Perspective: Detecting adaptive molecular polymorphism: Lessons from the MHC

Evolution

Volumn 57, Issue 8, 2003, Pages 1707-1722

  Garrigan, Daniel ^a,b   Hedrick, Philip W ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Adaptive polymorphism; Balancing selection; Major histocompatibility complex; Neutral theory; Nonsynonymous substitution

Indexed keywords

EVOLUTION; GENETIC VARIATION; POLYMORPHISM; SELECTION;

ANIMALIA; VERTEBRATA;

EID: 0042785584     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2003.tb00580.x     Document Type: Review

References (113)

1. Adams, E. J., S. Cooper, G. Thomson, and P. Parham. 2000. Common chimpanzees have greater diversity than humans at two of the three highly polymorphic MHC class I genes. Immunogenetics 51:410-424.
2. Aldrich, C., C. Wambebe, L. Odama, A. DiRienzo, and C. Ober. 2002. Linkage disequilibrium and age estimates of deletion polymophism (1597ΔC) in HLA-G suggest non-neutral evolution. Hum. Immunol. 63:405-412.
3. Arkush, K., A. Giese, H. L. Mendonca, A. M. McBride, G. D. Marty, and P. W. Hedrick. 2002. Resistance to three pathogens in the endangered winter-run chinook salmon (Oncorhynchus tshawytscha): effects of inbreeding and major histocompatibility complex genotypes. Can. J. Fish. Aquat. Sci. 59:966-975.
4. Bamshad, M. J., S. Mummidi, E. Gonzalez, S. S. Ahuja, D. M. Dunn, W. S. Watkins, S. Wooding, A. C. Stone, L. B. Jorde, R. B. Weiss, and S. K. Ahuja. 2002. A strong signature of balancing selection in the 5′ cis-regulatory region of CCR5. Proc. Natl. Acad. Sci. USA 99:10539-10544.
5. Bannai, M., J. Ohashi, S. Harihara, Y. Takahashi, T. Juji, K. Omoto, and K. Tokunaga. 2000. Analysis of HLA genes and haplotypes in Ainu (from Hokkaido, northern Japan) supports the premise that they descend from Upper Paleolithic populations of East Asia. Tissue Antigens 55:128-139.
6. Beck, S., and J. Trowsdale. 2000. The human major histocompatibility complex: lessons from the DNA sequence. Annu Rev. Genom. Hum. Genet. 1:117-137.
7. Begovich, A. B., P. V. Moonsamy, S. J. Mack, L. F. Barcellos, L. L. Steiner, S. Grams, V. Suraj-Baker, J. Hollenbach, E. Trachtenberg, L. Louie, P. Zimmerman, A. V. S. Hill, M. Stoneking, T. Sasazuki, V. I. Konenkov, M. L. Sartakova, V. P. K. Titanji, O. Rickards, and W. Klitz. 2001. Genetic variability and linkage disequilibrium with the HLA-DP region: analysis of 15 different populations. Tissue Antigens 57:424-439.
8. Bjorkman, P. J., M. A. Saper, B. Samraoui, W. S. Bennett, J. L. Stromlinger, and D. C. Wiley. 1987. Structure of the human class I histocompatibility antigen, HLA-A2. Nature 329:506-512.
9. Black, F. L., and P. W. Hedrick. 1997. Strong balancing selection at HLA loci: evidence from segregation in South Amerindian families. Proc. Natl. Acad. Sci. USA 94:12452-12456.
10. Black, F. L., and F. M. Salzano. 1981. Evidence for heterosis in the HLA system. Am. J. Hum. Genet. 33:894-899.
11. Briles, W. E., H. Stone, and R. Cole. 1977. Marek's disease: effects of B histocompatibility alloalleles in resistant and susceptible chicken lines. Science 195:193-195.
12. Brown, J. H., T. S. Jardetzky, J. C. Gorga, L. J. Stern, R. G. Urban, J. L. Stromlinger, and D. C. Wiley. 1993. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364:33-39.
13. Bugawan, T. L., W. Klitz, A. Blair, and H. A. Erlich. 2000. High-resolution HLA class I typing in the CEPH families: analysis of linkage disequilibrium among HLA loci. Tissue Antigens 56:392-404.
14. Bugawan, T. L., S. J. Mack, M. Stoneking, M. Saha, H. P. Beck, and H. A. Erlich. 1999. HLA class I allele distributions in six Pacific/Asian populations: evidence of selection at the HLA-A locus. Tissue Antigens 53:311-319.
15. Carrington, M., G. W. Nelson, M. P. Martin, T. Kissner, D. Vlahov, J. J. Goedert, R. Kaslow, S. Buchbinder, K. Hoots, and S. J. O'Brien. 1999. HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science 283:1748-1752.
16. Cavalli-Sforza, L. L., and W. F. Bodmer. 1971. The genetics of human populations. W. H. Freeman, San Francisco, CA.
17. Chen, J. J., J. A. Hollenbach, E. A. Trachtenberg, J. J. Just, M. Carrington, K. S. Rønningen, A. Begovich, M.-C. King, S. McWeeney, S. J. Mack, H. A. Erlich, and G. Thomson. 1999. Hardy-Weinberg testing for HLA class II (DRB1, DQA1, DQB1, and DPB1) loci in 26 human ethnic groups. Tissue Antigens 54:533-542.
18. Crow, J. F., and K. Aoki. 1984. Group selection for a polygenic behavioral trait: estimating the degree of population subdivision. Proc. Natl. Acad. Sci. USA 81:6073-6077.
19. Doherty, C., and R. M. Zinkernagel. 1975. Enhanced immunological surveillance in mice heterozygous at the H-2 complex. Nature 256:50-52.
20. Edwards, S. V., E. K. Wakeland, and W. K. Potts. 1995. Contrasting histories of avian and mammalian Mhc genes revealed by class II B sequences from songbirds. Proc. Natl. Acad. Sci. USA 92:12200-12204.
21. Edwards, S. V., K. Chesnut, Y. Satta, and E. K. Wakeland. 1997. Ancestral polymorphism of Mhc class II genes in mice: implications for balancing selection and the mammalian molecular clock. Genetics 146:655-668.
22. Egid, K., and J. L. Brown. 1989. The major histocompatibility complex and female mating preference in mice. Anim. Behav. 38:548-560.
23. Ewens, W. J. 1972. The sampling theory of selectively neutral alleles. Theor. Popul. Biol. 3:87-112.
24. Fay, J. C., G. J. Wyckoff, and C.-I. Wu. 2002. Testing the neutral theory of molecular evolution with genomic data from Drosophila. Nature 415:1024-1026.
25. Flajnik, M. F., Y. Ohta, C. Namikawa-Yamada, and M. Nonaka. 1999. Insight into the primordial MHC from studies of ectothermic vertebrates. Immunol. Rev. 167:59-67.
26. Franklin, I. R., and R. C. Lewontin. 1970. Is the gene the unit of selection? Genetics 65:707-734.
27. Gao, X., S. Lester, A. Veale, B. Boettcher, B. Currie, J. McCluskey, and G. Chelvanayagam. 2000. HLA class I alleles in Australian aborigines and their peptide binding profiles. Pp. 446-462 in M. Kasahara, ed. Major histocompatibility complex: evolution, structure, and function. Springer, Tokyo.
28. Garboczi, D. N., P. Ghosh, U. Utz, Q. R. Fan, W. E. Biddison, and D. C. Wiley. 1996. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 384:134-141.
29. Garrigan, D., and P. W. Hedrick. 2001. MHC class I polymorphism and evolution in endangered California chinook and other Pacific salmon. Immunogenetics 53:483-489.
30. Gaudieri, S., R. L. Dawkins, K. Habara, J. K. Kulski, and T. Gojobori. 2000. SNP profile within the human major histocompatibility complex reveals an extreme and interrupted level of nucleotide diversity. Genome Res. 10:1579-1586.
31. Gillespie, J. H. 1978. A general model to account for enzyme variation in natural populations. V. The SAS-CFF model. Theor. Popul. Genet. 14:1-45.
32. Gutierrez-Espeleta, G. A., S. T. Kalinowski, W. M. Boyce, and P. W. Hedrick. 2000. Genetic variation and population structure in desert bighorn sheep: implications for conservation. Conserv. Genet. 1:3-15.
33. Gutierrez-Espeleta, G. A., P. W. Hedrick, S. T. Kalinowski, D. Garrigan, and W. M. Boyce. 2001. Is the decline of desert bighorn sheep from infectious disease the result of low MHC variation? Heredity 86:439-450.
34. Harding, R. M., S. M. Fullerton, R. C. Griffiths, J. Bond, M. J. Cox, J. A. Schneider, D. S. Moulin, and J. B. Clegg. 1997. Archaic African and Asian lineages in the genetic ancestry of modern humans. Am. J. Hum. Genet. 60:772-789.
35. Harris, H. 1966. Enzyme polymorphism in man. Proc. Roy. Soc. Lond. B 164:298-310.
36. Hedrick, P. W. 1999. Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53:313-318.
37. _. 2000. Genetics of populations. 2d ed. Jones and Bartlett, Boston, MA.
38. _. 2003. Estimation of relative fitnesses from relative risk data and the predicted future of hemoglobin alleles S and C. J. Evol. Biol. In press.
39. Hedrick, P. W., and F. L. Black. 1997. HLA and mate selection in humans: no evidence in South Amerindians. Am. J. Hum. Genet. 61:505-511.
40. Hedrick, P. W., and T. J. Kim. 2000. Genetics of complex polymorphisms: parasites and maintenance of the major histocompatibility complex variation. Pp. 204-234 in R. S. Singh and C. B. Krimbas, eds. Evolutionary genetics: from molecules to morphology. Cambridge Univ. Press, New York.
41. Hedrick, P. W., and G. Thomson. 1983. Evidence for balancing selection at HLA. Genetics 104:449-456.
42. Hedrick, P. W., M. Ginevan, and E. Ewing. 1976. Genetic polymorphism in heterogeneous environments. Annu. Rev. Ecol. Syst. 7:1-32.
43. Hedrick, P. W., W. Klitz, W. P. Robinson, M. K. Kuhner, and G. Thomson. 1991a. Evolutionary genetics of HLA. Pp. 248-271 in R. Selander, A. G. Clark and T. Whittam, eds. Evolution at the molecular level. Sinauer Assoc., Sunderland, MA.
44. Hedrick, P. W., T. S. Whittam, and P. Parham. 1991b. Heterozygosity at individual amino acid sites: extremely high levels for HLA-A and -B genes. Proc. Natl. Acad. Sci. USA 88:5897-5901.
45. Hedrick, P. W., K. M. Parker, E. L. Miller, and P. S. Miller. 1999. Major histocompatibility complex variation in the endangered Przewalski's horse. Genetics 152:1701-1710.
46. Hedrick, P. W., K. M. Parker, and R. N. Lee. 2001. Using microsatellite and MHC variation to identify species, ESUs, and MUs in the endangered Sonoran topminnow. Mol. Ecol. 10:1399-1412.
47. Hedrick, P. W., R. N. Lee, and D. Garrigan. 2002. Major histocompatibility complex variation in red wolves: evidence for common ancestry with coyotes and balancing selection. Mol. Ecol. 11:1905-1913.
48. Hill, A. V. S., C. E. M. Allsop, D. Kwiatdowski, N. M. Antsey, P. Twumasi, P. A. Rowe, S. Bennett, D. Brewster, A. J. McMichael, and B. M. Greenwood. 1991. Common West African HLA antigens are associated with protection from severe malaria. Nature 352:595-600.
49. Hollenbach, J. A., G. Thomson, K. Cao, M. Fernandez-Viña, H. A. Erlich, T. L. Bugawan, C. Winkler, M. Winter, and W. Klitz. 2001. HLA diversity, differentiation, and haplotype evolution in Mesoamerican natives. Hum. Immunol. 62:378-390.
50. Hughes, A. L. 1999. Adaptive evolution of genes and genomes. Oxford Univ. Press, New York.
51. Hughes, A. L., and M. Nei. 1988. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335:167-170.
52. _. 1989. Nucleotide substitution at major histocompatibility complex II loci: evidence for overdominant selection. Proc. Natl. Acad. Sci. USA 86:958-962.
53. Huttley, G. A., M. W. Smith, M. Carrington, and S. J. O'Brien. 1999. A scan for linkage disequilibrium across the human genome. Genetics 152:1711-1722.
54. Ioerger, T. R., A. G. Clark, and T.-H. Kao. 1990. Polymorphism at the self-incompatibility locus in Solanaceae predates speciation. Proc. Natl. Acad. Sci. USA 87:9732-9735.
55. Jacob, S., M. K. McClintick, B. Zelano, and C. Ober. 2002. Paternally inherited HLA alleles are associated with women's choice of male odor. Nat. Genet. 30:175-179.
56. Jin, L., and R. Chakraborty. 1995. Population structure, stepwise mutations, heterozygote deficiency and their implications in DNA forensics. Heredity 74:274-285.
57. Jukes, T. H., and C. R. Cantor. 1969. Evolution of protein molecules. Pp. 21-132 in H. N. Munro, ed. Mammalian protein metabolism. Academic Press, New York.
58. Kaufman, J., S. Milne, T. W. F. Gobel, B. A. Walker, J. P. Jacob, C. Auffray, R. Zoorob, and S. Beck. 1999. The chicken B locus in a minimal essential MHC. Nature 401:923-925.
59. Kimura, M. 1957. Some problems of stochastic processes in genetics. Ann. Math. Stat. 28:882-901.
60. _. 1968. Evolutionary rate at the molecular level. Nature 217:624-626.
61. _. 1983. The neutral theory of molecular evolution. Cambridge Univ. Press, Cambridge, U.K.
62. Kimura, M., and J. F. Crow. 1964. The number of alleles that can be maintained in a finite population. Genetics 49:725-738.
63. Kimura, M., and T. Ohta. 1969. The average number of generations until fixation of a mutant gene in a finite population. Genetics 61:763-771.
64. Klein, J. 1980. Generation of diversity at MHC loci: implications for T-cell receptor repertoires. Pp. 239-253 in M. Fougereau and J. Dausset, eds. Immunology 80. Academic Press, London.
65. Klitz, W., and G. Thomson. 1987. Disequilibrium pattern analysis. II. Application to Danish HLA A and B locus data. Genetics 116:633-643.
66. Kojima, K. 1971. Is there a constant fitness for a given genotype? No! Evolution 25:281-285.
67. Kreitman, M. 1996. The neutral theory is dead. Long live the neutral theory. Bioessays 18:678-683.
68. Kumar, S., and S. B. Hedges. 1998. A molecular timescale for vertebrate evolution. Nature 392:917-920.
69. Kumar, S., K. Tamura, I. B. Jakobsen, and M. Nei. 2001. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244-1245.
70. Landry, C., and L. Bernatchez. 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. 10:2525-2539.
71. Landry, C., D. Garant, P. Duchesne, and L. Bernatchez. 2001. "Good genes as heterozygosity": the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proc. R. Soc. Lond. B 268:1279-1285.
72. Lewontin, R. C., and J. L. Hubby. 1966. A molecular approach to the study of genic heterozygosity in natural populations. II. Amount of variation and the degree of heterozygosity in natural populations of Drosophila pseudoobscura. Genetics 54:595-609.
73. Madden, D. R. 1995. The three-dimensional structure of peptide-MHC complexes. Annu. Rev. Immunol. 13:587-622.
74. Markow, T. A., P. W. Hedrick, K. Zuerlein, J. F. Martin, T. Vyvial, and C. Armstrong. 1993. HLA polymorphism in the Havasupai: evidence for balancing selection. Am. J. Hum. Genet. 53:943-952.
75. McDonald, J. H., and M. Kreitman. 1991, Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652-654.
76. Middleton, D., F. Williams, A. Meenagh, A. S. Daar, C. Gorodezky, M. Hammond, E. Nascimento, I. Briceno, and M. P. Perez. 2000. Analysis of the distribution of HLA-A alleles in populations from five continents. Hum. Immunol. 61:1048-1052.
77. Miller, K. M., K. H. Kaukinen, T. D. Beacham, and R. E. Withler. 2001. Geographic heterogeneity in natural selection on an MHC locus in sockeye salmon. Genetica 111:237-257.
78. Modiano, D., G. Luoni, B. S. Sirima, J. Simpore, F. Verra, A. Konate, E. Rastrelli, A. Olivieri, C. Calissano, G. M. Paganotti, L. D'Urbano, I. Sanou, A. Sawadogo, G. Modiano, and M. Coluzzi. 2001. Haemoglobin C protects against clinical Plasmodium falciparum malaria. Nature 414:305-308.
79. Nei, M. 1987. Molecular evolutionary genetics. Columbia Univ. Press, New York.
80. Nei, M., and T. Gojobori. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3:418-426.
81. Nei, M., and S. Kumar. 2000. Molecular evolution and phylogenetics. Oxford Univ. Press, New York.
82. Ober, C., S. Elias, D. D. Kostyu, and W. W. Hauck. 1992. Decreased fecundability in Hutterite couples sharing HLA-DR. Am. J. Hum. Genet. 50:6-14.
83. Paterson, S. 1998. Evidence for balancing selection at the major histocompatibility complex in a free-living ruminant. J. Hered. 89:289-294.
84. Paterson, S., and J. M. Pemberton. 1998. No evidence for major histocompatibility complex-dependent mating patterns in a free-living ruminant population. Proc. R. Soc. Lond. B 264:1813-1819.
85. Paterson, S., K. Wilson, and J. M. Pemberton. 1998. Major histocompatibility complex variation associated with juvenille survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Proc. Natl. Acad. Sci. USA 95:3714-2719.
86. Penn, D. J. 2002. The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108:1-21.
87. Penn, D. J., and W. K. Potts. 1999. The evolution of mating preferences and major histocompatibility complex genes. Am. Nat. 153:145-164.
88. Potts, W. K., C. J. Manning, and E. K. Wakeland. 1991. Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature 352:619-621.
89. Reusch, T. B. H., M. A. Häberli, B. Aeschlimann, and M. Milinski. 2001. Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414:300-302.
90. Robinson, J., M. J. Waller, P. Parham, J. G. Bodmer, and S. G. E. Marsh. 2001. IMGT/HLA database-a sequence database for the human major histocompatibility complex. Nucleic Acids Res. 29:210-213.
91. Salamon, H., W. Klitz, S. Easteal, X. Gao, H. A. Erlich, M. Fernandez-Viña, E. A. Trachtenberg, S. K. McWeeney, M. P. Nelson, and G. Thomson. 1999. Evolution of HLA class II molecules: allelic and amino acid site variability across populations. Genetics 152:393-400.
92. Sato, A., F. Figueroa, B. W. Murray, E. Malaga-Trillo, Z. Zaleska-Rutczynska, H. Sultmann, S. Toyosawa, C. Wedekind, N. Steck, and J. Klein. 2000. Nonlinkage of major histocompatibility complex class I and class II loci in bony fishes. Immunogenetics 51:108-116.
93. Satta, Y., Y.-J. Li, and N. Takahata. 1998. The neutral theory and natural selection in the HLA region. Front. Biosci. 3:459-467.
94. Satta, Y., C. O'hUigin, N. Takahata, and J. Klein. 1994. Intensity of natural selection at the major histocompatibility complex loci. Proc. Natl. Acad. Sci. USA 91:7184-7188.
95. Simonsen, K. L., G. A. Churchill, and C. F. Aquadro. 1995. Properties of statistical tests of neutrality for DNA polymorphism data. Genetics 141:413-429.
96. Tajima, F. 1983. Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437-460.
97. _. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
98. Takahata, N. 1990. A simple genealogical structure of strongly balanced allelic lines and trans-species evolution of polymorphism. Proc. Natl. Acad. Sci. USA 87:2419-2423.
99. Takahata, N., and Y. Satta. 1998. Selection, convergence, and intragenic recombination in HLA diversity. Genetica 102/ 103:157-169.
100. Tavaré, S. 1984. Line-of-descent and genealogical processes, and their applications in population genetics models. Theor. Popul. Biol. 26:119-164.
101. The MHC Sequencing Consortium. 1999. Complete sequence and gene map of a human major histocompatibility complex. Nature 401:921-923.
102. Thurz, M. R., H. C. Thomas, B. M. Greenwood, and A. V. S. Hill. 1997. Heterozygote advantage for HLA class II type in hepatitis B virus infection. Nat. Genet. 17:11-12.
103. Tormo, J., K. Natarjan, D. H. Margulies, and R. A. Marluzza. 1999. Crystal structure of a lectin-like natural killer cell receptor bound to its MHC class I ligand. Nature 402:623-631.
104. Valdes, A. M., S. K. McWeeney, D. Meyer, M. P. Nelson, and G. Thomson. 1999. Locus and population specific evolution of HLA class II genes. Ann. Hum. Genet. 63:27-43.
105. van Haeringen, W. A., P. S. Gwakisa, S. Mikko, E. Eythorsdottir, L. E. Holm, I. Olsaker, P. Outteridge, and L. Andersson. 1999. Heterozygote excess at the cattle DRB locus revealed by large scale genotyping of two closely linked microsatellites. Anim. Genet. 30:169-176.
106. Verrelli, B. C., J. H. Mc Donald, G. Argyropoulos, G. Destro-Bisol, A. Froment, A. Drousiotou, G. Lefranc, A. N. Helal, J. Loiselet, and S. A. Tishkoff. 2002. Evidence for balancing selection from nucleotide sequence analysis of human G6PD. Am. J. Hum. Genet. 71:1112-1128.
107. Watterson, G. A. 1975. On the number of segregting sites in genetical models without recombination. Theor. Popul. Biol. 7:256-276.
108. _. 1978. The homozygosity test of neutrality. Genetics 88:405-417.
109. _. 1986. The homozygosity test after a change in population size. Genetics 112:899-907.
110. Yamazaki, K., E. A. Boyse, V. Mike, H. T. Thaler, B. J. Mathieson, J. Abbott, J. Boyse, and Z. A. Zayas. 1976. Control of mating preferences in mice by genes in the major histocompatibility complex. J. Exp. Med. 144:1324-1335.
111. Yang, Z. 1998. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol. Biol. Evol. 15:568-573.
112. Zhang, J., S. Kumar, and M. Nei. 1997. Small-sample tests of episodic adaptive evolution: a case study of primate lysozymes. Mol. Biol. Evol. 14:1335-1338.
113. Zhang, J., H. F. Rosenberg, and M. Nei. 1998. Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc. Natl. Acad. Sci. USA 95:3708-3713.