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Wolf population genetics at the south-eastern edge of their European range

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Abstract

Gray wolf populations have been recovering recently across Europe, a fact that poses serious challenges to the management of the species. We investigate the population genetics of wolves at the south-eastern edge of their European range, in Greece, and identify conservation priorities for the species in the country. During population monitoring efforts (1998–2014)48 tissue and hair samples were collected and genotyped at 14 microsatellite loci. Eight samples were discarded from further downstream analysis because of possible dog-wolf admixture. Unlike many other edge populations, wolves in Greece showed high levels of genetic variation (HE = 0.73; HO = 0.66). We detected two genetic clusters of wolves but no genetic bottleneck, which suggests that the human-caused population reduction of wolves in Greece may not have been as severe as previously assumed and that enough wolves may have survived in inaccessible areas and/or neighboring countries to maintain genetic diversity. Two of the main conservation priorities identified for gray wolves in Greece are non-invasive genetic monitoring and ensuring the functional connectivity of the Natura 2000 network through the identification and protection of ecological corridors and road-less areas.

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References

  • Arnaud-Haond, S., Teixeira, S., Massa, S.I., Billot, C, Saenger, P., Coupland, G., Duarte, CM., Serrão, EA, 2006. Genetic structure at range edge: low diversity and high inbreeding in Southeast Asian mangrove (Avicennia marina) populations. Mol. Ecol. 15, 3515–3525.

    Article  CAS  PubMed  Google Scholar 

  • Balloux, F., Lugon-Moulin, N., 2002. The estimation of population differentiation with microsatellite markers. Mol. Ecol. 11, 155–165.

    Article  PubMed  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.

  • Breitenmoser, U., 1998. Large predators in the Alps: the fall and rise of man’s competitors. Biol. Conserv. 83, 279–289.

    Article  Google Scholar 

  • Chapron, G., et al., 2014. Recovery of large carnivores in Europe’s modern human-dominated landscapes. Science 346, 1517–1519.

    Article  CAS  PubMed  Google Scholar 

  • Czarnomska, S.D., et al., 2013. Concordant mitochondrial and microsatellite DNA structuring between Polish lowland and Carpathian Mountain wolves. Conserv. Genet. 14, 573–588.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • European Commission, 2011. Our life insurance, our natural capital: an EU biodiversity strategy to 2020. Communication from the Commission to the European Parliament, the Council, the Economic and Social Committee and the Committee of the Regions, Brussels.

  • 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 

  • Excoffier, L, Lischer, H.E.L., 2010. Arlequin suite ver3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567.

    Article  PubMed  Google Scholar 

  • Excoffier, L., Foll, M., Petit, R.J., 2009. Genetic consequences of range expansions. Annu. Rev. Ecol. Evol. Syst. 40, 481–501.

    Article  Google Scholar 

  • Fabbri, E., et al., 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 

  • Frantz, A.C., Cellina, S., Krier, A., Schley, L., Burke, T., 2009. Using spatial Bayesian methods to determine the genetic structure of a continously distributed population: clusters and isolation by distance. J. Appl. Ecol. 46, 493–505.

    Article  Google Scholar 

  • Hardy, O.J., Vekemans, X., 2002. SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol. Ecol. Notes 2, 618–620.

    Article  Google Scholar 

  • Hoffmann, AA, Blows, M.W., 1994. Species borders—ecological and evolutionary perspectives. Trends Ecol. Evol. 9, 223–227.

    Article  PubMed  Google Scholar 

  • IENE, 2014. Malmö declaration protect remaining roadless areas. Call for a European Strategy to protect roadless areas. In: IENE 2014 International Conference on Ecology and Transportation Life for a Greener Transport Infrastructure, Malmö, Sweden.

  • Iliopoulos, G., 2009. Canis lupus (Linnaeus, 1758). In: Legakis, A., Maragou, P. (Ed.), Red Data Book of the Threatened Animal Species of Greece. Hellenic Zoological Society, Athens, pp. 389–390.

    Google Scholar 

  • Kalinowski, S.T., 2005. HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol. Ecol. Notes 5, 187–189.

    Article  CAS  Google Scholar 

  • Karamanlidis, A.A., De Gabriel Hernando, M., Georgiadis, L., Kusak, J., 2016. Activity, movement, home range and habitat use of an adult gray wolf in a Mediterranean landscape of northern Greece. Mammalia, https://doi.org/10.1515/mammalia-2015–0091.

  • Linnell, J.D.C., Boitani, L., 2012. Building biological realism into wolf management policy: the development of the population approach in Europe. Hystrix Ital. J. Mammal. 23, 80–91.

    Google Scholar 

  • Linnell, J., Salvatori, V., Boitani, L, 2008. Guidelines for Population Level Management Plans for Large Carnivores in Europe. pp. 1–78.

  • Loiselle, BA, Sork, V.L., Nason, J., Graham, C, 1995. Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubicaceae). Am. J. Bot. 82, 1420–1425.

    Article  Google Scholar 

  • Moura, A.E., Tsingarska, E., Dabrowski, M.J., Czarnomska, S.D., Jędrzejewska, B., Pilot, M., 2014. Unregulated hunting and genetic recovery from a severe population decline: the cautionary case of Bulgarian wolves. Conserv. Genet. 15, 405–417.

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Piry, S., Luikart, G.L., Cornuet, J.M., 1999. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J. Hered. 90, 502–503.

    Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  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., 2011. Genetics and conservation of wolves Canis lupus in Europe. Mamm. Rev. 41, 99–111.

    Article  Google Scholar 

  • Rousset, F., Raymond, M., 1995. Testing heterozygote excess and deficiency. Genetics 140, 1413–1419.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rousset, F., 2008. GENEPOP ‘007: a complete reimplementation of the GENEPOP software for Windows and Linux. Mol. Ecol. Resour. 8, 103–106.

    Article  PubMed  Google Scholar 

  • Stenglein, J.L., Waits, L.P., Ausband, D.E., Zager, P., Mack, CM., 2010. Efficient, noninvasive genetic sampling for monitoring reintroduced wolves. J. Wildl. Manage. 74, 1050–1058.

    Article  Google Scholar 

  • Stronen, A.V., et al., 2013. North-south differentiation and a region of high diversity in European wolves (Canis lupus). PLoS One 8, e76454.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valière, N., 2002. GIMLET: a computer program for analysing genetic individual identification data. Mol. Ecol. Notes 2, 377–379.

    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  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Votsi, N.E.P., Zomeni, M.S., Pantis, J.D., 2016. Evaluating the effectiveness of Natura 2000 Network for wolf conservation: a case-study in Greece. Environ. Manage. 57, 257–270.

    Article  PubMed  Google 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.

    Article  CAS  PubMed  Google Scholar 

  • Yannic, G., Basset, P., Buchi, L., Hausser, J., Broquet, T., 2012. Scale-specific sex-biased dispersal in the Valais shrew unveiled by genetic variation on the Y-chromosome, autosomes, and mitochondrial DNA. Evolution 66, 1737–1750.

    Article  PubMed  Google Scholar 

  • Zachariah Peery, M., Kirby, R., Reid, B.N., Stoelting, R., Doucet-Beer, E., Robinson, S., Vásquez-Carillo, C, Pauli, J.N., Palsbøll, P.J., 2012. Reliability of genetic bottleneck tests for detecting recent population declines. Mol. Ecol. 21, 3403–3418.

    Article  PubMed  Google Scholar 

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Author notes

  1. These authors are the lead co-authors of this study.

Authors and Affiliations

  1. ARCTUROS, Civil Society for the Protection and Management of Wildlife and the Natural Environment, GR-53075, Aetos, Florina, Greece

    Alexandros A. Karamanlidis & Lazaros Georgiadis

  2. Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, NO-1432, Ås, Norway

    Alexandros A. Karamanlidis

  3. Mammal Research Institute, Polish Academy of Sciences, 17-230, Białowieża, Poland

    Sylwia D. Czarnomska & Bogumiła Jędrzejewska

  4. NIBIO-Norwegian Institute of Bioeconomy Research, 9925, Svanhovd, Svanvik, Norway

    Alexander Kopatz

Authors
  1. Alexandros A. Karamanlidis
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  2. Sylwia D. Czarnomska
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  3. Alexander Kopatz
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  4. Lazaros Georgiadis
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  5. Bogumiła Jędrzejewska
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Correspondence to Alexandros A. Karamanlidis.

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Karamanlidis, A.A., Czarnomska, S.D., Kopatz, A. et al. Wolf population genetics at the south-eastern edge of their European range. Mamm Biol 81, 506–510 (2016). https://doi.org/10.1016/j.mambio.2016.06.007

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  • DOI: https://doi.org/10.1016/j.mambio.2016.06.007

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