V. David Munteanu

The evolution of archosaurs provides an important context for understanding the mechanisms behind major functional transformations in vertebrates, such as shifts from sprawling to erect limb posture and the acquisition of powered flight. While comparative anatomy and ichnology of extinct archosaurs have offered insights into musculoskeletal and gait changes associated with locomotor transitions, reconstructing the evolution of motor control requires data from extant species. However, the scarcity of electromyography (EMG) data from the forelimb, especially of crocodylians, has hindered understanding of neuromuscular evolution in archosaurs. Here, we present EMG data for nine forelimb muscles from American alligators during terrestrial locomotion. Our aim was to investigate the modulation of motor control across different limb postures and examine variations in motor control across phylogeny and locomotor modes. Among the nine muscles examined, m. pectoralis, the largest forelimb muscle and primary shoulder adductor, exhibited significantly smaller mean EMG amplitudes for steps in which the shoulder was more adducted (i.e., upright). This suggests that using a more adducted limb posture helps to reduce forelimb muscle force and work during stance. As larger alligators use a more adducted shoulder and hip posture, the sprawling to erect postural transition that occurred in the Triassic could be either the cause or consequence of the evolution of larger body size in archosaurs. Comparisons of EMG burst phases among tetrapods revealed that a bird and turtle, which have experienced major musculoskeletal transformations, displayed distinctive burst phases in comparison to those from an alligator and lizard. These results support the notion that major shifts in body plan and locomotor modes among sauropsid lineages were associated with significant changes in muscle activation patterns. Electromyographic data from the forelimb muscles of American alligators indicate that alligators modulate the activity patterns of a primary shoulder adductor muscle across a range of limb postures. Among sauropsids, forelimb muscle burst phases from birds and turtles are distinct compared to those of alligators and lizards, suggesting that muscle activation patterns were influenced by major changes in body plan and locomotor modes.image

Scaling of body shape, gait, limb kinematics, and kinetics can inform about mechanical and energetic constraints influencing animal locomotion on land. However, our knowledge of terrestrial locomotion among tetrapods is biased towards animals that use parasagittal limb postures (mammals and birds). Whether species that use non-parasagittal limb postures (e.g., crocodylians and lizards) share similar scaling principles remains uncertain, especially towards the larger end of the body size spectrum. Here, we compare new data from large adult American alligators (140–223 kg) with previous data from smaller individuals (0.2–5.6 kg) to evaluate the scaling of gait, limb posture, ground reaction forces, and inertial properties of body segments over a size range spanning three orders of magnitude. Larger alligators walked with higher relative stride frequencies and shorter relative stride lengths at equal dimensionless speeds, suggesting that alligators prioritize stance phase mechanical work reduction at the expense of higher costs for swing as they increase in size. Limb posture also changed with body mass: ∼1 kg and larger alligators typically used more adducted and extended limbs, which is expected to mitigate limb muscle forces during stance. Ground reaction forces were increasingly hindlimb dominant as alligators grow to larger size, paralleled by a posterior shift in the center of mass. Counterintuitively, the forelimb grew faster in mass than the hindlimb, possibly because recruited muscle volume is closer to its maximum capacity in the forelimb, compelling larger alligators to keep up with increased mechanical demands via muscle growth more for the forelimb than the hindlimb. These results highlight the numerous changes in body proportions and locomotor performance that are required among animals that use non-parasagittal limb posture, as they grow from neonatal sizes into large adults.

Across vertebrate diversity, limb bone morphology is typically expected to reflect differences in the habitats and functional tasks that species utilize. Arboreal vertebrates are often recognized to have longer limbs than terrestrial relatives, a feature thought to help extend the reach of limbs across gaps between branches. Among terrestrial vertebrates, longer limbs can experience greater bending moments that might expose bones to a greater risk of failure. However, changes in habitat or behavior can impose changes in the forces that bones experience. If locomotion imposed lower loads in trees than on the ground, such a release from loading demands might have produced conditions under which potential constraints on the evolution of long limbs were removed, making it easier for them to evolve in arboreal species. We tested for such environmental differences in limb bone loading using the green iguana (Iguana iguana), a species that readily walks over ground and climbs trees. We implanted strain gauges on the humerus and femur, and then compared loads between treatments modeling substrate conditions of arboreal habitats. For hindlimbs, inclined substrate angles were most correlated with strain increases, whereas the forelimbs had a similar pattern but of lesser magnitude. Unlike some other habitat transitions, these results do not support biomechanical release as a mechanism likely to have facilitated limb elongation. Instead, limb bone adaptations in arboreal habitats were likely driven by selective pressures other than responses to skeletal loading.