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Scale Demographic Processes Resulting from Multiple Overseas Journal of Biogeography (J. Biogeogr.) (2016) ORIGINAL Fine-scale demographic processes ARTICLE resulting from multiple overseas colonization events of the Japanese stream tree frog, Buergeria japonica Shohei Komaki1,2, Si-Min Lin3, Masafumi Nozawa4,5, Shohei Oumi6, Masayuki Sumida7 and Takeshi Igawa1* 1Division of Developmental Science, Graduate ABSTRACT School for International Development and Aim Amphibians are considered poor transoceanic dispersers because of their Cooperation, Hiroshima University, Higashi- permeable skin. However, overseas dispersal of amphibian species has been Hiroshima, Hiroshima 739-8529, Japan, 2Global Career Design Center, Hiroshima revealed by recent phylogeographical studies and the role of overseas coloniza- University, Higashi-Hiroshima, Hiroshima tion of amphibians on their evolution and diversification has also been high- 739-8514, Japan, 3Department of Life Science, lighted. However, no studies have investigated in detail the demographic National Taiwan Normal University, Taipei processes related to these overseas colonization events. To clarify how amphib- 116, Taiwan, 4Department of Genetics, ians achieve overseas colonization, we estimated the demographic history of SOKENDAI, Mishima, Shizuoka 411-8540, the Japanese stream tree frog, Buergeria japonica, which is distributed on Japan, 5Center for Information Biology, Amami Island and four northern neighbouring islands of the Tokara Archipelago, National Institute of Genetics, Mishima, Japan. Shizuoka 411-8540, Japan, 6Section of Location South-western islands of Japan and Taiwan. Agriculture and Forest, Amami City Government, Amami, Kagoshima 894-0048, Methods We analysed the mitochondrial cytb gene and 20 microsatellite loci, Japan, 7Institute for Amphibian Biology, and constructed phylogenetic trees based on these data. We also performed Graduate School of Science, Hiroshima demographic analyses by applying approximate Bayesian computation (ABC) University, Higashi-Hiroshima, Hiroshima method and an isolation-with-migration model. 739-8526, Japan Results Phylogenetic and demographic analyses based on cytb and 20 microsatellite genotype data revealed that divergence among island populations took place recently, mostly within the last few thousand years. Populations from the northern islands had reduced genetic diversity compared with south- ern islands, and ABC analyses supported the hypothesis that the species colo- nized islands from south to north. Main conclusions Given that the islands are separated from each other by deep sea, the recent divergences observed indicate overseas colonization events among the five islands. ABC analyses support the hypothesis that B. japonica underwent a stepping-stone overseas colonization from southern to northern neighbouring islands during the past few thousand years accompanied by mul- tiple founder effects. These results support the hypothesis that overseas colo- nization could have had a substantial impact on amphibian evolution and *Correspondence: Takeshi Igawa, Division of diversification. Developmental Science, Graduate School for International Development and Cooperation, Keywords Hiroshima University, Higashi-Hiroshima, ABC model, amphibian, biogeography, founder effect, IM model, island Hiroshima 739-8529, Japan. E-mail:[email protected] populations osmotic stress; thus, their biogeographical patterns have gen- INTRODUCTION erally been explained by the historical formation of sea barri- Ever since Darwin (1859), overseas dispersal of amphibians ers or land connections (Beerli et al., 1996; Igawa et al., was believed to be unusual or exceptional. Because of their 2006; Blackburn et al., 2010; Komaki et al., 2015). However, permeable skin, amphibians are particularly sensitive to recent molecular phylogenetic studies have highlighted ª 2016 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/jbi 1 doi:10.1111/jbi.12922 S. Komaki et al. instances of overseas dispersal and colonization of amphib- between populations on Amami/Takara Islands and the other ians that strongly influenced the evolution and diversification islands of the Tokara Archipelago estimated by IM analysis. on focal islands (e.g. Vences et al., 2003, 2004; Kurabayashi However, their analysis was based on a single mitochondrial et al., 2011; Pinto-Sanchez et al., 2012; Pyron, 2014; Bell gene with insufficient nucleotide variation. Furthermore, the et al., 2015; Brown et al., 2016). These studies applied migration rate between island populations was simultane- molecular phylogenetic approaches to focus on divergence ously estimated in their analysis based on the limited events that dated back millions of years ago and that resulted sequence data. Therefore, their estimation could have led the in speciation. Their conclusions were thus derived from esti- wrong interpretation on the demographic history of B. mated divergence times between island populations that japonica. Here, by comprehensive sample collection covering post-date the formation of sea barriers. Consequently, the distribution range of the species, and analyses using a although overseas colonization is considered to be an impor- combination of mtDNA sequences and highly polymorphic tant process that has affected amphibian diversity, distribu- microsatellite loci, we re-examine the hypothesis that B. tions, evolution and demography, the detailed processes of japonica populations in the Tokara Archipelago arose from such events have not been investigated in amphibians to overseas dispersal, and explore the fine-scale demographic date. processes related to dispersal and colonization of B. japonica The genetic signals of overseas colonization events may be on islands of the Tokara Archipelago. We then discuss how obscured over time because of genetic drift, natural selection B. japonica colonized these islands in the context of geo- and migration between island and continental populations graphical features, and ecological and physiological character- (Stuessy et al., 2012; Habel & Zachos, 2013), which could istics of this species. have hampered the study of demographic processes related to overseas dispersal. For this reason, considering recent MATERIALS AND METHODS overseas dispersal events may be more promising for eluci- dating finer scale demographic processes of overseas dispersal Sample collection and colonization. The Japanese stream tree frog, Buergeria japonica,isan In total, 199 adult B. japonica were sampled by hand from ideal species to address overseas dispersal of amphibians. 15 localities on eight islands and toe clipped to obtain tissue This species is widely distributed throughout the Ryukyu samples for molecular analysis (Fig. 1). Archipelago in Japan and Taiwan (Maeda & Matsui, 1999), In the Tokara Archipelago, 76 samples were collected from and, in particular, is the only amphibian species naturally four islands (Tables 1 & see S5 in Supporting Information): distributed in the Tokara Archipelago (Maenosono & Toda, Kuchinoshima (Kuchi; N = 20), Nakanoshima (Naka; 2007). The Tokara Archipelago consists of 10 small islands N = 20), Tairajima (Taira; N = 16), and Takarajima (Takara; with areas that range from 0.36 to 24.47 km2, six of which N = 20). Since the population on Akusekijima Is. was artifi- are inhabited by B. japonica. Although a population on cially introduced we did not study this island population. We Akusekijima Island was introduced from the other island were also unable to study individuals from Gajajima (Gaja) around four decades ago (Maenosono & Toda, 2007; per- Is., where B. japonica occurs since it is an abandoned island. sonal communication), the populations on the remaining On islands outside the Tokara Archipelago, 123 toe clips five islands (Kuchinoshima, Nakanoshima, Tairajima, were sampled from the following locations (Tables 1 & S5): Takarajima and Gajajima) are considered native. Islands of Fukumoto (N = 20), Tatsugo (N = 20), Uragami (N = 4), the Tokara Archipelago are separated from each other by Sumiyo (N = 5) and Setouchi (N = 3) on Amamioshima deep sea water of > 400 m in depth, which is deeper than (Amami) Is.; Kunigami (N = 16) and Ogimi (N = 20) on the lowest sea level during glacial maxima in the last Okinawajima (Okinawa) Is.; Shirahama (N = 17) on Iri- 500,000 years (À120 m) (Grant et al., 2014). As the islands omotejima (Iriomote) Is.; and Taipei (N = 16), Chichi are located on different island shelves and their volcanic edi- (N = 1) and Hualien (N = 1) on Taiwan Is. fices are developed from the bottom of the deep sea, none of the islands should have been connected by land bridges and DNA extraction and genotyping of mitochondrial they are therefore considered isolated volcanic islands (ocea- haplotypes and microsatellite loci nic islands) (Yokose et al., 2010; Osozawa et al., 2012). Con- sequently, B. japonica populations on these islands appear to Genomic DNA of 199 tissue samples was extracted using have colonized across sea barriers. DNA suisui-F (RIZO, Ibaraki, Japan) following the manufac- Phylogenetic studies based on allozyme data and mito- turer’s instructions. A 777-bp fragment of the mitochondrial chondrial cytochrome b and 16S rRNA nucleotide sequence cytochrome b gene (cytb) was amplified and sequenced from data reported little genetic differentiation between Amami 134 specimens (detailed methods are described in and Tokara populations (Nishioka et al., 1987; Tominaga Appendix S1), including all individuals from the four focal et al., 2015), which indicates that B. japonica dispersed and
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