Genetica

, Volume 140, Issue 7–9, pp 349–364 | Cite as

MHC class I variation in a natural blue tit population (Cyanistes caeruleus)

Article

Abstract

The major histocompatibility complex (MHC) is central to the vertebrate immune system and its highly polymorphic genes are considered to influence several life-history traits of individuals. To characterize the MHC in a natural population of blue tits (Cyanistes caeruleus) we investigated the class I exon 3 diversity of more than 900 individuals. We designed two pairs of motif-specific primers that reliably amplify independent subsets of MHC alleles. Applying denaturing gradient gel electrophoresis (DGGE) we obtained 48 independently inherited units of unique band patterns (DGGE-haplogroups), which were validated in a segregation analysis within 105 families. In a second approach, we extensively sequenced 6 unrelated individuals to confirm that DGGE-haplogroup composition reflects individual allelic variation. The highest number of different DGGE-haplogroups in a single individual corresponded in 19 MHC exon 3 sequences, suggesting a minimum of 10 amplified MHC class I loci in the blue tit. In total, we identified 50 unique functional and 3 non-functional sequences. Functional sequences showed high levels of recombination and strong positive selection in the antigen binding region, whereas nucleotide diversity was comparatively low in the range of all passerine species. Finally, in a phylogenetic comparison of passerine MHC class I exon 3 sequences we discuss conflicting evolutionary signals possibly due to recent gene duplication, recombination events and concerted evolution. Our results indicate that the described method is suitable to effectively explore the MHC diversity and its ecological impacts in blue tits in future studies.

Keywords

MHC class I Blue tit Cyanistes caeruleus DGGE Population genetics 

Supplementary material

10709_2012_9679_MOESM1_ESM.doc (212 kb)
Supplementary material 1 (DOC 211 kb)

References

  1. Alcaide M, Edwards SV, Cadahía L, Negro JJ (2009) MHC class I genes of birds of prey: isolation, polymorphism and diversifying selection. Conserv Genet 10:1349–1355CrossRefGoogle Scholar
  2. Andersson S, Örnborg J, Andersson M (1998) Ultraviolet sexual dimorphism and assortative mating in blue tits. Proc R Soc Lond B 265:445–450CrossRefGoogle Scholar
  3. Anmarkrud JA, Johnsen A, Bachmann L, Lifjeld JT (2010) Ancestral polymorphism in exon 2 of bluethroat (Luscinia svecica) MHC class II B genes. J Evol Biol 23:1206–1217PubMedCrossRefGoogle Scholar
  4. Apanius V, Penn D, Slev PR, Ruff LR, Potts WK (1997) The nature of selection on the major histocompatibility complex. Crit Rev Immunol 17:179–224PubMedCrossRefGoogle Scholar
  5. Arriero E (2009) Rearing environment effects on immune defence in blue tit Cyanistes caeruleus nestlings. Oecologia 159:697–704PubMedCrossRefGoogle Scholar
  6. Ashelford AE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2005) At least one in twenty 16S rRNA sequence records currently held in public repositories estimated to contain substantial anomalies. Appl Environ Microbiol 12:7724–7736CrossRefGoogle Scholar
  7. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2006) New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl Environ Microbiol 72:5734–5741PubMedCrossRefGoogle Scholar
  8. Balakrishnan CN, Ekblom R, Völker M, Westerdahl H, Godinez R, Kotkiewicz H, Burt DW, Graves T, Griffin DK, Warren WC (2010) Gene duplication and fragmentation in the zebra finch major histocompatibility complex. BMC Biol 8:29PubMedCrossRefGoogle Scholar
  9. Bensch S, Stjernman M, Hasselquist D, Ostmann O, Hansson B, Westerdahl H, Pinheiro RT (2000) Host specificity in avian blood parasites: a study of plasmodium and haemoproteus mitochondrial DNA amplified from birds. Proc R Soc Lond B 267:1583–1589CrossRefGoogle Scholar
  10. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol 16:363–377PubMedCrossRefGoogle Scholar
  11. Bodmer WF (1972) Evolutionary significance of the HL-A system. Nature 237:139–183PubMedCrossRefGoogle Scholar
  12. Bollmer JL, Vargas FH, Parker PG (2007) Low MHC variation in the endangered Galapagos penguin (Spheniscus mendiculus). Immunogenetics 59:593–602PubMedCrossRefGoogle Scholar
  13. Bollmer JL, Dunn PO, Wittingham LA, Wimpee C (2010) Extensive MHC class II B gene duplication in a passerine, the common yellowthroat (Geothlypis trichas). J Hered 101:448–460PubMedCrossRefGoogle Scholar
  14. Bonneaud C, Mazuc J, Chastel O, Westerdahl H, Sorci G (2004a) Terminal investment induced by immune challenge and fitness traits associated with major histocompatibility complex in the house sparrow. Evolution 58:2823–2830PubMedGoogle Scholar
  15. Bonneaud C, Sorci G, Morin V, Westerdahl H, Zoorob R, Wittzell H (2004b) Diversity of Mhc class I and IIB genes in house sparrows (Passer domesticus). Immunogenetics 55:855–865PubMedCrossRefGoogle Scholar
  16. Bonneaud C, Chastel O, Federici P, Westerdahl H, Sorci G (2006a) Complex Mhc-based mate choice in a wild passerine. Proc R Soc B 273:1111–1116PubMedCrossRefGoogle Scholar
  17. Bonneaud C, Perez-Tris J, Federici P, Chastel O, Sorci G (2006b) Major histocompatibility alleles associated with local resistance to malaria in a passerine. Evolution 60:383–389PubMedGoogle Scholar
  18. Bryant D, Moulton V (2004) Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21(2):255–265Google Scholar
  19. Burri R, Niculita-Hirzel H, Roulin A, Fumagalli L (2008a) Isolation and characterization of major histocompatibility complex (MHC) class II B genes in the Barn owl (Aves: Tyto alba). Immunogenetics 60:543–550PubMedCrossRefGoogle Scholar
  20. Burri R, Niculita-Hirzel H, Salamin N, Roulin A, Fumagalli L (2008b) Evolutionary patterns of MHC class II B in owls and their implications for the understanding of avian MHC evolution. Mol Biol Evol 25:1180–1191PubMedCrossRefGoogle Scholar
  21. Chaves LD, Krueth SB, Reed KM (2009) Defining the turkey MHC: sequence and genes of the B locus. Am Assoc Immnol 183:6530–6537Google Scholar
  22. Delany ME, Robinson CM, Goto RM, Miller MM (2009) Architecture and organization of chicken microchromosome 16: order of the NOR, MHC-Y, and MHC-B subregions. J Hered 100(5):507–514PubMedCrossRefGoogle Scholar
  23. Doherty PC, Zinkernagel RM (1975) Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256:50–52PubMedCrossRefGoogle Scholar
  24. Doutrelant C, Blondel J, Perret P, Lambrechts MM (2000) Blue tit song repertoire size, male quality and interspecific competition. J Avian Biol 31:360–366CrossRefGoogle Scholar
  25. Edwards SV, Dillon M (2004) Hitchhiking and recombination in birds: evidence from Mhc-linked and unlinked loci in Red-winged Blackbirds (Agelaius phoeniceus). Genet Res 84:175–192Google Scholar
  26. 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 92:12200–12204PubMedCrossRefGoogle Scholar
  27. Eimes JA, Bollmer JL, Dunn PO, Whittingham LA, Wimpee C (2010) Mhc class II diversity and balancing selection in greater prairie-chickens. Genetica 138:265–271PubMedCrossRefGoogle Scholar
  28. Ekblom R, Grahn M, Hoglund J (2003) Patterns of polymorphism in the MHC class II of a non-passerine bird, the great snipe (Gallinago media). Immunogenetics 54:734–741PubMedGoogle Scholar
  29. Ekblom R, Stapley J, Ball AD, Birkhead T, Burke T, Slate J (2011) Genetic mapping of the major histocompatibility complex in the zebra finch (Taeniopygia guttata). Immunogenetics 63:523–530PubMedCrossRefGoogle Scholar
  30. Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717PubMedCrossRefGoogle Scholar
  31. Foerster K, Valcu M, Johnsen A, Kempenaers B (2006) A spatial genetic structure and effects of relatedness on mate choice in a wild bird population. Mol Ecol 15:4555–4567PubMedCrossRefGoogle Scholar
  32. Freeman-Gallant CR, Johnson EM, Saponara F, Stanger M (2002) Variation at the major histocompatibility complex in Savannah sparrows. Mol Ecol 11(6):1125–1130PubMedCrossRefGoogle Scholar
  33. Garrigan D, Hedrick PW (2003) Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 57:1707–1722PubMedGoogle Scholar
  34. Gasper JS, Shiina T, Inoko H, Edwards SV (2001) Songbird genomics: analysis of 45 kb upstream of a polymorphic Mhc class II gene in red-winged blackbirds (Agelaius phoeniceus). Genomics 75:26–34PubMedCrossRefGoogle Scholar
  35. Gill FB, Slikas B, Sheldon FH (2005) Phylogeny of titmice (Paridae): II. Species relationships based on sequences of the mitochondrial cytochrome-B gene. Auk 122:121–143CrossRefGoogle Scholar
  36. Gillingham MAF, Richardson DS, Løvlie H, Moynihan A, Worley K, Pizzari T (2009) Cryptic preference for MHC-dissimilar females in male red junglefowl, Gallus gallus. Proc R Soc B 276:1083–1092PubMedCrossRefGoogle Scholar
  37. Guillemot F, Billault A, Pourquie O, Behar G, Chausse AM, Zoorob R, Kreibich G, Auffray C (1988) A molecular map of the chicken major histocompatibility complex: the class II beta genes are closely linked to the class I genes and the nucleolar organizer. EMBO J 7:2775–2785PubMedGoogle Scholar
  38. Guindon S, Gascuel O (2008) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704CrossRefGoogle Scholar
  39. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  40. Hedrick PW (1999) Balancing selection and MHC. Genetica 104:207–214CrossRefGoogle Scholar
  41. Hess CM, Edwards SV (2002) The evolution of the major histocompatibility complex in birds. Bioscience 52:423–431CrossRefGoogle Scholar
  42. Hudson R, Kaplan N (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147–164PubMedGoogle Scholar
  43. Hughes CR, Miles S, Walbroehl JM (2008) Support for the minimal essential MHC hypothesis: a parrot with a single, highly polymorphic MHC class II B gene. Immunogenetics 60:219–231PubMedCrossRefGoogle Scholar
  44. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23(2):254–267PubMedCrossRefGoogle Scholar
  45. 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 13:2157–2168PubMedCrossRefGoogle Scholar
  46. Johansson US, Fjeldså J, Bowie RCK (2008) Phylogenetic relationships within Passerida (Aves: Passeriformes): a review and a new molecular phylogeny based on three nuclear intron markers. Mol Phylogenet Evol 48:858–876PubMedCrossRefGoogle Scholar
  47. Johnsen A, Delhey K, Andersson S, Kempenaers B (2003) Plumage colour in nestling blue tits: sexual dichromatism, condition dependence and genetic effects. Proc R Soc Lond B 270:1263–1270CrossRefGoogle Scholar
  48. Kaufman J, Salomonsen J, Flajnik M (1994) Evolutionary conservation of MHC class I and class II molecules-different yet the same. Semin Immunol 6:411–424PubMedCrossRefGoogle Scholar
  49. Kaufman J, Milne S, Gobel TWF, Walker BA, Jacob JP, Auffray C, Zoorob R, Beck S (1999) The chicken B locus is a minimal essential major histocompatibility complex. Nature 401:923–925PubMedCrossRefGoogle Scholar
  50. Kempenaers B, Verheyen GR, Vandenbroeck M, Burke T, Vanbroeckhoven C, Dhondt AA (1992) Extra-pair paternity results from female preference for high-quality males in the blue tit. Nature 357:494–496CrossRefGoogle Scholar
  51. Kempenaers B, Verheyren GR, Dhondt AA (1997) Extrapair paternity in the blue tit (Parus caeruleus): female choice, male characteristics, and offspring quality. Behav Ecol 8:481–492CrossRefGoogle Scholar
  52. Klein J (1986) Natural history of the major histocompatibility complex. Wiley, New YorkGoogle Scholar
  53. Klein J (1987) Origin of major histocompatibility complex polymorphism: the trans-species hypothesis. Hum Immunol 19:155–162PubMedCrossRefGoogle Scholar
  54. Koch M, Camp S, Collen T, Avila D, Salomonsen J, Wallny HJ, van Hateren A, Hunt L, Jacob JP, Johnston F, Marston DA, Shaw I, Dunbar PR, Cerundolo V, Jones EY, Kaufman J (2007) Structures of an MHC class I molecule from B21 chickens illustrate promiscuous peptide binding. Immunity 27:885–899PubMedCrossRefGoogle Scholar
  55. Langefors Å, Lohm J, Von Schantz T, Grahn M (2000) Screening of Mhc variation in Atlantic salmon (Salmo salar): a comparison of restriction fragment length polymorphism (RFLP), denaturing gradient gel electrophoresis (DGGE) and sequencing. Mol Ecol 9:215–219PubMedCrossRefGoogle Scholar
  56. Loiseau C, Zoorob R, Garnier S, Birard J, Federici P, Julliard R, Sorci G (2008) Antagonistic effects of a Mhc class I allele on malaria-infected house sparrows. Ecology 11:258–265Google Scholar
  57. Merino S, Moreno J, José Sanz J, Arriero E (2000) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proc R Soc Lond B 267:2507–2510CrossRefGoogle Scholar
  58. Mesa CM, Thulien KJ, Moon DA, Veniamin SM, Magor KE (2004) The dominant MHC class I gene is adjacent to the polymorphic TAP2 gene in the duck, Anas platyrhynchos. Immunogenetics 56:192–203PubMedCrossRefGoogle Scholar
  59. Milinski M (2003) The function of mate choice in sticklebacks: optimizing Mhc genetics. J Fish Biol 63:1–16CrossRefGoogle Scholar
  60. Milinksi M (2006) The major histocompatibility complex, sexual selection, and mate choice. Annu Rev Ecol Evol Syst 37:159–186CrossRefGoogle Scholar
  61. Miller HC, Lambert DM (2004) Gene duplication and gene conversion in class II MHC genes of New Zealand robins (Petroicidae). Immunogenetics 56:178–191PubMedGoogle Scholar
  62. Miller KM, Ming TB, Schulze AD, Withler RE (1999) Denaturing gradient gel electrophoresis (DGGE): a rapid and sensitive technique to screen nucleotide sequence variation in populations. Biotechniques 27:1016–1030PubMedGoogle Scholar
  63. Miller MM, Bacon LD, Hala K, Hunt HD, Ewald SJ, Kaufman J, Zoorob R, Briles WE (2004) 2004 Nomenclature for the chicken major histocompatibility (B and Y) complex. Immunogenetics 56:261–279PubMedGoogle Scholar
  64. Miller HC, Bowker-Wright G, Kharkrang M, Ramstad K (2011) Characterisation of class II B MHC genes from a ratite bird, the little spotted kiwi (Apteryx owenii). Immunogenetics 63:223–233PubMedCrossRefGoogle Scholar
  65. Møller AP (1999) Good-genes effects in sexual selection. Proc Biol Sci 226:85–91CrossRefGoogle Scholar
  66. Murphy KP, Travers P, Walport M (2008) Janeway’s immunobiology, 7th edn. Taylor & Francis, LondonGoogle Scholar
  67. Myers RM, Maniatis T, Lerman LS (1987) Detection and localization of single base changes by denaturing gradient gel electrophoresis. Meth Enzymol 155:501–527PubMedCrossRefGoogle Scholar
  68. Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol 14:19–38PubMedCrossRefGoogle Scholar
  69. Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121–152PubMedCrossRefGoogle Scholar
  70. Ohta T (1999) Effect of gene conversion on polymorphic patterns at major histocompatibility complex loci. Immunol Rev 167:319–325PubMedCrossRefGoogle Scholar
  71. Parker TH, Barr IR, Griffith SC (2006) The blue tit’s song is an inconsistent signal of male condition. Behav Ecol 17:1029–1040CrossRefGoogle Scholar
  72. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21PubMedGoogle Scholar
  73. Poesel A, Foerster K, Kempenaers B (2001) The dawn song of the blue tit Parus caeruleus and its role in sexual selection. Ethology 107:521–531CrossRefGoogle Scholar
  74. Pond SLK, Frost SDW (2005a) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531–2533PubMedCrossRefGoogle Scholar
  75. Pond SLK, Frost SDW (2005b) Not so different after all: a comparison of methods for detecting amino acid sites under selection. SMBE 22:1208–1222Google Scholar
  76. Pond SLK, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21(5):676–679PubMedCrossRefGoogle Scholar
  77. Posada (2009) Selection of models of DNA evolution with jModelTest. Methods Mol Biol 537:93–112PubMedCrossRefGoogle Scholar
  78. Potts WK, Wakeland EK (1990) Evolution of diversity at the major histocompatibility complex. Trends Ecol Evol 5:181–187PubMedCrossRefGoogle Scholar
  79. Potts WK, Wakeland EK (1993) Evolution of Mhc genetic diversity—a tale of incest, pestilence and sexual preference. Trends Genet 9:408–412PubMedCrossRefGoogle Scholar
  80. Promerová M, Albrecht T, Bryja J (2009) Extremely high MHC class I variation in a population of a long-distance migrant, the Scarlet Rosefinch (Carpodacus erythrinus). Immunogenetics 61:451–461PubMedCrossRefGoogle Scholar
  81. Reusch TBH, Haberli MA, Aeschlimann PB, Milinski M (2001) Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414:300–302PubMedCrossRefGoogle Scholar
  82. Richardson DS, Westerdahl H (2003) MHC diversity in two Acrocephalus species: the outbred Great reed warbler and the inbred Seychelles warbler. Mol Ecol 12:3523–3529PubMedCrossRefGoogle Scholar
  83. Richardson DS, Komdeur J, Burke T, von Schantz T (2005) MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler. Proc R Soc B 272:759–767PubMedCrossRefGoogle Scholar
  84. Rozas J (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Oxford University Press, Oxford, pp 174–175Google Scholar
  85. Sato A, Mayer WE, Tichy H, Grant PR, Grant BR, Klein J (2001) Evolution of Mhc class II B genes in Darwin’s finches and their closest relatives: birth of a new gene. Immunogenetics 53:792–801PubMedCrossRefGoogle Scholar
  86. Sato A, Tichy H, Grant PR, Grant BR, Sato T, O’hUigin C (2011) Spectrum of MHC Class II variability in Darwin’s finches and their close relatives. Mol Biol Evol 28(6):1943–1956PubMedCrossRefGoogle Scholar
  87. Sawyer SA (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538PubMedGoogle Scholar
  88. Schut E, Aguilar JR, Merino S, Magrath MJL, Komdeur J, Westerdahl H (2011) Characterization of MHC-I in the blue tit (Cyanistes caeruleus) reveals low levels of genetic diversity and trans-population evolution across European populations. Immunogenetics 63:531–542PubMedCrossRefGoogle Scholar
  89. Seutin G, White BN, Boag P (1991) Preservation of avian blood and tissue for DNA analyses. Can J Zool 69:82–90CrossRefGoogle Scholar
  90. Sheldon FH, Gill FB (1996) A reconsideration of songbird phylogeny, with emphasis on the evolution of titmice and their sylvioid relatives. Syst Boil 45:473–495CrossRefGoogle Scholar
  91. Shiina T, Shimizu S, Hosomichi K, Kohara S, Watanabe S, Hanzawa K, Beck S, Kulski JK, Inoko H (2004) Comparative genomic analysis of two avian (quail and chicken) MHC regions. J Immunol 172:6751–6763PubMedGoogle Scholar
  92. Slikas B, Sheldon FH, Gill FB (1996) Phylogeny of titmice (Paridae): I. Estimate of relationships among subgenera based on DNA–DNA hybridization. J Avian Biol 27:70–82CrossRefGoogle Scholar
  93. Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2:16–34PubMedCrossRefGoogle Scholar
  94. Stjernman M, Raberg L, Nilsson JA (2004) Survival costs of reproduction in the blue tit (Parus caeruleus): a role for blood parasites? Proc R Soc Lond 271:2387–2394CrossRefGoogle Scholar
  95. Strand T, Westerdahl H, Hoeglund J, Alatalo RV, Siitari H (2007) The Mhc class II of the Black grouse (Tetrao tetrix) consists of low numbers of B and Y genes with variable diversity and expression. Immunogenetics 59:725–734PubMedCrossRefGoogle Scholar
  96. Strandh M, Lannefors M, Bonadonna F, Westerdahl H (2011) Characterization of MHC class I and II genes in a subantarctic seabird, the blue petrel, Halobaena caerulea (Procellariiformes). Immunogenetics 63:653–666PubMedCrossRefGoogle Scholar
  97. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. SMBE 24:1596–1599Google Scholar
  98. Tomás G, Merino S, Moreno J, Sanz JJ, Morales J, García-Fraile S (2006) Nest weight and female health in the blue tit (Cyanistes caeruleus). Auk 123:1013–1021Google Scholar
  99. Tomás G, Merino S, Moreno J, Morales J (2007) Consequences of nest reuse for parasite burden and female health and condition in blue tits, Cyanistes caeruleus. Anim Behav 73:805–814CrossRefGoogle Scholar
  100. Wallny H, Avila D, Hunt L, Powell T, Riegert P, Salomonsen J, Skjodt K, Vainio O, Vilbois F, Wiles M, Kaufman J (2006) Peptide motifs of the single dominantly expressed class I molecule explain the striking MHC-determined response to Rous sarcoma virus in chicken. Proc Natl Acad Sci USA 103:1434–1439Google Scholar
  101. Wegner K, Kalbe M, Schaschl H, Reusch T (2004) Parasites and individual major histocompatibility complex diversity-an optimal choice? Microbes Infect 6:1110–1116PubMedCrossRefGoogle Scholar
  102. Westerdahl H (2004) No evidence of an MHC-based female mating preference in great reed warblers. Mol Ecol 13:2465–2470PubMedCrossRefGoogle Scholar
  103. Westerdahl H (2007) Passerine MHC: genetic variation and disease resistance in the wild. J Ornithol 148:469–477CrossRefGoogle Scholar
  104. Westerdahl H, Wittzell H, von Schantz T (1999) Polymorphism and transcription of Mhc class I genes in a passerine bird, the great reed warbler. Immunogenetics 49:158–170PubMedCrossRefGoogle Scholar
  105. Westerdahl H, Wittzell H, von Schantz T, Bensch S (2004) MHC class I typing in a songbird with numerous loci and high polymorphism using motif-specific PCR and DGGE. Heredity 92:534–542PubMedCrossRefGoogle Scholar
  106. Westerdahl H, Waldenström 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 272:1511–1518PubMedCrossRefGoogle Scholar
  107. Wittzell H, Madsen T, Westerdahl H, Shine R, von Schantz T (1998) MHC variation in birds and reptiles. Genetica 104:301–309PubMedCrossRefGoogle Scholar
  108. 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 16:479–490PubMedCrossRefGoogle Scholar
  109. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13(5):555–556PubMedGoogle Scholar
  110. Yang Z (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591PubMedCrossRefGoogle Scholar
  111. Yang Z, Wong WSW, Nielsen R (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22(4):1107–1118PubMedCrossRefGoogle Scholar
  112. Ziegler A, Kentenich H, Uchanska-Ziegier B (2005) Female choice and the MHC. Trends Immunol 26:496–502PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Department of Behavioural Ecology and Evolutionary GeneticsMax Planck Institute for OrnithologySeewiesenGermany
  2. 2.Comparative ZoologyInstitute of Evolution and Ecology, University of TübingenTübingenGermany

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