Major Histocompatibility Complex (MHC) Markers in Conservation Biology
Open accessAbstract
Human impacts through habitat destruction, introduction of invasive species and climate change are increasing the number of species threatened with extinction. Decreases in population size simultaneously lead to reductions in genetic diversity, ultimately reducing the ability of populations to adapt to a changing environment. In this way, loss of genetic polymorphism is linked with extinction risk. Recent advances in sequencing technologies mean that obtaining measures of genetic diversity at functionally important genes is within reach for conservation programs. A key region of the genome that should be targeted for population genetic studies is the Major Histocompatibility Complex (MHC). MHC genes, found in all jawed vertebrates, are the most polymorphic genes in vertebrate genomes. They play key roles in immune function via immune-recognition and -surveillance and host-parasite interaction. Therefore, measuring levels of polymorphism at these genes can provide indirect measures of the immunological fitness of populations. The MHC has also been linked with mate-choice and pregnancy outcomes and has application for improving mating success in captive breeding programs. The recent discovery that genetic diversity at MHC genes may protect against the spread of contagious cancers provides an added impetus for managing and protecting MHC diversity in wild populations. Here we review the field and focus on the successful applications of MHC-typing for conservation management. We emphasize the importance of using MHC markers when planning and executing wildlife rescue and conservation programs but stress that this should not be done to the detriment of genome-wide diversity.
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Genetic diversity in the MHC impacts wildlife health and conservation.
“Genetic diversity in the MHC is believed to impact wildlife health and conservation128–131.”
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 [130]
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1 retracted
Retracted:MHC diversity and differential exposure to pathogens in kestrels (Aves:Falconidae)
Alcaide, M., Lemus, J. Á., Blanco, G., Tella, J. L., Serrano, D., Negro, J. J., Rodríguez, A., & García-Montijano, M. (2010) · Molecular Ecology · doi:10.1111/j.1365-294x.2009.04507.x · Cited by 61 · see citing works
RetractedNext-generation DNA sequencing
Shendure, J., & Ji, H. (2008) · Nature Biotechnology · doi:10.1038/nbt1486 · Cited by 4,509 · see citing works
Introduction to conservation genetics
Frankham, R., Ballou, J. D., & Briscoe, D. A. (2002) · Choice Reviews Online · doi:10.5860/choice.40-1529 · Cited by 3,521 · see citing works
Introduction to Conservation Genetics
Frankham, R., Ballou, J. D., Briscoe, D. A., & McInnes, K. H. (2002) · Cambridge University Press eBooks · doi:10.1017/cbo9780511808999 · Cited by 3,139 · see citing works
Genome sequence, comparative analysis and haplotype structure of the domestic dog
members, B. S. P., Lindblad-Toh, K., Wade, C. M., Mikkelsen, T. S., Karlsson, E. K., Jaffe, D. B., Kamal, M., Clamp, M., Chang, J. L., Kulbokas, E. J., et al. (2005) · Nature · doi:10.1038/nature04338 · Cited by 2,568 · see citing works
Frankham, R. (2005) · Biological Conservation · doi:10.1016/j.biocon.2005.05.002 · Cited by 2,414 · see citing works
Inbreeding and extinction in a butterfly metapopulation
Saccheri, I. J., Kuussaari, M., Kankare, M., Vikman, P., Fortelius, W., & Hanski, I. (1998) · Nature · doi:10.1038/33136 · Cited by 1,719 · see citing works
Relationship of Genetic Variation to Population Size in Wildlife
Frankham, R. (1996) · Conservation Biology · doi:10.1046/j.1523-1739.1996.10061500.x · Cited by 1,547 · see citing works
The power and promise of population genomics: from genotyping to genome typing
Luikart, G., England, P. R., Tallmon, D. A., Jordan, S., & Taberlet, P. (2003) · Nature Reviews Genetics · doi:10.1038/nrg1226 · Cited by 1,367 · see citing works
The sequence and de novo assembly of the giant panda genome
Li, R., Fan, W., Tian, G., Zhu, H., He, L., Cai, J., Huang, Q., Cai, Q., Li, B., Bai, Y., et al. (2010) · Nature · doi:10.1038/nature08696 · Cited by 1,180 · see citing works
PERSPECTIVE: HIGHLY VARIABLE LOCI AND THEIR INTERPRETATION IN EVOLUTION AND CONSERVATION
Hedrick, P. W. (1999) · Evolution · doi:10.1111/j.1558-5646.1999.tb03767.x · Cited by 1,144 · see citing works
Limits to the Adaptive Potential of Small Populations
Willi, Y., Buskirk, J. V., & Hoffmann, A. A. (2006) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev.ecolsys.37.091305.110145 · Cited by 987 · see citing works
MHC-dependent mate preferences in humans
Wedekind, C., Seebeck, T., Bettens, F., & Paepke, A. J. (1995) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1995.0087 · Cited by 957 · see citing works
The evolutionary ecology of the major histocompatibility complex
Piertney, S. B., & Oliver, M. K. (2005) · Heredity · doi:10.1038/sj.hdy.6800724 · Cited by 941 · see citing works
The importance of immune gene variability (MHC) in evolutionary ecology and conservation
Sommer, S. (2005) · Frontiers in Zoology · doi:10.1186/1742-9994-2-16 · Cited by 913 · see citing works
Edmands, S. (2006) · Molecular Ecology · doi:10.1111/j.1365-294x.2006.03148.x · Cited by 911 · see citing works
MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years?
Bernatchez, L., & Landry, C. R. (2003) · Journal of Evolutionary Biology · doi:10.1046/j.1420-9101.2003.00531.x · Cited by 894 · see citing works
Genetic Basis for Species Vulnerability in the Cheetah
O’Brien, S. J., Roelke, M. E., Marker, L. L., Newman, A., Winkler, C. A., Meltzer, D. G. A., Colly, L., Evermann, J. F., Bush, Μ., & Wildt, D. E. (1985) · Science · doi:10.1126/science.2983425 · Cited by 867 · see citing works
The alluring simplicity and complex reality of genetic rescue
TALLMON, D., LUIKART, G., & WAPLES, R. (2004) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2004.07.003 · Cited by 857 · see citing works
Adaptive population divergence: markers, QTL and traits
McKay, J., & Latta, R. G. (2002) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(02)02478-3 · Cited by 839 · see citing works
HOW CLOSELY CORRELATED ARE MOLECULAR AND QUANTITATIVE MEASURES OF GENETIC VARIATION? A META-ANALYSIS
Reed, D. H., & Frankham, R. (2001) · Evolution · doi:10.1111/j.0014-3820.2001.tb00629.x · Cited by 813 · see citing works
Tracking the Long-Term Decline and Recovery of an Isolated Population
Westemeier, R. L., Brawn, J. D., Simpson, S. A., Esker, T. L., Jansen, R. W., Walk, J. W., Kershner, E. L., Bouzat, J. L., & Paige, K. N. (1998) · Science · doi:10.1126/science.282.5394.1695 · Cited by 766 · see citing works
The Evolution of Mating Preferences and Major Histocompatibility Complex Genes
Penn, D. J., & Potts, W. K. (1999) · The American Naturalist · doi:10.1086/303166 · Cited by 754 · see citing works
Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex
Doherty, P. C., & Zinkernagel, R. M. (1975) · Nature · doi:10.1038/256050a0 · Cited by 749 · see citing works
How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings
Spurgin, L. G., & Richardson, D. S. (2010) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2009.2084 · Cited by 747 · see citing works
Role of MHC Gene Products in Immune Regulation
Benacerraf, B. (1981) · Science · doi:10.1126/science.6165083 · Cited by 701 · see citing works
Cytotoxic T cells recognize fragments of the influenza nucleoprotein
Townsend, A., Gotch, F. M., & Davey, J. F. (1985) · Cell · doi:10.1016/0092-8674(85)90103-5 · Cited by 671 · see citing works
Inbreeding and Extinction: A Threshold Effect
Frankham, R. (1995) · Conservation Biology · doi:10.1046/j.1523-1739.1995.09040792.x · Cited by 614 · see citing works
Restoration of an inbred adder population
Madsen, T. R. L., Shine, R., Olsson, M. M., & Wittzell, H. (1999) · Nature · doi:10.1038/46941 · Cited by 613 · see citing works
Inbreeding and Extinction: Island Populations
Frankham, R. (1998) · Conservation Biology · doi:10.1111/j.1523-1739.1998.96456.x · Cited by 612 · see citing works
Dausset, J. B. (2009) · Acta Haematologica · doi:10.1159/000205478 · Cited by 531 · see citing works
Interactive influence of infectious disease and genetic diversity in natural populations
O’Brien, S. J., & Evermann, J. F. (1988) · Trends in Ecology & Evolution · doi:10.1016/0169-5347(88)90058-4 · Cited by 527 · see citing works
The Scent of Genetic Compatibility: Sexual Selection and the Major Histocompatibility Complex
Penn, D. J. (2002) · Ethology · doi:10.1046/j.1439-0310.2002.00768.x · Cited by 503 · see citing works
Conservation genetics: where are we now?
Hedrick, P. W. (2001) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(01)02282-0 · Cited by 500 · see citing works
Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant
Vilà, C., Sundqvist, A., Flagstad, Ø., Seddon, J. M., rnerfeldt, S. B., Kojola, I., Casulli, A., Sand, H., Wabakken, P., & Ellegren, H. (2003) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2002.2184 · Cited by 499 · see citing works
A BIOLOGICAL ROLE FOR THE MAJOR HISTOCOMPATIBILITY ANTIGENS
Doherty, P. C., & Zinkernagel, R. M. (1975) · The Lancet · doi:10.1016/s0140-6736(75)92610-0 · Cited by 492 · see citing works
Clonal Origin and Evolution of a Transmissible Cancer
Murgia, C., Pritchard, J. K., Kim, S. Y., Fassati, A., & Weiss, R. A. (2006) · Cell · doi:10.1016/j.cell.2006.05.051 · Cited by 489 · see citing works
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
High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal
Aguilar, A., Roemer, G. W., Debenham, S. L., Binns, M. M., Garcelon, D. K., & Wayne, R. K. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0306582101 · Cited by 442 · see citing works
Mechanisms of MHC class I‐restricted antigen processing and cross‐presentation
Cresswell, P., Ackerman, A. L., Giodini, A., Peaper, D. R., & Wearsch, P. A. (2005) · Immunological Reviews · doi:10.1111/j.0105-2896.2005.00316.x · Cited by 435 · see citing works
Comparative genomics of major histocompatibility complexes
Kelley, J. M., Walter, L., & Trowsdale, J. (2004) · Immunogenetics · doi:10.1007/s00251-004-0717-7 · Cited by 429 · see citing works
Conservation genetics in transition to conservation genomics
Ouborg, N. J., Pertoldi, C., Loeschcke, V., Bijlsma, R., & Hedrick, P. W. (2010) · Trends in Genetics · doi:10.1016/j.tig.2010.01.001 · Cited by 409 · see citing works
A Quantitative-Genetic Perspective on Conservation Issues
Lynch, M. (1996) · Springer eBooks · doi:10.1007/978-1-4757-2504-9_15 · Cited by 404 · see citing works
Perspective: Highly Variable Loci and Their Interpretation in Evolution and Conservation
Hedrick, P. W. (1999) · Evolution · doi:10.2307/2640768 · Cited by 403 · see citing works
Mate choice decisions of stickleback females predictably modified by MHC peptide ligands
Milinski, M., Griffiths, S. W., Wegner, K. M., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408264102 · Cited by 396 · see citing works
Inbreeding and Extinction: Island Populations
Frankham, R. (1998) · Conservation Biology · doi:10.1046/j.1523-1739.1998.96456.x · Cited by 390 · see citing works
Parasite Selection for Immunogenetic Optimality
Wegner, K. M., Kalbe, M., Kurtz, J., et al. (2003) · Science · doi:10.1126/science.1088293 · Cited by 373 · see citing works
Slate, J., Kruuk, L. E. B., MARSHALL, T. C., Pemberton, J. M., & Clutton‐Brock, T. H. (2000) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2000.1192 · Cited by 341 · see citing works
INBREEDING AND ITS FITNESS EFFECTS IN AN INSULAR POPULATION OF SONG SPARROWS (MELOSPIZA MELODIA)
Keller, L. F. (1998) · Evolution · doi:10.1111/j.1558-5646.1998.tb05157.x · Cited by 339 · see citing works
Molecular Genetic Approaches in Conservation
(1996) · doi:10.1093/oso/9780195095265.001.0001 · Cited by 337 · see citing works
Do population size bottlenecks reduce evolutionary potential?
Frankham, R., Lees, K., Montgomery, M. E., England, P. R., Lowe, E. H., & Briscoe, D. A. (1999) · Animal Conservation · doi:10.1111/j.1469-1795.1999.tb00071.x · Cited by 332 · see citing works
Siddle, H. V. T., Kreiss, A., Eldridge, M. D. B., Noonan, E., Clarke, C. J., Pyecroft, S., Woods, G. M., & Belov, K. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704580104 · Cited by 299 · see citing works
Self-citationMajor histocompatibility complex and mate choice in sand lizards
Olsson, M. M., Madsen, T. R. L., Nordby, J., Wapstra, E., Újvári, B., & Wittsell, H. (2003) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rsbl.2003.0079 · Cited by 295 · see citing works
Genomics and conservation genetics
Kohn, M. H., Murphy, W. J., Ostrander, E. A., & Wayne, R. K. (2006) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2006.08.001 · Cited by 266 · see citing works
A role for molecular genetics in biological conservation.
O’Brien, S. J. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.13.5748 · Cited by 258 · see citing works
GASTRIC CANCER IN PATIENTS WHO HAVE TAKEN CIMETIDINE
Mullen, P. W., & Guslandi, M. (1979) · The Lancet · doi:10.1016/s0140-6736(79)92040-3 · Cited by 243 · see citing works
Inbreeding leads to extinction
Frankham, R., & Ralls, K. (1998) · Nature · doi:10.1038/33022 · Cited by 240 · see citing works
Is MHC enough for understanding wildlife immunogenetics?
Acevedo‐Whitehouse, K. A., & CUNNINGHAM, A. (2006) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2006.05.010 · Cited by 238 · see citing works
Inbreeding and Its Fitness Effects in an Insular Population of Song Sparrows (Melospiza melodia)
Keller, L. F. (1998) · Evolution · doi:10.2307/2410939 · Cited by 237 · see citing works
Inbreeding depression in an isolated population of adders Vipera berus
Madsen, T. R. L., Stille, B., & Shine, R. (1996) · Biological Conservation · doi:10.1016/0006-3207(95)00067-4 · Cited by 232 · see citing works
Gorer, P. A., Lyman, S., & Snell, G. D. (1948) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1948.0026 · Cited by 227 · see citing works
Miller, H. C., & Lambert, D. M. (2004) · Molecular Ecology · doi:10.1111/j.1365-294x.2004.02368.x · Cited by 203 · see citing works
Palo, J. U., O’Hara, R. B., Laugen, A. T., Laurila, A., Primmer, C. R., & Merilä, J. (2003) · Molecular Ecology · doi:10.1046/j.1365-294x.2003.01865.x · Cited by 200 · see citing works
Wildlife cancer: a conservation perspective
McAloose, D., & Newton, A. L. (2009) · Nature reviews. Cancer · doi:10.1038/nrc2665 · Cited by 200 · see citing works
Tasmanian devil facial tumour disease: lessons for conservation biology
McCallum, H. I. (2008) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2008.07.001 · Cited by 193 · see citing works
(1996) · Springer eBooks · doi:10.1007/978-1-4757-2504-9 · Cited by 192 · see citing works
Ellegren, H., Hartman, G. L., Johansson, M., & Andersson, L. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.17.8150 · Cited by 188 · see citing works
High‐resolution, high‐throughput HLA genotyping by next‐generation sequencing
Bentley, G., Higuchi, R., Hoglund, B. N., et al. (2009) · Tissue Antigens · doi:10.1111/j.1399-0039.2009.01345.x · Cited by 185 · see citing works
Bouzat, J. L., Johnson, J. A., Toepfer, J. E., et al. (2008) · Conservation Genetics · doi:10.1007/s10592-008-9547-8 · Cited by 180 · see citing works
MHC‐based mate choice combines good genes and maintenance of MHC polymorphism
Eizaguirre, C., Yeates, S. E., Lenz, T. L., et al. (2009) · Molecular Ecology · doi:10.1111/j.1365-294x.2009.04243.x · Cited by 179 · see citing works
Schwensow, N., Fietz, J., Dausmann, K. H., & Sommer, S. (2007) · Heredity · doi:10.1038/sj.hdy.6800993 · Cited by 173 · see citing works
The European Bioinformatics Institute
Griffin, H. G., & Griffin, A. M. (1995) · Molecular Biotechnology · doi:10.1007/bf02821337 · Cited by 172 · see citing works
Methods for MHC genotyping in non‐model vertebrates
Babik, W. (2009) · Molecular Ecology Resources · doi:10.1111/j.1755-0998.2009.02788.x · Cited by 167 · see citing works
MHC Polymorphism and the Design of Captive Breeding Programs
Hughes, A. L. (1991) · Conservation Biology · doi:10.1111/j.1523-1739.1991.tb00130.x · Cited by 161 · see citing works
New generation sequencers as a tool for genotyping of highly polymorphic multilocus MHC system
Babik, W., Taberlet, P., Ejsmond, M. J., et al. (2009) · Molecular Ecology Resources · doi:10.1111/j.1755-0998.2009.02622.x · Cited by 160 · see citing works
Lifetime reproductive success is maximized with optimal major histocompatibility complex diversity
Kalbe, M., Eizaguirre, C., Dankert, I., et al. (2008) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2008.1466 · Cited by 148 · see citing works
Froeschke, G., & Sommer, S. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi112 · Cited by 146 · see citing works
Kloch, A., Babik, W., Bajer, A., et al. (2010) · Molecular Ecology · doi:10.1111/j.1365-294x.2009.04476.x · Cited by 143 · see citing works
Potts, W. K., Manning, C. J., & Wakeland, E. K. (1994) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1994.0154 · Cited by 142 · see citing works
Siddle, H. V. T., Marzec, J. A., Cheng, Y., Jones, M. E., & Belov, K. (2010) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2009.2362 · Cited by 141 · see citing works
Self-citationSchad, J., Ganzhorn, J. U., & Sommer, S. (2005) · Evolution · doi:10.1111/j.0014-3820.2005.tb01002.x · Cited by 138 · see citing works
HLA sharing and spontaneous abortion in humans
Thomas, M. L., Harger, J. H., Wagener, D. K., et al. (1985) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(85)90379-5 · Cited by 134 · see citing works
Harf, R., & Sommer, S. (2004) · Molecular Ecology · doi:10.1111/j.1365-294x.2004.02402.x · Cited by 131 · see citing works
Captive breeding and the reintroduction of Mexican and red wolves
Hedrick, P. W., & Fredrickson, R. (2007) · Molecular Ecology · doi:10.1111/j.1365-294x.2007.03400.x · Cited by 130 · see citing works
Comparative genomics: lessons from cats
O’Brien, S. J., Wienberg, J., & Lyons, L. A. (1997) · Trends in Genetics · doi:10.1016/s0168-9525(97)01297-3 · Cited by 128 · see citing works
Zagalska‐Neubauer, M., Babik, W., Stuglik, M., Gustafsson, L., Cichoń, M., & Radwan, J. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-395 · Cited by 126 · see citing works
Snell, G. D. (1981) · Science · doi:10.1126/science.7017931 · Cited by 123 · see citing works
Low major histocompatibility complex class II diversity in European and North American moose.
Mikko, S., & Andersson, L. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.10.4259 · Cited by 121 · see citing works
Hansen, M. M., Skaala, Ø., Jensen, L. F., Bekkevold, D., & Mensberg, K. D. (2007) · Molecular Ecology · doi:10.1111/j.1365-294x.2007.03255.x · Cited by 113 · see citing works
Inbreeding and extinction: Effects of purging
Frankham, R., Gilligan, D. M., Morris, D. D., & Briscoe, D. A. (2001) · Conservation Genetics · doi:10.1023/a:1012299230482 · Cited by 111 · see citing works
Genetic diversity and differentiation at MHC genes in island populations of tuatara (Sphenodon spp.)
Miller, H. C., Allendorf, F. W., & Daugherty, C. H. (2010) · Molecular Ecology · doi:10.1111/j.1365-294x.2010.04771.x · Cited by 109 · see citing works
Toward Immunogenetic Studies of Amphibian Chytridiomycosis: Linking Innate and Acquired Immunity
Richmond, J. Q., Savage, A. E., Zamudio, K. R., & Rosenblum, E. B. (2009) · BioScience · doi:10.1525/bio.2009.59.4.9 · Cited by 109 · see citing works
Is the decline of desert bighorn sheep from infectious disease the result of low MHC variation?
Gutiérrez‐Espeleta, G. A., Hedrick, P. W., Kalinowski, S. T., et al. (2001) · Heredity · doi:10.1046/j.1365-2540.2001.00853.x · Cited by 107 · see citing works
Richardson, D. S., & Westerdahl, H. (2003) · Molecular Ecology · doi:10.1046/j.1365-294x.2003.02005.x · Cited by 103 · see citing works
Major histocompatibility complex (MHC) variation in the endangered Mexican wolf and related canids
Hedrick, P. W., Lee, R. N., & Parker, K. M. (2000) · Heredity · doi:10.1046/j.1365-2540.2000.00805.x · Cited by 101 · see citing works
Hedrick, P. W., Parker, K. M., & Lee, R. N. (2001) · Molecular Ecology · doi:10.1046/j.1365-294x.2001.01289.x · Cited by 100 · see citing works
Novel genes continue to enhance population growth in adders (Vipera berus)
Madsen, T. R. L., Újvári, B., & Olsson, M. M. (2004) · Biological Conservation · doi:10.1016/j.biocon.2004.01.022 · Cited by 99 · see citing works
MHC Variability of a Small Lemur in the Littoral Forest Fragments of Southeastern Madagascar
Schad, J., Sommer, S., & Ganzhorn, J. U. (2004) · Conservation Genetics · doi:10.1023/b:coge.0000031137.50239.d3 · Cited by 99 · see citing works
MHC class II genes in European wolves: a comparison with dogs
Seddon, J. M., & Ellegren, H. (2002) · Immunogenetics · doi:10.1007/s00251-002-0489-x · Cited by 96 · see citing works
Characterization, Polymorphism, and Evolution of MHC Class II B Genes in Birds of Prey
Alcaide, M., Edwards, S. V., & Negro, J. J. (2007) · Journal of Molecular Evolution · doi:10.1007/s00239-007-9033-9 · Cited by 95 · see citing works
Stuglik, M., Radwan, J., & Babik, W. (2011) · Molecular Ecology Resources · doi:10.1111/j.1755-0998.2011.02997.x · Cited by 91 · see citing works
Seddon, J. M., & Baverstock, P. R. (1999) · Molecular Ecology · doi:10.1046/j.1365-294x.1999.00822.x · Cited by 89 · see citing works
Major histocompatibility complex variation at three class II loci in the northern elephant seal
Weber, D. S., Stewart, B. S., Schienman, J. E., & Lehman, N. (2004) · Molecular Ecology · doi:10.1111/j.1365-294x.2004.02095.x · Cited by 88 · see citing works
The role of the Major Histocompatibility Complex in the spread of contagious cancers
Belov, K. (2010) · Mammalian Genome · doi:10.1007/s00335-010-9294-2 · Cited by 87 · see citing works
Self-citationMHC class I variation associates with parasite resistance and longevity in tropical pythons
Madsen, T. R. L., & Újvári, B. (2006) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2006.01158.x · Cited by 86 · see citing works
Vrijenhoek, R. C., & Leberg, P. L. (1991) · Conservation Biology · doi:10.1111/j.1523-1739.1991.tb00131.x · Cited by 84 · see citing works
Pfrender, M. E., Spitze, K., Hicks, J., et al. (2000) · Conservation Genetics · doi:10.1023/a:1011518125488 · Cited by 81 · see citing works
Population size and genetic diversity in sand lizards (Lacerta agilis) and adders (Vipera berus)
Madsen, T. R. L., Olsson, M. M., Wittzell, H., et al. (2000) · Biological Conservation · doi:10.1016/s0006-3207(99)00127-5 · Cited by 77 · see citing works
Low MHC variation in the endangered Galápagos penguin (Spheniscus mendiculus)
Bollmer, J. L., Vargas, F. H., & Parker, P. G. (2007) · Immunogenetics · doi:10.1007/s00251-007-0221-y · Cited by 76 · see citing works
Maternal-fetal interactions and the maintenance of HLA polymorphism.
Hedrick, P. W., & Thomson, G. (1988) · Genetics · doi:10.1093/genetics/119.1.205 · Cited by 74 · see citing works
Major Histocompatibility Complex Variation in the Endangered Przewalski’s Horse
Hedrick, P. W., Parker, K. M., Miller, E., et al. (1999) · Genetics · doi:10.1093/genetics/152.4.1701 · Cited by 72 · see citing works
MHC VARIATION IN THE ENDANGERED GILA TOPMINNOW
Hedrick, P. W., & Parker, K. M. (1998) · Evolution · doi:10.1111/j.1558-5646.1998.tb05152.x · Cited by 68 · see citing works
van Oosterhout, C., Smith, A. M., Hänfling, B., Ramnarine, I. W., Mohammed, R. S., & Cable, J. (2007) · Conservation Biology · doi:10.1111/j.1523-1739.2007.00809.x · Cited by 67 · see citing works
Gómez-Mestre, I., & Tejedo, M. (2004) · Evolution · doi:10.1111/j.0014-3820.2004.tb01608.x · Cited by 67 · see citing works
Újvári, B., Madsen, T. R. L., Kotenko, T., et al. (2002) · Biological Conservation · doi:10.1016/s0006-3207(01)00176-8 · Cited by 66 · see citing works
SMULDERS, M. J. M., Snoek, B. L., Booy, G., et al. (2003) · Conservation Genetics · doi:10.1023/a:1024767114707 · Cited by 64 · see citing works
Siddle, H. V. T., Sanderson, C., & Belov, K. (2007) · Immunogenetics · doi:10.1007/s00251-007-0238-2 · Cited by 63 · see citing works
Self-citationMHC diversity of endemic Malagasy rodents in relation to geographic range and social system
Sommer, S., Schwab, D., & Ganzhorn, J. U. (2002) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-001-0432-4 · Cited by 62 · see citing works
Major histocompatibility complex class II variation in the giant panda (Ailuropoda melanoleuca)
Wan, Q., Zhu, L., Wu, H., et al. (2006) · Molecular Ecology · doi:10.1111/j.1365-294x.2006.02966.x · Cited by 57 · see citing works
Antigen processing and presentation
Cresswell, P. (2005) · Immunological Reviews · doi:10.1111/j.0105-2896.2005.00320.x · Cited by 54 · see citing works
Marsden, C. D., Mable, B. K., Woodroffe, R., Rasmussen, G. S. A., Cleaveland, S., McNutt, J. W., Emmanuel, M., Thomas, R., & Kennedy, L. J. (2009) · Journal of Heredity · doi:10.1093/jhered/esp031 · Cited by 53 · see citing works
Radwan, J., Demiaszkiewicz, A. W., Kowalczyk, R., Lachowicz, J., Kawałko, A., Wójcik, J. M., Pyziel, A. M., & Babik, W. (2010) · Biological Conservation · doi:10.1016/j.biocon.2010.05.012 · Cited by 52 · see citing works
MHC class I genes of birds of prey: isolation, polymorphism and diversifying selection
Alcaide, M., Edwards, S. V., Cadahía, L., et al. (2008) · Conservation Genetics · doi:10.1007/s10592-008-9653-7 · Cited by 50 · see citing works
MHC Polymorphism and the Design of Captive Breeding Programs: Simple Solutions Are Not the Answer
Miller, P. S., & Hedrick, P. W. (1991) · Conservation Biology · doi:10.1111/j.1523-1739.1991.tb00369.x · Cited by 48 · see citing works
The Causes of Biological Diversity
Clarke, B. C. (1975) · Scientific American · doi:10.1038/scientificamerican0875-50 · Cited by 47 · see citing works
Reduced MHC variation in a threatened tuatara species
Miller, H. C., Miller, K. A., & Daugherty, C. H. (2008) · Animal Conservation · doi:10.1111/j.1469-1795.2008.00168.x · Cited by 44 · see citing works
Pokorny, I., Sharma, R., Goyal, S. P., et al. (2010) · Immunogenetics · doi:10.1007/s00251-010-0475-7 · Cited by 43 · see citing works
Yang, G., Yan, J., Zhou, K., et al. (2005) · Journal of Heredity · doi:10.1093/jhered/esi055 · Cited by 43 · see citing works
The distribution of nuclear genetic variation and historical demography of sea otters
Aguilar, A., Jessup, D. A., Estes, J. A., & Garza, J. C. (2007) · Animal Conservation · doi:10.1111/j.1469-1795.2007.00144.x · Cited by 42 · see citing works
A Comparative Analysis of Mhc DRB3 Polymorphism in the American Bison (Bison bison)
Mikko, S., Spencer, M., Morris, B. G., Stabile, S. D. S., Basu, T., Stormont, C. J., & Andersson, L. (1997) · Journal of Heredity · doi:10.1093/oxfordjournals.jhered.a023144 · Cited by 42 · see citing works
Drake, G. J., Kennedy, L. J., Auty, H. K., et al. (2003) · Molecular Ecology · doi:10.1046/j.1365-294x.2003.02027.x · Cited by 41 · see citing works
MHC genetic structure and divergence across populations of Chinook salmon (Oncorhynchus tshawytscha)
Evans, M. L., Neff, B. D., & Heath, D. D. (2009) · Heredity · doi:10.1038/hdy.2009.121 · Cited by 41 · see citing works
Becker, L., Nieberg, C., Jahreis, K., & Peters, E. (2009) · Immunogenetics · doi:10.1007/s00251-009-0362-2 · Cited by 39 · see citing works
DLA-DRB1, DQA1, and DQB1 Alleles and Haplotypes in North American Gray Wolves
Kennedy, L. J., Angles, J. M., Barnes, A., et al. (2007) · Journal of Heredity · doi:10.1093/jhered/esm051 · Cited by 39 · see citing works
Bowen, L., Aldridge, B. M., Gulland, F. M. D., et al. (2002) · Immunogenetics · doi:10.1007/s00251-002-0472-6 · Cited by 38 · see citing works
Dausset, J. B. (1958) · Vox Sanguinis · doi:10.1111/j.1423-0410.1958.tb03559.x · Cited by 37 · see citing works
Bowen, L., Aldridge, B. M., DeLong, R. L., et al. (2005) · Immunogenetics · doi:10.1007/s00251-004-0757-z · Cited by 37 · see citing works
Sommer, S., & Tichy, H. (1999) · Molecular Ecology · doi:10.1046/j.1365-294x.1999.00687.x · Cited by 37 · see citing works
Hedrick, P. W., Lee, R. N., & Buchanan, C. (2003) · Journal of Wildlife Diseases · doi:10.7589/0090-3558-39.4.909 · Cited by 35 · see citing works
Reduced MIC Gene Repertoire Variation in West African Chimpanzees as Compared to Humans
de Groot, N. G., García-Sepúlveda, C. A., Verschoor, E. J., et al. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi127 · Cited by 32 · see citing works
Mason, R. A. B., Browning, T. L., & Eldridge, M. D. B. (2009) · Conservation Genetics · doi:10.1007/s10592-009-9993-y · Cited by 31 · see citing works
Peters, M. B., & Turner, T. F. (2007) · Conservation Genetics · doi:10.1007/s10592-007-9336-9 · Cited by 30 · see citing works
Kanthaswamy, S., Kou, A., Satkoski, J., Penedo, M. C. T., Ward, T., Ng, J., Gill, L., Lerche, N. W., Erickson, B. J., & Smith, D. G. (2010) · American Journal of Primatology · doi:10.1002/ajp.20811 · Cited by 30 · see citing works
Balancing selection, sexual selection and geographic structure in MHC genes of Great Snipe
Ekblom, R., Sæther, S. A., Fiske, P., et al. (2008) · Genetica · doi:10.1007/s10709-008-9335-x · Cited by 30 · see citing works
Zhu, L., Ruan, X., Ge, Y.-F., Wan, Q., & Fang, S. (2007) · BMC Genetics · doi:10.1186/1471-2156-8-29 · Cited by 30 · see citing works
A Contagious Tumor of the Hamster
Brindley, D. C., & Banfield, W. G. (1961) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/26.4.949 · Cited by 29 · see citing works
Archie, E. A., Henry, T., Maldonado, J. E., et al. (2010) · Immunogenetics · doi:10.1007/s00251-009-0413-8 · Cited by 26 · see citing works
Major histocompatibility complex diversity in the endangered Ethiopian wolf (Canis simensis)
Kennedy, L. J., Randall, D. A., Knobel, D. L., et al. (2011) · Tissue Antigens · doi:10.1111/j.1399-0039.2010.01591.x · Cited by 26 · see citing works
II. One size fits all: nonclassical MHC molecules fulfill multiple roles in epithelial cell function
Blumberg, R. S. (1998) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1998.274.2.g227 · Cited by 25 · see citing works
World Association of Zoos and Aquariums
Russell, J. R., & Cohn, R. D. (2012) · Bookvika Publishing , LENNEX Corp · Cited by 23 · see citing works
MHC Variation in the Endangered Gila Topminnow
Hedrick, P. W., & Parker, K. M. (1998) · Evolution · doi:10.2307/2410934 · Cited by 23 · see citing works
MHC and Captive Breeding: A Rebuttal
Gilpin, M. E., & Wills, C. J. (1991) · Conservation Biology · doi:10.1111/j.1523-1739.1991.tb00368.x · Cited by 22 · see citing works
Studbooks: the basis of breeding programmes
Glatston, A. R. (1986) · International Zoo Yearbook · doi:10.1111/j.1748-1090.1985.tb02533.x · Cited by 21 · see citing works
Genes of the MHC class III region and the functions of the proteins they encode
Milner, C. M., Aguado, B., Campbell, R. D., et al. (1996) · Research Explorer (The University of Manchester) · Cited by 21 · see citing works
Aldridge, B. M., Bowen, L., Smith, B. R., et al. (2006) · Immunogenetics · doi:10.1007/s00251-005-0069-y · Cited by 20 · see citing works
Zhang, B., Fang, S., & Xi, Y. (2006) · Biochemical Genetics · doi:10.1007/s10528-006-9018-1 · Cited by 20 · see citing works
Schad, J., Ganzhorn, J. U., & Sommer, S. (2005) · Evolution · doi:10.1554/04-312 · Cited by 19 · see citing works
Újvári, B., Madsen, T. R. L., & Olsson, M. M. (2005) · Amphibia-Reptilia · doi:10.1163/156853805774408630 · Cited by 17 · see citing works
Traul, D. L., Li, H., Dasgupta, N., O’Toole, D., Eldridge, J. A., Besser, T. E., & Davies, C. J. (2007) · Animal Genetics · doi:10.1111/j.1365-2052.2007.01575.x · Cited by 16 · see citing works
de Mera, I. G. F., Vicente, J., de la Lastra, J. M. P., et al. (2009) · Journal of Zoology · doi:10.1111/j.1469-7998.2008.00524.x · Cited by 16 · see citing works
Smith, S., Belov, K., & Hughes, J. M. (2009) · Conservation Genetics · doi:10.1007/s10592-009-0029-4 · Cited by 15 · see citing works
Self-citationGoda, N., Mano, T., Kosintsev, P. A., et al. (2010) · Tissue Antigens · doi:10.1111/j.1399-0039.2010.01528.x · Cited by 13 · see citing works
Relevance of Studbook Data to the Successful Captive Management of Grey Mouse Lemurs
Glatston, A. R. (2001) · International Journal of Primatology · doi:10.1023/a:1026414031373 · Cited by 12 · see citing works
Huisinga, M., Failing, K., & Reinacher, M. (2007) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2007.05.020 · Cited by 12 · see citing works
Go, Y., Rakotoarisoa, G., Kawamoto, Y., et al. (2004) · Primates · doi:10.1007/s10329-004-0101-0 · Cited by 10 · see citing works
AN INDUCED TRANSMISSIBLE SARCOMA IN HAMSTERS: ELEVEN-YEAR OBSERVATION THROUGH 288 PASSAGES.
Fabrizio, A. M. (1965) · PubMed · Cited by 9 · see citing works
Mhc class II DRB sequences of lion‐tailed macaques (Macaca silenus)
Blankenburg, A., Kaup, F. ‐., & Sauermann, U. (2003) · Tissue Antigens · doi:10.1034/j.1399-0039.2003.00094.x · Cited by 8 · see citing works
Kurbel, S., Pleština, S., & Vrbanec, D. (2006) · Medical Hypotheses · doi:10.1016/j.mehy.2006.10.006 · Cited by 4 · see citing works
Molecular ecology of the endangered Gouldian Finch Erythrura gouldiae
Esparza‐Salas, R. (2008) · Cited by 3 · see citing works
MHC expression of African green monkeys of Barbados is limited in heterogeneity
Lekutis, C., & Letvin, N. L. (1995) · Journal of Medical Primatology · doi:10.1111/j.1600-0684.1995.tb00150.x · Cited by 3 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- [114]Glatston AR Ten years after: The history of the red panda studbook Proceedings of the 5th World Conference on Breeding Endangered Species in Captivity Dresser BL Reece RW Maruska EJ Cincinnati Zoo and Botanical Garden Cincinnati, OH, USA 9–12 10 1988 53 66
- [166]Browning TL Inbreeding, the MHC and infectious disease susceptibility in the Tammar wallaby, Macropus eugenii Ph.D. Thesis Department of Biological Sciences, Faculty of Science, Macquarie University Sydney, Australia 2009
Cited by
Sorted by citations
Lok, S., Lau, T. N. H., Trost, B., Tong, A. H. Y., Paton, T., Wintle, R. F., Engstrom, M. D., Gunn, A., & Scherer, S. W. (2024) · Scientific Reports · doi:10.1038/s41598-024-67270-9 · Cited by 4 · see citing works
- Authors
- Ujvari, B., & Belov, K.
- Affiliations
- Faculty of Veterinary Science, University of Sydney, RMC Gunn Bldg, Sydney, NSW 2006, Australia
- The University of Sydney (AU)
- Corresponding author
- Belov, Katherine
- ORCID
- Belov, Katherine
- Venue
- International Journal of Molecular Sciences
- Publisher
- MDPI AG
- Published
- 2011-08-15
- Volume
- 12
- Issue
- 8
- Pages
- 5168-5186
- ISSN
- 1422-0067 (ISSN-L)
- PMC
- PMC3179158
- OpenAlex
- W2143197765
- Cited by
- 154
- References
- 170
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 12 · 2023: 6 · 2022: 40 · 2021: 9 · 2020: 6 · 2019: 10 · 2018: 12 · 2017: 9 · 2016: 10 · 2015: 11 · 2014: 5 · 2013: 8 · 2012: 5
- FWCI
- 0.61
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- International Journal of Molecular Sciences (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- University of Sydney
- Australian 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 › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- major histocompatibility complex, MHC polymorphism, genetic diversity, conservation genetics, extinction risk, captive breeding, mate choice, contagious cancer, wildlife rescue, host-parasite interactions, MHC typing
- MeSH terms
- Animals, Breeding, Biological Evolution, Humans, Major Histocompatibility Complex, Neoplasms, Polymorphism, Genetic, Genetic Variation
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