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

Abstract

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.

Suppression of ovarian hormones in adolescent rats has no effect on anxiety‐like behaviour or c‐fos activation in the amygdala

“…This finding is consistent with a previous study showing that the total amount of adolescent social play was not influenced by pre‐pubertal ovariectomy in female rats 33 . By contrast, a recent study reported increased frequencies of play with a familiar partner following pre‐pubertal gonadectomy in female Siberian hamsters 85 . In addition, subtle aspects of posture during social interactions have been shown to be influenced by early gonadal hormone exposure in rats, 31,33 and so we cannot exclude the possibility that Antide treatment might have had more fine‐grained effects on social behaviour that were not evident in the present study.…”

The Makorin lep-2 and the lncRNA lep-5 regulate lin-28 to schedule sexual maturation of the C. elegans nervous system

“…In this view, the activational effects of gonadal steroids at puberty (McCarthy et al, 2012) are likely to be a recent evolutionary adaptation that reinforces sexual differentiation of the mammalian nervous system via an endocrine feedback loop. Moreover, it suggests that puberty-independent events outside the hypothalamus that contribute to behavioral maturation during mammalian adolescence, such as the transition from play to aggression in Siberian hamsters (Paul et al, 2018), could also be timed by the heterochronic pathway.…”

Function and Evolution of Nuclear Receptors in Environmental-Dependent Postembryonic Development

“…Steroid signaling is thereby orchestrated by a range of environmental and developmental cues, which again, are highly species specific. Vertebrates include day length and/or body size information to time puberty with season and food availability ( Leka-Emiri et al, 2017 ; Paul et al, 2018 ; Hanlon et al, 2020 ), which are the most common sources for environmentally induced variation (phenotypic plasticity).…”