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

  1. Shiying Wang
  2. Yubo Ma
  3. Qian Wu
  4. Min Wang  Is a corresponding author
  5. Dongyu Hu  Is a corresponding author
  6. Corwin Sullivan
  7. Xing Xu  Is a corresponding author
  1. Chinese Academy of Sciences, China
  2. University of Alberta, Canada
  3. Shenyang Normal University, China

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 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.

Data availability

All data are available in the article

Article and author information

Author details

  1. Shiying Wang

    Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6067-0303
  2. Yubo Ma

    University of Alberta, Edmonton, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Qian Wu

    Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Min Wang

    Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China
    For correspondence
    wangmin@ivpp.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8506-1213
  5. Dongyu Hu

    Paleontological Museum of Liaoning, Shenyang Normal University, Shenyang, China
    For correspondence
    hudongyu@synu.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
  6. Corwin Sullivan

    University of Alberta, Edmonton, Canada
    Competing interests
    The authors declare that no competing interests exist.
  7. Xing Xu

    Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China
    For correspondence
    xingxu@vip.sina.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4786-9948

Funding

National Natural Science Foundation of China (41688103)

  • Dongyu Hu

National Natural Science Foundation of China (42072030)

  • Dongyu Hu

International Partnership Program of Chinese Academy of Sciences (132311KYSB20180016)

  • Corwin Sullivan

Natural Sciences and Engineering Research Council of Canada funding (Discovery Grant RGPIN-2017-06246)

  • Corwin Sullivan

start-up funding awarded by the University of Alberta to C.S.

  • Corwin Sullivan

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

Copyright

© 2022, Wang et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,807
    views
  • 341
    downloads
  • 8
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Shiying Wang
  2. Yubo Ma
  3. Qian Wu
  4. Min Wang
  5. Dongyu Hu
  6. Corwin Sullivan
  7. Xing Xu
(2022)
Digital restoration of the pectoral girdles of two Early Cretaceous birds, and implications for early flight evolution
eLife 11:e76086.
https://doi.org/10.7554/eLife.76086

Share this article

https://doi.org/10.7554/eLife.76086

Further reading

    1. Evolutionary Biology
    Xuankun Li, Adriana E Marvaldi ... Duane D McKenna
    Research Article

    The rise of angiosperms to ecological dominance and the breakup of Gondwana during the Mesozoic marked major transitions in the evolutionary history of insect-plant interactions. To elucidate how contemporary trophic interactions were influenced by host plant shifts and palaeogeographical events, we integrated molecular data with information from the fossil record to construct a time tree for ancient phytophagous weevils of the beetle family Belidae. Our analyses indicate that crown-group Belidae originated approximately 138 Ma ago in Gondwana, associated with Pinopsida (conifer) host plants, with larvae likely developing in dead/decaying branches. Belids tracked their host plants as major plate movements occurred during Gondwana’s breakup, surviving on distant, disjunct landmasses. Some belids shifted to Angiospermae and Cycadopsida when and where conifers declined, evolving new trophic interactions, including brood-pollination mutualisms with cycads and associations with achlorophyllous parasitic angiosperms. Extant radiations of belids in the genera Rhinotia (Australian region) and Proterhinus (Hawaiian Islands) have relatively recent origins.

    1. Evolutionary Biology
    Amanda D Melin
    Insight

    Studying the fecal microbiota of wild baboons helps provide new insight into the factors that influence biological aging.