Shape, size, and structure affect obliquely striated muscle function in squid

Abstract

Hollow, cylindrical body plans and obliquely striated muscles are characteristic of soft-bodied invertebrates, and both affect the biomechanics of movement in these diverse animals. We highlight two different aspects of functional heterogeneity in obliquely striated muscles, one driven by animal shape and size and the other by the intrinsic mechanical properties of the fibers. First, we show how a hollow, cylindrical shape in the mantle of cephalopod molluscs causes a significant difference in muscle strain (defined as the change in length divided by resting length) across the mantle wall, and describe the implications of such "transmural gradients of strain" for the length-tension relationship of the obliquely striated muscles that power movements in these animals. We show that transmural gradients of strain increase in magnitude as mantle wall proportions change during ontogeny, with the relatively thin mantle walls of newly hatched squid experiencing significantly smaller differences in strain than the thicker mantle walls of adults. Second, we describe how the length-tension relationship of obliquely striated mantle muscles varies with position to accommodate the transmural gradient of strain, with the result that circular muscle fibers near the inner and outer surfaces of the mantle are predicted to produce similar force during mantle contraction. The factors that affect the length-tension relationship in obliquely striated muscles are unknown, and thus we have not yet identified the mechanism(s) responsible for the transmural shift in the length-tension properties of the mantle circular fibers. We have, however, developed a mathematical model that predicts small changes in the oblique striation angle (which varies from 4 to 12° in adult squid) have a significant effect on the shape of the length-tension relationship, with lower angles predicted to result in a broader length-tension curve.