Exoskeleton (Insects)

The exoskeleton is noncellular material that is located on top of the epidermal cell layer and constitutes the outermost part of the integument. The local properties and appearance of the exoskeleton are highly variable, and nearly all visible features of an insect result from the exoskeleton. The exoskeleton serves as a barrier between the interior of the insect and the environment, preventing desiccation and penetration of microorganisms. Muscles governing the insect’s movements are attached to the exoskeleton.
Although the exoskeleton is a continuous structure, its mechanical properties differ from region to region. Sometimes the transition between regions is gradual, but often it is quite abrupt; pliant and elastic regions can border on hard and heavily sclerotized regions. Most exoskeletal regions of soft-bodied larvae, such as larvae of moths and flies, are soft and pliant, and only restricted regions of their exoskeletons, such as legs, head capsule, and mandibles, are hard and stiff. Most of the body surface of adult, winged insects is covered by a stiff exocuticle, which can be somewhat flexible and bendable but also serves as a hard protective armor. The exoskeleton covering the dorsal abdomen of many beetle species is thin and easily flexed, whereas the ventral abdominal exoskeleton of the same animals is hard and resistant. The mechanical properties of all exoskeletal regions are precisely adapted to be optimal for the lifestyle of the insect.

FORMATION OF THE EXOSKELETON

The exoskeleton is produced and modified by the epidermal cell layer, and each cell in the epidermis must have the necessary information for producing and depositing the right amount of the right cuticular components at the right time; later some of them will modify the secreted products to give a mature material. The timing of the various events is often hormonally controlled, but the quantitative information on how much to produce must be inherent in individual epidermal cells.
A new exocuticle is produced at each molt. A thin, lipid-rich epi-cuticle is initially secreted from the epidermal cells and deposited beneath the old cuticle, followed by secretion of a thicker procuticle, consisting of chitin and proteins. To allow growth, the total surface area of the new cuticle is larger than that of the old one, and expansion and stretching of the new cuticle take place during and after emergence from the old cuticle (exuvium). Some exoskeletal regions, such as the head capsule, mouthparts, and spines, may be sclerotized before ecdysis; this will help emergence from the old cuticle. These regions cannot be further expanded but will keep their pre-ecdysial size and shape. Other exoskeletal regions are soft and pliant at ecdysis and are sclerotized soon after emergence when the cuticular expansion is complete; as soon as the sclerotization process has started, these regions are irreversibly locked in their new shape.
Sclerotization not only makes the exoskeleton harder and stiffer, it also makes the proteins inextractable and more resistant to enzymatic digestion. Before sclerotization, the exoskeletal proteins are bound to each other and to chitin by various noncovalent links, such as electrostatic interactions, hydrogen bonds, and hydrophobic interactions. Such links can be weakened by changes in pH and ionic strength, making the cuticle more pliant, because displacements of the cuticular components will be easier. During the sclerotization process the proteins are linked firmly to each other, polymerized sclerotizing material fills the voids between proteins and chitin molecules, the cuticle is dehydrated, and deformations of the material will be more difficult.
The sclerotization precursors, N-acetyldopamine (NADA) and N-p-alanyldopamine (NBAD), are synthesized from tyrosine in the epidermal cells. The tyrosine molecules are transformed by decarboxy-lation and hydroxylation to dopamine, which is acylated to NADA and NBAD. These precursors are secreted from the epidermal cells into the cuticular matrix, where they encounter enzymes (phenoloxidases), which oxidize them to the corresponding orthoquinones. Oxidases of different types (tyrosinases, laccases, peroxidases) have been reported and characterized from cuticle. The quinones produced are highly reactive; they will react spontaneously with histidine and lysine residues in the matrix proteins, resulting in cross-links between neighboring proteins, and they will also react with each other, resulting in complex phenolic polymer mixtures. Depending on the precise reaction conditions, the exoskeleton may remain colorless, or a lighter or darker brown coloration may appear during sclerotization.
The water content of the exoskeleton decreases during incorporation of the sclerotizing precursors into the matrix, probably from a decrease in the number of positively charged amino acid residues in the cuticular proteins, which makes the matrix proteins less hydrophilic. Exclusion of water from the intracuticular voids due to accumulation of polymerized material will also contribute to dehydration of the exoskeletal material. Often only the exocuticular layer of the sclerites is sclerotized, but in some insects the sclerotization process continues for extended periods after ecdysis, resulting in sclerotization of parts of the endocuticle, although to a lesser extent than the exocuticle.
Both the loss in cuticular water content and the formation of crosslinks between proteins contribute to a stabilization of the exoskeletal material. The amounts of sclerotizing material incorporated into the various exoskeletal regions varies from less than 1% to more than 10% of cuticular dry weight. These differences are assumed to be responsible for most of the variation in hardness and stiffness of the various exoskeletal regions. Exocuticle tends to be harder and more difficult to deform than endocuticle, presumably because of more extensive sclerotization. The endocuticular layer tend to be compressed when a piece of exoskeleton is bent, whereas the stiffer exocuticle will be little deformed, although it will be in tension.


MUSCLE ATTACHMENTS

The muscles that act on the exoskeleton are connected to the basal surface of the epidermal cells by means of desmosomes. The muscular forces are transferred through the cells by a rich array of microtubules, running in parallel from the basal to the apical surface of the cells, where they attach to hemidesmosomes, and from each hemidesmo-some a dense attachment fiber passes through the cuticle to the epicu-ticle. The muscles are often attached to infoldings of the exoskeleton, the apodemes, which can stretch deep into the body of the insect, allowing larger muscles to act on the same skeletal region. The muscle attachment fibers in the cuticle are not digested by melting fluid. As a result, the insect is able to continue its activities after apolysis during the deposition of the new cuticle. The attachment fibers of the old cuticle are only broken during ecdysis.

ELASTIC EXOSKELETONS

Some small exoskeletal regions are characterized by a rubberlike elasticity; they can undergo considerable deformation when exposed to mechanical stress and will return to their original shape when unstressed. The amount of energy used for deformation is almost completely recovered during relaxation. Its elasticity is the result of the matrix protein resilin. Resilin-containing ligaments are used for energy storage when a fast release of mechanical energy is needed: for example, in the flight system of insects and in the jumping systems of fleas and click beetles. Most resilin-containing ligaments contain chitin microfibrils, making them inextensible and readily flexible, but some ligaments consist of nearly pure resilin and are devoid of chi-tin. Such ligaments can be reversibly stretched to three to four times their unstrained length before breaking. The protein chains in resi-lin are cross-linked by a mechanism different from that used for the solid cuticle; the chains are linked together by covalent bonds formed between side chains of tyrosine residues during the secretion of soluble resilin from the epidermal cells. The elastic properties of the cross-linked material are due to the flexibility and random coiling of the chain segments between cross-links.

PLASTICIZATION

Sometimes the mechanical properties of the exoskeleton can be changed rapidly and reversibly. In bloodsucking bugs (e.g., nymphs of Rhodnius prolixus), the abdominal cuticle is stiff and inextensible before a blood meal. When a meal is initiated, the abdominal cuticle is plasticized, enabling the animal to gorge itself with a volume of blood 10-12 times larger than the total volume of the animal before the meal. To do this, stretch receptors send nerve impulses via the central nervous system to axons terminating in the abdominal epidermis. A neurohormone is released from these nerve endings, and the epidermal cells respond by effecting a slight decrease in intrac-uticular pH. The water content of the abdominal cuticle increases simultaneously, probably owing to the pH change, and the interactions between cuticular proteins decrease, resulting in increased plasticity of the cuticular material.
To facilitate emergence from the old cuticle during ecdysis, the stretchability of the new, pharate cuticle may be temporarily increased to make it easier for the animal to escape from the rather stiff exu-vium and facilitate expansion of the new cuticle after emergence. In the tobacco hornworm Manduca sexta, and probably in many other insects, the plasticization of the pharate adult cuticle is triggered by release of eclosion hormone into the hemolymph. As in Rhodnius nymphal abdominal cuticle, the plasticization of Manduca pharate cuticle at emergence is probably due to an intracuticular pH decrease in combination with increased hydration.
Newly emerged blowflies, which must dig free of the soil before they can expand to their proper size, have a relatively stiff cuticle until they have reached the surface and can begin to swallow air for expansion. For a brief period, their cuticle is plasticized, from release of the neurohormone bursicon. This hormone also plays a role in initiating sclerotization and deposition of endocuticle in the blowflies and probably in other insects.

VISCOELASTICITY

Most types of cuticle are more or less viscoelastic; when exposed to a deforming force for extended periods, they will suffer a slight, time-dependent elongation, and recovery after release of the force may not be complete. A special type of highly stretchable, viscoelas-tic cuticle is found in the abdominal intersegmental membranes of sexually mature female locusts. This stretchability allows elongation of the abdomen necessary for depositing eggs in the soil at a sufficient depth. The membranes in both male and female locusts are soft and pliable, but not very stretchable, as long as the animals are sexually immature. When sexual maturation is initiated in the females by resumed production of juvenile hormone, the organization of the chitin microfibrils in the intersegmental membranes changes from a helicoidal arrangement to one that is perpendicular to the long axis of the animal; at the same time, special hydrophilic proteins are deposited in the membranes. The fully mature intersegmental membranes stretch when loaded, but recover only partly when the load is released. When reloaded with the same load as before, they elongate significantly more than during the first load, and by repeated application of even small loading forces the females can elongate the membranes to about 10-15 times their relaxed length, corresponding to a threefold elongation of the total abdomen. Such stretching enables the female locust to deposit eggs in the soil to a depth of 10-12 cm.

METAL REINFORCEMENT

The mandibles of plant-eating insects are often extremely hard and abrasion resistant because of incorporation of metals, such as zinc and manganese, in the cuticular matrix of the cutting edge of the mandibles. Up to 5% zinc has been registered in some mandibles.

PROTECTIVE BARRIER

The exoskeleton serves also as a water-impermeable barrier, protecting the insect against desiccation. The main part of the barrier is located in the wax-covered epicuticle.
An important function for the exoskeleton is to act as a barrier preventing microorganisms from access to interior of the animal. Soft, pliant cuticles are more easily damaged and penetrated by microorganisms than the sclerotized regions, but they contain a defense system of inactive precursors of phenoloxidases. When the cuticle is damaged, these precursors are activated by limited proteolysis to active phenoloxidases, which will oxidize tyrosine and other phenols to highly reactive quinones. The reaction products are toxic for microorganisms, and they will close minor wounds in the cuticular surface.

COLORATION

Coloration is often the result of various pigments present in granules in the epidermal cells, but the color of insects can also be due to colored material in the cuticle, to diffraction or interference of light caused by special cuticular structures, or to the Tyndall effect.
A brown coloration in the cuticle often develops during sclerotiza-tion of the exocuticle, especially when NBAD is used as precursor for the sclerotization agents, whereas uncolored and transparent cuticles results when NADA is the sole sclerotization precursor. The intensity of the color varies from very light brown over tan to a very dark brown, which can be difficult to discern from the genuinely black cuticles that contain melanins. Melanins are formed when free tyrosine or dopamine is oxidized to orthoquinones, which readily polymerize to complex, black, intractable materials. Melanins are either diffusely distributed in the cuticle or occur in discrete, membrane-bounded granules.
Structural colors of the cuticle from interference of light can be caused by regularly spaced layers in the cuticle in, for example, the cornea of the compound eyes in many flies. Light reflected from the individual layers will interfere to give colors varying with the angle of reflection. Structural colors may also be produced by diffraction of light by regularly spaced microscopic structures on the cuticular surface. The brilliant colors of many beetle species are due to such surface diffraction.
Light scattered by sufficiently small particles (<0.7|im in diameter) looks blue because of the Tyndall effect, as in the blue colors of many dragonflies. The light-scattering particles may be located in the epidermal cells underlying a transparent cuticle, or the light may be scattered by a very fine bloom of wax filaments deposited on the cuticular surface after emergence.

SENSE ORGANS

Several exoskeletal structures are involved in sense perception. Various types of mechanoreceptor are involved in registering the exact position of, and deformation in, the various exoskeletal regions and body parts, movements of surrounding objects, currents of air or water, vibrations in the substrate, and sound oscillations. Chemoreceptors are involved in registering and discerning the presence of various chemical substances; these receptors can be contact chemoreceptors (taste) or olfactory chemoreceptors (smell). Many of the sense organs take the form of setae (bristles, hairs, etc.), which are sensilla consisting of an elongated cuticular structure in connection with the sensory cell(s). A trichogen cell in the epidermis produces a more or less elongated structure, which can be variously shaped, often as a flexible hair, a rigid spine, or an arched dome. The hairs are usually connected to the surrounding cuticle by a joint, flexible membrane, and the sensory cell responds to deformations of the cutaneous membrane. The campani-form sensilla are rigidly connected to the surrounding cuticle, and they respond to tensions in the dome shaped cuticle.
The cuticle covering the elongated sensilla of olfactory chemore-ceptors contains numerous narrow pores, allowing access for the airborne stimulatory molecules into the interior of the sensilla, where they come in contact with and stimulate the dendritic membrane of the sensory cell. The contact chemoreceptors are constructed according to the same principle, but they often contain a single larger pore through which molecules can get access to the sensory cell.
A characteristic feature of the visual system in insects is that both the compound eyes and the single eyes (ocelli) are covered by a transparent cuticle, the lens or cornea, through which light reaches the light-sensitive cells. Both the corneal cuticles and the cuticles used for construction of the other sense organs are constructed according to the common cuticular plan.

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