Transient flagellar waveforms during intermittent swimming in sea urchin sperm. II. Analysis of tubule sliding

Patterns of tubule sliding that occur during the stopping and starting transients of sea urchin sperm flagella have been analysed and compared to those occurring during steady-state beating. During steady-state symmetrical beating, the overall pattern of tubule sliding appears to be composed of three distinct classes, two of which, interbend growth and an oscillatory synchronous component, are associated with bend development at the basal end of the flagellum, while the third, metachronal sliding, is associated with the propagation of bends of constant angle. During the blocked stage of stopping and starting transients in which no bends are propagated to the tip, three additional classes of sliding occur: proximal transfer, interbend decay and delocalization. The increasing asymmetry in the flagellar waves that occurs during the transitional stage of a stopping transient is the result of the increasing magnitude of a nonoscillatory synchronous component, which leads to formation of a nonpropagating bend in the basal region of the flagellum, upon which are superimposed the pre-existing patterns of interbend growth and the oscillatory synchronous component that continue unchanged from the earlier steady-state beating. When the angle between the midregion of the flagellum and the axis of the sperm head attains a value of about 3 rad, bends no longer propagate into the midregion and the flagellum becomes quiescent. Upon reinitiation of flagellar movement the reverse bends during the blocked stage of the starting transient develop by interbend growth, while the principal bends develop by a combination of proximal transfer and interbend growth. As the bends propagate into the distal region, they lose angle by interbend decay and, after the reverse bend has been lost completely, the remaining portion of the principal bend is abruptly delocalized. During this blocked stage, the flagellar asymmetry, as indicated by the time-averaged angle between the axis of the sperm head and the flagellar tip, remains unchanged from the prior quiescent stage. Once principal bends begin to be propagated to the tip, corresponding to the end of the blocked stage and the beginning of the transitional stage, the nonoscillatory synchronous component increases abruptly from zero to a net positive value and no further proximal transfer occurs. The decreasing asymmetry during the transitional stage then results from a gradual decrease in the magnitude of this nonoscillatory synchronous component. The pattern of the oscillatory synchronous component is particularly apparent in starting transients with long blocked stages. After the first two beat cycles, the amplitude of the oscillatory synchronous sliding remains constant at about 0.2 rad for the rest of the blocked stage, through the whole transitional stage and on into the steady-state beating, while its phase maintains a constant relationship to that of the oscillations in interbend growth, lagging the latter by about 0.2 beat cycle. This oscillatory synchronous component could be the result of either a limited amount of actual synchronous sliding in the distal region of the flagellum or of some form of elastic structural distortion producing an oscillatory cryptic bending of limited extent in the basal region of the flagellum. However, the nonoscillatory synchronous component can be explained simply only on the basis of actual synchronous sliding. The process of synchronous sliding, in which shear strain is transferred longitudinally along the flagellum without affecting the angle or propagation of intervening bends, may be the result of the sliding in a limited group of tubules being temporarily uncoupled from bending.