Reconstruction of pectoral musculature in non-avialan paravians and basal birds: implications in the acquisition of flapping flight.

Several studies analyzed the origin of flapping birds, but only a few of them explored the scapular girdle myology in early birds and non-avian paravians. We analyze the pectoral girdle morphology in different groups of non-ornithothoracine paravians with the aim to hypothesize the anchorage sites of selected pectoral muscles and determine their main functions in forelimb movements. Notably, the pectoral girdle remained morphologically stable among non-ornithothoracine paravians since certain aspects of the coracoid and scapula are similar in non-flying taxa, such as the cursorial Buitreraptor, as well as those with the ability to fly, such as the four-winged Microraptor, the long-tailed Archaeopteryx and the pygostylians Confuciusornis and Sapeornis. The distinctions among these taxa are slightly discernible in bone morphology, but they are obvious in the forelimbs feather coverage. In this sense, main pectoral muscles (i.e., mm. supracoracoideus, pectoralis and deltoideus scapularis/major) had similar origin and insertion places, and their inferred functions were similar across a wide array of body shapes of early paravians. The most significant muscular changes occurred in the common ancestor of Pygostylia, and consisted in the displacement of the origin of the mm. biceps brachii and coracobrachialis p. cranialis, accompanying the greater development of the acrocoracoid process and the loss of the subglenoid fossa. These modifications allowed more muscles to participate in humeral protraction and in the maintenance of wing extension. Subsequently, in the Ornithothoraces node, coracoid transformations contributed to the medial reorientation of the supracoracoidal canal thus allowing the m. supracoracoideus to fulfill a wing elevation function. Our study suggests that in non-ornithothoracine paravians, the main movements of the forelimb (either fliers or not) were predominantly craniodorsal to caudoventral. The humeral movements were performed in a similar manner, in which the main elevators were the mm. deltoideus and latissimus dorsi group, while the mm. supracoracoideus and pectoralis would have acted as protractor and depressor, respectively. Therefore, the ability to maintain a continuous flapping flight present in extant volant birds may have been acquired at the Ornithothoraces node, while Archaeopterygidae, Confuciusornithidae and Omnivoropterygidae may have had functional flight, short in duration and space displacement.