How Did Flight Evolve? Four Separate Solutions to the Same Problem

Insects got there about 325 million years ago, at least a hundred million years before anything else, and how remains the least settled of the four. Their wings are not modified limbs, which is what makes the case difficult: they are outgrowths of the body wall, so there is no intermediate structure to look for in the way there is for a vertebrate arm. Two main hypotheses compete, one deriving the wing from the gill plates of an aquatic ancestor, supported by developmental genetics showing shared genes between wings and the gill-bearing appendages of crustaceans, the other from the side lobes of the thorax, used first for gliding or for gathering warmth. A third possibility now favoured by some researchers is that both are correct and the wing is a composite of two tissues. Whatever its origin, the result was extraordinarily successful, and for a hundred million years insects were the only things in the air, which is when they reached the sizes seen in the Carboniferous.

The first flying vertebrates appeared in the late Triassic, around 220 million years ago, and their wing is a membrane stretched between an enormously elongated fourth finger and the body, anchored down to the ankle. The membrane was not simple skin: it contained stiffening fibres, muscle and blood vessels, and could be tensioned actively, which made it an adjustable aerofoil rather than a passive sheet. Their bones were hollow and pneumatised, invaded by air sacs from the lungs in the way a bird's are, giving strength at very low weight, and the largest species, Quetzalcoatlus and its relatives, stood as tall as a giraffe with wingspans over ten metres, making them the largest flying animals that have ever existed. How something that size took off was long a puzzle, and the current answer is a quadrupedal launch in which the animal vaults off its folded forelimbs, which are far more powerfully muscled than a bird's and act like a pole vault. They died out completely at the end of the Cretaceous, leaving no descendants.

The bird wing is the best documented transition in the fossil record, because the feathers came first and had other uses. Feathers appear in dinosaurs that could not fly, beginning as simple filaments for insulation and developing into branched and then vaned structures used for display and for covering eggs, so that by the time anything was flying, the aerofoil already existed. The sequence assembled over tens of millions of years:

• •Filamentous feathers for insulation, present in many theropods and probably ancestral to the whole group
• •Vaned, asymmetric feathers, whose asymmetry is a signature of aerodynamic function, on arms and in Microraptor on the legs as well
• •A hinged wrist that folds the hand against the body, which evolved for prey capture and turns out to be the flight stroke's foundation
• •Hollow bones, air sacs and a one-way respiratory system inherited from theropod ancestors
• •A keeled breastbone and enlarged flight muscles, which arrive late and mark the transition to sustained powered flight
• •Loss of teeth, a shortened tail fused into a stub and a reduced body size, all of which came after flight rather than before

Bats are the only mammals that fly and they did it differently again, stretching a membrane between hugely elongated fingers, so that where a pterosaur used one finger a bat uses four. The membrane is living skin with muscle fibres, sensory hairs that detect airflow and a blood supply, and it is more manoeuvrable than a feathered wing, though more vulnerable to tearing and to heat loss. Their origin is the worst documented of the four: the oldest known fossils, from Wyoming and around 52 million years old, are already fully formed bats capable of flight, and Onychonycteris, described in 2008, is the most primitive known and still has complete wings, though it lacks the ear structures for echolocation, which settles at least the order of those two developments. Small, fragile, forest-dwelling animals fossilise badly, so the transitional forms are simply missing. Bats then diversified enormously and now account for roughly a fifth of all mammal species.

The long argument about how flight begins has been run mostly about birds and applies to all of them. The arboreal hypothesis has an animal climbing, leaping and gliding, with each increment of surface area improving the glide, which has the advantage that gravity supplies the energy and that gliding has evolved dozens of times, so the intermediate stages are demonstrably viable. The cursorial hypothesis has a running animal flapping to gain speed and lift, and was long criticised because the intermediate stages seemed useless. A third proposal, wing-assisted incline running, described by Kenneth Dial in 2003, may have resolved it: young game birds that cannot yet fly flap their partial wings while running up steep surfaces, and the flapping presses them against the slope rather than lifting them, which lets them climb trees and escape predators. Every increment of wing helps immediately, which is exactly what the objection required, and the behaviour is observable in living birds today.

Powered flight evolved four separate times, in insects around 325 million years ago from body wall outgrowths of disputed origin, in pterosaurs from a membrane on one enormously elongated finger, in birds from feathers that already existed for insulation and display, and in bats from skin stretched across four fingers. Gliding has evolved dozens of times, which suggests the intermediate stages are easy. The best current account of how flapping begins is wing-assisted incline running, observed in living game bird chicks, where every increment of wing pays immediately.