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Marine Ecology Progress Series 529:159 Vol. 529: 159–169, 2015 MARINE ECOLOGY PROGRESS SERIES Published June 8 doi: 10.3354/meps11267 Mar Ecol Prog Ser FREEREE ACCESSCCESS Genetic population structure of four hydrothermal vent shrimp species (Alvinocarididae) in the Okinawa Trough, Northwest Pacific Takuya Yahagi1,2,*, Hiromi Watanabe3, Jun-ichiro Ishibashi4, Shigeaki Kojima1,2 1Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan 2Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8561, Japan 3Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061, Japan 4Department of Earth and Planetary Sciences, Faculty of Sciences, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka 812-8581, Japan ABSTRACT: Understanding the formative factors of connectivity among deep-sea chemosynthetic communities may clarify the biogeographic mechanisms that facilitate the establishment and development of vent/seep fauna. This study identified interspecific differences in the geographi- cal distribution and genetic population structure of 4 alvinocaridid shrimp species inhabiting hydrothermal vents in the Okinawa Trough, Northwest Pacific. Shinkaicaris leurokolos popula- tions were widely distributed at 580 to 1651 m depth, with partial nucleotide sequences of the mitochondrial COI gene revealing extremely high genetic diversity (haplotype diversity: 0.98 to 1.00). In contrast, local populations of Alvinocaris dissimilis and A. longirostris, both of which have narrower bathymetric distributions, were characterised by low haplotype diversity (0.29 to 0.52). In the Okinawa Trough, Alvinocaris sp. only occurs at the Irabu Knoll, but this species also inhab- its the Suiyo Seamount on the volcanic front of the Izu-Bonin Arc (Northwest Pacific). This unde- scribed species had relatively high haplotype diversity (0.70 to 0.82), with no genetic differentia- tion between the 2 sites. Certain factors may allow this species to occur at both sites (e.g. a chemical environment derived from similar substratum), despite geological differences in hydrothermal circulation (i.e. a back-arc basin versus an arc volcanic front, respectively). The findings of this study indicate that (1) the wide geographical and bathymetrical distributional ranges of the vent shrimp species cause high genetic diversity associated with stable population connectivity and (2) certain environmental features (e.g. depth and substratum) and life-history traits (e.g. feeding habitat and larval characteristics) represent important formative factors in the connectivity of alvinocaridids in the Northwest Pacific. KEY WORDS: Alvinocaridid shrimp · Biogeography · Connectivity · Genetic diversity Resale or republication not permitted without written consent of the publisher INTRODUCTION that are supported by the primary production of chemoautotrophic bacteria (Corliss et al. 1979). Ani- Since the discovery of the first hydrothermal vent in mals endemic to vent systems are expected to have a 1977, many vents associated with chemosynthetic high dispersal ability to maintain gene flow among lo- communities have been documented (e.g. Connelly et cal populations (Tyler & Young 2003), as their habitats, al. 2012). In deep-sea reducing environments within which were formed by volcanic activities along mid- hydrothermal vent fields, faunal communities mainly ocean ridge systems, in back-arc basins, and on off- consist of endemic species (Tunnicliffe & Fowler 1996) axis submarine volcanoes, are unstable and patchi ly *Corresponding author: [email protected] © Inter-Research 2015 · www.int-res.com 160 Mar Ecol Prog Ser 529: 159–169, 2015 distributed (Holm & Hennet 1992, Van Dover 2000). A. longirostris, and Shinkaicaris leurokolos (Komai & Consequently, dispersal and connectivity among vent Segonzac 2005, Watanabe & Kojima 2015). A. brevi- sites have a significant role in both the population dy- telsonis and A. dissimilis were only collected from namics and evolution of species endemic to hydrother- the Minami-Ensei Knoll (Komai & Segonzac 2005). A. mal vent ecosystems. Understanding the formative brevitelsonis was described based on a single speci- factors of connectivity among deep-sea chemosyn- men collected from this site (Komai & Segonzac thetic communities may clarify the biogeographic 2005), and has not been subsequently recorded. A. mechanisms that lead to the establishment and devel- longirostris occurs in the vent fields of the North opment of endemic fauna. However, research on the Knoll of the Iheya Ridge, Izena Hole, Hatoma Knoll, connectivity of vent-endemic species remains limited and Dai-yon (No. 4) Yonaguni Knoll, in addition to a in the West Pacific (Vrijenhoek 2010), despite the evo- cold seep area off Hatsushima in Sagami Bay (Fu- lutionary importance of this region (Moalic et al. 2012). jikura et al. 1995, 2008, Kikuchi & Ohta 1995, Watabe Comparative analyses of the vent fauna from this re- & Miyake 2000, Ohta & Kim 2001, Komai & Segonzac gion with other oceanic regions may provide important 2005). Moreover, this species has been reported to be information about the biogeographic history of deep- present at the Brothers Caldera in New Zealand and sea chemosynthetic communities. the Jiaolong Cold Seep I in northeastern South China The caridean family Alvinocarididae is comprised (Webber 2004, Li 2015). This species might have a of 28 described species belonging to 8 genera, which bathymetrically restricted distribution, as it has not are known from chemosynthetic environments be - been reported at vent sites shallower than 700 m tween depths of 252 and 4960 m in the world’s oceans depth, even when geographically close to deeper (Nye et al. 2012, Yahagi et al. 2014). Molecular evi- habitats (Komai & Segonzac 2005). S. leurokolos is dence indicates that they were established during widespread, and is one of the representative species the late Cretaceous/Early Tertiary (Yang et al. 2013). of the Okinawa Trough (Watanabe & Kojima 2015). In the Northwest Pacific, alvinocaridids have been In the latest review on the distribution of alvinocari- reported in the hydrothermal vent fields of the Oki- did shrimp, 2 distributional range patterns were ad- nawa Trough, the Izu-Bonin Arc, and the Mariana vocated; namely, local (single vent field) and regional Arc, as well as in cold seep areas in Sagami Bay and (>3 to 6 vent fields). The distributional ranges of most the South China Sea (Komai & Segonzac 2005, Pacific species were classified as the local type, Fujikura et al. 2008, Li 2015). whereas those of the Atlantic species were classified The Okinawa Trough is a back-arc basin located as the regional type (Lunina & Vereshchaka 2014). behind the Ryukyu trench-arc system, where the However, the alvino caridids of the Okinawa Trough Philippine Sea Plate subducts beneath the Eurasian seem to exhibit both local and regional distributional plate. The recent magmatism related to the rifting patterns. Thus, the factors that determine the geo- stage of the Okinawa Trough is considered to have graphical distribution and population connectivity of begun ~2 million years ago (Kimura 1996). At least 8 alvinocaridids require identification. hydrothermal vent fields associated with chemosyn- The present study aimed to reveal the distributional thetic communities have been discovered in the Oki- ranges and genetic population structure of 4 alvino- nawa Trough (Fujikura et al. 2008, Watanabe et al. caridid species inhabiting the Okinawa Trough to un- 2010). These communities are distributed from ap- derstand connectivity and its formative factors. This proximately 600 to 1600 m depth in the central and study is the first to investigate population genetics of southern parts of the trough, which extend about 800 vent shrimps in the Northwest Pacific, facilitating km in length (Fujikura et al. 2008, Watanabe et al. comparison with the observed patterns on the Mid- 2010). Two vent sites, the Yoron Hole (Fukuba et al. Atlantic Ridge (MAR; Teixeira et al. 2011, 2012), Cen- 2015a) and the Irabu Knoll of the Yaeyama Central tral Indian Ridge (CIR; Beedessee et al. 2013), and in Graben (Fukuba et al. 2015b), were recently discov- the southwestern Pacific (SWP; Thaler et al. 2014). ered, and little information is available about the fauna at these sites. Alvinocaridid shrimps are dominant megafaunal MATERIALS AND METHODS invertebrates in vent fields in the Okinawa Trough, in addition to the galatheid crab Shinkaia crosnieri Sampling and Bathymodiolus mussels (Watanabe et al. 2010). To date, 4 alvinocaridid species have been reported Specimens were collected from 5 hydrothermal in this area: Alvinocaris brevitelsonis, A. dissimilis, vent fields in the Okinawa Trough; namely, the Yahagi et al.: Genetic structure of hydrothermal vent shrimps 161 taining part of the mitochondrial COI gene (658 bp) was amplified by polymerase chain reaction (PCR) using the LCO1490/HCO2198 universal primer set (Folmer et al. 1994). Amplification was performed in 20 µl reaction mixture containing approximately 5 ng genomic DNA, 2 µl 10× Ex Taq buffer, 0.3 µM dNTP mix, 20 µM of each primer, and 0.05 U of EX Taq DNA polymerase (TaKaRa Bio Inc.). PCR reac- tions were carried out with an initial denaturation step at 94°C (40 s), followed by 35 cycles consisting of a denaturation step at 94°C (40 s), an annealing step at 50°C (60 s), and an extension step at 72°C (90 s). The products were purified using Exo-SAP-IT
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