In the intricate realm of animal behavior, social dominance is a crucial factor that governs the daily routines of numerous species. Among non-human primates, dominance rank is more than just a theoretical hierarchy; it is a tangible power that regulates access to vital resources such as food, mates, and shelter1–5. Dominance also plays a significant role in reproductive success and survival strategies such as grooming, hunting, and predator avoidance5–9. The resulting social structures are formed through repeated and uneven aggressive interactions, ultimately shaping the dynamics of animal communities and establishing a clear and often inflexible hierarchy of dominance4,5,10.
Various non-human primate species, alone or in large groups, display intricate social hierarchies5. Numerous factors, such as physical strength, aggression, and social intelligence, shape these hierarchies. They can be seen through displays of aggressive and submissive behaviors, often resulting in unequal confrontations that establish one's position and status within groups4,5,10,11.
Mirroring these animal hierarchies, human communities also comprise structured social layers. Numerous brain structures, particularly within the limbic system, have been implicated in governing human social behaviors. For instance, the uncinate fasciculus, a pathway connecting frontal to temporal limbic brain regions, has been shown to regulate various aspects of social behavior12. Alteration in the uncinate fasciculus is linked to social disorders characterized by antisocial behavior, aggression, and rule violations, as seen in conditions like frontotemporal dementia13, brain lesions14,15, and psychopathy16. The cingulate bundle, meanwhile, connecting multiple points in the limbic system17, plays a critical role in regulating internal mental states18 and is associated with emotional detachment observed in psychopathic traits19.
Although there is a well-established correlation between psychopathy and dominance in humans20–22, research on the link between these traits in non-human primates is surprisingly scarce due to the difficulty to either perform anatomical post-mortem study in large groups of animals or to collect both brain imaging and behavioural data in the same animal group. Initial findings from tests conducted on a small sample of macaques from social groups ranging from two to five individuals indicate a link between social status and various brain regions such as the amygdala, brainstem, septum, and striatum, as well as frontotemporal networks23.
In our research, we aim to fill this gap by investigating the anatomical connections that underpin social dominance within a colony of squirrel monkeys (Saimiri sciureus). Brain development and evolution are unequivocally linked to an increase in brain size24–26. This notable increase in brain size also exerts a significant impact on white matter fibres27. As brain size increases, fibers also lengthen, causing a delay in conduction and slower information transfer. While some fibres can adapt to this by increasing myelination and diameter, not all can due to space and energy constraints28. This variability in fiber length may reveal adaptive principles underlying brain development and evolution24–26. Diffusion MRI tractography has been used to understand primate evolution through the comparative analysis of individual anatomical pathways from various species29–31.
Leveraging the unique social structure of squirrel monkeys, which fosters cohesive and extensive communities in laboratory settings, we conducted an in-depth study of three key white matter fiber pathways - the uncinate fasciculus, the cingulum, and the fornix. These pathways were analyzed in relation to behavioral hierarchy measures controlling for variables such as age, weight, handedness, brain size and hormonal factors (testosterone and progesterone). Our objective was to identify the cerebral anatomical variations that support hierarchy in the largest primate colony investigated to date consisting of 15 female squirrel monkeys. We hypothesized that the anatomical cerebral connections involved dominance-related behaviors in non-human primates will parallel those seen in human neurological and psychiatric disorders, providing new insights into the evolutionary origins of behavior.