Mammalian Seasonal Rhythms: Behavior and Neuroendocrine Substrates

Stevenson, Tyler J.; Prendergast, Brian J.; Nelson, Randy J.

doi:10.1016/b978-0-12-803592-4.00013-4

Cited by 31 publications

(18 citation statements)

References 295 publications

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“…The VTA contains dopaminergic neurones that project to several forebrain regions and have been shown to regulate motivation, reproduction and parental behaviours 42,81,82. The PVN has a critical role in regulating seasonal reproduction, particularly by serving as a control center for the hypothalamic‐pituitary‐gonadal (HPG) axis 1‐3. Furthermore, the PVN contains neurones that synthesise the neuropeptides arginine vasopressin (AVP) and oxytocin (OXT),83,84 and changes in AVP and OXT levels within the PVN have been associated with reproductive and sexual behaviours 41.…”

Section: Discussionmentioning

confidence: 99%

“…Such fluctuations in temperature, water and food availability in the environment require individuals to respond to temporal and spatial niches from winter to summer. The unique demands of these extreme conditions result in reproductive inhibition during unfavourable conditions 1,2 . Thus, seasonally breeding animals limit reproduction to the spring and summer, which coincide with relatively warm ambient temperatures and abundant resources, and shift to reproductive quiescence during the winter, when physiological and behavioural adaptations tend to be geared towards survival rather than reproduction 1‐4 …”

Section: Introductionmentioning

confidence: 99%

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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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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

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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“…If this occurs, behavioral development seen in the seasonal-species approach could be regulated by the combination of changing pubertal hormones, changes in the sensitivity to these hormones, as well as puberty-independent changes in neural circuits. Photoperiod also regulates many seasonal traits in addition to puberty (e.g., body mass, immune function, thermoregulation) [29,30], and effects of SD-rearing could be due to photoperiod influences on these non-reproductive systems. This is less of an issue when photoperiod does not alter the adolescent trait, as seen in the present study for the timing of the transition from play to aggression.…”

Section: Discussionmentioning

confidence: 99%

Dissociation of Puberty and Adolescent Social Development in a Seasonally Breeding Species

et al. 2018

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Alongside the development of sexual characteristics and reproductive competence, adolescents undergo marked cognitive, social, and emotional development [1]. A fundamental question is whether these changes are triggered by activation of the hypothalamic-pituitary-gonadal (HPG) axis at puberty (puberty dependent) or whether they occur independently of HPG activation (puberty independent). Disentangling puberty-dependent from puberty-independent mechanisms is difficult because puberty and adolescence typically proceed concurrently. Here, we test a new approach that leverages natural adaptations of a seasonally breeding species to dissociate pubertal status from chronological age. Siberian hamsters (Phodopus sungorus) reared in a long, summer-like day length (LD) exhibit rapid pubertal development, whereas those reared in a short, winter-like day length (SD) delay puberty by several months to synchronize breeding with the following spring [2, 3]. We tested whether the SD-induced delay in puberty delays the peri-adolescent decline in juvenile social play and the rise in aggression that characterizes adolescent social development in many species [4-6] and compared the results to those obtained after prepubertal gonadectomy. Neither SD rearing nor prepubertal gonadectomy altered the age at which hamsters transitioned from play to aggression; SD-reared hamsters completed this transition prior to puberty. SD rearing and prepubertal gonadectomy, however, increased levels of play in male and female juveniles, implicating a previously unknown role for prepubertal gonadal hormones in juvenile social behavior. Levels of aggression were also impacted (decreased) in SD-reared and gonadectomized males. These data demonstrate that puberty-independent mechanisms regulate the timing of adolescent social development, while prepubertal and adult gonadal hormones modulate levels of age-appropriate social behaviors.

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“…Over evolutionary time, there has been selection for exquisite precision in photoperiodic regulation of physiology and behavior tied to environmental conditions (Stevenson, Prendergast, & Nelson, 2017). Over evolutionary time, there has been selection for exquisite precision in photoperiodic regulation of physiology and behavior tied to environmental conditions (Stevenson, Prendergast, & Nelson, 2017).…”

Section: Climate Chang E and Photoperiodmentioning

confidence: 99%

Global climate change and invariable photoperiods: A mismatch that jeopardizes animal fitness

Walker

Meléndez-Fernández

Nelson

et al. 2019

Ecology and Evolution

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The Earth's surface temperature is rising, and precipitation patterns throughout the Earth are changing; the source of these shifts is likely anthropogenic in nature. Alterations in temperature and precipitation have obvious direct and indirect effects on both plants and animals. Notably, changes in temperature and precipitation alone can have both advantageous and detrimental consequences depending on the species. Typically, production of offspring is timed to coincide with optimal food availability; thus, individuals of many species display annual rhythms of reproductive function. Because it requires substantial time to establish or re‐establish reproductive function, individuals cannot depend on the arrival of seasonal food availability to begin breeding; thus, mechanisms have evolved in many plants and animals to monitor and respond to day length in order to anticipate seasonal changes in the environment. Over evolutionary time, there has been precise fine‐tuning of critical photoperiod and onset/offset of seasonal adaptations. Climate change has provoked changes in the availability of insects and plants which shifts the timing of optimal reproduction. However, adaptations to the stable photoperiod may be insufficiently plastic to allow a shift in the seasonal timing of bird and mammal breeding. Coupled with the effects of light pollution which prevents these species from determining day length, climate change presents extreme evolutionary pressure that can result in severe deleterious consequences for individual species reproduction and survival. This review describes the effects of climate change on plants and animals, defines photoperiod and the physiological events it regulates, and addresses the consequences of global climate change and a stable photoperiod.

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Mammalian Seasonal Rhythms: Behavior and Neuroendocrine Substrates

Cited by 31 publications

References 295 publications

Seasonal patterns of melatonin alter aggressive phenotypes of female Siberian hamsters

Seasonal patterns of melatonin alter aggressive phenotypes of female Siberian hamsters

Dissociation of Puberty and Adolescent Social Development in a Seasonally Breeding Species

Global climate change and invariable photoperiods: A mismatch that jeopardizes animal fitness

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