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ABSTRACT Muscle loading is known to influence skeletal morphology. Therefore, modification of the biomechanical environment is expected to cause coordinated morphological changes to the bony and cartilaginous tissues. Understanding how this musculoskeletal coordination contributes to morphological variation has relevance to health sciences, developmental biology, and evolutionary biology. To investigate how muscle loading influences skeletal morphology, we replicate a classic in ovo embryology experiment in the domestic chick (Gallus gallus domesticus) while harnessing modern methodologies that allow us to quantify skeletal anatomy more precisely and in situ. We induced rigid muscle paralysis in developing chicks mid‐incubation, then compared the morphology of the cranium and mandible between immobilized and untreated embryos using microcomputed tomography and landmark‐based geometric morphometric methods. Like earlier studies, we found predictable differences in the size and shape of the cranium and mandible in paralyzed chicks. These differences were concentrated in areas known to experience high strains during feeding, including the jaw joint and jaw muscle attachment sites. These results highlight specific areas of the skull that appear to be mechanosensitive and suggest muscles that could produce the biomechanical stimuli necessary for normal hatchling morphology. Interestingly, these same areas correspond to areas that show the greatest disparity and fastest evolutionary rates across the avian diversity, which suggests that the musculoskeletal integration observed during development extends to macroevolutionary scales. Thus, selection and evolutionary changes to muscle physiology and architecture could generate large and predictable changes to skull morphology. Building upon previous work, the adoption of modern imaging and morphometric techniques allows richer characterization of musculoskeletal integration that empowers researchers to understand how tissue‐to‐tissue interactions contribute to overall phenotypic variation.
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The importance of comparative physiology: mechanisms, diversity and adaptation in skeletal muscle physiology and mechanics
ABSTRACT Skeletal muscle powers animal movement, making it an important determinant of fitness. The classic excitation–contraction coupling, sliding-filament and crossbridge theories are thought to describe the processes of muscle activation and the generation of force, work and power. Here, we review how the comparative, realistic muscle physiology typified by Journal of Experimental Biology over the last 100 years has supported and refuted these theories. We examine variation in the contraction rates and force–length and force–velocity relationships predicted by these theories across diverse muscles, and explore what has been learnt from the use of workloop and force-controlled techniques that attempt to replicate aspects of in vivo muscle function. We suggest inclusion of features of muscle contraction not explained by classic theories in our routine characterization of muscles, and the use of phylogenetic comparative methods to allow exploration of the effects of factors such as evolutionary history, ecology, behavior and size on muscle physiology and mechanics. We hope that these future directions will improve our understanding of the mechanisms of muscle contraction, allow us to better characterize the variation in muscle performance possible, and enable us to infer adaptation.
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- Award ID(s):
- 1942893
- PAR ID:
- 10433519
- Date Published:
- Journal Name:
- Journal of Experimental Biology
- Volume:
- 226
- Issue:
- Suppl_1
- ISSN:
- 0022-0949
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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ABSTRACT Recent studies have demonstrated that muscle force is not determined solely by activation under dynamic conditions, and that length history has an important role in determining dynamic muscle force. Yet, the mechanisms for how muscle force is produced under dynamic conditions remain unclear. To explore this, we investigated the effects of muscle stiffness, activation and length perturbations on muscle force. First, submaximal isometric contraction was established for whole soleus muscles. Next, the muscles were actively shortened at three velocities. During active shortening, we measured muscle stiffness at optimal muscle length (L0) and the force response to time-varying activation and length perturbations. We found that muscle stiffness increased with activation but decreased as shortening velocity increased. The slope of the relationship between maximum force and activation amplitude differed significantly among shortening velocities. Also, the intercept and slope of the relationship between length perturbation amplitude and maximum force decreased with shortening velocity. As shortening velocities were related to muscle stiffness, the results suggest that length history determines muscle stiffness and the history-dependent muscle stiffness influences the contribution of activation and length perturbations to muscle force. A two-parameter viscoelastic model including a linear spring and a linear damper in parallel with measured stiffness predicted history-dependent muscle force with high accuracy. The results and simulations support the hypothesis that muscle force under dynamic conditions can be accurately predicted as the force response of a history-dependent viscoelastic material to length perturbations.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1242/jeb.245158
