Box Extension 20.2

Insect Flight

Humans have long admired and envied the ability of other animals to fly. Insects—from lazily looping butterflies to dive-bombing mosquitoes (or buzzing bees; Figure A)—have captivated our attention. Insect flight muscles possess the familiar features of striated skeletal muscle fibers found in other animals. The myofibrils are organized into sarcomeres; t-tubules and sarcoplasmic reticulum are present; and Ca²⁺ ions bind to the TN–TM complex to permit cross-bridge cycling that produces tension. Box Extension 20.2 describes how physiologists studying the flight muscles of insects have begun to reveal the special features of insect muscles that underlie insects’ aerial feats.

Figure A A honeybee (Apis mellifera) Some insects, such as dragonflies and locusts, use synchronous flight muscles (Figure B1), so named because each muscle contraction is synchronized with the action potential that initiated it, as is the case in vertebrate skeletal muscle. Synchronous flight muscles are arranged vertically to the long axis of the animal, with one end attached to the wings and the other to the floor of the thorax. Contraction of the medial elevator muscles pulls the wings up, and contraction of the lateral depressor muscles pulls the wings down.

Several species of insects (including flies, wasps, bees, and beetles) have evolved muscles that are unique to insects—asynchronous flight muscles (Figure B2), which are capable of contracting at much faster frequencies than synchronous flight muscles or any other known muscles. In asynchronous muscles, individual contractions are not synchronized with individual nerve action potentials. Instead, they typically produce many oscillating contractions for each action potential. Each contraction produces a wing beat. Wing-beat frequencies of more than 1000 beats/s have been recorded in a midge! In addition, unlike fast-contracting muscles in other animals, such as the rattlesnake shaker muscle, asynchronous flight muscles also develop large amounts of tension with economy of ATP. These attributes give insects stunning agility to maneuver their small wings (relative to body size) to accomplish aerial behaviors such as evading predators and seeking out and competing for mates.

Figure B Insects exhibit two types of flight muscles: synchronous and asynchronous (1) Synchronous flight muscles of the dragonfly attach directly to the wings. (2) Asynchronous flight muscles of the housefly attach to the thorax and are arranged perpendicular to each other. Oscillating wing beats result from the two sets of asynchronous muscles alternately changing the shape of the thorax and stimulating each other by stretch. Contracting muscles are colored red and relaxed muscles pink. (After Pringle 1975.)

Asynchronous flight muscles are not attached directly to the wings. Instead, vertical and longitudinal muscles attach to the walls of the thorax (see Figure B2). These opposing pairs of muscles make use of the elastic properties of the thorax. When the vertical elevator muscles contract, they pull down on the roof of the thorax and deform its sides, causing the wings to move up through a hinge arrangement. When the longitudinal depressor muscles contract, the roof of the thorax bulges up and has the effect of moving the wings down.

The most striking functional feature of asynchronous flight muscle is that a single nerve action potential (which causes the release of Ca²⁺ from the SR) initiates a series of subsequent contractions that are each triggered by stretch. When the longitudinal muscles contract to elevate the roof of the thorax, they stretch the vertical muscles. The imposed stretch activates the contractile machinery of the vertical muscles. When the vertical muscles contract, they pull down on the roof of the thorax, and in turn stretch the longitudinal muscles. The release of elastic strain stored in the thoracic wall by contraction of one muscle aids in the stretching of the opposing muscle. Because the two sets of muscles are out of phase, contraction of one induces contraction of the other, and vice versa.

The frequency of the alternating contraction of vertical and longitudinal muscles depends on the resonant mechanical properties of the thorax and wings, not on the frequency of nerve action potentials. If the wings are clipped, the flight frequency increases because of decreased wing inertia and air resistance, but the frequency of initiating nerve action potentials is unchanged. As long as there is sufficient Ca²⁺ in the cytoplasm, the cross-bridges will function. Over time, the Ca²⁺ is pumped back into the SR, and contractions will cease until another action potential is generated by the motor neuron.

In having this property of many contraction–relaxation cycles happening in the continuous presence of Ca²⁺ ions in the cytoplasm, asynchronous flight muscles are distinctly different from all other known skeletal muscle fibers. In all other fibers, Ca²⁺ ions are released from the SR and taken back up with each contraction–relaxation cycle. This difference provides an explanation of how asynchronous flight muscles can produce impressive amounts of tension with metabolic efficiency. The SR in asynchronous muscle occupies only about 3% of the volume of the muscle cells, simply because the muscle fiber does not pump Ca²⁺ ions into the SR with each contraction–relaxation cycle. Furthermore, because less ATP is needed to power the SR Ca²⁺-ATPase pumps, fewer mitochondria are required to support the total metabolism of the cell, which is nevertheless significant because each cross-bridge cycle requires a molecule of ATP. The space that would have been occupied by both mitochondria and SR can instead be occupied by tension-generating myofibrils.

Thus, with the evolution of asynchronous flight muscles, insects saved space and energy. Because asynchronous muscles are found in many different insect groups, it is thought that asynchronous muscles evolved as many as seven to ten times. This example of convergent evolution suggests that asynchronous flight muscles have contributed to the impressive success that insects have achieved in terrestrial environments.

References

Pringle, J. W. S. 1975. Insect Flight. Oxford Biology Reader No. 52 (J. J. Head, ed.), p.4. Oxford University Press, Oxford.