Vol 461 | 1 October 2009 | doi:10.1038/nature08322 LETTERS A pre-Archaeopteryx troodontid theropod from China with long feathers on the metatarsus Dongyu Hu1, Lianhai Hou1,2, Lijun Zhang1,3 & Xing Xu1,2 600–2,890m 176–2,624m Ber Jehol Group Tuchengzi Formation ~125 Myr ~155 Myr Haifanggou Formation 104–580m Aal-Tit Tiaojishan Formation 230–1,800m Jurassic Cretaceous on the lateral surface near the junction of the neural arch and centrum (Fig. 3b), and the coracoid bears a laterally located coracoid tubercle (Fig. 3c). The ischium is strongly curved posteriorly, with an obturator Basalt Plb-Toa Beipiao Formation 500–1,300m Andesite Siltstone Mudstone Conglomerate Sandstone Tuff Het-Sin Xinglonggou Formation 130–500m The early evolution of the major groups of derived non-avialan theropods is still not well understood, mainly because of their poor fossil record in the Jurassic. A well-known result of this problem is the ‘temporal paradox’ argument that is sometimes made against the theropod hypothesis of avian origins1. Here we report on an exceptionally well-preserved small theropod specimen collected from the earliest Late Jurassic Tiaojishan Formation of western Liaoning, China2. The specimen is referable to the Troodontidae, which are among the theropods most closely related to birds. This new find refutes the ‘temporal paradox’1 and provides significant information on the temporal framework of theropod divergence. Furthermore, the extensive feathering of this specimen, particularly the attachment of long pennaceous feathers to the pes, sheds new light on the early evolution of feathers and demonstrates the complex distribution of skeletal and integumentary features close to the dinosaur–bird transition. Anchiornis huxleyi has been recently described, based on an incomplete specimen, as a basal avialan filling the morphological gap between non-avian and avian dinosaurs3. A nearly complete, extensively feathered specimen (LPM-B00169, housed in Liaoning Paleontological Museum) referable to Anchiornis huxleyi (Supplementary Information) has now been recovered from the Tiaojishan Formation at the Daxishan locality, Jianchang County. The Tiaojishan Formation has traditionally been regarded as Middle Jurassic but was recently dated to between 161 and 151 Myr (ref. 2) (Fig. 1; Supplementary Information). It is therefore older than the Archaeopteryx-bearing strata near Solnhofen, Germany, which date to less than 150 Myr (ref. 4). The new specimen exhibits a sub-triangular skull in lateral view and a large surangular foramen, as in other paravians and deinonychosaurs, respectively5–7 (Figs 2 and 3a). It has a large maxillary fenestra separated from the antorbital fenestra by a narrow interfenestral bar, a dorsoventrally flattened internarial bar, a distinct, posteriorly widening groove on the labial surface of the dentary housing the neurovascular foramina, and closely packed premaxillary and dentary teeth in the symphyseal region, derived features shared with other troodontids5,7–9. Furthermore, Anchiornis resembles Mei in having a large external naris extending posteriorly well beyond the anterior border of the antorbital fossa5, a longitudinal groove along the dorsomedial margin of the slender sub-orbital ramus of the jugal, a maxillary tooth row that approaches the preorbital bar posteriorly5 and unserrated teeth (also seen in the troodontid Byronosaurus8). A large paraquadrate foramen is present, in contrast to other troodontids but in agreement with dromaeosaurs6. Postcranially, Anchiornis also possesses a few troodontid features, including relatively long and slender transverse processes on the dorsal vertebrae and anterior-most caudal vertebrae8. As in Archaeopteryx4, the middle and posterior caudal vertebrae each bear a distinct groove Agglomerate Shale Breccia Coal measures Figure 1 | Stratigraphic column of Jurassic and Lowest Cretaceous strata in western Liaoning, showing horizons from which feathered dinosaurs have been described. Two major horizons have produced such specimens: the Tiaojishan Formation has yielded Anchiornis huxleyi LPM-B00169 and dates to about 155 Myr, whereas the Jehol Group has yielded Microraptor and other feathered dinosaurs and dates to about 125 Myr. 1 Paleontological Institute, Shenyang Normal University, 253 North Huanghe Street, Shenyang 110034, China. 2Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, 142 Xiwai Street, Beijing 100044, China. 3Shenyang Institute of Geology and Mineral Resources, 25 Beiling Street, Shenyang 110032, China. 640 ©2009 Macmillan Publishers Limited. All rights reserved LETTERS NATURE | Vol 461 | 1 October 2009 a a f g b c h i j d k l m e b sk lp lm lt ma lu ril sy dv lil cav lh ls lfe ga fu dr rc f Figure 3 | Selected skeletal elements and associated feathers of LPMB00169. a, Skull and mandible. b, Middle caudal vertebrae. c, Furcula and right scapulocoracoid. d, Left forelimb. e, Right forelimb. f, Left hindlimb. g, Right pes. h, Feathers near skull. i, Feathers near pectoral region. j, Distalmost primary remiges. k, Middle primary remiges. l, Secondary primary remiges. m, Pennaceous feathers attached to metatarsus. Arrows indicate the boundary of the soft tissue. Scale bars: a, b, d–g, 2 cm; c, 1 cm; h, k, l, 2 mm in; i, j, m, 1 mm. lfi lr cev lis pu rs rfe rt f rp rr f rh ru rm Figure 2 | Anchiornis huxleyi LPM-B00169. a, Photograph and b, line drawing of LPM-B00169 A (slab). Abbreviations: cav, caudal vertebra; cev, cervical vertebra; dr, dorsal rib; dv, dorsal vertebra; f, feather; fu, furcula; ga, gastralia; lfe, left femur; lfi, left fibula; lh, left humerus; lil, left ilium; lis, left ischium; lm, left manus; lp left pes; lr, left radius; ls, left scapula; lt, left tibiotarsus; lu, left ulna; ma, mandible; pu, pubis; rc, right coracoid; rfe, right femur; rh, right humerus; ril, right ilium; rm, right manus; rp, right pes; rr, right radius; rs, right scapula; rt, right tibiotarsus; ru, right ulna; sk, skull; sy, synsacrum. Scale bar, 5 cm. process located close to the midpoint of the ischial shaft as in the dromaeosaurid Buitreraptor10. As in Mei and some dromaeosaurids11, the distal articulation of metatarsal II is about as wide as that of metatarsal III. There are about ten large pennaceous feathers attached to the forearm, 11 to the manus (Fig. 3d, e), 12–13 to the crus (Fig. 3f) and 10–11 to the metatarsus (Fig. 3g). The primary and secondary remiges are similar in size and morphology (Fig. 3j–l). The longest remiges, located near the distal end of the forearm and the proximal end of the manus, are about 150% of the humeral length. Because the longest wing feathers are close to the wrist, the broadest part of the wing is relatively proximal, in contrast to the basal dromaeosaurid Microraptor and basal avians such as Archaeopteryx12. The distal primary remiges resemble those of Microraptor and basal avians4,12,13 in having curved rachides, but the remiges are relatively small, with thin rachides, symmetrical vanes, and blunt ends. In Microraptor and basal avians12, the primary remiges are not only significantly longer than the secondary ones but also possess prominent rachides, asymmetrical vanes and somewhat pointed tips. Large pennaceous feathers also cover nearly the whole length of the lower leg of Anchiornis (Fig. 3m). The crural feathers are longer than the metatarsal feathers, which are nearly perpendicular to the long axis of the metatarsus. Much shorter feathers also attach to the pedal phalanges, apart from the unguals. These feathers appear to be pennaceous, a condition previously unknown in any fossil taxon. Two types of plumulaceous feather can be distinguished, corresponding to types previously identified in the dromaeosaurid Sinornithosaurus14. Feathers of the first type are each composed of a bundle of filaments that are joined together proximally and remain nearly parallel as they pass distally (Fig. 3h). Feathers of the second type each consist of a series of filaments branching laterally from a slender central rachial filament (Fig. 3i). Anchiornis huxleyi is posited as a basal troodontid by our phylogenetic analysis (Fig. 4) but also possesses several salient features of the Avialae and Dromaeosauridae, further blurring distinctions among the three major paravian groups (Supplementary Information). In particular, the forelimbs of Anchiornis are proportionally much longer than those of other troodontids, but similar in length to those of basal avialans and dromaeosaurids. Anchiornis huxleyi even exceeds Microraptor in the length of the forelimbs3, a feature often 641 ©2009 Macmillan Publishers Limited. All rights reserved LETTERS Aptian 121 Barremian Hauterivian Valanginian Berriasian 144 Kimmeridgian Middle Jurassic Oxfordian 159 Callovian Bathonian Bajocian Aalenian 190 Other avians Coelophysoidea Late Tithonian Scansoriopterygidae Archaeopteryx Early Albian Mei long 99 Sinovenator changii Cretaceous Cenomanian Anchiornis huxleyi Santonian Coniacian Turonian Compsognathidae Late Campanian Ornitholestes hermanni Basal tetanurans Maastrichtian Other troodontids Dromaeosauridae Therizinosauroidae Alvarezsauroidea Oviraptorosauria Ceratosauria Tyrannosauroidea Ornithomimosauria NATURE | Vol 461 | 1 October 2009 Early Toarcian Pliensbachian Sinemurian Late Triassic Hettangian Rhaetian 206 Norian Carnian 227 Figure 4 | Temporally calibrated phylogeny of the Theropoda. (See Supplementary Information for details.) The known temporal durations (solid bars) of the major theropod groups, based on well-corroborated fossil occurrences, indicate that the major tetanuran theropod groups diverged rapidly in the Middle Jurassic to earliest Late Jurassic. regarded as an indicator of aerial capability. However, the remiges of Anchiornis are not obviously flight-adapted as in Microraptor and basal avians12. Furthermore, the extreme elongation of the lower legs in Anchiornis huxleyi suggests strong cursorial capability3, but their long and extensive plumage is not common among cursorial animals: in cursorial birds and mammals, the lower legs tend to show reduction or even complete loss of the feathers or hair, respectively. Similarly, the recently reported Jurassic basal avialan Epidexipteryx hui closely resembles basal birds in various skeletal features usually interpreted as being related to aerial capability, but lacks pennaceous feathers that would facilitate aerial locomotion15. Collectively, these data point to a complex pattern of morphological evolution at the base of the Paraves. The distribution of large pennaceous feathers, both phylogenetic and anatomical, implies that these structures first evolved on the distal portions of the forelimbs and tail in maniraptoran theropods and only spread proximally at a subsequent stage in theropod evolution12. Interestingly, such a distal-first pattern seems also to apply to the evolution of pennaceous feathers on the hindlimbs of paravians. Large pennaceous feathers are now known to occur on the lower leg and particularly the metatarsus of at least one basal member of each of the three major paravian groups, namely the basal troodontid Anchiornis, the basal avialan Pedopenna and the basal dromaeosaurid Microraptor13,16. Furthermore, many basal avians have proportionally large pennaceous feathers on the lower leg13,17, which are reduced in more derived birds. This suggests that large pennaceous feathers first evolved distally on the hindlimbs, as on the forelimbs and tail. This distal-first development led to a four-winged condition at the base of the Paraves. Whereas the large feathers of the forewing developed further in subsequent avian evolution, the large hindwing feathers were reduced and even lost12. This suggests that extensive feathering of the pes was a critical modification in the transition to birds and that the pedal scales of extant birds might be secondarily derived structures, a possibility also supported by some developmental studies18. Extensive feathering of the pes is also seen in some modern birds, and serves an insulating or protective function19. In most cases the feathers are not organized into a coherent planar surface as in Microraptor, Pedopenna and Anchiornis20, which indicates that the pedal feathers of these fossil taxa may have differed from those of extant birds in having an aerodynamic function. This would imply that a four-winged condition played a role in the origin of avian flight, as suggested by previous studies12,17, although this conclusion is not universally accepted21. However, the significant differences noted above between the large pedal feathers of Anchiornis and those of Microraptor suggest that these feathers might have been less aerodynamically effective in Anchiornis than in Microraptor. The poor fossil record of derived non-avialan theropods has hindered understanding of early coelurosaurian theropod evolution, and has created an apparent discrepancy between stratigraphy and phylogeny that has sometimes been used to argue against the theropod hypothesis of bird origins1. Although derived theropods including troodontids have been reported in the Jurassic, all have been based on fragmentary material22–25. Anchiornis huxleyi is probably Oxfordian in age, and unquestionably represents the oldest troodontid reported so far7. The presence of a troodontid in the earliest Late Jurassic indicates that all groups of derived theropods had originated by this time. A calibrated theropod phylogeny based only on well-corroborated fossil occurrences suggests that all major tetanuran groups, including Aves, might have originated and diversified rapidly in the Middle to earliest Late Jurassic (Fig. 4). This rapid divergence event would have coincided with documented palaeogeographical changes that took place around the same time. Alternatively, a calibrated theropod phylogeny incorporating fragmentary material suggests that tetanurans have a much longer evolutionary history, and that great potential exists for discovering derived theropod fossils, even in the Triassic24. Received 29 April; accepted 27 July 2009. 1. Feduccia, A. Birds are dinosaurs: simple answer to a complex problem. Auk 119, 1187–1201 (2002). 2. Xu, K. et al. Jurassic System in the North of China (VII): The Stratigraphic Region of Northeast China (Petroleum Industry Press, 2003). 3. Xu, X. et al. A new feathered maniraptoran dinosaur fossil that fills a morphological gap in avian origin. Chin. Sci. Bull. 54, 430–435 (2009). 4. Wellnhofer, P. Archaeopteryx—Der urvogel von Solnhofen (Friedrich Pfeil, 2008). 5. Xu, X. & Norell, M. A. A new troodontid from China with avian-like sleeping posture. Nature 431, 838–841 (2004). 6. Norell, M. A. & Makovicky, P. J. in The Dinosauria 2nd edn (eds Weishampel, D. B., Dodson, P. & Osmolska, H.) 196–209 (Univ. California Press, 2004). 7. Makovicky, P. J. & Norell, M. A. in The Dinosauria 2nd edn (eds Weishampel, D. B., Dodson, P., Osmolska, H.) 184–195 (Univ. California Press, 2004). 8. Makovicky, P. J., Norell, M. A., Clark, J. M. & Rowe, T. Osteology and relationships of Byronosaurus jaffei (Theropda: Troodontidae). Am. Mus. Novit. 3402, 1–32 (2003). 9. Currie, P. J. Bird-like characteristics of the jaws and teeth of troodontid theropods (Dinosauria: Saurischia). J. Vert. Paleontol. 7, 72–81 (1987). 10. Makovicky, P. J. Apesteguı́a, S. & Agnolı́n, F. L. The earliest dromaeosaurid theropod from South America. Nature 437, 1007–1011 (2005). 11. Xu, X. & Wang, X.-L. A new dromaeosaur (Dinosauria: Theropoda) from the Early Cretaceous Yixian Formation of western Liaoning. Vert. PalAsia. 42, 111–119 (2004). 12. Xu, X. et al. Four-winged dinosaurs from China. Nature 421, 335–340 (2003). 642 ©2009 Macmillan Publishers Limited. All rights reserved LETTERS NATURE | Vol 461 | 1 October 2009 13. Zhang, F.-C. & Zhou, Z.-H. Leg feathers in an Early Cretaceous bird. Nature 431, 925 (2004). 14. Xu, X., Zhou, Z.-H. & Prum, R. O. Branched integumental structures in Sinornithosaurus and the origin of feathers. Nature 410, 200–204 (2001). 15. Zhang, F.-C., Zhou, Z.-H., Xu, X., Wang, X.-L. & Sullivan, C. A bizarre Jurassic maniraptoran from China with elongate ribbon-like feathers. Nature 455, 1105–1108 (2008). 16. Xu, X. & Zhang, F.-C. A new maniraptoran with long metatarsalian feathers from China. Naturwissenschaften 92, 173–177 (2005). 17. Longrich, N. R. Structure and function of hindlimb feathers in Archaeopteryx lithographica. Paleobiology 32, 417–431 (2006). 18. Sawyer, R. H. & Knapp, L. W. Avian skin development and the evolutionary origin of feathers. J. Exp. Zool. 298B, 57–72 (2003). 19. Weidensaul, S. Raptors—The Birds of Prey (Lyons & Burford, 1995). 20. Xu,X.etal.Originofflight:couldfour-wingeddinosaursfly?Nature438,E3–E4(2005). 21. Padian, K. Four-winged dinosaurs, bird precursors, or neither? Bioscience 53, 450–452 (2003). 22. Jensen, J. A. & Padian, K. Small pterosaurs and dinosaurs from the Uncompahgre Fauna (Brushy Basin Member, Morrison Formation: ?Tithonian), Late Jurassic, western Colorado. J. Paleontol. 63, 364–373 (1989). 23. Chure, D. J. Koparion douglassi, a new dinosaur from the Morrison Formation (Upper Jurassic) of Dinosaur National Monument: the oldest troodontid (Theropoda: Maniraptora). Brigham Young Univ. Geol. Stud. 40, 11–15 (1994). 24. Xu, X., Zhao, X.-J. & Clark, J. M. A new therizinosaur from the Lower Jurassic Lufeng Formation of Yunnan, China. J. Vert. Paleontol. 21, 477–483 (2001). 25. Evans, S. E. & Milner, A. R. in In the Shadow of the Dinosaurs (eds Fraser, N. C. & Sues, H.-D.) 303–321 (Cambridge Univ. Press, 1985). Supplementary Information is linked to the online version of the paper at www.nature.com/nature. Acknowledgements We thank S. Zheng for help with the fieldwork, T. Yu for preparing the specimen, C. Sullivan for editing and commenting on the manuscript, G. Sun, P. Cheng and F. Jin for discussions and comments, and J. Huang for Supplementary Fig. 4i. The fieldwork was supported by grants from the Education Bureau of Liaoning Province (numbers 20060805 and 2008S214) and the Special Fund of Shenyang Normal University. This study was also supported by grants to X.X. from the Chinese Academy of Sciences, the National Natural Science Foundation of China, and Major Basic Research Projects of the Ministry of Science and Technology, China. Author Contributions D.-Y.H and X.X. designed the project. D.-Y.H., X.X., L.-H.H and L.-J.Z. performed the research. X.X. and D.-Y.H. wrote the manuscript. Author Information Reprints and permissions information is available at www.nature.com/reprints. Correspondence and requests for materials should be addressed to X.X. (xingxu@vip.sina.com) or D.-Y.H. (hudongyu@synu.edu.cn). 643 ©2009 Macmillan Publishers Limited. All rights reserved