Abstract
In recent years, the golden jackal (Canis aureus) has rapidly expanded its distribution throughout Europe. In Bosnia and Herzegovina, the jackal has also been found to have increased its range, while establishing a core population in the northern lowlands of the country. This core population has been augmented by individuals from Serbia and Croatia, indicating an ongoing gene flow between the neighboring regions. Given the lack of comprehensive population-genetic data in the country, we aimed to produce the first information on jackal genetic diversity and population structure. We analyzed 24 autosomal microsatellite loci and found moderately high genetic diversity (Na = 5.83, Ho = 0.56, He = 0.59) in 48 jackals from Bosnia and Herzegovina, comparable to most other European populations. Analyses of population structure revealed two genetic clusters (K = 2) with an uncertain spatial pattern. Given the continuing expansion of its populations throughout Europe, the distribution of golden jackal is gradually overlapping with that of humans and other Canidae. Consequently, conflicts are steadily increasing, as are additional concerns regarding potential hybridization with dogs and wolves. This study is therefore a valuable contribution to the understanding of future actions and measures that should be established for jackals in Bosnia and Herzegovina.
References
Ahmetbegović S (2014) Reljef kao faktor razmještaja stanovništva u Bosni i Hercegovini. Acta Geographica Bosniae at Herzegovinae 1:97–111
Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Gen 11(10):697–709
Arbanas MS, Sečanj M, Bernat GS, Krkač M, Begić H, Džindo A, Zekan S, Arbanas Ž (2017) Landslides in the Dinarides and Pannonian Basin—from the largest historical and recent landslides in Croatia to catastrophic landslides caused by Cyclone Tamara (2014) in Bosnia and Herzegovina. Landslides 14:1861–1876
Ćirović D, Penezić A, Krofel M (2016) Jackals as cleaners: ecosystem services provided by a mesocarnivore in human-dominated landscapes. Biol Conserv 199:51–55
Cohen MT, King R, Dolev A, Boldo A, Lichter PA, Kahila BGG (2013) Genetic characterization of populations of the golden jackal and the red fox in Israel. Conserv Genet 14(1):55–63
Djan M, Šnjegota D, Veličković N, Stefanović M, Obreht VD, Ćirović D (2016) Genetic variability and population structure of grey wolf (Canis lupus) in Serbia. Russ J Genet 52(8):821–827
Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Res 14(1):209–214
Earl DA, VonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4(2):359–361
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620.
Fabbri E, Caniglia R, Galov A, Arbanasić H, Lapini L, Bošković I, Florijančić T, Vlasseva A, Atidzhe A, Mirchev R, Randi E (2014) Genetic structure and expansion of golden jackals (Canis aureus) in the north-western distribution range (Croatia and eastern Italian Alps). Conserv Genet 15(1):187–199
Francis RM (2017) pophelper: an R package and web app to analyse and visualize population structure. Mol Ecol Resour 17(1):27–32
Frankham R, Bradshaw CJ, Brook BW (2014) 50/500 or 100/1000 debate is not about the time frame-Reply to Rosenfeld. arXiv preprint arXiv:1406.6424.
Galov A, Fabbri E, Caniglia R, Arbanasić H, Lapalombella S, Florijančić T, Bošković I, Galaverni M, Randi E (2015) First evidence of hybridization between golden jackal (Canis aureus) and domestic dog (Canis familiaris) as revealed by genetic markers. R Soc Open Sci 2(12):15450
Goudet J, Jombart T (2015) Estimation and tests of hierarchical F-statistics. R Core Team, 58
Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9(5):1322–1332
Jombart T, Ahmed I (2011) adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinform 27(21):3070–3071
Katuwal HB, Dahal S (2013) Golden jackals in human dominated landscapes of the Manaslu Conservation Area. Nepal Vertebr Zool 63(3):329–334
Kemenszky P, Jánoska F, Nagy G, Csivincsik Á (2022) The golden jackal (Canis aureus) and the African swine fever pandemic: its role is controversial but not negligible (a diet analysis study). Vet Med Sci 8(1):97–103
Krofel M, Giannatos G, Ćirović D, Stoyanov S, Newsome TM (2017) Golden jackal expansion in Europe: a case of mesopredator release triggered by continent-wide wolf persecution? Hystrix 28(1):9–15
Kryštufek B, Murariu D, Kurtonur C (1997) Present distribution of the golden jackal Canis aureus in the Balkans and adjacent regions. Mammal Rev 27(2):109–114
Kusza S, Nagy K, Lanszki J, Heltai M, Szabó C, Czarnomska SD (2019) Moderate genetic variability and no genetic structure within the European golden jackal (Canis aureus) population in Hungary. Mammal Res 64(1):63–69
Milenković M (1987) The distribution of the jackals, Canis aureus Linnaeus 1758 (Mammalia, Canidae) in Yugoslavia. Proc Fauna SR Serbia 4:233–248
Mitchell-Jones AJ, Amori G, Bogdanowicz W, Krystufek B, Reijnders PJH, Spitzenberger F, Stubbe M, Thissen JBM, Zima JE (1999) The atlas of European mammals, vol 3. Academic Press, London
Moran PA (1948) The interpretation of statistical maps. J Royal Stat Soc 10(2):243–251
Moran PA (1950) A test for the serial independence of residuals. Biometrika 37(1/2):178–181
Moura AE, Tsingarska E, Dąbrowski MJ, Czarnomska SD, Jędrzejewska B, Pilot M (2014) Unregulated hunting and genetic recovery from a severe population decline: the cautionary case of Bulgarian wolves. Conserv Genet 15(2):405–417
Nikitović J (2020) Phenotypic and genotyping characterization of Bosnian broken-haired hound-Barak (Doctoral dissertation, University of Banja Luka, Faculty of Agriculture, Bosnia and Herzegovina)
Paradis E (2010) pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics 26(3):419–420
Penezić A, Ćirović D (2015) Seasonal variation in diet of the golden jackal (Canis aureus) in Serbia. Mammal Res 60(4):309–317
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959
R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43(1):223–225
Rutkowski R, Krofel M, Giannatos G, Ćirović D, Männil P, Volokh AM, Lanszki J, Heltai M, Szabó L, Banea OC, Yavruyan E, Hayrapetyan V, Kopaliani N, Miliou A, Tryfonopoulos A, Lymberakis P, Penezić A, Pakeltytė G, Suchecka E, Bogdanowicz W (2015) A European concern? Genetic structure and expansion of golden jackals (Canis aureus) in Europe and the Caucasus. PLoS ONE 10(11):e0141236
Sambrook J, Russell DW (2001) Molecular Cloning-Sambrook & Russel-Vol. 1, 2, 3. Cold Springs Harbor Lab Press: Long Island, NY, USA
Selimovic A, Schöll EM, Bosseler L, Hatlauf J (2021) Habitat use of golden jackals (Canis aureus) in riverine areas of northern Bosnia and Herzegovina. Eur J Wildl Res 67(1):1–8
Shakarashvili M, Kopaliani N, Gurielidze Z, Dekanoidze D, Ninua L, Tarkhnishvili D (2020) Population genetic structure and dispersal patterns of grey wolfs (Canis lupus) and golden jackals (Canis aureus) in Georgia, the Caucasus. J Zool 312(4):227–238
Šnjegota D, Stefanović M, Veličković N, Ćirović D, Djan M (2018) Genetic characterization of grey wolves (Canis lupus L. 1758) from Bosnia and Herzegovina: implications for conservation. Conserv Genet 19(3):755–760
Šnjegota D, Stronen AV, Boljte B, Ćirović D, Djan M, Huber D, Jelnečič M, Konec M, Kusak J, Skrbinšek T (2021) Population genetic structure of wolves in the northwestern Dinaric-Balkan region. Ecol Evol 11(24):18492–18504
Sofradžija A, Muzaferović Š (2007) Biodiverzitet sisara Bosne i Hercegovine: katalog. Institut za genetičko inženjerstvo i biotehnologiju
Spassov N, Acosta-Pankov I (2019) Dispersal history of the golden jackal (Canis aureus moreoticus Geoffroy, 1835) in Europe and possible causes of its recent population explosion. BDJ 7
Stronen AV, Konec M, Boljte B, Bošković I, Gačić D, Galov A, Heltai M, Jelenčič M, Kljun F, Kos I, Kovačić T, Lanszki J, Pintur K, Pokorny B, Skrbinšek T, Suchentrunk F, Szabó L, Šprem N, Tomljanović K, Potočnik H (2021) Population genetic structure in a rapidly expanding mesocarnivore: golden jackals in the Dinaric-Pannonian region. Glob Ecol Conserv 28:e01707
Trbojević I, Trbojević T, Malešević D, Krofel M (2018) The golden jackal (Canis aureus) in Bosnia and Herzegovina: density of territorial groups, population trend and distribution range. Mammal Res 63(3):341–348
Trouwborst A, Krofel M, Linnell JD (2015) Legal implications of range expansions in a terrestrial carnivore: the case of the golden jackal (Canis aureus) in Europe. Biodivers Conserv 24(10):2593–2610
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4(3):535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x
Waples RS, Do CHI (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3(3):244–262
Zachos FE, Ćirović D, Kirschning J, Otto M, Hartl GB, Petersen B, Honnen AC (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(3):241–250
Acknowledgements
We thank the Srna – Srbac Hunting Association, and numerous hunters and foresters throughout Bosnia and Herzegovina for their help in sampling. Our special thanks go to Astrid Vik Stronen for valuable comments during the preparation of the manuscript and Richard Harrison-Cripps for technical assistance.
Funding
This study was financially supported by the Rufford Foundation, UK, and by the Serbian Ministry of Education, Science, and Technological Development (451–03-68/2022–14/ 200178).
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All authors contributed to the study conception and design. Material preparation, data collection, and data analyses were performed by Dragana Šnjegota. The first draft of the manuscript was written by Dragana Šnjegota. All authors commented on previous versions of the manuscript, read, and approved the final manuscript.
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Nikitović, J., Djan, M., Ćirović, D. et al. The first report on genetic variability and population structure in jackals from Bosnia and Herzegovina. Mamm Res 68, 243–247 (2023). https://doi.org/10.1007/s13364-022-00665-z
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DOI: https://doi.org/10.1007/s13364-022-00665-z