Patterns of historical balancing selection on the salmonid major histocompatibility complex class II β gene

Journal of Molecular Evolution

Volumn 65, Issue 1, 2007, Pages 34-43

  Aguilar, Andres ^a,b   Garza, John Carlos ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Ancestral polymorphism; Gene conversion; Oncorhynchus; Recombination; Salmo; Salvelinus

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2 BETA; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CODON; EXON; FISH GENETICS; GENE CONVERSION; GENE SEQUENCE; GENETIC VARIABILITY; HYPOTHESIS; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR EVOLUTION; MONOPHYLY; NATURAL SELECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCORHYNCHUS; ONCORHYNCHUS CLARKII; PHYLOGENY; PROTEIN POLYMORPHISM; RAINBOW TROUT; RECOMBINANT GENE; SALMON; SALMONID; TELEOST;

AMINO ACID SEQUENCE; ANIMALS; EVOLUTION, MOLECULAR; GENES, MHC CLASS II; MAJOR HISTOCOMPATIBILITY COMPLEX; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PHYLOGENY; SALMONIDAE; SELECTION (GENETICS); SEQUENCE ALIGNMENT;

MAMMALIA; ONCORHYNCHUS; ONCORHYNCHUS CLARKII; ONCORHYNCHUS MYKISS; SALMO; SALMONIDAE; SALVELINUS; TELEOSTEI; VERTEBRATA;

EID: 34547700728     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-006-0222-8     Document Type: Article

References (53)

1. Aguilar A, Garza JC (2006) A comparison of variability and population structure for major histocompatibility complex and microsatellite loci in California coastal steelhead (Oncorhynchus mykiss Walbaum). Mol Ecol 15:923-937
2. Alledorf FW, Leary RF (1988) Hybridization dynamics between sympatric species of trout: loss of reproductive isolation. Conserv Biol 2:170-184
3. Anisimova M, Nielsen R, Yang ZH (2003) Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164:1229-1236
4. Apanius V, Penn D, Slev PR, Ruff LR, Potts WK (1997) The nature of selection on the major histocompatibility complex. Crit Rev Immunol 17:179-224
5. Baumsteiger J, Hankin D, Loudenslager EJ (2005) Genetic analyses of juvenile steelhead, coastal cutthroat trout, and their hybrids differ substantially from field identifications. Trans Am Fish Soc 134:829-840
6. Bergstrom TF, Josefsson A, Erlich HA, Gyllensten U (1998) Recent origin of HLA-DRB1 alleles and implications for human evolution. Nature Genet 18:237-242
7. Bettles CM, Docker MF, Dufour B, Heath DD (2005) Hybridization dynamics between sympatric species of trout: loss of reproductive isolation. J Evol Biol 18:1220-1233
8. BingulacPopovic J, Figueroa F, Sato A, Talbot WS, Johnson SL, Gates M, Postlethwait JH, Klein J (1997) Mapping of MHC class I and class II regions to different linkage groups in the zebrafish, Danio rerio. Immunogenetics 46:129-134
9. 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 364:33-39
10. Crespi BJ, Fulton MJ (2004) Molecular systematics of Salmonidae: combined nuclear data yields a robust phylogeny. Mol Phylogenet Evol 31:658-679
11. Cummings MP, Otto SP, Wakeley J (1995) Sampling properties of DNA-sequence data in phylogenetic analysis. Mol Biol Evol 12:814-822
12. Dorschner MO, Duris T, Bronte CR, Curtis MKB, Phillips RB (2000) High levels of MHC class II allelic diversity in lake trout from Lake Superior. J Hered 91:359-363
13. 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
14. Edwards SV, Hedrick PW (1998) Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 13:305-311
15. Edwards SV, Wakeland EK, Potts WK (1995) Contrasting histories of avian and mammalian MHC genes revealed by class II B sequences from songbirds. Proc Natl Acad Sci USA 92:12200-12204
16. Fan WM, Kasahara M, Gutknecht J, Klein D, Mayer WE, Jonker M, Klein J (1989) Shared class-II MHC polymorphisms between humans and chimpanzees. Hum Immunol 26:107-121
17. Figueroa F, Gunther E, Klein J (1988) MHC polymorphism predating speciation. Nature 335:265-267
18. Figueroa F, Mayer WE, Sultmann H, O'hUigin C, Tichy H, Satta Y, Takezaki N, Takahata N, Klein J (2000) MHC class IIB gene evolution in East African cichlid fishes. Immunogenetics 51:556-575
19. Garrigan D, Hedrick PN (2001) Class I MHC polymorphism and evolution in endangered California Chinook and other Pacific salmon. Immunogenetics 53:483-489
20. Garrigan D, Hedrick PW (2003) Perspective: detecting adaptive molecular polymorphism: Lessons from the MHC. Evolution 57:1707-1722
21. Graser R, O'hUigin C, Vincek V, Meyer A, Klein J (1996) Trans-species polymorphism of class II MHC loci in danio fishes. Immunogenetics 44:36-48
22. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696-704
23. Hedrick PW (1994) Evolutionary genetics of the major histocompatibility complex. Am Nat 143:945-964
24. Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA-sequences. Genetics 111:147-164
25. Hughes AL, Nei M (1989) Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci USA 86:958-962
26. Hughes AL, Ota T, Nei M (1990) Positive Darwinian selection promotes charge profile diversity in the antigen-binding cleft of class I major-histocompatibility-complex molecules. Mol Biol Evol 7:515-524
27. Kim TJ, Parker KM, Hedrick PW (1999) Major histocompatibility complex differentiation in Sacramento River chinook salmon. Genetics 151:1115-1122
28. Klein J (1986) Natural history of the major histocompatibility complex. John Wiley, New York
29. Klein J, Sato A, Nagl S, O'hUigin C (1998) Molecular trans-species polymorphism. Annu Rev Ecol Syst 29:1-21
30. Kruiswijk CP, Hermsen T, van Heerwaarden J, Dixon B, Savelkoul HFJ, Stet RJM (2005) Major histocompatibility genes in the Lake Tana African large barb species flock: evidence for complete partitioning of class IIB, but not class I, genes among different species. Immunogenetics 56:894-908
31. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150-163
32. Landry C, Bernatchez L (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
33. Langefors AA, Von Schantz T, Widegren B (1998) Allelic variation of Mhc class II in Atlantic salmon: a population genetic analysis. Heredity 80:568-575
34. McKay SJ, Devlin RH, Smith MJ (1996) Phylogeny of Pacific salmon and trout based on growth hormone type-2 and mitochondrial NADH dehydrogenase subunit 3 DNA sequences. Can J Fish Aquat Sci 53:1165-1176
35. Miller KM, Withler RE (1996) Sequence analysis of a polymorphic MHC class II gene in Pacific salmon. Immunogenetics 43:337-351
36. Miller KM, Withler RE, Beacham TD (1997) Molecular evolution at MHC genes in two populations of chinook salmon Oncorhynchus tshawytscha. Mol Ecol 6:937-954
37. Miller KM, Kaukinen KH, Beacham TD, Withler RE (2001) Geographic heterogeneity in natural selection on an MHC locus in sockeye salmon. Genetica 111:237-257
38. Oakley TH, Phillips RB (1999) Phylogeny of salmonine fishes based on growth hormone introns: Atlantic (Salmo) and Pacific (Oncorhynchus) salmon are not sister taxa. Mol Phylogenet Evol 11:381-393
39. Ono H, O'hUigin C, Tichy H, Klein J (1993) Major-histocompatibility- complex variation in two species of cichlid fishes form Lake Malawi. Mol Biol Evol 10:1060-1072
40. Ottova E, Simkova A, Martin JF, de Bellocq JG, Gelnar M, Allienne JF, Morand S (2005) Evolution and trans-species polymorphism of MHC class II beta genes in cyprinid fish. Fish Shellfish Immunol 18:199-222
41. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818
42. Reusch TBH, 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 61:531-545
43. Reusch TBH, Schaschl H, Wegner KM (2004) Recent duplication and interlocus gene conversion in major histocompatibility class II genes in a teleost, the three-spined stickleback. Immunogenetics 56:427-437
44. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496-2497
45. Sawyer S (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526-538
46. Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114-1116
47. Shum BP, Guethlein L, Flodin LR, Adkison MA, Hedrick RP, Nehring RB, Stet RJM, Secombes C, Parham P (2001) Modes of salmonid MHC class I and II evolution differ from the primate paradigm. J Immunol 166:3297-3308
48. Stet RJM, de Vries B, Mudde K, Hermsen T, van Heerwaarden J, Shum BP, Grimholt U (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. Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland, MA
50. Wittzell H, Bernot A, Auffray C, Zoorob R (1999) Concerted evolution of two MHC class II B loci in pheasants and domestic chickens. Mol Biol Evol 16:479-490
51. Yang ZH (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555-556
52. Young WP, Ostberg CO, Keim P, Thorgaard GH (2001) Genetic characterization of hybridization and introgression between anadromous rainbow trout (Oncorhynchus mykiss irideus) and coastal cutthroat trout (O-clarki clarki). Mol Ecol 10:921-930
53. Yuhki N, OBrien SJ (1997) Nature and origin of polymorphism in feline MHC class II DRA and DRB genes. J Immunol 158:2822-2833