The muscular anatomy that allows many insects to fly. The ability of flight in flying insects (class Insecta, phylum Arthropoda) is one of the key evolutionary adaptations that ensured the survival and dissemination of these animals. In general, insect flight muscle is divided on structural and physiological grounds into synchronous and asynchronous types, and on the basis of its mechanical operation within the insect into direct and indirect flight muscles. There is a large degree of structural diversity between the types of synchronous muscle, but the functional distinction between synchronous muscle and asynchronous muscle is far more fundamental. The fibers of all insect flight muscles are rich in mitochondria (specialized organelles that are necessary for cellular respiration and energy production) and rely on aerobic metabolism, furnishing the means to meet the high energy demands of flight. Overall, the elements of the muscular system of flying insects evolved to provide these creatures with a highly efficient and specialized ability of flight (Fig. 1). See also: Adaptation (biology); Animal evolution; Flight; Insect physiology; Insecta; Metabolism; Mitochondria; Muscle; Muscular system
Direct flight muscle
Direct flight muscle is present in the so-called primitive insects, that is, the mayflies (order Ephemeroptera), dragonflies [panel (a) of Fig. 2], and damselflies (the latter two groups comprising the order Odonata). One end of each direct flight muscle is attached to the base of the wing, and the other end is attached to the inside of the thorax. Contraction of the flight muscles, therefore, drives the wings directly. The wingbeat frequencies of insects with direct flight muscles are typically less than 100 Hz. All insects with direct flight muscles have synchronous muscle. See also: Ephemeroptera; Odonata
Indirect flight muscle
In most insects, including butterflies, moths, flies, and bees (Fig. 3), indirect muscles attach to the inside of the thorax rather than the wing. Muscle contraction deforms the thorax and, through a complex hinge, moves the wings up and down. The indirect elevator muscles run between the roof and floor of the thorax, and contraction pulls the roof downward and raises the wings. Contraction of the depressors, which run from front to back, buckles the thorax, raises the roof, and lowers the wings [panel (b) of Fig. 2]. The mass of wings, the aerodynamic forces acting upon them, and the elasticity of the thorax act as a resonant system that enables some insects to operate with wingbeat frequencies up to 1000 Hz. In these insects, both synchronous and asynchronous indirect flight muscles are found, but only those insects with asynchronous muscle can achieve the high wingbeat frequencies.
Synchronous muscle is characterized by an equal and simultaneous neural input and muscular contraction, with each mechanical contraction being caused by a burst of neural activity. The rhythm of the wingbeat is thus neurogenic in origin. Insects with this type of muscle rarely have wingbeat frequencies that exceed 100 Hz. This is a limitation imposed by the neurogenic nature, as well as by the time required to activate and relax the muscle in each wingbeat. Some highly modified synchronous flight muscles are found, for example, in the singing muscles of cicadas. See also: Cicada; Nervous system (invertebrate); Neurobiology
Very high wingbeat frequencies are found in some species of insects; for example, the wingbeat frequency of some midges is of the order of 1000 Hz. These high frequencies are found in insects that possess asynchronous flight muscles, that is, muscles where the number of nerve impulses to the muscle is much lower than the high wingbeat frequency. The wingbeat frequency of the blowfly is approximately 120 Hz, but the frequency of neural input is only 3 Hz. The nervous input to these muscles facilitates (rather than controls) the frequency of contraction.
The rhythmic contraction of asynchronous muscle that drives the wings results from a unique resonant coupling between the flight muscles and the elastic thorax. When the active muscle is stretched by the recoil of the elastic thorax, it develops force after a short delay. However, this delay is long enough to allow a complete recoil of the thorax, before delayed force development deforms it. This property of a stretch-induced delayed force development is the result of a unique myosin filament structure. The depressor and elevator muscles work in opposition to oscillate the thorax and beat the wings. The time course of delayed force development enables the muscles and thorax to resonate at the same natural frequency. Because the system is operating at its resonant frequency, a minimum amount of energy is required to maintain the oscillations once the wingbeating has started. Because the muscle does not need to be repeatedly switched on and off, and because the thorax is relatively stiff, the system can operate at high frequencies. See also: Muscle proteins
If evolution has resulted in optimization of muscle function, size-dependent changes in these processes should be reflected in the properties of the muscles that drive them. The main function of muscle is to generate power, normally cyclically and repetitively (for example, contracting and relaxing of the diaphragm during breathing, or of the leg extensor muscles in walking). The body demands the greatest effort from the muscles at particular frequencies. Therefore, under normal circumstances, the muscles should perform best over those frequencies. See also: History of insect body size