Journal of Molecular Evolution

, Volume 72, Issue 5–6, pp 474–483 | Cite as

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

Article

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.

Keywords

MHC II B gene Ardeid birds Trans-species polymorphism Concerted evolution Genetic exchange 

Notes

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.

Supplementary material

239_2011_9446_MOESM1_ESM.doc (80 kb)
Supplementary material 1 (DOC 80 kb)
239_2011_9446_MOESM2_ESM.tif (2.1 mb)
Supplementary material 2 (TIFF 2147 kb)

References

  1. Abbas AK, Lichtman AH, Pober JS (2000) Cellular and molecular immunology. W.B. Saunders Company, PhiladelphiaGoogle Scholar
  2. 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 97:133–142PubMedCrossRefGoogle Scholar
  3. Alcaide M, Edwards S, Negro J (2007) Characterization, polymorphism, and evolution of MHC class II B genes in birds of prey. J Mol Evol 65:541–554PubMedCrossRefGoogle Scholar
  4. Alcaide M, Edwards S, Cadahí L, Negro J (2008) MHC class I genes of birds of prey: isolation, polymorphism and diversifying selection. Conserv Genet 10:1349–1355CrossRefGoogle Scholar
  5. 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 8:29PubMedCrossRefGoogle Scholar
  6. 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
  7. 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 101:448–460PubMedCrossRefGoogle Scholar
  8. 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 55:855–865PubMedCrossRefGoogle Scholar
  9. Bos DH, DeWoody JA (2005) Molecular characterization of major histocompatibility complex class II alleles in wild tiger salamanders (Ambystoma tigrinum). Immunogenetics 57:775–781PubMedCrossRefGoogle Scholar
  10. 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
  11. 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 60:543–550PubMedCrossRefGoogle Scholar
  12. Drouin G, Prat F, Ell M, Clarke GDP (1999) Detecting and characterizing gene conversion events in multigene family members. Mol Biol Evol 16:1369–1390PubMedGoogle Scholar
  13. 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 4:719–729PubMedCrossRefGoogle Scholar
  14. 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 92:12200–12204PubMedCrossRefGoogle Scholar
  15. 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 146:655–668PubMedGoogle Scholar
  16. 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 15:236–250PubMedGoogle Scholar
  17. Edwards SV, Hess CM, Gaspar J, Garrigan D (1999) Toward and evolutionary genomics of the avian MHC. Immunol Rev 167:119–132PubMedCrossRefGoogle Scholar
  18. 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
  19. Figueroa F, Gunther E, Klein J (1988) MHC polymorphism predating speciation. Nature 335:265–267PubMedCrossRefGoogle Scholar
  20. Frank SA (2002) Immunology and evolution of infectious disease. Princeton University press, Princeton, OxfordGoogle Scholar
  21. 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 75:26–34PubMedCrossRefGoogle Scholar
  22. 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 16:147–156PubMedGoogle Scholar
  23. Guillemot F, Kaufman JF, Skjoedt K, Auffray C (1989) The major histocompatibility complex in the chicken. Trends Genet 5:300–304PubMedCrossRefGoogle Scholar
  24. Hess CM, Edwards SV (2002) The evolution of major histocompatibility genes in birds. Bioscience 52:423–431CrossRefGoogle Scholar
  25. 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
  26. 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 58:805–816PubMedCrossRefGoogle Scholar
  27. Hughes AL, Yeager M (1998) Natural selection at major histocompatibility complex loci of vertebrates. Annu Rev Genet 32:415–435PubMedCrossRefGoogle Scholar
  28. Huson H, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267PubMedCrossRefGoogle Scholar
  29. 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 127:67–73PubMedCrossRefGoogle Scholar
  30. Kaufman J, Salamonsen J, Flajnik M (1994) Evolutionary conservation of MHC class I and class II molecules-different yet the same. Semin Immunol 6:411–424PubMedCrossRefGoogle Scholar
  31. 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 401:923–925PubMedCrossRefGoogle Scholar
  32. Klein J (1987) Origin of major histocompatibility complex polymorphism: the trans-species hypothesis. Hum Immunol 19:155–162PubMedCrossRefGoogle Scholar
  33. 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 31:217–219PubMedGoogle Scholar
  34. Kriener K, O’hUigin C, Klein J (2001) Independent origin of functional MHC class II genes in humans and new world monkeys. Hum Immunol 62:1–14PubMedCrossRefGoogle Scholar
  35. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  36. 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 335:268–271PubMedCrossRefGoogle Scholar
  37. 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 63:529–537PubMedCrossRefGoogle Scholar
  38. Li WH (1997) Molecular evolution. Sinauer, Sunderland, MAGoogle Scholar
  39. Marchler-Bauer A, Bryant SH (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32:W327–W331PubMedCrossRefGoogle Scholar
  40. Martinsohn JT, Sousa AB, Guethlein LA, Jonathan C, Howard JC (1999) The gene conversion hypothesis of MHC evolution: a review. Immunogenetics 50:168–200PubMedCrossRefGoogle Scholar
  41. MHC Sequencing Consortium (1999) Complete sequence and gene map of a human major histocompatibility complex. Nature 401:921–923CrossRefGoogle Scholar
  42. Miller HC, Lambert DM (2004) Gene duplication and gene conversion in class II MHC genes in New Zealand robins (Petroicidae). Immunogenetics 56:178–191PubMedGoogle Scholar
  43. 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 56:420–426PubMedCrossRefGoogle Scholar
  44. Ohta T (1999) Effect of gene conversion on polymorphic patterns at major histocompatibility complex locus. Immunol Rev 167:319–325PubMedCrossRefGoogle Scholar
  45. Otting N, de Groot N, Doxiadis G, Bontrop R (2002) Extensive Mhc-DQB variation in humans and non-human primate species. Immunogenetics 54(4):230–239PubMedCrossRefGoogle Scholar
  46. Parham P, Ohta T (1996) Population biology of antigen presentation by MHC class I molecules. Science 272:67–74PubMedCrossRefGoogle Scholar
  47. 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 61:451–461PubMedCrossRefGoogle Scholar
  48. 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 61:531–541PubMedCrossRefGoogle Scholar
  49. Richardson DS, Westerdahl H (2003) MHC diversity in two Acrocephalus species: the outbreed Great reed warbler and the inbred Seychelles warbler. Mol Ecol 12:3523–3529PubMedCrossRefGoogle Scholar
  50. 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, BerlinGoogle Scholar
  51. 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. LouisGoogle Scholar
  52. 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 PubMedCrossRefGoogle Scholar
  53. 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 95:5857–5864PubMedCrossRefGoogle Scholar
  54. 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 58:542–588PubMedCrossRefGoogle Scholar
  55. Trowsdale J (1995) ‘Both bird and man and beast’: comparative organization of MHC genes. Immunogenetics 41:1–17PubMedCrossRefGoogle Scholar
  56. 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 15:1153–1164PubMedCrossRefGoogle Scholar
  57. 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):158–170PubMedCrossRefGoogle Scholar
  58. 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 92:534–542PubMedCrossRefGoogle Scholar
  59. 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 16:479–490PubMedGoogle Scholar
  60. Xu SX, Sun P, Zhou KY, Yang G (2007) Sequence variability at three MHC loci of finless porpoises (Neophocaena phocaenoides). Immunogenetics 59:581–592PubMedCrossRefGoogle Scholar
  61. 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 147:36–44CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Key Laboratory of Ministry of Education for Coast and Wetland Ecosystems School of Life SciencesXiamen UniversityXiamenChina

Personalised recommendations