Independent evolution of functional MHC class II DRB genes in New World bat species

Immunogenetics

Volumn 64, Issue 7, 2012, Pages 535-547

  Schad, Julia ^a   Voigt, Christian C ^a   Greiner, Sabine ^a   Dechmann, Dina K N ^a,b   Sommer, Simone ^a  

^a LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

^b MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

Author keywords

Carollia perspicillata; DRB evolution; Major histocompatibility complex; Noctilio albiventris; Noctilio leporinus; Saccopteryx bilineata

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ALLELE; ANIMAL TISSUE; ARTICLE; BAT; CAROLLIA PERSPICILLATA; COPY NUMBER VARIATION; DRB GENE; EXON; GENE; GENE CONVERSION; GENE DUPLICATION; GENE LOCUS; GENE SEQUENCE; GENETIC RECOMBINATION; GENETIC VARIABILITY; IMMUNE SYSTEM; MOLECULAR EVOLUTION; NEW WORLD BAT; NOCTILIO ALBIVENTRIS; NOCTILIO LEPORINUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; SACCOPTERYX BILINEATA; VERTEBRATE;

ANIMALS; CHIROPTERA; CODON; EVOLUTION, MOLECULAR; GENETIC VARIATION; HISTOCOMPATIBILITY ANTIGENS CLASS II; HLA-DR BETA-CHAINS; PHYLOGENY; POLYMORPHISM, GENETIC;

CAROLLIA PERSPICILLATA; CHIROPTERA; MAMMALIA; MYOTIS; NOCTILIO; NOCTILIO ALBIVENTRIS; NOCTILIO LEPORINUS; SACCOPTERYX BILINEATA; VERTEBRATA;

EID: 84864194503     PISSN: 00937711     EISSN: 14321211     Source Type: Journal    
DOI: 10.1007/s00251-012-0609-1     Document Type: Article

References (78)

1. 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)
2. Axtner J, Sommer S (2011) Heligmosoides polygyrus infection is associated with lower MHC class II gene expression in Apodemys flavicolis: indication for immune suppression? Inf Gen Evol 2063-2071
3. Babik W, Radwan J (2007) Sequence diversity of MHC class II DRB genes in the bank vole Myodes glareolus. Acta Theriol 52(3):227-235 (Pubitemid 47235405)
4. Baker ML, Tachedjian M, Wang LF (2010) Immunoglobulin heavy chain diversity in Pteropid bats: evidence for a diverse and highly specific antigen binding reservoir. Immunogenetics 62:173-184
5. 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(4):448-460
6. Bowen L, Aldridge BM, Gulland F, Woo J, Van Bonn W, DeLong R, Stott JL, Johnson ML (2002) Molecular characterization of expressed DQA and DQB genes in the California sea lion (Zalophus californianus). Immunogenetics 54:332-347 (Pubitemid 34983951)
7. Bowen L, Aldridge BM, Gulland F, Van Bonn W, DeLong R, Melin S, Lowenstein LJ, Stott JL, Johnson ML (2004) Class II multiformity generated by variable MHC-DRB region configurations in the California sea lion (Zalophus californianus). Immunogenetics 56:12-27 (Pubitemid 38626418)
8. Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL et al (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA DR1. Nature 364:33-39 (Pubitemid 23233452)
9. Bryja J, Galan M, Charbonnel N, Cosson J-F (2006) Duplication, balancing selection and trans-species evolution explain the high levels of polymorphism of DQA MHC class II gene in voles (Arvicolinae). Immunogenetics 58:191-202
10. Burri R, Hirzel HN, Salamin N, Roulin A, Fumagalli L (2008) Evolutionary patterns of MHC class II B in owls and their implication for the understanding of avian MHC evolution. Mol Biol Evol 25 (6):1180-1191
11. Burri R, Salamin N, Studer RA, Roulin A, Fumagalli L (2010) Adaptive divergence of ancient duplicates in the avian MHC class II β. Mol Biol Evol 27(10):2360-2374
12. Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T (2006) Bats: important reservoir hosts of emerging viruses. Clin Micro-biol Rev 19(3):531-545 (Pubitemid 44134308)
13. Dobson AP (2005) What links bats to emerging infectious diseases? Science 310:628-629 (Pubitemid 41528145)
14. Doxiadis GGM, de Groot N, de Groot NG, Rotmans G, deVos-Reouweler AJM, Bontrop RE (2010) Extensive DRB region diversity in cynomolgus macaques: recombination as a driving force. Immunogenetics 62:137-147
15. Ellis SA, Bontrop RE, Antczak DF, Ballingall K, Davies CJ, Kaufman J et al (2006) ISAG/IUIS-VIC Comparative MHC Nomenclature Committee report, 2005. Immunogenetics 57:953-958 (Pubitemid 43185430)
16. Field HE (2009) Bats and emerging zoonoses: henipaviruses and SARS. Zoonoses Public Hlth 56(6-7):278-284
17. Figuroa F, Günther G, Klein J (1988) MHC polymorphism predating speciation. Nature 335:265-67
18. Gannon WL, Sikes RS (2007) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 88:809
19. Goüy de Bellocq J, Suchentrunk F, Baird SEB, Schaschl H (2009) Evolutionary history of an MHC gene in two leporid species: characterisation of Mhc-DQA in the European brown hare and comparison with European rabbit. Immunogenetics 61:131-144
20. Hess CM, Edwards SV (2002) The evolution of the major histocom-patibility complex in birds. Bioscience 52(5):423-431 (Pubitemid 34458435)
21. Hughes AL (1994) The evolution of functionally novel proteins after gene duplications. Proc R Soc Lond B 256:119-124 (Pubitemid 24168165)
22. Hughes AL (2000) Evolution of introns and exons of class II major histocompatibility complex genes of vertebrates. Immunogenetics 51:473-486 (Pubitemid 30265038)
23. Hughes AL (2007) Looking for Darwin in all the wrong places: the misguided quest for positive selection at the nucleotide sequence level. Heredity 99:364-373 (Pubitemid 47482647)
24. Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335:167-170
25. Hughes AL, Yeager M (1998) Natural selection at major histocompat-ibility complex loci of vertebrates. Annu Rev Genet 32:415-435 (Pubitemid 29045319)
26. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munroe HN (ed) Mammalian protein metabolism. Academic, New York, pp 21-132
27. Kennedy LJ, Ryvar R, Gaskell RM, Addie DD, WilloughbyK, Carter SD et al (2002) Sequence analyses of MHC DRB alleles in domestic cats from the United Kingdom. Immunogenetics 54:348-352 (Pubitemid 34983952)
28. 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
29. Klein J (1986) Natural history of the major histocompatibility complex. Wiley, New York
30. Klein J (1987) Origin of major histocompatibility complex polymorphism: the trans-species hypothesis. Human Immunol 19:155-162 (Pubitemid 17151465)
31. Klein J, Sato A, Nikolaides N (2007) MHC, TSP, and the origin of species: from immunogenetics to evolutionary genetics. Annu Rev Genet 41:281-304
32. Kriener K, O'hUigin C, Tichy H, Klein J (2000) Convergent evolution of major histocompatibility complex molecules in humans and New World monkeys. Immunogenetics 51:69-178
33. Kriener K, O'hUigin C, Klein J (2001) Independent origin of functional MHC class II genes in humans and new world monkeys. Hum Immun 62:1-14 (Pubitemid 32163929)
34. Kumanovics A, Takada T, Fischer Lindahl K (2003) Genomic organization of the mammalian MHC. Annu Rev Immunol 21:629-657 (Pubitemid 37174543)
35. Kunz TH, Braun de Torres E, Bauer D, Lobova T, Fleming TH (2011) Ecosystem services provided by bats. Ann N Y Acad Sci 1223:1-3
36. Kupfermann H, Satta Y, Takahata N, Tichy H, Klein J (1999) Evolution of MHC-DRB introns: implication for the origin of primates. J Mol Evol 48:663-674 (Pubitemid 29287956)
37. Lewis-Oritt N, Van den Busche RA, Baker RJ (2001) Molecular evidence for evolution of piscivory in Noctilio (Chiroptera: Noc-tilionidae). J Mammal 82:748-759 (Pubitemid 32818433)
38. Mansai SP, Innan H (2010) The power of the methods for detecting interlocus gene conversion. Genetics 184:517-572
39. Mayer F, Brunner A (2007) Non-neutral evolution of the major histo-compatibility complex class II gene DRB1 in the sac-winged bat Saccopteryx bilineata. Heredity 99:257-264 (Pubitemid 47295855)
40. Mayer WE, Jonker M, Klein D, Ivanyi P, van Seventer G, Klein J (1988) Nucleotide sequences of chimpanzee MHC class I alleles: evidence for trans-species mode of evolution. EMBO 7(9):2765-2774
41. Mikko S, Roed K, Schmutz S, Andersson L (1999) Monomorphism and polymorphism at MHC DRB loci in domestic and wild ruminants. Immunol Rev 167:169-178 (Pubitemid 29178979)
42. Musolf K, Meyer-Lucht Y, Sommer S (2004) Evolution of MHC-DRB class II polymorphism in the genus Apodemus and a comparison of DRB sequences within the family Muridae (Mammalia: Rodentia). Immunogenetics 56(6):420-426 (Pubitemid 39349883)
43. Nemeth E, Baird AW, O'Farrelly C (2009) Microanatomy of the liver immune system. Semin Immunopathol 31:333-343
44. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3(5):418-426 (Pubitemid 16010523)
45. Nei M, Hughes AL (1992) Balanced polymorphism and evolution by the birth-and-death process in the MHC loci. In: Tsuij K, Aizawa M, Sasazuki T (eds) 11th Histocompatibility Workshop and Conference. Oxford University Press, Oxford
46. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
47. Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121-152 (Pubitemid 43011110)
48. O'hUigin C (1995) Quantifying the degree of convergence in primate MHC-DRB genes. Immunol Rev 143:123-140
49. Otha T (1999) Effect of gene conversion on polymorphic patterns at major histocompatibility complex loci. Immunol Rev 167:319-325
50. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7-21
51. Posada D (2002) Evaluation of methods for detecting recombination from DNA sequences: empirical data. Mol Biol Evol 19(5):708-717 (Pubitemid 34521302)
52. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253-1256 (Pubitemid 351882013)
53. Reusch TBH, Langefors A (2005) Inter-and intralocus recombination drive MHC class II B gene diversification in a teleost, three-spined stickleback Gasterosteus aculeatus. J Mol Evol 61:531-545
54. Richman AD, Herrera LG, Nash D, Schierup HM (2003) Relative roles of mutation and recombination in generating allelic polymorphism at a MHC class II locus in Peromyscus maniculatus. Genet Res Camb 82:89-99 (Pubitemid 37527160)
55. Richman AD, Herrera LG, Ortega-Garcia S, Flores-Martinez JJ, Arroyo-Cabrales J, Morales-Malacara JB (2010) Class II DRB polymorphism and sequence diversity in two vesper bats in the genus Myotis. Immunogenetics 37(5):401-405
56. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574 (Pubitemid 37038874)
57. Sawyer SA (1999) GENECONV: a computer package for the statistical detection of gene conversion. Distribution by the author, Dept of Mathematics, Washington University, St Louis (http://www.math. wustl.edu/-sawyer)
58. Schad J, Sommer S, Ganzhorn J (2004) MHC variability of a small lemur in the littoral forest fragments of south-eastern Madagascar. Conserv Genet 5:299-309 (Pubitemid 38983078)
59. Schad J, Dechmann DKN, Voigt CC, Sommer S (2011) MHC class II DRB diversity, selection pattern and population structure in a neotropical bat species, Noctilio albiventris. Heredity 107:115-126
60. Schaschl H, Suchentrunk F, Hammer S, Goodman SJ (2005) Recombination and the origin of sequence diversity in the MHC class II DRB in chamois (Rupicapra spp.). Immunoge-netics 57:108-115 (Pubitemid 40591251)
61. Schaschl H, Wandeler P, Suchentrunk F, Obexer-Ruff G, Goodman SJ (2006) Selection and recombination drive evolution of MHC class II DRB diversity in ungulates. Heredity 97:427-437 (Pubitemid 44851250)
62. Srithayakumar V, Castillo S, Mainguy J, Kyle CJ (2012) Evidence for evolutionary convergence at MHC in two broadly distributed mesocarnivores. Immunogenetics. doi:10.1007/s00251.011-0588-7
63. Stern LJ, Brown JH, Jardetzky JCG, Urban RG, Strominger JL, Wiley DC (1994) Crystal structure of the human class II MHC protein HLA-DR1 complexed with an influenza virus peptide. Nature 368:215-221 (Pubitemid 24108837)
64. Suárez CF, Patarroyo ME, Trujillo E, Estupiñán M, Baquero JE, Parra C, Rodriguez R (2006) Owl monkey MHC DRB exon 2 reveals high similarity with several HLA-DRB lineages. Immunogenetics 58:542-558 (Pubitemid 44025529)
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. Trowsdale J (1995) Both man & bird & beast: comparative organization of MHC genes. Immunogenetics 41:1-17 (Pubitemid 24373334)
67. Vilamiu RP, Correa MM, Pessoa LM, Oliveira JA, Oliveira LFB (2010) The karyotype of Noctilio albiventris (Chiroptera: Nocti-lionidae) from Brazil and its taxonomic implications. Mastozool Neotrop 17(1):219-224
68. Virtue ER, Marsh GA, Baker ML, Wang LF (2011) Interferon production and signalling pathways are antagonized during Henipavirus infection in fruit bat cell lines. Plos One 6(7): e22488
69. Wei K, Zhang Z, Wang X, Zhang W, Xu X, Shen F, Yue B (2010) Lineage pattern, trans-species polymorphism, and selection pressure among the major lineages of feline MHC-DRB peptide-binding region. Immunogenetics 62:307-317
70. Wibbelt G, Moore M, Schountz T, Voigt CC (2010) Emerging diseases in Chiroptera: why bats? Biol Lett 6:438-440
71. Worthington-Wilmer J, Baratt E (1996) A non-lethal method of tissue-sampling for genetic studies of chiropterans. Bat Res News 37:1-3
72. Xu SX, Chen BY, Zhou KY, Yang G (2008) High sequence similarity at three MHC loci between baiji and finless porpoise: trans-species or convergent evolution? Mol Phylogenet Evol 47:36-44
73. Xu SX, Ren WH, Li SZ, Wei FW, Zhou KY, Yang G (2009) Sequence polymorphism and evolution of three Cetacean MHC genes. J Mol Evol 69:260-275
74. Yang ZH (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586-1591
75. Yang ZH, Bielawski JP (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15:496-503
76. Yang ZH, Wong WSW, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107-1118 (Pubitemid 40471423)
77. Yeager M, Hughes AL (1999) Evolution of the mammalian MHC: natural selection, recombination and convergent evolution. Immun Rev 167:45-58 (Pubitemid 29178970)
78. Yuhki N, Beck T, Stephens R, Neelam B, O'Brien ST (2007) Comparative genomic structure of human, dog and cat MHC: HLA, DLA, and FLA. J Hered 98(5):390-399 (Pubitemid 47357595)