Stress, Condition, and Ornamentation

In the latter half of the twentieth century, biologists interested in explaining the mechanisms for how vertebrates respond to stressful environmental circumstances created a conceptual framework based primarily on physiological measures. This field of stress responsiveness became the domain primarily of neuroendocrinologists, and researchers in this field focused on the physiological actions of the hypothalamus, pituitary gland, and adrenal glands (the HPA axis) (Herman and Cullinan 1997; Sapolsky et al. 2000; Romero 2004). Great advances were made in demonstrating how the HPA serves as a key mediator of the responsiveness of vertebrates to environmental perturbations by regulating physiology and behavior (e.g., Wingfield et al. 1997; Reeder and Kramer 2005; Breuner et al. 2008). Glucocorticoids, particularly cortisol and corticosterone, were identified as important signaling molecules that link external stressors to internal physiological responses—particularly immune and metabolic responses—in vertebrates (Wingfield et al. 1998; Buchanan 2000; Sapolsky et al. 2000). The mechanisms by which individuals cope with stress became a major area of study in physiological ecology. In a parallel universe that sometimes co-existed within the same laboratory group studying responsiveness to stress, a theory of condition-dependent signaling emerged to explain why female animals use males’ ornamentation as a criterion in mate choice. This theory of sexual signaling began by invoking the costs of ornamentation as necessary to maintain honesty (Zahavi 1975; updated in Kotiaho [2001]). Initially, discussions of costs were focused on the maintenance of ornamentation, and display traits were viewed as potential handicaps to survival with direct negative effects on fitness (MaynardSmith 1976, 1978; Zahavi 1977; Nur and Hasson 1984). As theory developed, explanations for honest signaling shifted to the costs of production and particularly to the challenges of allocating energy away from body maintenance to ornamentation (KodricBrown and Brown 1984; Rowe and Houle 1996; Morehouse 2014, this issue). More recently, it has been proposed that no fitness costs or tradeoffs of resources are required for honest signaling, so long as the production of ornaments is inexorably linked to system function through shared biochemical pathways (Hill 2011, 2014, this issue). The union of the theory of stress responsiveness with concepts of condition-dependent signaling was inevitable because the connections between stress, condition, and ornamentation are inescapable. By definition, environmental stressors are expected to reduce the condition of individuals (Badyaev 2005; Charmandari et al. 2005; Careau et al. 2014). Moreover, ornaments are proposed to be sensitive signals of individual condition (Cotton et al. 2004; Hill 2011) and hence should reflect the degree to which an individual is impacted by stressors such as parasites or poor nutrition (Andersson 1994; Peters et al. 2014, this issue; Schmidt et al. 2014, this issue). Thus, for decades, ornamental traits have been viewed as signals of either the ability to avoid stressors (e.g., Hamilton and Zuk 1982; Balenger and Zuk 2014, this issue) or the ability to cope with stressors (Westneat and Birkhead 1998; Bortolotti et al. 2009), but discussions of honest signaling typically have not integrated known pathways and conceptual frameworks about mechanisms for responding to stress. Integrative and Comparative Biology