Lawrence M. Witmer’s research while affiliated with Ohio University and other places

Thalattosuchian crocodylomorphs underwent a major evolutionary transition, evolving from semiaquatic forms reminiscent of extant crocodylians, into pelagic marine forms with flippers, a tail fin and smooth scaleless skin. These fully aquatic forms – the Metriorhynchidae – evolved a novel suite of endocranial anatomies hypothesised to be related to living in saltwater. However, much remains to be discovered about the evolution of these internal braincase structures. Herein, we describe the endocranial anatomy of an early diverging metriorhynchid, Thalattosuchus superciliosus, using microfocus computed tomography (μCT) data and three-dimensional modelling. We compared it against geosaurine and metriorhynchine metriorhynchids, as well as the early diverging metriorhynchoid Pelagosaurus. We found that non-geosaurine metriorhynchids differ from geosaurines in having less laterally expanded cerebral hemispheres, shallower curvatures of the brain’s dorsal margin, and lacking the ventral deflection of the pneumatic diverticulum ventral to the pituitary fossa chamber. However, early-diverging metriorhynchids have well-defined otoccipital diverticula and lacked the ‘extreme pelagic’ endosseous labyrinth morphology. We hypothesise that early metriorhynchids were not adapted to a sustained pursuit lifestyle. Moreover, we posit that within both metriorhynchid subfamilies there was parallel evolution towards becoming pursuit predators.

During major evolutionary transitions, groups develop radically new body plans and radiate into new habitats. A classic example is cetaceans which evolved from terrestrial ancestors to become pelagic swimmers. In doing so, they altered their air-filled sinuses, transitioning some of these spaces to allow for fluctuations in air capacity and storage via soft tissue borders. Other tetrapods independently underwent land-to-sea transitions, but it is unclear if they similarly changed their sinuses. We use computed tomography to study sinus changes in thalattosuchian crocodylomorphs that transformed from land-bound ancestors to become the only known aquatic swimming archosaurs. We find that thalattosuchian braincase sinuses reduced over their transition, similar to cetaceans, but their snout sinuses counterintuitively expanded, distinct from cetaceans, and that both trends were underpinned by high evolutionary rates. We hypothesize that aquatic thalattosuchians were ill suited to deep diving by their snout sinuses, which seem to have remained large to help drain their unusual salt glands. Thus, although convergent in general terms, thalattosuchians and cetaceans were subject to different constraints that shaped their transitions to water. Thalattosuchians attained a stage similar to less pelagic transitional forms in the cetacean lineage (late protocetid-basilosaurid) but did not become further specialized for ocean life.

The evolution of whole-body endothermy occurred independently in dinosaurs and mammals and was associated with some of the most significant neurocog-nitive shifts in life's history. These included a 20-fold increase in neurons and the evolution of new brain structures, supporting similar functions in both line-ages. We propose the endothermic brain hypothesis, which holds that elabora-tions in endotherm brains were geared towards increasing caloric intake through efficient foraging. The hypothesis is grounded in the intrinsic coupling of cognition and organismic self-maintenance. We argue that coevolution of increased metabolism and new forms of cognition should be jointly investigated in comparative studies of behaviors and brain anatomy, along with studies of fossil species. We suggest avenues for such research and highlight critical open questions. Endothermy and a neurocognitive revolution Major events in animal evolution often involve neuroanatomical transformations [1]. A revolutionary milestone in animal evolution was the emergence of tachymetabolic endothermy (see Glossary), which independently occurred in two groups: the sauropsid lineage including birds and the synapsid lineage including mammals (Figure 1, Key figure). While the precise timing and reasons behind the evolution of endothermy in these lineages remain uncertain (Box 1), we understand the overall behavioral impact. In essence, endothermy liberated animals from several environmental constraints, opening previously inaccessible environments and niches. They were no longer limited to specific habitats required for behavioral thermoregulation and their ability for sustained activity increased massively [2]. In both the bird and mammal lines, this expansion of their world coincided with an approximately tenfold surge in relative brain size, marking two of the most dramatic shifts in vertebrate brain evolution [3]. Prima facie, this presents a paradox, as nervous systems are extremely energy intensive and the endothermic lifestyle itself requires up to 20 times more energy than an ectothermic one [4]. Therefore, it has been suggested that the bulk of the brain's expansion resulted from a multiplication of the less energy-consuming glial cells [5]. However, recent evidence contradicts this, revealing an even more remarkable change: the shifts to endothermy brought about at least a 20-fold increase in the number of neurons, hence not only enlarging brains but also elevating neuronal density [3]. Undoubtedly, endothermic cognition plays a crucial role in the behavioral flexibility observed in mammals and birds. Despite sharing their last common ancestor as far back as 325 million years ago [6-8], mammals and birds have converged in their cognitive and brain functions [1]. While extant ectothermic amniote cognition remains understudied and probably underestimated, Highlights Endotherms have 20-75 times more brain neurons than similarly sized ecto-therms, marking one of the greatest transformations in brain history. Costly neurons no longer stand in strong competition with somatic processes, but pay for themselves and help meet the 20 times higher energy requirement of endothermy. A major difference between ectotherms and endotherms is the latter's extreme reliance on food. To secure necessary amounts, new foraging strategies are required. Birds and mammals evolved similar neurocognitive functions, absent in ectotherms, providing cognitive maps for highly efficient foraging. We argue for studies of cognition and brain anatomy in extant ectotherms and endotherms to identify key differences. Additionally, we call for studies of dinosaur brains, informed by the findings in the extant species, to trace the cognitive transition related to the evolution of en-dothermy.

Modern birds possess highly encephalized brains that evolved from non-avian dinosaurs. Evolutionary shifts in developmental timing, namely juvenilization of adult phenotypes, have been proposed as a driver of head evolution along the dinosaur-bird transition, including brain morphology. Testing this hypothesis requires a sufficient developmental sampling of brain morphology in non-avian dinosaurs. In this study, we harness brain endocasts of a postnatal growth series of the ornithischian dinosaur Psittacosaurus and several other immature and mature non-avian dinosaurs to investigate how evolutionary changes to brain development are implicated in the origin of the avian brain. Using three-dimensional characterization of neuroanatomical shape across archosaurian reptiles, we demonstrate that (i) the brain of non-avian dinosaurs underwent a distinct developmental trajectory compared to alligators and crown birds; (ii) ornithischian and non-avialan theropod dinosaurs shared a similar developmental trajectory, suggesting that their derived trajectory evolved in their common ancestor; and (iii) the evolutionary shift in developmental trajectories is partly consistent with paedomorphosis underlying overall brain shape evolution along the dinosaur-bird transition; however, the heterochronic signal is not uniform across time and neuroanatomical region suggesting a highly mosaic acquisition of the avian brain form.

Thalattosuchian crocodylomorphs were a ubiquitous component of shallow marine ecosystems during the Jurassic and Early Cretaceous. Alas, their origins remain a mystery. Here we describe three specimens from the Sinemurian (and possibly Early Pliensbachian) of the UK: a partial cranial rostrum, a series of cervical vertebrae, and two dorsal vertebrae adhered with matrix. These specimens are amongst the oldest known thalattosuchian fossils, with the partial cranial rostrum being the oldest known non-neothalattosuchian thalattosuchian. This partial cranial rostrum has a unique combination of rostral characters never seen before in any crocodylomorph, and helps to elucidate early thalattosuchian internal rostrum evolution, suggesting that the reduction in thalattosuchian paranasal sinuses was not related to either the reorganization of rostral neurovasculature seen in later diverging taxa or the increased cancellous bone microstructure. Based on our CT sample, a shift in cranial bone microstructure occurred in the Eoneustes + Metriorhynchidae subclade, one that coincided with the enlargement of the salt glands and decoupling of the external antorbital fenestra from the paranasal sinuses. Without extensive histological sampling we cannot determine whether the shift to an obligate aquatic lifestyle occurred prior to the evolution of Metriorhynchidae.

In recent decades, advances in computed tomographic (CT) scanning and three-dimensional (3D) visualization technology such as 3D Slicer have broadened the capabilities of paleontological research, providing a window into the internal structures of fossilized remains. This form of study is particularly useful for visualizing internal cranial features, which often cannot be physically observed without damaging remains. Rendering 3D images of a skull’s interior enables the reconstruction of cerebral structures, and the neurology of present-day organisms can provide a basis for formulating hypotheses about the neural anatomy and function of extinct ones. The focus of this study is a complete, isolated, and relatively un-deformed braincase of an adult individual of the centrosaurine ceratopsid dinosaur Pachyrhinosaurus lakustai (UALVP 54444), collected from the Wapiti Formation of northern Alberta in 2011, and CT scanned at the University of Alberta Hospital in Edmonton in May 2023. The specimen currently resides at the Philip J. Currie Dinosaur Museum and has not been formally described since its excavation. A 2008 study by Witmer and Ridgely is currently the only published description of the braincase of P. lakustai. The specimen they described (TMP 1989.55.1243) is highly taphonomically deformed and belongs to an unusually small individual, potentially a sub-adult. This project aims to provide a description of UALVP 54444, compare its features to those of TMP 1989.55.1243 and other previously described ceratopsid braincases, and provide new ethological and ontogenetic insights. Relative to TMP 1989.55.1243, UALVP 54444 shows evidence of a more robust cerebral hemisphere and better-developed optic nerves. The olfactory bulb of P. lakustai appears to be modestly developed even by ornithischian standards, but nevertheless larger than in the presumably less social chasmosaurines. The relative sizes of certain nerve and brain structures may hold implications for how neurology impacts the inference of sociality in centrosaurines, as opposed to chasmosaurines. Current data and assessments on the structure of the brain, cranial nerves, inner ear, and encephalic vasculature in UALVP 54444 are presented based on CT scanning of the braincase followed by 3D visualization in the program 3D Slicer.

Many modifications to the skull and brain anatomy occurred along the lineage encompassing non-avialan theropod dinosaurs and modern birds. Anatomical changes to the endocranium include an enlarged endocranial cavity, relatively larger optic lobes that imply elevated visual acuity, and proportionately smaller olfactory bulbs that suggest reduced olfactory capacity. Here, we use micro-computed tomographic (μCT) imaging to reconstruct the endocranium and its neuroanatomical features from an exceptionally well-preserved skull of Sinovenator changii (Troodontidae, Theropoda). While its overall morphology resembles the typical endocranium of other troodontids, Sinovenator also exhibits unique endocranial features that are similar to other paravian taxa and non-maniraptoran theropods. Landmark-based geometric morphometric analysis on endocranial shape of non-avialan and avialan dinosaurs points to the overall brain morphology of Sinovenator most closely resembling that of Archaeopteryx, thus indicating acquisition of avialan-grade brain morphology in troodontids and wide existence of such architecture in Maniraptora.

The nasal passage performs multiple functions in amniotes, including olfaction and thermoregulation. These functions would have been present in extinct animals as well. However, fossils preserve only low‐resolution versions of the nasal passage due to loss of soft‐tissue structures after death. To test the effects of these lower resolution models on interpretations of nasal physiology, we performed a broadly comparative analysis of the nasal passages in extant diapsid representatives, e.g., alligator, turkey, ostrich, iguana, and a monitor lizard. Using computational fluid dynamics, we simulated airflow through 3D reconstructed models of the different nasal passages and compared these soft‐tissue‐bounded results to similar analyses of the same airways under the lower‐resolution limits imposed by fossilization. Airflow patterns in these bony‐bounded airways were more homogeneous and slower flowing than those of their soft‐tissue counterparts. These data indicate that bony‐bounded airway reconstructions of extinct animal nasal passages are far too conservative and place overly restrictive physiological limitations on extinct species. In spite of the diverse array of nasal passage shapes, distinct similarities in airflow were observed, including consistent areas of nasal passage constriction such as the junction of the olfactory region and main airway. These nasal constrictions can reasonably be inferred to have been present in extinct taxa such as dinosaurs.

Thalattosuchian crocodylomorphs were a diverse clade that lived from the Early Jurassic to the Early Cretaceous. The subclade Metriorhynchoidea underwent a remarkable transition, evolving from semi-aquatic ambush predators into fully aquatic forms living in the open oceans. Thalattosuchians share a peculiar palatal morphology with semi-aquatic and aquatic fossil cetaceans: paired anteroposteriorly aligned grooves along the palatal surface of the bony secondary palate. In extant cetaceans, these grooves are continuous with the greater palatine artery foramina, arteries that supply their oral thermoregulatory structures. Herein, we investigate the origins of thalattosuchian palatal grooves by examining CT scans of six thalattosuchian species (one teleosauroid, two early-diverging metriorhynchoids and three metriorhynchids), and CT scans of eleven extant crocodylian species. All thalattosuchians had paired osseous canals, enclosed by the palatines, that connect the nasal cavity to the oral cavity. These osseous canals open into the oral cavity via foramina at the posterior terminus of the palatal grooves. Extant crocodylians lack both the external grooves and the internal canals. We posit that in thalattosuchians these novel palatal canals transmitted hypertrophied medial nasal vessels (artery and vein), creating a novel heat exchange pathway connecting the palatal vascular plexus to the endocranial region. Given the general hypertrophy of thalattosuchian cephalic vasculature, and their increased blood flow and volume, thalattosuchians would have required a more extensive suite of thermoregulatory pathways to maintain stable temperatures for their neurosensory tissues.

Secondarily marine tetrapod lineages have independently evolved osmoregulatory adaptations for life in salt water but inferring physiological changes in extinct marine tetrapods is difficult. The Mesozoic crocodylomorph clade Thalattosuchia is unique in having both direct evidence from natural endocasts and several proposed osteological correlates for salt exocrine glands. Here, we investigate salt gland evolution in thalattosuchians by creating endocranial reconstructions from CT scans of eight taxa (one basal thalattosuchian, one teleosauroid, two basal metriorhynchoids and four metriorhynchids) and four outgroups (three extant crocodylians and the basal crocodyliform Protosuchus) to identify salt gland osteological correlates. All metriorhynchoids show dorsolateral nasal cavity expansions corresponding to the location of nasal salt glands in natural casts, but smaller expansions in teleosauroids correspond more with the cartilaginous nasal capsule. The different sizes of these expansions suggest the following evolutionary sequence: (1) plesiomorphically small glands present in semi-aquatic teleosauroids draining through the nasal vestibule; (2) moderately sized glands in the basalmost metriorhynchoid Pelagosaurus; and (3) hypertrophied glands in the clade comprising Eoneustes and metriorhynchids, with a pre-orbital fenestra providing a novel exit for salt drainage. The large gland size inferred from basal metriorhynchoids indicates advanced osmoregulation occurred while metriorhynchoids were semi-aquatic. This pattern does not precisely fit into current models of physiological evolution in marine tetrapods and suggests a unique sequence of changes as thalattosuchians transitioned from land to sea.