Skip to main content
Log in

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

  • Original Paper
  • Published:
Immunogenetics Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • 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 17:2652–2665

    Article  PubMed  CAS  Google Scholar 

  • 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 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • 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 20:485–495

    Article  PubMed  Google Scholar 

  • 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 8:29

    Article  PubMed  Google Scholar 

  • Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263–265

    Article  PubMed  CAS  Google Scholar 

  • Begun DJ, Aquadro CF (1992) Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356:519–520

    Article  PubMed  CAS  Google Scholar 

  • Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol 16:363–377

    Article  PubMed  CAS  Google Scholar 

  • Birkhead TR, Pellatt EJ, Brekke P, Yeates R, Castillo-Juarez H (2005) Genetic effects on sperm design in the zebra finch. Nature 434:383–387

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 25:1180–1191

    Article  PubMed  CAS  Google Scholar 

  • Chaves LD, Krueth SB, Reed KM (2007) Characterization of the turkey MHC chromosome through genetic and physical mapping. Cytogenet Gen Res 117:213–220

    Article  CAS  Google Scholar 

  • Chaves L, Faile G, Krueth S, Hendrickson J, Reed K (2010) Haplotype variation, recombination, and gene conversion within the turkey MHC-B locus. Immunogenetics 62:465–477

    Article  PubMed  CAS  Google Scholar 

  • Edwards SV, Hedrick PW (1998) Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 13:305–311

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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

    PubMed  CAS  Google Scholar 

  • Ekblom R, Balakrishnan CN, Burke T, Slate J (2010) Digital gene expression analysis of the zebra finch genome. BMC Genomics 11:219

    Article  PubMed  Google Scholar 

  • Green P, Falls K, Crooks S (1990) Documentation for CRIMAP. Available at http://compgen.rutgers.edu/Crimap/Default.aspx

  • 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 10:137–147

    PubMed  CAS  Google Scholar 

  • Hess CM, Edwards SV (2002) The evolution of the major histocompatibility complex in birds. Bioscience 52:423–431

    Article  Google Scholar 

  • 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 10:613–623

    Article  PubMed  CAS  Google Scholar 

  • 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 7:322

    Article  PubMed  Google Scholar 

  • 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 60:219–231

    Article  PubMed  CAS  Google Scholar 

  • International Chicken Genome Sequencing Consortium (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:695–716

    Article  Google Scholar 

  • 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 10:22

    Article  PubMed  Google Scholar 

  • Kaufman J, Völk H, Wallny HJ (1995) A “minimal essential Mhc” and an “unrecognized MHC”: two extremes in selection for polymorphism. Immunol Rev 143:63–88

    Article  PubMed  CAS  Google Scholar 

  • 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 167:101–117

    Article  PubMed  CAS  Google Scholar 

  • 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 401:923–925

    Article  PubMed  CAS  Google Scholar 

  • Lister R, Gregory BD, Ecker JR (2009) Next is now: new technologies for sequencing of genomes, transcriptomes, and beyond. Curr Opin Plant Biol 12:107–118

    Article  PubMed  CAS  Google Scholar 

  • 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 93:3958–3962

    Article  PubMed  CAS  Google Scholar 

  • 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 56:261–279

    PubMed  CAS  Google Scholar 

  • Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21

    PubMed  CAS  Google Scholar 

  • 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 97:427–437

    Article  PubMed  CAS  Google Scholar 

  • 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 78:629–644

    Article  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 

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

    Article  PubMed  Google Scholar 

  • 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 11:616

    Article  PubMed  Google Scholar 

  • Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2:16

    Article  PubMed  Google Scholar 

  • 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 179:651–667

    Article  PubMed  CAS  Google Scholar 

  • Stapley J, Birkhead TR, Burke T, Slate J (2010) Pronounced inter- and intrachromosomal variation in linkage disequilibrium across the zebra finch genome. Genome Res 20:496–502

    Article  PubMed  CAS  Google Scholar 

  • The MHC Sequencing Consortium (1999) Complete sequence and gene map of a human major histocompatibility complex. Nature 401:921–923

    Article  Google Scholar 

  • 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 53:712–716

    Article  PubMed  CAS  Google Scholar 

  • Warren WC, Clayton DF, Ellegren H et al (2010) The genome of a songbird. Nature 464:757–762

    Article  PubMed  CAS  Google Scholar 

  • Westerdahl H (2007) Passerine MHC: genetic variation and disease resistance in the wild. J Ornithol 148:469–477

    Article  Google Scholar 

  • Wheat C (2010) Rapidly developing functional genomics in ecological model systems via 454 transcriptome sequencing. Genetica 138:433–451

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Andy Krupa for lab assistance. Christopher Balakrishnan kindly shared MHC BAC sequences and provided valuable discussions on our results, and three anonymous reviewers provided valuable comments on a previous version of this manuscript. This work was partially funded by an EC Transfer of Knowledge grant (MAERO) and a BBSRC grant (BB/E017509/1), both awarded to JS.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robert Ekblom.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1

Table with information on all the MHC related SNPs identified in this study (96SNPinfo.xls) (XLS 46 kb)

Online Resource 2

Sequences of all SNPs included in this study (SNPs.fas) (FAS 3 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ekblom, R., Stapley, J., Ball, A.D. et al. Genetic mapping of the major histocompatibility complex in the zebra finch (Taeniopygia guttata). Immunogenetics 63, 523–530 (2011). https://doi.org/10.1007/s00251-011-0525-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-011-0525-9

Keywords

Navigation