The History of Vertebrate Flight
d.w.rowlands [at] gmail.com
The following is the material I covered in a one-hour class for high school students as part of the MIT Educational Studies Program's Splash 2014.
While gliding vertebrates appear to have evolved independently a couple of dozen times, true powered flight has only evolved in three vertebrate lineages: first among pterosaurs in the late Triassic about 230 million years ago, then among the theropod dinosaur ancestors of modern birds in the late Jurassic about 160 million years ago, and finally among bats in the Eocene about 50 million years ago. There are some basic similarities of the flight techniques that each group developed---in each case wings developed from forelimbs---but there are also significant differences that have affected what niches they are best adapted for.
Powered flight requires a lot of energy and a fast metabolism, so it's not surprising that all three times that vertebrate flight evolved, it did so among animals that were already warm-blooded. While cold-blooded vertebrates never developed powered flight, both of the main lineages of warm-blooded vertebrates did.
During the Carboniferous period, around 325 million years ago, the early amniotes---vertebrates that had developed hard-shelled eggs that could survive on land and so were no longer tied to living parts of their lives in the water---divided into two main lineages, the synapsids and the sauropsids. A group of synapsids called therapsids arose about 275 million years ago and were the dominant land vertebrates in the Permian. They were also the first animals to develop warm-blooded metabolisms and related traits such as hair for insulation and upright gates that allowed them to breath while running. This trend towards better insulation and more regulated, faster metabolisms was accelerated when the Permian-Triassic mass extinction at the start of the Paleozoic eliminated most synapsids species except for small, nocturnal insectivorous therapsids whose sole living descendants are the mammals.
After the Triassic mass extinction, the therapsids were displaced as the dominant land vertebrates by a group of sauropsids that had also begun to develop warm-blooded metabolisms and upright gates: the archosaurs. The dominant group of archosaurs during the Triassic, the pseudosuchia, went extinct at the beginning of the Jurassic period with the exception of crocodilians, which became secondarily cold-blooded for greater efficiency in their niche as aquatic ambush predators but retained various archosaur traits. Meanwhile, an initially minor archosaur lineage that had developed into dinosaurs and pterosaurs in the mid-Triassic flourished for the rest of the Mesozoic. Pterosaurs were the first vertebrate group to develop flight, in the late Triassic. A group of theropod dinosaurs in the mid-Jurassic evolved flight separately and became the ancestors of modern birds. Meanwhile, the first flying bats did not evolve until the Eocene, 50 million years ago.
Breathing and Metabolism
Bats, birds, and pterosaurs all evolved from warm-blooded ancestors, and faster warm-blooded metabolisms are probably prerequisites for powered vertebrate flight. The details of how they support this metabolism are similar in birds and pterosaurs, whose ancestors diverged after becoming warm-blooded, while bats have fairly different approaches.
Bats, like all mammals, breath via what is called tidal respiration. Oxygen absorption occurs at dead-end sacs in the lungs called alveoli. This means that respiration involves a two part cycle of inhaling and then exhaling air through the same bronchial tube. A significant amount of air is wasted, since the air that fills tubes leading to the alveoli when the lungs are full will be expelled during the following exhalation without exchanging oxygen with the blood stream. Furthermore, since the lungs do not completely empty before the next inhalation, not all oxygen-depleted air will leave the lungs in a single respiratory cycle.
All archosaurs, including birds, pterosaurs, and the cold-blooded crocodilians, on the other hand, have a unidirectional respiratory system. Instead of dead-end alveoli, oxygen absorption happens in tubes in the lungs called atria that air is pushed through continuously during the respiration cycle. This flow is pumped by air sacs that act as bellows pushing air through the lungs, unlike the expansion-contraction cycle that mammal lungs are driven in by the diaphragm. Unidirectional respiration results in significantly less wasted air, since all air that enters the lungs passes through the atria. Because of this, bats with tidal respiration don't breathe as efficiently as birds and pterosaurs with unidirectional respiration, which limits the energy they can devote to flight. This more-efficient breathing is also likely what enabled sauropods to absorb enough oxygen despite the very long trachea required by their long necks.
Although they evolved them separately, mammals and archosaurs both have four-chambered hearts, unlike the three-chambered hearts of other reptiles. Three-chambered hearts allow some deoxygenated blood to pass through the circulatory system a second time before being sent-back to the lungs, which results in more efficient use of oxygen, since oxygen not taken up from the blood on the first pass may be on the second pass. Four-chambered hearts force all blood to return to the lungs after a single circuit through the body, which ensures a higher oxygen content for blood leaving the heart for the circulatory system. While four-chambered hearts seem to be essential for faster, warm-blooded metabolisms, crocodilians, which have become secondarily cold-blooded but are aquatic and benefit from being able to hold their breath for as long as possible have developed a bypass tube that lets them operate their hearts as though they are three-chambered when holding their breaths.
The small body sizes and fast, warm-blooded metabolisms that are necessary for vertebrate flight generally require insulation to avoid losing too much heat. By the time bats evolved, mammals had long had fur as a result of being the descendants of small, nocturnal, warm-blooded Mesozoic insectivores. Pterosaurs, on the other hand, seem to have evolved fur around the same time as flight, though the fossil record is sparse. And in the case of birds, small predatory dinosaurs seem to have evolved feathers for insulation and then discovered that they had aerodynamic properties that were useful for gliding and eventually flight.
While birds, bats, and pterosaurs all developed wings from specialized forelimbs, each one developed a significantly different wing structure with different effects on its flight capabilities. They also developed different ground locomotion strategies, with effects on how they can take off.
Bats appear to have evolved from tree-climbing mammals; their fossil ancestors already had longer forelimbs and fingers than hind limbs and toes, as is common in many tree-climbing and hanging primates before they developed flight. This is possibly related to the fact that bats have limited mobility on the ground and generally take off by dropping from a perch. It also make be connected to the specific structure of bats' wings: leather membranes stretched between four of their five fingers and their torsos. Having fingers splayed out along the length of their wings gives bats significantly more ability to control the shapes of their wings while in flight than birds and pterosaur wings allow. This, along with very sensitive pressure-detecting hairs on the surfaces of their wing membranes make bats much more maneuverable than birds, as they have much better ability to modify their aerodynamics rapidly. This allows them to fly in a jerky manner, changing direction rapidly to chase fast-moving insects, that birds can't imitate. It also means that nectar-eating bats can hover while beating their wings at only fifteen beats a second, while hummingbirds have to be smaller to be able to hover and need to beat their wings much faster, fifty to two hundred beats a second, and have much faster metabolisms, which bats with their tidal respiration likely couldn't match.
Pterosaurs, on the other hand, evolved from ground-dwelling ancestors and walked as quadrupeds when on the ground. Being quadrupeds meant that they could use all four limbs---including their powerful flight muscles---to leap into the air on take-off, making take-off from the ground easier for large pterosaurs than for birds of a similar size. Like bats, pterosaurs had wings consisting of skin membranes stretched between their forelimbs and fingers and bodies. However pterosaur wings were only connected to the pterosaurs' "little fingers", with the other digits used as claws and for walking. This allowed them to function as quadrupeds, unlike bats, which have only one claw on each wing, but means that they had much less control of wing shape than bats do, since they only had bone and muscle along the leading edges of their wings.
Birds' wings developed somewhat differently. It is not clear exactly how birds first took to the air. However, unlike both bats and pterosaurs, they clearly evolved from bipedal ancestors, coelurosaurian "raptor" dinosaurs, that used their forelimbs for grasping. Furthermore, unlike bats and pterosaurs---and most gliding vertebrates---birds don't use flaps of skin as their flight surfaces. Instead, they use feathers, which seem to have originally evolved as a form of insulation among theropod dinosaurs. Birds wings have arm bones and muscles along the leading edge with the rest of the wing solely constructed of feathers projecting from the arm. This dependence on feathers puts an upper limit on the size of bird wings, and thus the size of birds. Since feather shafts have a limited rigidity and are much more flexible than bone, they can only grow so long before they become too flexible to be useful for flight. In addition, while pterosaurs were quadrupeds that used their wings as forelegs, flying birds' wings are only usable for flight. This means that pterosaurs could use their flight muscles to launch themselves into the air, while birds must depend on leg muscles that are deadweight once they are in flight. This puts a constraint on the maximum size of birds and explains why the largest flying birds are significantly smaller and lighter than the largest pterosaurs.