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<I>Shinkaia Crosnieri</I>

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<I>Shinkaia Crosnieri</I> Bull Mar Sci. 92(1):17–31. 2016 research paper http://dx.doi.org/10.5343/bms.2015.1031 Connectivity of the squat lobsters Shinkaia crosnieri (Crustacea: Decapoda: Galatheidae) between cold seep and hydrothermal vent habitats 1 Institute of Marine Biology, Chien-Hui Yang 1 National Taiwan Ocean Shinji Tsuchida 2 University, 2 Pei-Ning Road, 2 Keelung 20224, Taiwan, ROC. Katsunori Fujikura 2 2 Japan Agency of Marine-Earth Yoshihiro Fujiwara Science and Technology, 2-15 Masaru Kawato 2 Natsushima-cho, Yokosuka, 3 * Kanagawa, 237-0061, Japan. Tin-Yam Chan 3 Institute of Marine Biology and Center of Excellence for the Oceans, National Taiwan Ocean ABSTRACT.—The deep-sea squat lobster, Shinkaia University, 2 Pei-Ning Road, crosnieri Baba and Williams, 1988, previously only observed Keelung 20224, Taiwan, ROC. in hydrothermal vents, was recently found in a cold-seep site * Corresponding author email: off the coast of southwestern Taiwan in the South China <[email protected]>. Sea. Although no morphological difference was detected, molecular genetic analysis of the mitochondrial cytochrome c oxidase I (COI) gene revealed that the vent and cold-seep populations form separate clades with 2.1%–3.8% sequence divergence. Nevertheless, no significant genetic distinction was detected in the nuclear adenine nucleotide translocase (ANT) intron gene. These results indicate that vent and Date Submitted: 5 May, 2015. cold seep S. crosnieri are conspecific, but represent separate Date Accepted: 22 October, 2015. Available Online: 21 December, 2015. populations. Although both deep-sea hydrothermal vents and cold seeps are chemosynthetic ecosystems, they are generally composed of different communities Sibuet( and Olu 1998, Hourdez and Lallier 2007, Govenar 2010). More than 600 animal species have been reported in deep-sea vents and cold seeps (Van Dover et al. 2002, Desbruyères et al. 2006), including at least 125 species of decapod crustaceans in 33 families (Martin and Haney 2005). However, only a few decapod crustaceans (e.g., Alvinocaris longirostris Kikuchi and Ohta, 1995, Munidopsis acutispina Benedict, 1902, Munidopsis lauensis Baba and de Saint Laurent, 1992, Munidopsis naginata Cubelio, Tsuchida and Watanabe, 2007, and Shinkaia crosnieri Baba and Williams, 1988) have been reported in both deep-sea vents and cold seeps (Desbruyères et al. 2006, Fujikura et al. 2008, Baba et al. 2009, Lin et al. 2013, Li 2015). Among them, the galatheid S. crosnieri is often found to be particularly abundant (Fig. 1), except at the Minami-Ensei Knoll (Hashimoto et al. 1995). Moreover, this species is distinct from the other squat lobsters and was once placed in a separate subfamily, Shinkaiinae (Baba and Williams 1998). Shinkaia crosnieri was previously reported only in the deep-sea hydrothermal vents in the Okinawa Trough, northeast Taiwan, and the Bismarck Archipelago (Baba and Williams 1998, Chan et al. 2000). Recently, this species has also been determined to be a dominant species at a deep-sea cold seep on Bulletin of Marine Science 17 © 2016 Rosenstiel School of Marine & Atmospheric Science of the University of Miami 18 Bulletin of Marine Science. Vol 92, No 1. 2016 Figure 1. Shinkaia crosnieri communities from (A) deep-sea hydrothermal vent and (B) cold seep. (A) is located at Okinawa Trough, Hatoma Knoll, 27°51.4’N 123°50.5’E, 1490 m, 27 April 2005; (B) is located at Formosa Ridge, South China Sea, 22°6.9’N 119°17.1’E, 1126 m, March 2007. the Formosa Ridge off the coast of southwestern Taiwan in the South China Sea Baba( et al. 2009, Li 2015; Fig. 1B). The geographic distance between the vents in the East China Sea and the cold seep in the South China Sea is not long (i.e., approximately 800 km; Fig. 2), and no noticeable morphological difference is observed between the materials in the two areas. Nevertheless, the two habitats represent distinct ecosystems (i.e., vent vs cold seep) and belong to different basins (i.e., the East and South China seas). Because hydrothermal vents and cold seeps are special chemosynthetic ecosystems with many endemic fauna, but are often geographically distant from each other, the connectivity of the various populations and the presence of cryptic species in these areas have become prominent research topic. Most of this population genetics research has examined vent animals. Some studies have found high gene flow among different populations (e.g.,Creasey et al. 1996 for the vent shrimp Rimicaris exoculata William and Rona, 1986; and Vrijenhoek 1997 for various vent animal groups), whereas some have not (e.g., Won et al. 2003 for Bathymodiolus mussels; Hurtado et al. 2004 for various annelids; and Johnson et al. 2006 for Lepetodrilus limpets). However, few population genetics studies have investigated species distributed in both hydrothermal vents and cold seeps (e.g., Kojima et al. 1995, Kyuno et al. 2009, both of which were conducted on bivalves). The present work attempted to elucidate the connectivity between northern and southern Taiwan, as well as between the vent and cold seep populations of S. crosnieri. Molecular analyses are now widely employed in population genetics studies, including those from chemosynthetic ecosystems (e.g., Craddock et al. 1995, Won et al. 2003, Hurtado et al. 2004, Smith et al. 2004, Johnson et al. 2006, Mateos et al. 2012). The present study used the mitochondrial cytochrome c oxidase (COI) and nuclear adenine nucleotide translocase (ANT) intron genes as genetic markers to investigate the connectivity between the hydrothermal vent and cold seep S. crosnieri populations. These two genetic markers have been successfully used to study the connectivity in decapod crustaceans, such as crabs and lobsters (e.g., Barber et al. 2012, Groeneveld et al. 2012, Tourinho et al. 2012, Yednock and Neigel 2014). Furthermore, principal component analysis (PCA) was used to identify any morphological differences among the cold seep and hydrothermal vent populations. The cold seep off the coast of southwestern Taiwan is now considered a potential site for deep-sea gas hydrate exploitation. More knowledge of the population characteristics of the dominant species at this site is crucial for exploitation management planning. Yang et al.: Connectivity of the squat lobster Shinkaia crosnieri 19 Figure 2. Location of sampling stations for Shinkaia crosnieri used for the molecular study. “r” cold seep; “q” hydrothermal vent; “Stn.” station; “spec.” number of specimens used; “HPD” collecting gear ROV Hyper-Dolphin of the JAMSTEC; “SONNE” collecting gear TV grabber of the RV SONNE. Photograph of S. crosnieri from the Formosa Ridge cold seep specimen labeled as “50_1_1” in Figure 4. Materials and Methods Molecular Analysis Sample Collection.—Sixty-five individual S. crosnieri samples were used in the pres- ent study, collected from the Okinawa Trough hydrothermal vents and the cold seep off the coast of southwestern Taiwan Fig.( 2). Specimens from the Okinawa Trough were from two different sites 300 km apart, with 12 samples from the Hatoma Knoll and 21 from the Izena Calderon. The Formosa Ridge cold seep site material had 32 specimens. Materials from the hydrothermal vents at the Okinawa Trough were col- lected using the remotely operated vehicle (ROV) Hyper-Dolphin (3000 m class) of the Japan Agency for Marine-Earth Science and Technology (JAMSTEC). Specimens from the cold seep off the coast of southwestern Taiwan were sampled using the Hyper-Dolphin and the TV grabber, which was deployed using the RV SONNE (Universität Bremen, Germany). The specimens were deposited at the JAMSTEC (Okinawa Trough, Izena Calderon, and Hatoma Knoll: 31 specimens; southwest Taiwan: 25 specimens) and the National Taiwan Ocean University (Okinawa Trough, Izena Calderon: 3 specimens; southwest Taiwan: 7 specimens). DNA Extraction, PCR Amplification, and Sequencing.—Genomic DNA was extracted from the chelae or abdomen muscle by using the QIAGEN® DNeasy Blood and Tissue Kit following the manufacturer’s protocol. COI and ANT genes 20 Bulletin of Marine Science. Vol 92, No 1. 2016 were amplified using the primer set from Folmer et al. (1994) (657 bp, LCO1490/ HCO2198) and Teske and Beheregaray (2009) (680 bp, DecapANT-F/DecapANT-R). PCR reactions were performed in 25 μl reactions with 50–250 ng of the DNA tem- plates, 2.5 μl of 10× polymerase buffer (TaKaRa TaqTM), 0.5 μl of 25 mM magnesium TM chloride (MgCl2, TaKaRa Taq ), 0.5 μl of 2.5 mM of deoxyribonucleotide triphos- phate (dNTPs) (TaKaRa Taq TM), 0.5 μl of 10 μM for each primer (MDBio Inc.), and 0.5 U of Taq polymerase (5 U μl−1, TaKaRa Taq TM). An additional 0.5 μL of 1% bovine serum albumin (stock concentration: 0.5 mg μl−1) was used only for the COI gene. The PCR cycling conditions were as follows: 5 min at 95 °C for initial denaturation, then 40 cycles of 30 s at 94 °C, 40 s at 48 °C (COI) or 52.5 °C (ANT), 30 s at 72 °C, and final extension for 7 min at 72 °C. After checking the size and quality of the PCR products by using 1% agarose gel electrophoresis, the remaining PCR products were transferred to the commercial biocompany for subsequent sequencing. Those PCR products were sequenced (forward and reverse) with the same PCR primer set on an ABI 3730 Genetic Analyzer (Applied Biosystems). SeqMan ProTM (LASERGENE®, DNASTAR) was used to clean and edit sequences for contig assembly. Data Analysis—A dataset of the COI sequence was translated into the correspond- ing amino acid by using EditSeq (LASERGENE®, DNASTAR) to determine whether pseudogene was included (Song et al. 2008). All COI and ANT sequences were depos- ited in GenBank (accession numbers: COI KU285501-KU285565, ANT KU285566- KU285603). MAFFT v7 (Katoh and Standley 2013) was used to align the generated sequences. The aligned data set was edited using BioEdit v7.1.3.0 Hall( 1999).
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