An evaluation of muscle maintenance costs during fiber hypertrophy in the lobster Homarus americanus: are larger muscle fibers cheaper to maintain?

Abstract

SUMMARYLarge muscle fiber size imposes constraints on muscle function while imparting no obvious advantages, making it difficult to explain why muscle fibers are among the largest cell type. Johnston and colleagues proposed the 'optimal fiber size' hypothesis, which states that some fish have large fibers that balance the need for short diffusion distances against metabolic cost savings associated with large fibers. We tested this hypothesis in hypertrophically growing fibers in the lobster Homarus americanus. Mean fiber diameter was 316±11m in juveniles and 670±26m in adults, leading to a surface area to volume ratio (SA:V) that was 2-fold higher in juveniles. Na -ATPase over a broad fiber size range showed that if fibers were much smaller than those observed, maintenance of the membrane potential would constitute a large fraction of whole-animal metabolic rate, suggesting that the fibers grow large to reduce maintenance costs. However, a reaction-diffusion model of aerobic metabolism indicated that fibers in adults could attain still larger sizes without diffusion limitation, although further growth would have a negligible effect on cost. Therefore, it appears that decreased fiber SA:V makes larger fibers in H. americanus less expensive to maintain, which is consistent with the optimal fiber size hypothesis.

Mechanisms underlying parallel reductions in aerobic capacity in non-migratory threespine stickleback (Gasterosteus aculeatus) populations

“…the osmo-respiratory compromise influencing fish gill size (Sardella and Brauner, 2007) and muscle fibre size (Johnston et al, 2005;Jimenez et al, 2011)] and the energetic costs of trait maintenance [e.g. the cost of maintaining large cardiac and skeletal muscle masses (e.g.…”

“…If all else is equal, smaller fibres will decrease the diffusion distance to the mitochondria compared with larger fibres , but incur higher costs from maintaining ion gradients, resulting in an energetic trade-off ['optimal fibre number hypothesis' (e.g. Johnston et al, 2005;Jimenez et al, 2011)]. We predicted that if selection for a high oxygen diffusion rate were relaxed, streamresident fish with larger fibres would have a decreased cost of maintaining ion gradients and be at a selective advantage.…”

“…There was also a non-significant trend towards larger red abductor and adductor fibres in stream-resident Tables3,4). Further studies examining the ion transporter content of stickleback muscles are needed to determine whether changes in muscle size impact the costs of ion regulation as they do in lobster muscle fibres (Jimenez et al, 2011), and measurements of mitochondrial placement within a fibre, myoglobin content and muscle capillarity are needed to examine other possible differences in oxygen diffusion capacity (e.g. Scott et al, 2009;Kinsey et al, 2011).…”

Does the membrane pacemaker theory of metabolism explain the size dependence of metabolic rate in marine mussels?

“…This allowed the authors to suggest an 'optimal fibre size hypothesis', which explains the allometry of muscle fibre diameter in relation to body size through a trade-off between avoiding diffusion limitations and the need to minimize the costs of ion pumping across membranes (Johnston et al, 2004). This hypothesis has been experimentally supported for fish and crustaceans by Jimenez et al (2011Jimenez et al ( , 2013, who showed that bigger specimens have larger muscle fibres than smaller ones, and that the Na + /K + -ATPase activity as well as the energetic cost of its function is lower in larger cells because of the reduced surface area to volume ratio. An inverse relationship between cell size and animal metabolic rate was found in intraspecific studies of a few species, such as mice (Konarzewski and Ksiazėk, 2013) and fish (Maciak et al, 2011;Zhang et al, 2014).…”

“…This leads to a decrease in membrane fluidity and permeability, which in turn results in reduced energy expenditure of the processes maintaining transmembrane ion gradients (e.g. Na + /K + -ATPase activity, Jimenez et al, 2011) and counteracts the futile cycling of protons through the inner mitochondrial membrane (Porter et al, 1996). Thus, changes in the fatty acid composition, and consequently in the fluidity of membranes, enhance metabolic efficiency at larger body sizes.…”