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

Citation

wang, Xing et al. (2022), Muscle systems and motility of early animals highlighted by cnidarians from the basal Cambrian, Dryad, Dataset, https://doi.org/10.5061/dryad.pvmcvdnn1

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.

Methods

All studied fossils come from phosphatic limestones collected from the Kuanchuanpu Formation at the Shizhonggou section, (Ningqiang County, Shaanxi Province, China; see Figure 1—figure supplement 4). Biostratigraphy (AnabaritesProtohertzinaArthrochities zone, the SiphogonuchitesParagloborilus zone and LapworthellaTannuolinaSinosachites zone; refs. Qian, 1977; 1999) indicates that these rocks correspond to the Meishucunian Stage that is the equivalent of the lowermost Cambrian Terreneuvian Stage. Radiochronology (U-Pb method; refs. Sawaki et al., 2008; Peng et al., 2012) confirms that the Kuanchuanpu Formation is approximately 535 Ma. Secondarily phosphatized fossils were extracted from rocks via a standard acid digestion in 7% acetic acid. Dried residues with a grain-size >60 μm were sorted and picked under a binocular microscope. Twelve specimens of Olivooidae (Cnidaria) bearing well-preserved muscle fibers were selected for the present study and mounted for SEM (FEI Quanta 400 FEG scanning electron microscope at Northwest University, China; Au-coating, high-vacuum). They belong to Sinaster petalon Wang et al. (2017) (ELISN115-39), Hanagyroia orientalis Wang et al. (2020) (ELISN107-470) and Olivooidae sp. (ELISN150-278, ELISN111-54, ELISN052-33, ELISN045-143, ELISN012-16, ELISN061-19, ELISN087-64, ELISN088-48, ELISN087-33 and ELISN098-19). All specimens are deposited in the collections of the Shaanxi Key Laboratory of Early Life & Environments and the Department of Geology, Northwest University, China (‘ELI’ is an acronym of the former Early Life Institute that is now replaced by the Shaanxi Key Laboratory of Early Life & Environments; ‘SN’ means south Shaanxi Province, China in Chinese). Data concerning these specimens are available on request from JH and XW.

Two-week-old Clytia hemisphaerica medusae, newly released Eirene sp.  medusae, one-month-old Chrysaora colorata and Pelagia noctiluca metaephyrae were raised in the laboratory (Villefranche-sur-mer) following Lechable et al. (2020) and Ramondenc et al. (2017) culture protocols. Fixation followed by Phalloidin (actin) and Hoechst (nuclei) staining was performed on the four species as described for Clytia hemisphaerica in Sinigaglia et al. (2020). Samples were mounted in 50% Citifluor AF1 antifade mountant and imaged using Leica SP8 confocal and Zeiss Axio-Observer microscopes.

Extant priapulid worms (Priapulus caudatus) (see Figure 4—figure supplement 1) were collected (JV) from near the Kristineberg Marine Station (Sweden), fixed with glutaraldehyde and dried (Critical Point) for SEM observations (Univ. Lyon).