A stem group echinoderm from the basal Cambrian of China and the origins of Ambulacraria

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 deuterostomes 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.

Theca, feeding appendages and stalk. d. Detail of distal stalk and post anal anchoring organ. e -h. Specimen HS998A (e-h; part) and Specimen HS998B (i-l; counterpart). e. Specimen with muscular stalk, theca and feeding appendages.
f. Differentiated proximal and distal stalk. g. Detail of theca and proximal stalk. h. Detail of distal stalk with fine striations. i. Specimen showing a muscular stalk, theca and feeding appendages. j. Differentiated proximal and distal stalk. k. Detail of theca and proximal stalk. l. Detail of the proximal to distal stalk region. Scale bars 5 mm (a-c, f, j), 1 mm (d, l), 1 cm (e, i), 2 mm (g, k) and 0.5 mm (h). Abbreviations: ds, distal stalk; dt, digestive tract; fa, feeding appendage; m, mouth; p, plate; ps, proximal stalk; paao, post anal anchoring organ; s, muscular stalk; t, theca. Taxa: Twenty-one taxa have been included in our analysis, incorporating fourteen total group Echinoderms (including Yanjianella biscarpa), four enteropneust taxa (including both Spartobranchus tenuis and Oesia disjuncta from the Cambrian Burgess Shale Lagerstätte), two pterobranch taxa and the Cephalochordates (used as the outgroup). The taxa encompass all the major echinoderm body plans present in the early to middle part of the Cambrian, such as the bilateral symmetrical ctenocystoids (coded from Courtessolea) and the asymmetrical cinctans (coded from Asturicystis) and solutes (coded from Castericystis). However, we have excluded the stylophorans, whose interpretation remains highly contentious [4][5][6][7][8][9] . We included Pleurocystites (an Early Ordovician to Middle Devonian glyptocystitid rhombiferan) and its probable stem-relative Ubaghsicystis (Cambrian Series 3, Wuliuan), as both taxa share some similarities with Yanjianella (two arms, globular to flattened theca, probable muscular appendage) 10 . Different pelmatozoan representatives have been added to the study such as the Ordovician  [13][14][15][16][17] . The relationships between living enteropneust families is not the focus of this study and as we could provide no further morphological details than that which has already been presented in previous studies 13

Possession of a dorsal collar nerve cord (neurocord): no (0); yes (1)
Chordates possess a dorsal hollow nerve cord and hemichordates possess a neurocord. Although the homology of these structures is unclear 25 , the collar cord of enteropneusts has been considered by some to be homologous with the neurulation in chordates 26 . This discussion appears far from settled, however for the purpose of this analysis we have united them here under a single character state.

Body plan: bilaterial (0); asymmetric (1); radial (2)
The body plan of cinctans varies from asymmetrical to nearly bilaterally symmetrical, with symmetry expressed in the shape of the theca and the size/ number of the anterior feeding grooves [27][28] . This is most likely related to their asymmetric development of the hydrocoel during their metamorphosis from larva to adult [27][28] . As such, cinctans have been here coded as exhibiting an asymmetric body plan.

Pentaradial symmetry developed: no (0) yes (1)
Of those echinoderm forms with a radial body plan Helicoplacus does not show pentaradial symmetry, instead showing three-fold symmetry 23 .

Possession of symmetrical mesocoels (hydrocoels) as adult: no (0); yes (1)
Hemichordates and echinoderms have a homologous mesocoel (hydrocoel in echinoderms). This is paired and symmetrical in Hemichordates. Most echinoderms have an asymmetric hydrocoelom, the right mesocoel regressing (to complete degeneration in crown groups). Even if a bilateral symmetry is seen in Yanjianella biscarpa and the ctenocystoids the presence of a paired, symmetrical mesocoel can only be at best suggested. As such, the presence of paired hydrocoel in the apparently symmetrical Yanjianella biscarpa cannot be accurately assessed (scored as ?).

Torsion resulting in vertical stacking of body coeloms and complete suppression of right hydrocoel development in adult form: no (0); yes (1)
Echinoderms have a unique ontogeny where the organism undergoes a phase of torsion in development that rotates the axis of the developing adult 29 . Although no ontogenetic information regarding Yanjiahella biscarpa is known, the clear Anterior-Posterior (A-P) axis in all specimens, suggests that the taxon did not undergo torsion.
The A-P axis in solutes has been used to support a pre-torsion history of the echinoderms 29 and it has been suggested that the helicoplacoids represent the earliest echinoderms to have undergone complete torsion, as both dorsoventral and left-right body axes are lost and the hydrocoel displays a radial organization 29 . We follow this interpretation herein and have coded all bilateral and asymmetric total group echinoderm taxa (Yanjiahella biscarpa, ctenocystoids, cinctans and solutes) as not having undergone complete torsion.

Pharyngeal gill slits and/or pore(s) present: no (0); yes (1)
A recent study 21 regarding gill development genes, supported the homology of echinoderm and hemichordates gills. Such gills slits and, or pores have been described in stylophoran echinoderms (not included in this analysis) and there are strong morphological indications that such structures are present in cinctans and ctenocystoids [30][31] (character state for both taxa coded here as present). Poor plate preservation does not allow an accurate assessment regarding the presence of gills/pore in Yanjianella biscarpa. Thecal plates of Yanjianella biscarpa might not have abutted during life so it is possible that gills may have opened between the plates, within the soft tegument (consequently character state is questioned herein).

Gill slits have secondary (or tongue) bars: no (0); yes (1)
Gill bars are a morphological feature shared by enteropneusts, including the two Cambrian taxa (Oesia and Spartobranchus) where such structures are among the most common and well-preserved internal features [18][19][20] . The Cambrian hemichordate taxa are tubiculous organisms [18][19][20] . Even if all four families of extant enteropneust can secrete mucous "tubes" when stressed, this structure is not homologous to those of their Cambrian relatives 19 .