Conservation Genetics

, Volume 19, Issue 2, pp 275–282 | Cite as

Cryptic genetic diversity of Neverita didyma in the coast of China revealed by phylogeographic analysis: implications for management and conservation

Research Article
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Abstract

Revealing cryptic biodiversity and understanding the processes that promote lineage diversification will provide valuable insights into management and protection of exploitable species. Neverita didyma is one of the most common marine species along the coast of China and possesses highly economic and nutritional value. Despite being heavily harvested each year, the genetic diversity of this species has never been assessed in the coastal areas of China. Here, we analyzed the diversity of this species based on the barcode region of the mitochondrial gene Cytochrome Oxidase subunit I (COI) and utilized different species delineation approaches to infer evolutionarily significant units (ESUs). Three distinct ESUs, with high genetic distance among each, were identified. Divergence time estimates suggested that the high genetic distances were probably associated with historical isolation of the marginal seas during Pleistocene low sea level periods. The three ESUs did not map to distinct geographical distribution, possibly attributing to the repeated isolation in different refugia and random postglacial recolonization. Moreover, N. didyma in Haizhou Bay deserves priority protection due to its unique ESU. To improve management regulations in the marine realm, our research also stresses the need for more empirical studies on genetic diversity of commercially exploited species in coastal environments of China.

Keywords

Evolutionarily significant units Genetic conservation Phylogeography East Asia 

Notes

Acknowledgements

This study was supported by research grants from National Natural Science Foundation of China (41276138), Doctoral Program of Ministry of Education of China (20130132110009), and Fundamental Research Funds for the Central Universities.

Supplementary material

10592_2017_998_MOESM1_ESM.docx (14 kb)
Supplementary material 1 (DOCX 13 KB)

References

  1. Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744CrossRefPubMedGoogle Scholar
  2. Bandelt HJ (2008) Clock debate: when times are a-changin’: time dependency of molecular rate estimates: tempest in a teacup. Heredity 100(1):1–2CrossRefPubMedGoogle Scholar
  3. Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefPubMedGoogle Scholar
  4. Bensasson D, Zhang DX, Hartl DL, Hewitt GM (2001) Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends Ecol Evol 16:314–321CrossRefPubMedGoogle Scholar
  5. Corl A, Ellegren H (2013) Sampling strategies for species trees: the effects on phylogenetic inference of the number of genes, number of individuals, and whether loci are mitochondrial, sex-linked, or autosomal. Mol Phylogen Evol 67:358–366CrossRefGoogle Scholar
  6. Cronin TM, Kitamura A, Ikeya N, Watanabe M, Kamiya T (1994) Late Pliocene climate-change 3.4–2.3 ma: paleoceanographic record from the Yabuta formation, Sea of Japan. Palaeogeogr Palaeoclimatol Palaeoecol 108:437–455CrossRefGoogle Scholar
  7. Crowder L, Norse E (2008) Essential ecological insights for marine ecosystem-based management and marine spatial planning. Mar policy 32:772–778CrossRefGoogle Scholar
  8. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772CrossRefPubMedPubMedCentralGoogle Scholar
  9. Dong YW, Wang HS, Han GD, Ke CH, Zhan X, Nakano T, Williams GA (2012) The impact of Yangtze River discharge, ocean currents and historical events on the biogeographic pattern of Cellana toreuma along the China coast. PLoS ONE 7:e36178CrossRefPubMedPubMedCentralGoogle Scholar
  10. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973CrossRefPubMedPubMedCentralGoogle Scholar
  11. Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752CrossRefPubMedGoogle Scholar
  12. Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Ann Rev Ecol Evol Syst 34:397–423CrossRefGoogle Scholar
  13. Guo X, Zhao D, Jung D, Li Q, Kong LF, Ni G, Nakano T, Matsukuma A, Kim S, Park C (2015) Phylogeography of the rock shell Thais clavigera (Mollusca): evidence for long-distance dispersal in the northwestern Pacific. PloS ONE 10:e0129715CrossRefPubMedPubMedCentralGoogle Scholar
  14. Han ZQ, Zheng W, Zhu WB, Yu CG, Shui BN, Gao TX (2015) A barrier to gene flow in the Asian paddle crab, Charybdis japonica, in the Yellow Sea. ICES J Mar Sci 72:1440–1448CrossRefGoogle Scholar
  15. Hellberg ME, Vacquier VD (1999) Rapid evolution of fertilization selectivity and lysin cDNA sequences in teguline gastropods. Mol Biol Evol 16:839–848CrossRefPubMedGoogle Scholar
  16. Huelsken T, Schreiber S, Hollmann M (2011) COI amplification success from mucus-rich marine gastropods (Gastropoda: Naticidae) depends on DNA extraction method and preserving agent. Mitteilungen der Deutschen Malakozoologischen Gesellschaft 85:17–26Google Scholar
  17. Huelsken T, Tapken D, Dahlmann T, Wägele H, Riginos C, Hollmann M (2012) Systematics and phylogenetic species delimitation within Polinices sl (Caenogastropoda: Naticidae) based on molecular data and shell morphology. Org Divers Evol 12:349–375CrossRefGoogle Scholar
  18. Hülsken T, Clemmensen M, Hollmann M (2006) Neverita delessertiana (Recluz in Chenu, 1843): a naticid species (Gastropoda: Caenogastropoda) distinct from Neverita duplicata (Say, 1822) based on molecular data, morphological characters, and geographical distribution. Zootaxa 1257:1–25Google Scholar
  19. Kitamura A (2015) Constraints on eustatic sea-level changes during the Mid-Pleistocene Climate Transition: evidence from the Japanese shallow-marine sediment record. Quatern Int 397:417–421CrossRefGoogle Scholar
  20. Leasi F, Norenburg JL (2014) The necessity of DNA taxonomy to reveal cryptic diversity and spatial distribution of meiofauna, with a focus on Nemertea. PLoS ONE 9:e104385CrossRefPubMedPubMedCentralGoogle Scholar
  21. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  22. Liu H, Xu M, Wu C (2013) Evaluation of nutritional composition in Nevertia didyma and Natica vitellus from Zhoushan Sea area. Food Sci 34:228–231 (In Chinese with English abstract)Google Scholar
  23. Mace GM (2004) The role of taxonomy in species conservation. Philos Trans R Soc B 359:711–719CrossRefGoogle Scholar
  24. Mcgovern TM, Keever CC, Saski CA, Hart MW, Marko PB (2010) Divergence genetics analysis reveals historical population genetic processes leading to contrasting phylogeographic patterns in co-distributed species. Mol Ecol 19:5043–5060CrossRefPubMedGoogle Scholar
  25. Moritz C (1994) Defining ‘Evolutionarily Significant Units’ for conservation. Trends Ecol Evol 9:373–375CrossRefPubMedGoogle Scholar
  26. Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Biol 51:238–254CrossRefPubMedGoogle Scholar
  27. Ni G, Li Q, Kong LF, Yu H (2014) Comparative phylogeography in marginal seas of the northwestern Pacific. Mol Ecol 23:534–548CrossRefPubMedGoogle Scholar
  28. Ni G, Li Q, Ni LH, Kong L-F, Yu H (2015) Population subdivision of the surf clam Mactra chinensis in the East China Sea: Changjiang River outflow is not the sole driver. PeerJ 3:e1240CrossRefPubMedPubMedCentralGoogle Scholar
  29. Pisias NG, Moore T (1981) The evolution of Pleistocene climate: a time series approach. Earth Planet Sci Lett 52:450–458CrossRefGoogle Scholar
  30. 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
  31. Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Mol Ecol 21:1864–1877CrossRefPubMedGoogle Scholar
  32. Reilly SB, Corl A, Wake DB (2015) An integrative approach to phylogeography: investigating the effects of ancient seaways, climate, and historical geology on multi-locus phylogeographic boundaries of the Arboreal Salamander (Aneides lugubris). BMC Evol Biol 15:241CrossRefPubMedPubMedCentralGoogle Scholar
  33. Schulenburg J, Hancock JM, Pagnamenta A, Sloggett JJ, Majerus MEN, Hurst GDD (2001) Extreme length and length variation in the first ribosomal internal transcribed spacer of ladybird beetles (Coleoptera: Coccinellidae). Mol Biol Evol 18:648–660CrossRefPubMedGoogle Scholar
  34. Sosdian S, Rosenthal Y (2009) Deep-Sea temperature and ice volume changes across the Pliocene-Pleistocene climate transitions. Science 325:306–310CrossRefPubMedGoogle Scholar
  35. Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M, Halpern BS, Jorge MA, Lombana A, Lourie SA (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57:573–583CrossRefGoogle Scholar
  36. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313CrossRefPubMedPubMedCentralGoogle Scholar
  37. Sun Z, Song Z, Yang J, Chang L (2012) Analysis of phenotypic variation of Neverita didyma in the Yellow Sea and Bohai Sea. Oceanolgia et Limnologia Sinica 43:1163–1169 (In Chinese with English abstract)Google Scholar
  38. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  39. Tang CQ, Humphreys AM, Fontaneto D, Barraclough TG (2014) Effects of phylogenetic reconstruction method on the robustness of species delimitation using single-locus data. Methods Ecol Evol 5:1086–1094CrossRefPubMedPubMedCentralGoogle Scholar
  40. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882CrossRefPubMedPubMedCentralGoogle Scholar
  41. Torres-Cambas Y, Ferreira S, Cordero-Rivera A, Lorenzo-Carballa MO (2017) Identification of evolutionarily significant units in the cuban endemic damselfly Hypolestes trinitatis, (Odonata: Hypolestidae). Conserv Genet. doi: 10.1007/s10592-017-0959-1 Google Scholar
  42. Villanova VL, Hughes PT, Hoffman EA (2017) Combining genetic structure and demographic analyses to estimate persistence in endangered key deer (Odocoileus virginianus clavium). Conserv Genet. doi: 10.1007/s10592-017-0958-2 Google Scholar
  43. Wang BC, Yu ZY, Liu CZ (1980) The change of coasts and beaches and the movement of longshore sediments of Haizhou Bay. Acta Oceanologica Sinica 2:80–96 (In Chinese with English abstract)Google Scholar
  44. Wang J, Ling MT, Dong YW (2015) Causations of phylogeographic barrier of some rocky shore species along the Chinese coastline. BMC Evol Biol 15:114CrossRefPubMedPubMedCentralGoogle Scholar
  45. Wang J, Ganmanee M, Shauhwai AT, Mujahid A, Dong YW (2016) Pleistocene events and present environmental factors have shaped the phylogeography of the intertidal limpet Cellana toreuma (Reeve, 1855) (Gastropoda: Nacellidae) in Southeast Asia and China. J Mollus Stud 82(3):378–390CrossRefGoogle Scholar
  46. Wilke T, Schultheiß R, Albrecht C (2013) As time goes by: a simple fool's guide to molecular clock approaches in invertebrates*. Am Malacol Bull 462(27): 25–45Google Scholar
  47. Zhang SP (2003) Chinese species of Naticidae III, subfamily Polinicinae. Chin J Zool 38:101–110 (Chinese with English abstract)Google Scholar
  48. Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29:2869–2876CrossRefPubMedPubMedCentralGoogle Scholar
  49. Zhao D, Li Q, Ni L, Kong LF, Yu H (2017) Cryptic diversity of marine gastropod Monodonta labio (Trochidae): did the early Pleistocene glacial isolation and sea surface temperature gradient jointly drive diversification of sister species and/or subspecies in the north-western Pacific? Mar Ecol-Evol Persp. doi: 10.1111/maec.12443

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.Fisheries CollegeOcean University of ChinaQingdaoChina

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