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Marine Biology

, Volume 160, Issue 6, pp 1395–1406 | Cite as

New insight on population genetic connectivity of widespread amphidromous prawn Macrobrachium lar (Fabricius, 1798) (Crustacea: Decapoda: Palaemonidae)

  • Magalie Castelin
  • Pierre Feutry
  • Mélyne Hautecoeur
  • Gérard Marquet
  • Daisy Wowor
  • Gabrielle Zimmermann
  • Philippe Keith
Original Paper

Abstract

Due to the sparse and unstable nature of insular freshwater habitats, marine larval dispersal of amphidromous species is considered a critical element of population persistence. We assessed population genetic structure of freshwater prawn Macrobrachium lar across its range that encompasses two biogeographic barriers: the vast open ocean separating Western and Central Pacific regions and the Indo-Malay archipelago separating Indian and Pacific oceans. A total of 173 samples collected from 21 islands throughout the Indo-Pacific were sequenced at 16S and 28S rDNA. We observed distinct genetic isolation of populations located at the eastern and southwestern edge of the species range but no evidence of an effect of the Indo-Pacific barrier. Differentiation patterns are consistent with a stepping-stone model of dispersal. Genetic differences of Central Pacific populations may reflect founder events associated with colonization of isolated islands, or be a signature of a past bottleneck after population depletion caused by drastic climatic events.

Keywords

Reef Fish Population Genetic Structure Haplotype Network Larval Dispersal Pelagic Larval Duration 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank all the partners that have financially supported this work: (1) the New Caledonian Government; (2) the Muséum national d’Histoire naturelle; (3) the Indonesian Institute of Sciences; (4) the ATM Barcode (PIs: Sarah Samadi and Jean-Noël Labat); and (5) the “Service de Systématique Moléculaire” (UMS 2700 CNRS-MNHN). This project was also supported by the network “Bibliothèque du Vivant” funded by the CNRS, the Muséum national d’Histoire naturelle, the INRA, and the CEA (Centre National de Séquençage). We thank the Vanuatu Environment Unit (D. Kalfatak) and the New Caledonian North and South Provinces (J-J. Cassan and C. Méresse) for allowing sampling (permit No 1224-08/PS), and ARDA (Association Réunionaise de Développement de l’Aquaculture) in Réunion Island for giving us samples. This study was made possible through assistance in sampling expeditions and field contact: P. Bosc, P. Gaucher, P. Gerbeaux, H. Grondin, R.K. Hadiaty, D. Kalfatak, G. MacCormack, N. Mary, J.Y. Meyer, Mulyadi, A. Mun’im, T. Robinet, S. Sauri, G. Ségura, L. Taillebois, P. Valade, and Wahyudin. We would like to thank C. Lord, B. Lynch, and C. Abbott for constructive comments and English improvement of the manuscript. We are grateful to the referees and to Timothy J. Page for their productive review of the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

All research presented in the manuscript was conducted in accordance with all applicable laws and rules set forth by their governments and institutions, and all necessary permits were in hand when the research was conducted.

References

  1. Atkinson JM (1977) Larval development of a freshwater prawn, Macrobrachium lar (Decapoda, Palaemonidae), reared in the laboratory. Crustaceana 33:119–132CrossRefGoogle Scholar
  2. Bandel K, Riedel F (1998) Ecological zonation of gastropods in the Matutinao River (Cebu, Philippines), with focus on their life cycles. Ann Limnol Int J Lim 34:171–191CrossRefGoogle Scholar
  3. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. http://www.fluxus-technology.com Google Scholar
  4. Benzie JAH (1998) Genetic structure of marine organisms and SE Asian biogeography. In: Hall R, Holloway JD (eds) Biogeography and Geological Evolution of SE Asia. Backhuys Publishers, Leiden, pp 197–209Google Scholar
  5. Berrebi P, Cattaneo-Berrebi G, Valade P, Ricou JF, Hoareau T (2005) Genetic homogeneity in eight freshwater populations of Sicyopterus lagocephalus, an amphidromous gobiid of La Réunion Island. Mar Biol 148:179–188CrossRefGoogle Scholar
  6. Bowen BW, Bass AL, Rocha LA, Grant WS, Robertson DR (2001) Phylogeography of the trumpetfishes (Aulostomus): ring species complex on a global scale. Evolution 55:1029–1039CrossRefGoogle Scholar
  7. Briggs JC (1974) Marine zoogeography. McGraw-Hill Companies, New YorkGoogle Scholar
  8. Chapman P, Marco SFD, Davis R, Coward A (2003) Flow at intermediate depths around Madagascar based on ALACE float trajectories. Deep Sea Res Part II 50:1957–1986CrossRefGoogle Scholar
  9. Chen RT, Tsai CF, Tzeng WN (2009) Freshwater prawns (Macrobrachium Bate, 1868) of Taiwan with special references to their biogeographical origins and dispersion routes. J Crustac Biol 29:232–244CrossRefGoogle Scholar
  10. Chubb AL, Zink RM, Fitzsimons JM (1998) Patterns of mtDNA variation in Hawaiian freshwater fishes: the phylogeographic consequences of amphidromy. J Hered 89:8–16CrossRefGoogle Scholar
  11. Cook BD, Bernays S, Pringle CM, Hughes JM (2009) Marine dispersal determines the genetic population structure of migratory stream fauna of Puerto Rico: evidence for island-scale population recovery processes. J North Am Benthol Soc 28:709–718CrossRefGoogle Scholar
  12. Crandall ED, Frey MA, Grosberg RK, Barber PH (2008) Contrasting demographic history and phylogeographical patterns in two Indo Pacific gastropods. Mol Ecol 17:611–626CrossRefGoogle Scholar
  13. Crandall E, Taffel J, Barber P (2010) High gene flow due to pelagic larval dispersal among South Pacific archipelagos in two amphidromous gastropods (Neritomorpha: Neritidae). Heredity 104:563–572CrossRefGoogle Scholar
  14. de Bruyn M, Mather PB (2007) Molecular signatures of Pleistocene sea-level changes that affected connectivity among freshwater shrimp in Indo-Australian waters. Mol Ecol 16:4295–4307CrossRefGoogle Scholar
  15. de Bruyn M, Wilson JA, Mather PB (2004a) Huxley’s line demarcates extensive genetic divergence between eastern and western forms of the giant freshwater prawn, Macrobrachium rosenbergii. Mol Phylogenet Evol 30:251–257CrossRefGoogle Scholar
  16. de Bruyn M, Wilson JC, Mather PB (2004b) Reconciling geography and genealogy: phylogeography of giant freshwater prawns from the Lake Carpentaria region. Mol Ecol 13:3515–3526CrossRefGoogle Scholar
  17. de Bruyn M, Nugroho E, Hossain MM, Wilson J, Mather P (2005) Phylogeographic evidence for the existence of an ancient biogeographic barrier: the Isthmus of Kra Seaway. Heredity 94:370–378CrossRefGoogle Scholar
  18. Dodson J, Colombani F, Ng P (1995) Phylogeographic structure in mitochondrial DNA of a South-east Asian freshwater fish, Hemibagrus nemurus (Siluroidei; Bagridae) and Pleistocene sea-level changes on the Sunda shelf. Mol Ecol 4:331–346CrossRefGoogle Scholar
  19. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefGoogle Scholar
  20. 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 131:479–491Google Scholar
  21. Feutry P, Castelin M, Ovenden JR, Dettaï A, Robinet T, Cruaud C, Keith P (2013a) Evolution of diadromy in fish: insights from a tropical genus (Kuhlia species). Am Nat 181:52–63CrossRefGoogle Scholar
  22. Feutry P, Vergnes A, Broderick D, Lambourdière JR, Keith P, Ovenden JR (2013b) Stretched to the limit; can a short pelagic larval duration connect adult populations of an Indo-Pacific diadromous fish (Kuhlia rupestris)? Mol Ecol 22:1518–1530Google Scholar
  23. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925Google Scholar
  24. Gaither MR, Toonen RJ, Robertson DR, Planes S, Bowen BW (2010) Genetic evaluation of marine biogeographical barriers: perspectives from two widespread Indo-Pacific snappers (Lutjanus kasmira and Lutjanus fulvus). J Biogeogr 37:133–147CrossRefGoogle Scholar
  25. Gaither MR, Bowen BW, Bordenave TR, Rocha LA, Newman SJ, Gomez JA, van Herwerden L, Craig MT (2011) Phylogeography of the reef fish Cephalopholis argus (Epinephelidae) indicates Pleistocene isolation across the Indo-Pacific Barrier with contemporary overlap in the Coral Triangle. BMC Evol Biol 11:189CrossRefGoogle Scholar
  26. Gamba A, Rodriguez G (1987) Migratory behavior of postlarval white, Penaeus Schmitti, and river shrimps, Macrobrachium acanthurus, in their zone of overlap in a tropical lagoon. Bull Mar Sci 40:454–463Google Scholar
  27. Gillespie RG, Claridge EM, Goodacre SL (2008) Biogeography of the fauna of French Polynesia: diversification within and between a series of hot spot archipelagos. Philos Trans R Soc B Biol Sci 363:3335–3346CrossRefGoogle Scholar
  28. 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
  29. Hassouna M, Michot B, Bachellerie J-P (1984) The complete nucleotide sequence of mouse 28SRNA gene. Implications for the process of size increase of the large subunit rRNA of higher eukaryotes. Nucleic Acids Res 12:3563–3583CrossRefGoogle Scholar
  30. Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913CrossRefGoogle Scholar
  31. Hodges MH, Allendorf FW (1998) Population genetics and pattern of larval dispersal of the endemic Hawaiian freshwater amphidromous gastropod Neritina granosa (Prosobranchia: Neritidae). Pac Sci 52:237–249Google Scholar
  32. Holthuis LB (1980) FAO species catalogue. Shrimps and prawns of the world, vol 1, Food and Agriculture Organization of the United Nations, Rome, ItalyGoogle Scholar
  33. Horne JB, Van Herwerden L, Choat JH, Robertson DR (2008) High population connectivity across the Indo-Pacific: congruent lack of phylogeographic structure in three reef fish congeners. Mol Phylogenet Evol 49:629–638CrossRefGoogle Scholar
  34. Jovelin R, Justine J-L (2001) Phylogenetic relationships within the Polyopisthocotylean monogeneans (Plathyhelminthes) inferred from partial 28S rDNA sequences. Int J Parasitol 31:393–401CrossRefGoogle Scholar
  35. Kano Y, Kase T (2003) Systematics of the Neritilia rubida complex (Gastropoda: Neritiliidae): three amphidromous species with overlapping distributions in the Indo-Pacific. J Molluscan Stud 69:273–284CrossRefGoogle Scholar
  36. Kano Y, Kase T (2004) Genetic exchange between anchialine cave populations by means of larval dispersal: the case of a new gastropod species Neritilia cavernicola. Zool Scr 33:423–437CrossRefGoogle Scholar
  37. Keith P (2003) Biology and ecology of amphidromous Gobiidae of the Indo-Pacific and the Caribbean regions. J Fish Biol 63:831–847CrossRefGoogle Scholar
  38. Keith P, Vigneux E, Bosc P (1999) Atlas des poissons et des crustaces d’eau douce de la Reunion. MNHN, Paris, FranceGoogle Scholar
  39. Keith P, Vigneux E, Marquet G (2002) Atlas des poissons et des crustacés d’eau douce de la Polynésie française. MNHN, Paris, FranceGoogle Scholar
  40. Keith P, Marquet G, Valade P, Bosc P, Vigneux E (2006) Atlas des poissons et des crustacés d’eau douce des Comores. Mascareignes et Seychelles, MNHN, Paris, FranceGoogle Scholar
  41. Keith P, Lord C, Lorion J, Watanabe S, Tsukamoto K, Couloux A, Dettai A (2011) Phylogeny and biogeography of Sicydiinae (Teleostei: Gobiidae) inferred from mitochondrial and nuclear genes. Mar Biol 158:311–326CrossRefGoogle Scholar
  42. Lavery S, Moritz C, Fielder D (1995) Changing patterns of population structure and gene flow at different spatial scales in Birgus latro (the coconut crab). Heredity 74:531–541CrossRefGoogle Scholar
  43. Lavery S, Moritz C, Fielder D (1996) Genetic patterns suggest exponential population growth in a declining species. Mol Biol Evol 13:1106–1113CrossRefGoogle Scholar
  44. Lessios H (1998) The first stage of speciation as seen in organisms separated by the Isthmus of Panama. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, OxfordGoogle Scholar
  45. Lohman DJ, de Bruyn M, Page T, von Rintelen K, Hall R, Ng PKL, Shih HT, Carvalho GR, von Rintelen T (2011) Biogeography of the Indo-Australian archipelago. Annu Rev Ecol Evol Syst 42:205–226CrossRefGoogle Scholar
  46. Lord C, Brun C, Hautecoeur M, Keith P (2010) Insights on endemism: comparison of the duration of the marine larval phase estimated by otolith microstructural analysis of three amphidromous Sicyopterus species (Gobioidei: Sicydiinae) from Vanuatu and New Caledonia. Ecol Freshw Fish 19:26–38CrossRefGoogle Scholar
  47. Lord C, Lorion J, Dettai A, Watanabe S, Tsukamoto K, Cruaud C, Keith P (2012) From endemism to widespread distribution: phylogeography of three amphidromous Sicyopterus species (Teleostei: Gobioidei: Sicydiinae). Mar Ecol Prog Ser 455:269–285CrossRefGoogle Scholar
  48. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220Google Scholar
  49. Marquet G, Keith P, Vigneux X (2003) Atlas des poissons et des crustacés d’eau douce de Nouvelle-Calédonie. MNHN, Paris, FranceGoogle Scholar
  50. McDowall R (2007) On amphidromy, a distinct form of diadromy in aquatic organisms. Fish Fish 8:1–13CrossRefGoogle Scholar
  51. Minegishi Y, Aoyama J, Tsukamoto K (2008) Multiple population structure of the giant mottled eel, Anguilla marmorata. Mol Ecol 17:3109–3122CrossRefGoogle Scholar
  52. Murphy CA, Cowan JH (2007) Production, marine larval retention or dispersal, and recruitment of amphidromous Hawaiian Gobioids: issues and implications. In: Evenhuis NL, Fitzsimons JM (eds) Biology of Hawaiian streams and estuaries. Bishop Museum Bulletin in Cultural and Environmental Studies, pp 63–74Google Scholar
  53. Muths D, Tessier E, Gouws G, Craig M, Mwale M, Mwaluma J, Mwandya A, Bourjea J (2011) Restricted dispersal of the reef fish Myripristis berndti at the scale of the SW Indian Ocean. Mar Ecol Prog Ser 443:167–180CrossRefGoogle Scholar
  54. Myers MJ, Meyer CP, Resh VH (2000) Neritid and thiarid gastropods from French Polynesian streams: how reproduction (sexual, parthenogenetic) and dispersal (active, passive) affect population structure. Freshw Biol 44:535–545CrossRefGoogle Scholar
  55. Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New YorkGoogle Scholar
  56. Nichols R (2001) Gene trees and species trees are not the same. Trends Ecol Evol 16:358–364CrossRefGoogle Scholar
  57. Page TJ, von Rintelen K, Hughes JM (2007) An island in the stream: Australia’s place in the cosmopolitan world of Indo-West Pacific freshwater shrimp (Decapoda: Atyidae: Caridina). Mol Phylogenet Evol 43:645–659CrossRefGoogle Scholar
  58. Page TJ, Torati LS, Cook BD, Binderup A, Pringle CM, Reuschel S, Schubart CD, Hughes JM (2013) Invertébrés sans frontières: large scales of connectivity of selected freshwater species among Caribbean Islands. Biotropica 45:236–244Google Scholar
  59. Palumbi SR (1996) Nucleic acids II: the polymerase chain reaction. In: Hillis DM, Mable BK, Moritz C (eds) Molecular systematics. Sinauer Associates, Sunderland, pp 205–247Google Scholar
  60. Palumbi SR, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR. Version 2. Department of Zoology and Kewalo Marine Laboratory. University of Hawaii, Honolulu, USAGoogle Scholar
  61. Palumbi SR, Grabowsky G, Duda T, Geyer L, Tachino N (1997) Speciation and population genetic structure in tropical Pacific sea urchins. Evolution 51:1506–1517Google Scholar
  62. Paula J (1998) Larval retention and dynamics of the prawns Palaemon longirostris H. Milne Edwards and Crangon crangon Linnaeus (Decapoda, Caridea) in the Mira estuary, Portugal. Invertebr Reprod Dev 33:221–228CrossRefGoogle Scholar
  63. Planes S, Fauvelot C (2002) Isolation by distance and vicariance drive genetic structure of a coral reef fish in the Pacific Ocean. Evolution 56:378–399Google Scholar
  64. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  65. Read GHL (1986) A surface response analysis of the role of salinity in the development of larval and post larval Macrobrachium petersi (Hilgendorf). Comp Biochem Phys A 84:159–168CrossRefGoogle Scholar
  66. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228Google Scholar
  67. Rousset F, Raymond M (1997) Statistical analyses of population genetic data: new tools, old concepts. Trends Ecol Evol 12:313–317CrossRefGoogle Scholar
  68. Shokita S (1979) The distribution and speciation of the inland water shrimps and prawns from the Ryukyu Islands-II. Bull Coll Sci Univ Ryukyus 28:193–278Google Scholar
  69. Short J (2004) A revision of Australian river prawns, Macrobrachium (Crustacea: Decapoda: Palaemonidae). Hydrobiologia 525:1–100CrossRefGoogle Scholar
  70. Slatkin M (1985) Rare alleles as indicators of gene flow. Evolution 39:53–65CrossRefGoogle Scholar
  71. Smith GC, Covich AP, Brasher AMD (2003) An ecological perspective on the biodiversity of tropical island streams. Bioscience 53:1048–1051CrossRefGoogle Scholar
  72. Sponaugle S, Cowen RK, Shanks A, Morgan SG, Leis JM, Pineda J, Boehlert GW, Kingsford MJ, Lindeman KC, Grimes C (2002) Predicting self-recruitment in marine populations: biophysical correlates and mechanisms. Bull Mar Sci 70:341–375Google Scholar
  73. Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460Google Scholar
  74. Voris HK (2001) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167CrossRefGoogle Scholar
  75. Waters JM, Dijkstra LH, Wallis GP (2000) Biogeography of a southern hemisphere freshwater fish: how important is marine dispersal? Mol Ecol 9:1815–1821CrossRefGoogle Scholar
  76. Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276CrossRefGoogle Scholar
  77. White C, Selkoe KA, Watson J, Siegel DA, Zacherl DC, Toonen RJ (2010) Ocean currents help explain population genetic structure. Proc Roy Soc B Biol Sci 277:1685–1694CrossRefGoogle Scholar
  78. Winters KL, van Herwerden L, Choat JH, Robertson D (2010) Phylogeography of the Indo-Pacific parrotfish Scarus psittacus: isolation generates distinctive peripheral populations in two oceans. Mar Biol 157:1679–1691CrossRefGoogle Scholar
  79. Wowor D (2012) Krustasea di kawasan karst Gunungsewu dan Menoreh. Puslit Biologi-LIPI, BKSDA Yogyakarta & Yayasan Kanopi, IndonesiaGoogle Scholar
  80. Wowor D, Muthu V, Meier R, Balke M, Cai Y, Ng PKL (2009) Evolution of life history traits in Asian freshwater prawns of the genus Macrobrachium (Crustacea: Decapoda: Palaemonidae) based on multilocus molecular phylogenetic analysis. Mol Phylogenet Evol 52:340–350CrossRefGoogle Scholar
  81. Wright S (1949) The genetical structure of populations. Ann Hum Genet 15:323–354. doi: 10.1111/j.1469-1809.1949.tb02451.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Magalie Castelin
    • 1
    • 2
  • Pierre Feutry
    • 1
    • 3
  • Mélyne Hautecoeur
    • 1
  • Gérard Marquet
    • 1
  • Daisy Wowor
    • 4
  • Gabrielle Zimmermann
    • 1
  • Philippe Keith
    • 1
  1. 1.Biologie des Organismes et Ecosystèmes Aquatiques, UMR 7208, Département Milieux et Peuplements AquatiquesMuséum national d’Histoire naturelleParis Cedex 05France
  2. 2.Fisheries and Oceans CanadaNanaimoCanada
  3. 3.Research Institute for Environment and LivelihoodsCharles Darwin UniversityDarwinAustralia
  4. 4.Division of Zoology, Research Center for BiologyIndonesian Institute of Sciences (LIPI)CibinongIndonesia

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