Nature 399, 350 - 354 (1999) © Macmillan Publishers Ltd.
XING XU*, ZHI-LU TANG* & XIAO-LIN WANG*†
Therizinosauroidea ('segnosaurs') are little-known group of Asian dinosaurs with an unusual combination of features that, until recently, obscured their evolutionary relationships. Suggested affinities include Ornithischia1, Sauropodomorpha2,3, Theropoda4,5,6,7,8,9,10,11 and Saurischia sedis mutabilis12. Here we describe a new therizinosauroid from the Yixian Formation (Early Cretaceous, Liaoning, China)13. This new taxon provides fresh evidence that therizinosauroids are nested within the coelurosaurian theropods8,9,10,11. Our analysis suggests that several specialized therizinosauroid characters, such as the Sauropodomorpha-like tetradactyl pes1,2, evolved independently within this group. Most interestingly, this new dinosaur has integumentary filaments as in Sinosauropteryx14,15. This indicates that such feather-like structures may have a broad distribution among non-avian theropods, and supports the hypothesis that the filamentous integumentary structures may be homologous to the feathers of birds14,15.
Dinosauria Owen 1842
Theropoda Marsh 1881
Coelurosauria sensu Gauthier 1986
Therizinosauroidea Russell and Dong 1993
Beipiaosaurus inexpectus gen. et sp. nov.
Etymology. Beipiao: the city near the locality where the specimen was found; saurus: lizard; inexpectus: referring to the surprising features in this animal.
Holotype. IVPP V11559 (Institute of Vertebrate Paleontology & Paleoanthropology, Beijing, China; see Fig. 1).
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| Figure 1 Beipiaosaurus inexpectus (V11559, holotype). Photograph (a) and outline (b) of the skeleton (broken lines indicate features preserved in impressions). The holotype was collected in 1996 by a farmer, Li Yinxian, from the famous Sihetun locality. It was later (1997) determined to be from the lower part of the Yixian Formation. According to communication with the collector, and consistent with the close proximity, preservation and proportions of the elements, all elements (including the integumentary structures) are from a single individual. V11559 includes the partial right dentary with dentition, right postorbital, right parietal, right nasal?, right prootic, a few cervicals and dorsals, an incomplete caudal, incomplete ribs, partial scapula, coracoids and furcula, partial humerus, radius and ulna, nearly complete hands, partial ilium, pubis and ischium, complete right femur, right tibia and right fibula, incomplete left femur, tibia and fibula, incomplete right foot. Some elements are represented by impressions. Sacral and most caudal vertebrae are missing. a, astragalus; c, cervical vertebra; ca, caudal vertebra; co, coracoids; d, dentary; dcI, distal carpal I; do, dorsal vertebra; f, femur; fi, fibula; fu, furcula; I-III, metacarpals I-III, I-1 to III-4, manual phalanges I-1 to phalanges III-4; il, ilium; is, ischium; lh, left humerus; lr, left radius; lu, left ulna; ?n, ?nasal; p, parietal; pe, pes; po, postorbital; pr, prootic; pu, pubis; r, rib; ?ra, ?radiale; rh, right humerus; rr, right radius; ru, right ulna; s, scapula; sl, semilunate distal carpal; t, tibia |
Locality and horizon. Sihetun locality near Beipiao, Liaoning, China. The lower part of the Yixian Formation, probably from the Lower Cretaceous based on latest radiometric evidence13.
Diagnosis. Beipiaosaurus inexpectus differs from other
therizinosauroids in having shorter and more bulbous tooth crowns, a larger skull, a
tridactyl pes with a splint-like proximal first metatarsal, a shallow anterior iliac
process, a long manus (10% longer than a femur), a long tibia (
Beipiaosaurus is the largest known theropod from the Yixian Formation, with an
estimated length of 2.2 m. It has a relatively large skull compared to other
therizinosauroids (preserved dentary is 65% of femur length). The anterior end of its
dentary is down-turned. The dentary has a lateral shelf, similar to other
therizinosauroids and ornithischians1.
Beipiaosaurus has a large number of teeth (more than 37, inferred from the
preserved alveoli in the broken dentary). They resemble those of Protarchaeopteryx16, but have larger serrations (3
serrations per mm) as in other therizinosauroids and troodontids9. Replacement teeth developed in oval
resorption pits next to the roots of erupted teeth (Fig. 2a), as in Archaeopteryx17. Dorsally pointed, triangular interdental plates are
present.
| Figure 2 Beipiaosaurus inexpectus. a, Nine right dentary teeth in medial view. Note the resorption pits and replacement teeth. b, A dentary tooth in lateral view. c, Close-up of the left semilunate carpal of V11559. d, Drawing of part of the right manus of V11559. Note the shape and position of the semilunate, which is very similar to that of birds17. e, Drawing of the partially preserved right pes of V11559. f, Close-up of the first metatarsal of V11559. Note the proximally pinched theropod first metatarsal. The theropod first metatarsal is absent in other therizinosauroids, which has been argued as being strong evidence against the theropod affinities of therizinosauroids1. Additional abbreviations: mc I-III, metacarpals I-III; mt I-IV, metatarsals I-IV; pul, pedal ungual; r, radius; ra, radiale; ta, tarsal; u, ulna. |
The cervical vertebrae bear low, anteroposteriorly short neural spines. Lateral depressions are present on the lateral sides of the centra of the fused posterior dorsals.
The coracoid is subrectangular, as in some maniraptoran theropods, with a pronounced coracoid tubercle. Exquisite impressions show that the furcula is a widely arched bone, oblate-shaped in cross section, without a hypocleidium. Compared to the short and stout hindlimb, the forelimbs are relatively long. The elongate hand is longer than the foot, as in dromaeosaurids and primitive Avialae18. As in other therizinosauroids, the humerus has a pointed internal tuberosity on its proximal end, and anteriorly positioned radial and ulnar condyles on its distal end. A depression on the proximal surface of the humerus separates the head and internal tuberosity, as in other therizinosauroids and Mononykus19. Five carpals are preserved. The largest distal carpal, the semilunate (Fig. 2c, d), is smaller than but otherwise identical to that of Deinonychus20. It primarily contacts metacarpal II but also touches metacarpal I (Fig. 2d), unlike the condition in Alxasaurus, in which the largest carpal is the distal carpal I8. Distal carpal I is large and oval (Fig. 2c). The proximal carpals are represented by a V-shaped radiale in close contact with the radius, and a small rounded carpal between the distal ends of the radius and ulna (Fig. 2c, d). The manus is slender and elongate, proportionally similar to that of Deinonychus20. Metacarpal I has a pronounced distal flange, as in Deinonychus. The proximal parts of metacarpals I and II are closely appressed. Metacarpal III is slender and slightly bowed. The combined lengths of phalanges III-1 and III-2 are equal to the length of phalanx III-3, as in advanced theropods2. There are well developed ligament pits on the lateral sides of the distal ends of the phalanges. The manual unguals are laterally compressed and strongly curved. As in other therizinosauroids8, their proximal ends are deep but taper to needle-sharp points. The second manual claw is slightly longer than the first, resembling those of Archaeopteryx and Protarchaeopteryx21.
The ilium is shaped like a parallelogram, similar to those of dromaeosaurids and basal birds, but unlike the sauropod-like ilia of derived therizinosauroids1,22. The posterodorsal margin of the ilium curves ventrally in lateral view. The anterior and posterior processes are almost the same length. The posteroventral margin of the ilium is deflected laterally at a right angle to the vertical ramus, and has a shallow brevis fossa similar to those of other coelurosaurians23. The partial pubic peduncle of the ilium is longer than the ischiadic peduncle, similar to those of therizinosauroids, dromaeosaurids and Archaeopteryx23. Both the pubic and the ischial shafts are more rounded than flattened, unlike those of Alxasaurus and Segnosaurus. As in some theropods, the pubic apron is compressed and positioned more distally. The femur of Beipiaosaurus has a wing-like lesser trochanter, a cleft between the greater trochanter and the lesser trochanter, and a crest-like fourth trochanter. The tibia has a fibular crest, a feature of theropods2. The fibula is very slender compared to the tibia, especially the distal half. As in Alxasaurus8 and the Avialae24, the medial surface of the fibula is flat, lacking the medial fossa of some theropods. As in other therizinosauroids, the astragalus has a tall ascending process and reduced condyles that only partly cover the distal end of the tibia. The calcaneum is sub-oval and disk-shaped. The metatarsus is 39% of the length of the tibia, larger than in known therizinosauroids but less than in other theropods (>45%)8. The proximal end of metatarsal I is flattened and tapered and, as in most maniraptorans, does not contact the tarsus (Fig. 2e, f). The proximal ends of both metatarsals III and IV are compressed, especially on the medial side. Metatarsal V is slender and strap-like, being only half the length of the other metatarsals. One pedal ungual is preserved, and is shorter than any manual unguals.
Large patches of integumentary structures were found in close association with the ulna, radius, femur and tibia, as well as with pectoral elements. The filamentous structures are best preserved near the ulna, almost perpendicular to the bone (Fig. 3). They are similar to the integumentary structures of Sinosauropteryx15 in their parallel arrangement. Unlike those of Sinosauropteryx, the integumentary structures of Beipiaosaurus contact the ulna. They are densest close to the bone. Most of the integumentary filaments are about 50 mm long, although the longest is up to 70 mm. Some filaments have shallow and faint median grooves, possibly indicating hollow cores that had collapsed, and have indications of branching distal ends as in Sinosauropteryx15. As in Sinosauropteryx15 and birds from the same locality, it is difficult to isolate a single filament and thus difficult to describe the branching pattern of the integumentary filaments.
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| Figure 3 Beipiaosaurus inexpectus. a, Partially preserved forelimb with unusual integumentary impression. b, Close-up of the integumentary impression. |
Therizinosauroidea has many perplexing features for a theropod, such as a very small head, a sauropod-like ilium and a short and broad tetradactyl pes with rudimentary metatarsal V1,2,12,22. Until now, no cladogram has been proposed for the relationships and morphological evolution of therizinosauroids. We ran a phylogenetic analysis with an 84-character dataset (see Supplementary Information for the character list and matrix). We left out the unnamed 'segnosaur' from the Early Jurassic Lower Lufeng Formation25 as it is too incomplete. Using PAUP (3.1.1. Exhaustive search, Deltran optimization; Swofford, 1993), we obtained a single most parsimonious tree (tree length, 133; consistency index, 0.707; retention index, 0.645; rescaled consistency index, 0.456). Our analysis (Fig. 4) places Beipiaosaurus as a basal taxon within Therizinosauroidea. Beipiaosaurus has a relatively large skull (1.0) among therizinosaurs, a tridactyl pes (79.0) and a fibular crest on the tibia, all of which are primitive theropod features. The pelvic elements are also very similar to those of other coelurosaurians. These characteristics support the hypothesis that therizinosauroids (including Beipiaosaurus) are nested within the coelurosaurian theropods8,9,10,11. Given this phylogeny (Fig. 4), some derived characters of therizinosauroids other than Beipiaosaurus are most parsimoniously interpreted as having evolved convergently with some other dinosaur groups, sauropodomorphs in particular. Thus, therizinosauroids re-evolved a robust first digit in which the proximal end of metatarsal I articulates with the tarsals (79.1).
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| Figure 4 Phylogenetic relationships of Beipiaosaurus inexpectus. Beipiaosaurus and other therizinosauroids share 18 synapomorphies, including the following unique characters: a prominent dorsolateral shelf on the dentary (21.1), teeth that increase in size anteriorly (25.1), tooth crowns with sub-circular basal cross-sections that lack mediolateral compression (27.1), anteroposteriorly narrow and dorsoventrally deep pubic peduncle of ilium (46.1 and 47.1), very deep proximal end of manual unguals (70.1), short metatarsus (78.1) and reduced main body of astragalus (82.1). It is less derived than other therizinosauroids because it lacks 13 characters of Therizinosauroidea (1.1, 36.1, 38.0, 43.0, 48.1, 49.1, 51.1, 52.1, 58.1, 60.0, 66.0, 77.1, 79.1), including the following unusual characters: a very small head (1.1), the long and deep preacacetabular portion of ilium (48.1 nd 49.1) and absence of the theropod first metatarsal (79.1). |
Feathers are complex structures. Their abrupt appearance in the bird fossil record has been difficult to explain, mainly because no intermediate structures are preserved in the related theropod taxa. The integumentary filaments of Sinosauropteryx have been considered to be 'proto-feathers' by some, but this idea has been rejected by others26. Such structures have not been preserved with any other theropods26 until the discovery of Beipiaosaurus. The filamentous structures in Beipiaosaurus are similar to, but longer than, those of the compsognathid Sinosauropteryx. They are perpendicular to the limb bones, and are unlikely to be muscle fibres or frayed collagen27. Their presence in both therizinosauroids and compsognathids indicates that there may be a broader distribution of similar structures in theropod dinosaurs. This supports the idea that these simple integumentary filaments may represent an intermediate evolutionary stage to the more complex feathers of Protarchaeopteryx, Caudipteryx16 and more derived Avialae. The absence of such structures in most theropod fossils is probably attributable to the lack of such ideal preservation as is found in the Yixian Formation. This again indicates that feathers preceded flight16, because both therizinosaurids and compsognathids apparently could not fly and did not descend from flying animals.
Supplementary information is available on Nature's World-Wide Web site (http://www.nature.com) or as paper copy from the London editorial office of Nature.
Received 4 November 1998;accepted 31 March 1999.
References
Acknowledgements. We thank J. Clark for advice and reviewing the manuscript; Z.-X. Luo for improving the organization and language of the manuscript as well as the use of PAUP 3.11; Z.-H. Zhou and O. Rauhut for discussions; P. Currie, M. Norell, P. Sereno, X.-C. Wu and H. Osmolska for reviews and comments; and the Liaoxi expedition members of the IVPP. Photographs were taken by J. Zhang, electronic photography by L. Oyang, and line drawings are by R.-S. Li, Y.-T. Li, H.-J. Wang and J.-Z. Ding prepared the specimen. This study was supported by research grants from the Chinese Academy of Sciences and the National Natural Science Foundation of China.
