Science 7 September 2007:
Vol. 317. no. 5843, pp. 1378 - 1381
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26. We thank the field crew of the 1993 field season for their work; X. Xu, Z. Zhou, C. Forster, and D. Krause for specimen access; P. Makovicky, N. Smith, J. Conrad, A. Balanoff, G. Bever, R. Irmis, and S. Nesbitt for discussions; M. Ellison for photographs; and B. Amaral, A. Davidson, and A. Balcarcel for preparation. Support was provided by NSF through a Doctoral Dissertation Improvement Grant (DEB 0608003, presented to A.H.T. and M.A.N.); grant ATOL 0228693 (presented to M.A.N.); the Program in Geoscience, Division of Earth Sciences (grant EAR 0207744, presented to G.M.E. and M.A.N.); and the Division of Biological Infrastructure, Program in Biological Databases and Information (grant DBI 0446224, presented to G.M.E.). Additional support was provided to A.H.T. by the American Museum of Natural History and Columbia University.
A Basal Dromaeosaurid and Size Evolution Preceding Avian FlightAlan H. Turner,1*Diego Pol,2Julia A. Clarke,3,4,1Gregory M. Erickson,5Mark A. Norell1
Fossil evidence for changes in dinosaurs near the lineage leadingto birds and the origin of flight has been sparse. A dinosaurfrom Mongolia represents the basal divergence within Dromaeosauridae.The taxon's small body size and phylogenetic position implythat extreme miniaturization was ancestral for Paraves (theclade including Avialae, Troodontidae, and Dromaeosauridae),phylogenetically earlier than where flight evolution is stronglyinferred. In contrast to the sustained small body sizes amongavialans throughout the Cretaceous Period, the two dinosaurianlineages most closely related to birds, dromaeosaurids and troodontids,underwent four independent events of gigantism, and in somelineages size increased by nearly three orders of magnitude.Thus, change in theropod body size leading to flight's originwas not unidirectional.
1 Division of Paleontology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 100245192, USA.
2 CONICET, Museo Paleontológico Egidio Feruglio, Avenida Fontana 140, (9100) Trelew, Argentina.
3 Department of Marine, Earth and Atmospheric Sciences, North Carolina State University, Campus Box 8208, Raleigh, NC 276958298, USA.
4 Division of Paleontology, North Carolina Museum of Natural Sciences, 11 West Jones Street, Raleigh, NC 276011029, USA.
5 Department of Biological Sciences, Florida State University, Dewey Street and Palmetto Drive, Tallahassee, FL 323061100, USA.
* To whom correspondence should be addressed. E-mail: firstname.lastname@example.org
Which nonflying maniraptoran dinosaurs are the closest relativesto birds (Avialae) has been debated (15). Dromaeosauridsand troodontids are the two clades consistently found to bemost closely related to avialans (18). Discoveries ofthese dinosaurs, which illuminate the features ancestrally presentin the first flighted theropods, have remained rare. Here wereport a basal dromaeosaurid theropod: Theropoda Marsh, 1884;Maniraptora Gauthier, 1986; Paraves Sereno, 1997; DromaeosauridaeMatthew and Brown, 1922; Mahakala omnogovae, new taxon. Thenew taxon is small (70 cm long) and possesses features absentin other dromaeosaurids but shared with early troodontids andavialans.
Holotype. Specimen number IGM (Mongolian Institute of Geology,Ulanbaatar) 100/1033, a partial skull and postcranial skeleton(Figs. 1 and 2).
||Fig. 1. Mahakala omnogovae IGM 100/1033, holotype. (A) Skull in occipital view. (B) Braincase in left lateral view. (C) Sacrum and partial right leg in ventral view. (D) Frontal in dorsal (left) and ventral (right) views. (E) Axisvertebrain left lateral view. Scale bars, 5 mm in (A), (B), (D), and E) and 1 cm in (C). Abbreviations are as follows: cav, caudal vertebra; ctr, caudal tympanic recess; dtr, dorsal tympanic recess; ep, epipophysis; f.l, lacrimal facet; f.po, postorbital facet; fm, foramen magnum; mt, metatarsus; oc, occipitalcondyle; od, odontoid; pap, paroccipital process; pf, pneumatic foramen; ph, phalanx; prz, prezygapophysis; q.pr, contactsurface on prootic for quadrate; q, quadrate; ti, tibia; tl, tectal lobe; sac, sacrum; v.o, occipital vein track. [View Larger Version of this Image (40K GIF file)]|
||Fig. 2. Mahakala omnogovae IGM 100/1033, holotype. (A) Rightulna in lateral (right) and medial (left) views. (B) Ilium in medial (top) and lateral (bottom) views. (C) Femurinposterior (left) and lateral (right) views. (D) Tibia in anterior view. (E) Left metatarsus in anterior view. (F) Right raptorial claw. (G) Midcaudal vertebrae. Scale bars, 1 cm in (B) to (E) and 5 mm in (A), (F), and (G). Abbreviations are as follows: aa, ascending process of astragalus; as, astragalus; bf, brevis fossa; brs, brevisshelf; bs, biccipital scar; ca, calcaneum; cc, cnemial crest; ch, chevron; fc, fibular crest; fi, fibula; gtr, greater trochanter; lr, lateralridge; lc, lateral crest; mco, medial condyle; mt, metatarsal; obr, oblique ridge; pat, posterior antitrochanter; prz, prezygapophysis; pt, posterior trochanter; ts, trochanteric shelf. [View Larger Version of this Image (45K GIF file)]|
Etymology. "Mahakala," Sanskrit for one of the eight protectordeities (dharmapalas) in Tibetan Buddhism. The specific epithetrefers to the southern Gobi provenance of this taxon.
Locality and horizon. The Tugrugyin Member of the DjadokhtaFormation (Campanian) (9, 10), Tugrugyin Shireh, Ömnögov,Mongolia (10, 11).
Diagnosis. A small paravian diagnosed by the following combinationof characters (autapomorphies are noted by *): a strongly compressedand anteroposteriorly broad ulna tapering posteriorly to a narrowedge*; an elongate lateral crest on the posterodistal part ofthe femur*; anterior caudal vertebrae with subhorizontal, laterallydirected prezygapophyses*; a prominent supratrochanteric process;and the absence of a cuppedicus fossa.
Estimated at 70 cm long, Mahakala is similar in size to thebasal avialan Archaeopteryx and basal members of other maniraptoranclades such as the oviraptorosaur Caudipteryx and the troodontidMei long. The specimen is a young adult or near adult, basedon the degree of neurocentral and astragalocalcaneal fusion,braincase coossification, and histological analysis (fig. S4).Thus, it can be distinguished from the contemporaneous Archaeornithoides,which is of similar size but is a juvenile (12).
The braincase, quadrate, and frontals are well preserved. Unlikedromaeosaurids but similar to troodontids such as Sinovenator(7) and Mei (8), the frontals are dorsoventrally vaulted andthe interorbital region is narrow, indicating proportionallylarge orbits. The anterolateral corner of the frontal lacksthe articulation notch present in other dromaeosaurids. Thefrontals transition smoothly from the orbital margin to thepostorbital processes as in troodontids (13), but unlike theabrupt transition and sharply demarcated postorbital processesof dromaeosaurids. The supratemporal fossa margin is weaklycurved, not sinuous as in all other dromaeosaurids except Tsaagan(5) and Dromaeosaurus [AMNH (American Museum of Natural History)FR 5356]. The quadrate is incipiently bistylic, unlike the single-headedball-shaped process in other dromaeosaurids. A depression onthe prootic may correspond to a secondary articulation surfacefor the quadrate. This depression corresponds topographicallyto the braincase articulation facet in birds and alvarezsauridsbut is also present in the troodontid Byronosaurus (14). Thelateral braincase wall lacks any indication of a well-developedotosphenoidal crest like that in troodontids (14). The paroccipitalprocesses are relatively short and distally twisted rostrolaterallyas in other dromaeosaurids.
The axis bears a single pneumatic opening and has small epipophysesthat do not overhang the postzygapophyses. The sacrum comprisessix apneumatic, coossified centra as in Rahonavis and maturespecimens of Velociraptor (IGM 100/986 and IGM 100/985). Thefused neural arches of the posterior sacral vertebrae form abony lamina as in other dromaeosaurids. The tail is long asin basal avialans (such as Archaeopteryx and Jeholornis), basaltroodontids (such as Jinfengopteryx and Mei), and other dromaeosaurids.The transition point occurs between caudals (Cd's) 11 and 12and is more posteriorly located than in Rahonavis (proximalto Cd 9) or Velociraptor (proximal to Cd 10). The distal caudalpostzygapophyses are smaller than the prezygapophyses. As into other basal paravians, the postzygapophyses do not exceedthe posterior margin of the vertebral centra. The lateral surfaceof the proximal caudals bears a low ridge similar to that inBuitreraptor (4) and Rahonavis [UA (University of Antananarivo)8656]. The chevrons in Mahakala are platelike as in many derivedcoelurosaurs.
The scapula is narrow and straplike and has a strongly compressedovoid cross section. The preserved portion of the incompletehumerus suggests that the entire humerus was reduced in contrastto the condition of most coelurosaurs. The ulna is distinctlybowed as in most maniraptorans (1) but is strongly compressedand possesses a small biceps tubercle. The distal region ofthe radius is expanded and flattened as in paravians (11). Asemilunate carpal covers the proximal surfaces of metacarpalsI and II; a plesiomorphic conformation lost in most avialans.
The ilium is dolichoiliac. A prominent supratrochanteric processis present as in Unenlagia, Rahonavis, and many avialans. Thebrevis shelf is triangular and does not extend laterally asin some other basal dromaeosaurids. No antiliac shelf is present,therefore Mahakala lacks a defined cuppedicus fossaanabsence unique within dromaeosaurids but characteristic of avialanssuch as Apsaravis (15) and Yixianornis (16).
The femur is anteriorly bowed. The lesser trochanter is welldeveloped, and its anterior edge is continuous with the greatertrochanter. The fourth trochanter is present as a smooth andweakly developed ridge. Unlike Velociraptor (IGM 100/986), thelateral ridge is poorly developed, and the moundlike trochantericshelf is proximodistally elongated and closely connected tothe posterior trochanter. A prominent crest extends from thedistal third of the shaft to the ectocondylar tubercle. Thetibia is longer than the femur and possesses a single cnemialcrest. The lateral surface of the calcaneum is distinctly concaveand lacks the notch for the articulation with the distal fibulathat is present in dromaeosaurids and other nonavian theropods.This condition is shared with Rahonavis, basal avialans (2),and derived alvarezsaurids. Unlike most troodontids and microraptorines,but similar to Archaeopteryx and derived dromaeosaurids, thefoot of Mahakala exhibits the plesiomorphic unconstricted conditionfor metatarsal III, further indicating that this avian traitmay be the primitive condition for paravians. The distal endof metatarsal II is composed of an asymmetrical ginglymoid articularsurface and phalanx II-2 has a well-developed proximal heeland hypertrophied ginglymoid trochlea. This suite of charactersis present only in dromaeosaurids.
Phylogenetic analysis identifies Mahakala as a basal dromaeosauridand supports paravian monophyly with birds (Avialae) as thesister group to a monophyletic Deinonychosauria (Dromaeosauridae+ Troodontidae) (Fig. 3 and fig. S1). Although discovered inrelatively young Cretaceous deposits, the basal position ofMahakala has several implications regarding our understandingof the early history of deinonychosaurians (17). First, Shanagfrom the Early Cretaceous of Mongolia (18) nests within thepurported Gondwanan lineage of dromaeosaurids, Unenlagiinae.This topology complicates recently proposed vicariance-drivenorigin hypotheses for these groups (4, 19). Second, these dinosaursare united with Jehol microraptorines (Microraptor, Graciliraptor,and Sinornithosaurus) to form the sister group to derived dromaeosauridsfrom Laurasia (velociraptorines and allied forms). Third, thepurported avialan Jinfengopteryx (20) is a troodontid. Jinfengopteryxhas feathers; it thus demonstrates the presence of feathersof modern aspect in a troodontid.
||Fig. 3. Phylogeny and body size change within paravian theropods. A temporally calibrated cladogram depicting the phylogenetic position of Mahakala and paravian body size through time and across phylogeny is shown. Characters uniting Mahakala with other dromaeosaurids include the absence of an accessory tympanic recess dorsal to the crista interfenestralis, and elongate paroccipital process with parallel dorsal and ventral edges that twist rostrolaterally distally, and the presence of a distinct ginglymus on the distal end of metatarsal II (17). Silhouettes are to scale, illustrating the relative magnitude of body size differences. Left-facing silhouettes near open circles show reconstructed ancestral body sizes. Ancestral paravian body size is estimated to be 600 to 700 g and 64 to 70 cm long (17). The ancestral deinonychosaur, troodontid, and dromaeosaurid body size is estimated at 700 g. Large numbers (1, 2, 3, and 4) indicate the four major body increase trends in Deinonychosauria. See the supporting online material for further ancestral body size reconstruction data. Ma, Maastrichtian; Ca, Campanian; Sa, Santonian; Co, Coniacian; Tu, Turonian; Ce, Cenomanian; Ab, Albian; Ap, Aptian; Bar, Barremian; Hau, Hauterivian; Va, Valanginian; Ber, Berriasian; Ti, Tithonian; Ki, Kimmeridgian. Ma, million years ago. [View Larger Version of this Image (35K GIF file)]|
Decrease in body size is a trend in coelurosaurs (3, 8, 21)and is thought to have played an important role in the originof birds and flight (6, 11, 2224). Dromaeosaurids andother coelurosaurs, however, may have undergone clade-specificincreases in body size (8, 25). Testing these trends requiresempirical size reconstructions for each node of the coelurosaurtree. We estimated ancestral body sizes for each internal node(ancestral node) using body mass estimates from femoral lengthmeasurements. These data were treated as a continuous additivetrait and optimized across the phylogeny (16).
Our analysis (fig. S2) indicates that small body size was nota derived condition at Archaeopteryx or Avialae, where flightevolution in theropods is currently inferred. The ancestraldromaeosaurid, troodontid, and deinonychosaurian are reconstructedas small, each with a body mass around 700 g (Fig. 3). The basalmembers of these lineages are the same size as the early avialanJeholornis. Additionally, our results indicate that deinonychosaursunderwent four parallel trends of body size increase. Threeof these events occurred within Dromaeosauridae: Deinonychusincreased in size by more than two orders of magnitude, as didUnenlagia, and the Achillobator + Utahraptor clade increasedby three orders of magnitude. A single trend of body size increasewas observed in troodontid body size. These events were contemporaneouswith a decrease in avialan body sizes. Our analysis impliesthat the ancestral paravian had a body size of 600 to 700 gand was 65 cm long, roughly the size of the largest specimensof Archaeopteryx or Sapeornis and entailing the size range reconstructedfor basal deinonychosaurs. Thus, miniaturization preceded theavialan node and the origin of flight, and as a result, hypothesesrelating ontogenetic or metabolic controls on miniaturizationto flight origin in theropods must be equally capable of explainingthe size reduction within ancestral paravians and the iterativetrends of size increase in deinonychosaurs.
References and Notes
Supporting Online Material
Figs. S1 to S5
Received for publication 20 April 2007. Accepted for publication 30 July 2007.
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