Brain‐infecting parasites leave lasting effects on behaviour even in resistant hosts

Abstract

Parasites can have profound effects on intra‐ and interspecific interactions at the population and community levels through their influence on host behaviour, physiology and fitness. While host phenotypic changes are typically thought of in terms of established infections, parasite encounters may be sufficient to induce behavioural changes, even when no viable infections are established. Here, we use the Japanese rice fish medaka Oryzias latipes and the brain‐infecting microsporidan parasite Pseudoloma neurophilia to understand how parasite resistance influences behaviour. Although a previous study suggested that medaka are a suitable host for P. neurophilia, an eight‐week parasite exposure regime resulted in no detectable infection in our study. Both parasite‐exposed and control (no parasite exposure) medaka were tested in behavioural assays that assessed boldness, activity and sociality. We detected considerable changes in medaka behaviour following parasite exposure, with parasite‐exposed fish being more active, less bold and more social when compared to control fish. These data indicate that parasite encounters may induce behavioural alterations even in non‐susceptible hosts. In addition to established infection, individual differences in parasite exposure must also be considered in studies of host responses across ecological scales. Read the free Plain Language Summary for this article on the Journal blog.

Mechanisms and consequences of infection‐induced phenotypes

“…immunity, predator vigilance) (Lopes et al, 2021; Tillman & Adelman, 2023). Behavioural alterations can occur even in the absence of any detectable infection; Vindas et al (2023) show that parasite‐exposed (but uninfected) medaka Oryzias latipes exhibit greater activity, aversion to risk and sociality than individuals that were not exposed to parasites.…”

“…Animal phenotypes are likely shaped and selected in response to both the risk of infection as well as infection itself (Alves & Aubin-Horth, 2023;Lopes, 2023;Vindas et al, 2023). The recognition of parasites' critical role in generating phenotypic variation among individuals is needed more than ever as we grapple with predicting how anthropogenic stressors, such as pollutants, climate change and physical habitat destruction, will impact disease dynamics in the short and long term (Ortega et al, 2021;Tabachnick, 2010).…”

“…Recognition of the pivotal role that parasites play in the variability of animal phenotypes in nature is surprisingly low (Chretien et al, 2023). Several contributions to this special feature present practical guidance for researchers working in a range of disciplines to assess the role of infection in their study system, including behaviour (Salerno et al, 2023; Stockmaier et al, 2023; Tillman & Adelman, 2023; Vindas et al, 2023), performance (Chretien et al, 2023), physiology (Alves & Aubin‐Horth, 2023; Lopes, 2023; Seguel et al, 2023; Wu, 2023) and epigenetics (Ngo et al, 2023). Yet, there are still many unanswered questions.…”

“…While biologists often work under the assumption that their study animals lack infections that drive major changes in their morphology, behaviour and physiology (Chretien et al, 2023), most animals are (co)infected by parasitic species at different intensities that may vary in their impacts on hosts (Seguel et al, 2023; Wu, 2023). Animal phenotypes are likely shaped and selected in response to both the risk of infection as well as infection itself (Alves & Aubin‐Horth, 2023; Lopes, 2023; Vindas et al, 2023). The recognition of parasites' critical role in generating phenotypic variation among individuals is needed more than ever as we grapple with predicting how anthropogenic stressors, such as pollutants, climate change and physical habitat destruction, will impact disease dynamics in the short and long term (Ortega et al, 2021; Tabachnick, 2010).…”

“…This special feature highlights the various ways that parasites drive variation in host phenotypes. The contributed articles highlight diverse host–parasite systems across a broad range of taxa and include perspective and concept articles (Adamo, 2023; Lopes, 2023; Pavey & Vyas, 2023; Poulin et al, 2023; Stockmaier et al, 2023; Tillman & Adelman, 2023), a systematic literature review (Chretien et al, 2023), a meta‐analysis (Wu, 2023) and observational and experimental research conducted in laboratory and field settings (Alves & Aubin‐Horth, 2023; Ngo et al, 2023; Salerno et al, 2023; Seguel et al, 2023; Vindas et al, 2023; Will et al, 2023). In this Editorial, we contextualize each featured article's contribution to our understanding of how parasites generate intra‐ and interindividual differences in host phenotypes, how this trait variation reverberates across levels of biological organization from cells to communities and the role of the host's external environment in modulating these effects.…”