In quest of the origin of birds
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1 In quest of the origin of birds Two opposing schools ofthought question how birds arose from reptilian ancestors The incident was, by any standard, of little apparent significance: On an arid, tropical island shrouded in low, palmlike shrubs and ginkgo trees, a crowsized bird flapped out of the sky to perch on a branch. This bird was not like any that we know today. Its feathered tail was long and lizardlike. Even more reptilian was the bird's head, which was shaped like that of a small Tyrannosaurus and armed with teeth. Each wing bore three long, clawed fingers that the bird could use to cling to branches when it wasn't aloft with other now-vanished flying species, such as leather-winged pterodons and giant dragonflies. After the bird landed, it may have scanned its surroundings for dangerous predators, then settled down to preen itself, much as modern birds do. Perhaps it pulled loose a wing feather, held the feather briefly in its jaws, then released it to the wind. Maybe a gentle breeze wafted the feather into the sky, took it floating and tumbling through the air, blew it seaward, out over a shallow lagoon that bordered the island. Possibly, over the water, the feather careered downward, sank into the lagoon, and vanished into the fine, calciumrich muck of the bottom. And there it lay, in silence and darkness, as years and centuries, generations and millennia, passed by interminably. Meanwhile, the accumulating weight of the sediments compressed the muck into limestone, and changing climate, shifting seas, and the drifting of landmasses across the face of the globe incorporated the island into the continent that we call Europe. by Roger L. DiSilvestro The feather remained undisturbed until 1861, when its stone bed vibrated with the pounding of steel against rock, a pickax breaking the bonds of the ages. Once again, sunlight fell on the remnant of the ancient bird, discovered by a rockcutter working in a limestone quarry outside Solnhofen, Germany. The fossil arrived in the hands of a Frankfurt paleontologist, Hermann von Meyer, who recognized that it came from sediments dating to the Age of Reptiles. His report on the fossil in the New Yearbook ofmineralogy stirred the scientific community, because the single fossil feather, only 2.5 inches long and less than half an inch wide, proved for the first time that birds had lived in the dinosaur era. An even more startling discovery, also reported by von Meyer, occurred later in 1861: At a quarry in the Langenaltheim region of Bavaria, a miner turned up a complete skeleton of a bird from 150 million years ago. The skeleton was so reptilian in appearance, with its toothed jaws, long, clawed wing fingers, and multivertebrae tail, that the animal would have been classified as a lizard or dinosaur were it not that the fine limestone matrix retained the impressions of feathers on tail, front limbs, and body. After examining the fossil, which revealed a clear evolutionary link between birds and reptiles, von Meyer named the new species Archaeopteryx (" ancient wing") lithographica (a reference to use of the limestone matrix in lithography). The discovery kicked off a flurry of theorizing about bird origins that continues to this day. Although called the Rosetta Stones of avian evolution because they provide so many clues to bird origins, the seven Archaeopteryx fossils that have accumulated on museum shelves during the past 130 or so years represent a creature quite removed from the dawn of birds. Archaeopteryx is widely accepted as the earliest bird in the fossil record. Its only rival for that title is a fossil creature from Texas called Protoavis, which is 85 million years older than Archaeopteryx and shows a number of birdlike skeletal traits. However, because its fossil remains lack any sign of complete feathers, the majority opinion does not yet accept Protoavis as the first bird. That honor remains with Archaeopteryx, which is, nevertheless, anatomically much like modern birds, with a feathery body covering and virtually modern wings. To get closer to the beginnings of bird origins requires a look into a past that lies beyond Archaeopteryx, a past in which no feathered creature yet flew across the skies. Speculation based on fossils from that era has led to two opposing schools of thought that lately have aired their controversial views on bird origins with impressive regularity and frequency in publications ranging from Nature and Science to The New York Times. Hypothesis one: dinosaurs + feathers =birds One school of thought is represented by Luis Chiappe, a paleornithologist in the American Museum of Natural History's Department of Ornithology. "If asked," he says, "about the origin of birds, I would say dinosaurs." Specifically, Chiappe would say theropod dinosaurs, creatures that looked something like reptilian kangaroos, with long, powerful hind legs designed for running, a long tail for September
2 balance, and short forelimbs. Perhaps the most famous theropodalthough hardly the sort of creature that springs to mind when contemplating the likely ancestor of, say, the barnyard turkey-is Tyrannosaurus rex. The theropod hypothesis is the oldest and most venerable of the avian genesis creeds. It dates back to 1862, the year that the British Museum bought the first Archaeopteryx fossil from its German handlers. Beea use this missing link between birds and reptiles had been hacked from rock only two years after British naturalist Charles Darwin published On the Origin of Species, the fossil figured prominently in arguments over Darwin's ideas about evolution. Thomas Huxley, Darwin's intellectual sidekick and a zealous defender and promoter of evolution, published a paper in 1868 on the origin of birds in which he concluded that Archaeopteryx was a true bird. He drew special attention to the ancient bird's close resemblance to Compsognathus, a theropod also found in Solnhofen limestone. Huxley found this similarity so impressive that he decided that Compsognathus was even more of a missing link betweenreptile and birdthanwas Archaeopteryx. Birds, he concluded, must have descended from such dinosaurs. Thus, he launched the theropod hypothesis. Chiappe's studies of theropod bone morphology have led him to concur with Huxley's opinion. For proof, Chiappe says, look at the theropod foot. The primitive foot among terrestrial vertebrates features five digits. But the theropod has only three main toes-and, Chiappe says, not just any toes, but the same three main toes that grace a bird's foot. Moreover, the toes have the same alignment and proportions in both birds and theropods. That two distinct groups of vertebrates-birds and theropods-should have such pedal similarity indicates an evolutionary relationship between the groups, Chiappe suggests. Other evidence occurs in the wristbones of a closely related group of birdlike theropods that includes animals such as Oviraptor and Velociraptor, Chiappe says. Carpal bones in these theropods have fused to form a compound bone called the semilunate. This bone is not present in any other vertebrate, Chiappe says, except Archaeopteryx and some other early birds. Birds and dinosaurs also share a type of hip socket found in no other animal. To Chiappe, such findings suggest that birds and creatures such as Velociraptor shared a common ancestor. Further evidence of their common ancestry comes from a theropod species discovered this year in Argentina and reported in the 22 May 1997 issue of Nature by paleontologists Fernando Nova and Pablo Puerta. The shoulder socket of the new species, according to Nova and Puerta, faces laterally, as it does in Archaeopteryx and other birds, rather than down and back, as in other dinosaurs. The lateral position allowed the animal to tuck its upper arm bones close to its body in much the way that birds fold their wings. The hip socket and some elements of the pelvis also resemble those of birds. Mark Norell, a dinosaur specialist with the American Museum ofnatural History, says that the new theropod fills a wide gap in the evolutionary history leading up to birds. The birdlike qualities of the new animal have even won it the name Unenlagia comahuensis, which means"half bird from northwest Patagonia." "Take any bone in theropods and birds, and I can show how it links birds to dinosaurs," Chiappe says. But he also points to behavioral similarities between birds and theropods as further evidence of an evolutionary link. For example, fossil remains indicate that at least one theropod, Oviraptor, laid its eggs in nests and sat on them, incubating or protecting the eggs just as birds do, Chiappe says. Based on such evidence, Chiappe speculates that the earliest ancestor of birds was a bipedal dinosaur with forelimbs that were proportionately longer than those of T. rex but shorter than the wings of Archaeopteryx. The creature probably wore a covering of feathers, evolved from scales, for insulation. This is not to say that the animal was warm blooded, says Chiappe. However, it may have been at some stage intermediate between warm and cold blooded, so that it needed some form of insulation. The animal was most likely terrestrial, Chiappe says, a creature designed by evolution for running. This last point, which at first blush may seem obvious, lies at the heart of the bird origins controversy. Opponents of the idea that birds descended directly from dinosaurs argue that a terrestrial species such as the theropods simply could not have given rise to a flying creature. Flight, they say, could not have evolved from the ground up. Hypothesis two: thecodont + feathers + flight = birds The origin of birds is, in fact, synonymous with the origin of feathered flight, according to Alan Feduccia, head of the Department of Biology at the University of North Carolina and one of the leading opponents of the theropod hypothesis. Only a creature capable of evolving flight could have given rise to birds, he says. And when he looks at the physical demands of flight, he concludes that "it is biophysically impossible to evolve flight from the theropods. That is the Achilles' heel of the theropod hypothesis." Larry Martin, a paleontologist at the University of Kansas, agrees. Theropods were ground runners, he points out. "If you're running on the ground and trying to get enough speed for flight-it's impossible," he says. A bird's body is flattened from top to bottom, he adds, making it suitable for flight. Theropods were flattened from side to side, which is not good for flying. Feduccia and Martin argue that flight in birds occurred not from the 482 BioScience Vol. 47 No. 8
3 Th is was the look of Germ any's Bavaria approximately 150 million years ago, when the fossil-rich limestone of the Solhh ofen deposits was the sandy bottom of shoreline lagoons. Arcbaeopteryx, the oldest known bird species, wings acros s the cent er of the picture, while pterosaurs fly in the background. T homas Hu xley believed that the chicken-sized, bipedal dinosaur in the foreground, Campsognathus, was an ancestor of bird s. Photo: Field Mu seum of Natural History, Chicago (nega tive number 75017). ground up but from tr ees down and that it began with gliding. " If you can get up a tree," sa ys Feduccia, " one of the most effi cie nt ways to travel through a forest is to glide fro m tree to tree." Today, a number ofsp ecies travel by gliding across the world's forests. These creatures are usuall y small, with specia l, enlarged surface areas for slow ing th eir falls. They include the North American flying squirrel, which sprea ds its four legs when it glides, revealing a flap of skin, called a pat agiurn, that ser ves as a sort of par achute. Another glider is the flying dragon, a native of the Malay Pen insul a a nd islands of the western Pacific. Flying dragons can glide for up to 200 fee t on a patagium th at stretches bet ween the hind limbs and forelimbs and is stiffened by six long ribs. This lizard can even navigate well eno ug h to select landing sites in individua l trees. The flyin g dragon could serve as a model for the type of reptile that Fedu ccia and M artin believe gave rise to birds. Specifically, the y ha ve in mind some sort of a ncient archosaur. At th is point in th eir spec ulation th ey are no t to o far rem oved from the th eropod hypothesis, beca use archosaurs compose a broad group of rept iles th at includes dinosaurs. Arch osaurs are char act erized by a skull with two temporal openi ngs and a large opening in front of the eye-a description th at fits everything from alligators and crocodiles to flying pterosaurs. Septemb er
4 The earliest of the archosaurs were the thecodonts, which date back 245 million years and probably gave rise at some point to dinosaurs. Feduccia and Martin think that the thecodonts also are responsible for the evolution of birds. The scientists hypothesize that perhaps 200 million years ago an arboreal thecodont traveled through forests by leaping from tree to tree. Over the years, evolution turned the animal into a glider by bestowing on it large scales along the edges of its forelimbs, tail, sides, and hind limbs. These scales, which slowed the creature's falls, ultimately became subdivided along their lengths, with the sides of the scales forming a sort of fringe along a central axis. This structure led to the vaned feather found in birds today. Along the way, the thecodont became better adapted to gliding, and then finally to sustained flight. Natural selection for better and better aerodynamics eventually produced birds. As beguiling and logical as Feduccia's hypothesis is, he cannot support it with fossil evidence. No partiallyfeathered thecodonthas ever been found, although Feduccia believes that such a fossil is buried in the sediments of some part of the globe. The problem, he says, is that small arboreal creatures do not preserve well. Fossilization occurs mainly when animals or plants die in wet areas, such as rivers, lakes, marshes, or swamps, and sink into or are covered by sediments. Small, fragile-boned animals that tumble from trees to a forest floor when they die are not as likely to be preserved. However, some thecodont fossils, although not the remains of species ancestral to birds, do provide support for Feduccia's idea. One of these is Longisquama insignis, a 4 or 5 inch-long thecodont that lived in the Turkistan area approximately 200 million years ago. It bore a row of ten enlongated and highly modified featherlike, vaned scales along its back, each apparently corresponding to a vertebra. These modified scales, which may have been intermediate between reptilian scales and feathers, were actually longer than the animal itself and could be held horizontally for gliding. Another provocative thecodont is Megalancosaurus preonensis, a footlong species that lived in Italy's Preone Valley region around the same time as Longisquama. This creature had elongated forelimbs and a birdlike skull and scapulae. After studying Megalancosaurus, John Ruben, a paleontologist at Oregon State University, has concluded that the creature was arboreal, with a rudderlike tail and a proto-patagium. Although the species is not ancestral to birds, Ruben says, it does show that animals of the kind Feduccia is hypothesizing did exist "at the right time." Moreover, says Feduccia, the morphological diversity displayed by these thecodont fossils indicates that many small, early archosaurs exhibited anatomical similarities to birds, making thecodonts "intuitively pleasing" as bird ancestors. They also "fit nicely with the arboreal theory for the origin of flight," he says-the only theory of flight origins that he believes can be explained easily in biophysical terms. Although much of Feduccia and Martin's debunking of the theropod hypothesis revolves around flight, they also draw on other arguments. For example, the theropod hypothesis contends that feathers evolved as insulation for a terrestrial species. Feduccia discounts this idea on the grounds that feathers are too complex to have evolved just for insulation. If you look at birds in which feathers are used strictly for insulation, such as emus and ostriches, you find, Feduccia says, that the feathers simplify in structure, becoming hairlike. Only in flighted birds do you find feathers with a complex vane structure. "Feathers are the most complex appendages ever produced by the vertebrate integument," he says. "Unless there's continued evolutionary pressure for their maintenance, they go to pot." He believes that feathers must have originated not as insulation but as stablizers in a gliding species. Feduccia also dismisses another tenet of the theropod hypothesis, the idea that Archaeopteryx fossils are so theropodlike that they would have been mistaken for theropod remains were it not for the feather impressions. Feduccia contends that skeletal evidence shows that Archaeopteryx was something new and different. "If you viewed [the Archaeopteryx fossil and a theropod skeleton] through binoculars at 50 yards, yes, they'd look alike," he says. But close examination reveals that the teeth of Archaeopteryx are peglike, whereas those of theropods are sharp and serrated. The forelimbs of Archaeopteryx are long, relative to the hind limbs, but in theropods those proportions are reversed. "The similarity is very superficial," he says. "It will not hold up to scrutiny." Feduccia and Martin also take issue with the use of theropod fossils to support the idea that birds descended from dinosaurs, primarily because all of the fossils are tens of millions of years younger than Archaeopteryx. For example, Unenlagia comahuensis dates from 90 million years ago, making it million years younger than Archaeopteryx. Even the dinosaur genus that theropod partisans use to tie the evolutionary knot between dinosaurs and birds, Deinonychus, did not appear until some 40 million years after Archaeopteryx flew the skies. Moreover, Feduccia says, recent theropods were more birdlike than older theropods. The newer theropods had developed through time a closer and closer resemblance to small, running birds such as chickens and roadrunners. These similarities, Martin says, stem from convergent evolution in two separate lineages that both feature adaptations for bipedal running. For example, Martin says, Unenlagia's forelimb was an adaptation for keeping the arm close to the body while the 484 BioScience Vol. 47 No. 8
5 theropod was running. It had nothing to do with a relationship to birds, Martin says. If the two schools of thought concerning avian genesis seem miles apart, it is probably because they are. But those miles that separate them leave plenty of room for a middle ground, a middle ground in which at least one paleontologist has set up camp. Early birds catch no consensus John Ruben is not yet ready to pledge allegiance to one side or the other. Feduccia's lack of fossil evidence casts doubt on the thecodont hypothesis, Ruben says. On the other hand, theropods do not make convincing bird ancestors, he says, because there is "no way flight could have evolved from the ground up. It's beyond ridiculous." Moreover, the theropod partisans lack fossils from the right time period, Ruben says. And yet, Ruben adds ambivalently, "There's credible evidence on both sides of the issue." Just enough, it seems, to make the issue murky. "What we ought to be saying is, 'We don't know,'" says Ruben. "So much of this is justhot air, because the fossil evidence is too incomplete." Chiappe, to the contrary, argues that the fossil evidence for the theropod hypothesis is perfectly satisfactory. Indeed, what troubles him is Feduccia's lack of fossils, a concern that reveals a fundamental methodological difference between Chiappe and Feduccia. Chiappe ignores the question of the origins of flight on the grounds that it is too speculative. He prefers to stick strictly to the evidence he sees in the fossils, evidence that can be measured, touched, assessed. Trying to put the origin of birds into the less tangible context of the origin of flight, he says, "is not the way we should infer the origin of birds." Chiappe and his colleagues remain untroubled by the fact that the theropods they use to support their ideas are younger than the birds to which theropods are supposed to be ancestors. "We don't see time as particularly important," he says. The theropods represent not direct ancestors but creatures related to birds via a common theropod ancestor. The evidence found in the bones of younger theropods indicates, according to Chiappe, that older, undiscovered theropods shared traits with birds. "We think the fossil record is incomplete," he says. "So I'm not concerned about those 30 or 40 or 50 million years separating bird and theropod fossils." For Chiappe, the main point is that bones tell tales, and the tale theropod bones tell is of a relationship to birds. Feduccia, on the other hand, is more of a logician. His contention that birds could not have evolved from theropods because theropods could not have evolved to fly is based on purely rational grounds without recourse to the fossil record. Fossils are not critical to backing up his argument, although it would be nice to have them. The differences between the two camps may reflect differences between the way paleontologists, such as Chiappe, and ornithologists, such as Feduccia, look at the world. Or perhaps the heart of the issue cannot be reached via science alone. Perhaps the theropod hypothesis comes freighted with a powerful emotional baggage. Feduccia, Martin, and Ruben believe that it does. For who would deny the emotional appeal of the idea that birds descended from theropods? As John R. Horner, curator of paleontology at the Museum of the Rockies in Bozeman, Montana, has pointed out, if you accept the theropod hypothesis, then you could argue that "dinosaurssmall, flying ones-are alive today." And for many dinosaur enthusiasts, the idea that all manner of dinosaurs fly, walk, flock, migrate, quack, and warble throughout the world packs quite an emotional wallop. From that perspective, enthusiasts can link directly with the lost Age of Reptiles and find exciting new dimensions in watching a roadrunner kill a snake, or a flock of geese pass by overhead. Doubtless many dinosaurophiles, from paleontologists to children playing with plastic dinosaurs in sandboxes, would like to believe that dinosaurs still exist. As a result, the theropod hypothesis, with its implication that dinosaurs did not simply vanish from the face of the earth, brings with it a tremendous impulse to want to believe that it is correct. Robert Bakker, a paleontologist at the University of Colorado, a theropod partisan, and a leading popularizer of dinosaur science, has declared, "It must be said, restoring Archaeopteryx to its proper place in the dinosaur's family tree has been a great boost to the morale of dinosaurophiles. " So what may be at stake among experts on the origin of birds is not just scientific fact but the survival of the dinosaurs. Even Feduccia feels the emotional tug of that issue. Although Martin says, "People like Alan Feduccia and I are trying to reexterminate the dinosaurs," Feduccia feels a little guilty about it. "It's like taking candy from a baby," he says. "I feel like a heel, but somebody's got to do it." 0 BioScience features editor Roger L. DiSiluestro's interest in birds began with membership in the Omaha (Nebraska) Bird Club when he was 14 years old. September
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