Rostral neurovasculature indicates sensory trade-offs in Mesozoic pelagic crocodylomorphs

Abstract

Metriorhynchoid thalattosuchians were a marine clade of Mesozoic crocodylomorphs that evolved from semi-aquatic, “gharial”-like species into the obligately pelagic subclade Metriorhynchidae. To explore whether the sensory and physiological demands of underwater life necessitates a shift in rostral anatomy, both in neurology and vasculature, we investigate the trigeminal innervation and potential somatosensory abilities of metriorhynchoids by digitally segmenting the rostral neurovascular canals in CT scans of 10 extant and extinct crocodyliforms. The dataset includes the terrestrial, basal crocodyliform Protosuchus haughtoni, two semi-aquatic basal metriorhynchoids, four pelagic metriorhynchids and three extant, semi-aquatic crocodylians. In the crocodylian and basal metriorhynchoid taxa, we find three main neurovascular channels running parallel to one another posteroanteriorly down the length of the snout, whereas in metriorhynchids there are two, and in P. haughtoni only one. Crocodylians appear to be unique in their extensive trigeminal innervation, which is used to supply the integumentary sensory organs (ISOs) involved with their facial somatosensory abilities. Crocodylians have a far higher number of foramina on the maxillary bones than either metriorhynchoids or P. haughtoni, suggesting that the fossil taxa lacked the somatosensory abilities seen in extant species. We posit that the lack of ISO osteological correlates in metriorhynchoids is due to their basal position in Crocodyliformes, rather than a pelagic adaptation. This is reinforced by the hypothesis that extant crocodyliforms, and possibly some neosuchian clades, underwent a long “nocturnal bottleneck”—hinting that their complex network of ISOs evolved in Neosuchia, as a sensory trade-off to compensate for poorer eyesight.