Functional immune diversity in reindeer reveals a high Arctic population at risk

Lukacs, Morten; Nymo, Ingebjørg H.; Madslien, Knut; Våge, Jørn; Veiberg, Vebjørn; Rolandsen, Christer Moe; Bøe, Cathrine Arnason; Sundaram, Arvind Y. M.; Grimholt, Unni

doi:10.3389/fevo.2022.1058674

Cited by 4Genetic diversity and population structureGenetic and phenotypic traits in livestockEvolution and Genetic Dynamics

Functional immune diversity in reindeer reveals a high Arctic population at risk

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Lukacs, Morten, Nymo, Ingebjørg H., Madslien, Knut, Våge, Jørn, Veiberg, Vebjørn, Rolandsen, Christer Moe, Bøe, Cathrine Arnason, Sundaram, Arvind Y. M. +1 more·2023·Frontiers in Ecology and Evolution

DOI 10.3389/fevo.2022.1058674

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Abstract

Climate changes the geographic range of both species as well as pathogens, causing a potential increase in the vulnerability of populations or species with limited genetic diversity. With advances in high throughput sequencing (HTS) technologies, we can now define functional expressed genetic diversity of wild species at a larger scale and identify populations at risk. Previous studies have used genomic DNA to define major histocompatibility complex (MHC) class II diversity in reindeer. Varying numbers of expressed genes found in many ungulates strongly argues for using cDNA in MHC typing strategies to ensure that diversity estimates relate to functional genes. We have used available reindeer genomes to identify candidate genes and established an HTS approach to define expressed MHC class I and class II diversity. To capture a broad diversity we included samples from wild reindeer from Southern Norway, semi-domesticated reindeer from Northern Norway and reindeer from the high Artic archipelago Svalbard. Our data show a medium MHC diversity in semi-domesticated and wild Norwegian mainland reindeer, and low MHC diversity reindeer in Svalbard reindeer. The low immune diversity in Svalbard reindeer provides a potential risk if the pathogenic pressure changes in response to altered environmental conditions due to climate change, or increased human-related activity.

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The diversity of the muskox MHC appears similar to the level reported for reindeer in selective regions that could be compared.
“Although an extensive direct gene-to-gene comparison could not be made, at least qualitatively in selective regions that could be compared, the diversity of the muskox MHC appears to be similar to the level reported for the reindeer, another Arctic ruminant under threat138.”
From Chromosomal-level reference genome assembly of muskox (Ovibos moschatus) from Banks Island in the Canadian Arctic, a resource for conservation genomics (2024) · cites this paper as [138]

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MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms
Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018) · Molecular Biology and Evolution · doi:10.1093/molbev/msy096 · Cited by 37,683 · see citing works
Clustal W and Clustal X version 2.0
Larkin, M., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., López, R., et al. (2007) · Bioinformatics · doi:10.1093/bioinformatics/btm404 · Cited by 28,221 · see citing works
FLASH: fast length adjustment of short reads to improve genome assemblies
Magoč, T., & Salzberg, S. L. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr507 · Cited by 15,366 · see citing works
Jalview Version 2—a multiple sequence alignment editor and analysis workbench
Waterhouse, A. M., Procter, J. B., Martin, D. M. A., Clamp, M. E., & Barton, G. J. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp033 · Cited by 10,011 · see citing works
The rapid generation of mutation data matrices from protein sequences
Jones, D. T., Taylor, W. R., & Thornton, J. M. (1992) · Computer applications in the biosciences · doi:10.1093/bioinformatics/8.3.275 · Cited by 6,916 · see citing works
Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases.
Tamura, K. (1992) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040752 · Cited by 2,167 · see citing works
Mammal Species of the World
Wilson, D. E. (2005) · Johns Hopkins University Press eBooks · doi:10.56021/9780801882210 · Cited by 1,880 · see citing works
High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco
Mousadik, A. E., & Petit, R. J. (1996) · Theoretical and Applied Genetics · doi:10.1007/bf00221895 · Cited by 1,539 · see citing works
Automatic annotation of eukaryotic genes, pseudogenes and promoters
Solovyev, V. V., Kosarev, P., Seledsov, I., & Vorobyev, D. (2006) · Genome biology · doi:10.1186/gb-2006-7-s1-s10 · Cited by 923 · see citing works
The genome sequence of Atlantic cod reveals a unique immune system
Star, B., Nederbragt, A. J., Jentoft, S., Grimholt, U., Malmstrøm, M., Gregers, T. F., Rounge, T. B., Paulsen, J., Solbakken, M. H., Sharma, A., et al. (2011) · Nature · doi:10.1038/nature10342 · Cited by 803 · see citing works
Self-citation
The HLA genomic loci map: expression, interaction, diversity and disease
Shiina, T., Hosomichi, K., Inoko, H., & Kulski, J. K. (2009) · Journal of Human Genetics · doi:10.1038/jhg.2008.5 · Cited by 788 · see citing works
P op G en R eport : simplifying basic population genetic analyses in R
Adamack, A. T., & Gruber, B. (2014) · Methods in Ecology and Evolution · doi:10.1111/2041-210x.12158 · Cited by 643 · see citing works
Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population ( Ovis aries L. )
Paterson, S., Wilson, K. L., & Pemberton, J. M. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.7.3714 · Cited by 481 · see citing works
The inflated significance of neutral genetic diversity in conservation genetics
Teixeira, J. C., & Huber, C. D. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2015096118 · Cited by 474 · see citing works
Conservation of caribou (Rangifer tarandus) in Canada: an uncertain future1This review is part of the virtual symposium “Flagship Species – Flagship Problems” that deals with ecology, biodiversity and management issues, and climate impacts on species at risk and of Canadian importance, including the polar bear (Ursus maritimus), Atlantic cod (Gadus morhua), Piping Plover (Charadrius melodus), and caribou (Rangifer tarandus).
Festa-Bianchet, M., Ray, J. C., Boutin, S., Côté, S. D., & Gunn, A. (2011) · Canadian Journal of Zoology · doi:10.1139/z11-025 · Cited by 426 · see citing works
Life and times of the Bering land bridge
Elias, S. A., Short, S. K., Nelson, C., & Birks, H. H. (1996) · Nature · doi:10.1038/382060a0 · Cited by 345 · see citing works
HIV and HLA Class I: An Evolving Relationship
Goulder, P., & Walker, B. D. (2012) · Immunity · doi:10.1016/j.immuni.2012.09.005 · Cited by 325 · see citing works
MHC polymorphism and disease resistance in Atlantic salmon (Salmo salar); facing pathogens with single expressed major histocompatibility class�I and class�II loci
Grimholt, U., Larsen, S., Nordmo, R., Midtlyng, P. J., Kjøglum, S., Storset, A., Saeb�, S., & Stet, R. J. M. (2003) · Immunogenetics · doi:10.1007/s00251-003-0567-8 · Cited by 319 · see citing works
Self-citation
Association between major histocompatibility complex class IIB alleles and resistance toAeromonas salmonicidain Atlantic salmon
Langefors, Å., Lohm, J., Grahn, M., Andersen, Ø., & von Schantz, T. (2001) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2000.1378 · Cited by 273 · see citing works
Comparative genomic analysis of the MHC: the evolution of class I duplication blocks, diversity and complexity from shark to man
Kulski, J. K., Shiina, T., Anzai, T., Kohara, S., & Inoko, H. (2002) · Immunological Reviews · doi:10.1034/j.1600-065x.2002.19008.x · Cited by 240 · see citing works
Human MHC architecture and evolution: implications for disease association studies
Traherne, J. A. (2008) · International Journal of Immunogenetics · doi:10.1111/j.1744-313x.2008.00765.x · Cited by 232 · see citing works
Genetic diversity in caribou linked to past and future climate change
Yannic, G., Pellissier, L., Ortego, J., Lecomte, N., Couturier, S., Cuyler, C., Dussault, C., Hundertmark, K. J., Irvine, R. J., Jenkins, D. A., et al. (2013) · Nature Climate Change · doi:10.1038/nclimate2074 · Cited by 192 · see citing works
Genetic Mapping of Quantitative Trait Loci Affecting Susceptibility to Marek's Disease Virus Induced Tumors in F2 Intercross Chickens
Vallejo, R. L., Bacon, L. D., Liu, H., Witter, R. L., Groenen, M. A. M., Hillel, J., & Cheng, H. H. (1998) · Genetics · doi:10.1093/genetics/148.1.349 · Cited by 187 · see citing works
Class II genes of the human major histocompatibility complex. Organization and evolutionary relationship of the DR beta genes.
Andersson, G., Larhammar, D., Widmark, E., Servenius, B., Peterson, P. A., & Rask, L. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)47480-7 · Cited by 185 · see citing works
REFUGIAL ORIGINS OF REINDEER (RANGIFER TARANDUS L.) INFERRED FROM MITOCHONDRIAL DNA SEQUENCES
Flagstad, Ø., & Røed, K. H. (2003) · Evolution · doi:10.1111/j.0014-3820.2003.tb01557.x · Cited by 175 · see citing works
Climate and environmental change drives Ixodes ricinus geographical expansion at the northern range margin
Jore, S., Vanwambeke, S., Viljugrein, H., Isaksen, K., Kristoffersen, A. B., Woldehiwet, Z., Johansen, B. E., Brun, E., Brun‐Hansen, H., Westermann, S., et al. (2014) · Parasites & Vectors · doi:10.1186/1756-3305-7-11 · Cited by 154 · see citing works
The critically endangered vaquita is not doomed to extinction by inbreeding depression
Robinson, J. A., Kyriazis, C. C., Nigenda‐Morales, S. F., Beichman, A. C., Rojas‐Bracho, L., Robertson, K. M., Fontaine, M. C., Wayne, R. K., Lohmueller, K. E., Taylor, B. L., et al. (2022) · Science · doi:10.1126/science.abm1742 · Cited by 150 · see citing works
The Major Histocompatibility Complex in Bovines: A Review
Behl, J. D., Verma, N. K., Tyagi, N., Mishra, P. P., Behl, R., & Joshi, B. K. (2012) · ISRN Veterinary Science · doi:10.5402/2012/872710 · Cited by 147 · see citing works
Post-glacial flooding of the Bering Land Bridge dated to 11 cal ka BP based on new geophysical and sediment records
Jakobsson, M., Pearce, C., Cronin, T. M., Backman, J., Anderson, L. G., Barrientos, N., Björk, G., Coxall, H. K., Boer, A. M. D., Mayer, L. A., et al. (2017) · Climate of the past · doi:10.5194/cp-13-991-2017 · Cited by 141 · see citing works
A novel ultra high-throughput 16S rRNA gene amplicon sequencing library preparation method for the Illumina HiSeq platform
de Muinck, E. J., Trosvik, P., Gilfillan, G. D., Hov, J. R., & Sundaram, A. Y. M. (2017) · Microbiome · doi:10.1186/s40168-017-0279-1 · Cited by 141 · see citing works
Self-citation
Expression levels of MHC class I molecules are inversely correlated with promiscuity of peptide binding
Chappell, P. E., Meziane, E. K., Harrison, M., Magiera, Ł., Hermann, C., Mears, L., Wrobel, A. G., Durant, C., Nielsen, L. L., Buus, S., et al. (2015) · eLife · doi:10.7554/elife.05345 · Cited by 140 · see citing works
Mosquitoes and Culicoides biting midges: vector range and the influence of climate change
Elbers, A. R. W., Koenraadt, C. J. M., & Meiswinkel, R. (2015) · Scientific and Technical Review (World Organisation for Animal Health) · doi:10.20506/rst.34.1.2349 · Cited by 136 · see citing works
Structure, function and disease susceptibility of the bovine major histocompatibility complex
Takeshima, S., & Aida, Y. (2006) · Animal Science Journal · doi:10.1111/j.1740-0929.2006.00332.x · Cited by 132 · see citing works
Generalists and Specialists: A New View of How MHC Class I Molecules Fight Infectious Pathogens
Kaufman, J. (2018) · Trends in Immunology · doi:10.1016/j.it.2018.01.001 · Cited by 130 · see citing works
Cloning and sequence analysis of 14 DRB alleles of the bovine major histocompatibility complex by using the polymerase chain reaction
SIGURDARDÓTTIR, S., Borsch, C., Gustafsson, K. T., & Andersson, L. (1991) · Animal Genetics · doi:10.1111/j.1365-2052.1991.tb00670.x · Cited by 124 · see citing works
Monomorphism and polymorphism at Mhc DRB loci in domestic and wild ruminants
Mikko, S., Røed, K., Schmutz, S., & Andersson, L. (1999) · Immunological Reviews · doi:10.1111/j.1600-065x.1999.tb01390.x · Cited by 116 · see citing works
Biology of the chicken MHC (B complex).
Plachý, J., Pink, J. R. L., & Hala, K. (1992) · PubMed · Cited by 107 · see citing works
The major histocompatibility complex and human evolution
Klein, J., Gutknecht, J., & Fischer, N. (1990) · Trends in Genetics · doi:10.1016/0168-9525(90)90042-5 · Cited by 74 · see citing works
Emergence of tick-borne diseases at northern latitudes in Europe: a comparative approach
Mysterud, A., Jore, S., Østerås, O., & Viljugrein, H. (2017) · Scientific Reports · doi:10.1038/s41598-017-15742-6 · Cited by 74 · see citing works
Pathogen diversity drives the evolution of generalist MHC-II alleles in human populations
Manczinger, M., Boross, G., Kemény, L., Müller, V., Lenz, T., Papp, B., & Pál, C. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000131 · Cited by 74 · see citing works
Identifying climate-sensitive infectious diseases in animals and humans in Northern regions
Omazic, A., Bylund, H., Boqvist, S., Högberg, A., Björkman, C., Tryland, M., Evengård, B., Koch, A., Berggren, C., Malogolovkin, A. S., et al. (2019) · Acta veterinaria Scandinavica · doi:10.1186/s13028-019-0490-0 · Cited by 70 · see citing works
Range dynamics of the reindeer in Europe during the last 25,000 years
Sommer, R. S., Kalbe, J., Ekström, J., Benecke, N., & Liljegren, R. (2013) · Journal of Biogeography · doi:10.1111/jbi.12193 · Cited by 69 · see citing works
Vectors and transmission dynamics for Setaria tundra (Filarioidea; Onchocercidae), a parasite of reindeer in Finland
Laaksonen, S., Solismaa, M., Kortet, R., Kuusela, J., & Oksanen, A. (2009) · Parasites & Vectors · doi:10.1186/1756-3305-2-3 · Cited by 64 · see citing works
Ancient DNA reveals prehistoric habitat fragmentation and recent domestic introgression into native wild reindeer
Røed, K. H., Bjørnstad, G., Flagstad, Ø., Haanes, H., Hufthammer, A. K., Jordhøy, P., & Rosvold, J. (2014) · Conservation Genetics · doi:10.1007/s10592-014-0606-z · Cited by 58 · see citing works
Capturing Differential Allele-Level Expression and Genotypes of All Classical HLA Loci and Haplotypes by a New Capture RNA-Seq Method
Yamamoto, F. F., Suzuki, S., Mizutani, A., Shigenari, A., Ito, S., Kametani, Y., Kato, S., Fernández-Viña, M., Murata, M., Morishima, S., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00941 · Cited by 52 · see citing works
A century of conservation: The ongoing recovery of Svalbard reindeer
Moullec, M. L., Pedersen, Å. Ø., Stien, A., Rosvold, J., & Hansen, B. B. (2019) · Journal of Wildlife Management · doi:10.1002/jwmg.21761 · Cited by 51 · see citing works
Quantitative analysis of the expression of the HLA-DRB genes at the transcriptional level by competitive polymerase chain reaction
Vincent, R., Louis, P., Gongora, C., Papa, I., Clot, J., & Eliaou, J. (1996) · The Journal of Immunology · doi:10.4049/jimmunol.156.2.603 · Cited by 48 · see citing works
Colonizing the world in spite of reduced MHC variation
Gangoso, L., Alcaide, M., Grande, J. M., MUÑOZ, J., Talbot, S. L., Sonsthagen, S. A., Sage, G. K., & Figuerola, J. (2012) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2012.02529.x · Cited by 47 · see citing works
IPD-MHC: nomenclature requirements for the non-human major histocompatibility complex in the next-generation sequencing era
Maccari, G., Robinson, J., Bontrop, R. E., Otting, Ń., de Groot, N. G., Ho, C., Ballingall, K. T., Marsh, S. G. E., & Hammond, J. A. (2018) · Immunogenetics · doi:10.1007/s00251-018-1072-4 · Cited by 45 · see citing works
The Effect of Specific MHC Class I and Class II Combinations on Resistance to Furunculosis in Atlantic Salmon (Salmo salar)
Kjøglum, S., Larsen, S., Bakke, H. G., & Grimholt, U. (2007) · Scandinavian Journal of Immunology · doi:10.1111/j.1365-3083.2007.02052.x · Cited by 44 · see citing works
Self-citation
Past Vegetation and Reindeer on Edgeoya (Spitsbergen) Between c. 7900 and c. 3800 BP, Studied by Means of Peat Layers and Reindeer Faecal Pellets
van der Knaap, W. O. (1989) · Journal of Biogeography · doi:10.2307/2845229 · Cited by 43 · see citing works
From wild to domestic reindeer – Genetic evidence of a non-native origin of reindeer pastoralism in northern Fennoscandia
Røed, K. H., Bjørklund, I., & Olsen, B. J. (2018) · Journal of Archaeological Science Reports · doi:10.1016/j.jasrep.2018.02.048 · Cited by 40 · see citing works
Infectious Disease Outbreak Associated With Supplementary Feeding of Semi-domesticated Reindeer
Tryland, M., Nymo, I. H., Romano, J. S., Mørk, T., Klein, J., & Rockström, U. (2019) · Frontiers in Veterinary Science · doi:10.3389/fvets.2019.00126 · Cited by 39 · see citing works
Self-citation
Diversity associated with the second expressed H L A - D R B locus in the human population
Robbins, F., Hurley, C. K., Tang, T. F., Yao, H., Lin, Y.-S., Wade, J. A., Goeken, N. E., & Hartzman, R. J. (1997) · Immunogenetics · doi:10.1007/s002510050248 · Cited by 36 · see citing works
Evolution of HLA-DRB Genes
Doxiadis, G. G. M., Hoof, I., de Groot, N., & Bontrop, R. E. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss186 · Cited by 36 · see citing works
West Nile Virus Infection in Reindeer ( Rangifer Tarandus )
Palmer, M. V., Stoffregen, W. C., Rogers, D. G., Hamir, A. N., Richt, J. A., Pedersen, D. D., & Waters, W. R. (2004) · Journal of Veterinary Diagnostic Investigation · doi:10.1177/104063870401600307 · Cited by 32 · see citing works
Genetic drift vs. natural selection in a long‐term small isolated population: major histocompatibility complex class II variation in the Gulf of California endemic porpoise (Phocoena sinus)
Munguía‐Vega, A., Garrigos, Y. E., Rojas‐Bracho, L., Vázquez‐Juárez, R., Castro-Prieto, A., & Flores-Ramírez, S. (2007) · Molecular Ecology · doi:10.1111/j.1365-294x.2007.03319.x · Cited by 32 · see citing works
Comparative MHC nomenclature: report from the ISAG/IUIS-VIC committee 2018
Ballingall, K. T., Bontrop, R. E., Ellis, S. A., Grimholt, U., Hammond, J. A., Ho, C., Kaufman, J., Kennedy, L. J., Maccari, G., Miller, D. C., et al. (2018) · Immunogenetics · doi:10.1007/s00251-018-1073-3 · Cited by 32 · see citing works
Self-citation
Valuing time: Tourism transitions in Svalbard
Saville, S. M. (2022) · Polar Record · doi:10.1017/s0032247422000055 · Cited by 31 · see citing works
Can management regulate the population size of wild reindeer (Rangifer tarandus) through harvest?
Strand, O., Nilsen, E. B., Solberg, E. J., & Linnell, J. D. C. (2012) · Canadian Journal of Zoology · doi:10.1139/z11-123 · Cited by 30 · see citing works
Sea ice loss increases genetic isolation in a high Arctic ungulate metapopulation
Peeters, B., Moullec, M. L., Raeymaekers, J. A. M., Marquez, J., Røed, K. H., Pedersen, Å. Ø., Veiberg, V., Loe, L. E., & Hansen, B. B. (2019) · Global Change Biology · doi:10.1111/gcb.14965 · Cited by 30 · see citing works
Self-citation
Positive selection and climatic effects on MHC class II gene diversity in hares (Lepus capensis) from a steep ecological gradient
Awadi, A., Slimen, H. B., Smith, S., Knauer, F., Makni, M., & Suchentrunk, F. (2018) · Scientific Reports · doi:10.1038/s41598-018-29657-3 · Cited by 29 · see citing works
Loss of Mhc and Neutral Variation in Peary Caribou: Genetic Drift Is Not Mitigated by Balancing Selection or Exacerbated by Mhc Allele Distributions
Taylor, S. S., Jenkins, D. A., & Arcese, P. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036748 · Cited by 28 · see citing works
Very high MHC Class IIB diversity without spatial differentiation in the mediterranean population of greater Flamingos
Gillingham, M. A. F., Béchet, A., Courtiol, A., Rendón‐Martos, M., Amat, J. A., Samraoui, B., Onmuş, O., Sommer, S., & Cézilly, F. (2017) · BMC Evolutionary Biology · doi:10.1186/s12862-017-0905-3 · Cited by 28 · see citing works
Identification of a New Bovine MHC Class II DRB Allele by Nucleotide Sequencing and an Analysis of Phylogenetic Relationships
Aida, Y., Niimi, M., Asahina, M., Okada, K., Nakai, Y., & OGIMOTO, K. (1995) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1995.1594 · Cited by 26 · see citing works
HLA RNA Sequencing With Unique Molecular Identifiers Reveals High Allele-Specific Variability in mRNA Expression
Johansson, T., Yohannes, D. A., Koskela, S., Partanen, J., & Saavalainen, P. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.629059 · Cited by 25 · see citing works
Copy number variations in BOLA‐DQA2 , BOLA‐DQB , and BOLA‐DQA5 show the genomic architecture and haplotype frequency of major histocompatibility complex class II genes in Holstein cows
Fukunaga, K., Yamashita, Y., & Yagisawa, T. (2020) · HLA · doi:10.1111/tan.14086 · Cited by 22 · see citing works
Can extreme MHC class I diversity be a feature of a wide geographic range? The example of Seba’s short-tailed bat (Carollia perspicillata)
Qurkhuli, T., Schwensow, N., Brändel, S. D., Tschapka, M., & Sommer, S. (2019) · Immunogenetics · doi:10.1007/s00251-019-01128-7 · Cited by 21 · see citing works
Recent large-scale landscape changes, genetic drift and reintroductions characterize the genetic structure of Norwegian wild reindeer
Kvie, K. S., Heggenes, J., Bårdsen, B., & Røed, K. H. (2019) · Conservation Genetics · doi:10.1007/s10592-019-01225-w · Cited by 20 · see citing works
A Multi-Pathogen Screening of Captive Reindeer (Rangifer tarandus) in Germany Based on Serological and Molecular Assays
Romano, J. S., Grund, L., Obiegala, A., Nymo, I. H., Ancin‐Murguzur, F. J., Li, H., Król, N., Pfeffer, M., & Tryland, M. (2019) · Frontiers in Veterinary Science · doi:10.3389/fvets.2019.00461 · Cited by 20 · see citing works
Self-citation
Genetic diversity of the major histocompatibility complex class II in Alaskan caribou herds
Kennedy, L. J., Modrell, A., Groves, P., Wei, Z., Single, R. M., & Happ, G. M. (2010) · International Journal of Immunogenetics · doi:10.1111/j.1744-313x.2010.00973.x · Cited by 19 · see citing works
Herding conditions related to infectious keratoconjunctivitis in semi-domesticated reindeer: a questionnaire-based survey among reindeer herders
Tryland, M., Stubsjøen, S. M., Ågren, E. O., Johansen, B. E., & Kielland, C. (2015) · Acta veterinaria Scandinavica · doi:10.1186/s13028-016-0203-x · Cited by 19 · see citing works
Population Differences at MHC Do Not Explain Enhanced Resistance of Song Sparrows to Local Parasites
Slade, J. W. G., Sarquis‐Adamson, Y., Gloor, G. B., Lachance, M., & MacDougall‐Shackleton, E. A. (2016) · Journal of Heredity · doi:10.1093/jhered/esw082 · Cited by 15 · see citing works
Highly‐contiguous bovine genomes underpin accurate functional analyses and updated nomenclature of MHC class I
Schwartz, J. C., Maccari, G., Heimeier, D., & Hammond, J. A. (2021) · HLA · doi:10.1111/tan.14494 · Cited by 15 · see citing works
A review of reindeer ( Rangifer tarandus tarandus ) disturbance research in Northern Europe: towards a social-ecological framework?
Gundersen, V., Myrvold, K. M., Kaltenborn, B. P., Strand, O., & Kofinas, G. P. (2022) · Landscape Research · doi:10.1080/01426397.2022.2078486 · Cited by 15 · see citing works
Structural and functional diversity arising from intra- and inter-haplotype combinations of duplicated DQA and B loci within the ovine MHC
Ballingall, K. T., Lantier, I., Todd, H., Lantier, F., & Rocchi, M. (2017) · Immunogenetics · doi:10.1007/s00251-017-1029-z · Cited by 14 · see citing works
Adult survival in migratory caribou is negatively associated with MHC functional diversity
Gagnon, M., Yannic, G., Boyer, F., & Côté, S. D. (2020) · Heredity · doi:10.1038/s41437-020-0347-3 · Cited by 11 · see citing works
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Self-citation
The relationship between quotas and harvest in the alpine reindeer population on Hardangervidda, Norway
Mysterud, A., Viljugrein, H., L'Abée‐Lund, J. H., Lund, S. E., Rolandsen, C. M., & Strand, O. (2021) · European Journal of Wildlife Research · doi:10.1007/s10344-021-01542-x · Cited by 9 · see citing works
Self-citation
Organization of the Addax Major Histocompatibility Complex Provides Insights Into Ruminant Evolution
Li, C., Huang, R., Nie, F., Li, J., Zhu, W., Shi, X., Guo, Y., Chen, Y., Wang, S., Zhang, L., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00260 · Cited by 7 · see citing works

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What’s cooking? The effect of temperature on the immune response
Old, J. M., & Dixon, B. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1701016 · Cited by 6 · see citing works
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“Although an extensive direct gene-to-gene comparison could not be made, at least qualitatively in selective regions that could be compared, the diversity of the muskox MHC appears to be similar to the level reported for the reindeer, another Arctic ruminant under threat 138 .”
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Feng, T., Wu, Y., Xu, Y., & Chen, W. (2026) · GigaScience · doi:10.1093/gigascience/giag016 · Cited by 1 · see citing works
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Konorov, E. A., Андреевич, К. К., Семина, М. Т., Воронкова, В. Н., Onokhov, A. A., & Layshev, K. A. (2025) · Russian Journal of Genetics · doi:10.1134/s1022795425700358

First assessment of MHC diversity in wild Scottish red deer populations
Pérez‐Espona, S., Goodall-Copestake, W. P., Savirina, A., Bobovikova, J., Molina-Rubio, C., & Pérez-Barbería, F. J. (2019) · European Journal of Wildlife Research · doi:10.1007/s10344-019-1254-x · Cited by 7 · see citing works
Low MHC DRB class II diversity in the mountain goat: past bottlenecks and possible role of pathogens and parasites
Mainguy, J., Worley, K., Côté, S. D., & Coltman, D. W. (2006) · Conservation Genetics · doi:10.1007/s10592-006-9243-5 · Cited by 53 · see citing works
The major histocompatibility complex of reindeer
Olsaker, I., & Røed, K. H. (1990) · Rangifer · doi:10.7557/2.10.3.881 · Cited by 7 · see citing works
(Lack of) Genetic Diversity in Immune Genes Predates Glacial Isolation in the North American Mountain Goat (Oreamnos americanus)
Shafer, A. B. A., Fan, C. W., Côté, S. D., & Coltman, D. W. (2012) · Journal of Heredity · doi:10.1093/jhered/esr138 · Cited by 21 · see citing works
Spatial variation and low diversity in the major histocompatibility complex in walrus (Odobenus rosmarus)
Sonsthagen, S. A., Fales, K., Jay, C. V., Sage, G. K., & Talbot, S. L. (2014) · Polar Biology · doi:10.1007/s00300-014-1450-9 · Cited by 11 · see citing works

Authors: Lukacs, M., Nymo, I. H., Madslien, K., Våge, J., Veiberg, V., Rolandsen, C. M., Bøe, C. A., Sundaram, A. Y. M., & Grimholt, U.
Affiliations: Norwegian Veterinary Institute (NO)
Norwegian Institute for Nature Research (NO)
Oslo University Hospital (NO)
Corresponding author: Grimholt, Unni
ORCID: Lukacs, Morten
Nymo, Ingebjørg H.
Madslien, Knut
Våge, Jørn
Veiberg, Vebjørn
Rolandsen, Christer Moe
Bøe, Cathrine Arnason
Sundaram, Arvind Y. M.
Grimholt, Unni
Venue: Frontiers in Ecology and Evolution
Publisher: Frontiers Media SA
Published: 2023-01-11
Volume: 10
ISSN: 2296-701X (ISSN-L)
DOI: 10.3389/fevo.2022.1058674
OpenAlex: W4315650963
Cited by: 4
References: 80
Citations by year: 2026: 1 · 2025: 2 · 2024: 1
FWCI: 0.66
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: Frontiers in Ecology and Evolution (publishedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
NORA - Norwegian Open Research Archives (submittedVersion, cc-by)
Funders: Environment Agency
the Research Council
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and phenotypic traits in livestock
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Keywords: reindeer, MHC diversity, major histocompatibility complex, Svalbard reindeer, semi-domesticated reindeer, wild reindeer, climate change, population vulnerability

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Functional immune diversity in reindeer reveals a high Arctic population at risk

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