The current hypothesis regarding the mechanics of breathing in crocodylians is that the double-headed ribs, with both a capitulum and tuberculum, rotate about a constrained axis passing through the two articulations; moreover, this axis shifts in the caudal thoracic ribs, as the vertebral parapophysis moves from the centrum to the transverse process. Additionally, the ventral ribcage in crocodylians is thought to possess additional degrees of freedom through mobile intermediate ribs. In this study, X-ray reconstruction of moving morphology (XROMM) was used to quantify rib rotation during breathing in American alligators. Whilst costovertebral joint anatomy predicted overall patterns of motion across the ribcage (decreased bucket handle motion and increased calliper motion), there were significant deviations: anatomical axes overestimated pump handle motion and, generally, ribs in vivo rotate about all three body axes more equally than predicted. The intermediate ribs are mobile, with a high degree of rotation measured about the dorsal intracostal joints, especially in the more caudal ribs. Motion of the sternal ribs became increasingly complex caudally, owing to a combination of the movements of the vertebral and intermediate segments. As the crocodylian ribcage is sometimes used as a model for the ancestral archosaur, these results have important implications for how rib motion is reconstructed in fossil taxa, and illustrate the difficulties in reconstructing rib movement based on osteology alone.
The sprawling-parasagittal postural shift was a major transition during synapsid evolution, underpinned by reorganization of the forelimb, and considered key to mammalian ecological diversity. Determining when and how this transition occurred in the fossil record is challenging owing to limited comparative data on extant species. Here, we built forelimb musculoskeletal models of three extant taxa that bracket sprawling-parasagittal postures-tegu lizard, echidna, and opossumand tested the relationship between three-dimensional joint mobility, muscle action, and posture. Results demonstrate clear functional variation between postural grades, with the parasagittal opossum occupying a distinct region of pose space characterized by a highly retracted and depressed shoulder joint that emphasizes versatility and humeral elevation. Applying our data to the fossil record support trends of an increasingly retracted humerus and greater elevation muscle moment arms indicative of more parasagittal postures throughout synapsid evolution.
The Archosauria are a highly successful group of vertebrates, and their evolution is marked by the appearance of diverse respiratory and metabolic strategies. This review examines respiratory function in living and fossil archosaurs, focusing on the anatomy and biomechanics of the respiratory system, and their physiological consequences. The first archosaurs shared a heterogeneously partitioned parabronchial lung with unidirectional air flow; from this common ancestral lung morphology, we trace the diverging respiratory designs of bird- and crocodilian-line archosaurs. We review the latest evidence of osteological correlates for lung structure and the presence and distribution of accessory air sacs, with a focus on the evolution of the avian lung-air sac system and the functional separation of gas exchange and ventilation. In addition, we discuss the evolution of ventilation mechanics across archosaurs, citing new biomechanical data from extant taxa and how this informs our reconstructions of fossils. This improved understanding of respiratory form and function should help to reconstruct key physiological parameters in fossil taxa. We highlight key events in archosaur evolution where respiratory physiology likely played a major role, such as their radiation at a time of relative hypoxia following the Permo-Triassic mass extinction, and their evolution of elevated metabolic rates. This article is part of the theme issue ‘Vertebrate palaeophysiology’.
Deciphering the biological function of rare or extinct species is key to understanding evolutionary patterns across the tree of life. While soft tissues are vital determinants of joint function, they are rarely available for study. Therefore, extracting functional signals from skeletons, which are more widely available via museum collections, has become a priority for the field of comparative biomechanics. While most work has focused on the limb skeleton, the axial skeleton plays a critical role in body support, respiration, and locomotion, and is therefore of central importance for understanding broad-scale functional evolution. Here, we describe and experimentally validate AutoBend, an automated approach to estimating intervertebral joint function from bony vertebral columns. AutoBend calculates osteological range of motion (oROM) by automatically manipulating digitally articulated vertebrae while incorporating multiple constraints on motion, including both bony intersection and the role of soft tissues by restricting excessive strain in both centrum and zygapophyseal articulations. Using AutoBend and biomechanical data from cadaveric experiments on cats and tegus, we validate important modeling parameters required for oROM estimation, including the degree of zygapophyseal disarticulation, and the location of the center of rotation. Based on our validation, we apply a model with the center of rotation located within the vertebral disc, no joint translation, around 50% strain permitted in both zygapophyses and discs, and a small amount of vertebral intersection permitted. Our approach successfully reconstructs magnitudes and craniocaudal patterns of motion obtained from ex vivo experiments, supporting its potential utility. It also performs better than more typical methods that rely solely on bony intersection, emphasizing the importance of accounting for soft tissues. We estimated the sensitivity of the analyses to vertebral model reconstruction by varying joint spacing, degree of overlap, and the impact of landmark placement. The effect of these factors was small relative to biological variation craniocaudally and between bending directions. Within, we also present a new approach for estimating joint stiffness directly from oROM and morphometric measurements that can successfully reconstruct the craniocaudal patterns, but not magnitudes, derived from experimental data. Together, this work represents a significant step forward for understanding vertebral function in difficult-to-study (e.g., rare or extinct) species, paving the way for a broader understanding of patterns of functional evolution in the axial skeleton.
The lung-air sac system of modern birds is unique among vertebrates. However, debate surrounds whether an avian-style lung is restricted to birds or first appeared in their dinosaurian ancestors, as common osteological correlates for the respiratory system offer limited information on the lungs themselves. Here, we shed light on these issues by using axial morphology as a direct osteological correlate of lung structure, and quantifying vertebral shape using geometric morphometrics in birds, crocodilians and a wide range of dinosaurian taxa. Although fully avian lungs were a rather late innovation, we quantitatively show that non-avian dinosaurs and basal dinosauriforms possessed bird-like costovertebral joints and a furrowed thoracic ceiling. This would have immobilized the lung's dorsal surface, a structural prerequisite for a thinned blood-gas barrier and increased gas exchange potential. This could have permitted high levels of aerobic and metabolic activity in dinosaurs, even in the hypoxic conditions of the Mesozoic, contributing to their successful radiation.
The muscles that effect lung ventilation are key to understanding the evolutionary constraints on animal form and function. Here, through electromyography, we demonstrate a newly discovered respiratory function for the iliocostalis muscle in the American alligator ( Alligator mississippiensis ). The iliocostalis is active during expiration when breathing on land at 28°C and this activity is mediated through the uncinate processes on the vertebral ribs. There was also an increase in muscle activity during the forced expirations of alarm distress vocalizations. Interestingly, we did not find any respiratory activity in the iliocostalis when the alligators were breathing with their body submerged in water at 18°C, which resulted in a reduced breathing frequency. The iliocostalis is an accessory breathing muscle that alligators are able to recruit in to assist expiration under certain conditions.
Studies of joint structure and function have played a central role in understanding palaeobiology and major functional transitions in evolutionary history, where fossilized hard parts (e.g. bones) are often all that remain. Current digital methods for quantifying articular function depend on exhaustively sampling all possible joint poses, but this is computationally intensive, becoming prohibitively so with more degrees of freedom. This has impeded more sophisticated analyses or broader application of these methods to more diverse questions and species. The present study introduces ‘APSE’ (Accelerated Pose Searching with Electrostatics), an iterative algorithm for rapidly and intelligently sampling high‐dimensional joint pose space to quantify articular function and mobility. Key features of the algorithm are: known viable joint poses inform the search for new poses in successive generations; the search preferentially targets under‐explored regions of pose space, while avoiding over‐explored regions; large swaths of inviable pose space are never evaluated, thus minimizing wasted time; and parallelizability. The efficacy of the algorithm was benchmarked with diverse theoretical and biological joints. As a case study to demonstrate its utility, APSE was used to investigate mobility in the enigmatic shoulder joint of the extinct ‘pelycosaur’‐grade synapsid Dimetrodon, the function of which has been widely debated. APSE produces high‐dimensional joint mobility assessments with greater precision than state‐of‐the‐art exhaustive sampling methods. More viable poses are identified at a greater sampling density, but in a fraction of the time taken by current methods (hours, not days or weeks). Results for Dimetrodon shoulder mobility indicate strong coupling between most degrees of freedom across the joint's full range of motion, a stark contrast to the flexible shoulder of most extant tetrapods. APSE provides a time‐efficient means to quantitatively measure articular function and mobility, especially when more degrees of freedom are considered. By greatly reducing computational requirements, APSE lowers the barrier to researchers seeking to undertake more complex or more numerous analyses of articular function in modern and extinct animals. This will accelerate the pace of research in comparative or evolutionary analyses of joint and animal function.
Primates are interpreted to be ancestrally adapted to frugivory, although some modern groups show clear adaptations to other diets. Among them, pitheciids stand out for specifically predating seeds. This dietary specialization is known as sclerocarpy and refers to the extraction of seeds from surrounding hard tissues using the anterior dentition followed by the mastication of seeds by the molars. It has been proposed that Callicebus-Pithecia-Chiropotes-Cacajao represent a morphocline of increasingly specialized anatomical traits for sclerocarpic foraging. This study addresses whether there is a sclerocarpic specialization gradient in the mandibular morphology of pitheciids. Finite element analysis (FEA) was used to simulate two biting scenarios and the obtained stress values were compared between different pitheciids. Geometric morphometrics (GM) were used to display the morphological variation of this group. No support was found for the morphocline hypothesis from a biomechanical viewpoint since all pitheciins showed similar stress values and on average Chiropotes rather than Cacajao exhibited the strongest mandible. From a morphological perspective, it was found that there is indeed relative "robusticity" continuum in the pitheciid mandible for some aspects of shape as expected for the morphocline hypothesis, but this gradient could be related to other factors rather than sclerocarpic specialization. The present results are expected to contribute to a better insight regarding the ecomorphological relationship between mandibular morphology and mechanical performance among pitheciids.
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