DOI: 10.1111/jbi.13111 ORIGINAL ARTICLE Riding the Kuroshio Current: Stepping stone dispersal of the Okinawa tree lizard across the East Asian Island Arc Shang-Fang Yang1 | Shohei Komaki2 | Rafe M. Brown3 | Si-Min Lin1 1Department of Life Science, National Taiwan Normal University, Taipei, Taiwan Abstract 2Division of Biomedical Information Aim: Located hundreds of kilometres offshore of continental mainland Asia, the Analysis, Iwate Tohoku Medical Megabank extremely high level of land vertebrate endemism in the East Asian Island Arc pro- Organization, Iwate Medical University, Morioka, Iwate, Japan vides an excellent opportunity to test hypotheses regarding biogeographic processes 3Biodiversity Institute and Department of and speciation. In this study, we aim to test alternative explanations for lineage Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS, USA diversification (vicariance versus dispersal models), and further develop a temporal framework for diversification in our focal taxon, which is consistent with the known Correspondence Si-Min Lin, Department of Life Science, age of these islands. We achieve these tests by investigating the historical biogeog- National Taiwan Normal University, Taipei, raphy of the Okinawa tree lizard (Japalura polygonata), one of the few widely- Taiwan. Email: [email protected] distributed reptiles across this archipelago. Location: The East Asian Island Arc: (1) Central Ryukyu (Amami and Okinawa Funding information Japan Society for the Promotion of Science, groups); (2) Southern Ryukyu (Miyako and Yaeyama groups); (3) Taiwan and Grant/Award Number: No. 25-5065; adjacent islands. Ministry of Science and Technology, Taiwan, Grant/Award Number: MOST 105-2621-B- Methods: A total of 246 tissues were sampled from 10 localities in the Ryukyu 003-001-MY3, MOST 105-2621-B-003- archipelago and 17 localities in Taiwan, covering the entire distributional range of 002-MY3; National Science Foundation, USA, Grant/Award Number: DEB 0743491, this species, including all subspecies. DNA sequences of the mitochondrial cyto- NSF DEB 1418895 chrome b, 16S ribosomal RNA, nuclear BACH-1 and RAG-1 genes (total: 4,684 bp) Editor: Isabel Sanmartın were obtained from these samples. We used maximum likelihood and Bayesian methods to infer phylogeny and divergence time, and used a model-fitting method of biogeographical inference to estimate ancestral range evolution. Results: Multiple lines of evidence combine to identify a general pattern of disper- sal-mediated diversification northward through the archipelago, following initial dis- persal from Taiwan. These included (1) a phylogenetic estimate, revealing a sequential, south-to-north branching pattern; (2) ancestral range estimation, inferring multiple overseas dispersals and subsequent colonization of new landmasses; and (3) a reduction in genetic variation observed in successively-diverging lineages, decreasing from Taiwan northward, towards more remote islands. These results pro- vide strong statistical support for an interpretation of successive bouts of dispersal via the powerful, well-documented, south-to-north Kuroshio Current. Estimation of divergence times suggests that most clades in southern Ryukyu and Taiwan diverged early, giving rise to lineages that have remained isolated, and that more recently-diverged lineages then colonized northward to subsequently occupy the landmasses of the Central Ryukyu archipelago. Main conclusions: Our general inference of biogeographic history in Japalura polyg- onata suggested that this species originated on Taiwan and the Yaeyama group, and | Journal of Biogeography. 2018;45:37–50. wileyonlinelibrary.com/journal/jbi © 2017 John Wiley & Sons Ltd 37 38 | YANG ET AL. arrived at its current distribution in Miyako, Okinawa, Toku and Amami islands by a series of stepping-stone dispersals, which we report for the first time for a terres- trial vertebrate endemic to this region. KEYWORDS Agamidae, geographical range evolution, historical biogeography, Japalura polygonata, Ryukyu archipelago, Taiwan 1 | INTRODUCTION intraspecific population genetic studies of Ryuku fauna are still extremely rare. Today’s evolutionary biologists continue a rich tradition of the study The Okinawa tree lizard, Japalura polygonata (Hallowell, 1861), is of speciation on islands (Grant & Grant, 2008; Shaw & Gillespie, one of only two terrestrial vertebrates that are widely distributed 2016). Archipelagos, consisting of a group of geographically and/or throughout the East Asian Island Arc (the other is Buergeria japonica, geologically related islands, provide unique opportunities to evaluate a tree frog of the family Rhacophoridae), and its distributional range competing biogeographical hypotheses of pattern and processes. extends from northern Taiwan to Central Ryukyus (Ota, 1991, Multiple geological and climatic factors have been invoked to explain 2003). The species inhabits evergreen broad-leaf forest and is the variation in distributional and genetic patterns of archipelago terres- most common arboreal insectivore in the archipelago (Shang, 2008; trial organisms. These include as sea-level changes, land bridge for- Uchiyama, Maeda, Numata, & Seki, 2009). Five subspecies have mation and island connectivity, ocean currents, and long-term been proposed: J. p. polygonata, J. p. ishigakiensis, J. p. miyakensis, J. climate oscillations (Atkins, Preston, & Cronk, 2001; Bittkau & p. xanthostoma and J. p. donan. Matsumoto, 1979 synonymized J. p. Comes, 2005; Hedges, Hass, & Maxson, 1992; Ohdachi, Dokuchaev, miyakensis with J. p. ishigakiensis, leaving four subspecies recognized Hasegawa, & Masuda, 2001; Poulakakis et al., 2003). With recent in most recent studies (Ota, 1991, 2003). progress in the development of novel molecular tools and analytical How these lizards came to occupy their current geographical approaches, archipelagoes continue to provide opportunities to test range remains poorly understood, yet the linear configuration of the key predictions in biogeography, which have played formative roles East Asian Island Arc provides an opportunity to test statistically in the development of the field ever since the 19th century (reviews two prevailing classes of alternative hypotheses. On one side of this by Brown, 2016; Lomolino, Riddle, Whittaker, & Brown, 2010): dichotomy, many biogeographers have assumed that periodic dry namely, the role of vicariance versus dispersal in the shaping of dis- land connections (land bridges), driven by climate oscillations and junct distribution patterns. (Brown, 2016; de Queiroz, 2005, 2014; fluctuating sea levels, may provide the most plausible route for ter- Morrone, 2009). restrial vertebrates to colonize across ocean barriers (Brown & Dies- The East Asian Island Arc, comprising Japan, the Ryukyu archipe- mos, 2009; Brown et al., 2013). Several studies in the late 20th lago, Taiwan, and their surrounding islets, provides an ideal setting century have suggested the existence of a land connection among to study diversification of terrestrial organisms. The central region of the East Asian Island Arc during glaciations, which may have resulted this island arc is the Ryukyu archipelago, which extends more than in continuous distributions for terrestrial species (Kimura, 2000; Ota, 1,000 km and forms a long chain of highly isolated landmasses ori- 1999, 2000). Under a purely vicariant scenario, gradual separation of ented in a north-east to south-west direction between Japan and continuous landmasses could have resulted in a series of sequential Taiwan (Figure 1). The region was left relatively unexplored until the diversification events. Under such a scenario, the topology of last decade of the 20th century, when biogeographers became inferred phylogenetic/phylogeographic relationships should be influ- attracted to the Ryuku’s high levels of faunal endemism, long-term enced by the sequence of landmass separation and depths of inter- isolation, and relatively low estimates of the diversity of terrestrial vening straits. As such, if Okinawa tree lizard lineages underwent fauna (Ota, 1999, 2000). More than two-thirds (68.4%) of native ter- population divergence in response to pure vicariance, then we might restrial reptiles are endemic to the archipelago (Ota, 2000), with the predict that populations occurring on remote north-eastern islands majority of species restricted to a single island or a small group of (e.g., Amami or Okinawa islands, separated from Southern Ryukyu by islets. Moreover, deep divergences between insular endemic species the deepest oceanic channels, the Kerama Straight; Figure 1) would and their continental relatives provide valuable opportunities to test be the first-diverging group(s) inferred in phylogeographic analyses. phylogeny-based biogeographical hypotheses and infer the mecha- As a corollary, we would expect these first-diverging lineages to pos- nism of speciation in codistributed lineages (Honda, Okamoto, sess higher standing genetic variation (relative to recently isolated Hikida, & Ota, 2008; Lin, Chen, & Lue, 2002; Matsui et al., 2005; demes) as a consequence of their longer period of isolation. This Ota et al., 2002; Toda, Hikida, & Ota, 2001). However, only a hand- pattern has been shown in lizards (Lin et al., 2002), frogs (Tominaga, ful of terrestrial vertebrates possess wide distributional ranges Matsui, Eto, & Ota, 2015), and spiders (Su, Brown, Chang, Lin, & throughout the archipelago. As a result, phylogeographic and Tso, 2016; Xu et al., 2016).