Biochemical Genetics

, Volume 47, Issue 3–4, pp 241–250 | Cite as

Genetic Variability, Differentiation, and Founder Effect in Golden Jackals (Canis aureus) from Serbia as Revealed by Mitochondrial DNA and Nuclear Microsatellite Loci

  • Frank E. ZachosEmail author
  • Dusko Cirovic
  • Julia Kirschning
  • Marthe Otto
  • Günther B. Hartl
  • Britt Petersen
  • Ann-Christin Honnen


We analyzed 121 golden jackals (Canis aureus) from six sample sites in Serbia with regard to genetic variability and differentiation as revealed by mitochondrial control region sequences and eight nuclear microsatellite loci. There was no variation at all in the mtDNA sequences, and nuclear variability was very low (average observed and expected heterozygosity of 0.29 and 0.34, respectively). This is in line with the considerable recent range expansion of this species in the Balkans and indicates a strong founder effect in the recently established Serbian population. We did not find evidence of differentiation between the northeastern jackals and those from the plain of Srem or those in between. F-statistics and Bayesian Structure analyses, however, were indicative of a low degree of overall differentiation in the Serbian population. A vagrant Austrian jackal that was also analyzed was genetically indistinguishable from its Serbian conspecifics.


Canis aureus Serbia Founder effect Microsatellites Mitochondrial DNA 



The authors wish to express their gratitude to all persons involved in the collection of samples: Zoran Gubin (Smederevo), Borko Dimitrijevic (Svilajnac), Zivorad Pavlovic (Velika Plana), Sladan Markovic and Nenad Mirkovic (Veliko Gradiste), and Franz Suchentrunk (Austria).


  1. Bauer K, Suchentrunk F (1995) Weitere Ausbreitung des Goldschakals Canis aureus L., 1758 in Österreich. Z Säugetierkd 60:307–309Google Scholar
  2. Belkhir K (2000) Genetix v. 4.01. Laboratoire Génome et Populations, CNRS UPR 9060, Université de MontpellierGoogle Scholar
  3. Ben Slimen H, Suchentrunk F, Shahin AB, Ben Ammar Elgaaied A (2007) Phylogenetic analysis of mtCR-1 sequences of Tunisian and Egyptian hares (Lepus sp. or spp., Lagomorpha) with different coat colours. Mamm Biol 72:224–239CrossRefGoogle Scholar
  4. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Am J Hum Genet 19:233–257PubMedGoogle Scholar
  5. Demeter A, Spassov N (1993) Canis aureus Linnaeus, 1758–Schakal, Goldschakal. In: Niethammer J, Krapp F (eds) Handbuch der Säugetiere Europas, vol 5/I Raubsäuger (Part I). AULA-Verlag, Wiesbaden, Germany, pp 107–138Google Scholar
  6. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  7. Ewen KR, Bahlo M, Treloar SA, Levinson DF, Mowry B, Barlow JW, Foote SJ (2000) Identification and analysis of error types in high-throughput genotyping. Am J Hum Genet 67:727–736PubMedCrossRefGoogle Scholar
  8. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedGoogle Scholar
  9. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedGoogle Scholar
  10. Genov P, Wassilev S (1989) Der Schakal (Canis aureus L.) in Bulgarien. Ein Beitrag zu seiner Verbreitung und Biologie. Z Jagdwiss 35:145–150CrossRefGoogle Scholar
  11. Giannatos G, Marinos Y, Maragou P, Catsadorakis G (2005) The status of the Golden Jackal (Canis aureus L.). Belg J Zool 135:145–149 (in Greece)Google Scholar
  12. Goudet J (1995) FStat (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  13. 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
  14. Hajji GM, Zachos FE, Charfi-Cheikrouha F, Hartl GB (2007) Conservation genetics of the imperilled Barbary red deer in Tunisia. Anim Conserv 10:229–235CrossRefGoogle Scholar
  15. Hmwe SS, Zachos FE, Eckert I, Lorenzini R, Fico R, Hartl GB (2006) Conservation genetics of the endangered red deer from Sardinia and Mesola with further remarks on the phylogeography of Cervus elaphus corsicanus. Biol J Linn Soc 88:691–701CrossRefGoogle Scholar
  16. Kirschning J, Zachos FE, Cirovic D, Radovic IT, Hmwe SS, Hartl GB (2007) Population genetic analysis of Serbian red foxes (Vulpes vulpes) by means of mitochondrial control region sequences. Biochem Genet 45:409–420PubMedCrossRefGoogle Scholar
  17. Krystufek B, Tvrtkovic N (1990) Range expansion by Dalmation jackal population in the 20th century (Canis aureus Linnaeus, 1758). Folia Zool 39:291–296Google Scholar
  18. Krystufek B, Murariu D, Kurtonur C (1997) Present distribution of the Golden Jackal Canis aureus in the Balkans and adjacent regions. Mammal Rev 27:109–114CrossRefGoogle Scholar
  19. Kühn W (1935) Die dalmatinischen Schakale. Z Säugetierkd 10:144–146Google Scholar
  20. Lucchini V, Galov A, Randi E (2004) Evidence of genetic distinction and long-term population decline in wolves (Canis lupus) in the Italian Apennines. Mol Ecol 13:523–536PubMedCrossRefGoogle Scholar
  21. Milenkovic M (1987) The distribution of the jackal, Canis aureus Linnaeus, 1758 (Mammalia, Canidae) in Yugoslavia. In: Proceeding on the Fauna of SR Serbia, 4:233–248 (in Serbian with an English summary)Google Scholar
  22. Mitchell-Jones AJ, Amori G, Bogdanowicz W, Krystufek B, Reijnders PJH, Spitzenberger F, Stubbe M, Thissen JBM, Vohralík V, Zima J (1999) The atlas of European mammals. T. & A. D. Poyser, London, EnglandGoogle Scholar
  23. Nei M (1972) Genetic distance between populations. Am Nat 106:283–292CrossRefGoogle Scholar
  24. Ostrander EA, Sprague GF, Rine J (1993) Identification and characterization of dinucleotide repeat (CA)n markers for genetic mapping in dog. Genomics 16:207–213PubMedCrossRefGoogle Scholar
  25. Ostrander EA, Mapa FA, Yee M, Rine J (1995) One hundred and one new simple sequence repeat-based markers for the canine genome. Mamm Genome 6:192–195PubMedCrossRefGoogle Scholar
  26. Pemberton JM, Slate J, Bancroft DR, Barrett JA (1995) Nonamplifying alleles at microsatellite loci: a caution for parentage and population studies. Mol Ecol 4:249–252PubMedCrossRefGoogle Scholar
  27. Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539PubMedCrossRefGoogle Scholar
  28. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  29. Raymond M, Rousset F (1995) Genepop (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  30. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  31. Roy MS, Geffen E, Smith D, Ostrander EA, Wayne RK (1994) Patterns of differentiation and hybridization in North American wolflike canids, revealed by analysis of microsatellite loci. Mol Biol Evol 11:553–570PubMedGoogle Scholar
  32. Sommer R, Benecke N (2005) Late-Pleistocene and early Holocene history of the canid fauna of Europe (Canidae). Mamm Biol 70:227–241CrossRefGoogle Scholar
  33. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-Checker (version 2.2.3): software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  34. Wahlund S (1928) Zusammensetzung von Populationen und Korrelationserscheinungen vom Standpunkt der Vererbungslehre aus betrachtet. Hereditas 11:65–106CrossRefGoogle Scholar
  35. Wattier R, Engel CR, Saumitou-Laprade P, Valero M (1998) Short allele dominance as a source of heterozygote deficiency at microsatellite loci: experimental evidence at the dinucleotide locus Gv1CT in Gracilaria gracilis (Rhodophyta). Mol Ecol 7:1569–1573CrossRefGoogle Scholar
  36. Zachos F, Hartl GB, Apollonio M, Reutershan T (2003) On the phylogeographic origin of the Corsican red deer (Cervus elaphus corsicanus): evidence from microsatellites and mitochondrial DNA. Mamm Biol 68:284–298CrossRefGoogle Scholar
  37. Zachos FE, Hmwe SS, Hartl GB (2006) Biochemical and DNA markers yield strikingly different results regarding variability and differentiation of roe deer (Capreolus capreolus, Artiodactyla: Cervidae) populations from northern Germany. J Zool Syst Evol Res 44:167–174CrossRefGoogle Scholar
  38. Zachos FE, Althoff C, v Steynitz Y, Eckert I, Hartl GB (2007a) Genetic analysis of an isolated red deer (Cervus elaphus) population showing signs of inbreeding depression. Eur J Wildl Res 53:61–67CrossRefGoogle Scholar
  39. Zachos FE, Cirovic D, Rottgardt I, Seiffert B, Oeking S, Eckert I, Hartl GB (2007b) Geographically large-scale genetic monomorphism in a highly successful introduced species: the case of the muskrat (Ondatra zibethicus) in Europe. Mamm Biol 72:123–126CrossRefGoogle Scholar
  40. Zachos FE, Otto M, Unici R, Lorenzini R, Hartl GB (2008) Evidence of a phylogeographic break in the Romanian brown bear (Ursus arctos) population from the Carpathians. Mamm Biol 73:93–101CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Frank E. Zachos
    • 1
    Email author
  • Dusko Cirovic
    • 2
  • Julia Kirschning
    • 1
  • Marthe Otto
    • 1
  • Günther B. Hartl
    • 1
  • Britt Petersen
    • 1
  • Ann-Christin Honnen
    • 1
  1. 1.Zoological InstituteChristian-Albrechts-UniversityKielGermany
  2. 2.Faculty of BiologyUniversity of BelgradeBelgradeSerbia

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