Skip to main content

Advertisement

Log in

Genetic structure and expansion of golden jackals (Canis aureus) in the north-western distribution range (Croatia and eastern Italian Alps)

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

The golden jackal, widely distributed in Europe, Asia and Africa, is one of the less studied carnivores in the world and the genetic structure of the European populations is unknown. In the last century jackals strongly declined mainly due to human persecution, but recently they expanded again in eastern Europe. With the aim to determine the genetic structure and the origin of expanding jackals, we analyzed population samples obtained from Bulgaria, Serbia, Croatia (Dalmatia and Slavonia) and individuals sampled in north-eastern Italy. Samples were typed at the hypervariable part of the mitochondrial DNA control-region (mtDNA CR1) and at 15 canine autosomal microsatellite loci (STR), and analyzed using multivariate, Bayesian and landscape genetic methods. The mtDNA CR1 was monomorphic, showing a single haplotype shared among all the populations. The STR loci were variable, with 2–14 alleles and intermediate values of heterozygosity (Ho = 0.47; He = 0.51). Genetic diversity was significantly partitioned (θST = 0.07; P < 0.001) and the populations were partially distinct, perhaps in consequence of recent fragmentations. Jackals from Dalmatia were the most genetically differentiated. Assignment testing and gene flow analyses suggested that jackals colonizing Italy have admixed origins from Dalmatian and Slavonian populations. They are not first generation migrants, suggesting that dispersal towards north-eastern Italy is a stepping-stone process. Golden jackal and wolf colonization patterns might be different, with prevalent short-distance dispersal in jackals versus prevalent long distance dispersal in wolves. The admixed origin of jackals in the Alps ensures abundant genetic variability, which may enhance adaptive fitness and expectancy of population growth. The intersections between Dinaric–Balkan and Eastern Alps are areas of population expansion and admixture, highlighting their conservation, ecological and evolutionary values.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aguilar A, Roemer G, Debenham S, Binns M, Garcelon D, Wayne RK (2004) High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci USA 101:3490–3494

    Article  CAS  PubMed  Google Scholar 

  • Arnold J, Humer A, Heltai M, Murariu D, Spassov N, Hackländer K (2012) Current status and distribution of golden jackals Canis aureus in Europe. Mamm Rev 42:1–11

    Article  Google Scholar 

  • Banea OC, Krofel M, Červinka J, Gargarea P, Szabó L (2012) New records, first estimates of densities and questions of applied ecology for jackals in Danube Delta Biosphere Reserve and hunting terrains from Romania. Acta Zool Bulg 64:353–366

    Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) Genetix 4.05, logiciel sous Windows TM pour la génétique des Populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier, France

  • Caniglia R, Fabbri E, Mastrogiuseppe L, Randi E (2013) Who is who? Identification of livestock predators using forensic genetic approaches. Forensic Sci Int Genet 7:397–404

    Article  CAS  PubMed  Google Scholar 

  • Cohen TM, King R, Dolev A, Boldo A, Lichter-Peled A, Bar-Gal GK (2013) Genetic characterization of populations of the golden jackal and the red fox in Israel. Con Gen 14:55–63

    Article  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:611–2620

    Google Scholar 

  • 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 131:479–491

    CAS  PubMed  Google Scholar 

  • Fabbri E, Miquel C, Luchini V, Santini A, Caniglia R, Duchamp C, Weber J-M, Lequette B, Marucco F, Boitani L, Fumagalli L, Taberlet P, Randi E (2007) From the Apennines to the Alps: colonization genetics of the naturally expanding Italian wolf (Canis lupus) population. Mol Ecol 16:1661–1671

    Article  CAS  PubMed  Google Scholar 

  • Fabbri E, Caniglia R, Kusak J, Galov A, Gomerčić T, Arbanasić H, Huber D, Randi E (2013) 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 (in press)

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  Google Scholar 

  • Faubet P, Waples RS, Gaggiotti OE (2007) Evaluating the performance of a multilocus Bayesian method for the estimation of migration rates. Mol Ecol 16:1149–1166

    Article  PubMed  Google Scholar 

  • Francisco LV, Langston AA, Mellersh CS, Neal CL, Ostrander EA (1996) A class of highly polymorphic tetranucleotide repeats for canine genetic mapping. Mamm Genome 7:359–362

    Article  CAS  PubMed  Google Scholar 

  • Fredholm M, Wintero AK (1995) Variation of short tandem repeats within and between species belonging to the Canidae family. Mamm Genome 6:11–18

    Article  CAS  PubMed  Google Scholar 

  • Genov P, Wassilev S (1989) Der Schakal (Canis aureus L.) in Bulgarien. Ein Beitrag zu seiner Verbreitung und Biologie. Z Jagdwiss 35:145–150

    Google Scholar 

  • Giannatos G (2004) Conservation action plan for the golden jackal Canis aureus L. in Greece. WWF Greece, p 47

  • Goudet J (1995) Fstat (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Guillot G (2008) Inference of structure in subdivided populations at low levels of genetic differentiation. The correlated allele frequencies model revisited. Bioinformatics 24:2222–2228

    Article  CAS  PubMed  Google Scholar 

  • Guillot G, Mortier F, Estoup A (2005) Geneland: a computer package for landscape genetics. Mol Ecol Notes 5:708–711

    Article  Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Article  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/97/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hubisz M, Falush D, Stephens M, Pritchard J (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

    Article  PubMed Central  PubMed  Google Scholar 

  • Humer A, Heltai M, Murariu D, Spassov N, Häcklander K (2007) Current status and distribution of golden jackals (Canis aureus) in Europe. In: Sjöberg K, Tuulikki R (eds) Abstracts XXVII Congress IUGB, Uppsala, Sweden. Swedish University of Agricultural Sciences, Umeå, p 272

  • Ibrahim KM, Nichols RA, Hewitt GM (1996) Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77:282–291

    Article  Google Scholar 

  • Jombart T, Devillard S, Dufour A-B, Pontier D (2008) Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 101:92–103

    Article  CAS  PubMed  Google Scholar 

  • Kaeuffer R, Réale D, Coltman DW, Pontier D (2007) Detecting population structure using STRUCTURE software: effect of background linkage disequilibrium. Heredity 99:374–380

    Article  CAS  PubMed  Google Scholar 

  • Kalinowski ST (2011) The computer program STRUCTURE does not reliably identify the main genetic clusters within species: simulations and implications for human population structure. Heredity 106:625–632

    Article  CAS  PubMed  Google Scholar 

  • Kryštufek B, Tvrtković N (1990) Range expansion by Dalmatian jackal population in the 20th century (Canis aureus L. 1758). Folia Zool 39:291–296

    Google Scholar 

  • Kryštufek B, Murariu D, Kurtonur C (1997) Present distribution of the Golden Jackal Canis aureus in the Balkans and adjacent regions. Mamm Review 27:109–114

    Article  Google Scholar 

  • Lapini L (2006) Il cane viverrino Nyctereutes procyonoides ussuriensis Matschie, 1908 in Italia: segnalazioni 1980–2005 (Mammalia: Carnivora: Canidae). Boll Mus Civ St Nat Venezia 57:235–239

    Google Scholar 

  • Lapini L, Bonesi L (2011) Evidence of a natural recovery of the Eurasian otter in northeast Italy. In: Proceedings of the 29th European Mustelid Colloquium, Southampton, UK

  • Lapini L, Dall’Asta A, Dublo L, Spoto M, Vernier E (1996) Materials for the theriofauna in north-eastern Italy (Mammalia, Friuli-Venezia Giulia) Gortania. In: Proceeding of the museum of the natural history of friuli 17, pp 149–248 (in Italian)

  • Lapini L, Molinari P, Dorigo L, Are G, Beraldo P (2009) Reproduction of the golden jackal (Canis aureus moreoticus I. Geoffroy Saint Hilaire, 1835) in Julian pre-Alps, with new data on its range-expansion in the high-adriatic Hinterland (Mammalia, Carnivora, Canidae). Boll Mus Civ St Nat Venezia 60:169–186

    Google Scholar 

  • Lapini L, Brugnoli S, Krofel M, Kranz A, Molinari P (2010) A grey wolf (Canis lupus Linné, 1758) from Fiemme Valley (Mammalia: Canidae: north-eastern Italy). Boll Mus Civ St Nat Venezia 61:117–129

    Google Scholar 

  • Lapini L, Conte D, Zupan M, Kozlan L (2011) Italian jackals 1984–2011. An updated review (Canis aureus: Carnivora, Canidae). Boll Mus Civ St Nat Venezia 62:219–232

    Google Scholar 

  • Mawdsley JR, O’Malley R, Ojima DS (2008) A review of climate-change adaptation strategies for wildlife management and biodiversity. Conserv Biol 23:1080–1089

    Article  Google Scholar 

  • Mech LD (1970) The wolf: the ecology and behavior of an endangered species. Natural History Press, Garden City, NY

  • Mucci N, Arrendal J, Ansorge H et al (2010) Genetic diversity and landscape genetic structure of otter (Lutra lutra) populations in Europe. Conserv Genet 11:583–599

    Article  Google Scholar 

  • Oliveira R, Godinho R, Randi E, Alves PC (2008) Hybridization versus conservation: are domestic cats threatening the genetic integrity of wildcats (Felis silvestris silvestris) in Iberian Peninsula? Philos Trans R Soc B 363:2953–2961

    Article  Google Scholar 

  • Ostrander EA, Sprague GF, Rine J (1993) Identification and characterization of dinucleotide repeat (CA)n markers for genetic mapping in dog. Genomics 16:207–213

    Article  CAS  PubMed  Google Scholar 

  • Paetkau D, Slade R, Burdens M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation based exploration of accuracy and power. Mol Ecol 13:55–65

    Article  CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  Google Scholar 

  • Quignon P, Rimbault M, Robin S, Galibert F (2012) Genetics of canine olfaction and receptor diversity. Mamm Genome 23:132–143

    Article  PubMed  Google Scholar 

  • Randi E (2008) Detecting hybridization between wild species and their domesticated relatives. Mol Ecol 17:285–293

    Article  PubMed  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    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

    Article  PubMed  Google Scholar 

  • Selanec J, Lauš B, Sindičić M (2011) Golden jackal (Canis aureus) distribution in Croatia. In: Abstract of VI European Congress of mammalogy, Paris, France, p 60

  • Sillero-Zubiri C, Hoffmann M, Macdonald DW (2004) Canids: foxes, wolves, jackals and dogs: status survey and conservation action plan, 2nd edn. IUCN Canid Specialist Group, Cambridge

    Google Scholar 

  • Simon C (1991) Molecular systematics at the species boundary: exploiting conserved and variable regions of the mitochondrial genome of animals via direct sequencing from amplified DNA. In: Hewitt GM, Johnston AWB, Young JPW (eds) Molecular techniques in taxonomy. Springer, Berlin, pp 33–71

    Chapter  Google Scholar 

  • Spassov N (1989) The position of jackals in the Canis genus and life-history of the golden jackal (Canis aureus L.) in Bulgaria and on Balkans. Hist Nat Bulg 1:44–56

    Google Scholar 

  • Taryannikov VI (1977) On the population structure and dynamics of Canis aureus aureus in the Syrdarja river valley. Zool Z Mosca 71:1423–1425

    Google Scholar 

  • Trouwborst A (2010) Managing the carnivore comeback: international and EU species protection law and the return of lynx, wolf and bear to western Europe. J Environ Law 22:347–372

    Article  Google Scholar 

  • Valière N, Fumagalli L, Gielly L, Miquel C, Lequette B, Poulle M-L, Weber J-M, Arlettaz R, Taberlet P (2003) Long-distance wolf recolonization of France and Switzerland inferred from non-invasive genetic sampling over a period of 10 years. Animal Conserv 6:83–92

    Article  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Microchecker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Vila C, Sundqvist AK, Flagstad O et al (2003) Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant. Proc R Soc London B 270:91–97

    Article  Google Scholar 

  • vonHoldt B, Stahler D, Pollinger J, Smith D, Bangs E et al (2010) A novel assessment of population structure and gene flow in gray wolf populations of the Northern Rocky Mountains of the United States. Mol Ecol 19:4412–4427

    Article  PubMed  Google Scholar 

  • Waits LP, Paetkau D (2005) Noninvasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection. J Wildl Manag 69:1419–1433

    Article  Google Scholar 

  • Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256

    Article  CAS  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistic for the analysis of population structure. Evolution 6:1358–1370

    Article  Google Scholar 

  • Whitlock MC, Maccauley DE (1999) Indirect measures of gene flow and migration: Fst =/1/(4Nm + 1). Heredity 82:117–125

    Article  PubMed  Google Scholar 

  • Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    PubMed  Google Scholar 

  • Zachos FE, Cirovic D, Kirschning J, Otto M, Hartl GB, Petersen B, Honnen A (2009) Genetic variability, differentiation, and founder effect in golden jackals (Canis aureus) from Serbia as revealed by mitochondrial DNA and nuclear microsatellite loci. Biochem Genet 47:241–250

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We warmly thank everybody who made it possible to realize this research project, and that contributed to obtain samples used in this study. This project was supported by ISPRA, by the Italian Ministry of Environment, Direction of Nature Protection, and it was partly supported by the European Social Fund through the Ministry of Education, Youth and Science of Bulgaria (BG051PO001-3.3.04/41). We are particularly grateful to Aritz Ruiz-Gonzalez for his useful suggestions and help in landscape genetic analysis and for his comments on a preliminary version of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elena Fabbri.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fabbri, E., Caniglia, R., Galov, A. et al. Genetic structure and expansion of golden jackals (Canis aureus) in the north-western distribution range (Croatia and eastern Italian Alps). Conserv Genet 15, 187–199 (2014). https://doi.org/10.1007/s10592-013-0530-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-013-0530-7

Keywords

pFad - Phonifier reborn

Pfad - The Proxy pFad of © 2024 Garber Painting. All rights reserved.

Note: This service is not intended for secure transactions such as banking, social media, email, or purchasing. Use at your own risk. We assume no liability whatsoever for broken pages.


Alternative Proxies:

Alternative Proxy

pFad Proxy

pFad v3 Proxy

pFad v4 Proxy