The asymmetry of the carpal joint and the evolution of wing folding in maniraptoran theropod dinosaurs

Abstract

In extant birds, the hand is permanently abducted towards the ulna, and the wrist joint can bend extensively 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 convexity 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 (15 degrees) in primitive coelurosaurs but considerably larger (25 degrees) in primitive maniraptorans, indicating that the radiale was more wedge-shaped and the carpal joint more asymmetric. The radiale angle progressively 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.

Figure 1.

Left distal forelimb of a turkey, Meleagris gallopavo (IVPP 1222): (a) wrist in minimum abduction; (b) wrist in maximum 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 carpometacarpal surface shown in (c). Note that measuring with respect to the palmar part of carpometacarpal surface would result in even larger radiale angle.

Figure 2.

Evolution of wrist structure and the radiale angle in tetanuran theropods, based on simplified tetanuran phylogeny after Smith et al. (2007) and Zanno et al. (2009). Numbers indicate values of radiale angle between proximal and distal articular surfaces of radiale, in degrees. Values in bold are direct measurements of individual taxa; values in normal italic type are reconstructed ancestral states. See table 1 and electronic supplementary material, figure S1 for full list of measurements used as the basis for reconstructing ancestral states. Wrist drawings show positions close to zero abduction (Guanlong, Alxasaurus, Deinonychus) or minimum abduction (Caudipteryx, Eoconfuciusornis). II–IV, metacarpals II–IV (numbering convention follows extant birds); d, distal carpal; i, intermedium; R, radius; r, radiale; s, semilunate carpal; U, ulna; u, ulnare. Scale bars: 0.25 cm in Eoconfuciusornis, 0.50 cm in Caudipteryx, 1.00 cm in all other taxa.

Figure 3.

Effect of abduction through angle of 60° in the dromaeosaurid Microraptor gui: (a) whole-body reconstruction showing the position of the left-hand relative to the body in straight (black) and abducted (grey) configurations; (b) left wrist in anatomically dorsal view, showing carpus in straight (left) and abducted (right) configurations. Abbreviations as in figure 2. Image modified from Hu et al. (2009).