ORNITOLOGIA NEOTROPICAL 15 (Suppl.): – , 2004
© The Neotropical Ornithological Society
THE CLOSEST RELATIVES OF BIRDS
Luis M. Chiappe
Department of Vertebrate Paleontology, Natural History Museum of Los Angeles County, 900
Exposition Boulevard, Los Angeles, CA 90007, USA. Email: firstname.lastname@example.org
Resúmen. – Los ancestros más cercanos de las aves. – El origen de las aves, el clado originado a partir del
ancestro común de Archaeopteryx del Jurásico tardío y las aves vivientes, ha estado inmerso dentro de un
gran debate científico durante toda la historia de la biología evolutiva. Si bien muchas hipótesis diferentes
sobre el origen de las aves han sido propuestas en los últimos dos siglos, hoy en día existe un enorme con-
senso en favor de la idea de que las aves evolucionaron a partir de dinosaurios terópodos clasificados den-
tro de los Maniraptora. El sustento osteológico de esta hipótesis es enorme. Los esqueletos de dinosaurios
maniraptores como los dromaeosáuridos, troodóntidos y oviraptóridos, comparten muchas similitudes
con aquellos de las aves. Además, una serie de espectaculares descubrimientos realizados durante la última
década ha brindado diversas líneas de evidencia que complementan el ya inmenso cúmulo de característi-
cas osteológicas que sustenta la hipótesis Maniraptora. Esta reciente evidencia deriva fundamentalmente
del estudio de la morfología de los huevos y de la anatomía tegumentaria, pero también incluye inferencias
de comportamiento basadas en un pequeño, pero extraordinario, número de fósiles. Todos estos descubri-
mientos han documentado la presencia de atributos tales como plumas, empollamiento, ovodeposición
secuencial (autocrónica), y otras características avianas en dinosaurios maniraptores basales. La evidencia
disponible sugiere fuertemente que las aves deben ser clasificadas dentro de los terópodos y que muchos
atributos previamente considerados como únicos de las aves (desde el comportamiento de empollamiento
a la capacidad de volar) evolucionaron por primera vez en dinosaurios maniraptores. Si bien los críticos de
la hipótesis Maniraptora han resaltado problemas temporales y ontogenéticos, dichas objeciones son clara-
mente irrelevantes. Los dos argumentos más frecuentemente utilizados, la llamada “paradoja temporal” y
la homología de los dedos de la mano aviana, se encuentran embebidos en inconsistencias lógicas. Quizás
más importante es el hecho de que los críticos de la hipótesis Maniraptora han sido incapaces de formular
una hipótesis filogenética alternativa que pueda explicar la enorme similitud entre terópodos no-avianos y
aves, dentro del marco de la parsimonia cladista.
Abstract. — The origin of birds, the clade originating from the common ancestor of the Late Jurassic
Archaeopteryx and extant birds, has been at the center of a heated debate throughout the history of evolu-
tionary biology. Although many disparate hypotheses of bird origins have been proposed in the last two
centuries, an overwhelming consensus exists in support of the idea that birds evolved from maniraptoran
theropod dinosaurs. Osteological support for this hypothesis is plentiful. The skeletons of such manirapto-
ran dinosaurs as dromaeosaurids, troodontids, and oviraptorids, share a great deal of similarity with those
of birds. In addition, a series of spectacular discoveries in the last decade has provided new lines of evi-
dence that supplement the already overwhelming osteological data. This recent evidence is derived prima-
rily from the study of egg morphology and integumentary anatomy but also includes behavioral inferences
based on a handful of rare fossils. These discoveries have documented the presence of feathers, brooding
behavior, autochronous ovideposition, and other avian attributes among basal maniraptoran dinosaurs.
The available evidence strongly supports the classification of birds within theropods and indicates that
many avian attributes previously thought to be unique to birds (from brooding behavior to flight) first
evolved among maniraptoran dinosaurs. Although dissenters of the Maniraptoran hypothesis of bird ori-
gins have countered by highlighting temporal and developmental limitations, these criticisms are clearly
spurious. The most frequently voiced arguments, the so called “temporal paradox” and the homology of
the digits of the avian hand, are tainted by logical inconsistencies. Perhaps the most important is the fact
that these dissenters have been unable to produce alternative phylogenetic hypotheses that could explain,
within the methodological framework of cladistic parsimony, the vast amount of similarity between non-
avian theropods and birds. Accepted 11 December 2003.
Key words: Bird origin, evolution, Theropoda, Maniraptora.
Birds diversified more than 150 million years
ago. Their oldest known records are still from
the Late Jurassic of southern Germany, where
Archaeopteryx was first discovered in the mid-
century. Identifying the closest relatives
to the group’s ancestor (the most recent
common ancestor of Archaeopteryx and
modern birds) has been a matter of scientific
debate and scrutiny throughout the history
of evolutionary biology. As early as the
century, birds were placed immediately
ahead of flying fishes in the ‘chain of being’
postulated by the naturalists of that
time. With the advent of evolutionary
thinking, especially after Darwin’s theory
of evolution by natural selection, more
explicit hypotheses of relationships were
formulated. Indeed, in post-Darwinian
times, birds were considered to be most
closely related to a variety of extinct
and extant lineages of reptiles, including
turtles, lizards, crocodylomorphs (modern
crocodiles and its Triassic relatives), a
diversity of basal archosaurs and archosauro-
morphs (e.g., the Triassic Euparkeria,
Longisquama, and Megalancosaurus), pterosaurs
(pterodactyls and their kin) as well as thero-
pod and ornithischian dinosaurs (Fig. 1).
Today, however, although most of these
hypothetical relationships have been aban-
doned, the theropod hypothesis is receiving
nearly universal acceptance. Hypotheses
identifying crocodylomorphs, basal archo-
saurs, or basal archosauromorphs as the
closest relatives of birds have occasionally
resurfaced in the recent literature but
these have been used more as default
hypotheses than as real alternatives to
the theropod origin of birds. Indeed, a
close examination of these “alternative”
hypotheses reveals a lack of empirical support
because character evidence in support
of these hypotheses has also been discovered
among theropod dinosaurs. Furthermore,
these “alternative” hypotheses have continued
to be framed outside modern systematic
methods (i.e., cladistics), and thus also
lack the rigor of current phylogenetic
Today, the debate on bird ancestry has
been resolved. The uncertainties that led to
this long controversy, both empirical and
methodological, have been clarified. The clos-
est relatives of birds can be found among
theropod dinosaurs, the carnivorous preda-
tors that ruled the Mesozoic ecosystems. The
history of this fascinating scientific debate has
been summarized in a number of recent
reviews, among them those of Witmer (1991,
2002), Padian & Chiappe (1998), Chiappe
(2001), and Prum (2002). A discussion in
Spanish can also be found in Chiappe & Var-
gas (2003). In this paper, addressed to the
ornithological community, I hope to convey
the message that the scientific hypothesis of
their diverse disciplines, from ecology to
behavior to systematics, will greatly benefit
from incorporating the notion that modern
birds are highly specialized, short-tailed, and
flighted theropod dinosaurs.
CLOSEST RELATIVES OF BIRDS
BREEF HISTORY OF THEROPOD
HYPOTHESIS OF BIRD ORIGINS
The first suggestion that birds could have
been related to dinosaurs came soon after the
publication of Darwin’s “Origin of Species”.
Similarities in the structure of the tarsus led
Gegenbaur (1864) to place the small, Late
Jurassic theropod Compsognathus in an interme-
diate position between birds and other rep-
FIG. 1. Cladogram illustrating the diversity of hypotheses of the origin of birds (within Archosauromor-
pha). BA, hypotheses that relate birds to some basal archosaurs or basal archosauromorphs; CRO,
hypotheses in support of a crocodylomorph origin of birds; OR, a hypothesis in favor of a common ori-
gin between birds and ornithischian dinosaurs; PT, a hypothesis supporting the ancestry of birds from
pterosaurs (flying reptiles); TH, hypotheses in favor of the origin of birds from theropod dinosaurs; this
hypothesis is the one endorsed in the present study. Modified from Chiappe & Vargas (2003).
tiles. At about the same time, Cope (1867)
compared the tarsus of the Jurassic theropod
Megalosaurus to that of an ostrich and, on the
basis of this and on similarities in the elonga-
tion of the neck vertebrae and the lightness of
the skull, he argued for a close relationship
between theropods and birds. Despite these
initial considerations, it was Huxley (1868,
1869) who championed the 19
cussions of the origin of birds from theropod
dinosaurs. In 1869, Huxley argued that “if the
whole hind quarters, from the ilium to the
FIG. 2. Some osteological synapomorphies in support of the maniraptoran origin of birds. Modified from
Chiappe & Vargas (2003).
CLOSEST RELATIVES OF BIRDS
toes, of a half-hatched chicken could be sud-
denly enlarged, ossified, and fossilized as they
are, they would furnish us with the last step of
the transition between Birds and Reptiles; for
there would be nothing in their characters to
prevent us referring them to the Dinosauria.”
(Huxley 1869). During the second half of the
century, the theropod hypothesis of bird
origins was one of a pool of other hypotheses.
Just as today, detractors argued that the simi-
larities between birds and theropod dinosaurs
could well be explained by convergence [see
Seeley’s discussion in Huxley (1869)]. In the
century, with the discovery of more
generalized, Triassic archosaurs, in particular
the South African Euparkeria (Broom 1913),
the theropod hypothesis lost ground. Thero-
pods were deemed as too specialized to be the
ancestors of birds (Heillman 1926). Such a
notion dominated the field for several decades
(see Romer 1966) until the early 1970s, when
renewed interest on the origin of birds took
place (see Witmer 1991). Among this new
wave of interest was Ostrom’s work on
Archaeopteryx (Ostrom 1973, 1976), who revi-
talized Huxley’s hypothesis of the theropod
origin of birds. During the thirty years that
has passed since Ostrom’s initial work on bird
origins, a large quantity of fossil documenta-
tion supporting the dinosaurian ancestry of
the group has been accumulated. Today,
despite disagreement regarding the specific
theropod clade phylogenetically closest to
birds (e.g., dromaeosaurids, troodontids, ovi-
raptorids), an overwhelming consensus exists
in support to the notion that birds evolved
from maniraptoran theropods (Chiappe &
EVIDENCE FOR MANIRAPTORAN
ORIGIN OF BIRDS
Several lines of evidence converge in support
of the hypothesis that the closest relatives of
birds are to be found among maniraptoran
theropod dinosaurs (Chiappe 2001). The
most visible evidence of this hypothesis is
based on comparisons of the osteology,
behavior, oology, and integument of birds
with that of a variety of nonavian theropods.
These lines of evidence are summarized
Osteology. A multitude of derived osteological
characters are shared by all, or some, nona-
vian maniraptoran theropods and birds (Fig.
2). Comparisons between these taxa are
greatly assisted by the many newly discovered
basal birds (Padian & Chiappe 1998, Chiappe
& Dyke 2002), which possess a skeletal mor-
phology only slightly modified from the
ancestral maniraptoran condition. Some of
these derived characters are the presence of
rostral, dorsal, and caudal tympanic recesses
(air spaces connected to the ear region), ven-
tral processes on cervicothoracic vertebrae,
ossified ventral segments of thoracic ribs,
forelimbs that are more than half the length
of hindlimbs, a semilunate carpal bone allow-
ing swivel-like movements of the wrist, clavi-
cles fused into a wishbone (probably a
synapomorphy of a more inclusive theropod
group), a pubic peduncle of the ilium longer
than the ischiadic peduncle (these peduncles
form the front and rear borders of the hip-
socket), a vertically to caudoventrally oriented
pubis ending in a boot-like expansion that
projects only caudally, an ischium two-thirds
or less the length of the pubis, a femur with a
feeble fourth trochanter (the attachment of
the caudofemoralis longus muscle), and many
other characters distributed over the entire
skeleton (Novas & Puerta 1997, Holtz 1998,
Sereno 1999, Clark et al. 2002). Birds also
share a number of derived characters with
more inclusive theropod clades such as the
Coelurosauria, Tetanurae, and Neotheropoda,
and evolutionary trends towards the modern
avian condition can be seen when these are
examined across cladograms of theropods
(e.g., forelimb elongation, pubic rotation,
braincase amplification, stiffening of the tail).
Indeed, many osteological features previ-
ously thought to be exclusively avian, such as
a furcula, laterally facing glenoids, large bony
sterna, uncinate processes on ribs, have now
been discovered among non-avian manirap-
torans (Padian & Chiappe 1998).
Behavior. Evidence of the behavior of extinct
organisms is rarely preserved in the fossil
record. A handful of extraordinary discover-
ies, however, have shed light on the nesting
conduct of certain nonavian maniraptorans.
Several skeletons of Late Cretaceous ovirap-
torids from the Gobi Desert, belonging to
both Oviraptor (Osborn 1924) and Citipati
FIG. 3. A partial skeleton of the oviraptorid Citipati from the Late Cretaceous of the Gobi Desert brood-
ing a clutch of its own eggs (A) and an interpretation of the posture of this animal when in life (B). Modi-
fied from Clark et al. (1999).
CLOSEST RELATIVES OF BIRDS
(Clark et al. 2001), have been discovered on
top of their clutches of eggs (Fig. 3). The
specimens of Citipati show that the animals
adopted a posture similar to those of brood-
ing birds, with their legs tucked inside an open
space at the center of the clutch and their
forelimbs surrounding the periphery of the
clutch (Clark et al. 1999). An oviraptorid
embryo inside an egg of comparable mor-
phology to those in these clutches strongly
supports the idea that these specimens were
brooding their own nest (Clark et al. 1999).
These discoveries have forced the reinterpre-
tation of inferences made decades ago on the
basis of the holotype of Oviraptor philoceratops
(Osborn 1924) which, because it had also
been found on top of a clutch of eggs, had
been interpreted (and consequently named) as
FIG. 4. Some oological synapomorphies in support of the maniraptoran origin of birds. Note the pres-
ence of two or more layers in the eggshell of oviraptorids, troodontids, and birds, and the asymmetric
shape of the egg in the last two lineages. Modified from Chiappe & Vargas (2003).
an egg-predator (Norell et al. 1995). A similar
discovery of a Late Cretaceous troodontid
skeleton from Montana in an identical brood-
ing position suggests that, regardless of its
specific function (e.g., protection, incubation),
the typical avian nesting behavior (i.e., adults
sitting on top of their nests) was widespread
among nonavian maniraptorans.
Oology. The general morphology and micro-
structure of calcified eggs is specific to certain
groups of extant and extinct reptiles
(Mikhailov 1997, Grellet-Tinner 2000). Until
recently, the precise characteristics of the egg-
shell microstructure of nonavian theropods
remained elusive due to the absence of diag-
nostic embryonic material. The discovery of
the Gobi oviraptorid embryo provided the
first definitive evidence of a nonavian thero-
pod egg (Clark et al. 1999). Since then, other
nonavian maniraptorans embryos have been
found. These include other species of ovirap-
torids (Weishampel et al. 2000), therizinosau-
rids (Manning et al. 2000), and troodontids
(Varricchio et al. 2002). Comparative studies
between the eggshell microstructure of these
eggs and those of extant birds have revealed
features exclusively common to them (Fig. 4)
(Mikhailov 1992, Varricchio et al. 1997, Zelen-
itzky et al. 2002, Grellet-Tinner & Chiappe in
press). One of these features involves the
presence of more than one distinct micro-
structural layer, most commonly distin-
guished by the differential disposition of the
calcitic crystals (Grellet-Tinner & Chiappe in
press). The dinosaurian eggshell is character-
ized by the presence of shell units, of which
the inner portion is formed by a crystalline
structure that radiates from a core, often
termed the organic core. In nonavian thero-
pods, these units also possess an external
zone with a more spongeus microstructural
appearance, although in thin sections this
layer exhibits a more laminar appearance (this
layer is often referred as the squamatic zone).
In birds, this external zone may grade into, or
be completely separated from, a third, outer-
most zone and, in paleognaths, even a fourth
zone can be recognized (Grellet-Tinner
2000). Even though up to now only two lay-
ers have been found in the eggshell of non-
avian theropods, no other hard-shelled egg
possesses a similar zonation. Additional char-
acter states shared by the eggs of nonavian
maniraptorans and those of birds include a
reduction in the porosity of the shell, a rela-
tive increase in the volume of the egg (with
respect to the size of the adult), and the pres-
ence of a longer axis (eggs that are elongated)
(Zelenitzky et al. 2002). Another oological fea-
ture easily recognizable is the presence of
asymmetrical eggs, those in which one pole is
narrower than the other. While turtles, croco-
diles, and nearly all non-avian dinosaurs are
characterized for having symmetrical eggs, the
eggs of birds and those of troodontid
maniraptoran theropods have one pole that is
narrower than the other. Further similarities
between nonavian maniraptorans and birds
involve the mode of ovideposition. Unlike in
the clutches of other dinosaurs where eggs
have no spatial arrangement, in theropod
clutches, the eggs are clearly arranged in pairs.
Such a pairing is suggestive of autochronous
ovideposition, a mode of deposition in which
eggs are not laid en masse but sequentially, at
discrete time intervals. The pairing of eggs
found in fossil egg-clutches attributed to
theropod dinosaurs thus suggests that it could
have taken several days for a theropod female
to lay its egg-clutch (Varricchio et al. 1997,
Grellet-Tinner & Chiappe in press), a condi-
tion shared with birds.
Integument. Feathers have always been the
quintessential bird feature. In recent times,
however, feathers have been found in a vari-
ety of maniraptoran theropods, where skele-
tons are found in a series of Early Cretaceous
lacustrine deposits in the northeastern corner
CLOSEST RELATIVES OF BIRDS
of China (Fig. 5). Carbonized remains of
feathers are now known for the therizinosau-
rid Beipiaosaurus (Xu et al. 1999), the oviraptor-
osaur Caudipteryx (Ji et al. 1998, Zhou & Wang
2000), the dromaeosaurids Sinornithosaurus
(Xu et al. 1999) and Microraptor (Xu et al. 2000
FIG. 5. The integument of nonavian maniraptorans (A, B) and a cladogram (C) illustrating the phyloge-
netic relationships of known feathered nonavian theropods. A represents the oviraptorosaur Caudipteryx.
The inset highlights the vaned feathers attached to the distal end of the forelimb. Note also the tuft of
feathers attached to the tail of this dinosaur. B represents filamentous feathers near the tail of the dro-
maeosaurid Sinornithosaurus. Modified from Chiappe & Dyke (2002).
2003), and the long-armed Protarchaeopteryx (Ji
et al. 1998), which phylogenetic placement
among maniraptorans is less well-known.
Integumentary structures interpreted as feath-
ers have also been found in more primitive
theropods such as the basal coelurosaurian
Sinosauropteryx (Chen et al. 1998, Currie &
Chen 2001), also from the same Early Creta-
ceous rocks of China. While the latter exhibits
feathers that are filament-like, with a minimal
degree of branching, Caudipteryx, Protarchaeop-
teryx, Sinosauropteryx, and Microraptor display
pennaceous feathers with distinct shafts and
vanes. Down-like feathers also cover portions
of the skeletons of all these taxa. A fan-
shaped cluster of pennaceous feathers is
attached to the distal part of the tail of Caudip-
teryx (Fig. 5). The frond-like tails similar to
those in Archaeopteryx are present in the dro-
maeosaurids Sinosauropteryx and Microraptor,
although these pennaceous feathers are more
restricted to the distal half of the tail. Long
pennaceous feathers are also attached to the
tip of the forelimbs of Caudipteryx (Ji et al.
1998) (Fig. 5) while in the tiny Microraptor gui,
they form a wing of essentially modern design
(Xu et al. 2003). There is also the remarkable
presence in the latter taxon of pennaceous
feathers attached to the distal half of the
hindlimb. Such an attribute has been used to
argue that Microraptor gui was able to glide
using these hindlimb feathers as an additional
airfoil (Xu et al. 2003). Despite functional
considerations that make this idea untenable
(Chiappe & Vargas 2003), there is little doubt
that with such a small wing loading, Microrap-
tor gui was able to fly [see Padian & Chiappe
(1998) for a recent discussion on the origin of
flight]. The presence of feathers in so many
coelurosaurian taxa suggests that these integ-
umentary appendages evolved in the com-
mon ancestor of the group if not earlier.
Given the evidence at hand, the presence of
simple, filament-like feathers is considered as
a synapomorphy of Coelurosauria while the
presence of more derived, pennaceous feath-
ers is interpreted as synapomorphic of
Maniraptora. These discoveries not only doc-
ument the presence of feathers outside birds
but also, suggest that some nonavian thero-
pod dinosaurs (e.g., Microraptor gui) may have
been able to fly.
CRITICISMS OF THE MANIRAPT-
ORAN HYPOTHESIS OF BIRD
The evidence summarized above is so com-
pelling that the idea that birds are the descen-
dants of a maniraptoran ancestor has been
accepted by a great number of evolutionary
biologists. Nonetheless, the maniraptoran
hypothesis of bird origins is not exempt of
critics, even though it is fair to say that these
represent only a tiny fraction of specialists.
Concerns have been expressed primarily
highlighting apparent inconsistencies within
the known fossil record and with the inferred
homology of certain structures. These appar-
ent inconsistencies are briefly discussed
INCONSISTENCIES WITHIN THE
KNOWN FOSSIL RECORD
This criticism highlights the chronological
gap between the oldest known bird, the Late
Jurassic Archaeopteryx, and the Cretaceous
nonavian maniraptorans that are typically
used in discussions of bird origins (e.g.,
Deinonychus, Velociraptor, Oviraptor). This argu-
ment has become known as the “temporal
paradox” since it highlights the inconsistency
of arguing that birds evolved from creatures
that lived several million years after their own
origin (Feduccia 1996, 1999). However, exam-
ination of the theoretical basis and supporting
evidence of the “temporal paradox” indicates
that this argument stems from philosophical
misconceptions, disregards critical fossil evi-
CLOSEST RELATIVES OF BIRDS
dence, and it constitutes an artifact caused by
not considering all alternative hypotheses of
bird origins at the same time (Brochu &
In the first place, the “temporal paradox”
stems from a philosophical misconception
because none of these Cretaceous dinosaurs is
regarded as the direct ancestor of birds
(Padian Chiappe 1998, Witmer 2002). In
modern times, the hypothesis of a manirapto-
ran ancestry of birds has been framed as a cla-
distic hypothesis that postulates the existence
of a most recent common ancestor of these
Cretaceous dinosaurs and Archaeopteryx that
obviously existed before the divergence of the
oldest of these taxa, Archaeopteryx (e.g., Gau-
thier 1986, Forster et al. 1998, Holtz 1998, Se-
reno 1999, Norell et al. 2001, Clark et al. 2002).
Thus, in contrast to what has been claimed by
the proponents of the “temporal paradox”,
the maniraptoran hypothesis does set the ori-
gin of birds in pre-Jurassic times.
In addition, the absence of the pre-Creta-
ceous maniraptorans the “temporal paradox”
seems to highlight has long been proved to be
mistaken. Late Jurassic maniraptorans have
been known for decades, even if from frag-
mentary remains (Padian & Jensen 1980), and
a lower jaw of a maniraptoran therizinosaurid,
Eshanosaurus deguchiianus, has been discovered
in the Early Jurassic of China (Xu et al. 2001).
This and the fact that the stratigraphic ranges
of theropod groups containing the clade
Maniraptora have been recently extended
back by many millions of years [e.g., basal tet-
anurans are now known from the Late Trias-
sic; Arcucci & Coria (2003)], suggest that the
divergence of maniraptorans occurred much
earlier than in the Late Jurassic. The fact that
maniraptoran fossils are exceedingly rare in
pre-Cretaceous times may be related to a clear
bias against small-sized dinosaurs of Jurassic
age (most maniraptorans are of relatively
small size) and the much smaller volume of
Jurassic outcrops than those of Cretaceous
age (Clark et al. 2002).
Finally, the “temporal paradox” appears to
exist only if one considers the temporal gap
between the 100-million-year old Deinonychus,
to take an example of a well-known dromaeo-
saurid, and the 150-million-year old Archaeop-
teryx. Yet, as shown by the statistical test of
Brochu & Norell (2000), when other records
of well-known maniraptorans are included
(e.g., the 125-million-year old dromaeosaurids
Sinornithosaurus and Microraptor) and when
hypotheses of bird origins are compared
against each other, placing birds within
groups indicated by hypotheses (e.g., crocody-
lomorphs or more basally within archosaurs;
see Fig. 1) other than the theropod hypothesis
may increase the temporal disparity by as
much as 15%. Thus, when the “temporal par-
adox” is considered in the context of current
alternative hypotheses of bird origins (Fig. 1),
the maniraptoran hypothesis is temporally the
most consistent (Brochu & Norell 2000).
INCONSISTENCIES WITH THE
INFERRED HOMOLOGY OF SOME
Embryology of the avian hand. Opponents to the
maniraptoran origin of birds (e.g., Feduccia
1999, 2003) have highlighted the conflict
between the correspondence of the three
wing digits of birds with respect to the ances-
tral pentadactyl hand of tetrapods, as indi-
cated by embryological studies, and that
inferred from the palaeontological evidence.
Embryological investigations of extant birds
have identified five precartilaginous conden-
sations of which only those in positions II,
III, and IV develop into the three osseous
digits of the adult hand (Feduccia & Nowicki
2002, Larsson & Wagner 2002). This observa-
tion has often been extrapolated to include all
birds, even the Late Jurassic Archaeopteryx, and
the three fingers of the avian hand have been
identified as homologous to digits II–IV of
the ancestral pentadactyl hand (Burke &
Feduccia 1997, Feduccia 1999, Feduccia &
Nowicki 2002). In contrast, inferences based
on the transformation of the hand as
observed from fossils representing different
stages of dinosaur evolution have identified
the homology of the three fingers of Archaeop-
teryx as those corresponding to digits I, II,
and III of the ancestral pentadactyl hand.
This paleontological evidence shows a trend
of reduction of the outermost two digits (VI
and V) from the most basal theropods, where
these digits are abbreviated but still present,
to tetanuran theropods bearing a tridactyl
hand (Padian & Chiappe 1998). The three
digits of the latter theropods have the same
phalangeal formula as digits I, II, and III of
the primitive five-fingered theropods, thus
indicating that the three fingers of tetanurans
(a group that also includes Maniraptora) cor-
respond to digits I–III of the ancestral penta-
dactyl hand. The remarkable similarity in
morphology, proportions, and phalangeal for-
mula of the manual digits of certain nonavian
FIG. 6. Chondrification and ossification patterns of the right hand of the scincid lizards Hemiergis perioni
and H. quadrilineata – an example of a homeotic frame shift in the development of the hand of a tetrapod.
H. perioni includes morphs with three and four manual digits (A, B). In these morphs, digital condensa-
tions II and III develop into the two anteriormost digits of the adult hand, which have three and four pha-
langes, respectively. Adults of H. quadrilineata have only two manual digits, the anteriormost of them with
three phalanges and the other one with four phalanges (C). While in H. perioni the two anteriormost man-
ual digits, those with three and four phalanges, ossify from condensations II and III, in H. quadrilineata,
these digits ossify from condensations III and IV. The morphological similarity between the mature digits
of this species and digits II and III of other Hemiergis species is such that the positional identity of the two
digits of H. quadrilineata can only be verified through ontogenetic studies. Modified from Shapiro (2002).
CLOSEST RELATIVES OF BIRDS
maniraptorans (e.g., Velociraptor, Deinonychus)
to those of Archaeopteryx has extended this
conclusion to this and to other basal birds.
Two different issues are involved in this
controversy. On the one hand is the question
of whether there is empirical basis for extrap-
olating the ontogenetic development of mod-
ern birds to Archaeopteryx. On the other hand
is whether the maniraptoran ancestry of birds
can be sustained even if nonavian theropods
developed their manual digits through a devel-
opmental pathway different than that of mod-
ern avians. The extrapolation of the
embryogenesis of the hand of extant birds to
archaic avian lineages including Archaeopteryx
appears unwarranted given that the hand of
modern birds is highly transformed and that
embryological evidence is unavailable for
either Archaeopteryx or any other basal avian
lineage. Indeed, the fact that the hand of
Archaeopteryx is remarkably similar to that of
nonavian maniraptorans such as dromaeosau-
rids (Ostrom 1976) suggests that if any devel-
opmental trajectory is to be extrapolated to
this Late Jurassic bird, it should be the one
inferred for dromaeosaurid theropods. The
second issue, namely whether embryogenetic
differences should take precedence over the
enormous volume of evidence supporting the
phylogenetic relationship between birds and
certain lineages of nonavian maniraptorans, is
also problematic. Certainly, such an approach
would be in direct conflict with the parsimony
methods endorsed by modern systematic
techniques. If the maniraptoran origin of
birds is to be rejected because the digits of the
hand of living birds have ontogenetic trajecto-
ries different from those inferred for extinct
maniraptorans, the unquestionable similari-
ties in the osteology, plumage, oology, and
behavior of all these organisms would have to
be explained in the context of evolutionary
convergence. Nonetheless, the apparent
incongruence between the manual osteogene-
sis of modern birds and that of their nonavian
theropod relatives can be explained without
resorting to a different phylogenetic hypothe-
sis. Wagner & Gauthier (1999) have argued
that homeotic frame shifts could have led to a
developmental pattern in which digits that
previously ossified from condensations I–III
became ossified from condensations II–IV.
Homeotic frame shifts are relatively common
among other vertebrate lineages. An illustra-
tive example involves the development of the
hand of the two-toed earless skink (Hemiergis
quadrilineata), an Australian scincid lizard (Sha-
piro 2002) (Fig. 6). Many studies have docu-
mented the fact that ontogenetic trajectories
do evolve and that these transformations
could occur without affecting either the mor-
phology or function of the developing struc-
ture (Wagner & Misof 1993, Mabee 2000, Hall
2003). These structures are homologous, even
if their development pathways are different.
Lung structure and ventilation. Interpretations of
soft structures supposed to indicate visceral
compartmentalization in the early Cretaceous
basal coelurosaurian theropod Sinosauropteryx
prima (Chen et al. 1998) played a paramount
role in Ruben et al.’s (1997) claim that nona-
vian theropods had a crocodile-like, hepatic-
piston mechanism for lung ventilation. Ruben
et al. (1997) questioned the close relationship
between birds and nonavian theropods on the
basis of this interpretation, because according
to these authors, the transition from the croc-
odile-like pulmonary system to the flow-
through lung system of birds would have
required the evolution of a diaphragmatic her-
nia in the alleged partition that would have
compromised the efficiency of the pulmonary
system of the transitional forms.
As in the case of other critics to the thero-
pod hypothesis of bird origins, this argument
is based on problematic interpretations.
Detailed studies of the skeleton of the speci-
men of Sinosauropteryx prima used by Ruben et
al. (1997) have demonstrated that the struc-
ture interpreted as a septum separating the
abdominal cavity from the thoracic cavity is a
preservational artifact (Currie & Chen 2001).
Furthermore, the osteological correlates of
the avian flow-through lung are well-known
among nonavian theropods, in particular the
vertebral pneumatization for the entrance of
pulmonary air sacs. The presence of intracos-
tal articulations delimiting costal and ventral
ribs and the relatively large ossified sternal
plates of nonavian maniraptorans also suggest
that the coordinated costal and sternal move-
ments that ventilate the lungs of extant birds
may have already been present in these dino-
saurs (Clark et al. 1999). There is undeniable
evidence for the presence of skeletal struc-
tures correlated to the avian system of lung
structure and ventilation among nonavian
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are empirically and methodologically mislead-
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