Biological Invasions

, 12:253 | Cite as

High regional differentiation in a North American crab species throughout its native range and invaded European waters: a phylogeographic analysis

  • Joana Projecto-Garcia
  • Henrique Cabral
  • Christoph D. Schubart
Original Paper


Rhithropanopeus harrisii (Gould 1841) has a native distribution from New Brunswick (Canada) to Veracruz (Mexico) and is considered an invasive species in northwestern North American (Oregon and California), South American (Brazil) and European estuaries and rivers. In Europe, it was observed for the first time in 1874, in The Netherlands. We sequenced and analyzed part of the cytochrome oxidase subunit I gene (mitochondrial DNA) of eight populations, three from the east coast of the United States of America (USA) and five from Europe, in order to assess their genetic diversity and to determine a potential founder population. European populations are characterized by a lower number of haplotypes than the whole native region of the eastern USA, suggesting that genetic bottlenecks occurred during the European colonisation. Along the North American East Coast, there is evidence of clearcut genetic heterogeneity, New Jersey being the most similar population in its genetic structure to the postulated Europe-founding population. Also the different European populations are heterogeneous and there is a tendency of higher genetic diversity in the populations founded earlier. R. harrisii is still in the process of expansion in Europe and may have been introduced once or repeatedly by different invasion mechanisms. The pronounced lack of gene flow among populations is of great ecological significance, since it may facilitate rapid adaptation and specialization to local conditions within single estuarine systems.


Rhithropanopeus harrisii Invasive species mtDNA diversity Genetic bottleneck Population isolation Larval retention 



We would like to thank F. Martinho, J. P. Domingues, N. R. Duarte, C. Fidalgo, R. Ribeiro and F. Gonçalves for helping with the sampling in the Mondego estuary (Portugal); C. d’Udekem d’Acoz, J. A. Cuesta, R. Forward, P. Jivoff, L. Mizzan, M. Normant, S. Algarín Vélez and S. Uzumov for their help with sampling European and North American populations; C. Petersen for making available additional sequence information; R. Jesse, T. Santl, S. Klaus L. Heine and P. Koller for advice and support; S. Reuschel, I. Silva and A. I. Catarino for statistical discussions; N. T. Goulart and M. Bruneaux for figures enhancements; J. Heinze and the entire group from Biologie 1, Universität Regensburg for making this study possible in every way and to the Deutscher Akademischer Austausch Dienst (DAAD) for the financial support. The authors would like also to acknowledge the comments of two anonymous reviewers that greatly improved this manuscript.


  1. Alvarez F, Hines AH, Reaka-Kudla ML (1995) The effects of parasitism by the barnacle Loxothylacus panopaei (Gissler) (Cirripedia: Rhizocephala) on growth and survival of the host crab Rhithropanopeus harrisii (Gould) (Brachyura: Xanthidae). J Exp Mar Biol Ecol 192:221–232. doi: 10.1016/0022-0981(95)00068-3 CrossRefGoogle Scholar
  2. Arzul I, Renault T, Thébault A, Gérard A (2002) Detection of oyster herpesvirus DNA and proteins in asymptomatic Crassostrea gigas adults. Virus Res 84:151–160. doi: 10.1016/S0168-1702(02)00007-2 CrossRefPubMedGoogle Scholar
  3. Avise JC (2004) Molecular markers, natural history and evolution. Sinauer Associates, SuderlandGoogle Scholar
  4. Briggs JC (1974) Marine zoogeography. McGraw-Hill, New YorkGoogle Scholar
  5. Cabral HN, Costa MJ (1999) On the occurrence of the Chinese mitten crab, Eriocheir sinensis, in Portugal (Decapoda, Brachyura). Crustac 72:55–58Google Scholar
  6. Carlton JT (1985) Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanogr Mar Biol Annu Rev 23:313–371Google Scholar
  7. Christiansen ME (1969) Crustacea Decapoda Brachyura. Marine invertebrates of Scandinavia, vol 2. Universitetsforlaget, OsloGoogle Scholar
  8. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659. doi: 10.1046/j.1365-294x.2000.01020.x CrossRefPubMedGoogle Scholar
  9. Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–558. doi: 10.1126/science.279.5350.555 CrossRefPubMedGoogle Scholar
  10. Cripe GM, McKenney CL Jr, Hoglund MD, Harris PS (2003) Effects of fenoxycarb exposure on complete larval development of the xanthid crab, Rhithropanopeus harrisii. Environ Pollut 125:295–299. doi: 10.1016/S0269-7491(02)00414-1 CrossRefPubMedGoogle Scholar
  11. Cronin TW (1982) Estuarine retention of larvae of the crab Rhithropanopeus harrisii. Estuar Coast Mar Sci 15:207–220Google Scholar
  12. Cronin TW, Forward RB Jr (1986) Vertical migration cycles of crab larvae and their role in larval dispersal. Bull Mar Sci 39:192–201Google Scholar
  13. Cuesta JA, García-Raso JE, González JI (1991) Primera cita de Rhithropanopeus harrisii (Gould, 1841) (Crustacea, Decapoda, Brachyura, Xanthidae) en la Península Ibérica. Boll Inst Esp Oceanogr 7:149–153Google Scholar
  14. Excoffier L, Laval G, Schneider S (2005) Arlequin ver 3.0—an integrated software package for population genetics data analysis. Computational and Molecular Genetics Lab, Institute of Zoology, University of Berne, BerneGoogle Scholar
  15. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedGoogle Scholar
  16. Galil B, Froglia C, Noel P (2002) CIESM atlas of exotic species in the Mediterranean 2. Crustaceans: decapods and stomatopods. CIESM Publishers, MonacoGoogle Scholar
  17. Gonçalves F, Ribeiro R, Soares AMVM (1995) Rhithropanopeus harrisii (Gould), an American crab in the estuary of the Mondego River, Portugal. J Crustac Biol 15:756–762. doi: 10.2307/1548824 CrossRefGoogle Scholar
  18. Grosholz E (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17:22–27. doi: 10.1016/S0169-5347(01)02358-8 CrossRefGoogle Scholar
  19. Grosholz ED, Ruiz GM (1995) Does spatial heterogeneity and genetic variation in populations of the xanthid crab Rhithropanopeus harrisii (Gould) influence the prevalence of an introduced parasitic castrator? J Exp Mar Biol Ecol 187:129–145. doi: 10.1016/0022-0981(94)00175-D CrossRefGoogle Scholar
  20. 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
  21. Hänfling B, Carvalho GR, Brandl R (2002) mt-DNA sequences and possible invasion pathways of the Chinese mitten crab. Mar Ecol Prog Ser 238:307–310. doi: 10.3354/meps238307 CrossRefGoogle Scholar
  22. Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600PubMedGoogle Scholar
  23. Harpending HC, Sherry ST, Rogers AR, Stoneking M (1993) The genetic structure of ancient human populations. Curr Anthropol 34:483–496. doi: 10.1086/204195 CrossRefGoogle Scholar
  24. ICES (2005) Vector pathways and the spread of exotic species in the sea, ICES cooperative research report, No. 271Google Scholar
  25. Kirby MX (2004) Fishing down the coast: historical expansion and collapse of oyster fisheries along continental margins. Proc Natl Acad Sci USA 101:13096–13099. doi: 10.1073/pnas.0405150101 CrossRefPubMedGoogle Scholar
  26. Knowlton N, Weigt LA (1998) New dates and new rates for divergence across the isthmus of panama. Proc R Soc Lond B Biol Sci 265:2257–2263. doi: 10.1098/rspb.1998.0568 CrossRefGoogle Scholar
  27. Knowlton N, Weigt LA, Solorzano LA, Mills DK, Bermingham E (1993) Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the isthmus of panama. Science 260:1629–1632. doi: 10.1126/science.8503007 CrossRefPubMedGoogle Scholar
  28. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391. doi: 10.1016/S0169-5347(02)02554-5 CrossRefGoogle Scholar
  29. Marck MC, D’Antonio CM (1998) Impacts of biological invasions on disturbance regimes. Trends Ecol Evol 13:195–198. doi: 10.1016/S0169-5347(97)01286-X CrossRefGoogle Scholar
  30. Mathews LM, Schubart CD, Neigel JE, Felder DL (2002) Genetic, ecological, and behavioural divergence between two sibling snapping shrimp species (Crustacea: Decapoda: Alpheus). Mol Ecol 11:1427–1437. doi: 10.1046/j.1365-294X.2002.01539.x CrossRefPubMedGoogle Scholar
  31. Mizzan L (1999) Le specie alloctone del macrozoobenthos della laguna di Venezia: il punto della situazione. Boll Mus Civ Storio Nat Venezia 49:145–177Google Scholar
  32. Mizzan L, Zanella L (1996) First record of Rhithropanopeus harrisii (Gould, 1841) (Crustacea, Decapoda, Xanthidae) in the Italian water. Boll Mus Civ Storio Nat Venezia 46:109–120Google Scholar
  33. Müller J (2001) Invasion history and genetic population structure of riverine macroinvertebrates. Zool Jena 104:346–355. doi: 10.1078/0944-2006-00040 CrossRefGoogle Scholar
  34. Nehring S (2000) Zur Bestandssituation von Rhithropanopeus harrisii (Gould, 1841) in deutschen Gewässern: die sukzessive Ausbreitung eines amerikanischen Neozoons (Crustacea: Decapoda: Panopeidae). Senckenberg marit 30:115–122CrossRefGoogle Scholar
  35. Nehring S (2001) After the TBT era: alternative anti-fouling paints and their ecological risks. Senckenberg marit 31:341–351CrossRefGoogle Scholar
  36. Nehring S (2005) International shipping—a risk for aquatic biodiversity in Germany. In: Nentwig W, Bacher S, Cock M, Dietz HJ, Gigon A, Wittenberg R (eds) Biological invasions—from ecology to control. NEOBIOTA 6, Prague, pp 125–143Google Scholar
  37. Neubert MG, Kot M, Lewis MA (2000) Invasion speeds in fluctuating environments. Proc R Soc Lond B Biol Sci 267:1603–1610. doi: 10.1098/rspb.2000.1185 CrossRefGoogle Scholar
  38. Payen GG, Bonami JR (1979) Mise en evidence de particles d’allure virale associees aux noyaux des cellules mesodermiques de la zone germinative testiculaire du crabe Rhithropanopeus harrisii (Gould) (Brachyoure, Xanthide). Rev Trav Inst Peches Mar 43:361–365Google Scholar
  39. Petersen C (2006) Range expansion in the northeast Pacific by an estuary mud crab—a molecular study. Biol Invasions 8:565–576. doi: 10.1007/s10530-005-0160-1 CrossRefGoogle Scholar
  40. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818. doi: 10.1093/bioinformatics/14.9.817 CrossRefPubMedGoogle Scholar
  41. Reeb CA, Avise JC (1990) A genetic discontinuity in a constinuously distributed species: mitochondrial DNA in the American oyster, Crassostrea virginica. Genetics 124:397–406PubMedGoogle Scholar
  42. Renault T (1998) Infections herpétiques chez les invertébrés: détection de virus de type herpès chez les mollusques bivalves marins. Virology 2:401–403Google Scholar
  43. Reuschel S, Schubart CD (2006) Phylogeny and geographic differentiation of Atlanto-Mediterranean species of the genus Xantho (Crustacea: Brachyura: Xanthidae) based on genetic and morphometric analyses. Mar Biol (Berl) 148:853–866. doi: 10.1007/s00227-005-0095-1 CrossRefGoogle Scholar
  44. Roche D, Torchin M (2007) Established population of the North American Harris mud crab, Rhithropanopeus harrisii (Gould 1841)(Crustacea: Brachyura: Xanthidae) in the Panama Canal. Aquat Invasions 2:155–161CrossRefGoogle Scholar
  45. Rodríguez G, Suárez H (2001) Anthropogenic dispersal of decapod crustaceans in aquatic environments. Interciencia 26:282–289Google Scholar
  46. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  47. Roman J, Palumbi SR (2004) A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Mol Ecol 13:2891–2898. doi: 10.1111/j.1365-294X.2004.02255.x CrossRefPubMedGoogle Scholar
  48. Rozas J, Rozas R (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175. doi: 10.1093/bioinformatics/15.2.174 CrossRefPubMedGoogle Scholar
  49. Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089PubMedGoogle Scholar
  50. Schubart C, Diesel R, Hedges SB (1998) Rapid evolution to terrestrial life in Jamaican crabs. Nature 393:363–365. doi: 10.1038/30724 CrossRefGoogle Scholar
  51. Schubart CD, Neigel JE, Felder DL (2000) Use of the mitochondrial 16S rRNA gene for phylogenetic and population studies of Crustacea. Crustac Issues 12:817–830Google Scholar
  52. Shields JD, Behringer DC Jr (2004) A new pathogenic virus in the Caribbean spiny lobster Palinurus argus from the Florida keys. Dis Aquat Organ 59:109–118. doi: 10.3354/dao059109 CrossRefPubMedGoogle Scholar
  53. Slatkin M, Hudson RR (1991) Pairwise comparisons of mithochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562PubMedGoogle Scholar
  54. Stachowicz JJ, Whitlatch RB, Osman RW (1999) Species diversity and invasion resistance in a marine ecosystem. Science 286:1577–1579. doi: 10.1126/science.286.5444.1577 CrossRefPubMedGoogle Scholar
  55. Tajima F (1989a) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  56. Tajima F (1989b) The effect of change in population size on DNA polymorphism. Genetics 123:597–601PubMedGoogle Scholar
  57. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonucleases mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633PubMedGoogle Scholar
  58. Wolff T (1954) Occurence of two East American species of crabs in European waters. Nature 174(4421):188–189. doi: 10.1038/174188a0 CrossRefGoogle Scholar
  59. Yamada SB, Dumbauld BR, Kalin A, Hunt CE, Figlar-Barnes R, Randall A (2005) Growth and persistence of a recent invader Carcinus maenas in estuaries of the northeastern Pacific. Biol Invasions 7:309–321. doi: 10.1007/s10530-004-0877-2 CrossRefGoogle Scholar
  60. Young AM, Torres C, Mack JE, Cunningham CW (2002) Morphological and genetic evidence for vicariance and refugium in Atlantic and Gulf of Mexico populations of the hermit crab Pagurus longicarpus. Mar Biol (Berl) 140:1059–1066. doi: 10.1007/s00227-002-0780-2 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Joana Projecto-Garcia
    • 1
    • 2
  • Henrique Cabral
    • 3
  • Christoph D. Schubart
    • 1
  1. 1.Biologie IUniversität RegensburgRegensburgGermany
  2. 2.Équipe de Ecophysiologie/GAMEStation Biologique de RoscoffRoscoff CedexFrance
  3. 3.Instituto de OceanografiaFaculdade de Ciências da Universidade de LisboaLisboaPortugal

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