The consequences of parasite infection for individual hosts depend on key features of host–parasite ecology underpinning parasite growth and immune defense, such as age, sex, resource supply, and environmental stressors. Scaling these features and their underlying mechanisms from the individual host is challenging but necessary, as they shape parasite transmission at the population level. Translating individual-level mechanisms across scales could inherently improve the way we think about feedbacks among parasitism, the mechanisms driving transmission, and the consequences of human impact and disease control efforts. Here, we use individual-based models (IBMs) based on general metabolic theory, Dynamic Energy Budget (DEB) theory, to scale explicit life-history features of individual hosts, such as growth, reproduction, parasite production, and death, to parasite transmission at the population level over a range of resource supplies focusing on the major human parasite, Schistosoma mansoni, and its intermediate host snail, Biomphalaria glabrata. At the individual level, infected hosts produce fewer parasites at lower resources as competition increases. At the population level, our DEB–IBM predicts brief, but intense parasite peaks early during the host growth season when resources are abundant and infected hosts are few. The timing of these peaks challenges the status quo that high densities of infected hosts produce the highest parasite densities. As expected, high resource supply boosts parasite output, but parasite output also peaks at modest to high host background mortality rates, which parallels overcompensation in stage-structured models. Our combined results reveal the crucial role of individual-level physiology in identifying how environmental conditions, time of the year, and key feedbacks within host–parasite ecology interact to define periods of elevated risk. The testable forecasts from this physiologically-explicit epidemiological model can inform disease management to reduce human risk of schistosome infection.
Individuals experience heterogeneous environmental conditions that can affect within-host processes such as immune defense against parasite infection. Variation among individuals in parasite shedding can cause some hosts to contribute disproportionately to population-level transmission, but we currently lack mechanistic theory that predicts when environmental conditions can result in large disease outbreaks through the formation of immunocompromised superspreading individuals. Here, I present a within-host model of a microparasite’s interaction with the immune system that links an individual host’s resource intake to its infectious period. For environmental scenarios driving population-level heterogeneity in resource intake (resource scarcity and resource subsidy relative to baseline availability), I generate a distribution of infectious periods and simulate epidemics on these heterogeneous populations. I find that resource scarcity can result in large epidemics through creation of superspreading individuals, while resource subsidies can reduce or prevent transmission of parasites close to their invasion threshold by homogenizing resource allocation to immune defense. Importantly, failure to account for heterogeneity in competence can result in under-prediction of outbreak size, especially when parasites are close to their invasion threshold. More generally, this framework suggests that differences in conditions experienced by individual hosts can lead to superspreading via differences in resource allocation to immune defense alone, even in the absence of other heterogeneites such as host contacts.
more » « less- NSF-PAR ID:
- 10114803
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- ISSN:
- 1540-7063
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract The prevalence and intensity of parasites in wild hosts varies across space and is a key determinant of infection risk in humans, domestic animals and threatened wildlife. Because the immune system serves as the primary barrier to infection, replication and transmission following exposure, we here consider the environmental drivers of immunity. Spatial variation in parasite pressure, abiotic and biotic conditions, and anthropogenic factors can all shape immunity across spatial scales. Identifying the most important spatial drivers of immunity could help pre‐empt infectious disease risks, especially in the context of how large‐scale factors such as urbanization affect defence by changing environmental conditions.
We provide a synthesis of how to apply macroecological approaches to the study of ecoimmunology (i.e. macroimmunology). We first review spatial factors that could generate spatial variation in defence, highlighting the need for large‐scale studies that can differentiate competing environmental predictors of immunity and detailing contexts where this approach might be favoured over small‐scale experimental studies. We next conduct a systematic review of the literature to assess the frequency of spatial studies and to classify them according to taxa, immune measures, spatial replication and extent, and statistical methods.
We review 210 ecoimmunology studies sampling multiple host populations. We show that whereas spatial approaches are relatively common, spatial replication is generally low and unlikely to provide sufficient environmental variation or power to differentiate competing spatial hypotheses. We also highlight statistical biases in macroimmunology, in that few studies characterize and account for spatial dependence statistically, potentially affecting inferences for the relationships between environmental conditions and immune defence.
We use these findings to describe tools from geostatistics and spatial modelling that can improve inference about the associations between environmental and immunological variation. In particular, we emphasize exploratory tools that can guide spatial sampling and highlight the need for greater use of mixed‐effects models that account for spatial variability while also allowing researchers to account for both individual‐ and habitat‐level covariates.
We finally discuss future research priorities for macroimmunology, including focusing on latitudinal gradients, range expansions and urbanization as being especially amenable to large‐scale spatial approaches. Methodologically, we highlight critical opportunities posed by assessing spatial variation in host tolerance, using metagenomics to quantify spatial variation in parasite pressure, coupling large‐scale field studies with small‐scale field experiments and longitudinal approaches, and applying statistical tools from macroecology and meta‐analysis to identify generalizable spatial patterns. Such work will facilitate scaling ecoimmunology from individual‐ to habitat‐level insights about the drivers of immune defence and help predict where environmental change may most alter infectious disease risk.
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Community composition is driven by a few key assembly processes: ecological selection, drift and dispersal. Nested parasite communities represent a powerful study system for understanding the relative importance of these processes and their relationship with biological scale. Quantifying β‐diversity across scales and over time additionally offers mechanistic insights into the ecological processes shaping the distributions of parasites and therefore infectious disease. To examine factors driving parasite community composition, we quantified the parasite communities of 959 amphibian hosts representing two species (the Pacific chorus frog, Pseudacris regilla and the California newt, Taricha torosa) sampled over 3 months from 10 ponds in California. Using additive partitioning, we estimated how much of regional parasite richness (γ‐diversity) was composed of within‐host parasite richness (α‐diversity) and turnover (β‐diversity) at three biological scales: across host individuals, across species and across habitat patches (ponds). We also examined how β‐diversity varied across time at each biological scale. Differences among ponds comprised the majority (40%) of regional parasite diversity, followed by differences among host species (23%) and among host individuals (12%). Host species supported parasite communities that were less similar than expected by null models, consistent with ecological selection, although these differences lessened through time, likely due to high dispersal rates of infectious stages. Host individuals within the same population supported more similar parasite communities than expected, suggesting that host heterogeneity did not strongly impact parasite community composition and that dispersal was high at the individual host-level. Despite the small population sizes of within‐host parasite communities, drift appeared to play a minimal role in structuring community composition. Dispersal and ecological selection appear to jointly drive parasite community assembly, particularly at larger biological scales. The dispersal ability of aquatic parasites with complex life cycles differs strongly across scales, meaning that parasite communities may predictably converge at small scales where dispersal is high, but may be more stochastic and unpredictable at larger scales. Insights into assembly mechanisms within multi‐host, multi‐parasite systems provide opportunities for understanding how to mitigate the spread of infectious diseases within human and wildlife hosts.more » « less
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Abstract Community composition is driven by a few key assembly processes: ecological selection, drift and dispersal. Nested parasite communities represent a powerful study system for understanding the relative importance of these processes and their relationship with biological scale. Quantifying
β ‐diversity across scales and over time additionally offers mechanistic insights into the ecological processes shaping the distributions of parasites and therefore infectious disease.To examine factors driving parasite community composition, we quantified the parasite communities of 959 amphibian hosts representing two species (the Pacific chorus frog,
Pseudacris regilla and the California newt,Taricha torosa ) sampled over 3 months from 10 ponds in California. Using additive partitioning, we estimated how much of regional parasite richness (γ ‐diversity) was composed of within‐host parasite richness (α ‐diversity) and turnover (β ‐diversity) at three biological scales: across host individuals, across species and across habitat patches (ponds). We also examined howβ ‐diversity varied across time at each biological scale.Differences among ponds comprised the majority (40%) of regional parasite diversity, followed by differences among host species (23%) and among host individuals (12%). Host species supported parasite communities that were less similar than expected by null models, consistent with ecological selection, although these differences lessened through time, likely due to high dispersal rates of infectious stages. Host individuals within the same population supported more similar parasite communities than expected, suggesting that host heterogeneity did not strongly impact parasite community composition and that dispersal was high at the individual host-level. Despite the small population sizes of within‐host parasite communities, drift appeared to play a minimal role in structuring community composition.
Dispersal and ecological selection appear to jointly drive parasite community assembly, particularly at larger biological scales. The dispersal ability of aquatic parasites with complex life cycles differs strongly across scales, meaning that parasite communities may predictably converge at small scales where dispersal is high, but may be more stochastic and unpredictable at larger scales. Insights into assembly mechanisms within multi‐host, multi‐parasite systems provide opportunities for understanding how to mitigate the spread of infectious diseases within human and wildlife hosts.
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Abstract The immune system is the primary barrier to parasite infection, replication, and transmission following exposure, and variation in immunity can accordingly manifest in heterogeneity in traits that govern population-level infectious disease dynamics. While much work in ecoimmunology has focused on individual-level determinants of host immune defense (e.g., reproductive status and body condition), an ongoing challenge remains to understand the broader evolutionary and ecological contexts of this variation (e.g., phylogenetic relatedness and landscape heterogeneity) and to connect these differences into epidemiological frameworks. Ultimately, such efforts could illuminate general principles about the drivers of host defense and improve predictions and control of infectious disease. Here, we highlight recent work that synthesizes the complex drivers of immunological variation across biological scales of organization and scales these within-host differences to population-level infection outcomes. Such studies note the limitations involved in making species-level comparisons of immune phenotypes, stress the importance of spatial scale for immunology research, showcase several statistical tools for translating within-host data into epidemiological parameters, and provide theoretical frameworks for linking within- and between-host scales of infection processes. Building from these studies, we highlight several promising avenues for continued work, including the application of machine learning tools and phylogenetically controlled meta-analyses to immunology data and quantifying the joint spatial and temporal dependencies in immune defense using range expansions as model systems. We also emphasize the use of organismal traits (e.g., host tolerance, competence, and resistance) as a way to interlink various scales of analysis. Such continued collaboration and disciplinary cross-talk among ecoimmunology, disease ecology, and mathematical modeling will facilitate an improved understanding of the multi-scale drivers and consequences of variation in host defense.
