Skip to main content
SpringerLink
Log in

Mitochondrial Genetic Diversity of the Freshwater Snail Melanoides tuberculata

  • Original Article
  • Published:
Biochemical Genetics Aims and scope Submit manuscript

Abstract

According to geological history, Peninsular Malaysia and Borneo formed at different times and were once connected during Quaternary glaciations. To determine how this history has influenced phylogeography, our study examined the population genetic structure of the tropical freshwater gastropod Melanoides tuberculata across Peninsular Malaysia and Borneo using the sequences from mitochondrial DNA 16S rRNA and cytochrome oxidase subunit I genes (1168 bp). In total, 104 specimens were collected from seventeen populations. All mtDNA haplotypes were identified as belonging to two highly divergent lineages, and these lineages were almost allopatric in their distributions. Our study found that the freshwater fauna in Malaysia might be divided into four regions: northeast Peninsular Malaysia, northwest Peninsular Malaysia, south Peninsular Malaysia, and Borneo. The phylogeography of M. tuberculata in Malaysia was shaped by the landforms of Peninsular Malaysia and by the paleo-river systems in the Sunda continental shelf. In addition, our study found that these two lineages in Malaysia have invaded the globe. These results suggest that Malaysia is located in important shipping lanes throughout the world, and the populations of M. tuberculate might be widely distributed throughout the world by shipping.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Azman AG (2000) The Western Belt granite of Peninsular Malaysia: some emergent problems on granite classification and its implication. Geosci J 4:283–293

    Article  Google Scholar 

  • Chen XL, Chiang TY, Lin HD, Zheng HS, Shao KT, Zhang Q, Hsu KC (2007) Mitochondrial DNA phylogeographyof Glyptothorax fokiensis and Glyptothorax hainanensis in Asia. J Fish Biol 70:75–93

    Article  CAS  Google Scholar 

  • Chiu YW, Bor H, Kuo PH, Hsu KC, Tan MS, Lin HD (2017) Origins of Semisulcospira libertina (Gastropoda: Semisulcospiridae) in Taiwan. Mitochondrial DNA A 28:518–525

    Article  CAS  Google Scholar 

  • Cox CB, Moore PD (2000) Biogeography: an ecological and evolutionary approach. Wiley-Blackwell, Hoboken

    Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Bruyn M, Wilson JA, Mather PB (2004) Huxley’s line demarcates extensive genetic divergence between eastern and western forms of the giant freshwater prawn, Macrobrachium rosenbergii. Mol Phylogenet Evol 30:251–257

    Article  CAS  PubMed  Google Scholar 

  • Drummond AJ, Rambau A, Suchard M (2013) BEAST 1.8.0. http://beast.bio.ed.ac.uk

  • Duggan IC (2002) First record of a wild population of the tropical snail Melanoides tuberculata in New Zealand natural waters. New Zeal J Mar Fresh Res 36:825–829

    Article  Google Scholar 

  • Dundee DS, Pain A (1977) Ecology of the snail, Melanoides tuberculata (Müller), intermediate host of the human liver fluke (Opisthorchis sinensis) in New Orleans, Louisiana. Nautilus 91:17–20

    Google Scholar 

  • Esa YB, Siraj SS, Daud SK, Rahim KAA, Japning JRR, Tan SG (2008) Mitochondrial DNA diversity of Tor tambroides Valenciennes (Cyprinidae) from five natural populations in Malaysia. Zool Stud 47:360–367

    CAS  Google Scholar 

  • 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 3:294–299

    CAS  PubMed  Google Scholar 

  • Guo X, He S, Zhang Y (2005) Phylogeny and biogeography of Chinese sisorid catfishes re-examined using mitochondrial cytochrome b and 16S rRNA gene sequences. Mol Phylogenet Evol 35:344–362

    Article  CAS  PubMed  Google Scholar 

  • Hanebuth TJJ, Voris HK, Yokoyama Y, Saito Y, Okuno JI (2011) Formation and fate of sedimentary depocentres on Southeast Asia’s Sunda Shelf over the past sea-level cycle and biogeographic implications. Earth Sci Rev 104:92–110

    Article  Google Scholar 

  • Hebert PD, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc Biol Sci 270:313–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu KC, Bor H, Lin HD, Kuo PH, Tan MS, Chiu YW (2014) Mitochondrial DNA phylogeography of Semisulcospira libertina (Gastropoda: Cerithioidea: Pleuroceridae): implications the history of landform changes in Taiwan. Mol Biol Rep 41:3733–3743

    Article  CAS  PubMed  Google Scholar 

  • Inger RF, Chin PK (2002) The freshwater fishes of North Borneo. Revised edition with supplementary chapter by PK Chin. Natural History Publications, Kota Kinabalu

    Google Scholar 

  • Jenkins TM, Jones SC, Lee CY, Forschler BT, Chen Z, Lopez-Martinez G, Gallagher NT, Brown G, Neal M, Thistleton B, Kleinshmidt S (2007) Phylogeography illuminates maternal origins of exotic Coptotermes gestroi (Isoptera: Rhinotermitidae). Mol Phylogenet Evol 42:612–621

    Article  CAS  PubMed  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Monro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132

    Chapter  Google Scholar 

  • 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 165:337–362

    Article  Google Scholar 

  • Lasso CA, Martínez ER, Capelo JC, Morales B, Sánchez-Maya A (2009) Lista de los moluscos (Gastropodos_Bivalvia) dulceacuícolas y estuarinos de la cuenca del Orinoco (Venezuela). Biota Colombiana 10:63–74

    Google Scholar 

  • Liu J, Liu HL, Zhang HB (2018) Phylogeny and evolutionary radiation of the marine mussels (Bivalvia: Mytilidae) based on mitochondrial and nuclear genes. Mol Phylogenet Evol 126:233–240

    Article  PubMed  Google Scholar 

  • Madsen H, Frandsen F (1989) The spread of freshwater snails including those of medical and veterinary importance. Acta Trop 46:139–146

    Article  CAS  PubMed  Google Scholar 

  • McConnell SKJ (2004) Mapping aquatic faunal exchanges across the Sunda shelf, South-East Asia, using distributional and genetic data sets from the cyprinid fish Barbodes gonionotus (Bleeker, 1850). J Nat Hist 38:651–670

    Article  Google Scholar 

  • Nei M, Tajima F (1983) Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data. Genetics 105:207–217

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered vs. unordered alleles. Genetics 144:1237–1245

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reeves WK, Dillon RT, Dasch GA (2008) Freshwater snails (Mollusca: Gastropoda) from the Commonwealth of Dominica with a discussion of their roles in the transmission of parasites. Am Malacol Bull 24:59

    Article  Google Scholar 

  • Ronquist F (1997) Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Syst Biol 57:195–203

    Article  Google Scholar 

  • Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Ryan JRJ, Esa YB (2006) Phylogenetic analysis of Hampala fishes (Subfamily Cyprininae) in Malaysia inferred from partial mitochondrial cytochrome b DNA sequences. Zool Sci 23:893–901

    Article  CAS  Google Scholar 

  • Santos SBD, Miyahira IC, Lacerda LEMD (2007) First record of Melanoides tuberculatus (Müller, 1774) and Biomphalaria tenagophila (d´Orbigny, 1835) on Ilha Grande, Rio de Janeiro, Brazil. Biota Neotropic 7:361

    Article  Google Scholar 

  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701

    Article  CAS  Google Scholar 

  • 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 23:19–25

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Templeton AR (1993) The ‘Eve’ hypothesis: a genetic critique and reanalysis. Am Anthropol 95:51–72

    Article  Google Scholar 

  • 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 Acid Res 24:4876–4882

    Article  Google Scholar 

  • Van Damme D, Lange C (2017) Melanoides tuberculate (amended version of 2016 assessment). The IUCN red list of threatened species 2017: e.T155675A110779677

  • Vázquez AA, Perera S (2010) Endemic freshwater molluscs of Cuba and their conservation status. Trop Conserv Sci 3:190–199

    Article  Google Scholar 

  • Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167

    Article  Google Scholar 

  • Xia X (2013) DAMBE5: A comprehensive software package for data analysis. Mol Biol Evol 30:1720–1728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeo DCJ, Shih HT, Meier R, Ng PKL (2007) Phylogeny and biogeography of the freshwater crab genus Johora (Crustacea: Brachyura: Potamidae) from the Malay Peninsula, and the origins of its insular fauna. Zool Scr 36:255–269

    Article  Google Scholar 

  • Yu Y, Harris AJ, He X (2010) S-DIVA (statistical dispersal-vicariance analysis): a tool for inferring biogeographic histories. Mol Phylogenet Evol 56:848–850

    Article  PubMed  Google Scholar 

  • Zainudin R, Nor SM, Ahmad N, Md-Zain BM, Rahman MA (2010) Genetic structure of Hylarana erythraea (Amphibia: Anura: Ranidae) from Malaysia. Zool Stud 49:688–702

    CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the National Science Council grants to Yuh-Wen Chiu (NSC 96‐2313‐B‐037‐001‐MY3). We also thank the anonymous referees for their help comments.

Author information

Authors and Affiliations

  1. Center for Research in Water Science and Technology, National Cheng Kung University, Tainan, 701, Taiwan

    Yuh-Wen Chiu

  2. Department of Hydraulic and Ocean Engineering, National Cheng Kung University, Tainan, 701, Taiwan

    Yuh-Wen Chiu

  3. AECOM Taiwan Corporation, Taipei, 106, Taiwan

    Ye-Chen Gan

  4. Department of Industrial Management, National Taiwan University of Science and Technology, Taipei, 106, Taiwan

    Po-Hsun Kuo

  5. College of Fisheries, Guangdong Ocean University, Zhanjiang, 524088, China

    Kui-Ching Hsu

  6. Department of Biomedical Science and Environmental Biology, Kaohsiung Medical University, Kaohsiung, 807, Taiwan

    Mian-Shin Tan

  7. National Museum of Marine Biology and Aquarium, Pingtung, Taiwan

    Yu-Min Ju

  8. Graduate Institute of Marine Biology, National Dong Hwa University, Pingtung, Taiwan

    Yu-Min Ju

  9. Department of Biology, The Affiliated School of National Tainan First Senior High School, Tainan, 701, Taiwan

    Hung-Du Lin

Authors
  1. Yuh-Wen Chiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ye-Chen Gan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Po-Hsun Kuo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kui-Ching Hsu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mian-Shin Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yu-Min Ju
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hung-Du Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hung-Du Lin.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chiu, YW., Gan, YC., Kuo, PH. et al. Mitochondrial Genetic Diversity of the Freshwater Snail Melanoides tuberculata. Biochem Genet 57, 323–337 (2019). https://doi.org/10.1007/s10528-018-9892-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10528-018-9892-3

Keywords

Search

Navigation