Abstract
The nucleotide sequences of the alleles of the DRB3 gene of the major histocompatibility complex (class II) of saiga antelope are described. A high degree of heterozygosity is found. The results of the analysis are consistent with the hypothesis of overdominance of heterozygotes. Phylogenetic relations of the DRB3 gene alleles of the saiga antelope and other Bovidae species do not correspond to the systematic position of Saiga tatarica. It is assumed that the polymorphism of the DRB3 gene alleles of saiga is primarily due to the variety of extracellular pathogens (bacteria, protozoa, helminths, and others) affecting its population during the evolutionary history of the species.
Similar content being viewed by others
REFERENCES
Soulé, M.E., Viable Populations for Conservation, Cambridge: Cambridge Univ. Press, 1987. https://doi.org/10.1017/CBO9780511623400
Luikart, G., Sherwin, W.B., Steele, B.M., and Allendorf, F.W., Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change, Mol. Ecol., 1998, no. 7, pp. 963—974. https://doi.org/10.1046/j.1365-294x.1998.00414.x
Frankham, R., Ecosystem recovery enhanced by genotypic diversity, Heredity, 2005, vol. 95, p. 183. https://doi.org/10.1038/sj.hdy.6800706
Fox, C.W. and Reed, D.H., Inbreeding depression increases with environmental stress: an experimental study and meta-analysis, Evolution, 2011, vol. 65, no. 1, pp. 246—258. https://doi.org/10.1111/j.1558-5646.2010.01108.x
Willi, Y., Van Buskirk, J., and Hoffmann, A.A., Limits to the adaptive potential of small populations, Annu. Rev. Ecol. Evol. Syst., 2006, vol. 37, pp. 433−458. https://doi.org/10.1146/annurev.ecolsys.37.091305.110145
Bensaid, A., Young, J.R., Kaushal, A., and Teale, A.J., Pulsed-field gel electrophoresis and its application in the physical analysis of the bovine MHC, Gene Mapping Techniques 122 and Applications, McLaren, Ed., New York: Marcel Dekker, 1991, p. 127.
Fries, R., Aggen, A., and Womack, J.E., The bovine genome map, Mamm. Genome, 1993, vol. 4, pp. 405—428.
Behl, J.D., Verma, N.K., Tyagi, N., et al., The major histocompatibility complex in Bovines: a review, ISRN Vet. Sci., 2012, рр. 1–12. https://doi.org/10.5402/2012/872710
Paracha, H., Hussain, T., Tahir, M.Z., et al., Multifunctional DRB3, a MHC class II gene, as a useful biomarker in small ruminants: a review, J. Inf. Mol. Biol., 2015, vol. 3, no. 1, pp. 19—23. https://doi.org/10.14737/journal.jimb/2015/3.1.19.23
Subramani, K.V., Sankar, M., Raghunatha, R.R., et al., Association of genetic resistance to gastrointestinal nematodes and the polymorphism at CAHI-DQA1 exon 2, Int. J. Sci. Environ. Technol., 2016, vol. 5, no. 2, pp. 678—687.
Tarasyan, K.K., Sorokin, P.A., Kholodova, M.V., and Rozhnov, V.V., Major histocompatibility complex (MHC) in mammals and its importance for studies of rare species (with Felidae family as an example), Zh. Obshch. Biol., 2014, vol. 75, no. 4, pp. 302—314.
Kumar, S., Sangwan, M.L., Ahlawat, S., and Barwar, A., Polymorphism in DRB3 exon 2 by PCR-RFLP and its association with mastitis in Murrah baffaloes, Ind. J. Biotech., 2011, vol. 10, pp. 232—234.
Sommer, S., The importance of immune gene variability (MHC) in evolutionary ecology and conservation, Front. Zool., 2005, vol. 2, no. 16, pp. 1—18. https://doi.org/10.1186/1742-9994-2-16
Neronov, V.M., Karimova, T.Yu., and Lushchekina, A.A., Ecosystem approach and GAP analysis of the saiga population state in the North-West Pre-Caspian Region, Astrakh. Vestn. Ekol. Obraz., 2011, no. 2(18), pp. 151−157.
Neronov, V.M., Arylova, N.Yu., Dubinin, M.Yu., et al., Current state and prospects of preserving saiga antelope in Northwest Pre-Caspian region, Arid. Ecosyst., 2013, vol. 3, no. 2, pp. 57−64. https://doi.org/10.1134/S2079096113020078
Neronov, V.M., Lushchekina, A.A., Karimova, T.Y., and Arylova, N.Y., Population dynamics of a key steppe species in a changing world: the critically endangered saiga antelope, Eurasian Steppes: Ecological Problems and Livelihoods in a Changing World in Plant and Vegetation, no. 6, Werger M.J.A. and van Staalduinen M.A., Eds., Dordrecht: Springer-Verlag, 2012, chapter 12, pp. 335—357. https://doi.org/10.1007/978-94-007-3886-7_12
Soulé, M.E., Threshold for survival: maintaining fitness and evolutionary potential, in Conservation Biology: An Evolutionary-Ecologial Perspective, Soulé, M.E. and Wilcox, B.A., Eds., Sunderland: Sinauer, 1980, pp. 151—169.
Lynch, M. and Lande, R., The critical effective size for a genetically secure population, Anim. Conserv., 1998, vol. 1, pp. 70—72. https://doi.org/10.1111/j.1469-1795.1998.tb00229.x
Frankham, R., Bradshaw, C.J., and Brook, B.W., Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses, Biol. Conserv., 2014, vol. 170, pp. 56—63. https://doi.org/10.1016/j.biocon.2013.12.036
Frankham, R., Bradshaw, C.J., and Brook, B.W., 50/500 rules need upward revision to 100/1000—response to Franklin et al., Biol. Conserv., 2014, vol. 176, p. 286. https://doi.org/10.1016/j.biocon.2014.05.006
Bannikov, A.G., Zhirnov, L.V., Lebedeva, L.S., and Fandeev, A.A., Biologiya saigaka (Biology of Saiga Antelope), Moscow: Izd. S-kh. Lit., Zh., Plakatov, 1961.
Baryshnikov, G.F., Dmitrieva, E.L., Krakhmal’naya, T.V., and Sher, A.V., The origin, evolution, and systematics of saiga antelope, in Saigak: filogeniya, sistematika, ekologiya, okhrana i ispol’zovanie (Saiga Antelope: Phylogeny, Systematics, Ecology, Conservation, and Use), Sokolov, V.E. and Zhirnov, L.V., Eds., Moscow, 1998, pp. 9−20.
Campos, P.F., Kristensen, T., Orlando, L., et al., Ancient DNA sequences point to a large loss of mitochondrial genetic diversity in the saiga antelope (Saiga tatarica) since the Pleistocene, Mol. Ecol., 2010, vol. 19, no. 22, pp. 4863—4875. https://doi.org/10.1111/j.1365-294X.2010.04826.x
Baitursinov, K.K., Saiga antelope helminths in Kazakhstan, Vestn. Pedagog. Gos. Univ. im. S. Toraigyrova, Ser. Khim.—Biol., 2005, no. 2, pp. 67—81.
Baitursinov, K.K., Brief data on the biology and helminth infestation of saiga antelope (Saiga tatarica L., 1766) in Kazakhstan, Vestn. Kaz. Natl. Univ., Ser. Biol., 2009, no. 3(42), pp. 83—87.
Petrov, V.S., Saiga antelope helminths and their significance in epizootology by sheep worms, Extended Abstract of Cand. Sci. Dissertation, Moscow: Vsesoyuz. Inst. Gig. Sanit., 1985.
Grachev, Yu.A. and Bekenov, A.B., Mass death of saiga antelopes—about 12 thousand deaths, Saiga News, 2010, no. 11, pp. 2—3.
Sigurdardottir, S., Borsch, C., Gustafsson, K., and Andersson, L., Cloning and sequence analysis of 14 DBR alleles of the bovine major histocompatibility complex using the polymerase chain reaction, Anim. Genet., 1991, vol. 22, pp. 199—209.
Mikko, S., Roed, K., Schmutz, S., and Andersson, L., Monomorphism and polymorphism at MHC DRB loci in domestic and wild ruminants, Immunol. Rev., 1999, vol. 167, pp. 169—178. https://doi.org/10.1111/j.1600-065X.1999.tb01390.x
Kennedy, L.J., Modrell, A., Groves, P., et al., Genetic diversity of the major histocompatibility complex class II in Alaskan caribou herds, Int. J. Immunogenet., 2010, vol. 38, pp. 109—119. https://doi.org/10.1111/j.1744-313X.2010.00973.x
Taylor, S.S., Jenkins, D.A., and Arcese, P., Loss of MHC and neutral variation in Peary caribou: genetic drift is not mitigated by balancing selection or exacerbated by MHC allele distributions, PLoS One, 2012, vol. 7, no. 5, pp. 1—11. https://doi.org/10.1371/journal.pone.0036748
Villesen, P., FaBox: an online toolbox for fasta sequences, Mol. Ecol. Notes, 2007, vol. 7, no. 6, pp. 965—968. https://doi.org/10.1111/j.1471-8286.2007.01821.x
Excoffier, L. and Lischer, H.E.L., Arlequin Suite ver. 3.5: a new series of programs to perform population genetics analyses under Linux and Windows, Mol. Ecol. Resour., 2010, vol. 10, pp. 564—567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Tamura, K., Stecher, G., Peterson, D., et al., MEGA6: molecular evolutionary genetics analysis version 6.0, Mol. Biol. Evol., 2013, vol. 30, pp. 2725—2729. https://doi.org/10.1093/molbev/mst197
Bandelt, H.J., Forster, P., and Rohl, A., Median-joining networks for inferring intraspecific phylogenies, Mol. Biol. Evol., 1999, vol. 16, no. 1, pp. 37—48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Doherty, P.C. and Zinkernagel, R.M., A biological role for the major histocompatibility antigens, Lancet, 1975, vol. 1, no. 7922, pp. 1406—1409.
Takahata, N. and Nei, M., Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci, Genetics, 1990, vol. 124, no. 4, pp. 967—978.
Wakeland, E.K., Boehme, S., She, J.X., et al., Ancestral polymorphisms of MHC class II genes: divergent allele advantage, Immunol. Res., 1990, vol. 9, no. 2, pp. 115—122. https://doi.org/10.1007/BF02918202
Barmann, E.V., Rossner, G.E., and Worheide, G., A revised phylogeny of Antilopini (Bovidae, Artiodactyla) using combined mitochondrial and nuclear genes, Mol. Phylogenet. Evol., 2013, vol. 67, pp. 484−493. https://doi.org/10.1016/j.ympev.2013.02.015
Khademi, T.G., Evaluation of phylogenetic relationships of Antilopini and Oreotragini tribes (Bovidae: Artiodactyla) based on complete mitochondrial genomes, J. Wildlife Biodiv., 2017, vol. 1, no. 1, pp. 1—11. https://doi.org/10.22120/JWB.2017
Bekenov, A.B., Pole, S.B., Pole, S.B., et al., Saiga death from diseases and parasitic invasions, in Saigak: filogeniya, sistematika, ekologiya, okhrana i ispol’zovanie (Saiga: Phylogeny, Systematics, Ecology, Conservation, and Use), Sokolov, V.E. and Zhirnov, L.V., Eds., Moscow, 1998, pp. 247—251.
ACKNOWLEDGMENTS
We thank A.V. Davydov for assistance in organizing the sample collection; N.V. Koroban, an expert in the products of Roche Diagnostics Russia; and A.V. Kudryavtseva, head of the Center of Collective Use “Genome” of the Institute of Molecular Biology (Russian Academy of Sciences), for their help in performing the sequencing, as well as G.A. Bazykin, head of the sector of molecular evolution of Institute for Information Transmission Problems (Russian Academy of Sciences), for consultations on data processing.
This work was supported by the Russian Foundation for Basic Research, project no. 17-04-01351.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interests. The authors declare that they have no conflict of interest.
Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Additional information
Translated by A. Lisenkova
Rights and permissions
About this article
Cite this article
Tarasyan, K.K., Sorokin, P.A., Kashinina, N.V. et al. High Allelic Diversity of the DRB3 Gene (MHC Class II) in Saiga (Saiga tatarica) L., 1766), Obtained by Next Generation Sequencing Method. Russ J Genet 55, 212–219 (2019). https://doi.org/10.1134/S1022795419020133
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1022795419020133