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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-
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© The Neotropical Ornithological Society
Luis M. Chiappe
Department of Vertebrate Paleontology, Natural History Museum of Los Angeles County, 900
Exposition Boulevard, Los Angeles, CA 90007, USA. Email:
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 Darwins 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.
The first suggestion that birds could have
been related to dinosaurs came soon after the
publication of Darwins “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
century dis-
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).
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
early 20
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 &
Dyke 2002).
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).
(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
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.
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
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-
dence, and it constitutes an artifact caused by
not considering all alternative hypotheses of
bird origins at the same time (Brochu &
Norell 2000).
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).
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).
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).
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among nonavian theropods, in particular the
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ribs and the relatively large ossified sternal
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may have already been present in these dino-
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evidence for the presence of skeletal struc-
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... The dinosaurian origin of birds, originating as an idea in the 1860s with Huxley (1868aHuxley ( , b, 1870, is widely accepted today (Prum 2002;Chiappe 2004Chiappe , 2007Chiappe , 2009Erickson et al. 2009) and remains a very active and dynamic area of research. The re-emergence of the view that dinosaurs are in fact bird-like creatures is relatively recent, but first mentions of the shared anatomical characteristics between birds and (non-avian) dinosaurs, date back much further. ...
... The finds are, for the most part, from Asia (China and Mongolia). They include dinosaurs preserved in an avian sleeping posture (Xu and Norell 2004), dinosaurs sitting on a clutch of eggs (Norell et al. 1995;Clark et al. 1999;Varricchio and Jackson 2004), adopting a bird-like resting pose (Milner et al. 2009) and outlines of fully feathered limb-or tail-sections (Xu et al. 2003;Chiappe 2004) (Fig. 7). ...
... The large number of key discoveries cementing the role of predatory dinosaurs as bird ancestors led to intense debates about the origin of flight (Padian and de Ricqlès 2009). Clearly, some forms could not fly and used feathers for display and/or insulation, but others did have the anatomical features necessary for flight (Chiappe 2004). ...
Full-text available
Over many years of his life, the British naturalist Alfred Russel Wallace (1823-1913) explored the tropical forests of Malaysia, collecting numerous specimens, including hundreds of birds, many of them new to science. Subsequently, Wallace published a series of papers on systematic ornithology, and discovered a new species on top of a volcano on Ternate, where he wrote, in 1858, his famous essay on natural selection. Based on this hands-on experience, and an analysis of an Archaeopteryx fossil, Wallace suggested that birds may have descended from dinosaurian ancestors. Here, we describe the "dinosaur-bird hypothesis" that originated with the work of Thomas H. Huxley (1825-1895). We present the strong evidence linking theropod dinosaurs to birds, and briefly outline the long and ongoing controversy around this concept. Dinosaurs preserving plumage, nesting sites and trace fossils provide overwhelming evidence for the dinosaurian origin of birds. Based on these recent findings of paleontological research, we conclude that extant birds indeed descended, with some modifications, from small, Mesozoic theropod dinosaurs. In the light of Wallace's view of bird origins, we critically evaluate recent opposing views to this idea, including Ernst Mayr's (1904-2005) arguments against the "dinosaur-bird hypothesis", and document that this famous ornithologist was not correct in his assessment of this important aspect of vertebrate evolution.
... Extant vultures are characterized by large body size and static soaring flight, which are adaptations to being an obligate scavenger which, can greatly reduce the energy needed for flight (Ruxton & Houston, 2004). This strategy of saving muscular work might have originated early in avian history, as fossil records suggest that the varieties of modern flight modes have evolved from the Early Cretaceous (Chiappe, 2004). ...
Flight is an energetically costly form of transport imparting biomechanical stress that acts upon the wing bones. Previous studies have suggested that the cross‐sectional and microstructural features of wing bones may be adapted to resist biomechanical loads. During flight, however, each wing bone potentially experiences a unique loading regime. To assess possible differences among wing bones, we analyzed the microstructural features of the humerus, radius, ulna, and carpometacarpus (CMC) in eight griffon vultures (Gyps fulvus). Vascular canal orientation was evaluated in the diaphysis of the wing bones. Laminarity index (LI) was significantly different in the humerus versus CMC and ulna versus CMC. Results showed a lower proportion of circular vascular canals, due to resistance to torsional loads, in CMC than in humerus and ulna. The midshaft cross‐section revealed an elliptical shape in the CMC compared to the circular shape observed in the other wing bones, with a maximum second moment of inertia (Imax) orientation which suggests a capacity to withstand bending loads in a dorsoventral direction. The volumetric bone mineral density in the diaphysis was statistically different in CMC compared to the other bones analyzed. Its lower mineral density may reflect an adaptation to a different type and load of stresses in CMC compared to the proximal wing bones. No significant difference was found in the relative cortical area (CA/TA) among the four elements, while the polar moment of area J (Length‐standardized) revealed a higher resistance to torsional load in the humerus than in the other bones. Our results would seem to indicate that griffon wing bones are structured as an adaptation, represented by two segments that respond to force in two ways: the proximal segment is specially adapted to resist torsional loads, whereas the distal one is adapted to resist bending loads.
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The epiblast is a single cell-layered epithelium which generates through gastrulation all tissues in an amniote embryo proper. Specification of the epiblast as a cell lineage in early development is coupled with that of the trophoblast and hypoblast, two lineages dedicated to forming extramebryonic tissues. The complex relationship between molecular specification and morphogenetic segregation of these three lineages is not well understood. In this review I will compare the ontogeny of epithelial epiblast in different amniote groups and emphasize the diversity in cell biological mechanisms employed by each group to reach this conserved epithelial structure as the pre-requisite for gastrulation. The limitations of associating cell fate with cell shape and position will also be discussed. In most amniote groups, bi-potential precursors for the epiblast and hypoblast, similar to the inner cell mass in the eutherian mammals, are not associated with an apolar, inside location in the blastocyst. Conversely, a blastocyst cell with epithelial morphology and superficial location is not indicative of its trophoblast fate. The polar trophoblast is absent in all amniotes except for the eutherian mammals. In the avian, reptilian and eutherian groups, epithelialization of the epiblast occurs after its fate specification and involves a mesenchymal-to-epithelial transition (MET) process, whereas in the monotremes and marsupials, pre-epiblast cells adopt an epithelial morphology prior to their commitment to the epiblast fate. The conservation of an epithelialized epiblast is viewed as an adaptation to evolutionary constraints placed on pre-gastrulation ectoderm in the ancestral amniote. The relationship between epiblast MET and epiblast pluripontency will also be discussed. Whether such an MET/epithelialization process is advantageous for the self-renewal and/or differentiation of human epiblast stem cells in vitro is unclear.
... As a successful group with 10 000 living species, birds occupy a unique position among the amniotes. Modern birds evolved from theropod dinosaurs (Chiappe 2004), and molecular phylogeny studies revealed that their closest living relatives are the crocodiles (Chiari et al. 2012). Birds therefore should be considered as representing the reptiles when compared to mammals. ...
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The primitive streak is where the mesoderm and definitive endoderm precursor cells ingress from the epiblast during gastrulation. It is often described as an embryological feature common to all amniotes. But such a feature has not been associated with gastrulation in any reptilian species. A parsimonious model would be that the primitive streak evolved independently in the avian and mammalian lineages. Looking beyond the primitive streak, can one find shared features of mesoderm and endoderm formation during amniote gastrulation? Here, we survey the literature on reptilian gastrulation and provide new data on Brachyury RNA and laminin protein expression in gastrula-stage turtle (Pelodiscus sinensis) embryos. We propose a model to reconcile the primitive streak-associated gastrulation in birds and the blastopore-associated gastrulation in extant reptiles.
... CARPAL DEVELOPMENT: Ostrom's (1969) seminal study of the Early Cretaceous theropod Deinonychus antirrhopus recognized a large distal carpal (misinterpreted in his study as a proximal carpal, the radiale) of semicircular aspect as a fundamental element of the dromaeosaurid wrist. In subsequent studies, Ostrom (1973Ostrom ( , 1975Ostrom ( , 1976 proposed the homology between this ''semilunate'' carpal and a similar element of the wrist of Archaeopteryx (Wellnhofer, 1974;Wellnhofer and Rö per, 2005), a hypothesis that has been frequently highlighted by studies favoring the origin of birds from manirapto-ran theropod dinosaurs (e.g., Gauthier, 1986;Witmer, 1991;Padian and Chiappe, 1998;Chiappe, 2004Chiappe, , 2007Weishampel et al., 2004). Although acknowledging the striking similarity between the semilunate carpal of Deinonychus and Archaeopteryx ( fig. ...
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Mesozoic remains of embryonic and early juvenile birds are rare. To date, a handful of in ovo embryos and early juveniles of enantiornithines from the Early Cretaceous of China and Spain and the Late Cretaceous of Mongolia and Argentina have comprised the entire published record of perinatal ontogenetic stages of Mesozoic birds. We report on the skeletal morphology of three nearly complete early juvenile avians from the renowned Early Cretaceous Yixian Formation of Liaoning Province in northeastern China. Evidence of the immaturity of these specimens is expressed in the intense grooving and pitting of the periosteal surfaces, the disproportionately small size of the sterna, and the relative size of the skull and orbits. Size notwithstanding, anatomical differences between these three specimens are minimal, leaving no basis for discriminating them into separate taxa. Numerous osteological synapomorphies indicate that they are euenantiornithine birds, the most diverse clade of Enantiornithes, but their identification as members of a particular euenantiornithine taxon remains unclear. Their early ontogenetic stage, however, provides important information about the postnatal development of this specious clade of Cretaceous birds. The presence of pennaceous wing feathers suggests that fledging occurred very early in ontogeny, thus supporting a precocial or highly precocial strategy for enantiornithine hatchlings. The morphology of these new early-stage juveniles is also significant in that they allow a better understanding of the homologies of several avian compound bones because the components of these skeletal compounds are preserved prior to their coossification. The general morphology of the wrist and ankle of these juveniles highlights once again the striking similarity between nonavian theropods and early birds.
... Since Ostrom's pioneering studies (1973Ostrom's pioneering studies ( , 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, 2001Chiappe, , 2004Holtz, 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;Clark et al., 2002). ...
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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.
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En este libro de biología y diversidad animal, dedicado especialmente a la temática de la reconstrucción filogenética, se desarrollan los temas de “Introducción a la clasificación biológica”, “El carácter en la sistemática filogenética”, “Interpretación de diferentes expresiones de un carácter”, “Caracteres homólogos y análogos (homologías vs homoplasias)”, “Series de transformación evolutivas” y “Construcción e interpretación de Cladogramas”. Además, se presentan numerosos ejemplos y variadas actividades específicas de interpretación y reelaboración. Las autoras están convencidas de la gran importancia que tiene la transferencia de la actividad de investigación a la docencia de grado, por lo que estas las actividades de aprendizaje propuestas cumplen un rol trascendente en la formación profesional de los estudiantes de las carreras de grado de Licenciatura en Ciencias Biológicas, Biología y otras carreras afines. Para la resolución de estas, en el libro se incluye la guía para responder a consignas académicas “Las respuestas a consignas de escritura académica”, extraída y modificada de Ana Atorresi.
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This first attempt to summarize knowledge on the eggshell structure in amniotic vertebrates, and in particular, the global diversity of the fossil remains, is based on original observations, and employs advanced microscopic techniques. The nomenclature, terminology, nature of eggshell biocrystalline matter and regularities of biomineralization are discussed in detail. Various classifications, based on different levels of eggshell matter organization (ultrastructure, microstructure and general morphology), are also considered. It is argued that basic (ultrastructural) types, microstructural morphotypes, types of pore system and types of surface ornamentation should be employed as the main structural categories in systematic description. A systematic section includes descriptions of all main fossil egg groups. Fourteen parafamilies and 32 paragenera of dinosaur and Cretaceous avian egg remains are considered, and a comparative review is provided for all the material (18 paragenera and 42 paraspecies) known from Asia. A full listing of known fossil egg parataxa is given in an appendix.
A spectacular pair of Sinosauropteryx skeletons from Jurassic-Cretaceous strata of Liaoning in northeastern China attracted worldwide notoriety in 1996 as the first dinosaurs covered with feather-like structures. Sinosauropteryx prima is important not only because of its integument, but also because it is a basal coelurosaur and represents an important stage in theropod evolution that is poorly understood. Coelurosauria, which includes (but is not limited to) dromaeosaurids, ornithomimosaurs, oviraptorosaurs, troodontids, and tyrannosaurids, formed the most important radiation of Cretaceous carnivorous dinosaurs in the Northern Hemisphere. It also includes Aves. Sinosauropteryx prima has a number of characters that were poorly preserved in known specimens of the closely related Compsognathus longipes from Europe. These include the longest tail known for any theropod and a three-fingered hand dominated by the first digit, which is longer and thicker than either of the bones of the forearm. Both specimens have a thick coat of feather-like structures, which seem to be simple branching structures. The claim that one skeleton of Sinosauropteryx has preserved the shape of the liver is unsupportable, if only because the fossil had collapsed into a single plane, which would have distorted any soft, internal organs.
Birds evolved from and are phylogenetically recognized as members of the theropod dinosaurs; their first known member is the Late Jurassic Archaeopteryx, now represented by seven skeletons and a feather, and their closest known non-avian relatives are the dromaeosaurid theropods such as Deinonychus. Bird flight is widely thought to have evolved from the trees down, but Archaeopteryx and its outgroups show no obvious arboreal or tree-climbing characters, and its wing planform and wing loading do not resemble those of gliders. The ancestors of birds were bipedal, terrestrial, agile, cursorial and carnivorous or omnivorous. Apart from a perching foot and some skeletal fusions, a great many characters that are usually considered ‘avian’ (e.g. the furcula, the elongated forearm, the laterally flexing wrist and apparently feathers) evolved in non-avian theropods for reasons unrelated to birds or to flight. Soon after Archaeopteryx, avian features such as the pygostyle, fusion of the carpometacarpus, and elongated curved pedal claws with a reversed, fully descended and opposable hallux, indicate improved flying ability and arboreal habits. In the further evolution of birds, characters related to the flight apparatus phylogenetically preceded those related to the rest of the skeleton and skull. Mesozoic birds are more diverse and numerous than thought previously and the most diverse known group of Cretaceous birds, the Enantiornithes, was not even recognized until 1981. The vast majority of Mesozoic bird groups have no Tertiary records: Enantiornithes, Hesperornithiformes, Ichthyornithiformes and several other lineages disappeared by the end of the Cretaceous. By that time, a few Linnean ‘Orders’ of extant birds had appeared, but none of these taxa belongs to extant ‘families’, and it is not until the Paleocene or (in most cases) the Eocene that the majority of extant bird ‘Orders’ are known in the fossil record. There is no evidence for a major or mass extinction of birds at the end of the Cretaceous, nor for a sudden ‘bottleneck’ in diversity that fostered the early Tertiary origination of living bird ‘Orders’.