Feats of supercontractile strength: Functional convergence of supercontracting muscle properties among hyoid musculature in chameleons

The structure of sarcomeres imposes limits to the capacity of striated muscle to change length and produce force, with z-disc and myosin filament interactions constraining shortening. Conversely, supercontracting muscles, hitherto only known among vertebrates in the tongue retractor muscle (m. hyoglossus) of chameleons, have perforated z-discs that allow myosin filaments to extend through them into adjacent sarcomeres, permitting continued shortening and force development. Additional hyolingual muscles in chameleons undergo extreme length changes during feeding as well and may benefit from supercontractile properties. We compared length-tension relationship data and transmission electron microscopy (TEM) images from four chameleon muscles to test for the presence of additional supercontracting muscle. We document the second known example of a supercontracting muscle among vertebrates (the m. sternohyoideus superficialis) and show that the m. sternohyoideus profundus exhibits functional convergence with supercontracting muscles by increasing the range of muscle lengths over which it can exert force through the exploitation of sarcomere length non-uniformity across its muscle fibers. Additionally, we show that chameleon supercontracting muscles may share common contractile and structural properties due to a common origin from occipital somites. These results provide important insights into the developmental and evolutionary patterns associated with supercontracting muscle and extreme muscle elongation.

肌节（sarcomere）的结构限制了横纹肌改变长度与产生张力的能力，Z盘（Z-disc）与肌球蛋白丝（myosin filament）的相互作用会约束肌肉缩短过程。与之相反，迄今仅在变色龙的舌回缩肌（m. hyoglossus）中发现过的超收缩肌肉（supercontracting muscles），其拥有穿孔Z盘，可允许肌球蛋白丝穿过Z盘进入相邻肌节，从而实现持续缩短与张力产生。变色龙的其他舌骨肌在摄食过程中同样会发生极端长度变化，或可从超收缩特性中获益。我们对比了四种变色龙肌肉的长度-张力关系数据与透射电子显微镜（TEM）图像，以验证是否存在其他超收缩肌肉。本研究记录了脊椎动物中超收缩肌肉的第二个已知案例——胸舌浅肌（m. sternohyoideus superficialis），并发现胸舌深肌（m. sternohyoideus profundus）通过利用肌纤维间的肌节长度不均一性，扩大了其可产生张力的肌肉长度范围，表现出与超收缩肌肉的功能趋同。此外，我们发现变色龙的超收缩肌肉或许因源自枕体节（occipital somites）的共同起源，共享相似的收缩与结构特性。上述结果为与超收缩肌肉及极端肌肉伸长相关的发育与演化模式提供了重要见解。