Synapsids and sensitivity: Broad survey of tetrapod trigeminal canal morphology supports an evolutionary trend of increasing facial tactile specialization in the mammal lineage

Abstract

The trigeminus nerve (cranial nerve V) is a large and significant conduit of sensory information from the face to the brain, with its three branches extending over the head to innervate a wide variety of integumentary sensory receptors, primarily tactile. The paths of the maxillary (V2) and mandibular (V3) divisions of the trigeminus frequently transit through dedicated canals within the bones of the upper and lower jaws, thus allowing this neuroanatomy to be captured in the fossil record and be available to interpretations of sensory ability in extinct taxa. Here, we use microCT and synchrotron scans from 38 extant and fossil species spanning a wide phylogenetic sample across tetrapods to investigate whether maxillary and mandibular canal morphology can be informative of sensory biology in the synapsid lineage. We found that in comparison to an amphibian and sauropsid outgroup, synapsids demonstrate a distinctive evolutionary pattern of change from canals that are highly ramified near the rostral tip of the jaws to canals with increasingly simplified morphology. This pattern is especially evident in the maxillary canal, which came to feature a shortened infraorbital canal terminating in a single large infraorbital foramen that serves as the outlet for branches of V2 that then enter the soft tissues of the face. A comparison with modern analogues supports the hypothesis that this morphological change correlates to an evolutionary history of synapsid‐specific innovations in facial touch. We interpret the highly ramified transitional form found in early nonmammalian synapsids as indicative of enhanced tactile sensitivity of the rostrum via direct or proximal contact, similar to tactile specialists such as probing shorebirds and alligators that possess similar proliferative ramifications of the maxillary and mandibular canals. The transition toward a simplified derived form that emerged among Mid‐Triassic prozostrodont cynodonts and is retained among modern mammals is a unique configuration correlated with an equally unique and novel tactile sensory apparatus: mobile mystacial whiskers. Our survey of maxillary and mandibular canals across a phylogenetic and ecological variety of tetrapods highlights the morphological diversity of these structures, but also the need to establish robust form‐function relationships for future interpretations of osteological correlates for sensory biology.