University of Missouri Columbia, Missouri, United States
Abstract Body : Crocodylians are vertebrates that generate the highest bite forces ever measured. Modern crocodylians have flat skulls that are well-suited to aquatic ambush predation. However, fossil ancestors of crocodylians were terrestrial predators with tall skulls, and thus the origin of modern crocodylians involved a substantial reorganization of the feeding apparatus. Although this reorganization is thought to reflect adaptation to crocodylians’ semiaquatic predatory habits, a flat skull likely poses biomechanical challenges to generating and resisting high bite force. Thus, this evolutionary transition likely involved biomechanical tradeoffs and functional compromises.
We hypothesize that the evolutionary flattening of crocodylian skulls will result in inefficient muscle orientations, leading to 1) the evolution of larger muscle masses to overcome these inefficient orientations and 2) more oblique loads on the jaw joints. We also hypothesize that the orientation of joint surfaces will reflect the orientation of joint load. To evaluate these hypotheses, we used imaging data to create 3D models of six extant and five fossil relatives of crocodylians. We used osteological correlates to reconstruct jaw muscle anatomy and reconstructed muscle force by estimating muscle physiological cross-sectional area. Muscle forces and used as input for finite element models and used to estimate skull loading. We developed novel metrics to quantify the orientation of joint surface and its correspondence with joint loading.
Muscle orientations became more mediolateral and rostrocaudal as the skull flattened, supporting our first hypothesis. Modern crocodylians evoloved larger jaw muscle masses relative to earlier relatives of crocodylians, supporting our second hypotheses. Finally, we found that the amount of joint surface and joint force oriented dorsoventrally (p= 0.044) and rostrocaudally (p=0.014) were related, but this was not true for the mediolateral forces (p=0.723), potentially highlighting the role of the pteryomandibular joint in resisting mediolateral forces. These results show that extant crocodylian skulls have key features that accommodate the inefficient muscle orientations caused by flat skulls.
These results depict coordinated coevolution of skull shape, muscle orientation, and joint loading in one of the great transformations in vertebrate evolution. In contrast to many studies in other taxa, our results show that extant crocodylians generate high bite forces not by efficient jaw muscle systems but by overall larger amounts of muscle force. This highlights importance of the many-to-one mapping of form to function in understanding the evolution of biomechanical performance in vertebrate musculoskeletal systems.
