A new theory of MHC evolution: Beyond selection on the immune genes

Proceedings of the Royal Society B: Biological Sciences

Volumn 276, Issue 1657, 2009, Pages 657-665

  Van Oosterhout, Cock ^a  

^a UNIVERSITY OF HULL   (United Kingdom)

Author keywords

Balancing selection; Disease associations; Human leucocyte antigen; Linkage disequilibrium; Major histocompatibility complex; Plant self incompatibility loci (S loci)

Indexed keywords

ALLELE; DOMINANCE; EVOLUTION; MAJOR HISTOCOMPATIBILITY COMPLEX; MUTATION; POLYMORPHISM; POPULATION GENETICS; RECOMBINATION;

EID: 58249101033     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2008.1299     Document Type: Article

References (55)

1. Aguilar, A., Roemer, G., Debenham, S., Binns, M., Garcelon, D. & Wayne, R. K. 2004 High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc. Natl Acad. Sci. USA 101, 3490-3494.
2. Bell, G. 1982 The masterpiece of nature: the evolution and genetics of sexuality. Berkeley, CA: University of California Press.
3. Bernatchez, L. & Landry, C. 2003MHCstudies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J. Evol. Biol. 16, 363-377.
4. Bos, D. H. &Waldman, B. 2006 Evolution by recombination and transspecies polymorphism in the MHC class I gene of Xenopus laevis. Mol. Biol. Evol. 23, 137-143.
5. Charlesworth, D., Kamau, E., Hagenblad, J. & Tang, C. L. 2006 Trans-specificity at loci near the self-incompatibility loci in Arabidopsis. Genetics 172, 2699-2704.
6. Chen, J.-M., Cooper, D. N., Chuzhanova, N., Férec, C. & Patrinos, G. P. 2007 Gene conversion: mechanisms, evolution and human disease. Nat. Rev. Genet. 8, 762-775.
7. Clarke, B. C. & Kirby, D. R. S. 1966 Maintenance of histocompatibility polymorphism. Nature 211, 999-1000.
8. Crow, J. F. & Kimura, M. 1970 An introduction to population genetics theory. New York, NY: Harper & Row Publishers.
9. Dawkins, R., Leelayuwat, C., Gaudieri, S., Tay, G., Hui, J., Cattley, S., Martinez, P. & Kulski, J. 1999 Genomics of the major histocompatibility complex: haplotypes, duplication, retroviruses and disease. Immunol. Rev. 167, 275-304.
10. de Bakker, P. I. W. et al. 2006 A high resolution HLA and SNP haplotype map for disease association studies in the extended human MHC. Nat. Genet. 38, 1166-1172.
11. de Boer, R. J., Borghans, J. A. M., Van Boven, M., Keşmir, C. & Weissing, F. J. 2004 Heterozygote advantage fails to explain the high degree of polymorphism of the MHC. Immunogenetics 55, 725-731.
12. Doherty, P. C. & Zinkernagel, R. M. 1975 Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256, 50-52.
13. Dorak, M. T., Lawson, T., Machulla, K. G., Mills, K. I. & Burnett, A. K. 2002 Increased heterozygosity for MHC class II lineages in newborn males. Genes Immun. 3, 263-269.
14. Gaya, D. R., Russell, R. K., Nimmo, E. R. & Satsangi, J. 2006 New genes in inflammatory bowel disease: lessons from complex diseases? Lancet 367, 1271-1284.
15. Gregersen, J. W., Kranc, K. R., Ke, X., Svendsen, P., Madsen, L. S., Thomsen, A. R., Cardon, L. R., Bell, J. I. & Fugger, L. 2006 Functional epistasis on a common MHC haplotype associated with multiple sclerosis. Nature 443, 574-577.
16. Haddrill, P. R., Halligan, D. L., Tomaras, D. & Charlesworth, B. 2007 Reduced efficacy of selection in regions of the Drosophila genome that lack crossing over. Genome Biol. 8, R18.
17. Hedrick, P. W. 1999 Highly variable loci and their interpretations in evolution and conservation. Evolution 53, 313-318.
18. Kaufman, J., Milne, S., Gobel, T. W. F., Walker, B. A., Jacob, J. P., Auffray, C., Zoorob, R. & Beck, S. 1999 The chicken B locus is a minimal essential major histocompatibility complex. Nature 401, 923-925.
19. Klein, J., Satta, Y., Takahata, N. & O'hUigin, C. 1993 Transspecies MHC polymorphisms and the origin of species in primates. J. Med. Primatol. 22, 57-64.
20. Little, J. T. 2002 The evolutionary significance of parasitism: do parasite-driven genetic dynamics occur ex silico? J. Evol. Biol. 15, 1-9.
21. Kelley, J., Walter, L. & Trowsdale, J. 2005 Comparative genomics of major histocompatibility complexes. Immunogenetics 56, 683-695.
22. Kennedy, L. J., Davison, L. J., Barnes, A., Short, A. D., Fretwell, N., Jones, C. A., Lee, A. C., Ollier, W. E. & Catchpole, B. 2006 Identification of susceptibility and protective major histocompatibility complex haplotypes in canine diabetes mellitus. Tissue Antig. 68, 467-476.
23. Kennedy, L. J. et al. 2008 Risk of anal furunculosis in German Shepherd dogs is associated with the major histocompatibility complex. Tissue Antig. 71, 51-56.
24. Kuroda, N., Figueroa, F., O'hUigin, C. & Klein, J. 2002 Evidence that the separation of MHC class II from class I loci in the zebrafish, Danio rerio, occurred by translocation. Immunogenetics 54, 418-430.
25. Lynch, M. & Walsh, B. 1998 Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer.
26. Mangalam, A. K., Rajagopalan, G., Taneja, V. & David, C. S. 2008 HLA class II transgenic mice mimic human inflammatory diseases. Adv. Immunol. 97, 65-147.
27. May, G., Shaw, F., Badrane, H. & Vekemans, X. 1999 The signature of balancing selection: fungal mating compatibility gene evolution. Proc. Natl Acad. Sci. USA 96, 9172-9177.
28. Muirhead, C. A. 2001 Consequences of population structure on genes under balancing selection. Evolution 55, 1532-1541.
29. Muller, H. J. 1932 Some genetic aspects of sex. Am. Nat. 66, 118-138.
30. Nei, M. & Rooney, A. P. 2005 Concerted and birth-and-death evolution of multigene families. Annu. Rev. Genet. 39, 121-152.
31. Ohta, T. 1989 The mutational load of a multigene family with uniform members. Genet. Res. 53, 141-145.
32. Okamoto, K. et al. 2003 Identification of I kappa BL as the second major histocompatibility complex-linked susceptibility locus for rheumatoid arthritis. Am. J. Hum. Genet. 72, 303-312.
33. Palti, Y., Rodriguez, M. F., Gahr, S. A. & Hansen, J. D. 2007 Evolutionary history of the ABCB2 genomic region in teleosts. Dev. Comp. Immunol. 31, 483-498.
34. Piertney, S. B. & Oliver, M. K. 2006 The evolutionary ecology of the major histocompatibility complex. Heredity 96, 7-21.
35. Raymond, C. K. et al. 2005 Ancient haplotypes of the HLA class II region. Genome Res. 15, 1250-1257.
36. Richman, A. 2000 Evolution of balanced genetic polymorphism. Mol. Ecol. 9, 1953-1963.
37. Richman, A. D., Herrera, L. G. & Nash, D. 2001 MHC class II beta sequence diversity in the deer mouse (Peromyscus maniculatus): implications for models of balancing selection. Mol. Ecol. 10, 2765-2773.
38. Richman, A. D., Herrera, L. G., Nash, D. & Schierup, M. H. 2003 Relative roles of mutation and recombination in generating allelic polymorphism at an MHC class II locus in Peromyscus maniculatus. Genet. Res. Camb. 82, 89-99.
39. She, J. X., Wakeland, E. K. & Boehme, S. 1990 The generation and maintenance of MHC class II gene polymorphism in rodents. Immunol. Rev. 113, 207-226.
40. Shiina, T. et al. 2006 Rapid evolution of major histocompatibility complex class I genes in primates generates new disease alleles in humans via hitchhiking diversity. Genetics 173, 1555-1570.
41. Stenzel, A., Lu, T., Koch, W. A., Hampe, J., Guenther, S. M., De La Vega, F. M., Krawczak, M. & Schreiber, S. 2004 Patterns of linkage disequilibrium in the MHC region on human chromosome 6p. Hum. Genet. 114, 377-385.
42. Stone, J. L. 2004 Sheltered load associated with S-alleles in Solanum carolinense. Heredity 92, 335-342.
43. 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.
44. Takahata, N. 1993 Allelic genealogy and human evolution. Mol. Biol. Evol. 10, 2-22.
45. Takahata, N. & Nei, M. 1990 Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics 124, 967-978.
46. Uyenoyama, M. K. 1997 Genealogical structure among alleles regulating self-incompatibility in natural populations of flowering plants. Genetics 147, 1389-1400.
47. Uyenoyama, M. K. 2003 Genealogy-dependent variation in viability among self-incompatibility genotypes. Theor. Popul. Biol. 63, 281-293.
48. Uyenoyama, M. K. 2005 Evolution under tight linkage to mating type. New Phytol. 165, 63-70.
49. van Oosterhout, C., Joyce, D. A., Cummings, S. M., Blais, J., Barson, N. J. & Cable, J. 2006 Balancing selection, random genetic drift and genetic variation at the major histocompatibility complex (MHC) in two wild populations of guppies (Poecilia reticulata). Evolution 60, 2562-2574.
50. van Oosterhout, C., Mohammed, R. S., Hansen, H., Archard, G. A., McMullan, M., Weese, D. J. & Cable, J. 2007a Selection by parasites in spate conditions in wild Trinidadian guppies (Poecilia reticulata). Int. J. Parasitol. 37, 805-812.
51. van Oosterhout, C., Smith, A. M., Hänfling, B., Ramnarine, I. W., Mohammed, R. S. & Cable, J. 2007b The guppy as a conservation model: implications of parasitism and inbreeding for reintroduction success. Conserv. Biol. 21, 1573-1583.
52. Vekemans, X. & Slatkin, M. 1994 Gene and allelic genealogies at a gametophytic self-incompatibility locus. Genetics 137, 1157-1165.
53. Wakeland, E. K., Boehme, S., She, J. X., Lu, C. C., McIndoe, R. A., Cheng, I., Ye, Y. & Potts, W. K. 1990 Ancestral polymorphisms of MHC class II genes: divergent allele advantage. Immunol. Res. 9, 115-122.
54. Westerdahl, H., Hansson, B., Bensch, S. & Hasselquist, D. 2004 Between-year variation of MHC allele frequencies in great reed warblers: selection or drift? J. Evol. Biol. 17, 485-492.
55. Woolhouse, M. E. J., Webster, J. P., Domingo, E., Charlesworth, B. & Levin, B. R. 2002 Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat. Genet. 32, 569-577.