Priority effects within coinfected hosts can drive unexpected population‐scale patterns of parasite prevalence

Organisms are frequently coinfected by multiple parasite strains and species, and interactions between parasites within hosts are known to influence parasite prevalence and diversity, as well as epidemic timing. Importantly, interactions between coinfecting parasites can be affected by the order in which they infect hosts (i.e. within‐host priority effects). In this study, we use a single‐host, two‐pathogen, SI model with environmental transmission to explore how within‐host priority effects scale up to alter host population‐scale infection patterns. Specifically, we ask how parasite prevalence changes in the presence of different types of priority effects. We consider two scenarios without priority effects and four scenarios with priority effects where there is either an advantage or a disadvantage to being the first to infect in a coinfected host. Models without priority effects always predict negative relationships between the prevalences of both parasites. In contrast, models with priority effects can yield unimodal prevalence relationships where the prevalence of a focal parasite is minimized or maximized at intermediate prevalences of a coinfecting parasite. The mechanism behind this pattern is that as the prevalence of the coinfecting parasite increases, most infections of the focal parasite change from occurring as solo infections, to first arrival coinfections, to second arrival coinfections. The corresponding changes in parasite fitness as the focal parasite moves from one infection class to another then map to changes in focal parasite prevalence. Further, we found that even when parasites interact negatively within a host, they still can have positive prevalence relationships at the population scale. These results suggest that within‐host priority effects can change host population‐scale infection patterns in systematic (and initially counterintuitive) ways, and that taking them into account may improve disease forecasting in coinfected populations.     

Niche theory for within-host parasite dynamics: Analogies to food web modules via feedback loops

Why do parasites exhibit a wide dynamical range within their hosts? For instance, why does infecting dose either lead to infection or immune clearance? Why do some parasites exhibit boom-bust, oscillatory dynamics? What maintains parasite diversity, that is coinfection v single infection due to exclusion or priority effects? For insights on parasite dose, dynamics and diversity governing within-host infection, we turn to niche models. An omnivory food web model (IGP) blueprints one parasite competing with immune cells for host energy (PIE). Similarly, a competition model (keystone predation, KP) mirrors a new coinfection model (2PIE). We then drew analogies between models using feedback loops. The following three points arise: first, like in IGP, parasites oscillate when longer loops through parasites, immune cells and resource regulate parasite growth. Shorter, self-limitation loops (involving resources and enemies) stabilise those oscillations. Second, IGP can produce priority effects that resemble immune clearance. But, despite comparable loop structure, PIE cannot due to constraints imposed by production of immune cells. Third, despite somewhat different loop structure, KP and 2PIE share apparent and resource competition mechanisms that produce coexistence (coinfection) or priority effects of prey or parasites. Together, this mechanistic niche framework for within-host dynamics offers new perspective to improve individual health.     

Mixed infection,risk projection,and misdirection: Interactions among pathogens alter links between host resources and disease

A growing body of literature links resources of hosts to their risk of infectious disease. Yet most hosts encounter multiple pathogens, and projections of disease risk based on resource availability could be fundamentally wrong if they do not account for interactions among pathogens within hosts. Here, we measured infection risk of grass hosts (Avena sativa) exposed to three naturally co‐occurring viruses either singly or jointly (barley and cereal yellow dwarf viruses [B/CYDVs]: CYDV‐RPV, BYDV‐PAV, and BYDV‐SGV) along experimental gradients of nitrogen and phosphorus supply. We asked whether disease risk (i.e., infection prevalence) differed in single versus co‐inoculations, and whether these differences varied with rates and ratios of nitrogen and phosphorus supply. In single inoculations, the viruses did not respond strongly to nitrogen or phosphorus. However, in co‐inoculations, we detected illustrative cases of 1) resource‐dependent antagonism (lower prevalence of RPV with increasing N; possibly due to competition), 2) resource‐dependent facilitation (higher prevalence of SGV with decreasing N:P; possibly due to immunosuppression), and 3) weak or no interactions within hosts (for PAV). Together, these within‐host interactions created emergent patterns for co‐inoculated hosts, with both infection prevalence and viral richness increasing with the combination of low nitrogen and high phosphorus supply. We demonstrate that knowledge of multiple pathogens is essential for predicting disease risk from host resources and that projections of risk that fail to acknowledge resource‐dependent interactions within hosts could be qualitatively wrong. Expansions of theory from community ecology theory may help anticipate such relationships by linking host resources to diverse pathogen communities.     

Parasite predators exhibit a rapid numerical response to increased parasite abundance and reduce transmission to hosts

Predators of parasites have recently gained attention as important parts of food webs and ecosystems. In aquatic systems, many taxa consume free‐living stages of parasites, and can thus reduce parasite transmission to hosts. However, the importance of the functional and numerical responses of parasite predators to disease dynamics is not well understood. We collected host–parasite–predator cooccurrence data from the field, and then experimentally manipulated predator abundance, parasite abundance, and the presence of alternative prey to determine the consequences for parasite transmission. The parasite predator of interest was a ubiquitous symbiotic oligochaete of mollusks, Chaetogaster limnaei limnaei, which inhabits host shells and consumes larval trematode parasites. Predators exhibited a rapid numerical response, where predator populations increased or decreased by as much as 60% in just 5 days, depending on the parasite:predator ratio. Furthermore, snail infection decreased substantially with increasing parasite predator densities, where the highest predator densities reduced infection by up to 89%. Predators of parasites can play an important role in regulating parasite transmission, even when infection risk is high, and especially when predators can rapidly respond numerically to resource pulses. We suggest that these types of interactions might have cascading effects on entire disease systems, and emphasize the importance of considering disease dynamics at the community level.     

Shifts from competition to facilitation between a foundation tree and a pioneer shrub across spatial and temporal scales in a semiarid woodland

* Theoretical and empirical research has supported the hypothesis that plant-plant interactions change from competition to facilitation with increasing abiotic stress. However, the consistency of such changes has been questioned in arid and semiarid ecosystems. * During a drought in the semiarid south-western USA, we used observations and a field experiment to examine the interactions between juveniles of a foundation tree (Pinyon pine, Pinus edulis) and a common shrub (Apache plume, Fallugia paradoxa) in replicated areas of high and low stress. * The presence of F. paradoxa reduced P. edulis performance at low-stress sites, but had the opposite effect at high-stress sites. However, the intensity of the interactions depended on temporal variation in climate and age of P. edulis. Both above- and below-ground factors contributed to competition, while only above-ground factors contributed to facilitation. * These results support the hypothesis that interactions can change from competition to facilitation as abiotic stress increases in semiarid environments. A shift from competition to facilitation may be important for the recovery of P. edulis and other foundation species that have experienced large-scale mortality during recent droughts.     

Parental effects in Pieris rapae in response to variation in food quality: adaptive plasticity across generations?

1. Herbivores using seasonal resources must cope with variation in the quality of their host plants. The effects of variation in protein concentration of artificial diet and glucosinolate concentration in canola, Brassica napus, on Pieris rapae parental and progeny growth were investigated. 2. The hypothesis that parents respond to variation in food quality by altering the phenotype of their progeny to enhance progeny fitness was tested. Consistent with previous studies, P. rapae was not affected strongly by variation in the protein concentration of artificial diet and had equal mass on completing development. 3. The mass of individual eggs of P. rapae progeny was correlated negatively with the amount of protein in the diet on which parents fed. Moreover, mothers reared in extreme conditions (high and low protein) produced progeny that grew best under those conditions. These potentially adaptive parental effects were detected early in progeny growth but not later in their development. 4. Early larval growth of P. rapae was affected negatively by increasing glucosinolates in B. napus plants, although no effects of glucosinolates were detected later in growth or on the progeny's phenotype. 5. Thus, evidence is presented that variation in food quality (protein concentration) has major consequences for the progeny of P. rapae. Given the multivoltine life history of P. rapae and the seasonal differences in food quality it encounters, such parental effects may be adaptive.     

Biotic context and soil properties modulate native plant responses to enhanced rainfall

Background and Aims The environmental and biotic context within which plants grow have a great potential to modify responses to climatic changes, yet few studies have addressed both the direct effects of climate and the modulating roles played by variation in the biotic (e.g. competitors) and abiotic (e.g. soils) environment.Methods In a grassland with highly heterogeneous soils and community composition, small seedlings of two native plants, Lasthenia californica and Calycadenia pauciflora, were transplanted into factorially watered and fertilized plots. Measurements were made to test how the effect of climatic variability (mimicked by the watering treatment) on the survival, growth and seed production of these species was modulated by above-ground competition and by edaphic variables.Key Results Increased competition outweighed the direct positive impacts of enhanced rainfall on most fitness measures for both species, resulting in no net effect of enhanced rainfall. Both species benefitted from enhanced rainfall when the absence of competitors was accompanied by high soil water retention capacity. Fertilization did not amplify the watering effects; rather, plants benefitted from enhanced rainfall or competitor removal only in ambient nutrient conditions with high soil water retention capacity.Conclusions The findings show that the direct effects of climatic variability on plant fitness may be reversed or neutralized by competition and, in addition, may be strongly modulated by soil variation. Specifically, coarse soil texture was identified as a factor that may limit plant responsiveness to altered water availability. These results highlight the importance of considering the abiotic as well as biotic context when making future climate change forecasts.