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

Abstract

The context-dependent investigations of host-pathogen genotypic interactions, where environmental factors are explicitly incorporated, allow the assessment of both coevolutionary history and contemporary ecological influences. Such a functional explanatory framework is particularly valuable for describing mortality trends and identifying drivers of disease risk more accurately. Using two common North American frog species (Lithobates pipiens and Lithobates sylvaticus) and three strains of frog virus 3 (FV3) at different temperatures, we conducted a laboratory experiment to investigate the influence of host species/genotype, ranavirus strains, temperature, and their interactions, in determining mortality and infection patterns. Our results revealed variability in host susceptibility and strain infectivity along with significant host-strain interactions, indicating that the outcome of an infection is dependent on the specific combination of host and virus genotypes. Moreover, we observed a strong influence of temperature on infection and mortality probabilities, revealing the potential for genotype-genotype-environment interactions to be responsible for unexpected mortality in this system. Our study thus suggests that amphibian hosts and ranavirus strains genetic characteristics should be considered in order to understand infection outcomes and that the investigation of coevolutionary mechanisms within a context-dependent framework provides a tool for the comprehensive understanding of disease dynamics.

Keywords: Lithobates pipiens; Lithobates sylvaticus; genotype–genotype–environment interactions; host–pathogen interactions; ranavirus..

Figure 1

Interaction plot showing average probability of infection (±SE) for all nine combinations of the three host genotypes and three ranavirus strains (azacR = solid line and circles; SsMeV = dotted line and triangles; wt-FV3 = dashed line and squares; n = 36 ± 3.09 on average per combination), at 22°C (A) and 14°C (B).

Figure 2

(A) Probability of death over time for azacR, SsMeV, wt-FV3 and control treatments at 14°C and 22°C illustrating strain × temperature interactions (n = 49 ± 3.72 on average per strain-temperature combination). (B) Interaction plot showing average probability of death (±SE) per strain-temperature combination. The complement of the Kaplan–Meier estimate was used to estimate the probability of death.

Figure 3

(A) Probability of death over time for leopard frog (LF) and wood frog (WF) tadpoles exposed to azaC, SsMeV and wt-FV3 illustrating strain × species interactions (n = 53 ± 7.01 on average per strain-species combination). (B) Interaction plot showing average probability of death (±SE) per strain-temperature combination. The complement of the Kaplan–Meier estimate was used to calculate the probability of death.

Figure 4

(A) Probability of death over time for northern leopard frog (LF) and wood frog (WF) individuals at 14°C and 22°C illustrating species × temperature interactions (n = 96 ± 4.73 on average per species-temperature combination). (B) Interaction plot showing average probability of death (±SE) per species-temperature combination. The complement of the Kaplan–Meier estimate was used to calculate the probability of death.