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Context-dependent effects of ranaviral infection on northern leopard frog life history traits.

Echaubard P, Little K, Pauli B, Lesbarrères D - PLoS ONE (2010)

Bottom Line: We observed a linear increase of detrimental effects when Ranavirus doses increased in low-density conditions, with control tadpoles having a significantly higher overall relative fitness.However, this pattern was no longer observed in high-density conditions, where the effects of increasing Ranavirus dose were limited.Our results illustrate how the net fitness of organisms may be shaped by ecological context and emphasize the necessity of examining the direct/indirect costs and benefits balance to fully understand host-pathogen interactions.

View Article: PubMed Central - PubMed

Affiliation: Genetics and Ecology of Amphibians Research Group, Department of Biology, Laurentian University, Sudbury, Canada.

ABSTRACT
Pathogens have important effects on host life-history traits, but the magnitude of these effects is often strongly context-dependent. The outcome of an interaction between a host and an infectious agent is often associated with the level of stress experienced by the host. Ranavirus causes disease and mortality in amphibian populations in various locations around the world, but most known cases of ranaviral infection have occurred in North America and the United Kingdom. While Ranavirus virulence has been investigated, the outcome of Ranavirus infection has seldom been related to the host environment. In a factorial experiment, we exposed Northern leopard frog (Lithobates pipiens, formerly Rana pipiens) tadpoles to different concentrations of Ranavirus and investigated the effect of host density on certain life-history traits, namely survival, growth rate, developmental stage and number of days from virus exposure to death. Our results suggest a prominent role of density in driving the direction of the interaction between L. pipiens tadpoles and Ranavirus. We showed that increasing animal holding density is detrimental for host fitness as mortality rate is higher, day of death earlier, development longer and growth rate significantly lower in high-density tanks. We observed a linear increase of detrimental effects when Ranavirus doses increased in low-density conditions, with control tadpoles having a significantly higher overall relative fitness. However, this pattern was no longer observed in high-density conditions, where the effects of increasing Ranavirus dose were limited. Infected and control animals fitness were consequently similar. We speculate that the host may eventually diverts the energy required for a metabolic/immune response triggered by the infection (i.e., direct costs of the infection) to better cope with the increase in environmental "stress" associated with high density (i.e., indirect benefits of the infection). Our results illustrate how the net fitness of organisms may be shaped by ecological context and emphasize the necessity of examining the direct/indirect costs and benefits balance to fully understand host-pathogen interactions.

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Related in: MedlinePlus

Interactions between tadpole density and exposure dose (Dose 1 =  low dose, Dose 2 =  medium dose, Dose 3 =  high dose; control animals were not exposed to Ranavirus).Mortality rate (A), day of death (B) developmental stage (C) and growth rate (D). Letters indicate grouping based on observed means in homogeneous subsets. Significant differences (α = 0.05) between means imply grouping in different subsets (a or b) are based on a Tukey post hoc test.
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pone-0013723-g001: Interactions between tadpole density and exposure dose (Dose 1 =  low dose, Dose 2 =  medium dose, Dose 3 =  high dose; control animals were not exposed to Ranavirus).Mortality rate (A), day of death (B) developmental stage (C) and growth rate (D). Letters indicate grouping based on observed means in homogeneous subsets. Significant differences (α = 0.05) between means imply grouping in different subsets (a or b) are based on a Tukey post hoc test.

Mentions: Few deceased tadpoles showed external signs of Ranavirus infection such as blood near the mouth or cloacal region. This observation seems to indicate a rather low virulence of the Ranavirus strain used. Nevertheless, the average percent mortality that occurred in the high density tanks was almost twice as high as the percent mortality observed in the low density tanks (Figure 1A, Table S1). In the low density tanks, the high dose (Dose 3) caused the highest percent mortality, followed by Dose 2, then Dose 1, and the control (Figure 1A). The same dose response was not seen in the high density tanks; although the results were not significant, with fewer tadpoles dying when exposed to Dose 3 as compared to tadpoles exposed to lower virus doses.


Context-dependent effects of ranaviral infection on northern leopard frog life history traits.

Echaubard P, Little K, Pauli B, Lesbarrères D - PLoS ONE (2010)

Interactions between tadpole density and exposure dose (Dose 1 =  low dose, Dose 2 =  medium dose, Dose 3 =  high dose; control animals were not exposed to Ranavirus).Mortality rate (A), day of death (B) developmental stage (C) and growth rate (D). Letters indicate grouping based on observed means in homogeneous subsets. Significant differences (α = 0.05) between means imply grouping in different subsets (a or b) are based on a Tukey post hoc test.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2965661&req=5

pone-0013723-g001: Interactions between tadpole density and exposure dose (Dose 1 =  low dose, Dose 2 =  medium dose, Dose 3 =  high dose; control animals were not exposed to Ranavirus).Mortality rate (A), day of death (B) developmental stage (C) and growth rate (D). Letters indicate grouping based on observed means in homogeneous subsets. Significant differences (α = 0.05) between means imply grouping in different subsets (a or b) are based on a Tukey post hoc test.
Mentions: Few deceased tadpoles showed external signs of Ranavirus infection such as blood near the mouth or cloacal region. This observation seems to indicate a rather low virulence of the Ranavirus strain used. Nevertheless, the average percent mortality that occurred in the high density tanks was almost twice as high as the percent mortality observed in the low density tanks (Figure 1A, Table S1). In the low density tanks, the high dose (Dose 3) caused the highest percent mortality, followed by Dose 2, then Dose 1, and the control (Figure 1A). The same dose response was not seen in the high density tanks; although the results were not significant, with fewer tadpoles dying when exposed to Dose 3 as compared to tadpoles exposed to lower virus doses.

Bottom Line: We observed a linear increase of detrimental effects when Ranavirus doses increased in low-density conditions, with control tadpoles having a significantly higher overall relative fitness.However, this pattern was no longer observed in high-density conditions, where the effects of increasing Ranavirus dose were limited.Our results illustrate how the net fitness of organisms may be shaped by ecological context and emphasize the necessity of examining the direct/indirect costs and benefits balance to fully understand host-pathogen interactions.

View Article: PubMed Central - PubMed

Affiliation: Genetics and Ecology of Amphibians Research Group, Department of Biology, Laurentian University, Sudbury, Canada.

ABSTRACT
Pathogens have important effects on host life-history traits, but the magnitude of these effects is often strongly context-dependent. The outcome of an interaction between a host and an infectious agent is often associated with the level of stress experienced by the host. Ranavirus causes disease and mortality in amphibian populations in various locations around the world, but most known cases of ranaviral infection have occurred in North America and the United Kingdom. While Ranavirus virulence has been investigated, the outcome of Ranavirus infection has seldom been related to the host environment. In a factorial experiment, we exposed Northern leopard frog (Lithobates pipiens, formerly Rana pipiens) tadpoles to different concentrations of Ranavirus and investigated the effect of host density on certain life-history traits, namely survival, growth rate, developmental stage and number of days from virus exposure to death. Our results suggest a prominent role of density in driving the direction of the interaction between L. pipiens tadpoles and Ranavirus. We showed that increasing animal holding density is detrimental for host fitness as mortality rate is higher, day of death earlier, development longer and growth rate significantly lower in high-density tanks. We observed a linear increase of detrimental effects when Ranavirus doses increased in low-density conditions, with control tadpoles having a significantly higher overall relative fitness. However, this pattern was no longer observed in high-density conditions, where the effects of increasing Ranavirus dose were limited. Infected and control animals fitness were consequently similar. We speculate that the host may eventually diverts the energy required for a metabolic/immune response triggered by the infection (i.e., direct costs of the infection) to better cope with the increase in environmental "stress" associated with high density (i.e., indirect benefits of the infection). Our results illustrate how the net fitness of organisms may be shaped by ecological context and emphasize the necessity of examining the direct/indirect costs and benefits balance to fully understand host-pathogen interactions.

Show MeSH
Related in: MedlinePlus