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Timeframe of speciation inferred from secondary contact zones in the European tree frog radiation (Hyla arborea group).

Dufresnes C, Brelsford A, Crnobrnja-Isailović J, Tzankov N, Lymberakis P, Perrin N - BMC Evol. Biol. (2015)

Bottom Line: We found concordant geographic distributions of nuclear and mitochondrial gene pools, and replicated narrow transitions (~30 km) across two independent transects, indicating an advanced state of reproductive isolation and potential local barriers to dispersal.This result parallels the situation between H. arborea and H. intermedia, which share the same amount of divergence with H. orientalis.General assumptions on the time necessary for speciation based on evidence from unrelated taxa may thus be unreliable.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology & Evolution, University of Lausanne, Biophore Building, 1015, Lausanne, Switzerland. Christophe.Dufresnes@unil.ch.

ABSTRACT

Background: Hybridization between incipient species is expected to become progressively limited as their genetic divergence increases and reproductive isolation proceeds. Amphibian radiations and their secondary contact zones are useful models to infer the timeframes of speciation, but empirical data from natural systems remains extremely scarce. Here we follow this approach in the European radiation of tree frogs (Hyla arborea group). We investigated a natural hybrid zone between two lineages (Hyla arborea and Hyla orientalis) of Mio-Pliocene divergence (~5 My) for comparison with other hybrid systems from this group.

Results: We found concordant geographic distributions of nuclear and mitochondrial gene pools, and replicated narrow transitions (~30 km) across two independent transects, indicating an advanced state of reproductive isolation and potential local barriers to dispersal. This result parallels the situation between H. arborea and H. intermedia, which share the same amount of divergence with H. orientalis. In contrast, younger lineages show much stronger admixture at secondary contacts.

Conclusions: Our findings corroborate the negative relationship between hybridizability and divergence time in European tree frogs, where 5 My are necessary to achieve almost complete reproductive isolation. Speciation seems to progress homogeneously in this radiation, and might thus be driven by gradual genome-wide changes rather than single speciation genes. However, the timescale differs greatly from that of other well-studied amphibians. General assumptions on the time necessary for speciation based on evidence from unrelated taxa may thus be unreliable. In contrast, comparative hybrid zone analyses within single radiations such as our case study are useful to appreciate the advance of speciation in space and time.

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Distribution of H. arborea (green) and H. orientalis (blue) mtDNA haplotypes (a) and nuclear gene pools (b). The latter is shown by Bayesian clustering assignments of individual microsatellite genotypes (barplots) and mean probability assignment of each population (map) into two groups (STRUCTURE, K = 2). Pie charts are proportional to sample size. Dash lines highlight the two transects considered in the cline analyses. Zooms on hybrid zones are provided in Additional file 1: Figure S1. Color shadings (top right frames) show the distribution ranges of the two species, following [15]
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Fig1: Distribution of H. arborea (green) and H. orientalis (blue) mtDNA haplotypes (a) and nuclear gene pools (b). The latter is shown by Bayesian clustering assignments of individual microsatellite genotypes (barplots) and mean probability assignment of each population (map) into two groups (STRUCTURE, K = 2). Pie charts are proportional to sample size. Dash lines highlight the two transects considered in the cline analyses. Zooms on hybrid zones are provided in Additional file 1: Figure S1. Color shadings (top right frames) show the distribution ranges of the two species, following [15]

Mentions: The distributions of the two mitochondrial haplotypes were mostly delineated by the Balkan and Rhodope Mountains, where several parapatric populations occur (Fig. 1a). Over the study area, H. arborea mtDNA was found across Kosovo region, southern Serbia, FYR Macedonia and northern Greece, where it reaches its most eastern range in Thrace. It is also present at the extreme southwestern end of Bulgaria, namely at two sites in the upper Struma valley (loc. 35, 37). Reciprocally, H. orientalis mtDNA extends from Turkey over most of Bulgaria, and meets H. arborea in Thrace and southeastern Serbia.Fig. 1


Timeframe of speciation inferred from secondary contact zones in the European tree frog radiation (Hyla arborea group).

Dufresnes C, Brelsford A, Crnobrnja-Isailović J, Tzankov N, Lymberakis P, Perrin N - BMC Evol. Biol. (2015)

Distribution of H. arborea (green) and H. orientalis (blue) mtDNA haplotypes (a) and nuclear gene pools (b). The latter is shown by Bayesian clustering assignments of individual microsatellite genotypes (barplots) and mean probability assignment of each population (map) into two groups (STRUCTURE, K = 2). Pie charts are proportional to sample size. Dash lines highlight the two transects considered in the cline analyses. Zooms on hybrid zones are provided in Additional file 1: Figure S1. Color shadings (top right frames) show the distribution ranges of the two species, following [15]
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4528686&req=5

Fig1: Distribution of H. arborea (green) and H. orientalis (blue) mtDNA haplotypes (a) and nuclear gene pools (b). The latter is shown by Bayesian clustering assignments of individual microsatellite genotypes (barplots) and mean probability assignment of each population (map) into two groups (STRUCTURE, K = 2). Pie charts are proportional to sample size. Dash lines highlight the two transects considered in the cline analyses. Zooms on hybrid zones are provided in Additional file 1: Figure S1. Color shadings (top right frames) show the distribution ranges of the two species, following [15]
Mentions: The distributions of the two mitochondrial haplotypes were mostly delineated by the Balkan and Rhodope Mountains, where several parapatric populations occur (Fig. 1a). Over the study area, H. arborea mtDNA was found across Kosovo region, southern Serbia, FYR Macedonia and northern Greece, where it reaches its most eastern range in Thrace. It is also present at the extreme southwestern end of Bulgaria, namely at two sites in the upper Struma valley (loc. 35, 37). Reciprocally, H. orientalis mtDNA extends from Turkey over most of Bulgaria, and meets H. arborea in Thrace and southeastern Serbia.Fig. 1

Bottom Line: We found concordant geographic distributions of nuclear and mitochondrial gene pools, and replicated narrow transitions (~30 km) across two independent transects, indicating an advanced state of reproductive isolation and potential local barriers to dispersal.This result parallels the situation between H. arborea and H. intermedia, which share the same amount of divergence with H. orientalis.General assumptions on the time necessary for speciation based on evidence from unrelated taxa may thus be unreliable.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology & Evolution, University of Lausanne, Biophore Building, 1015, Lausanne, Switzerland. Christophe.Dufresnes@unil.ch.

ABSTRACT

Background: Hybridization between incipient species is expected to become progressively limited as their genetic divergence increases and reproductive isolation proceeds. Amphibian radiations and their secondary contact zones are useful models to infer the timeframes of speciation, but empirical data from natural systems remains extremely scarce. Here we follow this approach in the European radiation of tree frogs (Hyla arborea group). We investigated a natural hybrid zone between two lineages (Hyla arborea and Hyla orientalis) of Mio-Pliocene divergence (~5 My) for comparison with other hybrid systems from this group.

Results: We found concordant geographic distributions of nuclear and mitochondrial gene pools, and replicated narrow transitions (~30 km) across two independent transects, indicating an advanced state of reproductive isolation and potential local barriers to dispersal. This result parallels the situation between H. arborea and H. intermedia, which share the same amount of divergence with H. orientalis. In contrast, younger lineages show much stronger admixture at secondary contacts.

Conclusions: Our findings corroborate the negative relationship between hybridizability and divergence time in European tree frogs, where 5 My are necessary to achieve almost complete reproductive isolation. Speciation seems to progress homogeneously in this radiation, and might thus be driven by gradual genome-wide changes rather than single speciation genes. However, the timescale differs greatly from that of other well-studied amphibians. General assumptions on the time necessary for speciation based on evidence from unrelated taxa may thus be unreliable. In contrast, comparative hybrid zone analyses within single radiations such as our case study are useful to appreciate the advance of speciation in space and time.

Show MeSH