Intracranial Soft Tissue Adaptations in the Land-to-Sea Transition: Shifts in Marine Crocodylomorph (Crocodylomorpha: Thalattosuchia) Vasculature and Paratympanic Sinus Systems

Abstract

From an osteological perspective, the secondary aquatic adapta- tions of vertebrates are well understood; from a soft tissue one, less so. Here, we use an ancient group of crocodylomorphs, Thalattosuchia, as an exemplar of the land-to-sea transition. During the Jurassic, thalattosuchians transitioned from shallow marine to open ocean habitats, with the subclade Metriorhynchidae con- vergently evolving osteological adaptations seen in other Mesozoic marine reptile groups (e.g., hydrofoil-like forelimbs, hypocercal tail). However, the soft tissue adaptations underpinning the suc- cess of Thalattosuchia remain obscure. Our team microCT-scanned and digitally segmented the cranial endocasts of extinct and extant crocodylomorphs. All thalattosuchians share the same profound shifts in intracranial vasculature and pneumaticity (although met- riorhynchids adapted these systems further). There was hypertro- phy of the carotid-orbital system, temporoorbital system, transverse sinuses and possibly the cavernous sinus. Based on the blood flow pat- terns of extant species, thalattosuchians would have had far greater blood flow entering and exiting the orbital and nasal regions. This increase corresponds with their proportionally large eyes, and suggests that the nasal salt glands of Metriorhynchidae evolved at the base of Thalattosuchia. In thalattosuchians, invasion of the cranium by the paratympanic sinus systems was less extensive than those of sphenosuchians, protosuchians and extant species. The recessus epit- ubaricum, otoccipital diverticula and vestigial infundibular diverticula were confluent with the tympanic cavity (rather than discrete divertic- ula), while the intertympanic, prootic and quadrate diverticula were absent. Our results suggest that at least some of the major soft tissue adaptations that underpinned the metriorhynchid radiation into the pelagic realm occurred much earlier in thalattosuchian evolution, and occurred prior to their osteological and locomotory adaptations.