Nature's strategy for optimizing power generation in insect flight muscle.

Table 1 summarizes the primary mechanisms most likely responsible for modifying wing beat frequency (WBF) and muscle power in the Drosophila mutants discussed above. The different outcomes reflect different mechanisms that come into play, depending on the protein and site of the mutation. For example, the reduced muscle power and WBF of the RLC phosphorylation site mutant Mlc2(S6sA,S67A) reflect the reduced number of myosin heads available to form working cross-bridges and the concomitant reduction in muscle stiffness. The mixed results of the other mutants are more difficult to explain. For example, while the reduced muscle stiffness of the paramyosin rod mutant pm(S18A) and the projectin mutant bent(D)/+ may in part reflect mutation-related increases in compliance of the thick filaments (pm(S18A)) or connecting filaments (bent(D)/+), the elevated WBF is unexpected because one would expect reduced muscle stiffness to lower WBF rather than raise it. Other aspects of the results are equally baffling. In the case of pm(S18A), e.g., myofilament kinetics are enhanced, opposite to what one would predict from reduced myofilament stiffness (Wang et al. 1999), but consistent with a direct effect of the mutation on cross-bridge kinetics. It is tempting to speculate that the fly increases the resonance frequency of its flight system, perhaps even over-compensating, as a mechanism for bringing the optimum frequency of power output of the flight system in line with the optimum frequency of power output of the myofilaments in order to achieve flight. The fly might accomplish this by voluntarily activating flight control muscles that change the stiffness and shape of the thoracic box (Tu and Dickinson, 1996), thereby significantly changing the basal stiffness of the resonance system. This effective strategy would serve to tune flight system kinetics to that of the actomyosin motor for optimum power transmission. Notably, of the four thick filament mutations listed in Table 1 produce no significant changes in wing beat frequency, three exhibit reduced muscle power, so these flies must make other adjustments to maintain flight competency. These may be additional cases in which the effects of marked changes in cross-bridge kinetics (MHC IFI-EC), cross-bridge deployment (Mlc2(delta2-46), or sarcomere (thick filament) stiffness (pm(S-A4) and Df(3L) fln(1)/+) are ameliorated by the intervention of direct flight muscles. In summary, it may well be that the fly's general response to mutations that alter one component of the flight system is to alter another in order to maintain optimum transmission of power and flight competency. That is, nature's strategy for optimizing power generation throughout the flight system is probably the same as that at the level of the myofibril: that is, strengthen weak links, orient parts for optimum power production, and modify power train proteins through isoform switches or post-translational modifications to assure all components are in tune with one another.