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The use of museum skins for genomic analyses of temporal genetic diversity in wild species

  • Astrid Vik Stronen
  • Laura Iacolina
  • Cino Pertoldi
  • Szilvia Kusza
  • Pavel Hulva
  • Ihor Dykyy
  • Ilpo Kojola
  • Søren Faurby
Perspectives

Abstract

Analyses of museum specimens can help illuminate temporal changes in wildlife genetics and distributions, and the objective of our study was to evaluate the suitability of skin samples from the past century for genomic analyses. We examined two European species with extensive genomic resources and existing data: the wild boar (Sus scrofa) and the wolf (Canis lupus). Populations of both species declined during the twentieth century, followed by a strong recovery. Moreover, Carpathian Mountain wolves are genetically divergent from Northern European lowland wolves, and their evolutionary history is incompletely understood. We analysed genetic variation from skins of 14 European and Near Eastern wild boars (1903–1948) and 18 Carpathian and Northern wolves (1938–1998). Samples were genotyped in duplicates with standard Illumina single nucleotide polymorphism (SNP) arrays (wild boar 60 K and wolves 170 K), and we retained SNPs with a genotyping rate of > 90%. We obtained a final set of 1595 SNPs for six wild boars (genotyping rate 0.99) and 1806 SNPs for 18 wolves (genotyping rate 0.96). We merged the best performing duplicate with modern data and calculated polymorphism (P), observed (HO) and expected (HE) heterozygosity per population. Our findings underline the difficulties in obtaining quality genomic profiles from museum skins, though a limited number of SNPs provided insights for future research. Wild boars exhibited lower polymorphism in historical than modern samples. In contrast, patterns in wolves appeared spatial rather than temporal, with higher P, HO and HE observed in Carpathian than Northern wolves across historical and modern samples.

Keywords

Canis lupus Historic samples Museum collections Single nucleotide polymorphism Sus scrofa 

Notes

Acknowledgements

We thank Marcel Eras, Bendegúz Mihalik, Massimo Scandura, Frank Zachos, and staff from the Mammal Research Institute Polish Academy of Sciences. We gratefully acknowledge the assistance of the National History Museums in Vienna and Hungary, the University of Sassari, the Finnish Museum of Natural History, the National Museum Prague and Silesian Museum Opava of the Czech Republic, and the Slovak National Museum in obtaining skin samples and information. AVS and SF were supported by the Danish Natural Science Research Council (AVS #1337-00007, SF #4090-00227), LI by the European Union’s Horizon 2020 (MCSA-IF #656697). The work was supported by the Aalborg Zoo Conservation Foundation.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

12686_2018_1036_MOESM1_ESM.pdf (180 kb)
Supplementary material 1 (PDF 179 KB)

References

  1. Alexandri P, Megens H-J, Crooijmans RPMA, Groenen MAM, Goedbloed DJ, Herrero-Medrano JM, Rund LA, Schook LB, Chatzinikos E, Triantaphyllidis C, Triantaphyllidis A (2017) Distinguishing migration events of the different timing for wild boar in the Balkans. J Biogeogr 44:259–270CrossRefGoogle Scholar
  2. Bakan J, Lavadinović V, Popović Z, Paule L (2014) Genetic differentiation of grey wolf population (Canis lupus L.) from Balkan and Carpathians. Balkan J Wildl Res 1:87–93Google Scholar
  3. Casas-Marce M, Marmesat E, Soriano L, Martínez-Cruz B, Lucena-Perez M, Nocete F, Rodríguez-Hidalgo A, Canals A, Nadal J, Detry C, Bernáldez-Sánchez CDE, Fernández-Rodríguez C, Pérez-Ripoll M, Stiller M, Hofreiter M, Rodríguez A, Revilla E, Delibes M, Godoy JA (2017) Spatio-temporal dynamics of genetic variation in the Iberian Lynx along its path to extinction reconstructed with ancient DNA. Mol Biol Evol 34:2893–2907CrossRefPubMedGoogle Scholar
  4. Czarnomska SD, Jędrzejewska B, Borowik T, Niedziałkowska M, Stronen AV, Nowak S, Mysłajek RW, Okarma H, Konopiński M, Pilot M, Śmietana 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 14:573–588CrossRefGoogle Scholar
  5. 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 ZSL, BirdLife International and the European Bird Census Council. ZSL, LondonGoogle Scholar
  6. Goedbloed DJ, van Hooft P, Megens H-J, Langenbeck K, Lutz W, Crooijmans RPMA., van Wieren SE, Ydenberg RC, Prins HHT (2013) Reintroductions and genetic introgression from domestic pigs have shaped the genetic population structure of Northwest European wild boar. BMC Genet 14:43CrossRefPubMedPubMedCentralGoogle Scholar
  7. Hulva P, Bolfíková B, Woznicová V, Jindřichova M, Benešová M, Mysłajek RW, Nowak S, Szewczyk M, Niedźwiecka N, Figura M, Hájková A, Sándor AD, Zyka V, Romportl D, Kutal M, Finďo S, Antal V (2018) Wolves at the crossroad: fission–fusion range biogeography in the Western Carpathians and Central Europe. Divers Distrib 24:179–192CrossRefGoogle Scholar
  8. Iacolina L, Scandura M, Goedbloed DJ, Alexandri P, Crooijmans RPMA., Larson G, Archibald A, Apollonio M, Schook LB, Groenen MAM, Megens H-J (2016) Genomic diversity and differentiation of a managed island wild boar population. Heredity 116:60–67CrossRefPubMedGoogle Scholar
  9. Jansson E, Ruokonen M, Kojala I, Aspi J (2012) Rise and fall of a wolf population: genetic diversity and structure during recovery, rapid expansion and drastic decline. Mol Ecol 21:5178–5193CrossRefPubMedGoogle Scholar
  10. Jombart T, Devillard S, Dufour AB, Pontier D (2008) Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 101:92–103CrossRefPubMedGoogle Scholar
  11. Larson G, Albarella U, Dobney K, Rowley-Conwy P, Schibler J, Tresset A et al (2007) Ancient DNA, pig domestication, and the spread of the Neolithic into Europe. Proc Natl Acad Sci USA 104:15276–15281CrossRefPubMedPubMedCentralGoogle Scholar
  12. Linck EB, Hanna ZR, Sellas A, Dumbacher JP (2017) Evaluating hybridization capture with RAD probes as a tool for museum genomics with historical bird specimens. Ecol Evol 7:4755–4767CrossRefPubMedPubMedCentralGoogle Scholar
  13. Manunza A, Zidi A, Yeghoyan S, Balteanu VA, Carsai TC, Scherbakov O, Ramírez O, Eghbalsaied S, Castelló A, Mercadé A, Amills M (2013) A high throughput genotyping approach reveals distinctive autosomal genetic signatures for European and Near Eastern wild boar. PLoS ONE 8(2):e55891CrossRefPubMedPubMedCentralGoogle Scholar
  14. Oleński K, Tokarska M, Hering DM, Puckowska P, Ruść A, Pertoldi C, Kamiński S (2015) Genome-wide association study for posthitis in the free-living population of European bison (Bison bonasus). Biol Direct 10:2CrossRefPubMedPubMedCentralGoogle Scholar
  15. Pereira HM, Navaro LM (eds) (2015) Rewilding European landscapes. Springer, New YorkGoogle Scholar
  16. Pilot M, Jędrzejewski W, Branicki W, Sidorovich V, Jędrzejewska B, Stachura K, Funk SM (2006) Ecological factors influence population genetic structure of European grey wolves. Mol Ecol 15:4533–4553CrossRefPubMedGoogle Scholar
  17. Pilot M, Greco C, vonHoldt BM, Jędrzejewska B, Randi E, Jędrzejewski W, Sidorovich V, Ostrander EA, Wayne RK (2014) Genome-wide signatures of population bottlenecks and diversifying selection in European wolves. Heredity 112:428–442CrossRefPubMedGoogle Scholar
  18. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de bakker PI, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575CrossRefPubMedPubMedCentralGoogle Scholar
  19. R Development Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  20. Scandura M, Iacolina L, Crestanello B, Pecchioli E, Di Benedetto MF, Russo V, Davoli R, Apollonio M, Bertorelle G (2008) Ancient vs. recent processes as factors shaping the genetic variation of the European wild boar: are the effects of the last glaciation still detectable? Mol Ecol 17:1745–1762CrossRefPubMedGoogle Scholar
  21. Straka M, Paule L, Ionescu O, Štofík J, Adamec M (2012) Microsatellite diversity and structure of Carpathian brown bears (Ursus arctos): consequences of human caused fragmentation. Conserv Genet 13:153–164CrossRefGoogle Scholar
  22. Stronen AV, Jędrzejewska B, Pertoldi C, Demontis D, Randi E, Niedziałkowska M, Pilot M, Sidorovich VE, Dykyy I, Kusak J, Tsingarska E, Kojola I, Karamanlidis AA, Ornicans A, Lobkov VA, Dumenko V, Czarnomska S (2013) North-south differentiation and a region of high diversity in European wolves (Canis lupus). PLoS ONE 8(10):e76454CrossRefPubMedPubMedCentralGoogle Scholar
  23. Stronen AV, Jędrzejewska B, Pertoldi C, Demontis D, Randi E, Niedziałkowska M, Borowik T, Sidorovich VE, Kusak J, Kojola I, Karamanlidis AA, Ozolins J, Dumenko V, Czarnomska SD (2015) Genome-wide analyses suggest parallel selection for universal traits may eclipse local environmental selection in a highly mobile carnivore. Ecol Evol 5:4410–4425CrossRefPubMedPubMedCentralGoogle Scholar
  24. Suchan T, Pitteloud C, Gerasimova NS, Kostikova A, Schmid S, Arrigo N, Pajkovic M, Ronikier M, Alvarez N (2016) Hybridization capture using RAD probes (hyRAD), a new tool for performing genomic analyses on collection specimens. PLoS ONE 11(3):e0151651CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Chemistry and BioscienceAalborg UniversityAalborgDenmark
  2. 2.Biology Department, Biotechnical FacultyUniversity of LjubljanaLjubljanaSlovenia
  3. 3.Aalborg ZooAalborgDenmark
  4. 4.Animal Genetics Laboratory, Institute of Animal Science, Biotechnology and Nature ConservationUniversity of DebrecenDebrecenHungary
  5. 5.Department of ZoologyCharles UniversityPragueCzech Republic
  6. 6.Department of Biology and EcologyCharles University of OstravaOstravaCzech Republic
  7. 7.Department of Zoology, Faculty of BiologyIvan Franko National University of LvivLvivUkraine
  8. 8.Natural Resources Institute FinlandRovaniemiFinland
  9. 9.Department of Biological and Environmental SciencesUniversity of GothenburgGothenburgSweden
  10. 10.Gothenburg Global Biodiversity CentreGothenburgSweden

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