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Phylogeography reveals an ancient cryptic radiation in East-Asian tree frogs ( Hyla japonica group) and complex relationships between continental and island lineages

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ABSTRACT

Background: In contrast to the Western Palearctic and Nearctic biogeographic regions, the phylogeography of Eastern-Palearctic terrestrial vertebrates has received relatively little attention. In East Asia, tectonic events, along with Pleistocene climatic conditions, likely affected species distribution and diversity, especially through their impact on sea levels and the consequent opening and closing of land-bridges between Eurasia and the Japanese Archipelago. To better understand these effects, we sequenced mitochondrial and nuclear markers to determine phylogeographic patterns in East-Asian tree frogs, with a particular focus on the widespread H. japonica.

Results: We document several cryptic lineages within the currently recognized H. japonica populations, including two main clades of Late Miocene divergence (~5 Mya). One occurs on the northeastern Japanese Archipelago (Honshu and Hokkaido) and the Russian Far-East islands (Kunashir and Sakhalin), and the second one inhabits the remaining range, comprising southwestern Japan, the Korean Peninsula, Transiberian China, Russia and Mongolia. Each clade further features strong allopatric Plio-Pleistocene subdivisions (~2-3 Mya), especially among continental and southwestern Japanese tree frog populations. Combined with paleo-climate-based distribution models, the molecular data allowed the identification of Pleistocene glacial refugia and continental routes of postglacial recolonization. Phylogenetic reconstructions further supported genetic homogeneity between the Korean H. suweonensis and Chinese H. immaculata, suggesting the former to be a relic population of the latter that arose when the Yellow Sea formed, at the end of the last glaciation.

Conclusions: Patterns of divergence and diversity were likely triggered by Miocene tectonic activities and Quaternary climatic fluctuations (including glaciations), causing the formation and disappearance of land-bridges between the Japanese islands and the continent. Overall, this resulted in a ring-like diversification of H. japonica around the Sea of Japan. Our findings urge for important taxonomic revisions in East-Asian tree frogs. First, they support the synonymy of H. suweonensis (Kuramoto, 1980) and H. immaculata (Boettger, 1888). Second, the nominal H. japonica (Günther, 1859) represents at least two species: an eastern (new taxon A) on the northern Japanese and Russian Far East islands, and a southwestern species (n. t. B) on southern Japanese islands and possibly also forming continental populations. Third, these continental tree frogs may also represent an additional entity, previously described as H. stepheni Boulenger, 1888 (senior synonym of H. ussuriensis Nikolskii, 1918). A complete revision of this group requires further taxonomic and nomenclatural analyses, especially since it remains unclear to which taxon the species-epitheton japonica corresponds to.

Electronic supplementary material: The online version of this article (doi:10.1186/s12862-016-0814-x) contains supplementary material, which is available to authorized users.

No MeSH data available.


Related in: MedlinePlus

Haplotype network of mitochondrial cyt-b and distribution of the main lineages. For H. japonica, pies are proportional to sample sizes and colors correspond to the different clades. Haplotypes of H. suweonensis (ours and GenBank data) were all sampled within the vicinity of Seoul, Korea, where it is endemic
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Fig3: Haplotype network of mitochondrial cyt-b and distribution of the main lineages. For H. japonica, pies are proportional to sample sizes and colors correspond to the different clades. Haplotypes of H. suweonensis (ours and GenBank data) were all sampled within the vicinity of Seoul, Korea, where it is endemic

Mentions: The mitochondrial phylogenetic tree recovered a very diverse, old but monophyletic radiation of H. japonica, including at least nine mitochondrial lineages with varying degrees of divergence (Fig. 1) and clear geographic association (Fig. 3).Fig. 3


Phylogeography reveals an ancient cryptic radiation in East-Asian tree frogs ( Hyla japonica group) and complex relationships between continental and island lineages
Haplotype network of mitochondrial cyt-b and distribution of the main lineages. For H. japonica, pies are proportional to sample sizes and colors correspond to the different clades. Haplotypes of H. suweonensis (ours and GenBank data) were all sampled within the vicinity of Seoul, Korea, where it is endemic
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC5121986&req=5

Fig3: Haplotype network of mitochondrial cyt-b and distribution of the main lineages. For H. japonica, pies are proportional to sample sizes and colors correspond to the different clades. Haplotypes of H. suweonensis (ours and GenBank data) were all sampled within the vicinity of Seoul, Korea, where it is endemic
Mentions: The mitochondrial phylogenetic tree recovered a very diverse, old but monophyletic radiation of H. japonica, including at least nine mitochondrial lineages with varying degrees of divergence (Fig. 1) and clear geographic association (Fig. 3).Fig. 3

View Article: PubMed Central - PubMed

ABSTRACT

Background: In contrast to the Western Palearctic and Nearctic biogeographic regions, the phylogeography of Eastern-Palearctic terrestrial vertebrates has received relatively little attention. In East Asia, tectonic events, along with Pleistocene climatic conditions, likely affected species distribution and diversity, especially through their impact on sea levels and the consequent opening and closing of land-bridges between Eurasia and the Japanese Archipelago. To better understand these effects, we sequenced mitochondrial and nuclear markers to determine phylogeographic patterns in East-Asian tree frogs, with a particular focus on the widespread H. japonica.

Results: We document several cryptic lineages within the currently recognized H. japonica populations, including two main clades of Late Miocene divergence (~5 Mya). One occurs on the northeastern Japanese Archipelago (Honshu and Hokkaido) and the Russian Far-East islands (Kunashir and Sakhalin), and the second one inhabits the remaining range, comprising southwestern Japan, the Korean Peninsula, Transiberian China, Russia and Mongolia. Each clade further features strong allopatric Plio-Pleistocene subdivisions (~2-3 Mya), especially among continental and southwestern Japanese tree frog populations. Combined with paleo-climate-based distribution models, the molecular data allowed the identification of Pleistocene glacial refugia and continental routes of postglacial recolonization. Phylogenetic reconstructions further supported genetic homogeneity between the Korean H. suweonensis and Chinese H. immaculata, suggesting the former to be a relic population of the latter that arose when the Yellow Sea formed, at the end of the last glaciation.

Conclusions: Patterns of divergence and diversity were likely triggered by Miocene tectonic activities and Quaternary climatic fluctuations (including glaciations), causing the formation and disappearance of land-bridges between the Japanese islands and the continent. Overall, this resulted in a ring-like diversification of H. japonica around the Sea of Japan. Our findings urge for important taxonomic revisions in East-Asian tree frogs. First, they support the synonymy of H. suweonensis (Kuramoto, 1980) and H. immaculata (Boettger, 1888). Second, the nominal H. japonica (Günther, 1859) represents at least two species: an eastern (new taxon A) on the northern Japanese and Russian Far East islands, and a southwestern species (n. t. B) on southern Japanese islands and possibly also forming continental populations. Third, these continental tree frogs may also represent an additional entity, previously described as H. stepheni Boulenger, 1888 (senior synonym of H. ussuriensis Nikolskii, 1918). A complete revision of this group requires further taxonomic and nomenclatural analyses, especially since it remains unclear to which taxon the species-epitheton japonica corresponds to.

Electronic supplementary material: The online version of this article (doi:10.1186/s12862-016-0814-x) contains supplementary material, which is available to authorized users.

No MeSH data available.


Related in: MedlinePlus