MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years?

Journal of Evolutionary Biology - Tập 16 Số 3 - Trang 363-377 - 2003
Louis Bernatchez1, Christian R. Landry2
1Département de biologie, Université Laval, Ste Foy, Québec, Canada
2Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA

Tóm tắt

Abstract Elucidating how natural selection promotes local adaptation in interaction with migration, genetic drift and mutation is a central aim of evolutionary biology. While several conceptual and practical limitations are still restraining our ability to study these processes at the DNA level, genes of the major histocompatibility complex (MHC) offer several assets that make them unique candidates for this purpose. Yet, it is unclear what general conclusions can be drawn after 15 years of empirical research that documented MHC diversity in the wild. The general objective of this review is to complement earlier literature syntheses on this topic by focusing on MHC studies other than humans and mice. This review first revealed a strong taxonomic bias, whereby many more studies of MHC diversity in natural populations have dealt with mammals than all other vertebrate classes combined. Secondly, it confirmed that positive selection has a determinant role in shaping patterns of nucleotide diversity in MHC genes in all vertebrates studied. Yet, future tests of positive selection would greatly benefit from making better use of the increasing number of models potentially offering more statistical rigour and higher resolution in detecting the effect and form of selection. Thirdly, studies that compared patterns of MHC diversity within and among natural populations with neutral expectations have reported higher population differentiation at MHC than expected either under neutrality or simple models of balancing selection. Fourthly, several studies showed that MHC-dependent mate preference and kin recognition may provide selective factors maintaining polymorphism in wild outbred populations. However, they also showed that such reproductive mechanisms are complex and context-based. Fifthly, several studies provided evidence that MHC may significantly influence fitness, either by affecting reproductive success or progeny survival to pathogens infections. Overall, the evidence is compelling that the MHC currently represents the best system available in vertebrates to investigate how natural selection can promote local adaptation at the gene level despite the counteracting actions of migration and genetic drift. We conclude this review by proposing several directions where future research is needed.

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Tài liệu tham khảo

Apanius, 1997, The nature of selection on the major histocompatibility complex, Crit. Rev. Immunol., 17, 179, 10.1615/CritRevImmunol.v17.i2.40

Arkush, 2002, Resistance to three pathogens in the endangered winter-run chinook salmon (Oncorhynchus tsawytscha): effects of inbreeding and major histocompatibility complex genotypes, Can. J. Fish Aquat. Sci., 59, 966, 10.1139/f02-066

Bakke, 1998, Diseases and parasites in wild Atlantic salmon (Salmo salar) populations, Can. J. Fish. Aquat. Sci., 55, 247, 10.1139/d98-021

Bergstrom, 1998, Recent origin of HLA-DRB1 alleles and implication for human evolution, Nat. Genet., 18, 237, 10.1038/ng0398-237

Bingulac-Popovic, 1997, Mapping of mhc class I and class II regions to different linkage groups in the zebrafish, Danio rerio, Immunogenetics, 46, 129, 10.1007/s002510050251

Bodmer, 1972, Evolutionary significance of the HLA-system, Nature (London), 237, 139, 10.1038/237139a0

Boyce, 1997, Genetic variation of major histocompatibility complex and microsatellite loci: a comparison in bighorn sheep, Genetics, 145, 421, 10.1093/genetics/145.2.421

Clarke, 1966, Maintenance of histocompatibility polymorphism, Nature, 211, 999, 10.1038/211999a0

Cohen, 2002, Strong positive selection and habitat specific substitution patterns in Mhc from an estuarine fish under intense pollution stress, Mol. Biol. Evol., 19, 1870, 10.1093/oxfordjournals.molbev.a004011

Cowell, 1998, The distribution of variation in regulatory gene segments, as present in MHC class II promoters, Genome Res., 8, 124, 10.1101/gr.8.2.124

Dean, 2002, Balanced polymorphism selected by genetic versus infectious human disease, Annu. Rev. Genomics. Hum. Genet., 3, 263, 10.1146/annurev.genom.3.022502.103149

Ditchkoff, 2001, Major-histocompatibility-complex-associated variation in secondary sexual traits of white-tailed deer (Odocoileus virginianus): evidence for good-genes advertisement, Evolution, 55, 616, 10.1554/0014-3820(2001)055[0616:MHCAVI]2.0.CO;2

Dixon, 1996, Evolution of MHC classII B chain-encoding genes in the Lake Tana barbel species flock (Barbus intermedius complex), Immunogenetics, 44, 419

Doherty, 1975, Enhanced immunological surveillance in mice heterozugous at the H-2 gene complex, Nature, 256, 50, 10.1038/256050a0

Duchesne, 2002, PAPA (Package for the Analysis of Parental Allocation): a computer program for simulated and real parental allocation, Mol. Ecol. Notes., 2, 191, 10.1046/j.1471-8286.2002.00164.x

Edwards, 1998, Evolution and ecology of MHC molecules: from genomics to sexual selection, Trends Ecol. Evol., 13, 305, 10.1016/S0169-5347(98)01416-5

Ewens, 1972, The sampling theory of selectively neutral alleles, Theo. Pop. Bio., 3, 87, 10.1016/0040-5809(72)90035-4

Figueroa, 1988, MHC polymorphism pre-dating speciation, Nature, 335, 265, 10.1038/335265a0

Flajnik, 1993, A novel type of class I gene organization in vertebrates: a large family of non-MHC-linked class I genes is expressed at the RNA level in the amphibian Xenopus, EMBO J., 12, 4385, 10.1002/j.1460-2075.1993.tb06123.x

Ford, 2002, Applications of selective neutrality tests to molecular ecology, Mol. Ecol., 11, 1245, 10.1046/j.1365-294X.2002.01536.x

Garant, 2000, Ecological determinants and temporal stability of whitin-river population structure in Atlantic salmon (Salmo salar L.), Mol. Ecol., 9, 615, 10.1046/j.1365-294x.2000.00909.x

Garrigan, 2001, Class I MHC polymorphism and evolution in endangered California Chinook and other Pacific salmon, Immunogenetics, 53, 483, 10.1007/s002510100352

Guardiola, 1996, Functional significance of polymorphism among MHC class II gene promoters, Tissue Antigens, 48, 615, 10.1111/j.1399-0039.1996.tb02684.x

Hambuch, 2002, Enhanced selection for MHC diversity in social tuco-tucos, Evolution, 56, 841

Hansen, 1999, Expression, linkage, and polymorphism of MHC-related genes in rainbow trout, Oncorhynchus mykiss, J. Immunol., 163, 774, 10.4049/jimmunol.163.2.774

Hedrick, 1994, Evolutionary genetics of the major histocompatibility complex, Am. Nat., 143, 945, 10.1086/285643

Hedrick, 1999, Perspective: highly variable loci and their interpretation in evolution and conservation, Evolution, 53, 313, 10.2307/2640768

Hedrick, 2001, Parasite resistance and genetic variation in the endangered Gila topminnow, Anim. Cons., 4, 103, 10.1017/S1367943001001135

Hedrick, 2001, Using microsatellite and MHC variation to identify species, ESUs, and MUs in the endangered Sonoran topminnow, Mol. Ecol., 10, 1399, 10.1046/j.1365-294X.2001.01289.x

Hess, 2002, The evolution of the major histocompatibility complex in birds, Bioscience, 52, 423, 10.1641/0006-3568(2002)052[0423:TEOTMH]2.0.CO;2

Hill, 1987, Accelerated evolution in the reactive centre regions of serine protease inhibitors, Nature, 326, 96, 10.1038/326096a0

Hogstrand, 1994, A determination of the frequency of gene conversion in unmanipulated mouse sperm, Proc. Natl. Acad. Sci. USA, 91, 9921, 10.1073/pnas.91.21.9921

Hughes, 1988, Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection, Nature, 335, 167, 10.1038/335167a0

Hughes, 1998, Natural selection and the evolutionary history of major histocompatibility complex loci, Front. Biosci., 3, d509, 10.2741/A298

Jeffery, 2000, Do infectious diseases drive MHC diversity?, Microbes. Infect., 2, 1335, 10.1016/S1286-4579(00)01287-9

Jordan, 1998, New perspectives on mate choice and the MHC, Heredity, 81, 239, 10.1038/sj.hdy.6884280

Kim, 1999, Major histocompatibility complex differentiation in Sacramento River chinook salmon, Genetics, 151, 1115, 10.1093/genetics/151.3.1115

Klein, 1986, The Natural History of the Major Histocompatibility Complex

Klein, 1987, Origin of major histocompatibility complex polymorphism: the trans-species hypothesis, Hum. Immunol., 19, 155, 10.1016/0198-8859(87)90066-8

Landry, 2001, Comparative analysis of population structure across environments and geographical scales at major histocompatibility complex and microsatellite loci in Atlantic salmon (Salmo salar), Mol. Ecol., 10, 2525, 10.1046/j.1365-294X.2001.01383.x

Landry, 2001, ‘Good genes as heterozygosity’: the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar), Proc. R. Soc. Lond. B, 268, 1279, 10.1098/rspb.2001.1659

Langefors, 2001, Association between major histocompatibility complex class IIB alleles and resistance to Aeromonas salmonicida in Atlantic salmon, Proc. R. Soc. Lond. B, 268, 479, 10.1098/rspb.2000.1378

Lohm, 2002, Experimental evidence for major histocompatibiltiy complex-allele-specific resistance to a bacterial infection, Proc. R. Soc. Lond. B., 2114, 2029, 10.1098/rspb.2002.2114

Malaga-Trillo, 1998, Linkage relationships and haplotype polymorphism among cichlid Mhc class II B loci, Genetics, 149, 1527, 10.1093/genetics/149.3.1527

Marshall, 1998, Statistical confidence for likelihood-based paternity inference in natural populations, Mol. Ecol., 7, 639, 10.1046/j.1365-294x.1998.00374.x

Martinsohn, 1999, The gene conversion hypothesis of MHC evolution: a review, Immunogenetics, 50, 168, 10.1007/s002510050593

Meyer, 2001, How selection shapes variation on the human major histocompatibility complex: a review, Ann. Hum. Gen., 65, 1, 10.1046/j.1469-1809.2001.6510001.x

Miller, 2001, Geographic heterogeneity in natural selection on an MHC locus in sockeye salmon, Genetica, 111, 237, 10.1023/A:1013716020351

Miller, 1997, MHC diversity in Pacific salmon: population structure and trans-species allelism, Hereditas, 127, 163

Miller, 1998, The salmonids class I MHC: limited diversity in a primitive teleost, Immuno. Rev., 166, 279, 10.1111/j.1600-065X.1998.tb01269.x

Muirhead, 2001, Consequences of population structure on genes under balancing selection, Evolution, 55, 1532

Navarro, 2002, The effects of multilocus balancing selection on neutral variability, Genetics, 161, 849, 10.1093/genetics/161.2.849

Nielsen, 2001, Statistical tests of selective neutrality in the age of genomics, Heredity, 86, 641, 10.1046/j.1365-2540.2001.00895.x

Nowak, 1992, The optimal number of major histocompatibility complex molecules in an individual, Proc. Natl. Acad. Sci. USA, 89, 10 896, 10.1073/pnas.89.22.10896

Olsén, 2002, Influence of MHC on sibling discrimination in Arctic char, Salvelinus alpinus (L.), J. Chem. Ecol., 28, 783, 10.1023/A:1015240810676

Olsén, 1998, MHC and kin discrimination in juvenile Arctic charr, Salvelinus alpinus (L.), Anim. Behav., 56, 319, 10.1006/anbe.1998.0837

Paterson, 1998, Evidence for balancing selection at the major histocompatibility complex in a free-living ruminant, J. Hered., 89, 289, 10.1093/jhered/89.4.289

Paterson, 1997, No evidence for major histocompatibility complex-dependent mating patterns in a free-living ruminant population, Proc. R. Soc. Lond. B, 264, 1813, 10.1098/rspb.1997.0250

Paterson, 1998, Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.), Proc. Natl. Acad. Sci. USA, 95, 3714, 10.1073/pnas.95.7.3714

Penn, 2002, The scent of genetic compatibility: sexual selection and the major histocompatibility complex, Ethology, 108, 1, 10.1046/j.1439-0310.2002.00768.x

Penn, 2002, MHC heterozygosity confers a selective advantage against multiple-strain infections, Proc. Natl. Acad. Sci. USA, 99, 11 260, 10.1073/pnas.162006499

Penn, 1998, Chemical signals and parasite-mediated sexual selection, Trends Ecol. Evol., 13, 391, 10.1016/S0169-5347(98)01473-6

Penn, 1999, The evolution of mating preference and major histocompatibility complex genes, Am. Nat., 153, 145, 10.1086/303166

Ploegh, 1998, Antigen recognition, Curr. Opin. Immunol., 10, 57, 10.1016/S0952-7915(98)80032-0

Potts, 1990, Evolution of diversity at the major histocompatibility complex, Trends Ecol. Evol., 5, 181, 10.1016/0169-5347(90)90207-T

Reusch, 2001, Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism, Nature, 414, 300, 10.1038/35104547

Richman, 2000, Evolution of balanced genetic polymorphism, Mol. Ecol., 9, 1953, 10.1046/j.1365-294X.2000.01125.x

Richman, 2001, MHC class II beta sequence diversity in the deer mouse (Peromyscus maniculatus): implications for models of balancing selection, Mol. Ecol., 10, 2765, 10.1046/j.0962-1083.2001.01402.x

Richman, 1999, Self-incompatibility alleles from Physalis: implications for historical inference from balanced genetic polymorphisms, Proc. Natl. Acad. Sci. USA, 96, 168, 10.1073/pnas.96.1.168

Sammut, 2002, The fate of duplicated major histocompatibility complex class Ia genes in a dodecaploid amphibian, Xenopus ruwenzoriensis, Eur. J. Immunol., 32, 1593, 10.1002/1521-4141(200206)32:6<1593::AID-IMMU1593>3.0.CO;2-6

Sauermann, 2001, Increased reproductive success of MHC class II heterozygous males among free-ranging rhesus macaques, Hum. Gen., 108, 249, 10.1007/s004390100485

Schierup, 1998, The number of self-incompatibility alleles in a finite, subdivided population, Genetics, 149, 1153, 10.1093/genetics/149.2.1153

Schierup, 2000, The effect of subdivision on variation at multi-allelic loci under balancing selection, Genet. Res., 76, 51, 10.1017/S0016672300004535

Slatkin, 1994, An exact test for neutrality based on the Ewens sampling distribution, Genet. Res., 64, 71, 10.1017/S0016672300032560

Slatkin, 2000, A method for estimating the intensity of overdominant selection from the distribution of allele frequencies, Genetics, 156, 2119, 10.1093/genetics/156.4.2119

Stet, 1991, The histocompatibility system in teleostean fishes: from multiple histocompatibility loci to a major histocompatibility complex, Fish Shell. Immunol., 1, 1, 10.1016/S1050-4648(06)80016-1

Streelman, 2000, From phenotype to genotype, Evol. Dev., 2, 166, 10.1046/j.1525-142x.2000.00056.x

Takahata, 1990, Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci, Genetics, 124, 967, 10.1093/genetics/124.4.967

Tregenza, 2000, Genetic compatibility, mate choice and patterns of parentage: invited review, Mol. Ecol., 9, 1013, 10.1046/j.1365-294x.2000.00964.x

Van Eden, 1983, The genetic approach to infectious disease with special emphasis on the MHC, Dis. Mark., 1, 221

Van Muiswinkel, 1999, The influence of environmental and genetic factors on the disease resistance of fish, Aquaculture, 172, 103, 10.1016/S0044-8486(98)00444-X

Von Schantz, 1989, Female choice selects for a viability-based male trait in pheasant, Nature, 337, 166, 10.1038/337166a0

Von Schantz, 1997, Mate choice, male condition-dependent ornamentation and MHC in the pheasant, Hereditas, 127, 133, 10.1111/j.1601-5223.1997.t01-1-00133.x

Von Schantz, 1996, MHC genotype and male ornamentation: genetic evidence for the Hamilton–Zuk model, Proc. R. Soc. Lond. B, 263, 265, 10.1098/rspb.1996.0041

Watkins, 1988, A primate species with limited major histocompatibility complex class I polymorphism, Proc. Natl. Acad. Sci. USA, 85, 7714, 10.1073/pnas.85.20.7714

Watterson, 1978, The homozygosity test of neutrality, Genetics, 88, 405, 10.1093/genetics/88.2.405

Wegner, 2003, Multiple parasites are driving major histocompatibility complex polymorphism in the wild, J. Evol. Biol., 16, 224, 10.1046/j.1420-9101.2003.00519.x

Yang, 2000, Statistical methods for detecting molecular adaptation, Trends Ecol. Evol., 15, 496, 10.1016/S0169-5347(00)01994-7

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Journal of Evolutionary Biology

Tập 16 Số 3

363-377

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