期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2015
卷号：112
期号：5
页码：1481-1486
DOI：10.1073/pnas.1412279112
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：SignificanceInsect wing movements must be both precise and fast. This requirement is especially challenging in smaller insects whose flapping frequencies exceed 100 Hz, because the nervous system cannot exercise stroke-by-stroke control at such rates. In flies, the hind wings have evolved into halteres, gyroscopic sense organs that oscillate exactly antiphase to wings. We show that wing-wing and wing-haltere coordination at high frequencies is mediated by passive biomechanical linkages in thorax. This system requires a clutch mechanism in the wing hinge to independently engage each wing with the vibrating thorax. Once the wings are engaged, the gearbox modulates the amplitude of each wing. Thus, the force transmission mechanism from thorax to wings in flies bears remarkable similarity to automobile transmission systems. The spectacular success and diversification of insects rests critically on two major evolutionary adaptations. First, the evolution of flight, which enhanced the ability of insects to colonize novel ecological habitats, evade predators, or hunt prey; and second, the miniaturization of their body size, which profoundly influenced all aspects of their biology from development to behavior. However, miniaturization imposes steep demands on the flight system because smaller insects must flap their wings at higher frequencies to generate sufficient aerodynamic forces to stay aloft; it also poses challenges to the sensorimotor system because precise control of wing kinematics and body trajectories requires fast sensory feedback. These tradeoffs are best studied in Dipteran flies in which rapid mechanosensory feedback to wing motor system is provided by halteres, reduced hind wings that evolved into gyroscopic sensors. Halteres oscillate at the same frequency as and precisely antiphase to the wings; they detect body rotations during flight, thus providing feedback that is essential for controlling wing motion during aerial maneuvers. Although tight phase synchrony between halteres and wings is essential for providing proper timing cues, the mechanisms underlying this coordination are not well understood. Here, we identify specific mechanical linkages within the thorax that passively mediate both wing-wing and wing-haltere phase synchronization. We demonstrate that the wing hinge must possess a clutch system that enables flies to independently engage or disengage each wing from the mechanically linked thorax. In concert with a previously described gearbox located within the wing hinge, the clutch system enables independent control of each wing. These biomechanical features are essential for flight control in flies.
