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Dose and host characteristics influence virulence of ranavirus infections

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Abstract

Parasites play a prominent role in the ecology, evolution, and more recently, conservation of many organisms. For example, emerging infectious diseases, including a group of lethal ranaviruses, are associated with the declines and extinctions of amphibians around the world. An increasingly important basic and applied question is: what controls parasite virulence? We used a dose-response experiment with three laboratory-bred clutches of tiger salamander larvae (Ambystoma tigrinum) to test how the size of inoculum and host genetic factors influence the dynamics and outcome of ranavirus infections. We found that infection rates increased with dose and were strongly affected by clutch identity and host life history stage. Case mortality increased with dose of inoculum, but was unaffected by host characteristics. Average survival time decreased with dose and differed among clutches, but this was largely due to differences in the time to onset of symptoms. Overall, our results suggest that dose of inoculum and host characteristics (life history stage and genetic background) influence the establishment and early virus replication, and therefore the virulence of ranavirus infections.

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References

  • Arthurs S, Thomas MB (2001) Effect of dose, pre-mortem host incubation temperature and thermal behaviour on host mortality, mycosis and sporulation of Metarhizium anisopliae var. acridum in Schistocerca gregaria. Biocontrol Sci Technol 11:411–420

    Article  Google Scholar 

  • van Beek NAM, Wood HA, Hughes PR (1988) Quantitative aspects of nuclear polyhedrosis virus infections in lepidopterous larvae: the dose–survival time relationship. J Invertebr Pathol 51:58–63

    Article  Google Scholar 

  • van Beek N, Hughes PR, Wood HA (2000) Effects of incubation temperature on the dose–survival time relationship of Trichoplusia ni larvae infected with Autographa californica nucleopolyhedrovirus. J Invertebr Pathol 76:185–190

    Article  PubMed  Google Scholar 

  • Bollinger TK, Mao J, Schock D, Brigham RM, Chinchar VG (1999) Pathology, isolation, and preliminary molecular characterization of a novel iridovirus from tiger salamanders in Saskatchewan. J Wildl Dis 35:413–429

    PubMed  CAS  Google Scholar 

  • Brunner JL, Schock DM, Collins JP, Davidson EW (2004) The role of an intraspecific reservoir in the persistence of a lethal ranavirus. Ecology 85:560–566

    Article  Google Scholar 

  • Carey C, Cohen N, Rollins-Smith L (1999) Amphibian declines: an immunological perspective. Dev Comp Immunol 23:459–472

    Article  PubMed  CAS  Google Scholar 

  • Chotivanich K, Udomsangpetch R, Simpson JA, Newton P, Pukrittayakamee S, Looareesuwan S, White NJ (2000) Parasite multiplication potential and the severity of falciparum malaria. J Infect Dis 181:1206–1209

    Article  PubMed  CAS  Google Scholar 

  • Cleaveland S, Laurenson MK, Taylor LH (2001) Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Philos Trans R Soc Lond Ser B Biol Sci 356:991–999

    Article  CAS  Google Scholar 

  • Cohen N (1969) Immunogenetic and developmental aspects of tissue transplantation immunity in Urodele amphibians. In: Mizell M (ed) Biology of amphibian tumors. Springer, Berlin Heidelberg New York, pp 153–168

    Google Scholar 

  • Collins JP, Jones TR, Berna HJ (1988) Conserving genetically-distinctive populations: the case of the Huachuca tiger salamander (Ambystoma tigrinum stebbinsi Lowe). In: Szaro RC, Severson KC, Patton DR (eds) Management of amphibians, reptiles, and small mammals in North America, vol GTR-RM-166. USDA Forest Service, Rocky Mountain Forest and Range Experiment Station, Fort Collins, pp 45–53

    Google Scholar 

  • Collins JP, Brunner JL, Miera V, Parris MJ, Schock DM, Storfer S (2003) Ecology and evolution of infectious disease. In: Semlitsch R (ed) Amphibian conservation. Smithsonian Institution Press, Washington, pp 137–151

    Google Scholar 

  • Collins JP, Brunner JL, Jancovich J, Schock DM (2004) A model host-pathogen system for studying infectious disease dynamics in amphibians: tiger salamanders (Ambystoma tigrinum) and Ambystoma tigrinum virus. Herpetol J 14:195–200

    Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop 78:103–116

    Article  PubMed  CAS  Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2003) Infectious disease and amphibian population declines. Divers Distrib 9:141–150

    Article  Google Scholar 

  • Day T (2002a) The evolution of virulence in vector-borne and directly transmitted parasites. Theor Popul Biol 62:199–213

    Article  PubMed  Google Scholar 

  • Day T (2002b) On the evolution of virulence and the relationship between various measures of mortality. Proc R Soc Lond Ser B Biol Sci 269:1317–1323

    Article  Google Scholar 

  • Day T (2002c) Virulence evolution via host exploitation and toxin production in spore-producing pathogens. Ecol Lett 5:471–476

    Article  Google Scholar 

  • Diffley P, Scott JO, Mama K, Tsen TNR (1987) The rate of proliferation among African trypanosomes is a stable trait that is directly related to virulence. Am J Trop Med Hyg 36:533–540

    PubMed  CAS  Google Scholar 

  • Dobson A, Foufopoulos J (2001) Emerging infectious pathogens of wildlife. Philos Trans R Soc Lond Ser B Biol Sci 356:1001–1012

    Article  CAS  Google Scholar 

  • Dybdahl MF, Storfer A (2003) Parasite local adaptation: Red Queen versus Suicide King. Trends Ecol Evol 18:523–530

    Article  Google Scholar 

  • Ebert D (1999) The evolution and expression of parasite virulence. In: Stearns SC (ed) Evolution in health and disease. Oxford University Press, New York, pp 161–172

    Google Scholar 

  • Ebert D, Zschokke-Rohringer CD, Carius HJ (2000) Dose effects and density-dependent regulation of two microparasites of Daphnia magna. Oecologia 122:200–209

    Article  Google Scholar 

  • Elliott SL, Blanford S, Thomas MB (2002) Host–pathogen interactions in a varying environment: temperature, behavioural fever and fitness. Proc R Soc Lond Ser B Biol Sci 269:1599–1607

    Article  Google Scholar 

  • Ewald PW (1991) Waterborne transmission and the evolution of virulence among gastrointestinal bacteria. Epidemiol Infect 106:83–119

    PubMed  CAS  Google Scholar 

  • Friend M, McLean RG, Dein FJ (2001) Disease emergence in birds: challenges for the twenty-first century. Auk 118:290–303

    Article  Google Scholar 

  • Galvani AP (2003) Epidemiology meets evolutionary ecology. Trends Ecol Evol 18:132–139

    Article  Google Scholar 

  • Gibbons JW, Scott DE, Ryan TJ, Buhlmann KA, Tuberville TD, Metts BS, Greene JL, Mills T, Leiden Y, Poppy S, Winne CT (2000) The global decline of reptiles, Deja Vu amphibians. Bioscience 50:653–666

    Article  Google Scholar 

  • Green DE, Converse KA, Schrader AK (2002) Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996–2001. Ann N Y Acad Sci 969:323–339

    Article  PubMed  Google Scholar 

  • Hochberg ME (1991) Intra-host interactions between a braconid endoparasitoid, Apanteles glomeratus, and a baculovirus for larvae of Pieris brassicae. J Anim Ecol 60:51–63

    Article  Google Scholar 

  • Jancovich JK, Davidson EW, Morado JF, Jacobs BL, Collins JP (1997) Isolation of a lethal virus from the endangered tiger salamander Ambystoma tigrinum stebbinsi. Dis Aquat Organ 31:161–167

    Article  Google Scholar 

  • Jancovich JK, Davidson EW, Seiler A, Jacobs BL, Collins JP (2001) Transmission of the Ambystoma tigrinum virus to alternate hosts. Dis Aquat Organ 46:159–163

    Article  PubMed  CAS  Google Scholar 

  • Koella JC, Agnew P (1999) A correlated response of a parasite’s virulence and life cycle to selection on its host’s life history. J Evol Biol 12:70–79

    Article  Google Scholar 

  • Mackinnon MJ, Read AF (1999) Selection for high and low virulence in the malaria parasite Plasmodium chabaudi. Proc R Soc Lond Ser B Biol Sci 266:741–748

    Article  CAS  Google Scholar 

  • Mao J, Tham TN, Gentry GA, Aubertin A, Chinchar VG (1996) Cloning, sequence analysis, and expression of the major capsid protein of the iridovirus frog virus 3. Virology 216:431–436

    Article  PubMed  CAS  Google Scholar 

  • Morand S, Poulin R (2000) Optimal time to patency in parasitic nematodes: host mortality matters. Ecol Lett 3:186–190

    Article  Google Scholar 

  • Prybylski D, Khaliq A, Fox E, Sarwari AR, Strickland GT (1999) Parasite density and malaria morbidity in the Pakistani Punjab. Am J Trop Med Hyg 61:791–801

    PubMed  CAS  Google Scholar 

  • Rollins-Smith LA (1998) Metamorphosis and the amphibian immune system. Immunol Rev 166:221–230

    Article  PubMed  CAS  Google Scholar 

  • Sabelis MW, Metz JAJ (2002) Taking stock: relating theory to experiment. In: Dieckmann U, Metz JAJ, Sabelis MW, Sigmund K (eds) Adaptive dynamics of infectious diseases: in pursuit of virulence management. Cambridge University Press, New York, pp 379–398

    Google Scholar 

  • Straley SC, Perry RD (1995) Environmental modulation of gene-expression and pathogenesis in Yersinia. Trends Microbiol 3:310–317

    Article  PubMed  CAS  Google Scholar 

  • Timms R, Colegrave N, Chan BHK, Read AF (2001) The effect of parasite dose on disease severity in the rodent malaria Plasmodium chabaudi. Parasitology 123:1–11

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported in part by NSF IRCEB (Integrated Research Challenges in Environmental Biology) grant #DEB 0213851 to JPC and 22 collaborators, and by an NSF Doctoral Dissertation Improvement grant #DEB 0309099 to JLB. Animal experiments were approved under ASU animal care protocols 99-526R and 03-670R and comply with the current laws of the United States of America. Thanks also to Thomas Dowling and Ann Kelsen for help with PCR, and to V. Gregory Chinchar, Nicholas Cohen, Elizabeth Davidson, Stanley Faeth, Amy Greer, Angela Picco, Richard Retallick, and two anonymous reviewers for helpful comments and suggestions that significantly improved this manuscript.

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Authors and Affiliations

  1. School of Life Sciences, Arizona State University, Tempe, AZ, 85287-4501, USA

    Jesse L. Brunner, Kathryn Richards & James P. Collins

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  1. Jesse L. Brunner
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  2. Kathryn Richards
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  3. James P. Collins
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Correspondence to Jesse L. Brunner.

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Communicated by Carla Caceres

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Brunner, J.L., Richards, K. & Collins, J.P. Dose and host characteristics influence virulence of ranavirus infections. Oecologia 144, 399–406 (2005). https://doi.org/10.1007/s00442-005-0093-5

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  • DOI: https://doi.org/10.1007/s00442-005-0093-5

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