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. 2017 Aug 15;114(33):8835-8840.
doi: 10.1073/pnas.1701650114. Epub 2017 Jul 31.

Three Cambrian Fossils Assembled Into an Extinct Body Plan of Cnidarian Affinity

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Free PMC article

Three Cambrian Fossils Assembled Into an Extinct Body Plan of Cnidarian Affinity

Qiang Ou et al. Proc Natl Acad Sci U S A. .
Free PMC article

Abstract

The early Cambrian problematica Xianguangia sinica, Chengjiangopenna wangii, and Galeaplumosus abilus from the Chengjiang biota (Yunnan, China) have caused much controversy in the past and their phylogenetic placements remain unresolved. Here we show, based on exceptionally preserved material (85 new specimens plus type material), that specimens previously assigned to these three species are in fact parts of the same organism and propose that C. wangii and G. abilus are junior synonyms of X. sinica Our reconstruction of the complete animal reveals an extinct body plan that combines the characteristics of the three described species and is distinct from all known fossil and living taxa. This animal resembled a cnidarian polyp in overall morphology and having a gastric cavity partitioned by septum-like structures. However, it possessed an additional body cavity within its holdfast, an anchoring pit on the basal disk, and feather-like tentacles with densely ciliated pinnules arranged in an alternating pattern, indicating that it was a suspension feeder rather than a predatory actiniarian. Phylogenetic analyses using Bayesian inference and maximum parsimony suggest that X. sinica is a stem-group cnidarian. This relationship implies that the last common ancestor of X. sinica and crown cnidarians was probably a benthic, polypoid animal with a partitioned gastric cavity and a single mouth/anus opening. This extinct body plan suggests that feeding strategies of stem cnidarians may have been drastically different from that of their crown relatives, which are almost exclusively predators, and reveals that the morphological disparity of total-group Cnidaria is greater than previously assumed.

Keywords: Chengjiangopenna wangii; Galeaplumosus abilus; Xianguangia sinica; ciliary suspension feeder; cnidarian stem group.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Xianguangia sinica, lower Cambrian, South China. (A) Complete specimen ELEL-SJ120376A showing feather-like tentacles, column, and holdfast. (B) Close-up of a pinnate tentacle (arrowed) in A. (C) Close-up of focus area in B showing long cilia fringing the pinnules. [Scale bars: (A) 5 mm; (B) 2 mm; (C) 1 mm.] Cc, circumferential constriction; Ci, cilia; Co, column; Ho, holdfast; Pi, pinnule; Ra, rachis; Te, tentacle.
Fig. 2.
Fig. 2.
Tentacle architecture of X. sinica (ELEL-SJ080827B; SI Appendix, Fig. S1). (A) Upper part showing numerous pinnate tentacles (arrowed). (BD) Close-up of focus areas in A showing sinuous pinnules (B), attachment sites (arrowheads) of pinnules branching from the rachis (C), and closely spaced cilia (arrows) fringing the pinnules (D), respectively. [Scale bars: 10 mm (A), 1 mm (BD).]
Fig. 3.
Fig. 3.
Anatomy of X. sinica. (A and B) Specimens ELEL-SJ120379 and SJ120380, respectively, showing column with external ridges and internal dark remains, circumferential constriction, and tentacles (arrowheads). (C) Aborally compacted specimen SJ101880 showing basal disk bearing a prominent pit filled with sediment. (D) Specimen SJ080827 showing upturned holdfast and basal pit (sediment removed). [Scale bars: 2 mm (A and B); 5 mm (C and D).] Bd, basal disk; Bp, basal pit; Cc, circumferential constriction; Co, column; Hc, holdfast cavity; Ho, holdfast; Om, organic material.
Fig. 4.
Fig. 4.
Reconstruction and phylogenetic position of X. sinica. (A) Three-dimensional model generated with 3ds Max. (B) Summary of metazoan relationships inferred from Bayesian analyses based on 111 characters and 37 taxa under Mkv + Γ model (see SI Appendix, Figs. S5–S7 and Text S2 and S3 for details). Numbers at nodes indicate posterior probabilities. X. sinica is resolved as a stem-group cnidarian. Eumetazoa, Neuralia, Bilateria, Nephrozoa, Protostomia, and Deuterostomia are monophyletic, whereas the monophyly of Spiralia is unresolved. Animal silhouettes are by courtesy of PhyloPic (www.phylopic.org).

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