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An Mhc class I allele associated to the expression of T-dependent immune response in the house sparrow

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Abstract

The major histocompatibility complex (Mhc) encodes for highly variable molecules, responsible for foreign antigen recognition and subsequent activation of immune responses in hosts. Mhc polymorphism should hence be related to pathogen resistance and immune activity, with individuals that carry either a higher diversity of Mhc alleles or one specific Mhc allele exhibiting a stronger immune response to a given antigen. Links between Mhc alleles and immune activity have never been explored in natural populations of vertebrates. To fill this gap, we challenged house sparrows (Passer domesticus) with two T-dependent antigens (phytohemagglutinin and sheep red blood cells) and examined both primary and secondary immune responses in relation to their Mhc class I genotypes. The total number of Mhc alleles had no influence on either primary or secondary response to the two antigens. One particular Mhc allele, however, was associated with an increased response to both antigens. Our results point toward a contribution of the Mhc, or of other genes in linkage disequilibrium with the Mhc, in the regulation of immune responses in a wild animal species.

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References

  • Aguilar AG, Roemer S, Debenham M, Binns D, Garcelon, Wayne RK (2004) High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci U S A 101:3490–3494

    Article  PubMed  Google Scholar 

  • Apanius V, Penn D, Slev PR, Ruff LR, Potts WK (1997) The nature of selection on the major histocompatibility complex. Crit Rev Immunol 17:179–224

    PubMed  CAS  Google Scholar 

  • Arkush KD, Giese AR, Mendonca HL, McBride AM, Marty GD, Hedrick PW (2002) Resistance to three pathogens in the endangered winter-run chinook salmon (Oncorhynchus tshawyscha): effects of inbreeding and major histocompatibility complex genotypes. Can J Fish Aquat Sci 59:966–975

    Article  Google Scholar 

  • Belkhir K, Castric V, Bonhomme F (2002) IDENTIX, a software to test for relatedness in a population using permutation methods. Mol Ecol Notes 2:611–614

    Article  Google Scholar 

  • Bilbo SD, Drazen DL, Quan N, He L, Nelson RJ (2002) Short day lengths attenuate the symptoms of infection in Siberian hamsters. Proc R Soc Lond B 269:447–454

    Article  Google Scholar 

  • Bodmer WF (1972) Evolutionary significance of the HL-A system. Nature 237:139–145

    Article  PubMed  CAS  Google Scholar 

  • Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Faivre B, Sorci G (2003) Assessing the cost of mounting an immune response. Am Nat 161:367–379

    Article  PubMed  Google Scholar 

  • Bonneaud C, Sorci G, Morin V, Westerdahl H, Zoorob R, Wittzell H (2004) Diversity of Mhc class I and IIB genes in house sparrows (Passer domesticus). Immunogenetics 55:855–865

    Article  PubMed  CAS  Google Scholar 

  • Briles WE, Stone HA, Cole RK (1977) Marek's disease: effects of B histocompatibility alloalleles in resistant and susceptible chicken lines. Science 195:193–195

    Article  PubMed  CAS  Google Scholar 

  • Carrington M, Nelson GW, Martin MP, Kissner T, Vlahov D, Goedert JJ, Kaslow R, Buchbinder S, Hoots K, O'Brien SJ (1999) HLA and HIV-1: heterozygote advantage and B*35–Cw*04 disadvantage. Science 283:1748–1752

    Article  PubMed  CAS  Google Scholar 

  • Cheng S, Lamont SJ (1988) Genetic analysis of immunocompetence measures in a White Leghorn chicken line. Poult Sci 67:989–995

    PubMed  CAS  Google Scholar 

  • Cotter PF, Taylor RL Jr, Wing TL, Briles WE (1987) Major histocompatibility (B) complex-associated differences in the delayed wattle reaction to staphylococcal antigen. Poult Sci 66:203–208

    PubMed  CAS  Google Scholar 

  • Cotter PF, Taylor RL Jr, Abplanalp H (1992) Differential resistance to Staphylococcus aureus challenge in major histocompatibility (B) complex congenic lines. Poult Sci 71:1873–1878

    PubMed  CAS  Google Scholar 

  • Demas GE, Chefer V, Talan MI, Nelson RJ (1997) Metabolic costs of mounting an antigen-stimulated immune response in adult and aged C57BL/6J mice. Am J Physiol 273:1631–1637

    Google Scholar 

  • Doherty PC, Zinkernagel RM (1975) Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256:50–52

    Article  PubMed  CAS  Google Scholar 

  • Dunnington EA, Briles RW, Briles WE, Gross WB, Siegel PB (1984) Allelic frequencies in eight alloantigen systems of chickens selected for high and low antibody response to sheep red blood cells. Poult Sci 63:1470–1472

    PubMed  CAS  Google Scholar 

  • Dunnington EA, Martin A, Briles RW, Briles WE, Gross WB, Siegel PB (1989) Antibody responses to sheep erythrocytes for White Leghorn chickens differing in haplotypes of the major histocompatibility complex (B). Anim Genet 20:213–216

    Article  PubMed  CAS  Google Scholar 

  • Faivre B, Grégoire A, Préault M, Cézilly F, Sorci G (2003) Immune activation rapidly mirrored in a secondary sexual trait. Science 300:103

    Article  PubMed  CAS  Google Scholar 

  • Fredericksen TL, Gilmour DG (1983) Ontogeny of con A and PHA responses of chicken blood cells in MHC-compatible lines 6(3) and 7(2). J Immunol 130:2528–2533

    PubMed  CAS  Google Scholar 

  • Gehad AE, Mashaly MM, Siegel HS, Dunnington EA, Siegel PB (1999) Effect of genetic selection and MHC haplotypes on lymphocyte proliferation and interleukin-2 like activity in chicken lines selected for high and low antibody production against sheep red blood cells. Vet Immunol Immunopathol 68:13–24

    Article  PubMed  CAS  Google Scholar 

  • Griffith SC, Stewart IRK, Dawson DA, Owens IPF, Burke T (1999) Extra-pair paternity in mainland and island populations of a socially monogamous bird, the house sparrow (Passer domesticus): is there an “island effect”? Biol J Linn Soc 68:303–316

    Article  Google Scholar 

  • Gonzalez G, Sorci G, Møller AP, Ninni P, Haussy C, De Lope F (1999) Immunocompetence and condition-dependent sexual advertisement in male house sparrows (Passer domesticus). J Anim Ecol 68:1225–1234

    Article  Google Scholar 

  • Goto N, Kodama H, Okada K, Fujimoto Y (1978) Suppression of phytohemagglutinin skin response in thymectomized chickens. Poult Sci 57:246–250

    PubMed  CAS  Google Scholar 

  • Gross WG, Siegel PB, Hall RW, Domermuth CH, DuBoise RT (1980) Production and persistence of antibodies in chickens to sheep erythrocytes. 2. Resistance to infectious diseases. Poult Sci 59:205–210

    PubMed  CAS  Google Scholar 

  • Guo SW, Thompson EA (1992) A Monte Carlo method for combined segregation and linkage analysis. Am J Hum Genet 51:1111–1126

    PubMed  CAS  Google Scholar 

  • Hedrick PW (2002) Pathogen resistance and genetic variation at MHC loci. Evolution 56:1902–1908

    PubMed  Google Scholar 

  • Hedrick PW, Kim T, Parker K (2001) Parasite resistance and genetic variation in the endangered Gila topminnow. Anim Conserv 4:103–109

    Article  Google Scholar 

  • Ilmonen P, Taarna T, Hasselquist D (2000) Experimentally activated immune defence in female pied flycatchers results in reduced breeding success. Proc R Soc Lond B 267:665–670

    Article  CAS  Google Scholar 

  • Janeway CA, Travers P (1999) Immunobiology: the immune system in health and disease, 4th edn. Current Biology Ltd., London

    Google Scholar 

  • Kaufman J, Venugopal K (1998) The importance of MHC for Rous sarcoma virus and Marek's disease virus—some Payne-ful considerations. Avian Pathol 27:S82–S87

    Article  Google Scholar 

  • Lamont SJ (1998) Impact of genetics on disease resistance. Poult Sci 77:1111–1118

    PubMed  CAS  Google Scholar 

  • Lamont SJ, Bolin C, Cheville N (1987) Genetic resistance to fowl cholera is linked to the major histocompatibility complex. Immunogenetics 25:284–289

    Article  PubMed  CAS  Google Scholar 

  • Langefors Å, Lohm J, Grahn M, Andersen Ø, 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 268:479–485

    Article  CAS  Google Scholar 

  • Lassila O, Nurmi T, Eskola J (1979) Genetic differences in the mitogenic response of peripheral blood lymphocytes in the chicken. J Immunogenet 6:37–43

    Article  PubMed  CAS  Google Scholar 

  • Lee LF, Bacon LD (1983) Ontogeny and line differences in the mitogenic response of chicken lymphocytes. Poult Sci 62:579–584

    PubMed  CAS  Google Scholar 

  • Lillehoj HS, Ruff MD, Bacon LD, Lamont SJ, Jeffers TK (1989) Genetic control of immunity to Eimeria tenella. Interaction of MHC genes and non-MHC linked genes influences levels of disease susceptibility in chickens. Vet Immunol Immunopathol 20:135–148

    Article  PubMed  CAS  Google Scholar 

  • Lively CM, Apanius V (1995) Genetic diversity in host-parasite interactions. In: Grenfell BT, Dobson AP (eds) Ecology of infectious diseases in natural populations. Cambridge University Press, Cambridge, UK, pp 421–449

    Google Scholar 

  • Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98

    Article  Google Scholar 

  • Longenecker BM, Gallatin WM (1978) Genetic control of resistance to Marek's disease. IARC Sci Publ 24(Pt 2):845–850

    PubMed  Google Scholar 

  • Loudovaris T, Brandon MR, Fahey KJ (1990) The major histocompatibility complex and genetic control of antibody response to sheep red blood cells in chickens. Av Patol 19:89–99

    Article  CAS  Google Scholar 

  • Martin LB, Scheuerlein A, Wikleski M (2003) Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc R Soc Lond B 270:153–158

    Article  Google Scholar 

  • Mathieu E, Autem M, Roux M, Bonhomme F (1990) Épreuves de validation dans l'analyse de structures génétiques multivariées: comment tester l'équilibre panmictique? Revue de Statistique Appliquée 38:47–66

    Google Scholar 

  • McClelland EE, Penn DJ, Potts WK (2003) Major histocompatibility complex heterozygote superiority during coinfection. Infect Immun 71:2079–2086

    Article  PubMed  CAS  Google Scholar 

  • McCorkle F, Taylor R, Stinson R, Day EJ, Glick B (1980) The effects of a megalevel of vitamin C on the immune response of the chicken. Poult Sci 59:1324–1327

    PubMed  CAS  Google Scholar 

  • Munns PL, Lamont SJ (1991) Research note: effects of age and immunization interval on the anamnestic response to T-cell-dependent and T-cell-independent antigens in chickens. Poult Sci 70:2371–2374

    PubMed  CAS  Google Scholar 

  • Myers RM, Maniatis T, Lerman LS (1987) Detection and localization of single base changes by denaturant gradient gel electrophoresis. Methods Enzymol 155:501–527

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Hughes AL (1991) Polymorphism due to balancing selection at the major histocompatibility complex loci. In: Dudley E (ed) The unity of evolutionary biology: Proc. IV Intl. Cong. System. Evol Biol, vol. 2 pp 878–889. Dioscorides Press, Portland, Oregon

    Google Scholar 

  • Norris K, Evans MR (2000) Ecological immunology: life history trade-offs and immune defences in birds. Behav Ecol 11:19–26

    Article  Google Scholar 

  • Ots I, Kerimov AB, Ivankina EV, Ilyina TA, Hõrak P (2001) Immune challenge affects basal metabolic activity in wintering great tits. Proc R Soc Lond B 268:1175–1181

    Article  CAS  Google Scholar 

  • Parham P, Ohta T (1996) Population biology of antigen presentation by MHC class I molecules. Science 272:67–74

    Article  PubMed  CAS  Google Scholar 

  • Penn DJ, Damjanovich K, Potts WK (2002) MHC heterozygocity confers a selective advantage against multiple-strain infections. Proc Natl Acad Sci U S A 99:11260–11264

    Article  PubMed  CAS  Google Scholar 

  • Pevzner I, Nordskog AW, Kaeberle ML (1975) Immune response and the B blood group locus in chickens. Genetics 80:753–759

    PubMed  CAS  Google Scholar 

  • Pinard MH, Janss LL, Maatman R, Noordhuizen JP, van der Zijpp AJ (1993) Effect of divergent selection for immune responsiveness and of major histocompatibility complex on resistance to Marek's disease in chickens. Poult Sci 72:391–402

    PubMed  CAS  Google Scholar 

  • Potts WK, Wakeland EK (1993) Evolution of MHC genetic diversity: a tale of incest, pestilence and sexual preference. Trends Genet 9:408–412

    Article  PubMed  CAS  Google Scholar 

  • Primmer CR, Møller AP, Ellegren H (1996) New microsatellites from the pied flycatcher Ficedula hypoleuca and the swallow Hirundo rustica genomes. Hereditas 124:281–283

    Article  PubMed  CAS  Google Scholar 

  • Puel A, Groot PC, Lathrop MG, Demant P, Mouton D (1995) Mapping of genes controlling quantitative antibody production in Biozzi mice. J Immunol 154:5799–5805

    PubMed  CAS  Google Scholar 

  • Puel A, Mevel JC, Bouthillier Y, Feingold N, Fridman WH, Mouton D (1996) Toward genetic dissection of high and low antibody responsiveness in Biozzi mice. Proc Natl Acad Sci U S A 93:14742–14746

    Article  PubMed  CAS  Google Scholar 

  • Puel A, Mevel JC, Bouthillier Y, Decreusefond C, Fridman WH, Feingold N, Mouton D (1998) Identification of two quantitative trait loci involved in antibody production on mouse chromosome 8. Immunogenetics 47:326–331

    Article  PubMed  CAS  Google Scholar 

  • Richardson DS, Jury FL, Dawson DA, Salgueiro P, Komdeur J, Burke T (2000) Fifty Seychelles warbler (Acrocephalus sechellensis) microsatellite loci polymorphic in Sylviidae species and their cross-species amplification in other passerine birds. Mol Ecol 9:2155–2234

    Article  PubMed  Google Scholar 

  • SAS (1999) SAS user's guide: statistics. Version 6.12 edn. SAS Institute, Cary

    Google Scholar 

  • Schierman LW, Collins WM (1987) Influence of the major histocompatibility complex on tumor regression and immunity in chickens. Poult Sci 66:812–818

    PubMed  CAS  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland

    Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321

    Article  Google Scholar 

  • Shou-Hsien L, Yi-Jiun H, Brown JL (1997) Isolation of tetranucleotide microsatellites from the Mexican jay Aphelocoma ultramarina. Mol Ecol 6:499–501

    Article  PubMed  Google Scholar 

  • Soler JJ, de Neve L, Pérez-Contreras T, Soler M, Sorci G (2002) Trade-off between immunocompetence and growth in magpies: an experimental study. Proc R Soc Lond B 270:241–248

    Article  Google Scholar 

  • Sorci G, Møller AP, Boulinier T (1997) Genetics of host-parasite interactions. Trends Ecol Evol 12:196–199

    Article  Google Scholar 

  • Stadecker MJ, Lukic M, Dvorak A, Leskowitz S (1977) The cutaneous basophil response to phytohemagglutinin in chickens. J Immunol 118:1564–1568

    PubMed  CAS  Google Scholar 

  • Taylor RL Jr, Cotter PF, Wing TL, Briles WE (1987) Major histocompatibility (B) complex and sex effects on the phytohaemagglutinin wattle response. Anim Genet 18:343–350

    PubMed  Google Scholar 

  • Wakelin D (1996) Immunology to parasites, 2nd edn. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Wegner KM, Kalbe M, Kurtz J, Reusch TBH, Milinski M (2003) Parasite selection for immunogenetic optimality. Science 301:1343

    Article  PubMed  CAS  Google Scholar 

  • Weigend S, Mielenz N, Lamont SJ (1997) Application of a nonlinear regression function to evaluate the kinetics of antibody response to vaccines in chicken lines divergently selected for multitrait immune response. Poult Sci 76:1248–1255

    PubMed  CAS  Google Scholar 

  • Yonash N, Kaiser MG, Heller ED, Cahaner A, Lamont SJ (1999) Major histocompatibility complex (MHC) related cDNA probes associated with antibody response in meat-type chickens. Anim Genet 30:92–101

    Article  PubMed  CAS  Google Scholar 

  • Yoo BH, Sheldon BL (1992) Association of the major histocompatibility complex with avian leukosis virus infection in chickens. Br Poult Sci 33:613–620

    Article  PubMed  CAS  Google Scholar 

  • Zhou H, Lamont SJ (2003) Chicken MHC class I and II gene effects on antibody response kinetics in adult chickens. Immunogenetics 55:133–140

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We are grateful to the staff of the Station Biologique de Foljuif for their help. CB would like to thank everybody in Lund for their warm welcome and for making her stay productive. Financial support was provided by the Ministère de la Recherche (bourse doctorale to CB and ACI Jeunes Chercheurs to GS).

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  1. Gabriele Sorci

    Present address: BioGéoSciences, CNRS UMR 5561, Université de Bourgogne, 6 Boulevard Gabriel, 21000, Dijon, France

Authors and Affiliations

  1. Laboratoire de Parasitologie Evolutive CNRS UMR 7103, Université Pierre et Marie Curie Paris 6, 7 quai St Bernard, bât. A 7e étage, case 237, Paris cedex 05, 75252, France

    Camille Bonneaud, Murielle Richard & Gabriele Sorci

  2. Université de Bourgogne, UMR CNRS 5561 BioGéoSciences, Equipe Ecologie Evolutive, 6 Blvd Gabriel, 21000, Dijon, France

    Bruno Faivre

  3. Molecular Population Biology Laboratory, Department of Animal Ecology, University of Lund, 22363, Lund, Sweden

    Helena Westerdahl

  4. Center for Tropical Research, Institute of the Environment , University of California, Los Angeles, CA, 90095-1496, USA

    Camille Bonneaud

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  1. Camille Bonneaud
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  3. Bruno Faivre
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Correspondence to Camille Bonneaud.

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Bonneaud, C., Richard, M., Faivre, B. et al. An Mhc class I allele associated to the expression of T-dependent immune response in the house sparrow. Immunogenetics 57, 782–789 (2005). https://doi.org/10.1007/s00251-005-0046-5

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