Skip to main content

Advertisement

SpringerLink
Log in

Evidence for multiple MHC class II β loci in New Zealand’s critically endangered kakapo, Strigops habroptilus

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

Abstract

Immunologically important genes of the major histocompatibility complex (MHC) have been characterized in a number of avian species with the general finding of considerable variation in size and structural organization among organisms. A range of nonpasserines which represent early-diverging Neoave lineages have been described as having only one MHC class II β locus potentially leading to the conclusion that this is the ancestral condition. Here, we examine the monotypic, early-diverging, critically endangered kakapo, Strigops habroptilus, for allelic variation at MHC class II β exon 2, as part of species’ recovery efforts. We found two to four confirmed sequence variants per individual indicating the presence of more than one MHC class II β locus. Given the kakapo’s basal evolutionary status, evidence for multiple MHC class II β loci seems to counter the proposed mono-locus history of modern birds. However, MHC gene duplication, maintenance, and loss among and within bird species may confound avian relationships making it difficult to elucidate the ancestral state. This study adds essential data for disentangling the course of MHC structural evolution in birds.

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

Access this article

Log in via an institution

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 (2007) Characterization, polymorphism and evolution of MHC class II B genes in birds of prey. J Mol Evol 65:541–554

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Bollmer JL, Herna Vargas F, Parker PG (2007) Low MHC variation in the endangered Galapagos penguin (Spheniscus mendiculus). Immunogenetics 59:593–602

    Article  CAS  PubMed  Google Scholar 

  • Bollmer JL, Dunn PO, Whittingham LA, Wimpee C (2010) Extensive MHC class II B gene duplication in a passerine, the common yellowthroat (Geothlypis trichas). J Hered 101:448–460

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Edwards SV, Nusser J, Gasper J (2000) 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

    Google Scholar 

  • Galan M, Guivier E, Caraux G, Charbonnel N, Cosson J-F (2010) A 454 multiplex sequencing method for rapid and reliable genotyping of highly polymorphic genes in large-scale studies. BMC Genomics 11:296

    Article  PubMed Central  PubMed  Google Scholar 

  • Gibb GC, Kardailsky O, Kimball RT, Braun EL, Penny D (2007) Mitochondrial genomes and avian phylogeny: complex characters and resolvability without explosive radiations. Mol Biol Evol 24:269–280

    Article  CAS  PubMed  Google Scholar 

  • Gyllensten U, Sundvall M, Ezcurra I, Erlich HA (1991) Genetic diversity at class II DRB loci of the primate MHC. J Immunol 146:4368

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Hedrick PW (1994) Evolutionary genetics of the major histocompatibility complex. Am Nat 143:945–964

    Article  Google Scholar 

  • Holt KE, Parkhill J, Mazzoni CJ, Roumagnac P, Weill FX et al (2008) Highthroughput sequencing provides insights into genome variation and evolution in Salmonella typhi. Nat Genet 40:987–993

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hughes CR, Miles S, Walbroehl JM (2008) Support for the minimal essential MHC hypothesis: a parrot with a single, highly polymorphic MHC class IIB gene. Immunogenetics 60:219–231

    Article  CAS  PubMed  Google Scholar 

  • Huson D (1998) SplitsTree: a progam for analyzing and visualizing evolutionary data. Bioinformatics 14:68–73

    Article  CAS  PubMed  Google Scholar 

  • Huson D, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kaufman J, Milne S, Göbel T, Walker BA, Jacob JP, Auffrey C, Zoorob R, Beck S (1999) The chicken B locus is a minimal-essential major histocompatibility complex. Nature 401:923–925

    Article  CAS  PubMed  Google Scholar 

  • Klein J, Sato A, Nagl S, O’hUigin C (1998) Molecular trans-species polymorphism. Annu Rev Ecol Syst 29:1–21

    Article  Google Scholar 

  • Kryazhimskiy S, Plotkin JB (2008) The population genetics of dN/dS. PLoS Genet 4:e1000304

    Article  PubMed Central  PubMed  Google Scholar 

  • Lenz T, Becker S (2008) Simple approach to reduce PCR artifact formation leads to reliable genotyping of MHC and other highly polymorphic loci—implications for evolutionary analysis. Gene 427:117–123

    Article  CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DNAsp v 5: A software for computational analysis of DNA polymorphism Data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • McCormack WT, Hurley EA, Thompson CB (1993) Germ line maintenance of the pseudogene donor pool for somatic immunoglobulin gene conversion in chickens. Mol Cell Biol 13:821–830

    CAS  PubMed Central  PubMed  Google Scholar 

  • Miller HC, Lambert DM, Millar CD, Robertson BC, Minot EO (2003) Minisatellite DNA profiling detects lineages and parentage in the endangered kakapo (Strigops habroptilus) despite low microsatellite DNA variation. Conserv Genet 4:265–273

    Article  CAS  Google Scholar 

  • Miller HC, Bowker-Wright G, Kharkrang M, Ramstad K (2011) Characterisation of class II B MHC genes from a ratite bird, the little spotted kiwi (Apteryx owenii). Immunogenetics 63:223–233

    Article  CAS  PubMed  Google Scholar 

  • Moon DA, Veniamin SM, Parks-Dely JA, Magor KE (2005) The MHC of the duck (Anas platyrhynchos) contains five differentially expressed class I genes. J Immunol 175:6702–6712

    CAS  PubMed  Google Scholar 

  • Nei M, Gu X, Sitnikova T (1997) Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci U S A 94:7799–7806

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Powlesland RG, Merton DV, Cockrem JF (2006) A parrot apart: the natural history of the kakapo (Strigops habroptilus), and the context of its conservation. Notornis 53:3–26

    Google Scholar 

  • Pratt RC, Gibb GC, Morgan-Richards M, Phillips MJ, Hendy MD, Penny D (2009) Toward resolving deep neoaves phylogeny: data, signal enhancement, and priors. Mol Biol Evol 26:313–326

    Article  CAS  PubMed  Google Scholar 

  • Richardson DS, Westerdahl H (2003) MHC diversity in two Acrocephalus species: the outbreed Great reed Warbler and the inbred Seychelles warbler. Mol Ecol 12:3253–3259

    Article  Google Scholar 

  • Robertson BC (2006) The role of genetics in kakapo recovery. Notornis 53:173–183

    Google Scholar 

  • Robertson BC, Minot EO, Lambert DM (2000) Microsatellite primers for the kakapo (Strigops habroptilus) and their utility in other parrots. Cons Gen 1:93–95

    Article  CAS  Google Scholar 

  • Sawyer SA (1999) GENECONV: a computer package for the statistical detection of gene conversion. [Internet]. St. Louis (MO): Distributed by the author, Department of Mathematics, Washington University Available from: http://www.math.wustl.edu/;sawyer. Accessed 5 Oct 2013

  • 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  CAS  PubMed  Google Scholar 

  • Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analysis. Can J Zool 69:82–90

    Google Scholar 

  • Shiina T, Shimizu S, Hosomichi K, Kohara S, Watanabe S, Hanzawa K, Beck S, Kulski JK, Inoko H (2004) Comparative genomic analysis of two avian (quail and chicken) MHC regions. J Immunol 172:6751–6763

    CAS  PubMed  Google Scholar 

  • Suh A, Paus M, Kiefmann M, Churakov G, Franke FA, Brosius J, Kriegs JO, Schmitz J (2011) Mesozoic retroposons reveal parrots as the closest living relatives of passerine birds. Nat Commun 2:443. doi:10.1038/ncomms1448

    Article  PubMed Central  PubMed  Google Scholar 

  • Sutton JT, Nakagawa S, Robertson BC, Jamieson IG (2011) Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes. Mol Ecol 20:4408–4420

    Article  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513

    CAS  PubMed  Google Scholar 

  • Wang Z, Zhou X, Lin Q, Fang W, Chen X (2013) Characterization, polymorphism and selection of major histocompatibility complex (MHC) DAB genes in vulnerable Chinese egret (Egretta eulophotes). PLoS ONE 8:e74185. doi:10.1371/journal.pone.0074185

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Westerdahl H, Wittzell H, von Schantz T, Bensch S (2004) MHC class I typing in a songbird with numerous loci and high polymorphism using motif-specific PCR and DGGE. Heredity 92:534–542. doi:10.1038/sj.hdy.6800450

    Article  CAS  PubMed  Google Scholar 

  • Wright TF, Schirtzinger EE, Matsumoto T, Eberhard JR, Graves GR, Snachez JJ, Capelli S, Müller H, Sharpegge J, Chambers G, Fleischer RC (2008) A multilocus molecular phylogeny of the parrots (Psittaciformes): support for a Gondwanan origin during the Cretaceous. Mol Biol Evol 25:2141–2156. doi:10.1093/molbev/msn160

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Thanks to the National Kakapo Team members for collecting the blood samples for DNA analysis. We thank P. Jameson and N. Gemmell for use of laboratory space at the University of Canterbury at the beginning of the study. We are grateful to F. Robertson for assistance with lab work at Otago University and C. Grueber for helpful comments on earlier drafts of the manuscript. Cloning of the kakapo, kea, and kaka MHC was done under ERMA application GMD07039. Funding for this research was provided by the Department of Conservation Kakapo Recovery Group, McKee Trust (funding to BCR) and the Allan Wilson Centre (funding to IGJ). GK was supported by a University of Otago PhD Scholarship.

Author information

Authors and Affiliations

  1. Allan Wilson Centre for Molecular Ecology and Evolution, Department of Zoology, University of Otago, Dunedin, New Zealand

    Gabrielle J. Knafler, Ian G. Jamieson & Bruce C. Robertson

  2. Cawthron Institute, Private Bag 2, Nelson, 7012, New Zealand

    Andrew Fidler

  3. Department of Zoology, University of Otago, PO Box 56, Dunedin, 9054, New Zealand

    Bruce C. Robertson

Authors
  1. Gabrielle J. Knafler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrew Fidler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ian G. Jamieson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bruce C. Robertson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bruce C. Robertson.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 64 kb)

ESM 2

(DOCX 164 kb)

ESM 3

(DOCX 14.1 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Knafler, G.J., Fidler, A., Jamieson, I.G. et al. Evidence for multiple MHC class II β loci in New Zealand’s critically endangered kakapo, Strigops habroptilus . Immunogenetics 66, 115–121 (2014). https://doi.org/10.1007/s00251-013-0750-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-013-0750-5

Keywords

Search

Navigation