Vocalizations convey sex, seasonal phenotype, and aggression in a seasonal mammal

Rendon, Nikki M.; Keesom, Sarah M.; Amadi, Chima; Hurley, Laura M.; Demas, Gregory E.

doi:10.1016/j.physbeh.2015.09.014

Cited by 23 publications

(21 citation statements)

References 39 publications

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“…Further, in response to inhibitory photoperiods, females displayed considerable variation in the onset of reproductive incompetence (between 5 and 14 weeks) and subsequent refractoriness, observed by the onset of reproduction (as late as week 28). Such findings greatly expand our knowledge of female seasonal aggression (see Badura & Nunez 1989;Scotti, Place & Demas 2007;Rendon et al 2015a). It is predicted that anoestrous females would not mate during periods of gonadal regression and the transitional period (i.e.…”

Section: A G G R E S S I V E B E H a V I O U R S T R A C K S E A S O mentioning

confidence: 71%

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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: A G G R E S S I V E B E H a V I O U R S T R A C K S E A S O mentioning

confidence: 71%

“…Such findings greatly expand our knowledge of female seasonal aggression (see Badura & Nunez ; Scotti, Place & Demas ; Rendon et al . ). It is predicted that anoestrous females would not mate during periods of gonadal regression and the transitional period (i.e.…”

Section: Discussionmentioning

confidence: 97%

Aggressive behaviours track transitions in seasonal phenotypes of female Siberian hamsters

et al. 2017

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“…Although sex differences in auditory communication have been suggested to be common in animals [53], particularly in the context of attracting mating patterns [30,40], differences in USV emission under stress between males and females have been less frequently investigated in mouse pups. In our study, USV emission was sexually dimorphic when the age effect was taken into account in MD180 Post and MD360 Post pups; we found that the female pups called more frequently and for longer durations than the males on P7 and P8 in the MD180 Post group, and the females vocalized for a longer period of time on P3 than the males among MD360 Post pups; no obvious differences were found on the other test days and in terms of USV frequency.…”

Section: Discussionmentioning

confidence: 99%

Maternal Deprivation Influences Pup Ultrasonic Vocalizations of C57BL/6J Mice

et al. 2016

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Maternal deprivation (MD) is frequently used as an early life stress model in rodents to investigate behavioral and neurological responses under stressful conditions. However, the effect of MD on the early postnatal development of rodents, which is when multiple neural systems become established, is rarely investigated due to methodological limitations. Ultrasonic vocalizations (USVs) are one of the few responses produced by neonatal rodents that can be quantitatively analyzed, and the quantification of USVs is regarded as a novel approach to investigate possible alterations in the neurobehavioral and emotional development of infant rodents under stress. To investigate the effect of MD on pup mice, we subjected C57BL/6J mice to MD and recorded the USVs of pups on postnatal days 1, 3, 7, 8, and 14. To determine whether the effect of MD on USVs was acute or cumulative, pre- and post-separation USV groups were included; sex differences in pup USV emission were also investigated. Our results suggest that (i) USV activity was high on postnatal days 3–8; (ii) the MD effect on USVs was acute, and a cumulative effect was not found; (iii) the MD mice vocalized more and longer than the controls at a lower frequency, and the effect was closely related to age; and (iv) female pups were more susceptible than males to the effect of MD on USV number and duration between postnatal days 3–8.

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“…Pre‐ and post‐aggression levels of serum DHEA, T and E 2 were quantified using commercially available enzyme immunoassay kits that have been previously validated in this species (DHEA: assay sensitivity = 0.108 ng mL ‐1 ; ALPCO Diagnostics, Salem, NH, USA; 20‐DHEHU‐E01 39,53 ; T: assay sensitivity = 5.67 pg mL ‐1 ; Assay Design, Ann Arbor, MI, USA; 900‐065 54,55 ; E 2 : assay sensitivity = 14.0 pg mL ‐1 ; Enzo Life Sciences, Farmingdale, NY, USA; ADI‐900‐174 25 ). Each of these kits is highly specific for the hormone of interest and have negligible or undetectable cross‐reactivity with other steroid hormones (DHEA kit: sulfated DHEA = 0.01%, T = 0.01%, E 2 = < 0.01%, cortisol = < 0.01%; T kit: 19‐hydroxytestosterone = 14.6%, androstenedione = 7.2%, DHEA = 0.7%, E 2 = 0.4%; E 2 kit: oestrone = 17.8%, oestriol = 0.9%, T = 0.01%, DHEA = < 0.001%).…”

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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Vocalizations convey sex, seasonal phenotype, and aggression in a seasonal mammal

Cited by 23 publications

References 39 publications

Aggressive behaviours track transitions in seasonal phenotypes of female Siberian hamsters

Aggressive behaviours track transitions in seasonal phenotypes of female Siberian hamsters

Maternal Deprivation Influences Pup Ultrasonic Vocalizations of C57BL/6J Mice

Seasonal patterns of melatonin alter aggressive phenotypes of female Siberian hamsters

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