Evolution of flight in animals U.M. Lindhe Norberg Department of Zoology, University of Göteborg, Sweden. Abstract The evolution of flight in animals has long been debated and different hypotheses have been suggested for their origins. Controversial opinions about morphology, locomotion and flight evo- lution can, however, be understood by functional approaches, e.g. by biomechanical treatments and aerodynamic models. New fossils of proto-fliers will constantly increase our understanding of how animals evolved flapping flight. Insects may have developed powered flight via ‘surface- skimming’ on water as used by stoneflies and mayflies. Articulated, movable gill-plates were used for underwater swimming and for circulating water over the gills in aquatic nymphal stages of non-flying insects. They were later raised above the water surface for wind-propelled skim- ming, and beating of the winglets enabled powered skimming. Eventually, flight muscles became stronger and were used for true powered flight. Vertebrates most probably developed flapping flight via gliding intermediates. The conflicting ‘ground-up’ model includes a number of limi- tations. Several modifications of the various evolutionary steps in the main theories have been suggested, but particular stress has been laid on whether a gliding stage was included or not. In terms of energy, time, and aerodynamics, the gliding model is the most attractive alternative. If the ground-runner began to use hang-gliding on steep slopes, a running mode of life before the animal could fly would be beneficial. Morphological changes must have evolved in small steps over a long time span, and each new modification towards flight must have contributed to fitness long before the proto-flier could fly. 1 Introduction Flight is one of the most demanding adaptations found in nature because of the physical problems of moving in air. Therefore, fliers in nature have been subjected to strong selection for optimal morphology to increase flight performance and to minimize flight costs. The characteristics of flying animals are low total mass, large surface area and rigidity of wings. Their wings must meet the requirements of strength and rigidity with least possible mass, and their wing form must be coupled with particular flight modes. WIT Transactions on State of the Art in Science and Engineering, Vol 3, © 2006 WIT Press www.witpress.com, ISSN 1755-8336 (on-line) doi:10.2495/1-84564-001-2/1c Evolution of Flight in Animals 37 The crucial thing in the evolutionary pathway to powered flight is the production of lift and thrust. While aircraft produce thrust with the engine, animals have to flap their wings. The most important parameter affecting the lift and drag coefficient over the entire size range of flying animals and machines is the Reynolds number, which represents the ratio of inertial to viscous forces in a flow. It is Re = ρul/µ, where ρ is the density, µ is the viscosity of the flow, u is the speed and l is a characteristic length (such as wing chord). Low Reynolds number flight and flapping wing dynamics, which are characteristics of animal flight, involve large-scale vortical motion and detached flows. This is why the Strouhal number enters as a second important parameter for the dynamics (a dimensionless value useful for analysing oscillating, unsteady flow and which is a function of the Reynolds number; St = ωa/u, where ω is the oscillation frequency and a is the amplitude, such as wingtip excursion). A flexible wing has superior performance to a rigid aeroplane wing in this situation. An important benefit from flapping wings of animals compared to fixed-wing aircraft is that animals can manoeuvre better and also make compensating wing movements to avoid stall. Animals can also change wing form to meet different flight conditions and requirements. Insects make up the most diverse and numerous animal class with about 750 000 recorded species. Tiny insects operate at Re < 10 and larger insects at Re ≈ 102 −104.At very low Reynolds numbers viscous forces are large and the flow is more laminar, whereas inertial forces increase with increasing size and speed. Birds comprise more than 8000 species and bats about 1000 species. Their Reynolds numbers vary between 104 and 105, whereas the range for aircraft usually is 106–108. If birds only appeared as fossils we would probably have placed them among the class Reptilia. They would have formed another reptile group that could fly. If pterosaurs were alive today, we may have put them a separate class, like birds, and separate from reptiles. But birds are more different from reptiles than pterosaurs, because they have wing feathers. Long fingers and a flexible membrane make up the bat wings, and it is still debated whether the pterosaur wing was made of a flexible membrane or stiff keratin material, or both. 2 Evolution of insect flight Several theories have been suggested for the origin of flight in insects (summarized in Thomas and Norberg [1]). An early theory is that insects evolved flight by jumping and gliding down from trees, like early birds and bats [2–4]. Flattened outgrowths at the top of the thorax allowed insects to maintain stable flight. Progressively increasing size of the extensions improved glide angle, they became moveable, and incipient flapping eventually led to powered flight, as in the vertebrate model [3, 4]. A second theory suggests that evolution of insect flight may have originated with relatively large, terrestrial, leaping insects, which launch themselves voluntarily into the air, as many modern insects do [5]. Winglets, which were of help, progressively increased for stability, then gliding, partially powered flight, and eventually fully powered flight. The ‘floating hypothesis’ [4–6] suggests that dorsal extensions in tiny insects aided dispersal by convectional air currents and eventually evolved to flapping wings. Kingsolver and Koehl [7] suggested that flaps first evolved for thermoregulation. The most interesting scenario for the evolution of flapping flight in insects, presented by Marden and Kramer [8, 9] and illustrated in Fig. 1, is that powered flight developed via ‘surface-skimming’ on water. Stoneflies and mayflies, for example, often use water-skimming, which could thus be one stage in the origin of flight. Fossil and developmental evidence indicate that insect wings are WIT Transactions on State of the Art in Science and Engineering, Vol 3, © 2006 WIT Press www.witpress.com, ISSN 1755-8336 (on-line) 38 Flow Phenomena in Nature Figure 1: Probable steps in the evolution of insect flight according to the ‘surface-skimming’ hypothesis [1, 2]. Top: Articulated, movable gill-plates were used for underwater swim- ming and for circulating water over the gills in aquatic nymphal stages of non-flying insects. Bottom left: The plates were later raised above the water surface for wind- propelled skimming, and beating of the winglets enabled powered skimming. The figure shows a male stonefly sailing. Bottom right: Female stonefly sailing. The bottom drawings are based on photographs by Marden and Kramer [9]. homologous to specific epipodites (gills, with respiratory function) of crustacean limbs (traced by gene expression; [10, 11]). Steps leading to flight could have been: (1) articulated, movable gill-plates were used for underwater swimming and for circulating water over the gills in aquatic nymphal stages of non-flying insects; (2) gill-plates, functioning as winglets, were raised above the water surface for wind-propelled skimming; (3) beating of the winglets enabled powered skimming; (4) the flight muscles became stronger and used for true powered flight. This hypothesis makes the gill-to-wing transition possible. Modern stoneflies, which are an ancient group that differs little from their Carboniferous ancestors, use skimming in this way and might be regarded as a functional intermediate form. In surface-skimming there are three sources of water drag: (1) friction between leg and water surface film, (2) inertial drag due to continuous acceleration of water out of the moving dimples as the insect skims on, and (3) inertial drag due to the generation of ripples. The weight of the displaced water from the dimples matches the weight of the insect. Thomas and Norberg [6] suggested that the transition from surface-skimming to true powered flight would be greatly enhanced by the ground-effect; reduction of the aerodynamic induced power could be reduced by 50% just after take-off from water. 3 Evolution of vertebrate flight 3.1 Up–down or down–up? In his comprehensive book The Origin and Evolution of Birds Feduccia [12] summarized and treated the different theories of the origin of flight in birds. Most aspects of early birds were also WIT Transactions on State of the Art in Science and Engineering, Vol 3, © 2006 WIT Press www.witpress.com, ISSN 1755-8336 (on-line) Evolution of Flight in Animals 39 discussed in 1999 at the International Symposium in honour of John H. Ostrom in New Haven, Connecticut [13]. Powered flight in birds, as well as in pterosaurs and bats, may have evolved via gliding in tree- living animals, as described by the arboreal (‘trees-down’) theory [12–25], or from hang-gliding on steep slopes [26] (Fig. 2). Morphological changes must have evolved in small steps over a long time span, and each new modification towards flight must have contributed to fitness long before the proto-flier could fly [15–17]. Whether birds evolved flight via a gliding stage (starting from some height or slope) and working with gravity, or from a running cursor, working against gravity, is still intensely debated. Several modifications of the various evolutionary steps in the main theories also are suggested but particular stress has been laid on whether a gliding stage was included or not, and also on the climbing ability in ancient birds.