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"In fact, living birds are nothing less than small, feathered, short tailed theropod dinosaurs."  
              K. Padian and L.M. Chiappe  
                             The Origin of Birds and Their Flight  
                             Scientific American (Feb. 1998), pg. 47 

"Nowhere has the trap (of convergent evolution) been more successful than in luring paleontologists to the dinosaurian origin of birds."
                 A. Feduccia 
                            preface to his book
                            The Origin and Evolution of Birds (1996), pg. viii

III. Dinosaurs Among Us? 

The Mystery of Avian Ancestry 

The origin and evolution of birds has been one of the great mysteries of evolution; when and how did such a creature arise from the ancestral reptiles?  Birds are in many ways unlike any other living terrestrial vertebrates (i.e., amphibians, reptiles, and mammals).  They have radically different bone structure (hollow bones, wishbones, deep breast bones), lungs, perching feet, and of course, feathers.  The current debate on the origin and evolution of birds is one of the most heated in science.  The same piece of evidence is often put forward by either camp to support their position, and the language of the debate has often bordered on personal attack. 

Part of the dispute regarding avian origins comes from the ways that the sometime fragmentary fossil evidence, along with comparisons of modern forms, are conducted.  Evolutionary systematics is a method by which multiple lines of evidence from a wide variety of disciplines like biomechanics, genetics, embryology, comparative anatomy, and behavior are used to establish phylogenetic relationships between organism.  This approach has often been considered part science and part art, often lacking quantitative guidelines in the selection of the most appropriate characters upon which to establish phylogenetic relationships.

There are two major competing hypotheses regarding avian evolution, which differ primarily with respect to when the first true birds appeared.  One hypothesis proposes that the first birds descended directly from ancestral reptiles about 230 million years ago in the early to middle Triassic.  Here, we refer to this idea as the basal archosaur hypothesis; "archosaur" is the name for the ancestral reptiles from which birds, crocodiles, and dinosaurs evolved.  The other hypothesis advocates a much later entry of birds, with derivation from the dinosaurs some 100 million years after the time proposed by the basal archosaur hypothesis.  This idea we refer to as the theropod dinosaur hypothesis.

Archaeopteryx. One can trace the origins of the debate to more than 100 hundred years ago, to the discovery of one of the most famous of all fossils, Archaeopteryx.  In 1860, workers in the Solnhofen limestone quarry in Bavaria had found the imprint of a small feather.  This finding suggested that an animal coated with feathers must have existed around the Jurassic period.  Then, in 1861 a complete skeleton of Archaeopteryx lithographica was found near Solnhofen.   One of the reasons why the specimens of Archaeopteryx are so important is that while indeed had feathers, it also possessed many non-avian features.  It had small teeth in its jaws, claws on its forelimb digits which were free to move, and a long vertebral tail, which are all reptilian characteristics not seen in modern birds.  The skeletal characteristics of Archaeopteryx are closer to those of reptiles - dinosaurs, in particular.  Does this mean that Archaeopteryx is a "missing link" between reptiles and birds?  There was quite a debate (and disbelief) in both scientific circles and the culture at large after its discovery.  Recall that this was only two years after the publication of Darwin's controversial Origin of Species in 1859. 

The reign of dinosaurs. In order to understand the differences in the two hypotheses of bird origins, we must take a brief look at the evolution of dinosaurs. The Mesozoic era (next 150 million years) is often called "the Age of Reptiles."  During this era, dinosaurs, as well as other reptiles, took over the role of Paleozoic amphibians as the dominant terrestrial vertebrates.  Mammals already existed in the Upper Triassic, but they were small and powerless in the presence of huge dinosaurs.   

What are dinosaurs?  Based on skeletal features, dinosaurs are characterized by their upright posture of the rear limbs.  Many of the early dinosaurs were probably bipedal and walked parasagittally.  But, these feature are not all that differentiate other Mesozoic reptiles from dinosaurs.  For a long period of time, it was assumed that dinosaurs had a low metabolic rate and relatively small brains, and that they were slow and clumsy animals.  This view has been changed drastically during the last 20 years.  Some evidence suggests that dinosaurs were much more active animals than previously considered.  Some dinosaurs may have had a high metabolic rate and large brain size, comparable to birds and mammals.  Some of them might have even been warm-blooded.  This changing view has been reflected in movies and books about dinosaurs: old films often show rather slow, lumbering, and dumb dinosaurs while new films (e.g., Jurassic Park, The Lost World) present fast-moving, agile, and cunning animals.  However, the notion of warm-blooded dinosaurs is not without its critics. The temperature during this period was much different than that of today.  Due in part to prevelant volcanic activity, warmer and tropical climates existed over much of the earth. Therefore, even cold-blooded reptiles may have been more active that their modern counterparts, deriving the necessary operating body warmth from the ambient temeprature. 

Where did dinosaurs come from? Dinosaurs belong to the superorder Archosauria, an assemblage of different forms, which originally diverged from the ancestral diapsids by the late Paleozoic.  The first dinosaurs appeared by the Middle Triassic in South America.  From the late Triassic to the end of the Cretaceous, dinosaurs showed extensive radiation into a variety of groups and ruled the land, sea, and aerial environments.  Dinosaurs can be divided into two large groups based on the structure of the pelvis: the saurischians and the ornithischians.  The saurischian dinosaurs split further into two distinct lineages, the herbivorous sauropods (e.g., Brachiosaurus) and the carnivorous theropods (e.g., Tyrannosaurus), which appeared in the late Jurassic.  All ornithischians were herbivores (e.g., Stegosaurus).  

Where did dinosaurs go?  All dinosaurs disappeared suddenly (by geological time standards) by the end of the Cretaceous (65 million years ago).  The exact cause of the extinction has been debated rigorously and extensively.  At the end of the Mesozoic, did a catastrophic event (e.g., the impact of a large meteorite or asteroid) occur and kill plants and animals, as in the Alvarez hypothesis (Alvarez, 1987)?  Or, were dinosaurs vulnerable to gradual geological changes (e.g., lowering of the temperature) occurring on the earth at this time?  Whatever the probable cause, whereas dinosaurs (as well as numerous other plant and animal species) disappeared, the ancestors of mammals and birds survived. 

The Theropod Dinosaur Hypothesis 
(Origin of Birds: Approx. 150 MYA) 

Early theory. Thomas Huxley, friend and prominent defender of Charles Darwin and his then radical theory of evolution, was an early proponent of the dinosaur origin of birds.  He was impressed by the many structural similarities in the bones of Archaeopteryx and Compsognathus, a theropod from the Solnhofen Limestone.  In fact, for several decades a specimen of Archaeopteryx  was misidentified as a juvenile Compsognathus (Chatterjee, 1997).  Huxley also noted 35 features shared between the hindlimbs of the giant theropod Megalosaurus and modern ostriches, which did not occur together in any other animal (Padian & Chiappe, 1998).  He was particularly impressed by the similarities in the mesotarsal ankle structure indicative of a bipedal gait, which is somewhat rare in the overall scheme of vertebrate locomotion.  

However, the theropod dinosaur origin of birds was largely discarded with the publication of the influential The Origin of Birds by Gerhard Heilmann in 1916, and its English translation in 1926.  Even though Heilmann showed that birds were more anatomically similar to theropod dinosaurs than any other fossil group, he concluded that birds and dinosaurs must have originated from a more ancient reptilian group.  His conclusion relied on the widely accepted concept of the time that evolution is irreversible.  It was thought that once a feature was lost in evolution it could not be regained.  The small theropod fossils known at that time (e.g., the coelurosaurs) lacked clavicles, which are thought to have become fused to form the wishbone in birds.  Since reptiles have clavicles, this would have meant that theropods lost their clavicles, and then clavicles reappeared in the reptiles leading to birds.  To Heilmann, this was too large a discrepancy to support a theropod origin of birds.  Heilmann argued that both birds and dinosaurs must have originated from some common ancient reptilian group that had clavicles, probably the pseudosuchian thecodonts.  This line of thecodonts then led to the two great divergent lineages of dinosaurs and birds (Padian & Chiappe, 1998).  Heilmann's arguments held sway for about the next 50 years in evolutionary biology.

The theropod revival. Heilmann's fatal argument regarding the loss of clavicles was overcome by the discovery of other fossils.  In 1936, Charles Camp discovered the fossil remains of an early Jurassic theropod which possessed clavicles, and since that time other theropods with clavicles have been found (Padian & Chiappe, 1998).  Huxley's theropod dinosaur origin hypothesis was resurrected primarily by John Ostrom in the late 1960's.  Ostrom studied Dromaeosaurs, a small theropod form which included the sickle-clawed predatory dinosaurs Deinonychus and Velociraptor (the inspiration for one of the villains of Steven Spielberg's Jurassic Park).  There are several distinctive characteristics that Ostrom argues links birds and the dromaeosaurs.  The Dromaeosaurs had a unique semilunate (moon-shaped) carpal wrist morphology, a long coracoid, three-fingered arms and three-toed feet, and a stiff tail (Chatterjee, 1997).  Studies from Jacques Gauthier employing cladistic analysis confirmed Ostrom's assertion that birds evolved from small theropod dinosaurs (Padian & Chiappe, 1998).  Gauthier's studies, and ones conducted more recently, demonstrate that before the existence of birds many preavian theropods had features traditionally considered exclusively "bird-like."  These bird-like characters include: a bipedal stance, hollow bones, elongated forelimbs with three-fingered hands, elongated metatarsals (foot bones) with three-toed feet, a wishbone, and a backward-pointing pelvis (Padian & Chiappe, 1998).  

Feathered dinosaurs? Feathers are an unmistakable trait of birds, and the relative lack of fossils showing the origin and evolution of feathers has driven much of the debate over bird origins.  A turkey-sized dinosaur named Sinosauropteryx and another find dubbed Protarchaeopteryx, were described by Ji Qiang and Ji Shu'an of the National Geological Museum of China in two reports (Padian & Chiappe, 1998).  These fossils were found in Liaoning province in strata dating to the late Jurassic or early Cretaceous.  Sinosauropteryx has fringed elements along its backbone and body surface which may be feather precursors.  It does, however, have many differences with birds and probably is related to the theropod Compsognathus.  This finding may be either a maniraptoran theropod or possibly a bird, but a full description of its anatomy still awaits publication (Padian & Chiappe, 1998).  Hou and colleagues (1995) have reported the finding of Confuciusornis sanctus, a pigeon-sized specimen from a formation in northeastern China dated to the Jurassic-Cretaceous boundary.  This species may have lived before Archaeopteryx, but exhibits the hindlimbs and retroverted pubis similar to Archaeopteryx.  The skeleton also has unfused carpal elements and long fingers with long, curved claws (Hou et al, 1995).  There also exist avian-like contour feathers, which could indicate endothermic physiology (Chatterjee, 1997).

 The Basal Archosaur Hypothesis 
(Origin of Birds: Approx. 230 MYA) 

There are several other lines of criticism leveled at the theropod dinosaur hypothesis.  First, scientists disputing the theropod dinosaur origin of birds note that the appearance of "bird-like" theropods in the fossil record (at least those found to this point) occurs about 75 million years after the origin of birds as indicated by Archaeopteryx specimens (Feduccia,  1996).  In addition, the arguments for a more ancient ancestry of birds, from the basal archosaurs and not their theropod dinosaur descendants, can be summarized by considering the debate over "hot-blooded" dinosaurs, feather development, and the origins of flight.  

Hot-blooded dinosaurs? In living vertebrates, only birds and mammals are warm-blooded or endothermic ("heat from within").  These organisms have high metabolic rates (5-10x that of reptiles) and can maintain a more constant body temperature.  Heat in birds and mammals is aerobically produced from the breakdown of glucose in the presence of oxygen.  Most reptiles, fish, and amphibians are cold-blooded or ectothermic ("heat from outside"), meaning their body heat is primarily derived from the environment.  Ectothermic organisms like reptiles are constrained by their reliance on environmental warmth and their metabolic system.  They are capable of brief bursts of intense activity, followed by periods of rest.  These inactive periods are necessary due to the large amounts of lactic acid accumulation which results from their anaerobic-type metabolism.  Because birds with feathers and mammals with hair do not rely on ambient temperature for warmth as reptiles do, they can operate in a wider variety of environmental temperatures.  This has enabled them to forage and migrate over large distances, contributing to their wide ecological dispersion.  The trade-off for endothermic organisms, however, is a relatively constant and large intake of  food to maintain the calories needed for heat generation. 

The traditional view of all the dinosaurs as large, lumbering cold-blooded reptiles has been challenged by several scientists.  Proponents of the "hot-blooded" dinosaur hypothesis include Robert Bakker and, to a lesser extent, John Ostrom.  Arguments for endothermic dinosaurs include considerations of their bipedal stance, the microscopic structure of their bones, and theories on brain size and intelligence in dinosaurs (Feduccia, 1996).  While beyond the scope of this review, there are several other lines of evidence both for and against the existence of endothermy in dinosaurs, and the reader is referred to an excellent book by Feduccia (1996).  The existence of hot-blooded dinosaurs has important implications for attempts at reconstructing the origin and evolution of birds.  Endo- versus ecto-thermy is tied together with the original adaptive value of feathers, whether they evolved primarily as adaptations of scales to assist in flight, or whether they originally served as insulation and then secondarily developed the complex structure which makes them so effective for flight.  

Theories of flight. The excellence of the avian design for flight, along with the paucity of fossil evidence for transitional forms, has made the evolution of flight in birds an area of tremendous speculation.  There are two primary theories regarding the origins of flight, the cursorial ("ground-up") and  arboreal ("tree-down") theories.  Cursorial theories in general assume that protobirds and Archaeopteryx were bipedal and terrestrial, and they evolved feather-like precursor structures primarily as insulation.  Endothermy is usually assumed to have existed in these avian precursor organisms.  Basically feathered dinosaurs, these forms eventually began to use their feathered forearms to leap and glide.  They may have even used their feathered wings as insect traps for feeding (Ostrom, 1979).  If endothermic, these forms could be rapid bipedal runners, eventually leaping and hopping their way into powered flight.  

Arboreal theories tend to view the protobirds as already having invaded the trees to escape ground predation, to nest, or some other adaptive reason.  They would have been able to climb trees with their foreclaws and then glide to lower perches, from tree to tree, or to the ground.  The claws of Archaeopteryx are argued to be like those of many modern perching species and inappropriate for a swift, ground-running organism (Feduccia, 1996).  Amongst the trees, the danger of falling led to strategies to slow descent; for example, increasing drag by enlarging the body surface area (outstretching the limbs) and the evolution of ever-longer feathers.  These adapted forms would be more likely to survive an accidental fall from the trees compared to equally clumsy conspecifics.  

If early bird-like forms like Archaeopteryx may have been ectothermic, arboreal theories suggest feathers were not crucial for body temperature regulation.  Arboreal theories suggest that the scales which gradually evolved into feathers did so for the sole purpose to facilitating gliding, lift, and eventually flight.  The structure of Archaeopteryx feathers is similar to that of modern birds.  The flight feathers (on avian wings) and contour feathers (like those found on the breast) have dissimilar structure.  The primary flight feathers show vane asymmetry, with differing widths of the vane on either side of the shaft, or rachis.  In birds who have lost the ability to fly, like some species of rail (Atlantisia rogersi), the feathers have degenerated into superficially hair-like structures (Feduccia, 1996). Of course, it is possible that some variant theory encompassing both ground-up and tree-down behaviors drove the unique structure of skeleton, musculature, and feathers in birds leading to flight.  Since it would be cooler above ground in the trees, there could have been a tandem development of the flight-supporting and thermoregulatory contributions of feathers.  New fossil findings, more sophisticated models of flight physics, and comparative anatomical studies of modern forms will undoubtedly shed new light on the questions of avian evolution and flight.  Constructing the evolution of birds and complex behaviors like powered flight requires a great deal of speculation and interpretation of sometimes meager data; in light of this fact the debate over bird origins is sure to continue.  

Next Section:  Evolution of Retinal Structures