Neuropeptides of the arginine vastocin (AVT) family, including the mammalian peptides arginine vasopressin (AVP) and oxytocin (OXT), comprise neuroendocrine circuits that range from being evolutionarily conserved to evolutionarily diverse. For instance, the functions and anatomy of the AVT/AVP projections to the pituitary (which arise in the preoptic area and hypothalamus) are strongly conserved, whereas the functions and anatomy of AVT/AVP circuits arising in the medial bed nucleus of the stria terminalis (BSTm) are species-specific and change rapidly over evolutionary time. Circuits arising in the BSTm mediate various affiliative behaviors and exhibit species-specific evolution in relation to mating system in mammals (monogamous vs. non-monogamous) and sociality in songbirds (gregarious vs. relatively asocial). In estrildid songbirds AVT neurons in the BSTm increase their Fos expression only in response to "positively-valenced" social stimuli (stimuli that normally elicit affiliation), whereas "negative" stimuli (which elicit aggression or aversion) produce no response or even suppress Fos expression. Relative to territorial species, gregarious species show: (1) greater social induction of Fos within AVT neurons, (2) a higher baseline of Fos expression in AVT neurons, (3) more AVT neurons in the BSTm and (4) a higher density of V(1a)-like binding sites in the lateral septum. Furthermore, septal AVT infusions inhibit resident-intruder aggression, but facilitate aggression that is motivated by mate competition (an affiliative context). This functional profile of the BSTm AVT neurons is quite distinct from that of hypothalamic AVT/AVP neurons, particularly those of the paraventricular nucleus (PVN), which are classically stress-responsive. This is paradoxical, given that AVT/AVP projections from the PVN and BSTm likely overlap. However, despite this overlap, each AVT/AVP cell group should produce a distinct pattern of modulation across brain regions. Relative weighting of hypothalamic and BSTm nonapeptide circuitries may therefore be an important determinant of approach-avoidance behaviour, and may be a prime target of natural selection related to sociality.