MHC Signaling during Social Communication

  • James S. Ruff
  • Adam C. Nelson
  • Jason L. Kubinak
  • Wayne K. Potts
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 738)

Abstract

The major histocompatibility complex (MHC) has been known to play a critical role in immune recognition since the 1950s. It was a surprise, then, in the 1970s when the first report appeared indicating MHC might also function in social signaling. Since this seminal discovery, MHC signaling has been found throughout vertebrates and its known functions have expanded beyond mate choice to include a suite of behaviors from kin-biased cooperation, parent-progeny recognition to pregnancy block. The widespread occurrence of MHC in social signaling has revealed conserved behavioral-genetic mechanisms that span vertebrates and includes humans. The identity of the signal’s chemical constituents and the receptors responsible for the perception of the signal have remained elusive, but recent advances have enabled the identification of the key components of the behavioral circuit. In this chapter we organize recent findings from the literature and discuss them in relation to four nonmutually exclusive models wherein MHC functions as a signal of (i) individuality, (ii) relatedness, (iii) genetic compatibility and (iv) quality. We also synthesize current mechanistic studies, showing how knowledge about the molecular basis of MHC signaling can lead to elegant and informative experimental manipulations. Finally, we discuss current evidence relating to the primordial functions of the MHC, including the possibility that its role in social signaling may be ancestral to its central role in adaptive immunity.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Manning CJ, Wakeland EK, Potts WK. Communal nesting patterns in mice implicate MHC genes in kin recognition. Nature 1992; 360:581–583.PubMedCrossRefGoogle Scholar
  2. 2.
    Yamazaki K, Boyse EA, Mike V et al. Control of mating preferences in mice by genes in the major histocompatibility complex. J Exp Med 1976; 144:1324–1335.PubMedCrossRefGoogle Scholar
  3. 3.
    Snell GD. Methods for the study of histocompatibility genes. J Genet 1948; 49:87–108.PubMedCrossRefGoogle Scholar
  4. 4.
    Piertney SB, Oliver MK. The evolutionary ecology of the major histocompatibility complex. Heredity 2006; 96:7–21.PubMedGoogle Scholar
  5. 5.
    Yamaguchi M, Yamazaki K, Beauchamp GK et al. Distinctive urinary odors governed by the major histocompatibility locus of the mouse. Proc Natl Acad Sci 1981; 78:5817–5820.PubMedCrossRefGoogle Scholar
  6. 6.
    Singh PB, Brown RE, Roser B. MHC antigens in urine as olfactory recognition cues. Nature 1987; 327:161–164.PubMedCrossRefGoogle Scholar
  7. 7.
    Leinders-Zufall T, Brennan P, Widmayer P et al. MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 2004; 306:1033–1037.PubMedCrossRefGoogle Scholar
  8. 8.
    Spehr M, Kelliher KR, Li XH et al. Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. J Neurosci 2006; 26:1961–1970.PubMedCrossRefGoogle Scholar
  9. 9.
    Murphy KP, Travers P, Janeway C et al. Immunobiology. New York: Garland Science, 2008.Google Scholar
  10. 10.
    Boehm T, Zufall F. MHC peptides and the sensory evaluation of genotype. Trends Neurosci 2006; 29:100–107.PubMedCrossRefGoogle Scholar
  11. 11.
    Spehr M, Spehr J, Ukhanov K et al. Parallel processing of social signals by the mammalian main and accessory olfactory systems. Cell Mol Life Sci 2006; 63:1476–1484.PubMedCrossRefGoogle Scholar
  12. 12.
    Kelliher KR, Spehr M, Li XH et al. Pheromonal recognition memory induced by TRPC2-independent vomeronasal sensing. Euro J Neuroscience 2006; 23:3385–3390.CrossRefGoogle Scholar
  13. 13.
    Kelliher KR, Spehr M, Li XH et al. Relative roles of the main and accessory olfactory systems in behavioral responses to MHC class I peptides: Bruce effect. Chem Senses 2005; 30:A18.Google Scholar
  14. 14.
    Milinski M, Griffiths S, Wegner KM et al. Mate choice decisions of stickleback females predictably modified by MHC peptide ligands. Proc Natl Acad Sci USA 2005; 102:4414–4418.PubMedCrossRefGoogle Scholar
  15. 15.
    Singer AG, Beauchamp GK, Yamazaki K. Volatile signals of the major histocompatibility complex in male mouse urine. Proc Natl Acad Sci USA 1997; 94:2210–2214.PubMedCrossRefGoogle Scholar
  16. 16.
    Willse A, Belcher AM, Preti G et al. Identification of major histocompatibility complex-regulated body odorants by statistical analysis of a comparative gas chromatography/mass spectrometry experiment. Anal Chem 2005; 77:2348–2361.PubMedCrossRefGoogle Scholar
  17. 17.
    Kwak J, Opiekun MC, Matsumura K et al. Major histocompatibility complex-regulated odortypes: peptide-free urinary volatile signals. Physiol Behav 2009; 96:184–188.PubMedCrossRefGoogle Scholar
  18. 18.
    Carroll LS, Penn DJ, Potts WK. Discrimination of MHC-derived odors by untrained mice is consistent with divergence in peptide-binding region residues. Proc Natl Acad Sci USA 2002; 99:2187–2192.PubMedCrossRefGoogle Scholar
  19. 19.
    Zelano B, Edwards SV. An Mhc component to kin recognition and mate choice in birds: Predictions, progress and prospects. Am Nat 2002; 160:S225–S237.PubMedCrossRefGoogle Scholar
  20. 20.
    Yamazaki K, Beauchamp GK, Kupniewski J et al. Familial imprinting determines H-2 selective mating preferences. Science 1988; 240:1331–1332.PubMedCrossRefGoogle Scholar
  21. 21.
    Yamazaki K, Beauchamp GK, Daisuke Y. Genetic Basis for MHC-Dependent Mate Choice. Adv Genet 2007; 59:129–145.PubMedCrossRefGoogle Scholar
  22. 22.
    Manning CJ, Wakeland EK, Potts WK. Communal nesting patterns in mice implicate MHC genes in kin recognition. Nature 1992b; 360:581–583.PubMedCrossRefGoogle Scholar
  23. 23.
    Jacek R, Aleksandra T, Agnieszka K. MHC and Preferences for Male Odour in the Bank Vole. Ethology 2008; 114:827–833.CrossRefGoogle Scholar
  24. 24.
    Sommer S. Major histocompatibility complex and mate choice in a monogamous rodent. Behav Ecol Sociobiol 2005; 58:181–189.CrossRefGoogle Scholar
  25. 25.
    Wedekind C, Seebeck T, Bettens F et al. MHC-dependent mate preferences in humans. Proc R Soc Lond B 1995; 260:245–249.CrossRefGoogle Scholar
  26. 26.
    Havlicek J, Roberts SC. MHC-correlated mate choice in humans: A review. Psychoneuroendocrinology 2009; 34:497–512.PubMedCrossRefGoogle Scholar
  27. 27.
    Setchell JM, Charpentier MJ, Abbott KM et al. Opposites attract: MHC-associated mate choice in a polygynous primate. J Evol Biol 2009; 23:136–148.PubMedCrossRefGoogle Scholar
  28. 28.
    Schwensow N, Fietz J, Dausmann K et al. MHC-associated mating strategies and the importance of overall genetic diversity in an obligate pair-living primate. Evol Ecol 2008; 22:617–636.CrossRefGoogle Scholar
  29. 29.
    Schwensow N, Eberle M, Sommer S. Compatibility counts: MHC-associated mate choice in a wild promiscuous primate. Proc R Soc Lond B Biol Sci 2008; 275:555–564.CrossRefGoogle Scholar
  30. 30.
    Paterson S, Pemberton JM. No evidence for major histocompatibility complex-dependent mating patterns in a free-living ruminant population. Proc R Soc Lond B 1997; 264:1813–1819.CrossRefGoogle Scholar
  31. 31.
    Freeman-Gallant CR, Meguerdichian M, Wheelwright NT et al. Social pairing and female mating fidelity predicted by restriction fragment length polymorphism similarity at the major histocompatibility complex in a songbird. Mol Ecol 2003; 12:3077–3083.PubMedCrossRefGoogle Scholar
  32. 32.
    Bonneaud C, Chastel O, Federici P et al. Complex Mhc-based mate choice in a wild passerine. Proc Biol Sci 2006; 273:1111–1116.PubMedCrossRefGoogle Scholar
  33. 33.
    Richardson DS, Komdeur J, Burke T et al. MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler. Proc Biol Sci 2005; 272:759–767.PubMedCrossRefGoogle Scholar
  34. 34.
    Westerdahl H. No evidence of an MHC-based female mating preference in great reed warblers. Molecular Ecology 2004; 13:2465–2470.PubMedCrossRefGoogle Scholar
  35. 35.
    Gillingham MAF, Richardson DS, Lovlie H et al. Cryptic preference for MHC-dissimilar females in male red junglefowl, Gallus gallus. Proc R Soc Lond B Biol Sci 2009; 276:1083–1092.CrossRefGoogle Scholar
  36. 36.
    Hale ML, Verduijn MH, Moller AP et al. Is the peacock’s train an honest signal of genetic quality at the major histocompatibility complex? J Evol Biol 2009; 22:1284–1294.PubMedCrossRefGoogle Scholar
  37. 37.
    Olsson M, Madsen T, Nordby J et al. Major histocompatibility complex and mate choice in sand lizards. Proc R Soc Lond B Biol Sci 2003; 270:S254–S256.CrossRefGoogle Scholar
  38. 38.
    Miller HC, Moore JA, Nelson NJ et al. Influence of major histocompatibility complex genotype on mating success in a free-ranging reptile population. Proc Biol Sci 2009; 276:1695–1704.PubMedCrossRefGoogle Scholar
  39. 39.
    Villinger J, Waldman B. Self-referent MHC type matching in frog tadpoles. Proc Biol Sci 2008; 275:1225–1230.PubMedCrossRefGoogle Scholar
  40. 40.
    Bos DH, Williams RN, Gopurenko D et al. Condition-dependent mate choice and a reproductive disadvantage for MHC-divergent male tiger salamanders. Molecular Ecology 2009; 18:3307–3315.PubMedCrossRefGoogle Scholar
  41. 41.
    Gerlach G, Hodgins-Davis A, MacDonald B et al. Benefits of kin association: related and familiar zebrafish larvae (Danio rerio) show improved growth. Behav Ecol Sociobiol 2007; 61:1765–1770.CrossRefGoogle Scholar
  42. 42.
    Gerlach G, Hodgins-Davis A, Avolio C et al. Kin recognition in zebrafish: a 24-hour window for olfactory imprinting. Proc Biol Sci 2008; 275:2165–2170.PubMedCrossRefGoogle Scholar
  43. 43.
    Aeschlimann PB, Haeberli MA, Reusch TBH et al. Female sticklebacks Gasterosteus aculeatus use self reference to optimize MHC allele number during mate selection. 2003; 54:119–126.Google Scholar
  44. 44.
    Reusch T, Haeberli MA, Aeschlimann PB et al. Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 2001; 414:300–302.PubMedCrossRefGoogle Scholar
  45. 45.
    Milinski M. The major histocompatibility complex, sexual selection and mate choice. Annu Rev Ecol Evol Syst 2006; 37:159–186.CrossRefGoogle Scholar
  46. 46.
    Rajakaruna RS, Brown JA, Kaukinen KH et al. Major histocompatibility complex and kin discrimination in Atlantic salmon and brook trout. Mol Ecol 2006; 15:4569–4575.PubMedCrossRefGoogle Scholar
  47. 47.
    Consuegra S, Garcia de Leaniz C. MHC-mediated mate choice increases parasite resistance in salmon. Proc Biol Sci 2008; 275:1397–1403.PubMedCrossRefGoogle Scholar
  48. 48.
    Neff BD, Garner SR, Heath JW et al. The MHC and nonrandom mating in a captive population of Chinook salmon. Heredity 2008; 101:175–185.PubMedCrossRefGoogle Scholar
  49. 49.
    Olsen KH, Grahn M, Lohm J. Influence of MHC on sibling discrimination in Arctic char, Salvelinus alpinus (L.). J Chem Ecol 2002; 28:783–795.PubMedCrossRefGoogle Scholar
  50. 50.
    Forsberg LA, Dannewitz J, Petersson E et al. Influence of genetic dissimilarity in the reproductive success and mate choice of brown trout—females fishing for optimal MHC dissimilarity. J Evol Biol 2007; 20:1859–1869.PubMedCrossRefGoogle Scholar
  51. 51.
    Wedekind C, Walker M, Portmann J et al. MHC-linked susceptibility to a bacterial infection, but no MHC-linked cryptic female choice in whitefish. J Evol Biol 2004; 17:11–18.PubMedCrossRefGoogle Scholar
  52. 52.
    Tibbetts EA, Dale J. Individual recognition: it is good to be different. Trends Ecol Evol 2007; 22:529–537.PubMedCrossRefGoogle Scholar
  53. 53.
    Singh PB. Chemosensation and genetic individuality. Reproduction 2001; 121:529–539.PubMedCrossRefGoogle Scholar
  54. 54.
    Thomas L. Symbiosis as an immunologic problem. The immune system and infectious diseases. In: Neter E, Milgrom F, eds. Fourth International Convocation of Immunology. Basel: S. Karger; 1975:2–11.Google Scholar
  55. 55.
    Tibbetts EA, Sheehan MJ, Dale J. A testable definition of individual recognition. Trends Ecol Evol 2008; 23:356–356.CrossRefGoogle Scholar
  56. 56.
    Novotny MV, Soini HA, Koyama S et al. Chemical identification of MHC-influenced volatile compounds in mouse urine. I: Quantitative proportions of major chemosignals. J Chem Ecol 2007; 33:417–434.PubMedCrossRefGoogle Scholar
  57. 57.
    Kwak J, Willse A, Matsumura K et al. Genetically-based olfactory signatures persist despite dietary variation. PLoS One 2008; 3:e3591.PubMedCrossRefGoogle Scholar
  58. 58.
    Schaefer ML, Young DA, Restrepo D. Olfactory fingerprints for major histocompatibility complex-determined body odors. J Neurosci 2001; 21:2481–2487.PubMedGoogle Scholar
  59. 59.
    Bruce HM. An exteroceptive block to pregnancy in the mouse. Nature 1959; 164:105.CrossRefGoogle Scholar
  60. 60.
    Brennan PA. Outstanding issues surrounding vomeronasal mechanisms of pregnancy block and individual recognition in mice. Behav Brain Res 2009; 200:287–294.PubMedCrossRefGoogle Scholar
  61. 61.
    Yamazaki K, Beauchamp GK, Wysocki CJ et al. Recognition of H-2 types in relation to the blocking of pregnancy in mice. Science 1983b; 221:186–188.PubMedCrossRefGoogle Scholar
  62. 62.
    Peele P, Salazar I, Mimmack M et al. Low molecular weight constituents of male mouse urine mediate the pregnancy block effect and convey information about the identity of the mating male. Eur J Neurosci 2003; 18:622–628.PubMedCrossRefGoogle Scholar
  63. 63.
    Thompson RN, McMillon R, Napier A et al. Pregnancy block by MHC class I peptides is mediated via the production of inositol 1,4,5-trisphosphate in the mouse vomeronasal organ. J Exp Biol 2007; 210:1406–1412.PubMedCrossRefGoogle Scholar
  64. 64.
    He J, Ma L, Kim S et al. Encoding gender and individual information in the mouse vomeronasal organ. Science 2008; 320:535–538.PubMedCrossRefGoogle Scholar
  65. 65.
    Slev PR, Nelson AC, Potts WK. Sensory neurons with MHC-like peptide binding properties: disease consequences. Curr Opin Immunol 2006; 18:608–616.PubMedCrossRefGoogle Scholar
  66. 66.
    Hurst JL, Payne CE, Nevison CM et al. Individual recognition in mice mediated by major urinary proteins. Nature 2001; 414:631–634.PubMedCrossRefGoogle Scholar
  67. 67.
    Hurst JL, Thom MD, Nevison CM et al. MHC odours are not required or sufficient for recognition of individual scent owners. Proc Biol Sci 2005; 272:715–724.PubMedCrossRefGoogle Scholar
  68. 68.
    Cheetham SA, Thom MD, Jury F et al. The genetic basis of individual-recognition signals in the mouse. Curr Biol 2007; 17:1771–1777.PubMedCrossRefGoogle Scholar
  69. 69.
    Penn D, Potts W. Untrained mice distinguish MHC-determined odors. Physiol Behav 1998;64:235–243.PubMedCrossRefGoogle Scholar
  70. 70.
    Manning CJ, Potts WK, Wakeland EK et al. What’s wrong with MHC mate choice experiments? In: Doty RL, Müller-Schwarze D, eds. Chemical Signals in Vertebrates. Vol VI. New York: Plenum; 1992; 229–235.Google Scholar
  71. 71.
    Hamilton WD. The genetical evolution of social behaviour. I II. J Theor Biol 1964; 7:1–52.PubMedCrossRefGoogle Scholar
  72. 72.
    Mateo JM. Kin-recognition abilities and nepotism as a function of sociality. Proc Biol Sci 2002; 269:721–727.PubMedCrossRefGoogle Scholar
  73. 73.
    Yamazaki K, Beauchamp GK, Curran M et al. Parent-progeny recognition as a function of MHC odortype identity. Proc Natl Acad Sci USA 2000; 97:10500–10502.PubMedCrossRefGoogle Scholar
  74. 74.
    Brown JL. Some paradoxical goals of cells and organisms: the role of the MHC. In: Pfaff DW, ed. Ethical Questions in Brain and Behavior. New York: Springer Verlag; 1983; 111–124.CrossRefGoogle Scholar
  75. 75.
    Penn D, Potts W. MHC-disassortative mating preferences reversed by cross-fostering. Proc R Soc London B 1998d; 265:1299–1306.CrossRefGoogle Scholar
  76. 76.
    Potts WK, Wakeland EK. Evolution of MHC genetic diversity: a tale of incest, pestilence and sexual preference. Trends Genet 1993; 9:408–412.PubMedCrossRefGoogle Scholar
  77. 77.
    Paterson S, Hurst JL. How effective is recognition of siblings on the basis of genotype? J Evol Biol 2009; 22:1875–1881.PubMedCrossRefGoogle Scholar
  78. 78.
    Sato A, Figueroa F, Murray BW et al. Nonlinkage of major histocompatibility complex class I and class II loci in bony fishes. Immunogenetics 2000; 51:108–116.PubMedCrossRefGoogle Scholar
  79. 79.
    Liu Y, Kasahara M, Rumfelt LL et al. Xenopus class II A genes: studies of genetics, polymorphism and expression. Dev Comp Immunol 2002; 26:735–750.PubMedCrossRefGoogle Scholar
  80. 80.
    Sherborne AL, Thom MD, Paterson S et al. The genetic basis of inbreeding avoidance in house mice. Curr Biol 2007; 17:2061–2066.PubMedCrossRefGoogle Scholar
  81. 81.
    Brown GE, Brown JA. Do kin always make better neighbours? The effects of territory quality. Behavioral Ecology and Sociobiology 1993; 33:225–231.CrossRefGoogle Scholar
  82. 82.
    Johnston RE, Muller-Schwartz D, Sorensen PW. Advances in Chemical Signals in Vertebrates: Klewer/ Plenum, New York; 1999.CrossRefGoogle Scholar
  83. 83.
    Lynch CB. Inbreeding effects upon animals derived from a wild population of Mus musculus. Evolution 1977; 31:526–537.CrossRefGoogle Scholar
  84. 84.
    Connor JL, Belucci MJ. Natural selection resisting inbreeding depression in captive wild house mice (Mus musculus). Evolution 1979; 33:929–940.CrossRefGoogle Scholar
  85. 85.
    Meagher S, Penn DJ, Potts WK. Male-male competition magnifies inbreeding depression in wild house mice. Proc Natl Acad Sci USA 2000; 97:3324–3329.PubMedCrossRefGoogle Scholar
  86. 86.
    Ilmonen P, Penn DJ, Damjanovich K et al. Experimental infection magnifies inbreeding depression in house mice. J Evol Biol 2008; 21:834–841.PubMedCrossRefGoogle Scholar
  87. 87.
    Neff BD, Pitcher TE. Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol 2005; 14:19–38.PubMedCrossRefGoogle Scholar
  88. 88.
    Wedekind C, Chapuisat M, Macas E et al. Non-random fertilization in mice correlates with MHC and something else. Heredity 1996; 77:400–409.PubMedCrossRefGoogle Scholar
  89. 89.
    Lulicke T, Chapuisat M, Homberger FR et al. MHC-genotype of progeny influenced by parental infection. Proc R Soc Lond B 1998; 265:711–716.CrossRefGoogle Scholar
  90. 90.
    Doherty PC, Zinkernagel RM. Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 1975; 256:50–52.PubMedCrossRefGoogle Scholar
  91. 91.
    Hughes AL, Nei M. Pattern of nucleotide substitution at major histocompatibity complex class I loci reveals overdominant selection. Nature 1988; 335:167–170.PubMedCrossRefGoogle Scholar
  92. 92.
    Hill AV, Allsopp CE, Kwiatkowski D et al. Common west African HLA antigens are associated with protection from severe malaria. Nature 1991; 352:595–600.PubMedCrossRefGoogle Scholar
  93. 93.
    Thursz MR, Thomas HC, Greenwood BM et al. Heterozygote advantage for HLA class-II type in hepatitis B virus infection. Nat Genet 1997; 17:11–12.PubMedCrossRefGoogle Scholar
  94. 94.
    Carrington M, Nelson GW, Martin MP et al. HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science 1999; 283:1748–1752.PubMedCrossRefGoogle Scholar
  95. 95.
    Arkush KD, Giese AR, Mendonca HL et al. Resistance to three pathogens in the endangered winter-run chinook salmon (Oncorhynchus tshawytscha): effects of inbreeding and major histocompatibility complex genotypes. Canadian Journal of Fisheries and Aquatic Science 2002; 59:966–975.CrossRefGoogle Scholar
  96. 96.
    Penn DJ, Damjanovich K, Potts WK. MHC heterozygosity confers a selective advantage against multiplestrain infections. Proc Natl Acad Sci USA 2002; 99:11260–11264.PubMedCrossRefGoogle Scholar
  97. 97.
    Froeschke G, Sommer S. MHC class II DRB variability and parasite load in the striped mouse (Rhabdomys pumilio) in the Southern Kalahari. Mol Biol Evol 2005; 22:1254–1259.PubMedCrossRefGoogle Scholar
  98. 98.
    Hraber P, Kuiken C, Yusim K. Evidence for human leukocyte antigen heterozygote advantage against hepatitis C virus infection. Hepatology 2007; 46:1713–1721.PubMedCrossRefGoogle Scholar
  99. 99.
    McClelland EE, Penn DJ, Potts WK. Major Histocompatibility Complex Heterozygote Superiority during Coinfection. Infect Immun 2003; 71:2079–2086.PubMedCrossRefGoogle Scholar
  100. 100.
    Kekalainen J, Vallunen JA, Primmer CR et al. Signals of major histocompatibility complex overdominance in a wild salmonid population. Proc Biol Sci 2009; 276:3133–3140.PubMedCrossRefGoogle Scholar
  101. 101.
    Oliver MK, Telfer S, Piertney SB. Major histocompatibility complex (MHC) heterozygote superiority to natural multi-parasite infections in the water vole (Arvicola terrestris). Proc Biol Sci 2009; 276:1119–1128.PubMedCrossRefGoogle Scholar
  102. 102.
    Penn D, Potts W. The evolution of mating preferences and major histocompatibility genes. Am Nat 1999; 153:145–164.CrossRefGoogle Scholar
  103. 103.
    Bertoletti A, Sette A, Chisari FV et al. Natural variants of cytotoxic epitopes are T-cell receptor antagonists for antiviral cytotoxic T-cells [see comments]. Nature 1994; 369:407–410.PubMedCrossRefGoogle Scholar
  104. 104.
    Moskophidis D, Zinkernagel RM. Immunobiology of cytotoxic T-cell escape mutants of lymphocytic choriiomeningitis virus. J Viriol 1995; 69:2187–2193.Google Scholar
  105. 105.
    McMichael AJ, Phillips RE. Escape of human immunodeficiency virus from immune control. Annu Rev Immunol 1997; 15:271–296.PubMedCrossRefGoogle Scholar
  106. 106.
    Jeffery KJ, Usuku K, Hall SE et al. HLA alleles determine human T-lymphotropic virus-I (HTLV-I) proviral load and the risk of HTLV-I-associated myelopathy. Proc Natl Acad Sci USA 1999; 96:3848–3853.PubMedCrossRefGoogle Scholar
  107. 107.
    Allen TM, O’Connor DH, Jing P et al. Tat-specific cytotoxic T-lymphocytes select for SIV escape variants during resolution of primary viraemia. Nature 2000; 407:386–390.PubMedCrossRefGoogle Scholar
  108. 108.
    Bowen DG, Walker CM. Mutational escape from CD8+ T-cell immunity: HCV evolution, from chimpanzees to man. J Exp Med 2005; 201:1709–1714.PubMedCrossRefGoogle Scholar
  109. 109.
    Furukawa Y, Tara M, Izumo S et al. HTLV-I viral escape and host genetic changes in the development of adult T-cell leukemia. Int J Cancer 2006; 118:381–387.PubMedCrossRefGoogle Scholar
  110. 110.
    Goulder PJ, Watkins DI. HIV and SIV CTL escape: implications for vaccine design. Nat Rev Immunol 2004; 4:630–640.PubMedCrossRefGoogle Scholar
  111. 111.
    McClelland EE, Granger DL, Potts WK. MHC-dependent susceptibility to Cryptococcus neoformans in mice. Infection and Immunity 2003; 71:4815–4817.PubMedCrossRefGoogle Scholar
  112. 112.
    Buseyne F, Janvier G, Teglas JP et al. Impact of heterozygosity for the chemokine receptor CCR5 32-bp-deleted allele on plasma virus load and CD4 T-lymphocytes in perinatally human immunodeficiency virus-infected children at 8 years of age. J Infect Dis 1998; 178:1019–1023.PubMedCrossRefGoogle Scholar
  113. 113.
    Misrahi M, Teglas JP, N’Go N et al. CCR5 chemokine receptor variant in HIV-1 mother-to-child transmission and disease progression in children. French Pediatric HIV Infection Study Group. Jama 1998; 279:277–280.PubMedCrossRefGoogle Scholar
  114. 114.
    MacDonald KS, Embree J, Njenga S et al. Mother-child class I HLA concordance increases perinatal human immunodeficiency virus type 1 transmission. J Infect Dis 1998; 177:551–556.PubMedCrossRefGoogle Scholar
  115. 115.
    Polycarpou A, Ntais C, Korber BT et al. Association between maternal and infant class I and II HLA alleles and of their concordance with the risk of perinatal HIV type 1 transmission. AIDS Res Hum Retroviruses 2002; 18:741–746.PubMedCrossRefGoogle Scholar
  116. 116.
    Woelfing B, Traulsen A, Milinski M et al. Does intra-individual major histocompatibility complex diversity keep a golden mean? Philos Trans R Soc Lond B Biol Sci 2009; 364:117–128.PubMedCrossRefGoogle Scholar
  117. 117.
    Wegner KM, Kalbe M, Kurtz J et al. Parasite selection for immunogenetic optimality. Science 2003; 301:1343.PubMedCrossRefGoogle Scholar
  118. 118.
    Kalbe M, Eizaguirre C, Dankert I et al. Lifetime reproductive success is maximized with optimal major histocompatibility complex diversity. Proc Biol Sci 2009; 276:925–934.PubMedCrossRefGoogle Scholar
  119. 119.
    Reusch TB, Haberli MA, Aeschlimann PB et al. Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 2001; 414:300–302.PubMedCrossRefGoogle Scholar
  120. 120.
    Boehm T. Quality control in self/nonself discrimination. Cell 2006; 125:845-858. 121. Zahavi A. Mate selection-a selection for a handicap. J theor Biol 1975; 53:205–214.CrossRefGoogle Scholar
  121. 122.
    Ditchkoff SS, Lochmiller RL, Masters RE et al. Major-histocompatibility-complex-associated variation in secondary sexual traits of white-tailed deer (Odocoileus virginianus): evidence for good-genes advertisement. Evolution 2001; 55:616–625.PubMedCrossRefGoogle Scholar
  122. 123.
    Von-Schantz THWGGMGKP. MHC genotype and male ornamentation: genetic evidence for the Hamilton-Zuk model. Proc R Soc Lond B 1996; 263:265–271.CrossRefGoogle Scholar
  123. 124.
    Ekblom R, Saether SA, Grahn M et al. Major histocompatibility complex variation and mate choice in a lekking bird, the great snipe (Gallinago media). Mol Ecol 2004; 13:3821–3828.PubMedCrossRefGoogle Scholar
  124. 125.
    Milinski M, Griffiths SW, Reusch TB et al. Costly major histocompatibility complex signals produced only by reproductively active males, but not females, must be validated by a ‘maleness signal’ in three-spined sticklebacks. Proc Biol Sci 2009; 2010; 277:391–398.Google Scholar
  125. 126.
    Zuk M. The role of parasites in sexual selection: current evidence and future directions. Adv Study Behav 1992; 21:39–68.CrossRefGoogle Scholar
  126. 127.
    Penn D, Potts WK. Chemical signals and parasite-mediated sexual selection. Trends Ecol Evol 1998; 13:391–396.PubMedCrossRefGoogle Scholar
  127. 128.
    Kavaliers M, Choleris E, Agmo A et al. Olfactory-mediated parasite recognition and avoidance: linking genes to behavior. Horm Behav 2004; 46:272–283.PubMedCrossRefGoogle Scholar
  128. 129.
    Moller AP, Saino N. Parasites, immunology of hosts and host sexual selection. J Parasitol 1994; 80:850-858. 130. Boehm T. Co-evolution of a primordial peptide-presentation system and cellular immunity. Nat Rev Immunol 2006; 6:79–84.CrossRefGoogle Scholar
  129. 131.
    Han BW, Herrin BR, Cooper MD et al. Antigen recognition by variable lymphocyte receptors. Science 2008; 321:1834–1837.PubMedCrossRefGoogle Scholar
  130. 132.
    Cooper MD, Alder MN. The evolution of adaptive immune systems. Cell 2006; 124:815–822.PubMedCrossRefGoogle Scholar
  131. 133.
    Guo P, Hirano M, Herrin BR et al. Dual nature of the adaptive immune system in lampreys. Nature 2009; 459:796–801.PubMedCrossRefGoogle Scholar
  132. 134.
    Scofield VL, Schlumpberger JM, West LA et al. Protochordate allorecognition is controlled by a Mhc-like gene system. Nature 1982; 295:499–502.PubMedCrossRefGoogle Scholar
  133. 135.
    Grosberg RK, Hart MW. Mate selection and the evolution of highly polymorphic self/nonself recognition genes. Science 2000; 289:2111–2114.PubMedCrossRefGoogle Scholar
  134. 136.
    De Tomaso AW, Nyholm SV, Palmeri KJ et al. Isolation and characterization of a protochordate histocompatibility locus. Nature 2005; 438:454–459.PubMedCrossRefGoogle Scholar
  135. 137.
    De Tomaso AW, Weissman IL. Evolution of a protochordate allorecognition locus. Science 2004; 303:977.PubMedCrossRefGoogle Scholar
  136. 138.
    Khalturin K, Bosch TC. Self/nonself discrimination at the basis of chordate evolution: limits on molecular conservation. Curr Opin Immunol 2007; 19:4–9.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2012

Authors and Affiliations

  • James S. Ruff
    • 1
  • Adam C. Nelson
    • 1
  • Jason L. Kubinak
    • 1
  • Wayne K. Potts
    • 1
  1. 1.Department of BiologyUniversity of UtahSalt Lake CityUSA

Personalised recommendations