Rachel M. Penczykowski

Ecological context influences epidemic size and parasite-driven evolution

Cost-Benefit Analysis Mounting resistance to infection is costly, requires energetic input, and may thus compromise fecundity. Duffy et al. (p. 1636; see the cover) tested the relationships between productivity, predation, and mortality in a combination of observations of a natural lake and an experimental replica of a clonal zooplankton-parasitic yeast population. In the wild, epidemics of the yeast could exceed 60% and cause significant host mortality. In this situation, the clonal zooplankton host faces the physiological dilemma of either increasing resistance to deal with infection or of safeguarding fecundity. Zooplankton that feed quickly can reproduce quickly, but also end up ingesting more yeast spores. However, because fish tend to cull infected hosts, fish predation counters infection. Ultimately, both wild and model systems showed that lakes with high productivity (more nitrogen) and/or few fish supported greater epidemics of yeast and more resistant hosts, whereas less productive lakes, or those with more fish, had smaller epidemics and hosts with higher susceptibility to the yeast. When the physiological cost of host resistance to a disease damages reproductive output, disease susceptibility can evolve. The occurrence and magnitude of disease outbreaks can strongly influence host evolution. In particular, when hosts face a resistance-fecundity trade-off, they might evolve increased resistance to infection during larger epidemics but increased susceptibility during smaller ones. We tested this theoretical prediction by using a zooplankton-yeast host-parasite system in which ecological factors determine epidemic size. Lakes with high productivity and low predation pressure had large yeast epidemics; during these outbreaks, hosts became more resistant to infection. However, with low productivity and high predation, epidemics remained small and hosts evolved increased susceptibility. Thus, by modulating disease outbreaks, ecological context (productivity and predation) shaped host evolution during epidemics. Consequently, anthropogenic alteration of productivity and predation might strongly influence both ecological and evolutionary outcomes of disease.

Understanding the ecology and evolution of host–parasite interactions across scales

Predicting the emergence, spread and evolution of parasites within and among host populations requires insight to both the spatial and temporal scales of adaptation, including an understanding of within‐host up through community‐level dynamics. Although there are very few pathosystems for which such extensive data exist, there has been a recent push to integrate studies performed over multiple scales or to simultaneously test for dynamics occurring across scales. Drawing on examples from the literature, with primary emphasis on three diverse host–parasite case studies, we first examine current understanding of the spatial structure of host and parasite populations, including patterns of local adaptation and spatial variation in host resistance and parasite infectivity. We then explore the ways to measure temporal variation and dynamics in host–parasite interactions and discuss the need to examine change over both ecological and evolutionary timescales. Finally, we highlight new approaches and syntheses that allow for simultaneous analysis of dynamics across scales. We argue that there is great value in examining interplay among scales in studies of host–parasite interactions.

Variation in costs of parasite resistance among natural host populations

Organisms that can resist parasitic infection often have lower fitness in the absence of parasites. These costs of resistance can mediate host evolution during parasite epidemics. For example, large epidemics will select for increased host resistance. In contrast, small epidemics (or no disease) can select for increased host susceptibility when costly resistance allows more susceptible hosts to outcompete their resistant counterparts. Despite their importance for evolution in host populations, costs of resistance (which are also known as resistance trade‐offs) have mainly been examined in laboratory‐based host–parasite systems. Very few examples come from field‐collected hosts. Furthermore, little is known about how resistance trade‐offs vary across natural populations. We addressed these gaps using the freshwater crustacean Daphnia dentifera and its natural yeast parasite, Metschnikowia bicuspidata. We found a cost of resistance in two of the five populations we studied – those with the most genetic variation in resistance and the smallest epidemics in the previous year. However, yeast epidemics in the current year did not alter slopes of these trade‐offs before and after epidemics. In contrast, the no‐cost populations showed little variation in resistance, possibly because large yeast epidemics eroded that variation in the previous year. Consequently, our results demonstrate variation in costs of resistance in wild host populations. This variation has important implications for host evolution during epidemics in nature.

Potassium stimulates fungal epidemics in Daphnia by increasing host and parasite reproduction

As natural enemies, parasites can dramatically harm host populations, and even catalyze their decline. Thus, identifying factors that promote disease spread is paramount. Environmental factors can drive epidemics by altering traits involved in disease spread. For example, nutrients (such as nitrogen and phosphorus) can stimulate reproduction of both hosts and parasites or alter rates of disease transmission by stimulating productivity and nutrition of food resources of hosts. Here, we demonstrate nutrient-trait-epidemic connections between the greatly understudied macronutrient potassium (K) and fungal disease (Metschnikowia bicuspidata) in a zooplankton host (Daphnia dentifera). In a three-year survey, epidemics grew larger in lakes with more potassium. In laboratory assays, potassium enrichment of low-K lake water enhanced both host and parasite reproduction. Parameterized with these data, a model predicted that potassium addition catalyzes disease spread. We confirmed this prediction with an experiment in large mesocosms (6000 L) in a low K-lake: potassium enrichment caused larger epidemics in replicated Daphnia populations. Consequently, the model--data combination mechanistically explained the field pattern and revealed a novel ecological role for the nutrient potassium. Furthermore, our findings highlight the need for further development of theory for nutrient limitation of epidemics. Such theory could help to explain heterogeneous eruptions of disease in space, connect these outbreaks to natural or anthropogenic enrichment of ecosystems, predict the ecological consequences of these outbreaks, and reveal novel strategies for disease management.

Resources, key traits and the size of fungal epidemics in Daphnia populations

Parasites can profoundly affect host populations and ecological communities. Thus, it remains critical to identify mechanisms that drive variation in epidemics. Resource availability can drive epidemics via traits of hosts and parasites that govern disease spread. Here, we map resource-trait-epidemic connections to explain variation in fungal outbreaks (Metschnikowia bicuspidata) in a zooplankton host (Daphnia dentifera) among lakes. We predicted epidemics would grow larger in lakes with more phytoplankton via three energetic mechanisms. First, resources should stimulate Daphnia reproduction, potentially elevating host density. Secondly, resources should boost body size of hosts, enhancing exposure to environmentally distributed propagules through size-dependent feeding. Thirdly, resources should fuel parasite reproduction within hosts. To test these predictions, we sampled 12 natural epidemics and tracked edible algae, fungal infection prevalence, body size, fecundity and density of hosts, as well as within-host parasite loads. Epidemics grew larger in lakes with more algal resources. Structural equation modelling revealed that resource availability stimulated all three traits (host fecundity, host size and parasite load). However, only parasite load connected resources to epidemic size. Epidemics grew larger in more dense Daphnia populations, but host density was unrelated to host fecundity (thus breaking its link to resources). Thus, via energetic mechanisms, resource availability can stimulate key trait(s) governing epidemics in nature. A synthetic focus on resources and resource-trait links could yield powerful insights into epidemics.

Poor resource quality lowers transmission potential by changing foraging behaviour

Summary Resource quality can have conflicting effects on the spread of disease. High-quality resources could hinder disease spread by promoting host immune function. Alternatively, high-quality food might enhance the spread of disease through other traits of hosts or parasites. Thus, to assess how resource quality shapes epidemics, we need to delineate mechanisms by which food quality affects key epidemiological traits. Here, we disentangle effects of food quality on ‘transmission potential’ – a key component of parasite fitness that combines transmission rate and parasite production – using a zooplankton host and fungal parasite. We estimated the components of transmission potential (i.e. parasite encounter rate, susceptibility and yield of parasite propagules) for hosts fed a high-quality green alga and a low-quality cyanobacterium. A focal experiment was designed to disentangle food quality effects on various components of transmission potential. The low-quality resource decreased transmission potential by stunting host growth and altering foraging behaviour. Hosts reared on low-quality food were smaller and had lower size-corrected feeding rates. Due to their slower grazing, they encountered fewer parasite spores in the water. Smaller hosts also had lower risk of an ingested spore causing infection (i.e. lower susceptibility) and yielded fewer parasite propagules. Hosts switched from high- to low-quality food during spore exposure also had low transmission potential – despite their large size – because the poor quality resource strongly depressed foraging. A follow-up experiment investigated traits of the low-quality resource that might have driven those results. Cyanobacterial compounds that can inhibit digestive proteases of a related grazer likely did not cause the observed reductions in transmission potential. Our study highlights the value of using mechanistic models to pinpoint how resource quality can change transmission potential. Overall, our results show that low-quality resources could inhibit the spread of disease through effects on multiple components of transmission potential. They also provide insight into how disease outbreaks in wildlife may respond to shifts in resource quality caused by eutrophication or climate change.

Linking winter conditions to regional disease dynamics in a wild plant–pathogen metapopulation

Pathogens are considered to drive ecological and evolutionary dynamics of plant populations, but we lack data measuring the population-level consequences of infection in wild plant-pathogen interactions. Moreover, while it is often assumed that offseason environmental conditions drive seasonal declines in pathogen population size, little is known about how offseason environmental conditions impact the survival of pathogen resting stages, and how critical the offseason is for the next seasons epidemic. The fungal pathogen Podosphaera plantaginis persists as a dynamic metapopulation in the large network of Plantago lanceolata host populations. Here, we analyze long-term data to measure the spatial synchrony of epidemics and consequences of infection for over 4000 host populations. Using a theoretical model, we study whether large-scale environmental change could synchronize disease occurrence across the metapopulation. During 2001-2013 exposure to freezing decreased, while pathogen extinction-colonization-persistence rates became more synchronized. Simulations of a theoretical model suggest that increasingly favorable winter conditions for pathogen survival could drive such synchronization. Our data also show that infection decreases host population growth. These results confirm that mild winter conditions increase pathogen overwintering success and thus increase disease prevalence across the metapopulation. Further, we conclude that the pathogen can drive host population growth in the Plantago-Podosphaera system.

Phosphorus sources and demand during summer in a eutrophic lake

Abstract.In pelagic systems, phytoplankton biomass may remain abundant or near equilibrium while concentrations of the limiting nutrient are below detection. In eutrophic lakes, it has been thought that episodic algal blooms are due to mixing events that break down this equilibrium by adding nutrients to the mixed layer. Alternatively, rapid rates of biotic recycling among primary producers and heterotrophic consumers could maintain high phytoplankton biomass, yet the recycling process has been difficult to observe in situ. Here we use free-water oxygen measurements and an associated metabolic model to infer rates of phosphorus (P) uptake and biotic mineralization in the epilimnion of a eutrophic lake. The rates of uptake and mineralization were compared to “external” sources of P such as loading and entrainment. Also, model results were assessed using sensitivity analysis. We found that the majority of phytoplankton P demand during the period of low P availability could be accounted for by biotic mineralization, but that it was important to consider the effects of entrainment in order to account fully for P uptake. These general results were relatively insensitive to model parameterization, though the relative C:P ratio of material taken up versus mineralized was an important consideration. This study integrates modeling and measurement tools that monitor ecosystem processes at finer temporal resolution than has previously been possible, complementing other studies that use experimental incubation and elemental tracers. Extension of this approach could enhance models that aim to integrate biological and physical processes in assessment of water quality and prediction of phytoplankton biomass.

Local adaptation at higher trophic levels: contrasting hyperparasite–pathogen infection dynamics in the field and laboratory

Predicting and controlling infectious disease epidemics is a major challenge facing the management of agriculture, human and wildlife health. Co‐evolutionarily derived patterns of local adaptation among pathogen populations have the potential to generate variation in disease epidemiology; however, studies of local adaptation in disease systems have mostly focused on interactions between competing pathogens or pathogens and their hosts. In nature, parasites and pathogens are also subject to attack by hyperparasitic natural enemies that can severely impact upon their infection dynamics. However, few studies have investigated whether this interaction varies across combinations of pathogen–hyperparasite strains, and whether this influences hyperparasite incidence in natural pathogen populations. Here, we test whether the association between a hyperparasitic fungus, Ampelomyces, and a single powdery mildew host, Podosphaera plantaginis, varies among genotype combinations, and whether this drives hyperparasite incidence in nature. Laboratory inoculation studies reveal that genotype, genotype × genotype interactions and local adaptation affect hyperparasite infection. However, observations of a natural pathogen metapopulation reveal that spatial rather than genetic factors predict the risk of hyperparasite presence. Our results highlight how sensitive the outcome of biocontrol using hyperparasites is to selection of hyperparasite strains.

Parasites destabilize host populations by shifting stage‐structured interactions

Should parasites stabilize or destabilize consumer-resource dynamics? Recent theory suggests that parasite-enhanced mortality may confer underappreciated stability to their hosts. We tested this hypothesis using disease in zooplankton. Across both natural and experimental epidemics, bigger epidemics correlated with larger--not smaller--host fluctuations. Thus, we tested two mechanistic hypotheses to explain destabilization or apparent destabilization by parasites. First, enrichment could, in principle, simultaneously enhance both instability and disease prevalence. In natural epidemics, destabilization was correlated with enrichment (indexed by total phosphorous). However, an in situ (lake enclosure) experiment did not support these links. Instead, field and experimental results point to a novel destabilizing mechanism involving host stage structure. Epidemics pushed hosts from relatively more stable host dynamics with less-synchronized juveniles and adults to less stable dynamics with more-synchronized juveniles and adults. Our results demonstrate how links between host stage structure and disease can shape host/consumer-resource stability.