Downloaded from rspb.royalsocietypublishing.org on March 3, 2010 The asymmetry of the carpal joint and the evolution of wing folding in maniraptoran theropod dinosaurs Corwin Sullivan, David W. E. Hone, Xing Xu and Fucheng Zhang Proc. R. Soc. B published online 3 March 2010 doi: 10.1098/rspb.2009.2281 Supplementary data "Data Supplement" http://rspb.royalsocietypublishing.org/content/suppl/2010/02/24/rspb.2009.2281.DC1.h tml References This article cites 27 articles, 4 of which can be accessed free http://rspb.royalsocietypublishing.org/content/early/2010/02/24/rspb.2009.2281.full.ht ml#ref-list-1 P<P Published online 3 March 2010 in advance of the print journal. Subject collections Articles on similar topics can be found in the following collections palaeontology (45 articles) evolution (1465 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here Advance online articles have been peer reviewed and accepted for publication but have not yet appeared in the paper journal (edited, typeset versions may be posted when available prior to final publication). Advance online articles are citable and establish publication priority; they are indexed by PubMed from initial publication. Citations to Advance online articles must include the digital object identifier (DOIs) and date of initial publication. To subscribe to Proc. R. Soc. B go to: http://rspb.royalsocietypublishing.org/subscriptions This journal is © 2010 The Royal Society Downloaded from rspb.royalsocietypublishing.org on March 3, 2010 Proc. R. Soc. B doi:10.1098/rspb.2009.2281 Published online The asymmetry of the carpal joint and the evolution of wing folding in maniraptoran theropod dinosaurs Corwin Sullivan*, David W. E. Hone, Xing Xu and Fucheng Zhang Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Palaeontology and Palaeoanthropology, Chinese Academy of Sciences, 142 Xiwai Street, Beijing 100044, People’s Republic of China In extant birds, the hand is permanently abducted towards the ulna, and the wrist joint can bend exten- sively in this direction to fold the wing when not in use. Anatomically, this asymmetric mobility of the wrist results from the wedge-like shape of one carpal bone, the radiale, and from the well-developed con- vexity of the trochlea at the proximal end of the carpometacarpus. Among the theropod precursors of birds, a strongly convex trochlea is characteristic of Coelurosauria, a clade including the highly derived Maniraptora in addition to tyrannosaurs and compsognathids. The shape of the radiale can be quantified using a ‘radiale angle’ between the proximal and distal articular surfaces. Measurement of the radiale angle and reconstruction of ancestral states using squared-change parsimony shows that the angle was small (158) in primitive coelurosaurs but considerably larger (258) in primitive maniraptorans, indicating that the radiale was more wedge-shaped and the carpal joint more asymmetric. The radiale angle pro- gressively increased still further within Maniraptora, with concurrent elongation of the forelimb feathers and the forelimb itself. Carpal asymmetry would have permitted avian-like folding of the forelimb in order to protect the plumage, an early advantage of the flexible, asymmetric wrist inherited by birds. Keywords: Theropoda; Maniraptora; Aves; carpus; radiale; feathers 1. INTRODUCTION been explicitly inferred in at least some advanced thero- Extant volant birds possess a highly specialized wrist joint, pods, including the dromaeosaurid Deinonychus (Senter in which two proximal carpals articulate with a fused car- 2006), and has often been tacitly assumed in discussions pometacarpus. The proximal part of the carpometacarpus of forelimb evolution on the line to birds. For example, forms an articular trochlea, comprising two convex ridges Padian (e.g. 1985, fig. 3a) has repeatedly presented separated by a transverse groove, and is largely homolo- reconstructions of the predatory strike of a dromaeo- gous to the structurally similar semilunate carpal (SLC) saurid theropod that begin with the manus in a position of derived non-avian theropods (Ostrom 1976). Taxa of considerable abduction and end with the manus and with a well-developed SLC would have been distin- antebrachium aligned. However, as acknowledged by guished by a wrist with enhanced flexibility in the plane Padian (2001), the functional advantage of beginning of the radius and ulna, a characteristic inherited by the predatory strike with the wrist deflected in this crown-group birds (following Gauthier (1986) we use manner has never been fully elucidated. By contrast, Aves for this crown-group, and Avialae for the larger, Sereno & Rao (1992) argued that Archaeopteryx and stem-based clade containing all maniraptorans closer to non-avialan theropods were in fact limited in their ability Aves than to dromaeosaurids). The mobility of the wrist to abduct the wrist joint, at least in comparison with contributes to the ability of a flapping bird to partly fold extant birds and some derived Mesozoic ones. Despite the wing during the upstroke, greatly improving flight effi- these differing opinions, the anatomical basis of wrist ciency (Vazquez 1992), and also permits the wing to be asymmetry in derived theropods has been little discussed. completely folded when not in use. Keeping the wing The issue of wrist asymmetry has become particularly folded can make a bird less conspicuous, protect the pertinent following the discovery of numerous non-avia- feathers from damage, and prevent the wing from inter- lan dinosaur specimens, mainly from the Jehol Group of fering with terrestrial locomotion. China (Xu & Norell 2006) that preserve feathers or Avian wing-folding is a biologically important behav- feather-like integumentary structures. For brevity, all iour that depends on a highly flexible wrist joint. such structures are referred to as feathers in this paper. However, this flexibility is exclusively in the ulnar direc- Some dromaeosaurid, troodontid, oviraptorosaur and tion (figure 1), and the typical avian manus is therizinosaur specimens show the presence of what we permanently abducted towards the ulna (Ostrom 1976). term a ‘pennibrachium’, a forelimb bearing long feathers A similar asymmetry in the flexibility of the wrist has that form a planar, wing-like surface but are not necess- arily used in aerial locomotion. For example, a pennibrachium could have been used by a non-volant * Author for correspondence ([email protected]). theropod in wing-assisted incline running (Dial 2003) Electronic supplementary material is available at http://dx.doi.org/10. or as a display structure. It is possible that pennibrachia 1098/rspb.2009.2281 or via http://rspb.royalsocietypublishing.org. were widespread or even predominant among derived Received 11 December 2009 Accepted 11 February 2010 1 This journal is q 2010 The Royal Society Downloaded from rspb.royalsocietypublishing.org on March 3, 2010 2 C. Sullivan et al. Evolution of theropod carpal asymmetry ulna carpometacarpus (a) cuneiform 5° radius radiale (c) 59° sc posterior 5 cm su distal sr (b) 1 cm 123° Figure 1. Left distal forelimb of a turkey, Meleagris gallopavo (IVPP 1222): (a) wrist in minimum abduction; (b) wrist in maxi- mum abduction; and (c) radiale. All views are dorsal. sc, articular surface for carpometacarpus; sr, articular surface for radius; su, articular surface for ulna. Angle of abduction shown in (a,b), radiale angle between ulnar surface and dorsal part of carpo- metacarpal surface shown in (c). Note that measuring with respect to the palmar part of carpometacarpal surface would result in even larger radiale angle. non-avialan theropods, despite the fact that direct fossil Table 1. Radiale angles in various theropods. (Bold evidence is limited to a few Lagerstatte. Any theropod indicates specimens that we examined directly.) with both a pennibrachium and an avian-like capacity for extensive wrist abduction would have been able to taxon angle specimen/source fold the pennibrachium during terrestrial locomotion, Allosaurus fragilis 2 Chure (2001, fig. 2c) presumably realizing benefits analogous to those of 8 Huaxiagnathus 188 Hwang et al. (2004, fig. 8a) wing-folding in modern birds. orientalis In the present paper we review the features of the Sinosauropteryx 68 Currie & Chen (2001, fig. 8a) avian carpus that facilitate a large range of abduction, prima and investigate the distribution of similar features Guanlong wucaii 88 IVPP V14531 among non-avialan theropods. Finally, we place these Alxasaurus 398 IVPP RV93001 results in phylogenetic context to trace the evolution of elesitaiensis the distinctive avian carpal configuration through incipi- Falcarius utahensis 268 Utah Museum of Natural ent stages prior to the origin of birds, and discuss History, Salt Lake City, implications for the evolution of the forelimb and of USA (UMNH) VP 12294 powered flight. Caudipteryx sp. 768 IVPP V12430 Haplocheirus 158 IVPP V15988 Sinovenator changii 358 IVPP V14009 Deinonychus 318 YPM 5208 2. MATERIAL AND METHODS antirrhopus The structure of the carpus was examined in several manirap- Eoconfuciusornis 558 IVPP V11977 toran and non-maniraptoran tetanuran theropods. Some zhengi specimens were studied firsthand, but in other cases we Meleagris gallopavo 598 IVPP 1222 relied on photographs or published descriptions (table 1). We use the terms adduction and abduction rather than extension and