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Phylogeny, Life History, and Ecology Contribute to Differences in Amphibian Susceptibility to Ranaviruses

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Abstract

Research that identifies the potential host range of generalist pathogens as well as variation in host susceptibility is critical for understanding and predicting the dynamics of infectious diseases within ecological communities. Ranaviruses have been linked to amphibian die-off events worldwide with the greatest number of reported mortality events occurring in the United States. While reports of ranavirus-associated mortality events continue to accumulate, few data exist comparing the relative susceptibility of different species. Using a series of laboratory exposure experiments and comparative phylogenetics, we compared the susceptibilities of 19 amphibian species from two salamander families and five anurans families for two ranavirus isolates: frog virus 3 (FV3) and an FV3-like isolate from an American bullfrog culture facility. We discovered that ranaviruses were capable of infecting 17 of the 19 larval amphibian species tested with mortality ranging from 0 to 100%. Phylogenetic comparative methods demonstrated that species within the anuran family Ranidae were generally more susceptible to ranavirus infection compared to species from the other five families. We also found that susceptibility to infection was associated with species that breed in semi-permanent ponds, develop rapidly as larvae, and have limited range sizes. Collectively, these results suggest that phylogeny, life history characteristics, and habitat associations of amphibians have the potential to impact susceptibility to ranaviruses.

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Acknowledgments

We thank the University of Georgia Veterinary Diagnostic and Investigational Laboratory, University of Tennessee Institute of Agriculture, and Tennessee Wildlife Resources Agency (TWRA) for funding this study. We thank C. Baldwin and D. Ingram for providing the virus isolate; N. Hilzinger and L. Whittington for conducting the PCR; and J. Hodges, B. Simpson, M. Campbell, and R. Long for various resources at JARTU. We also thank R. Relyea, J. Hammond, and J. Davenport for providing several species for the experiments. P. Stephens provided insightful comments on the phylogenetic methods. The P. Johnson Lab at the University of Colorado provided helpful feedback on initial drafts of the manuscript. We thank J. Rohr and several anonymous reviewers for helpful comments on the manuscript. All animal husbandry and euthanasia procedures followed an approved University of Tennessee IACUC protocol (#1755). Collection of egg masses was approved by the TWRA (Scientific Collection Permit #1990).

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309, USA

    Jason T. Hoverman

  2. Center for Wildlife Health, Department of Forestry, Wildlife, and Fisheries, University of Tennessee, Knoxville, USA

    Jason T. Hoverman, Matthew J. Gray, Nathan A. Haislip & Debra L. Miller

  3. Veterinary Diagnostic and Investigational Laboratory, College of Veterinary Medicine, University of Georgia, Georgia, TN, USA

    Debra L. Miller

  4. Department of Ectotherms, Fort Worth Zoo, Fort Worth, TX, USA

    Nathan A. Haislip

  5. Department of Biomedical and Diagnostic Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, TN, USA

    Debra L. Miller

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  1. Jason T. Hoverman
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Correspondence to Jason T. Hoverman.

Appendix

Appendix

See Tables 1, 2, 3, and 4; Figures 4, 5, and 6.

Figure 4
figure 4

Survival curves for wood frog (a), gopher frog (b), southern leopard frog (c), northern leopard frog (d), pickerel frog (e), green frog (f), and American bullfrog (g) tadpoles exposed to three ranavirus treatments. Tadpoles were exposed to virus-free media (Control), frog virus 3 (FV3), or an FV3-like isolate from a Georgia ranaculture facility (RI). For each treatment, n = 20 tadpoles.

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Figure 5
figure 5

Survival curves for western chorus frog (a), upland chorus frog (b), mountain chorus frog (c), Cope’s gray tree frog (d), eastern narrow-mouthed toad (e), American toad (f), and eastern spadefoot (g) tadpoles exposed to three ranavirus treatments. Tadpoles were exposed to virus-free media (Control), frog virus 3 (FV3), or an FV3-like isolate from a Georgia ranaculture facility (RI). For each treatment, n = 20 tadpoles.

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Figure 6
figure 6

Survival curves for tiger salamander (a), marbled salamander (b), spotted salamander (c), mole salamander (d), and red-spotted newt (e) larvae exposed to three ranavirus treatments. Larvae were exposed to virus-free media (Control), frog virus 3 (FV3), or an FV3-like isolate from a Georgia ranaculture facility (RI). For each treatment, n = 20 larvae except for the tiger salamander control treatment, which contained n = 7.

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Hoverman, J.T., Gray, M.J., Haislip, N.A. et al. Phylogeny, Life History, and Ecology Contribute to Differences in Amphibian Susceptibility to Ranaviruses. EcoHealth 8, 301–319 (2011). https://doi.org/10.1007/s10393-011-0717-7

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