A functional analysis of myotomal muscle-fibre reorientation in developing zebrafishDanio rerio

Abstract

SUMMARYThe fast muscle fibres in the anterior trunk of teleost fish are primarily responsible for large amplitude undulatory swimming motions. Previous theoretical studies suggested that the near-helical arrangement of these fibres results in a (fairly) uniform distribution of fibre strain and work output during swimming. However, the underlying simplifications of these studies precluded unequivocal support for this hypothesis. We studied the fast muscle-fibre reorientation and the concomitant myotomal strain variance in a body segment near the anus during larval and juvenile development in the zebrafish. From 2 to 4 days post fertilization (d.p.f.), the measured angles between the muscle fibres and the longitudinal axis of the zebrafish were small. Yet, onset of a near-helical muscle-fibre arrangement was recognized. Juveniles of 51·d.p.f. have larger mean fibre angles and already possess the near-helical pattern of adult teleosts. We present a model that computes the distribution of the strain along the muscle fibres from measured muscle-fibre orientations, body curvature and prescribed tissue deformations. We selected the most extreme body curvatures, which only occur during fast starts and turning manoeuvres. Using the model, we identified the (nonlinear) tissue deformations that yield the least variance in the muscle-fibre strain. We show that simple beam theory cannot reliably predict the strain distribution: it results in very small strains and negligible work output of the most medial fibres. In our model, we avoided these functional limitations by adding a shear deformation to the simple beam deformation. At 2·d.p.f., the predicted variance in the muscle-fibre strain for the shear deformation optimized for strain uniformity is fairly small, due to the small variation in the fibre distances to the medial plane that is caused by the relatively large spinal cord and notochord. The predicted minimal strain variance increases sharply from 2·d.p.f. to 3·d.p.f., remains relatively large at 4·d.p.f., but decreases again considerably at 15 and 39·d.p.f. The 51·d.p.f. stage exhibits the smallest variance in the fibre strains (for the identified optimal deformation), in spite of the widely varying muscle-fibre distances to the medial plane. The non-linear nature of the body deformations with the least strain variance implies an interesting optimization constraint: the juvenile muscle-fibre arrangement results in small predicted spatial strain variations at large-amplitude body curvatures, at the (modest) expense of a large coefficient of variation for small curvatures. We conclude that larval fish rapidly change their muscle-fibre orientations (probably in response to mechanical signals). Within the theoretically examined plausible range of deformations, the closest correspondence to a uniform strain field was found for the juvenile stage. Supplementary material available online at

Growth and the regulation of myotomal muscle mass in teleost fish

“…The much more abundant white muscle is composed of larger diameter fast fibres, packed tightly with myofibrils and delivering five to 10 times more power at the higher tail-beat frequencies associated with unsteady swimming behaviours (Altringham and Johnston, 1990). Fast muscle fibres acquire a complex geometry with development, adopting a near helical pattern over several myotomes, resulting in a uniform strain field as the body bends (van Leeuwen et al, 2008). Muscle fibres with intermediate contractile and metabolic phenotypes may arise during the larval or juvenile stages.…”

The length-force behavior and operating length range of squid muscle varies as a function of position in the mantle wall

“…Thus, fibers from a given region of the mantle wall may produce different instantaneous forces than those in other regions. Such transmural differences in force output by the circular fibers could reduce the mechanical efficiency of the mantle during contraction (Shadwick and Syme, 2008;van Leeuwen et al, 2008).…”

Mechanical characteristics of ultrafast zebrafish larval swimming muscles

“…Individual myotomes consist of bundles of striated muscle fibers (100 µm in length) that span the myotome and insert into myosepta at both ends (Fig. 1B), with fibers oriented nearly parallel to the long axis of the tail (16). In the tail’s central region, the locomotory muscles occupy 67.3±0.4% of the larva’s cross sectional area (CSA), and surround both the spinal cord and notochord, which is a semi-rigid connective-tissue sheath that surrounds cells with large pressurized vacuoles (29, 30) (Fig.…”

“…Larval tail muscle fibers lie nearly parallel to the long axis of the tail and constitute the majority of its mass (16). Therefore, investigators have mounted intact tails between a force transducer and a servo motor for controlling tail length and then electrically stimulated the tails to contract (8, 17-19).…”