Physiological Stress Mediates the Honesty of Social Signals

Abstract

BackgroundExtravagant ornaments used as social signals evolved to advertise their bearers' quality. The Immunocompetence Handicap Hypothesis proposes that testosterone-dependent ornaments reliably signal health and parasite resistance; however, empirical studies have shown mixed support. Alternatively, immune function and parasite resistance may be indirectly or directly related to glucocorticoid stress hormones. We propose that an understanding of the interplay between the individual and its environment, particularly how they cope with stressors, is crucial for understanding the honesty of social signals.Methodology/Principal FindingsWe analyzed corticosterone deposited in growing feathers as an integrated measure of hypothalamic-pituitary-adrenal activity in a wild territorial bird, the red grouse Lagopus lagopus scoticus. We manipulated two key, interrelated components, parasites and testosterone, which influence both ornamentation and fitness. Birds were initially purged of parasites, and later challenged with parasites or not, while at the same time being given testosterone or control implants, using a factorial experimental design. At the treatment level, testosterone enhanced ornamentation, while parasites reduced it, but only in males not implanted with testosterone. Among individuals, the degree to which both parasites and testosterone had an effect was strongly dependent on the amount of corticosterone in the feather grown during the experiment. The more stressors birds had experienced (i.e., higher corticosterone), the more parasites developed, and the less testosterone enhanced ornamentation.Conclusions/SignificanceWith this unique focus on the individual, and a novel, integrative, measure of response to stressors, we show that ornamentation is ultimately a product of the cumulative physiological response to environmental challenges. These findings lead toward a more realistic concept of honesty in signaling as well as a broader discussion of the concept of stress.

Parasites, mate attractiveness and female feather corticosterone levels in a socially monogamous bird

“…An effect of parasitism on CORTf has been documented in previous studies (Bortolotti et al 2009b, Harriman et al 2014, indicating that this measure is sensitive enough to detect the effects of parasites. In socially monogamous red grouse, both sexes display conspicuous red combs and comb size functions in intra-and inter-sexual selection.…”

“…Numbers above error bars = sample sizes (number of females) 2014; Sild et al 2014) (although estimated parasite abundances may possibly have been too low to have had such an effect). Alternatively, higher corticosterone levels may have induced a greater susceptibility to infective larvae (Mougeot et al 2005b) and a greater reinfection rate, as also shown in male red grouse following a standardized challenge with infective larvae (Bortolotti et al 2009b). Previous experiments showed that parasite transmission likely occurs within red grouse social pairs (Martinez-Padilla et al 2012).…”

“…Social mate choice, which appeared associated with female corticosterone levels , may therefore modulate the impacts that natural stressors, such as parasites, have on corticosterone levels. Further research on the mechanisms and functions of physiological stress is needed in free-living animals, and measures of integrated stress responses, like CORTf measurements (Bortolotti et al 2009b;Fairhurst et al 2012Fairhurst et al , 2014Lendvai et al 2013) will greatly contribute to this goal. Future experiments should determine whether the association between female corticosterone levels and male ornamentation is mediated via the quality of resources provided by males to breeding females or is a female adjustment to its achieved mate choice.…”

“…This opened up a new window of opportunity for understanding the role that physiological stress plays in the life of wild birds (Bortolotti et al 2009b;Fairhurst et al 2011;Fairhurst et al 2012;Koren et al 2012;Carrete et al 2013;Lendvai et al 2013;Martinez-Padilla et al 2013). However, to date, few studies have related measures of integrated stress responses, such as feather corticosterone levels (hereafter CORTf) to parasite abundance, levels of sexual ornamentation or mate quality (e.g.…”

“…We tested whether CORTf was lower and comb size greater in dosed females compared to controls. We also investigated whether a higher CORTf was associated with a greater natural parasite reinfection rate (Bortolotti et al 2009b), considering parasite burden 1 month after dosing with anthelminthic (previously shown to be effective at removing of T. tenuis worms) as an index of reinfection rate. We also investigated whether female CORTf varied according to their social mate's phenotype.…”