, Volume 59, Issue 9, pp 725–734 | Cite as

The Mhc class II of the Black grouse (Tetrao tetrix) consists of low numbers of B and Y genes with variable diversity and expression

  • Tanja StrandEmail author
  • Helena Westerdahl
  • Jacob Höglund
  • Rauno V. Alatalo
  • Heli Siitari
Original Paper


We found that the Black grouse (Tetrao tetrix) possess low numbers of Mhc class II B (BLB) and Y (YLB) genes with variable diversity and expression. We have therefore shown, for the first time, that another bird species (in this case, a wild lek-breeding galliform) shares several features of the simple Mhc of the domestic chicken (Gallus gallus). The Black grouse BLB genes showed the same level of polymorphism that has been reported in chicken, and we also found indications of balancing selection in the peptide-binding regions. The YLB genes were less variable than the BLB genes, also in accordance with earlier studies in chicken, although their functional significance still remains obscure. We hypothesize that the YLB genes could have been under purifying selection, just as the mammal Mhc-E gene cluster.


Mhc class II YLB Rfp-Y BLB Avian Mhc Purifying selection 



This work was supported by a grant from the Swedish Research Council (VR) to JH. We would like to thank Peter Halvarsson and Kerstin Persson for help and support with the lab work and Martin Carlsson for commenting on a draft of this paper. We also thank three anonymous referees for suggestions on the manuscript.

Supplementary material


  1. Ballingall KT, McKeever DJ (2005) Conservation of promoter, coding and intronic regions of the non-classical MHC class II DYA gene suggests evolution under functional constraints. Anim Genet 36:237–239PubMedCrossRefGoogle Scholar
  2. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evolution Biol 16:363–377CrossRefGoogle Scholar
  3. 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 55:855–865PubMedCrossRefGoogle Scholar
  4. Bourlet Y, Behar G, Guillemot F, Frechin N, Billault A, Chausse AM, Zoorob R, Auffray C (1988) Isolation of chicken major histocompatibility complex class II (B–L) beta-chain sequences—comparison with mammalian beta–chains and expression in lymphoid organs. Embo J 7:1031–1039PubMedGoogle Scholar
  5. Boyson JE, McAdam SN, Gallimore A, Golos TG, Liu XM, Gotch FM, Hughes AL, Watkins DI (1995) The-Mhc E locus in macaques is polymorphic and is conserved between macaques and humans. Immunogenetics 41:59–68PubMedCrossRefGoogle Scholar
  6. Briles WE, Goto RM, Auffray C, Miller MM (1993) A polymorphic system related to but genetically independent of the chicken major histocompatibility complex. Immunogenetics 37:408–414PubMedCrossRefGoogle Scholar
  7. Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC (1993) 3-dimensional structure of the human class-II histocompatibility antigen Hla-Dr1. Nature 364:33–39PubMedCrossRefGoogle Scholar
  8. de Vos GJ (1979) Adaptedness of arena behaviour in black grouse (Tetrao tetrix) and other grouse species (Tetraonidae). Behaviour 68:277–314Google Scholar
  9. Drake BM, Goto RM, Miller MM, Gee GF, Briles WE (1999) Molecular and immunogenetic analysis of major histocompatibility haplotypes in northern bobwhite enable direct identification of corresponding haplotypes in an endangered subspecies, the masked bobwhite. Zoo Biol 18:279–294CrossRefGoogle Scholar
  10. Edwards SV, Gasper J, Garrigan D, Martindale D, Koop BF (2000a) A 39-kb sequence around a blackbird Mhc class II gene: Ghost of selection past and songbird genome architecture. Mol Biol Evol 17:1384–1395PubMedGoogle Scholar
  11. Edwards SV, Nusser J, Gasper J (2000b) Characterization and evolution of Major histocompatibility complex (MHC) genes in non-model organisms, with examples from birds. In: Baker AJ (ed) Molecular methods in ecology. Blackwell, Oxford, pp 168–207Google Scholar
  12. 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 USA 92:12200–12204PubMedCrossRefGoogle Scholar
  13. Ekblom R, Grahn M, Höglund J (2003) Patterns of polymorphism in the MHC class II of a non-passerine bird, the great snipe (Gallinago media). Immunogenetics 54:734–741PubMedGoogle Scholar
  14. Emara MG, Kim H, Zhu J, Lapierre RR, Lakshmanan N, Lillehoj HS (2002) Genetic diversity at the major histocompatibility complex (B) and microsatellite loci in three commercial broiler pure lines. Poultry Sci 81:1609–1617Google Scholar
  15. Freeman-Gallant C, Johnson E, Saponara F, Stanger M (2002) Variation at the major histocompatibility complex in Savannah sparrows. Mol Ecol 11:1125–1130PubMedCrossRefGoogle Scholar
  16. Goto RM, Afanassieff M, Ha J, Iglesias GM, Ewald SJ, Briles WE, Miller MM (2002) Single-strand conformation polymorphism (SSCP) assays for major histocompatibility complex B genotyping in chickens. Poultry Sci 81:1832–1841Google Scholar
  17. Guillemot F, Billault A, Pourquie O, Behar G, Chausse AM, Zoorob R, Kreibich G, Auffray C (1988) A molecular map of the chicken major histocompatibility complex–the class-II beta-genes are closely linked to the class-I genes and the nucleolar organizer. EMBO J 7:2775–2785PubMedGoogle Scholar
  18. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98Google Scholar
  19. Hjorth I (1970) Reproductive behaviour in Tetraonidae. Swed Wildlife (Viltrevy) 7:190–596Google Scholar
  20. Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335:167PubMedCrossRefGoogle Scholar
  21. Hunt HD, Fulton JE (1998) Analysis of polymorphisms in the major expressed class I locus (B-FIV) of the chicken. Immunogenetics 47:456–467PubMedCrossRefGoogle Scholar
  22. Hunt HD, Goto RM, Foster DN, Bacon LD, Miller MM (2006) At least one YMHCI molecule in the chicken is alloimmunogenic and dynamically expressed on spleen cells during development. Immunogenetics 58:297–307PubMedCrossRefGoogle Scholar
  23. Höglund J, Alatalo R (1995) Leks. Princeton University Press, PrincetonGoogle Scholar
  24. Höglund J, Alatalo RV, Lundberg A, Rintamaki PT, Lindell J (1999) Microsatellite markers reveal the potential for kin selection on black grouse leks. Proceedings of the Royal Society Biological Sciences Series B 266:813–816Google Scholar
  25. Jacob JP, Milne S, Beck S, Kaufman J (2000) The major and a minor class II beta-chain (B-LB) gene flank the Tapasin gene in the B-F/B-L region of the chicken major histocompatibility complex. Immunogenetics 51:138–147PubMedCrossRefGoogle Scholar
  26. Jarvi SI, Goto RM, Briles WE, Miller MM (1996) Characterization of Mhc genes in a multigenerational family of ring-necked pheasants. Immunogenetics 43:125–135PubMedCrossRefGoogle Scholar
  27. 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 13:2157–2168PubMedCrossRefGoogle Scholar
  28. Juul-Madsen HR, Dalgaard TS, Guldbrandtsen B, Salomonsen J (2000) A polymorphic major histocompatibility complex class II-like locus maps outside of both the chicken B-system and Rfp-Y-system. Eur J Immunogenet 27:63–71PubMedCrossRefGoogle Scholar
  29. Kaufman J (2000) The simple chicken major histocompatibility complex: life and death in the face of pathogens and vaccines. Philos Trans R Soc Lond, B Biol Sci 355:1077–1084CrossRefGoogle Scholar
  30. Kaufman J, Milne S, Gobel TWF, Walker BA, Jacob JP, Auffray C, Zoorob R, Beck S (1999) The chicken B locus is a minimal essential major histocompatibility complex. Nature 401:923–925PubMedCrossRefGoogle Scholar
  31. Kaufman J, Volk H, Wallny HJ (1995) A minimal essential-Mhc and an unrecognized Mhc-2 extremes in selection for polymorphism. Immunol Rev 143:63–88PubMedCrossRefGoogle Scholar
  32. Knapp LA, Cadavid LF, Watkins DI (1998) The MHC-E locus is the most well conserved of all known primate class I histocompatibility genes. J Immunol 160:189–196PubMedGoogle Scholar
  33. Koivisto I (1965) Behavior of the black grouse, Lyrurus tetrix (L.), during the spring display. Finn Game Res 26:5–60Google Scholar
  34. Koller BH, Geraghty DE, Shimizu Y, DeMars R, Orr HT (1988) HLA-E. A novel HLA class I gene expressed in resting T lymphocytes. J Immunol 141:897–904PubMedGoogle Scholar
  35. Kruiswijk CP, Hermsen T, van Heerwaarden J, Dixon B, Savelkoul HFJ, Stet RJM (2005) Major histocompatibility genes in the Lake Tana African large barb species flock: evidence for complete partitioning of class IIB, but not class I, genes among different species. Immunogenetics 56:894–908PubMedCrossRefGoogle Scholar
  36. Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  37. Lakshmanan N, Gavora JS, Lamont SJ (1997) Major histocompatibility complex class II DNA polymorphisms in chicken strains selected for Marek’s disease resistance and egg production or for egg production alone. Poult Sci 76:1517–1523PubMedGoogle Scholar
  38. Li W-H (1997) Molecular evolution. Sinauer Associates, Sunderland, MAGoogle Scholar
  39. Miller HC, Lambert DM (2004) Gene duplication and gene conversion in class II MHC genes of New Zealand robins (Petroicidae). Immunogenetics 56:178–191PubMedGoogle Scholar
  40. Miller MM, Bacon LD, Hala K, Hunt HD, Ewald SJ, Kaufman J, Zoorob R, Briles WE (2004) Nomenclature for the chicken major histocompatibility (B and Y ) complex. Immunogenetics 56:261–279PubMedGoogle Scholar
  41. Miller MM, Goto RM, Taylor RL, Zoorob R, Auffray C, Briles RW, Briles WE, Bloom SE (1996) Assignment of Rfp-Y to the chicken major histocompatibility complex NOR microchromosome and evidence for high-frequency recombination associated with the nucleolar organizer region. Proc Natl Acad Sci USA 93:3958–3962PubMedCrossRefGoogle Scholar
  42. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426PubMedGoogle Scholar
  43. Paxton RJ, Thoren PA, Tengo J, Estoup A, Pamilo P (1996) Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera, Andrenidae), using microsatellites. Mol Ecol 5:511–519PubMedCrossRefGoogle Scholar
  44. Pharr GT, Dodgson JB, Hunt HD, Bacon LD (1998) Class II MHC cDNAs in 15I(5) B-congenic chickens. Immunogenetics 47:350–354PubMedCrossRefGoogle Scholar
  45. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21PubMedGoogle Scholar
  46. Pyo CW, Williams LM, Moore Y, Hyodo H, Li SS, Zhao LP, Sageshima N, Ishitani A, Geraghty DE (2006) HLA-E, HLA-F, and HLA-G polymorphism: genomic sequence defines haplotype structure and variation spanning the nonclassical class I genes. Immunogenetics 58:241–251PubMedCrossRefGoogle Scholar
  47. Richardson DS, Westerdahl H (2003) MHC diversity in two Acrocephalus species: the outbred Great Reed Warbler and the inbred Seychelles warbler. Mol Ecol 12:3523–3529PubMedCrossRefGoogle Scholar
  48. Rogers S, Shaw I, Ross N, Nair V, Rothwell L, Kaufman J, Kaiser P (2003) Analysis of part of the chicken Rfp-Y region reveals two novel lectin genes, the first complete genomic sequence of a class I alpha-chain gene, a truncated class II beta-chain gene, and a large CR1 repeat. Immunogenetics 55:100–108PubMedGoogle Scholar
  49. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  50. Sacco RE, Rimler RB, Ye X, Nestor KE (2001) Identification of new major histocompatibility complex class II restriction fragment length polymorphisms in a closed experimental line of Beltsville small white turkeys. Poultry Sci 80:1109–1111Google Scholar
  51. Sambrook J, Frotsch E, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbour Laboratory, Cold Springs Harbour, NYGoogle Scholar
  52. Shiina T, Hosomichi K, Hanzawa K (2006) Comparative genomics of the poultry major histocompatibility complex. Anim Sci J 77:151–162CrossRefGoogle Scholar
  53. Shimizu S, Shiina T, Hosomichi K, Takahashi S, Koyama T, Onodera T, Kulski JK, Inoko H (2004) MHC class IIB gene sequences and expression in quails (Coturnix japonica) selected for high and low antibody responses. Immunogenetics 56:280–291PubMedCrossRefGoogle Scholar
  54. Westerdahl H, Wittzell H, von Schantz T (1999) Polymorphism and transcription of Mhc class I genes in a passerine bird, the great reed warbler. Immunogenetics 49:158–170PubMedCrossRefGoogle Scholar
  55. Westerdahl H, Wittzell H, von Schantz T (2000) Mhc diversity in two passerine birds: no evidence far a minimal essential Mhc. Immunogenetics 52:92–100PubMedCrossRefGoogle Scholar
  56. Vincek V, Klein D, Graser RT, Figueroa F, Ohuigin C, Klein J (1995) Molecular-cloning of major histocompatibility complex class-II B-gene cDNA from the Bengalese Finch Lonchura-Striata. Immunogenetics 42:262–267PubMedCrossRefGoogle Scholar
  57. Wittzell H, Vonschantz T, Zoorob R, Auffray C (1995) Rfp-Y-like sequences assort independently of pheasant Mhc genes. Immunogenetics 42:68–71PubMedCrossRefGoogle Scholar
  58. von Schantz T, Wittzell H, Goransson G, Grahn M, Persson K (1996) MHC genotype and male ornamentation: genetic evidence for the Hamilton-Zuk model. Proc R Soc Lond, B Biol Sci 263:265–271CrossRefGoogle Scholar
  59. Zelano B, Edwards SV (2002) An Mhc component to kin recognition and mate choice in birds: Predictions, progress, and prospects. Am Nat 160:S225–S237CrossRefGoogle Scholar
  60. Zoorob R, Behar G, Kroemer G, Auffray C (1990) Organization of a functional chicken class-II B-gene. Immunogenetics 31:179–187PubMedCrossRefGoogle Scholar
  61. Zoorob R, Bernot A, Renoir DM, Choukri F, Auffray C (1993) Chicken major histocompatibility complex class-II B-genes—analysis of interallelic and interlocus sequence variance. Eur J Immunol 23:1139–1145PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Tanja Strand
    • 1
    Email author
  • Helena Westerdahl
    • 2
  • Jacob Höglund
    • 1
  • Rauno V. Alatalo
    • 3
  • Heli Siitari
    • 3
  1. 1.Population Biology and Conservation Biology,Department of Ecology and Evolution, Evolutionary Biology CenterUppsala UniversityUppsalaSweden
  2. 2.Department of Animal EcologyLund UniversityLundSweden
  3. 3.Department of Biological and Environmental ScienceUniversity of JyväskyläJyväskyläFinland

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