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1. Beyond single host, single parasite interactions: Quantifying competence for complete multi‐host, multi‐parasite communities

   https://doi.org/10.1111/1365-2435.14068  

   Stewart Merrill, Tara E. ; Calhoun, Dana M. ; Johnson, Pieter T. J. ( May 2022 , Functional Ecology)

   Understanding parasite transmission in communities requires knowledge of each species' capacity to support transmission. This property, ‘competence’, is a critical currency for modelling transmission under community change and for testing diversity–disease theory. Despite the central role of competence in disease ecology, we lack a clear understanding of the factors that generate competence and drive its variation.

   We developed novel conceptual and quantitative approaches to systematically quantify competence for a multi‐host, multi‐parasite community. We applied our framework to an extensive dataset: five amphibian host species exposed to four parasitic trematode species across five ecologically realistic exposure doses. Together, this experimental design captured 20 host–parasite interactions while integrating important information on variation in parasite exposure. Using experimental infection assays, we measured multiple components of the infection process and combined them to produce competence estimates for each interaction.

   With directly estimated competence values, we asked which components of the infection process best explained variation in competence: barrier resistance (the initial fraction of administered parasites blocked from infecting a host), internal clearance (the fraction of established parasites lost over time) or pre‐transmission mortality (the probability of host death prior to transmission). We found that variation in competence among the 20 interactions was best explained by differences in barrier resistance and pre‐transmission mortality, underscoring the importance of host resistance and parasite pathogenicity in shaping competence.

   We also produced dose‐integrated estimates of competence that incorporated natural variation in exposure to address questions on the basis and extent of variation in competence. We found strong signals that host species identity shaped competence variation (as opposed to parasite species identity). While variation in infection outcomes across hosts, parasites, individuals and doses was considerable, individual heterogeneity was limited compared to among‐species differences. This finding highlights the robustness of our competence estimates and suggests that species‐level values may be strong predictors for community‐level transmission in natural systems.

   Competence emerges from distinct underlying processes and can have strong species‐level characteristics; thus, this property has great potential for linking mechanisms of infection to epidemiological patterns.

   Read the freePlain Language Summaryfor this article on the Journal blog.

    

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2. Can hot temperatures limit disease transmission? A test of mechanisms in a zooplankton–fungus system

   https://doi.org/10.1111/1365-2435.13403  

   Shocket, Marta S. ; Magnante, Alexandra ; Duffy, Meghan A. ; Cáceres, Carla E. ; Hall, Spencer R. ; Hawley, ed., Dana ( August 2019 , Functional Ecology)

   Thermal ecology theory predicts that transmission of infectious diseases should respond unimodally to temperature, that is be maximized at intermediate temperatures and constrained at extreme low and high temperatures. However, empirical evidence linking hot temperatures to decreased transmission in nature remains limited.

   We tested the hypothesis that hot temperatures constrain transmission in a zooplankton–fungus (Daphnia dentifera–Metschnikowia bicuspidata) disease system where autumnal epidemics typically start after lakes cool from their peak summer temperatures. This pattern suggested that maximally hot summer temperatures could be inhibiting disease spread.

   Using a series of laboratory experiments, we examined the effects of high temperatures on five mechanistic components of transmission. We found that (a) high temperatures increased exposure to parasites by speeding up foraging rate but (b) did not alter infection success post‐exposure. (c) High temperatures lowered parasite production (due to faster host death and an inferred delay in parasite growth). (d) Parasites made in hot conditions were less infectious to the next host (instilling a parasite ‘rearing’ or 'trans‐host' effect of temperature during the prior infection). (e) High temperatures in the free‐living stage also reduce parasite infectivity, either by killing or harming parasites.

   We then assembled the five mechanisms into an index of disease spread. The resulting unimodal thermal response was most strongly driven by the rearing effect. Transmission peaked at intermediate hot temperatures (25–26°C) and then decreased at maximally hot temperatures (30–32°C). However, transmission at these maximally hot temperatures only trended slightly lower than the baseline control (20°C), which easily sustains epidemics in laboratory conditions and in nature. Overall, we conclude that while exposure to hot epilimnetic temperatures does somewhat constrain disease, we lack evidence that this effect fully explains the lack of summer epidemics in this natural system. This work demonstrates the importance of experimentally testing hypothesized mechanisms of thermal constraints on disease transmission. Furthermore, it cautions against drawing conclusions based on field patterns and theory alone.

   A freePlain Language Summarycan be found within the Supporting Information of this article.

    

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3. Host exposure to a common pollutant can influence diversity–disease relationships

   https://doi.org/10.1111/1365-2656.13988  

   Buss, Nicholas ; Hua, Jessica ( August 2023 , Journal of Animal Ecology)

   Hosts and parasites are embedded in communities where species richness and composition can influence disease outcomes (diversity–disease relationships). The direction and magnitude of diversity–disease relationships are influenced by variation in competence (ability to support and transmit infections) of hosts in a community. However, host susceptibility to parasites, which mediates host competence, is not static and is influenced by environmental factors, including pollutants. Despite the role that pollutants can play in augmenting host susceptibility, how pollutants influence diversity–disease dynamics is not well understood.

   Using an amphibian–trematode model, we tested how NaCl influences diversity–disease dynamics. We predicted that NaCl exposure can alter relative susceptibility of host species to trematodes, leading to cascading effects on the diversity–disease relationship. To test these predictions, we exposed hosts to benign or NaCl environments and generated communities that differed in number and composition of host species. We exposed these communities to trematodes and measured disease outcomes at the community (total infections across all hosts within a community) and species levels (average number of infections per host species within a community).

   Host species differed in their relative susceptibility to trematodes when exposed to NaCl. Consequently, at the community level (total infections across all hosts within a community), we only detected diversity–disease relationships (dilution effects) in communities where hosts were exposed to NaCl. At the species level, disease outcomes (average number of infections/species) and whether multi‐species communities supported lower number of infections relative to single‐species communities depended on community composition. Notably, however, as with overall community infection, diversity–disease relationships only emerged when hosts were exposed to NaCl.

   Synthesis.Pollutants are ubiquitous in nature and can influence disease dynamics across a number of host–parasite systems. Here, we show that NaCl exposure can alter the relative susceptibility of host species to parasites, influencing the relationship between biodiversity and disease at both community and species levels. Collectively, our study contributes to the limited knowledge surrounding environmental mediators of host susceptibility and their influence on diversity–disease dynamics.

    

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4. Parasite sharing in wild ungulates and their predators: Effects of phylogeny, range overlap, and trophic links

   https://doi.org/10.1111/1365-2656.12987  

   Stephens, Patrick R. ; Altizer, Sonia ; Ezenwa, Vanessa O. ; Gittleman, John L. ; Moan, Emili ; Han, Barbara ; Huang, Shan ; Pappalardo, Paula ; Dunn, ed., Jenny ( April 2019 , Journal of Animal Ecology)

   Understanding factors that facilitate interspecific pathogen transmission is a central issue for conservation, agriculture, and human health. Past work showed that host phylogenetic relatedness and geographical proximity can increase cross‐species transmission, but further work is needed to examine the importance of host traits, and species interactions such as predation, in determining the degree to which parasites are shared between hosts.

   Here we consider the factors that predict patterns of parasite sharing across a diverse assemblage of 116 wild ungulates (i.e., hoofed mammals in the Artiodactyla and Perissodactyla) and nearly 900 species of micro‐ and macroparasites, controlling for differences in total parasite richness and host sampling effort. We also consider the effects of trophic links on parasite sharing between ungulates and carnivores.

   We tested for the relative influence of range overlap, phylogenetic distance, body mass, and ecological dissimilarity (i.e., the distance separating species in a Euclidean distance matrix based on standardized traits) on parasite sharing. We also tested for the effects of variation in study effort as a potential source of bias in our data, and tested whether carnivores reported to feed on ungulates have more ungulate parasites than those that use other resources.

   As in other groups, geographical range overlap and phylogenetic similarity predicted greater parasite community similarity in ungulates. Ecological dissimilarity showed a weak negative relationship with parasite sharing. Counter to our expectations, differences, not similarity, in host body mass predicted greater parasite sharing between pairs of ungulate hosts. Pairs of well‐studied host species showed higher overlap than poorly studied species, although including sampling effort did not reduce the importance of biological traits in our models. Finally, carnivores that feed on ungulates harboured a greater richness of ungulate helminths.

   Overall, we show that the factors that predict parasite sharing in wild ungulates are similar to those known for other mammal groups, and demonstrate the importance of controlling for heterogeneity in host sampling effort in future analyses of parasite sharing. We also show that ecological interactions, in this case trophic links via predation, can allow sharing of some parasite species among distantly related host species.

    

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5. Tracking the assembly of nested parasite communities: Using β ‐diversity to understand variation in parasite richness and composition over time and scale

   https://doi.org/10.1111/1365-2656.13204  

   Moss, Wynne E. ; McDevitt‐Galles, Travis ; Calhoun, Dana M. ; Johnson, Pieter T. J. ; Cattadori, ed., Isabella ( March 2020 , Journal of Animal Ecology)

   Community composition is driven by a few key assembly processes: ecological selection, drift and dispersal. Nested parasite communities represent a powerful study system for understanding the relative importance of these processes and their relationship with biological scale. Quantifyingβ‐diversity across scales and over time additionally offers mechanistic insights into the ecological processes shaping the distributions of parasites and therefore infectious disease.

   To examine factors driving parasite community composition, we quantified the parasite communities of 959 amphibian hosts representing two species (the Pacific chorus frog,Pseudacris regillaand the California newt,Taricha torosa) sampled over 3 months from 10 ponds in California. Using additive partitioning, we estimated how much of regional parasite richness (γ‐diversity) was composed of within‐host parasite richness (α‐diversity) and turnover (β‐diversity) at three biological scales: across host individuals, across species and across habitat patches (ponds). We also examined howβ‐diversity varied across time at each biological scale.

   Differences among ponds comprised the majority (40%) of regional parasite diversity, followed by differences among host species (23%) and among host individuals (12%). Host species supported parasite communities that were less similar than expected by null models, consistent with ecological selection, although these differences lessened through time, likely due to high dispersal rates of infectious stages. Host individuals within the same population supported more similar parasite communities than expected, suggesting that host heterogeneity did not strongly impact parasite community composition and that dispersal was high at the individual host-level. Despite the small population sizes of within‐host parasite communities, drift appeared to play a minimal role in structuring community composition.

   Dispersal and ecological selection appear to jointly drive parasite community assembly, particularly at larger biological scales. The dispersal ability of aquatic parasites with complex life cycles differs strongly across scales, meaning that parasite communities may predictably converge at small scales where dispersal is high, but may be more stochastic and unpredictable at larger scales. Insights into assembly mechanisms within multi‐host, multi‐parasite systems provide opportunities for understanding how to mitigate the spread of infectious diseases within human and wildlife hosts.

    

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