In nonhuman primates, the measurement of behavioral responses to social intrusion by an unfamiliar conspecific, assessed under controlled conditions in the laboratory environment, has proved useful for assessing individual variation in temperament traits that relate to differences in sex, age, and genetic background (29
). In our analysis, we uncovered five behavioral dimensions characterizing the response of rhesus macaques to an unfamiliar conspecific. Of these, the High-Risk Aggression factor explained the highest amount of variance. This factor is labeled “high risk” because contact aggression directed toward an intruder, which is inherently risky, was exhibited even in the presence of an aggressive intruder. The fact that this type of behavior accounted for so much of the variance (17.2%) is not surprising when one considers that aggression is common in the context of intergroup encounters between unfamiliar animals in the natural habitat, especially among Old World primates. For the most part, this aggression is carried out by males targeting other males, although aggression between females is not uncommon (33
). As predicted, levels of High-Risk Aggression in this study were significantly higher in male test subjects compared with females. Further analysis of this factor also showed that male test subjects received more aggression from the intruder than did female test subjects.
In addition, adult males scored significantly higher on the Gregariousness/Boldness factor compared with all other age and sex groups. The fact that adult males spent significantly more time in social contact with the intruder suggests that adult males are more apt to engage the intruder in general, even in a nonaggressive manner. Females and subadult males, in contrast, are more likely to maintain a safe distance from the intruder. Together, our results support the notion that when faced with an environmental threat, males are more likely than females to adopt an aggressive or bold strategy. Interestingly, parallel findings have emerged in investigations of human defensive behaviors. When males and females are presented with scenarios involving an unfamiliar person, males are more likely to choose an attack response in highly threatening situations, whereas females are more likely to yell, scream, or call for help (35
). Furthermore, females tend to feel more threatened when faced with these scenarios. Considered together, the data from human and nonhuman primates highlight some of the similarities between species in defensive behavior and suggest that sex differences in response to social threat may have been preserved as part of our evolutionary history.
What is novel about the current findings is that the effects of genotype that were observed on aggressive responses were limited to individuals who also had a prior history of stress. Males carrying the s
allele who were exposed to early adversity in the form of nursery rearing showed significantly higher levels of High-Risk Aggression toward the intruder. This result was mirrored by a similar G×E interaction for contact aggression toward the intruder, one of the components of the High-Risk Aggression factor. Early life stress or maltreatment has been linked to adolescent and adult aggression in humans (37
) as well as in some animal models, including data from our own laboratory (41
). Interestingly, studies linking early-life maltreatment to aggression in rodents have observed these effects primarily in males (41
). Our findings for male rhesus macaques exposed to stress in the form of nursery rearing provides additional evidence of an association between early-life stress and later aggression that is limited to males. This effect of early adversity was mediated, however, by genetic variation in the serotonin transporter regulatory region. Variation in this region in humans has been related to aggression and violent behavior in some studies, but results for a main genotype effect have not been consistent (44
). Two recent studies have reported G×E effects involving 5-HTTLPR
. Verona et al.
) observed increased aggression (i.e., delivering shocks to a putative “employee” in a laboratory environment) in males homozygous for the serotonin transporter s
allele when they were exposed to an acute stressor (intermittent blasts of compressed air to the throat). Reif et al.
) found that males carrying the s
allele were more prone to violent criminal behavior if they also had an adverse childhood environment. Our results complement and expand on these human findings in several ways. First, whereas similar studies in humans typically rely on retrospective assessments of both childhood environment and aggression or violence, we were able to assess aggressive behavior directly in a sample of monkeys with carefully controlled early environments. Second, our finding of a G×E effect in males, but not females, with a history of early adversity underscores the need to consider sex differences in investigations of G×E interactions. Lastly, whereas our results parallel those of Verona and colleagues, both in the analysis of directly observable aggressive behavior and in the finding of male-limited G×E effect, the latter study used an acute stressor and did not take into account effects of early-life history. Our results also add to human studies of another functional variant that influences serotonin system functioning, monoamine oxidase (MAOA
), that has been shown to interact with early maltreatment to predict various indexes of aggression and related clinical outcomes (51
). Although many of these studies also are limited to males, there is emerging evidence that MAOA
interacts with maltreatment in females as well (56
The strategies adopted by males and females when faced with an environmental stressor in many ways parallel those described in the Hawk–Dove model, first proposed by Maynard Smith and Price (57
) and expanded on by Korte and colleagues (5
). In this model, an aggressive/bold strategy (Hawk) is opposed by a nonaggressive, cautious strategy (Dove), with natural selection maintaining a balance of traits preserving genes for these strategies within a population (5
). Similarly, Taylor and colleagues have proposed a model in which males have evolved to exhibit the classic “fight-or-flight” response to stress, whereas females have evolved to exhibit a “tend-and-befriend” response, protecting themselves as well as their offspring from environmental threat (58
). Both of these models map well onto the proposed genetic structure of externalizing and internalizing human psychiatric disorders (59
). It is important to note, however, that considerable individual differences exist within each sex when it comes to coping with environmental variation (5
). To an extent, our findings are consistent with these models. In general, male rhesus macaques adopted a more aggressive strategy when faced with the social threat of an intruder. In our report, we show that individual variation in this aggressive strategy is related to genetic variation influencing serotonin system functioning and exposure to early-life stress. The apparent lack of aggression toward intruder animals on the part of females also fits with these models, with a couple of caveats. First, female test subjects were exposed to female intruder animals, who were less aggressive and thus potentially less likely to elicit an aggressive response. Second, there is some evidence that females may act aggressively in the context of social intrusion, even if not toward the intruder animal. Redirected Aggression (i.e., aggression toward own group members in the context of threat from an unfamiliar animal) was slightly more common in females than males, although the difference was not significant (mean ± SEM for females, .083 ± .097; males, = −/−.158 ± .138). Furthermore, the data suggest an effect of rh5-HTTLPR
on this behavior in females, with s
allele carriers displaying higher levels of Redirected Aggression than l/l
subjects (Figure S1 in Supplement 1
). Aggression in this context could potentially be “protective,” that is, aimed at other group members to correct or modify their behaviors. Other forms of aggression (i.e., “displaced” or “redirected” aggression) occur in a variety of other animal species as well as humans and is argued by some to be a postconflict interaction that functions to reduce anxiety or stress (60
). In any case, it may be that among females, genetic variation that influences aggression is more likely to be reflected in intragroup relations than intergroup encounters.
Evolutionary psychology predicts that during evolutionary history, males and females will come to differ in those domains that have evolved in response to sex-differentiated adaptive problems (66
). On the basis of this viewpoint, one would expect that genetic and environmental factors, as well as interactions between the two, would have different effects on behavior and other outcomes in males and females. Responding to social threat is one domain in which males and females are likely to adopt different adaptive solutions. We have shown in this study that the rhesus macaque 5-HTTLPR
polymorphism differentially influences aggressive responses to social threat in males and females. Overall, our results lend further support to the notion that males are more vulnerable to externalizing disorders and that genetic variation that affects serotonin system function may play a role in this differential susceptibility (15
). These findings highlight the importance of interactions that exist among behavior, genes, and the environment and suggest that sex differences in vulnerability to psychopathology may be grounded in our evolutionary history.