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Isolation and characterization of novel polymorphic microsatellite loci for the deep-sea hydrothermal vent limpet, Lepetodrilus nux, and the vent-associated squat lobster, Shinkaia crosnieri

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Abstract

Recent genetic research has begun to reveal population structures of deep-sea, hydrothermal vent species, but detailed assessments of genetic diversity and connectivity in hydrothermal vent populations, based on multiple genetic loci, are still scarce, especially in the Northwest Pacific. Accordingly, we isolated 38 novel polymorphic microsatellite loci from the limpet, Lepetodrilus nux, and 14 from the squat lobster, Shinkaia crosnieri, two dominant hydrothermal vent species, using next-generation sequencing. These loci revealed polymorphism levels of 5–20 alleles per locus in L. nux and 5–25 in S. crosnieri. Observed and expected heterozygosities ranged from 0.240 to 0.960 and 0.283 to 0.938 in L. nux and from 0.450 to 0.950 and 0.620 to 0.941 in S. crosnieri, respectively. Twelve loci in L. nux and four loci in S. crosnieri showed significant deviation from Hardy–Weinberg equilibrium (p < 0.05). Microsatellite loci evaluated in this study will enable detailed measurements of genetic diversity and connectivity among populations, and better understanding of evolutionary divergence processes of L. nux and S. crosnieri in deep-sea communities in the Northwest Pacific.

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References

  • Adams DK, Arellano SM, Govenar B (2012) Larval dispersal: vent life in the water column. Oceanography 25:256–268

    Article  Google Scholar 

  • Aronesty E (2011) ea-utils: "Command-line tools for processing biological sequencing data". http://code.google.com/p/ea-utils

  • Baba K, Williams AB (1998) New Galatheoidea (Crustacea, Decapoda, Anomura) from hydrothermal systems in the West Pacific Ocean: Bismarck Archipelago and Okinawa Trough. Zoosystema 20:143–156

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

  • Breusing C, Biastoch A, Drews A, Metaxas A, Jollivet D, Vrijenhoek RC, Bayer T, Melzner F, Sayavedra L, Petersen JM, Dubilier N, Schilhabel MB, Rosenstiel P, Reusch TBH (2016) Biophysical and population genetic models predict the presence of “phantom” stepping stones connecting mid-Atlantic ridge vent ecosystems. Curr Biol 26:2257–2267

  • Castoe TA, Poole AW, de Koning APJ, Jones KL, Tomback DF, Oyler-McCance SJ, Fike JA, Lance SL, Streicher JW, Smith EN, Pollock DD (2012) Rapid microsatellite identification from Illumina paired-end genomic sequencing in two birds and a snake. PLoS ONE 7:e30953

  • Chan T-Y, Lee D-A, Lee C-S (2000) The first deep-sea hydrothermal animal reported from Taiwan: Shinkaia crosnieri Baba and Williams, 1998 (Crustacea: Decapoda: Galatheidae). Bull Mar Sci 67:799–804

  • Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12:499–510

    Article  PubMed  CAS  Google Scholar 

  • Desbruyères D, Segonzac M, Bright M (2006) Handbook of deep-sea hydrothermal vent fauna. Denisia 18, Linz, Austria

  • Johnson SB, Young CR, Jones WJ, Warén A, Vrijenhoek RC (2006) Migration, isolation, and speciation of hydrothermal vent limpets (Gastropoda; Lepetodrilidae) across the Blanco Transform Fault. Biol Bull 210:140–157

  • Johnson SB, Warén A, Vrijenhoek RC (2008) DNA barcoding of Lepetodrilus limpets reveals cryptic species. J Shellfish Res 27:43–51

  • Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659

    Article  PubMed  CAS  Google Scholar 

  • Lutz RA, Jablonski D, Turner RD (1984) Larval development and dispersal at deep-sea hydrothermal vents. Science 226:1451–1454

    Article  PubMed  CAS  Google Scholar 

  • Matabos M, Thiébaut E, Le Guen D, Sadosky F, Jollivet D, Bonhomme F (2008) Geographic clines and stepping-stone patterns detected along the East Pacific Rise in the vetigastropod Lepetodrilus elevatus reflect species crypticism. Mar Biol 153:545–563

  • Mitarai S, Watanabe H, Nakajima Y, Shchepetkin AF, McWilliams JC (2016) Quantifying dispersal from hydrothermal vent fields in the western Pacific Ocean. Proc Nat Acad Sci USA 113:2976–2981

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Miyake H, Kitada M, Itoh T, Nemoto S, Okuyama Y, Watanabe H, Tsuchida S, Inoue K, Kado R, Ikeda S, Nakamura K, Omata T (2010) Larvae of deep-sea chemosynthetic ecosystem animals in captivity. Cah Biol Mar 51:441–451

    Google Scholar 

  • Nakajima R, Yamamoto H, Kawagucci S, Takaya Y, Nozaki T, Chen C, Fujikura K, Miwa T, Takai K (2015) Post-drilling changes in seabed landscape and megabenthos in a deep-sea hydrothermal system, the Iheya North field, Okinawa Trough. PLoS ONE 10:e0123095

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nakamura M, Watanabe H, Sasaki T, Ishibashi J, Fujikura K, Mitarai S (2014) Life history traits of Lepetodrilus nux in the Okinawa Trough, based upon gametogenesis, shell size, and genetic variability. Mar Ecol Prog Ser 505:119–130

    Article  Google Scholar 

  • Okutani T, Fujikura K, Sasaki T (1993) New taxa and new distribution records of deepsea gastropods collected from or near the chemosynthetic communities in the Japanese waters. Bull Natl Sci Mus Tokyo A 19:123–143

    Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Plouviez S, Shank TM, Faure B, Daguin-Thiebaut C, Viard F, Lallier FH, Jollivet D (2009) Comparative phylogeography among hydrothermal vent species along the East Pacific Rise reveals vicariant processes and population expansion in the south. Mol Ecol 18:3903–3917

  • Raymond M, Rousset F (1995) Genepop (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Article  Google Scholar 

  • Roterman CN, Copley JT, Linse KT, Tyler PA, Rogers AD (2013) Development of polymorphic microsatellite loci for three species of vent-endemic megafauna from deep-sea hydrothermal vents in the Scotia Sea, Southern Ocean. Conserv Genet Resour 5:835–839

    Article  Google Scholar 

  • Roterman CN, Copley JT, Linse KT, Tyler PA, Rogers AD (2016) Connectivity in the cold: the comparative population genetics of vent-endemic fauna in the Scotia Sea, Southern Ocean. Mol Ecol 25:1073–1088

    Article  PubMed  CAS  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

  • Sasaki T, Okutani T, Fujikura K (2003) New taxa and new records of patelliform gastropods associated with chemoautosynthesis-based communities in Japanese waters. Veliger 46:189–210

    Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    Article  PubMed  CAS  Google Scholar 

  • Thaler AD, Zelnio K, Saleu W, Schultz TF, Carlsson J, Cunningham C, Vrijenhoek RC, Van Dover CL (2011) The spatial scale of genetic subdivision in populations of Ifremeria nautilei, a hydrothermal-vent gastropod from the southwest Pacific. BMC Evol Biol 11:372

    Article  PubMed  PubMed Central  Google Scholar 

  • Thaler AD, Plouviez S, Saleu W, Alei F, Jacobson A, Boyle EA, Schultz TF, Carlsson J, Van Dover CL (2014) Comparative population structure of two deep-sea hydrothermal-vent-associated decapods (Chorocaris sp. 2 and Munidopsis Lauensis) from southwestern Pacific back-arc basins. PLoS ONE 9:e101345

  • Van Dover CL, German CR, Speer KG, Parson LM, Vrijenhoek RC (2002) Evolution and biogeography of deep-sea vent and seep invertebrates. Science 295:1253–1257

    Article  PubMed  CAS  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  CAS  Google Scholar 

  • Vrijenhoek RC (1997) Gene flow and genetic diversity in naturally fragmented metapopulations of deep-sea hydrothermal vent animals. J Hered 88:285–293

    Article  PubMed  CAS  Google Scholar 

  • Vrijenhoek RC, Feldman RA, Lutz RA, Craddock C, Hashimoto J (1997) Genetic characterization of Lepetodrilus limpets from hydrothermal vents in the Mariana Trough. JAMSTEC Journal of Deep Sea Research, Special Volume “Deep sea research in subduction zones, spreading centers and backarc basins”, pp 111–116

  • Vrijenhoek RC (2010) Genetic diversity and connectivity of deep-sea hydrothermal vent metapopulations. Mol Ecol 19:4391–4411

    Article  PubMed  Google Scholar 

  • Xu T, Sun J, Lv J, Watanabe HK, Li T, Zou W, Rouse GW, Wang S, Qian P-Y, Bao Z, Qiu J-W (2017) Genome-wide discovery of single nucleotide polymorphisms (SNPs) and single nucleotide variants (SNVs) in deep-sea mussels: Potential use in population genomics and cross-species application. Deep Sea Res II 137:318–326

  • Yang C-H, Tsuchida S, Fujikura K, Fujiwara Y, Kawato M, Chan T-Y (2016) Connectivity of the squat lobsters Shinkaia crosnieri (Crustacea: Decapoda: Galatheidae) between cold seep and hydrothermal vent habitats. Bull Mar Sci 92:17–31

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. Hiroyuki Yamamoto, chief scientist of the KR12-02 and NT13-22 cruises, and to officers and crews of the ‘Natsushima,’ and the operation team of ROV ‘Hyper-Dolphin’ for collecting the specimens. This work was financially supported by The Canon Foundation and Okinawa Institute of Science and Technology Graduate University. We thank Dr. Steven D. Aird (Okinawa Institute of Science and Technology Graduate University) for editing the manuscript.

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Authors and Affiliations

  1. Marine Biophysics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa, 904-0495, Japan

    Yuichi Nakajima & Satoshi Mitarai

  2. Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, 277-8564, Japan

    Chuya Shinzato

  3. Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa, 904-0495, Japan

    Mariia Khalturina & Noriyuki Satoh

  4. School of Marine Science and Technology, Tokai University, Shimizu, Shizuoka, 424-8610, Japan

    Masako Nakamura

  5. Japan Agency for Marine-Earth Science and Technology, Yokosuka, Kanagawa, 237-0061, Japan

    Hiromi Kayama Watanabe

  6. Division of Applied Biosciences, Graduate School of Agriculture, Kyoto University, Kitashirakawa, Kyoto, 606-8502, Japan

    Satoshi Nakagawa

Authors
  1. Yuichi Nakajima
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  2. Chuya Shinzato
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  3. Mariia Khalturina
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  4. Masako Nakamura
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  5. Hiromi Kayama Watanabe
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  6. Satoshi Nakagawa
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  7. Noriyuki Satoh
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  8. Satoshi Mitarai
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Correspondence to Yuichi Nakajima.

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Communicated by S. Gollner

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Nakajima, Y., Shinzato, C., Khalturina, M. et al. Isolation and characterization of novel polymorphic microsatellite loci for the deep-sea hydrothermal vent limpet, Lepetodrilus nux, and the vent-associated squat lobster, Shinkaia crosnieri . Mar Biodiv 48, 677–684 (2018). https://doi.org/10.1007/s12526-017-0704-5

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  • DOI: https://doi.org/10.1007/s12526-017-0704-5

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