Dimorphic Substrates, Monomorphic Outcomes: Social Behavior Neural Circuit Tuning in Social Monogamy

Social behaviors are dramatically influenced by variations in mating systems that shape sex differences in the neural substrates underlying such displays. In polygamous species, distinct evolutionary pressures on males and females produce pronounced behavioral and anatomical sexual dimorphism, supported by strongly sexually differentiated social behavior and social decision-making networks at levels of brain structure, connectivity, physiology, and gene expression. By contrast, socially monogamous species display more similar or monomorphic social behaviors-such as shared parenting, convergent juvenile play, and selective pair bonding-accompanied by either reduced or more subtle neural dimorphism. Here, we discuss two nonexclusive models: that monomorphic behaviors arise from decreased circuit-level dimorphism, or instead, from conserved sexually dimorphic circuits that are differentially tuned in each sex to yield convergent behavioral outputs. Integrating pharmacological work on oxytocin, vasopressin, and other neuromodulators with modern genetic and circuit-level perturbations, including our recent studies in prairie voles, we highlight hidden molecular and circuit sexual dimorphism within nodes of the social behavior network and extended reward circuitry that support attachment, parenting, aggression, and social valuation. We propose that sex-biased weighting of shared, evolutionarily conserved circuits allows species- and sex-specific optimization of social strategies while preserving robustness in key behaviors like pair bonding and biparental care. Finally, we consider the implications of such masked sex differences for neurodevelopmental and psychiatric disorders marked by impaired social cognition and strong sex biases in incidence and presentation. We suggest that dissecting how dimorphic circuits support ostensibly monomorphic social behaviors may reveal sex-specific vulnerabilities and new targets for interventions.