The evolution of animal flight understanding a major transition in ecology

There is now little doubt among most biologists that birds derive from a group of theropod dinosaurs. The theropods were a bipedal carnivorous group that share many anatomical features with birds. A series of recent fossils, most notably from Liaoning province of China and described by Xu Xing and colleagues, include therapods with epidermal feather-like structures that we might collectively refer to as 'fuzz'. They were pre-adapted for flight through a fast cursorial predatory lifestyle. This resulted in a shortening and stiffening of the tail, reduction in the size of the midbody, lengthening of the raptorial arms, swivel-wrist joint, light hollow bones, and a reduction in body size (Sereno 1999).

What subsequently happened? There are several ecological scenarios. The arboreal hypothesis states that birds evolved from ancestors that lived in trees and gained the ability to glide from tree to tree. Arboreal gliding organisms are common today, and in general provide a plausible intermediate stage to flight because the energy for lift is supplied by gravity. The discovery of Microraptor ghui, with its apparently four gliding limbs (Xu et al. 2003), has recently renewed interest in this scenario. However, theropods were primarily bipedal ground dwelling runners and this has also focussed attention on a possible cursorial origin. By flapping their forearms as they ran, rather like a swan taking-off from water, therapods could have increased their running speed by taking weight off the hind legs, allowing the hind legs to provide more forward thrust. In this way the wings would gradually take over from the hind legs until both lift and forward thrust could be provided by the wings alone (Burgers and Chiappe 1999).

Other more complex scenarios have been also proposed. Garner and co-workers (1999) have suggested the 'Pouncing Proavis' hypothesis. They envisage therapods dropping onto prey from a perch, in the manner of modern owls and buzzards. The forearms could have assisted balance and the feather surface would develop initially to control the drop, rather than provide lift. Selection for greater horizontal range of drop (a swoop, involving lift generation) could then have transformed the role of the wing. Like the cursorial hypothesis this retains the functional distinctiveness of the fore-and hindlegs since both have separate roles, which is less likely in an arboreal origin. Another possible scenario (Dial 2003) is that wing flapping developed to assist therapods to climb to elevated refuges, such as trees or bolders, as it is still used today in birds, such as quails and chickens, even in their flightless chicks.

If birds developed flight from bipedal and basically ground-dwelling ancestors, what of insects? There is intriguing evidence that insect wings may have developed from leg segments supporting gills that originally developed along the length of the body. Some fossil mayfly nymphs possessed these, and the thoracic ones would then be homologous with modern wings (Kukalova-Peck 1978). In modern insects, genes are present that switch off the development of these structures in all but the wing segments, but the potential to form wings is present in every segment (Carroll et al. 1995). But how could an aquatic gill come to function as a wing? Some mayflies and stoneflies use their wings in a unique way (Figure 3.2): to sail or skim across the water surface to reach land after emerging as adults onto the water surface (Marden and Kramer 1995). Close to the water's surface,wing beating provides more power because the air is compressed between the wing and the water. The aquatic skimming origin therefore postulates ancestral apterygotes and pterygotes having aquatic larvae with moveable gills, and air-breathing adults. Retaining gills through to the adult stage aided sailing to land, and selected for larger but also fewer structures to aid directional stability. Skimming developed further speed and control via flapping, and eventually

Fig. 3.2 This male stonefly, Allocapnia vivipara, is flightless but has raised its short wings to sail across the water surface to dry land. Flight in insects may have originally evolved through such a stage. Photo courtesy of Jim Marden.

adults were created that were fully capable of flight. The hypothesis provides an explanation for the somewhat mysterious observation that while the primitive wingless insects and most derived insects are terrestrial, the extant primitive winged insects (mayflies and dragonflies) all retain aquatic larvae.

The origins of bats and pterosaurs are much more obscure. Neither have clearly identifiable fossil ancestors, nor do transitional fossil forms exist. In both taxa the flight membrane and lack of cursorial hind legs are much more suggestive of an arboreal gliding ancestor than for the birds and insects (Figure 3.3). Some candidate pterosaur ancestors may have been bipedal however, and bipedality was certainly common among the stem archosaur groups. In the bats, most scenarios envisage a nocturnal, arboreal, and insectivorous ancestor for the following reasons: the hind limbs help support the flight membrane (Figure 3.3), making a cursorial ancestor very unlikely; all bats are nocturnal hence that is a likely ancestral state; and the ancestral eutherians were doubtless insectivorous. Recently, Speakman (2001) has proposed an alternative hypothesis: that of an arboreal, diurnal, frugivorous ancestor. The advantage of this hypothesis is that one can imagine the ancestral bat leaping from branch to branch using vision effectively for foraging. Some then developed insectivory, and all were forced into nocturnality to escape raptorial birds, after which fruit bats specialized the visual system, and the microbats the echolocation system. There is agreement that the setting was arboreal and gliding, but beyond this many scenarios are possible. The origin arguments presented above are summarized in Table 3.1. It is exciting that of the three extant flying taxa, three completely different evolutionary scenarios may have played out.

Fig. 3.3 A lesser mouse-eared bat, Myotis blythii, taking to the air. Note the short hind limbs and flight membrane stretching from the forelimbs to the hind limbs. This is very un-bird-like and reminiscent of a quadrupedal glider. No bats have become flightless. Photo courtesy of John Altringham.

So we can imagine plausible scenarios for how these origins may have happened. Why to these organisms though, and why at those moments in time? There are dozens of gliding animals in today's forests: why have they not all developed powered flight? Have they simply not hit on the necessary mutations to transform a gliding animal into one with powered flight? It is unlikely. Our evolutionary understanding of the transitions involved is that they have been of a continuous nature, with small change building upon small change. This is well illustrated by the fossil record for bird evolution. None of the changes involved can be seen as particularly remarkable. Furthermore,birds, insects, and bats all have a different flight apparatus suggesting that selection can work through multiple routes. More likely then, specific external influences may be necessary. Recently, Dudley (2000) has championed the view that increases in atmospheric oxygen concentration may have facilitated the origins of powered flight. The Late Carboniferous period, characterized by the first pterygote insect fossils, represented the historical peak in Earth's oxygen concentration, about double that of today. The Mesozoic era, characterizing the origins of pterosaurs and birds, was a period of increasing oxygen concentration, reaching a secondary peak in the Late Cretaceous, reducing somewhat since. This secondary peak coincides

Table 3.1 Hypotheses on the origins of flight

Group

Who

What

Where did it

Why did it

Controversies

changed?

changed?

change?

change?

Pterygote

Apterygotes

Larval gills

Newly

Improved

No consensus

insects

with aquatic

derived from

emerged

speed over

on the origins

larvae

pleural

adults sailing

the water

of wing

structures

or skimming

surface

structures, or

became wing

over the water surface

on aquatic apterygote ancestors

Pterosaurs

Unknown

Gliding

Arboreal

Improved

Absence of

basal

membrane

setting

distance and

any fossil

archosaur

supported by a finger became wing

control of glide

ancestors makes this an open question

Birds

Feathered

Feathered

Cursorial

Flapping

Primarily

dromeosaurs

forearm became a wing

setting

aids running speed by providing life

about the ecological setting and reasons for change

Bats

Unknown

Gliding

Arboreal

Improved

Absence of

basal

membrane

setting

distance and

any fossil

eutherian

supported by fingers became wing

control of glide

ancestors makes this an open question

with the origins of flight in vertebrates. High oxygen concentrations would have two important effects: first, they would have increased the density of the air, and the flight surface would thus provide more lift. Second, they would increase metabolic capacity and hence provide more power per effort. Since flight is energetically expensive, slight increases in power and lift might have been sufficient to turn net cost into net benefit. Rather interestingly, changes in oxygen concentration may have been stimulated by other evolutionary transitions, such as the increase in productivity due to terrestrialization. Recently, Lenton et al. (2004) have suggested that a chain of such events might have occurred in the history of life, with evolutionary changes giving rise to environmental changes, which in turn give rise to evolutionary changes.

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