Tonic fibres in axial muscle of cyprinid fish larvae: their definition, possible origins and functional importance

Abstract

Teleost fish are known to develop small populations of muscle fibres that are assumed to be tonic in nature although their contractile properties and many other characteristics remain unknown. Here we attempt to resolve some of the ambiguity and confusions surrounding the definition and functional role of tonic fibres in teleosts and provide new information on their ontogeny. We investigate the differentiation of tonic muscle fibres in three species of cyprinid fish using electron microscopy, histochemistry, immunohistochemistry and in situ hybridization. The fine structure of the fibres defined as tonic in the larvae used in this study complies with patterns known from studies in teleost adults. This allows formal definition of tonic fibres in cyprinid larvae. The tonic fibres may be recognized by a variety of features: (1) by their characteristic position along the medial confines of the red muscle insertion at the horizontal septum, (2) their fine structure, including solid clusters of irregularly cleaved myofibrils, thick and wavy Z-lines, and T-tubules at the A-band/I-band transitions, (3) their histochemical features, specifically weak but obvious staining for mATPase after alkaline preincubation, and lack of SDH activity in the more advanced larval stages, (4) their unique immunological properties, being the only fibre type in the myotome that reacts with a serum against chicken tonic myosin (anti- T2). Expression of tonic characters usually begins within a few fibres in the dorsal domain of the superficial red muscle insertion at the horizontal septum and hence involves a high degree of dorso-ventral polarity. The present evidence indicates that tonic fibres arise from separate myogenic stem cells rather than by transdifferentiation from existing red fibres. First appearance of tonic fibres during ontogeny correlates closely with the onset of free swimming and exogeneous feeding. We use this fact to argue that tonic fibres are probably a prerequisite for efficient locomotory control during prey capture, shoaling and predator avoidance.

Evolution of myogenesis in fish: a sturgeon view of the mechanisms of muscle development

“…Anti-T2 marks all slow fibres in sturgeons (Figs. 2e,3f,4d), while in the teleosts, anti-T2 is a reliable marker only of tonic fibres (just as in amphibian and avian muscle) but does not react to slow fibres (Chayen et al 1993;Stoiber et al 2002b). The 4D9 antiengrailed antibody was applied to all sturgeon developmental stages examined where it stained some neurons in the posterior brain but did not stain in the somites.…”

“…Images were photographed digitally using the Gatan Image Acquisition software. For the immunostaining treatment of sections, freshly killed animals were processed according to the procedures described by Stoiber et al (2002b). Cryosections were reacted with the primary antisera listed in Table 2.…”

Slow-tonic muscle fibers and their potential innervation in the turtle,Pseudemys (Trachemys)scripta elegans

“…For example, because slow-tonic fibers 1) are highly oxidative, and 2) have myosin-ATPase activity that is acid-stable and alkali labile, they are histochemically indistinguishable from slowtwitch SO fibers (for a chronological review, see Hess, 1970;Guth, 1981;Morgan and Proske, 1984). This problem was resolved to large extent by the use of antibody staining (Shafiq et al, 1984;Stoiber et al, 2002), as used in the present study, Fig. 4.…”

“…Therefore, in the following discussion there is no mention of slow-tonic fiber presence and presumed function in fish and snakes, even though slow-tonic fibers are clearly present in both animals (e.g., fish, Sä nger, 1997; Tullis and Block, 1997;Stoiber et al, 2002;snake, Wilkinson and Lichtman, 1985;Robinson, 1987).…”

Muscle fine structure reflects ecotype in two nototheniids

“…They more likely serve the role of tonic muscle, stabilizing the trunk during locomotion driven by pectoral fins (Davison, 1983; Sänger, 1997). It is argued that tonic fibres are a prerequisite for efficient locomotory control during prey capture, shoaling and predator avoidance (Stoiber et al ., 2002 b ).…”