Nikki M. Rendon

Sex-specific modulation of the gut microbiome and behavior in Siberian hamsters

The gut microbiome is a diverse, host-specific, and symbiotic bacterial environment that is critical for mammalian survival and exerts a surprising yet powerful influence on brain and behavior. Gut dysbiosis has been linked to a wide range of physical and psychological disorders, including autism spectrum disorders and anxiety, as well as autoimmune and inflammatory disorders. A wealth of information on the effects of dysbiosis on anxiety and depression has been reported in laboratory model systems (e.g., germ-free mice); however, the effects of microbiome disruption on social behaviors (e.g., aggression) of non-model species that may be particularly important in understanding many aspects of physiology and behavior have yet to be fully explored. Here we assessed the sex-specific effects of a broad-spectrum antibiotic on the gut microbiome and its effects on social behaviors in male and female Siberian hamsters (Phodopus sungorus). In Experiment 1, we administered a broad-spectrum antibiotic on a short-term basis and found that antibiotic treatment altered the microbial communities in the gut in male and female hamsters. In Experiment 2, we tested the effects of single versus repeated antibiotic treatment (including a recovery phase) on behavior, and found that two, but not one, treatments caused marked decreases in aggressive behavior, but not other social behaviors, in males; aggression returned to normal levels following recovery. Antibiotic-treated females, in contrast, showed decreased aggression after a single treatment, with all other social behaviors unaffected. Unlike males, female aggression did not return to normal during either recovery period. The present findings demonstrate that modest antibiotic treatment results in marked disruption of the gut microbiome in hamsters, akin to research done in other rodent species and humans. Further, we show that treatment with a broad-spectrum antibiotic, which has dysbiotic effects, also has robust, sex-specific effects on aggression, a critical behavior in the survival and reproductive success of many rodent species.

Photoperiod and aggression induce changes in ventral gland compounds exclusively in male Siberian hamsters.

Chemical communication is a critical component of social behavior as it facilitates social encounters, allows for evaluation of the social partner, defines territories and resources, and advertises information such as sex and physiological state of an animal. Odors provide a key source of information about the social environment to rodents; however, studies identifying chemical compounds have thus far focused primarily on few species, particularly the house mouse. Moreover, considerably less attention has been focused on how environmental factors, reproductive phenotype, and behavioral context alter these compounds outside of reproduction. We examined the effects of photoperiod, sex, and social context on chemical communication in the seasonally breeding Siberian hamster. We sampled ventral gland secretions in both male and female hamsters before and after an aggressive encounter and identified changes in a range of volatile compounds. Next, we investigated how photoperiod, reproductive phenotype, and aggression altered ventral gland volatile compound composition across the sexes. Males exhibited a more diverse chemical composition, more sex-specific volatiles, and showed higher levels of excretion compared to females. Individual volatiles were also differentially excreted across photoperiod and reproductive phenotype, as well as differentially altered in response to an aggressive encounter. Female volatile compound composition, in contrast, did not differ across photoperiods or in response to aggression. Collectively, these data contribute to a greater understanding of context-dependent changes in chemical communication in a seasonally breeding rodent.

Lipid signaling and fat storage in the dark-eyed junco

Seasonal hyperphagia and fattening promote survivorship in migratory and wintering birds, but reduced adiposity may be more advantageous during the breeding season. Factors such as photoperiod, temperature, and food predictability are known environmental determinants of fat storage, but the underlying neuroendocrine mechanisms are less clear. Endocannabinoids and other lipid signaling molecules regulate multiple aspects of energy balance including appetite and lipid metabolism. However, these functions have been established primarily in mammals; thus the role of lipid signals in avian fat storage remains largely undefined. Here we examined relationships between endocannabinoid signaling and individual variation in fat storage in captive white-winged juncos (Junco hyemalis aikeni) following a transition to long-day photoperiods. We report that levels of the endocannabinoid 2-arachidonoylglycerol (2-AG), but not anandamide (AEA), in furcular and abdominal fat depots correlate negatively with fat mass. Hindbrain mRNA expression of CB1 endocannabinoid receptors also correlates negatively with levels of fat, demonstrating that fatter animals experience less central and peripheral endocannabinoid signaling when in breeding condition. Concentrations of the anorexigenic lipid, oleoylethanolamide (OEA), also inversely relate to adiposity. These findings demonstrate unique and significant relationships between adiposity and lipid signaling molecules in the brain and periphery, thereby suggesting a potential role for lipid signals in mediating adaptive levels of fat storage.

Neural androgen synthesis and aggression: Insights from a seasonally-breeding rodent

Aggression is an essential social behavior that promotes survival and reproductive fitness across animal systems. While research on the neuroendocrine mechanisms underlying this complex behavior has traditionally focused on the classic neuroendocrine model, in which circulating gonadal steroids are transported to the brain and directly mediate neural circuits relevant to aggression, recent studies have suggested that this paradigm is oversimplified. Work on seasonal mammals that exhibit territorial aggression outside of the breeding season, such as Siberian hamsters (Phodopus sungorus), has been particularly useful in elucidating alternate mechanisms. These animals display elevated levels of aggression during the non-breeding season, in spite of gonadal regression and reduced levels of circulating androgens. Our laboratory has provided considerable evidence that the adrenal hormone precursor dehydroepiandrosterone (DHEA) is important in maintaining aggression in both male and female Siberian hamsters during the non-breeding season, a mechanism that appears to be evolutionarily-conserved in some seasonal rodent and avian species. This review will discuss research on the neuroendocrine mechanisms of aggression in Siberian hamsters, a species that displays robust neural, physiological, and behavioral changes on a seasonal basis. Furthermore, we will address how these findings support a novel neuroendocrine pathway for territorial aggression in seasonal animals, in which adrenal DHEA likely serves as an essential precursor for neural androgen synthesis during the non-breeding season.