Characterization of MHC class I and II genes in a subantarctic seabird, the blue petrel, Halobaena caerulea (Procellariiformes)

Immunogenetics

Volumn 63, Issue 10, 2011, Pages 653-666

  Strandh, Maria ^a,b   Lannefors, Mimi ^b   Bonadonna, Francesco ^a   Westerdahl, Helena ^b  

^a CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^b LUND UNIVERSITY   (Sweden)

Author keywords

Aves; Class I; Class II B; Diversity; Major histocompatibility complex; Selection

Indexed keywords

DNA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NUCLEOTIDE;

ACROCEPHALUS ARUNDINACEUS; ALLELE; ANAS PLATYRHYNCOS; ANSER ANSER; ARTICLE; BIRD; CONTROLLED STUDY; DNA SEQUENCE; GALLIFORMES; GALLUS GALLUS; GENE LOCUS; GENETIC VARIABILITY; HALOBAENA CAERULEA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; SEABIRD; AMINO ACID SEQUENCE; ANIMAL; GENE; GENETICS; IMMUNOLOGY; MOLECULAR GENETICS; PHYLOGENY;

AVES; GALLIFORMES; HALOBAENA CAERULEA; PACHYPTILA BELCHERI; PASSERIFORMES; PROCELLARIIDAE; PROCELLARIIFORMES;

AMINO ACID SEQUENCE; ANIMALS; BIRDS; GENES, MHC CLASS I; GENES, MHC CLASS II; GENETIC LOCI; GENETIC VARIATION; MOLECULAR SEQUENCE DATA; PHYLOGENY;

EID: 80155164025     PISSN: 00937711     EISSN: 14321211     Source Type: Journal    
DOI: 10.1007/s00251-011-0534-8     Document Type: Article

References (79)

1. Aeschlimann PB, Haeberli MA, Reusch TBH, Boehm T, Milinski M (2003) Female sticklebacks Gasterosteus aculeatus use self-reference to optimize MHC allele number during mate selection. Behav Ecol Sociobiol 54:119-126 (Pubitemid 36844447)
2. Anisimova M, Nielsen R, Yang Z (2003) Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164:1229-1236 (Pubitemid 36935693)
3. Balakrishnan CN, Ekblom R, Voelker M, Westerdahl H, Godinez R, Kotkiewicz H, Burt DW, Graves T, Griffin DK, Warren WC, Edwards SV (2010) Gene duplication and fragmentation in the zebra finch major histocompatibility complex. BMC Biology 8: Article No.: 29
4. Bang BG, Cobb S (1968) The size of the olfactory bulb in 108 species of birds. Auk 85:55-61
5. Barbosa A, Palacios MJ (2009) Health of Antarctic birds: a review of their parasites, pathogens and diseases. Polar Biol 32:1095-1115
6. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL (2008) GenBank. Nucleic Acids Res 36:D25-D30 (Pubitemid 351149691)
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 (Pubitemid 36567968)
8. Bollmer JL, Dunn PO, Whittingham LA, Wimpee C (2010) Extensive MHC class II B gene duplication in a passerine, the common yellowthroat (Geothlypis trichas). J Hered 101:448-460
9. Bonadonna F, Mardon J (2010) One house two families: petrel squatters get a sniff of low-cost breeding opportunities. Ethology 116:176-182
10. Bonadonna F, Nevitt GA (2004) Partner-specific odor recognition in an Antarctic seabird. Science (Washington D C) 306:835 (Pubitemid 39446986)
11. Bonadonna F, Villafane M, Bajzak C, Jouventin P (2004) Recognition of burrow's olfactory signature in blue petrels, Halobaena caerulea: an efficient discrimination mechanism in the dark. Anim Behav 67:893-898 (Pubitemid 38617315)
12. Bonadonna F, Caro S, Jouventin P, Nevitt GA (2006) Evidence that blue petrel, Halobaena caerulea, fledglings can detect and orient to dimethyl sulfide. J Exp Biol 209:2165-2169 (Pubitemid 43987892)
13. Bonneaud C, Sorci G, Morin V, Westerdahl H, Zoorob R, Wittzell H (2004) Diversity of Mhc class I and IIB genes in house sparrows (Passer domesticus). Immunogenetics 55:855-865 (Pubitemid 38650991)
14. Bonneaud C, Chastel O, Federici P, Westerdahl H, Sorci G (2006) Complex MHC-based mate choice in a wild passerine. Proc R Soc Biol Sci B 273:1111-1116 (Pubitemid 47324480)
15. Bos DH, Waldman B (2006) Polymorphism, natural selection, and structural modeling of class Ia MHC in the African clawed frog (Xenopus laevis). Immunogenetics 58:433-442 (Pubitemid 43830107)
16. Brooke M (2004) Albatrosses and petrels across the world. Oxford University Press Inc., New York
17. Brown JL (1997) A theory of mate choice based on heterozygosity. Behav Ecol 8:60-65
18. Brown RE, Singh PB, Roser B (1987) The major histocompatibility complex and the chemosensory recognition of individuality in rats. Physiol Behav 40:65-74
19. Brown RE, Roser B, Singh PB (1989) Class I and class II regions of the major histocompatibility complex both contribute to individual odors in congenic inbred strains of rats. Behav Genet 19:659-674
20. Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature (London) 364:33-39 (Pubitemid 23233452)
21. Chaix R, Cao C, Donnelly P (2010) Is mate choice in humans MHC-dependent? PLoS Genetics 6:Article No.: e1000184
22. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497-3500 (Pubitemid 37442184)
23. Cherel Y, Bocher P, Trouve C, Weimerskirch H (2002) Diet and feeding ecology of blue petrels Halobaena caerulea at Iles Kerguelen, Southern Indian Ocean. Mar Ecol Prog Ser 228:283-299 (Pubitemid 34264639)
24. Doherty PC, Zinkernagel RM (1975) A biological role for the major histo compatibility antigens. Lancet 1:1406-1409
25. Ekblom R, Saether SA, Grahn M, Fiske P, Kalas JA, Hoglund J (2004) Major histocompatibility complex variation and mate choice in a lekking bird, the great snipe (Gallinago media). Mol Ecol 13:3821-3828 (Pubitemid 39569057)
26. Felsenstein J (1985) Confidence limits on phylogenies and approach using the bootstrap. Evolution 39:783-791
27. Freeman-Gallant CR, Meguerdichian M, Wheelwright NT, Sollecito SV (2003) Social pairing and female mating fidelity predicted by restriction fragment length polymorphism similarity at the major histocompatibility complex in a songbird. Mol Ecol 12:3077-3083 (Pubitemid 37425077)
28. Gillingham MAF, Richardson DS, Lovlie H, Moynihan A, Worley K, Pizzari T (2009) Cryptic preference for MHC-dissimilar females in male red junglefowl, Gallus gallus. Proc R Soc Biol Sci B 276:1083-1092
29. Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han K-L, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T (2008) A phylogenomic study of birds reveals their evolutionary history. Science (Washington D C) 320:1763-1768 (Pubitemid 351931288)
30. Havlicek J, Roberts SC (2009) MHC-correlated mate choice in humans: a review. Psychoneuroendocrinology 34:497-512
31. Hess CM, Edwards SV (2002) The evolution of the major histocom-patibility complex in birds. Bioscience 52:423-431 (Pubitemid 34458435)
32. Janeway CAJ, Travers P, Walport M, Shlomchik MJ (2001) Immunobiology, the immune system in health and disease. Garland Science, New York
33. Jeffery KJM, Bangham CRM (2000) Do infectious diseases drive MHC diversity? Microbes Infect 2:1335-1341
34. Jordan WC, Bruford MW (1998) New perspectives on mate choice and the MHC. Heredity 81:127-133 (Pubitemid 28403808)
35. Kaufman J, Voelk H, Wallny H-J (1995) A "minimal essential MHC" and an "unrecognized MHC": two extremes in selection for polymorphism. Immunol Rev 143:63-88
36. Kaufman J, Milne S, Goebel TWF, Walker BA, Jacob JP, Auffray C, Zoorob R, Beck S (1999) The chicken B locus is a minimal essential major histocompatibility complex. Nature (London) 401:923-925
37. Kikkawa EF, Tsuda TT, Sumiyama D, Naruse TK, Fukuda M, Kurita M, Wilson RP, LeMaho Y, Miller GD, Tsuda M, Murata K, Kulski JK, Inoko H (2009) Trans-species polymorphism of the Mhc class II DRB-like gene in banded penguins (genus Spheniscus). Immunogenetics 61:341-352
38. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111-120 (Pubitemid 11166431)
39. Klein J, Bontrop RE, Dawkins RL, Erlich HA, Gyllensten UB, Heise ER, Jones PP, Parham P, Wakeland EK, Watkins DI (1990) Nomenclature for the major histocompatibility complexes of different species: a proposal. Immunogenetics 31:217-219 (Pubitemid 20132749)
40. Mardon J, Bonadonna F (2009) Atypical homing or self-odour avoidance? Blue petrels (Halobaena caerulea) are attracted to their mate's odour but avoid their own. Behav Ecol Sociobiol 63:537-542
41. Mardon J, Saunders SM, Anderson MJ, Couchoux C, Bonadonna F (2010) Species, gender, and identity: cracking petrels' socio-chemical code. Chem Senses 35:309-321
42. Mays HL Jr, Hill GE (2004) Choosing mates: good genes versus genes that are a good fit. Trends Ecol Evol 19:554-559 (Pubitemid 39234762)
43. 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
44. Møller AP (1998) Evidence of larger impact of parasites on hosts in the tropics: investment in immune function within and outside the tropics. Oikos 82:265-270 (Pubitemid 28336109)
45. Møller AP, Erritzøe J (1996) Parasite virulence and host immune defense: host immune response is related to nest reuse in birds. Evolution 50:2066-2072 (Pubitemid 26394296)
46. Møller AP, Erritzøe J, Saino N (2003) Seasonal changes in immune response and parasite impact on hosts. Am Nat 161:657-671 (Pubitemid 36499903)
47. Moon DA, Veniamin SM, Parks-Dely JA, Magor KE (2005) The MHC of the duck (Anas platyrhynchos) contains five differentially expressed class I genes. J Immunol 175:6702-6712 (Pubitemid 41598914)
48. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and non synonymous nucleotide substitutions. Mol Biol Evol 3:418-426 (Pubitemid 16010523)
49. Nunn GB, Stanley SE (1998) Body size effects and rates of cytochrome b evolution in tube-nosed seabirds. Mol Biol Evol 15:1360-1371 (Pubitemid 28452419)
50. Olsén KH, Grahn M, Lohm J, Langefors A (1998) MHC and kin discrimination in juvenile Arctic charr, Salvelinus alpinus (L.). Anim Behav 56:319-327 (Pubitemid 28398019)
51. Penhallurick J, Wink M (2004) Analysis of the taxonomy and nomenclature of the Procellariiformes based on complete nucleotide sequences of the mitochondrial cytochrome b gene. Emu 104:125-147 (Pubitemid 38946266)
52. Penn DJ (2002) The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108:1-21 (Pubitemid 34134669)
53. Penn D, Potts W (1998) How do major histocompatibility genes influence odor and mating preferences? Adv Immunol 69:411-435
54. Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibility complex genes. Am Nat 153:145-164 (Pubitemid 29139433)
55. Piersma T (1997) Do global patterns of habitat use and migration strategies co-evolve with relative investments in immunocompe-tence due to spatial variation in parasite pressure? Oikos 80:623-631
56. 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 (Pubitemid 37496712)
57. 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 Biol Sci B 272:759-767 (Pubitemid 41411134)
58. Saitou N, Nei M (1987) The neighbor-joining method a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425
59. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor
60. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci U S A 74:5463-5467
61. 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 (Pubitemid 38669112)
62. Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds: a study in molecular evolution. Yale University Press, New Haven
63. Silva MC, Edwards SV (2009) Structure and evolution of a new avian MHC class II B gene in a sub-Antarctic seabird, the thin-billed prion (Procellariiformes: Pachyptila belcheri). J Mol Evol 68:279-291
64. Sitte K, Brinkworth R, East IJ, Jazwinska EC (2002) A single amino acid deletion in the antigen binding site of BoLA-DRB3 is predicted to affect peptide binding. Vet Immunol Immunopathol 85:129-135 (Pubitemid 34275427)
65. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596-1599 (Pubitemid 47236692)
66. Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013-1027 (Pubitemid 30613148)
67. Wallny H-J, Avila D, Hunt LG, Powell TJ, Riegert P, Salomonsen J, Skjodt K, Vainio O, Vilbois F, Wiles MV, Kaufman J (2006) Peptide motifs of the single dominantly expressed class I molecule explain the striking MHC-determined response to Rous sarcoma virus in chickens. Proc Natl Acad Sci U S A 103:1434-1439 (Pubitemid 43191183)
68. Warham J (1996) The behaviour, population biology and physiology of the petrels. Academic Press, London
69. Weimerskirch H, Zotier R, Jouventin P (1989) The avifauna of the Kerguelen islands Indian ocean. Emu 89:15-29 (Pubitemid 20418810)
70. Westerdahl H (2004) No evidence of an MHC-based female mating preference in great reed warblers. Mol Ecol 13:2465-2470 (Pubitemid 38946434)
71. 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 (Pubitemid 29054575)
72. Westerdahl H, Wittzell H, von Schantz T (2000) Mhc diversity in two passerine birds: no evidence for a minimal essential MHC. Immunogenetics 52:92-100 (Pubitemid 32803115)
73. 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 (Pubitemid 38847723)
74. Yamazaki K, Boyse EA, Mike V, Thaler HT, Mathieson BJ, Abbott J, Boyse J, Zayas ZA, Thomas L (1976) Control of mating preferences in mice by genes in the major histo compatibility complex. J Exp Med 144:1324-1335
75. Yamazaki K, Yamaguchi M, Baranoski L, Bard J, Boyse EA, Thomas L (1979) Recognition among mice: evidence from the use of a Y-maze differentially scented by congenic mice of different major histocompatiblity types. J Exp Med 150:755-760 (Pubitemid 10227327)
76. Yang Z (2006) Computational molecular evolution. Oxford University Press, New York
77. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586-1591 (Pubitemid 47236688)
78. Yang Z, Wong WSW, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107-1118 (Pubitemid 40471423)
79. Zelano B, Edwards SV (2002) An MHC component to kin recognition and mate choice in birds: predictions, progress, and prospects. Am Nat 160:S225-S237 (Pubitemid 36035849)