Diverse Tongue Base Retraction Strategies Drive Bolus Propulsion during Mammalian Swallowing

During swallowing, a diverse range of mammals-from opossums to humans-propel food boluses out of the oropharynx via tongue base retraction (TBR). The widespread distribution of TBR behavior implies an ancient evolutionary origin, but the biomechanical mechanisms of TBR remain poorly understood. The evolution of TBR behavior is further complicated by the diversity of hyoid and tongue anatomy across mammals: to what extent does hyolingual morphology shape TBR mechanism? Using biplanar videoradiography and the XROMM workflow, we collected high-resolution 3D kinematic data in opossums (Marsupialia), dogs (Placentalia), and macaques (Placentalia) to test hypotheses on the evolutionary conservation of TBR mechanisms. Despite differences in hyolingual morphology and resting hyoid position, both dogs and macaques drive TBR through hyoid movement: hyoid excursions reduce the oral volume and squeeze the tongue base posteriorly, analogous to a hydraulic pump displacing an incompressible fluid. In opossums, however, intrinsic lingual muscles deform the tongue base to initiate TBR, independent of hyoid movement and oral volume change. We suggest that multiple mechanisms are viable for the highly conserved TBR behavior across mammals, and the functional diversity of TBR mechanisms is decoupled from the morphological diversity of the hyolingual system. This decoupling may have facilitated the evolution of novel hyolingual phenotypes while avoiding trade-offs in swallowing performance.