House finch populations differ in early inflammatory signaling and pathogen tolerance at the peak of Mycoplasma Gallisepticum infection

American Naturalist

Volumn 181, Issue 5, 2013, Pages 674-689

  Adelman, James S ^a   Kirkpatrick, Laila ^a   Grodio, Jessica L ^b   Hawley, Dana M ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

Disease ecology; Emerging infectious disease; House finches; Inflammation; Mycoplasma gallisepticum; Resistance; Tolerance

Indexed keywords

ADAPTATION; BACTERIUM; COST-BENEFIT ANALYSIS; FITNESS; INFECTIOUS DISEASE; PATHOGENICITY; SIGNALING; SONGBIRD; TOLERANCE; WILD POPULATION;

ANIMAL; ANIMAL DISEASE; ARTICLE; BIRD DISEASE; COMPARATIVE STUDY; FINCH; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MICROBIOLOGY; MYCOPLASMA GALLISEPTICUM; MYCOPLASMOSIS; PATHOLOGY; SIGNAL TRANSDUCTION; UNITED STATES;

ALABAMA; ANIMALS; ARIZONA; BIRD DISEASES; FINCHES; HOST-PATHOGEN INTERACTIONS; MYCOPLASMA GALLISEPTICUM; MYCOPLASMA INFECTIONS; SIGNAL TRANSDUCTION;

ANIMALIA; AVES; BACTERIA (MICROORGANISMS); CARPODACUS MEXICANUS; MYCOPLASMA GALLISEPTICUM;

EID: 84876353143     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/670024     Document Type: Article

References (87)

1. Able, K. P., and J. R. Belthoff. 1998. Rapid "evolution" of migratory behaviour in the introduced house finch of eastern North America. Proceedings of the Royal Society B: Biological Sciences 265:2063- 2071.
2. Adelman, J. S., G. E. Bentley, J. C. Wingfield, L. B. Martin, and M. Hau. 2010a. Population differences in fever and sickness behaviors in a wild passerine: a role for cytokines. Journal of Experimental Biology 213:4099-4109.
3. Adelman, J. S., S. Cordoba-Cordoba, K. Spoelstra, M. Wikelski, and M. Hau. 2010b. Radio telemetry reveals variation in fever and sickness behaviours with latitude in a free-living passerine. Functional Ecology 24:813-823.
4. Altizer, S., A. K. Davis, K. C. Cook, and J. J. Cherry. 2004. Age, sex, and season affect the risk of mycoplasmal conjunctivitis in a southeastern house finch population. Canadian Journal of Zoology 82: 755-763.
5. Ashley, N. T., Z. M. Weil, and R. J. Nelson. 2012. Inflammation: mechanisms, costs, and natural variation. Annual Review of Ecology, Evolution, and Systematics 43:385-406, doi:10.1146 /annurev-ecolsys-040212-092530.
6. Aubert, A., G. Goodall, R. Dantzer, and G. Gheusi. 1997. Differential effects of lipopolysaccharide on pup retrieving and nest building in lactating mice. Brain Behavior and Immunity 11:107-118.
7. Badyaev, A. V., V. Belloni, and G. E. Hill. 2012. House finch: Hae-morhous mexicanus. The Birds of North America Online, ed. A. Poole. No. 46. Cornell Lab of Ornithology, Ithaca, NY, http:// www.bna.birds.cornell.edu/bna/species/046/articles/introduction.
8. Best, A., A. White, and M. Boots. 2008. Maintenance of host variation in tolerance to pathogens and parasites. Proceedings of the National Academy of Sciences of the USA 105:20786-20791.
9. Bonneaud, C, S. L. Balenger, A. F. Russell, J. Zhang, G. E. Hill, and S. V. Edwards. 2011. Rapid evolution of disease resistance is accompanied by functional changes in gene expression in a wild bird. Proceedings of the National Academy of Sciences of the USA 108:7866-7871.
10. Bonneaud, C, S. L. Balenger, J. Zhang, S. V. Edwards, and G. E. Hill. 2012. Innate immunity and the evolution of resistance to an emerging infectiouås disease in a wild bird. Molecular Ecology 21: 2628-2639.
11. Burness, G., C. Armstrong, T. Fee, and E. Tilman-Schindel. 2010. Is there an energetic-based trade-off between thermoregulation and the acute phase response in zebra finches? Journal of Experimental Biology 213:1386-1394.
12. Burnham, K. P., and D. R. Anderson. 2002. Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York.
13. Carroll, R. J., and D. Ruppert. 1988. Transformation and weighting in regression. Chapman & Hall, New York.
14. Carval, D., and R. Ferriere. 2010. A unified model for the coevolution of resistance, tolerance, and virulence. Evolution 64:2988-3009.
15. Dantzer, R. 2004. Cytokine-induced sickness behaviour: a neuroim-mune response to activation of innate immunity. European Journal of Pharmacology 500:399-411.
16. Day, T., A. L. Graham, and A. F. Read. 2007. Evolution of parasite virulence when host responses cause disease. Proceedings of the Royal Society B: Biological Sciences 274:2685-2692.
17. Decaestecker, E., S. Gaba, J. A. M. Raeymaekers, R. Stoks, L. Van Kerckhoven, D. Ebert, andL. De Meester. 2007. Host-parasite "Red Queen" dynamics archived in pond sediment. Nature 450:870- 873.
18. Dhondt, A. A., A. V. Badyaev, A. P. Dobson, D. M. Hawley, M. J. L. Driscoll, W. M. Hochachka, and D. H. Ley. 2006. Dynamics of mycoplasmal conjunctivitis in the native and introduced range of the host. EcoHealth 3:95-102.
19. Dhondt, A. A., D. L. Tessaglia, and R. L. Slothower. 1998. Epidemic mycoplasmal conjunctivitis in house finches from eastern North America. Journal of Wildlife Diseases 34:265-280.
20. Exton, M. S. 1997. Infection-induced anorexia: active host defence strategy. Appetite 29:369-383.
21. Faustino, C. R., C. S. Jennelle, V. Connolly, A. K. Davis, E. C. Swar-thout, A. A. Dhondt, and E. G. Cooch. 2004. Mycoplasma galli -septicum infection dynamics in a house finch population: seasonal variation in survival, encounter and transmission rate. Journal of Animal Ecology 73:651-669.
22. Ferrari, N, I. M. Cattadori, J. Nespereira, A. Rizzoli, and P. J. Hudson. 2004. The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecology Letters 7:88-94.
23. Ganapathy, K., and J. M. Bradbury. 2003. Effects of cyclosporin A on the immune responses and pathogenesis of a virulent strain of Mycoplasma gallisepticum in chickens. Avian Pathology 32:495-502.
24. Garland, T, Jr., and S. C. Adolph. 1994. Why not to do two-species comparative studies: limitations on inferring adaptation. Physiological Zoology 67:797-828.
25. Gaunson, J. E., C. J. Philip, K. G. Whithear, and G. F. Browning. 2006. The cellular immune response in the tracheal mucosa to Mycoplasma gallisepticum in vaccinated and unvaccinated chickens in the acute and chronic stages of disease. Vaccine 24:2627-2633.
26. Goldsby, R. A., T J. Kindt, and B. A. Osborne. 2000. Kuby immunology. W. H. Freeman, New York.
27. Graham, A. L., J. E. Allen, and A. F. Read. 2005. Evolutionary causes and consequences of immunopathology. Annual Review of Ecology, Evolution, and Systematics 36:373-397.
28. Graham, A. L., A. D. Hayward, K. A. Watt, J. G. Pilkington, J. M. Pemberton, and D. H. Nussey. 2010. Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science 330:662-665.
29. Graham, A. L., D. M. Shuker, L. C. Pollitt, S. K. J. R. Auld, A. J. Wilson, and T. J. Little. 2011. Fitness consequences of immune responses: strengthening the empirical framework for ecoimmu-nology. Functional Ecology 25:5-17.
30. Grau, G. E., L. F. Fajardo, P. F. Piguet, B. Allet, P. H. Lambert, and P. Vassalli. 1987. Tumor necrosis factor (cachectin) as an essential mediator in murine cerebral malaria. Science 237:1210-1212.
31. Grodio, J. L., E. L. Buckles, and K. A. Schat. 2009. Production of house finch (Carpodacus mexicanus) IgA specific anti-sera and its application in immunohistochemistry and in ELISA for detection of Mycoplasma gallisepticum-specific IgA. Veterinary Immunology and Immunopathology 132:288-294.
32. Grodio, J. L., K. V. Dhondt, P. H. ÓConnell, and K. A. Schat. 2008. Detection and quantification of Mycoplasma gallisepticum genome load in conjunctival samples of experimentally infected house finches (Carpodacus mexicanus) using real-time polymerase chain reaction. Avian Pathology 37:385-391.
33. Hart, B. L. 1988. Biological basis of the behavior of sick animals. Neuroscience and Biobehavioral Reviews 12:123-137.
34. Hawley, D. M., J. Briggs, A. A. Dhondt, and I. J. Lovette. 2008. Reconciling molecular signatures across markers: mitochondrial DNA confirms founder effect in invasive North American house finches (Carpodacus mexicanus). Conservation Genetics 9:637-643.
35. Hawley, D. M., A. K. Davis, and A. A. Dhondt. 2007a. Transmission-relevant behaviours shift with pathogen infection in wild house finches (Carpodacus mexicanus). Canadian Journal of Zoology 85: 752-757.
36. Hawley, D. M., K. V. Dhondt, A. P. Dobson, J. L. Grodio, W. M. Hochachka, D. H. Ley, E. E. Osnas, K. A. Schat, and A. A. Dhondt. 2010. Common garden experiment reveals pathogen isolate but no host genetic diversity effect on the dynamics of an emerging wildlife disease. Journal of Evolutionary Biology 23:1680-1688.
37. Hawley, D. M., S. E. DuRant, A. F. Wilson, J. S. Adelman, and W. A. Hopkins. 2012. Additive metabolic costs of thermoregulation and pathogen infection. Functional Ecology 26:701-710.
38. Hawley, D. M., and R. C. Fleischer. 2012. Contrasting epidemic histories reveal pathogen-mediated balancing selection on class II MHC diversity in a wild songbird. PLoS ONE 7:e30222.
39. Hawley, D. M., J. Grodio, S. Frasca Jr., L. Kirkpatrick, and D. H. Ley. 2011. Experimental infection of domestic canaries (Serinus canaria domestica) with Mycoplasma gallisepticum: a new model system for a wildlife disease. Avian Pathology 40:321-327.
40. Hawley, D. M., D. Hanley, A. A. Dhondt, and I. J. Lovette. 2006a. Molecular evidence for a founder effect in invasive house finch (Carpodacus mexicanus) populations experiencing an emergent disease epidemic. Molecular Ecology 15:263-275.
41. Hawley, D. M., C. S. Jennelle, K. V. Sydenstricker, and A. A. Dhondt. 2007b. Pathogen resistance and immunocompetence covary with social status in house finches (Carpodacus mexicanus). Functional Ecology 21:520-527.
42. Hawley, D. M., K. Lindström, and M. Wikelski. 2006b. Experimentally increased social competition compromises humoral immune responses in house finches. Hormones and Behavior 49:417-424.
43. Hochachka, W. M., and A. A. Dhondt. 2000. Density-dependent decline of host abundance resulting from a new infectious disease. I Proceedings of the National Academy of Sciences of the United States of America 97:5303-5306.
44. Janeway, C. A., P. Travers, M. Walport, and J. D. Capra. 2005. Immunobiology: the immune system in health and disease. 6th ed. Garland, New York. Javed, M. A., S. Frasca Jr., D. Rood, K. Cecchini, M. Gladd, S. J. Geary, and L. K. Silbart. 2005. Correlates of immune protection in chickens vaccinated with Mycoplasma gallisepticum strain GT5 following challenge with pathogenic M. gallisepticum strain Rlow. Infection and Immunity 73:5410-5419.
45. Jokela, J., P. Schmid-Hempel, and M. C. Rigby. 2000. Dr. Pangloss restrained by the Red Queen: steps towards a unified defence theory. Oikos 89:267-274.
46. Kjos, C. G., and W. W. Cochran. 1970. Activity of migrant thrushe s as determined by radio-telemetry. Wilson Bulletin 82:225-226.
47. Kluger, M. J. 1991. Fever: role of pyrogens andcryogens. Physiological Reviews 71:93-127.
48. Kollias, G. V, K. V. Sydenstricker, H. W. Kollias, D. H. Ley, P. R. Hosseini, V. Connolly, and A. A. Dhondt. 2004. Experimental infection of house finches with Mycoplasma gallisepticum. Journal of Wildlife Diseases 40:79-86.
49. Labocha, M. K., and J. P. Hayes. 2012. Morphometric indices of body condition in birds: a review. Journal of Ornithology 153:1-22.
50. Lazzaro, B. P., and T. J. Little. 2009. Immunity in a variable world. Philosophical Transactions of the Royal Society B: Biological Sci! ences 364:15-26.
51. Ley, D. H., J. E. Berkhoff, and J. M. McLaren. 1996. Mycoplasma gallisepticum isolated from house finches (Carpodacus mexicanus) with conjunctivitis. Avian Diseases 40:480-483.
52. Little, T. J., D. M. Shuker, N. Colegrave, T. Day, and A. L. Graham. 2010. The coevolution of virulence: tolerance in perspective. PLoS Pathogens 6:e1001006.
53. Lloyd-Smith, J. O., S. J. Schreiber, P. E. Kopp, and W. M. Getz. 2005. Superspreading and the effect of individual variation on disease emergence. Nature 438:355-359.
54. Long, G. H., and M. Boots. 2011. How can immunopathology shape the evolution of parasite virulence? Trends in Parasitology 27:300-305.
55. Long, G. H, B. H. K. Chan, J. E. Allen, A. F. Read, and A. L. Graham. 2006. Parasite genetic diversity does not influence TNF-mediated effects on the virulence of primary rodent malaria infections. Parasitology 133:673-684.
56. Long, G. H, B. H. K. Chan, J. E. Allen, A. F. Read, and A. L. Graham. 2008. Blockade of TNF receptor 1 reduces disease severity but increases parasite transmission during Plasmodium chabaudi chabaudi infection. International Journal for Parasitology 38:1073- I1081.
57. Lopes, P. C, J. Adelman, J. C. Wingfield, and G. E. Bentley 2012. Social context modulates sickness behavior. Behavioral Ecology™! and Sociobiology 66:1421-1428.
58. Luttrell, M. P., D. E. Stallknecht, J. R. Fischer, C. T Sewell, and S. H. Kleven. 1998. Natural Mycoplasma gallisepticum infection in a captive flock of house finches. Journal of Wildlife Diseases 34:289-296.
59. Mackinnon, M. J., and A. F. Read. 2004. Virulence in malaria: an evolutionary viewpoint. Philosophical Transactions of the Royal Society B: Biological Sciences 359:965-986.
60. Marais, M., S. K. Maloney, and D. A. Gray. 2011. The metabolic cost of fever in Pekin ducks. Journal of Thermal Biology 36:116-120.
61. Medzhitov, R. 2008. Origin and physiological roles of inflammation. Nature 454:428-435.
62. Meynell, G. C., and E. Meynell. 1970. Theory and practice in experimental bacteriology. 2nd ed. Cambridge University Press, Cambridge.
63. Miller, M. R., A. White, and M. Boots. 2006. The evolution of parasites in response to tolerance in their hosts: the good, the bad, and apparent commensalism. Evolution 60:945-956.
64. Mohammed, J., S. Frasca Jr., K. Cecchini, D. Rood, A. C. Nyaoke, S. J. Geary, and L. K. Silbart. 2007. Chemokine and cytokine gene expression profiles in chickens inoculated with Mycoplasma gal-lisepticum strains Rlow or GT5. Vaccine 25:8611-8621.
65. National Research Council. 2011. Guide for the care and use of laboratory animals. National Academies Press, Washington, DC.
66. Nolan, P. M., G. E. Hill, and A. M. Stoehr. 1998. Sex, size, and plumage redness predict house finch survival in an epidemic. Proceedings of the Royal Society B: Biological Sciences 265:961-965.
67. Pfennig, K. S. 2001. Evolution of pathogen virulence: the role of variation in host phenotype. Proceedings of the Royal Society B: Biological Sciences 268:755-760.
68. Pinheiro, J. C., and D. M. Bates. 2000. Mixed-effects models in S and S-PLUS. Springer, Berlin.
69. Poland, G. A., I. G. Ovsyannikova, and R. M. Jacobson. 2008. Im-munogenetics of seasonal influenza vaccine response. Vaccine 26S: D35-D40.
70. Råberg, L., A. L. Graham, and A. F. Read. 2009. Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society B: Biological Sciences 364:37-49.
71. Råberg, L., D. Sim, and A. F. Read. 2007. Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318:812-814.
72. Rausher, M. D. 2001. Co-evolution and plant resistance to natural enemies. Nature 411:857-864.
73. Razin, S., D. Yogev, and Y. Naot. 1998. Molecular biology and path-ogenicity of mycoplasmas. Microbiology and Molecular Biology Reviews 62:1094-1156.
74. R Development Core Team. 2010. R: a language and environment for statistical computing, version 2.11.0. R Foundation for Statistical Computing, Vienna.
75. Restif, O., and J. C. Koella. 2003. Shared control of epidemiological traits in a coevolutionary model of host-parasite interactions. American Naturalist 161:827-836.
76. Restif, O., and J. C. Koella. 2004. Concurrent evolution of resistance and tolerance to pathogens. American Naturalist 164:E90-E102.
77. Rohr, J. R., T. R. Raffel, and C. A. Hall. 2010. Developmental variation in resistance and tolerance in a multi-host-parasite system. Functional Ecology 24:1110-1121.
78. Rolff, J., and M. T. Siva-Jothy. 2003. Invertebrate ecological immunology. Science 301:472-475.
79. Roy, B. A., and J. W. Kirchner. 2000. Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54:51-63.
80. Savage, A. E., and K. R. Zamudio. 2011. MHC genotypes associate with resistance to a frog-killing fungus. Proceedings of the National Academy of Sciences of the USA 108:16705-16710.
81. Schmid-Hempel, P. 2011. Evolutionary parasitology: the integrated study of infections, immunology, ecology, and genetics. Oxford University Press, Oxford.
82. Sears, B. F., J. R. Rohr, J. E. Allen, and L. B. Martin. 2011. The economy of inflammation: when is less more? Trends in Parasi-tology 27:382-387.
83. Sydenstricker, K. V., A. A. Dhondt, D. M. Hawley, C. S. Jennelle, H. W. Kollias, and G. V. Kollias. 2006. Characterization of experimental Mycoplasma gallisepticum infection in captive house finch flocks. Avian Diseases 50:39-44.
84. Tobler, U., and B. R. Schmidt. 2010. Within- and among-population variation in chytridiomycosis-induced mortality in the toad Alytes obstetricans. PLoS ONE 5:e10927.
85. Viney, M. E., E. M. Riley, and K. L. Buchanan. 2005. Optimal immune responses: immunocompetence revisited. Trends in Ecology and Evolution 20:665-669.
86. Vollmer-Conna, U., B. F. Piraino, B. Cameron, T. Davenport, I. Hickie, D. Wakefield, and A. R. Lloyd. 2008. Cytokine polymorphisms have a synergistic effect on severity of the acute sickness response to infection. Clinical Infectious Diseases 47:1418-1425.
87. Woodworth, B. L., C. T. Atkinson, D. A. LaPointe, P. J. Hart, C. S. Spiegel, E. J. Tweed, C. Henneman, et al. 2005. Host population persistence in the face of introduced vector-borne diseases: Hawaii amakihi and avian malaria. Proceedings of the National Academy of Sciences of the USA 102:1531-1536.