It Is Hard to Be Soft: Length-Force Relationships in Muscles of Hydrostatically Supported Animals

Hydrostatic skeletal support is widespread among animals. If modeled as an isovolumetric cylinder that is longer than it is wide, a hydrostatic structure should undergo large changes in length for relatively small changes in diameter. This presents an underappreciated consequence for the muscle fibers controlling hydrostatic skeletal shape: longitudinally oriented muscle fibers may experience remarkably long operating ranges. Superelongation, or the ability to produce relatively high forces over an extreme range of muscle lengths, may thus be necessary for longitudinally oriented fibers. We discovered superelongation and an interesting morphological specialization in an obliquely striated muscle of the polychaete worm Glycera dibranchiata. These worms have an eversible proboscis that is used for burrowing and prey capture. The proboscis retractor muscles extend from the body wall to the gut and likely undergo a large stretch during proboscis eversion. Like two other previously described superelongating muscles in squid and leeches, the proboscis retractor muscles had a broad length-force relationship (LFR). At a given muscle length, however, some muscle fibers were folded while others were not (i.e., the folded fibers were longer than the whole muscle, at least when the muscle was partially contracted). The number of folded fibers and extent of folding were higher at shorter muscle lengths. We hypothesize that the short muscle fibers experience tension at all muscle lengths, while the folded fibers only experience tension at long whole muscle lengths. Thus, each retractor muscle contains populations of fibers of different lengths that may contribute differentially to the broad LFR. Superelongation with varying fiber folding may represent a previously unrecognized strategy in obliquely striated muscle for permitting high force production over a broad range of muscle lengths needed for hydrostatic skeletal support.