454 screening of individual MHC variation in an endemic island passerine

Immunogenetics

Volumn 67, Issue 3, 2015, Pages 149-162

  Gonzalez Quevedo, Catalina ^a   Phillips, Karl P ^a,b   Spurgin, Lewis G ^a,c   Richardson, David S ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b ADAM MICKIEWICZ UNIVERSITY   (Poland)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

454; Allele amplification efficiency; Anthus berthelotii; Anthus campestris; Berthelot s pipit; Major histocompatibility complex; Tawny pipit

Indexed keywords

ALLELE; ANTHUS BERTHELOTII; ANTHUS CAMPESTRIS; ARTICLE; GENE; GENE AMPLIFICATION; GENE CONVERSION; GENE FREQUENCY; GENETIC VARIABILITY; GENOTYPE; MAJOR HISTOCOMPATIBILITY COMPLEX; MAJOR HISTOCOMPATIBILITY COMPLEX CLASS 1 GENE; NEXT GENERATION SEQUENCING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SONGBIRD; ANIMAL; ANIMAL DISPERSAL; CLASSIFICATION; DNA SEQUENCE; EXON; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETICS; IMMUNOLOGY; PASSERIFORMES; PHYLOGENY; SPAIN; SPECIES DIFFERENTIATION;

ANTHUS BERTHELOTII; ANTHUS CAMPESTRIS; PASSERIFORMES; VERTEBRATA;

ALLELES; ANIMAL DISTRIBUTION; ANIMALS; EXONS; GENE CONVERSION; GENE FREQUENCY; GENES, MHC CLASS I; GENETIC SPECIATION; PASSERIFORMES; PHYLOGENY; POLYMORPHISM, GENETIC; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA; SPAIN;

EID: 84922691549     PISSN: 00937711     EISSN: 14321211     Source Type: Journal    
DOI: 10.1007/s00251-014-0822-1     Document Type: Article

References (106)

1. 454 Life Sciences Corp (2009) Using Multiplex Identifier (MID) Adaptors for the GS FLX titanium chemistry - extended MID Set 454 sequencing technical bulletin 005–2009:1–7
2. Alcaide M, Edwards SV, Negro JJ, Serrano D, Tella JL (2008) Extensive polymorphism and geographical variation at a positively selected MHC class IIB gene of the lesser kestrel (Falco naumanni). Mol Ecol 17:2652–2665
3. Alcaide M, Liu M, Edwards SV (2013) Major histocompatibility complex class I evolution in songbirds: universal primers, rapid evolution and base compositional shifts in exon 3. Peer J 1:e86
4. Babik W (2010) Methods for MHC genotyping in non-model vertebrates. Mol Ecol Resour 10:237–251
5. Babik W, Taberlet P, Ejsmond MJ, Radwan J (2009) New generation sequencers as a tool for genotyping of highly polymorphic multilocus MHC system. Mol Ecol Resour 9:713–719
6. Baquero JE et al (2006) Reference strand conformational analysis (RSCA) is a valuable tool in identifying MHC-DRB sequences in three species of Aotus monkeys. Immunogenetics 58:590–597
7. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol 16:363–377
8. Beuf KD, Schrijver JD, Thas O, Criekinge WV, Irizarry RA, Clement L (2012) Improved base-calling and quality scores for 454 sequencing based on a Hurdle Poisson model. BMC Bioinforma 13:303
9. Bjorkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, Wiley DC (1987) Structure of the human class-I histocompatibility antigen, HLA-A2. Nature 329:506–512
10. Bodmer JG et al (1997) Nomenclature for factors of the HLA system, 1996. Tissue Antigens 49:297–321
11. Bollmer JL, Hull JM, Ernest HB, Sarasola JH, Parker PG (2011) Reduced MHC and neutral variation in the Galapagos hawk, an island endemic. BMC Evol Biol 11:143
12. Boni MF, Posada D, Feldman MW (2007) An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176:1035–1047
13. Bonneaud C, Perez-Tris J, Federici P, Chastel O, Sorci G (2006) Major histocompatibility alleles associated with local resistance to malaria in a passerine. Evolution 60:383–389
14. Bradley RD, Hillis DM (1997) Recombinant DNA sequences generated by PCR amplification. Mol Biol Evol 14:592–593
15. Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC (1993) 3-Dimensional structure of the human class II-histocompatinility antigen HLA-DR1. Nature 364:33–39
16. Bryant D, Moulton V (2004) Neighbor-Net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21:255–265
17. Chelvanayagam G (1996) A roadmap for HLA-A, HLA-B, and HLA-C peptide binding specificities. Immunogenetics 45:15–26
18. Cheng Y et al (2012) Antigen-presenting genes and genomic copy number variations in the Tasmanian devil MHC. BMC Genomics 13:87
19. Cramp S, Perrins CM (1977–1994) Handbook of the birds of Europe, the Middle East and Africa. The birds of the western Palearctic. Oxford University Press, Oxford
20. Doytchinova IA, Flower DR (2005) In silico identification of supertypes for class II MHCs. J Immunol 174:7085–7095
21. Dunn PO, Bollmer JL, Freeman-Gallant CR, Whittingham LA (2013) MHC variation is related to a sexually selected ornament, survival, and parasite resistance in common yellowthroats. Evolution 67:679–687
22. Edwards SV, Hedrick PW (1998) Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 13:305–311
23. Ellison A, Allainguillaume J, Girdwood S, Pachebat J, Peat KM, Wright P, Consuegra S (2012) Maintaining functional major histocompatibility complex diversity under inbreeding: the case of a selfing vertebrate. Proc R Soc B Biol Sci 279:5004–5013
24. Evans ML, Neff BD (2009) Major histocompatibility complex heterozygote advantage and widespread bacterial infections in populations of Chinook salmon (Oncorhynchus tshawytscha). Mol Ecol 18:4716–4729
25. Frank SA (2002) Immunology and evolution of infectious disease. Princeton University Press, Princeton
26. Galan M, Guivier E, Caraux G, Charbonnel N, Cosson JF (2010) A 454 multiplex sequencing method for rapid and reliable genotyping of highly polymorphic genes in large-scale studies. BMC Genomics 11:15
27. Garcia-Del-Rey E, Cresswell W (2007) The breeding biology of the endemic Berthelot's Pipit, Anthus berthelotii, in a harsh oceanic island environment (Tenerife, Canary Islands). Ostrich 78:583–589
28. Geliebter J, Nathenson SG (1988) Microrecombinations generate sequence diversity in the murine major histocompatibility complex: analysis of the Kbm3, Kbm4, Kbm10, and Kbm11 mutants. Mol Cell Biol 8:4342–4352
29. Gibbs MJ, Armstrong JS, Gibbs AJ (2000) Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16:573–582
30. Gonzalez-Quevedo C, Davies RG, Richardson DS (2014) Predictors of malaria infection in a wild bird population: landscape-level analyses reveal climatic and anthropogenic factors. J Anim Ecol 83:1091–1102
31. 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
32. Hill AVS et al (1991) Common West African HLA antigens are associated with protection from severe malaria. Nature 352:595–600
33. Hogstrand K, Bohme J (1999) Gene conversion can create new MHC alleles. Immunol Rev 167:305–317
34. Holcomb CL, Rastrou M, Williams TC, Goodridge D, Lazaro AM, Tilanus M, Erlich HA (2014) Next-generation sequencing can reveal in vitro-generated PCR crossover products: some artifactual sequences correspond to HLA alleles in the IMGT/HLA database. Tissue Antigens 83:32–40
35. Huchard E, Weill M, Cowlishaw G, Raymond M, Knapp LA (2008) Polymorphism, haplotype composition, and selection in the Mhc-DRB of wild baboons. Immunogenetics 60:585–598
36. 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
37. Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class-I loci reveals overdominant selection. Nature 335:167–170
38. Huse SM, Huber JA, Morrison HG, Sogin ML, Mark Welch D (2007) Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol 8:R143
39. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267
40. Illera JC (2007) Bisbita Caminero Anthus berthelotii. In: Lorenzo JA (ed) Atlas de las aves nidificantes en el archipiélago Canario (1997–2003). General de Conservación de la Naturaleza-Sociedad Española de Ornitología, Madrid, pp 344–347
41. Illera JC, Emerson BC, Richardson DS (2007) Population history of Berthelot’s pipit: colonization, gene flow and morphological divergence in Macaronesia. Mol Ecol 16:4599–4612
42. Jaratlerdsiri W et al (2014) Evolution of MHC class I in the Order Crocodylia. Immunogenetics 66:53–65
43. Jarvi SI, Tarr CL, McIntosh CE, Atkinson CT, Fleischer RC (2004) Natural selection of the major histocompatibility complex (MHC) in Hawaiian honeycreepers (Drepanidinae). Mol Ecol 13:2157–2168
44. Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405
45. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94
46. Kelley J, Walter L, Trowsdale J (2005) Comparative genomics of major histocompatibility complexes. Immunogenetics 56:683–695
47. Kiemnec-Tyburczy KM, Richmond JQ, Savage AE, Zamudio KR (2010) Selection, trans-species polymorphism, and locus identification of major histocompatibility complex class II beta alleles of New World ranid frogs. Immunogenetics 62:741–751
48. Klein J, Satta Y, Ohuigin C, Takahata N (1993) The molecular descent of the major histocompatibility complex. Annu Rev Immunol 11:269–295
49. Klein J, O'Huigin C, Mims CA, Lines J, Deutsch J, Hughes AL (1994) MHC polymorphism and parasites (and discussion). Phil Trans R Soc Lond B Biol Sci 346:351–358
50. Klein J, Sato A, Nagl S, O'Huigin C (1998) Molecular trans-species polymorphism. Annu Rev Ecol Syst 29:1–21
51. Kloch A, Babik W, Bajer A, Sinski E, Radwan J (2010) Effects of an MHC-DRB genotype and allele number on the load of gut parasites in the bank vole Myodes glareolus. Mol Ecol 19:255–265
52. Lenz TL, Becker S (2008) Simple approach to reduce PCR artefact formation leads to reliable genotyping of MHC and other highly polymorphic loci—implications for evolutionary analysis. Gene 427:117–123
53. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
54. Lighten J, van Oosterhout C, Bentzen P (2014a) Critical review of NGS analyses for de novo genotyping multigene families. Mol Ecol 23:3957–3972
55. Lighten J, van Oosterhout C, Paterson IG, McMullan M, Bentzen P (2014b) Ultra-deep Illumina sequencing accurately identifies MHC class IIb alleles and provides evidence for copy number variation in the guppy (Poecilia reticulata). Mol Ecol Resour 14:753–767
56. Margulies M et al (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380
57. Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463
58. May S, Zeisset I, Beebee TJC (2011) Larval fitness and immunogenetic diversity in chytrid-infected and uninfected natterjack toad (Bufo calamita) populations. Conserv Genet 12:805–811
59. Meyerhans A, Vartanian JP, Wainhobson S (1990) DNA recombinatiion during PCR. Nucleic Acids Res 18:1687–1691
60. Meyer-Lucht Y, Otten C, Puettker T, Pardini R, Paul Metzger J, Sommer S (2010) Variety matters: adaptive genetic diversity and parasite load in two mouse opossums from the Brazilian Atlantic forest. Conserv Genet 11:2001–2013
61. Mona S et al (2008) Disentangling the effects of recombination, selection, and demography on the genetic variation at a major histocompatibility complex class II gene in the alpine chamois. Mol Ecol 17:4053–4067
62. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Pond SLK (2012) Detecting individual sites subject to episodic diversifying selection. PLoS Genet 8:e1002764
63. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Pond SLK, Scheffler K (2013) FUBAR: a fast, unconstrained bayesian approximation for inferring selection. Mol Biol Evol 30:1196–1205
64. Mwenda JM, Hashiba K, Bambra CS, Shotake T (1997) Analysis of primate major histocompatibility complex (MHC)-DQA1 locus by PCR-single strand conformation polymorphism (SSCP). Cell Mol Biol 43:471–475
65. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426
66. Niskanen AK et al (2014) Balancing selection and heterozygote advantage in major histocompatibility complex loci of the bottlenecked Finnish wolf population. Mol Ecol 23:875–889
67. 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
68. Ohta T (1999) Effect of gene conversion on polymorphic patterns at major histocompatibility complex loci. Immunol Rev 167:319–325
69. Padidam M, Sawyer S, Fauquet CM (1999) Possible emergence of new geminiviruses by frequent recombination. Virology 265:218–225
70. Pond SLK, Frost SDW (2005a) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531–2533
71. Pond SLK, Frost SDW (2005b) Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22:1208–1222
72. Posada D, Crandall KA (2001) Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A 98:13757–13762
73. Potts WK, Wakeland EK (1990) Evolution of diversity at the major histocompatibility complex. Trends Ecol Evol 5:181–187
74. Promerová M, Babik W, Bryja J, Albrecht T, Stuglik M, Radwan J (2012) Evaluation of two approaches to genotyping major histocompatibility complex class I in a passerine-CE-SSCP and 454 pyrosequencing. Mol Ecol Resour 12:285–292
75. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
76. Radwan J, Biedrzycka A, Babik W (2010) Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 143:537–544
77. Richardson DS, Westerdahl H (2003) MHC diversity in two Acrocephalus species: the outbred Great reed warbler and the inbred Seychelles warbler. Mol Ecol 12:3523–3529
78. Richardson DS, Jury FL, Blaakmeer K, Komdeur J, Burke T (2001) Parentage assignment and extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus sechellensis). Mol Ecol 10:2263–2273
79. Robinson J, Halliwell JA, McWilliam H, Lopez R, Parham P, Marsh SGE (2013) The IMGT/HLA database. Nucleic Acids Res 41:D1222–D1227
80. Sandberg M, Eriksson L, Jonsson J, Sjostrom M, Wold S (1998) New chemical descriptors relevant for the design of biologically active peptides. A multivariate characterization of 87 amino acids. J Med Chem 41:2481–2491
81. Schwensow N, Fietz J, Dausmann KH, Sommer S (2007) Neutral versus adaptive genetic variation in parasite resistance: importance of major histocompatibility complex supertypes in a free-ranging primate. Heredity 99:265–277
82. Sepil I, Moghadam HK, Huchard E, Sheldon BC (2012) Characterization and 454 pyrosequencing of Major Histocompatibility Complex class I genes in the great tit reveal complexity in a passerine system. BMC Evol Biol 12:68
83. Sepil I, Lachish S, Hinks AE, Sheldon BC (2013) Mhc supertypes confer both qualitative and quantitative resistance to avian malaria infections in a wild bird population. Proc R Soc B Biol Sci 280
84. Sidney J et al (1995) Several HLA alleles share overlapping peptide specificities. J Immunol 154:247–259
85. Smith JM (1992) Analyzing the mosaic structure of genes. J Mol Evol 34:126–129
86. Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2:16
87. Sommer S, Courtiol A, Mazzoni CJ (2013) MHC genotyping of non-model organisms using next-generation sequencing: a new methodology to deal with artefacts and allelic dropout. BMC Genomics 14:542
88. Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc B Biol Sci 277:979–988
89. Spurgin LG, van Oosterhout C, Illera JC, Bridgett S, Gharbi K, Emerson BC, Richardson DS (2011) Gene conversion rapidly generates major histocompatibility complex diversity in recently founded bird populations. Mol Ecol 20:5213–5225
90. Spurgin LG, Illera JC, Padilla DP, Richardson DS (2012) Biogeographical patterns and co-occurrence of pathogenic infection across island populations of Berthelot's pipit (Anthus berthelotii). Oecologia 168:691–701
91. Spurgin LG, Illera JC, Jorgensen TH, Dawson DA, Richardson DS (2014) Genetic and phenotypic divergence in an island bird: isolation by distance, by colonisation or by adaptation? Mol Ecol 23:1028–1039
92. Sutton JT, Robertson BC, Grueber CE, Stanton JAL, Jamieson IG (2013) Characterization of MHC class II B polymorphism in bottlenecked New Zealand saddlebacks reveals low levels of genetic diversity. Immunogenetics 65:619–633
93. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
94. Torimiro JN et al (2006) HLA class I diversity among rural rainforest inhabitants in Cameroon: identification of A*2612-B*4407 haplotype. Tissue Antigens 67:30–37
95. Ujvari B, Belov K (2011) Major histocompatibility complex (MHC) markers in conservation biology. Int J Mol Sci 12:5168–5186
96. van Oosterhout C (2009) Trans-species polymorphism, HLA-disease associations and the evolution of the MHC. Commun Integr Biol 2:408–410
97. van Oosterhout C (2013) Maintenance of major histocompatibility supertype variation in selfing vertebrate is no evidence for overdominant selection. Proc R Soc B Biol Sci 280:20122501
98. Voelker G (1999) Dispersal, vicariance, and clocks: historical biogeography and speciation in a cosmopolitan passerine genus (Anthus: motacillidae). Evolution 53:1536–1552
99. Wakelin D (1996) Immunity to parasites: how parasitic infections are controlled, 2nd edn. Cambridge University Press, Cambridge
100. Wakelin D, Apanius V (1997) Immune defence: genetic control. Host-parasite evolution, general principles and avian models. Oxford University Press, Oxford
101. Westerdahl H, Hansson B, Bensch S, Hasselquist D (2004) Between-year variation of MHC allele frequencies in great reed warblers: selection or drift? J Evol Biol 17:485–492
102. Westerdahl H, Waldenstrom J, Hansson B, Hasselquist D, von Schantz T, Bensch S (2005) Associations between malaria and MHC genes in a migratory songbird. Proc R Soc B Biol Sci 272:1511–1518
103. Worley K, Gillingham M, Jensen P, Kennedy LJ, Pizzari T, Kaufman J, Richardson DS (2008) Single locus typing of MHC class I and class IIB loci in a population of red jungle fowl. Immunogenetics 60:233–247
104. Wright DJ, Spurgin LG, Collar NJ, Komdeur J, Burke T, Richardson DS (2014) The impact of translocations on neutral and functional genetic diversity within and among populations of the Seychelles warbler. Mol Ecol 23:2165–2177
105. Yasukochi Y, Kurosaki T, Yoneda M, Koike H, Satta Y (2012) MHC class II DQB diversity in the Japanese black bear, Ursus thibetanus japonicus. BMC Evol Biol 12:230
106. Zagalska-Neubauer M, Babik W, Stuglik M, Gustafsson L, Cichon M, Radwan J (2010) 454 sequencing reveals extreme complexity of the class II Major Histocompatibility Complex in the collared flycatcher. BMC Evol Biol 10:395