Skip to main content
SpringerLink
Log in

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

  • Published:
Genetica Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alcaide M, Edwards SV, Cadahía L, Negro JJ (2009) MHC class I genes of birds of prey: isolation, polymorphism and diversifying selection. Conserv Genet 10:1349–1355

    Article  CAS  Google Scholar 

  • Andersson S, Örnborg J, Andersson M (1998) Ultraviolet sexual dimorphism and assortative mating in blue tits. Proc R Soc Lond B 265:445–450

    Article  Google Scholar 

  • 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 23:1206–1217

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Arriero E (2009) Rearing environment effects on immune defence in blue tit Cyanistes caeruleus nestlings. Oecologia 159:697–704

    Article  PubMed  Google Scholar 

  • 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 12:7724–7736

    Article  CAS  Google Scholar 

  • 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 72:5734–5741

    Article  PubMed  CAS  Google Scholar 

  • 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 8:29

    Article  PubMed  CAS  Google Scholar 

  • 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 267:1583–1589

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bodmer WF (1972) Evolutionary significance of the HL-A system. Nature 237:139–183

    Article  PubMed  CAS  Google Scholar 

  • Bollmer JL, Vargas FH, Parker PG (2007) Low MHC variation in the endangered Galapagos penguin (Spheniscus mendiculus). Immunogenetics 59:593–602

    Article  PubMed  CAS  Google Scholar 

  • 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 101:448–460

    Article  PubMed  CAS  Google Scholar 

  • 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 58:2823–2830

    PubMed  CAS  Google Scholar 

  • 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 55:855–865

    Article  PubMed  CAS  Google Scholar 

  • Bonneaud C, Chastel O, Federici P, Westerdahl H, Sorci G (2006a) Complex Mhc-based mate choice in a wild passerine. Proc R Soc B 273:1111–1116

    Article  PubMed  CAS  Google Scholar 

  • 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 60:383–389

    PubMed  CAS  Google Scholar 

  • Bryant D, Moulton V (2004) Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21(2):255–265

    Google Scholar 

  • 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 60:543–550

    Article  PubMed  CAS  Google Scholar 

  • 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 25:1180–1191

    Article  PubMed  CAS  Google Scholar 

  • Chaves LD, Krueth SB, Reed KM (2009) Defining the turkey MHC: sequence and genes of the B locus. Am Assoc Immnol 183:6530–6537

    CAS  Google Scholar 

  • 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):507–514

    Article  PubMed  CAS  Google Scholar 

  • Doherty PC, Zinkernagel RM (1975) Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256:50–52

    Article  PubMed  CAS  Google Scholar 

  • Doutrelant C, Blondel J, Perret P, Lambrechts MM (2000) Blue tit song repertoire size, male quality and interspecific competition. J Avian Biol 31:360–366

    Article  Google Scholar 

  • 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 84:175–192

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Eimes JA, Bollmer JL, Dunn PO, Whittingham LA, Wimpee C (2010) Mhc class II diversity and balancing selection in greater prairie-chickens. Genetica 138:265–271

    Article  PubMed  CAS  Google Scholar 

  • 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 54:734–741

    PubMed  CAS  Google Scholar 

  • 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 63:523–530

    Article  PubMed  CAS  Google Scholar 

  • Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717

    Article  PubMed  CAS  Google Scholar 

  • 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 15:4555–4567

    Article  PubMed  CAS  Google Scholar 

  • Freeman-Gallant CR, Johnson EM, Saponara F, Stanger M (2002) Variation at the major histocompatibility complex in Savannah sparrows. Mol Ecol 11(6):1125–1130

    Article  PubMed  CAS  Google Scholar 

  • Garrigan D, Hedrick PW (2003) Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 57:1707–1722

    PubMed  CAS  Google Scholar 

  • 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 75:26–34

    Article  PubMed  CAS  Google Scholar 

  • Gill FB, Slikas B, Sheldon FH (2005) Phylogeny of titmice (Paridae): II. Species relationships based on sequences of the mitochondrial cytochrome-B gene. Auk 122:121–143

    Article  Google Scholar 

  • 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 276:1083–1092

    Article  PubMed  CAS  Google Scholar 

  • 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 7:2775–2785

    PubMed  CAS  Google Scholar 

  • Guindon S, Gascuel O (2008) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hedrick PW (1999) Balancing selection and MHC. Genetica 104:207–214

    Article  CAS  Google Scholar 

  • Hess CM, Edwards SV (2002) The evolution of the major histocompatibility complex in birds. Bioscience 52:423–431

    Article  Google Scholar 

  • Hudson R, Kaplan N (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147–164

    PubMed  CAS  Google Scholar 

  • 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 60:219–231

    Article  PubMed  CAS  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23(2):254–267

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 48:858–876

    Article  PubMed  CAS  Google Scholar 

  • 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 270:1263–1270

    Article  Google Scholar 

  • Kaufman J, Salomonsen J, Flajnik M (1994) Evolutionary conservation of MHC class I and class II molecules-different yet the same. Semin Immunol 6:411–424

    Article  PubMed  CAS  Google Scholar 

  • 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 401:923–925

    Article  PubMed  CAS  Google Scholar 

  • 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 357:494–496

    Article  Google Scholar 

  • Kempenaers B, Verheyren GR, Dhondt AA (1997) Extrapair paternity in the blue tit (Parus caeruleus): female choice, male characteristics, and offspring quality. Behav Ecol 8:481–492

    Article  Google Scholar 

  • Klein J (1986) Natural history of the major histocompatibility complex. Wiley, New York

    Google Scholar 

  • Klein J (1987) Origin of major histocompatibility complex polymorphism: the trans-species hypothesis. Hum Immunol 19:155–162

    Article  PubMed  CAS  Google Scholar 

  • 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 27:885–899

    Article  PubMed  CAS  Google Scholar 

  • 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 9:215–219

    Article  PubMed  CAS  Google Scholar 

  • 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 11:258–265

    Google Scholar 

  • 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 267:2507–2510

    Article  CAS  Google Scholar 

  • 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 56:192–203

    Article  PubMed  CAS  Google Scholar 

  • Milinski M (2003) The function of mate choice in sticklebacks: optimizing Mhc genetics. J Fish Biol 63:1–16

    Article  Google Scholar 

  • Milinksi M (2006) The major histocompatibility complex, sexual selection, and mate choice. Annu Rev Ecol Evol Syst 37:159–186

    Article  Google Scholar 

  • Miller HC, Lambert DM (2004) Gene duplication and gene conversion in class II MHC genes of New Zealand robins (Petroicidae). Immunogenetics 56:178–191

    PubMed  CAS  Google Scholar 

  • 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 27:1016–1030

    PubMed  CAS  Google Scholar 

  • 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 56:261–279

    PubMed  CAS  Google Scholar 

  • 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 63:223–233

    Article  PubMed  CAS  Google Scholar 

  • Møller AP (1999) Good-genes effects in sexual selection. Proc Biol Sci 226:85–91

    Article  Google Scholar 

  • Murphy KP, Travers P, Walport M (2008) Janeway’s immunobiology, 7th edn. Taylor & Francis, London

    Google Scholar 

  • Myers RM, Maniatis T, Lerman LS (1987) Detection and localization of single base changes by denaturing gradient gel electrophoresis. Meth Enzymol 155:501–527

    Article  PubMed  CAS  Google Scholar 

  • Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol 14:19–38

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121–152

    Article  PubMed  CAS  Google Scholar 

  • Ohta T (1999) Effect of gene conversion on polymorphic patterns at major histocompatibility complex loci. Immunol Rev 167:319–325

    Article  PubMed  CAS  Google Scholar 

  • Parker TH, Barr IR, Griffith SC (2006) The blue tit’s song is an inconsistent signal of male condition. Behav Ecol 17:1029–1040

    Article  Google Scholar 

  • Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21

    PubMed  CAS  Google Scholar 

  • Poesel A, Foerster K, Kempenaers B (2001) The dawn song of the blue tit Parus caeruleus and its role in sexual selection. Ethology 107:521–531

    Article  Google Scholar 

  • Pond SLK, Frost SDW (2005a) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531–2533

    Article  PubMed  CAS  Google Scholar 

  • Pond SLK, Frost SDW (2005b) Not so different after all: a comparison of methods for detecting amino acid sites under selection. SMBE 22:1208–1222

    CAS  Google Scholar 

  • Pond SLK, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21(5):676–679

    Article  PubMed  CAS  Google Scholar 

  • Posada (2009) Selection of models of DNA evolution with jModelTest. Methods Mol Biol 537:93–112

    Article  PubMed  CAS  Google Scholar 

  • Potts WK, Wakeland EK (1990) Evolution of diversity at the major histocompatibility complex. Trends Ecol Evol 5:181–187

    Article  PubMed  CAS  Google Scholar 

  • Potts WK, Wakeland EK (1993) Evolution of Mhc genetic diversity—a tale of incest, pestilence and sexual preference. Trends Genet 9:408–412

    Article  PubMed  CAS  Google Scholar 

  • 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 61:451–461

    Article  PubMed  CAS  Google Scholar 

  • Reusch TBH, Haberli MA, Aeschlimann PB, Milinski M (2001) Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414:300–302

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 272:759–767

    Article  PubMed  Google Scholar 

  • Rozas J (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Oxford University Press, Oxford, pp 174–175

    Google Scholar 

  • 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 53:792–801

    Article  PubMed  CAS  Google Scholar 

  • 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):1943–1956

    Article  PubMed  CAS  Google Scholar 

  • Sawyer SA (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538

    PubMed  CAS  Google Scholar 

  • 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 63:531–542

    Article  PubMed  Google Scholar 

  • Seutin G, White BN, Boag P (1991) Preservation of avian blood and tissue for DNA analyses. Can J Zool 69:82–90

    Article  CAS  Google Scholar 

  • Sheldon FH, Gill FB (1996) A reconsideration of songbird phylogeny, with emphasis on the evolution of titmice and their sylvioid relatives. Syst Boil 45:473–495

    Article  Google Scholar 

  • 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 172:6751–6763

    PubMed  CAS  Google Scholar 

  • 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 27:70–82

    Article  Google Scholar 

  • Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2:16–34

    Article  PubMed  CAS  Google Scholar 

  • 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 271:2387–2394

    Article  Google Scholar 

  • 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 59:725–734

    Article  PubMed  CAS  Google Scholar 

  • 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 63:653–666

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. SMBE 24:1596–1599

    CAS  Google Scholar 

  • 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 123:1013–1021

    Google Scholar 

  • 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 73:805–814

    Article  Google Scholar 

  • 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 103:1434–1439

    Google Scholar 

  • Wegner K, Kalbe M, Schaschl H, Reusch T (2004) Parasites and individual major histocompatibility complex diversity-an optimal choice? Microbes Infect 6:1110–1116

    Article  PubMed  CAS  Google Scholar 

  • Westerdahl H (2004) No evidence of an MHC-based female mating preference in great reed warblers. Mol Ecol 13:2465–2470

    Article  PubMed  CAS  Google Scholar 

  • Westerdahl H (2007) Passerine MHC: genetic variation and disease resistance in the wild. J Ornithol 148:469–477

    Article  Google Scholar 

  • 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 49:158–170

    Article  PubMed  CAS  Google Scholar 

  • 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 92:534–542

    Article  PubMed  CAS  Google Scholar 

  • 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 272:1511–1518

    Article  PubMed  CAS  Google Scholar 

  • Wittzell H, Madsen T, Westerdahl H, Shine R, von Schantz T (1998) MHC variation in birds and reptiles. Genetica 104:301–309

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13(5):555–556

    PubMed  CAS  Google Scholar 

  • Yang Z (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  PubMed  CAS  Google Scholar 

  • Yang Z, Wong WSW, Nielsen R (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22(4):1107–1118

    Article  PubMed  CAS  Google Scholar 

  • Ziegler A, Kentenich H, Uchanska-Ziegier B (2005) Female choice and the MHC. Trends Immunol 26:496–502

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank K. Persson, K. Teltscher, U. Holter and S. Kuhn for their excellent laboratory work and to all the field assistants who were involved in the Kolbeterberg project. We are grateful to H. Westerdahl for her help in designing the optimal primers and her support throughout the study. Furthermore we are indebted to C. Oppelt, for his inspiring comments on the manuscript. The present study was funded by the German Research foundation (DFG KE 867/1) and the Max Planck Society.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology, 82305, Seewiesen, Germany

    R. Wutzler & B. Kempenaers

  2. Comparative Zoology, Institute of Evolution and Ecology, University of Tübingen, D-72076, Tübingen, Germany

    K. Foerster

Authors
  1. R. Wutzler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. Foerster
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. B. Kempenaers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. Wutzler.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 211 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wutzler, R., Foerster, K. & Kempenaers, B. MHC class I variation in a natural blue tit population (Cyanistes caeruleus). Genetica 140, 349–364 (2012). https://doi.org/10.1007/s10709-012-9679-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-012-9679-0

Keywords

Search

Navigation