Abstract The force-generating capacity of muscle depends upon many factors including the actin-myosin filament overlap due to the relative length of the sarcomere. Consequently, the force output of a muscle may vary throughout its range of motion, and the body posture allowing maximum force generation may differ even in otherwise similar species. We hypothesized that corn snakes would show an ontogenetic shift in sarcomere length range from being centered on the plateau of the length-tension curve in small individuals to being on the descending limb in adults. Sarcomere lengths across the plateau would be advantageous for locomotion, while the descending limb would be advantageous for constriction due to the increase in force as the coil tightens around the prey. To test this hypothesis, we collected sarcomere lengths from freshly euthanized corn snakes, preserving segments in straight and maximally curved postures, and quantifying sarcomere length via light microscopy. We dissected 7 muscles (spinalis, semispinalis, multifidus, longissimus dorsi, iliocostalis (dorsal and ventral), and levator costae) in an ontogenetic series of corn snakes (mass = 80–335 g) at multiple regions along the body (anterior, middle, and posterior). Our data shows all of the muscles analyzed are on the descending limb of the length-tension curve at rest across all masses, regions, and muscles analyzed, with muscles shortening onto or past the plateau when flexed. While these results are consistent with being advantageous for constriction at all sizes, there could also be unknown benefits of this sarcomere arrangement for locomotion or striking.
more »
« less
This content will become publicly available on March 1, 2026
Fluoromicrometry reveals minimal influence of tendon elasticity during snake locomotion
ABSTRACT Multiarticular muscle systems are widespread across vertebrates, including in their necks, digits, tails and trunks. In secondarily limbless tetrapods, the multiarticular trunk muscles power nearly all behaviors. Using snakes as a study system, we previously used anatomical measurements and mathematical modeling to derive an equation relating multiarticular trunk muscle shortening to postural change. However, some snake trunk muscles have long, thin tendinous connections, raising the possibility of elastic energy storage, which could lead to a decoupling of muscle length change from joint angle change. The next step, therefore, is to determine whether in vivo muscle shortening produces the postural changes predicted by mathematical modeling. A departure from predictions would implicate elastic energy storage. To test the relationship between muscle strain and posture in vivo, we implanted radio-opaque metal beads in three muscles of interest in four corn snakes (Pantherophis guttatus), then recorded X-ray videos to directly measure muscle shortening and vertebral column curvature during locomotion. Our in vivo results produced evidence that elastic energy storage does not play a substantial role in corn snake lateral undulation or tunnel concertina locomotion. The ability to predict muscle shortening directly from observed posture will facilitate future work. Moreover, the generality of our equation, which uses anatomical values that can be measured in many types of animals, means that our framework for understanding multiarticular muscle function can be applied in numerous study systems to provide a stronger mechanistic understanding of organismal function.
more »
« less
- PAR ID:
- 10574819
- Publisher / Repository:
- The Company of Biologists
- Date Published:
- Journal Name:
- Journal of Experimental Biology
- Volume:
- 228
- Issue:
- 5
- ISSN:
- 0022-0949
- Subject(s) / Keyword(s):
- Snake biomechanics fluoromicrometry muscle
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Muscles spanning multiple joints play important functional roles in a wide range of systems across tetrapods; however, their fundamental mechanics are poorly understood, particularly the consequences of anatomical position on mechanical advantage. Snakes provide an excellent study system for advancing this topic. They rely on the axial muscles for many activities, including striking, constriction, defensive displays, and locomotion. Moreover, those muscles span from one or a few vertebrae to over 30, and anatomy varies among muscles and among species. We characterized the anatomy of major epaxial muscles in a size series of corn snakes (Pantherophis guttatus) using diceCT scans, and then took several approaches to calculating contributions of each muscle to force and motion generated during body bending, starting from a highly simplistic model and moving to increasingly complex and realistic models. Only the most realistic model yielded equations that included the consequence of muscle span on torque‐displacement trade‐offs, as well as resolving ambiguities that arose from simpler models. We also tested whether muscle cross‐sectional areas or lever arms (total magnitude or pitch/yaw/roll components) were related to snake mass, longitudinal body region (anterior, middle, posterior), and/or muscle group (semispinalis‐spinalis, multifidus, longissimus dorsi, iliocostalis, and levator costae). Muscle cross‐sectional areas generally scaled with positive allometry, and most lever arms did not depart significantly from geometric similarity (isometry). The levator costae had lower cross‐sectional area than the four epaxial muscles, which did not differ significantly from each other in cross‐sectional area. Lever arm total magnitudes and components differed among muscles. We found some evidence for regional variation, indicating that functional regionalization merits further investigation. Our results contribute to knowledge of snake muscles specifically and multiarticular muscle systems generally, providing a foundation for future comparisons across species and bioinspired multiarticular systems.more » « less
-
Synopsis Locomotion in most tetrapods involves coordinated efforts between appendicular and axial musculoskeletal systems, where interactions between the limbs and the ground generate vertical (GV), horizontal (GH), and mediolateral (GML) ground-reaction forces that are transmitted to the axial system. Snakes have a complete absence of external limbs and represent a fundamental shift from this perspective. The axial musculoskeletal system of snakes is their primary structure to exert, transmit, and resist all motive and reaction forces for propulsion. Their lack of limbs makes them particularly dependent on the mechanical interactions between their bodies and the environment to generate the net GH they need for forward locomotion. As organisms that locomote on their bellies, the forces that enable the various modes of snake locomotion involve two important structures: the integument and the ribs. Snakes use the integument to contact the substrate and produce a friction-reservoir that exceeds their muscle-induced propulsive forces through modulation of scale stiffness and orientation, enabling propulsion through variable environments. XROMM work and previous studies suggest that the serially repeated ribs of snakes change their cross-sectional body shape, deform to environmental irregularities, provide synergistic stabilization for other muscles, and differentially exert and transmit forces to control propulsion. The costovertebral joints of snakes have a biarticular morphology, relative to the unicapitate costovertebral joints of other squamates, that appears derived and not homologous with the ancestral bicapitate ribs of Amniota. Evidence suggests that the biarticular joints of snakes may function to buttress locomotor forces, similar to other amniotes, and provide a passive mechanism for resisting reaction forces during snake locomotion. Future comparisons with other limbless lizard taxa are necessary to tease apart the mechanics and mechanisms that produced the locomotor versatility observed within Serpentes.more » « less
-
The ‘sprawling–parasagittal’ transition was a major postural shift that occurred in the ancestors of mammals, [PSE1] underpinned by musculoskeletal reorganization of the limbs. However, ‘when’ and ‘how’ this important postural shift occurred is unknown. While the anatomical changes characterizing this transition can be traced through the fossil record, how these relate to functional changes, and the acquisition of parasagittal posture, remains poorly understood. Here, we produced three-dimensional musculoskeletal models of the forelimbs of extant (n=3) and fossil (n=8) taxa that phylogenetically and functionally span the sprawling–parasagittal transition. We calculated joint range of motion (ROM) to determine a 3D pose space, using the novel APSE algorithm (Accelerated Pose Searching with Electrostatics). We then estimated muscle moment arms (MMAs) across the entire pose space for all muscles crossing the shoulder and elbow joints. Models of extant species were validated against empirical measures of ROM and MMA derived from ex vivo XROMM (X-ray reconstruction of moving morphology). Among extant species, our parasagittal taxon occupied a distinct region of pose-space, with more retracted and depressed shoulder joint angles. MMA data show increased emphasis on shoulder elevation associated with a parasagittal posture, but greater shoulder depression in sprawlers. Results from the fossil species show complex, non-linear patterns of forelimb transformation, demonstrating that the ‘sprawling-parasagittal’ transition is characterized by homoplasy and postural variation within the mammalian lineage.more » « less
-
The ‘sprawling-parasagittal’ transition was a major postural shift in the ancestors of mammals, resulting in musculoskeletal reorganization of the forelimbs that underpins modern mammal locomotor diversity. However, ‘when’ and ‘how’ this important postural shift occurred is unknown. While the anatomical changes characterizing this transition can be traced through the fossil record, how these relate to functional changes, and the acquisition of parasagittal posture, remains poorly understood. We produced three-dimensional musculoskeletal models of the forelimbs of extant (n=3) and fossil (n=8) taxa that phylogenetically and functionally span the sprawling–parasagittal transition. We calculated joint range of motion (ROM) to determine a 3D pose-space, using the novel APSE algorithm (Accelerated Pose Searching with Electrostatics). We then estimated muscle moment arms (MMAs) across the entire pose space for all muscles crossing the shoulder and elbow joints. Models of extant species were validated against empirical measures of ROM and MMA derived from ex vivo XROMM (X-ray reconstruction of moving morphology). Among extant species, in both models and experiments, our parasagittal taxon occupied a distinct region of pose-space, with more retracted and depressed shoulder joint angles. MMA data show increased emphasis on shoulder elevation associated with a parasagittal posture, but greater shoulder depression in sprawlers. We hypothesised the fossil taxa would follow trends in these postural variables – e.g., increasing shoulder retraction and elevation MMAs through time – but they instead showed complex, non-linear patterns of forelimb transformation. We demonstrate that the ‘sprawling-parasagittal’ transition is characterized by considerable homoplasy and continuous postural variation throughout mammalian evolution.more » « less
An official website of the United States government
