Winter madness: Melatonin as a neuroendocrine regulator of seasonal aggression

Abstract

Individuals of virtually all vertebrate species are exposed to annual fluctuations in the deterioration and renewal of their environments. As such, organisms have evolved to restrict energetically expensive processes and activities to a specific time of the year. Thus, the precise timing of physiology and behavior is critical for individual reproductive success and subsequent fitness. Although the majority of research on seasonality has focused on seasonal reproduction, pronounced fluctuations in other non‐reproductive social behaviors, including agonistic behaviors (e.g., aggression), also occur. To date, most studies that have investigated the neuroendocrine mechanisms underlying seasonal aggression have focused on the role of photoperiod (i.e., day length); prior findings have demonstrated that some seasonally breeding species housed in short “winter‐like” photoperiods display increased aggression compared with those housed in long “summer‐like” photoperiods, despite inhibited reproduction and low gonadal steroid levels. While fewer studies have examined how the hormonal correlates of environmental cues regulate seasonal aggression, our previous work suggests that the pineal hormone melatonin acts to increase non‐breeding aggression in Siberian hamsters (Phodopus sungorus) by altering steroid hormone secretion. This review addresses the physiological and cellular mechanisms underlying seasonal plasticity in aggressive and non‐aggressive social behaviors, including a key role for melatonin in facilitating a “neuroendocrine switch” to alternative physiological mechanisms of aggression across the annual cycle. Collectively, these studies highlight novel and important mechanisms by which melatonin regulates aggressive behavior in vertebrates and provide a more comprehensive understanding of the neuroendocrine bases of seasonal social behaviors broadly.

Short Photoperiod-Dependent Enrichment of Akkermansia spec. as the Major Change in the Intestinal Microbiome of Djungarian Hamsters (Phodopus sungorus)

“…Summing up, the present pilot study on the characterization of seasonality in the intestinal microbiome of Djungarian hamsters from Ulm University provides evidence for the natural existence of a seasonally rather than dietary-induced obese and lean microbiome in one and the same species, together with a diet-independent enrichment of Akkermansia muciniphila during winter-like short photoperiod acclimation. These preliminary data set the scientific basis for future in-depth research on A. muciniphila as a potential “acclimation-inducing probiotic,” including (a) energy metabolism, voluntary or forced body mass changes and daily torpor expression, as well as (b) neuroendocrine regulation underlying the bidirectional communication between the host and the microbiome via the brain–gut axis [ 47 ].…”

Brain and circulating steroids in an electric fish: Relevance for non-breeding aggression

“…Females had higher levels of AE, T and E 1 than males (Fig 1B ) while males had higher forebrain 11-KT than females (11-KT was non-detectable in females). This may be explained by: i) a sex difference in the expression of steroid binding globulins, leading to differences in brain uptake and/or retention of steroids [71,72], or ii) sex differences in brain steroidogenic enzymes that synthesize or metabolize steroids [73][74][75]. Although brain sex differences are usually related to sexually biased behavior, they can also compensate for basal physiological sex differences and ultimately produce a monomorphic behavioral output [76].…”

“…An important role for circulating steroid hormones during the non-breeding season is to serve as precursors that reach the brain and are locally converted into signaling molecules that are key in certain neurobiological processes [27,82,83]. In that sense, the quantification of circulating DHEA was of particular interest as it is an inactive androgen precursor that has been linked with the maintenance of non-breeding aggression in birds and mammals [29,74,82,84]. However, circulating and brain DHEA were non-detectable in G. omarorum during the non-breeding season, indicating that DHEA is absent or present at very low concentrations, similar to a recent report in song sparrows [14].…”

An introduction to the Special Issue on seasonal rhythms in birds and mammals

“…Melatonin actions have a powerful effect on multiple neural substrates involved in reproduction. Munley et al (2022) focussed on photoperiod induced changes in melatonin signaling to drive physiological and cellular changes involved in aggressive and nonaggressive social behavior. The authors cover recent findings indicating that melatonin‐dependent changes in steroid enzymes and receptors in localized brain regions, such as the lateral septum and medial amygdala, are critical for increasing the intensity and probability of male and female aggression.…”