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

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    Evaluation Summary:

    The authors provide new 3D fossil findings in Sapeornis, an avialan which lived during the early Cretaceous period, a key node in our understanding of the evolution of avian flight. The functional reconstruction of two critical skeletal elements of the avian flight apparatus, the scapula and coracoid, enable the authors to hypothesize how the evolution of the scapula and coracoid enabled the modern avian wing stroke. The new 3D morphological reconstruction enables future integrative studies of Sapeornis flight performance based on biomechanical, muscle physiological and aerodynamic principles and is thus a key building block to inform our general understanding of the evolution of avian flight.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)

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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.

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  1. Evaluation Summary:

    The authors provide new 3D fossil findings in Sapeornis, an avialan which lived during the early Cretaceous period, a key node in our understanding of the evolution of avian flight. The functional reconstruction of two critical skeletal elements of the avian flight apparatus, the scapula and coracoid, enable the authors to hypothesize how the evolution of the scapula and coracoid enabled the modern avian wing stroke. The new 3D morphological reconstruction enables future integrative studies of Sapeornis flight performance based on biomechanical, muscle physiological and aerodynamic principles and is thus a key building block to inform our general understanding of the evolution of avian flight.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)

  2. Reviewer #1 (Public Review):

    The authors are providing new important data through which to discuss the evolution of the scapula and coracoid and how it relates to the evolution of the modern avian flight stroke.

    The strength lies in the excellent new CT data. Weaknesses include inconsistency in terminology and a lack of recognition for previous work done.

    Information regarding the precise 3D morphology of the scapulocoracoid in Sapeornis is a major step in the direction of better understanding this important transformation in birds. The data once publically available can be used to further explore flight capabilities in this important taxon.

  3. Reviewer #2 (Public Review):

    The manuscript by Shiying Wang and co-authors entitled "Digital restoration of the pectoral girdles of two Early Cretaceous birds, and implications for early flight evolution" constitutes a wonderful and highly detailed study on two important fossil birds. For the first time a 3D reconstruction of their scapular girdle is provided, offering novel anatomical data which clarify the sequence of morphological features in the line to crown-birds. I have enjoyed reading this contribution.

    There are some minor aspects that the authors will be able to solve. Some other points concern the phylogenetic interpretations (mainly concerning the relationships of Rahonavis), for which I recommend modifications, that the authors should feel free to follow or not.

    I disagree with some topical aspects on the morphology of the coracoid of Sapeornis and the inferred function of such features. Nevertheless, even if the authors accept my thoughts on this issue, the main interpretations offered in the ms will not change, and only the origin of some adaptations (e.g., protactor vs elevator function of the m. supracoracoideus) would need to be revised. However, even if the authors do not accept my interpretations, this is a valuable "step forward" paper on the anatomy and evolution of early birds.