Immunogenetics

, Volume 63, Issue 8, pp 523–530

Genetic mapping of the major histocompatibility complex in the zebra finch (Taeniopygia guttata)

  • Robert Ekblom
  • Jessica Stapley
  • Alex D. Ball
  • Tim Birkhead
  • Terry Burke
  • Jon Slate
Original Paper
  • 391 Downloads

Abstract

Genes of the major histocompatibility complex (MHC) have received much attention in immunology, genetics, and ecology because they are highly polymorphic and play important roles in parasite resistance and mate choice. Until recently, the MHC of passerine birds was not well-described. However, the genome sequencing of the zebra finch (Taeniopygia guttata) has partially redressed this gap in our knowledge of avian MHC genes. Here, we contribute further to the understanding of the zebra finch MHC organization by mapping SNPs within or close to known MHC genes in the zebra finch genome. MHC class I and IIB genes were both mapped to zebra finch chromosome 16, and there was no evidence that MHC class I genes are located on chromosome 22 (as suggested by the genome assembly). We confirm the location in the MHC region on chromosome 16 for several other genes (BRD2, FLOT1, TRIM7.2, GNB2L1, and CSNK2B). Two of these (CSNK2B and FLOT1) have not previously been mapped in any other bird species. In line with previous results, we also find that orthologs to the immune-related genes B-NK and CLEC2D, which are part of the MHC region in chicken, are situated on zebra finch chromosome Z and not among other MHC genes in the zebra finch.

Keywords

MHC Bird Chromosome Linkage map SNP 

Supplementary material

251_2011_525_MOESM1_ESM.xls (46 kb)
Online Resource 1Table with information on all the MHC related SNPs identified in this study (96SNPinfo.xls) (XLS 46 kb)
251_2011_525_MOESM2_ESM.fas (4 kb)
Online Resource 2Sequences of all SNPs included in this study (SNPs.fas) (FAS 3 kb)

References

  1. Alcaide M, Edwards SV, Negro JJ, Serrano D, Tella JL (2008) Extensive polymorphism and geographical variation at a positively selected MHC class II B gene of the lesser kestrel (Falco naumanni). Mol Ecol 17:2652–2665PubMedCrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  3. Backström N, Forstmeier W, Schielzeth H, Mellenius H, Nam K, Bolund E, Webster MT, Öst T, Schneider M, Kempenaers B, Ellegren H (2010) The recombination landscape of the zebra finch Taeniopygia guttata genome. Genome Res 20:485–495PubMedCrossRefGoogle Scholar
  4. Balakrishnan C, Ekblom R, Volker M, Westerdahl H, Godinez R, Kotkiewicz H, Burt D, Graves T, Griffin D, Warren W, Edwards S (2010) Gene duplication and fragmentation in the zebra finch major histocompatibility complex. BMC Biol 8:29PubMedCrossRefGoogle Scholar
  5. Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263–265PubMedCrossRefGoogle Scholar
  6. Begun DJ, Aquadro CF (1992) Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356:519–520PubMedCrossRefGoogle Scholar
  7. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol 16:363–377PubMedCrossRefGoogle Scholar
  8. Birkhead TR, Pellatt EJ, Brekke P, Yeates R, Castillo-Juarez H (2005) Genetic effects on sperm design in the zebra finch. Nature 434:383–387PubMedCrossRefGoogle Scholar
  9. 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
  10. Burri R, Hirzel HN, Salamin N, Roulin A, Fumagalli L (2008) Evolutionary patterns of MHC class II B in owls and their implications for the understanding of avian MHC evolution. Mol Biol Evol 25:1180–1191PubMedCrossRefGoogle Scholar
  11. Chaves LD, Krueth SB, Reed KM (2007) Characterization of the turkey MHC chromosome through genetic and physical mapping. Cytogenet Gen Res 117:213–220CrossRefGoogle Scholar
  12. Chaves L, Faile G, Krueth S, Hendrickson J, Reed K (2010) Haplotype variation, recombination, and gene conversion within the turkey MHC-B locus. Immunogenetics 62:465–477PubMedCrossRefGoogle Scholar
  13. Edwards SV, Hedrick PW (1998) Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 13:305–311PubMedCrossRefGoogle Scholar
  14. Ekblom R, Galindo J (2011) Applications of next generation sequencing in molecular ecology of non-model organisms. Hered Adv. doi:10.1038/hdy.2010.152 Google Scholar
  15. 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
  16. Ekblom R, Balakrishnan CN, Burke T, Slate J (2010) Digital gene expression analysis of the zebra finch genome. BMC Genomics 11:219PubMedCrossRefGoogle Scholar
  17. Green P, Falls K, Crooks S (1990) Documentation for CRIMAP. Available at http://compgen.rutgers.edu/Crimap/Default.aspx
  18. Groenen MAM, Cheng HH, Bumstead N, Benkel BF, Briles WE, Burke T, Burt DW, Crittenden LB, Dodgson J, Hillel J, Lamont S, de Leon AP, Soller M, Takahashi H, Vignal A (2000) A consensus linkage map of the chicken genome. Genome Res 10:137–147PubMedGoogle Scholar
  19. Hess CM, Edwards SV (2002) The evolution of the major histocompatibility complex in birds. Bioscience 52:423–431CrossRefGoogle Scholar
  20. Hess CM, Gasper J, Hoekstra HE, Hill CE, Edwards SV (2000) MHC class II pseudogene and genomic signature of a 32-kb cosmid in the house finch (Carpodacus mexicanus). Genome Res 10:613–623PubMedCrossRefGoogle Scholar
  21. Hosomichi K, Shiina T, Suzuki S, Tanaka M, Shimizu S, Iwamoto S, Hara H, Yoshida Y, Kulski J, Inoko H, Hanzawa K (2006) The major histocompatibility complex (Mhc) class IIB region has greater genomic structural flexibility and diversity in the quail than the chicken. BMC Genomics 7:322PubMedCrossRefGoogle Scholar
  22. Hughes C, Miles S, Walbroehl J (2008) Support for the minimal essential MHC hypothesis: a parrot with a single, highly polymorphic MHC class II B gene. Immunogenetics 60:219–231PubMedCrossRefGoogle Scholar
  23. International Chicken Genome Sequencing Consortium (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:695–716CrossRefGoogle Scholar
  24. Jaramillo-Correa J, Verdu M, Gonzalez-Martinez S (2010) The contribution of recombination to heterozygosity differs among plant evolutionary lineages and life-forms. BMC Evol Biol 10:22PubMedCrossRefGoogle Scholar
  25. Kaufman J, Völk H, Wallny HJ (1995) A “minimal essential Mhc” and an “unrecognized MHC”: two extremes in selection for polymorphism. Immunol Rev 143:63–88PubMedCrossRefGoogle Scholar
  26. Kaufman J, Jacob J, Shaw J, Walker B, Milne S, Beck S, Salomonsen J (1999a) Gene organisation determines evolution of function in the chicken MHC. Immunol Rev 167:101–117PubMedCrossRefGoogle Scholar
  27. Kaufman J, Milne S, Göbel TWF, Walker BA, Jacob JP, Auffray C, Zoorob R, Beck S (1999b) The chicken B locus is a minimal essential major histocompatibility complex. Nature 401:923–925PubMedCrossRefGoogle Scholar
  28. Lister R, Gregory BD, Ecker JR (2009) Next is now: new technologies for sequencing of genomes, transcriptomes, and beyond. Curr Opin Plant Biol 12:107–118PubMedCrossRefGoogle Scholar
  29. Miller MM, Goto RM, Taylor RL, Zoorob R, Auffray C, Briles RW, Briles E, 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
  30. Miller MM, Bacon LD, Hala K, Hunt HD, Ewald SJ, Kaufman J, Zoorob R, Briles WE (2004) 2004 Nomenclature for the chicken major histocompatibility (B and Y) complex. Immunogenetics 56:261–279PubMedGoogle Scholar
  31. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21PubMedGoogle Scholar
  32. Schaschl H, Wandeler P, Suchentrunk F, Obexer-Ruff G, Goodman SJ (2006) Selection and recombination drive the evolution of MHC class II DRB diversity in ungulates. Heredity 97:427–437PubMedCrossRefGoogle Scholar
  33. Scheet P, Stephens M (2006) A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet 78:629–644PubMedCrossRefGoogle Scholar
  34. Shiina T, Hosomichi K, Hanzawa K (2006) Comparative genomics of the poultry major histocompatibility complex. Anim Sci J 77:151–162CrossRefGoogle Scholar
  35. Skjødt K, Koch C, Crone M, Simonsen M (1985) Analysis of chickens for recombination within the MHC (B-complex). Tissue Antigens 25:278–282PubMedCrossRefGoogle Scholar
  36. Solinhac R, Leroux S, Galkina S, Chazara O, Feve K, Vignoles F, Morisson M, Derjusheva S, Bed’hom B, Vignal A, Fillon V, Pitel F (2010) Integrative mapping analysis of chicken microchromosome 16 organization. BMC Genomics 11:616PubMedCrossRefGoogle Scholar
  37. Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2:16PubMedCrossRefGoogle Scholar
  38. Stapley J, Birkhead TR, Burke T, Slate J (2008) A linkage map of the zebra finch Taeniopygia guttata provides new insights into avian genome evolution. Genetics 179:651–667PubMedCrossRefGoogle Scholar
  39. Stapley J, Birkhead TR, Burke T, Slate J (2010) Pronounced inter- and intrachromosomal variation in linkage disequilibrium across the zebra finch genome. Genome Res 20:496–502PubMedCrossRefGoogle Scholar
  40. The MHC Sequencing Consortium (1999) Complete sequence and gene map of a human major histocompatibility complex. Nature 401:921–923CrossRefGoogle Scholar
  41. Tsuda TT, Tsuda M, Naruse T, Kawata H, Ando A, Shiina T, Fukuda M, Kurita M, LeMaho I, Kulski JK, Inoko H (2001) Phylogenetic analysis of penguin (Spheniscidae) species based on sequence variation in MHC class II genes. Immunogenetics 53:712–716PubMedCrossRefGoogle Scholar
  42. Warren WC, Clayton DF, Ellegren H et al (2010) The genome of a songbird. Nature 464:757–762PubMedCrossRefGoogle Scholar
  43. Westerdahl H (2007) Passerine MHC: genetic variation and disease resistance in the wild. J Ornithol 148:469–477CrossRefGoogle Scholar
  44. Wheat C (2010) Rapidly developing functional genomics in ecological model systems via 454 transcriptome sequencing. Genetica 138:433–451PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Robert Ekblom
    • 1
    • 2
  • Jessica Stapley
    • 2
  • Alex D. Ball
    • 2
    • 3
  • Tim Birkhead
    • 2
  • Terry Burke
    • 2
  • Jon Slate
    • 2
  1. 1.Department of Population Biology and Conservation BiologyUppsala UniversityUppsalaSweden
  2. 2.Department of Animal and Plant SciencesUniversity of SheffieldSheffieldUK
  3. 3.Department of Biology and BiochemistryUniversity of BathBathUK

Personalised recommendations