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

Rendon, Nikki M.; Soini, Helena A.; Scotti, Melissa-Ann L.; Weigel, Ellen R.; Novotný, Miloš V.; Demas, Gregory E.

doi:10.1016/j.yhbeh.2016.02.005

Cited by 11 publications

(21 citation statements)

References 37 publications

(65 reference statements)

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“…; Scotti, Place & Demas ; Rendon et al . , b). Throughout the duration of the experiment, body mass (weekly), coat colour (weekly) and oestrous cyclicity via vaginal cytology (weekly and 5 days prior to behavioural trials, Supporting Information) were assessed and reproductive tissues (ovaries and uterine horns) were collected at 10, 24 or 30 weeks.…”

Section: Methodsmentioning

confidence: 99%

“…Same‐sex aggressive encounters were staged, recorded and analysed for all animals after 10, 24 or 30 weeks in their respective photoperiodic treatments, using a 5‐min female–female resident‐intruder paradigm outlined previously (Rendon et al . , , b; Supporting Information). Latency to first attack (seconds) as well as number and duration (seconds) of attacks and chases were quantified for our suite of aggressive behaviours.…”

Section: Methodsmentioning

confidence: 99%

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Aggressive behaviours track transitions in seasonal phenotypes of female Siberian hamsters

et al. 2017

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SUMMARY Seasonally breeding animals exhibit profound physiological and behavioural responses to changes in ambient day length (photoperiod), including changes in reproductive function and territorial aggression. Species where aggression persists when gonads are regressed and circulating levels of gonadal hormones are low, such as Siberian hamsters (Phodopus sungorus) and song sparrows (Melospiza melodia), challenge the well-established framework that gonadal hormones are important mediators of aggression. A solution to this apparent paradox is that a season-specific increase in sensitivity to hormones in brain areas associated with aggression offsets low levels of gonadal hormones during periods of reproductive quiescence. To test this hypothesis, we manipulated photoperiod to induce natural fluctuations in seasonal phenotype across multiple stages of the annual reproductive cycle in female Siberian hamsters that display increased aggression during short-day reproductive quiescence, suggesting that behaviour persists independent of gonadal steroids. Females were housed in long “summer” days or short “winter” days for 10, 24 or 30 weeks to capture gonadal regression, transition back to a reproductively functional state and full gonadal recrudescence, respectively. Long-day animals maintained reproductive functionality and displayed low aggression across all time points. By week 10, short-day reproductively responsive females underwent gonadal regression and displayed increased aggression; non-responsive animals showed no such changes. At week 24, animals were in a transitional period and displayed an intermediate phenotype with respect to reproduction and aggression. By week 30, short-day females were fully recrudesced and returned to long-day-like levels of aggression. Consistent with our hypothesis, gonadally regressed females displayed decreases in 17β-oestradiol (oestradiol) levels, but site-specific increases in the abundance of brain oestrogen receptor-alpha (ERα) in regions associated with aggression, but not reproduction. Increased site-specific ERα may function as a compensatory mechanism to allow increased responsiveness to oestradiol in regulating aggression in lieu of high circulating concentrations of hormones. Collectively, these results broaden our understanding of how breeding phenology maps onto social behaviour and the mechanisms that have evolved to coordinate behaviours that occur in non-breeding contexts.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Aggressive behaviours track transitions in seasonal phenotypes of female Siberian hamsters

et al. 2017

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Section: Methodsmentioning

confidence: 99%

“…Seasonal phenotypes were determined based on a priori criteria that have been previously established for Siberian hamsters 46‐48 . Throughout the study, hamsters were weighed on a weekly basis to track changes in body mass, and coat colour was assessed to document the transition from summer brown/grey to winter white 47,48 . In addition, oestrous cycles were monitored via vaginal cytology for all experimental animals 5 days prior to behavioural trials to determine whether females were cycling, as described previously 25,47‐49 .…”

Section: Methodsmentioning

confidence: 99%

Seasonal patterns of melatonin alter aggressive phenotypes of female Siberian hamsters

Rendon

Petersen

Munley

et al. 2020

J Neuroendocrinology

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Many animal species exhibit year‐round aggression, a behaviour that allows individuals to compete for limited resources in their environment (eg, food and mates). Interestingly, this high degree of territoriality persists during the non‐breeding season, despite low levels of circulating gonadal steroids (ie, testosterone [T] and oestradiol [E2]). Our previous work suggests that the pineal hormone melatonin mediates a ‘seasonal switch’ from gonadal to adrenal regulation of aggression in Siberian hamsters (Phodopus sungorus); solitary, seasonally breeding mammals that display increased aggression during the short, ‘winter‐like’ days (SDs) of the non‐breeding season. To test the hypothesis that melatonin elevates non‐breeding aggression by increasing circulating and neural steroid metabolism, we housed female hamsters in long days (LDs) or SDs, administered them timed or mis‐timed melatonin injections (mimic or do not mimic a SD‐like signal, respectively), and measured aggression, circulating hormone profiles and aromatase (ARO) immunoreactivity in brain regions associated with aggressive or reproductive behaviours (paraventricular hypothalamic nucleus [PVN], periaqueductal gray [PAG] and ventral tegmental area [VTA]). Females that were responsive to SD photoperiods (SD‐R) and LD females given timed melatonin injections (Mel‐T) exhibited gonadal regression and reduced circulating E2, but increased aggression and circulating dehydroepiandrosterone (DHEA). Furthermore, aggressive challenges differentially altered circulating hormone profiles across seasonal phenotypes; reproductively inactive females (ie, SD‐R and Mel‐T females) reduced circulating DHEA and T, but increased E2 after an aggressive interaction, whereas reproductively active females (ie, LD females, SD non‐responder females and LD females given mis‐timed melatonin injections) solely increased circulating E2. Although no differences in neural ARO abundance were observed, LD and SD‐R females showed distinct associations between ARO cell density and aggressive behaviour in the PVN, PAG and VTA. Taken together, these results suggest that melatonin increases non‐breeding aggression by elevating circulating steroid metabolism after an aggressive encounter and by regulating behaviourally relevant neural circuits in a region‐specific manner.

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“…Siberian hamsters communicate with olfactory cues through multiple secretions such as urine, feces, ventral glands, and sacculi glands [40–43]. Urinary [44] and ventral gland [45] compounds vary across photoperiod, but only in males. Siberian hamsters also produce ultrasonic vocalizations (USVs) that differ according to photoperiod and sex during aggressive contexts, and likely use them in other contexts as well, potentially including reproduction [46, 47].…”

Section: Discussionmentioning

confidence: 99%

Food as a supplementary cue triggers seasonal changes in aggression, but not reproduction, in Siberian hamsters

Bailey

Rendon

O'Malley

et al. 2016

Physiology & Behavior

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Animals living in temperate regions prepare for harsh winter conditions by responding to environmental cues that signal resource availability (e.g., food, day length). Siberian hamsters (Phodopus sungorus) breed in long, summer-like days (LD, >14 h light), i.e., photoperiods, and undergo robust gonadal regression and become more aggressive when exposed to short, winter-like photoperiods that signal impending limited resources (SD, <10 h light). When hamsters are reared within an intermediate photoperiod (ID, 13.5 h light), they are re-productively active, but undergo gonadal regression in response to mild food restriction (FR) over 6–12 weeks. We hypothesized that short-term (1–2 weeks) FR inanID photoperiod would provide a signal of impending limited resources and initiate the seasonal increase in aggression typical of SD photoperiods, as well as alter reproductive behaviors in advance of gonadal regression. To test this, we housed male and female hamsters in LD or ID photoperiods, with ad libitum (AL) access to food or a 90%-AL ration. We tested aggressive behavior after one week and reproductive behavior after two weeks, and subsequently monitored females for pregnancy and litter production. Both sexes displayed increased aggression in the ID-FR treatment. Untreated male intruders were less likely to ejaculate when paired with ID females during reproductive encounters. ID-FR males were undergoing gonadal regression after two weeks, but were more likely to have ejaculated. Female pregnancy and litter characteristics were unaltered by treatment: females were equally likely to achieve pregnancy and produce comparable litters across treatment groups. Collectively, we demonstrate that a signal of diminishing resources in an ID photoperiod is sufficient to trigger seasonal aggression, but that hamsters are reproductively resilient to inhibitory environmental cues in the short term. Broadly, our findings provide an important context for exploring seasonal changes in behavior and physiology from an ultimate perspective.

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

Cited by 11 publications

References 37 publications

Aggressive behaviours track transitions in seasonal phenotypes of female Siberian hamsters

Aggressive behaviours track transitions in seasonal phenotypes of female Siberian hamsters

Seasonal patterns of melatonin alter aggressive phenotypes of female Siberian hamsters

Food as a supplementary cue triggers seasonal changes in aggression, but not reproduction, in Siberian hamsters

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