BIRDS

    Birds were the second of three vertebrate groups to evolve flight (pterosaurs, birds, and bats).   What makes a bird a bird?  They have feathers, a large brain, a developed sense of vision, fused wrist bones and metacarpals (forming a carpometacarpus), fused ankle and metatarsals (forming a tarsometatarsus), a pygostyle (fused tail bones), a furcula or fused clavicles (wishbone), fusion in other parts of the skeleton (such as the synsacrum—the pelvis and sacral vertebrae), a large keel on the sternum for the attachment of flight muscles, a foot three forward facing toes and one backward facing toe, a lack of teeth, and pneumatic bones (hollow bones with holes that enter into air cavities inside the bones). 

     Birds and mammals are the major groups of endothermic vertebrates (although endothermy is known in a few members of other groups) and share some features based on this, including some molecular similarities of molecules that carry oxygen, which is important in endothermy.  Despite this similarity with mammals, the closest relatives of birds alive today are crocodiles.  This can be shown both through a cladistic analysis of anatomical and physiological traits, through molecular evidence, and through embryological evidence.  Crocodiles and birds share a number of anatomical features and share the greatest similarity in a number of protein and gene sequences (crystallin, rhodopsin, Spi, pancreatic polypeptide, prolactin, ERVs, 28SrRNA, 12SrRNA, 16SrRNA, tRNA^val) (Hedges, 1994, Hedges, 1995; Kojima, 1999, Shintani, 2000, Bromham, 2002).  Anatomical, embryological, and genetic evidence group birds among the reptiles rather than with mammals.

      Are birds dinosaurs?  In 1863, it was observed that the legs of embryonic birds were similar to those of Compsognathus (Gauthier, 2001).In 1866, Haekel concluded that birds were reptilian in their characteristics.  Thomas Huxley proposed that birds evolved from dinosaurs in 1868 but the prevailing view became that birds descended from more primitive archosaurs and that any common traits between birds and dinosaurs would be common adaptations to a bipedal lifestyle. Heilmann compared the coelurosaur theropods to birds in 1926.  In 1973, John Ostrom renewed interest in this origin from dinosaurs after new fossil finds.  Cladistically, birds should be classified as dinosaurs if they descended from dinosaurs—they would simply be modified dinosaurs (in the same way that mammals are modified reptiles).  If this link to dinosaurs seems new, it is because this is a very exciting time: more than 3 times the number of prehistoric bird skeletons have been found since 1990 as were found in all the years previous and there are similarly exciting discoveries from theropod dinosaurs as well.  It is now the consensus that birds are most closely related to coelurosaurid maniraptoran theropods such as Deinonychus and Velociraptor.

      The major obstacle to the dinosaur ancestry of birds is the embryological development of the hand in modern birds.  In theropods, the 4^th and 5^th fingers were reduced while it seems (from embryological evidence) the avian hand contains digits II, III, and IV as opposed to the theropod I, II, III (Burke, 1997; Hinchliffe, 1997).  The most primitive bird Archaeopteryx utilized digits I, II, and III in its wing, just like the hand of dinosaurs (Padian, 2001).

     Although this is a serious point, it should be stressed that the homologies between bird and dinosaurian hands are simply enormous.  The wings of Archaeopteryx and the arms of Velociraptor are virtually identical in structure including the same phalangeal count and shape and the prominence of a semilunar carpal bone. 

     Genetic and embryological evidence can reconcile this apparent discrepancy in the identity of digits.  Some have proposed that in embryonic development, modern bird digits 2,3,and 4 develop according to the developmental mechanisms of ancestral 1,2, and 3 (Wagner, 1999).  The alteration of embryonic signals (such as noggin) can cause the homeotic transformation of a digit in the developing limbs of chicks.  This contradicts the assumption that digits with the same organization must have the same identity (Prum, 2002).

     In the past, there were other perceived obstacles in the acceptance of theropods as ancestors of birds.  For many years, few small theropods were known.  The clavicles were not preserved in many of the early theropod fossils and it was originally thought that theropods lacked them.  Finally, until recently, species of the group of dinosaurs considered to be the closest relatives of birds were only known from time periods after birds evolved.  New finds have identified coelurosaurid theropods which existed prior to the origin of birds (Zhao, 1998).

1) Birds as Theropods

     Theropods evolve three functional toes which face forward.  The earliest theropods had hollow and thin walled limb bones, holes to lighten skull, a horizontal back, deep pits at the end of metacarpals (as in Archaeopteryx), and a long neck.  All of these traits are also known in birds (although some are only known in the earliest birds).  Birds diverged from theropod lineages above the basal theropods because they have a semiopposable thumb, a semicircular antorbital fenestra, and expanded muscle attachment sites on shoulder and arm.  Three dimensional dinosaur footprints demonstrate many similarities with birds although there are also differences such as the position of the first toe (Gatesy, 1999). Theropods developed thin-walled bones, a glenoid cavity in the shoulder which faced posterolaterally, and a tibia which was longer than the femur. Digits IV and V were reduced (Padian, 2001).

     The following illustration gives the traits which are shared by both birds and theropod dinosaurs.

Birds and theropods share a number of features (derived features which characterize the theropods as a group): the structure of lower jaw bones, the mobility between lower jaw bones (some modern birds such as Larus still retain), fusion of the vomer bones, the first two intercentra, the pleurocoels in the presacral vertebrate, the reduction/loss of fifth finger and toe, claw morphology, metatarsal length and width, thin bones, and the articulation of the first metatarsal at the ankle (Gauthier, ).

2) Birds as Tetanuran Theropods

     There are a number of traits which identify tetanuran theropods as a group which are also known in birds.  Tetanurans have a stiff tail, a shortened tooth row (as in early birds), a shortened vertebral column, an astragalar groove, and an ascending process on astragalus (most agree that Archaeopteryx also had this process).  Modern birds have holes in many bones where air sacs invade them; this is called postcranial pneumatization.  Almost all tetanurans have pneumatization of their cervical and anterior thoracic vertebrae just as in Archaeopteryx and modern birds.  Among the maniraptorans, there is even more pneumatization—many possess pneumatization in all presacral vertebrae (except in atlas) as in the fossil bird Rahona.  Oviraptor had pneumatization in almost all its vertebrae.  Some modern birds have pneumatization of sacral and tail vertebrae as well. Comparative skeletal evidence supports the conclusion that theropod dinosaurs probably possessed a flow-through pulmonary system as do modern birds (O’Connor, 2005).

     The following illustration gives the traits which are shared by both birds and tetanuran theropod dinosaurs.

Birds and tetanurans share a number of important features which diagnose the tetanurans as a group such as similarities in: maxillary fenestrae, antorbital tooth row, the tail which is flexible at its anterior end and stiffened at the posterior end, the structure of the scapula, a hand which is more than 2/3 the length of the arm, the bases of metacarpals 1 & 3, the ascending process of the astragalus in the ankle, and the structure of the metatarsals (Gauthier, ).

   In 1996, Sinosauropteryx from China was found with feathers. Sinosauropteryx had downy feathers that were only about 2 cm long-- some had quills and they were not suited for flight.  Most of the feathers were on the neck, back, and tail and were not observed on limbs. It is a compsognath, not a coelurosaurid and thus feathers are known in a group of dinosaurs other than that which is most closely related to birds.  This suggests that feathers evolved in theropod dinosaurs prior to the lineage which gave rise to birds.  This dinosaur was not directly ancestral to birds since it lived after them (dated at 120 million years compared to Archaeopteryx which is dated at150 million years) (Chen, 1998; Padian, 1998;). As taxonomic terms are changed to match the changing understanding of bird and dinosaur relationships, the terms Avifilopluma and Metatheropoda have been used to describe the lineage which possesses feathers, including birds and dinosaurs after Sinosauropteryx (Gauthier, 2001).

     The fossils of Sinosauropteryx are among the best preservations of dinosaurs known.  Not only do they indicate the presence of feathers, they contain the remains of prey in the digestive tract (such as a lizard and a small mammal), and suggest the presence of eggs in paired oviducts (which would, if correct, indicate that the single oviduct of birds evolved later) (Unwin, 1998).

    Dilong paradoxus is a primitive, emu-sized tyrannosaur which was covered in feathers (Lemonick, 2004).

Not all theropods were apparently covered with feathers. One fossil specimen of Carnotaurus indicates that its skin was covered with scales rather than feathers (Gauthier, 2001). The basal coelurosaur Juravenator from the Late Jurassic did not possess feathers on its tail (Gohlich, 2006).

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3) Birds as Coelurosaurid Maniraptorans

Theropods classified in the Coelurosauria (a group which includes the maniraptorans) share a number of derived features with birds: cervical ribs are fused to the vertebrae, a furcula, the sternal plates fuse (at least later in life), the arm is more than half the length of the length of the leg and/or the presacral vertebral column, hand modifications, structure of greater trochanter on femur (still seen in ratites), and a more significant ascending process on the astragalus (Gauthier, ).Coelurosaurs evolved a larger brain (particularly the cerebrum) (Chatterjee, 1997). From the basal theropods through the early birds, the first toe (hallux) became smaller and positioned more distally over a series of gradual intermediates (Chatterjee, 1997). A reversed hallux is a characteristic of Maniraptorans (Rayner, 2001).

     The following illustration gives the traits which are shared by both birds and coelurosaurid maniraptoran tetanuran theropod dinosaurs.

 Eggs and Nests:

Comparisons of saurischian eggs indicate that the features which distinguish bird eggs and their brooding behavior evolved gradually over time (using comparisons of sauropods, oviraptors, troodontids, and other therpods). Four very small eggs (18 mm by 11 mm) have been found from the Cretaceous which either represent a primitive bird whose eggs retained features found in the eggs of dinosaurs or the eggs of a theropod dinosaur closely related to birds (Grellet-Tinner, 2006).

  Troodon formosis laid a small number of large eggs (like birds and unlike crocodiles). The egg shape, size, and microstructure more similar to birds than to crocodiles.  The eggs of Oviraptor are also known; they are also more like those of birds than crocodiles.  An adult Troodon is preserved over one nest and other nests show no evidence of vegetation over them (as is the case in crocodile nests) (Varricchio, 1997). An Oviraptor nest has also been preserved with an adult over the nest in a position similar to the way birds brood on their nests.  The sediments seem to have formed as a result of a sudden sandstorm indicating that the adult sacrificed its life to remain over the nest (Padian, 1998; Zimmer, 1997b).

In all theropods more advanced than basal forms, there is a fusion of the 1^st and 2^nd distal carpals bones.  In maniraptorans, the 3^rd also fuses to this composite bone to form a unique semilunate carpal bone, identical to that in the wrists of the early birds.  The semilunate carpal bone was formed by the fusion of two distal carpal bones. It is possible that this type of carpal bone evolved more than once in maniraptorans (Chure, 2001).

  Oviraptorids, dromaesaurids, and early birds lacked a restriction of the third meatatarsal in the foot which is found in other dinosaurs.  A relative of Oviraptor had a pygostyle, suggesting that it might have had a fan of feathers attached to its tail (Barsbold, 2000). 

The skeletal evidence indicates that theropods possessed lungs which were similar to those of birds (Paul, 2001).

Wishbones: In modern birds, the “wishbone” is formed by the fusion of the two clavicles.  In 1926, it was concluded that maniraptorans were closest to birds but this ancestry was rejected solely on the absence of clavicles in specimens known at that time.  Now furculas are known from a number of theropods including Pelicanimimus, Scipionyx, Beipiaosaurus, Sinornithosaurus, Velociraptor and Oviraptor (Norell, 1997; Norell, 2002). The furcula evolved prior to the lineage of Compsognathus and Sinosauropteryx (Rayner, 2001).

A fossil named Protoarchaeopteryx seems to be a maniraptoran theropod.  It had gastroliths in its gut which would have prevented it from flying.  Protoarchaeopteryx had teeth, which most closely resemble those of Archaeopteryx.  It had a furcula but no significant changes to the sternum.  Not only did it possess plume feathers seen in other dinosaurs (which reached up to 2.7 cm in length) but it also had long symmetrical tail feathers over 13 cm in length.  These long feathers had a central shaft (rachis) and might have had interlocking barbs.  Its arm was shorter than that of birds but longer than other theropods (Qiang, 1998; Padian, 1998)

     Beipiaosaurus is a 7 foot long coeulurosaur which had feathers—the same type as in Sinosauropteryx but longer.  It had a furcula and its teeth resemble those of Archaeopteryx and Protoarchaeopteryx (Xu, 1999). 

   Caudipteryx was first classified as a theropod with feathers, later some concluded that it was an early flightless bird because of its longer legs and short tail.  If it were a theropod, it would be closer to the ancestry of birds that Protoarchaeopteryx.  It also had the two types of feathers seen in Protoarchaeopteryx.   Some classify Caudipteryx is a basal oviraptorosaur (Serreno, 1999; Qiang, 1998; Padian, 1998; Normile, 2000).

--after Qiang, 1998

    In 1997, the discovery of Unenlagia comahuensis (“half bird”) from the early Late Cretaceous of Argentina, about 90 million years ago provided new evidence linking birds to the coelurosaurid maniraptorans.  Although it is not a complete set of bones (as is typical for theropods), it possessed a triangular obturator process (in hip) which typical of coelurosaurids but an additional process found only in birds was also present.  There was a depression in the ilium (hip) for a coelurosaur muscle but the closing of iliac portion of the hip socket is more birdlike  (almost all non-avian dinosaurs have an open hip socket).  The pubis still retains its boot (as in maniraptorans) but has lost a part of it (this boot is lost in birds).   There is some controversy over the shoulder: seems that it faces laterally (as in birds) as opposed to posteriorly (as in other dinosaurs).  This would show that some of the modifications birds need for flight and wing manipulations evolved before winged flight.  Also, the shaft of the scapula and the projection of the acromion were similar to birds rather than non-avian dinosaurs, indicating that this dinosaur could have its folded arms as if they were wings.  The rocks in which Unenlagia was preserved would not have preserved feathers had they existed.  Obviously, this species did not give rise to birds (since it existed after birds appeared) but its ancestors combined dinosaur and avian characteristics more than observed in other coelurosaurids (Witmer, 1997; Novas, 1997).

Buitreraptor, an early droaeosaurid theropod from South America, possessed a long tail comparable to Archaeopteryx, a furcula, a vertically oriented pubis, hip features similar to Unenlagia and Rahonavis (Makovicky, 2005).

     Most theropods possessed hips in which the pubis projects forward, unlike the condition in birds in which it projects backwards.  However, the theropods which seem to be most closely related to birds because of skeletal characteristics other than their hips, the pubis does possess the bird-like trait of projecting backwards.  Although the hips of modern birds may appear ornithischian superficially, they are modified saurischian pelvis; Archaeopteryx had a saurischian pelvis.  Maniraptorans such Deinonychus and Velociraptor have modified saurischian pelvises which resemble that of early birds.  The reversed pubis evolved prior to the Alvarezsaurids, Caudipteryx, and Protoarchaeopteryx (Rayner, 2001). Velociraptor also had a braincase similar to that of birds.

The following hip is that of a modern emu.

4) Birds as coelurosaurids which share a common ancestry with the Deinonychusauria/ dromaeosaurs

From the coelurosauria arose the ancestors of the Cretaceous Deinonychusauria/ dromaeosaurs.  Birds share a number of derived features with this group: the prefrontal bone of the skull is reduced or absent, longer processes on cervical vertebrae, the structure of tail vertebrae, the forelimb is at least 75% the length of the presacral vertebral column (in Archaeopteryx, it was 120-140%), the ulna is curved, the semilunate carpal, the shape of the ilium, the direction of the pubis, the reduced pubic boot, and the length of the pubis compared to the ischium (Gauthier, ).

     The sister group of Avialae (fossil and modern birds) is the group Deinonychosauria which is composed of Troodontidae and Dromaeosauridae.  Microraptor is a basal dromaeosaurid, a sister taxon to all other dromaeosaurids.  It is the smallest non-avian theropod (55 cm long) and small size seems to be the condition of the earliest members of Deinonychosauria.  It possessed a furcula  and a number of birdlike features of its teeth, hip, tail, and shoulder.  Microraptor, a basal dromaeosaur, also has a number of similarities to Sinoventor, a basal troodontid (Hwang, 2002).

Dromaeosaurs evolved a bony sternum (Rayner, 2001). Dromaeosaurs could fold their arms in the way that modern birds fold their wings (Chatterjee, 1997).

Deinonychus possessed forelimbs whose modifications were adaptations for prey capture but which would also facilitate flight. The elbow joint was similar to that of Archaeopteryx and the forearm and wrist could function as a unit. The motion of the arm of Deinonychus would have been similar to a flight stroke although its range of motion would have been less. The modifications of theropod arms which prepared the ancestors of birds for flight were actually adaptations to make them more effective predators. Feathers on their arms could have improved their maneuverability while running and their ability to control the direction of a leap (Gishlick, 2001).

     Two theropods of this group have been found with feathers: Sinornithosaurus and Microraptor.  Since Sinornithosaurus is an early member of the clade which leads to theropods such as Velociraptor and Deinonychus and it has downy feathers, it is entirely possible that all later forms had them too. After Sinornithosaurus, the unbranched filaments of primitive feathers became branched (Gauthier, 2001).

Microraptor may have possessed feet adapted for perching as indicated by its curved claws and a repositioned first toe. It was crow-sized and thus represents the first dinosaur known that was smaller than Archaeopteryx. Its trunk was less than 5 cm long and thus Microraptor is the smallest known adult dinosaur and the only theropod smaller than Archaeopteryx.(Stokstad, 2000). Its curved claws suggest that it lived in trees.  Microraptor gui possessed “flight feathers” on all four limbs--both the short plumule feathers and long feathers with a central shaft.  . Microraptor gui lacked a keel on its sternum and it probably was capable of gliding rather than flight. It has the most extensive plumage of any non-avian animal (Perkins, 2003). A partial fossil of dinosaur closely related to birds, named Pedopenna daohugouensis, is slightly smaller and older than Microraptor gui. Like Microraptor, it possessed flight feathers on its hind legs. Long leg feathers are even known in some fossils of Archaeopteryx (Hecht, 2005).

Feathers are also known in a Sinornithosaurus-like fossil theropod which is also classified in the family Dromaeosauridae.  Its furcula is similar to that of Sinornithosaurus in its boomerang shape.  The feathers were preserved all around its body unlike Sinosauropteryx.  There were three different structures of feathers, including some which resembled those of Protarchaeopteryx and Caudipteryx (Ji, 2001; Norell, 2001b). Sinornithosaurus was covered with filaments 30-45 mm long and 1-3 mm wide  which are indistinguishable from feathers of birds preserved in the same deposits (Xu, 2001). Some feel that the structures which cover Sinornithosaurus should be considered as proto-feathers rather than true feathers (Schweitzer, 2001).

A juvenile dromaeosaur is known to have been covered in feathers. Bambiraptor was very similar to the first birds (although it is not known whether it possesed feathers or not).

If feathers are the defining characteristic of birds, then many dinosaurs are birds. If flight is the defining characteristic of birds, then the long-armed, chicken-sized Bambiraptor might qualify as a bird (Gauthier, 2001).

In early theropods, the forelimbs were less than 40% the length of the legs. Many Maniraptorans possessed forelimbs which were more than 2/3 the length of the legs. The first birds possessed arms which were equal to the length of the legs (Padian, 2001).

Feathers:

     Modern birds obviously use their feathers for a variety of purposes including flight, thermoregulation, camouflage, and courtship.

How did feathered flight evolve?  Did arboreal dinosaurs evolve feathers to help them glide from tree to tree and only later did these feathers cover the body for thermoregulation?  Did feathers evolve for thermoregulation and display in running dinosaurs which they developed the ability to fly?  Modern consensus rests with the cursorial (running) hypothesis rather than the arboreal hypothesis.  Developmentally, feathers and scales are homologous (unlike hair).  Either feathers or scales can develop in an area but not both.

     There have been fossils of individual feathers and until recently they were assumed to be the feathers of birds.  Because of a growing list of dinosaurs which were feathered, that assumption can no longer be made.  A number of finds have indicated that at least some dinosaurs had feathers, including Sinosauropteryx, Beipiaosaurus, Sinornithosaurus (all three had hairlike, seemingly unbranched structures), Microraptor, Caudipteryx, Protarchaeopteryx (both of which seem to be true avian feathers although Caudipteryx might be a primitive bird), and unnamed Chinese fossils (Gibbons, 1996).   The feathers of Sinosauropteryx are simple, plumule structures which might represent an early stage in the evolution of feathers.  Microraptor is the smallest known dinosaur (about crow-sized) and its curved claws (similar to those of Archaeopteryx) perhaps indicate that it could live in trees.  In 1997 skin impression of a small theropod in Spain showed that it was featherless; although feathers seem to have been present on some theropods, they were not present on all. 

The feathers on the neck of Archaeopteryx included hairlike filaments which may represent the primitive structure from which advanced feathers evolved. There were several stages in the evolution of the types of feathers found in modern birds. The first step resulted in the evolution of simple, hair-like feathers which covered the body. This type of feather is the only feather which is definitely present in Sinosauropteryx and is one of several feather types present on the dinosaurs Caudipteryx and Bepiaosaurus and possibly on the birds Archaeopteryx and Confuciusornis. More complex hair-like body feathers were present on Sinornithosaurus and possibly on the dinosaurs Sinosauropteryx and Caudipteryx and the birds Archaeopteryx and Confuciusornis. Feathers classified as pennaceous and plumulaceous are present on modern birds. Pennaceous feathers are also known on fossil birds and the dinosaurs Protoarchaeopteryx, Microraptor, Sinornithosaurus, Caudipteryx, and possibly Sinosauropteryx. Plumulaceous feathers are known on Caudipteryx and Protoarchaeopteryx. Asymmetrical flight feathers are known on modern birds, fossil birds (such as Archaeopteryx and Confuciusornis), and the dinosaur Microraptor. A number of dinosaurs possesses long feathers on their hind limbs such as Microraptor, Cryptovolans, and another dromaeosaurid. Closer analysis of Archaeopteryx indicates that it also had long feathers on its hindlimb. During development, some modern birds (such as crows and herons) develop long feathers in the hip and leg region as well (Christiansen, 2004).

When considering the muscular and skeletal changes in leg anatomy which occurred in the ancestry of modern birds after their split with the crocodilian lineage, about half evolved in dinosaurs and their immediate ancestors ( Hutchinson, 2002).

What about Longisquama?

    As a search for bird ancestors progressed, most groups of archosaurs were linked to this ancestry at one time or another.  Interestingly, a mouse-sized archosaur is known which had feathers or feather-like structures, Longisquama.  Despite its small size, it possessed 6 feathers that measured up to 12 cm long.  They were originally described as scales (the name Longisquama literally means “long scale”) and some feel that they are not feathers but membranous structures of some sort. 

Longisquama did have a furcula (and thus is the earliest animal to have one at 220 mya).  Feathers in Longisquama would either indicate that feathers are much older than previously thought (and predate dinosaurs), feathers arose separately in 2 groups of archosaurs (theropods and Longisquama), or that the modern consensus that birds descended from dinosaurs is incorrect.   In Longisquama, feathers were involved in flight prior to their use in insulation whereas the reverse appears to be true of theropod dinosaurs (Stokstad, 2000; Jones 2000; Jones 20001). 

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