Highly extensible skeletal muscle in snakes

Abstract

Many snakes swallow large prey whole, and this process requires large displacements of the unfused tips of the mandibles and passive stretching of the soft tissues connecting them. Under these conditions, the intermandibular muscles are highly stretched but subsequently recover normal function. In the highly stretched condition we observed in snakes, sarcomere length (SL) increased 210% its resting value (SL 0 ), and actin and myosin filaments no longer overlapped. Myofibrils fell out of register and triad alignment was disrupted. Following passive recovery, SLs returned to 82% SL 0 , creating a region of double-overlapping actin filaments. Recovery required recoil of intracellular titin filaments, elastic cytoskeletal components for realigning myofibrils, and muscle activation. Stretch of whole muscles exceeded that of sarcomeres as a result of extension of folded terminal tendon fibrils, stretching of extracellular elastin and independent slippage of muscle fibers. Snake intermandibular muscles thus provide a unique model of how basic components of vertebrate skeletal muscle can be modified to permit extreme extensibility.

Crawling without wiggling: muscular mechanisms and kinematics of rectilinear locomotion in boa constrictors

“…Swallowing large prey could also affect the strain and locomotor function of the costocutaneous muscles because of the attendant increase in the distance between the tips of the ribs and the ventral scales (Cundall and Greene, 2000). Although it may not be as extreme as the 200% strain reported for the circumferentially oriented fibers of the intermandibularis muscle of snakes during swallowing (Close et al, 2014), nonetheless, the costocutaneous muscles may experience much larger strains after swallowing a large meal. After consuming large meals, many snakes also appear to have an impeded ability to flex the vertebral column (Crotty and Jayne, 2015), which suggests another possible benefit for being able to perform rectilinear locomotion.…”

Postnatal ontogeny and the evolution of macrostomy in snakes

“…By contrast, alethinophidian snakes included in the clade Macrostomata (pythons, boas, dwarf boas and colubroids) have developed in extreme this feeding strategy ingesting large prey with large cross-sectional area in relation to their head dimensions. This particular feeding behaviour present in macrostomatans is possible due to an anatomical feature labelled as macrostomy [1,2], which requires complementary notable modifications in skeletal and soft tissue organs such as increased length of the gnathic complex (palatomaxillary arch, suspensorium and mandible) and modifications of the intermandibular soft tissues to allow stretching [1][2][3][4][5][6][7]. Macrostomy permits exploiting an enormous diversity of prey types, a fact that has deep implications for the occupation of diverse macrohabitats and evolutionary success of macrostomatan snakes [1].…”

The Builders of the Junction: Roles of Junctophilin1 and Junctophilin2 in the Assembly of the Sarcoplasmic Reticulum–Plasma Membrane Junctions in Striated Muscle

“…While, in addition to junctophilins, neuronal cells express a variety of proteins that are able to form stable ER-PM junctions [ 41 ], JPH1 and JPH2 are the only proteins that form ER-PM junctions in striated muscle. The forces that keep these junctions together are considerably strong since they have to withstand mechanical stress provided by the repetitive contractions and stretching of the muscle fiber, which in some cases can reach extreme levels [ 42 , 43 ]. However, junctophilins’ role is not limited to building such strong structures; they also actively recruit and interact with the components that populate these SR-PM junctions and form the functional apparatus responsible for EC coupling.…”