The benefits of coinfection: trematodes alter disease outcomes associated with virus infection.
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.
Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN, 47907, USA.
Vanessa P
0000-0001-9479-2157
VP
Wuerthner
Biological Sciences Department, Binghamton University, Binghamton, NY, 13902, USA.
Jessica
J
Hua
Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN, 47907, USA.
Jason T
JT
Hoverman
D000818:Animals; D001001:Anura / Q000382:microbiology / Q000821:virology; D002025:Bufonidae; D060085:Coinfection; D017995:Ranavirus / Q000472:pathogenicity*; D014200:Trematoda / Q000821:virology*
anuran; echinostomes; frog virus 3; helminth; host-parasite interactions