Experimental evidence that parasites drive eco-evolutionary feedbacks

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 hostecosystem interactions. We provide experimental evidence that parasites influence host-mediated effects on ecosystems and, thereby, change the likelihood and strength of eco-evolutionary feedbacks.eco-evolutionary dynamics | three-spined stickleback | host-parasite interaction | Gyrodactylus | eutrophication

Analysing eco‐evolutionary dynamics—The challenging complexity of the real world

“…An example of the latter is the study of terHorst et al (), in which the impact of evolution of a plant to drought stress was studied on community composition of soil bacteria. The table excludes studies that address interaction modules such as predator–prey interactions (e.g., Becks et al, ; Hiltunen & Becks, ; Yoshida et al, ), host–parasite interactions (Brunner et al, ; Decaestecker et al, ; Frickel et al, ; Masri et al, ) and host–mutualist interactions (Ford et al, ; Macke et al, ), unless they involved whole communities of predators, prey, hosts, parasites or mutualists. Most eco‐evolutionary studies of predator–prey and host–parasite interactions involve one species of each type of interactors (predator and prey, host and parasite), and thus, while taking a two‐species approach, they do not allow estimating the degree to which evolution of competing predators or prey influence dynamics.…”

Eco‐evolutionary feedbacks—Theoretical models and perspectives

“…For example, Brunner et al. () demonstrated that the sole presence of a fish parasite in an experimental ecosystem alters the abiotic environment of the host in terms of nutrient content or dissolved oxygen. These altered environments were shown to impose selection on a subsequent generation of hosts, hence evidencing that macroparasites can mediate eco‐evolutionary feedbacks between fish and their environment.…”

Impacts of Nitrogen and Phosphorus: From Genomes to Natural Ecosystems and Agriculture

“…Such ecological feedbacks occur when interactions at one time determine the performance or interactions of organisms at another (Hendry, 2016). The impact of nutrient availability has already been demonstrated to alter eco-evolutionary dynamics in plants and in fish due to increased eutrophication, resulting in changes to parasite load and individual feeding ecology (Anaya-Rojas et al, 2016;Brunner et al, 2017). Future research will thus not only have to focus on direct effects of N and P on species but also on how they impact the interactions between species at the ecosystem level.…”