J. Paleont. Soc. Korea. Vol. 22, No. 1, (2006) : p.

133-151

THE EARLY EVOLUTIONARY HISTORY OF BIRDS

1

Luis M. Chiappe and Gareth J. Dyke

1

The Dinosaur Institute, Natural History Museum of Los Angeles County, 900 Exposition
Boulevard, Los Angeles, California 90007 U.S.A., chiappe@nhm.org
2
Department of Zoology, University College Dublin, Belfield Dublin 4, Ireland,
gareth.dyke@ucd.ie

Abstract: With more than 10,000 speciesroughly twice as many as there are mammals or lizardsbirds are
by far the most diverse group of living land vertebrates. However, this enormous diversity is just a remnant
of an ancient evolutionary radiation that can be traced back to the Jurassic, to the 150 million-year-old
Archaeopteryx from southern Germany. Research on the early history of birds and the development of flight
has been at the forefront of paleontology since the advent of evolutionary thought. For most of this time, however,
the available evidence was limited to a small number of fossils largely restricted to near-shore and marine environments, and greatly separated both anatomically and in time. A burst of discoveries of Cretaceous birds over
the last two decades has revealed a hitherto unexpected diversity; since the early 1990s, the number of new
species described has more than tripled those known for much of the last two centuries. This rapid increase
in discoveries has not only filled much of the anatomical and temporal gaps that existed previously, but has
also made the study of early birds one of the most dynamic fields of vertebrate paleontology.
Key words: Evolution, Mesozoic, birds

A CENTURY OF CONTROVERSY: THE ORIGIN OF BIRDS

Historical proposals for the ancestry of birds have included almost every group of reptiles (Witmer,
1991, 2002; Padian and Chiappe, 1998; Chiappe, 2001). Today, alternatives to the widely accepted view
that birds evolved from theropod dinosaurs (Chatterjee, 1997; Chiappe, 2001; Gauthier and Gall, 2001)
include poorly sustained hypotheses identifying a variety of primitive archosauromorphs (Tarsitano and
Hecht, 1980; Feduccia and Wild, 1993; Welman, 1995) or crocodylomorphs (Martin, 1983; Martin et al.,
1980; Martin and Stewart, 1999) as the closest relatives of birds.
The notion that the ancestry of birds is to be found among primitive archosauromorphs can be traced to
the discovery of Euparkeria from the Early Triassic of South Africa (Broom, 1913). Nonetheless, it was
Heilmann (1926) in his influential book The Origin of Birds, who championed this idea. At the time, discussions about the origin of birds were influenced by the Law of Irreversibilitynamely, that structures once lost cannot re-evolve. Although noticing a great deal of similarity between birds and theropods, Heilmann (1926) embraced this idea of archosauromorph ancestry (in the shape of an animal such
as Euparkeria) because these reptiles lack the specializations seen in theropod dinosaurs. Central to his
argument was the apparent loss of clavicles in theropodsan observation at odds with the evolutionary
view of structural irreversibility that prevailed at the time (Padian and Chiappe, 1998). Despite the subsequent discovery of clavicles in a variety of theropods (e.g., Camp, 1936; Chure and Madsen, 1996;
Makovicky and Currie, 1998), this default archosauromorph hypothesis remained virtually unchallenged until the early 1970s. Using primarily similarities in the braincase, Walker (1972) argued for a
close relationship between birds and basal crocodylomorphs (e.g., sphenosuchians). Almost at the same
time, Ostrom (1973) resurrected the 19th Century notion of a theropod ancestry for birds (Witmer, 1991,
2002; Padian and Chiappe, 1998). The work of Walker and Ostrom provided new impetus for the re-examination of the origin of birds, with the emergence of the crocodylomorph and theropod hypotheses as a
possible alternative to the archosauromorph ideas that had prevailed for much of the 20th Century.
Extending Walkers work, Martin et al. (1980; see also Martin and Stewart, 1999) regarded similarities in

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the structure of the teeth and ankle as evidence for a close relationship between birds and extant crocodiles, whereas Welman (1995) considers the braincase of Euparkeria as indicative of an avian
relationship. While both the archosauromorph and crocodylomorph hypotheses highlighted similarities
with birds, many of them have either been questioned or have subsequently been discovered in
dinosaurs. If one were to entertain either of these hypotheses they would have to go further to explain the
vast number of similarities that support a close relationship between birds and theropod dinosaurs
(Chiappe and Dyke, 2002).
Since Ostroms pioneering studies (1973, 1976), a wealth of evidence including similarities in the
skeletal, egg structure, nesting behavior, integument, and bone microstructure has been accumulated in
support of the hypothesis that birds originated within small and predominantly terrestrial theropods
(Gauthier, 1986; Chiappe, 2001, 2004; Holtz, 2001; Norell et al., 2001; Padian et al., 2001; Chiappe and
Dyke, 2002; Clark et al., 2002; Xu et al., 2003). Alternative hypotheses, however, compete regarding the
closest theropod group to birds, with dromaeosaurids, troodontids, oviraptorids, and alvarezsaurids
among the most commonly cited (e.g., Gauthier, 1986; Perle et al., 1993; Sereno, 1999; Chiappe et al.,
1998; Elzanowski, 1999; Xu et al., 2000; Holtz, 2001; Norell et al., 2001; Clark et al., 2002).

UNEXPECTED DIVERSITY: THE MESOZOIC AVIFAUNA

For almost a century, knowledge of the Mesozoic avifauna was greatly limited to just the Late Jurassic
Archaeopteryx and a series of fossils from the Late Cretaceous Pierre Seaway of North America. The
anatomy of these Late Cretaceous birds (e.g., Hesperornis and Ichthyornis) testified to an enormous gap
in the early history of the group when compared to the older and much more primitive Archaeopteryx.
Discoveries of recent years have considerably filled this gap (Chiappe and Dyke, 2002; Chiappe and
Witmer, 2002) and a genealogical framework for much of the diversity of Mesozoic birds has emerged
(Fig. 1).

ISLAND DWELLERS: ARCHAEOPTERYX AND RAHONAVIS

Although ten skeletal specimens and a feather (Elzanowski, 2002; Mayr et al., 2005) of Archaeopteryx
have been found in lagoonal limestones of a tropical archipelagodeposits today clustered in central
Bavaria, Germanysome of these have been used to erect new species, albeit not very convincingly. A
single, mostly disarticulated specimen of Rahonavis is known from the Late Cretaceous of Madagascar
(Forster et al., 1998), when the island had already lost its connections with both Africa and India.
Although they lived some 75 million years apart, these island dwellers are the most anatomically primitive known birds, having long bony tails, primitive proportions in the pelvis, and incomplete fusion of
some compound bones (e.g., tarsometatarsus, tibiotarsus) (Fig. 2).
If the single species approach is adopted, then the ten skeletal specimens of Archaeopteryx ranged in
size between a jay and a small gullalthough size comparisons of this bony-tailed bird with living species remain approximate. In spite of the spectacular preservation of several specimens (Hecht et al.,
1985; Mayr et al., 2005), limited anatomical information is available for certain areas of the skeleton; indeed not all specimens preserve the same details.
The anatomy of Archaeopteryx illustrates the most primitive condition seen in birds (Fig. 2), one that
in many respects only narrowly departs from nonavian theropods. Although its toothed skull was more
triangular, it shows a great deal of similarity to the latter (e.g., interdental plates, hooked ectopterygoid,
quadrate anatomy) (Elzanowski, 2002; Mayr et al., 2005). The sternum of Archaeopteryx was apparently
small and cartilaginous (the bone identified by Wellnhofer (1993) as a sternum has been proved to be the

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Fig. 1. Phylogenetic relationships and temporal occurrences of the major lineages of Mesozoic birds.

coracoid) and linked to the pelvis by a basket of belly ribs (gastralia) similar in number (12-13 pairs) and
appearance to those of nonavian theropods (Norell and Makovicky, 1997). Its long trunk lacked the rigidity of extant birds and its shoulder girdle did not have many of their specializations (e.g., strut-like
coracoid, triosseal canal) for flight. Despite a striking similarity in the shape and number of feathers
(11-12 primaries and 12-14 secondaries; Elzanowski, 2002) to living birds, just like in nonavian theropods the forelimb of Archaeopteryx terminated with a long, powerfully clawed hand. Indeed, the shape
and proportions of the pelvic bones and hindlimb are equally primitive. Shorter than most nonavian
theropods (21-22 elements; Elzanowski, 2002), the frond-like, feathered tail of Archaeopteryx retained
the long prezygapophyses (anterior zygapophysial articulations) as well as other details seen in these
dinosaurs. As in most nonavian theropods, and all birds, the skeleton of Archaeopteryx was lightweight
and pneumatizedin particular, the vertebrae and furcula (wishbone) were invaded by air sacs (Britt et
al., 1998; Christiansen and Bonde, 2000).
The anatomy of Rahonavis also suggests that this bird was a lightweight predator (Forster et al., 1998),
with a wingspan comparable to that of a red-tailed hawk. Quill knobs preserved on its forelimb indicates
at least 10 flight feathers attached to the ulna, a number within the range seen in living birds. The structure of the shoulder girdlein particular, the presence of a mobile glenoidapproaches more that of
extant birds than does the rigid, fused girdle of Archaeopteryx and some other early birds (e.g., confuciusornithids). The reconstructed position of the scapula with respect to the rib cage suggests Rahonavis

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was able to flap its wings with greater amplitude than Archaeopteryx or nonavian theropods (Forster et
al., 1998). All these features are consistent with well-developed aerodynamic capabilities. However, perhaps the most striking anatomical feature of Rahonavis is the presence of an enlarged, sickle-shaped foot
claw, presumably used for slashing prey, a specialization typical of dromaeosaurid and troodontid theropodsa proportionally smaller version of this condition has also been identified in Archaeopteryx (Mayr
et al., 2005).
Because of this apparently mosaic combination of features, some have claimed Rahonavis to in fact be
composed of the forequarters of a bird mixed with the hindquarters of a nonavian theropod (Geist and
Feduccia, 2000). The preservation of the fossil material as well as carefully conducted analyses by its describers indicates otherwise (Chiappe and Dyke, 2002). Nonetheless, the precise evolutionary relationships of Rahonavis remain unclear. Forster et al. (1998) regarded it as closer to Archaeopteryx than to
other birds, although cautioning about the possibility of Rahonavis being more akin to extant birds (see

Fig. 2. Skeletal reconstructions of the Late Jurassic Archaeopteryx and the Early Cretaceous Jeholornis. Drawings not
to scale.

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also Chiappe, 2002a; Fig. 2). Although subsequent studies have also supported a basal placement for
Rahonavis within birds (Holtz, 1998; Chiappe, 2002a; Zhou and Zhang, 2002a), some workers (Holtz,
2001; Clark et al., 2002; Makovicky et al., 2005) have also hypothesized that this fossil in fact falls immediately outside the group.
Although there is little doubt that Archaeopteryx was able to fly (Hecht et al. 1985; Padian and
Chiappe 1998; Feduccia 1999), the limited lift produced by its frond-like tail, the presumably weak flight
musculature as inferred from the absence of a bony sternum, the lack of an alula and several other important aerodynamic structures suggests that Archaeopteryx was most likely a weaker and less maneuverable flier than most of its living relativesthe Solnhofen bird probably required of a take-off run to
become airborne (Burgers and Chiappe, 1999). Similar aerodynamic inferences can be made for
Rahonavis and other long-tailed birds.

A LACUSTRINE CORNUCOPIA: THE NEW DIVERSITY FROM CHINA

If there is one region that has dramatically contributed to our understanding of the origin and early
evolution of birds, this is the northeastern Liaoning Province of China (Zhou et al., 2003). The exquisite
and numerous fossils recovered from these and other Early Cretaceous localities in China include more
than a dozen species breaching the enormous evolutionary gap between Archaeopteryx and modern birds
(Fig. 1). The majority of these birds are temporally distributed between two lacustrine beds in Liaoning:
the approximately 128-121 million-year-old Yixian Formation (Swisher et al., 2002; Zhou et al., 2003)
and the slightly younger Jiufotang Formation (approximately 120 million years old; He et al., 2004).
The turkey sized Jeholornis (Zhou and Zhang, 2002a) from the Jiufotang Formation also illustrates the
primitive, long-tailed condition of Archaeopteryx and Rahonavis (Fig. 2). This bird is one of the largest
from prior to the Late Cretaceous. The skull is triangular, with deep and robust jaws. Only a few tiny
teeth are present towards the tip of the lower jaw and these are absent in the upper jaw (Zhou and Zhang,
2003a). Like in Rahonavis, the shoulder girdle articulation is mobile. Jeholornis, however, shows significant modifications with respect to Archaeopteryx. The coracoid is elongate and the curved scapula
tapers distally, thus approaching the condition seen in extant birds (Zhou and Zhang, 2002a). The sternum of Jeholornis is ossified and large. The forelimb of this bird is also longer relative to its hindlimb
than that of Archaeopteryx. Its powerfully clawed hand is almost as long as the humerus, proportionally
shorter than that of Archaeopteryx, beginning the evolutionary transition towards living birds where the
proximal portion of the forelimb is substantially longer than its distal counterpart. The pelvis is similar to
that of Archaeopteryx and Rahonavis the pubis is vertically oriented although the portion at which the
two counterparts are joined to one another (i.e., the pubic apron) is shorter than that of at least the former.
As in most birds the foot had a retroverted first toe (hallux). Yet, the hindlimb exhibits several features
ancestral to all birds, including incompletely formed compound bones (e.g., tibiotarsus, tarsometatarsus),
the presence of a splint-like fifth metatarsal, and a very short hallux (Zhou and Zhang, 2002a, 2003a).
Furthermore, the tail of this animal is longer than that of any other bird. Even though its initial report described approximately 22 caudals (Zhou and Zhang, 2002a), two recent specimens have shown that its
tail contains 27 vertebrae (Zhou and Zhang, 2003a)several more elements than the shorter tail of
Archaeopteryxand that a fan-shaped tuft of feathers attached to its distal end. These new specimens
have also documented the presence of long and asymmetrically vaned feathers on the forelimbs. Zhou
and Zhang's study (2002a) was unable to precise whether Jeholornis was closer to extant birds than
Rahonavistheir cladogram placed these two long-tailed birds in a trichotomy with all other birds except Archaeopteryx. The discovery that Jeholornis had a tail longer than that of Archaeopteryx may add
more to this conflict, especially when the tail of Rahonavis is incompletely known. Nonetheless, these
three birds are undoubtedly more primitive than any other one.

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In the same month as the initial report of Jeholornis, another Jiufotang bird with long asymmetrical
flight feathers and a long tufted tail, Shenzhouraptor, was reported by Ji et al. (2002). In addition to being
three quarters the size of the holotype of Jeholornis, Ji et al. (2002) reported a few other differences including the lack of teeth and a greater number of caudals. As indicated earlier, however, this latter difference has been shown to be nill by new fossils documenting that the tail of the holotype of Jeholornis is
missing several proximal caudals (Zhou and Zhang, 2003a). Unfortunately, Zhou and Zhang (2003a)
made no comparisons between Jeholornis and Shenzhouraptor, but we believe that the "absence" of teeth
in the latter may well be a preservational artifact. Differences notwithstanding, we believe that the great
similarity between Jeholornis and Shenzhouraptor seriously raises the possibility that these birds are the
same species. Very similar to these birds is Dalianraptor, also known from the Jiufotang Formation (Gao
and Liu, 2005). However, several differences in the morphology and proportions of the forelimb (e.g.,
much shorter forelimbs, longer digit I) suggest that Dalianraptor is neither Jeholornis nor Shenzhouraptor,
although it is likely a close relative of these birds.
From the same Jiufotang beds as Jeholornis, Shenzhouraptor, and Dalianraptor comes a great diversity of short-tailed birds with opisthopubic pelves, whose genealogically are closer to extant avians than
the long-tailed forms. Perhaps the most primitive short-tailed bird is Sapeornis (Zhou and Zhang, 2002b,
2003b), a large animal with a wingspan comparable to that of a turkey vulture (Fig. 3). At least
half-a-dozen specimens of this unusual bird have been found. Sapeornis has a relatively short skull with
conical and robust teeth restricted to the tip of the rostrum, and lacking them in its lower jaws. The temporal region of the skull remains largely unmodified, with at least a complete upper temporal fenestra. In
the shoulder girdle, the articulation of the scapula and the coracoid is mobile but the latter bone is short
and axe-shaped. Interestingly, no specimen so far preserves an ossified sternum. This last fact suggests
that the sternum could have been cartilaginous and that the flight muscles needed to power the long
wings of this bird could have been originated on the expanded distal coracoids. The furcula is very robust
and shaped like a boomerang, with an angle of more than 100 degrees between its branches having a
short hypocleideumthe most primitive known occurrence of this feature within bird evolution. The elongate forelimb of Sapeornis is much longer than that of Archaeopteryx, Jeholornis, and Shenzhouraptor,
reaching approximately 1.5 times the length of the hindlimb. The humerus is shorter than the ulna-radius
and pierced by a large proximal foramen of uncertain function. The hand is about the same length as the
humerus, as in the Chinese long-tailed birds, but the presence of a clawless, reduced third digit illustrates
the first stage of finger reduction characterizing early bird evolution. Like in Archaeopteryx and other
long-tailed birds, the pelvis remains unfused but its pubic symphysis has become shorter. A full basket of
gastralia fills the space in front of the pelvis in several specimens. Perhaps the most notable difference
when compared to its more primitive long-tailed relatives is the abbreviation of the bony tail, which was
limited to a rather short pygostyle following 6-7 free caudals (Fig. 3). Based on the information of the
holotype alone, Zhou and Zhang (2002b) suggested that Sapeornis is the most primitive short-tailed bird.
This interpretation, however, needs to be tested in light of subsequent better preserved specimens and detailed comparisons with primitive short-tailed birds such as Confuciusornis.
By far the most abundant bird from the Mesozoic of China (and the world) is the toothless
Confuciusornis (Hou et al., 1995; Chiappe et al., 1999) (Fig. 3), a short-tailed species that maybe only
slightly more derived than Sapeornis (Zhou and Zhang, 2002b). Hundreds of well-preserved specimens
of this bird have been collected from both the Yixian and Jiufotang formations (Zhou et al., 2003). The
size of these fossils falls within a wide spectrum but the average specimen has dimensions comparable to
those of a magpie. Although several species of Confuciusornis have been named, most published specimens seem to comprise a single one (i.e., C. sanctus see Chiappe et al., 1999), thus providing the best
sample for studying intraspecific variation in any Mesozoic bird. Very similar to Confuciusornis is the

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equally toothless Changchengornis, a bird known from a single specimen of the Yixian Formation (Ji et
al., 1998; Chiappe et al., 1999) and differing from Confuciusornis by its strongly curved beak and a few
other skeletal details.
Confuciusornithids are very primitive in many respects. In the first place, the skull of Confuciusornis
(and likely of Changchengornis) is remarkable in exhibiting a complete diapsid (upper and lower) temporal fenestrae (Chiappe et al., 1999)a design that would have greatly limited cranial kinesis. The
shoulder bones of these birds are fused into a rigid scapulocoracoid, a condition more primitive than that
of the long-tailed Rahonavis, Jeholornis, and Sapeornis. The forelimb is proportionally much shorter
than in the latter birds, approaching the length of the hindlimb as in Archaeopteryx. The forelimb bones
also retain primitive proportionsthe hand is the longest segment and the ulna-radius is shorter than the
humerus. The robust wishbone has the boomerang appearance of Archaeopteryx and the sternum is es-

Fig. 3. Skeletal reconstructions of the Early Cretaceous Confuciusornis and Sapeornis.. Drawings not to scale.

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sentially flat (although some specimens do have a faint caudal ridge), lacking the prominent ventral keel
that is seen in more advanced birds. Like apparently all basal avians, confuciusornithids had a full set of
gastralia, although with fewer rows than seen in Archaeopteryx. The hindlimbs are robust and the reversed hallux is half (Confuciusornis) to two-thirds (Changchengornis) the length of the second toe. The
plumage of these Chinese birds is beautifully preservedboth taxa of confuciusornithids display a pair of
long, ribbon-like tail feathers that extend more than half the length of their skeletons. In Confuciusornis,
of which many well-preserved specimens are known, these feathers are either present or absent, a pattern
often interpreted as the result of sexual dimorphism. This argument, however, has yet to be sustained on
the basis of morphometric analyses of bones, including specimens with and without these feathers
(Chiappe et al., 1999).
By far the most speciose group of Early Cretaceous birds from Chinaindeed the rest of the Mesozoic
recordwere members of Enantiornithes (Chiappe and Walker, 2002) (Fig. 4). Close to one-third of the
25 or so valid species of these birds are from continental Chinese deposits, and mostly from Liaoning.
The remaining diversity of this lineage has been recorded from rocks spanning nearly the whole
Cretaceous and from every continent except Antarctica. Although most often recorded from inland deposits, enantiornithines are also known to have inhabited coastal and marine environments, and their
range even extended into polar regions (Chiappe, 1996). The oldest known enantiornithine is possibly
the Chinese Protopteryx (Zhang and Zhou, 2000), which comes from Early Cretaceous rocks of Hebei
Province (Dabeigou Formation) that appear to be slightly older than those of Liaonings Yixian Formation.
Early Cretaceous enantiornithines are represented by small toothed species such the Chinese Protopteryx
(Zhang and Zhou, 2000, Eoenantiornis (Hou et al., 1999), and Longipteryx (Zhang et al., 2001) (Fig. 4),
and the Spanish Concornis (Sanz et al., 1995) and Eoalulavis (Sanz et al., 1996). If an overall trend in
size reduction is visible during the transition from nonavian maniraptoran (e.g., dromaeosaurids, troodontids, oviraptorids) to basalmost birds (e.g. Archaeopteryx, Rahonavis), this pattern is further evidenced by the earliest enantiornithines, which were of sizes comparable to modern sparrows and

Fig. 4. Skeletal reconstructions of the Early Cretaceous enantiornithine Longipteryx.

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thrushes. General flight performance is often correlated with size reduction and the overall anatomy of
the flight apparatus of enantiornithines shows similarities to those of living birds in wing proportions, the
large size of the sternum, a Y-shaped furcula, and an alulathe latter structure, a small tuft of feathers attached to the first finger of the hand, plays a critical role in controlling take-off and landing (Sanz et al.,
1996). All these features suggest that even the earliest enantiornithines possessed a much more sophisticated flying apparatus than that of their avian predecessorsenantiornithines were likely able to take-off
from a stand still. In spite of the fact that definitive evidence for perching is lacking in more basal birds,
these capabilities were clearly present among the earliest enantiornithines as evidenced by their pedal
morphology (Chiappe and Calvo, 1994; Chiappe, 1995; Martin, 1995; Zhou, 1995; Sanz et al., 1995;
Sereno et al., 2002). A distinct increase in size characterizes later enantiornithine evolutionin the Late
Cretaceous, the Mongolian Gobipteryx (Chiappe et al., 2001), the only toothless enantiornithine, reached
the size of a quail, and the Argentine Enantiornis (Walker, 1981; Chiappe, 1996) had a wing span of
nearly one meter.
In addition to rich accumulations of more basal avians, the Early Cretaceous deposits of China have also provided critical information for understanding the evolution of birds much more closely related to
those of today.

BASAL ORNITHUROMORPHS: THE PRIMITIVE FORERUNNERS OF MODERN AVIANS

For nearly the entire history of paleornithology, the evolutionary transformations leading to the origin
of modern birds (i.e., Neornithes) were established on the evidence mostly provided by two lineages of
seabirds, the specialized diving hesperornithiforms and the less well-known Ichthyornis (Marsh, 1880).
Developments over the last decade, however, have furnished us with many more Mesozoic players from
which to examine this important evolutionary event. Alongside hesperornithiforms and Ichthyornis, this
new diversity constitutes the Ornithuromorpha, a vast clade sharing a common ancestor with Enantiornithes
and containing all 10,000 species of living birds (Fig. 1). Despite these new discoveries, the precise genealogical relationships of most Mesozoic ornithuromorphs are not entirely clear.
Among the best known of these taxa is the flightless Patagopteryx from the Late Cretaceous (early to
middle Campanian) of northwestern Patagonia (Argentina) (Chiappe, 2002b) (Fig. 5). Known from several specimens, this hen-sized bird is one of the most primitive known ornithuromorphs and the best-represented bird from the Mesozoic of the Southern Hemisphere. Its skull is incompletely known and it is
thus uncertain whether it was toothed. The cranial anatomy of this bird, however, shows a significant departure from that of more primitive forms, evidenced by the complete reduction of the postorbital and the
incorporation of the squamosal into the braincase. An important functional corollary of this transformation is the disappearance of individualized temporal openings, a landmark in the evolution of the
modern avian skull. However, several cranial features (e.g., quadratopterygoid fusion, interlocked quadratosquamosal articulation) suggest that the kinematic capabilities also characteristic of the modern
avian skull were not yet developed in Patagopteryx (Chiappe, 2002b). The cervical vertebrae of
Patagopteryx have the saddle-shaped articulations (i.e., heterocoely) typical of modern aviansalthough
a tendency towards this specialized type of vertebral articulation can be seen in Enantiornithes,
Patagopteryx is the most primitive bird with fully heterocoelous vertebrae and most likely, the tri-partite
functional subdivision typical of the neck of modern birds. With a long trunk and a relatively small (nine)
number of synsacral vertebrae, Patagopteryx represents an early stage in the elongation of the neck and
sacral region seen in more advanced ornithuromorphs. Its simplified shoulder, apparently reduced furcula and sternal keel, and strongly abbreviated forelimbs suggest that it was flightless, albeit a specialization clearly evolved from flying ancestors (Chiappe, 2002b) (Fig. 5). Several other advanced features
can be seen in its robust pelvis. Paramount are the lack of a pubic symphysis and the proximocaudal

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Fig. 5. Skeletal reconstructions of the Late Cretaceous basal ornithuromorph Patagopteryx.

process of the ischium, which primitive conditions are widespread among more basal birds. The robust
and muscular hindlimb of this obligated ground-dweller is more than twice as long as the forelimb; the
short tarsometatarsus and long toes suggests Patagopteryx was a slow moving bird.
A number of other basal ornithuromorphs have recently been discovered that are many millions of years
older than Patagopteryx. These discoveries include two exceptionally well preserved toothed birds from
the Early Cretaceous of China, the equal-sized Yanornis and Yixianornis (Zhou and Zhang, 2001; Zhou et
al., 2002) from the Jiufotang Formation and the older and much smaller Hongshanornis (Zhou and Zhang,
2005) from the Yixian Formation. Although the precise genealogical relationships of these taxa currently
remain unclear, the presence of a pubic symphysis suggests that these taxa may be more primitive than
Patagopteryx. These birds also retain a number of more primitive avian characteristics (i.e., gastralia, long
fingers that retain claws) while at the same time having an essentially modern flight apparatus. The pectoral girdle of both Yanornis and its shorter-snouted contemporary Yixianornis closely approach the condition seen in living birds (i.e., coracoid with a wide base and rounded procoracoid, curved scapula)
both these taxa were clearly capable of well-controlled and active flapping flight and future studies of
them are likely to clarify further aspects of the anatomical transition towards living birds.
Both Patagopteryx and these Chinese taxa appear to be more primitive than another recently discovered basal ornithuromorph, the Mongolian Late Cretaceous Apsaravis (Norell and Clarke, 2001;
Clarke and Norell, 2002). The single known specimen of Apsaravis consists of a well-preserved skeleton
lacking most of the skull together with portions of the forelimbs and feet. Its lower jaw is devoid of

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teeth and it is possible that Apsaravis was the most primitive toothless ornithuromorph (although
Hongshanornishas been regarded as toothless (Zhou and Zhang, 2005), the poor preservation of the only
know specimen makes difficult to determine whether it truly lacked teeth). Many features of the anatomy
of Apsaravis show clear similarity to modern avians (e.g., short fused dentary symphysis, reduced number of trunk vertebrae). Among the most notable is the development of a broad pelvis in which the pubis
and ischium are widely separated from each other. Another important transformation of functional significance has to do with metacarpal I developing a pronounced extensor process. In extant birds, this feature is involved in the automatic extension of the hand by the propatagial ligaments (Vazquez 1994). The
appearance of a pronounced extensor process in the carpometacarpus of Apsaravis indicates that this bird
was able to extend its wing automatically (Clarke and Norell, 2002), a functional property that highlights
the sophistication reached by the flight apparatus of this and more advanced ornithuromorphs.
Even more closely related to modern birds, although representing an early example of flightlessness,
are the diving hesperornithiforms (Fig. 6). Despite having been known since the 19th century and in
some instances monographed (i.e., Hesperornis regalis Marsh 1880), much revisionary work on their
anatomical diversity and genealogical interrelationships remains to be done. Ranging greatly in sizethe
largest being comparable to that of an Emperor Penguinthese birds are characterized by having an
elongate skull with a sharp and toothed snout, minute forelimbs, a long neck and short trunk, and a robust
hindlimb specialized for aquatic locomotion (Marsh, 1880; Martin and Tate, 1976). Represented by several taxa that together show a general trend towards an increase in size, flightlessness, and foot-propelled

Fig. 6. Skeletal reconstructions of the Late Cretaceous hesperornithiform Baptornis and its much larger relative
Hesperornis.

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diving specializations, these birds have been recorded over much of the Northern Hemisphere and across
a vast latitudinal extentfrom the Arctic Circle to the Gulf of Mexicoand from depositional environments ranging from offshore to fluvial (Galton and Martin, 2002). Hesperornithiforms are also the first
birds for which a modern type of skull kinesis (prokinesis) can be confirmed (Bhler et al., 1988).
Throughout their history, they evolved a suite of foot-propelled diving specializations, including long
and slender pelves, densely packed bones, very short femora, knees bearing enormous lever-like patellae,
and large feet with toes able to rotate sideways. Histological studies of their bones have also shown that
unlike more primitive birds, hesperornithiforms had growth rates similar to their modern counterparts,
thus suggesting that the elevated rates characteristic of neornithines developed early in ornithurine history (Chinsamy et al., 1995; Padian et al., 2001; Chinsamy, 2002).
The earliest known hesperornithiform is the 100 million-year-old Enaliornis from England (Galton
and Martin, 2002), a taxon known from disarticulated remains. Slightly younger still is the Canadian
Pasquiaornis (Tokaryk et al., 1997), whose wing anatomy hints at rudimentary flying capabilities.
However, by far the best represented taxa of these birds are those known from later Cretaceous
(Turonian-Campanian) rocks from the North American Pierre Seaway, including the flightless Baptornis
(Martin and Tate, 1976), Parahesperornis (Martin, 1984), and Hesperornis (Marsh, 1880) (Fig. 6). Some
even younger hesperornithiforms are known from marine deposits of the Turgay Strait, a shallow seaway
that bisected Eurasia, linking the Arctic Ocean with an equatorial basin, and connected shallow seas that
flooded much of Europe. Known only from fragmentary bones, these terminal Cretaceous occurrences of
marine hesperornithiforms from the Old World are identified as the large Asiahesperornis (Nessov, 1992)
and Hesperornis rossicus (Rees and Lindgren, 2005). Contemporaneous records of small members of the
group have also been reported from fluvial rocks of Central Asia (Kurochkin, 2000).
From many of the same environments as the hesperornithiforms comes the historically well-known
Late Cretaceous seabird Ichthyornis (Marsh, 1880). Although originally considered to comprise a series
of closely related taxa, recent revisionary work has clarified taxonomic problems associated with a large
collection of specimens collected in the 19th century, and has shown that these are likely members of just
the single species, Ichthyornis dispar (Clarke, 2002) (Fig. 7). As a matter of fact, one of the several original species types (i.e., I. victor) has been shown to be a chimera formed by numerous specimens, some
even of taxa that may be closer to modern avians (Clarke, 1999, 2002). In most aspects of its skeleton,
the flying Ichthyornis is anatomically modern, albeit still toothed. In recent times, this taxon has consistently been regarded as an immediate relative of modern avians (Fig. 1). Its specimens have been collected from marine and brackish deposits across North America (Feduccia, 1999) and remains of alleged
close relatives were reported from 90 million-year-old similar environments in Uzbekistan (Nessov,
1992). A range of sizes are represented among the known North American specimenssome are 20 percent larger than othersillustrating a general trend towards larger size over the 15 million years (early
Turonian-early Campanian) of the known history of Ichthyornis. Whether this large size range is significant taxonomically remains unclear and will to a great extent depend on interpretations of the growth
physiology of this bird (Clarke, 2002).

EARLY NEORNITHINE DIVERGENCE:

THE RISE OF MODERN BIRDS
Ichthyornis is certainly very intimately related to modern birds, Neornithes, but ongoing studies are revealing taxa that seem to be even more closely related. A number of anatomically modern Late
Cretaceous aviansLimenavis (Clarke and Chiappe, 2001), Apatornis (Clarke, 2004), Iaceornis (Clarke,

Chiappe and Dyke - The early evolutionary history of birds

145

2004), and others (Dyke et al., 2002)appear to be closer than Ichthyornis to the ancestry of extant
birds. Since the 19th century, a long list of Cretaceous fossils have been classified within the neornithine
lineages themselves (e.g., Marsh, 1873, 1880; Shufeldt, 1915; Brodkorb, 1963; Hou and Liu, 1984;
Kurochkin, 1985; Elzanowski and Brett-Surman, 1995; Hope, 1999, 2002; Howard, 1955; Tokaryk and
James, 1989; Nessov, 1992; Olson, 1992; Noriega and Tambussi, 1995; Stidham, 1998; Kurochkin et al.,
2002). These fossils are generally fragmentary and most of them are represented simply by isolated
bones. The essentially modern anatomy of these fossils has led to the notion that some neornithine lineages (e.g., charadriiforms, pelecaniforms, galliforms, anseriforms, gaviiforms) diversified in pre-Tertiary
times (e.g., Martin, 1984; Cracraft, 1986; Chiappe, 1995; Padian and Chiappe, 1998; Feduccia, 1999;
Hope, 2002) although this perception has not received confirmation from genealogical studiesbased on
cladistic methodologyof the most complete fossils (Clarke and Chiappe, 2001; Dyke et al., 2002). An
exception to this trend of fragmentary, supposedly Cretaceous 'neornithines' is the recently published
Vegavis (Clarke et al., 2005) from the Late Cretaceous of western Antarctica. Vegavis represents the first
skeleton complete enough to be placed unambiguously within a modern clade of birds, Anseriformes
(screamers, ducks and geese) (Clarke et al., 2005). Support for the Cretaceous differentiation of a diversity of neornithines has also been defended on the basis of temporal calibrations of genealogical hypotheses of living birds as inferred from their genetic makeup (e.g., Cooper and Penny, 1997; van Tuinen and
Hedges, 2001; Paton et al., 2002). These molecular studies have supported a pre-Tertiary radiation, or in-

Fig. 7. Skeletal reconstruction of the Late Cretaceous Ichthyornis.

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itial diversification, for at least ratites (ostriches, rheas, and their kin; van Tuinen and Hedges, 2001), parrots (Miyaki et al., 1998), songbirds (Barker et al., 2002), landfowl (van Tuinen and Dyke, 2004), and
shorebirds (Paton et al., 2002). Despite some of these inferences being based on doubtful calibration and
limited gene or taxon sampling (Dyke, 2001; Dyke and van Tuinen, 2004 van Tuinen and Hedges, 2004),
a contentious debate has been engendered (Dyke, 2003; Feduccia, 2003; van Tuinen et al., 2003). The
extreme viewpoints of this controversy are taken, on the one hand, by paleontologists reading the fossil
record primarily at face value (e.g., Feduccia, 1999, 2003) and on the other hand, by molecular systematists who either disregard the fossil record or use it uncritically, outside a genealogical framework (e.g.,
Cooper and Penny, 1997). Both viewpoints envision a Cretaceous origin for the group, but while one
endpoint hypothesis argues that most primitive neornithines survived the terminal Cretaceous extinction
and gave rise to an explosive radiation in the earliest Tertiary (Feduccia, 1995, 1999, 2003), the other
endpoint hypothesis supports a much earlier origin for the group with most divergences occurring during
the Mesozoic (Cooper and Penny, 1997; van Tuinen and Hedges, 2001). No solution to this debate is
likely to be forethcoming, but it is likely that a middle ground between both extreme positions will turn
out to be correct. The discovery of Vegavis suggests that at least some major divergences of neornithines
(anseriforms, galliforms, and paleognaths) must have diverged in pre-Tertiary times and the temporal
proximity to the K-T boundary of birds confidently placed within a much greater diversity of modern lineages also implies a substantial degree of differentiation prior to the end of the Cretaceous. Perhaps, as
has been suggested, some clades of modern birds did originate deep in the Cretaceous but maintained a
low Mesozoic diversity (Cooper and Fortey, 1998). Indeed, it could also be the case that much of
Cretaceous neornithine evolution took place in the Southern Hemisphere, from where the fossil record
has been far less thoroughly sampled (Cracraft, 2001). Yet arguments for an extensive Early Cretaceous
divergence are at odds with the complete absence of anatomically modern fossils from a number of
well-sampled deposits containing the abundant remains of more basal birds, and other small vertebrates
(Benton, 1999). The bottom line in this debate is that birds themselves are no longer rare in the
Cretaceous (more than 30 taxa alone are known from the Early Cretaceous; Chiappe and Dyke, 2002;
Chiappe and Witmer, 2002) but so far nothing that can be considered anatomically modern has ever been
found prior to the terminal stages of the Cretaceous.

ACKNOWLEDGEMENTS
We thank Yuong-Nam Lee for inviting us to participate in this Symposium. We are also grateful to
Stephanie Abramowicz, Ryan Urabe, and Ed Heck for producing the illustrations and to Bill Evans for editing the manuscript. Tim Rowe kindly provided us with his reconstructions of Archaeopteryx and
Ichthyornis. The manuscript benefited from the reviews of Yukimitsu Tomida and an anonymous reviewer.

Luis M. Chiappe and Gareth J. Dyke

1

The Dinosaur Institute, Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los
Angeles, California 90007 U.S.A., chiappe@nhm.org
2
Department of Zoology, University College Dublin, Belfield Dublin 4, Ireland, gareth.dyke@ucd.ie

Chiappe and Dyke - The early evolutionary history of birds

147

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