic networks, and no more within-individual pairwise nucleotide differences in males than in females, testifying to recurrent XY recombination. In contrast, populations of NW Europe, which originated from a recent postglacial expansion, show a clear pattern of XY differentiation; the X and Y gametologs of the sex-linked gene Med15 present different alleles, likely fixed by drift on the front wave of expansions, and kept differentiated since. Our results support the view that sex-chromosome homomorphy in H. arborea is maintained by occasional or historical events of recombination; whether the frequency of these events indeed differs between populations remains to be clarified.

Show MeSH
Related in: MedlinePlus