Muscle systems and motility of early animals highlighted by cnidarians from the basal Cambrian

  1. Xing Wang  Is a corresponding author
  2. Jean Vannier
  3. Xiaoguang Yang
  4. Lucas Leclère
  5. Qiang Ou
  6. Xikun Song
  7. Tsuyoshi Komiya
  8. Jian Han  Is a corresponding author
  1. Qingdao Institute of Marine Geology, China
  2. Claude Bernard University Lyon 1, France
  3. Northwest University, China
  4. Sorbonne Université, France
  5. China University of Geosciences, China
  6. Xiamen University, China
  7. University of Tokyo, Japan

Abstract

Although fossil evidence suggests that various animal groups were able to move actively through their environment in the early stages of their evolution, virtually no direct information is available on the nature of their muscle systems. The origin of jellyfish swimming, for example, is of great interest to biologists. Exceptionally preserved muscles are described here in benthic peridermal olivooid medusozoans from the basal Cambrian of China (Kuanchuanpu Formation, ca. 535 Ma) that have direct equivalent in modern medusozoans. They consist of circular fibers distributed over the bell surface (subumbrella) and most probably have a myoepithelial origin. This is the oldest record of a muscle system in cnidarians and more generally in animals. This basic system was probably co-opted by early Cambrian jellyfish to develop capacities for jet-propelled swimming within the water column. Additional lines of fossil evidence obtained from ecdysozoans (worms and panarthropods) show that the muscle systems of early animals underwent a rapid diversification through the early Cambrian and increased their capacity to colonize a wide range of habitats both within the water column and sediment at a critical time of their evolutionary radiation.

Data availability

Data for this study are available in the Dryad Digital Repository: https://doi.org/10.5061/dryad.pvmcvdnn1

The following data sets were generated

Article and author information

Author details

  1. Xing Wang

    China Geological Survey, Qingdao Institute of Marine Geology, Qingdao, China
    For correspondence
    wx5432813@126.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1777-864X
  2. Jean Vannier

    CNRS UMR 5276, Laboratoire de géologie de Lyon, Claude Bernard University Lyon 1, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0998-1231
  3. Xiaoguang Yang

    Department of Geology, Northwest University, Xi'an, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Lucas Leclère

    CNRS, Laboratoire de Biologie du Développement, Sorbonne Université, Villefranche-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7440-0467
  5. Qiang Ou

    Early Life Evolution Laboratory, School of Earth Sciences and Resources, China University of Geosciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Xikun Song

    State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3335-0029
  7. Tsuyoshi Komiya

    Department of Earth Science and Astronomy, University of Tokyo, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  8. Jian Han

    Department of Geology, Northwest University, Xi'an, China
    For correspondence
    elihanj@nwu.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2134-4078

Funding

China Postdoctoral Science Foundation (No. 2020M672013)

  • Xing Wang

National Natural Science Foundation of China (Nos. 41902012,41720104002)

  • Jian Han

the Strategic Priority Research Program of the Chinese Academy of Sciences (No. XDB26000000)

  • Jian Han

111 Project of the Ministry of Education of China (Nos. D17013,D163107)

  • Jian Han

the Most Special Fund from the State Key Laboratory of Continental Dynamics, Northwest University, China (BJ11060)

  • Jian Han

the Region Auvergne-Rhone-Alpes and the Univ. of Lyon (PAI grant to JV)

  • Jean Vannier

Agence Nationale de la Recherche (Lucas Leclère ANR-19-CE13-0003)

  • Lucas Leclère

National Natural Science Foundation of China (41876180)

  • Xikun Song

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

Reviewing Editor

  1. Min Zhu, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, China

Version history

  1. Received: October 14, 2021
  2. Preprint posted: October 26, 2021 (view preprint)
  3. Accepted: January 11, 2022
  4. Accepted Manuscript published: January 31, 2022 (version 1)
  5. Version of Record published: February 11, 2022 (version 2)
  6. Version of Record updated: June 16, 2022 (version 3)

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.

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  1. Xing Wang
  2. Jean Vannier
  3. Xiaoguang Yang
  4. Lucas Leclère
  5. Qiang Ou
  6. Xikun Song
  7. Tsuyoshi Komiya
  8. Jian Han
(2022)
Muscle systems and motility of early animals highlighted by cnidarians from the basal Cambrian
eLife 11:e74716.
https://doi.org/10.7554/eLife.74716

Share this article

https://doi.org/10.7554/eLife.74716

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