How Individual Variation in Host Tolerance Affects Competence to Transmit Parasites

Burgan, Sarah C.; Gervasi, Stephanie S.; Johnson, Leah R.; Martin, Lynn B.

doi:10.1086/701169

Cited by 25 publications

(27 citation statements)

References 100 publications

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“…Such work, alongside theory on resource variation and tolerance (Budischak & Cressler, 2018), highlights the need for future work in this area and to assess whether spatial variation in exposure has consistent effects. Alongside quantifying spatial parasite diversity, future studies on the macroecology of tolerance would also benefit from assessing spatial variation in parasite load (Burgan, Gervasi, Johnson, & Martin, 2019). Additionally, validations of biomarkers for these traits can facilitate more direct interpretations of how defence varies spatially.…”

Section: Methodological Recommendationsmentioning

confidence: 99%

Macroimmunology: The drivers and consequences of spatial patterns in wildlife immune defence

Becker

Albery

Kessler

et al. 2020

Journal of Animal Ecology

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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 immu...

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Section: Methodological Recommendationsmentioning

confidence: 99%

Macroimmunology: The drivers and consequences of spatial patterns in wildlife immune defence

Becker

Albery

Kessler

et al. 2020

Journal of Animal Ecology

Self Cite

100

122

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“…Many hosts are much less competent than their parasite burdens would suggest [13]. Some hosts tolerate infections well and shed many parasites in the right places and times to infect other hosts [14,15], but others, even those with high burdens, generate few infections because of particular behaviors or high mortality postinfection [9].…”

Section: Forms Of Ec and Their Biological Significancementioning

confidence: 99%

“…Parasite tolerance is a neglected aspect of host competence [14,15], probably because it is such a new concept to disease ecology. Tolerance is typically quantified by plotting a reaction norm between host fitness, health or performance (y axis) and parasite burden (x axis).…”

Section: Box 1 Parasite Tolerance and Host Competencementioning

confidence: 99%

Extreme Competence: Keystone Hosts of Infections

Martin

Addison

Bean

et al. 2019

Trends in Ecology & Evolution

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“…As animals navigate their environment, they address challenges such as food acquisition, predator avoidance and mating success. Although these forces are critical in shaping an individual's fitness, it has become apparent that the role of pathogens and parasites is also substantial (Burgan et al, 2019). Infection status and the subsequent immune response explains variation in host reproductive success (Bonneaud et al, 2003) and ability to escape from predators (Eraud et al, 2009;Stephenson et al, 2016), and response to parasitism may even foster the spread of non-native host species (Brown et al, 2018;Céspedes et al, 2019;Martin et al, 2017;White and Perkins, 2012).…”

Section: Introductionmentioning

confidence: 99%

Low-dose immune challenges result in detectable levels of oxidative damage

Armour

Bruner

Hines

et al. 2020

Journal of Experimental Biology

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Infection can result in substantial costs to animals, so they frequently respond by removing infectious agents with an immune response. However, immune responses entail their own costs, including upregulation of processes that destroy pathogens (e.g. the production of reactive oxygen species) and processes that limit the extent of self-damage during the immune response (e.g. production of anti-inflammatory proteins such as haptoglobin). Here, we simulated bacterial infection across a 1000-fold range using lipopolysaccharide (LPS) administered to northern bobwhite quail (Colinus virginianus), and quantified metrics related to pro-inflammatory conditions [i.e. generation of oxidative damage (d-ROMs), depletion of antioxidant capacity], anti-inflammatory mechanisms (i.e. production of haptoglobin, expression of the enzyme heme oxygenase, production of the organic molecule biliverdin) and nutritional physiology (e.g. circulating triglyceride levels, maintenance of body mass). We detected increases in levels of haptoglobin and d-ROMs even at LPS doses that are 1/1000th the concentration of doses frequently used in ecoimmunological studies, while loss of body mass and decreases in circulating triglycerides manifested only in individuals receiving the highest dose of LPS (1 mg LPS kg −1 body mass), highlighting variation among dosedependent responses. Additionally, individuals that lost body mass during the course of the experiment had lower levels of circulating triglycerides, and those with more oxidative damage had greater levels of heme oxygenase expression, which highlights the complex interplay between pro-and anti-inflammatory processes. Because low doses of LPS may simulate natural infection levels, variation in dose-dependent physiological responses may be particularly important in modeling how free-living animals navigate immune challenges.

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How Individual Variation in Host Tolerance Affects Competence to Transmit Parasites

Cited by 25 publications

References 100 publications

Macroimmunology: The drivers and consequences of spatial patterns in wildlife immune defence

Macroimmunology: The drivers and consequences of spatial patterns in wildlife immune defence

Extreme Competence: Keystone Hosts of Infections

Low-dose immune challenges result in detectable levels of oxidative damage

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