The benefits of coinfection: trematodes alter disease outcomes associated with virus infection

Abstract

Coinfections are increasingly recognized as important drivers of disease dynamics. Consequently, greater emphasis has been placed on integrating principles from community ecology with disease ecology to understand within-host interactions among parasites. Using larval amphibians and two amphibian parasites (ranaviruses and the trematode Echinoparyphium sp.), we examined the influence of coinfection on disease outcomes. Our first objective was to examine how priority effects (the timing and sequence of parasite exposure) influence infection and disease outcomes in the laboratory. We found that interactions between the parasites were asymmetric; prior infection with Echinoparyphium reduced ranaviral loads by 9% but there was no reciprocal effect of prior ranavirus infection on Echinoparyphium load. Additionally, survival rates of hosts (larval gray treefrogs; Hyla versicolor) infected with Echinoparyphium 10 days prior to virus exposure were 25% greater compared to hosts only exposed to virus. Our second objective was to determine whether these patterns were generalizable to multiple amphibian species under more natural conditions. We conducted a semi-natural mesocosm experiment consisting of four larval amphibian hosts [gray treefrogs, American toads (Anaxyrus americanus), leopard frogs (Lithobates pipiens) and spring peepers (Pseudacris crucifer)] to examine how prior Echinoparyphium infection influenced ranavirus transmission within the community, using ranavirus-infected larval wood frogs (Lithobates sylvaticus) as source of ranavirus. Consistent with the laboratory experiment, we found that prior Echinoparyphium infection reduced ranaviral loads by 19 to 28% in three of the four species. Collectively, these results suggest that macroparasite infection can reduce microparasite replication rates across multiple amphibian species, possibly through cross-reactive immunity. Although the immunological mechanisms driving this outcome are in need of further study, trematode infections appear to benefit hosts that are exposed to ranaviruses. Additionally, these results suggest that consideration of priority effects and timing of exposure are vital for understanding parasite interactions within hosts and disease outcomes.

Evolved pesticide tolerance influences susceptibility to parasites in amphibians

“…Previous studies have reported a similar correlation between viral load and mortality (Wuerthner et al., 2017). Our results suggest that regardless of population, wood frogs experience mortality when log viral loads passed a threshold of approximately 5 viral copies/ng of DNA.…”

“…Our results suggest that regardless of population, wood frogs experience mortality when log viral loads passed a threshold of approximately 5 viral copies/ng of DNA. A similar threshold was detected when log viral loads approached 4.5 viral copies/ng of DNA in gray tree frogs ( Hyla versicolor ; Wuerthner et al., 2017). Identifying a threshold value can potentially allow researchers to make predictions about the likelihood or timing of a ranavirus die‐off in natural populations.…”

The influence of landscape and environmental factors on ranavirus epidemiology in a California amphibian assemblage

“…For each individual, we pooled the liver and kidney tissues and extracted DNA using DNeasy Blood and Tissue Kits (Qiagen). To quantify infection status for each individual, we used quantitative polymerase chain reaction (Wuerthner, Hua, & Hoverman, ). Our qPCR mixture included a 1.0 μl mixture of each primer at 10 pmol/μl (rtMCP‐F [5′‐ACA CCA CCG CCC AAA AGT AC‐3′] and rtMCP‐R [5′‐CCG TTC ATG ATG CGG ATA ATG‐3′]), and a fluorescent probe (rtMCP‐probe [5′‐CCT CAT CGT TCT GGC CAT CAA CCA‐3′]), and 6.25 μl of TaqMan ® Universal PCR Master Mix (Applied Biosystems).…”

“…For each individual, we pooled the liver and kidney tissues and extracted DNA using DNeasy Blood and Tissue Kits (Qiagen). To quantify infection status for each individual, we used quantitative polymerase chain reaction (Wuerthner, Hua, & Hoverman, 2017). | 641 fluorescent probe (rtMCP-probe [5 0 -CCT CAT CGT TCT GGC CAT CAA CCA-3 0 ]), and 6.25 ll of TaqMan â Universal PCR Master Mix (Applied Biosystems).…”

Guidance for Developing Amphibian Population Models for Ecological Risk Assessment

“…Interactions between parasite occurrence, habitat degradation, and chemical exposure introduce further complications in assessment of vulnerability (Koprivinkar and Redfern 2012;Stutz et al 2017) with the potential for agrochemicals to reduce immunity to parasite infection (Kiesecker 2002;Rohr et al 2008) and decrease parasite survival (Hua et al 2016). Multiple parasites do not always produce synergistic effects; compensatory effects of coinfection are also possible (Wuerthner et al 2017). Positive identification of B. dendrobatidis in national field samples has been associated with dissolved organic content, total N, and P as well as cooler water temperatures (Battaglin et al 2016).…”