The Evolution of Sociality and the Polyvagal Theory

The polyvagal theory (PT), offered by Porges (2021), proposes that the autonomic nervous system (ANS) was repurposed in mammals, via a "second vagal nerve", to suppress defensive strategies and support the expression of sociality. Three critical assumptions of this theory are that (1) the transition of the ANS was associated with the evolution of 'social' mammals from 'asocial' reptiles; (2) the transition enabled mammals, unlike their reptilian ancestors, to derive a biological benefit from social interactions; and (3) the transition forces a less parsimonious explanation (convergence) for the evolution of social behavior in birds and mammals, since birds evolved from a reptilian lineage. Two recently published reviews, however, provided compelling evidence that the social-asocial dichotomy is overly simplistic, neglects the diversity of vertebrate social systems, impedes our understanding of the evolution of social behavior, and perpetuates the erroneous belief that one group-non-avian reptiles-is incapable of complex social behavior. In the worst case, if PT depends upon a transition from 'asocial reptiles' to 'social mammals,' then the ability of PT to explain the evolution of the mammalian ANS is highly questionable. A great number of social behaviors occur in both reptiles and mammals. In the best case, PT has misused the terms 'social' and 'asocial'. Even here, however, the theory would still need to identify a particular suite of behaviors found in mammals and not reptiles that could be associated with, or explain, the transition of the ANS, and then replace the 'asocial' and 'social' labels with more specific descriptors.

Keywords: Social behavior; autonomic nervous system; mammals; reptiles; vagus nerves.

PMID: 37094735 DOI: 10.1016/j.biopsycho.2023.108569