Melatonin mediates seasonal transitions in aggressive behavior and circulating androgen profiles in male Siberian hamsters

Abstract

Some seasonally-breeding animals are more aggressive during the short, "winter-like" days (SD) of the non-breeding season, despite gonadal regression and reduced circulating androgen levels. While the mechanisms underlying SD increases in aggression are not well understood, previous work from our lab suggests that pineal melatonin (MEL) and the adrenal androgen dehydroepiandrosterone (DHEA) are important in facilitating non-breeding aggression in Siberian hamsters (Phodopus sungorus). To characterize the role of MEL in modulating seasonal transitions in aggressive behavior, we housed male hamsters in long days (LD) or SD, treated them with timed MEL (M) or saline injections, and measured aggression after 3, 6, and 9 weeks. Furthermore, to assess whether MEL mediates seasonal shifts in gonadal and adrenal androgen synthesis, serum testosterone (T) and DHEA concentrations were quantified 36 h before and immediately following an aggressive encounter. LD-M and SD males exhibited similar physiological and behavioral responses to treatment. Specifically, both LD-M and SD males displayed higher levels of aggression than LD males and reduced circulating DHEA and T in response to an aggressive encounter, whereas LD males elevated circulating androgens. Interestingly, LD and SD males exhibited distinct relationships between circulating androgens and aggressive behavior, in which changes in serum T following an aggressive interaction (ΔT) were negatively correlated with aggression in LD males, while ΔDHEA was positively correlated with aggression in SD males. Collectively, these findings suggest that SD males transition from synthesis to metabolism of circulating androgens following an aggressive encounter, a mechanism that is modulated by MEL.

Seasonal patterns of melatonin alter aggressive phenotypes of female Siberian hamsters

“…More importantly, it is not the presence of melatonin per se, but the precise timing of melatonin that is critical for allowing individuals to integrate aspects of their environment and make seasonally appropriate adjustments in these neuroendocrine processes. These findings are in agreement with our previous work in male Siberian hamsters, in which we showed that administering timed melatonin to LD males induces gonadal regression, elevates aggressive behaviour and produces SD‐like changes in circulating androgen profiles 40 . It is also likely that this mode of integration for melatonin is involved in the regulation of aggression in other vertebrate species 17,18 , 63‐67.…”

“…Previously, we have shown that short‐term exogenous melatonin treatment induces SD‐like increases in aggression in male and female hamsters, yet does not affect reproductive physiology or circulating gonadal steroid levels 16,38,39 . Conversely, long‐term administration of melatonin induces gonadal regression, elevates aggressive behaviour, and produces SD‐like changes in circulating androgen profiles in male hamsters 40 ; suggesting that melatonin may be involved in the early onset of responding to changes in ambient day length (eg, the transition from ‘spring’ to ‘fall’). Moreover, we have shown that melatonin acts directly on the adrenal glands to increase the release of DHEA in SD females, whereas melatonin acts directly on the ovaries to increase the release of DHEA in LD females 39 .…”

“…After the acclimation period, experimental hamsters were either transferred to a room on a short‐day (SD) (8:16 hours) photocycle (n = 28) or were relocated to a new room on a LD cycle (n = 42). All hamsters were given daily s.c. injections of melatonin (15 μg day ‐1 dissolved in 1:10 ethanol:saline solution; M5250; Sigma‐Aldrich, St Louis, MO, USA) or a control solution (1:10 ethanol:saline solution), as described previously 39,40,45 . LD hamsters were divided into three treatment groups and received either a timed melatonin injection (Mel‐T, n = 14) 2 hours prior to lights off to extend the LD pattern of endogenous melatonin secretion to mimic that of SD animals; a mis‐timed melatonin injection (Mel‐M, n = 13) 8 hours prior to lights off to supplement circulating melatonin, but at a time at which the injection fails to summate with endogenous melatonin secretion; or a control injection (LD, n = 15) (Figure 1).…”

“…Scores from the two individuals were averaged, and inter‐rater reliability was accepted if less than 10% variation occurred. Measures of aggression were defined according to previous studies in male and female Siberian hamsters 40,47,48 …”

“…We have previously demonstrated that exogenous melatonin administration elevates aggressive behaviour in LD male hamsters 16,38 . Furthermore, we have shown that timed melatonin injections, which mimic SD patterns of melatonin secretion, increases aggression in LD females 39 and that long‐term timed melatonin administration induces gonadal regression, elevates aggressive behaviour, and produces SD‐like changes in circulating androgen profiles in LD males 40 . We have also found that administering melatonin in vitro to cultured adrenal glands elevates adrenal DHEA output in SD, but not LD females, whereas treating cultured ovaries with melatonin increases DHEA output in LD, but not SD females 39 .…”