Insects Take to the Skies

PTERYGOTA, WINGS, AND FLIGHT

Flight is usually considered to be the relatively recent acquisition of wings in vertebrates such as pterosaurs, birds, and bats. In fact, insects were the first organisms to have developed powered flight and took to the skies at least 90 my prior to the earliest winged vertebrates, perhaps even 170 my earlier (e.g., Engel and Grimaldi, 2004a). They are also the only group of invertebrates to have acquired powered flight (Figure 6.1). The most obvious effect of wings is on the organism's ability to disperse. A flying insect can readily exploit new spaces, and should the local environment become unfavorable, it can more effectively seek better habitats. Similarly, when faced with a predator or other threat, wings allow for a quick retreat. While the "springs" of springtails allow quick escape, there is little or no control over directionality, and a collembolan might find itself in a worse situation after leaping. Flight also enhances locating a mate, allowing once remote, inbred populations to experience a new influx of genes, thus increasing panmixis and genetic variability. Wings as a form of locomotion were clearly the first major morphological innovation of insects, but have been refined through time. Wings even serve functions in addition to flight. Just as the extinct reptile Dimetrodon is presumed to have done with its great dorsal fan, many insects use their wings for thermoregulation, acquiring heat from sunlight to recover from the torpor of cold nights. But this thermoregulation is generally related to flight because flight muscles must reach a critical temperature to function. In some insects, powerful flight muscles vigorously contract while the wings are held motionless, and this quickly generates the heat needed for flight. Wings also can provide passive and active protection, the way folded elytra of beetles protect the abdomen, or leathery forewings of membracid tree-hoppers are flailed against attacking wasps. Some mantises, katydids, and stick insects are efficiently camouflaged because their forewings are remarkably leaf-like (Figure 7.26); in other groups the wings have gaudy patterns to advertise toxicity or sex. Wings also function in auditory communication, for which Orthoptera are best known but hardly the only order of insects to use these structures for sound.

Wings and the refinement of flight have arguably comprised the most critical morphological innovation in the success of insects, and it is quite possible that those insects with complete metamorphosis would not have been so successful if flight did not precede this type of development. With the advent of wings, neural capabilites were expanded to control not just flight but also sensory and integrative neural systems so that the insect could cope with a vaster, three-dimensional environment. Indeed, some of the most "intelligent" insects (i.e., most capable of learning), and those with the most acute vision and olfaction, seem to be predators and pollinators that are active fliers.

Defining features of the Pterygota include the loss of ever-sible vesicles, the presence of a transverse stipital muscle, the fusion of the pleural apophyses with the sternal apophyses (strengthening the thorax during flight deformations), the formation of a pleural sulcus to strengthen the pterothoracic walls, two coxal proprioreceptor organs, a corporotentorium, sperm transfer through copulation (rather than via external spermatophores), and, of course, two pairs of wings (Kristensen, 1991). Wings are not merely modified limbs because the limbs homologous with those in apterygotes are still present in pterygotes. There is, unfortunately, no readily identifiable structure that can easily account for the appearance of wings, and debates over the origin of insects wings have raged for over a century. These twofold arguments highlight the dual nature of a question like, "What is the origin of insect wings?" This seemingly simple query actually consists of two components: (1) From what morphological elements are insect wings composed? (i.e., the homology question); and (2) For what purpose were wings, or winglike structures, first employed? That is, what conditions spurred the origin of wings? To answer these questions, we must first consider how wings function.

6.1. A paperwasp takes off from its nest in Ecuador. Insects were the first organisms to fly, they evolved various flight designs, and have the most maneuvered flight of all animals. Photo: R. Swanson.

INSECT WINGS Wing Function

Detailed reviews of insect flight mechanics are provided by Wootton (1992), Brodsky (1994), Grodnitsky (1999), Dudley (2000), and Alexander (2002), with only the more salient points elaborated here. The complex system of membrane, veins, flexion lines, and overall shape provides a strong but lightweight, flexible structure that can change shape in a controlled (but entirely passive!) way as it moves through air. To achieve flight, all flying animals must produce lift and thrust. Lift is the force that raises the insect off the ground, while thrust is the force moving the insect either forward or backward. The wings form what is called an air foil. This is owing to a slight convex curvature to the overall wing surface with a concave or flat ventral surface. The degree of curvature is the wing's camber: A low camber is weakly convex on the top, while a high camber is strongly convex on top. As air moves over the surface of the wing, it moves slightly faster over the convex surface than it does the ventral, concave surface. This generates an area of lower pressure on the upper surface of the wing (i.e., Bernoulli's principle) creating a force that lifts the wing, and thereby the remainder of the insect, into the air. The air speed and camber of the wing are critical for determining the amount of lift that is created. While the overall body of the wing is a passive actor in flight, muscles pulling on the pteralic plates and epipleurites at the base of the wing alter its tilt in the air stream. As a result, insects fly by maneuvering the wings in a convoluted figure-eight motion where the costal edge leads, not by merely flapping the wings up-and-down as is typically supposed. By tilting the leading edge of the wing downward, an insect can alter its angle of attack relative to the air stream. The angle of attack is the change in the position of the wing owing to a forward or backward tilt, created by pulling the leading edge downward (pronation mostly caused by pulling on the basalare) or upward (supination mostly caused by pulling on the subalare), respectively. Changing the angle of attack by tilting the wing forward is equivalent to altering the camber of the wing by simulating a more strongly curved surface. Thus, additional lift is generated for flight. Thrust, on the other hand, is generated by the pushing movement of the wing against the air mass. Flight thus proceeds by dipping the wing forward (i.e., pronating) from its highest point until the wing has reached the bottom of its downstroke. During the relatively slow downstroke, the wing is also being moved forward (called promotion), thereby generating most of the lift required for flight as well as some thrust. Once reaching the trough of the down-stroke, the wing is strongly tilted backward (i.e., supinated) such that the leading edge is brought upward as the wing begins its upstroke. Simultaneously the wing is shifted slightly to the rear (called remotion), thereby cutting across the path of its downstroke (hence the figure-eight motion) before reaching the peak of its upstroke and repeating the process. By comparison to the downstroke, the upstroke is relatively fast so as to minimize the loss of lift. During all of this gyrating, portions of the wing foil may fold along their lines of flexion, frequently generating vortices of air and additional lift or thrust.

Numerous modifications of this generalized pattern occur among insects, all associated with the peculiarities of flight among orders, families, or species. Highly maneuvered flight is made possible by synchronizing the two pairs of wings, and many orders have developed mechanisms for linking the wings in flight (e.g., Hymenoptera, Lepidoptera), or even by virtually dispensing with one pair of wings (e.g., Diptera). The Odonata are noteworthy exceptions because the forewings and hind wings are out of synchrony. The forewing generates vortices that are captured by the hind wing in hovering flight (see the section on Odonata for more details).

The powerhouse of insect flight, alluded to before, involves the indirect flight muscles. These consume almost all of the available space in the pterygote thorax and do not pull directly on the wing for generating the up- and downstroke of flight (hence their name as indirect). Instead, the muscles are attached such that contractions deform the overall shape of the entire thorax, causing the notum and pleuron to push on the base of the wing and move it up and down. The upstroke is generated by a series of dorsoventral muscles that pull down on the notum during a contraction. The notal wing processes thereby press downward on the leading and posterior edges of the wing base and cause the wing to move upward on the pleural wing process, which provides a pivot point from below. The downstroke is generated by the dorso-longitudinal muscles running lengthwise through the thorax. A contraction of these muscles causes the notum to buckle upward and moves the notal wing process inward. Elastic forces stored in the reinforced walls of the thorax thereby pull the wings upward. Thus, in insect flight the muscles are actually deforming the overall shape of the thorax and not pulling directly on the wings themselves. Despite the apparent absurdity of this design, it is remarkably efficient and powerful. The only exception to this design is once again found in the Odonata. Odonates fly with direct flight muscles, the name of which is self-explanatory regarding their operation. The flight muscles of dragonflies and damselflies are oriented dorsoventrally and are connected above to expanded plates, which themselves attach via tendons to the subalare, basalare, humeral plate, and axillary plate (refer back to the discussion on odonatoid pteralia). The upstroke of odonate flight is caused by contraction of these muscles, which insert just inside of the pleural wing process. The downstroke is produced by muscles inserting lateral to the pleural wing process.

Neuronal control of the wingbeat is not the same for all insects. In insects that beat their wings relatively slowly, each muscle contraction is stimulated by a nerve impulse. This obviously sets an upper limit to how fast a wing can move owing to the recovery time for the nerve to build an action potential. Such muscles are called synchronous flight muscles because one muscle contraction is associated with each nerve impulse. However, some insects beat their wings far more rapidly than a nerve impulse can be conducted, the record being around 1,000 cycles per second, with more typical species ranging from 400 to 600 cycles per second. Flight muscles that contract this rapidly are obviously not dependent on a single nerve transmission, but they function by fibrillation. In fact, the nerve impulse in such insects is instead a signal for beating to begin or to cease. Such muscular systems are called asynchronous flight muscles and are the most metabolically active tissues in nature. Insects with asynchronous muscles tend to have fewer muscles, although each is quite massive.

Most insect flight operates under what is generally called steady-state aerodynamics. For insects that are large enough, the physics of flight (although not the action) is fundamentally the same as in other flying animals. This simply means that the forces of lift and thrust are generated from a steady stream of continuous air flowing across the wing surface. Differences in the direction and velocity of air flow create the differences in thrust, lift, and drag. Incredible flight patterns can be generated under such physical conditions. However, insect flight continues to amaze researchers as they delve further into the complexities of model systems or examine the diversity of flight across species. Indeed, some insects employ non-steady-state aerodynamic principles. This is particularly true in minute insects, for which air is a viscous medium. Moving through air for such species is equivalent to a human swimming through a vat of melted chocolate! The best-studied system is that of the encyrtid wasp, Encarsia. This wasp employs a "clap-and-fling" flight mechanism in which the wings are moved up and down and forcefully clap above and below the body. In this system lift is not generated by air moving across the wing's surface but instead by vortices that swirl around the long axis and tips of the wings. These vortices create the lift necessary for flight.

Paleopterous Versus Neopterous

A single origin of winged insects is now generally undisputed (although see Lemche, 1940; Manton, 1977; La Greca, 1980; Matsuda, 1981), but relationships among its basal members are far from settled. Numerous arguments have been made for relationships among the four main branches of the Ptery-gota, namely the Ephemeroptera (mayflies), the Palaeodicty-opterida (an extinct superorder of haustellate insects), the Odonatoptera (a superorder containing the dragonflies, damseflies, and their extinct relatives), and the Neoptera, which comprises all other winged insects.

Martynov (1925a) was the first author to describe the two major differences in the construction of insect wings, although this division was independently noted by Cramp-ton (1924) at about the same time. They noted that most insects were capable of flexing the wings over the abdomen during rest. This consisted of a flexor muscle pulling on the third axillary sclerite, which in turn helped to collapse or fold the posterior part of the wing, thereby pulling the entire structure over the abdomen (Figure 4.6). The adaptive significance of this feature presumably lies in better exploitation of the environment while storing and protecting the wings, specifically the invasion of tight spaces such as under bark, in soil, among fallen leaves, and even through water. This opened the way for other major wing modifications, such as the development of the forewings into protective covers, like the elytra of beetles and hemelytra of true bugs. If true, it is remarkable to think that a microscopic muscle attached to a microscopic sclerite contributed to the great success of insects. Martynov noted that, in contrast to the neopterous lineages, a few groups were incapable of such movement, and the wings were therefore restricted to being held outstretched either at the insect's side or above the body. In this latter condition, although the wings can be brought together above the body, they cannot be twisted or flexed, such that the wing surface would become parallel to the abdomen; instead, the wing membrane remains perpendicular to the body's long axis. Martynov aptly termed this the paleopterous condition and believed it to be primitive relative to the neopterous insects. Martynov thus initiated a debate that continues today. He proposed two major groups of winged insects, which he named Palaeoptera, for the Ephemeroptera and Odonatoptera, and Neoptera, for all other winged insects.

The Neoptera has been universally supported as a monophyletic group based on the development of wing flexion via unique musculature attachments to the third axillary sclerite; the development of a median plate in the wing articulation, which is divided such that it can fold during wing flexion; the simplification of vein R, which does not branch from the extreme wing base; and the development of the gonoplac. In addition, studies based on DNA sequences have repeatedly recovered the Neoptera as a natural group (e.g., Wheeler et al., 2001).

The "Palaeoptera," on the other hand, presents quite a confusing tale and has been of legitimate contention. Some authors have argued that the palaeopterous condition is itself a derived condition, either respective to neoptery or relative to some unknown, presumably more simplistic, wing design mechanism that has since become extinct. Under these scenarios the Palaeoptera should be recognized as a monophyletic lineage and some authors have cited the bristle-like antennae of Odonata and Ephemeroptera, the aquatic lifestyle of their immatures, and the formation of intercalary veins, among other traits, as further evidence for the monophyly of this group (e.g., Hennig, 1981; Kukalova-Peck, 1983, 1985, 1987, 1991, 1992, 1997). Indeed, limited studies from 18S and 28S rDNA sequences have also supported the Palaeoptera (Hovmöller et al., 2002) but require expansion in taxon sampling before conclusive decisions can be made (e.g., inclusion of Zygentoma as an outgroup for character polarity). Other recent analyses of the same data have failed to support a monophyletic Palaeoptera (Ogden and Whiting, 2003). Alternatively, the Palaeoptera has been considered paraphyletic, but even here there is a difference of opinion. Kristensen (1975) highlighted the primitive attributes of mayflies and considered Ephemeroptera to be the sister group to Odonata + Neoptera (a position earlier heralded by Hennig (1953). In fact, Börner (1904) had already considered Odonata and Neoptera to represent a natural group and had even given them the name Metapterygota. The Metapterygota was defined by several attributes, the most notable being the absence of a subimago (i.e., the loss of molts after the mature, winged form). Ephemeroptera are the only insects to molt when they have wings, which is probably a vestige of the primitive condition seen in apterygotes, which have indefinite numbers of molts. Additional traits defining the Metapterygota are the absence of the caudal filament (which is present in Archaeognatha, Zygentoma, and Ephemeroptera and considered part of the hexapod groundplan), and the fixation of the anterior mandibular articulation. Boudreaux (1979) reversed this hypothesis by placing Odonata basal to Ephemeroptera + Neoptera (as had Lemche, 1940). Recent and extensive morphological and molecular work has continued to support Palaeoptera paraphyly and the mono-phyly of Metapterygota, which we believe to be the more compelling hypothesis. Thus, we must seek glimpses of traits possibly characteristic of the first fliers among the paleopterous orders.

Whence and Whither Wings?

How, when, and why insect wings originated is one of the most perplexing conundrums in evolution. While wings have been repeatedly lost among insects, it is essentially certain that insect wings evolved only once in spite of their stunning structural diversity. Indeed, a monophyletic Pterygota has been supported by every serious study of insect relationships. Arguments in support of a single origin for insect wings include, first, the basic structure of wing veins, which can be homologized across insect orders. Although minor arguments continue over points of detail, particularly in the number of branches for specific vein systems, the overlying pattern is consistent across all orders. Additionally, with the exception of Odonata, the thoracic musculature operating the wings can be homologized across all orders. Furthermore, the wings are always composed of membranous cuticle supported by veins, are always present on the same thoracic segments, and are associated with the same suite of thoracic modifications, such as the development of notal and pleural wing processes and the formation of pteralia. Wings are also congruent with other features that define features of the Pterygota not associated with flight, such as the formation of the gonoplac in the genitalia and evidence from DNA sequences.

With structures as complex as insect wings, it is not surprising that numerous theories have been proposed to explain the morphological and functional origin of wings. The plethora of ideas can be distilled into two current but contrasting theories (Figure 6.2).

Paranotal Lobes. The development of wings from fixed extensions of the thoracic terga, called paranotal lobes, is a traditional theory championed by classic workers such as Snodgrass (1935), and later by Hamilton (1971) and Quartau (1986). Under this theory paranotal lobes provided early insects with the ability to glide, and eventually, with the acquisition of an articulation at their base, these were used for controlling the aerial descent of the insect from perches on tall plants. The presence of paranotal lobes on the protho-racic segments of some Paleozoic insects (Figures 6.17, 6.21, 6.24, 7.9), complete with vein patterns similar to miniature wings, has been heralded as critical evidence for this theory. Indeed, such fossils have at times been referred to as "six-winged" insects! The prothoracic paranotal lobes, however, were not articulated in any of the known fossils so far as anyone can discern. Among extant insects, silverfish possess distinct paranotal lobes that can be used to control their descent while falling (e.g., Hasenfuss, 2002).

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