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Monoamine Neurotransmitter Metabolites in the Cerebrospinal Fluid of a Group of Hybrid Baboons (Papio hamadryas × P. anubis)

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Abstract

Comparatively little is known about the pathways of proximate causation that link divergent genotypes, via neurophysiological differences, to distinct, species-specific social behaviors and systems. One approach to the problem compares gross activity levels of monoamine neurotransmitters (norepinephrine, dopamine, and serotonin), evidenced by their metabolites —3-methoxy-4-hydroxyphenylglycol (MHPG), homovanillic acid (HVA), and 5-hydroxyindoleacetic acid (5-HIAA), respectively— in cerebrospinal fluid (CSF). We have applied this method to Papio hamadryas and P. anubis, closely related baboon species with divergent social behavior, living in the Awash National Park (ANP), Ethiopia. We had previously shown that adult males of the two species differ in the ratio of HVA to 5-HIAA, and in concentrations of MHPG and HVA, but not 5-HIAA. Here, we compare monoamine metabolite levels of the parental species with those of 49 members of a naturally formed, multigenerational hamadryas × anubis hybrid group. We cage-trapped the baboons in July 1998, sampled their CSF by cisternal puncture, and assayed monoamine metabolites by high-performance liquid chromatography. Previous findings suggested, anomalously, that hybrid males showed the high 5-HIAA levels predicted by the low-serotonin–early-dispersal hypothesis (originally based on observation of rhesus macaques, Macaca mulatta), while hamadryas did not. The present study failed to find higher 5-HIAA levels in hybrids, resolving the anomaly, but leaving the previous result unexplained. Among adult females (underrepresented in our sample) and juveniles, metabolite levels of the hybrids did not differ significantly from either parental species. Overall, adult male hybrids resembled anubis in HVA and HVA/5-HIAA ratio, but did not show the low MHPG levels characteristic of that species. Consistent with a significant genetic influence on species differences in these metabolites, the adult hybrids showed intermediate means and greater intra-population diversity than the parental species for most variables, but showed no indication of hybrid dysgenesis in the form of low intermetabolite correlation. To the contrary, an enhanced HVA–MHPG correlation in the hybrids suggested a species-associated factor (not necessarily genetic) influencing both of these monoamine neurotransmitter systems.

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Acknowledgments

We thank the General Manager, Ethiopian Wildlife Conservation Organization, the Warden and Staff of the Awash National Park, and the Biology Department, Addis Ababa University, for permitting and facilitating our research; Ato Minda Wondorfa for his many logistical contributions; the many graduate students who assisted in the field; Dr. Babette Fontenot, Dewayne Cairnes, and Melissa Ayers for their skilled collection of CSF; Dr. Yung-Yu Huang for expert assistance with the monoamine assays; and the editor and two anonymous reviewers for their many insightful comments on the manuscript. This work was supported by grants SBR9615150, the Center for Field Research/Earthwatch and the Harry Frank Guggenheim Foundation to C. J. Jolly and J. E. Phillips-Conroy and HL45666, HL79421 to J. R. Kaplan.

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Authors and Affiliations

  1. Department of Anthropology, New York University, New York, New York, 10003, USA

    Clifford J. Jolly

  2. Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri, 63110, USA

    Jane E. Phillips-Conroy

  3. Department of Anthropology, Washington University, St. Louis, Missouri, 63130, USA

    Jane E. Phillips-Conroy

  4. Department of Pathology (Comparative Medicine) and Wake Forest University Primate Center, Wake Forest University School of Medicine, Winston-Salem, North Carolina, 27157, USA

    Jay R. Kaplan

  5. Department of Molecular Imaging and Neuropathology, New York State Psychiatric Institute, New York, New York, USA

    J. John Mann

  6. Department of Psychiatry, Columbia University, New York, New York, 10032, USA

    J. John Mann

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  1. Clifford J. Jolly
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Correspondence to Clifford J. Jolly.

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Jolly, C.J., Phillips-Conroy, J.E., Kaplan, J.R. et al. Monoamine Neurotransmitter Metabolites in the Cerebrospinal Fluid of a Group of Hybrid Baboons (Papio hamadryas × P. anubis). Int J Primatol 34, 836–858 (2013). https://doi.org/10.1007/s10764-013-9698-4

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