The agonistic adrenal: melatonin elicits female aggression via regulation of adrenal androgens

Rendon, Nikki M.; Rudolph, Lauren M.; Sengelaub, Dale R.; Demas, Gregory E.

doi:10.1098/rspb.2015.2080

Cited by 48 publications

(102 citation statements)

References 44 publications

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“…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%

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%

Aggressive behaviours track transitions in seasonal phenotypes of female Siberian hamsters

et al. 2017

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“…Beginning at pnd25 and every day thereafter until reproductive maturity, all female offspring ( n =24 saline-treated; n =29 LPS-treated) were monitored daily to determine the time of initial vaginal opening [28]. Female estrous cycles were monitored via vaginal cytology during the 5 consecutive days of behavioral testing (pnd71-75) [29,30]. Vaginal cell samples were obtained via vaginal lavage.…”

Section: Methodsmentioning

confidence: 99%

Overcoming neonatal sickness: Sex-specific effects of sickness on physiology and social behavior

Sylvia

Demas

2017

Physiology & Behavior

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Early-life environmental stressors, including sickness, have the potential to disrupt development in ways that could severely impact fitness. Despite what is known about the effects of sickness on reproduction, the precise physiological mechanisms have not yet been determined. The goal of this study was to investigate the effects of a neonatal immune challenge on adult reproductive physiology and opposite-sex social behavior. Male and female Siberian hamster (Phodopus sungorus) pups were administered lipopolysaccharide ([LPS]; a cell wall component of gram-negative bacteria) or saline injections on postnatal days 3 and 5 and body mass, food intake, and measures of reproductive maturity were taken throughout development. In adulthood, hamsters were placed in staged mating pairs with reproductively mature individuals of the opposite sex, during which a series of behaviors were scored. We found that although males and females showed no change in food intake, body mass, or reproductive behaviors, LPS-treated females had abnormal estrous cycles and smaller ovaries. Females also showed increased investigation of and increased aggression towards males in a reproductive context. In contrast, LPS-treated males showed no change in any physiological measures, nor did they show any changes in behavior. The present findings demonstrate that females may be more robustly affected by neonatal sickness than males and that these effects could have potential impacts on reproductive success. Collectively, the results of this study can be used to expand upon what is already known about sickness and reproduction, specifically the importance of social behaviors involved in pre-copulation and information necessary to choose the appropriate mate.

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“…Notably, the adrenal androgen DHEA (a gonadal steroid precursor) has emerged as an important correlate of non-breeding season aggression in several species [7,12, 31,33,34]. In Siberian hamsters specifically, our group has demonstrated a “seasonal shift” in endocrine mechanisms supporting aggression from gonadal steroids in the breeding season to the adrenal androgen DHEA in the non-breeding season [12]. This shift allows for a decoupling of aggressive behavior from hormonal mechanisms underlying reproduction, which would be adaptive for species that must maintain aggression for other functions (i.e., defense of limited food resources) during times of reproductive quiescence.…”

Section: Discussionmentioning

confidence: 99%

“…Aggressive behavior was recorded and analyzed after 1 week of FR for same-sex social interactions according to previously outlined methods for males and females of this species, using a resident/intruder paradigm [4,12]. Dyads were staged such that they were composed of a resident hamster (exposed to experimental treatments) and a same-sex intruder hamster.…”

Section: Methodsmentioning

confidence: 99%

“…Photoperiod is encoded through a physiological signal of melatonin, which is secreted from the pineal gland during the night, in the absence of light (reviewed in: [9]). Greater durations of melatonin secretion in longer dark periods of winter (approximately 8–10 h of light) trigger seasonal responses such as robust gonadal regression to curtail reproduction as well as increased aggressive behavior [3–5,10–12]. Hamsters detect the duration of melatonin release in the present as well as the change in the duration of release over time in order to predict future environmental conditions.…”

Section: Introductionmentioning

confidence: 99%

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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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The agonistic adrenal: melatonin elicits female aggression via regulation of adrenal androgens

Cited by 48 publications

References 44 publications

Aggressive behaviours track transitions in seasonal phenotypes of female Siberian hamsters

Aggressive behaviours track transitions in seasonal phenotypes of female Siberian hamsters

Overcoming neonatal sickness: Sex-specific effects of sickness on physiology and social behavior

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

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