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Order and timing of infection with different parasite life stages impacts host and parasite life histories

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Abstract

Co-exposure to multiple parasites can alter parasite success and host life history when compared to single infections. These infection outcomes can be affected by the order of parasite arrival, the host immune response, and the interspecific interactions among co-infecting parasites. In this study, we examined how the arrival order of two trematode parasites, Schistosoma mansoni and Echinostoma caproni, influenced parasite ecology and the life history of their snail host, Biomphalaria glabrata. Snail hosts were exposed to E. caproni cercariae before, with, and after their exposure to S. mansoni miracidia. We then measured the effects of this timing on infection prevalence, infection intensity of E. caproni metacercariae, and cercarial output of S. mansoni, as well as on snail reproduction and survival. Snails infected only with S. mansoni and snails exposed to E. caproni after S. mansoni both shed more cercariae than simultaneously exposed snails. Additionally, S. mansoni prevalence was lower in snails that were first exposed to E. caproni compared to snails that were exposed to E. caproni after S. mansoni. Moreover, snails exposed to E. caproni before S. mansoni did not differ in their survival compared to control snails, whereas simultaneously exposed snails and snails exposed to E. caproni after S. mansoni had lower survival than control snails. Combined, this prevalence and survival data suggest a potential protective role of early E. caproni exposure. The timing of E. caproni exposure impacts S. mansoni establishment and reproduction, but host survival patterns are likely driven by S. mansoni prevalence alone.

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Data availability

Data and code for this paper are available online at https://github.com/vanna006/order-timing-stages-life-history.

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Acknowledgements

Bailey Pyle was supported by the Cable-Silkman Fellowship for undergraduate parasitology research. Biomphalaria glabrata snails were supplied by the Schistosomiasis Resource Center of the Biomedical Research Institute (Rockville, MD, USA). Echinostoma caproni was supplied by Dr. Thomas Platt. We thank the members of the Minchella and Searle labs for the productive conversations about the project and results.

Funding

BRP received funding from the Cable-Silkman Fellowship for undergraduate parasitology research. This project received no additional funding.

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Contributions

BRP and JTV conceptualized the experiment. GAS, BRP, and JTV conducted the experiment. JTV conducted the data analysis. GAS and BRP wrote the initial draft with input from DJM and JTV. All authors gave critical feedback and contributed to the editing of the paper.

Corresponding author

Correspondence to Grace A. Schumacher.

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Ethics approval

Infection of mice with Schistosoma mansoni, infection of chickens with Echinostoma caproni, and euthanasia of both mice and chickens all took place at Purdue University and followed methods approved by Purdue University’s Institutional Animal Care and Use Committee (Purdue Animal Care and Use Committee Protocol #1111000225).

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The authors declare no competing interests.

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Section Editor: Konstans Wells

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Schumacher, G.A., Pyle, B.R., Minchella, D.J. et al. Order and timing of infection with different parasite life stages impacts host and parasite life histories. Parasitol Res 123, 187 (2024). https://doi.org/10.1007/s00436-024-08205-1

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  • DOI: https://doi.org/10.1007/s00436-024-08205-1

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