An extinct clade of the basal Epitheliozoa: phylogenetic position and implication of the enigmatic Cambrian chancelloriids

Abstract

The notable disparity of animal body plans can be traced back to the morphological innovations during the Cambrian explosion and represented by a number of soft-bodied and skeletal fossils that provide a compelling narrative for animal evolution. Chancelloriids are an extinct group of Cambrian animals characterized by a distinctive sclerite-bearing, flexible integument and a single apical opening leading into a central cavity devoid of unequivocal internal organs. Their phylogenetic position within the Metazoa remains controversial. Here we show new exceptionally-preserved fossils from the 518-million-year-old Chengjiang biota of China, which corroborate the unique bauplan pattern of chancelloriids, and reveal exquisite integument microstructures including tiny protuberances and associated wrinkle-like structures that are interpreted to be related to epithelial contractions. A phylogenetic study assessing the interrelationship of chancelloriids among metazoans using modern cladistic methods is conducted to the best of our knowledge. The result suggests that chancelloriids constitute an evolutionary clade branched above and close to the Placozoa. Therefore, the enigmatic Cambrian chancelloriids represent an extinct, phylum-level basal Epitheliozoa and stem-group Eumetazoa. Their body plan has filled one of the anatomical gaps between the Placozoa and living eumetazoans within the evolutionary tree of animals.

Fig. 1. Microstructures of the chancelloriid integument.

a, b Specimen SJZ-B03-179A (a) and its counterpart SJZ-B03-179B (b) of the chancelloriid Allonnia phrixothrix from the Chengjiang biota, showing highlighted reddish colored soft integument. c, d Details of (a), showing obvious protuberances. e Detail of (b), showing both evenly-distributed protuberances (right and middle parts) and aligned protuberances (right side). f A. phrixothrix from the Chengjiang biota, specimen SJZ-B03-180A. g Detail of (f), showing distinctive evenly distributed protuberances on the surface of the integument.

Fig. 2. Aligned protuberances and wrinkle-like structure on the chancelloriid integument.

a–d Integuments of the chancelloriid Allonnia phrixothrix from the Chengjiang biota, showing distinctive aligned protuberances and locally distributed wrinkle-like structures; a detail of the specimen SJZ-B04-095B (Supplementary Fig. 1a); b detail of the specimen SJZ-B03-180A (Fig. 1f); c detail of the specimen SJZ-B03-179B (Fig. 1b); d detail of the specimen SJZ-B05-010A (Supplementary Fig. 2a). e A hypothetical interpretation of the wrinkle-like structure formed by couplets of parallel stripes (aligned protuberances) and grooves; the organization of epitheliomuscular cells refers to Schmidt-Rhaesa.

Fig. 3. Phylogenetic position and relationship of chancelloriids within an evolutionary scenario (modified placula hypothesis) of the epitheliozoan body plan.

The consensus tree is obtained by using Bayesian phylogenetic analysis based on a dataset containing 85 taxa and 248 characters (see Supplementary Fig. 3 and Data 1 for details). Numbers at the nodes are percentages of posterior probabilities, and the scale bar indicates the expected number of substitutions per site. Cross marks at the upper right of the taxa names indicate that they are fossil taxa. The relationship topology of the strict consensus tree obtained in the maximum parsimony (MP) analysis (Supplementary Fig. 4) is placed in the lower left corner. Silhouettes of the representative animal clades are from PhyloPic (www.phylopic.org). The evolutionary scenario, described as the Modified Placula Hypothesis, of the epitheliozoan body plan is generally based on the phylotypic stages of metazoan embryogenesis^,,, showing a sequence of the body plan complexity from Placozoa to Bilateria.

Fig. 4. Specialization of biomineralization in chancelloriids.

a Different sclerite forms of the chancelloriid Cambrothyra (see main text for interpretation). b–e Typical sclerite structures and body shape silhouettes of the chancelloriid genera Nidelric, Dimidia, Archiasterella, and Chancelloria, respectively.

Fig. 5. Reconstruction of representative chancelloriids from the Chengjiang biota.

Artworks of Allonnia erjiensis (left) and A. phrixothrix (right) are drawn by Xi Liu, copyright Northwest University.