The effects of skull flattening on suchian jaw muscle evolution.

Jaw muscles are key features of the vertebrate feeding apparatus. The jaw musculature is housed in the skull whose morphology reflects a compromise between multiple functions, including feeding, housing sensory structures, and defense, and the skull constrains jaw muscle geometry. Thus, jaw muscle anatomy may be suboptimally oriented for the production of bite force. Crocodylians are a group of vertebrates that generate the highest bite forces ever measured with a flat skull suited to their aquatic ambush predatory style. However, basal members of the crocodylian line (e.g., Prestosuchus) were terrestrial predators with plesiomorphically tall skulls, and thus the origin of modern crocodylians involved a substantial reorganization of the feeding apparatus and its jaw muscles. Here, we reconstruct jaw muscles across a phylogenetic range of crocodylians and fossil suchians to investigate the impact of skull flattening on muscle anatomy. We used imaging data to create 3D models of extant and fossil suchians that demonstrate the evolution of the crocodylian skull, using osteological correlates to reconstruct muscle attachment sites. We found that jaw muscle anatomy in early fossil suchians reflected the ancestral archosaur condition but experienced progressive shifts in the lineage leading to Metasuchia. In early fossil suchians, musculus adductor mandibulae posterior and musculus pterygoideus (mPT) were of comparable size, but by Metasuchia, the jaw musculature is dominated by mPT. As predicted, we found that taxa with flatter skulls have less efficient muscle orientations for the production of high bite force. This study highlights the diversity and evolution of jaw muscles in one of the great transformations in vertebrate evolution.

New frontiers in imaging, anatomy, and mechanics of crocodylian jaw muscles.

New imaging and biomechanical approaches have heralded a renaissance in our understanding of crocodylian anatomy. Here, we review a series of approaches in the preparation, imaging, and functional analysis of the jaw muscles of crocodylians. Iodine-contrast microCT approaches are enabling new insights into the anatomy of muscles, nerves, and other soft tissues of embryonic as well as adult specimens of alligators. These imaging data and other muscle modeling methods offer increased accuracy of muscle sizes and attachments without destructive methods like dissection. 3D modeling approaches and imaging data together now enable us to see and reconstruct 3D muscle architecture which then allows us to estimate 3D muscle resultants, but also measurements of pennation in ways not seen before. These methods have already revealed new information on the ontogeny, diversity, and function of jaw muscles and the heads of alligators and other crocodylians. Such approaches will lead to enhanced and accurate analyses of form, function, and evolution of crocodylians, their fossil ancestors and vertebrates in general.

2D and 3D visualizations of archosaur jaw muscle mechanics, ontogeny and phylogeny using ternary diagrams and 3D modeling.

Comparing patterns of performance and kinematics across behavior, development and phylogeny is crucial to understand the evolution of complex musculoskeletal systems such as the feeding apparatus. However, conveying 3D spatial data of muscle orientation throughout a feeding cycle, ontogenetic pathway or phylogenetic lineage is essential to understanding the function and evolution of the skull in vertebrates. Here, we detail the use of ternary plots for displaying and comparing the 3D orientation of muscle data. First, we illustrate changes in 3D jaw muscle resultants during jaw closing taxa the American alligator (Alligator mississippiensis). Second, we show changes in 3D muscle resultants of jaw muscles across an ontogenetic series of alligators. Third, we compare 3D resultants of jaw muscles of avian-line dinosaurs, including extant (Struthio camelus, Gallus gallus, Psittacus erithacus) and extinct (Tyrannosaurus rex) species to outline the reorganization of jaw muscles that occurred along the line to modern birds. Finally, we compare 3D resultants of jaw muscles of the hard-biting species in our sample (A. mississippiensis, T. rex, P. erithacus) to illustrate how disparate jaw muscle resultants are employed in convergent behaviors in archosaurs. Our findings show that these visualizations of 3D components of jaw muscles are immensely helpful towards identifying patterns of cranial performance, growth and diversity. These tools will prove useful for testing other hypotheses in functional morphology, comparative biomechanics, ecomorphology and organismal evolution.

Biomechanical performance of the cranio-mandibular complex of the small notosuchian Araripesuchus gomesii (Notosuchia, Uruguaysuchidae).

Notosuchia is a clade of crocodyliforms that was highly successful and diverse in the Cretaceous of Gondwana. Araripesuchus gomesii is a small notosuchian from the Early Cretaceous of Brazil that belongs to Uruguaysuchidae, one of the subgroups of notosuchians that first radiated, during the Aptian-Albian. Here we present a finite element analysis of A. gomesii based on a model reconstructed from CT scans and performed using published bone properties for crocodiles. The adductor musculature and their respective attachment areas were reconstructed based on Extant Phylogenetic Bracket. Different functional scenarios were tested applying an estimated 158 N bite force: unilateral bite, bilateral bite, pullback, head-shake, and head-twist. The results obtained were compared with those of Alligator mississippiensis, one of its closest living relatives. In the different simulations, the skull and lower jaws of Araripesuchus suffers more stress in the head-shake movement, followed by the unilateral and pullback bites with stress focalized in the premaxillary region. In contrast, the head-twist is the one with smaller stress values. Araripesuchus possess an oreinirostral skull that may provide greater overall resistance in the different scenarios on average, unlike Alligator that has a platyrostral skull with less resistance to dorsoventral mechanical loads. Previous hypotheses that considered A. gomesii as omnivorous coupled with our results, its small size, and likely limited bite force, suggest this taxon probably fed on small prey and other trophic items that could catch and handle entirely with its mouth, such as insects and small vertebrates.

Palatal Biomechanics and Its Significance for Cranial Kinesis in Tyrannosaurus rex.

The extinct nonavian dinosaur Tyrannosaurus rex, considered one of the hardest biting animals ever, is often hypothesized to have exhibited cranial kinesis, or, mobility of cranial joints relative to the braincase. Cranial kinesis in T. rex is a biomechanical paradox in that forcefully biting tetrapods usually possess rigid skulls instead of skulls with movable joints. We tested the biomechanical performance of a tyrannosaur skull using a series of static positions mimicking possible excursions of the palate to evaluate Postural Kinetic Competency in Tyrannosaurus. A functional extant phylogenetic bracket was employed using taxa, which exhibit measurable palatal excursions: Psittacus erithacus (fore-aft movement) and Gekko gecko (mediolateral movement). Static finite element models of Psittacus, Gekko, and Tyrannosaurus were constructed and tested with different palatal postures using anatomically informed material properties, loaded with muscle forces derived from dissection, phylogenetic bracketing, and a sensitivity analysis of muscle architecture and tested in orthal biting simulations using element strain as a proxy for model performance. Extant species models showed lower strains in naturally occurring postures compared to alternatives. We found that fore-aft and neutral models of Tyrannosaurus experienced lower overall strains than mediolaterally shifted models. Protractor muscles dampened palatal strains, while occipital constraints increased strains about palatocranial joints compared to jaw joint constraints. These loading behaviors suggest that even small excursions can strain elements beyond structural failure. Thus, these postural tests of kinesis, along with the robusticity of other cranial features, suggest that the skull of Tyrannosaurus was functionally akinetic. Anat Rec, 303:999-1017, 2020. © 2019 Wiley Periodicals, Inc.

The roles of joint tissues and jaw muscles in palatal biomechanics of the savannah monitor (Varanus exanthematicus) and their significance for cranial kinesis.

Numerous vertebrates exhibit cranial kinesis, or movement between bones of the skull and mandible other than at the jaw joint. Many kinetic species possess a particular suite of features to accomplish this movement, including flexible cranial joints and protractor musculature. Whereas the musculoskeletal anatomy of these kinetic systems is well understood, how these joints are biomechanically loaded, how different soft tissues affect joint loading and kinetic capacity, and how the protractor musculature loads the skull remain poorly understood. Here, we present a finite element model of the savannah monitor, Varanus exanthematicus, a modestly kinetic lizard, to better elucidate the roles of soft tissue in mobile joints and protractor musculature in cranial loading. We describe the 3D resultants of jaw muscles and the histology of palatobasal, otic and jaw joints. We tested the effects of joint tissue type, bite point and muscle load to evaluate the biomechanical role of muscles on the palate and braincase. We found that the jaw muscles have significant mediolateral components that can impart stability across palatocranial joints. Articular tissues affect the magnitude of strains experienced around the palatobasal and otic joints. Without protractor muscle loading, the palate, quadrate and braincase experience higher strains, suggesting this muscle helps insulate the braincase and palatoquadrate from high loads. We found that the cross-sectional properties of the bones of V. exanthematicus are well suited for performing under torsional loads. These findings suggest that torsional loading regimes may have played a more important role in the evolution of cranial kinesis in lepidosaurs than previously appreciated.

Ontogeny of bite force in a validated biomechanical model of the American alligator.

Three-dimensional computational modeling offers tools with which to investigate forces experienced by the skull during feeding and other behaviors. American alligators (Alligator mississippiensis) generate some of the highest measured bite forces among extant tetrapods. A concomitant increase in bite force accompanies ontogenetic increases in body mass, which has been linked with dietary changes as animals increase in size. Because the flattened skull of crocodylians has substantial mediolaterally oriented muscles, crocodylians are an excellent model taxon in which to explore the role of mediolateral force components experienced by the feeding apparatus. Many previous modeling studies of archosaur cranial function focused on planar analysis, ignoring the mediolateral aspects of cranial forces. Here, we used three-dimensionally accurate anatomical data to resolve 3D muscle forces. Using dissection, imaging and computational techniques, we developed lever and finite element models of an ontogenetic series of alligators to test the effects of size and shape on cranial loading and compared estimated bite forces with those previously measured in vivo in A. mississippiensis We found that modeled forces matched in vivo data well for intermediately sized individuals, and somewhat overestimated force in smaller specimens and underestimated force in larger specimens, suggesting that ontogenetically static muscular parameters and bony attachment sites alone cannot account for all the variation in bite force. Adding aponeurotic muscle attachments would likely improve force predictions, but such data are challenging to model and integrate into analyses of extant taxa and are generally unpreserved in fossils. We conclude that anatomically accurate modeling of muscles can be coupled with finite element and lever analyses to produce reliable, reasonably accurate estimate bite forces and thus both skeletal and joint loading, with known sources of error, which can be applied to extinct taxa.