Evolution Of Flight

Although many features have contributed to the radiation of insects in terrestrial ecosystems, the evolution of actively powered flight is almost certainly the key innovation responsible for their remarkable success. The relative abundance of extant winged (ptergygote) insects to wingless (apterygote) insects (a ratio of at least 500,000:1 in species richness) manifests the potent advantages of flight. Although the selective advantages of flight are obvious, the means by which ancestral hexapods evolved wings and associated flight behavior are not. Because flight is such a specialized form of behavior and is associated with morphological and physiological traits that represent extreme forms of the basic arthropod body plan, reconstructing the series of functional intermediates between flightless ancestors and flying insects continues to pose a challenging problem. The evolution of flight involves two distinct, but overlapping, questions. First, what is the morphological structure from which wings arose? And second, what suite of selective forces drove the evolution of wings as aerodynamic structures?

Morphological Origin of Wings

The morphological origin of the wing in pterosaurs, birds, and bats is unequivocal; in all these animals it arose from a modification of the forelimb. Insect wings are novel structures, at least in the sense that they are not homologous with the legs. Biologists have long debated which structure served as the anatomical precursor of insect wings. Of the various theories that have been proposed, the dominant view until recently was that wings arose from rigid lateral extensions of the notum. Such a scenario seems at first plausible, given the structural plasticity of the thoracic exoskeleton in extant insects. When considering function of flight morphology as a whole, however, the most complicated feature of the wing is not the flat distal blade that serves as the aerodynamic surface, but rather the complicated hinge with its associated muscle attachments that enables the wing to flap and rotate during the stroke. Over the past 15 years an alternative hypothesis, that the wings evolved from basal branches of the leg, has emerged from work in a number of disciplines. This theory owes much to the work of the paleontologist Jarmila Kukalova-Peck, who challenged the widely held view that insects, as distinct from other arthropods, possess unbranched limbs. According to her alternative view, the ancestors of winged insects possessed biramous appendages and used a developmental-genetic program for limb development that they shared with crustaceans and other arthropods. The structure that gave rise to the wing may have been a dorsal branch, or exite, of a precoxal segment of the leg called the epicoxa. Whereas the epicoxa has been lost or incorporated into the pleurum of the thorax, its exite has been retained as a wing. However, rather than classifying the wings of extant insects as direct morphological homologues of epicoxal podites in ancestral apterygotes, it may be more precise to view both as arising from homologous morphogenetic programs. The leg podite theory of wing origin solves an enigmatic step in the evolution of functional wings, the formation of the wing hinge and its complex arrangement of muscles. As a leg branch, the protowing would have been endowed with joints and muscles long before it ever took on an aerodynamic role. Further, because legs are replete with various mechanosensory structures, the protowing would have inherited the campani-form sensilla, stretch receptors, or chordotonal organs that may have mediated the reflexes and motor patterns that presumably served as the foundation of flight control circuitry. Although several lines of evidence support a leg podite origin for insect wings, this intriguing issue is far from resolved and the consensus may change with additional fossil evidence and further comparative studies of arthropod development.

Functional Origin of Flight Behavior

Hindered by the inherent difficulty of extracting behavior and physiology from fossil evidence, the functional origin of flight remains enigmatic. The fact that wings arose from small structures poses the same problem that Darwin first recognized for all organs of great complexity—it is difficult to reconstruct a series of functional intermediates between a tiny leg podite and an aerodynamic surface capable of sustaining active flight. The aerodynamic performance of a wing increases with length and surface area. Thus, a small wing is incapable of generating enough force to sustain active flight. Without a selective pressure driving the wing to larger sizes, how did the structure initially attain the size required to support active flight? It is unlikely that any single selective pressure was responsible for the hypertrophy of the wings. For example, if the direct ancestors of pterygotes possessed an aquatic nymph stage, protowings might have served as gill covers or respiratory paddles. Given the high density and buoyancy offered by an aquatic medium, it is even possible that wings may have functioned as hydrodynamic structures for underwater propulsion. However, no matter what role they may have played in the aquatic stage of life history, the use of wings in air would necessitate a substantial increase in size.

Hypotheses attempting to explain the early selective engine for true aerial flight segregate into two basic types. One set of hypotheses suggests that early selective pressures for an increase in wing size had nothing to do with aerodynamics per se, but rather with some other size-dependent selective force. For example, the use of wings as reflectors and conduits in basking butterflies has led to the proposal that wings first served a thermoregulatory role. Other possibilities include the use of wings in sexual displays or copulatory offerings by males. The second set of hypotheses asserts that protowings functioned aerodynamically before they were large enough to support active flight. For example, small wings might serve to increase glide angle or offer added stability during controlled descents. The utility of small protowings in gliding behavior might have been enhanced by their serial repetition, and fossil evidence indicates that pro-towings were present on the prothorax and abdominal segments in some groups of early insects. Vegetation and surface topography would have served as the most convenient launching points for gliding or parachuting insects. Another possibility is that protowings may have prolonged jumps, thereby serving as an important anti-predator behavior in response to the coevolutionary radiation of terrestrial predators at the time. Recently, James Marden suggested that protowings may have served as aerodynamic structures used to either sail or flutter insects across the surfaces of streams and ponds. This intriguing hypothesis is based on the behavior of extant stoneflies that skim across streams in this manner when the temperature is too low for their flight muscles to generate sufficient mechanical power to sustain flight. The atmospheric composition at the time, in which both oxygen levels and air density were elevated by today's standards, might also have aided the transition to active flight (see later). Whatever selective pressures led to the evolution of flight, analyses of insect phylogeny strongly suggest that flight evolved only once within the clade. However, no behavior that has been proposed as a model for ancestral pterygotes, such as sun basking or surface skimming, maps into the current phylogeny in a way that is entirely consistent with it being an ancestral trait. With no definitive means of excluding any of the proposed scenarios, the functional origins of insect flight are likely to remain alluring, controversial, and unresolved for years to come.

AERODYNAMICS Conventional Aerodynamics

The scientific study of insect flight is haunted by the widely told story of an engineer who proved that a bumblebee could not fly. Although the flight of insects is indeed more complicated than that of airplanes, the underlying physics is nevertheless fully explicable within the rubric of modern fluid mechanics. To understand how insects fly by flapping their wings, it is useful to first consider the means by which fixed-wing aircraft create aerodynamic forces. The design of conventional airplanes is based on the steady-state principle that the flow of air around the wings and the resulting forces generated by that flow are stable over time. As the wing of a plane moves through the air, it meets the oncoming flow at a small inclination, termed the angle of attack. As the flow of air approaches the leading edge of the wing, it divides into two streams on the undersurface of the wing. Because of the viscous behavior of air (a general property of all "fluids," including liquids and gases), the two streams meet again smoothly at the sharp trailing edge. For the flow to separate under the wing, but meet again at the trailing edge, the upper stream must travel faster than the lower because it covers a greater distance. By Bernoulli's principle, this higher velocity generates lower pressure, which sucks the wing upward producing lift.

Although the explanation of flight based on Bernoulli's principle is sufficient for simple situations, engineers and physicists often use a mathematical transformation to quantify the velocity difference above and below the wing and analyze more complex situations. Subtracting the background flow caused by the speed of the airplane from the local flow near the wing uncovers a net circular movement of air around the wing called vorticity. Cohesive filaments or loops of vorticity are called vortices, a term that also applies to more familiar flow structures such as tornadoes, whirlpools, and smoke rings. Although the net circular flow of air around a wing is a mathematical abstraction, wings are, in effect, vortex generators. At a low angle of attack a wing creates a bound vortex, so named because the center of vorticity is located within the wing. The Kutta—Joukowski theorem, perhaps the most essential equation in aerodynamics, states that the lift generated by each section of a wing is proportional to the strength of the vorticity it creates, a quantity termed circulation. The simplest way of increasing the amount of circulation, and thus the lift, is to increase the angle of attack. At angles of attack above about 10°, however, the flow over the top surface separates as it rounds the leading edge, resulting in a catastrophic loss of lift known as stall. For a wing operating according to conventional aerodynamics, the stall angle places an upper limit on the amount of stable circulation, and thus lift, that a wing can continuously generate. Early analyses of insect flight aerodynamics applied conventional steady-state theory unto the complex motion of flapping wings. This approach, termed quasi-steady theory, is equivalent to "freezing" the wing at one position within the stroke cycle and then testing it at that particular velocity and angle of attack in a wind tunnel under steady flow. If conventional theory were sufficient, then a series of such measurements repeated for each point in the stroke cycle should sum up to the animal's body weight. In most cases such simple quasi-steady approaches cannot account for the forces required to sustain flight, indicating that unsteady aerodynamic mechanisms play an important role in insect flight.

Scaling Parameters

Before discussing such mechanisms in detail, it is useful to introduce two important parameters that help organize the great diversity of flight patterns in insects. The first term, the Reynolds number, quantifies how changes in body size, wingbeat frequency, and atmospheric conditions affect aerodynamic mechanisms. The wing or body of an insect encounters two forces as it moves through the air, a shear force caused by fluid viscosity and an inertial force from the fluid momentum. The dimensionless Reynolds number is simply the ratio between these two forces and, for insects, is equal to the product of wing velocity, wing length, and air density divided by air viscosity. Reynolds numbers vary among insects from about 10 for the tiniest to 10,000 for the largest insect. At high Reynolds numbers, the inertial behavior of the air dominates and wings generate pressure forces acting perpendicular to their surface. At a Reynolds number less than 1, a viscous shear force dominates, acting parallel and opposite to the direction of motion. Recent measurements of force production by flapping wings indicate that aerodynamic performance is remarkably constant across a range of Reynolds numbers spanning from about 100 to 5000—encompassing the operating range of most insects. Nevertheless, miniaturization is a common theme in insect evolution, and many species are so small that viscous forces, if not dominant, are large enough to greatly influence force production. The functional peculiarities of lower Reynolds numbers are manifest in the unique wing morphology of the smallest insects, including the brush-like wings of thrips and the whip-like wings of some miniaturized beetles. Although the kinematics used by these tiny insects is as yet unknown, it is possible that they flap their "wings" in such a way as to generate an excess of viscous drag during the downstroke, akin to the power strokes of aquatic plankton. Reynolds numbers are also used to construct large mechanical models of flapping insects for the purpose of directly measuring aerodynamic forces and visualizing flow. This technique, termed dynamic scaling, is based on the principle that the fluid-based forces acting on two geometrically similar but different-sized objects are the same as long as the Reynolds numbers are identical.

Another important dimensionless parameter, called the advance ratio, is useful in coarsely assessing whether conventional steady-state aerodynamics is sufficient to explain force production. The advance ratio is simply the animal's airspeed divided by the flapping velocity of its wings. At one extreme, an infinitely high advance ratio indicates that an animal is gliding, and all the air flowing past the wings derives from the motion of the body as a whole, which is a condition amenable to conventional steady-state aerodynamics. Even if the wings flap up and down, steady-state approximations may be valid as long as the forward speed is substantially greater than the velocity of the wings. The situation is much more complicated for hovering or near-hovering conditions, in which the insect is essentially stationary and most of the airflow encountered by the wings is generated by their back-and-forth motion. Under these conditions, the flow of air around the wing changes substantially throughout the stroke, and the analysis of aerodynamic forces is more complex. Low advance ratio flight is typical of many insects, particularly those of small body size, and is characterized by a motion in which the wings flap back and forth in a roughly horizontal plane. During the two strokes (somewhat inappropriately named the downstroke and upstroke), the wings translate through the air at high angles of attack creating elevated vorticity. At the end of each stroke, the wings rapidly flip over such that the dorsal surface of the wing faces upward during the downstroke, and the ventral surfaces faces upward during the upstroke. As it flips, the wing sheds the vorticity it created in the previous stroke, thereby adding to a complex vortex wake that forms underneath the stroke plane akin to the downwash beneath a hovering helicopter. Thus, at the start of each stroke the wing travels not through still air, but through its own wake. These three peculiarities of wing motion during flapping flight, (1) the high angle of attack during translation, (2) the rapid rotation between strokes, and (3) the influence of the wake on subsequent flow of air around the wings, all profoundly influence the manner by which insects create and modify aerodynamic forces.

Aerodynamic Mechanisms

The total force created throughout a stroke by a flapping wing may be conveniently separated into four main components: translational force, rotational force, wake capture, and inertial force (Fig. 1). Inertial force results from the acceleration of the wing back and forth during each stroke. Although the mass of the wings is small, the acceleration is great and the resulting inertial forces are substantial. Peak values during stroke reversal may be many times greater than the aerodynamic forces. However, because the flapping motion is largely sinusoidal, wing inertia averages close to zero over each stroke and thus does not contribute to the average forces acting on the body. Another component of inertial force derives from the acceleration of the air displaced by the wing as it accelerates, termed virtual mass. Although the precise volume of air disturbed by an accelerating or rotating wing is difficult to calculate, conservative estimates indicate that added mass inertia is relatively small compared with the wing mass inertia and other aerodynamic components. Thus, although wing and virtual mass inertia may complicate the

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