Neural correlates of mating system diversity: oxytocin and vasopressin receptor distributions in monogamous and non-monogamous Eulemur

Abstract

Contemporary theory that emphasizes the roles of oxytocin and vasopressin in mammalian sociality has been shaped by seminal vole research that revealed interspecific variation in neuroendocrine circuitry by mating system. However, substantial challenges exist in interpreting and translating these rodent findings to other mammalian groups, including humans, making research on nonhuman primates crucial. Both monogamous and non-monogamous species exist within Eulemur, a genus of strepsirrhine primate, offering a rare opportunity to broaden a comparative perspective on oxytocin and vasopressin neurocircuitry with increased evolutionary relevance to humans. We performed oxytocin and arginine vasopressin 1a receptor autoradiography on 12 Eulemur brains from seven closely related species to (1) characterize receptor distributions across the genus, and (2) examine differences between monogamous and non-monogamous species in regions part of putative “pair-bonding circuits”. We find some binding patterns across Eulemur reminiscent of olfactory-guided rodents, but others congruent with more visually oriented anthropoids, consistent with lemurs occupying an ‘intermediary’ evolutionary niche between haplorhine primates and other mammalian groups. We find little evidence of a “pair-bonding circuit” in Eulemur akin to those proposed in previous rodent or primate research. Mapping neuropeptide receptors in these nontraditional species questions existing assumptions and informs proposed evolutionary explanations about the biological bases of monogamy.

On the Origins of Diversity in Social Behavior

“…OXTR mRNA is also highly expressed in the human NAc, although there is considerable variation in expression across individuals (Bethlehem et al, 2017). However, receptor expression in these areas do not predict mating strategy in monogamous and polygamous lemur species, suggesting that there is not a single neuropeptide modulated circuit that can give rise to monogamous behaviors across all species (Grebe et al, 2021).…”

Oxytocin receptors are widely distributed in the prairie vole (Microtus ochrogaster) brain: Relation to social behavior, genetic polymorphisms, and the dopamine system

“…In primates, OXTRs are more densely expressed in areas responsible for visual information processing and attention, including the nucleus basalis of Meynert and superior colliculus (S. M. Freeman et al, 2014;S. M. Freeman & Young, 2016;Grebe et al, 2021). In the auditory cortex of maternal mice, OXTRs enhance the salience of pup calls and facilitate pup retrieval by regulating cortical inhibition (Marlin et al, 2015).…”

Effect of sex and autism spectrum disorder on oxytocin receptor binding and mRNA expression in the dopaminergic pars compacta of the human substantia nigra

“…In order to address the receptor cross-reactivity, we used a previously optimized method for visualizing OXTR and AVPR1a in the primate brain through the use of a modified form of receptor autoradiography, where the radioligand is co-incubated on the tissue with a selective competitor that blocks one of the receptor subtypes to reveal binding only to the receptor of interest. This approach has been validated in postmortem brain tissue from non-human primates [38][39][40] and humans [36,41,42] to selectively visualize either OXTR or AVPR1a. In the current study, we used this method of competitive-binding receptor autoradiography to specifically locate OXTR binding in the SN of the human brain.…”