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, 1 (6), e1500092
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A Vanished History of Skeletonization in Cambrian Comb Jellies

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A Vanished History of Skeletonization in Cambrian Comb Jellies

Qiang Ou et al. Sci Adv.

Abstract

Ctenophores are traditionally regarded as "lower" metazoans, sharing with cnidarians a diploblastic grade of organization. Unlike cnidarians, where skeletonization (biomineralization and sclerotization) evolved repeatedly among ecologically important taxa (for example, scleractinians and octocorals), living ctenophores are characteristically soft-bodied animals. We report six sclerotized and armored ctenophores from the early Cambrian period. They have diagnostic ctenophore features (for example, an octamerous symmetry, oral-aboral axis, aboral sense organ, and octaradially arranged ctene rows). Unlike most modern counterparts, however, they lack tentacles, have a sclerotized framework, and have eight pairs of ctene rows. They are resolved as a monophyletic group (Scleroctenophora new class) within the ctenophores. This clade reveals a cryptic history and sheds new light on the early evolution of this basal animal phylum. Skeletonization also occurs in some other Cambrian animal groups whose extant members are exclusively soft-bodied, suggesting the ecological importance of skeletonization in the Cambrian explosion.

Keywords: Cambrian; Chengjiang biota; Ctenophora; skeleton.

Figures

Fig. 1
Fig. 1
Gemmactena actinala gen. et sp. nov. (A) Holotype (ELEL-SJ100756A) showing radiating flap-like structures outlined by spokes, comb rows, and oral lappets. Apical organ not preserved. (B) Close-up of small focus area in (A) showing fine striae on spoke surface. (C) Close-up of large focus area in (A) showing remains of comb rows, as well as upper and lower spokes that frame a flap. (D) Paratype (ELEL-SJ081292A). (E) Close-up of focus area in (D) showing rigidity of a spoke with a medial groove (internal view). (F) Close-up of aboral region in (D) showing an ellipsoidal statolith preserved as dark remains surrounded by apical plates. (G) Counterpart of (F) showing complete apical plates detached from each other; remains of organic carbon are partially preserved as a dark band on the statolith. (H) Paratype (ELEL-SJ081366A) showing pointed dome-like apical organ walled by rigid plates (each with a medial groove continuous with a spoke). (I) Aborally compacted specimen ELEL-SJ120375A showing an apical organ and partially dislocated upper spokes (arrows). The apex of the apical organ was truncated and retained in counterpart during splitting. (J) Close-up of focus area in (I) showing distal end of upper spoke, with the kink marked by arrow. (K) Close-up of apical organ in (I); dark, equally spaced bands (arrowheads) radiating from the base of apical organ may represent remains of underlying meridional canals. (L) Close-up of apical organ showing considerable positive relief, presumably due to its rigidity imparted by apical plates (numbered). ao, apical organ; cr, comb row; fp, flap-like structure; ls, lower spoke; ol, oral lappet; os, oral skirt; pl, apical plate; sl, statolith; us, upper spoke. Scale bars, 5 mm (A, D, H, and I); 2 mm (C, F, and G); 1 mm (B, E, and J to L).
Fig. 2
Fig. 2
Thaumactena ensis gen. et sp. nov. (A to D), Galeactena hemispherica gen. et sp. nov. (E to I), and Batofasciculus ramificans (J to N). (A) Holotype (ELEL-SJ081427A) showing apical organ, body with rigid spokes (arrows), and oral skirt. (B) Close-up of aboral region in (A) showing arcuate spokes (arrows) and remains of ctenes (arrowheads); dark residues may represent gastric system. (C) Oral region in (A) (counterpart) showing flared oral skirt and membranous tissue supported by spokes (arrows). (D) Paratype (ELEL-SJ081563), a juvenile, showing spokes (arrows) and remains of ctene rows. (E) Holotype (ELI-JSCT0001). (F) Close-up of apical organ in (E) showing internal aboral canal and statolith remains. (G) Close-up of focus area in (E) showing remains of ctenes. (H) Paratype (ELI-JSCT0002). (I) Close-up of apical organ in (H). (J) Paratype (ELEL-SJ101932A) showing apical organ, body with spinose spokes, and oral region. (K) Close-up of oral region in (J) showing lappet-like structures. (L) Close-up of a spine (arrowed in J). (M) Close-up of aboral part in (J) showing apical plates, statolith, and radiating spokes (arrowheads). (N) Close-up of focus area in (M) showing a spine sheathed by membrane (arrows). ac, aboral canal; ao, apical organ; cr, ctene row; lp, lappet; or, oral region; os, oral skirt; pl, apical plates; sl, statolith. Arrowheads in (E), (G), and (H) indicate medial ridges of radiating lobes mantled by membranous fins. Scale bars, 5 mm (A to E, H, J, and M); 1 mm (F, G, I, K, L, and N).
Fig. 3
Fig. 3
Idealized three-dimensional models of Cambrian skeletonized ctenophores. (A to C) Side views of Gemmactena actinala gen. et sp. nov, Batofasciculus ramificans, and Thaumactena ensis gen. et sp. nov., respectively. (A′ to C′) Oblique aboral views corresponding to (A) to (C).
Fig. 4
Fig. 4
Phylogenetic relationship of fossil and extant ctenophores based on a comprehensive cladistic analysis (tables S2 and S3). The skeletonized ctenophores from the Chengjiang biota form a clade here described as the new class Scleroctenophora. The cladogram is a strict consensus of the three most parsimonious trees. Apomorphies (character number and state above and below nodes, respectively) are mapped on the cladogram. Tree length = 53; consistency index = 0.9231; retention index = 0.9394; rescaled consistency index = 0.8671. Illustrated taxa are marked in bold.

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