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Single locus typing of MHC class I and class II B loci in a population of red jungle fowl

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Abstract

In species with duplicated major histocompatibility complex (MHC) genes, estimates of genetic variation often rely on multilocus measures of diversity. It is possible that such measures might not always detect more detailed patterns of selection at individual loci. Here, we describe a method that allows us to investigate classical MHC diversity in red jungle fowl (Gallus gallus), the wild ancestor of the domestic chicken, using a single locus approach. This is possible due to the well-characterised gene organisation of the ‘minimal essential’ MHC (BF/BL region) of the domestic chicken, which comprises two differentially expressed duplicated class I (BF) and two class II B (BLB) genes. Using a combination of reference strand-mediated conformation analysis, cloning and sequencing, we identify nine BF and ten BLB alleles in a captive population of jungle fowl. We show that six BF and five BLB alleles are from the more highly expressed locus of each gene, BF2 and BLB2, respectively. An excess of non-synonymous substitutions across the jungle fowl BF/BL region suggests that diversifying selection has acted on this population. Importantly, single locus screening reveals that the strength of selection is greatest on the highly expressed BF2 locus. This is the first time that a population of red jungle fowl has been typed at the MHC region, laying the basis for further research into the underlying processes acting to maintain MHC diversity in this and other species.

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References

  • Addie DD, Kennedy LJ, Ryvar R, Willoughby K, Gaskell RM, Ollier WER, Nart P, Radford AD (2004) Feline leucocyte antigen class II polymorphism and susceptibility to feline infectious peritonitis. J Fel Med Surg 6:59–62

    Article  Google Scholar 

  • Angles J, Kennedy L, Pedersen N (2005) Frequency and distribution of alleles of canine MHC-II DLA-DQB1, DLA-DQA1 and DLA-DRB1 in 25 representative American Kennel Club breeds. Tissue Antigens 66:173–184

    Article  PubMed  CAS  Google Scholar 

  • Argüello J, Little A, Pay AL et al (1998) Mutation detection and typing of polymorphic loci through double-strand conformation analysis. Nat Genet 18:192–194

    Article  PubMed  Google Scholar 

  • Bacon LD (1987) Influence of the major histocompatability complex on disease resistance and productivity. Poultry Sci 66(5):802–811

    CAS  Google Scholar 

  • Bacon LD, Witter RL, Crittenden LB, Fadly A, Motta J (1981) B-haplotype influence on Marek's disease, Rous sarcoma, and lymphoid leukosis virus-induced tumors in chickens. Poultry Sci 60:1132–1139

    CAS  Google Scholar 

  • Bakker PIW, McVean G, Sabeti PC 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

    Article  PubMed  CAS  Google Scholar 

  • Briles WE, Bumstead N, Ewert DL et al (1982) Nomenclature for chicken major histocompatibility (B) complex. Immunogenetics 15:441–447

    Article  PubMed  CAS  Google Scholar 

  • Briles WE, Briles RW, Taffs RE, Stone HA (1983) Resistance to a malignant-lymphoma in chickens is mapped to subregion of major histocompatibility (B) complex. Science 219:977–979

    Article  PubMed  CAS  Google Scholar 

  • Brown JH, Jardetzky TS, Gorga JC et al (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364:33–39

    Article  PubMed  CAS  Google Scholar 

  • Collins WM, Briles WE, Zsigray RM et al (1977) B locus (MHC) in chicken—association with fate of RSV-induced tumors. Immunogenetics 5:333–343

    Article  Google Scholar 

  • Edwards SV, Wakeland EK, Potts WK (1995) Contrasting histories of avian and mammalian MHC genes revealed by class II B sequences from songbirds. Proc Natl Acad Sci U S A 92:12200–12204

    Article  PubMed  CAS  Google Scholar 

  • Edwards SV, Hess CM, Gasper J, Garrigan D (1999) Toward an evolutionary genomics of the avian MHC. Immunol Rev 167:119–132

    Article  PubMed  CAS  Google Scholar 

  • Ewens WJ (1972) Sampling theory of selectively neutral alleles. Theor Popul Biol 3:87

    Article  PubMed  CAS  Google Scholar 

  • Figueroa F, Gunther E, Klein J (1988) MHC polymorphism predating speciation. Nature 335:265–267

    Article  PubMed  CAS  Google Scholar 

  • Fulton JE, Juul-Madsen HR, Ashwell CM, McCarron AM, Arthur JA, O'Sullivan NP, Taylor RL Jr (2006) Molecular genotype identification of the Gallus gallus major histocompatibility complex. Immunogenetics 58:407–21

    Article  PubMed  CAS  Google Scholar 

  • Goto R, Afanassieff M, Ha J et al (2002) Single-strand conformation polymorphism (SSCP) assays for major histocompatibility complex B genotyping in chickens. Poultry Sci 81:1832–1841

    CAS  Google Scholar 

  • Guillemot F, Billault A, Pourquie O et al (1988) A molecular map of the chicken major histocompatibility complex: the class II b genes are closely linked to the class I genes and the nucleolar organiser. EMBO J 7:2775–2785

    PubMed  CAS  Google Scholar 

  • Hala K, Vilhelmova M, Schulmannova J, Plachy J (1979) A new recombinant allele in the B-complex of the chicken. Folia Biologica (Praha) 25:323–324

    CAS  Google Scholar 

  • Hala K, Chausse A, Bourlet Y et al (1988) Attempt to detect recombination between B-F and B-L genes within the chicken B complex by serological typing, in vitro MLR, and RFLP analyses. Immunogenetics 28:433–438

    Article  PubMed  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hansson B, Richardson D (2005) Genetic variation in two endangered Acrocephalus species compared to a widespread congener: estimates based on functional and random loci. Anim Conserv 8:83–90

    Article  Google Scholar 

  • Hunt HD, Fulton JE (1998) Analysis of polymorphisms in the major expressed class I locus (B-FIV) of the chicken. Immunogenetics 47:456–467

    Article  PubMed  CAS  Google Scholar 

  • Jacob JP, Milne S, Beck S, Kaufman J (2000) The major and minor class II b-chain (B-LB) gene flank the Tapasin gene in the B-F/B-L region of the chicken major histocompatibility complex. Immunogenetics 51:138–147

    Article  PubMed  CAS  Google Scholar 

  • Jarvi SI, Tarr CL, McIntosh CE, Atkinson CT, Fleischer RC (2004) Natural selection of the major histocompatibility complex (MHC) in Hawaiian honeycreepers (Drepanidinae). Mol Ecol 13:2157–2168

    Article  PubMed  CAS  Google Scholar 

  • Joiner KS, Hoerr FJ et al (2005) The avian major histocompatibility complex influences bacterial skeletal disease in broiler breeder chickens. Vet Pathol 42(3):275–281

    Article  PubMed  CAS  Google Scholar 

  • Juul-Madsen HR, Dalgaard TS, Afanassieff M (2000) Molecular characterisation of major and minor MHC class I and II genes in B21-like haplotypes in chickens. Anim Genet 31:252–261

    Article  PubMed  CAS  Google Scholar 

  • Kaufman J, Andersen R, Avila D et al (1992) Different features of the MHC class I heterodimer have evolved at different rates. J Immunol 148:1532–1546

    PubMed  CAS  Google Scholar 

  • Kaufman J, Volk H, Wallny H-J (1995) A ‘minimal essential MHC’ and an ‘unrecognised MHC’: two extremes in selection for polymorphism. Immunol Rev 143:63–88

    Article  PubMed  CAS  Google Scholar 

  • Kaufman J, Jacob J, Shaw I et al (1999a) Gene organisation determines evolution of function in the chicken MHC. Immunol Rev 167:101–117

    Article  PubMed  CAS  Google Scholar 

  • Kaufman J, Milne S, Gobel TWF et al (1999b) The chicken B locus is a minimal essential major histocompatibility complex. Nature 401:923–925

    Article  PubMed  CAS  Google Scholar 

  • Kennedy LJ, Ryvar R, Gaskell RM et al (2002) Sequence analysis of MHC DRB alleles in domestic cats from the United Kingdom. Immunogenetics 54:348–352

    Article  PubMed  CAS  Google Scholar 

  • Koch C, Skjødt K, Toivanen A, Toivanen P (1983) New recombinants within the MHC (B-complex) of the chicken. Tissue Antigens 21:129–137

    PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Jakobsen IB, Nei M (2001) Mega 2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245

    Article  PubMed  CAS  Google Scholar 

  • Kurtz J, Kalbe M, Aeschlimann PB et al (2004) Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. Proc R Soc Lond B Biol Sci 271:197–204

    Article  CAS  Google Scholar 

  • Lima-Rosa CAV, Canal CW, Streck AF et al (2004) B-F DNA sequence variability in Brazilian (blue-egg Caipira) chickens. Anim Genet 35:278–284

    Article  PubMed  CAS  Google Scholar 

  • Liu YP, Wu GS, Yao YG et al (2006) Multiple maternal origins of chickens: out of the Asian jungles. Mol Phylogenet Evol 38:12–19

    Article  PubMed  CAS  Google Scholar 

  • Livant EJ, Ewald SJ (2005) High-resolution typing for chicken BF2 (MHC class I) alleles by automated sequencing. Anim Genet 36:432–4

    Article  PubMed  CAS  Google Scholar 

  • Livant EJ, Brigati JR, Ewald SJ (2004) Diversity and locus specificity of chicken MHC B class I sequences. Anim Genet 35:18–27

    Article  PubMed  CAS  Google Scholar 

  • Miller MM, Bacon LD, Hala K et al (2004) 2004 nomenclature for the chicken major histocompatibility (B and Y) complex. Immunogenetics 56:261–279

    PubMed  CAS  Google Scholar 

  • Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3(5):418–426

    PubMed  CAS  Google Scholar 

  • Nishibori M, Shimogiri T, Hayashi T, Yasue H (2005) Molecular evidence for hybridisation of species in the genus Gallus except for Gallus varius. Anim Genet 36:367–375

    Article  PubMed  CAS  Google Scholar 

  • Ramon DS, Argüello JR, Cox ST et al (1998) Application of RSCA for typing of HLA-DPB1. Hum Immunol 59:734–747

    Article  PubMed  CAS  Google Scholar 

  • Richardson DS, Westerdahl H (2003) MHC diversity in two Acrocephalus species: the outbred great reed warbler and the inbred Seychelles warbler. Mol Ecol 12:3523–3529

    Article  PubMed  CAS  Google Scholar 

  • Richardson DS, Komdeur J, Burke T, von Schantz T (2005) MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler. Proc R Soc Lond B Biol Sci 272:759–767

    Article  Google Scholar 

  • Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Schierman LW, Watanabe DH, McBride RA (1977) Genetic control of Rous sarcoma regression in chickens: linkage with the major histocompatibility complex. Immunogenetics 5:325–332

    Article  Google Scholar 

  • Schütz KE, Jensen P (2001) Effects of resource allocation on behavioural strategies: a comparison of red jungle fowl (Gallus gallus) and two domesticated breeds of poultry. Ethology 107:753–765

    Article  Google Scholar 

  • Shaw I, Powell TA, Marston DA et al (2007) Different evolutionary histories of the two classical class I gene BF1 and BF2 illustrate drift and selection within the stable MHC haplotypes of chickens. J Immunol 178:5744–5752

    PubMed  CAS  Google Scholar 

  • Shiina T, Hosomichi K, Hanzawa K (2006) Comparative genomics of the poultry major histocompatibility complex. Anim Sci J 77:151–162

    Article  CAS  Google Scholar 

  • Shiina T, Briles WE, Goto RM et al (2007) Extended gene map reveals tripartite motif, C-type lectin and Ig superfamily type genes within a subregion of the chicken MHC-B affecting infectious disease. J Immunol 178:7162–7172

    PubMed  CAS  Google Scholar 

  • Single RM, Martin MP, Gao XJ et al (2007) Global diversity and evidence for coevolution of KIR and HLA. Nat Genet 39:1114–1119

    Article  PubMed  CAS  Google Scholar 

  • Skjødt K, Koch C, Crone M, Simonsen M (1985) Analysis of chickens for recombination with the MHC (B complex). Tissue Antigens 25:278–282

    PubMed  Google Scholar 

  • Sunnocks P, Hales DF (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol Biol Evol 13:510–524

    Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Takahata N (1990) A simple genealogical structure of strongly balanced allelic lines and transspecies evolution of polymorphism. Proc Natl Acad Sci U S A 87:2419–2423

    Article  PubMed  CAS  Google Scholar 

  • Takahata N, Nei M (1990) Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics 124:967–978

    PubMed  CAS  Google Scholar 

  • Tong JC, Bramson J, Kanduc D et al (2006) Modelling the bound conformation of Pemphigus vulgaris associated peptides to MHC class II DR and DQ alleles. Immunome Res 2:1

    Article  PubMed  CAS  Google Scholar 

  • Vilà W, Seddon JM, Ellegren H (2005) Genes of domestic mammals augmented by backcrossing with wild ancestors. Trends Genet 21:214–218

    Article  PubMed  CAS  Google Scholar 

  • Wallny H-J, Avila D, Hunt LG et al (2006) Peptide motifs of the single dominantly expressed class I molecule explain the striking MHC-determined response to Rous sarcoma virus in chickens. Proc Natl Acad Sci U S A 103:1434–1439

    Article  PubMed  CAS  Google Scholar 

  • Watterson GA (1978) The homozygosity test of neutrality. Genetics 88:405–417

    PubMed  Google Scholar 

  • Westerdahl H, Waldenstrom J, Hansson B et al (2005) Associations between malaria and MHC genes in a migratory songbird. Proc R Soc Lond B Biol Sci 272:1511–1518

    Article  CAS  Google Scholar 

  • Worley K, Carey J, Veitch A, Coltman DW (2006) Detecting the signature of selection on immune genes in highly structured populations of wild sheep (Ovis dalli). Mol Ecol 15:623–637

    Article  PubMed  CAS  Google Scholar 

  • Zelano B, Edwards SV (2002) An MHC component to kin recognition and mate choice in birds: Predictions, progress, and prospects. Am Nat 160:S225–S237

    Article  PubMed  Google Scholar 

  • Zorn AM, Krieg PA (1991) PCR analysis of alternative splicing pathways: identification of artifacts generated by heteroduplex formation. Biotechniques 11:180–184

    PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by a Natural Environment Research Council grant to TP and DSR. All polymerase chain reaction amplifications, cloning and sequencing was carried out at the University of East Anglia while the running of the reference strand-mediated conformation analysis procedure was done with LJK at the University of Manchester.

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Correspondence to D. S. Richardson.

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Worley, K., Gillingham, M., Jensen, P. et al. Single locus typing of MHC class I and class II B loci in a population of red jungle fowl. Immunogenetics 60, 233–247 (2008). https://doi.org/10.1007/s00251-008-0288-0

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