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.
Highlights
Sex chromosomes have evolved along dramatically divergent pathways among vertebrates, depending on lineages
Our study was approved by the relevant Institutional Animal Care and Use Committee (IACUC), namely the Service de la Consommation et des Affaires Veterinaires du Canton de Vaud (Epalinges, Switzerland); no live animal was sacrificed for the study; other samples came from scientific collections specified in Table S1, Supporting Information
Two large indels in Ha-A103 were shared by X and Y haplotypes: the same 37 bp deletion occurred on the two copies of males from southeastern Europe (e.g. 3-=1, 7-=1 and 9-=3), the Pannonian Basin (e.g. 18-=2, 19-=3) and NW Europe (20-=1); the same 473 bp insertion was shared by the X and Y alleles of two males from the Pannonian Basin (15=2 and 18-=1)
Summary
Sex chromosomes have evolved along dramatically divergent pathways among vertebrates, depending on lineages. Occasional turnovers may replace established sex chromosomes before they had time to decay Occasional XY recombination may rejuvenate senescing Y chromosomes by purging the load of deleterious mutations that accumulate in non-recombining genomic regions [3]; very rare events of X-Y recombination seem sufficient to prevent Y degeneration [4]. Several species of the Hyla arborea radiation inherited the same pair of sex chromosomes from a common ancestor Mya); despite arrest of recombination in males, the X and Y allelic sequences of sex-linked genes cluster by species, not by gametologs [5,6], pointing to occasional events of recombination. West-European populations of the nominal species (Hyla arborea) consistently display sex-specific allelic frequencies at series of sex-linked microsatellite markers, often with male-diagnostic alleles West-European populations of the nominal species (Hyla arborea) consistently display sex-specific allelic frequencies at series of sex-linked microsatellite markers, often with male-diagnostic alleles (e.g. [5,8]), pointing to the absence of XY recombination in their recent history
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