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.
This content will become publicly available on January 5, 2025
As a consequence of ongoing climate change, heatwaves are predicted to increase in frequency, intensity, and duration in many regions. Such extreme events can shift organisms from thermal optima for physiology and behaviour, with the thermal stress hypothesis predicting reduced performance at temperatures where the maintenance of biological functions is energetically costly. Performance includes the ability to resist biotic stressors, including infectious diseases, with increased exposure to extreme temperatures having the potential to synergise with parasite infection. Climate change is a proposed threat to native bee pollinators, directly and through indirect effects on floral resources, but the thermal stress hypothesis, particularly pertaining to infectious disease resistance, has received limited attention. We exposed adult We demonstrate that survival and induced antibacterial immunity are reduced following heatwaves. Supporting that heatwave exposure compromised immunity, the cost of immune activation was thermal regime dependent, with survival costs in control but not heatwave exposed bees. However, in the face of real infections, an inability to mount an optimal immune response will be detrimental, which was reflected by increased trypanosomatid parasite infections following heatwave exposure. These results demonstrate interactions between heatwave exposure and bumblebee performance, including immune and infection outcomes. Thus, the health of bumblebee pollinator populations may be affected through altered interactions with parasites and pathogens, in addition to other effects of extreme manifestations of climate change.
- NSF-PAR ID:
- 10484472
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Journal of Animal Ecology
- Volume:
- 93
- Issue:
- 2
- ISSN:
- 0021-8790
- Format(s):
- Medium: X Size: p. 171-182
- Size(s):
- ["p. 171-182"]
- Sponsoring Org:
- National Science Foundation
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Abstract -
Can hot temperatures limit disease transmission? A test of mechanisms in a zooplankton–fungus systemmore » « less
Abstract Thermal ecology theory predicts that transmission of infectious diseases should respond unimodally to temperature, that is be maximized at intermediate temperatures and constrained at extreme low and high temperatures. However, empirical evidence linking hot temperatures to decreased transmission in nature remains limited.
We tested the hypothesis that hot temperatures constrain transmission in a zooplankton–fungus (
Daphnia dentifera–Metschnikowia bicuspidata ) disease system where autumnal epidemics typically start after lakes cool from their peak summer temperatures. This pattern suggested that maximally hot summer temperatures could be inhibiting disease spread.Using a series of laboratory experiments, we examined the effects of high temperatures on five mechanistic components of transmission. We found that (a) high temperatures increased exposure to parasites by speeding up foraging rate but (b) did not alter infection success post‐exposure. (c) High temperatures lowered parasite production (due to faster host death and an inferred delay in parasite growth). (d) Parasites made in hot conditions were less infectious to the next host (instilling a parasite ‘rearing’ or 'trans‐host' effect of temperature during the prior infection). (e) High temperatures in the free‐living stage also reduce parasite infectivity, either by killing or harming parasites.
We then assembled the five mechanisms into an index of disease spread. The resulting unimodal thermal response was most strongly driven by the rearing effect. Transmission peaked at intermediate hot temperatures (25–26°C) and then decreased at maximally hot temperatures (30–32°C). However, transmission at these maximally hot temperatures only trended slightly lower than the baseline control (20°C), which easily sustains epidemics in laboratory conditions and in nature. Overall, we conclude that while exposure to hot epilimnetic temperatures does somewhat constrain disease, we lack evidence that this effect fully explains the lack of summer epidemics in this natural system. This work demonstrates the importance of experimentally testing hypothesized mechanisms of thermal constraints on disease transmission. Furthermore, it cautions against drawing conclusions based on field patterns and theory alone.
A free
Plain Language Summary can be found within the Supporting Information of this article. -
Increasing ocean temperatures threaten coral reefs globally, but corals residing in habitats that experience high thermal variability are thought to be better adapted to survive climate-induced heat stress. Here, we used long-term ecological observations and in situ temperature data from Heron Island, southern Great Barrier Reef to investigate how temperature dynamics within various thermally variable vs. thermally stable reef habitats change during a marine heatwave and the resulting consequences for coral community survival. During the heatwave, thermally variable habitats experienced larger surges in daily mean and maxima temperatures compared to stable sites, including extreme hourly incursions up to 36.5 °C. The disproportionate increase in heat stress in variable habitats corresponded with greater subsequent declines in hard coral cover, including a three-times greater decline within the thermally variable Reef Flat (70%) and Deep Lagoon (83%) than within thermally stable habitats along sheltered and exposed areas of the reef slope (0.3–19%). Interestingly, the thermally variable Reef Crest experienced comparatively small declines (26%), avoiding the most severe tidal ponding and resultant heat stress likely due to proximity to the open ocean equating to lower seawater residence times, greater mixing, and/or increased flow. These results highlight that variable thermal regimes, and any acclimatization or adaptation to elevated temperatures that may lead to, do not necessarily equate to protection against bleaching and mortality during marine heatwaves. Instead, thermally stable habitats that have greater seawater exchange with the open ocean may offer the most protection to corals during the severe marine heatwaves that accompany a changing climate.more » « less
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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.
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Abstract External perturbations, such as multispecies infections or anthelmintic treatments, can alter host–parasite interactions with consequences on the dynamics of infection. While the overall profile of infection might appear fundamentally conserved at the host population level, perturbations can disproportionately affect components of parasite demography or host responses, and ultimately impact parasite fitness and long‐term persistence.
We took an immuno‐epidemiological approach to this reasoning and examined a rabbit–helminth system where animals were trickle‐dosed with either one or two helminth species, treated halfway through the experiment with an anthelmintic and reinfected one month later following the same initial regime. Parasite traits (body length and fecundity) and host immune responses (cytokines, transcription factors, antibodies) were quantified at fixed time points and compared before and after drug treatment, and between single and dual infections.
Findings indicated a resistant host phenotype to
Trichostrongylus retortaeformis where abundance, body length, and fecundity were regulated by a protective immune response. In contrast,Graphidium strigosum accumulated in the host and, while it stimulated a clear immune reaction, many genes were downregulated both following reinfection and in dual infection, suggestive of a low host resistance.External perturbations affected parasite fecundity, including body length and number of eggs in utero, more significantly than abundance; however, there was no consistency in the parasite‐immune relationships.
Disentangling the processes affecting parasite life history, and how they relate to host responses, can provide a better understanding of how external disturbances impact disease severity and transmission, and how parasites strategies adjust to secure persistence at the host and the population level.
