The metabolic demands of swimming behavior influence the evolution of skeletal muscle fiber design in the brachyuran crab family Portunidae

We investigated the influence of intracellular diffusion on muscle fiber design in several swimming and non-swimming brachyuran crabs. Species with sustained swimming behavior had aerobic dark fibers subdivided into small metabolic functional units, creating short diffusion distances necessary to support the high rates of aerobic ATP turnover associated with endurance activity. This dark fiber design was observed in all swimming species including Ovalipes ocellatus, which has apparently evolved swimming behavior independently of other Portunidae. In addition, we observed fiber and subdivision size-dependent differences in organelle distribution. Mitochondria, which rely on oxygen to function, were uniformly distributed in small fibers/subdivisions, but were clustered at the fiber periphery in larger fibers. The inverse pattern was observed for nuclei, which are not oxygen dependent, but rely on the transport of slow diffusing macromolecules. Phylogenetically independent contrast analysis revealed that these relationships were largely independent of phylogeny. Our results demonstrate cellular responses to diffusion that were necessary for the evolution of swimming and that are likely to be broadly applicable.