Innate immunity and testosterone rapidly respond to acute stress, but is corticosterone at the helm?

Abstract

When faced with a stressor, vertebrates can rapidly increase the secretion of glucocorticoids, which is thought to improve the chances of survival. Concurrent changes in other physiological systems, such as the reproductive endocrine or innate immune systems, have received less attention, particularly in wild vertebrates. It is often thought that glucocorticoids directly modulate immune performance during a stress response, but, in many species, androgens also rapidly respond to stress. However, to our knowledge, no study has simultaneously examined the interactions between the glucocorticoid, androgen, and innate immune responses to stress in a wild vertebrate. To address this issue, we tested the hypothesis that the change in plasma corticosterone (CORT) in response to the acute stress of capture and restraint is correlated with the concurrent changes in plasma testosterone (T) and innate immune performance (estimated by the capacity of plasma to agglutinate and lyse foreign cells) in the Abert's Towhee (Melozone aberti). Furthermore, to broaden the generality of the findings, we compared male and female towhees, as well as males from urban and non-urban populations. Acute stress increased plasma CORT, decreased plasma T in males, and decreased innate immune performance, but the increase in CORT during stress was not correlated with the corresponding decreases in either plasma T or innate immunity. By contrast, the plasma T stress response was positively correlated with the innate immune stress response. Collectively, our results challenge the proposition that the glucocorticoid stress response is correlated with the concurrent changes in plasma T, a key reproductive hormone, and innate immunity, as estimated by agglutination and lysis.

Corticosterone rapidly suppresses innate immune activity in the House Sparrow (Passer domesticus)

“…Overall, our results show stress-induced inhibition of innate immune activity and are consistent with previous findings in other free-living birds Matson et al, 2006;Cyr et al, 2007;Merrill et al, 2012;Zylberberg, 2015;Davies et al, 2016). They also indicate that the inhibition of complement-mediated activity occurs with a shorter latency than the inhibition of natural antibody-mediated activity.…”

“…Our findings do not, however, reveal whether elevated plasma CORT directly reduces innate immunity or exerts this effect through other mediators. In Abert's towhees (Melozone aberti), the stress-induced suppression of agglutination and lysis scores were not correlated with stress-induced plasma CORT levels (Davies et al, 2016), suggesting that plasma CORT acts indirectly on the innate immune system. With the present data, these observations suggest that stress-induced suppression of innate immune activity is at least indirectly caused by elevated plasma glucocorticoids rather than resulting from exposure to a stressor per se.…”

“…Many studies on this topic have used free-ranging birds as models because the diversity of habitats used by birds and of life history characteristics among species may help identify broad patterns of stress-induced effects on the immune response (Hasselquist, 2007). Several avian species exhibit stressinduced immunosuppression such as reduced microbicidal (Matson et al, 2006;Merrill et al, 2012) and lysozyme activity (Zylberberg, 2015), decreased natural antibody and complement-mediated activity (Davies et al, 2016), and reduced cutaneous immune activity Cyr et al, 2007). Stress, however, has also been observed to enhance acute phase protein activity in the Galápagos flycatcher (Myiarchus magnirostris; Zylberberg, 2015) and phagocytic activity in clay-colored thrushes (Turdus grayi; Millet et al, 2007).…”

“…These effects are mediated by the activation of glucocorticoid receptors (GR) and may involve both genomic and non-genomic mechanisms (Stahn and Buttgereit, 2008). In free-ranging birds, by contrast, it is unclear whether corticosterone (CORT), the primary avian glucocorticoid (Schmidt et al, 2010), plays a role in the regulation of stress-induced effects on immunity and whether plasma CORT can directly alter immune activity (Davies et al, 2016). Most studies on this subject have been correlative and do not, therefore, establish a causal relationship between changes in plasma CORT and immune activity (Lindström et al, 2005;Matson et al, 2006;Cyr et al, 2007;Buehler et al, 2008;Zylberberg, 2015).…”

Captivity effects on immune response and steroid plasma levels of a Brazilian toad (Rhinella schneideri)

“…Interestingly, PE was higher in individuals with higher plasma T levels over time in captivity. Although T shows several immunosuppressive effects (Martin, Weil, & Nelson, ; Roberts, Buchanan, & Evans, ), a positive correlation between plasma T levels and immune response, in an acute stress paradigm, has been reported in birds (Davies, Noor, Carpentier, & Deviche, ). Additionally, an immune enhancing effect of T‐implants has been demonstrated in anuran males, characterized by increased body mass (Desprat et al., ).…”