Skip to main content
Log in

Genetic variability and population structure of grey wolf (Canis lupus) in Serbia

  • Animal Genetics
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

Results of previous morphometric and genetic analyses of grey wolf (Canis lupus L.) population from Serbia indicated different patterns of population subdivision. In order to explore population structure, level of genetic variability, genetic drift, inbreeding and signals of bottleneck for grey wolves from Serbia, we applied highly polymorphic genetic markers (microsatellites). Obtained data are valuable in determination of conservation units and creation of appropriate management plans. We have amplified 18 highly polymorphic microsatellites, in a total sample of 75 grey wolves, from different localities across Serbia and multilocus genotypes were analyzed using appropriate software. Observed values of the basic genetic parameters (H O = 0.69; H E = 0.75) indicated moderate level of genetic variability, similar to genetic variability in other populations belonging to the Dinaric-Balkan population of grey wolf. In STRUCTURE analysis, although ΔK was estimated to be at first peak K = 2, and second peak K = 4, CLUMPAK analyses showed that there’s no structuring for any of assumed K, and therefore the population of grey wolf from Serbia may be considered as one continuous population and treated as one conservation unit in future management plans. Signals of bottleneck haven’t been observed (Wilcoxon test two phase mutation model p = 0.247; and stepwise mutation model p = 0.815).

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Wolves: Behaviour, Ecology and Conservation, Mech, L.D. and Boitani, L., Eds., Chicago: The University of Chicago Press, 2003.

  2. Boitani, L., Plan d’action pour la conservation du loup (Canis lupus) en Europe, 2003.

    Google Scholar 

  3. Delibes, M., Status and conservation needs of the wolf in the Council of Europe member States, Nat. Environ. Ser., 1990, vol. 47, pp. 1–46.

    Google Scholar 

  4. Randi, E., Lucchini, V., Christensen, M.F., et al., Mitochondrial DNA variability in Italian and East European wolves: detecting the consequences of small population size and hybridization, Conserv. Biol., 2000, vol. 14, pp. 464–473.

    Article  Google Scholar 

  5. Randi, E., Genetics and conservation of wolves Canis lupus in Europe, Mamm. Rev., 2011, vol. 41, pp. 99–111.

    Article  Google Scholar 

  6. Lucchini, V., Galov, A. and Randi, E., Evidence of genetic distinction and long-term population decline in wolves (Canis lupus) in the Italian Apennines, Mol. Ecol., 2004, vol. 13, pp. 523–536.

    Article  CAS  PubMed  Google Scholar 

  7. Gomercic, T., Sindicic, M., Galov, A., et al., High genetic variability of the grey wolf (Canis lupus L.) population from Croatia as revealed by mitochondrial DNA control region sequences, Zool. Stud., 2010, vol. 49, pp. 816–823.

    CAS  Google Scholar 

  8. Vilà, C., Walker, C., Sundqvist, A.K., et al., Combined use of maternal, paternal and bi-parental genetic markers for the identification of wolf–dog hybrids, Heredity, 2003, vol. 90, pp. 17–24.

    PubMed  Google Scholar 

  9. Leonard, J.A., Vila, C. and Wayne, R.K., Legacy lost: genetic variability and population size of extirpated US grey wolves (Canis lupus), Mol. Ecol., 2005, vol. 14, pp. 9–17.

    Article  PubMed  Google Scholar 

  10. Chapron, G., Quenette, P.Y., Legendre, S. and Clobert, J., Which future for the French Pyrenean brown bear (Ursus arctos) population? An approach using stage-structured deterministic and stochastic models, C. R. Biol., 2003, vol. 326, pp. 174–182.

    Article  Google Scholar 

  11. Nowak, S., MyslAjek, R.W., and Jedrzejewska, B., Density and demography of wolf, Canis lupus population in the western-most part of the Polish Carpathian Mountains, 1996–2003, Folia. Zool., 2011, vol. 57, pp. 392–402.

    Google Scholar 

  12. Valiere, N., Fumagalli, L., Gielly, C., et al., Long-distance wolf recolonization of France and Switzerland inferred from non-invasive genetic sampling over a period of 10 years, Anim. Conserv., 2003, vol. 6, pp. 83–92.

    Article  Google Scholar 

  13. Salvatori, V. and Linnell, J., Report on the Conservation Status and Threats for Wolves (Canis lupus) in Europe, Council of Europe T-PVS/Inf., 2005, 16, 1–24

    Google Scholar 

  14. Aspi, J., Roininen, E., Ruokonen, M., et al., Genetic diversity, population structure, effective population size and demographic history of the Finnish wolf population, Mol. Ecol., 2006, vol. 15, pp. 1561–1576.

    CAS  PubMed  Google Scholar 

  15. Kojola, I., Aspi, J., Hakala, A., et al., Dispersal in an expanding wolf population in Finland, J. Mammal., 2006, vol. 87, pp. 281–286.

    Article  Google Scholar 

  16. Fabbri, E., Miquel, C., Lucchini, V., et al., From the Apennines to the Alps: colonization genetics of the naturally expanding Italian wolf (Canis lupus) population, Mol. Ecol., 2007, vol. 16, pp. 1661–1671.

    Article  CAS  PubMed  Google Scholar 

  17. Gula, R., Legal protection of wolves in Poland: implications for the status of the wolf population, Eur. J. Wildl. Res., 2008, vol. 54, pp. 163–170.

    Article  Google Scholar 

  18. Chapron, G. and López-Bao, J.V., Conserving carnivores: politics in play, Science, 2014, vol. 343, pp. 1199–1200.

    Article  CAS  PubMed  Google Scholar 

  19. Hewitt, G.M., Post-glacial recolonization of European biota, Biol. J. Linn. Soc., 1999, vol. 68, pp. 87–112.

    Article  Google Scholar 

  20. Hewitt, G.M., The genetic legacy of the Quaternary ice ages, Nature, 2000, vol. 405, pp. 907–913.

    Article  CAS  PubMed  Google Scholar 

  21. Veličković, N., Djan, M., Obreht, D., and Vapa, Lj., Population genetic structure of wild boars in the West Balkan region. Russ. J. Genet., 2012, vol. 48, pp. 859–863.

    Article  Google Scholar 

  22. Apostolidis, A.P., Gelia, D., and Mamuris, Z., Genetic diversity among Balkan trout populations based on RAPD analysis. Russ. J. Genet., 2011, vol. 47, pp. 973–978.

    Article  CAS  Google Scholar 

  23. Dedkova, O.S., Badaeva, E.D., Amosova, A.V., et al., Diversity and the origin of the European population of Triticum dicoccum (Schrank) Schuebl. as revealed by chromosome analyses. Russ. J. Genet., 2009, vol. 45, pp. 1082–1091.

    Article  CAS  Google Scholar 

  24. Fabbri, E., Caniglia, R., Kusak, J., et al., Genetic structure of expanding wolf (Canis lupus) populations in Italy and Croatia, and the early steps of the recolonization of the Eastern Alps, Mamm. Biol., 2014, vol. 79, pp. 138–148.

    Google Scholar 

  25. Djan, M., Maletić, V., Trbojević, I., et al., Genetic diversity and structuring of the grey wolf population from the Central Balkans based on mitochondrial DNA variation. Mamm. Biol., 2014, vol. 79, pp. 277–282.

    Google Scholar 

  26. Milenković, M., Taxonomic—biogeographic status and ecological/economical significance of the wolf (Canis lupus Linnaeus 1758) in Yugoslavia. Ph. D. (Biol.) Dissertation, Belgrade: University of Belgrade, 1997.

    Google Scholar 

  27. Boitani, L. and Rondinini, C., In Evolution Lost: Status and Trends of the World’s Vertebrate’s, Mammalia, Baillie, J.E.M., Griffiths, J., Turvey, S.T., Loh, J., and Collen, B., Eds., 2010, ch. V, pp. 38–45.

  28. Verardi, A., Lucchini, V., and Randi, E., Detecting introgressive hybridization between free-ranging domestic dogs and wild wolves (Canis lupus) by admixture linkage disequilibrium analysis, Mol. Ecol., 2006, vol. 15, pp. 2845–2855.

    Article  CAS  PubMed  Google Scholar 

  29. Godinho, R., Laneza, L., Blanco, J.C., et al., Genetic evidence for multiple events of hybridization between wolves and domestic dogs in the Iberian Peninsula, Mol. Ecol., 2011, vol. 20, pp. 5154–5166.

    Article  PubMed  Google Scholar 

  30. Hinrikson, M., Männil, P., Ozolinš, J., et al., Bucking the trend in wolf–dog hybridization: first evidence from Europe of hybridization between female dogs and male wolves, PLoS One, 2012, 7. e46465. doi 10.1371/journalpone.0046465

    Article  Google Scholar 

  31. Vonholdt, B.M., Stahler, D.R., Smith, D.W., et al., The genealogy and genetic viability of reintroduced Yellowstone grey wolves, Mol. Ecol., 2013, vol. 17, pp. 252–274.

    Article  Google Scholar 

  32. Ciucci, P., Chapron, G., Guberti, V. and Boitani, L., Estimation of mortality parameters from (biased) samples at death: are we getting the basics right in wildlife field studies? A response to Lovari et al., J. Zool., 2007, vol. 273, pp. 125–127.

    Article  Google Scholar 

  33. Linnell, J.D.C. and Boitani, L., Building biological realism into wolf management policy: the development of the population approach in Europe, Hystrix, 2012, vol. 23. doi 10.4404/hystrix-23.1-4676

  34. Smith, D.W., Peterson, R.O., and Houston, D.B., Yellowstone after wolves, Bioscience, 2003, vol. 53, pp. 330–340.

    Article  Google Scholar 

  35. Duchamp, C., Boyer, J., Briaudet, P.E., et al., A dual frame survey to assess time and space-related changes of the colonizing wolf population in France, Hystrix, 2012, vol. 23, pp. 14–28.

    Google Scholar 

  36. Shafer, A.B.A., Gattepaille, L.M., Stewart, R.E.A., and Wolf, J.B.W., Demographic inferences using shortread genomic data in an approximate Bayesian computation framework: in silico evaluation of power, biases and proof of concept in Atlantic walrus, Mol. Ecol., 2015, vol. 24, pp. 328–345.

    PubMed  Google Scholar 

  37. Altukhov, Yu.P. and Salmenkova, E.A., DNA polymorphism in population genetics, Russ. J. Genet., 2002, vol. 38, pp. 989–1008.

    Article  CAS  Google Scholar 

  38. Grechko, V.V., Molecular DNA markers in phylogeny and systematics. Russ. J. Genet., 2002, vol. 38, pp. 851–868.

    Article  CAS  Google Scholar 

  39. Schlötterer, C., Opinion: the evolution of molecular markers—just a matter of fashion?, Nat. Rev. Genet., 2004, vol. 5, pp. 63–69.

    Article  PubMed  Google Scholar 

  40. Sambrook, J.F. and Russel, D.W., Molecular Cloning: A Laboratory Manual, Cold Spring Harbor: Cold Spring Harbor Laboratory Press, 2001, 3rd ed.

    Google Scholar 

  41. Excoffier, L. and Lischer, H.E.L., Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows, Mol. Ecol. Resour., 2010, vol. 10, pp. 564–567.

    Article  PubMed  Google Scholar 

  42. Belkir, K., Borsa, P., Chikhi, N., et al., Genetix 4.03 logiciel sous WindowsTM pour la genetique des populations, Montpellier: Laboratoire Genome, Populations, Interactions, CNRS UMR 5000, Univ. Montpellier II, 2001.

    Google Scholar 

  43. Weir, B.S. and Cockerham, C.C., Estimating F-statistics for the analysis of population structure, Evolution, 1984, vol. 38, pp. 1358–1370.

    Article  Google Scholar 

  44. Pritchard, J.K., Stephens, M. and Donnelly, P., Inference of population structure using multilocus genotype data, Genetics, 2000, vol. 155, pp. 945–959.

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Falush, D., Stephens, M., and Pritchard, J.K., Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies, Genetics, 2003, vol. 164, pp. 1567–1587.

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Falush, D., Stephens, M., and Pritchard, J.K., Inference of population structure using multilocus genotype data: dominant markers and null allele, Mol. Ecol. Notes, 2007, vol. 7, pp. 574–578.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Hubisz, M.J., Falush, D., Stephens, M., and Pritchard, J.K., Inferring weak population structure with the assistance of sample group information, Mol. Ecol. Resour., 2009, vol. 9, pp. 1322–1332.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Earl, D. A. and Vonholdt, B.M., Structure Harvester: a website and program for visualizing structure output and implementing the Evanno method, Conserv. Genet. Resour., 2012, vol. 4, pp. 359–361.

    Article  Google Scholar 

  49. Evanno, G., Regnaut, S., and Goudet, J., Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study, Mol. Ecol., 2005, vol. 14, pp. 2611–2620.

    Article  CAS  PubMed  Google Scholar 

  50. Kopelman, N.M., Mayzel, J., Jakobsson, M., et al., Clumpak: a program for identifying clustering modes and packaging population structure inferences across K, Mol. Ecol. Resour., 2015. doi 10.1111/1755-0998.12387

    Google Scholar 

  51. Cornuet, J.M. and Luikart, G., Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data, Genet., 1996, vol. 144, pp. 2001–2014.

    CAS  Google Scholar 

  52. Luikart, G., Allendorf, F.W., Cornuet, J.M., and Sherwin, W.B., Distortion of allele frequency distributions provided a test for recent population bottlenecks, J. Hered., 1998, vol. 89, pp. 238–247.

    Article  CAS  PubMed  Google Scholar 

  53. Di Rienzo, A., Peterson, A.C., Garza, J.C., et al., Mutational processes of simple-sequence repeat loci in human populations. Proc. Acad. Sci. U.S.A., 1994, vol. 91, pp. 3166–3170.

    Article  Google Scholar 

  54. Kimura, M. and Crow, J., The number of alleles that can be maintained in a finite population, Genet., 1964, vol. 49, pp. 725–738.

    CAS  Google Scholar 

  55. Ohta, T. and Kimura, K., The model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a genetic population, Genet. Res., 1973, vol. 22, pp. 201–204.

    Article  CAS  PubMed  Google Scholar 

  56. Luikart, G. and Cornuet, J.M., Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data, Conserv. Biol., 1996, vol. 12, pp. 228–237.

    Article  Google Scholar 

  57. Paule, L., Bakan, J., Lavadinovic, V., and Popovic, Z., Genetic differentiation of grey wolf population (Canis lupus L.) from Balkan and Carpathians, Eur. J. Wildl. Res., 2014, vol. 1, pp. 87–93.

    Google Scholar 

  58. Hulva, P., Bolfíková, B., Ríhová, J., et al., Landscape genetics of the grey wolf in the Western Carpathian Mountains, in Migration Corridors in the Western Carpathians, 2013, pp. 4–6.

    Google Scholar 

  59. Fabbri, E., Caniglia, R., Mucci, N., et al., Comparison of single nucleotide polymorphisms and microsatellites in non-invasive genetic monitoring of a wolf population, Arch. Biol. Sci. Belgrade, 2012, vol. 64, pp. 321–335.

    Article  Google Scholar 

  60. Milenkovic, M., Jojic Šipetic, V., Blagojevic, J., et al., Skull variation in Dinaric—Balkan and Carpathian gray wolf populations revealed by geometric morphometric approaches, J. Mamm., 2010, vol. 91, no. 2, pp. 376–386.

    Article  Google Scholar 

  61. Pilot, M., Jedrzejewski, W., Branicki, W., et al., Ecological factors influence population genetic structure of European grey wolves, Mol. Ecol., 2006, vol. 15, pp. 4533–4553.

    Article  CAS  PubMed  Google Scholar 

  62. Saccheri, I., Wilson, I.J., Nichols, R.A., et al., Inbreeding of bottlenecked butterfly populations: estimation using the likelihood of changes in marker allele frequencies, Genetics, 1999, vol. 151, pp. 1053–1063.

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Reed, J.M., Mills, J.R., Dunning, J.B., et al., Emerging issues in population viability analysis, Conserv. Biol., 2002, vol. 16, pp. 7–19.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. Šnjegota.

Additional information

The article is published in the original.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ðan, M., Šnjegota, D., Veličković, N. et al. Genetic variability and population structure of grey wolf (Canis lupus) in Serbia. Russ J Genet 52, 821–827 (2016). https://doi.org/10.1134/S1022795416080044

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795416080044

Keywords

Navigation