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We acknowledge GSECARS, APS, and ANL for the use of the synchrotron and laser facilities and the High Pressure Collaborative Access Team for the use of the ruby system. We thank F. de Groot, J.-P. Rueff, W. Sturhahn, T. Tsuchiya, and W. J. Evans for helpful discussions and G. Shen, M. Hu, and K. Visbeck for their assistance in the experiments. Use of the APS was supported by U.S. Department of Energy (DOE), Office of Science, Basic Energy Sciences, under contract DE-AC02-06CH11357. GSECARS is supported by NSF Earth Sciences (EAR- 0622171) and DOE Geosciences (DE-FG02-94ER14466). This work at LLNL was performed under the auspices of the U.S. DOE by University of California and LLNL under contract W-7405-Eng-48. J.-F.L. is also supported by the Lawrence Livermore Fellowship. S.D.J. acknowledges financial support from NSF/EAR 0721449, and V.V.S. acknowledges financial support from DOE. Supporting Online Material www.sciencemag.org/cgi/content/full/317/5845/1740/DC1 Materials and Methods Figs. S1 to S3 References 11 May 2007; accepted 24 July 2007 10.1126/science.1144997 The Primitive Wrist of Homo floresiensis and Its Implications for Hominin Evolution Matthew W. Tocheri,1* Caley M. Orr,2,3 Susan G. Larson,4 Thomas Sutikna,5 Jatmiko,5 E. Wahyu Saptomo,5 Rokus Awe Due,5 Tony Djubiantono,5 Michael J. Morwood,6 William L. Jungers4 Whether the Late Pleistocene hominin fossils from Flores, Indonesia, represent a new species, Homo floresiensis, or pathological modern humans has been debated. Analysis of three wrist bones from the holotype specimen (LB1) shows that it retains wrist morphology that is primitive for the African ape-human clade. In contrast, Neandertals and modern humans share derived wrist morphology that forms during embryogenesis, which diminishes the probability that pathology could result in the normal primitive state. This evidence indicates that LB1 is not a modern human with an undiagnosed pathology or growth defect; rather, it represents a species descended from a hominin ancestor that branched off before the origin of the clade that includes modern humans, Neandertals, and their last common ancestor. The debate over the affinity of the LatePleistocene hominin fossils from theisland of Flores has focused primarily on the craniodental remains of the first specimen (LB1) recovered from Liang Bua cave (1?6). LB1 is the holotype specimen of a new species, Homo floresiensis (1, 7), but some argue that it is a pathological modern human (4, 6). Here we examine the morphology of three wrist bones attributed to LB1 to test these competing hypotheses. Wrist morphology can be a powerful indi- cator of phylogenetic relationships in Mammalia because of variation in the number and shape of carpal elements and in the configuration of the articular surfaces (8?12). In primates, the trape- zoid is the wrist bone situated directly proximal to the index finger. The modern human trapezoid is shaped like a boot (9, 13, 14), wherein the palmar half of the bone is radio-ulnarly and proximo-distally wide (Fig. 1). In contrast, other primates have a trapezoid that is more wedge- shaped with a narrow palmar tip and a wide dorsal base (9, 13?15). This difference between human and nonhuman primate trapezoid shape is concomitantly reflected by the shapes and articular configurations of the carpals that artic- ulate with the trapezoid, and all of these carpals are derived in modern humans in comparison to those in other primates (Figs. 2 and 3) (9, 13). Upper PaleolithicHomo sapiens and Neandertals share these derived morphological features with modern humans, suggesting that they are most likely inherited from a recent common ancestor (13). A capitate attributed to Homo antecessor (16) and dated to ~0.8 million years ago (Ma) (17) also shares the derived condition (13, 16). Thus, the current paleontological evidence sug- gests that this complex of wrist features evolved by at least 800,000 years ago. Three complete carpals?a trapezoid, scaph- oid, and capitate?all of which are from a left wrist, were recovered along with the cranium, mandible, and additional postcranial material of LB1 in Spit No. 59 of Sector VII during the September 2003 excavation (fig. S1 and table S3) (1, 2, 18). Each is well preserved and shows no signs of pathology or abnormal development. As shown in Figs. 1 to 3, these three articulating bones display none of the shared, derived fea- tures of modern human and Neandertal carpals (13). Instead, they show the general symplesio- morphic pattern exhibited by all extant African apes, as well as fossil hominins that preserve comparable wrist morphology and date before 1.7 Ma (13, 19?22). Like other nonhuman pri- mates, LB1?s trapezoid is (i) wedge-shaped; (ii) the ulnar side of its second metacarpal articula- tion is oriented more sagittally (Fig. 1, top and bottom rows); (iii) its scaphoid articular surface is more triangular in shape (Fig. 1, middle row); and (iv) it lacks the expanded palmar non- articular area (Fig. 1, top row) and the more palmarly placed capitate articulation observed in modern humans and Neandertals (Fig. 1, bottom row). We quantified these shape differ- ences using three-dimensional (3D) methods measuring the relative areas and angles of carpal articular surfaces (13, 14, 18, 23). Multivariate statistical analysis of these data distinguishes modern humans and Neandertals from the great apes, Papio, and LB1 (Fig. 1). Primarily, the trapezoids of modern humans and Neandertals are distinct in their shape and articular con- figuration as a consequence of the large expan- sion of palmar nonarticular area, which tends to square off the entire palmar half of the bone (Fig. 1, top row) (13). The scaphoid and capitate of LB1 both exhibit the shapes and articular configurations that occur concomitantly with the primitive hominid trapezoid condition (13, 18), and mul- tivariate analyses of these carpals provide similar results (Figs. 2 and 3). For example, LB1?s capi- tate lacks the enlarged palmarly placed articular surface for the trapezoid observed in modern humans and Neandertals (9, 13) and, instead, shows the waisted neck characteristic of extant 1Human Origins Program, Department of Anthropology, National Museum of Natural History, Smithsonian Institu- tion, Washington, DC 20013, USA. 2School of Human Evolution and Social Change, Arizona State University, AZ 85287, USA. 3Institute of Human Origins, Arizona State University, AZ 85287, USA. 4Department of Anatomical Sci- ences, School of Medicine, Stony Brook University, NY 11794, USA. 5The National Research and Development Centre for Archaeology, Jakarta, Indonesia. 6School of Earth and Environmental Sciences, University of Wollongong, NSW 2522, Australia. *To whom correspondence should be addressed. E-mail: tocherim@si.edu www.sciencemag.org SCIENCE VOL 317 21 SEPTEMBER 2007 1743 REPORTS o n S ep te m be r 2 0, 2 00 7 w w w .s ci en ce m ag .o rg D ow nl oa de d fro m great apes and Australopithecus (Fig. 3, middle row) (20). Similarly, the articular surface for the trapezium on LB1?s scaphoid does not extend out onto the scaphoid tubercle as it does in modern humans and Neandertals (Fig. 2, middle row) (13). However, LB1?s scaphoid includes a fused centrale, as does the OH7 scaphoid fromOlduvai Gorge (Fig. 2) (21, 24). Congenital fusion of these two carpal elements is a synapomorphy of Gorilla, Pan, and Homo (25), and the fossil evidence from LB1 and OH7 further indicates that fusion is the most likely primitive condition for all hominins. The consistent carpal shape differences be- tween human and nonhuman primates are the result of differences in the cavitation of the carpal mesenchyme during embryonic development (18, 26). In modern humans, the trapezoid, capitate, and trapezium arise in the mesenchyme in essentially their adult form by the 11th week of development, long before the processes of chondrification and ossification are complete, and the remaining carpal elements achieve their distinctive shapes shortly thereafter (26). Because of the timing of carpal formation, dysostoses (i.e., errors in cell patterning) or disruptions (i.e., through exposure to toxic substances or infec- tion) may result in malformation of the initial carpal shape (27, 28). However, the transient characteristics of such disturbances most often produce localized skeletal shape abnormalities (e.g., individual bones are affected) that are not typically associated with skeletal dwarfism (27, 28). In contrast, dysplasias usually involve systemic errors in ossification and growth, fre- quently resulting in dwarfism (27, 28). The genes that result in dysplasias, however, do not nor- mally become expressed until after normal shape formation of the carpal mesenchyme (27). Al- though skeletal dysplasias may include carpal and digit abnormalities related to ossification errors, as well as various forms of microcephaly (27), none are known to result in abnormal carpal morphology that closely mimics a plesiomorphic state. Our diverse modern human sample in- cludes a pituitary dwarf (USNM 314306) and a Fig. 1. (Top) Palmar (top row), proximal (middle row), and ulnar views (bottom row) of trapezoid morphology (the distal, palmar, and distal borders, respectively, shown toward the page top). All bones are scaled to approximately the same size and shown as from the left wrist. Articular surfaces are as follows: 2nd metacarpal (radial side), yellow; 2nd metacarpal (ulnar side), dark blue; capitate, green; trapezium, light blue; scaphoid, medium blue; nonarticular, pink. (Bottom) Plots of the canonical variables (CAN1 to CAN3) generated from 3D trapezoid shape analysis (13, 14, 18). CAN1 accounts for 76% of the variation, CAN2 accounts for 14%, and CAN3 8% (modern humans, open squares; Pan, closed triangles; Gorilla, open diamonds; Pongo, closed circles; Papio, X?s; Upper Paleo- lithic H. sapiens (e.g., Qafzeh 9), blue squares (UP); Neandertals (e.g., Kebara 2), red squares (N); modern human pituitary dwarf, yellow square (D); modern human pituitary giant, yellow square (G); H. floresiensis (LB1), green square (F). Fig. 2. (Top) Radial (top row), distal (middle row), and ulnar views (bottom row) of scaphoid morphology (the distal, palmar, and distal borders, respectively, shown toward the page top). All bones are scaled to approximately the same size and shown as from the left wrist. Regourdou 1 is a Neandertal. Articular surfaces are as follows: radius, dark blue; trapezium-trapezoid, light blue; capitate, medium blue; lunate, green; nonarticular, pink. (Bottom left) Plot of the canonical variables (CAN1, CAN2) generated from 3D scaphoid shape analysis (13, 18). CAN1 accounts for 89% of the variation, CAN2 accounts for 11% [symbols as in Fig. 1 plus H. habilis (OH7), brown square (O)]. (Bottom right) The separate centrale (the primitive condition in primates) is shown articulated with the scaphoid in Pongo. 21 SEPTEMBER 2007 VOL 317 SCIENCE www.sciencemag.org1744 REPORTS o n S ep te m be r 2 0, 2 00 7 w w w .s ci en ce m ag .o rg D ow nl oa de d fro m pituitary giant (USNM 227508) (tables S1 and S2). Both show normal modern human carpal shapes and articular configurations despite their abnormal sizes, demonstrating that LB1?s wrist morphology is not the result of allometric scal- ing, errors in metabolism, or a skeletal growth disorder. Our analyses support hypotheses that LB1 is descended from a hominin ancestor that migrated out of Africa before the evolution of the shared, derived wrist morphology that is characteristic of modern humans, Neandertals, and their last common ancestor. The associa- tion of LB1 with direct evidence of stone flaking technology comparable to that found at Oldowan or other Lower Paleolithic sites throughout the Old World (29) provides additional support for the hypothesis that the earliest hominins to use and make stone tools retained primitive hominin wrist morphology (13, 21, 30, 31). The structurally modified wrist of modern humans and Neandertals probably evolved sometime between 1.8 and 0.8 Ma (13). These structural modifications form a morphological complex that may represent an adaptation for better distribution of forces radio-ulnarly across the wrist to facilitate the full commitment to tool-related manipulative behaviors that arose in the hominin lineage leading to modern humans and Neandertals (13). The wrist morphology of LB1may ultimately help falsify or support specific hypotheses re- garding the phylogenetic position of H. flor- esiensis (1, 5, 7). Unfortunately, no carpals are attributed to Homo erectus sensu lato, which is otherwise well represented in the fossil record between 1.8 and 0.8 Ma, with the exception of a partial lunate from Zhoukoudian (32). However, if hominin carpals that date within this period of time are discovered, their primitive or derived morphology will allow a firmer assessment of their phylogenetic relationship to other Pleisto- cene hominin species, such as modernH. sapiens and H. floresiensis. References and Notes 1. P. 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Wood, Evol. Anthropol. 11, 235 (2002). 31. S. Semaw et al., Nature 385, 333 (1997). 32. F. Weidenreich, Paleontol. Sin. Ser. D 5, 1 (1941). 33. We thank the people and staff of the National Research and Development Centre for Archaeology (formerly the Indonesian Centre for Archaeology) for their kind and continuing assistance in the field and lab; L. Cornish for conservation efforts on the Flores hominins funded by the Wenner-Gren Foundation; R. Potts, D. Ortner, C. Tryon, B. Pobiner, K. Kovarvic, C. Campisano, J. Clark, B. Frohlich, J. Yellen, A. Brooks, C. Ward, J. Hodgkins, L. Delezene, J. Scott, and M. Nargowalla for thoughtful discussions; and D. Hunt, L. Gordon, R. Thorington, B. Latimer, L. Jellema, E. Gilissen, W. Wendelen, B. Kimbel, D. Johanson, and E. Trinkaus for access to comparative material. Additional thanks to M. Marzke, R. Williams, A. Razdan, J. Femiani, G. Farin, D. Collins, and the Partnership for Research In Spatial Modeling (PRISM) at Arizona State University (ASU). Aspects of this research were supported in part by NSF [grant IIS-998016 to A. Razdan (ASU), grant BCS-0218511 to R. Potts (Smithsonian)], a Social Sciences and Humanities Research Council of Canada Doctoral Fellowship (award 752-2002-0432 to M.W.T.), a Smithsonian Institution Predoctoral Fellowship (M.W.T.), a Discovery Project Grant from the Australian Research Council (M.J.M.), and grants from the University of New England (M.J.M.). Additional support from the School of Human Evolution and Social Change at ASU, the Leakey Foundation, the National Geographic Society, and the Human Origins Program and Department of Anthropology at the Smithsonian Institution National Museum of Natural History is also greatly appreciated. Supporting Online Material www.sciencemag.org/cgi/content/full/317/5845/1743/DC1 SOM Text Fig. S1 Tables S1 to S11 References 28 June 2007; accepted 15 August 2007 10.1126/science.1147143 Fig. 3. (Top): Palmar (top row), radial (middle row), and distal views (bottom row) of capitate morphology (the distal, distal, and palmar borders, respectively, shown toward the page top). All bones are scaled to approximately the same size and shown as from the left wrist. Articular surfaces as follows: trapezoid, dark blue; scaphoid-lunate, light blue; 3rd metacarpal, medium blue; 2nd metacarpal, green; nonarticular, pink. (Bottom) Plots of the canonical variables (CAN1 to CAN3) generated from 3D capitate shape analysis (18). CAN1 accounts for 86% of the variation, CAN2 accounts for 13%, and CAN3 1% [symbols as in Fig. 1 plus A. africanus (TM1526), orange square (A); A. afarensis (AL333-40 and AL288-1w), brown squares (A)]. www.sciencemag.org SCIENCE VOL 317 21 SEPTEMBER 2007 1745 REPORTS o n S ep te m be r 2 0, 2 00 7 w w w .s ci en ce m ag .o rg D ow nl oa de d fro m