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The benefits of coinfection: trematodes alter disease outcomes associated with virus infection
Author(s) -
Wuerthner Vanessa P.,
Hua Jessica,
Hoverman Jason T.
Publication year - 2017
Publication title -
journal of animal ecology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 2.134
H-Index - 157
eISSN - 1365-2656
pISSN - 0021-8790
DOI - 10.1111/1365-2656.12665
Subject(s) - ranavirus , biology , amphibian , coinfection , lithobates , iridovirus , larva , ecology , zoology , intermediate host , host (biology) , hyla , virus , virology
Summary 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 E chinoparyphium 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 E chinoparyphium reduced ranaviral loads by 9% but there was no reciprocal effect of prior ranavirus infection on E chinoparyphium load. Additionally, survival rates of hosts (larval gray treefrogs; H yla 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 ( A naxyrus americanus ), leopard frogs ( L ithobates pipiens ) and spring peepers ( P seudacris crucifer )] to examine how prior E chinoparyphium infection influenced ranavirus transmission within the community, using ranavirus‐infected larval wood frogs ( L ithobates sylvaticus ) as source of ranavirus. Consistent with the laboratory experiment, we found that prior E chinoparyphium 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.