Skip to main content
SpringerLink
Log in

Characterization and Evolution of MHC Class II B Genes in Ardeid Birds

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Major histocompatibility complex (MHC) is a multi-gene family that is very suitable to investigate a wide range of open questions in evolutionary ecology. In this study, we characterized two expressed MHC class II B genes (DAB1 and DAB2) in the Grey Heron (Aves: Ardea cinerea). We further developed the primer pairs to amplify and sequence two MHC class II B loci in ten ardeid birds. Phylogenetic analysis revealed that different parts of the genes showed different evolutionary patterns. The exon 2 sequences tended to cluster two gene-specific lineages. In each lineage, exon 2 sequences from several species showed closer relationships than sequences within species, and two shared identical alleles were found between species (Egretta sacra and Nycticorax nycticorax; Egretta garzetta and Bubulcus ibis), supporting the hypothesis of trans-species polymorphism. In contrast, the species-specific intron 2 plus partial exon 3 tree suggested that DAB1 and DAB2 were subject to concerted evolution. GENECONV analyses showed the gene exchange played an important role in the ardeid MHC evolution.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abbas AK, Lichtman AH, Pober JS (2000) Cellular and molecular immunology. W.B. Saunders Company, Philadelphia

    Google Scholar 

  • Aguilar A, Edwards SV, Smith TB, Wayne RK (2006) Patterns of variation in MHC class II B loci of the little greenbul (Andropadus virens) with comments on MHC evolution in birds. J Hered 97:133–142

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Alcaide M, Edwards S, Cadahí L, Negro J (2008) MHC class I genes of birds of prey: isolation, polymorphism and diversifying selection. Conserv Genet 10:1349–1355

    Article  Google Scholar 

  • Balakrishnan CN, Ekblom R, Volker M, Westerdahl H, Godinez R, Kotkiewicz H, Burt DW, Graves T, Griffin DK, Warren WC, Edwards SV (2010) Gene duplication and fragmentation in the zebra finch major histocompatibility complex. BMC Biol 8:29

    Article  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  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bos DH, DeWoody JA (2005) Molecular characterization of major histocompatibility complex class II alleles in wild tiger salamanders (Ambystoma tigrinum). Immunogenetics 57:775–781

    Article  PubMed  CAS  Google Scholar 

  • Brown JW, Payne RB, Mindell DP (2007) Nuclear DNA does not reconcile ‘rocks’ and ‘clocks’ in Neoaves: a comment on Ericson et al. Biol Lett 3(3). doi:10.1098/rsbl.2006.0611

  • Burri R, Niculita-Hirzel H, Roulin A, Fumagalli L (2008) Isolation and characterization of major histocompatibility complex (MHC) class II B genes in the Barn owl (Aves: Tyto alba). Immunogenetics 60:543–550

    Article  PubMed  CAS  Google Scholar 

  • Drouin G, Prat F, Ell M, Clarke GDP (1999) Detecting and characterizing gene conversion events in multigene family members. Mol Biol Evol 16:1369–1390

    PubMed  CAS  Google Scholar 

  • Edwards SV, Grahn M, Potts WK (1995a) Dynamics of Mhc evolution in birds and crocodilians: amplification of class II genes with degenerate primers. Mol Ecol 4:719–729

    Article  PubMed  CAS  Google Scholar 

  • Edwards SV, Wakeland EK, Potts W (1995b) Contrasting histories of avian and mammalian Mhc genes revealed by class II B sequences from songbirds. Proc Natl Acad Sci USA 92:12200–12204

    Article  PubMed  CAS  Google Scholar 

  • Edwards SV, Chesnut K, Satta Y, Wakeland EK (1997) Ancestral polymorphism of MHC class II genes in mice: implications for balancing selection and the mammalian molecular clock. Genetics 146:655–668

    PubMed  CAS  Google Scholar 

  • Edwards SV, Gasper J, Stone M (1998) Genomics and polymorphism of Agph-DAB1, an Mhc class II B gene in red-winged blackbirds (Agelaius phoenicus). Mol Biol Evol 15:236–250

    PubMed  CAS  Google Scholar 

  • Edwards SV, Hess CM, Gaspar J, Garrigan D (1999) Toward and evolutionary genomics of the avian MHC. Immunol Rev 167:119–132

    Article  PubMed  CAS  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 

  • Figueroa F, Gunther E, Klein J (1988) MHC polymorphism predating speciation. Nature 335:265–267

    Article  PubMed  CAS  Google Scholar 

  • Frank SA (2002) Immunology and evolution of infectious disease. Princeton University press, Princeton, Oxford

    Google Scholar 

  • Gasper JS, Shiina T, Inoko H, Edwards SV (2001) Songbird genomics: analysis of 45 kb upstream of a polymorphic MHC class II gene in red-winged blackbirds (Agelaius phoeniceus). Genomics 75:26–34

    Article  PubMed  CAS  Google Scholar 

  • Gu X, Nei M (1999) Locus specificity of polymorphic alleles and evolution by a birth-and-death process in mammalian MHC genes. Mol Biol Evol 16:147–156

    PubMed  CAS  Google Scholar 

  • Guillemot F, Kaufman JF, Skjoedt K, Auffray C (1989) The major histocompatibility complex in the chicken. Trends Genet 5:300–304

    Article  PubMed  CAS  Google Scholar 

  • Hess CM, Edwards SV (2002) The evolution of major histocompatibility genes 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 

  • Huchard E, Cowlishaw G, Raymond M, Weill M, Knapp LA (2006) Molecular study of Mhc-DRB in wild chacma baboons reveals high variability and evidence for trans-species inheritance. Immunogenetics 58:805–816

    Article  PubMed  CAS  Google Scholar 

  • Hughes AL, Yeager M (1998) Natural selection at major histocompatibility complex loci of vertebrates. Annu Rev Genet 32:415–435

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kaufman J, Salomonsen J (1997) The “minimal essential MHC” revisited: Both peptide-binding and cell surface expression level of MHC molecules are polymorphisms selected by pathogens in chickens. Hereditas 127:67–73

    Article  PubMed  CAS  Google Scholar 

  • Kaufman J, Salamonsen J, Flajnik M (1994) Evolutionary conservation of MHC class I and class II molecules-different yet the same. Semin Immunol 6:411–424

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Klein J (1987) Origin of major histocompatibility complex polymorphism: the trans-species hypothesis. Hum Immunol 19:155–162

    Article  PubMed  CAS  Google Scholar 

  • Klein J, Bontrop R, Dawkins RL, Erlich HA, Gryllensten UB, Heise ER, Jones PP, Parham P, Wakeland EK, Watkins DI (1990) Nomenclature for major histocompatibility complexes of different species: a proposal. Immunogenetics 31:217–219

    PubMed  CAS  Google Scholar 

  • Kriener K, O’hUigin C, Klein J (2001) Independent origin of functional MHC class II genes in humans and new world monkeys. Hum Immunol 62:1–14

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Lawlor DA, Ward FE, Ennis PD, Jackson AP, Parham P (1988) HLA-A and HLA-B polymorphism predate the divergence of humans and chimpanzees. Nature 335:268–271

    Article  PubMed  CAS  Google Scholar 

  • Leuchte N, Berry N, Khler B, Almond N, LeGrand R, Thorstenss on R, Titti F, Sauermann U (2004) MhcDRB-sequences from cynomolgus macaques (Macaca fascicularis) of different origin. Tissue Antigens 63:529–537

    Article  PubMed  CAS  Google Scholar 

  • Li WH (1997) Molecular evolution. Sinauer, Sunderland, MA

    Google Scholar 

  • Marchler-Bauer A, Bryant SH (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32:W327–W331

    Article  PubMed  CAS  Google Scholar 

  • Martinsohn JT, Sousa AB, Guethlein LA, Jonathan C, Howard JC (1999) The gene conversion hypothesis of MHC evolution: a review. Immunogenetics 50:168–200

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Miller HC, Lambert DM (2004) Gene duplication and gene conversion in class II MHC genes in New Zealand robins (Petroicidae). Immunogenetics 56:178–191

    PubMed  CAS  Google Scholar 

  • Musolf K, Meyer-Lucht Y, Sommer S (2004) Evolution of MHC-DRB class II polymorphism in the genus Apodemus and a comparison of DRB sequences within the familie Muridae (Mammalia: Rodentia). Immunogenetics 56:420–426

    Article  PubMed  CAS  Google Scholar 

  • Ohta T (1999) Effect of gene conversion on polymorphic patterns at major histocompatibility complex locus. Immunol Rev 167:319–325

    Article  PubMed  CAS  Google Scholar 

  • Otting N, de Groot N, Doxiadis G, Bontrop R (2002) Extensive Mhc-DQB variation in humans and non-human primate species. Immunogenetics 54(4):230–239

    Article  PubMed  CAS  Google Scholar 

  • Parham P, Ohta T (1996) Population biology of antigen presentation by MHC class I molecules. Science 272:67–74

    Article  PubMed  CAS  Google Scholar 

  • Promerová M, Albrecht T, Bryja J (2009) Extremely high MHC class I variation in a population of a long-distance migrant, the Scarlet Rosefinch (Carpodacus erythrinus). Immunogenetics 61:451–461

    Article  PubMed  Google Scholar 

  • Reusch T, Langefors A (2005) Inter- and intralocus recombination drive MHC class IIB gene diversification in a Teleost, the three-spined stickleback Gasterosteus aculeatus. J Mol Evol 61:531–541

    Article  PubMed  CAS  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 12:3523–3529

    Article  PubMed  CAS  Google Scholar 

  • Sato A, Figueroa F, Mayer WE, Grant PR, Grant BR, Klein J (2000) Mhc class II genes of Darwin’s Finches: divergence by point mutations and reciprocal recombination. In: Kasahara M (ed) Major histocompatibility complex: evolution, structure and function. Springer, Berlin

    Google Scholar 

  • Sawyer SA (1999) GENECONV: a computer package for the statistical detection of gene conversion. Distributed by the author, Department of Mathematics, Washington University in St. Louis, St. Louis

    Google Scholar 

  • Schaschl H, Suchentrunk F, Hammer S, Goodman SJ (2005) Recombination and the origin of sequence diversity in the DRB MHC class II locus in chamois (Rupicapra spp.). Immunogenetics 57:108–115. doi:10.1007/s00251-005-0784-4

    Article  PubMed  CAS  Google Scholar 

  • Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95:5857–5864

    Article  PubMed  CAS  Google Scholar 

  • Suárez CF, Patarroyo ME, Trujillo E, Estupin M, Baquero JE, Parra C, Rodriguez R (2006) Owl monkey MHC- DRB exon 2 reveals high similarity with several HLA-DRB lineages. Immunogenetics 58:542–588

    Article  PubMed  Google Scholar 

  • Trowsdale J (1995) ‘Both bird and man and beast’: comparative organization of MHC genes. Immunogenetics 41:1–17

    Article  PubMed  CAS  Google Scholar 

  • Wegner KM, Kalbe M, Rauch G, Kurtz J, Schaschl H, Reusch TBH (2006) Genetic variation in MHC class II expression and interactions with MHC sequence polymorphism in three-spined sticklebacks. Mol Ecol 15:1153–1164

    Article  PubMed  CAS  Google Scholar 

  • 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(3):158–170

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Wittzell H, Bernot A, Auffrey C, Zoorob R (1999) Concerted evolution of two Mhc class II B locus in pheasants and domestic chickens. Mol Biol Evol 16:479–490

    PubMed  CAS  Google Scholar 

  • Xu SX, Sun P, Zhou KY, Yang G (2007) Sequence variability at three MHC loci of finless porpoises (Neophocaena phocaenoides). Immunogenetics 59:581–592

    Article  PubMed  CAS  Google Scholar 

  • Xu SX, Chen BY, Zhou KY, Yang G (2008) High similarity at three MHC loci between the baiji and finless porpoise: trans-species or convergent evolution? Mol Phylogenet Evol 147:36–44

    Article  Google Scholar 

Download references

Acknowledgments

We thank Lin Qingxian for his assistance in samples collection. This research was supported by the National Natural Science Foundation of China (Grant code 30970380 and 40876077), the Fujian Natural Science Foundation of China (Grant code 2009J01195 and 2008S0007) and the Program for Innovative Research Team in Science and Technology in Fujian Province University.

Author information

Authors and Affiliations

  1. Key Laboratory of Ministry of Education for Coast and Wetland Ecosystems School of Life Sciences, Xiamen University, 422, Siming South Rd, Siming, Xiamen, 361005, China

    Li Li, Xiaopin Zhou & Xiaolin Chen

Authors
  1. Li Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaopin Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaolin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Li Li or Xiaolin Chen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 80 kb)

Supplementary material 2 (TIFF 2147 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, L., Zhou, X. & Chen, X. Characterization and Evolution of MHC Class II B Genes in Ardeid Birds. J Mol Evol 72, 474–483 (2011). https://doi.org/10.1007/s00239-011-9446-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-011-9446-3

Keywords

Search

Navigation