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.

Keywords: Siberian hamster; aggression; gonadal hormones; social play.

Figure 1

SD-rearing dissociates reproductive and social development in Siberian hamsters. Developmental profiles of (A) mean (±s.e.) estimated testis volume (ETV), (B) percent females exhibiting vaginal opening, (C) mean (±s.e.) number of play behaviors, and (D) mean (±s.e.) number of aggressive behaviors (D) of LD- and SD-reared male and female Siberian hamsters. ‘P’ indicates a main effect of Photoperiod within each time point (P<0.02, ANOVA); * indicates a significant difference between LD-reared males and SD-reared males (P<0.02, Fisher’s PLSD); # indicates a significant sex difference between LD-reared males and LD-reared females (P<0.003, Fisher’s PLSD); † indicates a significant increase in SD-male aggression at P100 versus all other ages (P<0.005, Fishers PLSD). Social behaviors were analyzed at the level of the pair and sample sizes were: LD-Female = 13; LD-Male = 10; SD-Female = 8; SD-Male = 7. Reproductive measures were analyzed at the level of the individual, hence samples sizes were double those of behavioral measures.

Figure 2

SD-rearing does not alter play asymmetry or its developmental increase across adolescence. Mean (+s.e.) asymmetry score for (A) playful and (B) aggressive interactions of LD- and SD-reared hamsters at postnatal day (P)20, P30, P40, P50, and P60. Play and aggression asymmetry of males and females did not differ; therefore data were collapsed across sex. Play and aggression asymmetry did not differ between LD and SD-reared hamsters at any age (P>0.28 for play at each age from P20 to P60, P>0.13 for aggression at each age from P30 to P60, ANOVA). Play asymmetry increased from P20 to P60 in both LD- and SD-reared hamsters (P<0.02, nonparametric sign test). Only a single pair exhibited aggression at P20. Sample sizes (pairs per group) are indicated within bars.

Figure 3

Prepubertal gonadectomy increases juvenile social play and decreases adult male aggression. Panels A, B, D, and E illustrate the mean (±s.e.) number of play and aggressive behaviors in sham-operated (Sham) and unoperated (Intact) LD-reared male and female hamsters; † indicates a significant difference between Sham and Intact female hamsters at P20 (P<0.008, Fisher’s PLSD). Because this surgical effect did not manifest at other ages for play or at any age for aggression, Sham and Intact groups were combined into a single control group (Con) at P30-P60 for play and at P20-P60 for aggression for comparisons with gonadectomized (GNX) hamsters in Panels C and F; ‘G’ indicates a significant main effect of GNX (P<0.004, ANOVA); ‘S’ indicates a significant main effect of Sex (P<0.02, ANOVA); * indicates a significant difference between GNX-Males and Con-Males (P<0.004, Fisher’s PLSD); # indicates significant a sex difference between Con-Males and Con-Females (P<0.001, Fisher’s PLSD). Sample sizes (pairs per group) were: Intact-Female = 13; Intact-Male = 10; Sham-Female = 3; Sham-Male = 5; Con-Female = 16; Con-Male = 15; GNX-Female = 7; GNX-Male = 6.

Figure 4

Gonadectomy does not alter play asymmetry or its developmental increase across adolescence. Mean (+s.e.) asymmetry score for playful interactions of LD-reared gonadectomized (GNX) and control hamsters at P20, P30, P40, P50, and P60. Play asymmetry of males and females did not differ; therefore data were collapsed across sex. Play and aggression asymmetry did not differ between GNX and Control hamsters at any age (P>0.09 at each age from P20 to P60, ANOVA). Play asymmetry increased from P20 to P60 in GNX and Control hamsters (P<0.02, nonparametric sign test). Sample sizes (pairs per group) are indicated within bars.