Does reduced MHC diversity decrease viability of vertebrate populations?

Radwan, Jacek; Biedrzycka, Aleksandra; Babik, Wiesław

doi:10.1016/j.biocon.2009.07.026

Cited by 260Genetic diversity and population structureEvolution and Genetic DynamicsAnimal Behavior and Reproduction

Does reduced MHC diversity decrease viability of vertebrate populations?

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Radwan, Jacek, Biedrzycka, Aleksandra, Babik, Wiesław·2010·Biological Conservation

DOI 10.1016/j.biocon.2009.07.026PMC PMC7092871

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Abstract

Loss of genetic variation may render populations more vulnerable to pathogens due to inbreeding depression and depletion of variation in genes responsible for immunity against parasites. Here we review the evidence for the significance of variation in genes of the Major Histocompatibility Complex (MHC) for conservation efforts. MHC molecules present pathogen-derived antigens to the effector cells of the immune system and thus trigger the adaptive immune response. Some MHC genes are the most variable functional genes in the vertebrate genome. Their variation is clearly of adaptive significance and there is considerable evidence that its maintenance is mainly due to balancing selection imposed by pathogens. However, while the evidence for selection shaping MHC variation on the historical timescale is compelling, a correlation between levels of MHC variation and variation at neutral loci is often observed, indicating that on a shorter timescale drift also substantially affects MHC, leading to depletion of MHC diversity. The evidence that the loss of MHC variation negatively affects population survival is so far equivocal and difficult to separate from effects of general inbreeding. Some species with depleted MHC variation seem to be particularly susceptible to infection, but other species thrive and expand following severe bottlenecks that have drastically limited their MHC variation. However, while the latter demonstrate that MHC variation is not always critical for population survival, these species may in fact represent rare examples of survival despite of the loss of MHC variation. There is clearly a compelling need for data that would disclose the possible consequences of MHC diversity for population viability. In particular, we need more data on the impact of MHC allelic richness on the abundance of parasites or prevalence of disease in populations, while controlling for the role of general inbreeding. Before such evidence accumulates, captive breeding programs and other conservation measures aimed at inbreeding avoidance should be favoured over those protecting only MHC variation, especially since inbreeding avoidance programs would usually conserve both types of genetic diversity simultaneously.

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The role of mhc polymorphism in anti-microbial resistance
Nikolich‐Žugich, J., Fremont, D. H., Miley, M. J., & Messaoudi, I. (2004) · Microbes and Infection · doi:10.1016/j.micinf.2004.01.006 · Cited by 55 · 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
Genetic variation in two endangered Acrocephalus species compared to a widespread congener: estimates based on functional and random loci
Hansson, B., & Richardson, D. S. (2005) · Animal Conservation · doi:10.1017/s1367943004001878 · Cited by 52 · see citing works
MHC and Preferences for Male Odour in the Bank Vole
Radwan, J., Tkacz, A., & Kloch, A. (2008) · Ethology · doi:10.1111/j.1439-0310.2008.01528.x · Cited by 50 · see citing works
Self-citation
Population fragmentation and major histocompatibility complex variation in the spotted suslik, Spermophilus suslicus
Biedrzycka, A., & Radwan, J. (2008) · Molecular Ecology · doi:10.1111/j.1365-294x.2008.03955.x · Cited by 48 · see citing works
Self-citation
The major histocompatibility complex (MHC) in declining populations: an example of adaptive variation
Hedrick, P. W. (2002) · Cambridge University Press eBooks · doi:10.1017/cbo9780511615016.009 · Cited by 46 · see citing works
Genetic variation of the major histocompatibility complex (MHC class II β gene) in the threatened Gila trout, Oncorhynchus gilae gilae
Peters, M. B., & Turner, T. F. (2007) · Conservation Genetics · doi:10.1007/s10592-007-9336-9 · Cited by 30 · see citing works
Low major histocompatibility complex class II DQA diversity in the Giant Panda (Ailuropoda melanoleuca)
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
Genetic variation and resistance to a bacterial infection in the endangered Gila topminnow
Giese, A. R., & Hedrick, P. W. (2003) · Animal Conservation · doi:10.1017/s1367943003003445 · Cited by 22 · see citing works
Evolutionary genomics: Foxy MHC selection story
Hedrick, P. W. (2004) · Heredity · doi:10.1038/sj.hdy.6800539 · Cited by 19 · see citing works
No evidence for female mate choice based on genetic similarity in the túngara frog Physalaemus pustulosus
Lampert, K. P., Bernal, X. E., Rand, A. S., Mueller, U. G., & Ryan, M. J. (2005) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-005-0125-5 · Cited by 18 · see citing works

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Infectious disease, shifting climates, and opportunistic predators: cumulative factors potentially impacting wild salmon declines
Miller, K. M., Teffer, A. K., Tucker, S., Li, S., Schulze, A. D., Trudel, M. J., Juanes, F., Tabata, A., Kaukinen, K. H., Ginther, N. G., et al. (2014) · Evolutionary Applications · doi:10.1111/eva.12164 · Cited by 321 · see citing works
Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species
Witzenberger, K. A., & Hochkirch, A. (2011) · Biodiversity and Conservation · doi:10.1007/s10531-011-0074-4 · Cited by 282 · see citing works
Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes
Sutton, J. T., Nakagawa, S., Robertson, B. C., & Jamieson, I. G. (2011) · Molecular Ecology · doi:10.1111/j.1365-294x.2011.05292.x · Cited by 255 · see citing works
Global Amphibian Declines, Loss of Genetic Diversity and Fitness: A Review
Allentoft, M. E., & O’Brien, J. (2010) · Diversity · doi:10.3390/d2010047 · Cited by 223 · see citing works
Applications and Implications of Neutral versus Non-neutral Markers in Molecular Ecology
Kirk, H., & Freeland, J. R. (2011) · International Journal of Molecular Sciences · doi:10.3390/ijms12063966 · Cited by 219 · see citing works
The impact of multiple infections on wild animal hosts: a review
Bordes, F., & Morand, S. (2011) · Infection Ecology & Epidemiology · doi:10.3402/iee.v1i0.7346 · Cited by 198 · see citing works
Wolf population genetics in E urope: a systematic review, meta‐analysis and suggestions for conservation and management
Hindrikson, M., Remm, J., Pilot, M., Godinho, R., Strønen, A. V., Baltrūnaitė, L., Czarnomska, S. D., Leonard, J. A., Randi, E., Nowak, C., et al. (2016) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12298 · Cited by 196 · see citing works
Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers
Benazzo, A., Trucchi, E., Cahill, J. A., Delser, P. M., Mona, S., Fumagalli, M., Bunnefeld, L., Cornetti, L., Ghirotto, S., Girardi, M., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1707279114 · Cited by 182 · see citing works
Molecular Evolution of the Toll-Like Receptor Multigene Family in Birds
Alcaide, M., & Edwards, S. V. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msq351 · Cited by 170 · 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
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Conspecifics can be aliens too: A review of effects of restocking practices in vertebrates
Champagnon, J., Elmberg, J., Guillemain, M., Gauthier‐Clerc, M., & Lebreton, J. (2012) · Journal for Nature Conservation · doi:10.1016/j.jnc.2012.02.002 · Cited by 160 · see citing works
Cheetah Paradigm Revisited: MHC Diversity in the World's Largest Free-Ranging Population
Castro-Prieto, A., Wachter, B., & Sommer, S. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq330 · Cited by 141 · see citing works
Immunogenetic novelty confers a selective advantage in host–pathogen coevolution
Phillips, K. P., Cable, J., Mohammed, R. S., Herdegen‐Radwan, M., Raubic, J., Przesmycka, K. J., van Oosterhout, C., & Radwan, J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1708597115 · Cited by 113 · see citing works
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Rapid loss of MHC class II variation in a bottlenecked population is explained by drift and loss of copy number variation
Eimes, J. A., Bollmer, J. L., Whittingham, L. A., Johnson, J. A., van Oosterhout, C., & Dunn, P. O. (2011) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2011.02311.x · Cited by 111 · see citing works
Gene conversion rapidly generates major histocompatibility complex diversity in recently founded bird populations
Spurgin, L. G., van Oosterhout, C., Illera, J. C., Bridgett, S., Gharbi, K., Emerson, B. C., & Richardson, D. S. (2011) · Molecular Ecology · doi:10.1111/j.1365-294x.2011.05367.x · Cited by 104 · see citing works
Warring brothers: The complex interactions between wolves (Canis lupus) and dogs (Canis familiaris) in a conservation context
Lescureux, N., & Linnell, J. D. C. (2014) · Biological Conservation · doi:10.1016/j.biocon.2014.01.032 · Cited by 104 · see citing works
Contribution of Systematic Reviews to Management Decisions
Cook, C. N., Possingham, H. P., & Fuller, R. A. (2013) · Conservation Biology · doi:10.1111/cobi.12114 · Cited by 101 · see citing works
Genetic drift outweighs natural selection at toll‐like receptor ( TLR ) immunity loci in a re‐introduced population of a threatened species
Grueber, C. E., Wallis, G. P., & Jamieson, I. G. (2013) · Molecular Ecology · doi:10.1111/mec.12404 · Cited by 94 · see citing works
Evaluating success of translocations in maintaining genetic diversity in a threatened mammal
Ottewell, K. M., Dunlop, J., Thomas, N., Morris, K., Coates, D., & Byrne, M. M. (2014) · Biological Conservation · doi:10.1016/j.biocon.2014.01.012 · Cited by 89 · see citing works
MHC diversity in bottlenecked populations: a simulation model
Ejsmond, M. J., & Radwan, J. (2009) · Conservation Genetics · doi:10.1007/s10592-009-9998-6 · Cited by 89 · see citing works
Self-citation
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
Long-Term Habitat Fragmentation Is Associated With Reduced MHC IIB Diversity and Increased Infections in Amphibian Hosts
Belasen, A. M., Bletz, M. C., Leite, D. D. S., Toledo, L. F., & James, T. Y. (2019) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2018.00236 · Cited by 81 · see citing works
Avian MHC Evolution in the Era of Genomics: Phase 1.0
O’Connor, E., Westerdahl, H., Burri, R., & Edwards, S. V. (2019) · Cells · doi:10.3390/cells8101152 · Cited by 80 · see citing works
Interspecific hybridization increases MHC class II diversity in two sister species of newts
Nadachowska‐Brzyska, K., Zieliński, P., Radwan, J., & Babik, W. (2011) · Molecular Ecology · doi:10.1111/j.1365-294x.2011.05347.x · Cited by 78 · see citing works
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Complex problems need detailed solutions: Harnessing multiple data types to inform genetic management in the wild
Grueber, C. E., Fox, S., McLennan, E. A., Gooley, R. M., Pemberton, D., Hogg, C. J., & Belov, K. (2018) · Evolutionary Applications · doi:10.1111/eva.12715 · Cited by 77 · see citing works
Specific alleles at immune genes, rather than genome‐wide heterozygosity, are related to immunity and survival in the critically endangered Attwater's prairie‐chicken
Bateson, Z. W., Hammerly, S. C., Johnson, J. A., Morrow, M. E., Whittingham, L. A., & Dunn, P. O. (2016) · Molecular Ecology · doi:10.1111/mec.13793 · Cited by 77 · see citing works
Simulating Retention of Rare Alleles in Small Populations to Assess Management Options for Species with Different Life Histories
Weiser, E. L., Grueber, C. E., & Jamieson, I. G. (2013) · Conservation Biology · doi:10.1111/cobi.12011 · Cited by 75 · see citing works
Variation at Innate Immunity Toll-Like Receptor Genes in a Bottlenecked Population of a New Zealand Robin
Grueber, C. E., Wallis, G. P., King, T. M., & Jamieson, I. G. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045011 · Cited by 75 · see citing works
Spatial and temporal patterns of neutral and adaptive genetic variation in the endangered African wild dog (Lycaon pictus)
Marsden, C. D., Woodroffe, R., Mills, M. G. L., McNutt, J. W., Creel, S., Groom, R. J., Emmanuel, M., Cleaveland, S., Kat, P. W., Rasmussen, G. S. A., et al. (2012) · Molecular Ecology · doi:10.1111/j.1365-294x.2012.05477.x · Cited by 73 · see citing works
Can balancing selection on MHC loci counteract genetic drift in small fragmented populations of black grouse?
Strand, T., Segelbacher, G., Quintela, M., Xiao, L., Axelsson, T., & Höglund, ‎. (2012) · Ecology and Evolution · doi:10.1002/ece3.86 · Cited by 69 · see citing works
Balancing selection and heterozygote advantage in major histocompatibility complex loci of the bottlenecked Finnish wolf population
Niskanen, A. K., Kennedy, L. J., Ruokonen, M., Kojola, I., Lohi, H., Isomursu, M., Jansson, E., Pyhäjärvi, T., & Aspi, J. O. (2013) · Molecular Ecology · doi:10.1111/mec.12647 · Cited by 63 · see citing works
Canine adenovirus type 1 (CAdV-1) in free-ranging European brown bear (Ursus arctos arctos): A threat for Cantabrian population?
Marı́n, J. F. G., Royo, L. J., Oleaga, Á., Gayo, E., Alarcia, O. E., Pinto, D., Martínez, I. Z., Gonzalez, P. J., Balsera, R., Marcos, J., et al. (2018) · Transboundary and Emerging Diseases · doi:10.1111/tbed.13013 · Cited by 60 · see citing works
Genetic diversity and disease: The past, present, and future of an old idea
Gibson, A. K. (2021) · Evolution · doi:10.1111/evo.14395 · Cited by 60 · see citing works
Sexual selection and the evolutionary dynamics of the major histocompatibility complex
Ejsmond, M. J., Radwan, J., & Wilson, A. B. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.1662 · Cited by 58 · see citing works
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Genetic diversity at neutral and adaptive loci determines individual fitness in a long-lived territorial bird
Agudo, R., Carrete, M., Alcaide, M., Rico, C., Hiraldo, F., & Donázar, J. A. (2012) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2011.2606 · Cited by 57 · see citing works
Drift, selection, or migration? Processes affecting genetic differentiation and variation along a latitudinal gradient in an amphibian
Cortázar‐Chinarro, M., Lattenkamp, E. Z., Meyer-Lucht, Y., Luquet, É., Laurila, A., & Höglund, ‎. (2017) · BMC Evolutionary Biology · doi:10.1186/s12862-017-1022-z · Cited by 56 · see citing works
Extraordinary MHC class II B diversity in a non‐passerine, wild bird: the Eurasian Coot Fulica atra (Aves: Rallidae)
Alcaide, M., Muñoz, J., la Puente, J. M., Soriguer, R. C., & Figuerola, J. (2014) · Ecology and Evolution · doi:10.1002/ece3.974 · Cited by 55 · see citing works
GENETIC EROSION IN WILD POPULATIONS MAKES RESISTANCE TO A PATHOGEN MORE COSTLY
Luquet, É., Garner, T. W. J., Léna, J., Bruel, C. A., Joly, P. B., Lengagne, T., Grolet, O., & Plénet, S. (2012) · Evolution · doi:10.1111/j.1558-5646.2011.01570.x · Cited by 54 · see citing works
The impact of translocations on neutral and functional genetic diversity within and among populations of the Seychelles warbler
Wright, D. J., Spurgin, L. G., Collar, N., Komdeur, J., Burke, T. A., & Richardson, D. S. (2014) · Molecular Ecology · doi:10.1111/mec.12740 · Cited by 53 · see citing works
Effects of emerging infectious diseases on host population genetics: a review
McKnight, D. T., Schwarzkopf, L., Alford, R. A., Bower, D. S., & Zenger, K. R. (2017) · Conservation Genetics · doi:10.1007/s10592-017-0974-2 · Cited by 53 · see citing works
An evaluation of two potential risk factors, MHC diversity and host density, for infection by an invasive nematode Ashworthius sidemi in endangered European bison (Bison bonasus)
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
Self-citation
Contagious cancer: Lessons from the devil and the dog
Belov, K. (2012) · BioEssays · doi:10.1002/bies.201100161 · Cited by 49 · see citing works
On the relative roles of selection and genetic drift in shaping MHC variation
Alcaide, M. (2010) · Molecular Ecology · doi:10.1111/j.1365-294x.2010.04772.x · Cited by 47 · 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
Repeated sampling of individuals reveals impact of tropical and temperate habitats on microbiota of a migratory bird
Skeen, H. R., Cooper, N. W., Hackett, S. J., Bates, J. M., & Marra, P. P. (2021) · Molecular Ecology · doi:10.1111/mec.16170 · Cited by 47 · see citing works
Challenges of next‐generation sequencing in conservation management: Insights from long‐term monitoring of corridor effects on the genetic diversity of mouse lemurs in a fragmented landscape
Montero, B. K., Ernest, R., Ramanamanjato, J., Randriatafika, F., Rakotondranary, S. J., Wilhelm, K., Ganzhorn, J. U., & Sommer, S. (2018) · Evolutionary Applications · doi:10.1111/eva.12723 · Cited by 46 · see citing works
Major histocompatibility complex class I evolution in songbirds: universal primers, rapid evolution and base compositional shifts in exon 3
Alcaide, M., Liu, M., & Edwards, S. V. (2013) · PeerJ · doi:10.7717/peerj.86 · Cited by 46 · see citing works
Maintaining functional major histocompatibility complex diversity under inbreeding: the case of a selfing vertebrate
Ellison, A., Allainguillaume, J., GIRDWOOD, S. E., Pachebat, J. A., Peat, K. M., Wright, P. A., & Consuegra, S. (2012) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2012.1929 · Cited by 45 · see citing works
Depleted genetic variation of the European ground squirrel in Central Europe in both microsatellites and the major histocompatibility complex gene: implications for conservation
Říčanová, Š., Bryja, J., Cosson, J., Gedeon, C. I., Choleva, L., Ambros, M., & Sedláček, F. (2011) · Conservation Genetics · doi:10.1007/s10592-011-0213-1 · Cited by 44 · see citing works
Major histocompatibility complex variation in insular populations of the Egyptian vulture: inferences about the roles of genetic drift and selection
Agudo, R., Alcaide, M., Rico, C., Lemus, J. Á., Blanco, G., Hiraldo, F., & Donázar, J. A. (2011) · Molecular Ecology · doi:10.1111/j.1365-294x.2011.05107.x · Cited by 44 · see citing works
Cheetahs have a stronger constitutive innate immunity than leopards
Heinrich, S. K., Hofer, H., Courtiol, A., Melzheimer, J., Dehnhard, M., Czirják, G. Á., & Wachter, B. (2017) · Scientific Reports · doi:10.1038/srep44837 · Cited by 43 · see citing works
Heterozygosity–fitness correlation at the major histocompatibility complex despite low variation in Alpine ibex (Capra ibex)
Brambilla, A., Keller, L. F., Bassano, B., & Grossen, C. (2017) · Evolutionary Applications · doi:10.1111/eva.12575 · Cited by 43 · see citing works
Habitat fragmentation in the Brazilian Atlantic Forest is associated with erosion of frog immunogenetic diversity and increased fungal infections
Belasen, A. M., Amses, K. R., Clemons, R. A., Becker, C. G., Toledo, L. F., & James, T. Y. (2022) · Immunogenetics · doi:10.1007/s00251-022-01252-x · Cited by 40 · see citing works
Limited mitochondrial DNA diversity is indicative of a small number of founders of the German raccoon (Procyon lotor) population
Frantz, A. C., Heddergott, M., Lang, J., Schulze, C., Ansorge, H., Runge, M., Braune, S., Michler, F., Wittstatt, U., Hoffmann, L., et al. (2013) · European Journal of Wildlife Research · doi:10.1007/s10344-013-0719-6 · Cited by 39 · see citing works
Macroevolutionary Immunology: A Role for Immunity in the Diversification of Animal life
Loker, E. S. (2012) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00025 · Cited by 39 · see citing works
MHC class II diversity of koala (Phascolarctos cinereus) populations across their range
Lau, Q., Jaratlerdsiri, W., Griffith, J. E., Gongora, J., & Higgins, D. P. (2014) · Heredity · doi:10.1038/hdy.2014.30 · Cited by 36 · see citing works
Impact of historical founder effects and a recent bottleneck on MHC variability in Commander Arctic foxes (Vulpes lagopus)
Ploshnitsa, A. I., Goltsman, M. E., Macdonald, D. W., Kennedy, L. J., & Sommer, S. (2011) · Ecology and Evolution · doi:10.1002/ece3.42 · Cited by 36 · see citing works
Balancing selection and genetic drift at major histocompatibility complex class II genes in isolated populations of golden snub-nosed monkey (Rhinopithecus roxellana)
Luo, M., Pan, H., Liu, Z., & Li, M. (2012) · BMC Evolutionary Biology · doi:10.1186/1471-2148-12-207 · Cited by 36 · see citing works
Drift and selection influence geographic variation at immune loci of prairie-chickens
Bollmer, J. L., Ruder, E. A., Johnson, J. A., Eimes, J. A., & Dunn, P. O. (2011) · Molecular Ecology · doi:10.1111/j.1365-294x.2011.05319.x · Cited by 35 · see citing works
Parasite load and MHC diversity in undisturbed and agriculturally modified habitats of the ornate dragon lizard
Radwan, J., Kuduk, K., Levy, E., LeBas, N. R., & Babik, W. (2014) · Molecular Ecology · doi:10.1111/mec.12984 · Cited by 35 · see citing works
Self-citation
Habitat split as a driver of disease in amphibians
Becker, C. G., Greenspan, S. E., Martins, R. A., Lyra, M. L., Prist, P. R., Metzger, J. P., Pedro, V. D. A. S., Haddad, C. F. B., Sage, E. H. L., Woodhams, D. C., et al. (2023) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12927 · Cited by 34 · see citing works
Balancing selection and introgression of newt immune-response genes
Fijarczyk, A., Dudek, K., Niedzicka, M., & Babik, W. (2018) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2018.0819 · Cited by 33 · see citing works
Self-citation
Is MHC diversity a better marker for conservation than neutral genetic diversity? A case study of two contrasting dolphin populations
Manlik, O., Krützen, M., Kopps, A. M., Mann, J., Bejder, L., Allen, S. J., Frère, C., Connor, R. C., & Sherwin, W. B. (2019) · Ecology and Evolution · doi:10.1002/ece3.5265 · Cited by 33 · see citing works
Selection on MHC class II supertypes in the New Zealand endemic Hochstetter’s frog
Lillie, M., Grueber, C. E., Sutton, J. T., Howitt, R., Bishop, P. J., Gleeson, D. M., & Belov, K. (2015) · BMC Evolutionary Biology · doi:10.1186/s12862-015-0342-0 · Cited by 33 · see citing works
Analyses of historical and current populations of black grouse in Central Europe reveal strong effects of genetic drift and loss of genetic diversity
Segelbacher, G., Strand, T., Quintela, M., Axelsson, T., Jansman, H. A. H., Koelewijn, H.-P., & Höglund, ‎. (2014) · Conservation Genetics · doi:10.1007/s10592-014-0610-3 · Cited by 31 · see citing works
Spatiotemporal adaptive evolution of an MHC immune gene in a frog-fungus disease system
Trujillo, A. L., Hoffman, E. A., Becker, C. G., & Savage, A. E. (2021) · Heredity · doi:10.1038/s41437-020-00402-9 · Cited by 30 · see citing works
Hybridization with mountain hares increases the functional allelic repertoire in brown hares
Pohjoismäki, J., Michell, C., Levänen, R., & Smith, S. (2021) · Scientific Reports · doi:10.1038/s41598-021-95357-0 · Cited by 30 · see citing works
Genetic restoration of a threatened population of greater prairie-chickens
Bateson, Z. W., Dunn, P. O., Hull, S. D., Henschen, A. E., Johnson, J. A., & Whittingham, L. A. (2014) · Biological Conservation · doi:10.1016/j.biocon.2014.03.008 · Cited by 30 · see citing works
Reduced MHC and neutral variation in the Galápagos hawk, an island endemic
Bollmer, J. L., Hull, J. M., Ernest, H. B., Sarasola, J. H., & Parker, P. G. (2011) · BMC Evolutionary Biology · doi:10.1186/1471-2148-11-143 · Cited by 30 · see citing works
High MHC gene copy number maintains diversity despite homozygosity in a Critically Endangered single‐island endemic bird, but no evidence of MHC‐based mate choice
Stervander, M., Dierickx, E., Thorley, J. B., Brooke, M. D. L., & Westerdahl, H. (2020) · Molecular Ecology · doi:10.1111/mec.15471 · Cited by 30 · see citing works
MHC variation reflects the bottleneck histories of N ew Z ealand passerines
Sutton, J. T., Robertson, B. C., & Jamieson, I. G. (2014) · Molecular Ecology · doi:10.1111/mec.13039 · Cited by 29 · see citing works
Assortative Mating on Ideology Could Operate Through Olfactory Cues
McDermott, R., Tingley, D. H., & Hatemi, P. (2014) · American Journal of Political Science · doi:10.1111/ajps.12133 · Cited by 29 · see citing works
Population genetic patterns among social groups of the endangered Central American spider monkey (Ateles geoffroyi) in a human‐dominated landscape
Hagell, S., Whipple, A. V., & Chambers, C. L. (2013) · Ecology and Evolution · doi:10.1002/ece3.547 · Cited by 28 · 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
Influence of immunogenetics, sex and body condition on the cutaneous microbial communities of two giant salamanders
Hernández‐Gómez, O., Briggler, J. T., & Williams, R. N. (2018) · Molecular Ecology · doi:10.1111/mec.14500 · Cited by 28 · see citing works
Genetic Diversity and Differentiation at Structurally Varying MHC Haplotypes and Microsatellites in Bottlenecked Populations of Endangered Crested Ibis
Lan, H., Zhou, T., Wan, Q., & Fang, S. (2019) · Cells · doi:10.3390/cells8040377 · Cited by 28 · see citing works
MHC Class IIB Exon 2 Polymorphism in the Grey Partridge (Perdix perdix) Is Shaped by Selection, Recombination and Gene Conversion
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DOES REDUCED MHC DIVERSITY DECREASE VIABILITY OF VERTEBRATE POPULATIONS? Systematic Review Protocol
(2009)
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Authors: Radwan, J., Biedrzycka, A., & Babik, W.
Affiliations: Institute of Nature Conservation (PL)
Institute of Systematics and Evolution of Animals (PL)
Corresponding author: Radwan, Jacek
ORCID: Radwan, Jacek
Biedrzycka, Aleksandra
Babik, Wiesław
Venue: Biological Conservation
Publisher: Elsevier BV
Published: 2010-03
Volume: 143
Issue: 3
Pages: 537-544
ISSN: 0006-3207 (ISSN-L)
DOI: 10.1016/j.biocon.2009.07.026
PMC: PMC7092871
OpenAlex: W2105554851
Cited by: 259
References: 101
Citations by year: 2026: 10 · 2025: 8 · 2024: 8 · 2023: 9 · 2022: 11 · 2021: 10 · 2020: 8 · 2019: 14 · 2018: 18 · 2017: 13 · 2016: 28 · 2015: 10 · 2014: 27 · 2013: 27 · 2012: 31
FWCI: 1.82
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Biological Conservation (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Fundacja na rzecz Nauki Polskiej
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Keywords: major histocompatibility complex, MHC diversity, inbreeding depression, population viability, genetic diversity, balancing selection, disease susceptibility, population bottleneck, captive breeding, inbreeding avoidance, conservation genetics, vertebrate immunity

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Does reduced MHC diversity decrease viability of vertebrate populations?

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