Our research involves broad-based investigation of primate biobehavioral development through comparative longitudinal studies of rhesus monkeys and other nonhuman primate species. Our primary research goals are to characterize different distinctive biobehavioral phenotypes in our rhesus monkey colony, to determine how genetic and environmental factors interact to shape this primate’s development, and to assess the long-term biobehavioral consequences for monkeys from different genetic backgrounds when they are reared in various physical and social environments. A second major focus of our research involves how rhesus monkeys and other nonhuman primate species born and raised under different laboratory conditions adapt to placement into environments that model specific features of their natural habitat. In this program of research, we assess adaptation by examining behavioral repertoires and monitoring a variety of physiological systems in monkeys throughout the lifespan, developing broad-based indices of relative physical and psychological well-being. We also assess the responses of subjects to experimental manipulations of selected features of their respective environments. Whenever possible, we collect field data for appropriate comparisons. We also focus on investigating the cognitive, behavioral, and social processes involved in adaptation to new settings and circumstances.

Developmental Continuity of Individual Differences in Rhesus Monkey Biobehavioral Development
Champoux, Higley S, Novak, Parker, Roma, Shannon-Lindell, Suomi; in collaboration with Bennett, Graham
Several of our ongoing studies focus on possible interactions between a polymorphism (due to length variation in the promoter region) in 5HTT, which is a candidate gene for impaired serotonergic function, and differential early social experience. This past year, we published the first report of a specific gene-environment interaction in a nonhuman primate species: rhesus monkeys with the “short” (LS) allele exhibited deficits in central serotonin metabolism compared with those with the “long” (LL) allele, but only if they had been nursery-reared; in contrast, LS monkeys reared by their biological mother had normal serotonin metabolism, suggesting a “buffering” effect of maternal rearing. A second study reported a similar buffering effect of maternal rearing for measures of state control and visual orienting obtained during the first month of life. Preliminary analyses have revealed additional examples of maternal buffering for LS rhesus monkeys in the expression of impulsive aggression and social play behavior during the monkeys’ juvenile years.

Rhesus monkeys are notoriously aggressive as a species compared with other macaques and most other primates; Barbary macaques, on the other hand, are unusual in their relatively low levels of aggression. This past year, we were able to genotype members of a group of free-ranging Barbary macaques with respect to the 5-HTT gene and, unlike the case for rhesus monkeys, found no individuals with either the LS or the LL allele. Instead, all the sampled Barbary macaques had an “extra long” (XL) allele, a form found in less than 2 percent of the rhesus monkeys genotyped to date. We are currently genotyping other Barbary macaques who came from different geographic regions than our original group to evaluate the generality of our finding. To model the evolutionary history of 5HTT in primates, we have also begun coding the promoter region of the 5-HTT gene in several other nonhuman primate species representing different taxa.

This past year, we also characterized a polymorphism in the MAO-A receptor gene, demonstrated functional differences among the different alleles, genotyped the LCE rhesus monkey colony with respect to the above polymorphism, and began analyzing a variety of behavioral and physiological measures as a function of genetic status and early rearing history. Our initial analysis revealed a significant allele–rearing history interaction for aggressive behavior during the juvenile years: whereas mother-reared monkeys with the “7” allele initiated more bouts of aggression than those with the “5” or “6” allele, nursery-reared monkeys exhibited the reverse. Similar analyses are currently under way for other behavioral and physiological measures collected from the same monkeys throughout their development.

We also completed a study investigating the relationship between serotonin metabolism and measures of impulsive and aggressive behavior in adult female rhesus monkeys living in free-ranging naturalistic social groups. Previous work had demonstrated that low cerebrospinal fluid (CSF) concentrations of 5-HIAA, the primary central serotonin metabolite, were associated with a relatively high incidence of risky, impulsive behavior and socially inappropriate, violent aggression (but not with low-level, socially appropriate dominance behavior) in free-ranging adult male rhesus monkeys and in both adult male and female rhesus monkeys reared in captivity. Our analyses revealed that low CSF 5-HIAA concentrations in free-ranging females were also associated with excessive risky, impulsive behavior but not with violent aggression; instead, we found a significant negative correlation between CSF 5-HIAA and socially appropriate dominance behavior. The findings suggest a divergence between male and female rhesus monkeys in their competitive strategies, which may be explicable in terms of the distinctive social structure and life history patterns in the species.

Behavioral Effects of Long-Chain Essential Fatty Acid Supplements
Champoux, Shannon-Lindell, Suomi; in collaboration with Higley J, Hibbeln
Finally, we published a study examining the biobehavioral consequences of adding a long-chain essential fatty acid supplement to the standard diet of nursery-reared rhesus monkey infants. The supplement effectively raised their serum levels to those characteristic of infants raised (and nursed) by their biological mothers. The standard nursery formula diet, like most commercially available human infant formula diets, is lacking in certain long-chain essential fatty acids, and monkey infants raised on the standard formula consistently have lower serum levels of long-chain essential fatty acids than their mother-reared counterparts. Nursery-reared infants receiving dietary supplements exhibited accelerated motor maturation and enhanced visual orientation capabilities during their first month of life compared with infants fed the standard formula, more closely resembling the patterns normally seen in mother-reared infants. A follow-up study examined heart rate variability in the monkeys when they were three years of age. Reduced heart rate variability has been associated with the development of aggressive and sociopathic behavior in human children and with vascular disease and congestive heart failure in adults. Monkeys that had received the formula supplement exhibited significantly greater heart rate variability than their counterparts that had received the standard formula during infancy, despite the fact that both groups had been maintained on a supplemented diet following weaning.

Adaptation of Laboratory-Reared Monkeys to Field Environments
DeVinney, Morin, O’Neill-Wagner, Robbins, Suomi, Turrio, Yang
This past year, we completed the analysis of data collected on mother-offspring pairs of rhesus monkeys during the offsprings’ first two years of life while residing in two free-ranging social groups at the field site at Cayo Santiago, PR. Our objective was to determine the degree to which individual differences in the monkeys’ behavior were related to individual differences in a variety of psychophysiological, endocrine, and morphometric measures in both the offspring and their mothers. Following capture for veterinary examination, offspring showed stable individual differences in heart rate, plasma concentrations of cortisol and prolactin, and virtually all morphometric measures from their first to second year. Body mass index and plasma concentrations of cortisol and growth hormone in offspring and their mothers were unrelated when the offspring were yearlings but became significantly correlated by the time the offspring were two years old. Mothers with low cortisol levels punished their infants more, whereas mothers with high cortisol levels showed the highest rate of infant carrying. Offspring exhibiting the highest frequencies of agitated behavior throughout the study also exhibited the highest cortisol levels following capture. These findings suggest that mothers’ morphological and physiological patterns are related to their offsprings’ behavior and physiology via developmental experience as well as through genetic/intrauterine factors.

We have also been conducting a study of the relationships between measures of neurobiological functioning and various dimensions of maternal behavior in rhesus monkey mother-offspring pairs living in the species-normative social group maintained in the Laboratory’s five-acre field enclosure. CSF samples were collected from mothers when their infants were three to five months of age and assayed for 5-HIAA and HVA (a major central dopamine metabolite); we then compared the resulting values with different aspects of maternal behavior recorded when their infants were one to three, four to six, and seven to nine months old, respectively. Measures of maternal protectiveness and infant restraint during the latter two time periods were negatively correlated with mothers’ 5-HIAA and HVA concentrations. In contrast, measures of two forms of active infant rejection were positively correlated with concentrations of both monoamine metabolites during the latter two time periods, whereas the rate of passive rejections was not significantly related to concentrations of either metabolite during any time period.
Another study investigating mother-infant relationships in rhesus monkeys housed in the LCE field enclosure compared primiparous with multiparous females with respect to various aspects of their maternal behavior and the behavior of their infants. During their first month of life, offspring of multiparous females were more active than were primiparous infants. They initiated and broke contact with and approached and left their mothers more frequently than their primiparous counterparts. Throughout most of their infants’ first five months of life, primiparous mothers exhibited higher rates of initiating ventral contact with their infants as well as higher rates of initiating nipple contact. These findings parallel parity differences in mother-infant relationships previously reported from field studies of rhesus monkeys and several other Old World monkey species.

We completed a study of continuity and change in patterns of adrenocortical functioning throughout the juvenile years in rhesus monkeys reared in three different physical and social environments for their first seven months of life but thereafter placed together and subsequently maintained in large peer groups. Monkeys from all three rearing conditions (mother-peer, surrogate-peer, and peer-only) exhibited significant increases in plasma cortisol over their first five months but then showed steady declines from one to three years of age; females consistently had higher concentrations than males at all ages. Plasma cortisol levels of surrogate-peer–reared subjects were lower than those of their mother-peer–reared counterparts (with peer-only–reared subjects intermediate) during the first month of life, but not at later ages. Juvenile cortisol levels were significantly correlated with infant levels in all samples collected after two weeks of age, indicating long-term developmental stability of individual differences. Saliva samples were collected from a subset of these subjects at one, two, and three years. Analysis of salivary cortisol concentra-tions from the subgroup revealed a significant age-related decline as well as lower levels for surrogate-peer–reared monkeys at each age, but no significant sex differences at any age. Comparison of salivary and plasma cortisol values obtained from the same subjects yielded a highly significant positive correlation.