Unusual pectoral apparatus in a predatory dinosaur resolves avian wishbone homology

Abstract

The furcula is a distinctive element of the pectoral skeleton in birds, which strengthens the shoulder region to withstand the rigor of flight. Although its origin among theropod dinosaurs is now well-supported, the homology of the furcula relative to the elements of the tetrapod pectoral girdle (i.e., interclavicle vs clavicles) remains controversial. Here, we report the identification of the furcula in the birdlike theropod Halszkaraptor escuilliei. The bone is unique among furculae in non-avian dinosaurs in bearing a visceral articular facet in the hypocleideal end firmly joined to and overlapped by the sternal plates, a topographical pattern that supports the primary homology of the furcula with the interclavicle. The transformation of the interclavicle into the furcula in early theropods is correlated to the loss of the clavicles, and reinforced the interconnection between the contralateral scapulocoracoids, while relaxing the bridge between the scapulocoracoids with the sternum. The function of the forelimbs in theropod ancestors shifted from being a component of the locomotory quadrupedal module to an independent module specialized to grasping. The later evolution of novel locomotory modules among maniraptoran theropods, involving the forelimbs, drove the re-acquisition of a tighter connection between the scapulocoracoids and the interclavicle with the sternal complex.

Figure 1

The alternative hypotheses on the homology of the avian furcula. Comparison between the pectoral apparatus of non-avian reptiles (left) and birds (right). The furcula has been alternatively considered homologous to the clavicles (a–d), the interclavicle (e–h), or as a compound bone including elements from both the clavicles and the interclavicle (i–l). Generalized pectoral apparatus in a non-avian reptile in ventral view (a,e,i) and in left anterolateral view (b,f,j); in the middle, list of the evolutionary changes inferred along the avian stem lineage following the selected hypothesis; generalized pectoral apparatus in a bird (scapula omitted for clarity) in ventral view (c,g,k) and in left lateral view (d,h,l). cl clavicle, co coracoid, fu furcula, ic interclavicle, lr lateral ramus of interclavicle, pr parasternal ramus of interclavicle, sc scapula, st sternum. Drawing by AC.

Figure 2

The furcula-sternum complex in Halszkaraptor escuilliei MPC D-102/109. (a) Exposed elements of H. escuilliei holotype. (b) Furcula and sternum in ventral view. (c) Furcula in dorsal (visceral) view. (d) Furcula in left lateral view. (e) Furcula in anterior (proximal) view. (f) Detail of the sternofurcular articulation in dorsal (visceral) view. (g) Reconstruction of the furcula-sternum complex in dorsal (visceral) view. Dark grey, exposed furcula; light grey, posterior region of furcula overlapped by the sternal plates; white, sternal plates. cf coracoid facet, ep epicleideum, es “external” side of the bone, hy hypocleideum, lm lipped margin of visceral fossa, sac sternal anterior end covering the furcula, sms sternal plates midline suture, st sternal plates, vf visceral fossa, vs “visceral” side of the bone. Scale bars: 70 mm (a), 8 mm (b), 6 mm (c–e). Visualization by VB using Volume Graphics vers. 2.2. (Heidelberg, Germany: https://www.volumegraphics.com).

Figure 3

Mechanically prepared pectoral region of Halszkaraptor escuilliei MPC D-102/109. (a) Exposed sternum and furcula in visceral view. (b) Detail of the sternal articular surface of the furcula in left laterovisceral view. c10 10th cervical vertebra, d1 1st dorsal vertebra, d12 12th dorsal vertebra, ep epicleideum, fe femur, hy hypocleideum, lm lipped margin of the sternal facet, ri ribs, sms open midline suture between the sternal plates, st sternal plate, ti tibia. Scale bar: 30 mm (a), 10 mm (b). Photos by T. Hubin.

Figure 4

Updated reconstruction of the skeleton of H. escuilliei. (a) Whole skeleton in left lateral view; (b) detail of the pectoral apparatus (left forelimb removed). Missing elements indicated in grey. co coracoid, fu furcula, sc scapula, st sternum. Scale bar: 10 cm. Drawing by M. Auditore.

Figure 5

The interclavicle-sternum complex in reptiles and birds. (a–c) Varanus storri BE-RBINS-VER-10900. (a) The specimen subjected to µCT scanning. (b,c) close-up of the digitally reconstructed pectoral complex in ventral view (b) and oblique lateroventral view (c). Note the positions of clavicle and interclavicle lateral ramus relative to the acromial region, and the visceral overlap of the sternum relative to the posterior end of the interclavicle. (d,e) sterno-furcular complex of Pelecanus crispus BE-RBINS-VER-83834 in ventral view (d) and lateral view (e). Arrows in (e) mark the dorsoventral extent of the hypocleideum-sternal articular surface. Note the visceral overlap of the sternum relative to the hypocleideum. ac acromion, cl clavicle, co coracoid, cof coracoid facet, ep epicleideum, hy hypocleideum, lri lateral ramus of interclavicle, sc scapula, sk sternal keel, st sternum, vsi ventral (parasternal) ramus of interclavicle. Scale bars: 20 mm (a), 2 mm (b,c), 30 mm (d,e). Photos in (a,d,e) by T. Hubin. Visualization in (b,c) performed by J. Brecko using Dragonfly vers. 4.0 for Windows (Object Research Systems Inc., Montreal, Canada, 2020: http://www.theobjects.com/dragonfly).

Figure 6

Evolution of the interclavicle and sternum along the avian stem lineage. (a) Time-calibrated phylogeny of Pan-Aves focusing on Theropoda with indicated the main morphological state transitions involving the interclavicle and the sternum^,. Nodal optimisation under accelerated transformation. Colored branches indicate clades mentioned in the text. (b–e) Evolution of the pectoral apparatus along the avian-stem lineage (ventral view, scapula omitted for clarity). (b) Dinosaurian ancestral pattern; (c) early theropod pattern; (d) pennaraptoran pattern; (e) ornithuromorph pattern. cl clavicle, co coracoid, ic interclavicle, st sternum. Drawing by AC, with silhouettes modified from previous studies^,,.