Effects of microclimate on disease prevalence across an urbanization gradient.

Increased temperatures associated with urbanization (the "urban heat island" effect) have been shown to impact a wide range of traits across diverse taxa. At the same time, climatic conditions vary at fine spatial scales within habitats due to factors including shade from shrubs, trees, and built structures. Patches of shade may function as microclimate refugia that allow species to occur in habitats where high temperatures and/or exposure to ultraviolet radiation would otherwise be prohibitive. However, the importance of shaded microhabitats for interactions between species across urbanized landscapes remains poorly understood. Weedy plants and their foliar pathogens are a tractable system for studying how multiple scales of climatic variation influence infection prevalence. Powdery mildew pathogens are particularly well suited to this work, as these fungi can be visibly diagnosed on leaf surfaces. We studied the effects of shaded microclimates on rates of powdery mildew infection on Plantago host species in (1) "pandemic pivot" surveys in which undergraduate students recorded shade and infection status of thousands of plants along road verges in urban and suburban residential neighborhoods, (2) monthly surveys of plant populations in 22 parks along an urbanization gradient, and (3) a manipulative field experiment directly testing the effects of shade on the growth and transmission of powdery mildew. Together, our field survey results show strong positive effects of shade on mildew infection in wild Plantago populations across urban, suburban, and rural habitats. Our experiment suggests that this relationship is causal, where microclimate conditions associated with shade promote pathogen growth. Overall, infection prevalence increased with urbanization despite a negative association between urbanization and tree cover at the landscape scale. These findings highlight the importance of taking microclimate heterogeneity into account when establishing links between macroclimate or land use context and prevalence of disease.

Pathways linking nutrient enrichment, habitat structure, and parasitism to host-resource interactions.

Human activities simultaneously alter nutrient levels, habitat structure, and levels of parasitism. These activities likely have individual and joint impacts on food webs. Furthermore, there is particular concern that nutrient additions and changes to habitat structure might exacerbate the size of epidemics and impacts on host density. We used a well-studied zooplankton-fungus host-parasite system and experimental whole water column enclosures to factorially manipulate nutrient levels, habitat structure (specifically: mixing), and presence of parasites. Nutrient addition increased infection prevalence, density of infected hosts, and total host density. We hypothesized that nutrients, mixing, and parasitism were linked in multiple ways, including via their combined effects on phytoplankton (resource) abundance, and we used structural equation modeling to disentangle these pathways. In the absence of the parasite, both nutrients and mixing increased abundance of phytoplankton, whereas host density was negatively related to phytoplankton abundance, suggesting a mixture of bottom-up and top-down control of phytoplankton. In the presence of the parasite, nutrients still increased phytoplankton abundance but mixing no longer did, and there was no longer a significant relationship between host density and phytoplankton. This decoupling of host-resource dynamics may have resulted from reduced grazing due to illness-mediated changes in feeding behavior. Overall, our results show that the impact of one human activity (e.g., altered habitat structure) might depend on other human impacts (e.g., parasite introduction). Fortunately, carefully designed experiments and analyses can help tease apart these multifaceted relationships, allowing us to understand how human activities alter food webs, including interactions between hosts and their parasites and resources.

Sublethal effects of parasitism on ruminants can have cascading consequences for ecosystems.

Parasitic infections are common, but how they shape ecosystem-level processes is understudied. Using a mathematical model and meta-analysis, we explored the potential for helminth parasites to trigger trophic cascades through lethal and sublethal effects imposed on herbivorous ruminant hosts after infection. First, using the model, we linked negative effects of parasitic infection on host survival, fecundity, and feeding rate to host and producer biomass. Our model, parameterized with data from a well-documented producer­caribou­helminth system, reveals that even moderate impacts of parasites on host survival, fecundity, or feeding rate can have cascading effects on ruminant host and producer biomass. Second, using meta-analysis, we investigated the links between helminth infections and traits of free-living ruminant hosts in nature. We found that helminth infections tend to exert negative but sublethal effects on ruminant hosts. Specifically, infection significantly reduces host feeding rates, body mass, and body condition but has weak and highly variable effects on survival and fecundity. Together, these findings suggest that while helminth parasites can trigger trophic cascades through multiple mechanisms, overlooked sublethal effects on nonreproductive traits likely dominate their impacts on ecosystems. In particular, by reducing ruminant herbivory, pervasive helminth infections may contribute to a greener world.

Virulent Disease Epidemics Can Increase Host Density by Depressing Foraging of Hosts.

AbstractAll else equal, parasites that harm host fitness should depress densities of their hosts. However, parasites that alter host traits may increase host density via indirect ecological interactions. Here, we show how depression of foraging rate of infected hosts can produce such a hydra effect. Using a foraging assay, we quantified reduced foraging rates of a zooplankton host infected with a virulent fungal parasite. We then parameterized a dynamical model of hosts, parasites, and resources with this foraging function, showing how foraging depression can create a hydra effect. Mathematically, the hydra arose when increased resource productivity exceeded any increase in resource consumption per host. Therefore, the foraging-mediated hydra effect more likely emerged (1) for hosts that strongly control logistic-like resources and (2) during larger epidemics of moderately virulent parasites. We then analyzed epidemics from 13 fungal epidemics in nature. We found evidence for a foraging-mediated hydra effect: large outbreaks depressed foraging rate and correlated with increased densities of both algal resources and Daphnia hosts. Therefore, depression of the foraging rate of infected hosts can produce higher host densities even during epidemics of parasites that increase host mortality. Such hydras might prevent the collapse of host populations but also could produce higher densities of infected hosts.

Plantago spp. as Models for Studying the Ecology and Evolution of Species Interactions across Environmental Gradients.

AbstractA central challenge in ecology and evolutionary biology is to understand how variation in abiotic and biotic factors combine to shape the distribution, abundance, and diversity of focal species. Environmental gradients, whether natural (e.g., latitude, elevation, ocean proximity) or anthropogenic (e.g., land-use intensity, urbanization), provide compelling settings for addressing this challenge. However, not all organisms are amenable to the observational and experimental approaches required for untangling the factors that structure species along gradients. Here we highlight herbaceous plants in the genus Plantago as models for studying the ecology and evolution of species interactions along abiotic gradients. Plantago lanceolata and P. major are native to Europe and Asia but distributed globally, and they are established models for studying population ecology and interactions with herbivores, pathogens, and soil microbes. Studying restricted range congeners in comparison with those cosmopolitan species can provide insight into abiotic and biotic determinants of range size and population structure. We highlight one such species, P. rugelii, which is endemic to eastern North America. We give an overview of the literature on these focal Plantago species and explain why they are logical candidates for studies of species interactions across environmental gradients. Finally, we emphasize collaborative and community science approaches that can facilitate such research and note the amenability of Plantago for authentic research projects in science education.

Model Systems in Ecology, Evolution, and Behavior: A Call for Diversity in Our Model Systems and Discipline.

AbstractEcologists and evolutionary biologists are fascinated by life's variation but also seek to understand phenomena and mechanisms that apply broadly across taxa. Model systems can help us extract generalities from amid all the wondrous diversity, but only if we choose and develop them carefully, use them wisely, and have a range of model systems from which to choose. In this introduction to the Special Feature on Model Systems in Ecology, Evolution, and Behavior (EEB), we begin by grappling with the question, What is a model system? We then explore where our model systems come from, in terms of the skills and other attributes required to develop them and the historical biases that influence traditional model systems in EEB. We emphasize the importance of communities of scientists in the success of model systems-narrow scientific communities can restrict the model organisms themselves. We also consider how our discipline was built around one type of "model scientist"-a history still reflected in the field. This lack of diversity in EEB is unjust and also narrows the field's perspective, including by restricting the questions asked and talents used to answer them. Increasing diversity, equity, and inclusion will require acting at many levels, including structural changes. Diversity in EEB, in both model systems and the scientists who use them, strengthens our discipline.

Infectious Diseases, Livestock, and Climate: A Vicious Cycle?

Ruminant livestock are a significant contributor to global methane emissions. Infectious diseases have the potential to exacerbate these contributions by elevating methane outputs associated with animal production. With the increasing spread of many infectious diseases, the emergence of a vicious climate-livestock-disease cycle is a looming threat.

Facilitative priority effects drive parasite assembly under coinfection.

Host individuals are often coinfected with diverse parasite assemblages, resulting in complex interactions among parasites within hosts. Within hosts, priority effects occur when the infection sequence alters the outcome of interactions among parasites. Yet, the role of host immunity in this process remains poorly understood. We hypothesized that the host response to the first infection could generate priority effects among parasites, altering the assembly of later-arriving strains during epidemics. We tested this by infecting sentinel host genotypes of Plantago lanceolata with strains of the fungal parasite Podosphaera plantaginis and measuring susceptibility to subsequent infection during experimental and natural epidemics. In these experiments, prior infection by one strain often increased susceptibility to other strains, and these facilitative priority effects altered the structure of parasite assemblages, but this effect depended on host genotype, host population and parasite genotype. Thus, host genotype, spatial structure and priority effects among strains all independently altered parasite assembly. Using a fine-scale survey and sampling of infections on wild hosts in several populations, we then identified a signal of facilitative priority effects, which altered parasite assembly during natural epidemics. Together, these results provide evidence that within-host priority effects of early-arriving strains can drive parasite assembly, with implications for how strain diversity is spatially and temporally distributed during epidemics.

Self-perpetuating ecological-evolutionary dynamics in an agricultural host-parasite system.

Ecological and evolutionary processes may become intertwined when they operate on similar time scales. Here we show ecological-evolutionary dynamics between parasitoids and aphids containing heritable symbionts that confer resistance against parasitism. In a large-scale field experiment, we manipulated the aphid's host plant to create ecological conditions that either favoured or disfavoured the parasitoid. The result was rapid evolutionary divergence of aphid resistance between treatment populations. Consistent with ecological-evolutionary dynamics, the resistant aphid populations then had reduced parasitism and increased population growth rates. We fit a model to quantify costs (reduced intrinsic rates of increase) and benefits of resistance. We also performed genetic assays on 5 years of field samples that showed persistent but highly variable frequencies of aphid clones containing protective symbionts; these patterns were consistent with simulations from the model. Our results show (1) rapid evolution that is intertwined with ecological dynamics and (2) variation in selection that prevents traits from becoming fixed, which together generate self-perpetuating ecological-evolutionary dynamics.

Manipulating host resistance structure reveals impact of pathogen dispersal and environmental heterogeneity on epidemics.

Understanding how variation in hosts, parasites, and the environment shapes patterns of disease is key to predicting ecological and evolutionary outcomes of epidemics. Yet in spatially structured populations, variation in host resistance may be spatially confounded with variation in parasite dispersal and environmental factors that affect disease processes. To tease apart these disease drivers, we paired surveys of natural epidemics with experiments manipulating spatial variation in host susceptibility to infection. We mapped epidemics of the wind-dispersed powdery mildew pathogen Podosphaera plantaginis in five populations of its plant host, Plantago lanceolata. At 15 replicate sites within each population, we deployed groups of healthy potted 'sentinel' plants from five allopatric host lines. By tracking which sentinels became infected in the field and measuring pathogen connectivity and microclimate at those sites, we could test how variation in these factors affected disease when spatial variation in host resistance and soil conditions was minimized. We found that the prevalence and severity of sentinel infection varied over small spatial scales in the field populations, largely due to heterogeneity in pathogen prevalence on wild plants and unmeasured environmental factors. Microclimate was critical for disease spread only at the onset of epidemics, where humidity increased infection risk. Sentinels were more likely to become infected than initially healthy wild plants at a given field site. However, in a follow-up laboratory inoculation study we detected no significant differences between wild and sentinel plant lines in their qualitative susceptibility to pathogen isolates from the field populations, suggesting that primarily non-genetic differences between sentinel and wild hosts drove their differential infection rates in the field. Our study leverages a multi-faceted experimental approach to disentangle important biotic and abiotic drivers of disease patterns within wild populations.

Allocation, not male resistance, increases male frequency during epidemics: a case study in facultatively sexual hosts.

Why do natural populations vary in the frequency of sexual reproduction? Virulent parasites may help explain why sex is favored during disease epidemics. To illustrate, we show a higher frequency of males and sexually produced offspring in natural populations of a facultative parthenogenetic host during fungal epidemics. In a multi-year survey of 32 lakes, the frequency of males (an index of sex) was higher in populations of zooplankton hosts with larger epidemics. A lake mesocosm experiment established causality: experimental epidemics produced a higher frequency of males relative to disease-free controls. One common explanation for such a pattern involves Red Queen (RQ) dynamics. However, this particular system lacks key genetic specificity mechanisms required for the RQ, so we evaluated two other hypotheses. First, individual females, when stressed by infection, could increase production of male offspring vs. female offspring (a tenant of the "Abandon Ship" theory). Data from a life table experiment supports this mechanism. Second, higher male frequency during epidemics could reflect a purely demographic process (illustrated with a demographic model): males could resist infection more than females (via size-based differences in resistance and mortality). However, we found no support for this resistance mechanism. A size-based model of resistance, parameterized with data, revealed why: higher male susceptibility negated the lower exposure (a size-based advantage) of males. These results suggest that parasite-mediated increases in allocation to sex by individual females, rather than male resistance, increased the frequency of sex during larger disease epidemics.

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.

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.

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.

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 season's 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.

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.

Ecological context influences epidemic size and parasite-driven evolution.

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.