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Home , Bird, Deinonychus, Eshanosaurus, Evolution of birds, Fin, Maniraptora

ORNITOLOGIA NEOTROPICAL 15 (Suppl.): 101–116, 2004 © The Neotropical Ornithological Society

THE CLOSEST RELATIVES OF

Luis M. Chiappe

Department of , Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, CA 90007, USA. Email: [email protected]

Resúmen. – Los ancestros más cercanos de las aves. – origen de las aves, el clado originado a partir del ancestro común de 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 . 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 , the originating from the common ancestor of the Late Archaeopteryx and extant birds, has been at the center of a heated debate throughout the history of evolu- tionary . Although many disparate hypotheses of origins have been proposed in the last two centuries, an overwhelming consensus exists in support of the idea that birds evolved from maniraptoran theropod . 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 morphology and integumentary but also includes behavioral inferences based on a handful of rare . These discoveries have documented the presence of , brooding behavior, autochronous ovideposition, and other avian attributes among 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 ) first evolved among maniraptoran dinosaurs. Although dissenters of the Maniraptoran hypothesis of bird ori-

101 CHIAPPE 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 of the digits of the avian , 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, , , Maniraptora.

INTRODUCTION closest relatives of birds have occasionally resurfaced in the recent literature but Birds diversified more than 150 million these have been used more as default ago. Their oldest known records are still from hypotheses than as real alternatives to the of southern , where the theropod origin of birds. Indeed, a Archaeopteryx was first discovered in the mid- close examination of these “alternative” 19th century. Identifying the closest relatives hypotheses reveals a lack of empirical support to the group’s ancestor (the most recent because character evidence in support common ancestor of Archaeopteryx and of these hypotheses has also been discovered modern birds) has been a matter of scientific among theropod dinosaurs. Furthermore, debate and scrutiny throughout the history these “alternative” hypotheses have continued of . As early as the to be framed outside modern systematic 18th century, birds were placed immediately methods (i.e., ), and thus also ahead of flying in the ‘chain of being’ lack the rigor of current phylogenetic postulated by the naturalists of that hypotheses. time. With the advent of evolutionary Today, the debate on bird ancestry has thinking, especially after Darwin’s theory been resolved. The uncertainties that led to of evolution by , more this long controversy, both empirical and explicit hypotheses of relationships were methodological, have been clarified. The clos- formulated. Indeed, in post-Darwinian est relatives of birds can be found among times, birds were considered to be most theropod dinosaurs, the carnivorous preda- closely related to a variety of extinct tors that ruled the ecosystems. The and extant lineages of , including history of this fascinating scientific debate has , , crocodylomorphs (modern been summarized in a number of recent and its relatives), a reviews, among them those of Witmer (1991, diversity of basal and archosauro- 2002), Padian & Chiappe (1998), Chiappe morphs (e.g., the Triassic , (2001), and Prum (2002). A discussion in , and ), Spanish can also be found in Chiappe & Var- (pterodactyls and their kin) as well as thero- gas (2003). In this paper, addressed to the pod and ornithischian dinosaurs (Fig. 1). ornithological community, I hope to convey Today, however, although most of these the message that the scientific hypothesis of hypothetical relationships have been aban- their diverse disciplines, from ecology to doned, the theropod hypothesis is receiving behavior to , will greatly benefit nearly universal acceptance. Hypotheses from incorporating the notion that modern identifying crocodylomorphs, basal archo- birds are highly specialized, short-tailed, and saurs, or basal archosauromorphs as the flighted theropod dinosaurs.

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FIG. 1. illustrating the diversity of hypotheses of (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).

HISTORY OF THE THEROPOD publication of Darwin’s “Origin of ”. HYPOTHESIS OF BIRD ORIGINS Similarities in the structure of the tarsus led Gegenbaur (1864) to place the small, Late The first suggestion that birds could have Jurassic theropod in an interme- been related to dinosaurs came soon after the diate position between birds and other rep-

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FIG. 2. Some osteological synapomorphies in support of the maniraptoran origin of birds. Modified from Chiappe & Vargas (2003). tiles. At about the same time, Cope (1867) between theropods and birds. Despite these compared the tarsus of the Jurassic theropod initial considerations, it was Huxley (1868, to that of an and, on the 1869) who championed the 19th century dis- basis of this and on similarities in the elonga- cussions of the origin of birds from theropod tion of the neck vertebrae and the lightness of dinosaurs. In 1869, Huxley argued that “if the the , he argued for a close relationship whole hind quarters, from the to the

104 CLOSEST RELATIVES OF BIRDS , of a half-hatched could be sud- theropod dinosaurs (Chiappe 2001). The denly enlarged, ossified, and fossilized as they most visible evidence of this hypothesis is are, they would furnish us with the last step of based on comparisons of the osteology, the transition between Birds and Reptiles; for behavior, , and integument of birds there would be nothing in their characters to with that of a variety of nonavian theropods. prevent us referring them to the Dinosauria.” These lines of evidence are summarized (Huxley 1869). During the second half of the below. 19th century, the theropod hypothesis of bird origins was one of a pool of other hypotheses. Osteology. A multitude of derived osteological Just as today, detractors argued that the simi- characters are shared by all, or some, nona- larities between birds and theropod dinosaurs vian maniraptoran theropods and birds (Fig. could well be explained by convergence [see 2). Comparisons between these taxa are Seeley’s discussion in Huxley (1869)]. In the greatly assisted by the many newly discovered early 20th century, with the discovery of more basal birds (Padian & Chiappe 1998, Chiappe generalized, Triassic archosaurs, in particular & Dyke 2002), which possess a skeletal mor- the South African Euparkeria (Broom 1913), phology only slightly modified from the the theropod hypothesis lost ground. Thero- ancestral maniraptoran condition. Some of pods were deemed as too specialized to be the these derived characters are the presence of ancestors of birds (Heillman 1926). Such a rostral, dorsal, and caudal tympanic recesses notion dominated the field for several decades (air spaces connected to the region), ven- (see Romer 1966) until the early 1970s, when tral processes on cervicothoracic vertebrae, renewed interest on the origin of birds took ossified ventral segments of thoracic ribs, place (see Witmer 1991). Among this new that are more than half the length wave of interest was Ostrom’s work on of hindlimbs, a semilunate carpal allow- Archaeopteryx (Ostrom 1973, 1976), who revi- ing swivel-like movements of the wrist, clavi- talized Huxley’s hypothesis of the theropod cles fused into a wishbone (probably a origin of birds. During the thirty years that synapomorphy of a more inclusive theropod has passed since Ostrom’s initial work on bird group), a pubic peduncle of the ilium longer origins, a large quantity of documenta- than the ischiadic peduncle (these peduncles tion supporting the dinosaurian ancestry of form the front and rear borders of the hip- the group has been accumulated. Today, socket), a vertically to caudoventrally oriented despite disagreement regarding the specific ending in a boot-like expansion that theropod clade phylogenetically closest to projects only caudally, an two-thirds birds (e.g., dromaeosaurids, troodontids, ovi- or less the length of the pubis, a with a raptorids), an overwhelming consensus exists feeble fourth trochanter (the attachment of in support to the notion that birds evolved the caudofemoralis longus muscle), and many from maniraptoran theropods (Chiappe & other characters distributed over the entire Dyke 2002). skeleton (Novas & Puerta 1997, Holtz 1998, Sereno 1999, Clark et al. 2002). Birds also EVIDENCE FOR THE MANIRAPT- share a number of derived characters with ORAN ORIGIN OF BIRDS more inclusive theropod such as the , , and , Several lines of evidence converge in support and evolutionary trends towards the modern of the hypothesis that the closest relatives of avian condition can be seen when these are birds are to be found among maniraptoran examined across of theropods

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FIG. 3. A partial skeleton of the oviraptorid from the Late of the Gobi Desert brood- ing a of its own (A) and an interpretation of the posture of this when in (B). Modi- fied from Clark et al. (1999).

(e.g., elongation, pubic rotation, Behavior. Evidence of the behavior of extinct braincase amplification, stiffening of the ). organisms is rarely preserved in the fossil Indeed, many osteological features previ- record. A handful of extraordinary discover- ously thought to be exclusively avian, such as ies, however, have shed light on the nesting a , laterally facing glenoids, large bony conduct of certain nonavian maniraptorans. , uncinate processes on ribs, have now Several skeletons of ovirap- been discovered among nonavian manirap- torids from the Gobi Desert, belonging to torans (Padian & Chiappe 1998). both (Osborn 1924) and Citipati

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FIG. 4. Some oological synapomorphies in support of the maniraptoran origin of birds. Note the pres- ence of two or more layers in the of oviraptorids, troodontids, and birds, and the asymmetric shape of the egg in the last two lineages. Modified from Chiappe & Vargas (2003).

(Clark et al. 2001), have been discovered on phology to those in these clutches strongly top of their clutches of eggs (Fig. 3). The supports the idea that these specimens were specimens of Citipati show that the brooding their own (Clark et al. 1999). adopted a posture similar to those of brood- These discoveries have forced the reinterpre- ing birds, with their legs tucked inside an open tation of inferences made decades ago on the space at the center of the clutch and their basis of the holotype of Oviraptor philoceratops forelimbs surrounding the periphery of the (Osborn 1924) which, because it had also clutch (Clark et al. 1999). An oviraptorid been found on top of a clutch of eggs, had embryo inside an egg of comparable mor- been interpreted (and consequently named) as

107 CHIAPPE an egg-predator (Norell et al. 1995). A similar In birds, this external zone may grade into, or discovery of a Late Cretaceous troodontid be completely separated from, a third, outer- skeleton from in an identical brood- most zone and, in paleognaths, even a fourth ing position suggests that, regardless of its zone can be recognized (Grellet-Tinner specific function (e.g., protection, incubation), 2000). Even though up to now only two lay- the typical avian nesting behavior (i.e., adults ers have been found in the eggshell of non- sitting on top of their ) was widespread avian theropods, no other group of nonavian among nonavian maniraptorans. reptiles possesses a similar zonation. Addi- tional character states shared by the eggs of Oology. The general morphology and micro- nonavian maniraptorans and those of birds structure of calcified eggs is specific to certain include a reduction in the porosity of the groups of extant and extinct reptiles shell, a relative increase in the volume of the (Mikhailov 1997, Grellet-Tinner 2000). Until egg (with respect to the size of the adult), and recently, the precise characteristics of the egg- the presence of a longer axis (eggs that are shell microstructure of nonavian theropods elongated) (Zelenitzky et al. 2002). Another remained elusive due to the absence of diag- oological feature easily recognizable is the nostic embryonic material. The discovery of presence of asymmetrical eggs, those in which the Gobi oviraptorid embryo provided the one pole is narrower than the other. While first definitive evidence of a nonavian thero- turtles, crocodiles, and nearly all non-avian pod egg (Clark et al. 1999). Since then, other dinosaurs are characterized for having sym- nonavian maniraptorans embryos have been metrical eggs, the eggs of birds and those of found. These include other species of ovirap- troodontid maniraptoran theropods have one torids (Weishampel et al. 2000), therizinosau- pole that is narrower than the other. Further rids (Manning et al. 2000), and troodontids similarities between nonavian maniraptorans (Varricchio et al. 2002). Comparative studies and birds involve the mode of ovideposition. between the eggshell microstructure of these Unlike in the clutches of other dinosaurs eggs and those of extant birds have revealed where eggs have no spatial arrangement, in features exclusively common to them (Fig. 4) theropod clutches, the eggs are clearly (Mikhailov 1992, Varricchio et al. 1997, Zelen- arranged in pairs. Such a pairing is suggestive itzky et al. 2002, Grellet-Tinner & Chiappe of autochronous ovideposition, a mode of 2004). One of these features involves the deposition in which eggs are not laid en masse presence of more than one distinct micro- but sequentially, at discrete time intervals. The structural layer, most commonly distin- pairing of eggs found in fossil egg-clutches guished by the differential disposition of the attributed to theropod dinosaurs thus sug- calcitic crystals (Grellet-Tinner & Chiappe gests that it could have taken several days for 2004). The dinosaurian eggshell is character- a theropod to lay its egg-clutch ized by the presence of shell units, of which (Varricchio et al. 1997, Grellet-Tinner & Chi- the inner portion is formed by a crystalline appe 2004), a condition shared with birds. structure that radiates from a core, often termed the organic core. In nonavian thero- Integument. Feathers have always been the pods, these units also possess an external quintessential bird feature. In recent times, zone with a more spongeus microstructural however, feathers have been found in a vari- appearance, although in thin sections this ety of maniraptoran theropods, whose skele- layer exhibits a more laminar appearance (this tons are found in a series of layer is often referred as the squamatic zone). lacustrine deposits in the northeastern corner

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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 . 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 . B represents filamentous feathers surrounding the tail of the dromaeosaurid . Modified from Chiappe & Dyke (2002). of (Fig. 5). Carbonized remains of osaur Caudipteryx (Ji et al. 1998, Zhou & Wang feathers are now known for the therizinosau- 2000), the dromaeosaurids Sinornithosaurus rid (Xu et al. 1999), the oviraptor- (Xu et al. 1999) and (Xu et al. 2000

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2003), and the long-armed (Ji presence of more derived, pennaceous feath- et al. 1998), which phylogenetic placement ers is interpreted as synapomorphic of among maniraptorans is less well-known. Maniraptora. These discoveries not only doc- Integumentary structures interpreted as feath- ument the presence of feathers outside birds ers have also been found in more primitive but also, suggest that some nonavian thero- theropods such as the basal coelurosaurian pod dinosaurs (e.g., Microraptor gui) may have (Chen et al. 1998, Currie & been able to . Chen 2001), also from the same Early Creta- ceous rocks of China. While the latter exhibits CRITICISMS OF THE MANIRAPT- feathers that are filament-like, with a minimal ORAN HYPOTHESIS OF BIRD degree of branching, Caudipteryx, Protarchaeop- ORIGINS teryx, Sinosauropteryx, and Microraptor display pennaceous feathers with distinct shafts and The evidence summarized above is so com- vanes. Down-like feathers also cover portions pelling that the idea that birds are the descen- of the skeletons of all these taxa. A - dants of a maniraptoran ancestor has been shaped cluster of pennaceous feathers is accepted by a great number of evolutionary attached to the distal part of the tail of Caudip- . Nonetheless, the maniraptoran teryx (Fig. 5). Frond-like similar to those hypothesis of bird origins is not exempt of in Archaeopteryx are present in the dromaeo- critics, even though it is fair to say that these saurids Sinosauropteryx and Microraptor, represent only a tiny fraction of specialists. although these pennaceous feathers are more Concerns have been expressed primarily restricted to the distal half of the tail. Long highlighting apparent inconsistencies within pennaceous feathers are also attached to the the known fossil record and with the inferred tip of the forelimbs of Caudipteryx (Ji et al. homology of certain structures. These appar- 1998) (Fig. 5) while in the tiny Microraptor gui, ent inconsistencies are briefly discussed they form a of essentially modern design below. (Xu et al. 2003). There is also the remarkable presence in the latter of pennaceous INCONSISTENCIES WITHIN THE feathers attached to the distal half of the KNOWN FOSSIL RECORD hindlimb. Such an attribute has been used to argue that Microraptor gui was able to glide This criticism highlights the chronological using these hindlimb feathers as an additional gap between the oldest known bird, the Late airfoil (Xu et al. 2003). Despite functional Jurassic Archaeopteryx, and the Cretaceous considerations that make this idea untenable nonavian maniraptorans that are typically (Chiappe & Vargas 2003), there is little doubt used in discussions of bird origins (e.g., that with such a small , Microrap- , , Oviraptor). This argu- tor gui was able to fly [see Padian & Chiappe ment has become known as the “temporal (1998) for a recent discussion on the origin of paradox” since it highlights the inconsistency flight]. The presence of feathers in so many of arguing that birds evolved from creatures coelurosaurian taxa suggests that these integ- that lived several million years after their own umentary appendages evolved in the com- origin (Feduccia 1996, 1999). However, exam- mon ancestor of the group if not earlier. ination of the theoretical basis and supporting Given the evidence at hand, the presence of evidence of the “temporal paradox” indicates simple, filament-like feathers is considered as that this argument stems from philosophical a synapomorphy of Coelurosauria while the misconceptions, disregards critical fossil evi-

110 CLOSEST RELATIVES OF BIRDS dence, and it constitutes an artifact caused by age (Clark et al. 2002). not considering all alternative hypotheses of Finally, the “temporal paradox” appears to bird origins at the same time (Brochu & exist only if one considers the temporal gap Norell 2000). between the 100-million- old Deinonychus, In the first place, the “temporal paradox” to take an example of a well-known dromaeo- stems from a philosophical misconception saurid, and the 150-million-year old Archaeop- because none of these Cretaceous dinosaurs is teryx. Yet, as shown by the statistical test of regarded as the direct ancestor of birds Brochu & Norell (2000), when other records (Padian Chiappe 1998, Witmer 2002). In of well-known maniraptorans are included modern times, the hypothesis of a manirapto- (e.g., the 125-million-year old dromaeosaurids ran ancestry of birds has been framed as a cla- Sinornithosaurus and Microraptor) and when distic hypothesis that postulates the existence hypotheses of bird origins are compared of a most recent common ancestor of these against each other, placing birds within Cretaceous dinosaurs and Archaeopteryx that groups indicated by hypotheses (e.g., crocody- obviously existed before the divergence of the lomorphs or more basally within archosaurs; oldest of these taxa, Archaeopteryx (e.g., Gau- see Fig. 1) other than the theropod hypothesis thier 1986, Forster et al. 1998, Holtz 1998, Se- may increase the temporal disparity by as reno 1999, Norell et al. 2001, Clark et al. 2002). much as 15%. Thus, when the “temporal par- Thus, in contrast to what has been claimed by adox” is considered in the context of current the proponents of the “temporal paradox”, alternative hypotheses of bird origins (Fig. 1), the maniraptoran hypothesis does set the ori- the maniraptoran hypothesis is temporally the gin of birds in pre-Jurassic times. most consistent (Brochu & Norell 2000). In addition, the absence of the pre-Creta- ceous maniraptorans the “temporal paradox” INCONSISTENCIES WITH THE seems to highlight has long been proved to be INFERRED HOMOLOGY OF SOME mistaken. Late Jurassic maniraptorans have STRUCTURES been known for decades, even if from frag- mentary remains (Padian & Jensen 1980), and of the avian hand. Opponents to the a lower jaw of a maniraptoran therizinosaurid, maniraptoran origin of birds (e.g., Feduccia deguchiianus, has been discovered 1999, 2003) have highlighted the conflict in the of China (Xu et al. 2001). between the correspondence of the three This and the fact that the stratigraphic ranges wing digits of birds with respect to the ances- of theropod groups containing the clade tral pentadactyl hand of , as indi- Maniraptora have been recently extended cated by embryological studies, and that back by many millions of years [e.g., basal tet- inferred from the palaeontological evidence. anurans are now known from the Late Trias- Embryological investigations of extant birds sic; Arcucci & Coria (2003)], suggest that the have identified five precartilaginous conden- divergence of maniraptorans occurred much sations of which only those in positions II, earlier than in the Late Jurassic. The fact that III, and IV develop into the three osseous maniraptoran fossils are exceedingly rare in digits of the adult hand (Feduccia & Nowicki pre-Cretaceous times may be related to a clear 2002, Larsson & Wagner 2002). This observa- bias against small-sized dinosaurs of Jurassic tion has often been extrapolated to include all age (most maniraptorans are of relatively birds, even the Late Jurassic Archaeopteryx, and small size) and the much smaller volume of the three fingers of the avian hand have been Jurassic outcrops than those of Cretaceous identified as homologous to digits II–IV of

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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 . 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). the ancestral pentadactyl hand (Burke & these digits are abbreviated but still present, Feduccia 1997, Feduccia 1999, Feduccia & to tetanuran theropods bearing a tridactyl Nowicki 2002). In contrast, inferences based hand (Padian & Chiappe 1998). The three on the transformation of the hand as digits of the latter theropods have the same observed from fossils representing different phalangeal formula as digits I, II, and III of stages of dinosaur evolution have identified the primitive five-fingered theropods, thus the homology of the three fingers of Archaeop- indicating that the three fingers of tetanurans teryx as those corresponding to digits I, II, (a group that also includes Maniraptora) cor- and III of the ancestral pentadactyl hand. respond to digits I–III of the ancestral penta- This paleontological evidence shows a trend dactyl hand. The remarkable similarity in of reduction of the outermost two digits (VI morphology, proportions, and phalangeal for- and V) from the most basal theropods, where mula of the manual digits of certain nonavian

112 CLOSEST RELATIVES OF BIRDS maniraptorans (e.g., Velociraptor, Deinonychus) theropod relatives can be explained without to those of Archaeopteryx has extended this resorting to a different phylogenetic hypothe- conclusion to this and to other basal birds. sis. Wagner & Gauthier (1999) have argued Two different issues are involved in this that homeotic frame shifts could have led to a controversy. On the one hand is the question developmental pattern in which digits that of whether there is empirical basis for extrap- previously ossified from condensations I–III olating the ontogenetic development of mod- became ossified from condensations II–IV. ern birds to Archaeopteryx. On the other hand Homeotic frame shifts are relatively common is whether the maniraptoran ancestry of birds among other vertebrate lineages. An illustra- can be sustained even if nonavian theropods tive example involves the development of the developed their manual digits through a devel- hand of the two-toed earless skink (Hemiergis opmental pathway different than that of mod- quadrilineata), an Australian scincid (Sha- ern avians. The extrapolation of the piro 2002) (Fig. 6). Many studies have docu- embryogenesis of the hand of extant birds to mented the fact that ontogenetic trajectories archaic avian lineages including Archaeopteryx do evolve and that these transformations appears unwarranted given that the hand of could occur without affecting either the mor- modern birds is highly transformed and that phology or function of the developing struc- embryological evidence is unavailable for ture (Wagner & Misof 1993, Mabee 2000, Hall either Archaeopteryx or any other basal avian 2003). These structures are homologous, even lineage. Indeed, the fact that the hand of if their development pathways are different. Archaeopteryx is remarkably similar to that of nonavian maniraptorans such as dromaeosau- structure and ventilation. Interpretations of rids (Ostrom 1976) suggests that if any devel- soft structures supposed to indicate visceral opmental trajectory is to be extrapolated to compartmentalization in the early Cretaceous this Late Jurassic bird, it should be the one basal coelurosaurian theropod Sinosauropteryx inferred for dromaeosaurid theropods. The prima (Chen et al. 1998) played a paramount second issue, namely whether embryogenetic role in Ruben et al.’s (1997) claim that nona- differences should take precedence over the vian theropods had a -like, hepatic- enormous volume of evidence supporting the piston mechanism for lung ventilation. Ruben phylogenetic relationship between birds and et al. (1997) questioned the close relationship certain lineages of nonavian maniraptorans, is between birds and nonavian theropods on the also problematic. Certainly, such an approach basis of this interpretation, because according would be in direct conflict with the parsimony to these authors, the transition from the croc- methods endorsed by modern systematic odile-like pulmonary system to the flow- techniques. If the maniraptoran origin of through lung system of birds would have birds is to be rejected because the digits of the required the evolution of a diaphragmatic her- hand of living birds have ontogenetic trajecto- nia in the alleged partition that would have ries different from those inferred for extinct compromised the efficiency of the pulmonary maniraptorans, the unquestionable similari- system of the transitional forms. ties in the osteology, , oology, and As in the case of other critics to the thero- behavior of all these organisms would have to pod hypothesis of bird origins, this argument be explained in the context of evolutionary is based on problematic interpretations. convergence. Nonetheless, the apparent Detailed studies of the skeleton of the speci- incongruence between the manual osteogene- men of Sinosauropteryx prima used by Ruben et sis of modern birds and that of their nonavian al. (1997) have demonstrated that the struc-

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