Genetic structure of expanding wolf (Canis lupus) populations in Italy and Croatia, and the early steps of the recolonization of the Eastern Alps
Abstract
After centuries of range contraction and demographic declines wolves are now expanding in Europe, colonizing regions from where they have been absent for centuries. Wolf colonizing the western Alps originate by the expansion of the Italian population. Vagrant wolves of Italian and Dinaric-Balkan origins have been recently observed in the Eastern Alps. In this study we compared the genetic structure of wolf populations in Italy and Croatia, aiming to identify the sources of the ongoing recolonization of the Eastern Alps. DNA samples, extracted from 282 Italian and 152 Croatian wolves, were genotyped at 12 autosomal microsatellites (STR), four Y-linked STR and at the hypervariable part of the mitochondrial DNA control-region (mtDNA CR1). Wolves in Croatia and Italy underwent recent demographic bottlenecks, but they differ in genetic diversity and population structure. Wolves in Croatia were more variable at STR loci (NA = 7.4, HO = 0.66, HE = 0.72; n = 152) than wolves in Italy (NA = 5.3, HO = 0.57, HE = 0.58; n = 282). We found four mitochondrial DNA (mtDNA CR1) and 11 Y-STR haplotypes in Croatian wolves, but only one mtDNA CR1 and three Y-STR haplotypes in Italy. Wolves in Croatia were subdivided into three genetically distinct subpopulations (in Dalmatia, Gorski kotar and Lika regions), while Italian wolves were not sub-structured. Assignment testing shows that the eastern and central Alps are recolonized by wolves dispersing from both the Italian and Dinaric populations. The recolonization of the Alps will predictably continue in the future and the new population will be genetically admixed and very variable with greater opportunities for local adaptations and survival.
Keywords
Canis lupus Colonization genetics Genetic structure Landscape genetics Population expansionPreview
Unable to display preview. Download preview PDF.
References
- Adamič, M., 1992. Status of the wolf (Canis lupus L.) in Slovenia. In: Promberger, C., Schröder, W. (Eds.), Proceedings of the Workshop: Wolves in Europe – Current Status, Prospects. Oberammergau, Germany, pp. 71–73.Google Scholar
- Allendorf, F.W., Leary, R.F., Spruell, P., Wenburg, J.K., 2001. The problems with hybrids: setting conservation guidelines. Trends Ecol. Evol. 16, 613–622.CrossRefGoogle Scholar
- Arnold, M.L., Martin, N.H., 2009. Adaptation by introgression. J. Biol. 8, 82.PubMedPubMedCentralCrossRefGoogle 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.Google Scholar
- Boitani, L., 2000. Action plan for conservation of the wolves (Canis lupus) in Europe. Nature and Environment N. 113 Council of Europe Publishing, Strasbourg, France.Google Scholar
- Boitani, L., 2003. Wolf conservation and recovery. In: Mech, L.D., Boitani, L. (Eds.), Wolves: Behavior, Ecology and Conservation. University of Chicago Press, Chicago, pp. 317–340.Google Scholar
- Breitenmoser, U., 1998. Large predators in the Alps: the fall and rise of Man’s competitors. Biol. Conserv. 83, 279–289.CrossRefGoogle Scholar
- Caniglia, R., Fabbri, E., Greco, C., Galaverni, M., Manghi, L., Boitani, L., Sforzi, A., Randi, E., 2013a. Black coats in an admixed wolf × dog pack is melanism an indicator of hybridization in wolves? Eur. J. Wildl. Res. 59, 543–555.CrossRefGoogle Scholar
- Caniglia, R., Fabbri, E., Mastrogiuseppe, L., Randi, E., 2013b. Who is Who? Identification of livestock predators using forensic genetic approaches. Forensic Sci. Int. Genet. 7, 397–404.PubMedCrossRefGoogle Scholar
- Carmichael, L.E., Nagy, J.A., Larter, N.C., Strobeck, C., 2001. Prey specialization may influence patterns of gene flow in wolves of the Canadian Northwest. Mol. Ecol. 12, 787–2798.Google Scholar
- Ciucci, P., Reggioni, W., Maiorano, L., Boitani, L., 2009. Long-distance dispersal of a rescued wolf from the northern Apennines to the western Alps. J. Wildl. Manag. 73, 1300–1306.CrossRefGoogle Scholar
- Ciucci, P., Boitani, L., Francisci, F., Andreoli, G., 1997. Home range, activity and movements of a wolf pack in central Italy. J. Zool. 243, 803–819.CrossRefGoogle Scholar
- Czarnomska, S.D., Jędrzejewska, B., Borowik, T., Niedziałkowska, M., Stronen, A.V., Nowak, S., Mysłajek, R.W., Okarma, H., Konopiň ski, M., Pilot, M., S´mietana, W., Caniglia, R., Fabbri, E., Randi, E., Pertoldi, C., Jędrzejewski, W., 2013. Concordant mitochondrial and microsatellite DNA structuring between Polish lowland and Carpathian Mountain wolves. Conserv. Genet. 14, 573–588.CrossRefGoogle 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
- Fabbri, E., Miquel, C., Lucchini, V., Santini, A., Caniglia, R., Duchamp, C., Weber, J.M., Lequette, B., Marucco, F., Boitani, L., Fumagalli, L., Taberlet, P., Randi, E., 2007. FromtheApenninestotheAlps:colonizationgeneticsofthenaturallyexpanding Italian wolf (Canis lupus) population. Mol. Ecol. 16, 1661–1671.PubMedCrossRefGoogle Scholar
- Falush, D., Stephens, M., Pritchard, J.K., 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587.PubMedPubMedCentralGoogle Scholar
- Frković, A., Huber, Ð., 1992. Wolves in Croatia: baseline data. In: Promberger, C., Schröder, W. (Eds.), Proceedings of the Workshop: Wolves in Europe – Current Status, Prospects. Oberammergau, Germany, pp. 67–69.Google Scholar
- Geffen, E., Anderson, M.J., Wayne, R.K., 2004. Climate and habitat barriers todispersal in the highly mobile grey wolf. Mol. Ecol. 13, 2481–2490.PubMedCrossRefGoogle Scholar
- Gomerčić, T., Sindičić, M., Galov, A., Arbanasić, H., Kusak, J., Kocijan, I., Gomerčić, M., Huber, Ð., 2010. High genetic variability of the grey wolf (Canis lupus L.) population from Croatia as revealed by mitochondrial DNA control region sequences. Zool. Studies 49, 816–823.Google Scholar
- Goudet, J., 1995. Fstat (Version 1.2): a computer program to calculate F-statistics. J. Hered. 86, 485–486.CrossRefGoogle Scholar
- Groff, C., Pedrini, P., 2009. Attenti al lupo . . . Avvistabile anche in Trentino! Natura Alpina 60, 1–12.Google Scholar
- Guillot, G., Mortier, F., Estoup, A., 2005. Geneland: a computer package for landscape genetics. Mol. Ecol. Notes 5, 708–711.CrossRefGoogle Scholar
- Hailer, F., Leonard, J.A., 2008. Hybridization among Three Native North American Species in a Region of Natural Sympatry. PLoS ONE 10, e3333.Google Scholar
- Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/97/NT. Nucleic Acids Symp. Ser. 41, 95–98.Google Scholar
- Hedrick, P.W., Fredrickson, R., 2010. Genetic rescue guidelines with examples from Mexican wolves and Florida panthers. Conserv. Genet. 11, 615–626.CrossRefGoogle Scholar
- Hofreiter, M., Stewart, J., 2009. Ecological change, range fluctuations and population dynamics during the Pleistocene. Curr. Biol. 19, 584–594.CrossRefGoogle Scholar
- Hubisz, M., Falush, D., Stephens, M., Pritchard, J., 2009. Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Res. 9, 1322–1332.CrossRefGoogle Scholar
- Hurlbert, S.H., 1971. The non-concept of species diversity: a critique and alternative parameters. Ecology 52, 577–586.PubMedCrossRefGoogle Scholar
- Ibrahim, K.M., Nichols, R.A., Hewitt, G.M., 1996. Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77, 282–291.CrossRefGoogle Scholar
- Jędrzejewski, W., Niedziałkowska, M., Hayward, M.W., Goszczyň ski, J., Jędrzejewska, B., Borowik, T., Bartoň , K.A., Nowak, S., Harmuszkiewicz, J., Juszczyk, A., Kałamarz, T., Kloch, A., Koniuch, J., Kotiuk, K., Mysłajek, R.W., Nȩdzyń ska, M., Olczyk, A., Teleon, M., Wojtulewicz, M., 2012. Prey choice and diet in wolves related to differentiation of ungulate communities and corresponding wolf subpopulations in Poland. J. Mamm. 93, 1480–1492.CrossRefGoogle 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.PubMedCrossRefGoogle Scholar
- Kays, R., Curtis, A., Kirchman, J.J., 2010. Rapid adaptive evolution of northeastern coyotes via hybridization with wolves. Biol. Lett. 6, 89–93.PubMedCrossRefGoogle Scholar
- Kojola, I., Aspi, J., Hakala, A., Heikinen, S., Ilmoni, C., Ronkainen, S., 2006. Dispersal in an expanding wolf population in Finland. J. Mamm. 87, 281–286.CrossRefGoogle 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
- Kusak, J., 2002. Uvjeti za život vuka (Canis lupus L.) u Hrvatskoj. Prirodoslovno-matematički fakultet Sveučilišta u Zagrebu, Zagreb.Google Scholar
- Kusak, J., 2010. Kretanje vukova i struktura čopora. In: Štrbenac, A (Ed.), Plan upravl-janja vukom u Republici Hrvatskoj. DZZP, Zagreb, pp. 21–26.Google Scholar
- Kusak, J., Huber, Ð., 2010a. Dinamika, brojnost i trend populacije vuka od 1992. do 2008. godine. In: Štrbenac, A. (Ed.), Plan upravljanja vukom u Republici Hrvatskoj. DZZP, Zagreb, pp. 21–23.Google Scholar
- Kusak, J., Huber, Ð., 2010b. Rasprostranjenost. In: Štrbenac, A. (Ed.), Plan upravl-janja vukom u Republici Hrvatskoj. Državni zavod za zaštitu prirode, Zagreb, pp. 14–15.Google Scholar
- Kusak, J., Krapinec, K., 2010. Ungulates and their management in Croatia. In: Apollonio, M., Andersen, R., Putman, R. (Eds.), European Ungulates and Their Management in the 21st Century. Cambridge University Press, New York, pp. 527–539.Google Scholar
- Kusak, J., Skrbins, A.M., Hubert, D., 2005. Home ranges, movements, and activity of wolves (Canis lupus) in the Dalmatian part of Dinarids, Croatia. Eur. J. Wildl. Res. 51, 254–262.CrossRefGoogle Scholar
- Lapini, L., Brugnoli, S., Krofel, M., Kranz, A., Molinari, P., 2010. A grey wolf (Canis lupus Linne, 1758) from Fiemme Valley (Mammalia: Canidae: North-Eastern Italy). Boll. Mus. Civ. St. Nat. Venezia 61, 117–129.Google Scholar
- Librado, P., Rozas, J., 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.CrossRefGoogle Scholar
- Linnell, J.D.C., Boitani, L., 2012. Building biological realism into wolf management policy: the development of the population approach in Europe. Hystrix 23, 80–91.Google Scholar
- Linnell, J.D.C., Brøseth, H., Solberg, E.J., Brainerd, S.M., 2005. The origins of the southern Scandinavian wolf population: potential for natural immigration in relation to dispersal distances, geography and Baltic ice. Wildl. Biol. 11, 383–391.CrossRefGoogle Scholar
- Linnell, J., Salvatori, V., Boitani, L., 2008. Guidelines for Population Level Management Plans for Large Carnivores. Large Carnivore Initiative for Europe c/o Istituto di Ecologia Applicata, Rome, pp. 78.Google Scholar
- Lucchini, V., Fabbri, E., Marucco, F., Ricci, S., Boitani, L., Randi, E., 2002. Noninvasive molecular tracking of colonizing wolf (Canis lupus) packs in the western Italian Alps. Mol. Ecol. 11, 857–868.PubMedCrossRefGoogle Scholar
- 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, 523–536.PubMedCrossRefGoogle Scholar
- Marucco, F., Avanzinelli, E., Boitani, L., 2012. Non-invasive integrated sampling design to monitor the wolf population in Piemonte, Italian Alps. Hystrix 23, 5–13.Google Scholar
- Marucco, F., McIntire, E.J.B., 2010. Predicting spatio-temporal recolonization of large carnivore populations and livestock depredation risk: wolves in the Italian Alps. J. Appl. Ecol. 47, 789–798.CrossRefGoogle Scholar
- MacNulty, D.R., Smith, D.W., Mech, L.D., Eberly, L.E., 2009. Body size and predatory performance in wolves: is bigger better? J. Anim. Ecol. 78, 532–539.CrossRefGoogle Scholar
- Milenković, M., Šipetić, V.J., Blagojević, J., Tatović, S., Vujošević, M., 2010. Skull variation in DinaricBalkan and Carpathian gray wolf populations revealed by geometric morphometric approaches. J. Mamm. 91, 376–386.CrossRefGoogle Scholar
- Nielsen, E.E., Bach, L.A., Kotlicki, P., 2006. Hybridlab (version 1.0): a program for generating simulated hybridsfrom populationsamples. Mol.Ecol.Notes6, 971–973.Google Scholar
- Nowak, S., Mysłajek, R.W., Kłosiň ska, A., Gabrys´, G., 2011. Diet and prey selection of wolves (Canis lupus) recolonising Western and Central Poland. Mamm. Biol. 76, 709–715.CrossRefGoogle Scholar
- Palomares, F., Godoy, J.A., Piriz, A., O’Brien, S.J., Johnson, W.E., 2002. Faecal genetic analysis todetermine the presence and distributionof elusive carnivores: design and feasibility for the Iberian lynx. Mol. Ecol. 11, 2171–2182.PubMedCrossRefGoogle Scholar
- Paetkau, D., Slade, R., Burdens, M., Estoup, A., 2004. Direct, real-time estimation of migration rate using assignment methods: a simulation-based exploration of accuracy and power. Mol. Ecol. 13, 55–65.PubMedCrossRefGoogle Scholar
- Peakall, R., Smouse, P.E., 2006. GenAlEx v.6.1: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6, 288–295.Google Scholar
- Pilot, M., Branicki, W., Jędrzejewski, W., Goszczyński, J., Jędrzejewska, B., Dykyy, I., Shkvyrya, M., Tsingarska, 2010. Phylogeographic history of grey wolves in Europe. BMC Evol. Biol. 10, 104.PubMedPubMedCentralCrossRefGoogle Scholar
- Pilot, M., Jędrzejewski, W., Branicki, W., Sidorovich, V.E., Jędrzejewska, B., Stachura, K., Funk, S.M., 2006. Ecological factors influence population genetic structure of European grey wolves. Mol. Ecol. 15, 4533–4553.PubMedCrossRefGoogle Scholar
- Pilot, M., Jędrzejewski, W., Sidorovich, V.E., Meier-Augenstein, W., Hoelzel, A.R., 2012. Dietary differentiation and the evolution of population genetic structure in a highly mobile carnivore. PLoS ONE 7, e39341.PubMedPubMedCentralCrossRefGoogle Scholar
- Piry, S., Alapetite, A., Cornuet, J., Paetkau, D., Baudouin, L., Estoup, A., 2004. GENECLASS2: a software for genetic assignment and first generation migrant detection. J. Heredity 95, 536–539.CrossRefGoogle Scholar
- Pritchard, J.K., Stephens, M., Donnelly, P., 2000. Inference of population structure using multilocus genotype data. Genetics 155, 945–959.PubMedPubMedCentralGoogle Scholar
- Randi, E., 2008. Detecting hybridization between wild species and their domesticated relatives. Mol. Ecol. 17, 285–293.PubMedCrossRefGoogle Scholar
- Randi, E., Lucchini, V., Christensen, M.F., Mucci, N., Funk, S.M., Dolf, G., Loeschcke, V., 2000. Mitochondrial DNA variability in Italian and east European wolves: detecting the consequencesofsmall population size and hybridization. Conserv. Biol. 2, 464–473.CrossRefGoogle Scholar
- Rannala, B., Mountain, J.L., 1997. Detecting immigrant by using multilocus genotypes. Proc. Natl. Acad. Sci. U.S.A. 94, 9197–9221.PubMedPubMedCentralCrossRefGoogle Scholar
- Rice, W.R., 1989. Analyzing tables of statistical tests. Evolution 43, 223–225.CrossRefGoogle Scholar
- Rosser, A.M., Sue, A.M., 2002. Overexploitation and species extinctions. Conserv. Biol. 16, 584–586.CrossRefGoogle Scholar
- Rousset, R., 2008. GENEPOP’007: a complete re-implementation of GENEPOP software for Windows and Linux. Mol. Ecol. Res. 8, 103–106.CrossRefGoogle Scholar
- Salvatori, V., Linnell, J., 2005. Report on the conservation status and threats for the wolf (Canis lupus) in Europe. Council of Europe T-PVS/Inf 16 Report: 1–24, Strasbourg.Google Scholar
- Schäfer, M., 2012. The National Wolf Strategy in Austria. Master Thesis in Environmental Science. Swish Federal Institute od Technology, Institute for Environmental Policy and Economics, Zurich, CH.Google Scholar
- Schede, J.U., Schumann, G., Wersin-Sielaff, A., 2010. Wolfe in Brandenburg-eine spurensuche im markischen Sand. Ministerium fur Umwelt. Gesundheit und Verbraucherschutz des Landes Brandenburg, Potsdam, pp. 152.Google Scholar
- Schwenk, S., 1985. Österreichische Jagdstatistiken von 1850 bis 1936. Dr. Rudolf Habelt GMBH, Bonn, pp. 203.Google Scholar
- Sommer, R., Benecke, N., 2005. Late-Pleistocene and early Holocene history of the canid fauna of Europe (Canidae). Mamm. Biol. 70, 227–241.CrossRefGoogle Scholar
- Sommer, R., Nadachowski, A., 2006. Glacial refugia ofmammals inEurope: evidence from fossil records. Mamm. Rev. 36, 251–266.CrossRefGoogle Scholar
- Stronen, A.V., Forbes, G.J., Paquet, P.C., Goulet, G., Sallows, T., Musiani, M., 2012. Dispersal in a plain landscape: short-distance genetic differentiation in southwestern Manitoba wolves, Canada. Conserv. Genet. 13, 359–371.CrossRefGoogle Scholar
- Sundqvist, A.K., Ellegren, H., Olivier, M., Vilà, C., 2001. Y chromosome haplotyping in Scandinavian wolves (Canis lupus) based on microsatellites markers. Mol. Ecol. 10, 1959–1966.PubMedCrossRefGoogle Scholar
- Tallmon, D.A., Luikart, G., Waples, R., 2004. The alluring simplicity and complex reality of genetic rescue. Trends Ecol. Evol. 19, 489–496.PubMedCrossRefGoogle Scholar
- Tamura, K., Nei, M., 1993. Estimation of the number of nucleotide substitutions in the control regionofmitochondrial-DNAinhumans and chimpanzees. Mol. Biol. Evol. 10, 512–526.Google Scholar
- Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., Shipley, P., 2004. MICROCHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4, 535–538.CrossRefGoogle Scholar
- Valière, N., Fumagalli, L., Gielly, L., et al., 2003. Long distance wolf recolonization of France and Switzerland inferred from noninvasive genetic sampling over a period of 10 years. Anim. Conserv. 6, 83–92.CrossRefGoogle Scholar
- vonHoldt, B.M., Pollinger, J.P., Earl, D.A., Knowles, J.C., Boyko, A.R., Parker, H., Geffen, E., Pilot, M., Jedrzejewski, W., Jedrzejewska, B., Sidorovich, V., Greco, C., Randi, E., Musiani, M., Kays, R., Bustamante, C.D., Ostrander, E.A., Novembre, J., Wayne, R.K., 2011. Agenome-wide perspective on the evolutionary historyof enigmatic wolf-like canids. Genome Res. 21, 1294–1305.PubMedPubMedCentralCrossRefGoogle Scholar
- vonHoldt, B.M., Stahler, D.R., Bangs, E.E., Smith, D.W., Jimenez, M.D., Mack, C.M., Niemeyer, C.C., Pollinger, J.P., Wayne, R.K., 2010. A novel assessment of population structure and gene flow in grey wolf populations of the Northern Rocky Mountains of the United States. Mol. Ecol. 20, 4412–4427.CrossRefGoogle Scholar
- Wabakken, P., Sand, H., Liberg, O., Bjärvall, A., 2001. The recovery, distribution, and population dynamicsofwolvesonthe Scandinavian peninsula,1978–1998. Can. J. Zool. 79, 710–725.CrossRefGoogle Scholar
- Waits, L.P., Luikart, G., Taberlet, P., 2001. Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol. Ecol. 10, 249–256.PubMedCrossRefGoogle Scholar
- Wawrzyniak, P., Jędrzejewski, W., Jędrzejewska, B., Borowik, T., 2010. Ungulate management in Poland. In: Apollonio, M., Putman, R., Andersen, R. (Eds.), Ungulate Management in Europe in the 21st Century. Cambridge University Press, Cambridge, United Kingdom, pp. 223–242.Google Scholar
- Weber, J.-M., Fattebert, J. (Eds.), 2008. Wolf Monitoring in the Alps, 5th Alpine Wolf Workshop. Kora Bericht Press N. 41.Google Scholar
- Weir, B.S., Cockerham, C.C., 1984. Estimating F-statistic for the analysis ofpopulation structure. Evolution 6, 1358–1370.Google Scholar