Acute peaks of testosterone suppress paternal care: evidence from individual hormonal reaction norms

Abstract

A long-standing tenet of evolutionary endocrinology states that testosterone mediates the life-history trade-off between mating and paternal care. However, the support for a role of testosterone in suppressing paternal care is mixed: implantation studies in birds suggest that high-level testosterone implants suppress paternal care, but circulating levels of testosterone and paternal care are typically not correlated. Because any trade-off in real life must be realized with hormone levels that are within an individual's reaction norm, it is crucial to show that natural changes in the hormone can modulate behaviour. Here, we used GnRH-injections to alter testosterone levels of free-living male black redstarts within each individual's hormonal reaction norm: individuals experiencing a short-term peak in testosterone resumed feeding their offspring later and showed a stronger suppression of offspring-feeding behaviour than control males. For the first time, this study demonstrated that short-term peaks in testosterone within the hormonal reaction norm of individuals can suppress paternal behaviour. Our findings reconcile previous seemingly contradictive effects that testosterone implants had on paternal care and the absence of correlations between circulating testosterone levels and paternal care, and demonstrate that the differential production of testosterone within the hormonal reaction norm of single individuals can indeed function as a mechanism to mediate a potential trade-off between mating and parenting. On a broader note, our results suggest that natural and short peaks in testosterone can elicit adaptive behavioural changes.

Probability of incubation by male Japanese Barn Swallows increases with plasma testosterone level

“…Additionally, because we only measured baseline testosterone levels, we cannot exclude the possibility that male incubation behaviour is affected by a hormonal reaction norm (i.e. changes in individual hormone levels in response to stimuli: Goyman & Dávila ), receptor sensitivity, or interactions with other endocrine or neuroendocrine secretions (Lynn ), although we have no explanation for the positive relationship between baseline testosterone levels and incubation participation. Testosterone manipulation, together with experimentally simulated predator exposure, is required to investigate the causal relationship between plasma testosterone levels, nest monitoring and male incubation investment.…”

“…Pinxten et al ; reviewed by Lynn , Lynn ), and some experimental studies have demonstrated suppressive effects of testosterone on paternal care (e.g. Saino & Møller , Van Roo , Goyman & Dávila ). However, most of these studies have focused on high levels of paternal care (e.g.…”

Developing a transcriptomic framework for testing testosterone-mediated handicap hypotheses

“…Moreover, studies should prioritize conducting experimental infections and/or immune challenges in combination with RNA-seq analyses to examine how transcriptomic signatures relate to immune function. Novel endocrine-based experiments, similar to (Goymann et al, 2015; Goymann and Flores Dávila, 2017), paired with RNA-seq analyses can also shed light on how acute changes in testosterone levels influence transcription over shorter timeframes. When possible, studies should also prioritize measuring testosterone’s effect on gene expression using a within-individual sampling approach as this allows for a more robust test of testosterone’s effect on gene expression (Williams, 2008).…”

Exogenous testosterone does not modulate aggression in sex-role-reversed female Barred Buttonquails, Turnix suscitator

“…This may have been caused by a non-constant release of the hormone by the implanted pellets (see also Fusani 2008;Quispe et al 2015). It therefore remains speculative whether such high testosterone concentrations could actually trigger a behavioural response, even though most hormone treatments of birds may lead to supra-physiological levels that still elicit expected responses [discussed in more detail by Goymann et al (2015); Goymann and Dávila (2017)]. Rosvall (2013) found increased levels of aggression in testosterone-treated female Tree Swallows (Tachycineta bicolor).…”