Beyond mammals: the evolution of chewing and other forms of oropharyngeal food processing in vertebrates

Oropharyngeal food processing exhibits a remarkable diversity among vertebrates, reflecting the evolution of specialised 'processing centres' associated with the mandibular, hyoid, and branchial arches. Although studies have detailed various food-processing strategies and mechanisms across vertebrates, a coherent and comprehensive terminology is lacking. Here, we provide a synthesis, including a unified terminology for the intricate complexity of vertebrate oropharyngeal processing. Among gnathostomes, mandibular food processing predominates, ranging from discrete bites to rhythmic, cyclic chewing facilitated by precise tongue mechanics in aquatic and terrestrial environments alike. By contrast, some taxa have abandoned oropharyngeal processing entirely, relying instead on post-oesophageal strategies such as gastric milling and chemical digestion. Interestingly, teleost (bony) fishes illustrate the evolutionary trade-off between increased jaw protrusion for prey capture and reduced mandibular processing capacity. They compensated for this trade-off by developing derived processing behaviours early in their evolutionary development. Through the re-evolution of mandibular chewing, they succeeded in utilising all three known processing centres. Mastication is a specialised, dimensionally complex form of unignathic mandibular chewing (i.e. chewing restricted to the lower jaw) exclusive to mammals. However, our findings demonstrate that dimensionally complex forms of mandibular chewing have arisen independently multiple times and are widespread among gnathostomes. Notably, diverse taxa, including elasmobranch stingrays, Australian lungfish, sirenid salamanders, various songbirds, herbivorous turtles, and the tuatara, exhibit complex jaw movements combining arcuate, longitudinal, and sometimes transverse components enabled by specialised jaw joints, suspensions, and intracranial motions ('cranial kinesis'). From a comparative, functional-morphological perspective, mammalian mastication may best be characterised as dimensionally complex chewing mediated by the secondary or temporomandibular joint. By contrast, analogous dimensionally complex non-mammalian chewing involving motions confined to the primary or quadrate-articular jaw joint qualifies as pseudomastication. Both mastication and pseudomastication resemble functional masticatory behaviours, while those incorporating intracranial motions and movements of the jaw suspension belong to distinct categories. Our anatomical analysis highlights the convergent evolution of dimensionally complex chewing among gnathostomes and emphasises the importance of comprehensive studies on jaw development and function to deepen our understanding of the evolution of oropharyngeal processing.