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Detection of an East European wolf haplotype puzzles mitochondrial DNA monomorphism of the Italian wolf population

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Abstract

Southern European wolves suffered from reiterated population declines during glacial periods and historically due to human persecution. Differently from other European wolf populations, a single mitochondrial DNA (mtDNA) control region haplotype (W14) has been so far described in the Italian wolves, although no intensive genetic sampling has ever been conducted in historical source populations from central and southern Italy. Using non-invasive genetic techniques, we report the occurrence of an unexpected mtDNA haplotype (W16) in the wolf population of the Abruzzo, Lazio and Molise National Park (PNALM), central Italy. This haplotype, detected in three out of 90 faecal samples from the PNALM, was previously reported in wolves from the North Carpathians, Slovakia and the Balkans only. Microsatellite analysis and molecular sex determination confirmed that the W16 samples belonged to three distinct wolves. Although alternative explanations can be formulated for the origin of this mtDNA haplotype in the otherwise monomorphic Italian wolf population, assignment procedures indicated the likely admixed ancestry of one W16 sample with East European wolves. Anthropogenic introgression with dogs has been detected in the Italian wolf population using nuclear DNA microsatellites, but no population-wide genetic survey had previously reported a mtDNA control region variant in Italian wolves. Our findings strongly suggest that, in addition to wolf × dog hybridization, captive-released wolves or wolf × dog hybrids may successfully interbreed with wolves in the wild, and that human-mediated introgression may occur even in well established protected areas.

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References

  • 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.

    Article  Google Scholar 

  • Arnason, U., Gullberg, A., Janke, A., Kullberg, M., 2007. Mitogenomic analyses of caniform relationships, Mol. Phylogenet. Evol. 45, 863–874.

    Article  CAS  PubMed  Google Scholar 

  • Belkhir, K., Castric, V., Bonhomme, F., 2002. IDENTIX, a software to test relatedness in a population using permutation methods, Mol. Ecol. Notes 2, 611–614.

    Article  Google Scholar 

  • Boitani, L., 1992. Wolf research and conservation in Italy, Biol. Conserv. 61, 125–132.

    Article  Google Scholar 

  • Boitani, L, Ciucci, P., 1993. Wolves in Italy: critical issues for their conservation. In: Promberger, C, Scröeder, W. (Eds.), Wolves in Europe. Status and perspectives. Wildbiologische Gesel, Munchen, 136p. (pp.75–90).

  • Caniglia, R., Fabbri, E., Cubaynes, S., Glimenez, O., Lebreton, J.D., Randi, E., 2011. An improved procedure to estimate wolf abundance using non-invasive genetic sampling and capture-recapture mixture models, Conserv. Genet. 13, 53–64.

    Article  Google Scholar 

  • Dolf, G., Schläpfer, J., Gaillard, C, Randi, E., Lucchini, V., Breitenmoser, U, Stahlberger-Saitbekova, N., 2000. Differentiation between Italian wolf and domestic dog based on microsatellite analysis, Genet. Sel. Evol. 32, 533–541.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Douzery, E., Randi, E., 1997. The mitochondrial control region of Cervidae: Evolutionary patterns and phylogenetic content, Mol. Biol. Evol. 14, 1154–1166.

    Article  CAS  PubMed  Google Scholar 

  • Earl, D.A.,vonHoldt, B.M., 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method, Conserv. Genet. Resour. 4, 359–361.

    Article  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, 2611–2620.

    Article  CAS  PubMed  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. 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 

  • Francisco, L.V., Langston, A.A., Mellersh, C.S., Neal, C.L., Ostrander, E.A., 1996. A class of highly polymorphic tetranucleotide repeats for canine genetic mapping, Mamm. Genome 7, 359–362.

    Article  CAS  PubMed  Google Scholar 

  • Fredholm, M., Winterø, A.K., 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 

  • Gomercic, T., Sindicic, M., Galov, A., Arbanasic, H., KusakJ., Kocijan, I., Gomercic, M.D., Huber, D., 2010. High genetic variability of the grey wolf (Canis lupus L.) population from Croatia as revealed by mitochondrial DNA control region sequences, Zool. Stud. 49, 816–823.

    CAS  Google Scholar 

  • Iacolina, L, Scandura, M., Gazzola, A., Cappai, N., Capitani, C, Mattioli, L, Vercillo, F., Apollonio, M., 2010. Y-chromosome microsatellite variation in Italian wolves: A contribution to the study of wolf-dog hybridization patterns, Mamm. Biol. 75, 341–347.

    Article  Google Scholar 

  • Jakobsson, M., Rosenberg, N.A., 2007. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure, Bioinformatics 23, 1801–1806.

    Article  CAS  PubMed  Google Scholar 

  • Koblmüller, S., Nord, M., Wayne, R.K., Leonard, J.A., 2009. Origin and status of the Great Lakes wolf, Mol. Ecol. 18, 2313–2326.

    Article  PubMed  CAS  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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google Scholar 

  • Lynch, M., Ritland, K., 1999. Estimation of pairwise relatedness with molecular markers, Genetics 152, 1753–1766.

    CAS  PubMed  PubMed Central  Google Scholar 

  • McKelvey, K.S., Schwartz, M.K., 2005. DROPOUT: a program to identify problem loci and samples for noninvasive genetic samples in a capture-mark-recapture framework, Mol. Ecol. Notes 5, 716–718.

    Article  CAS  Google Scholar 

  • Ostrander, E.A., Sprague, G.F., 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., 2003. An empirical exploration of data quality in DNA-based population inventories, Mol. Ecol. 12, 1375–1387.

    Article  CAS  PubMed  Google Scholar 

  • Peakall, R., Smouse, P.E., 2006. GENALEX 6: genetic analysis in Excel: population genetic software for teaching and research, Mol. Ecol. Notes 6, 288–295.

    Article  Google Scholar 

  • Pritchard, J.K., Stephens, M., Donnelly, P.J., 2000. Inference of population structure using moltilocus genotype data, Genetics 155, 945–959.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pilot, M., Jedrzejewsky, W., Branicki, W., Sidorovich, V.E., Jedrzejewska, B., Stachura, K., Funk, S.M., 2006. Ecological factors influence population genetic structure of European grey wolves, Mol. Ecol. 15, 4533–4553.

    Article  CAS  PubMed  Google Scholar 

  • Pilot, M., Branicki, W., Jedrzejewski, W., Goszcznski, J., Jędrzejewska, B., Dykyy, I., Shkvyrya, M., Tsingarska, E., 2010. Phylogeographic history of grey wolves in Europe. BMC Evol. Biol. 10, 104.

    Book  Google Scholar 

  • Pompanon, F., Bonin, A., Bellemain, E., Taberlet, P., 2005. Genotyping errors: causes, consequences and solutions, Nat. Rev. Genet. 6, 847–859.

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Randi, E., Lucchini, V., 2002. Detecting rare introgression of domestic dog genes into wild wolf (Canis lupus) populations by Bayesian admixture analyses of microsatellite variation, Conserv. Genet. 3, 31–45.

    Article  CAS  Google 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 consequences of small population size and hybridization, Conserv. Biol. 14, 464–473.

    Article  Google Scholar 

  • Schwartz, M.K., Luikart, G., Waples, R.S., 2006. Genetic monitoring as a promising tool for conservation and management, Trends Ecol. Evol. 22, 25–33.

    Article  PubMed  Google Scholar 

  • Schwartz, M.K., McKelvey, K.S., 2009. Why sampling scheme matters: the effect of sampling scheme on landscape genetic results, Conserv. Genet. 10, 441–452.

    Article  Google Scholar 

  • Seddon, J., 2005. Canid-specific primers for molecular sexing using tissue or noninvasive samples, Conserv. Genet. 6, 147–149.

    Article  Google Scholar 

  • Shibuya, H., Collins, B.K., Huang, T.H.M., Johnson, G.S., 1994. A polymorphic (AGGAAT)n tandem repeat in an intronofthe canine von Willebrand factor gene. Anim. Genet. 25, 122.

    Google Scholar 

  • Taberlet, P., Griffin, S., Goossens, B., Questiau, S., Manceau, V., Escaravage, N., Waits, L.P., Bouvet, J., 1996. Reliable genotyping of samples with very low DNA quantities using PCR, Nucleic Acids Res. 24, 3189–3194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taberlet, P., Waits, L., Luikart, G., 1999. Noninvasive genetic sampling: look before you leap, Trends Ecol. Evol. 14, 323–327.

    Article  CAS  PubMed  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, Anim. Conserv. 6, 83–92.

    Article  Google Scholar 

  • Van Oosterhout, C, Hutchinson, W.F., Wills, D.P.M., Shipley, P., 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data, Mol. Ecol. Notes 4, 535–538.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Vilà, C, Savolainen, P., Maldonado, J.E., Amorim, I.R., Rice, J.E., Honeycutt, R.L., Cran-dall, K.A., Lundeberg, J., Wayne, R.K., 1997. Multiple and ancient origins of the domestic dog, Science 276, 1687–1689.

    Article  PubMed  Google Scholar 

  • Wayne, R.K., Lehman, N., Allard, M.W., Honeycutt, R.L., 1992. Mitochondrial DNA variability of the gray wolf: genetic consequences of population decline and habitat fragmentation, Conserv. Biol. 6, 559–569.

    Article  Google Scholar 

  • Wayne, R.K., Vilà, C, 2003. Molecular genetic studies ofwolves. In: Mech, D., Boitani, L. (Eds.), Wolves, Behavior, ecology, and conservation. The University of Chicago Press, Chicago and London, pp. 218–238, 472p.

    Google Scholar 

  • Wilberg, M.J., Dreher, B.P., 2004. GENECAP: a program for analysis of multilocus genotype data for non-invasive sampling and capture-recapture population estimation, Mol. Ecol. 4, 783–785.

    Article  Google Scholar 

  • Zimen, E., Boitani, L, 1975. Number and distribution ofwolves in Italy, Z. Säugetierkd 40, 102–112.

    Google Scholar 

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Authors and Affiliations

  1. Department of Biology, University of Florence, Via Madonna del Piano 6, 50019, FI, Sesto Fiorentino, Italy

    Francesca Boggiano, Claudio Ciofi, Angela Formia & Chiara Natali

  2. Department of Biology and Biotechnologies, University of Rome “La Sapienza”, Viale dell’Università 32, 00185, Rome, Italy

    Luigi Boitani, Lorenza Grottoli & Paolo Ciucci

Authors
  1. Francesca Boggiano
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  2. Claudio Ciofi
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  3. Luigi Boitani
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  4. Angela Formia
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  5. Lorenza Grottoli
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  6. Chiara Natali
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  7. Paolo Ciucci
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Correspondence to Paolo Ciucci.

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Boggiano, F., Ciofi, C., Boitani, L. et al. Detection of an East European wolf haplotype puzzles mitochondrial DNA monomorphism of the Italian wolf population. Mamm Biol 78, 374–378 (2013). https://doi.org/10.1016/j.mambio.2013.06.001

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  • DOI: https://doi.org/10.1016/j.mambio.2013.06.001

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