An official website of the United States government
Abstract 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 coinfectionvsingle 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.
more »
« less
Dose relationships can exacerbate, mute, or reverse the impact of heterospecific host density on infection prevalence
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.
more »
« less
- PAR ID:
- 10450150
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecology
- Volume:
- 102
- Issue:
- 8
- ISSN:
- 0012-9658
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Transmission from one host to another is a crucial component of parasite fitness. For some aquatic parasites, transmission occurs via a free‐living stage that spends time in the water, awaiting an encounter with a new host. These parasite transmission stages can be impacted by biotic and abiotic factors that influence the parasite's ability to successfully infect or grow in a new host.Here we tested whether time spent in the water column and/or exposure to common cyanobacterial toxins impacted parasite transmission stages. More specifically, we tested whether the infectivity, within host growth, and virulence of the fungal parasiteMetschnikowia bicuspidatachanged as a result of time spent in the water or from exposure to cyanotoxins in the water column. We exposed parasite transmission spores to different levels of one of two ecologically important cyanotoxins, microcystin‐LR and anatoxin‐a, and factorially manipulated the amount of time spores were incubated in water. We removed the toxins and used those same spores to infect one genotype of the common lake zooplanktonDaphnia dentifera.We found that cyanotoxins did not impact parasite fitness (infection prevalence and spore yield per infected host) or virulence (host lifetime reproduction and survivorship) at the tested concentrations (10 and 30 μg/L). However, we found that spending longer as a transmission spore decreased a spore's chances for successful infection: spores that were only incubated for 24 hr infected approximately 75% of exposed hosts, whereas spores incubated for 10 days infected less than 50% of exposed hosts.We also found a negative relationship between the final spore yield from infected hosts and the proportion of hosts that became infected. In treatments where spores spent longer in the water column prior to encountering a host, infection prevalence was lower (indicating lower per spore infectivity), but each infected host yielded more spores at the end of infection. We hypothesise that this pattern may result from intraspecific parasite competition within the host.Overall, these results suggest that transmission spores of this parasite are not strongly influenced by cyanotoxins in the water column, but that other aspects of spending time in the water strongly influence parasite fitness.more » « less
-
Abstract The relationship between infection prevalence and host age is informative because it can reveal processes underlying disease dynamics. Most prior work has assumed that age‐prevalence curves are shaped by infection rates, host immunity and/or infection‐induced mortality. Interactions between parasites within a host have largely been overlooked as a source of variation in age‐prevalence curves.We used field survey data and models to examine the role of interspecific interactions between parasites in shaping age‐prevalence curves. The empirical dataset included quantification of parasite infection prevalence for eight co‐occurring trematodes in over 15,000 snail hosts. We characterized age‐prevalence curves for each taxon, examined how they changed over space in relation to co‐occurring trematodes and tested whether the shape of the curves aligned with expectations for the frequencies of coinfections by two taxa in the same host. The models explored scenarios that included negative interspecific interactions between parasites, variation in the force‐of‐infection (FOI) and infection‐induced mortality that varied with host age, which were mechanisms hypothesized to be important in the empirical dataset.In the empirical dataset, four trematode parasites had monotonic increasing age‐prevalence curves and four had unimodal age‐prevalence curves. Some of the curves remained consistent in shape in relation to the prevalence of other potentially interacting trematodes, while some shifted from unimodal to monotonic increasing, suggesting release from negative interspecific interactions. The most common taxa with monotonic increasing curves had lower co‐infection frequencies than expected, suggesting they were competitively dominant. Taxa with unimodal curves had coinfection frequencies that were closer to those expected by chance.The model showed that negative interspecific interactions between parasites can cause a unimodal age‐prevalence curve in the subordinate taxon. Increases in the FOI and/or infection‐induced mortality of the dominant taxon cause shifts in the peak prevalence of the subordinate taxon to a younger host age. Infection‐induced mortality that increased with host age was the only scenario that caused a unimodal curve in the dominant taxon.Results indicated that negative interspecific interactions between parasites contributed to variation in the shape of age‐prevalence curves across parasite taxa and support the growing importance of incorporating interactions between parasites in explaining population‐level patterns of host infection over space and time. Read the freePlain Language Summaryfor this article on the Journal blog.more » « less
-
Infection duration affects individual host fitness and between-host transmission. Whether an infection is cleared or becomes chronic depends on the complex interaction between host immune responses and parasite growth. Empirical and theoretical studies have suggested that there are critical thresholds of parasite dose that can determine clearance versus chronicity, driven by the ability of the parasite to manipulate host immunity. However, the mammalian immune response is characterized by strong positive and negative feedback loops that could generate duration thresholds even in the absence of direct immunomodulation. Here, we derive and analyse a simple model for the interaction between T-cell subpopulations and parasite growth. We show that whether an infection is cleared or not is very sensitive to the initial immune state, parasite dose and strength of immunological feedbacks. In particular, chronic infections are possible even when parasites provoke a strong and effective immune response and lack any ability to immunomodulate. Our findings indicate that the initial immune state, which often goes unmeasured in empirical studies, is a critical determinant of infection duration. This work also has implications for epidemiological models, as it implies that infection duration will be highly variable among individuals, and dependent on each individual’s infection history.more » « less
-
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.more » « less
