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Genome-wide profiles indicate wolf population connectivity within the eastern Carpathian Mountains

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Abstract

The Carpathian Mountains provide critical wildlife habitat in central Europe, and previous genome-wide studies have found western Carpathian Mountain wolves (Canis lupus) to be a separate population. Whereas differentiation to the north may be explained by a lowland-mountain transition and habitat fragmentation, the eastern Carpathian Mountains extending through Romania appear to offer continuous wildlife habitat southward. Our objective was to assess gene flow patterns and population connectivity among wolves in Romania, western Ukraine, and the Republic of Moldova. We sought to determine if the Carpathian Mountain region is best described by a north–south gradient in genetic profiles, or whether Romanian wolves show population structure with northern individuals clustering with western Ukraine. We genotyped 48 individuals with 170 000 single nucleotide polymorphism markers, and successful profiles from Romania (n = 27) and Moldova (n = 2) were merged with existing data from western Ukraine (n = 10). Expected heterozygosity was 0.234 (SE 0.001) for Romania and 0.229 (SE 0.001) for western Ukraine, whereas observed heterozygosity values were 0.230 (SE 0.001) versus 0.231 (SE 0.001). Population structure analyses with a maximum likelihood method supported K = 1 population, followed by K = 2 where Romania formed one cluster, and western Ukraine and Moldova formed another. Principal component analysis results were broadly consistent with K = 2. Pairwise FST between western Ukraine and Romania was 0.042 (p = 0.001). Our findings indicated weak population differentiation, and future research may clarify whether the spatial distribution of genetic diversity in the region is associated with environmental and ecological factors such as terrain ruggedness and the distribution of prey species.

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References

  • Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664

    Article  CAS  Google Scholar 

  • Andersen LW, Harms V, Caniglia R, Czarnomska SD, Fabbri E, Jędrzejewska B, Kluth G, Madsen AB, Nowak C, Pertoldi C et al (2015) Long-distance dispersal of a wolf, Canis lupus, in northwestern Europe. Mammal Res 60:163–168

    Article  Google Scholar 

  • Bakan J, Vukan L, Popović Z, Paule L (2014) Genetic differentiation of grey wolf population (Canis lupus L.) from Balkan and Carpathians. Balk J Wildl Res 1:87–93

    Google Scholar 

  • Bartoń KA, Zwijacz-Kozica T, Zięba F, Sergiel A, Selva N (2019) Bears without borders: long-distance movement in human-dominated landscapes. Glob Ecol Conserv 16:e000541

    Google Scholar 

  • Boitani L (2003) Wolf conservation and recovery. In: Mech LD, Boitani L (eds) Wolves: behavior, ecology, and conservation. University of Chicago Press, Chicago, pp 317–340

    Google Scholar 

  • Boitani L (2015) Key actions for large carnivore populations in Europe. European Commission DG Environment.

  • Chapron G, Kaczensky P, Linnell JDC, von Arx M, Huber D, Andrén H, López-Bao JV, Adamec M, Alvares F, Anders O et al (2014) Recovery of large carnivores in Europe’s modern human-dominated landscapes. Science 346:1517–1519

    Article  CAS  Google Scholar 

  • Czarnomska SD, Jęzdrzejewska B, Borowik T, Niedziałkowska M, Stronen AV, Nowak S, Mysłajek RW, Okarma H, Konopiński M, Pilot M et al (2013) Concordant mitochondrial and microsatellite DNA structuring between Polish lowland and Carpathian wolves. Conserv Genet 14:573–588

    Article  Google Scholar 

  • de Groot GA, Nowak C, Skrbinšek T, Andersen LW, Aspi J, Fumagalli L, Godinho R, Harms V, Jansman HAH, Liberg O et al (2016) Decades of population genetic research reveal the need for harmonization of molecular markers: the grey wolf Canis lupus as a case study: harmonization of genetic markers in wolves. Mammal Rev 46:44–59

    Article  Google Scholar 

  • Deinet S, Ieronymidou C, McRae L, Burfield IJ, Foppen RP, Collen B, Böhm M (2013) Wildlife comeback in Europe—the recovery of selected mammal and bird species (Final report to Rewilding Europe by the Zoological Society of London). BirdLife International and the European Bird Census Council, London.

  • Díaz CL (2010) The Bern Convention: 30 years of nature conservation in Europe: THE BERN CONVENTION. Rev Eur Community Int Environ Law 19:185–196

    Article  Google Scholar 

  • Djan M, Maletić V, Trbojević I, Popović D, Veličković N, Burazerović J, Ćirović D (2014) Genetic diversity and structuring of the grey wolf population from the Central Balkans based on mitochondrial DNA variation. Mamm Biol 79:277–282. https://doi.org/10.1016/j.mambio.2014.03.001

    Article  Google Scholar 

  • Geffen E, Anderson MJ, Wayne RK (2004) Climate and habitat barriers to dispersal in the highly mobile grey wolf. Mol Ecol 13:2481–2490

    Article  CAS  Google Scholar 

  • Hindrikson M, Remm J, Pilot M, Godinho R, Stronen AV, Baltrūnaité L, Czarnomska SD, Leonard JA, Randi E, Nowak C et al (2017) Wolf population genetics in Europe: a systematic review, meta-analysis and suggestions for conservation and management: wolf population genetics in Europe. Biol Rev 92:1601–1629

    Article  Google Scholar 

  • Hulva P, Bolfikova BC, Woznicova W, Jindrichova M, Benesova M, Myslajek RW, Nowak S, Szewczyk M, Niedzwieckna N, Figura M et al (2018) Wolves at the crossroads: fission-fusion range biography in the Western Carpathians and Central Europe. Divers Distrib 24:179–192

    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. https://doi.org/10.1038/hdy.2008.34

    Article  CAS  PubMed  Google Scholar 

  • Kaczensky P, Chapron G, von Arx M, Huber D, Andrén H, Linnell J (2013) Status, management and distribution of large carnivores—bear, lynx, wolf & wolverine—in Europe. Part 1- Europe summaries. Report: 1–72. A Large Carnivore Initiative for Europe Report prepared for the European Commission.

  • Matosiuk M, Śmietana W, Czajkowska M, Paule L, Štofik J, Krajmerová D, Bashta A-T, Jakimiuk S, Ratkiewicz M (2019) Genetic differentiation and asymmetric gene flow among Carpathian brown bear (Ursus arctos) populations—implications for conservation of transboundary populations. Ecol Evol 9:1501–1511

    Article  Google Scholar 

  • Meirmans PG, van Tienderen PG (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794

    Article  Google Scholar 

  • Milenković M, Šipetić VJ, Blagojević J, Tatović S, Vujošević M (2010) Skull variation in Dinaric-Balkan and Carpathian gray wolf populations revealed by geometric morphometric approaches. J Mammal 91:376–386

    Article  Google Scholar 

  • Okarma H, Buchalczyk T (1993) Craniometrical characteristics of wolves Canis lupus from Poland. Acta Theriol 38:253–262

    Article  Google Scholar 

  • Pilot M, Jedrzejewski W, Branicki W, Sidorovich VE, Jedrzejewska B, Stachura K, Funk SM (2006) Ecological factors influence population genetic structure of European grey wolves. Mol Ecol 15:4533–4553

    Article  CAS  Google Scholar 

  • Pilot M, Greco C, vonHoldt BM, Jędrzejewska B, Randi E, Jędrzejewski W, Sidorovich VE, Ostrander EA, Wayne RK (2014) Genome-wide signatures of population bottlenecks and diversifying selection in European wolves. Heredity 112:428–442

    Article  CAS  Google Scholar 

  • Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira M, Bender D, Maller J, Sklar P, de Bakker P, Daly M, Sham P (2007) PLINK: a toolset for whole-genome association and population-based linkage analysis. Am J Hum Genet 81:559–575

    Article  CAS  Google Scholar 

  • R Development Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Salvatori V, Okarma H, Ionescu O, Dovhanych Y, Find’o S, Boitani L, (2002) Hunting legislation in the Carpathian Mountains: implications for the conservation and management of large carnivores. Wildl Biol 8:3–10

    Article  Google Scholar 

  • Sommer RS, Nadachowski A (2006) Glacial refugia of mammals in Europe: evidence from fossil records. Mammal Rev 36:251–265

    Article  Google Scholar 

  • Stronen AV, Jędrzejewska B, Pertoldi C, Demontis D, Randi E, Niedziałkowska M, Pilot M, Sidorovich VE, Dykyy I, Kusak J et al (2013) North-south differentiation and a region of high diversity in European wolves (Canis lupus). PLoS ONE 8:e76454

    Article  CAS  Google Scholar 

  • Stronen AV, Jędrzejewska B, Pertoldi C, Demontis D, Randi E, Niedziałkowska M, Pilot M, Sidorovich VE, Dykyy I, Kusak J et al (2014) Data from: north-south differentiation and a region of high diversity in European wolves (Canis lupus). Dryad Digital Repos. https://doi.org/10.5061/dryad.9s1t9

    Article  Google Scholar 

  • Stronen AV, Jedrzejewska B, Pertoldi C, Demontis D, Randi E, Niedziałkowska M, Borowik T, Sidorovich VE, Kusak J, Kojola I et al (2015) Genome-wide analyses suggest parallel selection for universal traits may eclipse local environmental selection in a highly mobile carnivore. Ecol Evol 5:4410–4425

    Article  Google Scholar 

  • Tammeleht E, Remm J, Korsten M, Davison J, Tumanov I, Saveljev A, Männil P, Kojola I, Saarma U (2010) Genetic structure in large, continuous mammal populations: the example of brown bears in northwestern Eurasia. Mol Ecol 19:5359–5370

    Article  CAS  Google Scholar 

  • Trouwborst A (2011) Conserving European biodiversity in a changing climate: the Bern convention, the European Union Birds and Habitats Directives and the adaptation of nature to climate change. Rev Eur Community Int Environ Law 20:62–77

    Article  Google Scholar 

  • vonHoldt BM, Pollinger JP, Earl DA, Knowles JC, Boyko AR, Parker H, Geffen E, Pilot M, Jedrzejewski W, Jedrzejewska B et al (2011) A genome-wide perspective on the evolutionary history of enigmatic wolf-like canids. Genome Res 21:1294–1305

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful for the assistance of Cino Pertoldi, Sylwia Czarnomska, Attila Kecskés and Csaba Domokos. We also thank the anonymous reviewers for their feedback on the manuscript. The study was supported by a grant to HSE from Aalborg Zoo Conservation Foundation (2017-6), and AVS was funded by the Danish Natural Science Research Council (Grant 1337-00007) and a senior postdoctoral fellowship from Insubria University, Italy. DNA extraction of Romanian samples was supported by the National Authority for Scientific Research and Innovation (ANCSI) Project PN1330206/PN16330207 and sampling was conducted under Permits Nos. 2278/2011, 3456/2012 and 2187/2013 (Romanian Ministry of Environment).

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Ericson, H.S., Fedorca, A., Toderas, I. et al. Genome-wide profiles indicate wolf population connectivity within the eastern Carpathian Mountains. Genetica 148, 33–39 (2020). https://doi.org/10.1007/s10709-019-00083-1

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  • DOI: https://doi.org/10.1007/s10709-019-00083-1

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