Serotonergic influences on life‐history outcomes in free‐ranging male rhesus macaques

Abstract

Several studies have demonstrated that nonhuman primate males with low cerebrospinal fluid (CSF) levels of the serotonin metabolite 5-hydroxyindoleacetic acid (5-HIAA) exhibit antisocial behavior patterns. Included in these deleterious patterns are impulse control deficits associated with violence and premature death. No studies to date have longitudinally studied the long-term outcome of young subjects with low CSF 5-HIAA concentrations as they mature into adults. In this study we examined longitudinal relations among serotonergic and dopaminergic functioning, as reflected in CSF metabolite concentrations, aggression, age at emigration, dominance rank, and mortality in free-ranging rhesus macaque (Macaca mulatta) males. Our results indicate long-term consistency of individual differences in levels of 5-HIAA in CSF in the subject population from the juvenile period of development through adulthood. We found a significant negative correlation between 5-HIAA concentrations measured in juveniles and rates of high-intensity aggression in the same animals as adults. Further, CSF 5-HIAA concentrations were lower in juveniles that died than in animals that survived. For the young animals that migrated there was a positive correlation between CSF 5-HIAA concentration and age at emigration, whereas for the animals that remained in their troop until later in sexual maturity there was a negative correlation between CSF 5-HIAA concentration and age of emigration. After animals emigrated to a new troop, social dominance rank in the new troop was positively correlated with early family social dominance rank, but inversely correlated with juvenile CSF 5-HIAA concentrations. Taken together, our findings suggest that males with low central serotonin levels early in life delay migration and show high levels of violence and premature death, but the males that survive achieve high rank. These findings indicate that longitudinal measures of serotonergic and dopaminergic functioning are predictive of major life-history outcomes in nonhuman primate males. Low concentrations of CSF 5-HIAA are associated with negative life-history patterns characterized by social instability and excessive aggression, and positive life-history patterns characterized by higher dominance rank.

Brain Monoamine Oxidase A Activity Predicts Trait Aggression

“…In considering the clinical implications of our findings, it is important to note that, because MAO A enzymatic activity is responsible for the regulation of central serotonergic activity in terms of availability and subsequent extrasynaptic degradation (for a recent review, see Buckholtz and Meyer-Lindenberg, 2008), it would seemingly follow that having low MAO A activity will result in high serotonin levels. Indeed, MAO A knock-out mice have high circulating serotonin (Cases et al, 1995); however, when serotonin metabolites are examined in aggressive humans (Moffitt et al, 1998) as well as aggressive rhesus monkeys (Howell et al, 2007), they are found to be low. This difference is possibly attributable to compensatory mechanisms that primates may have developed to maintain control of high serotonin levels that could be neurotoxic (Baumgarten and Lachenmayer, 2004).…”

Personality-dependent dispersal: characterization, ontogeny and consequences for spatially structured populations

“…Mehlman et al (1995) showed that the concentration in cerebrospinal fluid (CSF) of the serotonin metabolite 5-hydroxyindoleacetic acid (5-HIAA), which is consistent over time (Howell et al 2007), is negatively correlated to aggressiveness in the natal group and positively correlated with age at emigration from the natal group (see also §3). Thus, aggressive individuals disperse earlier than less aggressive ones prior to or during adolescence (note that this relationship is reversed for individuals that dispersed after the age of sexual maturity; Howell et al 2007).…”

“…These results indicate the existence of an aggressive personality trait and suggest a strong role of personality in dispersal success and range expansion. In addition, in rhesus macaque males, social dominance rank in the new troop (after they emigrated to a new troop) was negatively correlated with juvenile CSF 5-HIAA concentrations, even if it has been shown that, males with low CSF 5-HIAA concentrations are less likely to be sought out as sexual partners by receptive females following emigration than are males with high CSF 5-HIAA concentrations (Howell et al 2007). …”

“…However, several studies reported that disperser behavioural differences are consistent over long periods of time. For example, the consistency of behaviour has been observed up to a year after dispersal events in common lizards (Aragon et al 2006b;Cote & Clobert 2007;Meylan et al 2009), and up to five months in mosquitofish (Cote et al submitted), and levels of serotonin metabolite as juveniles are correlated to both levels of serotonin metabolite and aggressiveness 8 -10 years later in the rhesus macaque (Howell et al 2007). This suggests that, at least in some species, the disperser behavioural syndrome is not simply a short-term shift in behaviour in response to conditions associated with dispersal per se, or establishment in a new site.…”

A quantitative trait locus for variation in dopamine metabolism mapped in a primate model using reference sequences from related species

“…Levels of HVA have been related to aggressive behavior, wounding, sexual behavior, and social dominance in vervets and macaques (12,(20)(21)(22)(23). Numerous studies suggest associations between CSF MA metabolite concentrations and various human behavioral disorders (15,24,25), but other than relationships of CSF 5-HIAA to suicidal and aggressive behaviors (26), these associations remain mostly equivocal and nonreplicated, in part because of the difficulty in obtaining CSF from sufficient human subjects.…”