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

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.

Evolved pesticide tolerance influences susceptibility to parasites in amphibians

“…Average final survival varied minimally across the populations (0% to 4.7%) suggesting that all populations, regardless of pesticide tolerance mechanism, were highly susceptible to ranavirus. This is consistent with past work demonstrating that wood frogs are one of the most susceptible amphibian species to ranavirus infection (Hoverman et al., 2011). Given the limited variability in survival across the populations, it is not surprising that we did not find a relationship with the mechanism of pesticide tolerance.…”

“…Although average TTD across the 14 populations varied more than survival (TTD ranging from 190 to 224 hr), we still did not find a relationship between the mechanism of pesticide tolerance and susceptibility to ranavirus. Amphibian species with intermediate levels of susceptibility to ranavirus (e.g., hylids; Hoverman et al., 2011) may be better suited to address our hypotheses regarding the interaction with evolved pesticide tolerance because there is the potential for more variation in survival rates. However, wood frogs are the only amphibian species that has been examined for patterns in evolved pesticide tolerance.…”

“…Ranavirus can lead to host mortality by initiating cell death within the liver, kidney, and spleen (Gray, Miller, & Hoverman, 2009; Jancovich, Qin, Zhang, & Chinchar, 2015). Wood frogs are one of the most susceptible amphibian species to ranavirus (Hoverman, Gray, Haislip, & Miller, 2011). …”

“…Eleven days after the addition of the virus, we assessed final survival, euthanized all surviving tadpoles using a MS‐222 overdose and preserved tadpoles in 70% EtOH to quantify viral load. We chose 11 days for the ranavirus exposure because past work has shown that this time period is sufficient to observe disease outcomes (infection and mortality) in wood frog tadpoles (Hoverman et al., 2011). …”

Design and Analysis of Ranavirus Studies: Surveillance and Assessing Risk

“…For example, if experimental exposures show that a species dies rapidly following ranavirus exposure, then high prevalence would be most consistent with sampling during the peak of an epidemic. Several studies have reported species-level susceptibility under controlled conditions (e.g., Hoverman et al 2011;Brenes et al 2014b;Brunner et al 2015). Biological context also can be gleaned from the density of the population and the timing of the survey relative to the phenology of the organism.…”