Functionally Driven Modulation of Sarcomeric Structure and Membrane Systems in the Fast Muscles of a Copepod (Gaussia princeps)

Abstract

Muscles of the mesopelagic copepod Gaussia princeps (Arthropoda, Crustacea, Calanoida) are responsible for repetitive movements of feeding and swimming appendages that are too fast to be followed by eye. This article provides a comparative functional and ultrastructural description of five muscles that have different contraction speeds and are located within different anatomical sites. All are very fast, as indicated by a thick:thin filament ratio of 3:1 and sarcomere lengths that vary between 1 and 3 μm. Measured lengths of thin and thick filaments indicate classification of the muscles into three distinct groups (short, medium, and long) and predict a difference in speed of up to threefold between fibers with the shortest and longest sarcomeres. Indeed, the kicking movement of the posterior legs (with the shortest sarcomere length) is approximately threefold faster than the simultaneous back‐folding of the antennae (with the longest length). Thus, a specific relationship between speed of movement and sarcomere length is established, and we can use the latter to predict the former. Regulatory systems of contraction (sarcoplasmic reticulum [SR] and transverse [T] tubules) match the different contractile properties, varying in frequency of distribution and overall content in parallel to sarcomere variations. All muscles from appendages and body musculature show a unique disposition of contractile material, SR, and T tubules found only in copepod muscles; muscle filaments are grouped in large supermyofibrils that are riddled with frequent cylindrical shafts containing SR and T tubules. This arrangement insures a high spatial frequency of regulatory components. Anat Rec, 301:2164–2176, 2018. © 2018 Wiley Periodicals, Inc.

Muscle: 50+ Years of Electron Microscopy

“…The myofibrils on the very fast muscles of a small copepod seem to be an exception because they are quite large (2.1.4.1 G). However in this case SR and T tubule elements penetrate into the heart of myofibrils thus establishing the essential proximity to acto-myosins, see 1.3.2.1 A Franzini- Armstrong, 1972;Appelt et al, 1991;Takekura and Franzini-Armstrong, 2002;Glaser et al, 2018.…”

“…Finally the TDT of Calliphora, as most body muscles, has a more conventional division of small myofibrils by SR/T tubules (2.1.5.2 D). Glaser et al, 2018;Takekura and Franzini-Armstrong, 2002;Polyak et al, 2003.…”

“…Slower fibers have longer thin and thick filaments and perhaps in order to make up for the thin filament fragility the all have a higher thin/filament ratio, up to a precise disposition of up to 24 thin filament around each thick one (2153 E and F, crab). Franzini- Armstrong, 1970a;Glaser et al, 2018.…”

“…A somewhat similar geometry is also encountered in a primitive fish (2.4.5 K), where dyads are longitudinally oriented and the SR network is not segmented (see 2.5.1.2). Franzini- Armstrong 1974;Eastwood et al, 1982;Franzini-Armstrong et al, 1986;Glaser et al, 2018. During differentiation triads have an initial longitudinal orientation but gradually rotate to a transverse orientation (2.5.1.1 E, prenatal mouse diaphragm, see 2.11.4).…”