Early evolution of the ecdysozoan body plan
- State Key Laboratory of Continental Dynamics, Shaanxi Key Laboratory of Early Life & Environments and Department of Geology, Northwest University, China
- School of Earth Science and Resources, Key Laboratory of Western China’s Mineral Resources and Geological Engineering, Ministry of Education, Chang’an University, China
- Université de Lyon, Université Claude Bernard Lyon 1, ENS de Lyon, CNRS, Laboratoire de Géologie de Lyon: Terre, Planètes, Environnement (CNRS-UMR 5276), France
- Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, China
- University of Chinese Academy of Sciences, China
- School of Information Science and Technology, Northwest University, China
Figures
Figure 1 with 3 supplements
Beretella spinosa gen. et sp. nov. from Member 5 of the Yanjiahe Formation (Cambrian Stage 2), Yichang, Hubei Province, China.
(A‒C) Holotype, CUBar138-12. (A) Dorsal view showing the external ornament: (five sclerites at the midline in yellow (S1); flanked by two rows of sclerites in blue (S2); large broad-based conical sclerites in two dorsolateral pairs and one antero-posterior pairs in green (S3)); white arrows indicate lateral constriction. (B) Right lateral view showing two additional rows of six sclerites (S4 and S5, in light blue and pink, respectively). (C) Ventral view showing a large opening that may have accommodated the mouth (see the text) and an empty body cavity. (D‒G) CUBar75-45. (D) Dorsal view showing a broken S3. (E) Micro-CT image, right lateral view displaying S4. (F) Ventral view depicting a tiny projection in purple. (G) An enlargement of the projection of F. (H‒I) Paratype, CUBar171-5. (H) Right dorsal view showing S1‒S4. (I) Right-lateral view showing S4 and S5. (J‒K) Paratype CUBar121-8. (J) Dorsal view showing poorly preserved S1 and S2. (K) Right-lateral view showing S3‒S5. A, assumed anterior end (see text); ef, exotic fragment; D, assumed dorsal side; L, left; P, posterior end; R, right; tp, tiny spine; V, ventral side. The same abbreviations are used throughout the manuscript including supplementary files.
Figure 1—figure supplement 1
Size variation between Saccorhytus coronarius and Beretella spinosa.
(A-D) Saccorhytus coronarius; ELIXX25-62, ELIXX48-64, ELIXX61-27, and ELIXX65-296, respectively. (E-G) Beretella spinosa; CUBar75-45, CUBar171-5, CUBar138-12, and CUBar121-8, respectively. All specimens at the same scale (500 µm). All SEM images. ‘A-C’ are new photographs of published specimens (Han et al., 2017).
Figure 1—figure supplement 2
Origin of fossil material.
(A-D) Geological background and locality map and stratigraphy (Guo et al., 2019). The red star indicates Member 5 of the Yanjiahe Formation where Beretella spinosa was found; this fossiliferous horizon is correlated with the bottom of Cambrian Stage 2 (Terreneuvian; ca. 529 Ma).
Figure 1—figure supplement 3
Typical Small Shelly Fossils (SSFs) found associated with Beretella spinosa in Member 5 of the Yanjiahe Formation.
(A) CUBar21-4, Watsonella crosbyi. (B) CUBar206-6, Aldanella attleborensis.
Figure 2 with 2 supplements
Beretella spinosa gen. et sp. nov.
(A) CUBar99-19, dorsal view showing an ornament S1‒S4. (B, C) CUBar136-9, general dorsal view and details. (D) CUBar136-11, dorsal view showing S1‒S5. (E, F) CUBar73-15 general view and details of the cuticular polygonal reticulation in black. (G‒J) CUBar128-27. (G) General view. (H, I) details of outer and inner surface of the bi-layered structure of the cuticular wall as seen in broken conical sclerites. (J) Micro-CT section showing possibly sclerite infilling. (K, L) CUBar99-18, cuticular fragment, general view and details of large sclerite (central feature represents possible phosphatic infilling). is, infilling sclerite; pr, polygonal reticulation; sb, sclerite base.
Figure 2—figure supplement 1
Truncated sclerites in early Cambrian saccorhytids and scalidophoran worms.
(A, B) Beretella spinosa (CUBar73-15 and CUBar99-18, respectively). (C) Undetermined scalidophoran worm (ELIXX57-320). (D) Saccorhytus coronarius (ELIXX34-298). (E-I) Beretella spinosa. (E, F) CUBar136-11, dorsal view showing arrangement of S1‒S5; ventral view. (G-I) CUBar75-45. (G) Dorsal view showing two pairs of S3 pointing outwards (tip broken). (H) Lateral-right view showing RS4 and RS5. (I) Micro-CT image, intermediate dorsal view showing S3-1. All SEM images except ‘I’. ‘D’ is a new photograph of a published specimen (Han et al., 2017). Sp, spiny sclerite; ts, truncated sclerite. (Rich media 3- Micro-CT render of CUBar128-27).
Figure 2—figure supplement 2
Saccorhytus coronarius, multi-layered secondarily phosphatized cuticle.
(A-C) ELIXX45-20, general view and close-ups showing chevron patterns on inner and outer layers. D-F, ELIXX58-336, general view and close-ups showing bi-layered cuticle (not on a sclerite) with chevron pattern on both layers. (G-L) ELIXX65-116, showing bi-layered cuticular structure; general view (SEM), Micro-CT section parallel to the specimen’s external surface, and close-up in I. (J-N) ELIXX99-420. (J-L) General view and details showing two- or three-layered cuticular structures. (M, N) Micro-CT transverse and vertical sections through the cuticle (see location in j) showing tri-layered cuticular structures. All SEM images except ‘H, L, M, N’. ‘A’ is a new photograph of a published specimen (Han et al., 2017). il, inner layer; ilc, inner layer chevron; Mo, mouth; ol, outer layer; olc, outer layer chevron. (Rich media 4. Micro-CT render of ELIXX65-116, Rich media 5. Micro-CT render of ELIXX99-420).
Figure 3 with 4 supplements
Position of Beretella spinosa in the animal tree based on cladistic analysis.
(A-C), artistic three-dimensional reconstructions of Beretella spinosa in the anterolateral (A), dorsal (B), and posterolateral views (C). (D) Phylogenetic tree obtained from cladistic analyses using maximum likelihood. Saccorhytus and Beretella join in a clade (new phylum Saccorhytida) resolved as the sister-group of all other ecdysozoans; numbers at key nodes denote probability. Fossil and extant taxa are in italics and bold, respectively. Known fossil record indicated by thicker vertical bars (after Shu and Han, 2020).
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Figure 3—source code 1
The dataset (matrix) for cladistic analysis.
- https://cdn.elifesciences.org/articles/94709/elife-94709-fig3-code1-v1.zip
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Figure 3—source data 1
Characters description for cladistic analysis.
- https://cdn.elifesciences.org/articles/94709/elife-94709-fig3-data1-v1.docx
Figure 3—figure supplement 1
Full maximum likelihood tree generated by IQTREE.
50% majority rule consensus. Total-group Ecdysozoa (TGE, yellow dot) contains Saccorhytida, Cycloneuralia, and Panarthropoda. Saccorhytida is resolved as the sister group of the crown-group Ecdysozoa (blue dot, Cycloneuralia and Panarthropoda). Cycloneuralia is well resolved as a monophyletic group including Scalidophora, Nematoida, and Acosmia. The relationships of cycloneuralian ingroups are unclear. Numbers close to nodes are probabilities. Taxa in bold represent extant species.
Figure 3—figure supplement 2
Bayesian inference tree generated by MrBayes.
50% majority rule consensus. Total-group Ecdysozoa (TGE, yellow dot) contains Saccorhytida, Cycloneuralia, and Panarthropoda. Saccorhytida is resolved as the sister group of the crown-group Ecdysozoa (blue dot, Cycloneuralia and Panarthropoda). Cycloneuralia is resolved as a monophyletic group including Scalidophora and Nematoida but the probabilities of Cycloneuralia and Nematoida +Acosmia nodes are very low. Acosmia is resolved as a stem member of Nematoida. Numbers close to nodes are posterior probabilities. Taxa in bold represent extant species.
Figure 3—figure supplement 3
Maximum parsimony tree generated by TNT (equal weight).
Strict consensus of four most parsimonious trees. Total-group Ecdysozoa (TGE, yellow dot) contains Saccorhytida, Acosmia, Nematoida, Scalidophora, and Panarthropoda. Saccorhytida is resolved as the sister group of the crown-group Ecdysozoa (blue dot, Acosmia, Nematoida, Scalidophora, and Panarthropoda). Note that Cycloneuralia does not appear as a monophyletic clade. The relationships of crown-group ecdysozoan ingroups are unclear. Taxa in bold represent extant species.
Figure 3—figure supplement 4
Maximum parsimony tree generated by TNT (implied weight, k=3).
Strict consensus of four most parsimonious trees. Total-group Ecdysozoa (TGE, yellow dot) contains Saccorhytida, Acosmia, Nematoda, Nematomorpha, Scalidophora, and Panarthropoda. Saccorhytida is resolved as the sister group of the crown-group Ecdysozoa (blue dot, Acosmia, Nematoda, Nematomorpha, Scalidophora, and Panarthropoda). Note that Cycloneuralia does not appear as a monophyletic clade. The relationships of crown-group ecdysozoan ingroups are unclear. Taxa in bold represent extant species.
Figure 4
Possible evolutionary scenario to explain the origin and early evolution of ecdysozoans.
(A) Summary tree (see Figure 3—figure supplements 1–4) showing saccorhytids as a sister-group of Cycloneuralia (Nematoida plus Scalidophora)+Panarthropoda; main morphological features of each group listed along each branch. (B) Potential evolutionary pathway to evolve Saccorhytida and crown-group Ecdysozoa. Numbers in green, red and blue circles designate pre-ecdysozoan (Spiralia), Saccorhytida and Cycloneuralia, respectively. Light brown gradient (circle) to emphasize ecdysis and sclerite secretion seen as key evolutionary steps. 1, Hypothetical pre-ecdysozoan animal with a ciliated epidermis and glycocalyx. 2, Saccorhytid exemplified by Beretella with a cuticle bearing sclerites. 3, Crown-group ecdysozoan exemplified by a scalidophoran worm with an elongated shape, a differentiated head (introvert) and trunk, sclerites, a through gut, a terminal mouth and abilities to burrow into bottom sediment. Animals not to scale. Abbreviations: a, anus; a?, uncertain status of anus; ci, cilia; cu, cuticle; ec, epidermal cell; gl, glycocalyx (mucous layer); m, mouth; in, introvert; sc, sclerite; se, sediment; TGE, total-group Ecdysozoa. Silhouettes from phylopic.org. (CC BY 3.0 or public domain): Spiralia (by Martin R. Smith), Nematoida (by Birgit Lang), Scalidophora (by Fernando Carezzano), and Panarthropoda (by Harold N Eyster). Saccorhytida generated from reconstruction of Figure 3.
Videos
Video 1
Animation of holotype of Beretella spinosa.
Video 2
Animation of holotype of Beretella spinosa without color.
Additional files
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Supplementary file 1
Meaurements of Saccorytida and ancestral character state reconstruction of Cycloneuralia.
(a) Measurements of Beretella. L, length; W, width; H, height; ae, anterior end; B, body; pe, posterior end; PP, polygonal net-like pattern; tp, tiny spine; VO, ventral opening;?, no accurate measurement possible. (b) Length/width ratio of Beretella and Saccorhytus. (c) Similarities and differences between Beretella and Saccorhytus. AP, antero-posterior; DV, dorso-ventral side; LR, left-right. (d) Ancestral character state reconstructions for the topology where Cycloneuralia is monophyly. Values of ancestral character state reconstructions. 0=absence of character, 1=presence of character, P=posterior probability. TGE, total-group Ecdysozoa; CGE, crown-group Ecdysozoa, SA, Saccorhytida. (e) Ancestral character state reconstructions for the topology where Cycloneuralia is paraphyletic. Values of ancestral character state reconstructions. 0=absence of character, 1=presence of character, P=posterior probability. TGE, total-group Ecdysozoa; CGE, crown-group Ecdysozoa, SA, Saccorhytida.
- https://cdn.elifesciences.org/articles/94709/elife-94709-supp1-v1.docx
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MDAR checklist
- https://cdn.elifesciences.org/articles/94709/elife-94709-mdarchecklist1-v1.docx
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Early evolution of the ecdysozoan body plan
eLife 13:RP94709.
https://doi.org/10.7554/eLife.94709.3
