Rapid evolution of the MH class I locus results in different allelic compositions in recently diverged populations of Atlantic salmon

Molecular Biology and Evolution

Volumn 22, Issue 4, 2005, Pages 1095-1106

  Consuegra, S ^a,c   Megens, H J ^b   Schaschl, H ^a,d   Leon, K ^b   Stet, R J M ^b,e   Jordan, W C ^a  

^a INSTITUTE OF ZOOLOGY   (United Kingdom)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c UNIVERSITY OF ST ANDREWS   (United Kingdom)

^d MAX PLANCK INSTITUTE FOR EVOLUTIONARY BIOLOGY   (Germany)

^e UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Atlantic salmon; MHC; Positive selection; Recombination; Salmo salar

Indexed keywords

AMINO ACID; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ADAPTATION; ALLELE; ALLELISM; AMINO ACID SUBSTITUTION; ARTICLE; ATLANTIC SALMON; GENETIC MARKER; GENETIC RECOMBINATION; GENETIC VARIABILITY; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; POINT MUTATION; PROTEIN BINDING;

ALLELES; ANIMALS; BASE SEQUENCE; DNA PRIMERS; DNA, COMPLEMENTARY; GENETICS, POPULATION; MAJOR HISTOCOMPATIBILITY COMPLEX; RECOMBINATION, GENETIC; SALMON;

EID: 16344371206     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msi096     Document Type: Article

References (60)

1. Akaike, H. 1974. A new look at the statistical model identification. IEEE Trans. Autom. Control AC-19:716-723.
2. Anisimova, M., J. P. Bielawski, and Z. Yang. 2002. Accuracy of Bayes prediction of amino acid sites under positive selection. Mol. Biol. Evol. 19:950-958.
3. Anisimova, M., R. Nielsen, and Z. Yang. 2003. Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164: 1229-1236.
4. Belich, M. P., J. A. Madrigal, W. H. Hildebrand, J. Zemmour, R. C. Williams, R. Luz, M. L. Petzl-Erler, and P. Parham. 1992. Unusual HLA-B alleles in two tribes of Brazilian Indians. Nature 357:326-329.
5. Bernatchez, L., and C. C. Wilson. 1998. Comparative phylogeography of Nearctic and Palearctic fishes. Mol. Ecol. 7:431-452.
6. Bjorkman, P. J., M. A. Saper, B. Samraoui, W. S. Bennett, J. L. Strominger, and D. C. Wiley. 1987a. Structure of the human class I histocompatibility antigen, HLA-A2. Nature 329:506-512.
7. -. 1987e. The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 329:512-518.
8. Bourke, E. A., J. Coughlan, H. Jansson, P. Galvin, and T. F. Cross. 1997. Allozyme variation in populations of Atlantic salmon located throughout Europe: diversity that could be compromised by introductions of reared fish. ICES J. Mar. Sci. 54:974-985.
9. Clifford, S. L., P. McGinnity, and A. Ferguson. 1998. Genetic changes in Atlantic salmon (Salmo salar) populations of Northwest Irish rivers resulting from escapes of adult farm salmon. Can. J. Fish. Aquat. Sci. 55:358-363.
10. Consuegra, S., C. García de Leâniz, A. Serdio, M. González Morales, L. G. Straus, D. Knox, and E. Verspoor. 2002. Mitochondrial DNA variation in Pleistocene and modern Atlantic salmon from the Iberian glacial refugium. Mol. Ecol. 11:2037-2048.
11. Edwards, S. V., and P. W. Hedrick. 1998. Evolution and ecology of MHC molecules: from genomics to sexual selection. TREE 13:305-311.
12. Felsenstein, J. 1989. PHYLIP-phylogeny inference package (Version 3.2). Cladistics 5:164-166.
13. Garant, D., I. A. Fleming, S. Einum, and L. Bernatchez. 2003. Alternative male life-history tactics as potential vehicles for speeding introgression of farm salmon traits into wild populations. Ecol. Lett. 6:541-549.
14. Garboczi, D. N., P. Ghosh, U. Utz, Q. R. Fan, W. E. Biddison, and D. C. Wiley. 1996. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 384: 134-141.
15. Garcia, K. C., M. Degano, R. L. Stanfield, A. Brunmark, M. R. Jackson, P. A. Peterson, L. Teyton, and I. A. Wilson. 1996. An alphabeta T cell receptor structure at 2.5 A and its orientation in the TCR-MHC complex. Science 274: 209-219.
16. Garrigan, D., and P. W. Hedrick. 2001. Class I MHC polymorphism and evolution in endangered California Chinook and other Pacific salmon. Immunogenetics 53:483-489.
17. -. 2003. Detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 57:1707-1722.
18. Grassly, N. C., and E. C. Holmes. 1997. A likelihood method for the detection of selection and recombination using sequence data. Mol. Biol. Evol. 14:239-247.
19. Grimholt, U., F. Drablõs, S. M. Jõrgensen, B. Hoyheim, and R. J. M. Stet. 2002. The major histocompatibility class I locus in Atlantic salmon (Salmo salar L.): polymorphism, linkage analysis and protein modelling. Immunogenetics 54: 570-581.
20. Grimholt, U., I. Hordvik, V. M. Fosse, I. Olsaker, C. Endresen, and O. Lie. 1993. Molecular cloning of major histocompatibilty complex class I cDNAs from Atlantic salmon (Salmo salar). Immunogenetics 37:469-473.
21. Hedrick, P. W., W. Klitz, W. P. Robinson, M. K. Kuhner, and G. Thomson. 1991. Evolutionary genetics of HLA. Pp. 248-271 in R. Selander, A. Clark and T. Whittam, eds. Molecular evolution. Sinauer, Sunderland, MA.
22. Hedrick, P. W. 1994. Evolutionary genetics of the major histocompatibility complex. Am. Nat. 143:945-964.
23. -. 2002 Pathogen resistance and genetic variation at MHC loci. Evolution 56:1902-1908.
24. Hewitt, G. M. 1999 Post-glacial re-colonization of European biota. Biol. J. Linn. Soc. 68:87-112.
25. Hudson, R. R., and N. L. Kaplan. 1985. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147-164.
26. Jeffery, K. J. M., and C. R. M. Bangham. 2000. Do infectious diseases drive MHC diversity? Microbes Infect. 2:1335-1341.
27. Jordan, W. C., and M. W. Bruford. 1998. New perspectives on mate choice and the MHC. Heredity 81:127-133.
28. Jukes, T. H., and C. R. Cantor. 1969. Evolution of protein molecules. Pp. 21-132 in H. M. Munro, ed. Mammalian protein metabolism. Academic Press, New York.
29. Koskinen, M. T., T. O. Haugen, and C. R. Primmer. 2002. Contemporary fisherian life-history evolution in small salmonid populations. Nature 419:926-930.
30. Kumar, S., K. Tamura, I. B. Jakobsen, and M. Nei. 2001. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244.
31. Landry, C., and L. Bernatchez. 2001. Comparative analysis of population structure across environments and geographical scales at major histocompatibility complex and microsatellite loci in Atlantic salmon (Salmo salar). Mol. Ecol. 10: 2525-2539.
32. Landry, C., D. Garant, P. Duchesne, and L. Bernatchez. 2001. 'Good genes as heterozygosity': the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proc. R. Soc. Lond. B Biol. Sci. 268:1279-1285.
33. Martinsohn, J. T., A. B. Sousa, L. A. Guethlein, and J. C. Howard. 1999. The gene conversion hypothesis of MHC evolution: a review. Immunogenetics 50:168-200.
34. McVean, G., P. Awadalla, and P. Fearnhead. 2002. A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160:1231-1241.
35. Meunier, J., and A. Eyre-Walker. 2001. The correlation between linkage disequilibrium and distance. Implications for recombination in Hominid mitochondria. Mol. Biol. Evol. 18: 2132-2135.
36. Miller, K. M., and R. E. Withler. 1998. The salmonid class IMHC: limited diversity in a primitive teleost. Immunol. Rev. 166:279-293.
37. Nei, M., and T. Gojobori, 1986. Simple methods for estimating the numbers of synonymous nucleotide substitutions. Mol. Biol. Evol. 3:418-426.
38. Nei, M. and T. Gojobori, 2000. Molecular Evolution and Phylogenetics. Oxford University Press, New York, NY.
39. Nilsson, J., R. Gross, T. Asplund et al. (16 co-authors). 2001. Matrilinear phylogeography of Atlantic salmon (Salmo salar L.) in Europe and postglacial colonization of the Baltic Sea area. Mol. Ecol. 10:89-102.
40. Ohta, T. 1995. Gene conversion vs point mutation in generating variability at the antigen recognition site of major histocompatibility complex loci. J. Mol. Evol. 41:115-119.
41. Ohta, Y., K. Okamura, E. C. McKinney, S. Bartl, K. Hashimoto, and M. F. Flajnik. 2000. Primitive synteny of vertebrate major histocompatibility complex class I and class II genes. Proc. Natl. Acad. Sci. USA 97:4712-4717.
42. Penn, D. J., K. Damjanovich, and W. K. Potts. 2002. MHC heterozygosity confers a selective advantage against multiple-strain infections. Proc. Natl. Acad. Sci. USA 99: 11260-11264.
43. Posada, D., and K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818.
44. Reche, P. A., and E. L. Reinherz. 2003. Sequence variability analysis of human class I and class II MHC molecules: functional and structural correlates of amino acid polymorphisms. J. Mol. Biol. 331:623-641.
45. Rozas, J., and R. Rozas. 1999. DnaSP Version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174-175.
46. Shannon, C. E. 1948. A mathematical theory of communication. Bell Syst. Tech. J. 27:379-423, 623-656.
47. Shum, B. P., L. Guethlein, L. R. Flodin, M. D. Adkison, R. P. Hedrick, R. B. Nehring, R. J. M. Stet, C. Secombes, and P. Parham. 2001. Modes of salmonid MHC Class I and II evolution differ from the primate paradigm. J. Immunol. 166: 3297-3308.
48. Stet, R. J. M., B. deVries, K. Mudde, T. Hermsen, J. van Heerwaarden, B. P. Shum, and U. Grimholt. 2002. Unique haplotypes of co-segregating major histocompatibility class II A and class II B alleles in Atlantic salmon (Salmo salar) give rise to diverse class II genotypes. Immunogenetics 54:320-331.
49. Stewart J. J., C. Y. Lee, S. Ibrahim, P. Watts, M. Shlomick, S. Weigert, and S. Litwin. 1997. A Shannon entropy analysis of immunoglobin and T cell receptors. Mol. Immunol. 34: 1067-1082.
50. Su, C. 2000. SGI: modified Suzuki and Gojobori's method for detecting positive and negative selection at individual codon sites. The Pennsylvania State University, University Park, Pa.
51. Suzuki, Y., and T. Gojobori. 1999. A method for detecting positive selection at single amino acid sites. Mol. Biol. Evol. 16:1315-1328.
52. Suzuki, Y., and M. Nei. 2001. Reliabilities of parsimony-based and likelihood-based methods for detecting positive selection at single amino acid sites. Mol. Biol. Evol. 18: 2179-2185.
53. -. 2004. False-positive selection identified by ML-based methods: examples from the Sig1 gene of the diatom Thalassiosira weissflogii amd the tax gene of a human T-cell lymphotropic virus. Mol. Biol. Evol. 21:914-921.
54. Taylor, E. B. 1991 A review of local adaptations in Salmonidae, with particular reference to Pacific and Atlantic salmon. Aquaculture 98:185-207.
55. Van den Berg, T. K., J. A. Yoder, and G. W. Litman. 2004. On the origins of adaptive immunity: innate immune receptors join the tale. Trends Immunol. 25:11-16.
56. Verspoor, E., E. M. McCarthy, D. Knox, E. Bourke, and T. F. Cross. 1999. The phylogeography of European Atlantic salmon (Salmo salar L.) based on RFLP analysis of the ND1/16sRNA region of mtDNA. Biol. J. Linn. Soc. 68: 129-146.
57. Watkins, D. I., S. N. McAdam, X. Liu et al. (13 co-authors). 1992. New recombinant HLA-B alleles in a tribe of South American Amerindians indicate rapid evolution of MHC class I loci. Nature 357:329-333.
58. Wong, W. S. W., Z. Yang, N. Goldman, and R. Nielsen. 2004. Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. Genetics 168:1041-1051.
59. Yang, Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. CABIOS 13:555-556.
60. Yang, Z., R. Nielsen, N. Goldman, and A.-M. K. Pedersen. 2000. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431-449.