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The Drivers and Consequences of Spatial Patterns in Wildlife Immune Defence

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The Drivers and Consequences of Spatial Patterns in Wildlife Immune Defence Received: 22 March 2019 | Accepted: 6 November 2019 DOI: 10.1111/1365-2656.13166 REVIEW Macroimmunology: The drivers and consequences of spatial patterns in wildlife immune defence Daniel J. Becker1,2 | Gregory F. Albery3 | Maureen K. Kessler4 | Tamika J. Lunn5 | Caylee A. Falvo6 | Gábor Á. Czirják7 | Lynn B. Martin8 | Raina K. Plowright6 1Department of Biology, Indiana University, Bloomington, IN, USA; 2Center for the Ecology of Infectious Disease, University of Georgia, Athens, GA, USA; 3Department of Biology, Georgetown University, Washington, DC, USA; 4Department of Ecology, Montana State University, Bozeman, MT, USA; 5Environmental Futures Research Institute, Griffith University, Nathan, Queensland, Australia; 6Department of Microbiology and Immunology, Montana State University, Bozeman, MT, USA; 7Department of Wildlife Diseases, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany and 8Department of Global and Planetary Health, University of South Florida, Tampa, FL, USA Correspondence Daniel J. Becker Abstract Email: [email protected] 1. The prevalence and intensity of parasites in wild hosts varies across space and is Funding information a key determinant of infection risk in humans, domestic animals and threatened National Science Foundation, Grant/Award wildlife. Because the immune system serves as the primary barrier to infection, Number: DEB-1716698, IOS-1257773 and IOS-1656618; Defense Advanced Research replication and transmission following exposure, we here consider the environ- Projects Agency, Grant/Award Number: mental drivers of immunity. Spatial variation in parasite pressure, abiotic and bi- D16AP00113 and D18AC00031; National Institutes of Health, Grant/Award Number: otic conditions, and anthropogenic factors can all shape immunity across spatial P20GM103474 and P30GM110732; scales. Identifying the most important spatial drivers of immunity could help pre- PREEMPT; National Institute of Food and Agriculture empt infectious disease risks, especially in the context of how large-scale factors such as urbanization affect defence by changing environmental conditions. Handling Editor: Andy Fenton 2. 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, im- mune measures, spatial replication and extent, and statistical methods. 3. 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 de- pendence statistically, potentially affecting inferences for the relationships be- tween environmental conditions and immune defence. 4. 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 972 | © 2019 British Ecological Society wileyonlinelibrary.com/journal/jane J Anim Ecol. 2020;89:972–995. BECKER ET AL. Journal of Animal Ecolog y | 973 guide spatial sampling and highlight the need for greater use of mixed-effects models that account for spatial variability while also allowing researchers to ac- count for both individual- and habitat-level covariates. 5. We finally discuss future research priorities for macroimmunology, including fo- cusing on latitudinal gradients, range expansions and urbanization as being espe- cially 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. KEYWORDS ecoimmunology, host competence, macroecology, resistance, spatial autocorrelation, zoonoses 1 | INTRODUCTION habitat heterogeneity plays in shaping immunity and infection out- comes (Gervasi, Civitello, Kilvitis, & Martin, 2015; Paull et al., 2012). Emerging infectious diseases threaten wildlife, humans and domes- Host genotypes, alongside factors such as nutrition or reproductive tic animals (Plowright et al., 2017; Smith, Acevedo-Whitehouse, & status, affect whether an individual in a particular habitat succumbs Pedersen, 2009). By serving as primary barrier to infection, replica- to infection or lives to transmit to a susceptible host (Plowright, tion and transmission following exposure, the host immune system Field, et al., 2008). For example, mathematical models show how plays a critical role in determining the outcome of these host–parasite resource-rich habitats can homogenize host infectious periods in a interactions (Combes, 2001). Variation in immunity can further pro- population and limit epidemics (Hall, 2019). duce heterogeneity in traits that govern the population dynamics of Environmental factors operating at multiple spatial scales can drive infectious disease (Hawley & Altizer, 2011; Jolles, Beechler, & Dolan, immunological variation. At least three non-exclusive factors may 2015). The primary aim of ecoimmunology has accordingly been to vary over space and modify immunity (Table 1): (a) spatial variation explain variation in individual immune phenotypes and to under- in parasite pressure that selects for and stimulates immune invest- stand their fitness consequences (Graham et al., 2011; Pedersen & ment, (b) spatial variation in abiotic conditions and biotic interactions Babayan, 2011). However, ecoimmunology increasingly acknowl- that modify allocation of energy and resources to costly defence and edges how broader evolutionary and ecological contexts shape de- (c) anthropogenic changes that alter either of these factors (e.g. urban- fence (Becker, Downs, Downs, & Martin, 2019; Schoenle, Downs, & ization) or directly alter immunity (e.g. contaminants). These spatial Martin, 2018). Between-population sources of immunological vari- factors commonly act on phenotypic plasticity (e.g. variation in food, ation are becoming increasingly important to consider in the con- temperature), although some can also affect host immunogenetics (e.g. text of environmental change, as large-scale anthropogenic factors parasite-mediated selection and population isolation via habitat loss). such as urbanization and deforestation are influencing immunity by Such spatial factors are more likely to act in concert, rather altering environmental conditions (Acevedo-Whitehouse & Duffus, than in isolation, to shape immunity. In some cases, captive stud- 2009; Martin, Hopkins, Mydlarz, & Rohr, 2010). ies or field manipulations can isolate particular factors and iden- Immune phenotypes are individual characteristics, and the tify causal links with immune phenotypes. These approaches are composition of susceptible and resistant hosts in a population de- most relevant when testing predominantly local sources of envi- termines whether parasites can invade and persist (e.g. herd immu- ronmental variation. For example, experimental artificial light at nity; Anderson & May, 1991). Individual heterogeneity is shaped night, an aspect of urban environments, alters immune gene regu- not only by the genetic variation of hosts (and parasites) but also by latory networks of house sparrows Passer domesticus and, in turn, the environment and resultant plasticity: the ability of genotypes to the duration of infectiousness for transmitting West Nile virus express different phenotypes across environmental con- to mosquitoes (Kernbach et al., 2019). In addition, common gar- texts (Schmid-Hempel, 2003; West-Eberhard, 2003). These den approaches can elucidate whether population differences in genotype-by-environment interactions highlight the role that immunity persist under identical environmental conditions; this 974 | Journal of Animal Ecology BECKER ET AL. TABLE 1 Select examples of multi-site studies of ecoimmunology, arranged by the spatial mechanism(s) expected to link environmental variation with immunity: parasite pressure, abiotic and biotic conditions, and anthropogenic factors Spatial Association with host Host speciesa Immune measure Study design mechanism immunity References House finch Spleen 2 sites, United Parasite pressure Few genes Zhang, Hill, (Haemorhous transcriptome States differentially Edwards, and mexicanus) expressed by site Backström (2014) exposure history Bank vole Frequency of 21 sites, across Parasite pressure Gene frequency Tschirren (2015) (Myodes TLR2 protective Europe positively associated glareolus) variant with human Lyme disease
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