Immunogenetics

, Volume 57, Issue 1–2, pp 108–115 | Cite as

Recombination and the origin of sequence diversity in the DRB MHC class II locus in chamois (Rupicapra spp.)

  • Helmut Schaschl
  • Franz Suchentrunk
  • Sabine Hammer
  • Simon J. Goodman
Original Paper

Abstract

We examined the evolutionary processes contributing to genetic diversity at the major histocompatibility complex (MHC) class II DRB locus in chamois (Rupicapra spp., subfamily Caprinae). We characterised the pattern of intragenic recombination (or homologous gene conversion) and quantified the amount of recombination in the genealogical history of the two chamois species, Pyrenean chamois (Rupicapra pyrenaica) and Alpine chamois (Rupicapra rupicapra). We found evidence for intragenic recombination, and the estimated amount of population recombination suggests that recombination has been a significant process in generating DRB allelic diversity in the genealogical history of the genus Rupicapra. Moreover, positive selection appears to act on the same peptide-binding residues in both analysed chamois species, but not in identical intensity. Recombination coupled with positive selection drives the rapid evolution at the peptide-binding sites in the MHC class II DRB gene. Many chamois MHC class II DRB alleles are thus much younger than previously assumed.

Keywords

MHC class II diversity Chamois Recombination Allelic polymorphism 

Notes

Acknowledgements

We would like to thank TBH Reusch from the Max-Planck Institute of Limnology for helpful comments on a previous version of this manuscript and A Hasselmeyer for assistance in sequencing.

References

  1. Andersson L, Mikko S (1995) Generation of MHC class II diversity by intra- and intergenic recombination. Immunol Rev 143:5–12Google Scholar
  2. Anisimova M, Nielsen R, Yang Z (2003) Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164:1229–1236PubMedGoogle Scholar
  3. Apanius V, Penn D, Slev PR, Ruff LR, Potts WK (1997) The nature of selection of the major histocompatibility complex. Crit Rev Immunol 17:179–224PubMedGoogle Scholar
  4. Awadalla P, Eyre-Walker AA, Maynard Smith J (1999) Linkage disequilibrium and recombination in hominid mitochondrial DNA. Science 286:2524–2525Google Scholar
  5. Bergstrom TF, Josefsson A, Erlich HA, Gyllensten U (1998) Recent origin of HLA-DRB1 alleles and implications for human evolution. Nat Genet 18:237–242Google Scholar
  6. Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 64:33–39Google Scholar
  7. Fearnhead P, Donnelly P (2001) Estimating recombination rates from population genetic data. Genetics 159:1299–1318Google Scholar
  8. Go Y, Satta Y, Kawamoto Y, Rakotoarisoa G, Randrianjafy A, Koyama N, Hirai H (2002) Mhc-DRB genes evolution in lemurs. Immunogenetics 54:403–417Google Scholar
  9. Gutierrez-Espeleta G, Hedrik PW, Kalinowski ST, Garrigan D, Boyce WM (2001) Is the decline of desert bighorn sheep from infectious disease the result of low MHC variation? Heredity 86:439–450Google Scholar
  10. Gyllensten UB, Sundvall M, Erlich HA (1991) Allelic diversity is generated by intraexon sequence exchange at the DRB1 locus of primates. Proc Natl Acad Sci USA 88:3686–3690Google Scholar
  11. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor an analysis program for Windows 96/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  12. Hammer S, Nadlinger K, Hartl GB (1995) Mitochondrial DNA differentiation in chamois (genus Rupicapra): implication for taxonomy, conservation, and management. Acta Theriol [Suppl 3]:145–155Google Scholar
  13. Hedrick PW, Parker KM, Gutierrez Espeleta GA, Rattink A, Lievers K (2000) Major histocompatibility complex variation in the Arabian oryx. Evolution 54:2145–2151Google Scholar
  14. Hudson RR (2001) Two-locus sampling distributions and their application. Genetics 159:1805–1817Google Scholar
  15. Hughes AL, Yeager M (1998) Natural selection at major histocompatibility complex loci of vertebrates. Annu Rev Genet 32:415–435CrossRefPubMedGoogle Scholar
  16. Janeway CA, Travers P, Walport M Capra JD (2001) Immunobiology: the immune system in health and disease, 5th edn. Garland, EdinburghGoogle Scholar
  17. Jugo BM, Vicario A (2000) Single-strand conformational polymorphism and sequence polymorphism of Mhc-DRB in Latxa and Karrantzar sheep: implication for Caprinae phylogeny. Immunogenetics 51:887–897Google Scholar
  18. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic, pp 21–32Google Scholar
  19. Karlin S, Altschul SF (1990) Methods for assessing the statistical significance of molecular sequences by using general scoring schemes. Proc Natl Acad Sci USA 87:2264–2268Google Scholar
  20. Klein J, O’hUigin C (1995) Class IIB Mhc motifs in an evolutionary perspective. Immunol Rev 143:89–111Google Scholar
  21. Klein J, Bontrop RE, Dawkins RL, Erlich HA, Gyllensten UB, Heise ER, Jones PP, Parham P, Wakeland EK, Watkins DI (1990) Nomenclature for the major histocompatibility complexes of different species: a proposal. Immunogenetics 31:217–219PubMedGoogle Scholar
  22. Klein JN, Takahata N, Ayala FJ (1993) Mhc diversity and human origins. Sci Am 269:46–51Google Scholar
  23. Kumar S, Tamura K, Jokobsen I, Nei M (2001) MEGA 2.1: Molecular evolutionary genetics analysis software. Version 2.1. Arizona State University, TempeGoogle Scholar
  24. León-Vizcaíno L, Ruíz de Ybáñz MR, Cubero MJ, Ortíz JM, Espinosa J, Pérez L, Simón MA, Alonso F (1999) Sarcoptic mange in Spanish Ibex from Spain. J Wildlife Dis 35:647–659Google Scholar
  25. Lovari S (1987) Evolutionary aspects of the biology of chamois, Rupicapra spp. (Bovidae, Caprinae). In: Soma H (ed) The biology and management of Capricornis and related mountain antelopes. Croom–Helm, London, pp 51–61Google Scholar
  26. Masini F, Lovari S (1988) Systematics, phylogenetic relationship and dispersal of the chamois (Rupicapra spp.) Quaternary Res 30:339–349Google Scholar
  27. McVean GAT, Awadalla P, Fearnhead P (2002) A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160:1231–1241Google Scholar
  28. McVean GAT, Myers SR, Hunt S, Deloukas P, Bentley DR, Donnelly P (2004) The fine-scale structure of recombination rate variation in the human genome. Science 304:581–584CrossRefPubMedGoogle Scholar
  29. Mikko S, Andersson L (1995) Low major histocompatibility complex class II diversity in European and North American moose. Proc Natl Acad Sci USA 92:4259–4263Google Scholar
  30. Mikko S, Roed K, Schmutz S, Andersson L (1999) Monomorphism and polymorphism at Mhc DRB loci in domestic and wild ruminants. Immunol Rev 167:169–178Google Scholar
  31. Nascetti G, Lovari S, Lanfranchi P, Berducou C, Mattiucci S, Rossi L, Bullini L (1985) Revision of Rupicapra genus III: electrophoretic studies demonstrating species distinction of chamois populations of the Alps from those of the Apennines and Pyrenees. In: Lovari S (ed) Biology and management of mountain ungulates. Croom–Helm, London, pp 57–62Google Scholar
  32. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and non-synonymous nucleotide substitutions. Mol Biol Evol 3:418–426PubMedGoogle Scholar
  33. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, OxfordGoogle Scholar
  34. Nielsen R, Yang Z (1998) Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148:929–936PubMedGoogle Scholar
  35. O’hUigin C (1995) Quantifying the degree of convergence in primate Mhc-DRB genes. Immunol Rev 143:123–140Google Scholar
  36. Pérez TM, Albornoz J, Domínguez A (2002) Phylogeography of chamois (Rupicapra spp.) inferred from microsatellites. Mol Phylogenet Evol 25:524–534Google Scholar
  37. Posada D (2002) Evaluation of methods for detecting recombination from DNA sequences: empirical data. Mol Biol Evol 19:708–717PubMedGoogle Scholar
  38. Richman AD, Herrera LG, Nash D (2003a) Evolution of MHC class II Eβ diversity within the genus Peromyscus. Genetics 164:197–289Google Scholar
  39. Richman AD, Herrera LG, Nash D, Schierup HM (2003b) Relative roles of mutation and recombination in generating allelic polymorphism at an MHC class II locus in Peromyscus maniculatus. Genet Res Camb 82:89–99CrossRefGoogle Scholar
  40. Robinson J, Waller MJ, Parham P, de Groot N, Bontrop R, Kennedy LJ, Stoehr P, Marsh SGE (2003) IMGT/HLA and IMGT/MHC: sequence databases for the study of the major histocompatibility complex. Nucleic Acids Res 31:311–314CrossRefPubMedGoogle Scholar
  41. Rossi L, Meneguz PG, De Martin P, Rodolfi M (1995) The epizootiology of sarcoptic mange in Chamois Rupicapra rupicapra, from the Italian Eastern Alps. Parassitologia 37:233–240Google Scholar
  42. Sägesser H, Krapp F (1986) Rupicapra rupicapra (Linnaeus, 1758), Gämse In: Niethammer J, Krapp F (eds) Handbuch der Säugetiere Europas. Aula Verlag, Wiesbaden, pp 316–348Google Scholar
  43. Sawyer SA (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538Google Scholar
  44. Sawyer SA (1999) GENECONV: a computer package for statistical detection of gene conversion. Available at http://www.math.wustl.edu/~sawyer/mbprogs/.
  45. Schaschl H, Kaulfus D, Hammer S, Suchentrunk F (2003) Spatial patterns of mitochondrial and nuclear gene pools in Chamois (Rupicapra r. rupicapra) from the Eastern Alps. Heredity 91:125–135Google Scholar
  46. Schaschl H, Goodman SJ, Suchentrunk F (2004) Sequence analysis of the MHC class II DRB alleles in Alpine chamois (Rupicapra r. rupicapra). Dev Comp Immunol 28:265–277Google Scholar
  47. Schierup MH, Hein J (2000) Consequences of recombination on traditional phylogenetic analysis. Genetics 156:879–891Google Scholar
  48. Schmulder MJM, Snoek LB, Booy G, Vosman B (2003) Complete loss of MHC genetic diversity in the common hamster (Cricetus cricetus) population in The Netherlands: consequences for conservation strategies. Conserv Genetics 4:441–451Google Scholar
  49. Shackleton DM (1997) Wild sheep and goats and their relatives: status survey and conservation action plan for Caprinae. IUCN/SSC Caprinae specialist group, GlandGoogle Scholar
  50. Takahata N, Satta Y (1998) Selection, convergence, and intragenic recombination in HLA diversity. Genetica 157:157–169Google Scholar
  51. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  52. Van Den Bussche RA, Hoofer SR, Lochmilr RL (1999) Characterisation of Mhc-DRB allelic diversity in white-tailed deer (Odocoileus virginianus) provides insight into Mhc-DRB allelic evolution within Cervidae. Immunogenetics 49:429–437CrossRefPubMedGoogle Scholar
  53. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Cabios 13:555–556PubMedGoogle Scholar
  54. Yang Z, Nielsen R, Goldman N, Pedersen A-MK (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Helmut Schaschl
    • 1
    • 4
  • Franz Suchentrunk
    • 2
  • Sabine Hammer
    • 3
  • Simon J. Goodman
    • 1
  1. 1.Institute of ZoologyZoological Society of LondonLondonUK
  2. 2.Research Institute of Wildlife EcologyUniversity of Veterinary Medicine ViennaViennaAustria
  3. 3.Laboratories of Genome DynamicsMedical University of ViennaViennaAustria
  4. 4.Department of Evolutionary EcologyMax-Planck-Institute of LimnologyPloenGermany

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