Hydrobiologia

, 638:11 | Cite as

High allelic variation of MHC class II alpha antigen and the role of selection in wild and cultured Sparus aurata populations

  • Nikoleta Karaiskou
  • Paloma Moran
  • George Georgitsakis
  • Theodore J. Abatzopoulos
  • Alexander Triantafyllidis
Primary research paper
First Online:
Received:
Revised:
Accepted:

Abstract

Genetic polymorphism and differentiation in wild and cultured sea bream samples were studied after amplification, cloning, and partial sequence of the major histocompatibility complex (MHC) class II alpha antigen. Forty-one alleles were detected from 43 unrelated individuals and sequence alignment of the obtained alleles revealed 28 polymorphic sites. High heterozygosity values and allelic richness were unveiled for both wild and cultured populations. The substitution pattern (dN /dS = 0.7) is not consistent with the effect of diversifying selection, indicating lower selection pressure on the a2 domain, as well as that too few advantageous non-synonymous mutations have accumulated as substrate for the diversifying selection to act. Comparison with previously published results on microsatellite markers suggests that balancing selection in MHC genes reduces the genetic drift and bottleneck effects that are common in aquaculture and which are known to reduce genetic variation at neutral markers. The present study stresses that both coding and non-coding loci should be analyzed for designing proper management strategies.

Keywords

MHC class II SSCP Sea bream Polymorphism Selection Cultured populations 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

We thank Pilar Alvarino for technical help as well as an anonymous reviewer for his constructive comments throughout the text.

References

  1. Aguilar, A., G. Roemer, S. Debenham, M. Binns, D. Garcelon & K. R. Wayne, 2004. High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proceedings of the National Academy of Science USA 101: 3490–3494.CrossRefGoogle Scholar
  2. Belkhir, K., 1999. GENETIX v.4.0. Laboratoire Genome populations Interactions, CNRS UPR 9060. Montpellier, France.Google Scholar
  3. Conejeros, P., A. Phan, M. Power, S. Alekseyev, M. O’Conell, B. Dempson & B. Dixon, 2008. MH class IIa polymorphism in local and global adaptation of Arctic charr (Salvelinus alpinus L.). Immunogenetics 60: 325–337.CrossRefPubMedGoogle Scholar
  4. Cuesta, A., M. A. Esteban & J. Meseguer, 2006. Cloning, distibution and up-regulation of the teleost fish MHC class II alpha suggests a role for granulocytes as antigen-presenting cells. Molecular Immunology 43: 1275–1285.CrossRefPubMedGoogle Scholar
  5. Cummings, S. M., M. McMullan, D. A. Joyce & C. van Oosterhout, 2009. Solutions for PCR, cloning and sequencing errors in population genetic analysis. Conservation Genetics. doi  10.1007/s10592-009-9864-6.
  6. Dimitriou, Ε., 2000. Results of the unintentional or deliberate release of fishes in the wild: impact in the production, in the environment, in the genetic pool of species. Forum of Research and Technology, Athens, 11–12 May 2000: 49–54.Google Scholar
  7. Dorschner, M. O., T. Duris, C. R. Bronte, M. K. Burnham Curtis & R. B. Phillips, 2000. High levels of MHC class II allelic diversity in Lake trout from Lake Superior. Journal of Heredity 91: 359–363.CrossRefPubMedGoogle Scholar
  8. Ferguson, A., J. B. Taggart, P. A. Prodohl, O. McMeel, C. Thompson, C. Stone, P. McGinnity & R. Hynes, 1995. The application of molecular markers to the study and conservation of fish populations, with special reference to Salmon. Journal of Fish Biology 47: 103–126.CrossRefGoogle Scholar
  9. Frankel, O. H. & M. E. Soule, 1981. Conservation and Evolution. Cambridge University Press, Cambridge.Google Scholar
  10. Gillespie, J. H., 1991. The Causes of Molecular Evolution. Oxford University Press, New York.Google Scholar
  11. Goudet, J., 1995. Fstat version 1.2: a computer program to calculate F-statistics. Journal of Heredity 86: 485–486.Google Scholar
  12. Grimholt, U., S. Larsen, R. Nordmo, P. Midtlyng, S. Kjoeglum, A. Storset, S. Saebo & R. J. M. Stet, 2003. MHC polymorphism and disease resistance in Atlantic salmon (Salmo salar); facing pathogens with single expressed major histocompatibility class I and class II loci. Immunogenetics 55: 210–219.CrossRefPubMedGoogle Scholar
  13. Hayashi, K., 1991. PCR-SSCP: a simple and sensitive method for detection of mutations in the genomic DNA. Genome Research 1: 34–38.CrossRefGoogle Scholar
  14. Hedrick, P. W., 1994. Evolutionary genetics of the major histocompatibility complex. American Naturalist 143: 945–964.CrossRefGoogle Scholar
  15. Hillis, D. M., C. Moritz & B. K. Mable, 1996. Molecular Systematics, 2nd ed. Sinauer Associates, Sunderland, MA.Google Scholar
  16. Hughes, A. L., 1999. Adaptive Evolution of Genes and Genomes. Oxford University Press, New York.Google Scholar
  17. Hughes, A. L. & M. Nei, 1988. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335: 167–170.CrossRefPubMedGoogle Scholar
  18. Karaiskou, N., A. Triantafyllidis, V. Katsares, T. J. Abatzopoulos & C. Triantaphyllidis, 2009. Microsatellite variability of wild and farmed populations of Sparus aurata. Journal of Fish Biology 74: 1816–1825.CrossRefGoogle Scholar
  19. Klein, J., 1987. Origin of the major histocompatibility complex polymorphism: the trans species hypothesis. Human Immunology 19: 155–162.CrossRefPubMedGoogle Scholar
  20. Krieg, F., A. Triantafyllidis & R. Guyomard, 2000. Mitochondrial DNA variation in European populations of Silurus glanis. Journal of Fish Biology 56: 713–724.CrossRefGoogle Scholar
  21. Kumar, S., K. Tamura & M. Nei, 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinformatics 5: 150–163.CrossRefPubMedGoogle Scholar
  22. Landry, C. & L. Bernatchez, 2001. Comparative analysis of population structure across environments and geographical scales at the major histocompatibility complex and microsatellite loci in Atlantic salmon (Salmo salar). Molecular Ecology 261: 2525–2539.CrossRefGoogle Scholar
  23. Landry, C., D. Garant, P. Duchesne & L. Bernatchez, 2001. Good genes as heterozygosity: the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proceedings of the Royal Society of London B 268: 1279–1286.CrossRefGoogle Scholar
  24. Langefors, A., T. Von Schantz & B. Widegren, 1998. Allelic variation of Mhc class II in Atlantic salmon; a population genetic analysis. Heredity 80: 568–575.Google Scholar
  25. Langefors, A., J. Lohm & T. von Schantz, 2001a. Allelic polymorphism in MHC class II B in four populations of Atlantic salmon (Salmon salar). Immunogenetics 53: 329–336.CrossRefPubMedGoogle Scholar
  26. Langefors, A., J. Lohm, M. Grahn, O. Andersen & T. von Schantz, 2001b. Association between major histocompatibility complex class IIB alleles and resistance to Aeromonas salmonicida in Atlantic salmon. Proceedings of the Royal Society of London B 268: 479–485.CrossRefGoogle Scholar
  27. McGinnity, P., P. Prodöhl, A. Ferguson, R. Hynes, N. Maoiléidigh, N. Baker, D. Cotter, B. O’Hea, D. Cooke, G. Rogan, J. Taggart & T. Cross, 2003. Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon. Proceedings of the Royal Society of London B 270: 2443–2450.CrossRefGoogle Scholar
  28. Nei, M., X. Gu & T. Sitnikova, 1999. Evolution by birth-and-death process in multigene families of the vertebrate immune system. Proceedings of the National Academy of Science USA 94: 7799–7806.CrossRefGoogle Scholar
  29. Orita, M., Y. Suzuki, T. Sekiya & K. Hayashi, 1989. Rapid and sensitive detection of point mutations and DNA polymorphisms using the polymerase chain reaction. Genomics 5: 874–879.CrossRefPubMedGoogle Scholar
  30. Pots, W. K., C. J. Manning & E. K. Wakeland, 1991. Mating patterns in semi-natural populations of mice influenced by MHC genotype. Nature 352: 619–621.CrossRefGoogle Scholar
  31. Raymond, M. & F. Rousset, 1995. GENEPOP (v3.1): Population genetics software for exact tests and ecumenicism. Journal of Heredity 86: 248–249.Google Scholar
  32. Reush, T. B. H., H. Schaschl & K. M. Wegner, 2004. Recent duplication and inter-locus gene conversion in major histocompatibility class II genes in a teleost, the three-spined stickleback. Immunogenetics 56: 427–437.Google Scholar
  33. Roberge, C., É. Normandeau, S. Einum, H. Guderley & L. Bernatchez, 2008. Genetic consequences of interbreeding between farmed and wild Atlantic salmon: insights from the transcriptome. Molecular Ecology 17: 314–324.CrossRefPubMedGoogle Scholar
  34. Tamura, K., J. Dudley, M. Nei & S. Kumar, 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596–1599.CrossRefPubMedGoogle Scholar
  35. Van Oosterhout, C., 2009. A new theory of MHC evolution: beyond selection on the immune genes. Proceedings of the Royal Society of London B 276: 657–665.CrossRefGoogle Scholar
  36. Van Oosterhout, C., D. A. Joyce & S. M. Cummings, 2006a. Evolution of MHC class IIB in the genome of wild and ornamental guppies, Poecilia reticulate. Heredity 97: 111–118.CrossRefPubMedGoogle Scholar
  37. Van Oosterhout, C., A. J. Domino, S. M. Cummings, J. Blais, N. J. Barson, I. W. Ramnarine, R. S. Mohammed, N. Persad & J. Cable, 2006b. Balancing selection, random genetic drift and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulate). Evolution 60: 2562–2574.CrossRefPubMedGoogle Scholar
  38. Wegner, K. M., M. Kalbe, G. Rauch, J. Kurtz, H. Schaschl & T. B. H. Reusch, 2006. Genetic variation in MHC Class II expression and interactions with MHC sequence polymorphism in three-spined sticklebacks. Molecular Ecology 15: 1153–1164.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Nikoleta Karaiskou
    • 1
  • Paloma Moran
    • 2
  • George Georgitsakis
    • 1
  • Theodore J. Abatzopoulos
    • 1
  • Alexander Triantafyllidis
    • 1
  1. 1.Department of Genetics, Development and Molecular Biology, School of BiologyAristotle University of ThessalonikiThessaloniki, MacedoniaGreece
  2. 2.Departamento de Bioquimica, Genetica and InmunologiaUniversidad de VigoVigoSpain

Personalised recommendations