Muscle and Joint Evolution in Crocodyliforms
Authors: Sellers Kaleb C. , Middleton Kevin M. , Clark James M. , Holliday Casey M. 
Published: April 2020

Modern crocodylians employ immense forces during feeding relative to other clades. Many characters that enable crocodylians to generate and resist these forces are not found in their ancestors, and thus the evolution of crocodylians involved a substantial reorganization of the feeding apparatus. This transformation saw changes to many cranial joints: the expansion of the pterygoid buttress, reshaping and reorienting of the articular surface of the jaw joint, and the suturing of the quadrate and palate to the braincase, closing the primitive and potentially‐kinetic otic and palatobasal joints. The jaw muscles that loaded cranial joints also experienced reorganization: the flatter skull of crocodylians led to mediolateral orientations, the pterygoideus ventralis muscle began attaching laterally on the mandible, and the retroarticular process enlarged caudally, expanding the size of the depressor mandibulae muscle. Once this suite of changes was in place, crocodyliforms radiated into forms with derived diets and craniodental modifications. However, the biomechanical effects of these morphological character shifts on feeding performance have not been explicitly evaluated, obscuring coevolutionary patterns of morphology and function. Here, we use select crocodylians and fossil relatives that characterize the evolution of the clade to reconstruct jaw muscle anatomy and estimate biomechanical loading of cranial joints. We hypothesize that crocodylians will be characterized by successive increases in jaw muscle mass relative to body size. We used CT data to create 3D models of extant and fossil suchians that demonstrate the evolution of the crocodylian skull, using osteological correlates to reconstruct muscles. Muscle forces were distributed with the computational package Boneload and used as input for finite element analysis and 3D lever analyses. We found that jaw muscles expanded and shifted attachments throughout suchian evolution: muscle orientations became more mediolateral as the skull flattened, the pterygoideus ventralis muscle began inserting on the lateral mandible, and the depressor mandibulae muscle expanded its attachment on the enlarged retroarticular process. Changes to cranial joints accompanied muscular changes: the pterygoid buttress expanded, the articular surfaces of the jaw joint changed, and the quadrate and palate sutured to the braincase. Our results showed that joint force orientation tracks with articular surface metrics. We found that as bite location moves caudally, working side joint force decreases in magnitude; it is likely that in feeding events such as shaking bites or death roll, the jaw joint is loaded in tension. This study depicts a feeding apparatus that defies traditional understanding. The combination of dual craniomandibular joints and jaw joints loaded in tension is unknown from other tetrapods.Support or Funding InformationNSF‐EAR 1631684Cladogram of representative crocodiles included in the study. The black arrows represent the orientation of joint reaction force; note that joint reaction force becomes more horizontally oriented in later specimens.Figure 1