Rapid effects of elevated stress hormones on male courtship signals suggest a major role for the acute stress response in intra‐ and intersexual selection

Abstract

Short‐term elevations in circulating stress hormones (glucocorticoids) often mediate reduced investment in reproductive behaviour in favour of self‐maintenance and survival, but the significance of these effects in sexual selection and communication remain largely unexplored. Here we examine the acute stress response in the context of intra‐ and intersexual selection in the green treefrog Hyla cinerea. Males of this species produce agonistic acoustic signals that stimulate elevations in the stress hormone corticosterone (CORT) in rival males, suggesting a central role for CORT in male–male competition. We hypothesized that elevated CORT levels in losers of vocal contests mediate an increase in the energy allocated towards self‐maintenance and survival that compromises investment in courtship signalling, resulting in reduced attractiveness to females. Consistent with this hypothesis, we show that CORT administration to calling males, simulating CORT production in vocal contest losers, caused a rapid reduction in the duration of advertisement calls and vocal effort. Elevated CORT also increased the propensity to produce aggressive calls during simulated territorial intrusions that was followed by an increased probability of non‐calling “satellite” mating behaviour. This suite of CORT effects on vocal behaviour are known to decrease attractiveness to females and were not related to a decrease in androgen level or differences in body condition in CORT‐ vs. saline‐injected males. Our results suggest that CORT production during intraspecific vocal contests compromises male attractiveness. Male vocalizations may therefore reliably indicate recent contest outcomes and/or the stress status of males, implicating CORT as a mediator of honest signalling. We propose that the effects of agonistic acoustic signals on CORT production in this species are maintained by CORT‐mediated life‐history trade‐offs; decreased conspicuous signalling in high stress‐responsive males potentially increases survival by reducing the likelihood of escalated contests with dominant males and detection by predators. Adoption of alternative non‐calling satellite mating tactics may contribute to maintaining individual variation in stress responsiveness by increasing the chances that competitively inferior males acquire mates. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13054/suppinfo is available for this article.

Vocalisation and its association with androgens and corticosterone in a night frog (Nyctibatrachus humayuni) with unique breeding behaviour

“…Androgens and corticosterone are believed to be involved in controlling the call parameters as they are important for the expression of calling behaviour of different anurans including N. humayuni (Joshi et al, 2017;Leary et al, 2008Leary et al, , 2004Leary & Harris, 2013). However, only a few studies have examined the endocrine basis of modulation of vocal behaviour (Leary, 2009;Leary & Crocker-Buta, 2018;Leary et al, 2006). In N. humayuni, androgens are involved in the expression of calling behaviour (Joshi et al, 2017).…”

“…A large body of information exists on the acoustic properties of vocalisation (Leary, ). However, information on the association of acoustic properties with androgens and corticosterone, and the role of steroid hormones, if any, in modulating acoustic properties, is limited (Leary, ; Leary & Crocker‐Buta, ; Leary, Garcia, & Knapp, ). In seasonally breeding anurans, increased androgen levels during the breeding season are responsible for the development of secondary sexual characters, which play a crucial role in successful reproduction (Emerson, Greig, Caroll, & Prins, ; Lynch & Blackburn, ).…”

“…Apparently, the role of corticosterone in anuran vocalisation is complex and context‐dependent. Although previous studies have shown that corticosterone could be involved in mediating male–male competition during vocal contests and agonistic interactions, its involvement in altering the fine acoustic properties is not clear (Leary, ; Leary & Crocker‐Buta, ).…”

“…A large body of information exists on the acoustic properties of vocalisation (Leary, 2009). However, information on the association of acoustic properties with androgens and corticosterone, and the role of steroid hormones, if any, in modulating acoustic properties, is limited (Leary, 2009;Leary & Crocker-Buta, 2018;Leary, Garcia, & Knapp, 2006).…”

Exposure to glucocorticoids alters life history strategies in a facultatively paedomorphic salamander

“…Samples were then incubated overnight with radiolabeled CORT (PerkinElmer, Inc.) for determination of recoveries. CORT was then extracted from samples using dichloromethane, dried under nitrogen gas at 40°C, resuspended in 10% ethyl acetate in iso‐octane, and loaded on to diatomaceous earth columns containing a diatomaceous earth:distilled water “glycol trap” and a propanediol:ethylene glycol mixture for hormone separation (see Leary & Crocker‐Buta, 2018). The CORT fraction was collected using stepwise elution with increasingly polar mixtures of ethyl acetate in iso‐octane.…”