Imaging, Behavior and Endocrine Analysis of “Jealousy” in a Monogamous Primate

Abstract

Understanding the neurobiology of social bonding in non-human primates is a critical step in understanding the evolution of monogamy, as well as understanding the neural substrates for emotion and behavior. Coppery titi monkeys (Callicebus cupreus) form strong pair bonds, characterized by selective preference for their pair mate, mate-guarding, physiological and behavioral agitation upon separation, and social buffering. Mate-guarding, or the “maintenance” phase of pair bonding, is relatively under-studied in primates. In the current study, we used functional imaging to examine how male titi monkeys viewing their pair mate in close proximity to a stranger male would change regional cerebral glucose metabolism. We predicted that this situation would challenge the pair bond and induce “jealousy” in the males. Animals were injected with [18F]-fluorodeoxyglucose (FDG), returned to their cage for 30 min of conscious uptake, placed under anesthesia, and then scanned for 1 hour on a microPET P4 scanner. During the FDG uptake, males (n=8) had a view of either their female pair mate next to a stranger male (“jealousy” condition) or a stranger female next to a stranger male (control condition). Blood and cerebrospinal fluid samples were collected and assayed for testosterone, cortisol, oxytocin, and vasopressin. Positron emission tomography (PET) was co-registered with structural magnetic resonance imaging (MRI), and region of interest analysis was carried out. Bayesian multivariate multilevel analyses found that the right lateral septum (Pr(b>0)=93%), left posterior cingulate cortex (Pr(b>0)=99%), and left anterior cingulate (Pr(b>0)=96%) showed higher FDG uptake in the jealousy condition compared to the control condition, while the right medial amygdala (Pr(b>0)=85%) showed lower FDG uptake. Plasma testosterone and cortisol concentrations were higher during the jealousy condition. During the jealousy condition, duration of time spent looking across at the pair mate next to a stranger male was associated with higher plasma cortisol concentrations. The lateral septum has been shown to be involved in mate-guarding and mating-induced aggression in monogamous rodents, while the cingulate cortex has been linked to territoriality. These neural and physiological changes may underpin the emotion of jealousy, which can act in a monogamous species to preserve the long-term integrity of the pair.

Oxytocin modulates mate-guarding behavior in marmoset monkeys

“…This suggests that testosterone secretion in males may be an anticipatory response to guard against reproductive conflict. Titi monkeys, which have a more rigid monogamous mating structure, that viewed their pairmate in close proximity to a sexual rival had higher levels of plasma testosterone compared to conditions when their viewed an opposite-sex stranger next to a sexual rival (Maninger et al, 2017), suggesting that HPG-axis activation is specific to challenges to the established bond. Overall, changes in androgen levels and behavior depend on both social status and group composition in species that engage varying mating strategies.…”

“…In the socially monogamous titi monkey, subjects that gazed longer at their pairmate in close proximity to a sexual rival experienced greater HPA-axis activity compared to conditions when they viewed a stranger male-female pair. Further, titi monkeys showed increased neural activity in central areas of the social behavior network with abundant OT receptors (Freeman et al, 2014; Maninger et al, 2017), which indicates that OT activity within these social network hubs may be sensitive and responsive to threats to the established bond. There is burgeoning evidence that the OT system regulates the anxiolytic and stress-reducing effects of social buffering in primates (Cavanaugh et al, 2018, 2016; Crockford et al, 2017; Parker et al, 2005).…”

Dopamine receptor manipulation does not alter patterns of partner preference in long-term marmoset pairs

“…Monogamous titi monkeys display altered patterns of proximity with their mate in the presence of a stranger [21]. Further, watching their mate interact with a potential sexual rival induces specific patterns of neural activity in male titi monkeys that are not seen when males watch a stranger female interact with a stranger male [22]. The differences observed across social contexts may be driven by changes in behavior from both members of the pair.…”

Dopamine Modulation of Reunion Behavior in Short and Long Term Marmoset Pairs

“…Social preference for the mate is a key marker of pair bond formation, and in voles is observed after 24 h of cohabitation (Williams et al, 1992), while selective aggression toward conspecifics is considered a marker of pair bond maintenance and is tied to onset of mating with a mate (Carter et al, 1995). While the phases of pair formation and maintenance in prairie voles appear to follow a strict and short timeline, primates tend to show longer and more variable transitions in relationships (Maninger et al, 2017). Patterns of behavior between mates in marmosets shift across time, including levels of sexual behavior (typically, high in the beginning and lower with increased length of pairing) and affiliative social behavior across pairing (typically, lower in the beginning and increasing with pairing length) (Schaffner et al, 1995;Ågmo et al, 2012;c.f.…”