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

Abstract

BackgroundIn 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.ResultsWe 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.ConclusionsPatterns 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 materialThe online version of this article (doi:10.1186/s12862-016-0814-x) contains supplementary material, which is available to author...

Nuclear microsatellite and mitochondrial DNA analyses reveal the regional genetic structure and phylogeographical history of a sanguivorous land leech, Haemadipsa japonica, in Japan

“…The divergence of these lineages was estimated to have occurred ~700,000 years ago, and sublineages B1 and B2 were estimated to have diverged ~400,000 years ago; both estimated times are in the middle Pleistocene (Figure ). Genetic differentiation between northeastern and southwestern lineages has been reported in several common animal species found across Honshu, Shikoku, and Kyushu, such as the Japanese sika deer ( Cervus nippon ), Japanese hare ( Lepus brachyurus ), tree frog ( Hyla japonica ), Pelophylax frog ( Pelophylax nigromaculatus ), and seed parasitic weevil ( Curculio hilgendorfi ) (Aoki, Kato, & Murakami, ; Dufresnes et al, ; Nagata et al, ; Nunome, Torii, Matsuki, Kinoshita, & Suzuki, ). The existence of two lineages in the aforementioned animal species was proposed based on intraspecific phylogenetic analyses, and it was tentatively explained by two biogeographical events: (a) independent migration of the two lineages from the Asian continent to Japan and (b) the expansion from northern and southern refugia within the Japanese archipelago.…”

Phylogeographic and population insights of the Asian common toad (Bufo gargarizans) in Korea and China: population isolation and expansions as response to the ice ages

“…Moreover, the Korean Peninsula is divided by geographical landscape barriers, leading to the emergence of several clades within Pelophylax chosenicus ( Min et al, 2008 ), Hynobius spp. ( Baek et al, 2011 ; Min et al, 2016 ) and Dryophytes japonicus ( Dufresnes et al, 2016 ), a consequence of allopatric divergence.…”

Interspecific Variation in Seasonal Migration and Brumation Behavior in Two Closely Related Species of Treefrogs

“…Whereas, D. japonicus migrates twice yearly between rice paddies and forested areas, to breed and overwinter, D. suweonensis is present at rice paddies all year round and hibernates buried underground. The ancestors of the two species diverged during the Late Miocene (8.7∼6.5 Mya Duellman et al, 2016;Dufresnes et al, 2016), apparently when one of the two species adapted to a different environment. It is likely that this happened when D. suweonensis preferentially selected marshes for breeding, whereas the preference of the ancestral species is expected to have been broader, a characteristic shared by most Hyla and Dryophytes species.…”

“…We conducted all experiments with the agreement of the Ministry of Environment from the Republic of Korea under permit numbers 2013-16, 2014-04, 2014-08, 2014-20, 2015-3, 2015-4, 2015-6, 2015-28, and 2016-5. Dryophytes suweonensis is slender and smaller than D. japonicus (Borzée et al, 2013), and the earlier species is active earlier in the afternoon than the latter, although both species are principally active at night (Borzée et al, 2016b). Dryophytes japonicus is widespread on the Asian mainland until central Mongolia and the Baikal lake region in Russia (Dufresnes et al, 2016;Kuzmin et al, 2017) but the two species only co-occur on the western lowlands of the Korean Peninsula, where the distribution of D. suweonensis is restricted to agricultural wetlands due to widespread habitat modification (Roh et al, 2014;Borzée and Jang, 2015;Borzée et al, 2015aBorzée et al, , 2018aBorzée and Seliger, 2018). The use of rice paddies impacts the breeding behavior of both species (Borzée et al, 2018b;Groffen et al, 2018), which display both temporal and spatial segregation during the breeding season (Borzée et al, 2016a,b).…”