European Journal of Wildlife Research

, Volume 56, Issue 2, pp 117–129 | Cite as

Going west—invasion genetics of the alien raccoon dog Nyctereutes procynoides in Europe

Original Paper

Abstract

The raccoon dog, a medium-sized carnivore, has long been recognised as a prominent example of an invasive alien species in Europe with a wide distribution, significant ecological impact and remarkable dynamics of spread at both national and continental scales. We conducted a study of genetic diversity of 73 individuals collected at 20 sites across North and Central Europe to (1) identify major phylogenetic lineages and (2) elucidate spatial patterns of population genetic structure. Reconstructed phylogenies reveal two major clades differing on average by Tamura–Nei corrected distance of 3.4% for a 599-bp segment of the mitochondrial control region corresponding to a coalescence time of approximately 457,800 years ago (95% CI, 223,300–773,900). Many expectations based on introduction history, such as the presence of signatures of repeated founder effects and subsequently rapid population expansion, were not confirmed by our demographic analyses, probably due to an insufficient amount of time since translocations. Nevertheless, global FST = 13.9% and landscape approaches provided evidence for weak population genetic structure that followed a pattern of isolation by distance. Finally, we found no congruence between previously reported morphological differentiation and the sorting of mtDNA variation. We therefore conclude that an exceptional combination of factors including multiple translocations, secondary contact and admixture of divergent matrilineages, as well as natural processes of colonisation associated with a wide ecological tolerance, promoted the successful spread of the raccoon dog into Europe.

Keywords

Nyctereutes Invasion Mitochondrial DNA Control region Population genetics Europe 

References

  1. Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30. doi:10.1046/j.1523-1739.2003.02365.x CrossRefGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  3. Ansorge H, Ranyuk M, Kauhala K, Kowalczyk R, Stier N (2009) Raccoon dog, Nyctereutes procyonoides, populations in the area of origin and in colonised regions—the epigenetic variability of an immigrant. Ann Zool Fenn 46:51–62Google Scholar
  4. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  5. Ayala FJ (1999) Molecular clock mirages. Bioessays 21:71–75. doi:1002/(SICI)1521-1878(199901)21:1<71::AID-BIES9>3.0.CO;2-B CrossRefPubMedGoogle Scholar
  6. Barbu P (1972) Beiträge zum Studium des Marderhundes, Nyctereutes procyonoides ussuriensis Matschie, 1907, aus dem Donaudelta. Säugetierkdl Mitt 20:375–405Google Scholar
  7. Bjornerfeldt S, Webster MT, Vila C (2006) Relaxation of selective constraint on dog mitochondrial DNA following domestication. Genome Res 16(8):990–994. doi:10.1101/gr.5117706 CrossRefPubMedGoogle Scholar
  8. Castric V, Bernatchez L (2003) The rise and fall of isolation by distance in the anadromous brook charr (Salvelinus fontinalis Mitchill). Genetics 163:983–996PubMedGoogle Scholar
  9. Cirovic D (2006) First record of the raccoon dog (Nyctereutes procyonoides Gray, 1834) in the former Yugoslav Republic of Macedonia. Eur J Wildl Res 52:136–137. doi:10.1007/s10344-005-0106-z CrossRefGoogle Scholar
  10. Clark SA, Richardson BJ (2002) Spatial analysis of genetic variation as a rapid assessment tool in the conservation management of narrow-range endemics. Invertebr Syst 16:583–587. doi:10.1071/IT01041 CrossRefGoogle Scholar
  11. Clavero M, Garcia-Berthou E (2005) Invasive species are a leading cause of animal extinction. Trends Ecol Evol 20:110. doi:10.1016/j.tree.2005.01.003 CrossRefPubMedGoogle Scholar
  12. Dermitzakis MD, Van Der Geer AAE, Lyras GA (2004) The phylogenetic position of raccoon dogs: implications of their neuroanatomy. 5th International Symposium on Eastern Mediterranean Geology Thessaloniki, Greece, 14–20 AprilGoogle Scholar
  13. Deutscher Jagdschutzverband (2009) Jahresstrecken Neozoen. Accessible at http://www.jagdschutzverband.de/datenfakten/jahresstrecken/?meta_id=257
  14. Diniz-Filho JAF, Telles MPDC (2002) Spatial autocorrelation analysis and the identification of operational units for conservation in continuous populations. Conserv Biol 16:924–935CrossRefGoogle Scholar
  15. Drygala F, Stier N, Zoller H, Boegelsack K, Mix HM, Roth M (2008) Habitat use of the raccoon dog (Nyctereutes procyonoides) in north-eastern Germany. Mamm Biol 73:371–378CrossRefGoogle Scholar
  16. Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci U S A 97:7043–7050CrossRefPubMedGoogle Scholar
  17. 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 131:479–491PubMedGoogle Scholar
  18. Excoffier L, Laval G, Schneider S (2005) Arlequin, version 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedGoogle Scholar
  19. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  20. Frankham R (2005) Resolving the genetic paradox in invasive species. Heredity 94:385CrossRefPubMedGoogle Scholar
  21. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedGoogle Scholar
  22. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709PubMedGoogle Scholar
  23. Gaubert P, Godoy JA, del Cerro I, Palomares F (2009) Early phases of a successful invasion: mitochondrial phylogeography of the common genet (Genetta genetta) within the Mediterranean Basin. Biol Invasions 11:523–546CrossRefGoogle Scholar
  24. Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–601PubMedGoogle Scholar
  25. Hassan M, Bonhomme F (2005) No reduction in neutral variation of mitochondrial and nuclear genes for a Lessepsian migrant, Upeneus moluccensis. J Fish Biol 66:865–870CrossRefGoogle Scholar
  26. Haubold B, Wiehe T (2001) Statistics of divergence times. Mol Biol Evol 18(7):1157–1160PubMedGoogle Scholar
  27. Helle E, Kauhala K (1991) Distribution history and present status of the raccoon dog in Finland. Holarct Ecol 14:278–286Google Scholar
  28. Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913CrossRefPubMedGoogle Scholar
  29. Hillis DM, Mable BK, Moritz C (1996) Applications of molecular systematics: the state of the field and a look to the future. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics. Sinauer, Sunderland, MA, pp 515–543Google Scholar
  30. Hudson RR (1990) Gene genealogies and the coalescent process. In: Futuyma DJ, Antonovics JD (eds) Oxford surveys in evolutionary biology. Oxford University Press, New York, pp 1–44Google Scholar
  31. Kauhala K (1996) Introduced carnivores in Europe with special reference to central and northern Europe. Wildlife Biol 2:197–204Google Scholar
  32. Kauhala K, Saeki M (2004) Raccoon dogs. In: Sillero-Zubiri C, Hoffmann M, Macdonald DW (eds) Canids: foxes, wolves, jackals and dogs. Status Survey and Conservation Action Plan IUCN/SSC Canid Specialist Group, Gland, Cambridge, pp 136–142Google Scholar
  33. Kingman JFC (1982) On the Genealogy of Large Populations. J Appl Prob 19A:27–43CrossRefGoogle Scholar
  34. Kolbe JJ, Glor RE, Rodriguez Schettino L, Lara AC, Larson A (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181CrossRefPubMedGoogle Scholar
  35. Lapini L (2006) Il Cane viverrino Nyctereutes procyonoides ussuriensis Matschie, 1908 in Italia : Segnalazioni 1980–2005 (Mammalia: Carnivora: Canidae). Boll Mus civ Stor nat Ven 57:235–239 (in Italian)Google Scholar
  36. Lavrov NP (1971) The results of the introductions of the raccoon dog (Nyctereutes procyonoides) in different provinces in the USSR. Trudy kafedry biologii Moskovskij Gosvdarstvennij Zaocnij Pedagogiceskij Institut 29:101–160 (in Russian)Google Scholar
  37. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391CrossRefGoogle Scholar
  38. Lutz W (1989) Zum Vorkommen des Marderhundes (Nyctereutes procyonoides GRAY 1834) in Deutschland. Drosera 89(1/2):79–83 (in German with English summary)Google Scholar
  39. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  40. Marshall CR (1990) The fossil record and estimating divergence times between lineages: maximum divergence times and the importance of reliable phylogenies. J Mol Evol 30:400–408CrossRefPubMedGoogle Scholar
  41. Miller MP (2005) Alleles in space (AIS): computer software for the joint analysis of interindividual spatial and genetic Information. J Heredity 96:722–724CrossRefGoogle Scholar
  42. Mitchell-Jones AJ, Amori G, Bogdanowicz W, Kryðtufek B, Reijnders PJ H, Spitzenberger F, Stubbe M, Thissen JBM, Vohralik V, Zima J (1999) Atlas of European mammals. Academic, LondonGoogle Scholar
  43. Morozov VF (1953) Akklimatizacija ussurskogo enota (Nyctereutes procyonoides, GRAY) kakprimer uspešnogo preobrazovanija fauny pušcnych sverej evropejskoj territorii SSSR. Zool Z 23:524–533Google Scholar
  44. Nowak E (1973) Ansiedlung und Ausbreitung des Marderhundes (Nyctereutes procyonoides GRAY) in Europa. Beitr Jagd-und Wildforschung 8:351–384Google Scholar
  45. Nowak E (1984) Verbreitungs-und Bestandsentwicklung des Marderhunds, Nyctereutes procyonoides (GRAY, 1834) in Europe. Range and population growth of the raccoon dogs in Europe. Z Jadgwiss 30:137–154Google Scholar
  46. Nowak E (1993) Nyctereutes procyonoides (Gray, 1834)—Marderhund. In: Stubbe M, Krapp F (eds) Handbuch der Säugetiere Europas, vol 5/1. Aula, Wiesbaden, pp 215–248Google Scholar
  47. Nowak E, Pielowski Z (1964) Die Verbreitung des Marderhundes in Polen im Zusammenhang mit seiner Einbürgerung und Ausbreitung in Europa. Acta Theriol 9:81–110Google Scholar
  48. Okumura N, Ishiguro N, Nakano M, Matsui A, Sahara M (1996) Intra- and interbreed genetic variations of mitochondrial DNA major non-coding regions in Japanese native dog breeds (Canis familiaris). Anim Genet 27(6):397–405PubMedCrossRefGoogle Scholar
  49. Palumbi SR, Martin A, Romano S, McMillan WO, Grabowski G (1991) The simple fool's guide to PCR, version 2.0. University of Hawaii, Honolulu, HawaiiGoogle Scholar
  50. Perry WL, Feder JL, Dwyer G, Lodge DM (2001) Hybrid zone dynamics and species replacement between Orconectes crayfishes in a northern Wisconsin lake. Evolution 55:1153–1166PubMedGoogle Scholar
  51. Pitra C, Rehbein S, Lutz W (2005) Tracing the genetic roots of the sika deer Cervus nippon naturalized in Germany and Austria. Eur J Wildl Res 51:237–241CrossRefGoogle Scholar
  52. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  53. Prokopenko AA, Williams DF, Kuzmin MI, Karabanov EB, Khursevich GK, Peck JA (2002) Muted climate variations in continental Siberia during the mid-Pleistocene epoch. Nature 418:65–68CrossRefPubMedGoogle Scholar
  54. Rafinski J, Babik W (2000) Genetic differentiation among northern and southern populations of the moor frog Rana arvalis Nilsson in central Europe. Heredity 84:610–618CrossRefPubMedGoogle Scholar
  55. Ralli UM, Kritskaya TI (1953) Erfahrungen über die Akklimatisierung des ussurischen Marderhundes im Gebiet von Rostow. Essai d'acclimation du chien viverrin dans la region de Rostov. An experiment in acclimation of Usurri raccoon dog in the Rostov region. Zool Zhurn 32:513–522 (in Russian)Google Scholar
  56. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100PubMedGoogle Scholar
  57. Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:11095–1103Google Scholar
  58. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  59. Rozas J, Sánchez-DelBarrio JC, Messegyer X (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497CrossRefPubMedGoogle Scholar
  60. Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, Kimberly A, Syndallas B, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O'Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332CrossRefGoogle Scholar
  61. Sax DF, Brown JH (2000) The paradox of invasion. Glob Ecol Biogeogr 9:363–371CrossRefGoogle Scholar
  62. Schwarz S, Sutor A, Pitra C (2004) Raccon dogs—silently colonizing Europe (Nyctereutes procynoides GRAY 1834). Proceedings volume, Neobiota Conference, BernGoogle Scholar
  63. Sheldon J (1992) Wild dogs: the natural history of the nondomestic Canidae. Academic, San DiegoGoogle Scholar
  64. Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279CrossRefGoogle Scholar
  65. Sokal RR, Oden NL (1978) Spatial autocorrelation analysis in biology 2. Some biological implications and four applications of evolutionary and ecological interest. Biol J Linn Soc 10:229–249CrossRefGoogle Scholar
  66. Sutor A (2008) Dispersal of the alien raccoon dog Nyctereutes procyonoides in Southern Brandenburg, Germany. Eur J Wildl Res 54:321–326CrossRefGoogle Scholar
  67. Swofford DL (2001) PAUP*: phylogenetic analysis using parsimony (* and other methods), version 4.0. Sinauer, Sunderland, MAGoogle Scholar
  68. Tajima F (1989) The effect of change in population size on DNA polymorphism. Genetics 123:597–601PubMedGoogle Scholar
  69. Tajima D, Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  70. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  71. Tedford RH, Qiu Z (1991) Pliocene Nyctereutes (Carnivora: Canidae) from Yushe, Shanxi, with comments on Chinese fossil raccoon-dogs. Vertebrata PalAsiatica 29:179–189Google Scholar
  72. Vilà C, Savolainen P, Maldonado JE, Amorim IR, Rice JE, Honeycutt RL, Crandall KA, Lundeberg J, Wayne RK (1997) Multiple and ancient origins of the domestic dog. Science 276:1687–1689CrossRefPubMedGoogle Scholar
  73. Ward OG, Wurster-Hill DH (1990) Mammalian species: Nyctereutes procyonoides. American Society of Mammalogists, no. 358, pp 1–5Google Scholar
  74. Ward OG, Wurster-Hill DH, Ratty FJ, Strong Y (1987) Comparative cytogenetics of Chinese and Japanese raccoon dogs, Nyctereutes procyonoides. Cytogenet Cell Genet 45:177–186CrossRefPubMedGoogle Scholar
  75. Wayne RK (1993) Molecular evolution of the dog family. Trends Genet 9:218–224CrossRefPubMedGoogle Scholar
  76. Weber E (2003) Invasive plant species of the world a reference guide to environmental weeds. CABI, WallingfordGoogle Scholar
  77. Zink RM, Pavlova A, Rohwer S, Drovetski SV (2006) Barn swallows before barns: population histories and intercontinental colonization. Proc R Soc B 273:1245–1251CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Christian Pitra
    • 1
  • Sabine Schwarz
    • 2
  • Joerns Fickel
    • 1
  1. 1.Department of Evolutionary GeneticsLeibniz Institute for Zoo and Wildlife ResearchBerlinGermany
  2. 2.Society for the Protection of Great Bustard e.V. (Germany)NennhausenGermany

Personalised recommendations