ARTICLE https://doi.org/10.1038/s41467-019-09059-3 OPEN A stem group echinoderm from the basal Cambrian of China and the origins of Ambulacraria Timothy P. Topper 1,2,3, Junfeng Guo4, Sébastien Clausen 5, Christian B. Skovsted2 & Zhifei Zhang1 Deuterostomes are a morphologically disparate clade, encompassing the chordates (including vertebrates), the hemichordates (the vermiform enteropneusts and the colonial tube-dwelling pterobranchs) and the echinoderms (including starfish). Although deuter- 1234567890():,; ostomes are considered monophyletic, the inter-relationships between the three clades remain highly contentious. Here we report, Yanjiahella biscarpa, a bilaterally symmetrical, solitary metazoan from the early Cambrian (Fortunian) of China with a characteristic echinoderm-like plated theca, a muscular stalk reminiscent of the hemichordates and a pair of feeding appendages. Our phylogenetic analysis indicates that Y. biscarpa is a stem- echinoderm and not only is this species the oldest and most basal echinoderm, but it also predates all known hemichordates, and is among the earliest deuterostomes. This taxon confirms that echinoderms acquired plating before pentaradial symmetry and that their history is rooted in bilateral forms. Yanjiahella biscarpa shares morphological similarities with both enteropneusts and echinoderms, indicating that the enteropneust body plan is ancestral within hemichordates. 1 Shaanxi Key Laboratory of Early Life and Environments, State Key Laboratory of Continental Dynamics and Department of Geology, Northwest University, 710069 Xi’an, China. 2 Department of Palaeobiology, Swedish Museum of Natural History, Box 50007104 05, Stockholm, Sweden. 3 Department of Earth Sciences, Durham University, Durham DH1 3LE, UK. 4 School of Earth Science and Resources, Key Laboratory for the study of Focused Magmatism and Giant Ore Deposits, MLR, Chang’an University, 710054 Xi’an, China. 5 Univ. Lille, CNRS, UMR 8198 – Evo-Eco-Paleo, 59000 Lille, France. Correspondence and requests for materials should be addressed to T.P.T. (email: [email protected]) NATURE COMMUNICATIONS | (2019) 10:1366 | https://doi.org/10.1038/s41467-019-09059-3 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-09059-3 chinoderms (pentaradially symmetrical forms) are one of known as Bed III14 and is Fortunian in age14–16 having been Ethe most familiar and ubiquitous of all animal groups. correlated with the Purella antiqua shelly fossil zone14 (Sup- Because of their sturdy calcitic skeletons, they have a rich plementary Figure 1). Carbon isotope chemostratigraphic fossil record, first appearing during Cambrian Stage 3 (about 520 studies support this age15,16. Ma ago)1. However, it was not until the advent of molecular analyses that there was a general agreement as to how echino- Description. Small (20–50 mm in height) bilateral animal having derms were related to other deuterostomes2–11. Molecular data a globular to conical multi-plated theca, two long organic walled consistently resolves echinoderms and hemichordates as sister feeding appendages, and a stalk divided into two morphologically taxa within the clade Ambulacraria, a sister group to the Chor- distinct zones (proximal and distal). The theca is covered with data2–5. Yet, the origins and early evolution of the group has been numerous irregular, ovoid to polygonal plates (Figs. 1a–c, 2a, c a source of considerable conjecture, not least because the radial and Supplementary Figs. 2a, 3a, d, g). Plates are up to 2.5 mm in body plan of echinoderms is quite different from the bilaterally length and width with an unknown original composition. In some symmetrical organization of hemichordates and chordates12.A specimens, partial recovery between adjacent plates suggests that pre-radial history of the echinoderms has been suggested, a the theca might have been imbricately plated (Fig. 2a and Sup- possibility supported by recent anatomical development ana- plementary Fig. 3a, c). However, plates seem to be grossly abutted lyses13. The fossil record has yet to resolve this debate, as the early in other specimens or areas, so that definite assumption over history of the clade remains poorly documented and the first plating type would be overstated (Fig. 1a and Supplementary echinoderms to emerge in Cambrian Stage 3 already appear Figs. 2a, 4b, d, h, 5a). Thecal plating is often preserved as slightly relatively derived1,2,12. Interpretation of characters at the base of dislocated (a possible alternative explanation for apparent the Ambulacraria is further complicated by the apparent diver- imbrication of plates) with juxtaposition of internal and external gent morphology of the two hemichordate groups2 and the body molds. Due to the variation in outer shape and size of individual plan of the ancestral ambulacrarian remains idealized. plates, plating was most probably irregularly arranged during life, Here we analyze the systematic affinity and phylogenetic with plates loosely embedded within tegument. The variable relationships of Yanjiahella biscarpa14 from the Yanjiahe For- shape of the theca (Figs. 1a–c, 2a and Supplementary Figs. 2a, 3a, mation in Hubei, China. Our analysis illustrates that Y. biscarpa is d, 4a–d, g–h, 5a, e, i) also supports this deduction. Some speci- a stem-group echinoderm, confirming that plating was acquired mens show an almost continuous transition between stalk and by echinoderms prior to pentaradial symmetry and that the early theca (Fig. 2f, g and Supplementary Figs. 4a–d, 5a, e, i), so only the members of the clade were bilaterally symmetrical. Yanjiahella change in plating marks that boundary between these areas, with biscarpa exhibits morphological characters that are shared with plates being absent in the stalk. Thecal plates have differentiated both enteropneusts and echinoderms, demonstrating that the smooth (inner) surface and an outer (external) surface ornament enteropneust body plan is ancestral within the Hemichordata. of parallel ribs (Fig. 1c, 2a and Supplementary Figs. 3a, c). The The mosaic of morphologies that this taxon displays may proximal stalk is cylindrical (Figs. 1a, d, 2a, f, g and Supple- illustrate the deepest roots of the Ambulacraria and is therefore mentary Figs. 2b–c, h, 3a, e, 4f, i, 5e, i) and tapers distally (Fig. 1a, crucial for interpreting the early history of the deuterostome e and Supplementary Figs. 2c, h, 4g, 5a, e, i). The proximal stalk is clade. transversely ridged (distance between two successive ridges about 100 µm); the ridges are usually very fine, but can be locally Results and discussion thickened (Fig. 1c, d, Supplementary Fig. 2b). The distal stalk is Systematic paleontology. not transversely ridged but finely, longitudinally striated (Fig. 1e, g and Supplementary Figs. 2e–h, 5h) and is otherwise in perfect Total-group Echinodermata continuity with the proximal stalk. The relative rigidity of the Class, Order, Family indet. stalk seems to decrease distally as the proximal part is generally Yanjiahella biscarpa Guo, Li, Han, Ou, Zhou and Zheng almost straight with accentuated folds (Figs. 1, 2 and Supple- (2012). mentary Figs. 2, 3, 5a, e, i), although it is sometimes gently curved distally (Fig. 1 and Supplementary Fig. 2), while the striated distal Yanjiahella biscarpa;Guoetal.(2012),p.793,Figs.2k–m, 3c. zone of the stalk is invariably curved and looped (Figs. 1a, 2a and – Yanjiahella ancarpa;Guoetal.(2012),p.793,Figs.2a c, 3a. Supplementary Figs. 2a, 3a, 4g, 5a, e, i). A median, internal Yanjiahella monocarpa; Guo et al. (2012), p. 795, structure, visible from the posterior margin of the theca extends Figs. 2d–j, 3b. through the muscular stalk (Fig. 2a, d, f and Supplementary Figs. 5a–d). This structure is interpreted as the digestive tract and 14 Holotype. ELI-HS722 (see Guo et al. , Fig. 2k). Originally it continues through the proximal stalk region into the distal zone three species were nominally described in the same publica- of the stalk (Fig. 2d and Supplementary Figs. 4g, 5a–d). However, 14 “ ” tion , based on the number of preserved arms (here termed the digestive tract always disappears before the posterior extre- feeding appendages). However, it is clear that the three species mity of the distal stalk (Fig. 2d and Supplementary Figs. 4g, share the same morphological features, including thecal and 5a–d). This region of the distal stalk that lacks the digestive tract stalk characters and the number of appendages is simply a is interpreted as a post-anal anchoring organ. The digestive tract taphonomic artifact. We here, as the First Reviser, consider is not always discernible in the upper region of the distal stalk the three species to be subjective synonyms, and under Art. (Fig. 1e and Supplementary Fig 2), possibly due to taphonomic 24.2.2 of the International Code of Zoological Nomenclature factors, but its detection may also be masked by the strong, (ICZN), we give precedence to the species name Y. biscarpa parallel longitudinal striations of this part of the distal stalk (referring to the possession of two feeding appendages). (Fig. 1e and Supplementary Figs. 2e, g–j). Two appendages pro- Material. Thirty five specimens. ject from opposing lateral sides of the thecal margin. The Locality. Gunziao Section, Sandouping, Yichang, Hubei pro- appendages are long and slender and can extend up to 43 mm in vince, China (Supplementary Figure 1). length and may reach 0.6 mm in diameter. The appendages are Stratigraphy. Specimens recovered from gray-black, silty not covered by plates, but sometimes transverse lines are obser- shale intercalations in a carbonaceous limestone of the Yan- vable, which could represent cases when two appendages are jiahe Formation14. This part of the Yanijahe Formation is preserved juxtaposed to each other (Fig. 2a and Supplementary 2 NATURE COMMUNICATIONS | (2019) 10:1366 | https://doi.org/10.1038/s41467-019-09059-3 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-09059-3 ARTICLE a b c p theca p t s fa ps dt fa ds ps de f dt ps dt ps g ps ds dt ds Fig.