Abstract
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.
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References
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 36:237–239
Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evolution Biol 16:363–377
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
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 7:1031–1039
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 41:59–68
Briles WE, Goto RM, Auffray C, Miller MM (1993) A polymorphic system related to but genetically independent of the chicken major histocompatibility complex. Immunogenetics 37:408–414
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 364:33–39
de Vos GJ (1979) Adaptedness of arena behaviour in black grouse (Tetrao tetrix) and other grouse species (Tetraonidae). Behaviour 68:277–314
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 18:279–294
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 17:1384–1395
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 168–207
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 92:12200–12204
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 54:734–741
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 81:1609–1617
Freeman-Gallant C, Johnson E, Saponara F, Stanger M (2002) Variation at the major histocompatibility complex in Savannah sparrows. Mol Ecol 11:1125–1130
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 81:1832–1841
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 7:2775–2785
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
Hjorth I (1970) Reproductive behaviour in Tetraonidae. Swed Wildlife (Viltrevy) 7:190–596
Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335:167
Hunt HD, Fulton JE (1998) Analysis of polymorphisms in the major expressed class I locus (B-FIV) of the chicken. Immunogenetics 47:456–467
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 58:297–307
Höglund J, Alatalo R (1995) Leks. Princeton University Press, Princeton
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 266:813–816
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 51:138–147
Jarvi SI, Goto RM, Briles WE, Miller MM (1996) Characterization of Mhc genes in a multigenerational family of ring-necked pheasants. Immunogenetics 43:125–135
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
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 27:63–71
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 355:1077–1084
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 401:923–925
Kaufman J, Volk H, Wallny HJ (1995) A minimal essential-Mhc and an unrecognized Mhc-2 extremes in selection for polymorphism. Immunol Rev 143:63–88
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 160:189–196
Koivisto I (1965) Behavior of the black grouse, Lyrurus tetrix (L.), during the spring display. Finn Game Res 26:5–60
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 141:897–904
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 56:894–908
Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
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 76:1517–1523
Li W-H (1997) Molecular evolution. Sinauer Associates, Sunderland, MA
Miller HC, Lambert DM (2004) Gene duplication and gene conversion in class II MHC genes of New Zealand robins (Petroicidae). Immunogenetics 56:178–191
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 56:261–279
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 93:3958–3962
Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426
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 5:511–519
Pharr GT, Dodgson JB, Hunt HD, Bacon LD (1998) Class II MHC cDNAs in 15I(5) B-congenic chickens. Immunogenetics 47:350–354
Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21
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 58:241–251
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
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 55:100–108
Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497
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 80:1109–1111
Sambrook J, Frotsch E, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbour Laboratory, Cold Springs Harbour, NY
Shiina T, Hosomichi K, Hanzawa K (2006) Comparative genomics of the poultry major histocompatibility complex. Anim Sci J 77:151–162
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 56:280–291
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 49:158–170
Westerdahl H, Wittzell H, von Schantz T (2000) Mhc diversity in two passerine birds: no evidence far a minimal essential Mhc. Immunogenetics 52:92–100
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 42:262–267
Wittzell H, Vonschantz T, Zoorob R, Auffray C (1995) Rfp-Y-like sequences assort independently of pheasant Mhc genes. Immunogenetics 42:68–71
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 263:265–271
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
Zoorob R, Behar G, Kroemer G, Auffray C (1990) Organization of a functional chicken class-II B-gene. Immunogenetics 31:179–187
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 23:1139–1145
Acknowledgements
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.
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Nucleotide sequence data reported in this paper are submitted to the GenBank database and have the accession numbers EF174539-EF174552.
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Strand, T., Westerdahl, H., Höglund, J. et al. The Mhc class II of the Black grouse (Tetrao tetrix) consists of low numbers of B and Y genes with variable diversity and expression. Immunogenetics 59, 725–734 (2007). https://doi.org/10.1007/s00251-007-0234-6
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DOI: https://doi.org/10.1007/s00251-007-0234-6