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

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ORIGINAL PAPER

Innate immunity and testosterone rapidly respond to acute stress, but is corticosterone at the helm? S. Davies1,2 · S. Noor1 · E. Carpentier3 · P. Deviche1 

Received: 9 February 2016 / Revised: 27 April 2016 / Accepted: 2 May 2016 © Springer-Verlag Berlin Heidelberg 2016

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

Communicated by G. Heldmaier. * S. Davies [email protected] 1

School of Life Sciences, Arizona State University, Tempe, AZ 85287, USA

2

Present Address: Department of Biological Sciences, Virginia Tech, Blacksburg, VA 24061, USA

3

Université de Poitiers, Faculté des Sciences Fondamentales et Appliquées, 86022 Poitiers, France



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. Keywords  Acute stress · Androgen · Complement · Glucocorticoid · Innate immunity · Natural antibody · Urbanization

Introduction Many physiological functions in vertebrates are modulated by the activity of a neuroendocrine cascade called the hypothalamo-pituitary-adrenal (HPA) axis. This cascade begins in the hypothalamus and, by way of the anterior pituitary gland, culminates in the release of glucocorticoids from the adrenal glands into the blood. In the absence of adverse stimuli, initial (often referred to as baseline) secretion of glucocorticoids helps to prepare an organism for predictable, daily energetic demands (Sapolsky et al. 2000). In addition t