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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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Pairwise nucleotide differences (pd) between the two Med15 alleles of every male (white bars) and female (black bars).Larger values are found in the southeastern Europe and the Pannonian Basin (left) than in NW Europe (right), and, in the latter region, in males than in females.
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pone-0097959-g002: Pairwise nucleotide differences (pd) between the two Med15 alleles of every male (white bars) and female (black bars).Larger values are found in the southeastern Europe and the Pannonian Basin (left) than in NW Europe (right), and, in the latter region, in males than in females.

Mentions: However, closer inspection reveals some differences between phylogeographic regions. In particular, the patterns of diversity and differentiation at Med15 display a clear trend with geography (Fig. 1c). Whereas male alleles from southeastern refugial (orange) and Pannonian (violet) populations mix randomly with female alleles in the network, sex-differences occur for NW Europe (green, loc. 20–30). With the single exception of individual 29-♂1, all males harbor one and only one copy of allele H16, otherwise identified from sibship analyses as the Y allele in several Swiss and French populations (referred to as allele Ha5-22 236 in [8], [16]. This allele was only found in males throughout the H. arborea range covered by our study, including some from the Pannonian Basin (violet) and southeastern European glacial refugia (orange), where it might also occur on the Y. The second allele (i.e., the X copy) from all Western and Northern European Hyla males belongs to the H1–H15 haplogroup, otherwise shared by all females from these populations, plus some from the Pannonian Basin. This was the only haplogroup found in females from Western and Northern Europe, but many more segregated in females from the Pannonian Basin and southeastern European refugial populations. Accordingly, a two-way ANOVA, with sex and geographic region (North-Western Europe versus Pannonian and southeastern populations) as factors, identified significant effects for both the region (F1,49 = 12.5, p-value = 0.009) and the interaction between sex and region (F1,49 = 3.38, p-value = 0.023). As shown in Fig. 2, this reflects respectively the higher diversity of southeastern European and Pannonian populations ( = 8.2 as opposed to 3.3 in Northern and Western Europe) and the strong XY differentiation in North-Western Europe ( = 5.1 in males versus 1.4 in females) compared to the rest of the range ( = 8.9 in males versus 7.4 in females). The only exception (male 29-♂1, from the westernmost part of the distribution range) deserves special mention: given the strong differentiation between the haplotypes H3 and H4 harbored by this male on one hand, and the haplotype H16 fixed on the Y of other males on the other hand, the pattern observed is most likely to result from a recent (post-glacial) event of XY recombination.


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)

Pairwise nucleotide differences (pd) between the two Med15 alleles of every male (white bars) and female (black bars).Larger values are found in the southeastern Europe and the Pannonian Basin (left) than in NW Europe (right), and, in the latter region, in males than in females.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0097959-g002: Pairwise nucleotide differences (pd) between the two Med15 alleles of every male (white bars) and female (black bars).Larger values are found in the southeastern Europe and the Pannonian Basin (left) than in NW Europe (right), and, in the latter region, in males than in females.
Mentions: However, closer inspection reveals some differences between phylogeographic regions. In particular, the patterns of diversity and differentiation at Med15 display a clear trend with geography (Fig. 1c). Whereas male alleles from southeastern refugial (orange) and Pannonian (violet) populations mix randomly with female alleles in the network, sex-differences occur for NW Europe (green, loc. 20–30). With the single exception of individual 29-♂1, all males harbor one and only one copy of allele H16, otherwise identified from sibship analyses as the Y allele in several Swiss and French populations (referred to as allele Ha5-22 236 in [8], [16]. This allele was only found in males throughout the H. arborea range covered by our study, including some from the Pannonian Basin (violet) and southeastern European glacial refugia (orange), where it might also occur on the Y. The second allele (i.e., the X copy) from all Western and Northern European Hyla males belongs to the H1–H15 haplogroup, otherwise shared by all females from these populations, plus some from the Pannonian Basin. This was the only haplogroup found in females from Western and Northern Europe, but many more segregated in females from the Pannonian Basin and southeastern European refugial populations. Accordingly, a two-way ANOVA, with sex and geographic region (North-Western Europe versus Pannonian and southeastern populations) as factors, identified significant effects for both the region (F1,49 = 12.5, p-value = 0.009) and the interaction between sex and region (F1,49 = 3.38, p-value = 0.023). As shown in Fig. 2, this reflects respectively the higher diversity of southeastern European and Pannonian populations ( = 8.2 as opposed to 3.3 in Northern and Western Europe) and the strong XY differentiation in North-Western Europe ( = 5.1 in males versus 1.4 in females) compared to the rest of the range ( = 8.9 in males versus 7.4 in females). The only exception (male 29-♂1, from the westernmost part of the distribution range) deserves special mention: given the strong differentiation between the haplotypes H3 and H4 harbored by this male on one hand, and the haplotype H16 fixed on the Y of other males on the other hand, the pattern observed is most likely to result from a recent (post-glacial) event of XY recombination.

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