Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2022 Mar 31:11:e76086.
doi: 10.7554/eLife.76086.

Digital restoration of the pectoral girdles of two Early Cretaceous birds and implications for early-flight evolution

Shiying Wang  1   2   3 , Yubo Ma  4 , Qian Wu  1   2   3 , Min Wang  1   2 , Dongyu Hu  5 , Corwin Sullivan  4   6 , Xing Xu  1   2   5   7
Affiliations

Digital restoration of the pectoral girdles of two Early Cretaceous birds and implications for early-flight evolution

Shiying Wang et al. Elife. .

Abstract

The morphology of the pectoral girdle, the skeletal structure connecting the wing to the body, is a key determinant of flight capability, but in some respects is poorly known among stem birds. Here, the pectoral girdles of the Early Cretaceous birds Sapeornis and Piscivorenantiornis are reconstructed for the first time based on computed tomography and three-dimensional visualization, revealing key morphological details that are important for our understanding of early-flight evolution. Sapeornis exhibits a double articulation system (widely present in non-enantiornithine pennaraptoran theropods including crown birds), which involves, alongside the main scapula-coracoid joint, a small subsidiary joint, though variation exists with respect to the shape and size of the main and subsidiary articular contacts in non-enantiornithine pennaraptorans. This double articulation system contrasts with Piscivorenantiornis in which a spatially restricted scapula-coracoid joint is formed by a single set of opposing articular surfaces, a feature also present in other members of Enantiornithines, a major clade of stem birds known only from the Cretaceous. The unique single articulation system may reflect correspondingly unique flight behavior in enantiornithine birds, but this hypothesis requires further investigation from a functional perspective. Our renderings indicate that both Sapeornis and Piscivorenantiornis had a partially closed triosseal canal (a passage for muscle tendon that plays a key role in raising the wing), and our study suggests that this type of triosseal canal occurred in all known non-euornithine birds except Archaeopteryx, representing a transitional stage in flight apparatus evolution before the appearance of a fully closed bony triosseal canal as in modern birds. Our study reveals additional lineage-specific variations in pectoral girdle anatomy, as well as significant modification of the pectoral girdle along the line to crown birds. These modifications produced diverse pectoral girdle morphologies among Mesozoic birds, which allowed a commensurate range of capability levels and styles to emerge during the early evolution of flight.

Keywords: Early Cretaceous; evolutionary biology; pectoral girdle; scapula-coracoid articulation; stem birds; triosseal canal.

PubMed Disclaimer

Conflict of interest statement

SW, YM, QW, MW, DH, CS, XX No competing interests declared

Figures

Figure 1.
Figure 1.. The position of the pectoral girdle and the form of the coracoid in different theropod groups.
(A–C) Skeletal silhouettes showing the anatomical position of the pectoral girdle in (A) the early-diverging theropod Coelophysis, (B) the early-diverging pennaraptoran Microraptor, and (C) the modern bird Columba. The M. supracoracoideus is illustrated in (C) but typically covered by the M. pectoralis, which is not illustrated. (D–G) Illustrations of the left coracoids of (D) Coelophysis (modified from Tykoski, 1998), (E) the early-diverging pennaraptoran Sinornithosaurus (modified from Xu et al., 1999), (F) the early-diverging avialan Archaeopteryx (modified from Wellnhofer et al., 2009), and (G) the early-diverging avialan Jeholornis (based on STM 2-49 and IVPP V 13886). Coracoid of Coelophysis in lateral view, coracoids of other taxa in ventral view.
Figure 2.
Figure 2.. Pectoral girdle bones of Sapeornis chaoyangensis PMoL-AB00015.
(A–D) Left scapula in lateral, dorsal, medial (costal), and ventral views. (E–H) Left coracoid in ventral, dorsal, lateral, and cranial views. (I–L) Furcula in cranial, caudal, lateral, and ventral views. The black arrows in (J) and (L) indicate the concave surface for the tendon of M. supracoracoideus.
Figure 3.
Figure 3.. Pectoral girdle bones of Piscivorenantiornis inusitatus IVPP V 22582.
(A–D) Left scapula in lateral, dorsal, medial (costal), and ventral views. (E–H) Right coracoid in ventral, dorsal, lateral, and cranial views. (I–L) Furcula in cranial, caudal, left, and ventral views.
Figure 4.
Figure 4.. Comparison of scapula and coracoid morphology across various paravian taxa.
Each panel shows articulated left scapula and coracoid in ventral view (on left) and opposing articular surfaces of left scapula and coracoid (on right, with cranial direction toward top of figure for both scapula and coracoid). (A) Sinovenator changii (mirrored), (B) Sapeornis chaoyangensis, (C) Piscivorenantiornis inusitatus, (D) Tyto alba, (E) Egretta garzetta, and (F) Pavo muticus.
Figure 5.
Figure 5.. Simplified phylogeny with hypothetical steps in pectoral girdle evolution.
The pectoral girdles of Sapeornis chaoyangensis, Piscivorenantiornis inusitatus, and Pavo muticus (from top to bottom) are shown in cranial, dorsal, and left lateral views. The pink lines in the dorsal and lateral views represent the tendon of M. supracoracoideus, and the gray line in the dorsal view of the Sapeornis rendering represents the coracoclavicular ligament that connects the coracoid and furcula. Phylogenetic framework following Wang et al., 2018a.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

References

    1. Atterholt J, Hutchison JH, O’Connor JK. The most complete enantiornithine from North America and a phylogenetic analysis of the Avisauridae. PeerJ. 2018;6:e5910. doi: 10.7717/peerj.5910. - DOI - PMC - PubMed
    1. Baier DB, Gatesy SM, Jenkins FA. A critical ligamentous mechanism in the evolution of avian flight. Nature. 2007;445:307–310. doi: 10.1038/nature05435. - DOI - PubMed
    1. Baumel JJ, Witmer LM. In: Handbook of Avian Anatomy: Nomina Anatomica Avium 2nd Ed: Publications of the Nuttall Ornithological Club. Baumel JJ, King AS, Breazile JE, Evans HE, Vanden Berge JC, editors. Acedemic Press; 1993. Osteologia; pp. 45–124.
    1. Bock WJ. The furcula and the evolution of avian flight. Paleontological Journal. 2013;47:1236–1244. doi: 10.1134/S0031030113110038. - DOI
    1. Boggs D, Jenkins F, Dial K. The effects of the wingbeat cycle on respiration in black-billed magpies (Pica pica) The Journal of Experimental Biology. 1997;200:1403–1412. doi: 10.1242/jeb.200.9.1403. - DOI - PubMed

Publication types

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.