Beyond mice and men: environmental change, immunity and infections in wild ungulates

Jolles, Anna E.; Beechler, Brianna R.; Dolan, Brian P.

doi:10.1111/pim.12153

Cited by 32 publications

(29 citation statements)

References 153 publications

(214 reference statements)

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“…By serving as primary barrier to infection, replication and transmission following exposure, the host immune system plays a critical role in determining the outcome of these host-parasite interactions (Combes, 2001). Variation in immunity can further produce heterogeneity in traits that govern the population dynamics of infectious disease (Hawley & Altizer, 2011;Jolles, Beechler, & Dolan, 2015). The primary aim of ecoimmunology has accordingly been to explain variation in individual immune phenotypes and to understand their fitness consequences (Graham et al, 2011;Pedersen & Babayan, 2011).…”

Section: Introductionmentioning

confidence: 99%

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

Becker

Albery

Kessler

et al. 2020

Journal of Animal Ecology

101

122

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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: Introductionmentioning

confidence: 99%

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

Becker

Albery

Kessler

et al. 2020

Journal of Animal Ecology

101

122

View full text Add to dashboard Cite

show abstract

“…than nests in natural wetlands (Gentes, Whitworth, Waldner, Fenton, & Smits, 2007). Nonetheless, relatively few studies have investigated the effects of macroparasitic infections in wild populations, and it is therefore unclear whether the consequences of infections are generally context-dependent (Jolles, Beechler, & Dolan, 2015).…”

mentioning

confidence: 99%

Botfly infections impair the aerobic performance and survival of montane populations of deer mice, Peromyscus maniculatus rufinus

et al. 2019

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Elevations >2,000 m represent consistently harsh environments for small endotherms because of abiotic stressors such as cold temperatures and hypoxia. These environmental stressors may limit the ability of populations living at these elevations to respond to biotic selection pressures—such as parasites or pathogens—that in other environmental contexts would impose only minimal energetic‐ and fitness‐related costs. We studied deer mice (Peromyscus maniculatus rufinus) living along two elevational transects (2,300–4,400 m) in the Colorado Rockies and found that infection prevalence by botfly larvae (Cuterebridae) declined at higher elevations. We found no evidence of infections at elevations >2,400 m, but that 33.6% of all deer mice, and 52.2% of adults, were infected at elevations <2,400 m. Botfly infections were associated with reductions in haematocrit levels of 23%, haemoglobin concentrations of 27% and cold‐induced VO2max measures of 19% compared to uninfected individuals. In turn, these reductions in aerobic performance appeared to influence fitness, as infected individuals exhibited 19‐34% lower daily survival rates. In contrast to studies at lower elevations, we found evidence indicating that botfly infections influence the aerobic capabilities and fitness of deer mice living at elevations between 2,000 and 2,400 m. Our results therefore suggest that the interaction between botflies and small rodents is likely highly context‐dependent and that, more generally, high‐elevation populations may be susceptible to additional biotic selection pressures. A plain language summary is available for this article.

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“…A study by Jolles et al . provides a comprehensive review of the current portfolio of ecoimmunological studies published in this area and also provides strong arguments as to their importance in attempts to understand patterns of parasite infection and immunity in wild populations and how these may be affected by climate change.…”

Section: This Special Editionmentioning

confidence: 99%

Wild Immunology

Bradley

2015

Parasite Immunology

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Beyond mice and men: environmental change, immunity and infections in wild ungulates

Cited by 32 publications

References 153 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

Botfly infections impair the aerobic performance and survival of montane populations of deer mice, Peromyscus maniculatus rufinus

Wild Immunology

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