Advertisement

Mammal Research

, Volume 64, Issue 1, pp 127–131 | Cite as

Genomic variability in the extinct steppe bison (Bison priscus) compared to the European bison (Bison bonasus)

  • Astrid Vik StronenEmail author
  • Laura Iacolina
  • Cino Pertoldi
  • Malgorzata Tokarska
  • Brita Singers Sørensen
  • Simon Bahrndorff
  • Kamil Oleński
  • Stanislaw Kamiński
  • Pavel Nikolskiy
Short Communication

Abstract

In 2009, a frozen mummy of the steppe bison (SB) (Bison priscus) was discovered between the lower Kolyma River and the Alazeya River in northeast Siberia, Russia. The specimen was dated with 14C and estimated to have lived more than 48,000 14C years before present (BP). The relationship between SB and the European Bison (EB) (Bison bonasus), also known as wisent or European wood bison, is unresolved and it is unclear whether the SB and EB overlapped in space and time. The aim of our study was to compare genetic variability between the SB specimen and modern EB. We expected higher SB variability due to substantial bottlenecks in the EB approximately one century ago when it became extinct in the wild. The EB (n = 167) and the SB specimen were genotyped with the Illumina BovineHD BeadChip with 777,962 single-nucleotide polymorphism (SNP) markers. Steppe bison DNA was extracted and genotyped six times to account for genotyping errors due to low-quality DNA. We obtained a final set of 7786 SNPs. The mean number of private alleles in EB was 0.027 (± 0.0002) and in SB, it was 0.288 (± 0.0006). This could be explained by factors including differences between species, spatiotemporal divergence, and bottleneck effects. Investigation of historic EB samples could help resolve phylogenetic relationships, the role of the recent bottleneck, and provide information for conservation management to reduce the incidence of disease in the population and maintain its evolutionary potential.

Keywords

BovineHD BeadChip Mummy Private alleles Single nucleotide polymorphism 

Notes

Acknowledgements

We thank Fedor Shidlovsky of the Ice Age Museum, Moscow, Russia, for the access to the bison mummy sample, Jonas Kiis for the help with the preparation of SB DNA for sequencing, and Joaquin Muñoz Garcia for the comments on an earlier version of the manuscript.

Funding information

Research was supported by the University of Warmia and Mazury in Olsztyn, grant no 0105-0804 and the Aalborg Zoo Conservation Foundation (AZCF). AVS was supported by the Danish Natural Science Research Council (Grant 1337-00007). LI received funding from the Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie Action (Grant Agreement no. 656697). PN is supported by Russian Science Foundation project N 16-18-10265-RNF and the research complies with the state theme AAAA-A17-117030610119-6 of the Geological Institute RAS.

Supplementary material

13364_2018_387_MOESM1_ESM.docx (224 kb)
ESM 1 (DOCX 223 kb)
13364_2018_387_MOESM2_ESM.map (11.2 mb)
ESM 2 (MAP 11447 kb)
13364_2018_387_MOESM3_ESM.ped (7.4 mb)
ESM 3 (PED 7616 kb)
13364_2018_387_MOESM4_ESM.map (274 kb)
ESM 4 (MAP 274 kb)

References

  1. Boeskorov GG, Potapova OR, Protopopov AV, Plotnikov VV, Agenbroad LD, Kirikov KS, Pavlov, IS, Shchelchkova MV, Belolyubskii IN, Tomshin MD, Kowalczyk R, Davydov SP, Kolesov SD, Tikhonov AN, van der Plicht J (2016) The Yukagir Bison: the exterior morphology of a complete frozen mummy of the extinct steppe bison, Bison priscus from the early Holocene of northern Yakutia, Russia. Quat Int 406(Part B):94–110Google Scholar
  2. Chang CC, Chow CC, Tellier LC, Vattikuti S, Purcell SM, Lee JJ (2015) Second-generation PLINK: rising to the challenge of larger and richer datasets. GigaScience 4:7CrossRefGoogle Scholar
  3. Croitor R (2016) Genus Bison (Bovidae, Mammalia) in Early Pleistocene of Moldova. Conferința științifică națională cu participare internațională “Mediul și dezvoltare durabilă”, Ediția a III-a, At Chișinău, Volume: Materialele conferinței 14–20Google Scholar
  4. Das G, Hickey DR, Principio L, Conklin KT, Short J, Miller JR, McLendon G, Sherman F (1988) Replacements of lysine 32 in yeast cytochrome c. Effects on the binding and reactivity with physiological partners. J Biol Chem 263:18290–18297Google Scholar
  5. Douglas KD, Halbert ND, Kolenda C, Childers C, Hunter DL, Derr JN (2011) Complete mitochondrial DNA sequence analysis of Bison bison and bison-cattle hybrids: function and phylogeny. Mitochondrion 11:166–175CrossRefGoogle Scholar
  6. Flerov KK (1979) Systematics and evolution. In: Sokolov VE (ed) European bison: morphology, systematics, evolution, ecology. Nauka, Moscow, pp 9–112 (In Russian)Google Scholar
  7. Froese D, Stiller M, Heintzman PD, Reyes AV, Zazula GD, Soares AER, Meyer M, Hall E, Jensen BJL, Arnold LJ, MacPhee RDE, Shapiro B (2017) Fossil and genomic evidence constrains the timing of bison arrival in North America. PNAS 114:3457–3462CrossRefGoogle Scholar
  8. Gautier M, Moazami-Goudarzi K, Levéziel H, Parinello H, Grohs C, Rialle S, Kowalczyk R, Flori L (2016) Deciphering the wisent demographic and adaptive histories from individual whole-genome sequences. Mol Biol Evol 33:2801–2814CrossRefGoogle Scholar
  9. Gromova VI (1935) Primeval bison (Bison priscus Bojanus) in the USSR. (Pervobytny zubr v SSSR). Proceedings of the Zoological Institute of the Soviet Academy of Sciences 2(2–3):77–202 (In Russian)Google Scholar
  10. Guthrie RD (1980) Bison and man in North America. Can J Anthropol v 1:55–74Google Scholar
  11. Hartl DL, Clark AG (1997) Principles of population genetics, 3rd Ed. Sunderland, Massachusetts (Sinauer Associates, Inc). 519 pp.Google Scholar
  12. Kahlke R-D (1999) The history of the origin, Evolution and Dispersal of the Late Pleistocene Mammuthus–Coelodonta Faunal Complex in Eurasia (Large Mammals). 219 pp.Google Scholar
  13. Kirillova IV, Zanina OG, Kosintsev PA, Kul’kova MA, Lapteva EG, Trofimova SS, Chernova OF, Shidlovsky FK (2013) The first finding of a frozen Holocene bison (Bison priscus Bojanus, 1827) carcass in Chukotka. Dokl Biol Sci 452:296–299CrossRefGoogle Scholar
  14. Kurtên B (1968) Pleistocene mammals of Europe. London (Weidenfeld & Nicolson) 317pGoogle Scholar
  15. Lorenzen ED, Nogues-Bravo D, Orlando L, Weinstock J, Binladen J et al (2011) Species-specific responses of late quaternary megafauna to climate and humans. Nature 479:359–364CrossRefGoogle Scholar
  16. Markova AK, Puzachenko AY, van Kolfschoten T, Kosintsev PA, Kuznetsova TV, Tikhonov AN, Bachura OP, Ponomarev DV, van der Pflicht J, Kuitems M (2015) Changes in the Eurasian distribution of the musk ox (Ovibos moschatus) and the extinct bison (Bison priscus) during the last 50 ka BP. Quat Int 378:99–110CrossRefGoogle Scholar
  17. Massilani D, Guimaraes S, Brugal JP, Bennett EA, Tokarska M, Arbogast R-M, Baryshnikov G, Boeskorov G, Castel J-C, Davydov S, Madelaine S, Putelat O, Spasskaya NN, Uerpmann H-P, Grange T, Geigl E-M (2016) Past climate changes, population dynamics and the origin of Bison in Europe. BMC Biol 14(93):93CrossRefGoogle Scholar
  18. McDonald J (1981) North American Bison, Their classification and Evolution. University of California Press, Berkeley, Los Angeles, London. 316 pp.Google Scholar
  19. Nikolskiy P, Shidlovsky F (2014) Preliminary data from the study of the intact 50 000 YBP frozen mummy of the Anyuy steppe bison (Anyuy River, Arctic Far East). Abstract Book of the VIth International Conference on Mammoths and their Relatives. Scientific Annals, School of Geology, Aristotle University of Thessaloniki, Greece, Special Volume 102: 140Google Scholar
  20. Nikolskiy PA, Pitulko VV (2016) West Beringian bison population dynamics during the Late Pleistocene and Early Holocene. Günther, F. and Morgenstern, A. (Eds.): XI. International Conference On Permafrost – Book of Abstracts, 20–24 June 2016, Potsdam, Germany. P. 512–513Google Scholar
  21. Palacio P, Berthonaud V, Guérin C, Lambourdière J, Maksud F, Philippe M, Plaire D, Stafford T, Marsolier-Kergoat MC, Elalouf JM (2017) Genome data on the extinct Bison schoetensacki establish it as a sister species of the extant European bison (Bison bonasus). BMC Evol Biol 17:48CrossRefGoogle Scholar
  22. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539CrossRefGoogle Scholar
  23. Pertoldi C, Wójcik JM, Tokarska M, Kawałko A, Kristensen TN, Loeschcke V, Gregersen VR, Coltman D, Wilson GA, Randi E, Henryon M, Bendixen C (2010) Genome variability in European and American bison detected using the BovineSNP50 BeadChip. Cons Genet 11:627–634CrossRefGoogle Scholar
  24. Pucek Z, Belousova IP, Krasińska M, Krasiński Z, Olech W (2004) European Bison Status Survey and Conservation Action Plan. IUCN/SSC Bison Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK. Ix + 54 ppGoogle Scholar
  25. Shapiro B, Drummond AJ, Rambaut A, Wilson MC, Matheus PE, Sher AV, Pybus OG, Gilbert MT, Barnes I, Binladen J, Willerslev E, Hansen AJ, Baryshnikov GF, Burns JA, Davydov S, Driver JC, Froese DG, Harington CR, Keddie G, Kosintsev P, Kunz ML, Martin LD, Stephenson RO, Storer J, Tedford R, Zimov S, Cooper A (2004) Rise and fall of the Beringian steppe bison. Science 306:1561–1565CrossRefGoogle Scholar
  26. Soubrier J, Gower G, Kefei C, Richards SM, Llamas B et al (2016) Early cave art and ancient DNA record the origin of European bison. Nat Commun 7:13158CrossRefGoogle Scholar
  27. Tokarska M, Marshall T, Kowalczyk R, Wójcik JM, Pertoldi C, Kristensen TN, Loeschcke V, Gregersen VR, Bendixen C (2009) Effectiveness of microsatellite and SNP loci (BovineSNP50 BeadChip, Illumina®) in parentage assignment and identity analysis in species with low genetic diversity: the case of European bison. Heredity 103:326–332CrossRefGoogle Scholar
  28. Tokarska M, Pertoldi C, Kowalczyk R, Perzanowski K (2011) Genetic status of the European bison Bison bonasus after extinction in the wild and subsequent recovery. Mammal Rev 41:151–162CrossRefGoogle Scholar
  29. Verkaar ELC, Nijman IJ, Beeke M, Hanekamp E, Lenstra JA (2004) Maternal and paternal lineages in cross-breeding bovine species. Has wisent a hybrid origin? Mol Biol Evol 21:1165–1170CrossRefGoogle Scholar
  30. Węcek K, Hartmann S, Paijmans JLA, Taron U, Xenikoudakis G, Cahill JA, Heintzman PD, Shapiro B, Baryshnikov G, Bunevich AN, Crees JJ, Dobosz R, Manaserian N, Okarma H, Tokarska M, Turvey ST, Wójcik JM, Żyla W, Szymura JM, Hofreiter M, Barlow A (2017) Complex admixture preceded and followed the extinction of wisent in the wild. Mol Biol Evol 34:598–612Google Scholar

Copyright information

© Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2018

Authors and Affiliations

  • Astrid Vik Stronen
    • 1
    • 2
    Email author
  • Laura Iacolina
    • 1
    • 3
  • Cino Pertoldi
    • 1
    • 3
  • Malgorzata Tokarska
    • 4
  • Brita Singers Sørensen
    • 5
  • Simon Bahrndorff
    • 1
  • Kamil Oleński
    • 6
  • Stanislaw Kamiński
    • 6
  • Pavel Nikolskiy
    • 7
    • 8
  1. 1.Department of Chemistry and BioscienceAalborg UniversityAalborgDenmark
  2. 2.Biology Department, Biotechnical FacultyUniversity of LjubljanaLjubljanaSlovenia
  3. 3.Aalborg ZooAalborgDenmark
  4. 4.Mammal Research InstitutePolish Academy of SciencesBiałowieżaPoland
  5. 5.Department of Experimental Clinical OncologyAarhus University HospitalAarhus CDenmark
  6. 6.Department of Animal GeneticsUniversity of Warmia and Mazury in OlsztynOlsztynPoland
  7. 7.Geological Institute of the Russian Academy of SciencesMoscowRussia
  8. 8.Ice Age MuseumNational Alliance of Shidlovskiy “Ice Age”MoscowRussia

Personalised recommendations