Conservation Genetics

, Volume 19, Issue 2, pp 255–263 | Cite as

Highly diversified population structure of the spider Lycosa ishikariana inhabiting sandy beach habitats

  • Akio Tanikawa
  • Akira Shinkai
  • Haruki Tatsuta
  • Tadashi Miyashita
Research Article

Abstract

Sandy beach ecosystems are decreasing worldwide and organisms living there are becoming threatened. The burrowing wolf spider Lycosa ishikariana is one such example. To establish effective conservation strategies under habitat fragmentation, we examined population genetic structure of L. ishikariana from mitochondrial cytochrome oxidase I gene and 6 microsatellite loci. Mitochondrial sequence data revealed 6 population subgroups with very high fixation indices, indicating that L. ishikariana has a clear phylogeographic structure and that the level of differentiation among regions is considerable. In particular, one subgroup in the western Honshu mainland (clade G) has a highly distinct genetic structure, despite having no clear geographic barriers from its parapatric population. Moreover, the distribution ranges of the other two subgroups (clades D and E) were highly restricted, suggesting their vulnerability to local human impacts and highlighting their high conservation priorities. Microsatellite data revealed 10 subgroups that were compatible with the clades identified from the mitochondrial data. Fixation indices among these groups were very high, indicating a limited gene flow induced by male spiders. Based on these results, we proposed six conservation units of L. ishikariana and effective conservation/restoration strategies in the face of ongoing coastal armoring.

Keywords

Conservation Endangered Mitochondria Microsatellite 

Notes

Acknowledgements

We wish to thank Nobuo Tsurusaki for his offering specimens and references for this study. Our sincere thanks are also due to Mayumi Matsuda, Naotake Inoue, Akihiko Yawata and Yuki G. Baba for useful information. This work was supported by Grants-in-Aid for Scientific Research (22924019, 15H04325 & 15H00453).

Supplementary material

10592_2017_996_MOESM1_ESM.docx (33 kb)
Supplementary material 1 (DOCX 32 KB)
10592_2017_996_MOESM2_ESM.jpg (436 kb)
The result of hierarchical STRUCTURE analysis of 6 microsatellite loci from Lycosa ishikariana. 1 to 43 represent the sampling sites, as in Fig. 1 and Table 1. Supplementary material 2 (JPEG 436 kb)

References

  1. Allendorf FW, Luikart GH, Aitken SN (2012) Conservation and the Genetics of Populations, 2nd edn. John Wiley, West SussexGoogle Scholar
  2. Association of Wildlife Research and EnVision conservation office (2007). Search system of, red data of Japan. http://www.jpnrdb.com/aboutsite.html. Accessed 20 February 2017
  3. Avise JC (2000) Phylogeography: The history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  4. Bascom W (1980) Waves and beaches: the dynamics of the ocean surface (revised). Anchor Press/Doubleday, New YorkGoogle Scholar
  5. Blacket M J, Robin C, Good R T, Lee S F, Miller A D (2012) Universal primers for fluorescent labelling of PCR fragments—an efficient and cost-effective approach to genotyping by fluorescence. Mol Ecol Resour 12:456–463CrossRefPubMedGoogle Scholar
  6. Bond JE, Hedin MC, Raminez MG, Opell BD (2001) Deep molecular divergence in the absence of morphological and ecological change in the Californian coastal dune endemic trapdoor spider Aptosticus simus. Mol Ecol 10:899–910CrossRefPubMedGoogle Scholar
  7. Bonte D, Vandenbroecke N, Lens L, Maelfait J-P (2003) Low propensity for aerial dispersal in specialist spiders from fragmented landscapes. Proc R Soc London B 270:1601–1607.CrossRefGoogle Scholar
  8. Carpaneto GM, Fattorini S (2001) Spatial and seasonal organisation of a darkling beetle (Coleoptera, Tenebrionidae) community inhabiting a Mediterranean coastal dune system. Ital J Zool 68:207–214CrossRefGoogle Scholar
  9. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660CrossRefPubMedGoogle Scholar
  10. Defeo O, McLachlan A, Schoeman DS, Schlacher TA, Dugan J, Jones A, Lastra M, Scapini F (2009) Threats to sandy beach ecosystems: a review. Estuar Coast Shelf Sci 81:1–12CrossRefGoogle Scholar
  11. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581CrossRefPubMedGoogle Scholar
  12. Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361Google Scholar
  13. Edgaer RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefGoogle Scholar
  14. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  15. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  16. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinfo Online 1:47–50Google Scholar
  17. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299Google Scholar
  18. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925Google Scholar
  19. Geospatial Information Authority of Japan (2011) Reports on ground subsidence. http://www.gsi.go.jp/common/000060316.pdf Accessed 20 February 2017
  20. Goudet J (2005) FSTAT: a computer package for PCs to estimates and tests gene diversities and differentiation statistics. http://www2.unil.ch/popgen/softwares/fstat.htm Accessed 15 January 2017
  21. Grootjans AP, Everts H, Bruin K, Fresco L (2001) Restoration of wet dune slacks on the Dutch Wadden Sea Islands: recolonization after large-scale sod cutting. Restor Ecol 9:137–146CrossRefGoogle Scholar
  22. Harris L, Campbell EE, Nel R, Schoeman D (2014) Rich diversity, strong endemism, but poor protection: addressing the neglect of sandy beach ecosystems in coastal conservation planning. Divers Distrib 20:1120–1135Google Scholar
  23. Inoue N, (1991) Records of Lycosa ishikariana in Pacific Coast. Nihon no Seibutu 5:75Google Scholar
  24. Kawamoto Y, Shotake T, Nozawa K, Kawamoto S, Tomari K, Kawai S, Shirai K, Morimitsu Y, Tak- agi N, Akaza H, Fujii H, Hagihara K, Aizawa K, Akachi S, T. Oi and S. Hayaishi(2007)Postglacial pop- ulation expansion of Japanese macaques (Macaca fuscata) inferred from mitochondrial DNA phyloge-ography. Primates 48:27–40Google Scholar
  25. Ketmaiera V, De Matthaeisb E, Faninic L, Rossanoc C, Scapinic F (2010) Variation of genetic and behavioural traits in the sandhopper Talitrus saltator (Crustacea: Amphipoda) along a dynamic sand beach. Ethol Ecol Evol 22:17–35CrossRefGoogle Scholar
  26. Kobashi S, Fujii N, Nojima A, Hori N (2006) Distribution of chloroplast DNA haplotypes in the contact zone of Fagus crenata in the southwest of Kanto District, Japan. J Plant Res 119:265–269CrossRefPubMedGoogle Scholar
  27. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefPubMedGoogle Scholar
  28. Loveless MD, Hamrick JL (1988) Genetic organization and evolutionary history in two North American species of Cirsium. Evol Int J org Evol 42:225–233CrossRefGoogle Scholar
  29. Malavasi M, Santoro R, Cutini M, Acosta ATR, Carranza ML (2013) What has happened to coastal dunes in the last half century? A multitemporal coastal landscape analysis in Central Italy. Landscape Urban Plan 119:54–63Google Scholar
  30. Maun MA (1994) Adaptations enhancing survival and establishment of seedings on coastal dune systems. Vegetatio 111:59–70Google Scholar
  31. McLachlan A, Brown A (2006) Sandy Beaches as Ecosystems. Elsevier Science Publishers, AmsterdamGoogle Scholar
  32. Meglécz E, Pech N, Gilles A, Dubut V, Hingamp P, Trilles A. Grenier R, Martin J-F (2014) QDD version 3.1: a user-friendly computer program for microsatellite selection and primer design revisited: experimental validation of variables determining genotyping success rate. Mol Ecol Resour 14:1302–1313CrossRefPubMedGoogle Scholar
  33. Michonneau F (2016) Using GMYC for species delineation. https://francoismichonneau.net/gmyc-tutorial/ Accessed 10 May 2017
  34. Minato M (1973) Atras: background of the Japanese Archipelago. Tsukiji-shokan Publishing, TokyoGoogle Scholar
  35. Ministry of the Environment (1980) Report of 2nd natural environment survey. https://www.biodic.go.jp/reports/2-08/2-08-02.pdf Accessed 20 February 2017
  36. Ministry of the Environment (1998) Report of 5th natural environment survey. https://www.biodic.go.jp/reports/umibe/umibedata1.pdf Accessed 20 February 2017
  37. Ministry of Land, Infrastructure, Transport and Tourism (2014) Coastal staticus. Ministry of Land, Infrastructure, Transport and Tourism, TokyoGoogle Scholar
  38. Ministry of Land, Infrastructure, Transport and Tourism (2016) Reconstruction plan for the Great East Japan Earthquake. http://www.mlit.go.jp/river/kaigan/main/fukkyufukko/index.html Accessed 20 February 2017
  39. Nagata J, Masuda R, Tamate HB, Hamasaki S, Ochiai K, Asada M, Tastuzawa S, Suda K, Tado H, Yoshida MC (1999) Two genetically distinct lineages of the sika deer, Cervus nippon, in Japanese islands: comparison of mitochondrial D-loop region sequences. Mol Phylogenet Evol 13:511–519CrossRefPubMedGoogle Scholar
  40. Nikula R, Fraser CI, Spencer HG, Waters JM (2010) Circumpolar dispersal by rafting in two subantarctic kelp-dwelling crustaceans. Mar Ecol Prog Series 405:221–230Google Scholar
  41. Nikula R, Spencer HG, Waters JM (2011) Comparison of population-genetic structuring in congeneric kelp- versus rock-associated snails: a test of a dispersal-by-rafting hypothesis. Ecol Evolution 1:169–180Google Scholar
  42. Nishikawa Y (2006) Lycosa ishikariana (S. Saito, 1934). In: Threatened Wildlife of Japan - Red Data Book 2nd ed. - Volume 7, Invertebrata (except Insecta and Mollusca) Ed by Ministry of the Environment, Japan. Japan Wildlife Research Center, TokyoGoogle Scholar
  43. Nguyen X D, Tanaka H, Adityawan M B, Udo K, Mano A (2013) Morphology changes on Ishinomaki coast due to the Great East Japan Tsunami. Jpn Soc Civil Eng 69:281–285Google Scholar
  44. Olff H, Huisman J, Van Tooren BF (1993) Species dynamics and nutrient accumulation during early primary succession in coastal sand dunes. J Ecol 81:693–706CrossRefGoogle Scholar
  45. Petracco M, Cardoso R S, Corbisier T N (2010) Population biology of Excirolana armata (Dana, 1853) (Isopoda, Cirolanidae) on an exposed sandy beach in Southeastern Brazil. Mar Ecol 31:330–340CrossRefGoogle Scholar
  46. Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55:595–609CrossRefPubMedGoogle Scholar
  47. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  48. Raminez MG, Froehlig JL (1997) Minimal genetic variation in a coastal dune arthropod: the trapdoor spider Aptostichus simus (Cytaucheniidae). Conserv Biol 11:256–259CrossRefGoogle Scholar
  49. Reaka ML, Rodgers PJ, Kudla AU (2008) Patterns of biodiversity and endemism on Indo-West Pacific coral reefs. P Natl Acad Sci 105:11474–11481Google Scholar
  50. Saito S (1934) Spiders from Hokkaido. J Fac Agric Hokkaido Univ 33:267–362Google Scholar
  51. Sato T, Tsurusaki N (2010) Preliminary report of insect fauna occurring in the Tottori Sand Dunes. Bull Tottori Pref Mus 47:45–81Google Scholar
  52. Satoh A, Sota T, Uéda T, Enokido Y, Paik JC, Hori M (2004) Evolutionary history of coastal tiger beetles in Japan based on a comparative phylogeography of four species. Mol Ecol 13:3057–3069CrossRefPubMedGoogle Scholar
  53. Schlacher TA, Dugan J, Schoeman DS, Lastra M, Jones A, Scapini F, McLachlan A, Defeo O (2007) Sandy beaches at the brink. Diver Distrib 13:556–560CrossRefGoogle Scholar
  54. Speybroeck J, Bonte D, Courtens W, Gheskiere T, Grootaert P, Maelfait J-P, Provoost S, Sabbe K, Stienen E W M, Van Lancker V, Van Landuyt W, Vincx M, Degraer S. (2008) The Belgian sandy beach ecosystem: a review. Mar Ecol 29:171–185CrossRefGoogle Scholar
  55. Suzuki S, Tsurusaki N, Kodama Y (2006) Distribution of an endangered burrowing spider Lycosa ishikariana in the San’in Coast of Honshu, Japan (Araneae: Lycosidae). Acta Arachnol 55:79–86CrossRefGoogle Scholar
  56. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595Google Scholar
  57. Tanaka, H. (2009). Lycosidae. In: Ono, H. (ed.) The Spiders of Japan with keys to the families and genera and illustrations of the species. Tokai University Press, KanagawaGoogle Scholar
  58. Uda T (2010) Japan’s Beach Erosion—reality and future measures. World Scientific, SingaporeCrossRefGoogle Scholar
  59. van der Meulen F, Udo de Haes FA (1996) Nature conservation and integrated coastal zone management in Europe: present and future. Landsc Urban Plan 34:401–410Google Scholar
  60. Yasumoto Y, Uda T, Matsubara Y, Hirano G (2007) Beach Erosion along Tottori Coast and Comprehensive Sediment Management. J Coast Res Sp Iss 50:82–87Google Scholar
  61. Yura H, Ogura A (2006) Sandblasting as a possible factor controlling the distribution of plants on a coastal dune system. Plant Ecol 185:199–208CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.Laboratory of Biodiversity Science, School of Agriculture and Life SciencesThe University of TokyoTokyoJapan
  2. 2.TokyoJapan
  3. 3.Department of Ecology and Environmental Sciences, Faculty of AgricultureUniversity of the RyukyusOkinawaJapan

Personalised recommendations