Experimental evidence that parasites drive eco-evolutionary feedbacks

Franziska S. Brunner; Jaime M. Anaya-Rojas; Blake Matthews; Christophe Eizaguirre

doi:10.1073/pnas.1619147114

New Research In

Edited by Andrew P. Hendry, McGill University, Montreal, Canada, and accepted by Editorial Board Member Douglas Futuyma February 22, 2017 (received for review November 19, 2016)

Significance

Anthropogenic effects on the environment are ubiquitous and have enormous impacts on individual and ecosystem health. It is widely accepted that environmental change affects disease distribution, but how it may affect parasite-driven evolution remains elusive. Our results provide experimental evidence that parasites play a major role in ecosystem dynamics and, as a result, can affect selection in subsequent host generations. This role is further modified by the prevailing environmental conditions that affect disease dynamics in two ways: through altered ecological opportunities for disease and through altered evolutionary effects on the host.

Abstract

Host resistance to parasites is a rapidly evolving trait that can influence how hosts modify ecosystems. Eco-evolutionary feedbacks may develop if the ecosystem effects of host resistance influence selection on subsequent host generations. In a mesocosm experiment, using a recently diverged (<100 generations) pair of lake and stream three-spined sticklebacks, we tested how experimental exposure to a common fish parasite (Gyrodactylus spp.) affects interactions between hosts and their ecosystems in two environmental conditions (low and high nutrients). In both environments, we found that stream sticklebacks were more resistant to Gyrodactylus and had different gene expression profiles than lake sticklebacks. This differential infection led to contrasting effects of sticklebacks on a broad range of ecosystem properties, including zooplankton community structure and nutrient cycling. These ecosystem modifications affected the survival, body condition, and gene expression profiles of a subsequent fish generation. In particular, lake juvenile fish suffered increased mortality in ecosystems previously modified by lake adults, whereas stream fish showed decreased body condition in stream fish-modified ecosystems. Parasites reinforced selection against lake juveniles in lake fish-modified ecosystems, but only under oligotrophic conditions. Overall, our results highlight the overlapping timescales and the interplay of host–parasite and host–ecosystem interactions. We provide experimental evidence that parasites influence host-mediated effects on ecosystems and, thereby, change the likelihood and strength of eco-evolutionary feedbacks.

Footnotes

↵¹F.S.B. and J.M.A.-R. contributed equally to this work.
↵²To whom correspondence should be addressed. Email: franziska.brunner{at}alumni.ethz.ch.
↵³B.M. and C.E. contributed equally to this work.

Author contributions: F.S.B., J.M.A.-R., B.M., and C.E. designed research; F.S.B. and J.M.A.-R. performed research; F.S.B. and J.M.A.-R. analyzed data; and F.S.B., J.M.A.-R., B.M., and C.E. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. A.P.H. is a guest editor invited by the Editorial Board.
Data deposition: The results from this paper are available through Dryad (doi: 10.5061/dryad.5q783).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1619147114/-/DCSupplemental.

Freely available online through the PNAS open access option.

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