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Cerebrospinal Fluid Monoaminergic Metabolites Differ in Wild Anubis and Hybrid (Anubis hamadryas) Baboons: Possible Relationships to Life History and Behavior Jay R. Kaplan, Ph.D., Jane Phillips-Conroy, Ph.D., M. Babette Fontenot, D.V.M., M.S., Ph.D., Clifford J. Jolly, Ph.D., Lynn A. Fairbanks, Ph.D., and J. John Mann, M.D. This article reports monoaminergic metabolite males characterized by hamadryas admixture had [homovanillic acid (HVA), 5-hydroxyindoleacetic acid (5- significantly higher concentrations of HVA, 5-HIAA, and HIAA), and 3-methoxy-4-hydroxyphenylglycol (MHPG)], MHPG (p , .05, respectively), a result possibly driven by values from the cerebrospinal fluid (CSF) of 27 wild differences in serotonergic activity. These data provide baboons (Papio hamadryas) aged 40 to 140 months. initial evidence that variation in central monoaminergic Animals were either anubis, or anubis with hamadryas activity, as indicated by CSF monoamine metabolite admixture; males of the latter subspecies generally have a concentrations, may reflect differences in behavior and life reduced tendency to disperse from their natal groups. history that have taxonomic and, perhaps, evolutionary Overall, the values and interrelationships among the CSF significance. [Neuropsychopharmacology 20: 517–524, monoamine metabolites resembled data reported from 1999] © 1999 American College of closely related, captive-housed animals. For example, age Neuropsychopharmacology. Published by Elsevier was significantly correlated with HVA concentrations (r 5 Science Inc. 260, p , .05), but not with the other metabolites. Notably, KEY WORDS: Primates; Serotonin; Dopamine; There is increasing interest in the neurobiologic factors Norepinephrine; CSF underlying variation in social behavior, both among in- dividuals and between species (Clarke and Boinski 1995; Young et al. 1997). Among such factors, consider- able attention has focused on the relationship between From the Department of Pathology (Comparative Medicine) (JRK, MBF), and Department of Anthropology, Wake Forest University behavioral characteristics and the monoaminergic neu- School of Medicine (JRK), Winston-Salem, North Carolina; Depart- rotransmitters (serotonin, dopamine, and norepineph- ment of Anatomy (JP-C), Washington University School of Medicine, rine) (Kraemer and Clarke 1996). Interest in these neu- St. Louis, Missouri; Department of Anthropology (CJJ), New York University, New York, New York; Department of Psychiatry (LAF), rotransmitters stems, in part, from the suggestion that University of California at Los Angeles, Los Angeles, California; interindividual variation in their release or uptake Department of Neuroscience (JJM), New York State Psychiatric Cen- might be under partial genetic regulation and thereby ter, New York, New York. Address correspondence to: Jay R. Kaplan, Ph.D., Professor of contribute to the enduring, trait-like behavioral differ- Comparative Medicine, Department of Pathology, Section of Com- ences often observed among individuals within groups parative Medicine, Wake Forest University School of Medicine, of primates, both human and nonhuman (Zuckerman Medical Center Boulevard, Winston-Salem, NC 27157-1040. Received April 30, 1998; revised July 23, 1998; accepted August 3, 1991; Mulder 1992; Cloninger 1994). An extensive litera- 1998. ture documents the inverse association between indices NEUROPSYCHOPHARMACOLOGY 1999–VOL. 20, NO. 6 © 1999 American College of Neuropsychopharmacology Published by Elsevier Science Inc. 0893-133X/99/$–see front matter 655 Avenue of the Americas, New York, NY 10010 PII S0893-133X(98)00078-5 518 J.R. Kaplan et al. NEUROPSYCHOPHARMACOLOGY 1999–VOL. 20, NO. 6 of serotonergic activity and aggressiveness in monkeys pithecus aethiops aethiops) that also live in the Awash (Raleigh et al. 1986; Higley et al. 1992; Botchin et al. Valley were subjected to a similar investigation; the re- 1993), or violence and impulsiveness in human beings sults of this latter study are reported elsewhere (Fair- (Brown et al. 1982; Asberg et al. 1986; Linnoila et al. banks et al., unpublished results).] The two baboon 1986; Berman et al. 1997; Manuck et al., 1998). Con- forms differ significantly in social behavior as well as versely, there are reports linking indices of elevated or appearance. One distinction of potential interest with high central serotonergic activity to positive social in- respect to central monoaminergic activity involves male teraction in human subjects (Knutson et al., 1998) and dispersal. Like most macaques, anubis baboons live in monkeys (Raleigh et al., 1983; Botchin et al. 1993). Such multimale–multifemale troops characterized by almost behavioral relationships are of interest not only because universal male dispersal and strong female philopatry of their impact on intragroup relationships but also be- (Pusey and Packer 1987). In contrast, hamadryas males cause they might represent strategies having life history rarely move permanently from their natal group, or consequence.s Supporting the latter suggestion are two band, where they normally remain in close contact with reports linking high serotonergic activity to delayed male kin (their “clan”) throughout their lives (Kummer dispersal of free-ranging male rhesus macaques (Ma- 1968; Abegglen 1984; but see also Phillips-Conroy et al. caca mulatta) from their natal groups (Kaplan et al. 1995; 1992). Perhaps as a correlate of their philopatry, ha- Mehlman et al. 1995). madryas males exhibit affiliative and mutually sup- The evaluation of neurotransmitter profiles seems portive behavior in a variety of social contexts in which especially useful in wild populations, where natural se- anubis males tend to be indifferent or hostile to each lective agents can unmask the fitness outcomes associ- other (Nystrom 1992). ated with behavioral variation and its neurochemical These behavioral contrasts, and the existence of hy- correlates or determinants. That such studies have not brids formed by interbreeding between the two baboon been done relates in part to the relatively invasive and forms (Nagel 1973; Phillips-Conroy and Jolly 1986), demanding nature of the data collection. Monoaminer- suggested three objectives for a pilot study: (1) to estab- gic activity in the central nervous system, for example, lish the feasibility of collecting neurochemical data un- is often assessed in monkeys by measuring serotoner- der field conditions; (2) to compare the monoamine me- gic, dopaminergic, and noradrenergic metabolite con- tabolite values obtained from animals captured in their centrations in cerebrospinal fluid (CSF). The CSF, in native habitat and natural social context with those re- turn, is sampled from the cisterna magna, which re- ported from laboratory and colony populations; and (3) quires placement of a needle through the dura into the to conduct an initial test of the hypothesis that seroton- subarachnoid space surrounding the brainstem. [The ergic metabolite concentrations would differ in the two existence of a rostral-caudal gradient in the monoamin- parental baboon forms, and their hybrids, in ways con- ergic metabolites of serotonin and dopamine suggests sistent with the distinct behavioral characteristics of the that cisternal sampling provides a more accurate repre- parental populations. In this pilot study, sampling was sentation of brain monoaminergic turnover than can be limited to one anubis and one hybrid group. From the obtained less invasively through a more caudal (e.g., previously established relationship between dispersal lumbar) site (Gordon et al. 1975; Shelton et al. 1988)]. Fi- and serotonergic activity in male rhesus, and the obser- nally, once collected, the CSF must be adequately pre- vation that the tendency to disperse in early adulthood served. The application of these procedures under field is much less pronounced among hamadryas than conditions is not trivial. As a result, virtually all knowl- among anubis males, we predicted that the level of se- edge concerning monoamine metabolites in nonhuman rotonin metabolites in males with hamadryas admix- primates is currently derived from laboratory and cap- ture would be higher than in their “pure” anubis coun- tive colony settings (Shelton et al. 1988; Higley et al. terparts. 1992; Raleigh et al. 1992; Clarke et al. 1995; Kaplan et al. 1995). In addition to the above-referenced association between low serotonergic activity (as indicated by CSF metabolite concentrations) and early dispersal, these METHODS studies often report high correlations among the Study Site and Animals monoamine metabolites and a significant age-related decline in dopaminergic, and perhaps serotonergic, ac- The study site was in the Awash National Park (ANP), tivity. It would be useful to determine whether such re- approximately 200 km east of Addis Ababa, Ethiopia, lationships extend to populations in their native habitat. within the East African Rift Valley. The altitude (about The foregoing considerations led us to undertake a 1000 m above sea level) and natural vegetation of the pilot investigation evaluating the neurochemical pro- park are intermediate between those of the Ethiopian files of anubis (Papio hamadryas anubis) and hamadryas high plateau and the semi-desert foothills and lowlands (P. h. hamadryas) baboons. [The grivet monkeys (Cerco- of the Danakil region (Jacobs and Schloeder 1993), NEUROPSYCHOPHARMACOLOGY 1999–VOL. 20, NO. 6 CSF Monoamine Metabolites in Wild Baboons 519 which are, respectively, typical anubis and hamadryas
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