Gonadectomy negatively impacts social behavior of adolescent male primates

Abstract

Social behavior changes dramatically during primate adolescence. However, the extent to which testosterone and other gonadal hormones are necessary for adolescent social behavioral development is unknown. In this study, we determined that gonadectomy significantly impairs social dominance in naturalistic settings and changes reactions to social stimuli in experimental settings. Rhesus macaques were castrated (n= 6) or sham operated (n=6) at age 2.4 years, group-housed for 2 years, and ethograms were collected weekly. During adolescence the gonadally intact monkeys displayed a decrease in subordinate behaviors and an increase in dominant behaviors, which ultimately related to a rise in social status and rank in the dominance hierarchy. We measured monkey's reactions to emotional faces (fear, threat, neutral) of conspecifics of three ages (adult, peer, infant). Intact monkeys were faster to retrieve a treat in front of a threatening or infant face, while castrated monkeys did not show a differential response to different emotional faces or ages. No group difference in reaction to an innate fear-eliciting object (snake) was found. Approach and proximity responses to familiar vs unfamiliar conspecifics were tested, and intact monkeys spent more time proximal to a novel conspecific as compared to castrates who tended to spend more time with a familiar conspecific. No group differences in time spent with novel or familiar objects were found. Thus, gonadectomy resulted in the emergence of significantly different responses to social stimuli, but not non-social stimuli. Our work suggests that intact gonads, which are needed to produce adolescent increases in circulating testosterone, impact social behavior during adolescences in primates.

Figure 1

Weight and testosterone levels throughout adolescence. The top panel shows body weights (kg) did not differ significantly between the intact animals (filled circles) and gonadectomized animals (unfilled circles) at any time point. The middle panel shows morning testosterone levels were significantly different between groups beginning at 49 months of age (*** p < 0.001). Night testosterone levels were significantly different between the intact group as compared to the gonadectomized group beginning at 38 months age (** p < 0.01). Data represent mean ± SEM.

Figure 2

Social dominance difference scores (defined as the difference between the total number of observed dominant and subordinate behaviors per monkey per ethogram session) before puberty (Pre) and after puberty (Post). In both cohorts, all but one intact animal (Intact ●) increased their dominance ranking while the gonadectomized animals (Gdx Δ) lost ranking or stayed equivalent over time.

Figure 3

Changes in the average frequency of dominant and subordinate behaviors were measured relative to the change in total social behaviors for each monkey. The left panel shows intact animals (Intact ●) had a significantly higher ratio of change in dominant behavior frequency to change in social behavior frequency than gonadectomized animals (Gdx ○) (p = 0.02). The right panel shows the ratio between the change in subordinate behavior frequency and change in social behavior frequency was significantly larger for gonadectomized animals (p = 0.02).

Figure 4

Latency to retrieve a food reward from in front of a photograph of a novel monkey or a rubber snake relative to the latency to retrieve a reward from in front of a blank picture or neutral object are plotted (means and SEMs). The top panel shows gonadectomized animals (Gdx, white bars) were significantly slower than intacts (Intacts, black bars) to respond to pictures of monkeys with threatening facial expressions (* p < 0.05). The middle panel shows gonadectomized animals were significantly slower to respond to pictures of infant monkeys than intact animals (** p < 0.01). The bottom panel shows there was no significant differences in response time to a rubber snake between groups, and responses for both groups got faster after the first testing day.

Figure 5

The average total duration of time (sec) each group spent in the proximate quadrant with the novel and familiar monkey (top panel) and the novel and familiar object (bottom panel) during the final test session are plotted (means and SEM). The intact group (black bar) spent significantly more time with the novel intruder than the gonadectomized group (white bar) (* p < 0.05). There were no significant differences between groups in the object novelty test, however both groups spent significantly more time with the novel object compared to the familiar object (* p < 0.05).