Structure, function and evolution of insect flight muscle

Abstract

Insects, the largest group of animals on the earth, owe their prosperity to their ability of flight and small body sizes. The ability of flight provided means for rapid translocation. The small body size allowed access to unutilized niches. By acquiring both features, however, insects faced a new problem: They were forced to beat their wings at enormous frequencies. Insects have overcome this problem by inventing asynchronous flight muscle, a highly specialized form of striated muscle capable of oscillating at >1,000 Hz. This article reviews the structure, mechanism, and molecular evolution of this unique invention of nature.

Keywords: asynchronous operation; insect flight muscle; stretch activation; thin-filament regulatory system.

Figure 1

Basic structure of insect flight muscle (IFM) and control of contraction and relaxation. Structure of a single sarcomere, the minimum unit of muscle function, is shown. A, thin filament; C, C-filament; M, thick filament; MT, mitochondrion; PM, plasma membrane; SR, sarcoplasmic reticulum; Tm, tropomyosin; Tn, troponin; Z, Z-line. In actual muscle, there is no one-to-one correspondence between mitochondria and SR.

Figure 2

Schematic diagram of action of flight muscles. (a), synchronous IFM; (b), asynchronous IFM. Upper trace, wing-beat; middle trace, impulses from motor nerve; bottom trace, intracellular calcium level. The broken line indicates the threshold calcium level above which contraction is initiated. Wing-beat frequencies vary greatly, depending on insect species.

Figure 3

Relative occupancy of various structure in the volume of muscle cell. (a), ordinary skeletal muscle of rattlesnake; (b) sound-producing tail muscle of rattlesnake; (c) timbal muscle of cicada; (d) flight muscle of bee. Others refers to the volume not occupied by any of these organelles (myofibril, SR, mitochondria). Modified from ref. .

Figure 4

Schematic diagram showing the action on indirect flight muscle and stretch activation. Upper left, phase in which dorsoventral muscle (DVM) shortens; upper right, phase in which dorsal longitudinal muscle (DLM) shortens. Note the relation between wing position and the deformation of thoracic exoskeleton. Lower panel, relation between the forces of DLM and DVM. Stretch activation (SA) refers to the delayed rise of force after stretch. The forces of DLM and DVM are complementary to each other. The diagram shows the responses to step stretches, but in live insects, the length change is sinusoidal.

Figure 5

Example of end-on X-ray diffraction pattern from a myofibril of asynchronous IFM, originating from a single hexagonal lattice of myofilaments.

Figure 6

Match-mismatch theory of stretch activation. The diagram shows the relations among 6 thin filaments (pink lines) surrounding a thick filament, the positions of target zones on the thin filament (red circles) and the positions of myosin heads (dots). Myosin heads bound to actin are represented as green circles. In (a) most of myosin heads are unable to bind to actin, but after a ~20-nm stretch, many myosin heads can bind to actin.