Does timing matter? How priority effects influence the outcome of parasite interactions within hosts
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In nature, hosts are exposed to an assemblage of parasite species that collectively form a complex community within the host. To date, however, our understanding of how within-host–parasite communities assemble and interact remains limited. Using a larval amphibian host (Pacific chorus frog, Pseudacris regilla) and two common trematode parasites (Ribeiroia ondatrae and Echinostoma trivolvis), we experimentally examined how the sequence of host exposure influenced parasite interactions within hosts. While there was no evidence that the parasites interacted when hosts were exposed to both parasites simultaneously, we detected evidence of both intraspecific and interspecific competition when exposures were temporally staggered. However, the strength and outcome of these priority effects depended on the sequence of addition, even after accounting for the fact that parasites added early in host development were more likely to encyst compared to parasites added later. Ribeiroia infection success was reduced by 14 % when Echinostoma was added prior to Ribeiroia, whereas no such effect was noted for Echinostoma when Ribeiroia was added first. Using a novel fluorescent-labeling technique that allowed us to track Ribeiroia infections from different exposure events, we also discovered that, similar to the interspecific interactions, early encysting parasites reduced the encystment success of later arriving parasites by 41 %, which could be mediated by host immune responses and/or competition for space. These results suggest that parasite identity interacts with host immune responses to mediate parasite interactions within the host, such that priority effects may play an important role in structuring parasite communities within hosts. This knowledge can be used to assess host–parasite interactions within natural communities in which environmental conditions can lead to heterogeneity in the timing and composition of host exposure to parasites.
KeywordsAmphibian Coinfection Developmental windows Immune priming Indirect competition
We thank J. Bowerman K. Richgels, S. Paull, and D. Preston for providing animals for the experiments. We are indebted to M. Redmond and S. Todd for assistance with experimental maintenance and animal husbandry. We also thank B. LaFonte for guidance on parasite identification and animal dissections. This project was supported by a grant from NSF (DEB-0841758), a fellowship from the David and Lucile Packard Foundation and a RUBICON fellowship from the Netherlands Organization for Scientific Research (NWO; grant 825.11.036).
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