Skip to main content
SpringerLink
Log in

Population genomics of the raccoon dog (Nyctereutes procyonoides) in Denmark: insights into invasion history and population development

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The raccoon dog (Nyctereutes procyonoides) has a wide distribution in Europe and is a prominent example of a highly adaptable alien species. It has been recorded sporadically in Denmark since 1980 but observations since 2008 suggested that the species had established a free-ranging, self-sustaining population. To elucidate the origin and genetic patterns of Danish raccoon dogs, we studied the population genomics of 190 individuals collected in Denmark (n = 141) together with reference captive individuals from Poland (n = 21) and feral individuals from different European localities (Germany, Poland, Estonia and Finland, n = 28). We used a novel genotyping-by-sequencing approach simultaneously identifying and genotyping a large panel of single nucleotide polymorphisms (n = 4526). Overall, there was significant indication for contemporary genetic structuring of the analysed raccoon dog populations, into at least four different clusters, in spite of the existence of long distance gene flow and secondary admixture from different population sources. The Danish population was characterized by a high level of genetic admixture with neighbouring feral European ancestries and the presence of private clusters, non-retrieved in any other feral or captive populations sampled. These results suggested that the raccoon dog population in Denmark was founded by escapees from genetically unidentified Danish captive stocks, followed by a recent admixture with individuals migrating from neighbouring Germany.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abdelkrim J, Pascal M, Calmet C, Samadi S (2005) Importance of assessing population genetic structure before eradication of invasive species: examples from insular Norway rat populations. Conserv Biol 19:1509–1518. doi:10.1111/j.1523-1739.2005.00206.x

    Google Scholar 

  • Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664. doi:10.1101/gr.094052.109

    PubMed  PubMed Central  CAS  Google Scholar 

  • Allendorf, Lundkvist (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30

    Google Scholar 

  • Anonymous (2015) Order regarding housing of specific animals (in Danish: Bekendtgørelse om forbud mod hold af særlige dyr, bek. nr. 1261 af 17/11/2015)

  • Ansorge H, Ranyuk M, Kauhala K et al (2009) Populations in the area of origin and in colonised regions—the epigenetic variability of an immigrant. Ann Zool Fenn 46:51–62. doi:10.5735/086.046.0106

    Google Scholar 

  • Asferg T (1991) Danmarks Pattedyr 2. Gyldendal, Copenhagen

    Google Scholar 

  • Baagøe HJ, Ujvári M (2007) Mårhund. Dansk Pattedyratlas. Gyldendal, Copenhagen, pp 182–183

    Google Scholar 

  • Cushman SA (2015) Pushing the envelope in genetic analysis of species invasion. Mol Ecol. doi:10.1111/mec.13043

    Article  PubMed  Google Scholar 

  • Danish Environmental Ministry (2010) Indsatsplan mod mårhund i Danmark, Copenhagen

  • Davey JW, Hohenlohe PA, Etter PD et al (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12:499–510. doi:10.1038/nrg3012

    PubMed  CAS  Google Scholar 

  • Drygala F, Zoller H, Stier N, Roth M (2010) Dispersal of the raccoon dog Nyctereutes procyonoides into a newly invaded area in Central Europe. Wildl Biol 16:150–161. doi:10.2981/08-076

    Google Scholar 

  • Drygala F, Korablev N, Ansorge H et al (2016) Homogenous population genetic structure of the non-native Raccoon dog (Nyctereutes procyonoides) in Europe as a result of rapid population expansion. PLoS ONE 11:e0153098. doi:10.1371/journal.pone.0153098

    PubMed  PubMed Central  Google Scholar 

  • Ekblom R, Galindo J (2010) Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity (Edinb) 107:1–15. doi:10.1038/hdy.2010.152

    Google Scholar 

  • Elshire RJ, Glaubitz JC, Sun Q et al (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379. doi:10.1371/journal.pone.0019379

    PubMed  PubMed Central  CAS  Google Scholar 

  • European Union (2014) Regulation no. 1143/2014 on the prevention and management of the introduction and spread of the invasive alien species. European Parliament and Council, Strasbourg, 22 Oct 2014

  • Fitzpatrick BM, Fordyce J, Niemiller ML, Reynolds RG (2012) What can DNA tell us about biological invasions? Biol Invasions 14:245–253. doi:10.1007/s10530-011-0064-1

    Google Scholar 

  • Garrick RC, Bonatelli IAS, Hyseni C et al (2015) The evolution of phylogeographic datasets. Mol Ecol 24:1164–1171. doi:10.1111/mec.13108

    PubMed  CAS  Google Scholar 

  • Glaubitz JC, Casstevens TM, Lu F et al (2014) TASSEL-GBS: a high capacity genotyping by sequencing analysis pipeline. PLoS ONE 9:e90346. doi:10.1371/journal.pone.0090346

    PubMed  PubMed Central  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) Past: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  • Hampton JO, Spencer PBS, Alpers DL et al (2004) Molecular techniques, wildlife management and the importance of genetic population structure and dispersal: a case study with feral pigs. J Appl Ecol 41:735–743. doi:10.1111/j.0021-8901.2004.00936.x

    CAS  Google Scholar 

  • Handley LJL, Estoup A, Evans DM, Thomas CE, Lombaert E, Facon B, Aebi A, Roy HE (2011) Ecological genetics of invasive alien species. Biocontrol 56(4):409–428. doi:10.1007/s10526-011-9386-2

    Google Scholar 

  • Helle F, Kauhala K (1991) Distribution history and present status of the raccoon dog in Finland. Holarct Ecol 14:278–286. doi:10.1111/j.1600-0587.1991.tb00662.x

    Google Scholar 

  • Hoffmann D, Schmüser H (2007) Wildzustandsbereicht Schlesvig-Holstein. Flinkbek

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. doi:10.1093/bioinformatics/btn129

    PubMed  CAS  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. doi:10.1186/1471-2156-11-94

    PubMed  PubMed Central  Google Scholar 

  • Kasperek K, Horecka B, Jakubcza A et al (2015) Analysis of genetic variability in farmed and wild populations of raccoon dog (Nyctereutes Procyonoides) using microsatellite sequences. Ann Anim Sci 15:889–901

    Google Scholar 

  • Kauhala K (1996) Introduced carnivores in Europe with special reference to central and northern Europe. Wildl Biol 2:197–204

    Google Scholar 

  • Kauhala K, Kowalczyk R (2011) Invasion of the raccoon dog Nyctereutes procyonoides in Europe: history of colonization, features behind its success, and threats to native fauna. Curr Zool 57:584–598

    PubMed  Google Scholar 

  • Kauhala K, Saeki M (2004) Raccoon dog (Nyctereutes procyonoides). Canids: foxes, wolves, jackals and dogs. Status survey and conservation action plan. IUCN/SSC Canid SPecialist Group, Gland, pp 136–138

    Google Scholar 

  • Korablev NP, Korablev MP, Rozhnov V, Korablev PN (2011) Polymorphism of the mitochondrial DNA control region in the population of raccoon dog (Nyctereutes procyonoides Gray, 1834) introduced into the Upper Volga basin. Russ J Genet 47:1227–1233. doi:10.1134/S1022795411100103

    CAS  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760. doi:10.1093/bioinformatics/btp324

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mantel N (1967) Detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    PubMed  CAS  Google Scholar 

  • Meirmans PG (2012) The trouble with isolation by distance. Mol Ecol 21:2839–2846. doi:10.1111/j.1365-294X.2012.05578.x

    PubMed  Google Scholar 

  • MELUR-SH (2014) Jagd und Artenschutz - Jahresbericht 2014. Ministerium für Energiewende, Landwirtschaft, Umwelt und ländliche Räume des Landes Schlesvig-Holstein (MELUR-SH), Flintbek

  • Morozov VF (1953) Akklimatizacija ussurskogo enota (Nyctereutes procyonoides, GRAY) kakprimer uspešnogo preobrazovanija fauny pušcnych sverej evropejskoj territorii SSSR. Zool Zhurnal 23:524–533

    Google Scholar 

  • Mulder JL (2012) A review of the ecology of the raccoon dog (Nyctereutes procyonoides) in Europe. Lutra 55:101–127

    Google Scholar 

  • Nørgaard LS, Mikkensen D, Rømer A et al (2014) Spredning af feral Mårhund (Nyctereutes procyonoides) i Danmark. Flora Fauna 120:8–14

    Google Scholar 

  • 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 30:137–154

    Google Scholar 

  • Paulauskas A, Griciuvienė L, Radzijevskaja J, Gedminas V (2015) Genetic characterization of the raccoon dog (Nyctereutes procyonoides), an alien species in the Baltic region. Turk J Zool 34:1–11. doi:10.3906/zoo-1502-34

    Google Scholar 

  • Peakall R, Smouse P (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pitra C, Schwarz S, Fickel J (2010) Going west-invasion genetics of the alien raccoon dog Nyctereutes procynoides in Europe. Eur J Wildl Res 56:117–129. doi:10.1007/s10344-009-0283-2

    Google Scholar 

  • Puillandre N, Dupas S, Dangles O et al (2008) Genetic bottleneck in invasive species: the potato tuber moth adds to the list. Biol Invasions 10:319–333. doi:10.1007/s10530-007-9132-y

    Google Scholar 

  • Purcell S, Neale B, Todd-Brown K et al (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575. doi:10.1086/519795

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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)

  • Rømer A, Nørgaard L, Mikkelsen D et al (2015) Population viability analysis of feral raccoon dog (Nyctereutes procyonoides) in Denmark. Arch Biol Sci 67:111–117. doi:10.2298/ABS140905012R

    Google Scholar 

  • Rousset F (2008) GENEPOP’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106. doi:10.1111/j.1471-8286.2007.01931.x

    PubMed  Google Scholar 

  • Simberloff D, Martin JL, Genovesi P et al (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66. doi:10.1016/j.tree.2012.07.013

    PubMed  Google Scholar 

  • Slaska B, Grzybowska-Szatkowska L (2011) Analysis of the mitochondrial haplogroups of farm and wild-living raccoon dogs in Poland. Mitochondrial DNA 22:105–110. doi:10.3109/19401736.2011.624603

    PubMed  CAS  Google Scholar 

  • Ślaska B, Zięba G, Rozempolska-Rucińska I et al (2010) Evaluation of genetic biodiversity in farm-bred and wild raccoon dogs in Poland. Folia Biol (Krakow) 58:195–199

    Google Scholar 

  • Sunde P, Elmeros M (2016) Bestandsudvikling af mårhund i Danmark 2009–2016 i relation til nutidig og fremtidig bekæmpelsesindsats. Technical report, Department of Bioscience, Aarhus University

  • Thioulouse J, Chessel D, Doledec S, Olivier JM (1997) ADE-4: a multivariate analysis and graphical display software. Stat Comput 7:75–83. doi:10.1023/A:1018513530268

    Google Scholar 

  • Thirstrup JP, Ruiz-Gonzalez A, Pujolar JM et al (2015) Population genetic structure in farm and feral American mink (Neovison 4 vison) inferred from RAD sequencing-generated single nucleotide 5 polymorphisms. J Anim Sci. doi:10.2527/jas2015-8996

    Article  PubMed  Google Scholar 

  • Travis JMJ, Park KJ (2004) Spatial structure and the control of invasive alien species. Anim Conserv 7:321–330. doi:10.1017/S1367943004001507

    Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S-PLUS. Springer, New York

    Google Scholar 

  • Wahlund S (1928) Zusammensetzung von populationen und korrelationserscheinungen vom standpunkt der vererbungslehre aus betrachtet. Hereditas 11:65–106. doi:10.1111/j.1601-5223.1928.tb02483.x

    Google Scholar 

  • Weir B, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    PubMed  CAS  Google Scholar 

  • White TA, Perkins SE, Heckel G, Searle JB (2013) Adaptive evolution during an ongoing range expansion: the invasive bank vole (Myodes glareolus) in Ireland. Mol Ecol 22:2971–2985. doi:10.1111/mec.12343

    PubMed  CAS  Google Scholar 

  • Wright S (1943) Isolation b y distance. Genetics 28:114–138

    PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

We gratefully thank the Danish Hunters Nature Organization (Jægernes Naturfond) and Aalborg Zoo Conservation Foundation (AZCF) for economical support to the genetic analyses of the Danish raccoon dogs. Additionally, we like to thank the Danish Nature Agency, the Danish hunters and other people involved in the collection of Danish raccoon dog carcasses, and submitted for necropsy at the National Veterinary Institute, Technical University of Denmark. Aritz Ruiz-González was supported by a post-doctoral fellowship (Ref: DKR-2012-64) awarded by the Department of Education, Universities and Research of the Basque Government. Finally, we thank the Subject Editor and one anonymous Reviewer for invaluable suggestions and comments on an earlier version of the manuscript.

Author information

Authors and Affiliations

  1. Section of Biology and Environmental Engineering, Chemistry and Environmental Engineering, Aalborg University, Aalborg, Denmark

    Louise Solveig Nørgaard, Dorthe Marlene Götz Mikkelsen, Jeppe Lund Nielsen, Cino Pertoldi & Ettore Randi

  2. Department of Bioscience, Aarhus University, Kalø, Grenåvej 14, 8410, Rønde, Denmark

    Louise Solveig Nørgaard, Dorthe Marlene Götz Mikkelsen, Morten Elmeros & Aksel Bo Madsen

  3. School of Biological Sciences, Monash University, Melbourne, VIC, 3800, Australia

    Louise Solveig Nørgaard

  4. National Veterinary Institute, Copenhagen, Technical University of Denmark, Bülowsvej 27, 1870, Frederiksberg C, Denmark

    Mariann Chriél

  5. Conservation Genetics Laboratory, National Institute for Environmental Protection and Research (ISPRA), Via Cà Fornacetta 9, 40064, Ozzano dell’Emilia, Bologna, Italy

    Ettore Randi & Aritz Ruiz-González

  6. Department of Evolutionary Genetics, Leibniz-Institute for Zoo and Wildlife Research (IZW), Alfred-Kowalke-Str 17, 10315, Berlin, Germany

    Joerns Fickel

  7. Department of Molecular Ecology and Evolution, Potsdam University, Karl-Liebknecht-Str. 24-25, 14476, Potsdam, Germany

    Joerns Fickel

  8. Department of Biological Bases of Animal Production, University of Life Sciences in Lublin, Lublin, Poland

    Slaska Brygida

  9. Department of Zoology and Animal Cell Biology, University of the Basque Country UPV/EHU, C/Paseo de la Universidad 7, 01006, Vitoria-Gasteiz, Spain

    Aritz Ruiz-González

  10. Systematics, Biogeography and Population Dynamics Research Group, Lascaray Research Center, University of the Basque Country (UPV/EHU), Avda. Miguel de Unamuno, 3, 01006, Vitoria-Gasteiz, Spain

    Aritz Ruiz-González

Authors
  1. Louise Solveig Nørgaard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dorthe Marlene Götz Mikkelsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Morten Elmeros
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mariann Chriél
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aksel Bo Madsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jeppe Lund Nielsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cino Pertoldi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ettore Randi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Joerns Fickel
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Slaska Brygida
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Aritz Ruiz-González
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aritz Ruiz-González.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 487 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nørgaard, L.S., Mikkelsen, D.M.G., Elmeros, M. et al. Population genomics of the raccoon dog (Nyctereutes procyonoides) in Denmark: insights into invasion history and population development. Biol Invasions 19, 1637–1652 (2017). https://doi.org/10.1007/s10530-017-1385-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-017-1385-5

Keywords

Search

Navigation