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

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 immu...

Fine-scale spatial patterns of wildlife disease are common and understudied

“…(Leu et al 2020). Finally, immunity is often quantified alongside parasite burden and prevalence, and it would be interesting to see whether spatial variation in immunity manifests on the same scale, and whether it predicts disease risk (Becker et al 2020).…”

“…Furthermore, host immunity and susceptibility can be affected by environmentally varying factors, with knock-on impacts on pathogen burden and transmission (Becker et al 2018(Becker et al , 2020. All these and other processes will create spatial patterns of infection, which hold important ramifications for epidemiological dynamics and disease control efforts (Cross et al 2005;Plowright et al 2019;Becker et al 2020). Yet, many epidemiological studies examine coarse spatial scales or assume that spatial patterns will be negligible compared to other hypothesized drivers.…”

Ecoimmunology at spatial scales

“…Against this backdrop of advances and challenges, Becker et al (2020) have proposed a framework to address ecoimmunology at spatial scales. Termed macroimmunology—akin to macroecology—they ask whether variation in immune phenotype occurs in predictable spatial contexts, such as along species invasion fronts, latitudinal gradients and urban–rural divides, and if these in turn, could be used to predict the risk and implications of infections.…”

Spatiotemporal variation in drivers of parasitism in a wild wood mouse population

“…The regularity of finding context dependent results presents an important problem when 82 understanding the dynamics of host-parasite interactions in the wild: specifically, what is the 83 consistency and repeatability of the observed trends across different replicates of the same system, 84 and how can researchers be sure that their replication is sufficient? Ecology is undergoing a 85 reproducibility crisis, and spatiotemporal variation is a likely culprit impacting variation in results 86 (Becker et al 2020). By quantifying how the drivers of parasitism vary over space and time for the 87 same host-parasite system, we can address three fundamental questions: (i) what are the key 88 (reproducible) factors that drive parasite infection intensity; (ii) how much of the variation in effect 89 sizes is biologically meaningful, rather than representing sampling biases; and (iii) how can we 90 optimise sampling regimes to improve our ability to detect important biological variation in drivers 91 within a system?…”