Pathogen load predicts host functional disruption: A meta‐analysis of an amphibian fungal panzootic

Abstract

1. The progression of infectious disease depends on the intensity of and sensitivity to pathogen infection. Understanding commonalities in trait sensitivity to pathogen infection across studies through meta-analytic approaches could provide insight to the pathogenesis of infectious diseases. The globally devastating amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd), offers a good case system due to the widely available dataset on disruption to functional traits across species.2. Here, I systematically conducted a phylogenetically controlled meta-analysis to test how infection intensity affects different functional traits (e.g. behaviour, physiology, morphology, reproduction) and the survival in amphibians infected with Bd.3. There was a consistent effect of Bd infection on energy metabolism, while traits related to body condition, osmoregulation, and behaviour generally decreased with Bd infection. Skin integrity, hormone levels, and osmoregulation were most sensitive to Bd infection (minimum Bd load ln 2.5 zoospore equivalent), while higher minimum Bd loads were required to influence reproduction (ln 10.6 zoospore equivalent). Mortality differed between life stages, where juvenile mortality was dependent on infection intensity and exposure duration, while adult mortality was dependent on infection intensity only. Importantly, there were strong biases for studies on immune response, body condition and survival, while locomotor capacity, energy metabolism and cardiovascular traits were lacking.4. The influence of pathogen load on functional disruption can help inform pathogen thresholds before the onset of irreversible damage and mortality. Metaanalytic approaches can provide quantitative assessment across studies to reveal commonalities, differences and biases of panzootic diseases, especially for understanding the ecological relevance of disease impact.

Mechanisms and consequences of infection‐induced phenotypes

“…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).…”

“…While many of the above phenotypic changes represent adaptive host responses, they were historically attributed to parasite‐induced host debilitation. Wu (2023) presents a thorough meta‐analysis of the various functional disruptions induced in amphibian hosts by the debilitating chytrid fungus Batrachochytrium dendrobatidis . The analysis indicated that across host species, this infection leads to a higher resting metabolic rate, lower body condition, impaired osmoregulation and altered behaviour in hosts.…”

“…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).…”

“…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.…”