Photoperiod modulates the gut microbiome and aggressive behavior in Siberian hamsters

Abstract

Seasonally breeding animals undergo shifts in physiology and behavior in response to changes in photoperiod (day length). Interestingly, some species, such as Siberian hamsters (Phodopus sungorus), are more aggressive during the short-day photoperiods of the non-breeding season, despite gonadal regression. While our previous data suggest that Siberian hamsters employ a 'seasonal switch' from gonadal to adrenal regulation of aggression during shortday photoperiods, there is emerging evidence that the gut microbiome, an environment of symbiotic bacteria within the gastrointestinal tract, may also change seasonally and modulate social behaviors. The goal of this study was to compare seasonal shifts in the gut microbiome, circulating levels of adrenal dehydroepiandrosterone (DHEA) and aggression in male and female Siberian hamsters. Hamsters were housed in either long-day (LD) or short-day (SD) photoperiods for 9 weeks. Fecal samples were collected and behaviors were recorded following 3, 6 and 9 weeks of housing, and circulating DHEA was measured at week 9. SD females that were responsive to changes in photoperiod (SD-R), but not SD-R males, displayed increased aggression following 9 weeks of treatment. SD-R males and females also exhibited distinct changes in the relative abundance of gut bacterial phyla and families, yet showed no change in circulating DHEA. The relative abundance of some bacterial families (e.g. Anaeroplasmataceae in females) was associated with aggression in SD-R but not LD or SD non-responder (SD-NR) hamsters after 9 weeks of treatment. Collectively, this study provides insight into the complex role of the microbiome in regulating social behavior in seasonally breeding species.

A novel role for the pineal gland: Regulating seasonal shifts in the gut microbiota of Siberian hamsters

“…The overall results of this study confirm and extend previous work establishing seasonal differences in the Siberian hamster gut microbiota. While previous results 23,27 indicate significant differences by photoperiod in the relative abundances of certain members of the microbiota, the significant bacteria in those studies are different than those in the present study. Diet, environment, and genetics play important roles in shaping the profile of the gut microbiota, 37,38 so it is therefore not surprising to see community differences across independent hamster colonies that are housed in different facilities and fed different diets.…”

“…Recent studies have established that there are seasonal rhythms in the gut microbial community in Siberian hamsters. 23,27 Our present findings provide an alternative hypothesis regarding the mechanism(s) through which photoperiod drives other seasonal rhythms in physiology and behavior. Given that the gut microbiota has been implicated in many physiological and behavioral functions, pineal-dependent alterations in the gut microbiota may serve as a mechanism to affect downstream seasonal responses (ie, energetics, food intake, and social and aggressive behaviors).…”

“…Additionally, previous investigations 23,27 indicate that individual OTU responses play a large role in explaining differential host-derived effects on the microbiota 23,27,[36][37][38][39][68][69][70] (ie, effect of treatment on microbiota), as well as effects of the microbiota on host physiology. 9,[11][12][13]15,16,31,71 To investigate individual OTU responses to treatments, we used two-way repeated-measures ANOVAs on OTU relative abundance values (for the 100 most abundant OTUs, which represents greater than 78% of all obtained sequences) against time, treatment, and the treatment-by-time interaction, with post hoc Tukey's HSD tests where applicable.…”

“…7 An increasing number of studies suggest that shifts in gut microbial community structure can lead to pathogenicity [8][9][10] and affect host metabolism. 11 Gut microbiota activity has also been linked to mammalian host behavior, including impacts on exploratory and motor behavior, [12][13][14] depression, 5,15 anxiety, 6,[16][17][18] social interactions, [19][20][21][22] aggression, 23,24 and diet choice. 25,26 The microbiota can be altered by changes in either endogenous factors related to the host (such as stress 1 ) or exogenous environmental factors (such as photoperiod 23,27 ).…”

“…The gut community appears to be sensitive to multiple signals from the host-including immune system signals 34 and stress hormones 31,35,36 -as well as environmental signals such as diet 37,38 and photoperiod. 23,27,39 To understand the relationship between environment, host, and microbiota, it is necessary to determine the role of photoperiod on the profile of the gut community. A robust role for photoperiod in regulating both the hypothalamus-pituitary-adrenal (HPA) axis and the immune system has already been established in Siberian hamsters.…”