James M Clark. Encyclopedia of Life Sciences: Supplementary Set. Volume 22. Chichester, UK: Wiley, 2007.

History of the Bird Origin Debate

The skeleton of the primitive bird Archaeopteryx was discovered just two years after Darwin published On the Origin of Species in 1859 and was quickly cited both as evidence of a transitional ‘missing link’ between birds and reptiles and more generally as proof of the utility of the fossil record in preserving evolutionary intermediates. Bearing teeth and a long bony tail absent in all living birds, yet with exquisitely preserved feathers on its wings and tail, it became the main focus of all studies on bird origins for over a century. Although the eminent palaeontologist Sir Richard Owen, founder of the British Museum of Natural History, disputed its support of Darwin’s ideas, the idea of evolution, if not Darwin’s proposed mechanisms, was widely accepted by the end of the nineteenth century, in part due to the debating skills of Sir Thomas Huxley. Huxley meanwhile presented a convincing case (e.g. Huxley, 1870) that Archaeopteryx and birds were closely related to a poorly known group of giant reptiles that was first named by Owen, the Dinosauria.

A lengthy treatise on bird origins published by Gerhard Heilmann in 1926 summarized the evidence known at that time, including several toothed birds from the Cretaceous chalks of Kansas unearthed in the late nineteenth century. Heilmann noted the many features shared by Archaeopteryx and the dinosaurs of the group Theropoda, but because Archaeopteryx and birds had fused their clavicles (the collar bones of humans) into a furcula (‘wish bone’), and no clavicles were known in dinosaurs, he concluded that birds must have evolved from some dinosaur precursor before theropods lost their clavicles. Other ideas were proposed (e.g. that ratite birds, including ostriches and emus, evolved from dinosaurs independent of other birds), but Heilmann’s book and his conclusion had a large impact on the field.

In 1970, John Ostrom was examining specimens of the flying reptiles known as pterosaurs from the Solnhofen Limestone of Bavaria, the same deposits that produced Archaeopteryx, when he realized that a specimen identified as a pterosaur in the Teyler Museum in Haarlem, The Netherlands, actually was a specimen of Archaeopteryx. Ostrom had recently described a new kind of theropod dinosaur from Montana, Deinonychus antirrhopus, and in shifting his focus from pterosaurs to Archaeopteryx he realized how similar Deinonychus is to Archaeopteryx. Ostrom meticulously compared Archaeopteryx with theropod dinosaurs and other fossil reptiles and in 1976 presented a detailed argument for a close relationship between birds and theropod dinosaurs. In addition to the many similarities he found between Deinonychus and Archaeopteryx, he pointed out that clavicles were indeed present in some the-ropod dinosaurs. Ostrom’s arguments prompted a heated debate that in some ways paralleled those of the late nineteenth century, in which the theropod hypothesis competed with alternative hypotheses of a closer relationship between birds and crocodilians or, more vaguely, with unspecified primitive members of the group to which dinosaurs, birds and crocodilians belong, the Archosauria.

Cladistic Analysis

During the 1970s, at the time that Ostrom formulated his argument, intense debate was also taking place on the best means of determining the evolutionary relationships among organisms. Dissatisfied with subjective interpretations of organismal relationships and armed with new computer technologies allowing quantitative analyses of large data sets, many evolutionary biologists turned to a technique known as cladistic analysis to study relationships. The modern debate about bird origins is framed largely within the context of cladistic analysis.

All analyses of evolutionary relationships are based upon the evidence provided by shared similarities, coupled in some forms of analysis by evidence from differences. Similarity is used here in a very general sense, and includes genetic similarity, such as the presence of a particular nucleotide at the same position within a gene, and anatomical similarity, such as the presence or absence of a particular bone or muscle. Molecular and other soft tissue evidence is largely absent from fossils, so the study of fossils relies almost exclusively on anatomical, especially skeletal similarities.

Cladistic analysis differs from other approaches to inferring evolutionary relationships in that it considers only the presence of shared similarities, not their absence. Thus, the shared presence of feathers in all living birds is evidence that they are related and form a group, but the absence of feathers in other organisms provides no evidence that they are related to one another or form a group. Shared similarities are used to identify clades, groups of organisms that are more closely related to one another than to any other organism. Because of the hierarchical organization of evolutionary relationships, clades are nested within other clades; for example, humans are members of the primate clade within the mammalian clade.

Cladistic analyses of fossil and living vertebrates (those animals with back bones) in the last twenty-five years have, with a few exceptions, largely confirmed the general outlines of evolutionary relationships inferred by more traditional methods. Birds belong to a group that includes mammals and reptiles called the Amniota, and although birds share some similarities with mammals, such as warm-bloodedness, cladistic analyses that include a large variety of fossil amniotes indicate that, among living animals, birds are most closely related to crocodilians. For example, both crocodilians and birds have air sacs in the ear regions of their skulls that no other reptile possesses. Molecular evidence of amniote relationships is somewhat in conflict with anatomical evidence, especially regarding the relationships of turtles, but generally supports a bird–crocodilian relationship. Because crocodilians are more closely related to birds than they are to other reptiles, the group Reptilia has been redefined to include birds, as reflected in the description of birds as ‘glorified reptiles’. The group containing crocodilians and birds is called the Archosauria, and includes dinosaurs and some other fossil reptiles.

The search for bird origins is therefore a search for the group of fossil archosaurs to which birds are most closely related. Fossil archosaurs include a variety of groups in addition to dinosaurs, such as pterosaurs and several different extinct relatives of crocodilians, such as aetosaurs and phytosaurs. Cladistic analyses of fossil archosaurs, such as the pioneering analysis published by Jacques Gauthier in 1986, all generally reach the same result—birds are most closely related to two groups of theropod dinosaurs, the dromaeosaurs (including Deinonychus) and the troodontids. Birds, dromaeosaurs and troodontids all belong to a group of theropods called the Coelurosauria. Also included in coelurosaurs are the Ornithomimosauria, Oviraptorosauria, Therizinosauroidea, Alvarezsauridae and Tyrannosauridae, as well as several other species.

The Evidence for Bird-Dinosaur Relationships

The evidence for the close relationship of birds to theropod dinosaurs is based almost exclusively on features of the skeleton. Much of it therefore comprises subtle differences in muscle scar size and placement or the shape of parts of bones. In general, the skeletal features that distinguish birds from other archosaurs, such as crocodilians, relate to several suites of changes evident in the skeleton:

1. Loss of teeth, increased size of the forebrain, and increased movement between parts of the skull.
2. Curvature of the neck and invasion of the respiratory system into some vertebrae.
3. Modifications of the shoulder girdle, ribs, breast bone, and forearms related to movements involved in breathing and flying.
4. Fusion of the wrist and finger bones and reduction in the number of fingers.
5. Elongation of the pelvis, backward rotation of one of its three bones, the pubis, and reduction of the tail.
6. Fusion of the ankle joint and reduction of the outside toes of the foot, with the fifth toe rotated to the back of the foot.

Nearly all of these features are found in theropod and other dinosaurs, and the similarities of the skeleton of dromaeosaurs and troodontids to primitive birds are particularly striking. For example, not only are the fingers reduced to three but the bones in the wrist and hand of dromaeosaurs and troodontids are almost identical to those of Archaeopteryx. The forebrain of troodontids is enlarged (that of dromaeosaurs has not been measured), as determined from the size of the brain cavity, and cavities presumed to be from the respiratory system are found in the curved neck of many theropods. Clavicles are now known in some the- ropods, and a true furcula is known to have been present in several coelurosaurs. The shoulder girdle of dromaeosaurs and troodontids is similar to that of birds in that the socket for the upper arm is rotated to face to the side rather than backwards, and the main shoulder bones—the scapula and coracoid—are nearly identical to those of Archaeopteryx. Unlike in crocodilians, dromaeosaurs and some other coelurosaurs have a large breast bone and two bony segments to the ribs, forming the basic mechanism that in birds operates the respiratory system. The pelvis of dromaeosaurs is longer than in primitive theropods but shorter than in birds, and the pubis has been rotated partially backward. The foot of most theropods has reduced the first toe and parts of the fifth toe as in Archaeopteryx and birds, and differs mainly in only one feature: the fifth toe of theropods had not yet rotated backwards.

Evidence for the theropod–bird relationship has also come from non-anatomical features. The microscopic structure of eggshells and bone provides further detailed similarities linking theropods and birds to the exclusion of crocodilians. Most surprisingly, multiple specimens of theropod dinosaurs of the group Oviraptorosauria have been found sitting directly on nests in the same position taken by birds; crocodilians bury their nests and do not sit directly on the eggs.

In short, in nearly every aspect of the skeleton, theropod dinosaurs share features with birds that are not found in other fossil archosaurs. Counted separately, these features number in the hundreds and group birds within the coelurosaurs, coelurosaurs within theropods, and theropods within dinosaurs. No other group of fossil archosaurs approaches this number of shared similarities with birds.

The advent of cladistic analysis also prompted a some-what different approach to taxonomy, the subdiscipline of evolutionary biology devoted to naming groups of organisms. For much of the previous century taxonomists had used an eclectic array of criteria for naming groups in addition to their evolutionary relationships, such as how distinctive is a group. Cladistic taxonomists argued instead that taxonomy should simply reflect the hierarchy of relationships among organisms without regard to distinctiveness or the other criteria used by traditional taxonomists; thus, taxonomic groups should all be clades. In the case of birds, although they were generally regarded as most closely related to crocodilians and other archosaurs, historically they were placed outside of the reptiles in their own group, Aves, to reflect their distinctiveness. In cladistic taxonomy, however, birds are a group not only within reptiles but within dinosaurs, theropods and coelurosaurs. Thus, birds are reptiles, dinosaurs and coelurosaurs.

The Feathered Dinosaurs of Liaoning, China

Soft tissue preservation is rare in the fossil record, so the discovery of dinosaur-age deposits in northeastern China that preserve complete skeletons of birds with feathers and mammals with hair was one of the most important events in twentieth-century vertebrate palaeontology. Soon after fossil fish and birds were discovered in these deposits—the Yixian Formation in the province of Liaoning near Sihetun—came startling fossils of theropod dinosaurs with feathers. The first of these discoveries, Sinosauropteryx, had only short, filamentous feathers, but subsequent discoveries, Protarchaeopteryx and Caudipteryx, possessed true feathers with vanes. Some of these feathered theropods, such as Sinornithosaurus, were dromaeosaurs, while Caudipteryx appears to be related to another group of theropods, the oviraptorosaurians, and Beipiaosaurus to an enigmatic coelurosaurian group known as therizinosaurs.

In the late 1990s a second set of beds preserving feathered dinosaurs was discovered in western Liaoning, over 130 km from the first sites. Unfortunately, parts of the first feathered dinosaur specimen from these deposits were glued together with a fossil bird by a commercial fossil dealer to make it easier to sell at the Tucson Gem and Mineral Show, producing a chimaera called Archaeoraptor that fooled some people (including National Geographic Magazine). The original specimen of this feathered dinosaur, subsequently called Microraptor, shows that it is among the most bird-like of the theropods. Some spectacular specimens have been discovered at this site, including one that appears to have long feathers not only on its wings but on its hindlimbs.

Currently these feathered dinosaurs include six named species represented by several dozen specimens, with new discoveries appearing every year (the first reports of these discoveries are compiled in Gee, 2002). Incorporated into cladistic analyses, they are beginning to provide the broad outline of the evolution of feathers. The theropods that are most distantly related to birds, such as Sinosauropteryx, have only filamentous feathers, sometimes with simple branching. Those most closely related to birds, such as dromaeosaurs like Microraptor, possess both filamentous feathers and feathers with vanes in the centre. Surprisingly, the presence of feathers in theropod dinosaurs now demonstrates that these structures all evolved before the appearance of powered flight, as none of the theropods appears to be capable of flying.

The historical accident of the discovery of Archaeopteryx before the feathered dinosaurs of China has had a lasting effect on how scientists recognize what is and is not a bird. Because it possesses feathers, considered by many to be the sine qua non of birds, Archaeopteryx became the fundamental point of reference for defining the group. Many ornithologists even now consider birds by definition to have begun with the origin of Archaeopteryx; so that all forms thought to be its descendants are birds and anything that is not its descendant is not a bird. But the feathered dinosaurs of China and recent discoveries of primitive birds now demonstrate that evolution was more complicated than this, and that the arbitrary definition of birds as the descendants of Archaeopteryx is overly simplistic. Feathers might still be used to define what is and is not a bird, but the variety of structures, from simple to complex, preserved in the different feathered dinosaurs obscure the definition of what is a feather. An alternative approach to the problem is simply to define birds as all living birds and the descendants of their closest common ancestor, but this has not been widely embraced as it would exclude Archaeopteryx and several other fossil forms that historically have been considered birds. This situation reflects a common, if paradoxical, occurrence in palaeontology: the better the fossil record of an evolutionary transition becomes, the more difficult it is to draw boundaries between groups.

Criticisms of Birds as Dinosaurs

In spite of the overwhelming evidence for the theropod–bird relationship, it has received some well-publicized criticisms (many of which are summarized by Alan Fedducia). However, none of the proposed alternative relationships are supported by stronger evidence from shared similarities, and the one valid weakness is insufficient to indicate that birds are related to some other group.

Birds are related to another group of fossil reptiles

Several non-dinosaurian fossils have been discussed as possibly being closely related to birds. At the same time that Ostrom formulated his argument for theropod dinosaurs, Alick Walker and, independently, Larry Martin argued that a group of primitive crocodilian relatives, sphenosuchians, were also closely related to birds. Unlike living crocodilians, sphenosuchians were long-limbed terrestrial animals that share several similarities in the skull with birds. However, all fossil crocodilians lack nearly all of the features of the body skeleton shared by theropods and birds, and work on the-ropod dinosaurs by Philip Currie and others later showed that some of them possessed the same features that Walker and Martin suggested tied sphenosuchians to birds. Several poorly known forms from the beginning of the age of dinosaurs have been looked to as possible bird relatives, including Megalancosaurus and Longisquama. However, skeletal evidence indicates that Megalancosaurus is not even an archosaur, and is instead related to a group called Prolacertiformes with no relevance to birds. Longisquama is an intriguing fossil from late deposits in Kazakhstan that preserves long scale-like structures that some have suggested to be feather precursors. However, the skeleton of Longisquama is so poorly preserved that few features shared with birds have been identified, and the suggestion that the scales had a feather-like internal structure was later shown to be wrong.

The development of the hand in birds indicates that the fingers are different from those of theropods

Developmental studies of the wing of birds, especially chickens, suggest that the three fingers are from the middle of the hand, the second to fourth of the original five. Cladistic analyses of archosaurs suggest instead that the fingers of theropods are the first to third, because more distant relatives possess the fourth and fifth fingers on the outside of the hand. This is indeed a paradox, and at first it might seem to present an insurmountable obstacle to the bird–dinosaur hypothesis. How could the first finger of theropod dinosaurs become the second finger of birds? However, recent discoveries in developmental genetics indicate that such positional shifts are possible during evolution, so that the fingers could have maintained their individual shapes but shifted position at some point during the evolution of birds. Similar shifts have been documented in other parts of the skeleton, such as the vertebral column, where vertebrae maintain a particular shape but develop in a different position. Unfortunately, there is no direct evidence available to test this hypothesis, since we know nothing of the development of the hand in fossil birds and theropods. In any case the skeletal evidence from theropod dinosaurs is so strong that even if the features of the hand are each considered as evidence against the theropod hypothesis, the other evidence still overwhelmingly places birds with theropods.

Theropod dinosaurs occur too late in the fossil record to be ancestral to birds

This criticism stems from the fact that most (but not all) of the theropod dinosaurs (including the feathered Chinese ones) closely related to birds occur later in time than Archaeopteryx. For example, definitive specimens of dromaeosaurs and troodontids first appear in the fossil record thirty or forty million years after Archaeopteryx (although frag-mentary fossils from older deposits might belong to dromaeosaurs). Thus, they could not be direct ancestors of Archaeopteryxand birds. However, palaeontologists generally do not look for direct ancestors in the fossil record, because they are rare and difficult to identify as such. Instead, the overall pattern of relationships among organisms—the evolutionary groupings discovered by cladistic analysis—are evident from their shared similarities, regardless of the age of the fossils. As an example, the near absence of fossil chimpanzees and gorillas in the fossil record does not affect the interpretation by anthropologists that gorillas and chimpanzees separated from humans at least five million years ago, based upon the presence of fossil humans of that age. In any case, the fossil record of theropods includes some forms that are closely related to birds and older than Archaeopteryx, and a theropod origin for birds implies the same or fewer gaps in the fossil record than does any alternative hypothesis. A potentially important form is Protoavis from Texas, which is tens of millions of years older than Archaeopteryx, but questions have been raised about the accuracy of its description by Chatterjee.

The respiratory system of birds could not have evolved from that of theropods

Birds and crocodilians both have peculiar respiratory systems, and it has been suggested that dinosaurs had a crocodilian-like respiratory system. The crocodilian system involves a muscle between the liver and pelvis that, when tensed, fills the lungs by pulling the liver into the abdomen and creating a negative pressure in the lungs that draws in the air. Birds, on the other hand, have a complex respiratory system in which air passes in a single direction through its chambers, unlike the in-and-out tidal flow of all other land vertebrate lungs. Birds move air through their lungs by rocking their breast bone up and down, and they lack any sign of the muscle attached to the liver in crocodilians. The feathered dinosaur Sinosauropteryx was interpreted as having a crocodilian-like respiratory system on the basis of poorly preserved abdominal tissues, and another small theropod, Scipionyx from Italy, was identified as preserving portions of the muscle that in crocodilians spans the liver and pelvis. However, both of these identifications have been disputed, another theropod specimen has been identified as preserving portions of a bird-like air sac within the pelvis, and the basic skeletal features of the sternal rocking mechanism are present in some theropods such as oviraptorids. In any case the presence of a crocodilian-like respiratory system in theropods would not preclude the evolution of a bird-like system in their descendants, and the argument is moot.

Birds must have evolved from an arboreal animal, and theropods were not arboreal

This criticism, from Feduccia, rests upon the assumption that the immediate ancestor of Archaeopteryx must have been arboreal because flight must have evolved facilitated by gravity, and since theropod dinosaurs are not arboreal they cannot be ancestors. However, no modern palaeontologist has suggested that any of the known theropod dinosaurs were the immediate, direct ancestors of birds, and even if there was an arboreal ancestor to Archaeopteryx (which is conjectural) there is every reason to believe it would have been a theropod. For example, the recently discovered feathered dinosaur Microraptor has gracile limbs and other features suggesting that it may have been arboreal. More importantly, this kind of argument reverses the logic of science; rather than using the evidence from fossils to test ideas of what the ancestors of birds might have been like, it instead tries to dictate what they must have been like regardless of the evidence.