Female alternative mating tactics, reproductive success and nonapeptide receptor expression in the social decision-making network

The decision to mate may be one of the most important decisions that animals make. For monogamous species, this decision can carry the added weight of limiting future mating opportunities. The mechanisms that govern these decisions have presumably been shaped by evolution in ways that optimize decision-making processes. In particular, a so-called social decision-making network (SDM) has been proposed, which integrates brain structures comprising the ‘social behavior network’ with a neural system associated with reward. Here, we investigate the neural phenotypic differences in the SDM for oxytocin and vasopressin receptors (OTR, V1aR) of female socially monogamous prairie voles living in naturalistic conditions. We focus on these receptors because they are profoundly involved in mammalian social behavior. We found that V1aR in the bed nucleus of the stria terminalis, medial amygdala and ventral pallidum, and OTR in the nucleus accumbens and hippocampus significantly differed between pregnant and non-pregnant females. Most of these areas are more closely related to the reward component of the SDM. V1aR in the ventral pallidum was also greater in paired than in single females. Finally, reproductive success within mating tactics was related to receptor density in brain structures across the SDM, particularly those serving as the interface between the social behavior network and the reward system. Our data support the hypothesis that neural phenotype for neuromodulatory nonapeptide receptors within the SDM relates to natural behavior associated with reproductive decisions.

► OTR expression in the SDM suggests oxytocin may modulate reward in social decisions.
► V1aR expression in the SDM suggests vasopressin broadly shapes social decisions.
► Monogamous females express more V1aR than single females in the ventral pallidum.
► OTR and V1aR density in much of the SDM relates to whether females reproduced.
► OTR/V1aR in parts of the SDM might facilitate context-dependant reproductive success.