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Microsatellite based assignment reveals history of extirpated mountain ungulate

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Abstract

During the early 1900s, Northern chamois (Rupicapra rupicapra) populations in the northern Dinaric Mountains were extirpated. During the 1960s and 1970s there were several reintroductions of individuals from two Northern chamois subspecies (Alpine chamois, R. r. rupicapra and Balkan chamois, R. r. balcanica) from neighbouring areas in the attempt to re-establish the population. Accurate taxonomic classification, at subspecies level, of the autochthonous extirpated population was not known. To clarify which subspecies was present before reintroduction, we genotyped four male chamois skulls originating from Velebit Mountain, collected around 25 years before the population local extinction. DNA was successfully extracted from middle layer and outer sheath of horns. Assignment based on microsatellite loci, using both Bayesian clustering in STRUCTURE (with q values between 0.55 and 0.73) and DAPC (with individual membership probabilities of 0.99 and 1.00) indicated higher assessed likelihood for the Alpine subspecies.

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References

  • Adler CJ, Haak W, Donlon D, Cooper A (2011) Survival and recovery of DNA from ancient teeth and bones. J Archaeol Sci 38:956–964

    Google Scholar 

  • Apollonio M, Scandura M, Šprem N (2014) Reintroductions as a management tool for European ungulates. In: Putman R, Apollonio M (eds) Behaviour and management of European ungulates. Whittles Publishing, Dunbeath, pp 46–77

    Google Scholar 

  • Archer FI, Adams PE, Schneiders BB (2016) strataG: an R package for manipulating, summarizing and analysing population genetic data. Mol Ecol Resour 17:5–11

    PubMed  Google Scholar 

  • Biosa D, Scandura M, Tagliavini J, Luccarini S, Mattioli L, Appolnio M (2015) Patterns of genetic admixture between roe deer of different origin in central Italy. J Mammal 296:30–37

    Google Scholar 

  • Burrell AS, Disotell TR, Bergey CM (2015) The use of museum specimens with high-throughput DNA sequencers. J Hum Evol 0:35–44

    Google Scholar 

  • Buzan E, Bryja J, Zemanová B, Kryštufek B (2013) Population genetics of chamois in the contact zone between the Alps and the Dinaric Mountains: uncovering the role of habitat fragmentation and past management. Conserv Genet 14:401–412

    Google Scholar 

  • Carpio AJ, Guerrero-Casado J, Barasona J, Tortosa F, Vicente JM, Hillström L, Delibes-Mateos M (2016) Hunting as a source of alien species: a European review. Biol Invasions 19:1197–1211

    Google Scholar 

  • Casas-Marce M, Revilla E, Godoy JA (2010) Searching for DNA in museum specimens: a comparison of sources in a mammal species. Mol Ecol Resour 10:502–507

    CAS  PubMed  Google Scholar 

  • Corlatti L, Lorenzini R, Lovari S (2011) The conservation of the chamois Rupicapra spp. Mammal Rev 41:163–174

    Google Scholar 

  • Cornuet J-M, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crestanello B, Pecchioli E, Vernesi C, Mona C, Martínková N, Janiga M, Hauffe HC, Bertorelle G (2009) The genetic impact of translocations and habitat fragmentation in chamois (Rupicapra spp.). J Hered 100:691–708

    CAS  PubMed  Google Scholar 

  • Dufresnes C, Miquel C, Taberlet P, Fumagalli L (2019) Last but not beast: the fall of the Alpine wolves told by historical DNA. Mammal Res.https://doi.org/10.1007/s13364-019-00426-5

    Article  Google Scholar 

  • Frantz AC, Pourtois JT, Heuertz M, Schley L, Flamand MC, Krier A, Bertouille S, Chaumont F, Burke T (2006) Genetic structure and assignment tests demonstrate illegal translocation of red deer (Cervus elaphus) into a continuous population. Mol Ecol 15:3191–3203

    CAS  PubMed  Google Scholar 

  • Frantz AC, Zachos FE, Bertouille S, Eloy M-C, Colyn M, Flamand M-C (2017) Using genetic tools to estimate the prevalence of non-native red deer (Cervus elaphus) in a Western European population. Ecol Evol 7:7650–7660

    PubMed  PubMed Central  Google Scholar 

  • Frković A (1981) Naseljavanje divokoze u lovište “Senjski Sjeverni Velebit.” Goransko-Primorsko šumsko gospodarstvo, Delnice, p 25

    Google Scholar 

  • Frković A (2008) Reintroduction of chamois in Northern Velebit. Sumar list 11–12:543–550 (In Croatian with English summary)

    Google Scholar 

  • Hoffmann GS, Griebeler EM (2013) An improved high yield method to obtain microsatellite genotypes from red deer antlers up to 200 years old. Mol Ecol Resour 18:440–446

    Google Scholar 

  • Iacolina L, Corlatti L, Buzan E, Safner T, Šprem N (2019) Hybridization in European ungulates: a review of the current status, causes and consequences. Mammal Rev 49:45–59

    Google Scholar 

  • Jing C, Zhigang J, Chunlin L, Xiaoge P, Shaopeng C, Songhua T, Hongjun C, Binwan L (2015) Identification of ungulates used in a traditional Chinese medicine with DNA barcoding technology. Evol 5:1818–1825

    Google Scholar 

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    CAS  PubMed  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94

    PubMed  PubMed Central  Google Scholar 

  • King LT, Burke T (1999) Special issue on gene conservation: identification and management of genetic diversity. Mol Ecol 8:S1–S3

    CAS  PubMed  Google Scholar 

  • Knežević M (1938) Chamois. Trgovačka štamparija. M. Ramljak, Sarajevo (In Bosnian)

    Google Scholar 

  • Linnell JDC, Zachos FE (2011) Status and distribution patterns of European ungulates: genetics, population history and conservation. In: Putman R, Apollonio M, Andersen R (eds) Ungulate management in Europe: problems and practices. Cambridge University Press, Cambridge, pp 12–53

    Google Scholar 

  • Lister AM, Climate Change Research Group (2011) Natural history collections as sources of long-term datasets. Trends Ecol Evol 26:153–154

    PubMed  Google Scholar 

  • Lorenzini R, Cabras P, Fanelli R, Carboni GL (2011) Wildlife molecular forensics: identification of the Sardinian mouflon using STR profiling and the Bayesian assignment test. Forensic Sci Int Genet 5:345–349

    CAS  PubMed  Google Scholar 

  • Luikart G, Ryman N, Tallmon DA, Schwartz MK, Allendorf FW (2010) Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conserv Genet 11:355–373

    CAS  Google Scholar 

  • Manel S, Gaggiotti OE, Waples RS (2005) Assignment methods: matching biological questions with appropriate techniques. Trends Ecol Evol 20:136–142

    PubMed  Google Scholar 

  • Miracle P, Sturdy D (1991) Chamois and the karst of Herzegovina. J Archaeol Sci 18:89–108

    Google Scholar 

  • Ogden R, Linacre A (2015) Wildlife forensic science: a review of genetic geographic origin assignment. Forensic Sci Int Genet 18:152–159

    CAS  PubMed  Google Scholar 

  • Olano-Marin J, Plis K, Sönnichsen L, Borowik T, Niedziałkowska M, Jędrzejewska B (2014) Week population structure in European roe deer (Capreolus capreolus) and evidence of introgressive hybridization with Siberian roe deer (C. pygargus) northeastern Poland. PLoS ONE 9(10):e109147. https://doi.org/10.1371/journal.pone.0109147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira R, Godinho R, Randi E, Alves PC (2008) Hybridization versus conservation: are domestic cats threatening the genetic integrity of wildcats (Felis silvestris silvestris) in Iberian Peninsula? Philos Trans R Soc B 363:2953–2961

    Google Scholar 

  • Paplinska JZ, Taggart DA, Corrigan T, Eldridge MDB, Austin JJ (2011) Using DNA from museum specimens to preserve the integrity of evolutionarily significant unit boundaries in threatened species. Biol Conserv 144:290–297

    Google Scholar 

  • Polanc P, Sindičić M, Jelenčič M, Gomerčić T, Kos I, Huber Đ (2012) Genotyping success of historical Eurasian lynx (Lynx lynx L.) samples. Mol Ecol Resour 12:293–298

    CAS  PubMed  Google Scholar 

  • Primmer CR, Koskinen MT, Piironen J (2000) The one that did not get away: individual assignment using microsatellite data detects a case of fishing competition fraud. Proc R Soc B 267:1699–1704

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rodríguez F, Pérez T, Hammer S, Albornoz J, Domínguez A (2010) Integrating phylogeographic patterns of microsatellite and mtDNA divergence to infer the evolutionary history of chamois. BMC Evol Biol 10:222–214

    PubMed  PubMed Central  Google Scholar 

  • Senn HV, Pemberton JM (2009) Variable extent of hybridization between invasive sika (Cervus nippon) and native red deer (C. elaphus) in a small geographical area. Mol Ecol 18:862–876

    CAS  PubMed  Google Scholar 

  • Skorup V (2005) Big game and hunting. In: Vukelić J (ed) Forest and forestry of Northern Velebit. Hrvatske šume d.o.o. Zagreb. Zagreb-Senj, Croatia, pp 141–169 (In Croatian)

    Google Scholar 

  • Šprem N, Zanella D, Ugarković D, Prebanić I, Gančević P, Corlatti L (2015) Unimodal activity pattern in forest-dwelling chamois: typical behaviour or interspecific avoidance? Eur J Wildl Res 61:789–794

    Google Scholar 

  • Šprem N, Buzan E (2016) The genetic impact of chamois management in the Dinarides. J Wildl Manag 80:783–793

    Google Scholar 

  • Wandeler P, Hoeck PEA, Keller LF (2007) Back to the future: museum specimens in population genetics. Trends Ecol Evol 22:634–642

    PubMed  Google Scholar 

  • Waples RS (2005) Genetic estimates of contemporary effective population size: to what time periods do the estimates apply? Mol Ecol 14:3335–3352

    CAS  PubMed  Google Scholar 

  • Woods R, Marr MM, Brace S, Barnes I (2017) The small and the dead: a review of ancient DNA studies analysing micromammal species. Genes 8:312

    PubMed Central  Google Scholar 

  • Zemanová B, Hájková P, Bryja J, Zima jrJ, Hájková A, Zima J (2011) Development of multiplex microsatellite sets for noninvasive population genetic study of the endangered Tatra chamois. Folia Zool 60:70–80

    Google Scholar 

  • Zemanová B, Hájková P, Hájek B, Martínková N, Mikulíček P, Zima J, Bryja J (2015) Extremely low genetic variation in endangered Tatra chamois and evidence for hybridization with an introduced Alpine population. Conserv Genet 16:729–741

    Google Scholar 

Download references

Acknowledgements

This study was funded by: (i) the Croatian Science Foundation, Project IP 2016-06-5751 “DNA as evidence of distribution and vitality of endangered Balkan chamois”; (ii) the STARBIOS2 European Union’s Horizon 2020 Research and Innovation Program under Grant Agreement No. 709517 oriented to promote responsible research and innovation in biosciences; (iii) the Slovenian Research Agency (Programme Groups P1-0386). We want to express our appreciation to prof. Krešimir Krapinec for contribution in locating museum samples for our analyses and to Croatian hunting association and Hunting club “Jarebica-Senj” on the donation of museum samples.

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Authors and Affiliations

  1. Department of Plant Breeding, Genetics and Biometrics, Faculty of Agriculture, University of Zagreb, Svetošimunska cesta 25, 10000, Zagreb, Croatia

    Toni Safner

  2. Centre of Excellence for Biodiversity and Molecular Plant Breeding (CoE CroP-BioDiv), Svetošimunska cesta 25, 10000, Zagreb, Croatia

    Toni Safner

  3. Department of Biodiversity, Faculty of Mathematics, Natural Sciences and Information Technologies, University of Primorska, Glagoljaška 8, 6000, Koper, Slovenia

    Elena Buzan & Sandra Potušek

  4. Environmental Protection College, Trg mladosti 7, 3320, Velenje, Slovenia

    Elena Buzan

  5. Department of Fisheries, Apiculture, Wildlife Management and Special Zoology, Faculty of Agriculture, University of Zagreb, Svetošimunska cesta 25, 10000, Zagreb, Croatia

    Laura Iacolina, Andrea Rezić, Krešimir Kavčić & Nikica Šprem

  6. Department for Game Biology, Pathology and Breeding, Faculty of Veterinary Medicine, University of Zagreb, Heinzelova 55, 10000, Zagreb, Croatia

    Magda Sindičić

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  1. Toni Safner
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Correspondence to Elena Buzan.

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Safner, T., Buzan, E., Iacolina, L. et al. Microsatellite based assignment reveals history of extirpated mountain ungulate. Genetica 148, 41–46 (2020). https://doi.org/10.1007/s10709-020-00084-5

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