Kinetics of flight muscles from insects with different wingbeat frequencies

Abstract

Small insects usually beat their wings at a higher frequency than large insects. For energetic reasons, the wingbeat frequency is close to the natural resonant frequency of the wing movement^1–3. In the flight muscles of many insects, termed fibrillar muscles, the contractions are myogenic: the muscle is only partially activated by calcium; full activation requires mechanical stretch. Demem-branated fibres can be stretch-activated in vitro, allowing both tension changes and the ATPase activity of the fibres to be monitored. The tension response to a sudden length change shows a large delayed tension component (Fig. 1), whose rate-constant determines the frequency at which the muscle can deliver maximum power to the wings. We show here that this rate-constant is roughly proportional to wingbeat frequency in the flying insect. We find that the ATPase rate is slower and is not related to the rate-constant of tension production, and show that insects with widely different wingbeat frequencies have muscles with similar mechanical power output. We conclude: (1) that the rate-limiting step in the cross-bridge cycle, which limits the ATPase activity, follows the state in which maximum active tension is produced and does not limit the rate at which tension is generated; (2) that the first tension-generating state is probably an actomyosin.ADP.Pi state; and (3) that a preceding step, probably an actomyosin.ADP.Pi isomeriz-ation, which controls the rate-constant for force generation, is faster in smaller insects than in larger ones.