Characterization of MHC-I in the blue tit (Cyanistes caeruleus) reveals low levels of genetic diversity and trans-population evolution across European populations

Immunogenetics

Volumn 63, Issue 8, 2011, Pages 531-542

  Schut, Elske ^a   Aguilar, Juan Rivero De ^b   Merino, Santiago ^b   Magrath, Michael J L ^c   Komdeur, Jan ^a   Westerdahl, Helena ^d  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^c Department of Wildlife Conservation and Science ^*  (Australia)

^d LUND UNIVERSITY   (Sweden)

Author keywords

Antigen recognition site; Blue tit (Cyanistes caeruleus; Parus caeruleus); Cloning and sequencing; MHC class I; Specific immune system

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NUCLEOTIDE;

ALLELE; ARTICLE; BIRD; CYANISTES CAERULEUS; EXON; FEMALE; GENE CLUSTER; GENE LOCUS; GENE SEQUENCE; GENETIC VARIABILITY; MALE; MOLECULAR EVOLUTION; NETHERLANDS; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN BINDING; SPAIN; SWEDEN;

AMINO ACID SEQUENCE; ANIMALS; EUROPE; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENETICS, POPULATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; MOLECULAR SEQUENCE DATA; PASSERIFORMES; PHYLOGENY; SEQUENCE ALIGNMENT;

ACROCEPHALUS SECHELLENSIS; CYANISTES CAERULEUS; PARUS CAERULEUS; PARUS MAJOR; PASSERIFORMES; VERTEBRATA;

EID: 79961032489     PISSN: 00937711     EISSN: 14321211     Source Type: Journal    
DOI: 10.1007/s00251-011-0532-x     Document Type: Article

References (75)

1. A Aguilar SV Edwards TB Smith RK Wayne 2006 Patterns of variation in MHC class II β loci of the little greenbul (Andropadus virens) with comments on MHC evolution in birds J Hered 97 133 142 16489149 10.1093/jhered/esj013 1:CAS:528:DC%2BD28XitVOqsLc%3D
2. E Arriero J Moreno S Merino J Martínez 2008 Habitat effects on physiological stress response in nestling blue tits are mediated through parasitism Physiol Biochem Zool 81 195 203 18197757 10.1086/524393 (Pubitemid 351269232)
3. C Balakrishnan R Ekblom M Volker H Westerdahl R Godinez H Kotkiewicz D Burt T Graves D Griffin W Warren S Edwards 2010 Gene duplication and fragmentation in the zebra finch major histocompatibility complex BMC Biol 8 29 20359332 10.1186/1741-7007-8-29
4. S Beck D Geraghty H Inoko L Rowen 1999 Complete sequence and gene map of a human major histocompatibility complex Nature 401 921 923 10.1038/44853 (Pubitemid 29518961)
5. S Bensch A Akesson 2003 Temporal and spatial variation of hematozoans in Scandinavian willow warblers J Parasitol 89 388 391 12760661 10.1645/0022-3395(2003)089[0388:TASVOH]2.0.CO;2 (Pubitemid 36523235)
6. WF Bodmer 1972 Evolutionary significance of the HL-A system Nature 237 139 146 4113158 10.1038/237139a0 1:STN:280:DyaE383gtVGqsQ%3D%3D
7. C Bonneaud G Sorci V Morin H Westerdahl R Zoorob H Wittzell 2004 Diversity of Mhc class I and IIB genes in house sparrows (Passer domesticus) Immunogenetics 55 855 865 14963619 10.1007/s00251-004-0648-3 1:CAS:528:DC%2BD2cXisV2isLk%3D (Pubitemid 38650991)
8. JAM Borghans JB Beltman RJ de Boer 2004 MHC polymorphism under host-pathogen coevolution Immunogenetics 55 732 739 14722687 10.1007/s00251-003-0630-5 1:CAS:528:DC%2BD2cXhsFeqt74%3D (Pubitemid 38316678)
9. Brommer JE, Korsten P, Bouwman KA, Berg ML, Komdeur J (2007) Is extrapair mating random? On the probability distribution of extrapair young in avian broods. Behavioral Ecology 18:895-904 (Pubitemid 47357646)
10. M Cichon A Dubiec 2005 Cell-mediated immunity predicts the probability of local recruitment in nestling blue tits J Evol Biol 18 962 966 16033568 10.1111/j.1420-9101.2005.00910.x 1:STN:280:DC%2BD2Mzns1Omuw%3D%3D (Pubitemid 40968548)
11. Cramp S, Perrins CM (1993) Birds of the Western Palearctic. Oxford University Press, Oxford
12. del Hoyo J, Elliot A, Bowles W (2007) Handbook of the birds of the world. [12]. Lynx Edicions, Barcelona
13. K Delhey A Johnsen A Peters A Andersson B Kempenaers 2003 Paternity analysis reveals opposing selection pressures on crown coloration in the blue tit (Parus caeruleus) Proc R Soc Lond B 270 2057 2063 10.1098/rspb.2003.2460 (Pubitemid 37211145)
14. SV Edwards PW Hedrick 1998 Evolution and ecology of MHC molecules: from genomics to sexual selection Trends Ecol Evol 13 305 311 21238318 10.1016/S0169-5347(98)01416-5 1:STN:280:DC%2BC3M7itF2nsA%3D%3D (Pubitemid 28368430)
15. SV Edwards J Gasper D Garrigan D Martindale BF Koop 2000 A 39-kb sequence around a blackbird Mhc class II gene: ghost of selection past and songbird genome architecture Mol Biol Evol 17 1384 1395 10958854 1:CAS:528: DC%2BD3cXmtFyrt74%3D
16. R Ekblom SA Sæther P Jacobsson P Fiske T Sahlman M Grahn JA Kålås J Höglund 2007 Spatial pattern of MHC class II variation in the great snipe (Gallinago media) Mol Ecol 16 7 1439 1451 17391268 10.1111/j.1365-294X.2007.03281.x (Pubitemid 46474783)
17. L Excoffier G Laval S Schneider 2005 Arlequin (version 3.0): an integrated software package for population genetics data analysis Evol Bioinform 1 47 50 1:CAS:528:DC%2BD28XjsFSltg%3D%3D
18. Foerster K, Westerdahl H, von Schantz T, Kempenaers B (2006) Typing MHC class I genes in blue tits (Parus caeruleus), using motif-specific PCR and denaturant gradient gel electrophoresis
19. CR Freeman-Gallant EM Johnson F Saponara M Stanger 2002 Variation at the major histocompatibility complex in Savannah sparrows Mol Ecol 11 1125 1130 12030987 10.1046/j.1365-294X.2002.01508.x 1:CAS:528:DC%2BD38Xls1ars78%3D (Pubitemid 34635180)
20. Goldsby RA, Kindt TJ, Osborne BA (2000) Immunology. Freeman, New York
21. TA Hall 2009 BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT Nucleic Acids Symp Ser 41 95 98
22. PW Hedrick 2002 Pathogen resistance and genetic variation at MHC loci Evolution 56 1902 1908 12449477 (Pubitemid 35302002)
23. CM Hess SV Edwards 2002 The evolution of the major histocompatibility complex in birds Bioscience 52 423 431 10.1641/0006-3568(2002)052[0423:TEOTMH]2. 0.CO;2 (Pubitemid 34458435)
24. JP Huelsenbeck F Ronquist 2001 MRBAYES: Bayesian inference of phylogenetic trees Bioinformatics 17 754 755 11524383 10.1093/bioinformatics/17. 8.754 1:STN:280:DC%2BD3MvotV2isw%3D%3D (Pubitemid 32851390)
25. AL Hughes M Nei 1988 Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection Nature 335 167 170 3412472 10.1038/335167a0 1:CAS:528:DyaL1cXlvVCktrY%3D
26. AL Hughes M Nei 1989 Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection Proc Natl Acad Sci USA 86 958 962 2492668 10.1073/pnas.86.3.958 1:CAS:528:DyaL1MXhsV2jsbs%3D (Pubitemid 19056271)
27. HD Hunt RM Goto DN Foster LD Bacon MM Miller 2006 At least one YMHCI molecule in the chicken is alloimmunogenic and dynamically expressed on spleen cells during development Immunogenetics 58 297 307 16607558 10.1007/s00251-005- 0074-1 1:CAS:528:DC%2BD28XjvFSns7Y%3D (Pubitemid 43673473)
28. Janeway CA, Murphy K, Travers P, Ehrenstein M (2008) Janeway's immunobiology. Garland, New York
29. SI Jarvi CL Tarr CE McIntosh CT Atkinson RC Fleischer 2004 Natural selection of the major histocompatibility complex (Mhc) in Hawaiian honeycreepers (Drepanidinae) Mol Ecol 13 2157 2168 15245391 10.1111/j.1365-294X. 2004.02228.x 1:CAS:528:DC%2BD2cXmsl2rtbo%3D (Pubitemid 38946407)
30. J Kaufman J Salomonsen M Flajnik 1994 Evolutionary conservation of MHC class I and class II molecules-different yet the same Semin Immunol 6 411 424 7654997 10.1006/smim.1994.1050 1:CAS:528:DyaK2MXltlagtbg%3D (Pubitemid 124001537)
31. J Kaufman H Völk HJ Wallny 1995 A "minimal essential Mhc"and an "unrecognized Mhc": two extremes in selection for polymorphism Immunol Rev 143 63 88 7558083 10.1111/j.1600-065X.1995.tb00670.x 1:CAS:528:DyaK2MXlsVCntLY%3D
32. J Kaufman S Milne TWF Göbel BA Walker JP Jacob C Auffray R Zoorob S Beck 1999 The chicken B locus is a minimal essential major histocompatibility complex Nature 401 923 925 10553909 10.1038/44856 1:CAS:528:DyaK1MXntFyksrg%3D (Pubitemid 29518962)
33. B Kempenaers GR Verheyen AA Dhondt 1997 Extra-pair paternity in the blue tit (Parus caeruleus): female choice, male characteristics, and offspring quality Behav Ecol 8 481 492 10.1093/beheco/8.5.481 (Pubitemid 28060766)
34. Klein J (1986) Natural history of the major histocompatibility complex. Wiley, New York
35. SCL Knowles V Palinauskas BC Sheldon 2010 Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population J Evol Biol 23 557 569 20070458 10.1111/j.1420-9101. 2009.01920.x 1:STN:280:DC%2BC3czkvFWmuw%3D%3D
36. J Komdeur MD Pels 2005 Rescue of the Seychelles warbler on Cousin Island, Seychelles: the role of habitat restoration Biol Conserv 124 15 26 10.1016/j.biocon.2004.12.009 (Pubitemid 40406065)
37. L Kvist M Ruokonen J Lumme M Orell 1999 Different population structures in northern and southern populations of the European blue tit (Parus caeruleus) J Evol Biol 12 798 805 10.1046/j.1420-9101.1999.00098.x (Pubitemid 29311754)
38. L Kvist M Ruokonen J Lumme M Orell 1999 The colonization history and present-day population structure of the European great tit (Parus major major) Heredity 82 495 502 10383669 10.1038/sj.hdy.6885130 (Pubitemid 29285218)
39. L Kvist K Viiri PC Dias S Rytkönen M Orell 2004 Glacial history and colonization of Europe by the blue tit Parus caeruleus J Evol Biol 35 352 359 (Pubitemid 39027099)
40. DI Leech IR Hartley IRK Stewart SC Griffith T Burke 2001 No effect of parental quality or quality of extrapair paternity on brood sex ration in the blue tit (Parus caeruleus) Behav Ecol 12 674 680 10.1093/beheco/12.6.674 (Pubitemid 34029708)
41. EJ Livant JR Brigati SJ Ewald 2004 Diversity and locus specificity of chicken MHC B class I sequences Anim Genet 35 18 27 14731225 10.1111/j.1365-2052.2003.01078.x 1:CAS:528:DC%2BD2cXitVKlsLc%3D (Pubitemid 38192987)
42. MJL Magrath O Vedder V Mvd J Komdeur 2009 Maternal effects contribute to the superior performance of extra-pair offspring Curr Biol 19 792 797 19409787 10.1016/j.cub.2009.03.068 1:CAS:528:DC%2BD1MXlslWmt7s%3D
43. Merino S, Møller AP (2010) Host-parasite interactions and climate change. In: Møller AP, Fiedler W, Berthold P (eds) Effects of climate change on birds. Oxford University Press, New York, pp 213-226
44. S Merino J Moreno JJ Sanz E Arriero 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 10.1098/rspb.2000.1312 1:STN:280: DC%2BD3MzjslSqtg%3D%3D (Pubitemid 32099440)
45. CM Mesa KJ Thulien DA Moon SM Veniamin KE Magor 2004 The dominant MHC class I gene is adjacent to the polymorphic TAP2 gene in the duck, Anas platyrhynchos Immunogenetics 56 194 203 10.1007/s00251-004-0672-3
46. HC Miller DM Lambert 2003 An evaluation of methods of blood preservation for TR-PCR from endangered species Convervation Genet 4 651 654 10.1023/A:1025675901387 1:CAS:528:DC%2BD3sXntFGhs7g%3D (Pubitemid 37216062)
47. HC Miller DM Lambert 2004 Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae) Mol Ecol 13 3709 3721 15548285 10.1111/j.1365-294X. 2004.02368.x 1:CAS:528:DC%2BD2MXhtVGntA%3D%3D (Pubitemid 39569048)
48. MM Miller R Goto A Bernot R Zoorob C Auffray N Bumstead WE Briles 1994 Two Mhc class I and two Mhc class II genes map to the chicken Rfp-Y system outside the B complex Proc Natl Acad Sci USA 91 4397 4401 7910407 10.1073/pnas.91.10.4397 1:CAS:528:DyaK2cXkt1ygsL4%3D
49. AP Møller J Erritzøe 1998 Host immune defence and migration in birds Evol Ecol 12 945 953 10.1023/A:1006516222343 (Pubitemid 29006851)
50. Nei M, Hughes AL (1991) Polymorphism and evolution of the major histocompatibility complex loci in mammals. In: Clark AG, Whittams TS, Selander RK (eds) Evolution at the molecular level. Sinauer Associates, Sunderland, pp 222-247
51. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University
52. VC Oosterhout 2008 A new theory of MHC evolution: beyond selection on the immune genes Proc R Soc Lond B 276 657 665 10.1098/rspb.2008.1299
53. Page RDM, Holmes EC (1998) Molecular evolution: a phylogentic approach. Blackwell Science, Oxford, UK
54. MA Peirce 1981 Distribution and host-parasite check-list of the haematozoa of birds in Western Europe J Nat Hist 15 419 458 10.1080/ 00222938100770321
55. WK Potts EK Wakeland 1990 Evolution of diversity at the major histocompatibility complex Trends Ecol Evol 5 181 187 21232350 10.1016/0169-5347(90)90207-T 1:STN:280:DC%2BC3M7hsVagtw%3D%3D (Pubitemid 120036285)
56. M Promerová T Albrecht J Bryja 2009 Extremely high MHC class I variation in a population of a long-distant migrant, the Scarlet Rosefinch (Carpodacus erythrinus) Immunogenetics 61 451 461 19452149 10.1007/s00251-009- 0375-x
57. DS Richardson H Westerdahl 2003 MHC diversity in two Acrocephalus species: the outbred Great reed warbler and the inbred Seychelles warbler Mol Ecol 12 3523 3529 14629367 10.1046/j.1365-294X.2003.02005.x 1:CAS:528: DC%2BD2cXks12juw%3D%3D (Pubitemid 37496712)
58. DS Richardson FJ Jury K Blaakmeer J Komdeur T Burke 2001 Parentage assignment and extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus seychellensis) Mol Ecol 10 2263 2273 11555268 10.1046/j.0962-1083.2001.01355.x 1:STN:280:DC%2BD3MrgslWitQ%3D%3D (Pubitemid 32901394)
59. DS Richardson J Komdeur T Burke T von Schantz 2005 MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler Proc R Soc Lond B 272 759 767 10.1098/rspb.2004.3028 (Pubitemid 41411134)
60. F Ronquist JP Huelsenbeck 2003 MrBayes 3: Bayesian phylogenetic inference under mixed models Bioinformatics 19 1572 1574 12912839 10.1093/bioinformatics/ btg180 1:CAS:528:DC%2BD3sXntlKms7k%3D (Pubitemid 37038874)
61. Sambrook J, Russell DW, Irwin N (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York
62. T Shiina A Ando T Imanishi H Kawata K Hanzawa T Gojobori H Inoko S Watanabe 1995 Isolation and characterization of cDNA clones for Japanese quail (Coturnix japonica) major histocompatibilty complex (MhcCoja) class I molecules Immunogenetics 42 213 216 7642233 10.1007/BF00191227 1:CAS:528: DyaK2MXnvFSgu7g%3D
63. BP Shum R Rajalingam KE Magor K Azumi WH Carr B Dixon RJM Stet MA Adkison RP Hedrick P Parham 1999 A divergent non-classical class I gene conserved in salmonids Immunogenetics 49 479 490 10380691 10.1007/s002510050524 1:CAS:528:DyaK1MXis1alsLw%3D (Pubitemid 29221779)
64. HG Smith JÅ Nilsson 1987 Intraspecific variation in migratory pattern of a partial migrant, the blue tit (Parus caeruleus): an evaluation of different hypotheses Auk 104 109 115
65. T Strand H Westerdahl J Höglund RV Alatalo H Siitari 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 17653538 10.1007/s00251-007-0234-6 1:CAS:528:DC%2BD2sXhtVCnsrjN (Pubitemid 47415562)
66. K Tamura J Dudley M Nei S Kumar 2007 MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0 Mol Biol Evol 24 1596 1599 17488738 10.1093/molbev/msm092 1:CAS:528:DC%2BD2sXpsVGrsL8%3D (Pubitemid 47236692)
67. G Tomás S Merino J Moreno J Morales 2007 Consequences of nest reuse for parasite burden and female health and condition in blue tits, Cyanistes caeruleus Anim Behav 73 805 814 10.1016/j.anbehav.2006.06.016 (Pubitemid 46693635)
68. Valkiunas G (2005) Avian malaria parasites and other haemosporidia. CRC, Boca Raton
69. GR Verheyen B Kempenaers F Adriaensen M van den Broeck E Matthysen C van Broeckhoven AA Dhondt 1995 The genetic structure of Parus caeruleus (blue tit) populations as revealed by minisatellite single locus probes Heredity 75 571 577 10.1038/hdy.1995.176 (Pubitemid 3009431)
70. V Vincek D Klein RT Graser F Figueroa C O'hUigin J Klein 1995 Molecular cloning of major histocompatibilty complex class II B gene cDNA from the Bengalese finch Lonchura striata Immunogenetics 42 262 267 7672820 10.1007/BF00176443 1:CAS:528:DyaK2MXos1CmtbY%3D
71. H Westerdahl 2007 Passerine MHC: genetic variation and disease resistance in the wild J Ornithol 148 s469 s477 10.1007/s10336-007-0230-5 (Pubitemid 350238500)
72. H Westerdahl H Wittzell S Tv 1999 Polymorphism and transcription of Mhc class I genes in a passerine bird, the great reed warbler Immunogenetics 49 158 170 9914330 10.1007/s002510050477 1:CAS:528:DyaK1MXjvFahtw%3D%3D (Pubitemid 29054575)
73. H Westerdahl H Wittzell T von Schantz 2000 Mhc diversity in two passerine birds: no evidence for a minimal essential Mhc Immunogenetics 52 92 100 11132162 10.1007/s002510000256 1:CAS:528:DC%2BD3cXot1yltLk%3D (Pubitemid 32803115)
74. H Wittzell T von Schantz R Zoorob C Auffray 1995 Rfp-Y-like sequences assort independently of pheasant Mhc genes Immunogenetics 42 68 71 7797271 10.1007/BF00164990 1:CAS:528:DyaK2MXnt1Chs78%3D
75. JA Zeh DW Zeh 1997 The evolution of polyandry II: post-copulatory defences against genetic incompatibility Proc R Soc Lond B 264 69 75 10.1098/rspb.1997.0010 (Pubitemid 27067932)