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Phylogeography and the genetic structure of the land-locked freshwater prawn Macrobrachium asperulum (Crustacea: Decapoda: Palaemonidae) in Taiwan

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Abstract

Macrobrachium asperulum is a land-locked macroinvertebrate species of freshwater prawn, which inhabits a wide range of freshwater bodies and has an abundant pan-island distribution in Taiwan. In this study, we used mitochondrial (mt) DNA fragment sequences of the large subunit ribosomal RNA (16S rRNA) gene and the cytochrome oxidase subunit I (COI) gene to examine the phylogeographical pattern and the genetic structure of M. asperulum in Taiwan. Genealogic reconstructions present four lineages distributed in three geographical regions. Analysis of molecular variance (AMOVA) shows a significant genetic structure across all hierarchical levels, indicating that genetic variance is geographically subdivided. The high genetic structure of within-catchment or within-river populations implies that the freshwater prawn M. asperulum with a land-locked life cycle has a more-limited dispersal ability. The spatial divisions are probably correlated with two dispersal routes from the Asian mainland during the tectonic evolution of Taiwan. Subsequently, the population genetic structure is deeply influenced by the periodic oscillation of glaciations, followed by fragmentation due to the formation of geographical barriers, which resulted in rare contemporary gene flow. Population divergences indicate coalescent events between populations of China (Ming River) and Taiwan, dated to between the late Pliocene and early Pleistocene (2.63–1.78 myr). The high diversity of the genetic structure of eastern populations suggested multiple artificial introductions mainly from rivers of west-central Taiwan, and this has permitted lineage sorting and random drift.

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References

  • Avise, J. C., 1994. Molecular Markers, Natural History and Evolution. Chapman and Hall, New York.

    Google Scholar 

  • Avise, J. C., 2000. Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, MA.

    Google Scholar 

  • Bermingham, E. & J. C. Avise, 1986. Molecular zoogeography of freshwater fishes in the southeastern United States. Genetics 113: 939–965.

    PubMed  CAS  Google Scholar 

  • Bermingham, E. & A. P. Martin, 1998. Comparative mtDNA phylogeography of neotropic freshwater fishes: testing shared history to infer the evolutionary landscape of lower Central America. Molecular Ecology 7: 499–517.

    Article  PubMed  CAS  Google Scholar 

  • Bilton, D. T., J. R. Freeland & B. Okamura, 2001. Dispersal in freshwater invertebrates. Annual Review of Ecology and Systematics 32: 159–181.

    Article  Google Scholar 

  • Bohlen, J. & P. Ráb, 2001. Species and hybrid richness in spined loaches of the genus Cobitis (Teleostei: Cobitidae), with a checklist of European forms and suggestions for conservation. Journal of Fish Biology 59(Suppl. A): 75–89.

    Article  Google Scholar 

  • Camin, J. H. & R. R. Sokal, 1965. A method for deducing branching sequences in phylogeny. Evolution 19: 311–326.

    Article  Google Scholar 

  • Chiang, Y. C., K. H. Hung, B. A. Schaal, X. J. Ge, T. W. Hsu & T. Y. Chiang, 2006. Contrasting phylogeographical patterns between mainland and island taxa of the Pinus luchuensis complex. Molecular Ecology 15: 765–779.

    Article  PubMed  CAS  Google Scholar 

  • Crandall, K. A. & J. F. J. Fitzpatrick, 1996. Crayfish systematics: using a combination of procedures to estimate phylogeny. Systematic Biology 45: 1–26.

    Article  Google Scholar 

  • Creer, S., A. Malhotra, R. S. Thorpe & W. H. Chou, 2001. Multiple causation of phylogeographical pattern as revealed by nested clade analysis of the bamboo viper (Trimeresurus stejnegeri) within Taiwan. Molecular Ecology 10: 1967–1981.

    Article  PubMed  CAS  Google Scholar 

  • Dlugosch, K. M. & C. G. Hays, 2008. Genotypes on the move: some things old and some things new shape the genetics of colonization during species invasions. Molecular Ecology 17: 4583–4585.

    Article  PubMed  Google Scholar 

  • Dlugosch, K. M. & I. M. Parker, 2008. Funding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology 17: 431–449.

    Article  PubMed  CAS  Google Scholar 

  • Emerson, B. C., 2002. Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Molecular Ecology 11: 951–966.

    Article  PubMed  CAS  Google Scholar 

  • Excoffier, L., P. E. Smouse & J. M. Quattro, 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491.

    PubMed  CAS  Google Scholar 

  • Facon, B., J. P. Pointier, M. Glaubrecht, C. Poux, P. Jarne & P. David, 2003. A molecular phylogeography approach to biological invasions of the New World by parthenogenetic Thiarid snails. Molecular Ecology 12: 3027–3039.

    Article  PubMed  CAS  Google Scholar 

  • Falconer, D. S. & T. F. C. Mackay, 1996. Introduction to Quantitative Genetics, 4th ed. Longman, Harlow, England.

    Google Scholar 

  • Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.

    Article  Google Scholar 

  • Felsenstein, J., 1988. Phylogenies from molecular sequences: inference and reliability. Annual Review of Genetics 22: 521–565.

    Article  PubMed  CAS  Google Scholar 

  • Folmer, O., B. W. Hoeh & R. Lutz, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.

    PubMed  CAS  Google Scholar 

  • Fu, Y. X., 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925.

    PubMed  CAS  Google Scholar 

  • Fu, Y. X. & W. H. Li, 1993. Statistical tests of neutrality of mutations. Genetics 133: 693–709.

    PubMed  CAS  Google Scholar 

  • Golding, G. B., 1987. The detection of deleterious selection using ancestors inferred from a phylogenetic history. Genetical research 49: 71–82.

    Article  PubMed  CAS  Google Scholar 

  • Hewitt, G. M., 1996. Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society 58: 247–276.

    Google Scholar 

  • Hewitt, G. M., 1999. Post-glacial re-colonization of European biota. Biological Journal of the Linnean Society 68: 87–112.

    Article  Google Scholar 

  • Hipp, A. L., J. C. Hall & K. J. Sytsma, 2004. Congruence versus phylogenetic accuracy: revisiting the incongruence length difference test. Systematic Biology 53: 81–89.

    Article  PubMed  Google Scholar 

  • Holthuis, L. B., 1950. The decapoda of the Siboga Expedition part X. The Palaemonidae collected by the Siboga and Snellius Expeditions with remarks of others species I. Subfamily Palaemoninae. Siboga Expedition Monograph 39a: 1–268.

    Google Scholar 

  • Huang, J., 1984. Change of sea-level since the late Pleistocene in China. In Whyte, R. O. (ed.), The Evolution of the East Asian Environment. Center of Asian Studies, University of Hong Kong, Hong Kong: 309–319.

    Google Scholar 

  • Hwang, J. J. & H. P. Yu, 1984. Key to the freshwater shrimp of the genus Macrobrachium (Crustacea, Decapoda, Palaemonidae) from Taiwan with their habitat and distribution. National Taiwan College of Marine Science and Technology 19: 117–121. (in Chinese with English abstract).

    Google Scholar 

  • Kotlik, P. & P. Berrebi, 2001. Phylogeography of the barbel (Barbus barbus) assessed by mitochondrial variation. Molecular Ecology 10: 2177–2185.

    Article  PubMed  CAS  Google Scholar 

  • Liao, T. Y., T. Y. Wang, H. D. Lin, S. C. Shen & C. S. Tzeng, 2008. Phylogeography of the endangered species, Sinogastromyzon puliensis (Cypriniformes: Balitoridae), in southwestern Taiwan based on mtDNA. Zoological Studies 47: 383–392.

    CAS  Google Scholar 

  • Liu, D. & M. Ding, 1984. The characteristics and evolution of the paleoenvironment of China since the late Tertiary. In Whyte, R. O. (ed.), The Evolution of the East Asian Environment. Center of Asian Studies, University of Hong Kong, Hong Kong: 11–40.

    Google Scholar 

  • Liu, M. Y., Y. Cai & C. S. Tzeng, 2007. Molecular systematics of the freshwater prawn genus Macrobrachium Bate, 1868 (Crustacea: Decapoda: Palaemonidae) inferred from mtDNA sequences, with emphasis on east Asian species. Zoological Studies 46: 272–289.

    CAS  Google Scholar 

  • Lundberg, J. G., 1993. Africa-South American freshwater fish clades and continental drift, problem with a paradigm. In Goldenblatt, P. (ed.), Biotic Relationships Between Africa and South America. Yale University Press, New Haven, Connecticut: 156–198.

    Google Scholar 

  • Mamuris, Z., M. T. Stoumboudi, C. Stamatis, R. Barbieri & K. A. Moutou, 2005. Genetic variation in populations of the endangered fish Ladigesocypris ghigii and its implications for conservation. Freshwater Biology 50: 1441–1453.

    Article  CAS  Google Scholar 

  • Morrison, C. L., R. Ríos & J. E. Duffy, 2004. Phylogenetic evidence for an ancient rapid radiation of Caribbean sponge-dwelling snapping shrimps (Synalpheus). Molecular Phylogenetics and Evolution 30: 563–581.

    Article  PubMed  CAS  Google Scholar 

  • Nei, M., 1987. Molecular Evolutionary Genetics. Columbia University Press, New York.

    Google Scholar 

  • Ota, H., 1998. Geographic patterns of endemism and speciation in amphibians and reptiles of the Ryukyu Archipelago, Japan, with special reference to their paleogeographical implications. Researches on Population Ecology 40: 189–204.

    Article  Google Scholar 

  • Page, B. M. & J. Suppe, 1981. The pliocene lichi melange of Taiwan: its plate tectonic and olistostromal origin. American Journal of Science 281: 193–227.

    Article  Google Scholar 

  • Posada, D. & K. A. Crandall, 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818.

    Article  PubMed  CAS  Google Scholar 

  • Posada, D. & K. A. Crandall, 2001. Intraspecific gene genealogies: trees grafting into networks. Trends in Ecology and Evolution 16: 37–45.

    Article  PubMed  Google Scholar 

  • Rogers, A. R. & H. Harpending, 1992. Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9: 552–569.

    PubMed  CAS  Google Scholar 

  • Rozas, J., J. C. Sanchez-Delbarrio, X. Messeguer & R. Rozas, 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496–2497.

    Article  PubMed  CAS  Google Scholar 

  • Saitou, N. & M. Nei, 1987. The neighbour-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406–425.

    PubMed  CAS  Google Scholar 

  • Sambrook, J. & D. W. Russell, 2001. Molecular Cloning: A Laboratory Manual, 3rd ed. Cold Spring Harbor Laboratory Press, New York.

    Google Scholar 

  • Schneider, S. D., D. Roessli & L. Excoffier, 2000. ARLEQUIN, Version 2.0: A Software for Population Genetic Data Analysis. Genetics and Biometry Laboratory, University of Geneva, Geneva, Switzerland.

    Google Scholar 

  • Schubart, C. D., R. Diesel & S. B. Hedges, 1998. Rapid evolution to terrestrial life in Jamaican crabs. Nature 393: 363–365.

    Article  CAS  Google Scholar 

  • Shen, C., 1997. The Biogeography of Taiwan: 2. Some preliminary thoughts and studies. Annual Report of Taiwan Museum 40: 361–450. (in Chinese with English summary).

    Google Scholar 

  • Shih, H. T., P. K. L. Ng & H. W. Chang, 2004. Systematics of the genus Geothelphusa (Crustacea, Decapoda, Brachyura, Potamidae) from Southern Taiwan: a molecular appraisal. Zoological Studies 43: 561–570.

    Google Scholar 

  • Shih, H. T., H. C. Hung, C. D. Schubart, C. A. Chen & H. W. Chang, 2006. Intraspecific genetic diversity of the endemic freshwater crab Candidiopotamon rathbunae (Decapoda, Brachyura, Potamidae) reflects five million years of geological history of Taiwan. Journal of Biogeography 33: 980–989.

    Article  Google Scholar 

  • Shokita, S., 1977. Abbreviated metamorphosis of land-locked fresh-water prawn, Macrobrachium asperulum (Von Martens) from Taiwan. Annotations Zoologicae Japonenses 50: 110–122.

    Google Scholar 

  • Shokita, S., 1985. Larval development of the Palaemonid prawn, Macrobrachium grandimanus (Randall), reared in the laboratory, with special reference to larval dispersal. Zoological Studies 2: 785–803.

    Google Scholar 

  • Shokita, S., 1996. The origin of land-lock freshwater shrimps and Potamoids from the Ryukyu Island, southern Japan. Journal of Geography 105: 343–353 (in Japanese with English abstract).

    Google Scholar 

  • Sibuet, J. C. & S. K. Hsu, 1997. Geodynamics of the Taiwan arc–arc collision. Tectonophysics 274: 221–251.

    Article  Google Scholar 

  • Sibuet, J. C. & S. K. Hsu, 2004. How was Taiwan created? Tectonophysics 379: 159–181.

    Article  Google Scholar 

  • Simonsen, K. L., G. A. Churchill & C. F. Aquadro, 1995. Properties of statistical tests of neutrality for DNA polymorphism data. Genetics 141: 413–429.

    PubMed  CAS  Google Scholar 

  • Slatkin, M., 1993. Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47: 264–279.

    Article  Google Scholar 

  • Swofford, D. L., 2002. PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.

    PubMed  CAS  Google Scholar 

  • Tamura, K. & M. Nei, 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10: 512–526.

    PubMed  CAS  Google Scholar 

  • Toda, M., M. Nishida, M. Matsui, K. Y. Lue & H. Ota, 1998. Genetic variation in the Indian rice frog, Rana limnocharis (Amphibia: Anura), in Taiwan, as revealed by allozyme data. Herpetologica 54: 73–82.

    Google Scholar 

  • Tzeng, C. S., 1986. Distribution of the freshwater fishes of Taiwan. Journal of Taiwan Museum 39: 127–146.

    Google Scholar 

  • Tzeng, C. S., Y. S. Lin, S. M. Lin, T. Y. Wang & F. Y. Wang, 2006. The phylogeography and population demographics of selected freshwater fishes in Taiwan. Zoological Studies 45: 285–297.

    CAS  Google Scholar 

  • Wang, H. Y., M. P. Tsai, M. J. Yu & S. C. Lee, 1999. Influence of glaciation on divergence patterns of the endemic minnow, Zacco pachycaphalus, in Taiwan. Molecular Ecology 8: 1879–1888.

    Article  PubMed  CAS  Google Scholar 

  • Wang, J. P., K. C. Hsu & T. Y. Chiang, 2000. Mitochondrial DNA phylogeography of Acrossocheilus paradoxus (Cyprinidae) in Taiwan. Molecular Ecology 9: 1483–1494.

    Article  PubMed  CAS  Google Scholar 

  • Wang, J. P., H. D. Lin, S. Huang, C. H. Pan, X. L. Chen & T. Y. Chianga, 2004. Phylogeography of Varicorhinus barbatulus (Cyprinidae) in Taiwan based on nucleotide variation of mtDNA and allozymes. Molecular Phylogenetics and Evolution 31: 1143–1156.

    Article  PubMed  CAS  Google Scholar 

  • Wang, T. Y., C. S. Tzeng, H. Y. Teng & T. Chang, 2007. Phylogeography and identification of a 187-bp-long duplication within the mitochondrial control region of Formosania lacustre (Teleostei: Balitoridae). Zoological Studies 46: 569–582.

    CAS  Google Scholar 

  • Williams, S. T. & N. Knowlton, 2001. Mitochondrial pseudogenes are pervasive and often insidious in the snapping shrimp genus Alpheus. Molecular Biology and Evolution 18: 1484–1493.

    PubMed  CAS  Google Scholar 

  • Yu, H. T., 1995. Patterns of diversification and genetic population structure of small mammals in Taiwan. Biological Journal of the Linnean Society 55: 69–89.

    Article  Google Scholar 

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Acknowledgments

We thank Yi-Xiong Cai and Tohru Naruse for specimen collection. Tzi-Yuan Wang helped with data analyses. We particularly thank Hsi-Te Shih and Te-Yu Liao for specimen collection, data analyses, and discussions. Two anonymous reviewers who greatly improved this manuscript are also acknowledged.

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Correspondence to Min-Yun Liu.

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Handling editor: Christian Sturmbauer

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Liu, MY., Tzeng, CS. & Lin, HD. Phylogeography and the genetic structure of the land-locked freshwater prawn Macrobrachium asperulum (Crustacea: Decapoda: Palaemonidae) in Taiwan. Hydrobiologia 671, 1–12 (2011). https://doi.org/10.1007/s10750-011-0699-z

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