Multiple parasites are driving major histocompatibility complex polymorphism in the wild

Journal of Evolutionary Biology

Volumn 16, Issue 2, 2003, Pages 224-232

  Wegner, K Mathias ^a   Reusch, T B H ^a   Kalbe, M ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY BIOLOGY   (Germany)

Author keywords

Balancing selection; Major histocompatibility complex (MHC); Multiple infections; Parasite induced selection; Polymorphism; Three spined stickleback (Gasterosteus aculeatus)

Indexed keywords

FRESH WATER; MICROSATELLITE DNA;

ANTIPARASITE DEFENSE; FISH; IMMUNOCOMPETENCE; PARASITE; PARASITE PREVALENCE; POLYMORPHISM; SELECTION;

ANIMAL; ARTICLE; COMPARATIVE STUDY; GENE FREQUENCY; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETICS; GERMANY; IMMUNOCOMPETENCE; IMMUNOLOGY; MAJOR HISTOCOMPATIBILITY COMPLEX; PARASITOLOGY; SMEGMAMORPHA;

ANIMALS; FRESH WATER; GENE FREQUENCY; GERMANY; IMMUNOCOMPETENCE; MAJOR HISTOCOMPATIBILITY COMPLEX; MICROSATELLITE REPEATS; POLYMORPHISM, GENETIC; SELECTION (GENETICS); SMEGMAMORPHA;

ANIMALIA; GASTEROSTEUS; GASTEROSTEUS ACULEATUS; SMEGMAMORPHA;

EID: 0037371150     PISSN: 1010061X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1420-9101.2003.00519.x     Document Type: Article

References (43)

1. Apanius, V., Penn, D., Slev, P.R., Ruff, L.R. & Potts, W.K. 1997. The nature of selection on the major histocompatibility complex. Crit. Rev. Immunol. 17: 179-224.
2. Binz, T., Reusch, T.B.H., Wedekind, C. & Milinski, M. 2001. SSCP analysis of Mhc class IIB genes in the three spined stickleback, Gasterosteus aculeatus. J. Fish Biol. 58: 887-890.
3. Boyce, W.M., Hedrick, P.W., Muggli-Cockett, N.E., Kalinowski, S., Penedo, M.C.T. & Ramey, R.R.I. 1997. Genetic variation of major histocompatibility complex and microsatellite loci: a comparison in bighorn sheep. Genetics 145: 421-433.
4. DeWoody, J.A. & Avise, J.C. 2000. Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J. Fish Biol. 56: 461-473.
5. Doherty, P.C. & Zinkernagel, R.M. 1975. Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256: 52.
6. Godot, V., Harraga, S., Beurton, I., Tiberghien, P., Sarciron, E., Gottstein, B. & Vuitton, D.A. 2000. Resistance/susceptibility to Echinococcus multilocularis infection and cytokine profile in humans. II. Influence of the HLA B8, DR3, DQ2 haplotype. Clin. Exp. Immunol. 121: 491-498.
7. Gutierrez-Espeleta, G.A., Hedrick, P.W., Kalinowski, S., Garrigan, D. & Boyce, W.M. 2001. Is the decline of desert bighorn sheep from infectious disease the result of low MHC variation? Heredity 86: 439-450.
8. Hamilton, W.D. & Zuk, M. 1982. Heritable true fitness and bright birds - a role for parasites. Science 218: 384-387.
9. Hedrick, P.W., Parker, K.M. & Lee, R.N. 2001. Using microsatellite and MHC variation to identify species, ESUs, ans MUs in the endangered Sonoran topminnows. Mol. Ecol. 10: 1399-1412.
10. Hill, A.V.S., Allsopp, C.E.M., Kwiatkowski, D., Anstey, N.M., Twumasi, P., Rowe, P.A., Bennet, S., Brewster, D., McMichad, A.J. & Greenwood, B.M. 1991. Common West African HLA antigens are associated with protection from severe malaria. Nature 352: 595-600.
11. Hughes, A.L. 1999. Adaptive Evolution of Genes and Genomes. Oxford University Press, Oxford.
12. Hughes, A.L. & Nei, M. 1988. Patterns of nucleotide substiution at MHC class loci reveals overdominant selection. Nature 335: 167-170.
13. Hughes, A.L. & Yeager, M. 1998. Natural selection at major histocompatibility complex loci of vertebrates. Annu. Rev. General 32: 415-435.
14. Kalbe, M., Wegner, K.M. & Reusch, T.B.H. 2002. Dispersion patterns of parasites in 0+ three-spined sticklebacks: a cross population comparison. J. Fish Biol. 60: 1529-1542.
15. Kaufman, J. & Salomonsen, J. 1997. The 'Minimal Essential MHC' revisited: both peptide-binding and cell surface expression level of MHC molecules are polymorphisms selected by pathogens in chickens. Hereditas 127: 67-73.
16. Kimura, M. 1983. The Neutral Theory of Molecular Evolution. Cambridge University Press, Cambridge.
17. Klein, J. 1986. Natural History of the Major Histocompatibility Complex. Wiley, New York.
18. Langefors, Å., von Schantz, T. & Widegren, B. 1998. Allelic variation of MHC class II in Atlantic Salmon; a population genetic analysis. Heredity 80: 568-575.
19. Langefors, Å., Lohm, J., Grahn, M., Andersen, Ö. & von Schantz, T. 2001. Association between major histocompatibility complex class IIB alleles and resistance to Aeromonas salmonicida in Atlantic salmon. Proc. R. Soc. Lond. B Biol. Sci. 268: 479-485.
20. Largiader, C., Fries, V., Kobler, B. & Bakker, C.M. 1999. Isolation and characterization of microsatellite loci from the three-spined stickleback, Gasterosteus aculeatus. Mol. Ecol. 8: 342-344.
21. Málaga-Trillo, E., Zaleska-Rutczynska, Z., McAndrew, B., Vincek, V., Figueroa, F., Sültmann, H. & Klein, J. 1998. Linkage relationships and haplotype polymorphism among cichlid Mhc Class IIB loci. Genetics 149: 1527-1537.
22. Mason, D. 2001. Some quantitative aspects of T-cell repertoire selection: the requirement for regulatory T cells. Immunol. Rev. 182: 80-88.
23. McClelland, E.E., Penn, D., Fujinami, R.S. & Potts, W.K. 2000. MHC heterozygote advantage under coinfection with Salmonella and Theiler's virus. Faseb J. 14: A1054-A1054.
24. McConnell, T.J., Godwin, U.B. & Cuthbertson, B.J. 1998. Expressed major histocompatibility complex class II loci in fishes. Immunol. Rev. 166: 294-300.
25. Meyer, D. & Thomson, G. 2001. How selection shapes variation of the human major histocompatibility complex: a review. Ann. Hum. Genet. 65: 1-26.
26. Milinski, M. & Bakker, T.C.M. 1990. Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344: 330-333.
27. Nei, M., Maruyama, T. & Chakraborty, R. 1975. The bottleneck effect and genetic variability in populations. Evolution 29: 1-10.
28. Nowak, M.A., Tarczy-Hornoch, K. & Austy, J.M. 1992. The optimal number of major histocompatibility complex molecules in an individual. Proc. Natl. Acad. Sci. U.S.A. 89: 10896-10899.
29. Ohta, T. 1998. On the pattern of polymorphisms at major histocompatibility complex loci. J. Mol. Evol. 46: 633-638.
30. Parsons, P.A. & Bodmer, W.F. 1961. Evolution of overdominance - natural selection and heterozygote advantage. Nature 190: 7-12.
31. Paterson, S., Wilson, K. & Pemberton, J.M. 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. U.S.A. 86: 3714-3719.
32. Penn, D.J., Damjanovich, K. & Potts, W.K. 2002. MHC heterozygosity confers a selective advantage against multiple-strain infections. Proc. Natl. Acad. Sci. U.S.A. 99: 11260-11264.
33. Peters, A.D. & Lively, C.M. 1999. The red queen and fluctuating epistasis: a population genetic analysis of antagonistic coevolution. Am. Nat. 154: 393-405.
34. Reusch, T.B.H., Aeschlimann, P.B., Häberli, M.A. & Milinski, M. 2001a. Female sticklebacks count alleles in a strategy of sexual selection explaining MHC-polymorphism. Nature 414: 300-302.
35. Reusch, T.B.H., Wegner, K.M. & Kalbe, M. 2001b. Rapid genetic divergence in postglacial populations of threespine stickleback (Gasterosteus aculeatus): the role of habitat type, drainage, and geographic proximity. Mol. Ecol. 10: 2435-2446.
36. Sato, A., Figueroa, F., O'hUigin, C., Steck, N. & Klein, J. 1998. Cloning of major histocompatibility complex (Mhc) genes from threespine stickleback, (Gaserosteus aculeatus). Mol. Mar. Biol. Biotechnol. 7: 221-231.
37. Schluter, D. 1996. Ecological causes of adaptive radiation. Am. Nat. 148: S40-S64.
38. Shaw, D.J., Grenfell, B.T. & A.P. 1998. Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117: 597-610.
39. Swarbrick, P.A. & Crawford, A.M. 1997. The red deer (Cervus elaphus) contains two expressed major histocompatibility complex class II DQB genes. Anim. Genet. 28: 49-51.
40. Thursz, M.R., Kwiatkowski, D., Allsopp, C.E.M, Greenwood, B.M., Thomas, H.C. & Hill, A.V.S. 1995. Association between an MHC class II allele and clearance of hepatitis B virus in Gambia. N. Eng. J. Med. 332: 1065-1069.
41. Van Valen, L. 1965. Morphological variation and width of ecological niche. Am. Nat. 99: 377-390.
42. Van Valen, L. 1973. A new evolutionary law. Evol Theo. 1: 1-30.
43. Windsor, D.A. 1998. Most of the species on earth are parasites. Int. J. Parasitol. 28: 1939-1941.