, Volume 125, Issue 2–3, pp 155–171 | Cite as

Population Genetics and Identity of an Introduced Terrestrial Slug: Arion subfuscus s.l. in the North-east USA (Gastropoda, Pulmonata, Arionidae)

  • Jan PinceelEmail author
  • Kurt Jordaens
  • Natalie Van Houtte
  • Gary Bernon
  • Thierry Backeljau


Several European species of the terrestrial slug genus Arion have been introduced into North America. A case in point is the species complex A. subfuscus s.l. which has become one of the most abundant slug taxa in North America. In Europe this complex consists of at least two cryptic species, viz. A. fuscus and A. subfuscus s.s., the latter of which is further subdivided in five strongly divergent mtDNA lineages (A. subfuscus S1–S5). In order to determine which of these A. subfsucus s.l. taxa are present in the NE USA and in order to assess their population genetic structure, we compared mtDNA, nDNA and allozyme variation between populations from the NE USA and Europe. Our results show that (1) at least A. subfuscus S1 has become successfully established in the NE USA, (2) founder effects are the most likely explanation for the loss of a large amount of molecular genetic variation in populations from the NE USA (i.e. a loss of 96% of the 16S rDNA haplotypes, 67% of the ITS1 alleles and 46% of the alleles at polymorphic allozyme loci), and (3) part of the remaining genetic variation in NE USA populations was probably due to multiple introductions from the British Isles and the European mainland, and the hybrid structure of most of these source populations. Apparently, the extreme loss of molecular genetic variation in this introduced species has not prevented it from successfully establishing and spreading in novel environments.


allozymes Arion subfuscus Europe founder effects Gastropoda invasive species ITS1 16S rDNA terrestrial slug USA 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Albrectsen, B.R., Gardfjell, H., Orians, C.M., Murray, B., Fritz, R.S. 2004Slugs, willow seedlings and nutrient fertilization: intrinsic vigor inversely affects palatabilityOikos105268278CrossRefGoogle Scholar
  2. Aldridge, D.C., Elliott, P., Moggridge, G.D. 2004The recent and rapid spread of the zebra mussel (Dreissena polymorpha) in Great BritainBiol. Conserv119253261CrossRefGoogle Scholar
  3. Allendorf, F.W., Lundquist, L.L. 2003Introduction: population biology, evolution, nd control of invasive speciesConserv. Biol172430CrossRefGoogle Scholar
  4. Backeljau, T., Ahmadyar, S.Z., Selens, M., Rompaey, J., Verheyen, W. 1987Comparative electrophoretic analyses of three European Carinarion species (Mollusca, Pulmonata, Arionidae)Zool. Scr16209222CrossRefGoogle Scholar
  5. Baudouin, L., Lebrun, P. 2000An operational Bayesian approach for the identification of sexually reproduced cross-fertilized populations using molecular markersActa Horticultura5468194Google Scholar
  6. Bousset, L., Henry, P.Y., Sourrouille, P., Jarne, P. 2004Population biology of the invasive freshwater snail Physa acuta approached through genetic markers, ecological characterization and demographyMol. Ecol1320232036CrossRefPubMedGoogle Scholar
  7. Buddo, D.S., Steele, R.D., D’Oyen, E.R. 2003Distribution of the invasive indo-pacific green mussel, Perna viridis, in Kingston Harbour, JamaicaBull. Mar. Sci73433441Google Scholar
  8. Chichester, L.F., Getz, L.L. 1969The zoogeography and ecology of arionid and limacid slugs introduced into northeastern North AmericaMalacologia7313346Google Scholar
  9. Chichester, L.F., Getz, L.L. 1973The terrestrial slugs of northeastern North AmericaSterkiana511142Google Scholar
  10. Collins, T.M., Trexler, J.C., Nico, L.G., Rawlings, T.A. 2002Genetic diversity in a morphologically conservative invasive taxon: multiple introductions of swamp eels to the Southeastern United StatesConserv. Biol1610241035CrossRefGoogle Scholar
  11. Cowie, R.H. 1996New records of introduced land and freshwater snails in the Hawaiian IslandsBishop Mus. Occ. Pap462527Google Scholar
  12. Ellstrand, N.C., Schierenbeck, K.A. 2000Hybridization as a stimulus for the evolution of invasiveness in plants?Proc. Natl. Acad. Sci. USA9770437050CrossRefPubMedGoogle Scholar
  13. Facon, B., Pointier, J.P., Glaubrecht, M., Poux, C., Jarne, P., David, P. 2003A molecular phylogeography approach to biological invasions of the New World by parthenogenetic Thiarid snailsMol. Ecol1230273039CrossRefPubMedGoogle Scholar
  14. Felsenstein, J. 1985Confidence-limits on phylogenies – an approach using the bootstrapEvolution39783791Google Scholar
  15. Ferguson, S.H. 2004Effects of poisoning nonindigenous slugs in a boreal forestCan. J. Forest Res34449455CrossRefGoogle Scholar
  16. Foltz, D.W., Ochman, H., Jones, J.S., Evangelisti, S.M., Selander, R.K. 1982Genetic population structure and breeding systems in arionid slugs (Mollusca: Pulmonata)Biol. J. Linn. Soc17225241Google Scholar
  17. Foltz, D.W., Ochman, H., Selander, R.K. 1984Genetic diversity and breeding systems in terrestrial slugs of the families Limacidae and ArionidaeMalacologia25593605Google Scholar
  18. Fritz, R.S., Hochwender, C.G., Lewkiewicz, D.A., Bothwell, S., Orians, C.M. 2001Seedling herbivory by slugs in a willow hybrid system: developmental changes in damage, chemical defense, and plant performanceOecologia1298797CrossRefGoogle Scholar
  19. Geenen, S., Jordaens, K., Castilho, R., Backeljau, T. 2003Congruence between starch gel and polyacrylamide gel electrophoresis in detecting allozyme variation in land slugsElectrophoresis24622627CrossRefPubMedGoogle Scholar
  20. Glen, D.M., Moens, R. 2002Agriolimacidae, Arionidae and Milacidae as pests in West European cerealsBarker, G.M. eds. Molluscs as Crop PestsCABI PublishingOxon, UK271300Google Scholar
  21. Goudet, J. 1995FSTAT (Version 1.2): A computer program to calculate F-statisticsJ. Hered.86485486Google Scholar
  22. Grewal, S.K., Grewal, P.S., Hammond, R.B. 2003Susceptibility of North American native and non-native slugs (Mollusca: Gastropoda) to Phasmarhabditis hermaphrodita (Nematoda: Rhabditidae)Biocontrol Sci. Techn13119125CrossRefGoogle Scholar
  23. Guo, S.W., Thompson, E.A. 1992Performing the exact test of Hardy–Weinberg proportion for multiple allelesBiometrics48361372PubMedGoogle Scholar
  24. Hammond, R.B., Byers, R.A. 2002Agriolimacidae and Arionidae as pests in conservation tillage soybean and maize cropping in North AmericaBarker, G.M. eds. Molluscs as Crop PestsCABI PublishingOxon, UK301314Google Scholar
  25. Harris,  H. , Hopkinson, D. A. 1976 Handbook of Enzyme Electrophoresis in Human GeneticsNorth Holland Publishing Co.OxfordGoogle Scholar
  26. Heuertz, M., Hausman, J.F., Hardy, O.J., Vendramin, G.G., Frascaria-Lacoste, N., Vekemans, X. 2004Nuclear microsatellites reveal contrasting patterns of genetic structure between western and southeastern European populations of the common ash (Fraxinus excelsior L.)Evolution58976988PubMedGoogle Scholar
  27. Hillis, D.M., Dixon, M.T. 1991Ribosomal DNA – molecular evolution and phylogenetic inferenceQ. Rev. Biol.66410453CrossRefGoogle Scholar
  28. Holland, B.S. 2001Invasion without a bottleneck: microsatellite variation in natural and invasive populations of the brown mussel Perna perna (L)Mar. Biotech.3407415CrossRefGoogle Scholar
  29. Hommay, G. 2002Agriolimacidae, Arionidae and Milacidae as pests in West European sunflower and maizeBarker, G.M. eds. Molluscs as Crop PestsCABI PublishingOxon, UK245254Google Scholar
  30. Huelsenbeck, J.P., Ronquist, F., Nielsen, R., Bollback, J.P. 2001Bayesian inference of phylogeny and its impact on evolutionary biologyScience29423102314CrossRefPubMedGoogle Scholar
  31. Jarne, P., Charlesworth, D. 1993The evolution of the selfing rate in functionally hermaphrodite plants and animalsAnnu. Rev. Ecol. Syst.24441466CrossRefGoogle Scholar
  32. Jordaens, K., Riel, P., Geenen, S., Verhagen, R., Backeljau, T. 2001Food-induced body pigmentation questions the taxonomic value of colour in the self-fertilizing slug Carinarion sppJ. Moll. Stud.67161167CrossRefGoogle Scholar
  33. Kerney, M.P., Cameron, R.A.D. , Jungbluth,  J.H. 1983Die Landschnecken Nord- und MitteleuropasPaul PareyHamburgGoogle Scholar
  34. Kolar, C.S., Lodge, D.M. 2001Progress in invasion biology: predicting invadersTrends Ecol. Evol.16199204CrossRefPubMedGoogle Scholar
  35. Kolbe, J.J., Glor, R.E., Schettino, L.R.G., Lara, A.C., Larson, A., Losos, J.B. 2004Genetic variation increases during biological invasion by a Cuban lizardNature431177181CrossRefPubMedGoogle Scholar
  36. Kumar, S., Tamura, K., Jakobsen, I.B., Nei, M. 2001MEGA2: molecular evolutionary genetics analysis softwareBioinformatics1712441245CrossRefPubMedGoogle Scholar
  37. Lee, C.E. 2002Evolutionary genetics of invasive speciesTrends Ecol. Evol.17386391CrossRefGoogle Scholar
  38. Levin, D.A. 2003Ecological speciation: lessons from invasive speciesSyst. Bot.28643650Google Scholar
  39. McCarthy , C., 1996. Chromas. Queensland, AustraliaGoogle Scholar
  40. McCracken, G.F., Selander, R.K. 1980Self-fertilization and monogenic strains in natural populations of terrestrial slugsProc. Natl. Acad. Sci. USA77684688Google Scholar
  41. Nei, M. 1978Estimation of average heterozygosity and genetic distance from a small number of individualsGenetics89583590Google Scholar
  42. Nystrand, O., Granström, A. 2000Predation on Pinus sylvestris seeds and juvenile seedlings in Swedish boreal forest in relation to stand disturbance by loggingJ. Appl. Ecol.37449463CrossRefGoogle Scholar
  43. Parker, H.G., Kim, L.V., Sutter, N.B., Carlson, S., Lorentzen, T.D., Malek, T.B., Johnson, G.S., DeFrance, H.B., Ostrander, E.A., Kruglyak, L. 2004Genetic structure of the purebred domestic dogScience30411601164CrossRefPubMedGoogle Scholar
  44. Petit, R.J. 2004Biological invasions at the gene levelDiv. Dist.10159165CrossRefGoogle Scholar
  45. Petit, R.J., Bialozyt, R., Garnier-Gere, P., Hampe, A. 2004Ecology and genetics of tree invasions: from recent introductions to Quaternary migrationsForest Ecol. Manage.197117137CrossRefGoogle Scholar
  46. Pfenninger, M., Reinhardt, F., Streit, B. 2002Evidence for cryptic hybridization between different evolutionary lineages of the invasive clam genus Corbicula (Veneroida, Bivalvia)J. Evol. Biol.15818829CrossRefGoogle Scholar
  47. Pimentel, D., Lach, L., Zuniga, R., Morrison, D. 2000Environmental and economic costs of nonindigenous species in the United StatesBioscience505365Google Scholar
  48. Pinceel, J., K. Jordaens & T. Backeljau, 2005. Extreme mtDNA divergences in a terrestrial slug (Arionidae, Pulmonata, Gastropoda): accelerated evolution, allopatric divergence and secondary contact. J. Evol. Biol., in pressGoogle Scholar
  49. Pinceel, J., Jordaens, K., Pfenninger, M., Backeljau, T. 2005Rangewide phylogeography of a terrestrial slug in Europe: evidence for Alpine refugia and rapid colonization after the Pleistocene glaciationsMol. Ecol.1411331150CrossRefPubMedGoogle Scholar
  50. Pinceel, J., Jordaens, K., Houtte, N., Winter, A.J., Backeljau, T. 2004Molecular and morphological data reveal cryptic taxonomic diversity in the terrestrial slug complex Arion subfuscus/fuscus (Mollusca, Pulmonata, Arionidae) in continental north-west EuropeBiol. J. Linn. Soc.832338CrossRefGoogle Scholar
  51. Piry, S., Alapetite, A., Cornuet, J.M., Paetkau, D., Baudouin, L., Estoup, A. 2004GENECLASS2: a software for genetic assignment and first-generation migrant detectionJ. Hered.95536539CrossRefPubMedGoogle Scholar
  52. Posada, D., Crandall, K.A. 1998MODELTEST: testing the model of DNA substitutionBioinformatics14817818CrossRefPubMedGoogle Scholar
  53. Pritchard, J.K., Stephens, M., Donnelly, P. 2000Inference of population structure using multilocus genotype dataGenetics155945959PubMedGoogle Scholar
  54. Raymond, M., Rousset, F. 1995Genepop (version-1.2) – population-genetics software for exact tests and ecumenicismJ. Hered.86248249Google Scholar
  55. Renard, E., Bachmann, V., Cariou, M.L., Moreteau, J.C. 2000Morphological and molecular differentiation of invasive freshwater species of the genus Corbicula (Bivalvia, Corbiculidea) suggest the presence of three taxa in French riversMol. Ecol.920092016CrossRefPubMedGoogle Scholar
  56. Ricciardi, A. 2003Predicting the impacts of an introduced species from its invasion history: an empirical approach applied to zebra mussel invasionsFreshw. Biol.48972981CrossRefGoogle Scholar
  57. Rice, W.R. 1989Analyzing tables of statistical testsEvolution43223225Google Scholar
  58. Rilov, G., Benayahu, Y., Gasith, A. 2004Prolonged lag in population outbreak of an invasive mussel: a shifting-habitat modelBiol. Invasions6347364CrossRefGoogle Scholar
  59. Robinson, D.G. 1999Alien invasions: The effects of the global economy on nonmarine gastropod introductions into the United StatesMalacologia41413438Google Scholar
  60. Rosenberg, N.A., Pritchard, J.K., Weber, J.L., Cann, H.M., Kidd, K.K., Zhivotovsky, L.A., Feldman, M.W. 2002Genetic structure of human populationsScience29823812385CrossRefPubMedGoogle Scholar
  61. Rozas, J., Sanchez-DelBarrio, J.C., Messeguer, X., Rozas, R. 2003DnaSP, DNA polymorphism analyses by the coalescent and other analysesBioinformatics1924962497CrossRefPubMedGoogle Scholar
  62. Saitou, N., Nei, M. 1987The Neighbor-Joining method – a new method for reconstructing phylogenetic treesMol. Biol. Evol.4406425PubMedGoogle Scholar
  63. Sakai, A.K., Allendorf, F.W., Holt, J.S., Lodge, D.M., Molofsky, J., With, K.A., Baughman, S., Cabin, R.J., Cohen, J.E., Ellstrand, N.C., McCauley, D.E., O’Neil, P., Parker, I.M., Thompson, J.N., Weller, S.G. 2001The population biology of invasive speciesAnnu. Rev. Ecol. Syst.32305332CrossRefGoogle Scholar
  64. Sala, O.E., Chapin, F.S., Armesto, J.J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, E., Huenneke, L.F., Jackson, R.B., Kinzig, A., Leemans, R., Lodge, D.M., Mooney, H.A., Oesterheld, M., Poff, N.L., Sykes, M.T., Walker, B.H., Walker,  M., Wall, D.H. 2000Biodiversity – global biodiversity scenarios for the year 2100Science28717701774CrossRefPubMedGoogle Scholar
  65. Schmidt, M., T. Niblack, C.R. Grau, A.E. Dorrance, G.L. Hartman & R. Frederick, 2002. Soybean pest management strategic plan. St. LouisGoogle Scholar
  66. Selander, R.K., Ochman, H. 1983The genetic structure of populations as illustrated by molluscsIsozymes: Curr. Top. Biol. Med. Res.1093123Google Scholar
  67. Smith, B.J. 1989Travelling snailsJ. Med. Appl. Malacol.1195204Google Scholar
  68. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., Higgins, D.G. 1997The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis toolsNucl. Acids Res.2448764882CrossRefGoogle Scholar
  69. Turgeon, D.D., Quinn, J.F.,Jr., Bogan, A.E., Coan,  E.V., Hochberg, F.G. , Lyons, W.G., Mikkelsen, P.M., Neves, R.J., Roper, C.F.E., Rosenberg, G. , Roth,  B. , Scheltema, A. , Thompson, F.G., Vecchioni ,  M. , Williams, J.D. 2004Common and Scientific Names of Aquatic Invertebrates from the United States and Canada: Mollusks2nd ednAmerican Fisheries SocietyMarylandGoogle Scholar
  70. Weir, B.S., Cockerham, C.C. 1984Estimating F-statistics for the analysis of population-structureEvolution3813581370Google Scholar
  71. Westerbergh, A., Nyberg, A.B. 1995Selective grazing of hairless Silene dioica plants by land gastropodsOikos73289298Google Scholar
  72. White, T.J., Bruns, S., Lee, S., Taylor, J. 1990Amplification and direct sequencing of fungal ribosomal RNA genes for phylogeneticsInnis, M.A.Gelfand, D.H.Sninsky, J.J.White, T.J. eds. PCR Protocols: A Guide to Methods and ApplicationsAcademic PressOrlando315322Google Scholar
  73. Wilcove, D.S., Rothstein, D., Dubow, J., Phillips, A., Losos, E. 1998Quantifying threats to imperiled species in the United StatesBioscience48607615Google Scholar
  74. Winnepenninckx, B., Backeljau, T., Wachter, R. 1993Extraction of high-molecular-weight DNA from molluscsTrends Genet.9407CrossRefPubMedGoogle Scholar
  75. Yeh, F.C., R.-C. Yang, T.B.J. Boyle, Z.-H. Ye & J.X. Mao, 1997. POPGENE, The User-Friendly Shareware for Population Genetic Analysis. Molecular Biology and Biotechnology Centre, University of Alberta, CanadaGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Jan Pinceel
    • 1
    Email author
  • Kurt Jordaens
    • 1
  • Natalie Van Houtte
    • 1
  • Gary Bernon
    • 2
  • Thierry Backeljau
    • 1
    • 3
  1. 1.Department of BiologyUniversity of AntwerpAntwerpBelgium
  2. 2.Pest Survey Detection and Exclusion LaboratoryOtis ANGBUSA
  3. 3.Department of InvertebratesRoyal Belgian Institute of Natural SciencesBrusselsBelgium

Personalised recommendations