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1. 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)

   Abstract 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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2. Age structure eliminates the impact of coinfection on epidemic dynamics in a freshwater zooplankton system

   https://doi.org/10.1086/726897  

   Clay, Patrick A.; Gattis, Sabrina; Garcia, Jade; Hernandez, Vincent; Ben-Ami, Frida; Duffy, Meghan A. (July 2023, The American Naturalist)

   Parasites often coinfect host populations, and, by interacting within hosts, might change the trajectory of multi-parasite epidemics. However, host-parasite interactions often change with host age, raising the possibility that within-host interactions between parasites might also change, influencing the spread of disease. We measured how heterospecific parasites interacted within zooplankton hosts and how host age changed these interactions. We then parameterized an epidemiological model to explore how age-effects altered the impact of coinfection on epidemic dynamics. In our model, we found that in populations where epidemiologically relevant parameters did not change with age, the presence of a second parasite altered epidemic dynamics. In contrast, when parameters varied with host age (based on our empirical measures), there was no longer a difference in epidemic dynamics between singly and coinfected populations, indicating that variable age structure within a population eliminates the impact of coinfection on epidemic dynamics. Moreover, infection prevalence of both parasites was lower in populations where epidemiologically relevant parameters changed with age. Given that hostpopulation age structure changes over time and space, these results indicate that age-effects are important for understanding epidemiological processes in coinfected systems and that studies focused on a single age group could yield inaccurate insights. 

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3. “Resistance Is Futile”: Weaker Selection for Resistance by Abundant Parasites Increases Prevalence and Depresses Host Density

   https://doi.org/10.1086/724426  

   Walsman, Jason C.; Duffy, Meghan A.; Cáceres, Carla E.; Hall, Spencer R. (June 2023, The American Naturalist)

   Theory often predicts that host populations should evolve greater resistance when parasites become abundant. Furthermore, that evolutionary response could ameliorate declines in host populations during epidemics. Here, we argue for an update: when all host genotypes become sufficiently infected, higher parasite abundance can select for lower resistance because its cost exceeds its benefit. We illustrate such a “resistance is futile” outcome with mathematical and empirical approaches. First, we analyzed an eco-evolutionary model of parasites, hosts, and hosts’ resources. We determined eco-evolutionary outcomes for prevalence, host density, and resistance (mathematically, “transmission rate”) along ecological and trait gradients that alter parasite abundance. With high enough parasite abundance, hosts evolve lower resistance, amplifying infection prevalence and decreasing host density. In support of these results, a higher supply of nutrients drove larger epidemics of survival-reducing fungal parasites in a mesocosm experiment. In two-genotype treatments, zooplankton hosts evolved less resistance under high-nutrient conditions than under low-nutrient conditions. Less resistance, in turn, was associated with higher infection prevalence and lower host density. Finally, in an analysis of naturally occurring epidemics, we found a broad, bimodal distribution of epidemic sizes consistent with the resistance is futile prediction of the eco-evolutionary model. Together, the model and experiment, supplemented by the field pattern, support predictions that drivers of high parasite abundance can lead to the evolution of lower resistance. Hence, under certain conditions, the most fit strategy for individual hosts exacerbates prevalence and depresses host populations. 

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4. Within-host priority effects and epidemic timing determine outbreak severity in co-infected populations

   https://doi.org/10.1098/rspb.2020.0046  

   Clay, Patrick A.; Duffy, Meghan A.; Rudolf, Volker H. (March 2020, Proceedings of the Royal Society B: Biological Sciences)

   Co-infections of hosts by multiple pathogen species are ubiquitous, but predicting their impact on disease remains challenging. Interactions between co-infecting pathogens within hosts can alter pathogen transmission, with the impact on transmission typically dependent on the relative arrival order of pathogens within hosts (within-host priority effects). However, it is unclear how these within-host priority effects influence multi-pathogen epidemics, particularly when the arrival order of pathogens at the host-population scale varies. Here, we combined models and experiments with zooplankton and their naturally co-occurring fungal and bacterial pathogens to examine how within-host priority effects influence multi-pathogen epidemics. Epidemiological models parametrized with within-host priority effects measured at the single-host scale predicted that advancing the start date of bacterial epidemics relative to fungal epidemics would decrease the mean bacterial prevalence in a multi-pathogen setting, while models without within-host priority effects predicted the opposite effect. We tested these predictions with experimental multi-pathogen epidemics. Empirical dynamics matched predictions from the model including within-host priority effects, providing evidence that within-host priority effects influenced epidemic dynamics. Overall, within-host priority effects may be a key element of predicting multi-pathogen epidemic dynamics in the future, particularly as shifting disease phenology alters the order of infection within hosts. 

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5. Dose relationships can exacerbate, mute, or reverse the impact of heterospecific host density on infection prevalence

   https://doi.org/10.1002/ecy.3422  

   Clay, Patrick A.; Cortez, Michael H.; Duffy, Meghan A. (July 2021, Ecology)

   Abstract The likelihood an individual becomes infected depends on the community in which it is embedded. For environmentally transmitted parasites, host community composition can alter host density, the density of parasites that hosts encounter in the environment, and the dose to which hosts are subsequently exposed. While some multi‐host theory incorporates some of these factors (e.g., competition among hosts), it does not currently consider the nonlinear relationships between parasite exposure dose and per‐propagule infectivity (dose–infectivity relationships), between exposure dose and infected host mortality (dose–mortality relationships), and between exposure dose and parasite propagule excretion (dose–excretion relationships). This makes it difficult to predict the impact of host species on one another’s likelihood of infection. To understand the implications of these nonlinear dose relationships for multi‐host communities, we first performed a meta‐analysis on published dose–infectivity experiments to quantify the proportion of accelerating, linear, or decelerating dose–infectivity relationships; we found that most experiments demonstrated decelerating dose–infectivity relationships. We then explored how dose–infectivity, dose–mortality, and dose–excretion relationships might alter the impact of heterospecific host density on infectious propagule density, infection prevalence, and density of a focal host using two‐host, one‐parasite models. We found that dose relationships either decreased the magnitude of the impact of heterospecific host density on propagule density and infection prevalence via negative feedback loops (decelerating dose–infectivity relationships, positive dose–mortality relationships, and negative dose–excretion relationships), or increased the magnitude of the impact of heterospecific host density on infection prevalence via positive feedback loops (accelerating dose–infectivity relationships and positive dose–excretion relationships). Further, positive dose–mortality relationships resulted in hosts that traditionally decrease disease (e.g., low competence, strong competitors) increasing infection prevalence, and vice versa. Finally, we found that dose relationships can create positive feedback loops that facilitate friendly competition (i.e., increased heterospecific density has a positive effect on focal host density because the reduction in disease outweighs the negative effects of interspecific competition). This suggests that without taking dose relationships into account, we may incorrectly predict the effect of heterospecific host interactions, and thus host community composition, on environmentally transmitted parasites. 

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