doi: 10.15389/agrobiology.2017.6.1083eng

UDC 636.977:599.735.3:575.22

Supported financially by Russian Science Foundation, project 16-16-10068.


IN REINDEER (Rangifer tarandus) (review)

V.R. Kharzinova, T.E. Deniskova, A.A. Sermyagin, A.V. Dotsev,
A.D. Solovieva, N.A. Zinovieva

L.K. Ernst Federal Science Center for Animal Husbandry, Federal Agency of Scientific Organizations, 60, pos. Dubrovitsy, Podolsk District, Moscow Province, 142132 Russia,
e-mail (corresponding author),,,,,

Kharzinova V.R.
Sermyagin A.A.
Solovieva A.D.
Deniskova T.E.
Dotsev A.V.
Zinovieva N.A.

Received September 9, 2017


Reindeer Rangifertarandus, the only member of the genus Rangifer, is an important component of the food security of the indigenous people of the Russian North, and is an indispensable part of the Arctic ecosystems (А. Savchenko, 2014; V.G. Loginov, 2014). To-date, due to a number of unfavorable natural and anthropogenic factors, population number of both domestic and wild reindeer is sharply decreasing. This leads to a loss of the genetic diversity, which is sufficient for survival in new habitats (Y.A. Stolpovsky, 2010). In this regard, it is significant to monitor the genetic diversity of resource breeds and wild reindeer populations with use of genetic markers. The review summarizes the results of the genetic diversity studies of reindeer using different molecular genetic analysis methods. The first genetic studies of reindeer began with the assessment of serum transferrin polymorphism in the 1960s (В. Gahne et al., 1961; М. Braend, 1964). Types of transferrin were distinguished from each other by the band position and mobility in gel electrophoresis (A.V. Soldal et al., 1979; K.H. Roed, 1985; P.N. Shubin et al., 1988). With the development of genetic technologies, DNA markers gained popularity (M. Çaliskan, 2012). The so-called “anonymous” markers (initially RAPD and later ISSR) became the first DNA markers used to investigate the biodiversity of reindeer populations (V.V. Goncharov et al., 2009; N.V. Kol et al., 2006; T.M. Romanenko et al., 2014; G.Y. Bryzgalov, 2016). Since the publication of the complete nucleotide sequence of the control region of the mitochondrial genome of reindeer subspecies of Eurasia and North America, analysis of the polymorphism of mitochondrial DNA (mtDNA) has become widespread (M.A. Cronin, 1992; E. Randi et al., 2001; A.V. Davydov et al., 2007; M.V. Kholodova et al., 2009; A.N. Korolev et al., 2017). The method is a highly informative for revealing the phylogeny and origin of breeds and populations by the maternal line (Ø. Flagstad et al., 2003; N.A. Akopyan et al., 2016). Microsatellites have found great implementation in applied studies of genetics of reindeer (establishment of genetic structure, characteristic of allele pool, identification and differentiation of individuals) (K.H. Røed et al., 1998; B.I. Jepsen et al., 2002; R. Courtois et al., 2003; M.A. Cronin et al., 2003; K.A. Zittlau, 2004; P.D. McLoughlin et al., 2004; A.D. McDevitt et al., 2009; A.I. Baranova et al., 2016). For Russian reindeer populations, a multiplex panel of nine microsatellites was developed (V.R. Kharzinova et al., 2015). It is successfully using in the routine testing of reindeer, including the detection of hybrids between wild and domestic forms (V.R. Kharzinova et al., 2016). However, with the development of new high-throughput technologies and new-generation analytical equipment (А. Vignal, 2002; E.K. Khlestkina, 2013), DNA chips based on genotyping of multiple SNPs come to the fore in genetic studies of farm animals (F.J. Steemers et al., 2007; S. Mastrangelo et al., 2014; Т.Е. Deniskova et al., 2015; В. Slim et al., 2015, N.A. Zinovieva et al., 2016; Т.Е. Deniskova et al., 2016, R. Yonesaka et al., 2016). To-date, despite the fact that there is no the specific DNA chip for reindeer, the use of the Bovine SNP50 BeadChip, designed for cattle, is the most effective and highly informative method for studying the reindeer genome (V.R. Kharzinova et al., 2015; V.R. Kharzinova et al., 2016; V.R. Kharzinova et al., 2017).

Keywords: Rangifer tarandus, reindeer, genetic diversity, genetic marker, SNP, DNA chip.


Full article (Rus)

Full article (Eng)



  1. Çaliskan M. Analysis of genetic variation in animals. Rijeka, Croatia, 2012. ISBN: 978-953-51-0093-5.
  2. Dubinin N.P., Mashurov A.M. Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 1986, 2: 76-79 (in Russ.).   
  3. Altukhov Yu.P. Geneticheskie protsessy v populyatsiyakh. Moscow, 1989 (in Russ.).   
  4. Kuznetsova I.V. Monitoring geneticheskoi struktury populyatsii krupnogo rogatogo skota cherno-pestroi porody. Avtoreferat kandidatskoi dissertatsii [Monitoring of genetic structure of black mottled cattle population. PhD Thesis]. Ryazan', 2010 (in Russ.).   
  5. Hamrick J.L., Godt M.J.W. Allozyme diversity in plant species. In: Plant population genetics, breeding, and genetic resources. A.H. Brown, M.T. Clegg, A.L. Kahler, B.S. Weir (eds.) Sunderland, 1989.
  6. Sheng Y., Zheng W., Pei K., Ma K. Genetic variation within and among populations of a dominant desert tree Haloxylon ammodendron (Amaranthaceae) in China. Ann. Bot., 2005, 96(2): 245-252 CrossRef
  7. Stolpovskii Yu.A. Populyatsionno-geneticheskie osnovy sokhraneniya resursov genofondov domestitsirovannykh vidov zhivotnykh. Avtoreferat doktorskoi dissertatsii [Genetic and population aspects of gene pool preservation in domesticated animal species. DSci Thesis]. Moscow, 2010 (in Russ.).   
  8. Vtoroi doklad o sostoyanii mirovykh geneticheskikh resursov zhivotnykh dlya proizvodstva prodovol'stviya i vedeniya sel'skogo khozyaistva. 2015 [Second report of world genetic resources for food production and agriculture, 2015]. Available Accessed September 18, 2017 (in Russ.).   
  9. Savchenko A. Informatsionnyi portal Izvestiya. Available Accessed September 18, 2017 (in Russ.).   
  10. Loginov V.G. Agrarnyi vestnik Urala, 2014, 11(129): 74-77 (in Russ.).   
  11. Donahoe B. The troubled taiga: survival on the move for the last nomadic reindeer herders of south Siberia, Mongolia, and China. In: Cultural survival quarterly. Cambridge (Spring), 2003: 12-18.
  12. Kol N.V. Geneticheskii polimorfizm v populyatsii severnogo olenya (Rangifer tarandus) Respubliki Tyva (Todzhinskogo raiona). Avtoreferat kandidatskoi dissertatsii [Gene polymorphism in Tyva reindeer (Rangifer tarandus)population of Todzhinskii region. PhD Thesis]. Moscow, 2006 (in Russ.).   
  13. Braend M. Polymorphism in the serum proteins of the reindeer. Nature, 1964, 203: 674 CrossRef
  14. Gahne B., Rendel J. Blood and serum groups in reindeer compared with those in cattle. Nature, 1961, 192: 529-530 CrossRef
  15. Storset A., Osaisen B., Wika M. Bjarghov R. Genetic markers in the Spitsbergen reindeer. Hereditas, 1978, 88: 113-115 CrossRef
  16. Soldal A.V., Staaland. H. Genetic variation in Norwegian reindeer. Proc. 2nd. Int. Reindeer/Caribou Symp. Roros, Norway, 1979: 396-402.
  17. Roed K.H. Genetic differences at the transferrin locus in Norwegian semidomestic and wild reindeer (Rangifer tarandus L.). Hereditas, 1985, 102: 199-206 CrossRef
  18. Shubin P.N. Genetika, 1969, 5(1): 37-41 (in Russ.).   
  19. Shubin P.N., Efimtseva E.A. Biokhimicheskaya i populyatsionnaya genetika severnogo olenya [Biochamical and population genetics of reindeer]. Leningrad, 1988 (in Russ.).   
  20. Shubin P.N., Ionova T.A. Tsitologiya i genetika, 1983, 25(3): 60-62 (in Russ.).   
  21. Yuzhakov A.A. Nenetskaya aborigennaya poroda severnykh olenei. Avtoreferat doktorskoi dissertatsii [Nenets indigenous reindeer breed. DSci Thesis]. Novosibirsk, 2004 (in Russ.).   
  22. Roed K.H. Genetic variability in Norwegian semi-domestic reindeer (Rangifer tarandus L.). Hereditas, 1985, 102: 177-184 (10.1111/j.1601-5223.1985.tb00612.x).
  23. Woese C., Kandler O., Wheelis M. Towards a natural system of organisms: Proposal for the domains Archaea, Bacteria, and Eucarya. PNAS USA, 1990, 87: 4576-4579.
  24. Abramson N.I. Trudy Zoologicheskogo instituta RAN, 2009, prilozhenie # 1: 185-198 (in Russ.).   
  25. Dodokhov V.V. Otsenka bioraznoobraziya loshadei yakutskoi porody s ispol'zovaniem DNK markerov. Avtoreferat kandidatskoi dissertatsii [Biodiversity of Yakut horse breed as estimated by DNA markers. PhD Thesis]. Yakutsk, 2017 (in Russ.).   
  26. Goncharov V.V., Mitrofanova O.V., Dement'eva N.V., Tyshchenko V.I., Sergeeva O.K., Batyrev O.M. Dostizheniya nauki i tekhniki APK, 2009: 43-45 (in Russ.). 
  27. Romanenko T.M., Kalashnikova L.A., Filippova G.I., Laishev K.A. Dostizheniya nauki i tekhniki APK, 2014, 4: 68-71 (in Russ.).   
  28. Romanenko T.M., Filippova G.I. Simvol nauki, 2015, 11: 44-52 (in Russ.).   
  29. Kol N.V., Lazebnyi O.E. Genetika, 2006, 42(12): 1731-1734 (in Russ.).   
  30. Bryzgalov G.Ya. Vestnik DVO RAN, 2016, 2: 108-112 (in Russ.).   
  31. Akopyan N.A., Kostyunina O.V., Zinov'eva N.A. Dostizheniya nauki i tekhniki APK, 2016, 7: 93-95 (in Russ.). 
  32. Flagstad Ø., Røed K.H. Refugial origins of reindeer (Rangifer tarandus L.) inferred from mitochondrial DNA sequences. Evolution, 2003, 57(3): 658-670.
  33. Kol N.V. Geneticheskii polimorfizm v populyatsii severnogo olenya (Rangifer tarandus) Respubliki Tyva (Todzhinskogo raiona). Avtoreferat doktorskoi dissertatsii [Gene polymorphism in Tyva reindeer (Rangifer tarandus)population of Todzhinskii region. PhD Thesis]. Moscow, 2006 (in Russ.).   
  34. Davydov A.V., Kholodova M.V., Meshcherskii I.G., Gruzdev A.R., Sip-
    ko T.P., Kol N.V., Tsarev S.A., Zheleznov-Chukotskii N.K., Miruten-
    ko B.C., Gubar' Yu.P., Lin'kov A.B., Rozhkov Yu.I. Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2007, 6: 48-53.
  35. Kholodova M.V., Zvychainaya E.Yu., Rozhnov V.V., Khakhin G.V., Davydov A.V., Rozhkov Yu.I. Vestnik okhotovedeniya, 2009, 6(2): 151-154 (in Russ.).   
  36. Baranova A.I., Kholodova M.V., Davydov A.V., Rozhkov Yu.I. Genetika, 2012, 48(9): 1-7 (in Russ.).   
  37. Korolev A.N., Mamontov V.N., Kholodova M.V., Baranova A.I., Shadrin D.M., Poroshin E.A., Efimov V.A., Kochanov S.K. Zoologicheskii zhurnal, 2017, 96(1): 106-118 (doi: 10.7868/S0044513417010147) (in Russ.).   
  38. Cronin M.A. Intraspecific variation in mitochondrial DNA of North American cervids. J. Mamm., 1992, 73(1): 70-82.
  39. Gravlund P., Meldgaard M., Paabo S., Arctander P. Polyphyletic origin of the small-bodied, high-arctic subspecies of tundra reindeer (Rangifer tarandus). Mol. Phylogenet. Evol., 1998, 10(2): 151-159 CrossRef
  40. Douzery E., Randi E. The mitochondrial control region of Cervidae: Evolutionary patterns and phylogenetic content. Mol. Biol. Evol., 1997, 14(11): 1154-1166.
  41. Polziehn R.O., Strobeck C. Phylogeny of wapiti, red deer, sika deer, and other North American cervids as determined from mitochondrial DNA. Mol. Phylogenet. Evol., 1998, 10(2): 249-258.
  42. Randi E., Pierpaoli M., Danilkin A. Mitochondrial DNA polymorphism in populations of Siberian and European roe deer (Capreolus pygargus and C. capreolus). Heredity, 1998, 80: 429-437.
  43. Litt M., Luty J.A. A hypervariable microsatellite revealed by in vitro amplification of dinucleotide repeat within the cardiac muscle actin gene. Am. J. Hum. Genet., 1989, 44: 397-401.
  44. Tautz D. Hypervariability of simple sequences as a general source for polymorphic DNA markers. Nuc. Acids Res., 1989, 17: 6463-6471.
  45. Weber J.L., May P.E. Abundant class of human DNA polymorphisms which can be typed using the polymerase chain reaction. Am. J. Hum. Genet., 1989, 44(3): 388-396.
  46. Chung A.M., Staub J.E., Chen J.F. Molecular phylogeny of Cucumis species as revealed by consensus chloroplast SSR marker length and sequence variation. Genome, 2006, 49: 219-229 CrossRef
  47. Rajendrakumar P., Biswal A.K., Balachandran S.M., Srinivasarao K., Sundaram R.M. Simple sequence repeats in organellar genomes of rice: frequency and distribution in genic and intergenic regions. Bioinformatics, 2007, 23: 1-4 CrossRef
  48. Engel S.R., Linn R.A., Taylor J.F., Davis S.K. Conservation of microsatellite loci across species of artiodactyls: implications for population studies. J. Mammal., 1996, 77: 504-518 CrossRef
  49. Wilson G.A., Strobeck C., Wu L., Coffin J.W. Characterization of microsatellite loci in caribou Rangifer tarandus, and their use in other artiodactyls. Mol. Ecol., 1997, 65: 697-699 CrossRef
  50. Cronin M.A., Patton J.C., Balmysheva N., MacNeil M.D. Genetic variation in caribou and reindeer (Rangifer tarandus). Anim. Genet., 2003, 34: 33-41 CrossRef
  51. Røed K.H., Midthjell L. Microsatellites in reindeer, Rangifer tarandus, and their use in other cervids. Mol. Ecol., 1998, 7: 1773-1776 CrossRef
  52. Røed K., Flagstad Ø, Nieminen M., Holand Ø., Dwyer M.J., Carles Vilà N.R. Genetic analyses reveal independent domestication origins of Eurasian reindeer. Proceedings of the Royal Society B, 2008, 275: 1849-1855 CrossRef
  53. Zittlau K.A. Population genetic analyses of North American caribou (Rangifer tarandus). PhD Thesis. Canada, University of Alberta, 2004.
  54. Courtois R., Bernatche L., Ouellet J.P., Breton L. Significance of caribou (Rangifer tarandus) ecotypes from a molecular genetics viewpoint. Conserv. Genet., 2003, 4: 393-404 CrossRef
  55. McLoughlin P.D., Paetkau D., Duda M., Boutin S. Genetic diversity and relatedness of boreal caribou populations in western Canada. Biol. Conserv., 2004, 118: 593-598 CrossRef
  56. Côté S.D., Dallas J.F., Marshall F., Irvine R.J., Langvatn R., Albon S.D. Microsatellite DNA evidence for genetic drift and philopatry in Svalbard reindeer. Mol. Ecol., 2002, 11: 1923-1930 CrossRef
  57. Jepsen B.I., Siegismund H.R., Fredholm M. Population genetics of the native caribou (Rangifer tarandus groenlandicus) and the semi-domestic reindeer (Rangifer tarandus tarandus) in Southwestern Greenland: evidence of introgression. Conserv. Genet., 2002, 3: 401-409 CrossRef
  58. McDevitt A.D., Mariani S., Hebblewhite M., DeCesare N.J., Morgantini L., Seip D., Weckworth B.V., Musiani M. Survival in the Rockies of an endangered hybrid swarm from diverged caribou (Rangifer tarandus) lineages. Mol. Ecol., 2009, 18: 665-679 CrossRef
  59. Kharzinova V.R., Gladyr' E.A., Fedorov V.I., Romanenko T.M., Shimit L.D., Laishev K.A., Kalashnikova L.A., Zinov'eva N.A. Development of multiplex microsatellite panel to assess the parentage verification in and differentiation degree of reindeer populations (Rangifer tarandus). Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2015, 50(6): 756-765 CrossRef
  60. Kharzinova V.R., Dotsev A.V., Solovieva A.D., Fedorov V.I., Brem G., Zinovieva N.A. Estimation of biodiversity and population structure of Russian reindeer (Rangifer tarandus) breeds inhabiting Northeastern Siberia (Republic of Sakha—Yakutia) using microsatellite markers. Journal of Acta Fytotechnica et Zootechnica, 2016, 19: 87-92 CrossRef
  61. Kholodova M.V., Baranova A.I., Mizin I.A., Rozhnov V.V., Sipko T.P., Davydov A.V., Rozhkov Yu.I. Materialy Mezhdunarodnogo soveshchaniya «Teriofauna Rossii i sopredel'nykh territorii». X S"ezd Teriologicheskogo obshchestva pri RAN [Proc. Int. Workshop on Theriofauna of Russia and Adjacent Territories]. Moscow, 2016: 445 (in Russ.).   
  62. Røed K.H. Refugial origin and postglacial colonization of Holarctic reindeer and caribou. Rangifer, 2003, 25: 19-30.
  63. Ball M.C., Finnegan L., Manseau M., Wilson P. Integrating multiple analytical approaches to spatially delineate and characterize genetic population structure: an application to boreal caribou (Rangifer tarandus caribou) in central Canada. Conserv. Genet., 2010, 11: 2131-2143 CrossRef
  64. Kushny J., Coffin J., Strobeck C. Genetic survey of caribou populations using microsatellite DNA. Rangifer, 1994, Special Issue No. 9: 351-354 CrossRef
  65. Baranova A.I., Kholodova M.V., Sipko T.P. Materialy Vserossiiskoi nauchnoi konferentsii, posvyashchennoi 70-letnemu yubileyu kafedry «Zoologiya i ekologiya» Penzenskogo gosudarstvennogo universiteta i pamyati professora V.P. Denisova (1932-1997) «Aktual'nye voprosy sovremennoi zoologii i ekologii zhivotnykh» [Proc. Conf. dedicated to 70th Anniversary of Zoology and Evology Department of Penza Uiversity]. Penza, 2016: 21 (in Russ.).   
  66. Kharzinova V.R., Dotsev A.V., Kramarenko A.S, Layshev K.A., Romanenko T.M., Solov’eva A.D., Deniskova T.E., Kostyunina O.V., Brem G., Zinovieva N.A. Study of the allele pool and the degree of genetic introgression of semi-domesticated and wild populations of reindeer (Rangifer tarandus L., 1758) using microsatellites. Agricultural Biology, 2016, 51(6): 811-823 CrossRef (in Engl.).
  67. Kotova S.A., Shilo E.A., Zablotskaya E.A., Nedzvetskaya D.E., Tsybovskii I.S. Trudy Belorusskogo gosudarstvennogo universiteta, 2016, 11(2): 56-69 (in Russ.).   
  68. Zinov'eva N.A., Dotsev A.V., Sermyagin A.A., Vimmers K., Reier Kh., Solkner I., Deniskova T.E., Brem G. Study of genetic diversity and population structure of five russian cattle breeds using whole-genome SNP analysis. Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2016, 51(6): 788-800 CrossRef (in Engl.).
  69. Vignal A., Milan D., SanCristobal M., Eggen A. A review on SNP and other types of molecular markers and their use in animal genetics. Genet. Sel. Evol., 2002, 34: 275-305 CrossRef
  70. Khlestkina E.K. Vavilovskii zhurnal genetiki i selektsii, 2013, 17(4/2): 1044-1054 (in Russ.). 
  71. Steemers F.J., Gunderson K.L. Whole genome genotyping technologies on the BeadArrayTM platform. Biotechnol. J., 2007, 2: 41-49 CrossRef
  72. Slim B.J., Mekki B., Mehdi M.B., Lee J.H., Lee S.H. Genome-wide insights into population structure and genetic history of tunisian local cattle using the illumina bovinesnp50 beadchip. BMC Genomics, 2015, 16(1): 677 CrossRef
  73. Yonesaka R, Sasazaki S., Yasue H., Niwata S., Inayoshi Y., Mukai F., Mannen H. Genetic structure and relationships of 16 Asian and European cattle populations using DigiTag2 assay. Anim. Sci. J., 2016, 87: 190-196 CrossRef
  74. Deniskova T.E., Okhlopkov I.M., Sermyagin A.A., Gladyr' E.A., Bagirov V.A., Selkner I., Mamaev N.V., Brem G., Zinov'eva N.A. Doklady Akademii nauk, 2016, 469(5): 625-630 (in Russ.).   
  75. Mastrangelo S., Gerlando R.D., Tolone M., Tortorici L., Sardina M.T., Portolano B. and International Sheep Genomics Consortium. Genome wide linkage disequilibrium and genetic structure in Sicilian dairy sheep breeds. BMC Genet., 2014, 15: 108 CrossRef
  76. Deniskova T.E., Sermyagin A.A., Bagirov V.A., Okhlopkov I.M., Gladyr' E.A., Ivanov R.V., Brem G., Zinov'eva N.A. Genetika, 2016, 52(1): 90-96 CrossRef (in Russ.).   
  77. Haynes G.D., Latch E.K. Identification of novel single nucleotide polymorphisms (SNPs) in deer (Odocoileus spp.) using the BovineSNP50 BeadChip. PLoS ONE, 2012, 7: e36536 CrossRef
  78. Kasarda R., Moravcíková N., Trakovická A. Advances in genomic sequencing using Bovine SNP BeadChip in deer. Acta Fytotechnica et Zootechnica, 2014, 17(2): 65-71 CrossRef
  79. Kharzinova V.R., Dotsev A.V., Okhlopkov I.M., Layshev K.A., Fedorov V.I., Shimit L.D., Brem G., Wimmers K., Reyer H., Zinovieva N.A. Genetic characteristics of semi-domesticated reindeer populations from different regions of Russia based on SNP analysis. J. Anim. Sci., 2016, 94(Suppl. 5.): 166 CrossRef
  80. Kasarda R., Moravcíková N., Zidek R., Mészáros G., Kadlecík O., Trakovická A., Pokorádi J. Investigation of the genetic distances of bovids and cervids using BovineSNP50k BeadChip. Arch. Anim. Breed., 2015, 58: 57-63 CrossRef
  81. Kharzinova V.R., Sermyagin A.A., Gladyr E.A., Okhlopkov I.M., Brem G., Zinovieva N.A. A study of applicability of SNP chips developed for Bovine and Ovine species to whole-genome analysis of reindeer Rangifer tarandus. J. Heredity, 2015, 106(6): 758-761. CrossRef
  82. Kharzinova V.R., Dotsev A.V., Solovieva A.D., Fedorov V.I., Okhlopkov I.M., Wimmers K., Reyer H., Brem G., Zinovieva N.A. Population-genetic characteristics of domestic reindeer of Yakutia based on whole-genome SNP analysis. Agricultural Biology, 2017, 52(4): 669-678 CrossRef (in Engl.).