387390a0Nature3876631199705223903920028-0836199710.1038/387390a01476-4679199723 December 199627 February 199722 May 1997ukNatureNatureNATUREnatureNature is a weekly international journal publishing the finest peer-reviewed research in all fields of science and technology on the basis of its originality, importance, interdisciplinary interest, timeliness, accessibility, elegance and surprising conclusions. Nature also provides rapid, authoritative, insightful and arresting news and interpretation of topical and coming trends affecting science, scientists and the wider public./nature/journal/v387/n6631issueJournal homeArchiveCurrent issueAdvance online publicationPrivacy policySubscribeNature Publishing GroupSupplementsCurrent issue387390a0New evidence concerning avian origins from the Late Cretaceous of Patagonia
AU  - Novas, Fernando E.
AU  - Puertat, Pablo F.[ast] Museo Argentina de Ciencias Naturales Bernardino Rivadavia, Av. Angel Gallardo 470, Buenos Aires (1405), Argentina[dagger] Museo Paleontologico Egidio Feruglio, Av. 9 de Julio 655, (9100) Trelew, ArgentinaThe spate of recent discoveries of Mesozoic birds has substantially improved our understanding of the early evolution of birds and flight1-5, but has failed to close the morphological gap between the Upper Jurassic Archaeopteryx lithographica, the earliest known bird, and the Dromaeosauridae, the group of non-avian theropod dinosaurs regarded as most closely related to birds6,7. Here we describe a theropod dinosaur from Patagonia, Unenlagia comahuensis gen. et sp. nov., which partially fills this gap. Despite the relatively late appearance of this dinosaur in the fossil record (Upper Cretaceous),  several features of Unenlagia are more bird-like than in any other non-avian theropod so far discovered.Unenlagia resembles Archaeopteryx in the morphology of the scapula, pelvis and hindlimb. But several shared, primitive features of the pubis, ischium and hindlimb proportions suggest that Unenlagia may represent the sister taxon of the Avialae (=Aves). The structure of the forelimb suggests that the avian mode of forelimb folding, and the extensive forelimb elevation necessary for powered, flapping flight, was already present in cursorial, non-flying theropod dinosaurs.Theropoda Coelurosauria7 Maniraptora7


Unenlagia comahuensis gen. et sp. nov.


Etymology. Unenlagia, Latinized from "unen" and "lag", Mapuche Indian  names  respectively  meaning  "half"   and   "bird"8;   and comahuensis,   from   Comahue,   a  Mapuche  name   referring  to North-West Patagonia. Holotype. (See Fig. 1).


Locality and horizon. Upper Cretaceous (Turonian-Coniacian9), Rio Neuquen Formation, Sierra del Portezuelo, Neuquen Province, Argentina. This formation has yielded remains of the basal bird Patagonykus puertai10'11, plus a variety of non-avian theropods12. Diagnosis. Possesses tall neural spines in posterior dorsals and anterior sacral vertebrae, being nearly twice the height of the centrum; deep lateral pits in the base of the neural spines of these vertebrae; twisted scapular shaft; inflected dorsal margin of post-acetabular iliac blade (Fig. 2).


Unenlagia is a medium-sized maniraptoran dinosaur, nearly 2 m long. Presacral vertebrae are amphiplatyan and have pleurocoels. Six fused sacrals are present, although the ilia extend the length of at least nine vertebrae (that is, six sacrals, two dorsals, and one caudal), instead of seven as in Deinonychus (Museum of Comparative Zoology, MCZ 4871) and Archaeopteryx13'14. Proximal haemal arches are craniocaudally short and dorsoventrally long (Fig. 1), resembling those of the dromaeosaurid Velociraptor15'.


The scapula (Fig. 2a, b) is strap-like in dorsal aspect and curved in lateral view, closely resembling that of Archaeopteryx6'16. As in the latter, the acromion is triangular in lateral aspect, and projected sharply cranioventrally. In contrast to the situation in non-avialan theropods (for example, Deinonychus16'17), the humeral articulation of the scapula of Unenlagia is laterally oriented as in birds6'16'18.


The humerus, estimated to be 27 cm long, is 71% of the femoral length, and is proportionally shorter than in Archaeopteryx13'14. As in other Maniraptora7, the internal tuberosity (bicipital crest of modern birds19) is proximodistally extended.


The pelvic bones are not fused (Fig. 2c). The ilium is extensive cranially, but the postacetabular blade is short. The latter is low and sharp as in Archaeopteryx and enantiornithines14'20. The fossa for the m. cuppedicus is well developed, a condition that is widely present among Coelurosauria, including basal birds10'17'18. In contrast to non-avialan coelurosaurs (that is, Deinoncyhus17'21), the acetabulum of Unenlagia tends to close off medially, resembling Archaeopteryx18, Patagopteryx22 and hesperornithiforms23'24. The brevis fossa is considerably more reduced than in Deinonychus10. The pubis is slightly shorter than the femur, is oriented ventrally as in other maniraptorans10'14, and distally bears a caudally projected 'foot'. The pubic shaft expands transversally into a 'pubic apron' (Fig. 2d) that is widely extended proximodistally as in Deinonychus (MCZ 4371), but in contrast with the more reduced symphysis of Archaeopteryx and more derived birds6'11. The ischium is a short, plate-like bone, triangular in side view. The obturator notch is enclosed distally by a triangular obturator process, a primitive condition lost in Archaeopteryx6'14 and more derived birds11'22. However, the dorsal edge of the ischium exhibits a prominent proximodorsal process (Fig. 2c), separated from the ischiadic antitrochanter by a deep notch. This character, which is absent in Dromaeosauridae and the remaining non-avialan theropods, is similar to that present in Archaeopteryx13'14'18.


Figure 1 Skeletal reconstruction of Unenlagia comahuensis, gen. et sp. nov, based on holotype specimen (MCF PVPH 78; Museo Carmen Funes, Plaza Huincul, Argentina). The specimen was found preserved in partial articulation, with the bones occupying their respective anatomical position. MCF PVPH 78 includes: three presacral vertebrae (presumably correspond to 8th, 10th, and 13th dorsals, the latter articulating to the sacrum), sacrum, dorsal ribs and two proximal haemal arches, left scapula and incomplete humerus, ilia, pubes, and right ischium, right femur and left tibia.


Figure 2 Unenlagia comahuensis, gen. et sp. nov. a, b, Left scapula in dorsal (a) and lateral (b) views, c, Pelvis in right lateral view, d, Pubes in anterior view, e, Dorsal 13th in left lateral aspect. Orientation of the scapula shown in a and b is primarily based on the assumption that the external surface of the acromium is craniolaterally faced as in other theropods, including birds; thus, the external surface of the scapular blade orientates dorsally (that is, scapular shaft twisted), and the glenoid cavity results laterally oriented. Abbreviations: ac, acromium; asc, articular surface for the coracoid; cf, fossa for origin of m. cuppedicus; g, glenoid cavity; hf, hyposphene; Ip, lateral pit; op, obturator process; pd, proximodorsal process on ischium; pi, pleurocoel.


Figure   3   Cladogram   depicting   phylogenetic   relationships   of  Unenlagia comahuensis, gen. et sp. nov. For details, see Methods.


The femur is long and slender, with a proportionally small head. The anterior trochanter projects proximally and is separated from the greater trochanter by a short cleft, as in Archaeopteryx6. Both the fourth tronchanter and the posterior trochanter6'21 are absent. The tibia is long and slender, and is 13% longer than the femur.


Deinonychuswas described nearly 25 years ago17 and its morphology was interpreted as closely resembling that of Archaeopteryx6'7'25. No other dinosaur has been discovered until now that closes the morphological gap between these taxa. Unenlagia represents such an 'intermediate' dinosaur, because it is more closely related to birds than are dromaeosaurids (Fig. 3). In particular, Unenlagia sheds light on the morphology of 'proavian' dinosaurs, clarifying interesting aspects of forelimb function that help us to understand how avian flight emerged.


Some features characterizing the avian mode of forelimb folding were already acquired by non-avialan theropods. For example, the pulley-shaped distal carpal present in basal maniraptorans allowed the manus to be flexed against the forearms7'17'26. However, the posteroventrally oriented glenoid cavity of Deinonychus16 (Fig. 4a) constrained the range of humeral movements as much as in other non-avialan theropods, preventing it from folding in the avian manner (that is, with the flexor surface of humerus laterally oriented at rest) (Fig. 4b). In Unenlagia, instead, the glenoid cavity is laterally oriented (Fig. 4a), a derived feature previously unreported in non-avialan dinosaurs18. This orientation of the glenoid cavity indicates that their forelimbs were capable of excursions in the avian manner (that is, forelimb folding involving rotation of humerus, thus exposing its flexor surface laterally; also, increased humeral abduction allowing an almost vertical positioning of the forelimb during maximum upstroke; Fig. 4b). Interestingly, the lateral orientation of the glenoid cavity of Archaeopteryx (Fig. 4a) suggests that this basal bird was also capable of extensive wing elevation (upstroke), as well as fixing the humerus against the body when the wing was held folded. Moreover, such postural activity was critical in protecting the wing feathers.


The large size of Unenlagia, together with its proportionally short forelimbs (based on humeral length), argue that this animal was flightless, and its phylogenetic position suggests that it was not derived from a flying form (Fig. 3). Yet Unenlagia had already acquired novel, almost avian, forelimb movements, which are lacking in more remote outgroups. The extensive forelimb elevation (upstroke) present in Unenlagia constituted a prerequisite for powered, flapping flight, offering the necessary thrust to lift winged theropods from the ground. The design and function of the forelimbs of Unenlagia do not suggest that there was a gliding phase before the acquisition of the avian flight; rather, they are more consistent with the idea that there was a flapping stage26'27, which would require a much greater arc of movement. Whether Unenlagia was feathered or not is unknown. The new evidence, however, reinforces the hypothesis that a bipedal, cursorial theropod was ancestral to birds6'7, and used its arms not only in predation, but probably also in maintenance of balance and to control its body attitude while running and leaping27'28.


Figure 4 a, Lateral view of the left scapula of Unenlagia (2), compared with those oWeinonychus (1) and Archaeopteryx (3) (not to scale; modified from refs 6 and 16). In Deinonychus, maximum humeral elevation (=upstroke) was restricted by the posteroventrally oriented glenoid cavity. This is not the case for Unenlagia and avialans, in which the glenoid cavity is laterally projected, indicative of extended elevatory range of humeral movements, b, Left humerus of Unenlagia depicting its maximum elevation (1,2) and depression (3,4) in lateral (1,3) and anterior (2,4) views. Forelimb upstroke was considerably increased dorsally, allowing an almost vertical positioning of the forelimb at maximum abduction. However, the reorientation of the glenoid cavity described for Unenlagia and Archaeopteryx also implied that maximum humeral depression (=downstroke) was reached when the humerus adopted a nearly horizontal and laterally projected position (3,4). In sum, the outward facing of the glenoid cavity was accompanied by the folding of the forelimbs in a transverse plane, a feature uniquely present in Unenlagia and birds among dinosaurs. Abbreviations: ac, acromium; dc, delto-pectoral crest; g, glenoid cavity; it, internal tuberosity (=bicipital tubercle).


Remarkably, main differences between forelimb bones of Archaeopteryx and those of Unenlagia, the closest outgroup of birds, have more to do with relative proportions among bones rather than with the acquisition of structural novelties. In consequence, the development of flying capabilities can be regarded more as changes in body proportions (that is, enlarged forelimbs, reduction in body size and mass) and integument transformations (enlargement of feathers to increase wing surface) than as the acquisition of specific osteological and muscular features.


Methods


The preserved character states of Unenlagia were scored into the data matrix (appendix of ref. 11), plus the following characters: acromium triangular and anteroventrally projected; humeral facet laterally oriented; femur elongate, with reduced femoral head; ischium with proximodorsal process on posterior edge; and humerus longer than femur. The resulting 80-character data set was processed using the implicit enumeration option in Hennig 86. The single most parsimonious tree consists of 116 steps, a consistency index of 0.68, and retention index of 0.71. Maniraptoran synapomorphies present in Unenlagia are: humerus with proximodistally elongate internal tuberosity, postacetabular blade acuminate, pubis ventrally directed, ischium nearly 50% of pubic length, adductor fossa and associated anterodistal crista of distal femur reduced or absent. No derived characters uniquely shared by Unenlagia and Dromaeo-sauridae were identified. On the contrary, Unenlagia shares with Avialae the following unequivocal synapomorphies: femoral fourth trochanter absent; pubic distal foot lacking cranial projection; acromium triangular and projected ventrally; humeral facet of scapula laterally oriented; elongate femur, with reduced femoral head. Unenlagia is less derived than Archaeopteryx and the remaining avialans because it lacks the following unambiguous characters of Avialae: pubic apron strongly reduced transversely and restricted to the distal 1/3 of the pubic length; obturator process on ischium absent (that is, antero-ventral margin of ischium is almost straight); and tibia 25% longer than the femur.


Acknowledgements. We thank L. Chiappe, P. Currie, F. A. lenkins and L. Witmer for review of the manuscript. The specimen was discovered by A. Scanferla, and prepared by P. Puerta and S. Reuil. We thank C. Schaff for access to specimens housed at MCZ, Massachusetts. Figures were drawn by J. Gonzalez. Assistance in Neuquen was kindly offered by R. Coria (MCF, Plaza Huincul). This research was supported by the National Geographic Society and The Dinosaur Society.


Correspondence and request for materials should be addressed to F.E.N. (e-mail: fernovas@muanbe.gov.ar).


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