Environmental dependency of amphibian-ranavirus genotypic interactions: Evolutionary perspectives on infectious diseases

Evolutionary Applications

Volumn 7, Issue 7, 2014, Pages 723-733

  Echaubard, Pierre ^a   Leduc, Joel ^a   Pauli, Bruce ^b   Chinchar, V Gregory ^c   Robert, Jacques ^d   Lesbarrères, David ^a  

^a LAURENTIAN UNIVERSITY   (Canada)

^b CARLETON UNIVERSITY   (Canada)

^c UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Genotype genotype environment interactions; Host pathogen interactions; Lithobates pipiens; Lithobates sylvaticus; Ranavirus

Indexed keywords

EID: 84906688865     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12169     Document Type: Article

References (75)

1. Altizer, S., D. Harvell, and E. Friedle 2003. Rapid evolutionary dynamics and disease threats to biodiversity. Trends in Ecology & Evolution 18:589-596.
2. Altizer, S., R. S. Ostfeld, P. T. J. Johnson, S. Kutz, and C. D. Harvell 2013. Climate change and infectious diseases: from evidence to a predictive framework. Science 341:514-519.
3. Antia, R., R. R. Regoes, J. C. Koella, and C. T. Bergstrom 2003. The role of evolution in the emergence of infectious diseases. Nature 426:658-661.
4. Balseiro, A., K. P. Dalton, A. del Cerro, I. Márquez, F. Parra, J. M. Prieto, and R. Casais 2010. Outbreak of common midwife toad virus in alpine newts (Mesotriton Alpestris Cyreni) and common midwife toads (Alytes Obstetricans) in Northern Spain: a comparative pathological study of an emerging ranavirus. Veterinary Journal 186:256-258.
5. Bayley, A. E., J. H. Barry, and S. W. Feist 2013. Susceptibility of the European common frog Rana Temporaria to a Panel of ranavirus isolates from fish and amphibian hosts. Diseases of Aquatic Organisms 103:171-183.
6. Bedhomme, S., P. Agnew, C. Sidobre, and Y. Michalakis 2004. Virulence reaction norms across a food gradient. Proceedings of the Royal Society B: Biological Sciences 271:739-744.
7. Berven, K. A. 1982. The genetic basis of altitudinal variation in the wood frog Rana Sylvatica. I. an experimental analysis of life history traits. Evolution 36:962-983.
8. Binder, S., A. M. Levitt, J. J. Sacks, and J. M. Hughes 1999. Emerging infectious diseases: public health issues for the 21st century. Science 284:1311-1313.
9. Bly, J. E., L. A. Lawson, A. J. Szalai, and L. W. Clem 1993. Environmental factors affecting outbreaks of winter saprolegniosis in channel catfish, Ictalurus Punctatus (Rafinesque). Journal of Fish Diseases 16:541-549.
10. Burdon, J. J., and P. H. Thrall 2009. Coevolution of plants and their pathogens in natural habitats. Science 324:755-756.
11. Byrne, P. G., and J. D. Roberts 2000. Does multiple paternity improve fitness of the frog Crinia Georgiana? Evolution 54:968-973.
12. Casadevall, A., and L. A. Pirofski 1999. Host-pathogen interactions: redefining the basic concepts of virulence and pathogenicity. Infection and Immunity 67:3703-3713.
13. Chinchar, V. G., A. Hyatt, T. Miyazaki, and T. Williams 2009. Family iridoviridae: poor viral relations no longer. In J. L. Van Etten, ed. Lesser Known Large dsDNA Viruses, pp. 123-170. Springer-Verlag, Berlin Heidelberg.
14. Cohen, M. L. 2000. Changing patterns of infectious disease. Nature 406:762-767.
15. Collins, J. P., and A. Storfer 2003. Global amphibian declines: sorting the hypotheses. Diversity and Distributions 9:89-98.
16. Cousyn, C., L. De Meester, J. K. Colbourne, L. Brendonck, D. Verschuren, and F. Volckaert 2001. Rapid, local adaptation of zooplankton behavior to changes in predation pressure in the absence of neutral genetic changes. Proceedings of the National Academy of Sciences 98:6256-6260.
17. Daskin, J. H., and R. A. Alford 2012. Context-dependent symbioses and their potential roles in wildlife diseases. Proceedings of the Royal Society B: Biological Sciences 279:1457-1465.
18. Daszak, P., A. A. Cunningham, and A. D. Hyatt 2000. Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 287:443-449.
19. De Castro, F., and B. Bolker 2005. Mechanisms of disease-induced extinction. Ecology Letters 8:117-126.
20. Du, H. H., W. F. Li, Z. R. Xu, and Z. S. Kil 2006. Effect of hyperthermia on the replication of white spot syndrome virus (WSSV) in Procambarus Clarkii. Diseases of Aquatic Organisms 71:175.
21. Du, H., W. Dai, X. Han, W. Li, Y. Xu, and Z. Xu 2008. Effect of low water temperature on viral replication of white spot syndrome virus in Procambarus Clarkii. Aquaculture 277:149-151.
22. Duffus, A. L. J., B. D. Pauli, K. Wozney, C. R. Brunetti, and M. Berrill 2008. Frog virus 3-like infections in aquatic amphibian communities. Journal of Wildlife Diseases 44:109-120.
23. Echaubard, P. 2012. Evolution and Ecology of an Amphibian Emerging Infectious Disease: a Context-dependant Approach of Ranavirus Virulence in Lithobates (Rana) Pipiens. PhD Thesis, Laurentian University, Sudbury, ON.
24. Echaubard, P., K. Little, B. D. Pauli, and D. Lesbarrères 2010. Context-dependent effects of ranaviral infection on northern leopard frog life history traits. PLoS One 5:e13723.
25. Essani, K., R. Goorha, and A. Granoff 1987. Mutation in a DNA-binding protein reveals an association between DNA-methyltransferase activity and a 26, 000-Da polypeptide in frog virus 3-infected cells. Virology 161:211-217.
26. Gahl, M. K., and A. J. K. Calhoun 2008. Landscape setting and risk of ranavirus mortality events. Biological Conservation 141:2679-2689.
27. Gantress, J., G. D. Maniero, N. Cohen, and J. Robert 2003. Development and characterization of a model system to study amphibian immune responses to iridoviruses. Virology 311:254-262.
28. Ghosh, S., and S. Bhattacharyya 2007. Effect of temperature on viral infection and its control: a mathematical approach. Journal of Theoretical Biology 247:50-63.
29. Gosner, K. L. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183-190.
30. Granoff, A., P. E. Came, and K. A. Rafferty 1965. The isolation and properties of viruses from Rana pipiens: their possible relationship to the renal adenocarcinoma of the leopard frog. Annals of the New York Academy of Science 126:237-255.
31. Gray, M. J., D. L. Miller, and J. T. Hoverman 2009. Ecology and pathology of amphibian ranaviruses. Diseases of Aquatic Organisms 87:243-266.
32. Greer, A. L., M. Berrill, and P. J. Wilson 2005. Five amphibian mortality events associated with ranavirus infection in South Central Ontario, Canada. Diseases of Aquatic Organisms 67:9-14.
33. Herreid, C. F. II, and S. Kinney 1967. Temperature and development of the wood frog, Rana Sylvatica, in Alaska. Ecology 48:579-590.
34. Hoverman, J. T., M. J. Gray, and D. L. Miller 2010. Anuran susceptibilities to ranaviruses: role of species identity, exposure route, and a novel virus isolate. Diseases of Aquatic Organisms 89:97-107.
35. Hoverman, J. T., M. J. Gray, N. A. Haislip, and D. L. Miller 2011. Phylogeny, life history, and ecology contribute to differences in amphibian susceptibility to ranaviruses. EcoHealth 8:301-319.
36. Hudson, P., and J. Greenman 1998. Competition mediated by parasites: biological and theoretical progress. Trends in Ecology & Evolution 13:387-390.
37. Hyatt, A., A. Gould, Z. Zupanovic, A. Cunningham, S. Hengstberger, R. Whittington, J. Kattenbelt et al. 2000. Comparative studies of piscine and amphibian iridoviruses. Archives of Virology 145:301-331.
38. Jancovich, J. K., V. G. Chinchar, A. Hyatt, T. Miyazaki, T. Williams, and Q. Y. Zhang 2012. Family Iridoviridae. In A. M. Q. King, M. J. Adams, E. B. Carstens, and E. B. Lefkowitz, eds. Family Iridoviridae, Virus Taxonomy: 9th Report of the ICTV, pp. 193-210. Elsevier, San Diego, CA.
39. Johnson, P. T. J., E. Kellermanns, and J. Bowerman 2011. Critical windows of disease risk: amphibian pathology driven by developmental changes in host resistance and tolerance. Functional Ecology 25:726-734.
40. Johnson, P. T. J., D. L. Preston, J. T. Hoverman, J. S. Henderson, S. H. Paull, K. L. D. Richgels, and M. D. Redmond 2012. Species diversity reduces parasite infection through cross-generational effects on host abundance. Ecology 93:56-64.
41. Johnson, P. T. J., D. L. Preston, J. T. Hoverman, and K. L. D. Richgels 2013. Biodiversity decreases disease through predictable changes in host community competence. Nature 494:230-233.
42. Keesing, F., R. D. Holt, and R. S. Ostfeld 2006. Effects of species diversity on disease risk. Ecology Letters 9:485-498.
43. Kerby, J. L., A. J. Hart, and A. Storfer 2011. Combined effects of virus, pesticide, and predator cue on the larval tiger salamander (Ambystoma Tigrinum). EcoHealth 8:46-54.
44. Kluger, M. J., W. Kozak, C. A. Conn, L. R. Leon, and D. Soszynski 1998. Role of fever in disease. Annals of the New York Academy of Sciences 856:224-233.
45. Lambrechts, L., S. Fellous, and J. C. Koella 2006. Coevolutionary interactions between host and parasite genotypes. Trends in Parasitology 22:12-16.
46. Laugen, A. T., A. Laurila, K. Räsänen, and J. Merilä 2003. Latitudinal countergradient variation in the common frog (Rana Temporaria) development rates-evidence for local adaptation. Journal of Evolutionary Biology 16:996-1005.
47. Lazzaro, B. P., and T. J. Little 2009. Immunity in a variable world. Philosophical Transactions of the Royal Society B: Biological Sciences 364:15-26.
48. Lesbarrères, D., A. Balseiro, J. Brunner, V. G. Chinchar, A. Duffus, J. Kerby, D. L. Miller et al. 2012. Ranavirus: past, present and future. Biology Letters 8:481-483.
49. Leung, K. M., R. M. Elashoff, and A. A. Afifi 1997. Censoring issues in survival analysis. Annual Review of Public Health 18:83-104.
50. MacPhee, R. D. E., and A. D. Greenwood 2013. Infectious disease, endangerment, and extinction. International Journal of Evolutionary Biology Volume 2013, Article ID 571939, 9 pages.
51. Mao, J., R. P. Hedrick, and V. G. Chinchar 1997. Molecular characterization, sequence analysis, and taxonomic position of newly isolated fish iridoviruses. Virology 229:212-220.
52. Miller, D. L., M. J. Gray, and A. Storfer 2011. Ecopathology of ranaviruses infecting amphibians. Viruses 3:2351-2373.
53. Miller, K. M., A. Teffer, S. Tucker, S. Li, A. D. Schultze, M. Trudel, F. Juanes et al. 2014. Infectious disease, shifting climates and opportunistic predators: cumulative factors potentially impacting wild salmon declines. Evolutionary Applications 7:812-855.
54. Mitchell, S. E., E. S. Rogers, T. J. Little, and A. F. Read 2005. Host-parasite and genotype by environment interactions: temperature modifies potential for selection by sterilizing pathogen. Evolution 59:70-80.
55. Morens, D. M., G. K. Folkers, and A. S. Fauci 2004. The challenge of emerging and re-emerging infectious diseases. Nature 430:242-249.
56. Morrison, E. A., S. Garner, P. Echaubard, D. Lesbarrères, C. J. Kyle, and C. R. Brunetti 2014. Complete genome analysis of a frog virus 3 (FV3) isolate and sequence comparison with isolates of differing levels of virulence. Virology Journal 11:46.
57. Pedersen, A. B., and A. Fenton 2007. Emphasizing the ecology in parasite community ecology. Trends in Ecology & Evolution 22:133-139.
58. Plowright, R. K., S. H. Sokolow, M. E. Gorman, P. Daszak, and J. E. Foley 2008. Causal inference in disease ecology: investigating ecological drivers of disease emergence. Frontiers in Ecology and the Environment 6:420-429.
59. R Core Team (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/ (accessed on 23 May 2014).
60. Ribeiro, H. C. T., and O. H. O. Pavan 1994. Effect of temperature on the development of baculoviruses. Journal of Applied Entomology 118:316-320.
61. Ridenhour, B. J., and A. T. Storfer 2008. Geographically variable selection in Ambystoma Tigrinum Virus (Iridoviridae) throughout the Western USA. Journal of Evolutionary Biology 21:1151-1159.
62. Robert, J., C. Guiet, and L. Du Pasquier 1995. Ontogeny of the alloimmune response against a transplanted tumor in Xenopus Laevis. Differentiation 59:135-144.
63. Robert, J., H. Morales, W. Buck, N. Cohen, S. Marr, and J. Gantress 2005. Adaptive immunity and histopathology in frog virus 3-infected Xenopus. Virology 332:667-675.
64. Rojas, S., K. Richards, J. K. Jancovich, and E. W. Davidson 2005. Influence of temperature on ranavirus infection in larval salamanders Ambystoma Tigrinum. Diseases of Aquatic Organisms 63:95-100.
65. Schock, D. M., T. K. Bollinger, V. G. Chinchar, J. K. Jancovich, and J. P. Collins 2008. Experimental evidence that amphibian ranaviruses are multi-host pathogens. Copeia 2008:133-143.
66. Stairs, G. R. 1978. Effects of a wide range of temperatures on the development of Galleria Mellonella and its specific Baculovirus. Environmental Entomology 7:297-299.
67. Storey, K. B., and J. M. Storey 1984. Biochemical adaptation for freezing tolerance in the wood frog, Rana sylvatica. Journal of Comparative Physiology 155:29-36.
68. Teacher, A. G. F., T. W. J. Garner, and R. A. Nichols 2009. Evidence for directional selection at a novel major histocompatibility class i marker in wild common frogs (Rana Temporaria) exposed to a viral pathogen (ranavirus). PLoS One 4:e4616.
69. Tétard-Jones, C., M. A. Kertesz, P. Gallois, and R. F. Preziosi 2007. Genotype-by-genotype interactions modified by a third species in a plant-insect system. American Naturalist 170:492-499.
70. Thomas, M. B., and S. Blanford 2003. Thermal biology in insect-parasite interactions. Trends in Ecology & Evolution 18:344-350.
71. Thompson, J. N. 2005. The Geographic Mosaic of Coevolution. University of Chicago Press, Chicago.
72. Vale, P. F., and T. J. Little 2009. Measuring parasite fitness under genetic and thermal variation. Heredity 103:102-109.
73. Wabl, M. R., and L. Du Pasquier 1976. Antibody patterns in genetically identical frogs. Nature 264:642-644.
74. Wang, J. W., R. Q. Deng, X. Z. Wang, Y. S. Huang, K. Xing, J. H. Feng, J. G. He et al. 2003. Cladistic analysis of iridoviruses based on protein and DNA sequences. Archives of Virology 148:2181-2194.
75. Wolinska, J., and K. C. King 2009. Environment can alter selection in host-parasite interactions. Trends in Parasitology 25:236-244.