How an important skeletomuscular correlate of flapping flight evolved
LINKED PAPER
Pectoral girdle morphology of Mesozoic birds and the evolution of the avian supracoracoideus muscle. Mayr, G. 2017. Journal of Ornithology. DOI: 10.1007/s10336-017-1451-x. VIEW
The evolution of avian flight muscles is poorly understood. The fact that the major flight muscles are situated below (anatomically speaking: ventral of) the wings is one of the characteristic features of the flight musculature of extant birds. This position comes as no surprise with respect to the large pectoralis muscle, which depresses the wing in the downstroke. However, it is more unexpected for the supracoracoideus muscle, which elevates the wing in the upstroke (Fig. 1).
Figure 1 (a) Wing and pectoral girdle bones of a Rock Pigeon, Columba livia, with the grey area indicating the surface of the sternal keel that serves as the area of origin of the supracoracoideus muscle (after George & Berger 1966: fig. III.1); the black arrow traverses through the triosseal canal formed by the coracoid, furcula, and scapula. (b) Schematic outline of the pectoral muscle, which originates from the sternal surface that is not occupied by the supracoracoideus muscle
For the supracoracoideus muscle to fulfill its function, its tendon runs through the triosseal canal formed by the scapula, furcula, and coracoid, which acts like a pulley and deflects the supracoracoideus tendon in such a way that the muscle can lift the humerus, despite being situated ventral of the wing (Fig. 2). Together, the pectoralis and supracoracoideus muscles constitute the main muscle masses attaching to the sternum, with the supracoracoideus muscle situated underneath the pectoralis muscle and originating from a large area of the sternal keel and the cranial portion of the sternal plate (George & Berger 1966; Fig. 1).
Figure 2 Triosseal canals of the Common Woodpigeon, Columba palumbus. The grey arrow indicates the course of the tendon of the supracoracoideus muscle
How this unique musculoskeletal system evolved remains poorly understood, and the evolution of the avian supracoracoideus muscle in particular has not yet been studied in detail. A new study provides a first step in this direction and identifies likely evolutionary steps based on the morphology of the pectoral girdle of Mesozoic birds.
The “urvogel” Archaeopteryx lacks a triosseal canal and an ossified sternum, and comparisons with crocodilians suggest that its supracoracoideus muscle most likely originated from the wide coracoid and mainly protracted (rather than elevated) the humerus (Fig. 3a). This condition is also found in non-avian theropod dinosaurs and is ancestral for birds. In the course of avian evolution, the supracoracoideus muscle became larger and shifted from the coracoid onto the ossified sternum. It is hypothesized that resulting space constraints in the cranial portion of the sternum, which also served as attachment site for the large pectoralis muscle, led to the evolution of a sternal keel – one of the anatomical hallmarks of modern birds.
Figure 3 Reconstructions of the pectoral girdle bones and the supracoracoideus muscle with its tendon of (a) the Late Jurassic Archaeopteryx, (b) the Early Cretaceous enantiornithine Rapaxavis, (c) the Early Cretaceous ornithuromorph Archaeorhynchus, and (d) an extant Rock Pigeon. Not to scale.
A distinctive pectoral morphology is found in the Enantiornithes, one of the major clades of Mesozoic birds (e.g. Chiappe & Meng 2016, Mayr 2016). In Early Cretaceous representatives of these birds, the cranial portion of the sternum lacks a well-developed keel (Fig. 3b) and a triosseal canal appears not to have been developed in Enantiornithes. It follows, therefore, that the development of the supracoracoideus muscle in these birds must have differed from that of extant birds. Absence of an efficient supracoracoideus pulley required different anatomical devices for flight control in early Mesozoic birds, and in enantiornithines this function may have been assumed by the long, streamer-like tail feathers.
Functionally, the enlargement and ventral shift of the supracoracoideus muscle is likely to have been correlated with the evolution of refined capabilities for flapping flight in early Mesozoic birds. The modern structure of the pectoral girdle, with a well-developed sternal keel and a functional triosseal canal, is a characteristic of Ornithuromorpha, the clade including extant birds. Unlike the predominantly arboreal Enantiornithes, all Early Cretaceous ornithuromorphs were terrestrial or semi-aquatic, and the evolution of the characteristic morphology of the supracoracoideus muscle of ornithuromorphs may have been an adaptation for rapid and powerful takeoffs from the ground.
Interestingly, a sternal keel with a deep cranial portion is present in some Enantiornithes from the Late Cretaceous of Argentina. This feature almost certainly evolved independently from the sternal keel of the Ornithuromorpha, although the reasons for development of a sternal keel in Late Cretaceous Enantiornithes are yet to be understood.
The disparate architectures of the shoulder girdle of phylogenetically basal Mesozoic avians such as Archaeopteryx, Jeholornis, and Sapeornis, in which the supracoracoideus muscle probably originated from the coracoid alone, clearly reflects very different locomotory characteristics. Archaeopteryx and other phylogenetically basal avians were probably not capable of sustained flapping flight and complicated aerial maneuvers and, until an efficient supracoracoideus pulley formed, wing flapping must have been assisted by the dorsal musculature.
References
Chiappe, L.M. & Meng, Q. 2016. Birds of Stone: Chinese Avian Fossils from the Age of Dinosaurs. Baltimore: Johns Hopkins University Press.
George, J.C. & Berger, A.J. 1966. Avian Myology. New York: Academic Press.
Mayr, G. 2016. Avian Evolution: The Fossil Record of Birds and its Paleobiological Significance. Chichester: Wiley-Blackwell.
Image credit
Featured image: Ultraviolet induced fluorescence photo of detail of the tenth skeleton of Archaeopteryx, the “Thermopolis specimen” © Sven Tränkner.
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