The origin of birds has been a contentious topic within evolutionary biology for many years, but more recently a scientific consensus has emerged which holds that birds are a group of theropod dinosaurs that evolved during the Mesozoic Era. A close relationship between birds and dinosaurs was first proposed in the nineteenth century after the discovery of the primitive bird Archaeopteryx in Germany and has been all but confirmed since the 1960s by comparative anatomy and the cladistic method of analyzing evolutionary relationships. The ongoing discovery of feathered dinosaur fossils in the Liaoning Province of China has shed new light on the subject for both specialists and the general public. In the phylogenetic sense, birds are dinosaurs.

Birds share hundreds of unique skeletal features with dinosaurs, especially with derived maniraptoran theropods like the dromaeosaurids, which most analyses show to be their closest relatives. Although harder to identify in the fossil record, similarities in the digestive and cardiovascular systems, as well as behavioral similarities and the shared presence of feathers, also link birds with dinosaurs. The ground-breaking discovery of fossilized Tyrannosaurus rex soft tissue allowed comparison of cellular anatomy and protein sequencing of collagen tissue, both of which provided additional evidence corroborating the dinosaur-bird relationship.

Only a few scientists still debate the dinosaurian origin of birds, suggesting descent from other types of archosaurian reptiles. Even among those who support dinosaurian ancestry, the exact phylogenetic position of early birds within theropods remains controversial. The origin of bird flight is a separate but related question for which there are also several proposed answers.

Research history

Scientific investigation into the origin of birds began shortly after the 1859 publication of Charles Darwin's The Origin of Species, the ground-breaking book which described his theory of evolution by natural selection.^[1] In 1860, a fossilized feather was discovered in Germany's Late Jurassic Solnhofen Limestone. Christian Erich Hermann von Meyer described this feather as Archaeopteryx lithographica the next year,^[2] and Richard Owen described a nearly complete skeleton in 1863, recognizing it as a bird despite many features reminiscent of reptiles, including clawed forelimbs and a long, bony tail.^[3]

Biologist Thomas Henry Huxley, known as "Darwin's Bulldog" for his ferocious support of the new theory of evolution, almost immediately seized upon Archaeopteryx as a transitional fossil between birds and reptiles. Starting in 1868, Huxley made detailed comparisons of Archaeopteryx with various prehistoric reptiles and found that it was most similar to dinosaurs like Hypsilophodon and Compsognathus.^[4][5] The discovery in the late 1870s of the iconic "Berlin specimen" of Archaeopteryx, complete with a set of reptilian teeth, provided further evidence. Huxley was the first to propose an evolutionary relationship between birds and dinosaurs, although he was opposed by the very influential Owen, who remained a staunch creationist. Huxley's conclusions were accepted by many biologists, including Baron Franz Nopcsa,^[6] while others, notably Harry Govier Seeley,^[7] argued that the similarities were due to convergent evolution.

Heilmann and the 'thecodont' hypothesis

A turning point came in the early twentieth century with the writings of Gerhard Heilmann of Denmark. An artist by trade, Heilmann had a scholarly interest in birds and from 1913 to 1916 published the results of his research in several parts, dealing with the anatomy, embryology, behavior, paleontology and evolution of birds.^[8] His work, originally written in Danish as Vor Nuvaerende Viden om Fuglenes Afstamning, was compiled, translated into English and published in 1926 as The Origin of Birds.

Like Huxley, Heilmann compared Archaeopteryx and other birds to an exhaustive list of prehistoric reptiles, and also came to the conclusion that theropod dinosaurs like Compsognathus were the most similar. However, Heilmann noted that birds possessed clavicles fused to form a bone called the furcula ('wishbone'), and while clavicles were known in more primitive reptiles, they had not yet been recognized in dinosaurs. A firm believer in Dollo's Law, which states that evolution is not reversible, Heilmann could not accept that clavicles were lost in dinosaurs and re-evolved in birds, so he was forced to rule out dinosaurs as bird ancestors and ascribe all of their similarities to convergence. Heilmann stated that bird ancestors would instead be found among the more primitive 'thecodont' grade of reptiles.^[9] Heilmann's extremely thorough approach ensured that his book became a classic in the field and its conclusions on bird origins, as with most other topics, were accepted by nearly all evolutionary biologists for the next four decades,^[10] despite the discovery of clavicles in the primitive theropod Segisaurus in 1936.^[11] Clavicles and even fully developed furculae have since been identified in numerous other non-avian dinosaurs.^[12][13]

Ostrom, Deinonychus, and the Dinosaur Renaissance

The tide began to turn against the 'thecodont' hypothesis after the 1964 discovery of a new theropod dinosaur in Montana. In 1969, this dinosaur was described and named Deinonychus by John Ostrom of Yale University.^[14] The next year, Ostrom redescribed a specimen of Pterodactylus in the Dutch Teyler Museum as another skeleton of Archaeopteryx.^[15] The specimen consisted mainly of a single wing and its description made Ostrom aware of the similarities between the wrists of Archaeopteryx and Deinonychus.^[16]

In 1972, British paleontologist Alick Walker hypothesized that birds arose not from 'thecodonts' but from crocodile ancestors like Sphenosuchus.^[17] Ostrom's work with both theropods and early birds led him to respond with a series of publications in the mid-1970s in which he laid out the many similarities between birds and theropod dinosaurs, resurrecting the ideas first put forth by Huxley over a century before.^[18][19][20] Ostrom's recognition of the dinosaurian ancestry of birds, along with other new ideas about dinosaur metabolism,^[21] activity levels and parental care,^[22] began what is known as the Dinosaur Renaissance, which began in the 1970s and continues to this day.

Ostrom's revelations also coincided with the increasing adoption of phylogenetic systematics (cladistics), which began in the 1960s with the work of Willi Hennig.^[23] Cladistics is a method of arranging species based strictly on their evolutionary relationships, using a statistical analysis of their anatomical characteristics. In the 1980s, cladistic methodology was applied to dinosaur phylogeny for the first time and showed unequivocally that birds were a derived group of theropod dinosaurs.^[24] Early analyses suggested that dromaeosaurid theropods like Deinonychus were particularly closely related to birds, a result which has been corroborated many times since.^[25][26]

Feathered dinosaurs in China

The early 1990s saw the discovery of spectacularly preserved bird fossils in several Early Cretaceous geological formations in the northeastern Chinese province of Liaoning.^[27][28] In 1996, Chinese paleontologists described Sinosauropteryx as a new genus of bird from the Yixian Formation,^[29] but this animal was quickly recognized as a theropod dinosaur closely related to Compsognathus. Surprisingly, its body was covered by long filamentous structures. These were dubbed 'protofeathers' and considered to be homologous with the more advanced feathers of birds.^[30] Chinese and North American scientists described Caudipteryx and Protarchaeopteryx soon after. Based on skeletal features, these animals were non-avian dinosaurs, but their remains bore fully-formed feathers closely resembling those of birds.^[31] "Archaeoraptor," described without peer review in a 1999 issue of National Geographic,^[32] turned out to be a smuggled forgery,^[33] but legitimate remains continue to pour out of the Yixian, both legally and illegally. Feathers or "protofeathers" have been found on a wide variety of theropods in the Yixian,^[34][35] and the discoveries of extremely bird-like dinosaurs,^[36] as well as dinosaur-like primitive birds,^[37] have almost entirely closed the morphological gap between theropods and birds.

A small but vocal minority, led by ornithologists Alan Feduccia and Larry Martin, continues to assert that birds are instead the descendants of earlier archosaurs like Longisquama or Euparkeria.^[38][39] However, due to the mountain of evidence provided by comparative anatomy and phylogenetics, as well as the dramatic feathered dinosaur fossils from China, the idea that birds are derived dinosaurs, first championed by Huxley and later by Nopcsa and Ostrom, enjoys near-unanimous support among today's paleontologists.^[10]

Features linking birds and dinosaurs

Over a hundred distinct anatomical^[40] features are shared by birds and theropod dinosaurs. Some of the more interesting similarities are discussed here:

Feathers

Main article: Feathered dinosaurs

Archaeopteryx, the first good example of a "feathered dinosaur", was discovered in 1861. The initial specimen was found in the Solnhofen limestone in southern Germany, which is a lagerstätte, a rare and remarkable geological formation known for its superbly detailed fossils. Archaeopteryx is a transitional fossil, with features clearly intermediate between those of modern reptiles and birds. Discovered just two years after Darwin's seminal The Origin of Species, its discovery spurred the nascent debate between proponents of evolutionary biology and creationism. This early bird is so dinosaur-like that, without a clear impression of feathers in the surrounding rock, at least one specimen was mistaken for Compsognathus.^[41]

Since the 1990s, a number of additional feathered dinosaurs have been found, providing even stronger evidence of the close relationship between dinosaurs and modern birds. Most of these specimens were unearthed in Liaoning province, northeastern China, which was part of an island continent during the Cretaceous period. Though feathers have been found only in the lagerstätte of the Yixian Formation and a few other places, it is possible that non-avian dinosaurs elsewhere in the world were also feathered. The lack of widespread fossil evidence for feathered non-avian dinosaurs may be due to the fact that delicate features like skin and feathers are not often preserved by fossilization and thus are absent from the fossil record.

A recent development in the debate centers around the discovery of impressions of "protofeathers" surrounding many dinosaur fossils. Said protofeathers suggest that the tyrannosauroids may have been feathered.^[42] However, others claim that these protofeathers are simply the result of the decomposition of collagenous fiber that underlaid the dinosaurs' integument.^[39]

The feathered dinosaurs discovered so far include Beipiaosaurus, Caudipteryx, Dilong, Microraptor, Protarchaeopteryx, Shuvuuia, Sinornithosaurus, Sinosauropteryx and Jinfengopteryx, along with dinosaur-like birds, like Confuciusornis, which are anatomically closer to modern avians. All of them have been found in the same area and formation, in northern China. The Dromaeosauridae family, in particular, seems to have been heavily feathered and at least one dromaeosaurid, Cryptovolans, may have been capable of flight.

Skeleton

Because feathers are often associated with birds, feathered dinosaurs are often touted as the missing link between birds and dinosaurs. However, the multiple skeletal features also shared by the two groups represent the more important link for paleontologists. Furthermore, it is increasingly clear that the relationship between birds and dinosaurs, and the evolution of flight, are more complex topics than previously realized. For example, while it was once believed that birds evolved from dinosaurs in one linear progression, some scientists, most notably Gregory S. Paul, conclude that dinosaurs such as the dromaeosaurs may have evolved from birds, losing the power of flight while keeping their feathers in a manner similar to the modern ostrich and other ratites.

Comparisons of bird and dinosaur skeletons, as well as cladistic analysis, strengthens the case for the link, particularly for a branch of theropods called maniraptors. Skeletal similarities include the neck, pubis, wrist (semi-lunate carpal), arm and pectoral girdle, shoulder blade, clavicle and breast bone.

Lungs

Large meat-eating dinosaurs had a complex system of air sacs similar to those found in modern birds, according to an investigation which was led by Patrick O'Connor of Ohio University. The lungs of theropod dinosaurs (carnivores that walked on two legs and had birdlike feet) likely pumped air into hollow sacs in their skeletons, as is the case in birds. "What was once formally considered unique to birds was present in some form in the ancestors of birds", O'Connor said. The study was funded in part by the National Science Foundation.^[43]

Heart and sleeping posture

Modern computerized tomography (CT) scans of a dinosaur chest cavity (conducted in 2000) found the apparent remnants of complex four-chambered hearts, much like those found in today's mammals and birds.^[44] The idea is controversial within the scientific community, coming under-fire for bad anatomical science^[45] or simply wishful thinking.^[46] A recently discovered troodont fossil demonstrates that the dinosaurs slept like certain modern birds, with their heads tucked under their arms.^[47] This behavior, which may have helped to keep the head warm, is also characteristic of modern birds.

Reproductive biology

A discovery of features in a Tyrannosaurus rex skeleton recently provided even more evidence that dinosaurs and birds evolved from a common ancestor and, for the first time, allowed paleontologists to establish the sex of a dinosaur. When laying eggs, female birds grow a special type of bone in their limbs. This medullary bone, which is rich in calcium, forms a layer inside the hard outer bone that is used to make eggshells. The presence of endosteally-derived bone tissues lining the interior marrow cavities of portions of the Tyrannosaurus rex specimen's hind limb suggested that T. rex used similar reproductive strategies, and revealed the specimen to be female.

Brooding and care of young

Several Citipati specimens (formerly referred to as Oviraptor) have been found resting over the eggs in its nest in a position most reminiscent of brooding.

Numerous dinosaur species, for example Maiasaura, have been found in herds mixing both very young and adult individuals, suggesting rich interactions between them.

A dinosaur embryo was found without teeth, which suggests some parental care was required to feed the young dinosaur, possibly the adult dinosaur regurgitated food into the young dinosaur's mouth (see altricial). This behaviour is seen in numerous bird species; parent birds regurgitate food into the hatchling's mouth.

Gizzard

Another piece of evidence that birds and dinosaurs are closely related is the use of gizzard stones. These stones are swallowed by animals to aid digestion and break down food and hard fibres once they enter the stomach. When found in association with fossils, gizzard stones are called gastroliths. Because a particular stone could have been swallowed at one location before being carried to another during migration, paleontologists sometimes use the stones found in dinosaur stomachs to establish possible migration routes.

Molecular evidence and soft tissue

One of the best examples of soft tissue impressions in a fossil dinosaur was discovered in Petraroia, Italy. The discovery was reported in 1998, and described the specimen of a small, very young coelurosaur, Scipionyx samniticus. The fossil includes portions of the intestines, colon, liver, muscles, and windpipe of this immature dinosaur.^[48]

In the March 2005 issue of Science, Dr. Mary Higby Schweitzer and her team announced the discovery of flexible material resembling actual soft tissue inside a 68-million-year-old Tyrannosaurus rex leg bone from the Hell Creek Formation in Montana. After recovery, the tissue was rehydrated by the science team. The seven collagen types obtained from the bone fragments, compared to collagen data from living birds (specifically, a chicken), reveal that older theropods and birds are closely related.

When the fossilized bone was treated over several weeks to remove mineral content from the fossilized bone marrow cavity (a process called demineralization), Schweitzer found evidence of intact structures such as blood vessels, bone matrix, and connective tissue (bone fibers). Scrutiny under the microscope further revealed that the putative dinosaur soft tissue had retained fine structures (microstructures) even at the cellular level. The exact nature and composition of this material, and the implications of Dr. Schweitzer's discovery, are not yet clear; study and interpretation of the artifacts is ongoing.^[49]

The successful extraction of ancient DNA from dinosaur fossils has been reported on two separate occasions, but upon further inspection and peer review, neither of these reports could be confirmed.^[50] However, a functional visual peptide of a theoretical dinosaur has been inferred using analytical phylogenetic reconstruction methods on gene sequences of related modern species such as reptiles and birds.^[51] In addition, several proteins have putatively been detected in dinosaur fossils,^[52] including hemoglobin.^[53]

Debates

Origin of bird flight

Two main theories have been proposed for the origins of flight: arboreal ("trees down") and cursorial ("ground up")

The cursorial theory of the origin of flight was first proposed by Samuel Wendell Williston, and elaborated upon by Baron Nopcsa. This hypothesis proposes that some fast-running animals with long tails used their arms to keep balance while running. Increasing the surface area of the outstretched arms could have helped them, and Nopsca theorized that the scales of the forearms had become elongated, evolving into feathers. The feathers could also have been used as a trap to catch insects or other prey. Progressively, the animals would have sprung on longer distances, helped by their forecoming wings. Nopsca also proposed the idea that three stages existed in the evolution of flight. First, passive flight was realized, in which the developed wing structures served as a sort of parachute. Second, active flight was possible, in which the animal achieved flight by flapping its wings. He used Archaeopteryx as an example of this second stage. Finally, birds gained the ability to soar.^[54]

The arboreal hypothesis states that the ancestors of birds lived in trees. They would have sprung from branch to branch, favoring the evolution of lengthened metatarsals and a backwards-directed hallux in order to grasp branches. The front limbs and rear limbs would have become adapted for separate purposes; the front for climbing and the rear for leaping. It proposes that the forelimbs, used for climbing, remained long, rather than being reduced, as is common in the evolution of cursorial animals.^[54] The surface of their 'wings' progressively increased to develop a good gliding ability. After gliding, they would have begun to flap to increase their flying efficiency. There is little evidence for tree-climbing dinosaurs—only Epidendrosaurus and maybe Microraptor—compared to the numerous long-legged, ground-dwelling theropods. However, the fact that forest sediments are only rarely preserved could account for this scarcity.

The initial ability to develop true avian, as opposed to gliding or four-winged, flight apparently evolved in a group of species. These then evolved into different lineages, each featuring a slightly different approach to the challenge, and probably were well advanced in this process already by the time of Archaeopteryx. Thus, the question might be rephrased more accurately: "did the ancestors of Neornithes develop flight from the ground up or from trees (slopes, cliffs...) down?"

Secondary flightlessness in dinosaurs

A theory, defended notably by Gregory Paul in his books Predatory Dinosaurs of the World (1988) and Dinosaurs of the Air (2002), suggests that some groups of carnivorous dinosaurs, especially deinonychosaurs but perhaps others such as oviraptorosaurs, therizinosaurs, alvarezsaurids and ornithomimosaurs, are actually descended from forms that could fly. This theory states that Archaeopteryx-like creatures are less closely related to extant birds than these dinosaurs are.

Though by most current cladistic analyses, Archaeopteryx is closer to birds than deinonychosaurs or oviraptorosaurs, such animals as Microraptor or Sinornithosaurus apparently lie close to the base of the deinonychosaurian clade and appear to have more flight adaptations than later deinonychosaurs. Archaeopteryx is still basal enough in its characteristics to suggest that early/mid-Cretaceous descendants of the earliest birds could theoretically have reverted to a more dinosaurian mode of life. Hesperornis, whose ancestors became secondarily flightless around the Jurassic/Cretaceous boundary, suggests that the avian beak was less likely to get lost again than avian flight ability, but that teeth might have re-evolved more easily than it seems at first glance. The fact that a modern chicken was born with teeth shows that that particular gene was able to lie dormant for nearly 100 million years and then re-appear in a mutant chicken.^[55]

By inserting the new data provided by the newly described tenth Archaeopteryx fossil into a major existing cladistic data matrix, Mayr et al. (2005) showed that Archaeopteryx was in a sister clade of a clade consisting of both two groups that are traditionally seen as non-avian theropods, namely the Deinonychosauria and the Troodontidae, as well as the more derived birds, represented in the analysis by Confuciusornis. As in Paul's hypothesis, in this scenario the Deinonychosauria and the Troodontidae are part of Aves, the bird lineage proper, and secondarily flightless. This is however a matter of taxonomical and phylogenetic definition;^[56] the only thing that appears clearly from Mayr et al.'s study is that of the two primitive birds compared — neither of which is necessarily very close to the ancestors of modern birds — Confuciusornis was closer to a distinct group of theropods, traditionally seen as non-avian, than to Archaeopteryx.

The paper launched a vigorous debate, in which the authors made clear that they considered their data still equivocal as to whether bird flight or major theropod diversification came first. Neither birds more modern than Confuciusornis, nor many interesting theropods were included, so the main point of the study is to harden the case that bird-like flight was present not only in the ancestors of modern birds. Whether it was developed independently several times as suggested by Barsbold or only once, with most if not all terrestrial theropods being secondarily flightless, is not resolved; although statistical evaluation of the data matrix tentatively suggested the latter, reliability is insufficient to draw a conclusion in this respect.

Digit homology

There is a debate between embryologists and paleontologists whether the hands of theropod dinosaurs and birds are essentially different, based on phalangeal counts, a count of the number of phalanges (fingers) in the hand.

Embryologists number the digits of birds II-III-IV on the basis of development in the egg.^[57] This is based on the fact that in most amniotes, the first digit to form in a 5-fingered hand is digit IV, which develops a primary axis. Therefore, embryologists identify the primary axis in birds as digit IV, and the surviving digits as II-III-IV.

The fossils of theropod dinosaurs and their immediate ancestors imply that the three digits left on advanced theropod hands are I-II-III. If this is true, then the II-III-IV development of digits in birds is incompatible with theropod (dinosaur) ancestry. However, with no ontogenical basis to definitively state which digits are which on a theropod hand, the labelling of the theropod hand is inconclusive.

However, paleontologists have traditionally identified avian digits as I-II-III. They argue that the digits of birds number I-II-III, just as those of theropod dinosaurs do, by the conserved phalangeal formula. The phalangeal count for archosaurs is 2-3-4-5-3; many archosaur lineages have a reduced number of digits, but have the same phalangeal formula in the digits that remain. The three digits of dromaeosaurs, and Archaeopteryx have the same phalangeal formula of I-II-III as digits I-II-III of basal archosaurs. Because maniraptorans are descended from dromaeosaurs, the reduction of digits in maniraptorans is believed to have occurred from the inside to the outside. Therefore, the lost digits would be V and IV. If this is true, then modern birds would also possess digits I-II-III, with further reduction during evolution.^[57]

Furculae

At one time, it was believed that dinosaurs lacked furculae (fused left and right clavicles, or "wishbones"). This was considered an overwhelming argument to refute the dinosaur ancestry of birds by Heilmann (1926). However, it has been shown since then that numerous tetanuran theropod species indeed have a furcula,^[58] apparently a tetanuran innovation. The presence of a furcula even in Allosaurus, a relatively basal tetanuran, has been confirmed, and in an Early Jurassic theropod^[59] and Late Triassic coelophysids, among others.

Footnotes

References

• Barsbold, Rinchen (1983): O ptich'ikh chertakh v stroyenii khishchnykh dinozavrov. ["Avian" features in the morphology of predatory dinosaurs]. Transactions of the Joint Soviet Mongolian Paleontological Expedition 24: 96-103. [Original article in Russian.] Translated by W. Robert Welsh, copy provided by Kenneth Carpenter and converted by Matthew Carrano. PDF fulltext
• Bostwick, Kimberly S. (2003): Bird origins and evolution: data accumulates, scientists integrate, and yet the "debate" still rages. Cladistics 19: 369–371. doi:10.1016/S0748-3007(03)00069-0 PDF fulltext
• Dingus, Lowell & Rowe, Timothy (1997): The Mistaken Extinction: Dinosaur Evolution and the Origin of Birds. W. H. Freeman and Company, New York. ISBN 0-7167-2944-X
• Dinosauria On-Line (1995): Archaeopteryx's Relationship With Modern Birds. Retrieved 2006-SEP-30.
• Dinosauria On-Line (1996): Dinosaurian Synapomorphies Found In Archaeopteryx. Retrieved 2006-SEP-30.
• Heilmann, G. (1926): The Origin of Birds. Witherby, London. ISBN 0-486-22784-7 (1972 Dover reprint)
• Mayr, Gerald; Pohl, B. & Peters, D. S. (2005): A Well-Preserved Archaeopteryx Specimen with Theropod Features. Science 310(5753): 1483-1486. doi:10.1126/science.1120331
• Olson, Storrs L. (1985): The fossil record of birds. In: Farner, D.S.; King, J.R. & Parkes, Kenneth C. (eds.): Avian Biology 8: 79-238. Academic Press, New York.

External links

• DinoBuzz A popular-level discussion of the dinosaur-bird hypothesis