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. 2017 Dec 20;284(1869):20172188.
doi: 10.1098/rspb.2017.2188.

The Early Cambrian Fossil Embryo Pseudooides Is a Direct-Developing Cnidarian, Not an Early Ecdysozoan

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Free PMC article

The Early Cambrian Fossil Embryo Pseudooides Is a Direct-Developing Cnidarian, Not an Early Ecdysozoan

Baichuan Duan et al. Proc Biol Sci. .
Free PMC article

Abstract

Early Cambrian Pseudooides prima has been described from embryonic and post-embryonic stages of development, exhibiting long germ-band development. There has been some debate about the pattern of segmentation, but this interpretation, as among the earliest records of ecdysozoans, has been generally accepted. Here, we show that the 'germ band' of P. prima embryos separates along its mid axis during development, with the transverse furrows between the 'somites' unfolding into the polar aperture of the ten-sided theca of Hexaconularia sichuanensis, conventionally interpreted as a scyphozoan cnidarian; co-occurring post-embryonic remains of ecdysozoans are unrelated. We recognize H. sichuanensis as a junior synonym of P. prima as a consequence of identifying these two form-taxa as distinct developmental stages of the same organism. Direct development in P. prima parallels the co-occuring olivooids Olivooides, and Quadrapyrgites and Bayesian phylogenetic analysis of a novel phenotype dataset indicates that, despite differences in their tetra-, penta- and pseudo-hexa-radial symmetry, these hexangulaconulariids comprise a clade of scyphozoan medusozoans, with Arthrochites and conulariids, that all exhibit direct development from embryo to thecate polyp. The affinity of hexangulaconulariids and olivooids to extant scyphozoan medusozoans indicates that the prevalence of tetraradial symmetry and indirect development are a vestige of a broader spectrum of body-plan symmetries and developmental modes that was manifest in their early Phanerozoic counterparts.

Keywords: Cambrian; Cnidaria; Ecdysozoa; Pseudooides; development; embryo.

Conflict of interest statement

We declare we have no competing interests.

Figures

Figure 1.
Figure 1.
Tomographic surface models of Pseudooides specimens preserving the initial stages of delineation of the ‘germ band’ (GMPKU3100). (a–e) SRXTM surface renderings. (a) Left, (b) central and (c) right views of the ‘germ band’; (d) lateral view, with ‘germ band’ top and centre; (e) opposing pole of the specimen. (f–h) SRXTM rendering of the longitudinal furrow (blue), transverse furrow (gold) and the basal folds (green, red): (f) central view of the ‘germ band’; (g) lateral view of the longitudinal furrow, (h) lateral view of the transverse furrow. Scale bar, (a–h) 52.5 µm. (Online version in colour.)
Figure 2.
Figure 2.
Tomographic surface models of Pseudooides specimens preserving the ‘germ band’. (a–e) SRXTM renderings of specimen preserved with complete ‘germ band’ with a pinch at mid-length (GMPKU3091). (a) Left, (b) central and (c) right views of ‘germ band’; (d) lateral view of the specimen, with ‘germ band’ top and centre; (e) opposing pole of the specimen. (f–j) SRXTM renderings of specimen with preserved complete ‘germ band’ without a pinch at mid-length (GMPKU3099). (f) Left, (g) central and (h) right views of the ‘germ band’; (i) side view of the specimen, with the ‘germ band’ top and centre; (j) opposing pole of the specimen. Scale bar, (a–e) 81 µm, (f–j) 66 µm.
Figure 3.
Figure 3.
Pseudooides specimens with furrows of the ‘germ band’. (a,b,d–i) SRXTM renderings of the specimen with delicate ‘germ band’ furrows preserved (GMPKU3099). (a) SRXTM renderings of the complete ‘germ band’ (indigo-blue); (b) the virtual section shows that the ‘inter-metameric’ furrows are largely surface features (arrows); (d) left, (e) central and (f) right views of the marginal furrows of the ‘germ band’ with surrounding material removed; (g) left, (h) central and (i) right close-ups of the tip end of the ‘germ band’. (c) The virtual section positioned between the pinch and one end of the ‘germ band’ shows the depth of the marginal furrow and the median furrow (arrows, GMPKU3094). Scale bar, (a,b) 100 µm, (c) 93 µm, (d–f) 62 µm, (g–i) 52 µm. (Online version in colour.)
Figure 4.
Figure 4.
Pseudooides specimens display the unfolding of the furrows. (a–c) Specimen with the unfolding median furrow (GMPKU3096). (a) The folded end of the ‘germ band’; (b) the middle part of the ‘germ band’ showing the median furrow starting to unfold; (c) the unfolding end of the ‘germ band’ with paired ‘metameres’ separated. (d,e) Specimen with a separated median furrow (GMPKU3091). (d) Front view of the ‘germ band’; (e) close-up of (d). (f–h) Specimen with a broken ‘germ band’ surface (GMPKU3104). (f) SEM image of the specimen, grey line marking the position of the virtual section of (h); (g) close-up of the exposed median furrow; (h) virtual section showing the extension of the putative ectoderm layer within the embryo. Scale bar, (a,b) 100 µm, (c) 105 µm, (d) 123 µm, (e) 78 µm, (f) 115 µm, (g) 70 µm, (h) 124 µm.
Figure 5.
Figure 5.
SEM images of post-embryonic ‘Hexaconularis sichuanensis' stages of P. prima. (a–d) GMPKU3132. (a) Lateral view of the polyp theca; (b) oblique view of the theca showing the concave base of the retained embryonic stage; (c) side view of the concave base of the retained embryonic stage; (d) close-up of the retained embryonic stage showing the four lateral cuticular folds represented as furrows in the ‘germ band’ of the embryo. (e) GMPKU3133; lateral view of the retained embryonic stage. (f–g) GMPKU3134. (f) Lateral view of the polyp theca; (g) close-up of the retained embryonic stage with the four lateral cuticular folds (arrows) reflecting the furrows in the ‘germ band’ of the embryo. (h–k) GMPKU3135. (h) Lateral view of the polyp theca; (i) close-up of the retained embryonic stage with the four lateral cuticular folds (down arrows) reflecting the furrows and the pinch (up arrow), respectively, in the ‘germ band’ of the embryo. Scale bar, (a,b) 409 µm, (c) 169 µm, (d) 119 µm, (e) 132 µm, (f) 406 µm, (g) 104 µm, (h) 444 µm, (i) 95 µm, (j) 189 µm, (k) 73 µm.
Figure 6.
Figure 6.
Development and phylogenetic affinity of P. prima. (a–h) Diagrammatic characterization of embryonic (a–d) and post-embryonic (e–h) development. (a) Delineation of the aperture; (b) opening of the central pinch of the aperture; (c–d) apertural and lateral view, respectively, at the first opening of the aperture; (e–f) apertural and lateral view, respectively, at the unfolding of the lateral apertural extremes and lateral compression of the original spherical embryonic tissue; (g–h) apertural and lateral view, respectively, of the first stages of post-embryonic thecal growth at the apertural margin. (i) Phylogenetic relationships among living Cnidaria and the direct-developing medusozoans considered here, including P. prima, based on a Bayesian phylogenetic analysis of phenotypic characters. Codings for Pseudooides are based on the interpretation presented in this study. Pseudooides, conulariids and the olivooids are resolved as a clade closely related to the living coronate scyphozoans, including Nausithoe. Numbers adjacent to nodes represent their posterior probabilities.

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