The Fine-Scale Landscape of Immunity and Parasitism in a Wild Ungulate Population

Abstract

Spatial heterogeneity in susceptibility and exposure to parasites is a common source of confounding variation in disease ecology studies. However, it is not known whether spatial autocorrelation acts on immunity at small scales, within wild animal populations, and whether this predicts spatial patterns in infection. Here we used a well-mixed wild population of individually recognized red deer (Cervus elaphus) inhabiting a heterogeneous landscape to investigate fine-scale spatial patterns of immunity and parasitism. We noninvasively collected 842 fecal samples from 141 females with known ranging behavior over 2 years. We quantified total and helminth-specific mucosal antibodies and counted propagules of three gastrointestinal helminth taxa. These data were analyzed with linear mixed models using the Integrated Nested Laplace Approximation, using a Stochastic Partial Differentiation Equation approach to control for and quantify spatial autocorrelation. We also investigated whether spatial patterns of immunity and parasitism changed seasonally. We discovered substantial spatial heterogeneity in general and helminth-specific antibody levels and parasitism with two helminth taxa, all of which exhibited contrasting seasonal variation in their spatial patterns. Notably, Fasciola hepatica intensity appeared to be strongly influenced by the presence of wet grazing areas, and antibody hotspots did not correlate with distributions of any parasites. Our results suggest that spatial heterogeneity may be an important factor affecting immunity and parasitism in a wide range of study systems. We discuss these findings with regards to the design of sampling regimes and public health interventions, and suggest that disease ecology studies investigate spatial heterogeneity more regularly to enhance their results, even when examining small geographic areas.

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

“…Considering this joint variation, spatial patterns in immunity could be most evident in seasons when food is limited or when abiotic conditions are harsh (Nelson & Demas, 1996). For example, work on red deer immunity found that spatial patterns in antibody concentrations varied substantially across seasons (Albery et al, 2018).…”

“…Correlograms often show a linear or exponential decline with increasing distance, suggesting a highly localized spatial mechanism. Recent work on red deer Cervus elaphus illustrates such fine-scale autocorrelation and suggests that environmental processes can shape defence within even an individual's home range (Albery, Becker, Kenyon, Nussey, & Pemberton, 2018). In contrast, correlograms applied to vampire bat leukocytes demonstrated autocorrelation at broad scales (thousands of kilometres), suggesting that conditions of the latitudinal range margins were more important determinants of immunity than local predictors (Becker, Nachtmann, et al, 2019).…”

“…INLA incorporates a two-dimensional spatial random effect that can be plotted to investigate hot-and cold spots of immunity. One INLA case study highlighted spatial agreement and discordance between several immune metrics and parasitism in red deer (Albery et al, 2018). Greater adoption of spatial statistics will strengthen our understanding of how the environment shapes immune defence while minimizing potential statistical artefacts.…”

Fitness costs of parasites explain multiple life history tradeoffs in a wild mammal

“…The relationship between parasitism and reproduction was especially steep (Figure 3b), and the deer will be selected to resist or tolerate infection to avoid such fitness consequences (Graham et al ., 2011). Combined with the considerable spatiotemporal variation in parasite exposure in this population (Albery et al ., 2019), parasite-mediated reproductive costs could create spatial and temporal variation in the fitness consequences of reproduction. In this case, females that give birth and lactate but then avoid areas with high parasite intensities may avoid the fitness reduction associated with reproduction, which could select for behavioural avoidance of infection (Hutchings et al ., 2006; Weinstein et al ., 2018).…”

“…The deer are infected with a selection of strongyle nematodes (Irvine et al ., 2006), including Teladorsagia circumcincta (unpublished data); thus, this measure is used to approximate anti-strongyle immune responses in the deer (Albery et al ., 2018b). To control for collection factors which introduce confounding variation in antibody levels we used the residuals from a model including extraction session, time to freezing, and collection day, as in previous studies (Albery et al ., 2018b, 2019). We also assayed faecal samples collected in November (e.g.…”