CY501-C06[155-187].qxd 2/14/05 5:53 PM Page 155 quark11 27B:CY501:Chapters:Chapter-06: 6 InsectsInsects Take Take to the Skies to the Skies advertise toxicity or sex. Wings also function in auditory PTERYGOTA, WINGS, AND FLIGHT communication, for which Orthoptera are best known but Flight is usually considered to be the relatively recent acqui- hardly the only order of insects to use these structures for sition of wings in vertebrates such as pterosaurs, birds, and sound. bats. In fact, insects were the first organisms to have devel- Wings and the refinement of flight have arguably com- oped powered flight and took to the skies at least 90 MY prior prised the most critical morphological innovation in the suc- to the earliest winged vertebrates, perhaps even 170 MY ear- cess of insects, and it is quite possible that those insects with lier (e.g., Engel and Grimaldi, 2004a). They are also the only complete metamorphosis would not have been so successful group of invertebrates to have acquired powered flight if flight did not precede this type of development. With the (Figure 6.1). The most obvious effect of wings is on the organ- advent of wings, neural capabilites were expanded to control ism’s ability to disperse. A flying insect can readily exploit not just flight but also sensory and integrative neural systems new spaces, and should the local environment become unfa- so that the insect could cope with a vaster, three-dimensional vorable, it can more effectively seek better habitats. Similarly, environment. Indeed, some of the most “intelligent” insects when faced with a predator or other threat, wings allow for a (i.e., most capable of learning), and those with the most acute quick retreat. While the “springs” of springtails allow quick vision and olfaction, seem to be predators and pollinators escape, there is little or no control over directionality, and a that are active fliers. collembolan might find itself in a worse situation after Defining features of the Pterygota include the loss of ever- leaping. Flight also enhances locating a mate, allowing once sible vesicles, the presence of a transverse stipital muscle, the remote, inbred populations to experience a new influx of fusion of the pleural apophyses with the sternal apophyses genes, thus increasing panmixis and genetic variability. (strengthening the thorax during flight deformations), the Wings as a form of locomotion were clearly the first major formation of a pleural sulcus to strengthen the pterothoracic morphological innovation of insects, but have been refined walls, two coxal proprioreceptor organs, a corporotentorium, through time. Wings even serve functions in addition to sperm transfer through copulation (rather than via external flight. Just as the extinct reptile Dimetrodon is presumed to spermatophores), and, of course, two pairs of wings have done with its great dorsal fan, many insects use their (Kristensen, 1991). Wings are not merely modified limbs wings for thermoregulation, acquiring heat from sunlight to because the limbs homologous with those in apterygotes are recover from the torpor of cold nights. But this thermoregu- still present in pterygotes. There is, unfortunately, no readily lation is generally related to flight because flight muscles identifiable structure that can easily account for the appear- must reach a critical temperature to function. In some ance of wings, and debates over the origin of insects wings insects, powerful flight muscles vigorously contract while have raged for over a century. These twofold arguments high- the wings are held motionless, and this quickly generates light the dual nature of a question like, “What is the origin of the heat needed for flight. Wings also can provide passive insect wings?” This seemingly simple query actually consists and active protection, the way folded elytra of beetles pro- of two components: (1) From what morphological elements tect the abdomen, or leathery forewings of membracid tree- are insect wings composed? (i.e., the homology question); hoppers are flailed against attacking wasps. Some mantises, and (2) For what purpose were wings, or winglike structures, katydids, and stick insects are efficiently camouflaged first employed? That is, what conditions spurred the origin of because their forewings are remarkably leaf-like (Figure wings? To answer these questions, we must first consider how 7.26); in other groups the wings have gaudy patterns to wings function. 155 CY501-C06[155-187].qxd 2/14/05 5:54 PM Page 156 quark11 27B:CY501:Chapters:Chapter-06: 156 EVOLUTION OF THE INSECTS 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 push- ing 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- 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 stroke, the wing is strongly tilted backward (i.e., supinated) most maneuvered flight of all animals. Photo: R. Swanson. 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) INSECT WINGS before reaching the peak of its upstroke and repeating the Wing Function process. By comparison to the downstroke, the upstroke is Detailed reviews of insect flight mechanics are provided by relatively fast so as to minimize the loss of lift. During all of Wootton (1992), Brodsky (1994), Grodnitsky (1999), Dudley this gyrating, portions of the wing foil may fold along their (2000), and Alexander (2002), with only the more salient lines of flexion, frequently generating vortices of air and points elaborated here. The complex system of membrane, additional lift or thrust. veins, flexion lines, and overall shape provides a strong but Numerous modifications of this generalized pattern occur lightweight, flexible structure that can change shape in a among insects, all associated with the peculiarities of flight controlled (but entirely passive!) way as it moves through air. among orders, families, or species. Highly maneuvered flight To achieve flight, all flying animals must produce lift and is made possible by synchronizing the two pairs of wings, and thrust. Lift is the force that raises the insect off the ground, many orders have developed mechanisms for linking the while thrust is the force moving the insect either forward or wings in flight (e.g., Hymenoptera, Lepidoptera), or even by backward. The wings form what is called an air foil. This is virtually dispensing with one pair of wings (e.g., Diptera). The owing to a slight convex curvature to the overall wing surface Odonata are noteworthy exceptions because the forewings with a concave or flat ventral surface. The degree of curva- and hind wings are out of synchrony. The forewing generates ture is the wing’s camber: A low camber is weakly convex on vortices that are captured by the hind wing in hovering flight the top, while a high camber is strongly convex on top. As air (see the section on Odonata for more details). moves over the surface of the wing, it moves slightly faster The powerhouse of insect flight, alluded to before, over the convex surface than it does the ventral, concave involves the indirect flight muscles. These consume almost all surface. This generates an area of lower pressure on the of the available space in the pterygote thorax and do not pull upper surface of the wing (i.e., Bernoulli’s principle) creat- directly on the wing for generating the up- and downstroke of ing a force that lifts the wing, and thereby the remainder of flight (hence their name as indirect). Instead, the muscles are the insect, into the air. The air speed and camber of the wing attached such that contractions deform the overall shape of are critical for determining the amount of lift that is created. the entire thorax, causing the notum and pleuron to push on While the overall body of the wing is a passive actor in flight, the base of the wing and move it up and down. The upstroke muscles pulling on the pteralic plates and epipleurites at is generated by a series of dorsoventral muscles that pull the base of the wing alter its tilt in the air stream. As a result, down on the notum during a contraction. The notal wing insects fly by maneuvering the wings in a convoluted figure- processes thereby press downward on the leading and poste- eight motion where the costal edge leads, not by merely rior edges of the wing base and cause the wing to move flapping the wings up-and-down as is typically supposed. upward on the pleural wing process, which provides a pivot By tilting the leading edge of the wing downward, an insect point from below. The downstroke is generated by the dorso- can alter its angle of attack relative to the air stream. The longitudinal muscles running lengthwise through the thorax.