Avian Origins

Avian Origins
The class Aves, with its more than 10,000 living species inhabiting the earth, is the most diverse of land vertebrates. Its members are examples of one of the richest and most controversial passages in animal evolution, and the descendants of an ancient radiation that finds its origins well into the Cretaceous period (Chiappe & Dyke, 2002). Even though birds represent one of most common and easily recognizable class within the animal kingdom, their origins remain the center of a debate that has for over a century filled the pages of scientific journals and produced spirited arguments among and between paleontologists and ornithologists. Despite such controversies, scientists from both disciplines agree that birds evolved from reptiles. While some paleontologists place avian origins some 230 million years ago among the archosaurs of the Triassic and long before the split between Saurischia and Ornithiscia (Feduccia, 1999), others sustain that modern birds rise from the mighty Theropoda (Chiappe & Dyke, 2002). Nevertheless, the research conducted for the purposes of this paper on the origin of birds yielded an overwhelming support for the latter hypothesis. Although the major focus of this paper will be to present part of the evidence that upholds that “birds are theropod dinosaurs” (Chiappe & Dyke, 2002, p. 92), the counterargument will be briefly discussed so as to offer an alternative to the study of avian origins.
The discovery of Archaeopteryx: A brief historical review on the establishment of avian ancestry
In 1863, Sir Richard Owen described in detail the morphology of a fossil that had been found in the Late Jurassic Solnhofen limestones of Germany two years earlier. After a thorough examination, Owen decided that Archaeopteryx lithographica belonged within the Aves, making it the oldest and only Jurassic bird to date (Chiappe & Dyke, 2002; Cracraft, 1986). A few years later, Thomas Henry Huxley also undertook an examination of the specimen and found several similarities between Archaeopteryx and reptiles, which prompted him to hypothesize the origin of birds within them, “with dinosaurs held to be highly probable sources” (Dodson, 2000, p. 505). These newly found phyletic connections of birds to reptiles were later challenged by Gerhard Heilmann, who proposed Thecodontia (an “incongruous assemblage…not easily definable by modern standards” [Feduccia, 1999, p.47], that is less anatomically specialized than Theropoda and includes most Triassic archosaurs such as pterosaurs, crocodiles, and dinosaurs [Prum, 2003]) as the ancestors of birds. Even though Heilmann had seen the connection between birds and dinosaurs, he considered the dinosaurs’ apparent lack of clavicles (the structure that preceded the avian furcula [wishbone] and which was later recognized among major Theropoda clades including dromaeosaurs, oviraptors, tyrannosaurs, allosaurs, and coelophysids [Prum, 2003]) as a drawback for the dinosaurian ancestry of birds.
Heilmann’s hypothesis reigned as the established answer to the origin of birds for forty years, until the early 1970s when John Ostrom—briefly after having concluded his study on Deinonychus antirrhopus and his examination on a newly discovered specimen of Archaeopteryx—published a series of papers in which he provided the “first detailed evidence” (Cracraft, 1986, p. 384) and proposed a close relationship between theropod dinosaurs—more specifically coelurosaurus, and within these maniraptorans—and birds. Ostrom had noticed several synapomorphies between higher coelurosaurs and Archaeopteryx; however the one trait that led him to question the established hypothesis and consequently support the theropod-avian relationship was the fused distal carpals 1 and 2 which allowed the wrists to swivel sideways (Prum, 2002). In 1986, Jacques Gautier proposed an initial cladistic interpretation of the theropod origin of birds which has been, and continues to be, modified and amended with new discoveries (see Appendix A).
Although widely accepted, the dinosaur-avian relationship remains much debated, not only among those who oppose it—who firmly believe that the phyletic connections still do not offer solid evidence for the case—but also among those who support it in their enthusiasm for determining the exact sister-taxon of Aves among coelurosaurians; dromaeosaurids (e.g. Deinonychus, Velociraptor), troodontis (e.g. Troodon), oviraptorids (e.g. Oviraptor), and alvavezsaurids (e.g. Shuvuuia deserti) are the most commonly cited taxa (Chiappe & Dyke, 2002).
Birds and dinosaurs: Getting closer
Much evidence has been accumulated since Ostrom’s work in support of the theropoda origin of birds. Although there are many traits shared by the two groups, there are a few that could be considered of particular interest as they better illustrate the relationship between birds and coelurosaurian theropods.
Feathers
Numerous wonderfully preserved specimens of coelurosauria from the Early Cretaceous of China have provided strong evidence that feathers arose within theropods and that they preceded the origin of flight and, by extension, the origin of birds as we know them (Wong, 2001). The specimens recovered from northeastern China’s Liaoning Province—which have preserved integumentary structures interpreted as feathers—include at least six taxa of non-avian theropods (Chiappe & Dyke, 2002). These structures vary in size and shape from the simpler filament-like to tufts attached at their bases, to more complex ones with vanes. Although their elaborated arrangements resemble those of avian feathers and are located externally, supporters of the opposing views of the origin of birds have claimed that these structures are only “frayed internal composite fibers of the structural protein collagen” (Chiappe & Dyke, 2002, p. 107). The discovery of structures surrounding a specimen of the alvarezsaurid Shuvuuia deserti provided further support for the avian hypothesis when they were shown to be composed of only β-keratin, the same component of avian feathers.
Feathers appear to have had purposes other than flight. It is important to clarify at this point that while modern birds (or neornothines) possess feathers that are adapted for flight, the primordial structures may have gone through several stages of development, independent of their functionality, until becoming feathers that could have had an aerodynamic function. Prum (2003) has hypothesized that the initial stage was represented by “hollow tubes”, followed by a “tuft of barbs”, then by “doubly branched feathers”, and finally by “feathers with a closed pennaceous vane” (p. 556). Such gradual development spanning millions of years, hints that feathers did not originally evolve for flight, but perhaps for insulation (Wong, 2001) or even as a result of sexual dimorphism as it had been originally hypothesized for Archaeopteryx (Owen, 2006).
Shared traits
Further support of a coelusaurian origin of birds has been provided by the Malagasy Rahonavis ostromi or “Ostrom’s menace from the clouds” (Leutwyler, 1998, para. 1). Found and described in 1998, R. ostromi embodies a complex combination of characters that place it in a basal position within Aves (Chiappe & Dyke, 2002). It has very defined dinosaurian features such as a thicker toe bone structure and sickle claw on the second toe of its pes (typical of maniraptorans), and a long tail (just like Archaeopteryx’s), but also very bird-like characters including long hollowed and light bones, a reversed first toe, hip and leg structure similar to that of modern birds, and quill knobs on its forearms represented by six “bumps” (Leutwyler, 1998). This extraordinary array of features, though it provides invaluable and strong evidence, has not gone unchallenged. Several dissenters to the theropod hypothesis have claimed the specimen to be a sham composed of avian (forelimb and shoulder girdle), and non-avian theropod parts (hindlimb, pelvis, and tail); nevertheless, the fact that the specimen was found on a surface of less than 0.14 m² suggests that the bones belong to only one individual (Chiappe & Dyke, 2002).
Flight
One of the unique characteristics of birds that accounts for their aerodynamic features (elongated forelimb with flexible wrists, arrangement of vaned feathers in remiges and retrices, and a lateral orientation of the shoulder socket) is their ability to fly or glide (Chiappe & Dyke, 2002). Nevertheless, all of these features evolved before the Aves became the vertebrates we know today. The development of such complex locomotor system led not only to physiological and muscular transformations, but also to behavioral and neurological changes. “Each major lineage of Mesozoic birds provides direct evidence of the changes in the skeleton and plumage” that occurred before these creatures were able to take off (Chiappe & Dyke, 2002, p. 110). Although Archaeopteryx was originally interpreted as a bird capable of flight, it is probable that its lack of well-developed flight musculature and several aerodynamic features may have made it less of a flying specimen and more of a glider. A younger species (25 million years younger to be exact), Microraptor gui from the fossil beds of Liaoning Province in China, has shed some light on the mode of life of these ancestors. This four-winged bird has led scientists to speculate that the evolution from dinosaurs to birds included a phase in which birds had flight feathers on all their limbs (Mayell, 2003). Whether they were capable of flying (or gliding) remains another much debated question, as it opens the arena for yet two more hypotheses: Were these ancestors gliders (they climbed trees [or were tree-dwellers] and learned to glide before flapping their wings), or were they flappers (they developed legs that gave them speed and lifted them off the ground while energetically flapping their wings)? The team that recovered Microraptor is convinced that the feathers on the hind limbs would have represented a burden for the animal if it attempted to run (Mayell, 2003). However, whether these birds took advantage of gravity or launched themselves into the air is still a matter of interpretation with no conclusive answers.
Similar Habitats
Numerous paleontologists have argued on the subdivisions of birds of the basal lineages. Although some of these interpretations have not been evaluated within a cladistic framework, several analyses have shown a strong and closer association between confuciusornithids and enantiornithines, and extant birds (Chiappe & Dyke, 2002). Of all the Cretaceous groups, Enantiornithes, with about 20 species reported to date, are by far the most diverse. The early members of this group were toothed and small, and shared many anatomical features with their living relatives including pedal morphology that evidenced perching. Most enantiornithines occupied the niche of current land birds; however, some specimens have also been found in littoral and marine environments. The discovery of the ornithurine Apsaravis ukhaana in 1998 in the Gobi desert of southern Mongolia contradicts a previous hypothesis which suggested that the enantiornithines had pushed the ornithurines, the closest relative to living birds, to coastal areas and marine habitats. The recovery of an ornithurine in a sand dune environment prompted scientists to suspect that these early birds occupied the same wide variance of niches modern birds fill today (Wong, 2001).
Brooding
Finally, the presence of brooding behavior similar to that of the Aves has been suggested after the discovery of theropoda remains associated with their clutches (Chiappe & Dyke, 2002). Furthermore, embryonic remains of coelurosaurians have revealed that these non-avian dinosaurs and birds shared the features of their egg shells microstructure.
Conclusion
There is no doubt that modern birds have evolved from reptiles; furthermore, the fossil record seems to provide the strongest evidence in support of the coelurosaurian hypothesis of the origin of birds. Despite the evident gaps from one taxon to the next and continuous disagreements among the experts—which in some instances appear to be driven by zeal and rhetoric rather than science—the level of understanding on the evolution of birds achieved in the past fifty years has swept old conceptions and opened the debate to the possibility of new (and why not, even radical) interpretations. Even though the discipline has made tremendous advancements regarding the way we look at dinosaurs and birds, everything seems to indicate that we should continue to stay tuned for the changes future discoveries may bring along.

References
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Appendix A
Figure extracted from Prum (2002).