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

Abstract

Several studies analyzed the origin of flapping birds, but only a few of them explored the scapular girdle myologyin early birds and non-avian paravians. We analyze the pectoral girdle morphology in different groups of nonornithothoracineparavians with the aim to hypothesize the anchorage sites of selected pectoral muscles anddetermine their main functions in forelimb movements. Notably, the pectoral girdle remained morphologicallystable among non-ornithothoracine paravians since certain aspects of the coracoid and scapula are similar innon-flying taxa, such as the cursorial Buitreraptor, as well as those with the ability to fly, such as the four-wingedMicroraptor, the long-tailed Archaeopteryx and the pygostylians Confuciusornis and Sapeornis. The distinctionsamong these taxa are slightly discernible in bone morphology, but they are obvious in the forelimbs feathercoverage. 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 shapesof early paravians. The most significant muscular changes occurred in the common ancestor of Pygostylia, andconsisted in the displacement of the origin of the mm. biceps brachii and coracobrachialis p. cranialis, accompanyingthe greater development of the acrocoracoid process and the loss of the subglenoid fossa. These modificationsallowed 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 ofthe supracoracoidal canal thus allowing the m. supracoracoideus to fulfill a wing elevation function. Our studysuggests that in non-ornithothoracine paravians, the main movements of the forelimb (either fliers or not) werepredominantly craniodorsal to caudoventral. The humeral movements were performed in a similar manner, inwhich the main elevators were the mm. deltoideus and latissimus dorsi group, while the mm. supracoracoideusand pectoralis would have acted as protractor and depressor, respectively. Therefore, the ability to maintain acontinuous 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 induration and space displacement.