Editor's Note: This story will be published in the December 2008 issue of Scientific American.

Survey the sky at twilight on a summer’s eve, and you just might glimpse one of evolution’s most spectacular success stories: bats. With representatives on every continent except Antarctica, they are extraordinarily diverse, accounting for one in every five species of mammal alive today. The key to bats’ rise to prominence is, of course, their ability to fly, which permits them to exploit resources that other mammals cannot reach. But their ascension was hardly a foregone conclusion: no other mammal has conquered the air. Indeed, exactly how these rulers of the night sky arose from terrestrial ancestors is a question that has captivated biologists for decades.

Answers have been slow in coming. This past February, however, my colleagues and I unveiled two fossils of a previously unknown species of bat that provides vital insights into this mysterious transformation. Hailing from Wyoming, the species—dubbed Onychonycteris finneyi—is the most primitive bat ever discovered. These fossils and others, together with the results of recent genetic analyses, have now led to a new understanding of the origin and evolution of bats.

Winged Wonder
To appreciate just how distinctive bats are, consider one of their trademark traits: wings. A few mammals, such as flying squirrels, can glide from tree to tree, thanks to a flap of skin that connects their front and hind limbs. And in fact, experts generally agree that bats probably evolved from an arboreal, gliding ancestor. But among mammals, bats alone are capable of powered flight, which is a much more complex affair than gliding. They owe this ability to the construction of their wings.

The bones of a bat’s wing consist of greatly elongated forearm and finger bones that support and spread the thin, elastic wing membranes. The membranes extend backward to encompass hind limbs that are quite a bit smaller than those of a terrestrial mammal of comparable body size. Many bats also have a tail membrane between their hind legs. A unique bone called the calcar projects from the bat’s heel to support the trailing edge of this membrane. By moving their fingers, arms, legs and calcars, bats can maneuver their wings in innumerable ways, making them superb fliers.

Most bats can also echolocate. By producing high-pitched sounds and then analyzing the returning echoes, these nocturnal animals can detect obstacles and prey much better than by using vision alone. (Contrary to the expression “blind as a bat,” all bats can see.) More than 85 percent of living bat species use echolocation to navigate. The rest belong to a single family—the Old World fruit bats, sometimes called flying foxes, which apparently lost the ability and instead rely strictly on sight and smell to find the fruit and flowers they feed on.

Echolocating bats have a distinctive suite of anatomical, neurological and behavioral characteristics that enable them to send and receive high-frequency sounds. Three bones in the skull have undergone modification. The first is the stylohyal, a long, slender bone that connects the base of the skull with an array of small bones—collectively termed the hyoid apparatus—that support the throat muscles and voice box. In most echolocating bats, the upper tip of the stylohyal is expanded into a kind of paddle that helps to anchor the hyoid apparatus to the skull.

The other two bones that bear the signature of echolocation occur in the ear. All mammals perceive sound by way of a chain of bones, known as ear ossicles, that transmit sound between the eardrum and the fluid-filled inner ear. The malleus is the first bone in this chain, and in echolocating bats it has a large, bulbous projection that helps to control its vibration. Once sounds pass through the ear ossicles, they travel to the inner ear, where they impinge on a coiled, fluid-filled structure known as the cochlea (Latin for “snail”) that contains special nerve cells responsible for sound perception. When compared with other mammals, echolocating bats have a cochlea that is enlarged relative to other skull structures, which makes them better able to detect high-frequency sounds and to discriminate among different frequencies of these sounds.

Which Came First?
The revelation more than 60 years ago that most of the world’s bats can “see with sound” made clear that echolocation contributed significantly to the great evolutionary success and diversity of bats. But which of the two key bat adaptations—flight and echolocation—came first, and how and why did they evolve? By the 1990s three competing theories had emerged.

The flight-first hypothesis holds that bat ancestors evolved powered flight as a way of improving mobility and reducing the amount of time and energy required for foraging. Under this scenario, echolocation evolved subsequently to make it easier for early bats to detect and track prey that they were already chasing in flight.

In contrast, the echolocation-first model proposes that gliding protobats hunted aerial prey from their perches in the trees using echolocation, which evolved to help them track their quarry at greater distances. Powered flight evolved later, to increase maneuverability and to simplify returning to the hunting perch.

The tandem-development hypothesis, for its part, suggests that flight and echolocation evolved simultaneously. This idea is based on experimental evidence showing that it is energetically very costly for bats to produce echolocation calls when they are stationary. During flight, however, the cost becomes nearly negligible, because contraction of the flight muscles helps to pump the lungs, producing the airflow that is required for intense, high-frequency vocalizations.

The only way to test these hypotheses about the origins of flight and echolocation is by mapping the distribution of relevant traits—wings and enlarged cochleas, for example—onto a family tree of bats to determine the point at which they evolved. Back in the 1990s, we simply did not have any fossils of bats that had some of these signature characteristics but not others.

Bat fossils are extremely rare. Ancient bats, like their modern counterparts, were small and fragile, and they tended to live in tropical habitats, where decay occurs very rapidly. Just about the only way a bat can become fossilized is if it dies in a place where it is swiftly covered with sediment that protects it from scavengers and microorganisms alike.

Until recently, the oldest and most primitive bat on record was the 52.5-million-year-old Icaronycteris index, named for the boy of Greek legend who flew too close to the sun. Icaronycteris was discovered in the 1960s in lake deposits in Wyoming’s famed Green River Formation, whose fine-grained mudstone and limestone rocks have yielded beautifully preserved fish, plants, mammals, insects, crocodiles and birds.

For the next four decades Icaronycteris formed the basis for understanding the earliest stage of bat evolution. Ironically, however, perhaps the most remarkable thing about Icaronycteris is just how much this ancient beast resembles extant bats. The shape of its teeth indicate that it ate insects, as do most bats today. Its limb proportions are similarly modern, with long, slender fingers, elongated forearms and diminutive hind legs. The creature’s scapulas (shoulder blades), sternum (breastbone) and rib cage also attest to a fully developed ability to fly. And it possessed the requisite anatomy for echolocation.

In fact, if it were alive today, Icaronycteris would be hard to tell apart from other bats. Its most distinctive feature is a tiny claw on the index finger (hence the species name index). Most bats retain a claw only on the thumb. Over time, the tips of the other four fingers were reduced to thin, flexible rods or nubs completely enclosed in the wing membrane. Icaronycteris’s index claw seems to be a holdover from a terrestrial ancestor.

Filling the Gap
In retrospect, Icaronycteris was never much of a “missing link.” But another fossil bat from the Green River Formation would turn out to fit that description nicely. Enter Onychonycteris. The two known specimens, unearthed by private collectors in the past decade and later made available for scientific study, were discovered in the same rock layer that yielded Icaronycteris and are thus considered to be of comparable antiquity. Onychonycteris, however, has a combination of archaic and modern traits that make it exactly the sort of transitional creature evolutionary biologists have longed for.

I was fortunate enough to lead the team that described and named O. finneyi. We chose the genus name Onychonycteris (“clawed bat”) because the fossil displays claws on all five fingers, just as its terrestrial predecessors did. The presence of these claws is not the only feature of Onychonycteris that recalls nonflying mammals. Most bats have very long forearms and tiny hind limbs. Onychonycteris, however, has proportionately shorter forearms and proportionately longer hind limbs than those of other bats. Compared with other mammals, the limb proportions of Onychonycteris are intermediate between those of all previously known bats (including Icaronycteris) and those of arboreal mammals that rely heavily on their forelimbs for locomotion, such as sloths and gibbons. These animals hang from branches much of the time as they climb around in the trees. Perhaps bats evolved from arboreal ancestors that used a similar form of locomotion.

Despite these primitive limb features, other aspects of the anatomy of Onychonycteris indicate that it was capable of powered flight. Its long fingers would have supported wing membranes, and robust clavicles (collarbones) would have helped anchor the forelimbs to the body. Meanwhile a wide rib cage and a keeled sternum would have supported large flight muscles, and a faceted scapula would have secured other specialized, flight-related muscles.

Additional clues to how Onychonycteris traveled come from the proportions of its arm and finger bones, which reveal that the animal’s wings had a very low aspect ratio and relatively small tips. Among living bats, only mouse-tailed bats possess similarly short and broad wings. These animals have an unusual gliding-fluttering flight style involving brief glides between periods of flapping flight. Our best guess is that Onychonycteris flew the same way. It may be that gliding-fluttering flight was the transitional mode of locomotion between the gliding of prebat ancestors and the continuous flapping flight seen in most modern bats.

Beyond illuminating how early bats flew, Onychonycteris has brought some much-sought-after evidence to bear on the debate over when flight and echolocation emerged. Unlike the other known bats that date back to the Eocene, the epoch spanning the time from 55.8 million to 33.5 million years ago, Onychonycteris seems to have lacked all three of the bony correlates of echolocation. It has a small cochlea and a relatively small protrusion on the malleus, and its stylohyal lacks an expanded tip. Yet features of its limbs and thorax clearly indicate that it could fly. Onychonycteris therefore seems to represent a stage in early bat evolution after flight had been achieved but before echolocation evolved. Fossils have finally given us an answer: flight first, echolocation later.

Ancient Diversity
The emergence of flight and echolocation set the stage for a dazzling adaptive radiation of bats. Such rapid periods of diversification are known to occur after a breakthrough adaptation. Living bats are classified into 19 families; fossil bats comprise an additional seven families. Remarkably, time-calibrated studies of the DNA sequences of multiple genes indicate that all 26 of these groups were already distinct by the end of the Eocene. This “big bang” of diversification is unprecedented in mammalian history.

Flight and echolocation certainly were not the only factors contributing to this radiation, however. The origin of these major bat lineages apparently coincided with a rise in mean annual temperature, a significant increase in plant diversity and a peak in insect diversity. From fast-flying beetles to caddis flies, cockroaches and tiny, fluttering moths, an aerial predator would have had a veritable buffet of insects from which to choose. And as the only nocturnal flying predators other than owls and nightjars, bats would have had few competitors for the rich resources of the Eocene night.

Fossils from a site called Messel in Germany provide a glimpse of this early diversification. Although at 47 million years old these fossils are only slightly younger than the bats from the Green River Formation, they are considerably more variable. Seven bat species have been found at Messel since scientific excavations began there in the 1970s, including two species of Archaeonycteris, two species of Palaeochiropteryx, two species of Hassianycteris, and Tachypteron franzeni, the oldest known member of a family of bats known as the Emballonuridae (the sheath-tailed bats) that is still alive today.

It is not hard to see why bats thrived at Messel. During the Eocene, it would have had a balmy climate, and it was home to several lakes surrounded by lush, subtropical forest. Judging from the abundance of their fossilized remains, thousands of aerial, aquatic and terrestrial insects were available for the taking. That, in fact, is just what the Messel bats did. All seven species were insectivorous, but each one specialized in a particular subset of insects, as evidenced by their preserved stomach contents. Whereas Palaeochiropteryx seems to have fed on small moths and caddis flies, Hassianycteris apparently favored larger moths and beetles. Archaeonycteris, on the other hand, may have only eaten beetles. As for Tachypteron, no stomach contents are preserved. Yet we know it was insectivorous based on the shape of its teeth.

What did Onychonycteris and Icaronycteris subsist on? We lack the stomach contents to answer this question in detail. Insects are a good bet, though, based on the form of the bats’ teeth and the wealth of insect fossils in the rocks of the Green River Formation. Most bats today subsist on insects, too. Only later in the evolutionary history of the group would some bats begin eating meat, fish, fruit, nectar, pollen and even blood.

Bat Relationships
The fossils recovered thus far from Messel and the Green River Formation have proved critical in helping researchers chart the rise of bats. Still, we lack fossils that establish how bats are related to other mammals. Tree-dwelling, gliding placental mammals known as colugos are sufficiently similar to bats that they were long thought to be close relatives. Over the past 14 years, however, Mark S. Springer of the University of California, Riverside, and others have conducted studies of DNA from large numbers of mammalian species that have shown that bats are not close relatives of any of the groups of placental mammals that include gliders such as colugos and flying squirrels. (Such creatures nonetheless offer compelling models for what the limb structure of bat ancestors might have looked like.)

Rather these genetic analyses place bats firmly in an ancient lineage known as Laurasiatheria. Other modern members of this group include such diverse beasts as carnivores, hoofed mammals, whales, scaly anteaters, shrews, hedgehogs and moles. Primitive laurasiatheres, however, were probably mouse- or squirrel-size creatures that walked on all fours and ate insects. Laurasiatheres are thought to have evolved on the ancient supercontinent of Laurasia, which comprised what is now North America, Europe and Asia, probably in the late Cretaceous period, some 65 million to 70 million years ago. The exact position of bats within this group is uncertain, but clearly a considerable amount of evolutionary change separates Onychonycteris and other bats from their terrestrial forebears.

Some of this change from land dweller to flier may have occurred surprisingly quickly, if recent discoveries in the field of developmental genetics are any indication. Though short by bat standards, the fingers of Onychonycteris are greatly elongated as compared with those of other mammals. How could this elongation have evolved?

In 2006 Karen E. Sears, now at the University of Illinois, and her colleagues reported in the Proceedings of the National Academy of Sciences USA that the key may lie in the activity of genes that control the growth and elongation of digits in the hand during development. Their comparisons of growth patterns in bat and mouse embryos revealed significant differences in the proliferation and speed of maturation of cartilage cells in developing fingers. A class of proteins called bone morphogenetic proteins (BMPs) plays a pivotal role in controlling these processes and in determining the length to which fingers grow. As it turns out, one of these proteins, BMP2, is produced at significantly higher levels in bat fingers than in those of mice, and manipulation of the gene that makes this protein can alter digit length. It is therefore possible that a small change in the genes regulating BMPs underlies both the developmental and evolutionary elongation of bat wing digits. If so, that might explain the absence in the fossil record of creatures intermediate between short-fingered, nonflying mammals and long-fingered bats such as Onychonycteris and Icaronycteris: the evolutionary shift may have been very rapid, and few or no transitional forms may have existed.

Despite many new discoveries about the rise of bats, mysteries remain. Bat ancestors must have existed prior to the Eocene, but we have no fossil record of them. Likewise, the identity of the closest relatives of bats is still unknown. Investigators are also eager to learn when the bat lineage first became distinct from that of the other laurasiatheres and how much of early bat evolution and diversification took place in the northern continents versus the southern continents. We therefore need fossils that lie even closer to the beginning of bats than Onychonycteris does. With luck, paleontologists will find such specimens, and they will help solve these and other riddles about the origins of these fascinating animals.