The differential evolutionary dynamics of avian cytokine and TLR gene classes

Journal of Immunology

Volumn 184, Issue 12, 2010, Pages 6993-7000

  Downing, Tim ^a,b   Lloyd, Andrew T ^a   O'Farrelly, Cliona ^a   Bradley, Daniel G ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 8; INTERLEUKIN 9; TOLL LIKE RECEPTOR; CYTOKINE;

ADAPTATION; ALLELE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHICKEN; CONTROLLED STUDY; FOWL; GENE; GENE FREQUENCY; GENE SEQUENCE; GENETIC VARIABILITY; HIGH THROUGHPUT SCREENING; IMMUNE RESPONSE; MEDIATOR; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TLR GENE; ANIMAL; BIRD; EVOLUTION; GENETICS; IMMUNOLOGY; MOLECULAR GENETICS; PHYLOGENY; POLYMERASE CHAIN REACTION; POPULATION GENETICS; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; BASE SEQUENCE; BIRDS; CHICKENS; CYTOKINES; EVOLUTION; GENE FREQUENCY; GENETICS, POPULATION; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION; POLYMORPHISM, SINGLE NUCLEOTIDE; TOLL-LIKE RECEPTORS;

EID: 77953632236     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903092     Document Type: Article

References (116)

1. Akira, S., K. Hoshino, and T. Kaisho. 2000. The role of Toll-like receptors and MyD88 in innate immune responses. J. Endotoxin Res. 6: 383-387. (Pubitemid 32241948)
2. Zhou, H., J. Gu, S. J. Lamont, and X. Gu. 2007. Evolutionary analysis for functional divergence of the toll-like receptor gene family and altered functional constraints. J. Mol. Evol. 65: 119-123.
3. Leulier, F., and B. Lemaitre. 2008. Toll-like receptors - taking an evolutionary approach. Nat. Rev. Genet. 9: 165-178.
4. Avery, S., L. Rothwell, W. D. Degen, V. E. Schijns, J. Young, J. Kaufman, and P. Kaiser. 2004. Characterization of the first nonmammalian T2 cytokine gene cluster: the cluster contains functional single-copy genes for IL-3, IL-4, IL-13, and GM-CSF, a gene for IL-5 that appears to be a pseudogene, and a gene encoding another cytokinelike transcript, KK34. J. Interferon Cytokine Res. 24: 600-610. (Pubitemid 39332197)
5. O'Garra, A. 1998. Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity 8: 275-283. (Pubitemid 28188888)
6. Kaiser, P., T. Y. Poh, L. Rothwell, S. Avery, S. Balu, U. S. Pathania, S. Hughes, M. Goodchild, S. Morrell, M. Watson, et al. 2005. A genomic analysis of chicken cytokines and chemokines. J. Interferon Cytokine Res. 25: 467-484. (Pubitemid 41193122)
7. Staeheli, P., F. Puehler, K. Schneider, T. W. Göbel, and B. Kaspers. 2001. Cytokines of birds: conserved functions - a largely different look. J. Interferon Cytokine Res. 21: 993-1010. (Pubitemid 34114278)
8. Xing, Z., C. J. Cardona, J. Li, N. Dao, T. Tran, and J. Andrada. 2008. Modulation of the immune responses in chickens by low-pathogenicity avian influenza virus H9N2. J. Gen. Virol. 89: 1288-1299.
9. Kogut, M. H., M. Iqbal, H. He, V. Philbin, P. Kaiser, and A. Smith. 2005. Expression and function of Toll-like receptors in chicken heterophils. Dev. Comp. Immunol. 29: 791-807.
10. Dil, N., and M. A. Qureshi. 2002. Involvement of lipopolysaccharide related receptors and nuclear factor kappa B in differential expression of inducible nitric oxide synthase in chicken macrophages from different genetic backgrounds. Vet. Immunol. Immunopathol. 88: 149-161.
11. Farnell, M. B., T. L. Crippen, H. He, C. L. Swaggerty, and M. H. Kogut. 2003. Oxidative burst mediated by toll like receptors (TLR) and CD14 on avian heterophils stimulated with bacterial toll agonists. Dev. Comp. Immunol. 27: 423-429.
12. Malek, M., J. R. Hasenstein, and S. J. Lamont. 2004. Analysis of chicken TLR4, CD28, MIF, MD-2, and LITAF genes in a Salmonella enteritidis resource population. Poult. Sci. 83: 544-549.
13. Iqbal, M., V. J. Philbin, G. S. Withanage, P. Wigley, R. K. Beal, M. J. Goodchild, P. Barrow, I. McConnell, D. J. Maskell, J. Young, et al. 2005. Identification and functional characterization of chicken toll-like receptor 5 reveals a fundamental role in the biology of infection with Salmonella enterica serovar typhimurium. Infect. Immun. 73: 2344-2350.
14. Ye, X., S. Avendano, J. C. Dekkers, and S. J. Lamont. 2006. Association of twelve immune-related genes with performance of three broiler lines in two different hygiene environments. Poult. Sci. 85: 1555-1569.
15. He, H., K. J. Genovese, D. J. Nisbet, and M. H. Kogut. 2006. Involvement of phosphatidylinositol-phospholipase C in immune response to Salmonella lipopolysacharide in chicken macrophage cells (HD11). Int. Immunopharmacol. 6: 1780-1787.
16. Higgs, R., P. Cormican, S. Cahalane, B. Allan, A. T. Lloyd, K. Meade, T. James, D. J. Lynn, L. A. Babiuk, and C. O'farrelly. 2006. Induction of a novel chicken Toll-like receptor following Salmonella enterica serovar Typhimurium infection. Infect. Immun. 74: 1692-1698.
17. Wang, X., A. J. Rosa, H. N. Oliverira, G. J. Rosa, X. Guo, M. Travnicek, and T. Girshick. 2006. Transcriptome of local innate and adaptive immunity during early phase of infectious bronchitis viral infection. Viral Immunol. 19: 768-774. (Pubitemid 46068070)
18. Keestra, A. M., and J. P. van Putten. 2008. Unique properties of the chicken TLR4/MD-2 complex: selective lipopolysaccharide activation of the MyD88-dependent pathway. J. Immunol. 181: 4354-4362.
19. Karpala, A. J., J. W. Lowenthal, and A. G. Bean. 2008. Activation of the TLR3 pathway regulates IFNbeta production in chickens. Dev. Comp. Immunol. 32: 435-444.
20. Higuchi, M., A. Matsuo, M. Shingai, K. Shida, A. Ishii, K. Funami, Y. Suzuki, H. Oshiumi, M. Matsumoto, and T. Seya. 2008. Combinational recognition of bacterial lipoproteins and peptidoglycan by chicken Toll-like receptor 2 subfamily. Dev. Comp. Immunol. 32: 147-155.
21. Abasht, B., M. G. Kaiser, and S. J. Lamont. 2008. Toll-like receptor gene expression in cecum and spleen of advanced intercross line chicks infected with Salmonella enterica serovar Enteritidis. Vet. Immunol. Immunopathol. 123: 314-323.
22. Keestra, A. M., M. R. de Zoete, R. A. van Aubel, and J. P. van Putten. 2008. Functional characterization of chicken TLR5 reveals species-specific recognition of flagellin. Mol. Immunol. 45: 1298-1307.
23. Chiang, H. I., C. L. Swaggerty, M. H. Kogut, S. E. Dowd, X. Li, I. Y. Pevzner, and H. Zhou. 2008. Gene expression profiling in chicken heterophils with Salmonella enteritidis stimulation using a chicken 44 K Agilent microarray. BMC Genomics 9: 526.
24. Nerren, J. R., C. L. Swaggerty, K. M. MacKinnon, K. J. Genovese, H. He, I. Pevzner, and M. H. Kogut. 2009. Differential mRNA expression of the avian-specific toll-like receptor 15 between heterophils from Salmonella-susceptible and -resistant chickens. Immunogenetics 61: 71-77.
25. Keestra, A. M., M. R. de Zoete, R. A. van Aubel, and J. P. van Putten. 2007. The central leucine-rich repeat region of chicken TLR16 dictates unique ligand specificity and species-specific interaction with TLR2. J. Immunol. 178: 7110-7119.
26. Abasht, B., M. G. Kaiser, J. van der Poel, and S. J. Lamont. 2009. Genetic lines differ in Toll-like receptor gene expression in spleens of chicks inoculated with Salmonella enterica serovar Enteritidis. Poult. Sci. 88: 744-749.
27. Ozoe, A., N. Isobe, and Y. Yoshimura. 2009. Expression of Toll-like receptors (TLRs) and TLR4 response to lipopolysaccharide in hen oviduct. Vet. Immunol. Immunopathol. 127: 259-268.
28. Shaughnessy, R. G., K. G. Meade, S. Cahalane, B. Allan, C. Reiman, J. J. Callanan, and C. O'Farrelly. 2009. Innate immune gene expression differentiates the early avian intestinal response between Salmonella and Campylobacter. Vet. Immunol. Immunopathol. 132: 191-198.
29. Bedard, P. A., D. Alcorta, D. L. Simmons, K. C. Luk, and R. L. Erikson. 1987. Constitutive expression of a gene encoding a polypeptide homologous to biologically active human platelet protein in Rous sarcoma virus-transformed fibroblasts. Proc. Natl. Acad. Sci. USA 84: 6715-6719.
30. Sugano, S., M. Y. Stoeckle, and H. Hanafusa. 1987. Transformation by Rous sarcoma virus induces a novel gene with homology to a mitogenic platelet protein. Cell 49: 321-328.
31. Berndt, A., A. Wilhelm, C. Jugert, J. Pieper, K. Sachse, and U. Methner. 2007. Chicken cecum immune response to Salmonella enterica serovars of different levels of invasiveness. Infect. Immun. 75: 5993-6007.
32. Kim, D. K., Y. H. Hong, D. W. Park, S. J. Lamont, and H. S. Lillehoj. 2008. Differential immune-related gene expression in two genetically disparate chicken lines during infection by Eimeria maxima. Dev. Biol. (Basel) 132: 131-140.
33. Heidari, M., H. M. Zhang, and S. Sharif. 2008. Marek's disease virus induces Th-2 activity during cytolytic infection. Viral Immunol. 21: 203-214.
34. Abdul-Careem, M. F., D. B. Hunter, M. D. Lambourne, L. R. Read, P. Parvizi, and S. Sharif. 2008. Expression of cytokine genes following pre- and post-hatch immunization of chickens with herpesvirus of turkeys. Vaccine 26: 2369-2377.
35. International Chicken Genome Sequencing Consortium. 2004. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432: 695-716.
36. Shiina, T., S. Shimizu, K. Hosomichi, S. Kohara, S. Watanabe, K. Hanzawa, S. Beck, J. K. Kulski, and H. Inoko. 2004. Comparative genomic analysis of two avian (quail and chicken) MHC regions. J. Immunol. 172: 6751-6763. (Pubitemid 38669112)
37. Kaiser, P., J. Howell, M. Fife, J. R. Sadeyen, N. Salmon, L. Rothwell, J. Young, P. van Diemen, M. Stevens, T. Y. Poh, et al. 2008. Integrated immunogenomics in the chicken: deciphering the immune response to identify disease resistance genes. Dev. Biol. (Basel) 132: 57-66.
38. Temperley, N. D., S. Berlin, I. R. Paton, D. K. Griffin, and D. W. Burt. 2008. Evolution of the chicken Toll-like receptor gene family: a story of gene gain and gene loss. BMC Genomics 9: 62.
39. Hosomichi, K., M. M. Miller, R. M. Goto, Y. Wang, S. Suzuki, J. K. Kulski, M. Nishibori, H. Inoko, K. Hanzawa, and T. Shiina. 2008. Contribution of mutation, recombination, and gene conversion to chicken MHC-B haplotype diversity. J. Immunol. 181: 3393-3399.
40. Ferrer-Admetlla, A., E. Bosch, M. Sikora, T. Marquès-Bonet, A. Ramírez-Soriano, A. Muntasell, A. Navarro, R. Lazarus, F. Calafell, J. Bertranpetit, and F. Casals. 2008. Balancing selection is the main force shaping the evolution of innate immunity genes. J. Immunol. 181: 1315-1322.
41. Fumagalli, M., U. Pozzoli, R. Cagliani, G. P. Comi, S. Riva, M. Clerici, N. Bresolin, and M. Sironi. 2009. Parasites represent a major selective force for interleukin genes and shape the genetic predisposition to autoimmune conditions. J. Exp. Med. 206: 1395-1408.
42. Sackton, T. B., B. P. Lazzaro, T. A. Schlenke, J. D. Evans, D. Hultmark, and A. G. Clark. 2007. Dynamic evolution of the innate immune system in Drosophila. Nat. Genet. 39: 1461-1468.
43. Moeller, D. A., and P. Tiffin. 2008. Geographic variation in adaptation at the molecular level: a case study of plant immunity genes. Evolution 62: 3069-3081.
44. Kim, P. M., J. O. Korbel, and M. B. Gerstein. 2007. Positive selection at the protein network periphery: evaluation in terms of structural constraints and cellular context. Proc. Natl. Acad. Sci. USA 104: 20274-20279.
45. Cui, Q., E. O. Purisima, and E. Wang. 2009. Protein evolution on a human signaling network. BMC Syst. Biol. 3: 21.
46. Yilmaz, A., S. Shen, D. L. Adelson, S. Xavier, and J. J. Zhu. 2005. Identification and sequence analysis of chicken Toll-like receptors. Immunogenetics 56: 743-753.
47. Cormican, P., A. T. Lloyd, T. Downing, S. J. Connell, D. G. Bradley, and C. O'Farrelly. 2009. The avian Toll-Like receptor pathway - subtle differences amidst general conformity. Dev. Comp. Immunol. 33: 967-973.
48. Downing, T., D. J. Lynn, S. Connell, A. T. Lloyd, A. K. Bhuiyan, P. Silva, A. N. Naqvi, R. Sanfo, R. S. Sow, B. Podisi, et al. 2009. Contrasting evolution of diversity at two disease-associated chicken genes. Immunogenetics 61: 303-314.
49. Cox, A. Eland: Efficient Local Alignment of Nucleotide Data (unpublished).
50. Librado, P., and J. Rozas. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
51. Watterson, G. A. 1975. On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7: 256-276.
52. Tajima, F. 1983. Evolutionary relationship of DNA sequences in finite populations. Genetics 105: 437-460. (Pubitemid 14247444)
53. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595. (Pubitemid 19274682)
54. Fu, Y. X., and W. H. Li. 1993. Statistical tests of neutrality of mutations. Genetics 133: 693-709.
55. Fu, Y. X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915-925.
56. Fay, J. C., and C. I. Wu. 2000. Hitchhiking under positive Darwinian selection. Genetics 155: 1405-1413.
57. Hudson, R. R., and N. L. Kaplan. 1985. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111: 147-164.
58. Hudson, R. R. 1987. Estimating the recombination parameter of a finite population model without selection. Genet. Res. 50: 245-250.
59. Betrán, E., J. Rozas, A. Navarro, and A. Barbadilla. 1997. The estimation of the number and the length distribution of gene conversion tracts from population DNA sequence data. Genetics 146: 89-99. (Pubitemid 27194392)
60. Depaulis, F., and M. Veuille. 1998. Neutrality tests based on the distribution of haplotypes under an infinite-site model. Mol. Biol. Evol. 15: 1788-1790.
61. Axelsson, E., and H. Ellegren. 2009. Quantification of adaptive evolution of genes expressed in avian brain and the population size effect on the efficacy of selection. Mol. Biol. Evol. 26: 1073-1079.
62. Liti, G., D. M. Carter, A. M. Moses, J. Warringer, L. Parts, S. A. James, R. P. Davey, I. N. Roberts, A. Burt, V. Koufopanou, et al. 2009. Population genomics of domestic and wild yeasts. Nature 458: 337-341.
63. Notredame, C., D. G. Higgins, and J. Heringa. 2000. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302: 205-217.
64. Hofmann, K., and W. Stoffel. 1993. TMbase - A database of membrane spanning proteins segments. Biol. Chem. Hoppe Seyler 374: 166.
65. Bandelt, H. J., P. Forster, and A. Röhl. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16: 37-48.
66. Wright, S. 1951. The genetical structure of populations. Ann. Eugen. 15: 323-354.
67. Schneider, S., D. Roessli, and L. Excofier. 2000. Arlequin, Version 2.0: a software for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneva, Geneva.
68. Yang, Z. 2002. Inference of selection from multiple species alignments. Curr. Opin. Genet. Dev. 12: 688-694.
69. Fu, Y. X. 1995. Statistical properties of segregating sites. Theor. Popul. Biol. 48: 172-197.
70. Beaumont, C., J. Protais, F. Pitel, G. Leveque, D. Malo, F. Lantier, F. Plisson-Petit, P. Colin, M. Protais, P. Le Roy, et al. 2003. Effect of two candidate genes on the Salmonella carrier state in fowl. Poult. Sci. 82: 721-726.
71. Leveque, G., V. Forgetta, S. Morroll, A. L. Smith, N. Bumstead, P. Barrow, J. C. Loredo-Osti, K. Morgan, and D. Malo. 2003. Allelic variation in TLR4 is linked to susceptibility to Salmonella enterica serovar Typhimurium infection in chickens. Infect. Immun. 71: 1116-1124.
72. Barreiro, L. B., M. Ben-Ali, H. Quach, G. Laval, E. Patin, J. K. Pickrell, C. Bouchier, M. Tichit, O. Neyrolles, B. Gicquel, et al. 2009. Evolutionary dynamics of human Toll-like receptors and their different contributions to host defense. PLoS Genet. 5: e1000562.
73. Liu, Y. P., G. S. Wu, Y. G. Yao, Y. W. Miao, G. Luikart, M. Baig, A. Beja-Pereira, Z. L. Ding, M. G. Palanichamy, and Y. P. Zhang. 2006. Multiple maternal origins of chickens: out of the Asian jungles. Mol. Phylogenet. Evol. 38: 12-19.
74. Bao, W., G. Chen, B. Li, X. Wu, J. Shu, S. Wu, Q. Xu, and S. Weigend. 2008. Analysis of genetic diversity and phylogenetic relationships among red jungle fowls and Chinese domestic fowls. Sci. China C Life Sci. 51: 560-568.
75. Worley, K., M. Gillingham, P. Jensen, L. J. Kennedy, T. Pizzari, J. Kaufman, and D. S. Richardson. 2008. Single locus typing of MHC class I and class II B loci in a population of red jungle fowl. Immunogenetics 60: 233-247.
76. Berlin, S., L. Qu, X. Li, N. Yang, and H. Ellegren. 2008. Positive diversifying selection in avian Mx genes. Immunogenetics 60: 689-697.
77. Downing, T., D. J. Lynn, S. Connell, A. T. Lloyd, A. K. Bhuiyan, P. Silva, A. N. Naqvi, R. Sanfo, R. S. Sow, B. Podisi, et al. 2009. Evidence of balanced diversity at the chicken interleukin 4 receptor alpha locus. BMC Evol. Biol. 9: 136.
78. Downing, T., C. O'Farrelly, A. K. Bhuiyan, P. Silva, A. N. Naqvi, R. Sanfo, R. S. Sow, B. Podisi, O. Hanotte, and D. G. Bradley. 2010. Variation in chicken populations may affect the enzymatic activity of lysozyme. Anim. Genet. 41: 213-217.
79. Innan, H., and Y. Kim. 2008. Detecting local adaptation using the joint sampling of polymorphism data in the parental and derived populations. Genetics 179: 1713-1720.
80. Hermisson, J., and P. S. Pennings. 2005. Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169: 2335-2352.
81. Przeworski, M., G. Coop, and J. D. Wall. 2005. The signature of positive selection on standing genetic variation. Evolution 59: 2312-2323.
82. Lyons, E. J., W. Amos, J. A. Berkley, I. Mwangi, M. Shafi, T. N. Williams, C. R. Newton, N. Peshu, K. Marsh, J. A. Scott, and A. V. Hill. 2009a. Homozygosity and risk of childhood death due to invasive bacterial disease. BMC Med. Genet. 10: 55.
83. Lyons, E. J., A. J. Frodsham, L. Zhang, A. V. Hill, and W. Amos. 2009b. Consanguinity and susceptibility to infectious diseases in humans. Biol. Lett. 5: 574-576.
84. Reid, J. M., P. Arcese, L. F. Keller, K. H. Elliott, L. Sampson, and D. Hasselquist. 2007. Inbreeding effects on immune response in free-living song sparrows (Melospiza melodia). Proc. Biol. Sci. 274: 697-706.
85. Mulard, H., E. Danchin, S. L. Talbot, A. M. Ramey, S. A. Hatch, J. F. White, F. Helfenstein, and R. H. Wagner. 2009. Evidence that pairing with genetically similar mates is maladaptive in a monogamous bird. BMC Evol. Biol. 9: 147.
86. Asthana, S., S. Schmidt, and S. Sunyaev. 2005. A limited role for balancing selection. Trends Genet. 21: 30-32.
87. Seow, H. F. 1998. Pathogen interactions with cytokines and host defence: an overview. Vet. Immunol. Immunopathol. 63: 139-148.
88. Alcami, A. 2003. Viral mimicry of cytokines, chemokines and their receptors. Nat. Rev. Immunol. 3: 36-50.
89. Pfeffer, K. 2003. Biological functions of tumor necrosis factor cytokines and their receptors. Cytokine Growth Factor Rev. 14: 185-191. (Pubitemid 36693140)
90. Conti, B., I. Tabarean, C. Andrei, and T. Bartfai. 2004. Cytokines and fever. Front. Biosci. 9: 1433-1449.
91. Zhang, C. 2008. The role of inflammatory cytokines in endothelial dysfunction. Basic Res. Cardiol. 103: 398-406.
92. Ferreira, M. A. 2003. Cytokine expression in allergic inflammation: systematic review of in vivo challenge studies. Mediators Inflamm. 12: 259-267.
93. Howard, T. D., D. A. Meyers, and E. R. Bleecker. 2000. Mapping susceptibility genes for asthma and allergy. J. Allergy Clin. Immunol. 105: S477-S481.
94. Khor, C. C., S. J. Chapman, F. O. Vannberg, A. Dunne, C. Murphy, E. Y. Ling, A. J. Frodsham, A. J. Walley, O. Kyrieleis, A. Khan, et al. 2007. A Mal functional variant is associated with protection against invasive pneumococcal disease, bacteremia, malaria and tuberculosis. Nat. Genet. 39: 523-528.
95. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124: 783-801.
96. Andrés, A. M., M. J. Hubisz, A. Indap, D. G. Torgerson, J. D. Degenhardt, A. R. Boyko, R. N. Gutenkunst, T. J. White, E. D. Green, C. D. Bustamante, et al. 2009. Targets of balancing selection in the human genome. Mol. Biol. Evol. 26: 2755-2764.
97. Hoffjan, S., D. Nicolae, and C. Ober. 2003. Association studies for asthma and atopic diseases: a comprehensive review of the literature. Respir. Res. 4: 14.
98. Ots, I., A. B. Kerimov, E. V. Ivankina, T. A. Ilyina, and P. Hõrak. 2001. Immune challenge affects basal metabolic activity in wintering great tits. Proc. Biol. Sci. 268: 1175-1181.
99. Wilson, J. N., K. Rockett, B. Keating, M. Jallow, M. Pinder, F. Sisay-Joof, M. Newport, and D. Kwiatkowski. 2006. A hallmark of balancing selection is present at the promoter region of interleukin 10. Genes Immun. 7: 680-683.
100. Mege, J. L., S. Meghari, A. Honstettre, C. Capo, and D. Raoult. 2006. The two faces of interleukin 10 in human infectious diseases. Lancet Infect. Dis. 6: 557-569.
101. Akey, J. M., M. A. Eberle, M. J. Rieder, C. S. Carlson, M. D. Shriver, D. A. Nickerson, and L. Kruglyak. 2004. Population history and natural selection shape patterns of genetic variation in 132 genes. PLoS Biol. 2: e286.
102. Sackton, T. B., B. P. Lazzaro, and A. G. Clark. 2010. Genotype and gene expression associations with immune function in Drosophila. PLoS Genet. 6: e1000797.
103. Bezbradica, J. S., and R. Medzhitov. 2009. Integration of cytokine and heterologous receptor signaling pathways. Nat. Immunol. 10: 333-339.
104. Muchadeyi, F. C., H. Eding, H. Simianer, C. B. Wollny, E. Groeneveld, and S. Weigend. 2008. Mitochondrial DNA D-loop sequences suggest a Southeast Asian and Indian origin of Zimbabwean village chickens. Anim. Genet. 39: 615-622.
105. Berthouly, C., G. Leroy, T. N. Van, H. H. Thanh, B. Bed'Hom, B. T. Nguyen, C. C. Vu, F. Monicat, M. Tixier-Boichard, E. Verrier, et al. 2009. Genetic analysis of local Vietnamese chickens provides evidence of gene flow from wild to domestic populations. BMC Genet. 10: 1.
106. West, B., and B. X. Zhou. 1989. Did chickens go north? New evidence for domestication. Worlds Poult. Sci. J. 45: 205-218.
107. Fumihito, A., T. Miyake, M. Takada, R. Shingu, T. Endo, T. Gojobori, N. Kondo, and S. Ohno. 1996. Monophyletic origin and unique dispersal patterns of domestic fowls. Proc. Natl. Acad. Sci. USA 93: 6792-6795.
108. Fumihito, A., T. Miyake, S. Sumi, M. Takada, S. Ohno, and N. Kondo. 1994. One subspecies of the red junglefowl (Gallus gallus gallus) suffices as the matriarchic ancestor of all domestic breeds. Proc. Natl. Acad. Sci. USA 91: 12505-12509.
109. Oka, T., Y. Ino, K. Nomura, S. Kawashima, T. Kuwayama, H. Hanada, T. Amano, M. Takada, N. Takahata, Y. Hayashi, and F. Akishinonomiya. 2007. Analysis of mtDNA sequences shows Japanese native chickens have multiple origins. Anim. Genet. 38: 287-293.
110. Razafindraibe, H., V. A. Mobegi, S. C. Ommeh, M. L. Rakotondravao, G. Bjørnstad, O. Hanotte, and H. Jianlin. 2008. Mitochondrial DNA origin of indigenous malagasy chicken. Ann. N. Y. Acad. Sci. 1149: 77-79.
111. Eriksson, J., G. Larson, U. Gunnarsson, B. Bed'hom, M. Tixier-Boichard, L. Strömstedt, D. Wright, A. Jungerius, A. Vereijken, E. Randi, et al. 2008. Identification of the yellow skin gene reveals a hybrid origin of the domestic chicken. PLoS Genet. 4: e1000010.
112. Silva, P., X. Guan, O. Ho-Shing, J. Jones, J. Xu, D. Hui, D. Notter, and E. Smith. 2009. Mitochondrial DNA-based analysis of genetic variation and relatedness among Sri Lankan indigenous chickens and the Ceylon junglefowl (Gallus lafayetti). Anim. Genet. 40: 1-9.
113. Nishibori, M., T. Shimogiri, T. Hayashi, and H. Yasue. 2005. Molecular evidence for hybridization of species in the genus Gallus except for Gallus varius. Anim. Genet. 36: 367-375.
114. Storey, A. A., J. M. Ramírez, D. Quiroz, D. V. Burley, D. J. Addison, R. Walter, A. J. Anderson, T. L. Hunt, J. S. Athens, L. Huynen, and E. A. Matisoo-Smith. 2007. Radiocarbon and DNA evidence for a pre-Columbian introduction of Polynesian chickens to Chile. Proc. Natl. Acad. Sci. USA 104: 10335-10339.
115. Kanginakudru, S., M. Metta, R. D. Jakati, and J. Nagaraju. 2008. Genetic evidence from Indian red jungle fowl corroborates multiple domestication of modern day chicken. BMC Evol. Biol. 8: 174.
116. Granevitze, Z., J. Hillel, M. Feldman, A. Six, H. Eding, and S. Weigend. 2009. Genetic structure of a wide-spectrum chicken gene pool. Anim. Genet. 40: 686-693.