RSCA genotyping of MHC for high-throughput evolutionary studies in the model organism three-spined stickleback Gasterosteus aculeatus

BMC Evolutionary Biology

Volumn 9, Issue 1, 2009, Pages

  Lenz, Tobias L ^a   Eizaguirre, Christophe ^a   Becker, Sven ^a,b   Reusch, Thorsten B H ^c  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY BIOLOGY   (Germany)

^b ENVIRONMENT CANADA   (Canada)

^c GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

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

ARTICLE; CONFORMATION; CONTROLLED STUDY; FISH; GASTEROSTEUS ACULEATUS; GENETIC VARIABILITY; GENOTYPE; HIGH THROUGHPUT SCREENING; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; REFERENCE STRAND MEDIATED CONFORMATION ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES DIFFERENTIATION; ALLELE; ANIMAL; DNA SEQUENCE; GENE; GENE LIBRARY; GENETIC MARKER; GENETIC POLYMORPHISM; GENETICS; METHODOLOGY; MOLECULAR EVOLUTION; SEQUENCE ALIGNMENT; SMEGMAMORPHA;

AVES; GASTEROSTEUS ACULEATUS; GNATHOSTOMATA (VERTEBRATE);

ALLELES; ANIMALS; CLONING, MOLECULAR; EVOLUTION, MOLECULAR; GENE LIBRARY; GENES, MHC CLASS II; GENETIC MARKERS; GENOTYPE; POLYMORPHISM, GENETIC; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SMEGMAMORPHA;

EID: 63449087306     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-9-57     Document Type: Article

References (75)

1. Evolutionary significance of the HL-A system. WF Bodmer, Nature 1972 237 5351 139 183 10.1038/237139a0 4113158
2. The major histocompatibility complex of the mouse. J Klein, Science 1979 203 4380 516 521 10.1126/science.104386 104386
3. J Klein, Natural history of the major histocompatibility complex New York: John Wiley &Sons 1986
4. The evolution of mating preferences and major histocompatibility complex genes. DJ Penn WK Potts, Am Nat 1999 153 2 145 164 10.1086/303166
5. The importance of immune gene variability (MHC) in evolutionary ecology and conservation. S Sommer, Front Zool 2005 2 1 16 16242022 10.1186/1742-9994-2- 16
6. MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years. L Bernatchez C Landry, J Evol Biol 2003 16 3 363 377 10.1046/j.1420-9101.2003.00531.x 14635837
7. The evolutionary ecology of the major histocompatibility complex. SB Piertney MK Oliver, Heredity 2006 96 1 7 21 16094301
8. The major histocompatibility complex, sexual selection, and mate choice. M Milinski, Annu Rev Ecol Evol Syst 2006 37 1 159 186 10.1146/annurev.ecolsys. 37.091305.110242
9. Contrasting histories of avian and mammalian Mhc genes revealed by class II B sequences from songbirds. SV Edwards EK Wakeland WK Potts, Proc Natl Acad Sci USA 1995 92 26 12200 12204 8618869 10.1073/pnas.92.26.12200
10. Evolution by the birth-and-death process in multigene families of the vertebrate immune system. M Nei X Gu T Sitnikova, Proc Natl Acad Sci USA 1997 94 15 7799 7806 9223266 10.1073/pnas.94.15.7799
11. Dynamics of Mhc evolution in birds and crocodilians: Amplification of class II genes with degenerate primers. SV Edwards M Grahn WK Potts, Mol Ecol 1995 4 6 719 729 10.1111/j.1365-294X.1995.tb00272.x 8564010
12. MHC class I typing in a songbird with numerous loci and high polymorphism using motif-specific PCR and DGGE. H Westerdahl H Wittzell T von Schantz S Bensch, Heredity 2004 92 6 534 542 10.1038/sj.hdy.6800450 15162116
13. Diversity of Mhc class I and IIB genes in house sparrows (Passer domesticus). C Bonneaud G Sorci V Morin H Westerdahl R Zoorob H Wittzell, Immunogenetics 2004 55 12 855 865 10.1007/s00251-004-0648-3 14963619
14. Molecular study of Mhc-DRB in wild chacma baboons reveals high variability and evidence for trans-species inheritance. E Huchard G Cowlishaw M Raymond M Weill L Knapp, Immunogenetics 2006 58 10 805 816 10.1007/s00251-006- 0156-8 17021859
15. Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. TB Reusch MA Haberli PB Aeschlimann M Milinski, Nature 2001 414 6861 300 302 10.1038/35104547 11713527
16. How many clones need to be sequenced from a single forensic or ancient DNA sample in order to determine a reliable consensus sequence? MA Bower M Spencer S Matsumura RER Nisbet CJ Howe, Nucleic Acids Res 2005 33 8 2549 2556 15870386 10.1093/nar/gki550
17. Simple approach to reduce PCR artefact formation leads to reliable genotyping of MHC and other highly polymorphic loci implications for evolutionary analysis. TL Lenz S Becker, Gene 2008 427 12 117 123 10.1016/j.gene.2008.09.013 18848974
18. Screening techniques for detecting allelic variation in DNA sequences. EP Lessa G Applebaum, Mol Ecol 1993 2 2 119 129 10.1111/j.1365-294X.1993.tb00006.x 8180734
19. SSCP analysis of Mhc class IIB genes in the threespine stickleback. T Binz TBH Reusch C Wedekind M Milinski, J Fish Biol 2001 58 3 887 890
20. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. AL Hughes M Nei, Nature 1988 335 6186 167 170 10.1038/335167a0 3412472
21. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. JH Brown TS Jardetzky JC Gorga LJ Stern RG Urban JL Strominger DC Wiley, Nature 1993 364 6432 33 39 10.1038/364033a0 8316295
22. Mutation detection and typing of polymorphic loci through double-strand conformation analysis. JR Argüello AM Little AL Pay D Gallardo I Rojas SGE Marsh JM Goldman JA Madrigal, Nat Genet 1998 18 2 192 194 10.1038/ng0298-192 9462755
23. RSCA (reference strand mediated conformation analysis) resolves HLA-DRB1*04 typing ambiguities where other molecular techniques fail. A Corell AL Pay JR Argüello M Borton C Dunne JA Madrigal SGE Marsh, Blood 1999 94 10 318B 318B
24. HLA typing by Reference Strand Mediated Conformation Analysis. JR Argüello JA Madrigal, Rev Immunogenet 1999 1 2 209 219 11253947
25. Reference strand conformational analysis (RSCA) is a valuable tool in identifying MHC-DRB sequences in three species of Aotus monkeys. J Baquero S Miranda O Murillo H Mateus E Trujillo C Suarez M Patarroyo C Parra-Lpez, Immunogenetics 2006 58 7 590 597 10.1007/s00251-006-0101-x 16733718
26. Analysis of pigtail macaque major histocompatibility complex class I molecules presenting immunodominant simian immunodeficiency virus epitopes. MZ Smith CJ Dale R De Rose I Stratov CS Fernandez AG Brooks J Weinfurter K Krebs C Riek DI Watkins, J Virol 2005 79 2 684 695 15613296 10.1128/JVI.79.2.684-695. 2005
27. Reference strand-mediated conformation analysis-based typing of multiple alleles in the rhesus macaque MHC class I Mamu-A and Mamu-B loci. Y Tanaka-Takahashi M Yasunami T Naruse K Hinohara T Matano K Mori M Miyazawa M Honda Y Yasutomi Y Nagai, Electrophoresis 2007 28 6 918 924 10.1002/elps. 200600586 17309048
28. Rapid high-resolution MHC class I genotyping of Chinese rhesus macaques by capillary reference strand-mediated conformational analysis. A Blasky J Karl R Wiseman D Read D O'Connor, Immunogenetics 2008 60 10 575 584 18629489 10.1007/s00251-008-0315-1
29. The use of reference strand-mediated conformational analysis for the study of cheetah (Acinonyx jubatus) feline leucocyte antigen class II DRB polymorphisms. GJC Drake LJ Kennedy HK Auty R Ryvar WER Ollier AC Kitchener AR Freeman AD Radford, Mol Ecol 2004 13 1 221 229 10.1046/j.1365-294X.2003.02027.x 14653802
30. Reference-strand-mediated conformation analysis of MHC alleles: a new method for high-resolution typing of the Ovar-DQB genes. P Feichtlbauer-Huber MJ Stear R Fries J Buitkamp, Immunogenetics 2000 51 1 65 68 10.1007/s002510050010 10663564
31. High-Resolution Characterization of the Canine DLA-DRB1 Locus Using Reference Strand-Mediated Conformational Analysis. LJ Kennedy S Quarmby N Fretwell AJ Martin PG Jones CA Jones WER Ollier, J Hered 2005 96 7 836 842 10.1093/jhered/esi112 16251520
32. Polymorphisms of the equine major histocompatibility complex class II DRA locus. JJ Brown W Thomson P Clegg S Eyre LJ Kennedy J Matthews S Carter WER Ollier, Tissue Antigens 2004 64 2 173 179 10.1111/j.1399-0039.2004.00269.x 15245372
33. Resolution of complex feline leukocyte antigen DRB loci by reference strand-mediated conformational analysis (RSCA). LJ Kennedy R Ryvar JJ Brown WER Ollier AD Radford, Tissue Antigens 2003 62 4 313 323 10.1034/j.1399-0039.2003. 00099.x 12974798
34. Genotypic Characterization of an MHC Class II Locus in Lake Trout (Salvelinus namaycush) from Lake Superior by Single-Stranded Conformational Polymorphism Analysis and Reference Strand-Mediated Conformational Analysis. MA Noakes T Reimer RB Phillips, Mar Biotechnol 2003 5 3 270 278 10.1007/s10126-002-0079-9 14502399
35. Single locus typing of MHC class I and class IIB loci in a population of red jungle fowl. K Worley M Gillingham P Jensen LJ Kennedy T Pizzari J Kaufman DS Richardson, Immunogenetics 2008 60 5 233 247 10.1007/s00251-008-0288-0 18389232
36. Evolution: The synthesis and evolution of a supermodel. G Gibson, Science 2005 307 5717 1890 1891 10.1126/science.1109835 15790836
37. Mate choice decisions of stickleback females predictably modified by MHC peptide ligands. M Milinski S Griffiths KM Wegner TBH Reusch A Haas-Assenbaum T Boehm, Proc Natl Acad Sci USA 2005 102 12 4414 4418 15755811 10.1073/pnas.0408264102
38. Condition-dependent expression of red colour differs between stickleback species. JW Boughman, J Evol Biol 2007 20 4 1577 1590 10.1111/j.1420-9101.2007. 01324.x 17584250
39. Parasite selection for immunogenetic optimality. KM Wegner M Kalbe J Kurtz TBH Reusch M Milinski, Science 2003 301 5638 1343 1343 10.1126/science.1088293 12958352
40. Local differences in immunocompetence reflect resistance of sticklebacks against the eye fluke Diplostomum pseudospathaceum. M Kalbe J Kurtz, Parasitology 2006 132 1 105 116 10.1017/S0031182005008681 16393359
41. Natural Selection and Parallel Speciation in Sympatric Sticklebacks. HD Rundle L Nagel JW Boughman D Schluter, Science 2000 287 5451 306 308 10.1126/science.287.5451.306 10634785
42. Parallel evolution of sexual isolation in sticklebacks. JW Boughman HD Rundle D Schluter, Evolution 2005 59 2 361 373 15807421
43. Ecological selection against hybrids in natural populations of sympatric threespine sticklebacks. JL Gow CL Peichel EB Taylor, J Evol Biol 2007 20 6 2173 2180 10.1111/j.1420-9101.2007.01427.x 17887972
44. Intraspecific competition drives increased resource use diversity within a natural population. R Svanback DI Bolnick, Proc R Soc Lond B Biol Sci 2007 274 1611 839 844 10.1098/rspb.2006.0198
45. MHC Adaptive Divergence between Closely Related and Sympatric African Cichlids. J Blais C Rico C van Oosterhout J Cable GF Turner L Bernatchez, PLoS ONE 2007 2 8 e734 17710134 10.1371/journal.pone.0000734
46. The genetic architecture of divergence between threespine stickleback species. CL Peichel KS Nereng KA Ohgi BLE Cole PF Colosimo CA Buerkle D Schluter DM Kingsley, Nature 2001 414 6866 901 905 10.1038/414901a 11780061
47. Parallel genetic origins of pelvic reduction in vertebrates. MD Shapiro MA Bell DM Kingsley, Proc Natl Acad Sci USA 2006 103 37 13753 13758 16945911 10.1073/pnas.0604706103
48. Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. J Kurtz M Kalbe PB Aeschlimann MA Haberli KM Wegner TBH Reusch M Milinski, Proc R Soc Lond B Biol Sci 2004 271 1535 197 204 10.1098/rspb.2003.2567
49. Female sticklebacks Gasterosteus aculeatus use self-reference to optimize MHC allele number during mate selection. PB Aeschlimann MA Haberli TBH Reusch T Boehm M Milinski, Behav Ecol Sociobiol 2003 54 2 119 126
50. Mortality selection during the 2003 European heat wave in three-spined sticklebacks: effects of parasites and MHC genotype. KM Wegner M Kalbe M Milinski TBH Reusch, BMC Evol Biol 2008 8 124 18447901 10.1186/1471-2148-8-124
51. Lifetime reproductive success is maximized with optimal major histocompatibility complex diversity. M Kalbe C Eizaguirre I Dankert TBH Reusch RD Sommerfeld KM Wegner M Milinski, Proc R Soc Lond B Biol Sci 2009 276 1658 925 934 10.1098/rspb.2008.1466
52. Cloning of major histocompatibility complex (Mhc) genes from threespine stickleback, Gasterosteus aculeatus. A Sato F Figueroa C O'Huigin N Steck J Klein, Mol Mar Biol Biotechnol 1998 7 3 221 231 9701617
53. Inter- and intralocus recombination drive MHC class IIB gene diversification in a teleost, the three-spined stickleback Gasterosteus aculeatus. TBH Reusch A Langefors, J Mol Evol 2005 61 4 531 541 10.1007/s00239-004-0340-0 16132469
54. Recent duplication and inter-locus gene conversion in major histocompatibility class II genes in a teleost, the three-spined stickleback. TB Reusch H Schaschl KM Wegner, Immunogenetics 2004 56 6 427 437 10.1007/s00251-004-0704-z 15322775
55. PCR Bias in Ecological Analysis: a Case Study for Quantitative Taq Nuclease Assays in Analyses of Microbial Communities. S Becker P Böger R Oehlmann A Ernst, Appl Environ Microbiol 2000 66 11 4945 4953 11055948 10.1128/AEM.66.11.4945-4953.2000
56. Ensembl: Genome of the three-spined stickleback (version March 2008). http://mar2008.archive.ensembl.org/Gasterosteus-aculeatus
57. Molecular trans-species polymorphism. J Klein A Sato S Nagl C O'HUigin, Annu Rev Ecol Syst 1998 29 1 21 10.1146/annurev.ecolsys.29.1.1
58. Mitochondrial DNA phylogeography of the three-spined stickleback (Gasterosteus aculeatus) in Europe Evidence for multiple glacial refugia. HS Mäkinen J Merilä Mol Phylogenet Evol 2008 46 1 167 182 10.1016/j.ympev.2007.06.011 17716925
59. Stimulation and suppression of PCR-mediated recombination. MSB Judo AB Wedel C Wilson, Nucleic Acids Res 1998 26 7 1819 1825 9512558 10.1093/nar/26.7.1819
60. Heteroduplexes in mixed-template amplifications: formation, consequence and elimination by 'reconditioning PCR'. JR Thompson LA Marcelino MF Polz, Nucleic Acids Res 2002 30 9 2083 2088 11972349 10.1093/nar/30.9.2083
61. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. T Hall, Nucleic Acids Symposium Series 1999 41 95 98
62. PRIMER v6: User Manual/Tutorial. KR Clarke RN Gorley, Plymouth: PRIMER-E 2006 190
63. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. K Tamura J Dudley M Nei S Kumar, Mol Biol Evol 2007 24 8 1596 1599 10.1093/molbev/msm092 17488738
64. Scoring residue conservation. WSJ Valdar, Proteins 2002 48 2 227 241 10.1002/prot.10146 12112692
65. Indices of multilocus linkage disequilibrium. P-M Agapow A Burt, Mol Ecol Notes 2001 1 12 101 102 10.1046/j.1471-8278.2000.00014.x
66. Charactreization of polymorphism within the H-2M MHC class II loci. E Hermel J Yuan JJ Monaco, Immunogenetics 1995 42 2 136 142 10.1007/BF00178588 7607704
67. Global Survey of Mitochondrial DNA Sequences in the Threespine Stickleback: Evidence for Recent Migrations. G Orti MA Bell TE Reimchen A Meyer, Evolution 1994 48 3 608 622 10.2307/2410473
68. Multiple parasites are driving major histocompatibility complex polymorphism in the wild. KM Wegner TBH Reusch M Kalbe, J Evol Biol 2003 16 2 224 232 10.1046/j.1420-9101.2003.00519.x 14635861
69. Comparative genomics of major histocompatibility complexes. J Kelley L Walter J Trowsdale, Immunogenetics 2005 56 10 683 695 10.1007/s00251-004-0717-7 15605248
70. PCR Conditions and DNA Denaturants Affect Reproducibility of Single-Strand Conformation Polymorphism Patterns for BRCA1 Mutations. LK Hennessy J Teare C Ko, Clin Chem 1998 44 4 879 882 9554503
71. A new theory of MHC evolution: beyond selection on the immune genes. C van Oosterhout, Proc R Soc Lond B Biol Sci 2009 276 1657 657 665 10.1098/rspb.2008.1299
72. Linkage relationships and haplotype polymorphism among cichlid Mhc class II B loci. E Malaga-Trillo Z Zaleska-Rutczynska B McAndrew V Vincek F Figueroa H Sultmann J Klein, Genetics 1998 149 3 1527 1537 9649539
73. Major histocompatibility complex class II polymorphisms in primates. RE Bontrop N Otting NG de Groot GGM Doxiadis, Immunol Rev 1999 167 1 339 350 10.1111/j.1600-065X.1999.tb01403.x 10319272
74. Variation analysis and gene annotation of eight MHC haplotypes: The MHC haplotype project. R Horton R Gibson P Coggill M Miretti RJ Allcock J Almeida S Forbes JGR Gilbert K Halls JL Harrow, Immunogenetics 2008 60 1 1 18 18193213 10.1007/s00251-007-0262-2
75. The accordion model of Mhc evolution. J Klein H Ono D Klein C O'hUigin, Progress in Immunology Heidelberg: Springer-Verlag, Gergely J, Petranyi G, 1993 137 143