Covariation between glucocorticoids, behaviour and immunity supports the pace-of-life syndrome hypothesis: an experimental approach

Abstract

The biomedical literature has consistently highlighted that long-term elevation of glucocorticoids might impair immune functions. However, patterns are less clear in wild animals. Here, we re-explored the stress-immunity relationship considering the potential effects of behavioural profiles. Thirteen captive roe deer (Capreolus capreolus) were monitored over an eight-week period encompassing two capture events. We assessed how changes in baseline faecal cortisol metabolite (FCM) concentrations following a standardized capture protocol and an immune challenge using anti-rabies vaccination affected changes in 13 immune parameters of innate and adaptive immunity, and whether these changes in baseline FCM levels and immune parameters related to behavioural profiles. We found that individuals with increased baseline FCM levels also exhibited increased immunity and were characterized by more reactive behavioural profiles (low activity levels, docility to manipulation and neophilia). Our results suggest that the immunity of large mammals may be influenced by glucocorticoids, but also behavioural profiles, as it is predicted by the pace-of-life syndrome hypothesis. Our results highlight the need to consider covariations between behaviour, immunity and glucocorticoids in order to improve our understanding of the among-individual variability in the stress-immunity relationships observed in wildlife, as they may be underpinned by different life-history strategies.

Keywords: adaptive immunity; coping style; cortisol; inflammation; innate immunity; stress.

Figure 1.

Summary of the experimental design. Data relative to the assessment of neophobia scores were obtained prior to this protocol (in February 2015 for all individuals, except two that were assessed for neophobia in February 2018, following the same protocol; see details in [29]). (Online version in colour.)

Figure 2.

Structural models of relationships among behavioural profiles, change in baseline glucocorticoid levels and change in immunity as determined by the partial least-squares path modelling analyses. Arrows indicates the direction of effect and the thickness of arrows indicates the strength of the correlation between latent variables. The absence of p-value (P) indicates the relationship was not significant. Scatterplots on each arrow indicate the underlying correlations. (Online version in colour.)

Figure 3.

Relationship between baseline FCMs level (log-transformed) and behavioural profiles. Behavioural profiles' scores correspond to the score for the first axis (PC1) of the PCA conducted using docility, activity and neophilia as covariables. The three variables were all positively correlated with PC1. Thus, this axis represents a gradient of behavioural profiles, with negative values indicating reactive behavioural profiles (low activity levels, neophilia and docility), and positive values indicating proactive behavioural profiles (high activity levels, neophobia and lack of docility). Points represent observed values, lines represent model predictions and grey area represents the 95% confidence interval. Each colour corresponds to one of the 13 individuals. (Online version in colour.)

Figure 4.

Summary of the observed outcomes and relationships between the latent variables considered in our study. Our protocol (see details in the main text) resulted in different outcomes, with part of the individuals showing an increase in baseline cortisol between the two study periods (indicated by an increase in FCMs), while others showed a decrease. Individuals that showed more reactive behavioural profiles (indicated by low activity levels, docility to manipulation and neophilia) also exhibited an increase in baseline cortisol levels, and an increase in immunity (both innate and adaptive immunity), while the opposite occurred for individuals that showed more proactive behavioural profile. (Online version in colour.)