Molecular Biology Reports

, Volume 41, Issue 6, pp 3733–3743 | Cite as

Mitochondrial DNA phylogeography of Semisulcospira libertina (Gastropoda: Cerithioidea: Pleuroceridae): implications the history of landform changes in Taiwan

  • Kui-Ching Hsu
  • Hor Bor
  • Hung-Du Lin
  • Po-Hsun Kuo
  • Mian-Shin Tan
  • Yuh-Wen Chiu


The mitochondrial DNA cytochrome c oxidase subunit I sequences from 95 specimens of Semisulcospira libertina in Taiwan were identified as two major phylogroups, exhibiting a southern and northern distribution, north of Formosa Bank and south of Miaoli Plateau. The genetic distance between these two phylogroups was 12.20 %, and the distances within-phylogroups were 4.97 and 5.56 %. According to a molecular clock of 1.56 % per lineage per million years, the divergence time between these two major phylogroups was estimated at 4.94 million years ago (mya), with the two phylogroups forming at 3.64 and 3.75 mya, respectively. Moreover, the geological events have suggested that Taiwan Island emerged above sea level at 4–5 mya, and became its present shape at 2 mya. These results suggested that these two phylogroups might originate from two independent ancestral populations or divergent before colonizing Taiwan. Within South phylogroup, the initial colonization was hypothesized to be in Kaoping River (WT), followed by its northward. The high divergence between south- and north of WT River was influenced by the formation of the Kaoping foreland basins. Within North phylogroup, the colonization was from central sub-region through paleo-Miaoli Plateau to northern and northeastern sub-regions. This study showed that the landform changes might have shaped the genetic structure of S. libertina in concert. Apparently, two cryptic species or five different genetic stocks of S. libertina could be identified; these results are useful for the evaluation and conservation of S. libertina in Taiwan.


Semisulcospira libertina Cryptic species Glacial event Orogenic activity Phylogeography Taiwan 



We thank Kun-Chan Tsai for English correction and suggestion. This research was supported by the National Science Council Grants to Yuh-Wen Chiu (NSC96-2313-B-037-001-MY3). The Associate Editor and three anonymous reviewers provided valuable comments on the manuscript.


  1. 1.
    Ho CS (1986) A synthesis of the geologic evolution of Taiwan. Tectonophysics 125:1–16CrossRefGoogle Scholar
  2. 2.
    Hsu V (1990) Seismicity and tectonics of a continental-island arc collision zone at the island of Taiwan. J Geophys Res 95:4725–4734CrossRefGoogle Scholar
  3. 3.
    Teng LS (1990) Geotectonic evolution of late Cenozoic arc-continent collision in Taiwan. Tectonophysics 183:57–76CrossRefGoogle Scholar
  4. 4.
    Liu TK, Chen YG, Chen WS, Jiang SH (2000) Rates of cooling and denudation of the early Penglai Orogeny, Taiwan, as assessed by fission-track constraints. Tectonophysics 320:69–82CrossRefGoogle Scholar
  5. 5.
    Huang CY, Yuan PB, Song SR, Lin CW, Wang CS, Chen MT, Shyu CT, Karp B (1995) Tectonics of short-lived intra-arc basins in the arc-continent collision terrene of the Coastal Range, eastern Taiwan. Tectonics 14:19–38CrossRefGoogle Scholar
  6. 6.
    Boggs S, Wang WC, Lewis FS, Chen JC (1979) Sediment properties and water characteristics of the Taiwan shelf and slope. Acta Oceanogr Taiwan 10:10–49Google Scholar
  7. 7.
    Wang HY, Tsai MP, Yu MJ, Lee SC (1999) Influence of glaciation on divergence patterns of the endemic minnow, Zacco pachycephalus, in Taiwan. Mol Ecol 8:1879–1888CrossRefPubMedGoogle Scholar
  8. 8.
    Wang CF, Hsieh CH, Lee SC, Wang HY (2011) Systematics and phylogeography of the Taiwanese endemic minnow Candidia barbatus (Pisces: Cyprinidae) based on DNA sequence, allozymic, and morphological analyses. Zool J Linn Soc 161:613–632CrossRefGoogle Scholar
  9. 9.
    Gascoyne M, Benjamin GJ, Schwarcz HP, Ford DC (1979) Sea level lowering during the Illinoian glaciation: evidence from a Bahama ‘Blue Bole’. Nature 205:806–808Google Scholar
  10. 10.
    Fairbanks RG (1989) A 17,000-year glacio-eustatic sea level record: influence of glacial melting rates on the Younger Dryas event and deep-ocean circulation. Nature 342:637–642CrossRefGoogle Scholar
  11. 11.
    Yu HT (1995) Patterns of diversification and genetic population structure of small mammals in Taiwan. Biol J Linn Soc 55:69–89CrossRefGoogle Scholar
  12. 12.
    Ota H (1991) Systematics and biogeography of terrestrial reptiles of Taiwan. In: Lin Y-S, Chang K-H (eds) Proceedings of the first international symposium on wildlife conservation, ROC. Council of Agriculture, Taipei, pp 47–112Google Scholar
  13. 13.
    Ota H (1997) Historical biogeographical implications in the variation and diversity of amphibians and reptiles in Taiwan. In: Kue K-Y, Chen TH (eds) Proceedings of the symposium on the phylogeny, biogeography and conservation of fauna and flora of East Asian region. National Science Council, ROC, Taipei, pp 75–86Google Scholar
  14. 14.
    Shih HT, Hung HC, Schubart CD, Chen CA, Chang HW (2006) Intraspecific genetic diversity of the endemic freshwater crab Candidiopotamon rathbunae (Decapoda, Brachyura, Potamidae) reflects five million years of the geological history of Taiwan. J Biogeogr 33:980–989CrossRefGoogle Scholar
  15. 15.
    Chiang TY, Lin HD, Shao KT, Hsu KC (2010) Multiple causations shaping phylogeography of Chinese spiny loach (Cobitis sinensis) in Taiwan inferred from mitochondrial DNA variations. J Fish Biol 76:1173–1189CrossRefPubMedGoogle Scholar
  16. 16.
    Lin SM, Chen CA, Lue KY (2002) Molecular phylogeny and biogeography of the grass lizards genus Takydromus (Reptilia: Lacertidae) of East Asia. Mol Phylogenet Evol 22:276–288CrossRefPubMedGoogle Scholar
  17. 17.
    Creer S, Malhotra A, Thorpe RS, Chou WH (2001) Multiple causation of phylogeographical pattern as revealed by nested clade analysis of the bamboo viper (Trimeresurus stejnegeri) within Taiwan. Mol Ecol 10:1967–1981CrossRefPubMedGoogle Scholar
  18. 18.
    Wang JP, Hsu KC, Chiang TY (2000) Mitochondrial DNA phylogeography of Acrossocheilus paradoxus (Cyprinidae) in Taiwan. Mol Ecol 9:1483–1494CrossRefPubMedGoogle Scholar
  19. 19.
    Yang YJ, Lin YS, Wu JL, Hui CF (1994) Variation in mitochondrial DNA and population structure of the Taipei tree frog Rhacophorus taipeianus in Taiwan. Mol Ecol 3:219–228CrossRefPubMedGoogle Scholar
  20. 20.
    Lin CC (1957) Topography in Taiwan. Taiwan Doc 1:67–79Google Scholar
  21. 21.
    Tzeng CS (1986) Distribution of freshwater fishes of Taiwan. J Taiwan Mus 39:127–146Google Scholar
  22. 22.
    Chen WS, Erh CH, Chen MM, Yang CC, Chang IS, Liu TK, Horng CS, Shea KS, Yeh MG, Wu JC, Ko CT, Lin CC, Huang NW (2000) The evolution of foreland basins in western Taiwan: evidence from Plio–Pleistocene sequences. Bull Cent Geol Surv 13:137–156 (in Chinese)Google Scholar
  23. 23.
    Oshima M (1923) Studies on the distribution of the fresh-water fishes of Taiwan and discuss the geographical relationship of the Taiwan Island and the adjacent area. Zool Mag 35:1–49 (in Japanese)Google Scholar
  24. 24.
    Wang JP, Lin HD, Huang S, Pan CH, Chen XL, Chiang TY (2004) Phylogeography of Varicorhinus barbatulus (Cyprinidae) in Taiwan based on nucleotide variation of mtDNA and allozymes. Mol Phylogenet Evol 31:1143–1156CrossRefPubMedGoogle Scholar
  25. 25.
    Shih HT, Ng PKL, Chang HW (2004) Systematics of the genus Geothelphusa (Crustacea: Decapoda, Brachyura, Potamidae) from southern Taiwan: a molecular appraisal. Zool Stud 43:519–526Google Scholar
  26. 26.
    Chou CH, Huang S, Chen SH, Kuoh CS, Chiang TY, Chiang YC (1999) Ecology and evolution of Miscanthus of Taiwan. Natl Sci Counc Mon 27:1158–1169Google Scholar
  27. 27.
    Liao TY, Wang TY, Lin HD, Shen SC, Tzeng CS (2008) Phylogeography of the endangered species, Sinogastromyzon puliensis (Cypriniformes: Balitoridae), in southwestern Taiwan based on mtDNA. Zool Stud 47:383–392Google Scholar
  28. 28.
    Davis GM (1972) Geographic variation in Semisulcospira libertina (Mesogastropoda: Pleuroceridae). Proc Malacol Soc Lond 40:7–32Google Scholar
  29. 29.
    Oniwa K, Kimura M (1986) Genetic variability and relationships in six snail species of the genus Semisulcospira. Jpn J Genet 61:503–514CrossRefGoogle Scholar
  30. 30.
    Oniwa K, Kimura M (1986) Genetic variability in two snail species Semisulcospira libertina and Semisulcospira reiniana. Jpn J Genet 62:137–146CrossRefGoogle Scholar
  31. 31.
    Urabe M (1992) A discrimination and morphological comparison of two snail species of the genus Semisulcospira in a single river. Venus 50:270–286Google Scholar
  32. 32.
    Martin JG, Jonathan AT, Ellimor M, Dirk E, Abayomi J, Domino AJ, Anderzej P, Jean PP (2007) Amassing diversity in an ancient lake: evolution of a morphologically diverse parthenogenetic gastropod assemblage in Lake Malawi. Mol Ecol 16:517–530Google Scholar
  33. 33.
    Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  34. 34.
    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 25:4876–4882PubMedCentralCrossRefPubMedGoogle Scholar
  35. 35.
    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA 5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralCrossRefPubMedGoogle Scholar
  36. 36.
    Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition–transversion and G+C content biases. Mol Biol Evol 9:678–687PubMedGoogle Scholar
  37. 37.
    Excoffier L, Smouse PE (1994) Using allele frequencies and geographic subdivision to reconstruct gene trees within a species, molecular variance parsimony. Genetics 136:343–359PubMedCentralPubMedGoogle Scholar
  38. 38.
    Nei M, Tajima F (1983) Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data. Genetics 105:207–217PubMedCentralPubMedGoogle Scholar
  39. 39.
    Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munroled HN (ed) Mammalian protein metabolism. Academic Press, New YorkGoogle Scholar
  40. 40.
    Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  41. 41.
    Templeton AR (1993) The ‘Eve’ hypothesis: a genetic critique and reanalysis. Am Anthropol 95:51–72CrossRefGoogle Scholar
  42. 42.
    Pearse DE, Crandall KA (2004) Beyond FST: analysis of population genetic data for conservation. Conserv Genet 5:585–602CrossRefGoogle Scholar
  43. 43.
    Buhay JE, Crandall KA (2005) Subterranean phylogeography of freshwater crayfishes shows extensive gene flow and surprisingly large population sizes. Mol Ecol 14:4259–4273CrossRefPubMedGoogle Scholar
  44. 44.
    Excoffier L, Smouse PE, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial restriction data. Genetics 131:479–491PubMedCentralPubMedGoogle Scholar
  45. 45.
    Excoffier L, Lischer HEL (2010) Arlequin suite version 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefPubMedGoogle Scholar
  46. 46.
    Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562PubMedCentralPubMedGoogle Scholar
  47. 47.
    Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  48. 48.
    Drummond AJ, Rambau A, Suchard M (2013) BEAST 1.8.0.
  49. 49.
    Rambaut A, Drummond AJ, Suchard M (2013) Tracer v1.6.
  50. 50.
    Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov Chain Monte Carlo approach. Genetics 158:885–896PubMedCentralPubMedGoogle Scholar
  51. 51.
    Marko PB (2002) Fossil calibration of molecular clocks and the divergence times of geminate species pairs separated by the Isthmus of Panama. Mol Biol Evol 19:2005–2021CrossRefPubMedGoogle Scholar
  52. 52.
    Hellberg ME, Vacquier VD (1999) Rapid evolution of fertilization selectivity and lysin cDNA sequences in teguline gastropods. Mol Biol Evol 16:839–848CrossRefPubMedGoogle Scholar
  53. 53.
    Wilke T (2003) Salenthydrobia n. gen. (Rissooidea: Hydrobiidae): a potential relict of the Messinian salinity crisis. Zool J Linn Soc 137:319–336CrossRefGoogle Scholar
  54. 54.
    Wilke T, Schultheiß R, Albrecht C (2009) As time goes by: a simple fool’s guide to molecular clock approaches in invertebrates. Am Malacol Bull 27:25–45CrossRefGoogle Scholar
  55. 55.
    Chiang TY, Lin HD, Zhao J, Kuo PH, Lee TW, Hsu KC (2013) Diverse processes shape deep phylogeographical divergence in Cobitis sinensis (Teleostei: Cobitidae) in East Asia. J Zool Syst Evol Res 51:316–326Google Scholar
  56. 56.
    Wiley EO (1978) The evolutionary species concept reconsidered. Syst Zool 27:17–26CrossRefGoogle Scholar
  57. 57.
    Cracraft J (1989) Speciation and its ontology: the empirical consequences of alternative species concepts for understanding patterns and processes of differentiation. In: Otte D, Endler JA (eds) Speciation and its consequences. Sinauer Associates, Sunderland, pp 28–59Google Scholar
  58. 58.
    Gill FB, Slikas B, Sheldon FH (2005) Phylogeny of titmice (Paridae): II. Species relationships based on sequences of the mitochondrial cytochrome-b gene. Auk 122:121–143CrossRefGoogle Scholar
  59. 59.
    Köhler F, Johnoson MS (2012) Species limits in molecular phylogenies: a cautionary tale from Australian land snails (Camaenidae: Amplirhagada Iredale, 1933). Zool J Linn Soc 165:337–362CrossRefGoogle Scholar
  60. 60.
    King TL, Eackles MS, Gjetvaj B, Hoeh WR (1999) Intraspecific phylogeography of Lasmigona subviridis (Bivalvia: Unionidae): conservation implications of range discontinuity. Mol Ecol 8:S65–S78CrossRefPubMedGoogle Scholar
  61. 61.
    Roe K, Lydeard C (1998) Molecular systematic of the freshwater mussel genus Potamilus (Bivalvia: Unionidae). Malacologia 39:195–205Google Scholar
  62. 62.
    Baker AM, Bartlett C, Bunn SE, Goudkamp K, Sheldon F, Hughes JM (2003) Cryptic species and morphological plasticity in long-lived bivalves (Unionoida: Hyriidae) from inland Australia. Mol Ecol 12:2707–2717CrossRefPubMedGoogle Scholar
  63. 63.
    Spencer HG, Marshall BA, Waters JM (2009) Systematics and phylogeny of a new cryptic species of Diloma Philippi (Mollusca: Gastropoda: Trochidae) from a novel habitat, the bull kelp holdfast communities of southern New Zealand. Invertebr Syst 23:19–25CrossRefGoogle Scholar
  64. 64.
    Yang JQ, Tang WQ, Liao TY, Sun Y, Zhou ZC, Han CC, Liu D, Lin HD (2012) Phylogeographical analysis on Squalidus argentatus recapitulates historical landscapes and drainage evolution on the island of Taiwan and mainland China. Int J Mol Sci 13:1405–1425PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Kui-Ching Hsu
    • 1
  • Hor Bor
    • 2
  • Hung-Du Lin
    • 3
  • Po-Hsun Kuo
    • 1
  • Mian-Shin Tan
    • 2
  • Yuh-Wen Chiu
    • 4
  1. 1.Department of Industrial ManagementNational Taiwan University of Science and TechnologyTaipeiTaiwan
  2. 2.Department of Biomedical Science and Environmental BiologyKaohsiung Medical UniversityKao-hsiungTaiwan
  3. 3.Department of Physical TherapyShu Zen College of Medicine and ManagementKao-hsiungTaiwan
  4. 4.National Museum of Marine Biology and AquariumPingtungTaiwan

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