A Basal Alvarezsauroid Theropod from the Early Late Jurassic of Xinjiang, China

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Science  29 Jan 2010:
Vol. 327, Issue 5965, pp. 571-574
DOI: 10.1126/science.1182143


The fossil record of Jurassic theropod dinosaurs closely related to birds remains poor. A new theropod from the earliest Late Jurassic of western China represents the earliest diverging member of the enigmatic theropod group Alvarezsauroidea and confirms that this group is a basal member of Maniraptora, the clade containing birds and their closest theropod relatives. It extends the fossil record of Alvarezsauroidea by 63 million years and provides evidence for maniraptorans earlier in the fossil record than Archaeopteryx. The new taxon confirms extreme morphological convergence between birds and derived alvarezsauroids and illuminates incipient stages of the highly modified alvarezsaurid forelimb.

The presence of the basal avialan (13) Archaeopteryx in the latest Late Jurassic (Tithonian) and the poor fossil representation of more basal maniraptoran taxa in contemporaneous or slightly older deposits indicate either a gap in the stratigraphic record or, more controversially, that birds are not related to theropods (4). Recent discoveries of Middle-Late Jurassic maniraptorans (57) from China are starting to fill in the temporal gap, but the ages of these new taxa are poorly resolved (8, 9), and they do not clarify basal maniraptoran diversification because very little character evidence separates them from birds (5, 7).

Here, we describe a three-dimensionally preserved, nearly complete skeleton of an alvarezsauroid theropod, Haplocheirus sollers, gen. et spec. nov. (10), from orange mudstone beds in the upper part of the Shishugou Formation in Wucaiwan area, Junggar Basin, Xinjiang, China. Radiometric dating constrains the age of this fossil to between 158.7 ± 0.3 and 161.2 ± 0.2 Ma (million years ago) (11), corresponding to the Oxfordian marine stage in the early Late Jurassic (12). The dates for Haplocheirus reduce the conflict between the fossil record and phylogenetic hypotheses that early maniraptoran diversification took place in the Jurassic. Alvarezsauroids are known from South America (1315), Asia (1619), North America (20, 21), and Europe (22, 23). The basal phylogenetic position and early temporal position of Haplocheirus imply that Alvarezsauroidea originated in Asia rather than South America (14, 20). Derived members of the Alvarezsauroidea were originally thought to be flightless basal avialans (18) because they share many morphological characteristics with birds, including a loosely sutured skull, a keeled sternum, fused wrist elements, and a posteriorly directed pubis. Haplocheirus preserves plesiomorphic morphological characteristics that confirm a basal position for Alvarezsauroidea within Maniraptora (24), demonstrating that these features of derived alvarezsauroids represent dramatic convergences with birds.

IVPP (Institute of Vertebrate Paleontology and Paleoanthropology) V15988 (Figs. 1 and 2 and figs. S4 to S9) is ~140 cm in total body length as preserved but is missing the end of the tail (estimated total length 190 to 230 cm; table S1). The bones of the braincase are coossified and the neurocentral sutures are visible, suggesting that the animal is likely a young adult or late-stage subadult.

Fig. 1

Haplocheirus sollers (IVPP V15988). (A) Photograph of holotype in dorsal view. (B) Line drawing of holotype in dorsal view. Dashed line indicates crocodyliform fossil underlying cervical vertebrae. (C) Reconstruction. Gray fill indicates portions of the skeleton that are not preserved. Abbreviations: cav, caudal vertebrae; cv, cervical vertebrae; gs, gastralia; il, left ilium; lf, left femur; lh, left humerus; lm, left manus; p, pubis; rf, right femur; rh, right humerus; rm, right manus; rmt, right metatarsus; rp, right pes; rs, right scapula; rtf, right tibia and fibula; sk, skull; sv, sacral vertebrae; tr, thoracic ribs; tv, thoracic vertebrae. Scale bar: 25 cm.

Fig. 2

Haplocheirus sollers (IVPP V15988) skull and forelimb elements. (A) Skull in left lateral view. (B) Right scapula in lateral view. (C) Right coracoid in lateral view. (D) Right humerus in lateral view. (E) Left distal humerus in flexor view. (F) Left distal humerus in distal view. (G) Right ulna in medial view. (H) Left manus in lateral view, with digit II separated from manus. Abbreviations: ac, acromion process; af, axial furrow; aof, antorbital fenestra; cf, coracoid foramen; ct, coracoid tuberosity; dpc, deltopectoral crest; eec, ectepicondyle of humerus; emf, external mandibular fenestrae; en, external naris; ft, flexor tubercle; g, glenoid; hh, humeral head; it, internal tuberosity; mcII to mcIV, metacarpals II to IV; mf, maxillary fenestra; o, orbit; op, olecranon process of the ulna; rap, retroarticular process; slc, semilunate carpal. Scale bar: 4 cm.

The gracile, low skull (Fig. 2A and figs. S4 to S7) is well preserved in three dimensions. The narrow, elongate rostrum becomes taller and wider just anterior to the large, anterolaterally facing orbits. The dorsoventrally thin jugal is triradiate, unlike the rodlike jugal of more derived alvarezsauroids (17). In lateral view, the basisphenoid is oriented at 45° to horizontal, a condition present in some troodontids (25) and in alvarezsauroids (17). The basipterygoid processes are long and project ventrolaterally, a morphology known only in primitive birds and alvarezsauroids among Theropoda (17).

At least 30 small maxillary teeth are present in Haplocheirus, as in Shuvuuia (17), Pelecanimimus (26), therizinosauroids (27), and troodontids (28). Unlike the conical, unserrated teeth of Mononykus (28) and Shuvuuia (29), however, the maxillary teeth of Haplocheirus are recurved and bear small serrations posteriorly (fig. S4). Haplocheirus shows marked heterodonty in both the maxilla and the dentary, with the maxillary teeth diminishing in size posteriorly (fig. S5) and the lower jaw bearing large, subconical, unserrated anterior teeth and smaller, recurved, serrated posterior teeth (fig. S4).

The cervical centra lack the strong opisthocoelous condition of Shuvuuia and Mononykus (29). The five sacral vertebrae all lack the ventral keel present in other alvarezsauroids (29). The centrum of sacral five is amphiplatyan, whereas in Mononykus and Shuvuuia (29) the last sacral centrum bears a convex posterior surface for articulation with the procoelous first caudal vertebra. Similar to other alvarezsauroids, the mid-caudal vertebrae have short and anterodorsally oriented prezygapophyses, whereas in most coelurosaurs the prezygapophyses of the mid-caudal vertebrae are long and horizontally oriented. A sternum was not found with the specimen.

The ovate coracoid has a long posteroventral process and bears a well-developed biceps tubercle, which is lost in other alvarezsauroids. Similar to the basal alvarezsauroid Patagonykus (30), the hypertrophied rectangular internal tuberosity of the humerus is separated from the humeral head by a distinct notch, and the humeral ectepicondyle is large and hemispherical distally. The incomplete ulna bears a well-developed olecranon process, as do all alvarezsauroids. Proximally, the radius articulates with a lateral concavity on the ulna.

Unlike the avianlike carpometacarpus (29) of more derived alvarezsauroids, the distal carpals are unfused. Metacarpal II (the medial metacarpal) is 1.9 times the width of metacarpal III (Fig. 3), wider than in most maniraptorans but narrower than in Mononykus and Shuvuuia (29). Metacarpal IV is only half the length of metacarpal III, a condition unknown in other theropod dinosaurs. The middle digit is the longest in the manus, unlike in Shuvuuia, where the second and third digits are both much shorter than the first digit (31). Manual phalanx II-1 bears a deep axial furrow ventrally, as in all alvarezsauroids (14). The manual unguals are curved and bear distally placed flexor tubercles, unlike the unusual unguals of derived alvarezsauroids (31), which are flat and lack flexor tubercles.

Fig. 3

Phylogenetic relationships of Haplocheirus sollers and hand comparisons of selected theropods. (A) Simplified, temporally calibrated cladogram of the strict consensus of 69 most parsimonious trees produced in this analysis (see also fig. S1). Thick lines with rounded end caps indicate stratigraphic range of known taxa. Thin black lines with square ends indicate phylogenetic relationship. Dashed lines represent ghost lineages implied by the stratigraphic distribution of fossils with respect to the phylogenetic relationships shown here (note the exceptionally long ghost lineage for Alvarezsauroidea). Arabic numerals indicate ages in millions of years before present. Boxes represent named clades. (B to E) Reconstructed theropod mani scaled to digit two length. (B) Allosaurus fragilis after Madsen (40). (C) Haplocheirus sollers (IVPP V15988). (D) Shuvuuia deserti after Suzuki et al. (31). (E) Deinonychus antirrhopus after Ostrom (41). Metacarpal elements are shaded, dashed lines in (D) indicate inferred digital elements. Abbreviations: II to IV, manual digits II to IV; Aa, Aalenian; Baj, Bajocian; Bat, Bathonian; Cal, Callovian; Ox, Oxfordian; Ki, Kimmeridgian; Ti, Tithonian; Be, Berriasian; Va, Valanginian; Ha, Hauterivian; Bar, Barremian; Ap, Aptian; Al, Albian; Ce, Cenomanian; Tu, Turonian; Co, Coniacian; Sa, Santonian; Cam, Campanian; Ma, Maastrichtian. Scale bar: 5 cm (B), 4 cm (C and E), 0.5 cm (D).

The pubis projects anteroventrally (figs. S8 and S9), which is the plesiomorphic condition for maniraptorans, in contrast with the vertical pubes of Patagonykus (30) and highly retroverted pubes of derived alvarezsauroids (29). The curved femur bears a plesiomorphic alariform lesser trochanter, consistent with the femoral morphology of Alvarezsaurus (14) and Patagonykus (30). The lateral distal condyle of the femur is conical (fig. S9) and projects further distally than the medial condyle, a morphology known only in some troodontids and alvarezsauroids (14). There is no development of an avianlike medial cnemial crest, as in Mononykus and Shuvuuia (26). The third metatarsal is fully exposed in anterior view and is a component of the ankle joint, as in the basal alvarezsauroids Patagonykus and Alvarezsaurus (13, 30).

A phylogenetic analysis of 99 theropod taxa shows that Haplocheirus is the basalmost member of the Alvarezsauroidea [Fig. 3 and fig. S1; see Supporting Online Material (SOM) for full details]. Haplocheirus possesses unambiguous synapomorphies that support the monophyly of the Alvarezsauroidea, including long basipterygoid processes, a vertically inclined basisphenoid, a hypertrophied internal tuberosity of the humerus proximally level with the humeral head, a large humeral ectepicondyle, a pronounced axial furrow on the flexor surface of manual phalanx II-1, and a conical lateral distal condyle of the femur.

Although a basal position of alvarezsauroids within Maniraptora has been proposed (24, 3234), the global phylogenetic placement of this group within Theropoda has been untested by the recent description of new alvarezsauroid material from Canada (20), Argentina (15), and Mongolia (19). Early analyses placed alvarezsauroids as either sister to, or nested within, Avialae (28, 29). Alvarezsauroidea has also been hypothesized as the sister taxon to Ornithomimosauria (33). Our phylogenetic analysis agrees with still other research (2, 24) in placing Alvarezsauroidea as a relatively basal maniraptoran group. Our most parsimonious trees do not support either avialan or ornithomimosaurian affinities for the Alvarezsauroidea, although the ornithomimosaur hypothesis is nearly as well supported. The shortest tree found when constraining the Alvarezsauroidea to be sister to or nested within Avialae is seven steps longer than the optimal tree. The minimum length of trees produced when constraining Alvarezsauroidea to be sister to or nested within Ornithomimosauria is one step longer than the optimal tree (see SOM for phylogenetic details).

The Middle to Late Jurassic (Bathonian-Kimmeridgian) age (8, 9) of newly described maniraptorans from China (6, 7) implies that the Alvarezsauroidea have a minimum ghost lineage (35) of ~63 million years (Fig. 3). The presence of Haplocheirus in the early Late Jurassic of China confirms the prediction made from this ghost lineage that alvarezsauroids were present at this time. To explore the effect of Haplocheirus on congruence between stratigraphic information and phylogenetic hypotheses for the Coelurosauria (3639), we compared the gaps in the fossil record implied before and after inclusion of Haplocheirus (37, 39). The addition of the earliest Late Jurassic Haplocheirus improves the stratigraphic fit of the maniraptoran fossil record to the topologies recovered in our analysis by an average of 14%, from a mean fit of 0.41 to 0.48 (fig. S3).

Haplocheirus is the largest alvarezsauroid known from complete material (see SOM), and its basal phylogenetic position suggests a pattern of miniaturization for the Alvarezsauroidea, relatively rare in dinosaurs but convergently evolved in Paraves (2). Derived alvarezsauroids have a simplified, homogeneous dentition convergent with that of some extant insectivorous mammals (20), but Haplocheirus has recurved, serrated teeth and caniniforms that suggest carnivory was the primitive condition for the clade. The presence in Haplocheirus of only slightly reduced second and third manual digits and curved unguals with flexor tubercles on these digits implies that the hand was fully functional and Haplocheirus retained some grasping ability, unlike the presumably limited function of the greatly reduced lateral manual elements of Mononykus and Shuvuuia (31). The mediolaterally narrow McIII (metacarpal three) and the greatly shortened and slender McIV suggest that the extensive digital reduction and fusion seen in derived alvarezsauroids was already under way by the earliest Late Jurassic, proceeded from lateral to medial on the manus and, surprisingly, initially involved reduction in length of only McIV.

Supporting Online Material

Materials and Methods

SOM Text

Figs. S1 to S9

Tables S1 and S2


References and Notes

  1. We use the definition of Avialae from (2), the least inclusive clade containing Archaeopteryx lithographica and crown group birds, rather than the definition from (3), all taxa sharing a more recent common ancestor with Archaeopteryx than with Troodon formosus.
  2. Systematic paleontology: Theropoda Marsh, 1881; Coelurosauria von Huene, 1914; Alvarezsauroidea Bonaparte, 1991; Haplocheirus sollers, gen. et spec. nov. Etymology: Haplocheirus, Latinized from haplocheir (Greek): “simple hand,” and referring to the lack of the specialized manus of derived alvarezsauroids; sollers, Latin for “skillful,” referring to the presumed ability of this taxon to perform digital actions that would be impossible for derived alvarezsaurids. Holotype: IVPP V15988 is a nearly complete skeleton, missing only the distal caudal vertebrae and the dorsal aspects of the ilia (Figs. 1 and 2 and figs. S4 to S9). Locality and horizon: Junggar Basin, Xinjiang, China. Lower orange mudstone beds in the upper part of the Shishugou Formation (Oxfordian). Diagnosis: Large alvarezsauroid with the following autapomorphies: accessory mandibular fenestra anterodorsal to the mandibular fenestra, fenestrae divided by posterior process of the dentary; metacarpal III one-half the length of metacarpal II. Differs from all other alvarezsauroids in the following derived features: heterodont dentary tooth row with enlarged dentary tooth 4; alveolar margin of anterior end of dentary is dorsally convex; maxillary and dentary teeth with posterior serrations. Plesiomorphic in the Alvarezsauroidea for the following characters: postorbital contacts the jugal to form a postorbital bar; recurved maxillary and dentary teeth with serrations; distal carpals not fused to metacarpals; manual digit III longer than digit II; manual digits III and IV bear recurved unguals; pubis projects anteroventrally; ventral surface of sacrum without keel; posterior surface of last sacral centrum flat.
  3. We measured congruence of stratigraphy with phylogeny using the modified Manhattan Stratigraphic Measure (MSM*) (37) with the phylogenetic software package TNT (38) and published scripts that allow for uncertainty in first appearance dates for fossil taxa (39).
  4. We thank W. Ding and T. Yu for finding the specimen, and the crew of the 2004 Sino-American field expedition for excavating the specimen; H.-j. Wang, X. Ding, and L. Xiang for preparing the fossil; A. Buscalioni, C. Mehling, and M. Norell for specimen access; and P. Barrett, H. Cameron, J. Conrad, M. Ellison, D. Hone, C. Sullivan, and A. Turner for discussions. Support for this research was provided by the National Science Foundation Division of Earth Sciences and Office of International Science and Engineering of the USA, the National Natural Sciences Foundation of China, and the Chinese Academy of Sciences; and the GWU Facilitating Fund, the Jurassic Foundation, the Hilmar Sallee bequest, and the George Washington University.
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