Highly context-specific activation of the HPG axis in the dark-eyed junco and implications for the challenge hypothesis

Abstract

One of the best studied hormone-behavior interactions is the transient rise in testosterone (T) associated with male-male aggression. However, recent research on songbirds has demonstrated numerous exceptions to this pattern.One species previously thought to elevate T in response to a simulated territorial intrusion is the dark-eyed junco (Junco hyemalis). Here, we show that under most circumstances male juncos do not elevate circulating T or CORT levels in response to social stimuli, despite being physiologically capable of elevating T as indicated by their response to GnRH. The lack of hormonal response was found regardless of the sex of the social stimulus (singing male vs. soliciting female), its sensory modality (song only, song + live lure, song + taxidermic mount), or the timecourse of sampling. Notably, males did elevate T levels when exposed to a simulated territorial intrusion in the days following simulated predation of their chicks. Whether the high T seen in these narrow circumstances represents stage-dependent social modulation of T or re-activation of male reproductive physiology in preparation for re-nesting (i.e. socially independent T modulation) remains to be determined. It is clear, however, that activation of the HPG axis is highly context-specific for male juncos. These results highlight important and unresolved issues regarding the socially mediated component of the challenge hypothesis and how it relates to the evolution of hormone-mediated traits.

Keywords: Androgen responsiveness; Challenge hypothesis; Corticosterone; Simulated courtship interaction; Simulated territorial intrusion; Testosterone.

Figure 1. Schematic of social treatments

Open boxes denote the duration of exposure to playback (PB) and/or a live lure or mount, as indicated. Male and female symbols denote the sex of the social stimulus. All trials simulating male intrusion were accompanied by male song, whereas trials simulating courtship interactions with females were accompanied by copulatory trills. “0 MIN” indicates the beginning of the trial, X indicates re-started playback (if applicable), and droplets indicate the approximate timing of blood sampling. Roman numerals are used as short-hand for these treatments in subsequent figures.

Figure 2. Testosterone

Plasma T did not differ significantly between controls and experimentals in any social treatment (A–C) except for males that experienced a 25-min STI in the days immediately following a simulated nest predation event. (D) T levels post-GnRH challenge were significantly higher than T-levels pre-GnRH challenge. Bars represent back-transformed means, and error bars show one standard error from the mean.

Figure 3. Corticosterone

Plasma CORT did not differ significantly among any social treatment (A–C), but CORT levels prior to GnRH challenge (D) were significantly higher than those of all other males (A–C). Bars represent back-transformed means, and error bars show one standard error from the mean. Note that the scale of the y-axis for D differs from A–C.

Figure 4

Prior to GnRH challenge, plasma T and CORT were negatively correlated.