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
Timing and order of exposure to two echinostome species affect patterns of infection in larval amphibians
Abstract The study of priority effects with respect to coinfections is still in its infancy. Moreover, existing coinfection studies typically focus on infection outcomes associated with exposure to distinct sets of parasite species, despite that functionally and morphologically similar parasite species commonly coexist in nature. Therefore, it is important to understand how interactions between similar parasites influence infection outcomes. Surveys at seven ponds in northwest Pennsylvania found that multiple species of echinostomes commonly co-occur. Using a larval anuran host ( Rana pipiens ) and the two most commonly identified echinostome species from our field surveys ( Echinostoma trivolvis and Echinoparyphium lineage 3), we examined how species composition and timing of exposure affect patterns of infection. When tadpoles were exposed to both parasites simultaneously, infection loads were higher than when exposed to Echinoparyphium alone but similar to being exposed to Echinostoma alone. When tadpoles were sequentially exposed to the parasite species, tadpoles first exposed to Echinoparyphium had 23% lower infection loads than tadpoles first exposed to Echinostoma . These findings demonstrate that exposure timing and order, even with similar parasites, can influence coinfection outcomes, and emphasize the importance of using molecular methods to identify parasites for ecological studies.
more »
« less
- PAR ID:
- 10250181
- Date Published:
- Journal Name:
- Parasitology
- Volume:
- 147
- Issue:
- 13
- ISSN:
- 0031-1820
- Page Range / eLocation ID:
- 1515 to 1523
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Synopsis The emergence and spread of infectious diseases is a significant contributor to global amphibian declines, requiring increased surveillance and research. We assessed host–vector–parasite dynamics using a population of eastern hellbender salamanders (Cryptobranchus alleganiensis) that harbor leeches (Placobdella appalachiensis) that transmit endoparasitic blood parasites (Trypanosoma spp) to the host, with coinfection frequently occurring. We centered our study on adult males throughout their extended 8-month paternal care period because recent research indicates that nest failure caused by lack of paternal care and filial cannibalism is contributing to hellbender population declines. Recognizing the potential for parasites to modulate host physiology and behavior, we explored how infection severity influences paternal health and reproductive success. We assessed white blood cell profiles of adult male hellbenders in response to parasites, coinfection, and seasonal temperature fluctuations, while also investigating whether parasite infection or coinfection was predictive of nest success. We found that hellbenders exhibited seasonal shifts in white blood cell indices; as temperatures increased across seasons (from 5°C to 20°C), the proportion of neutrophils and eosinophils decreased (by 14% and 46%, respectively) in circulation while the proportion of lymphocytes and basophils increased (by 8% and 101%, respectively). Moreover, the proportion of neutrophil precursors increased by 80% under colder temperatures, which signifies seasonal immune cell recruitment. We demonstrated that neutrophils and eosinophils increased while lymphocytes decreased in response to leech infection. However, as leech and trypanosome infection intensity increased together, the proportion of lymphocytes increased while neutrophils and eosinophils decreased, underscoring the complex interactions between coinfection and immune responses of hellbenders that warrant future research. Despite the influence of infection and coinfection on hellbender physiology, we detected no evidence to support the hypothesis that parasites influence the likelihood of nest failure or whole-clutch filial cannibalism. In light of amphibian declines being exacerbated by climate change and disease, our study emphasizes the need to establish hematological reference values that account for physiological adaptations to seasonal fluctuations in temperature and different life history stages and to study the physiological responses of imperiled amphibian species to parasites.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
-
Immunity changes through ontogeny and can mediate facilitative and inhibitory interactions among co-infecting parasite species. In amphibians, most immune memory is not carried through metamorphosis, leading to variation in the complexity of immune responses across life stages. To test if the ontogeny of host immunity might drive interactions among co-infecting parasites, we simultaneously exposed Cuban treefrogs ( Osteopilus septentrionalis ) to a fungus ( Batrachochytrium dendrobaditis , Bd) and a nematode ( Aplectana hamatospicula ) at tadpole, metamorphic and post-metamorphic life stages. We measured metrics of host immunity, host health and parasite abundance. We predicted facilitative interactions between co-infecting parasites as the different immune responses hosts mount to combat these infectious are energetically challenging to mount simultaneously. We found ontogenetic differences in IgY levels and cellular immunity but no evidence that metamorphic frogs were more immunosuppressed than tadpoles. There was also little evidence that these parasites facilitated one another and no evidence that A. hamatospicula infection altered host immunity or health. However, Bd, which is known to be immunosuppressive, decreased immunity in metamorphic frogs. This made metamorphic frogs both less resistant and less tolerant of Bd infection than the other life stages. These findings indicate that changes in immunity altered host responses to parasite exposures throughout ontogeny. This article is part of the theme issue ‘Amphibian immunity: stress, disease and ecoimmunology’.more » « less
-
Abstract Host populations often vary in the magnitude of coinfection they experience across environmental gradients. Furthermore, coinfection often occurs sequentially, with a second parasite infecting the host after the first has established a primary infection. Because the local environment and interactions between coinfecting parasites can both drive patterns of coinfection, it is important to disentangle the relative contributions of environmental factors and within‐host interactions to patterns of coinfection.Here, we develop a conceptual framework and present an empirical case study to disentangle these facets of coinfection. Across multiple lakes, we surveyed populations of five damselfly (host) species and quantified primary parasitism by aquatic, ectoparasitic water mites and secondary parasitism by terrestrial, endoparasitic gregarines. We first asked if coinfection is predicted by abiotic and biotic factors within the local environment, finding that the probability of coinfection decreased for all host species as pH increased. We then asked if primary infection by aquatic water mites mediated the relationship between pH and secondary infection by terrestrial gregarines.Contrary to our expectations, we found no evidence for a water mite‐mediated relationship between pH and gregarines. Instead, the intensity of gregarine infection correlated solely with the local environment, with the magnitude and direction of these relationships varying among environmental predictors.Our findings emphasize the role of the local environment in shaping infection dynamics that set the stage for coinfection. Although we did not detect within‐host interactions, the approach herein can be applied to other systems to elucidate the nature of interactions between hosts and coinfecting parasites within complex ecological communities.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1017/S0031182020001092
