Biomechanics of Segmented Axial Musculature in Salamanders and Fishes

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More than half of all vertebrate animals are fish, yet the fundamental relationship between the 3-dimensional (3D) geometry of their muscles and swimming behavior is poorly understood. The body muscles of fish are organized into short segments of muscle fibers, separated by sheets of tendon-like collagen (in "flaky" fish fillets, the segments are the flakes). Within each segment, muscle fibers run in complex trajectories and the segments themselves are folded into cone-like shapes. The complex, 3D structure of these muscles has made it difficult to understand how they function in swimming. The general objective of this study is to understand the function of segmented musculature in two model systems: adults of an aquatic salamander, Siren lacertina, and larvae of zebrafish, Danio rerio. These model species were chosen because they use segmented body muscles for swimming, but the 3D geometry of their muscle segments is simpler than in adult fishes. Interdisciplinary approaches to this problem will be used including mathematical modeling, 3D digital imaging with laser scanning confocal microscopy, and measurement of muscle contraction (muscle strain) during swimming with a sound-pulse based technique, sonomicrometry. The three specific aims of this study are: (1) to develop a mathematical model of the relationship between muscle fiber strain, longitudinal strain, and 3D segment deformation in S. lacertina; (2) to test and refine the model by measuring muscle fiber strain, longitudinal strain, and 3D segment deformation with sonomicrometry during swimming in S. lacertina; and (3) to use confocal microscopy to measure the 3D architecture of segmented musculature in zebrafish larvae, and apply our 3D model to gain insight into the relationship between structure and function of larval zebrafish muscle segments (larval zebrafish will be studied when they first begin to swim freely - a day or two after they hatch out of their eggs). The results of this study will yield an integrated understanding of the effects of muscle fiber angle, muscle segment shape, and connective tissue architecture on the mechanics of swimming. In the future, these results will be applied to the vast diversity of fish species, in order to understand the evolution of the musculoskeletal system in fishes.