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A paradox of parasite resistance: disease-driven trophic cascades increase the cost of resistance, selecting for lower resistance with parasites than without them

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Abstract

Most evolutionary theory predicts that, during epidemics, hosts will evolve higher resistance to parasites that kill them. Here, we provide an alternative to that typical expectation, with an explanation centered on resource feedbacks. When resistance is costly, hosts evolve decreasing resistance without parasites, as expected. But with parasites, hosts can evolve lower resistance than they would in the absence of parasites. This outcome arises in an eco-evolutionary model when four conditions are met: first, resistance has a fecundity cost (here, via decreased foraging/exposure rate); second, resources increase during epidemics via trophic cascades; third, increased resources magnify the benefit of maintaining a fast foraging rate, thereby magnifying the cost of evolving a slower foraging/exposure rate (i.e., resistance); fourth, that amplification of the cost outweighs the benefit of resistance. When these conditions are met, hosts evolve lower resistance than without parasites. This phenomenon was previously observed in a motivating mesocosm experiment with fungal parasites, zooplankton hosts, and algal resources. Re-analyzing this experiment produced evidence for our model’s mechanism. Thus, both model and experiment indicate that, via resource feedbacks, parasites can counterintuitively select against resistance.

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Acknowledgements

O. Schmidt assisted with the trait measurement assays. C. Lively, F. Bashey-Visser, and M. Wade provided valuable feedback on the manuscript.

Funding

This work was supported by NSF DEB 1353749 and 1655656 and NSF GRFP awards to J. Walsman and A. Strauss.

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Authors and Affiliations

  1. University of Pittsburgh, 410 Clapp Hall, 4249 Fifth Avenue, Pittsburgh, PA, 15260, USA

    Jason C. Walsman

  2. University of Georgia, 194A Ecology, 140 East Green St, Athens, GA, 30602, USA

    Alexander T. Strauss

  3. University of Wisconsin-Madison, 237 Hanson Labs, 1656 Linden Drive, Madison, WI, 53706, USA

    Jessica L. Hite

  4. University of Florida, 3125 Turlington Hall, Gainsville, FL, 32611, USA

    Marta S. Shocket

  5. Indiana University, 239 Jordan Hall, 1001 E Third Street, Bloomington, IN, 47405, USA

    Spencer R. Hall

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  1. Jason C. Walsman
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Correspondence to Jason C. Walsman.

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Walsman, J.C., Strauss, A.T., Hite, J.L. et al. A paradox of parasite resistance: disease-driven trophic cascades increase the cost of resistance, selecting for lower resistance with parasites than without them. Evol Ecol 37, 53–74 (2023). https://doi.org/10.1007/s10682-022-10203-7

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