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Home , Albumares, Coelenterata, Eoandromeda, Eumetazoa, Fasciculus, Rangea

& DEVELOPMENT 13:5, 408–414 (2011) DOI: 10.1111/j.1525-142X.2011.00499.x

Eoandromeda and the origin of

Feng Tang,a,b,∗ Stefan Bengtson,c,∗ Yue Wang,d Xun-lian Wang,e and Chong-yu Yina,b a Institute of Geology, Chinese Academy of Geological Sciences, Beijing, 100037, China b Key Laboratory of Stratigraphy and Paleontology, Chinese Academy of Geological Sciences, Beijing, 100037, China c Department of Palaeozoology and Nordic Center for Earth Evolution, Swedish Museum of Natural History, Box 50007, SE-104 05, Stockholm, Sweden d School of Resources and Environment, Guizhou University, Guiyang, 550003, China e School of Earth Sciences and Resources, China University of Geosciences, Beijing, 100083, China ∗Authors for correspondence (email: [email protected] and [email protected])

SUMMARY The octo- lacking crown-group synapomorphies such as , sta- brachiata had a high conical body with eight arms in he- toliths, polar fields, and biradial symmetry. It probably had a licospiral arrangement along the flanks. The arms carried pelagic mode of life. The early appearance in the fossil record transverse bands proposed to be homologous to ctenophore of octoradial ctenophores is most consistent with the Planulo- ctenes (comb plates). Eoandromeda is interpreted as an zoa hypothesis (Ctenophora is the sister group of + early stem-group ctenophore, characterized by the synapo- ) of metazoan phylogeny. morphies ctenes, comb rows, and octoradial symmetry but

INTRODUCTION The new data on Eoandromeda suggest that it represents a stem-group ctenophore, implying that ctenophores were Megascopic biotas of the 635–541 Ma (million years ago) among the first eumetazoan lineages to appear, and that Ediacaran Period represent the foreplay to the “ planktic predators were present in the ecosystems already Explosion” of , but Ediacaran are contentious during the heyday of the . as to their affinity (e.g., Dzik 2003; Seilacher et al. 2003; Narbonne 2005; Fedonkin et al. 2007; Budd 2008). The oc- toradial fossil Eoandromeda octobrachiata Tang et al. 2008 was described in two-dimensional preservation from 580– RESULTS 551 Ma black shales of the Doushantuo Formation in southern China (Tang et al. 2008; Zhu et al. 2008) and in Twelve specimens are figured in Fig. 1; three (Fig. 1B–E) semi-relief on bed soles in the Ediacara Member of the were previously figured by Wang et al. (2008) and are re- Rawnsley Quartzite in South Australia (Zhu et al. 2008). figured herein to illustrate some of the anatomical features. Both Tang et al. and Zhu et al. noted possible relationships Like the previous Doushantuo specimens (Tang et al. 2008; to the Ctenophora (comb jellies) and the Cnidaria, but left Zhu et al. 2008), the new ones are preserved as carbonaceous the question of systematic assignment open. films in a silty shale. Zhu et al. (2008) noted that of 38 Aus- Recently collected material from the type locality of E. tralian specimens, where the up versus down orientation was octobrachiata elucidates the of Eoandromeda and known, all had dextrally coiling arms (i.e., tips pointing in reveals new features that help a direct comparison with Re- the clockwise direction) when viewed from above. Assuming cent and fossil ctenophores. Cambrian ctenophore-like fossils that this symmetry holds true also for the Chinese specimens have been found in the ca. 505 Ma (Conway (where the stratigraphic orientation is mostly unknown), Morris and Collins 1996) and the ca. 520 Ma Chengjiang Fig.1E,F,K,L,andMshowthefossilfromabove;Fig.1A– (Chen and Zhou 1997; Hou et al. 2004; Hu et al. 2007) de- D, G, and H from below. posits, and the report of a ctenophore embryo from the ca. Specimens hitherto reported from China and Australia 535 Ma Kuanchuanpu Formation extended the record to are symmetrically compressed disks. The specimens in near the beginning of the Cambrian (Chen et al. 2007). Edi- Fig. 1H–J, however, seem to represent obliquely to later- acaran records are problematic, however, notwithstanding ally compressed specimens. The one in Fig. 1H clearly be- Dzik’s (2002, 2003) ingenious attempts to relate sedentary longs to E. octobrachiata, but the center of radiation of the frond-like organisms (“petalonomans”) to the . arms is offset toward the periphery, suggesting an oblique

408 C 2011 Wiley Periodicals, Inc. Tang et al. The origin of Ctenophora 409

Fig. 1. Carbonaceous compressions of Eoandromeda octobrachiata. Scale bars 5 mm. Specimens in Institute of Geology, Chinese Academy of Geological Sciences, Beijing (prefix JK); School of Resources and Environment, Guizhou University, Guiyang (prefix JK-A); and School of Earth Sciences and Resource, China University of Geosciences, Beijing (prefix WH-A). (A) JK10909. (B and C) WH-A-04178. C—close-up of B; arrows point to transverse bands. (D) WH-A-04023. (E) WH-A-04209. (F) WH-A-04719. (G) JK-A-55-0025. (H) JK08014. (I) JK-A-54-0089. (J) JK08016. (K) JK-A-40-0013. (L) JK10903. (M) JK10329. 410 EVOLUTION & DEVELOPMENT Vol. 13, No. 5, September–October 2011

Fig. 2. Reconstruction of Eoandromeda octobrachiata. Artwork Javier Herbozo. compression of a high dome. The specimen in Fig. 1I has a agenetic halo), shows that the spiral morphology was fully rounded triangular shape. Although the anatomical features developed already at this growth stage. are poorly preserved, there is clear evidence of spiral arms The central part inside the arms is mostly indistinctly in the lower part. The elliptical specimen in Fig. 1J shows preserved, but two specimens (Fig. 1L and M) show a ring- even less anatomical details, but the longitudinal streaks and like structure, ca. 3 mm in diameter, connected to the inner the clear area near the top indicate that this specimen too is ends of the arms through a narrow neck. In Fig. 1L, the ring, a preservational variety of E. octobrachiata. We thus inter- neck, and central parts of the arms are made up of a lighter pret these three specimens as oblique to lateral compressions (thinner?) material than the rest of the arms. of an originally conical body, about as high as wide, with a The specimens figured herein represent different modes of bluntly rounded apex, and with arms curving down along its taphonomic degradation. The most conspicuous difference flanks (Fig. 1I). regards the expression of the transverse bands of the spiral Zhu et al. (2008) noted that both Chinese and Australian arms. They vary from distinct (Fig. 1A, C, E, F, H, and specimens show evidence of partitions in the arms and con- M), through more indistinct and frayed (Fig. 1D and G), cluded that “the live organism consisted of eight spiral tubu- to largely absent (Fig. 1I–L and parts of the specimens in lar arms with possible transverse structures.” Our new mate- Fig. 1B and H). The fact that different modes of expression rial confirms the existence of transverse structures, showing can be seen in a single specimen (e.g., Fig. 1B) indicates that them to be band-like elements that are regularly distributed this is a taphonomic rather than taxonomic difference. The along the arms (Fig. 1A, C–F, H, and M). The bands are transverse bands, when present, tend to be expressed in a 0.3–2 mm apart and roughly perpendicular to the arms; in darker material than the arm itself, which in turn is darker one specimen, they are particularly distinct and can be seen than the interband area, which in turn is darker than the to keep their perpendicular orientation even when an arm matrix surrounding the specimen (see, e.g., Fig. 1A and H). forms an angular kink (Fig. 1A, upper left). In two speci- They sometimes extend beyond the visible boundaries of mens (Fig. 1D and G), the bands are crescent-shaped, convex the arms, giving the latter a frayed edge (Fig. 1M). These side facing centripetally (Fig. 1D and G, left) or centrifugally observations suggest that the transverse bands represent a (Fig. 1G, right). distinct from that of the arms proper. The tissue between the spiraling arms is usually expressed Other preservational differences are more subtle and by a dark stain, as in the holotype (Tang et al. 2008, Fig. 2A– mostly concern the distinctness of the arms and the expres- G). The arms are consequently not free -like struc- sion of the tissues within and between the arms. The specimen tures but are incorporated into the body. The specimen in in Fig. 1L has lighter central regions of the arms, suggesting Fig. 1K, the smallest one found (surrounded by a light di- that the center of the arms was thinner or less solid than the Tang et al. The origin of Ctenophora 411

periphery. Some specimens show an aggregation of irregu- Fig. 1L, on the contrary, shows arms with the interior lighter larly sized black grains up to 300 μm in size between the than the rim, suggesting that the interior was less dense. Zhu spiraling arms (Wang et al. 2008, Fig. 3H). These are ab- et al. (2008) interpreted the Australian specimens to show sent from the adjacent shale and may represent taphonomic tubular arms, possibly with transverse structures, and some- degradation of the interarm tissue. what deformed by compaction. A tubular structure is not The two laterally preserved specimens (Fig. 1I–J) have at odds with the preservation in the Doushantuo specimens, poorly expressed arms. This is probably at least partly due to and a homology with the eight meridional canals underlying the fact that they represent two arm-bearing flanks adpressed the eight comb rows in modern ctenophores (Ruppert et al. to one another. 2004, p. 193, Figs 18–13, 18–14) is plausible. These canals are part of the gastrovascular cavity system. The arms underlying the presumed comb rows in Eoandromeda would under this DISCUSSION interpretation constitute the major part of the gastrovascu- lar system. In comparison, the meridional canals in modern The new material strengthens the comparison between Eoan- ctenophores are not as prominent. dromeda’s characters and those of the Ctenophora (Tang The central ring seen in two specimens (Fig. 1L and M) et al. 2008; Zhu et al. 2008). The transverse bands along resembles in size, shape, and position the aboral ring in the the arms are strikingly similar to ctenes (comb plates) of Middle Cambrian Burgess Shale ctenophore Ctenorhabdo- modern ctenophores. Ctenes consist of giant cilia beating tus capulus (Conway Morris and Collins 1996, Fig 23c, d). as a unit. They are arranged in comb rows, which are rela- As in Eoandromeda, the ring in Ctenorhabdotus is joined to tively resistant structures that may remain recognizable in the eight outward radiating strands connected with comb rows stomach of a predator (Arai 2005). The ctenes are 0.5–2 mm (there are 24 such rows in Ctenorhabdotus). Another Burgess long, depending on species, and the distance between them Shale ctenophore, Xanioascus canadensis, has a similar ab- is about one-half to two-thirds of the ctene length (Tamm oral ring, about three times wider than the ones in Eoan- 1973). These ctene dimensions are comparable with the dis- dromeda and Ctenorhabdotus (Conway Morris and Collins tance between bands in Eoandromeda, and the size range 1996, Figs 6, 7D, E, 11). These ring structures appear to rep- of Eoandromeda is well within that of modern ctenophores. resent tissues in continuity with those underlying the comb Eoandromeda shows no direct evidence of a ciliary compo- rows. sition, but the thin diameter of cilia (about 0.2 μm) Figure 2 shows our revised reconstruction of E. octo- and the relative coarseness of shale preservation would make brachiata. Tang et al. (2008) and Zhu et al. (2008) regarded the preservation of ciliary fabric in Eoandromeda unlikely. Eoandromeda as benthic, because of the apparent absence of An alternative interpretation, that the transverse bands adaptations for swimming and because of its consistent ori- represent impressions of a radiating fabric on the body sur- entation on the bedding planes. If the transverse bands rep- face, similar to that present in the probably related triradial resent beating flaps analogous or homologous to ctenophore , as well as in the possibly also related Anfesta, ctenes, however, their position along spiraling tracts around ,andSkinnera (Fedonkin et al. 2007), is unlikely the flanks of the conical body would suit a function as a for several reasons: (1) although preservationally different swimming device, propelling the animal in a spiraling motion from the arms, the bands are not present in the interval be- through the water column (cf. Wang et al. 2008). Several liv- tween the arms; (2) in an arm with a kink, the bands change ing ctenophore species, for example, Beroe (Matsumoto and directions accordingly (Fig. 1A, upper left); (3) in the central Harbison 1993) and Mnemiopsis (Craig and Okubo 1990) parts of the body, where the arms are not semi-parallel to the swim in a spiral motion, although this is not related to a spi- body circumference, the bands traverse the arms rather than ral disposition of the comb rows but rather to the ctenes in follow the radial direction (e.g., Fig. 1A, D, F, G, and M); adjacent rows beating out of phase (Craig and Okubo 1990). (4) there is no close correspondence in position and direction Eoandromeda, however, does not display the biradial sym- between bands occupying equivalent positions in adjacent metry of crown-group ctenophores. It lacks the polar fields arms; and (5) the crescents oriented in opposing directions and tentacles that externally express this symmetry in most (Fig. 1D and G) suggest that the structures could be flapped modern ctenophores, and there is also no evidence of a bira- in either direction. We therefore interpret the bands as fea- dially symmetrical gastric canal system. Tentacles are absent tures connected to the arms. also in Cambrian taxa (Conway Morris and Collins 1996; The nature of the arms themselves is not clear from the Chen et al. 2007; Hu et al. 2007); polar fields may possibly preservation of the Doushantuo specimens. The arms are be present in the Cambrian, but the evidence for this is weak usually darker in the middle, but this seems to be mostly an (Conway Morris and Collins 1996). There are no remains effect of the dominance of the transverse bands along the of statocysts in Eoandromeda and no evidence of the aboral center of the arms (e.g., Fig. 1A). The unusual specimen in dome that houses the statocysts in modern ctenophores and 412 EVOLUTION & DEVELOPMENT Vol. 13, No. 5, September–October 2011

does not help resolve any of the above phylogenetic alter- natives. If correctly interpreted by us, Eoandromeda gives only a minimum age of 551–580 Ma (Zhu et al. 2008) of the ctenophore lineage, and this would accommodate even the hypothesis, the one that predicts the lat- est appearance of the lineage, since recent estimates based on well-calibrated studies indicate a more than 600 Ma age of the Bilateria lineage (Peterson et al. 2008). Nonetheless, Eoandromeda helps to establish the po- larity of character evolution in the ctenophore lineage and Fig. 3. Alternative views of basal metazoan relationships (Wall- thus throws light on the evolutionary pattern. berg et al. 2004; Dunn et al. 2008), poriferan (e.g., The appearance in the Ediacaran of a stem-group Peterson et al. 2008) not accounted for. ctenophore lacking outward signs of bilateral (or biradial) symmetry indicates that bilateral symmetry was never a fac- appears to be present in Cambrian forms such as Ctenorhab- tor in ctenophore evolution. This is also suggested by the fact dotus (Conway Morris and Collins 1996), Maotianoascus, that Ctenophora lack the Hox genes that are crucial in de- and Trigoides (Hu et al. 2007). termining the anterior–posterior patterning of the bilaterian Eoandromeda thus seems to have possessed characters body and are also present in cnidarians (Ryan and Baxeva- unique to ctenophores, but lacked several autapomorphies nis 2007); there is in fact no direct evidence that ctenophores of the crown group. Furthermore, a spiral arrangement of evolved from animals with an established anterior–posterior comb rows is not known in any Phanerozoic ctenophore. axis, as proposed by Conway Morris and Collins (1996). Eoandromeda may therefore be interpreted as a stem-group In any case, the biradial symmetry characteristic of modern ctenophore. As one of the earliest metazoans in the fossil (and possibly Cambrian; vide Conway Morris and Collins record, it can be brought to bear on the phylogenic position 1996) ctenophores is fundamentally different from bilateral of modern ctenophores. symmetry, and none of them is likely to have given rise to the The position of Ctenophora in the metazoan clade is un- other (Manuel 2009). clear, owing to conflicting results from morphological and Most Cambrian ctenophores have considerably more than molecular . Wallberg et al. (2004) summarized eight comb rows, apparently in multitudes of eight (Conway the main competing alternatives as the Coelenterata hypoth- Morris and Collins 1996; Hu et al. 2007), but an octora- esis (Ctenophora is the sister group of Cnidaria), the Acro- dial pattern may still be clearly visible in the central struc- somata hypothesis (Ctenophora is the sister group of Bilate- tures (e.g., Conway Morris and Collins 1996, Fig. 23a–d). ria), and the hypothesis (Ctenophora is the sister The post-Cambrian fossil record of ctenophores is exceed- group of Cnidaria + Bilateria) (cf. Fig. 3A–C). Based on ingly sparse, but two taxa possess a “modern” their analysis of published 18S rRNA data, they concluded anatomy with eight comb rows and a pair of tentacles (Stan- that the Planulozoa hypothesis had the best support. Most ley and Sturmer¨ 1983, 1987). A study of 18S rRNA sequences earlier work based on rRNA/rDNA data (e.g., Peterson and showed that modern ctenophores are closely similar to each Eernisse 2001; Podar et al. 2001) had given similar conclu- other genetically, suggesting that all are derived from a rela- sions (i.e., the Ctenophora are basal to a group including the tively recent common ancestor (Podar et al. 2001). Cnidaria and Bilateria). Morphological data, however, fa- Conway Morris and Collins (1996) suggested that post- vor the Acrosomata hypothesis, rendering the Cnidaria more Cambrian ctenophores with eight comb rows are derived basal than the Ctenophora in the metazoan tree (Peterson from Cambrian multirow forms by reduction of the num- and Eernisse 2001). ber of rows. The existence of an Ediacaran stem-group The last few years have added further complexity. A re- ctenophore with eight rows, and of some Cambrian forms cent phylogenomic study (Philippe et al. 2009) has revived with eight (Hu et al. 2007), would seem to render such a hy- the Coelenterata hypothesis. Analyses based on expressed pothesis redundant and would rather suggest that supranu- sequence tags conversely yielded the surprising result that meral comb rows in some Cambrian forms represent autapo- Ctenophora are the sister group of all other metazoans, in- morphies of extinct stem-group forms. cluding (the “Metazoa hypothesis” in Fig. 3D; Dunn Other stem-group ctenophores deviating from the eight- et al. 2008; Hejnol et al. 2009), but this has been challenged row pattern seem to occur in the Ediacaran. The classical as being due to insufficient sampling and long-branch attrac- Ediacaran fossil Tribrachidium has a triradially symmetrical tion (Pick et al. 2010). disk-like morphology with three radiating spiral arms; the Although Eoandromeda is one of the earliest indubitable less well-known Ediacaran forms Anfesta, Albumares,and metazoans in the fossil record, its early appearance in itself Skinnera are similar in morphology but have less prominent Tang et al. The origin of Ctenophora 413

radiating elements (Fedonkin et al. 2007). Wang et al. (2008, rows, and octoradial symmetry. It apparently lacked synapo- Fig. 3A–C) and Zhu et al. (2008, Fig. 1H) figured such trira- morphies of the crown group, such as tentacles, statoliths, dial forms from the Doushantuo Formation, showing them polar fields, and biradial symmetry. to be preserved in the same manner as Eoandromeda.Tang Eoandromeda had a conical body and spiral arms with et al. (2008) discussed the possible relationships with Eoan- comb rows descending down the flanks. It had a pelagic dromeda, drawing attention to the fact that the presence of mode of life, propelling itself in the water column by means three versus eight spiral arms resembled the pattern seen in of the eight comb rows. Although no traces of a gut have leaf phyllotaxis. Whether or not the patterns in the Ediacaran been observed, the mode of life may have been predatory, as fossils may be referred to such developmental mechanisms, in modern ctenophores and other pelagic animals of similar the triradially symmetrical ones, particularly Tribrachidium, morphology (e.g., scyphozoan medusae). are likely to represent another branch of the stem-group Tribrachidium is morphologically closely similar to Eoan- ctenophores. Thus, the n-radial (cf. Manuel 2009) symmetry dromeda and differs mainly in its triradial, rather than octor- of Ediacaran–Cambrian stem-group ctenophores is unstable adial, symmetry. It likely belongs to the same clade. Anfesta, with regard to the value of n, although n = 8 seems to be the Albumares,andSkinnera may also belong within this clade. pervading theme. The lack of traces of bilateral symmetry also in early stem- Xiao and LaFlamme (2008) suggested that the Ediacaran group ctenophores does not support any of the phylogenetic assemblage of tri-, tetra-, penta-, and octoradial forms might schemes that nest Ctenophora among the bilaterally sym- represent a variety of body symmetries that constituted a metrical Cnidaria and Bilateria, that is, the Coelenterata or diploblastic stock from which both radially and bilaterally Acrosomata hypotheses (Fig. 3A and B). Eoandromeda does symmetrical eumetazoans arose. Their phylogenetic diagram not add any new evidence to distinguish between the Plan- (Xiao and Laflamme 2008, Fig. 2) indicates unidentified ulozoa and Metazoa hypotheses (Fig. 3C and D), although members of this group as stem-group , stem- theprevalenceofn-radial, in particular octoradial, symmetry group Cnidaria, and stem-group Bilateria, respectively. This among early ctenophores and cnidarians is more consistent was clearly not intended as a testable phylogenetic hypoth- with the Planulozoa hypothesis. esis; in fact, the authors referred to it only as a possible scenario, admitting that these fossils are in “phylogenetic Acknowledgments limbo.” The ctenophoran synapomorphies identified herein Yu-sheng Xing and four anonymous reviewers of earlier manuscript help to break this limbo. versions provided valuable comments. Javier Herbozo did the art- Dzik (2002, 2003) has suggested that certain Ediacaran work for Fig. 2. Fieldwork and research were funded by the Key frond-like organisms represent sedentary ctenophore ances- Laboratory of Stratigraphy and Paleontology, Chinese Academy of Geological Sciences (grants no. JB0705, JB0902), the Institute tors lacking comb rows. This admittedly problematic sce- of Geology, Chinese Academy of Geological Sciences (grant no. nario (cf. Dzik 2003, p. 121) is based on some possibly shared J0716), the State Key Laboratory of Palaeobiology and Stratigra- anatomical features between Cambrian frond-like Thaumap- phy in China (grant no. 103104), the China Geology Survey (grants tilon and presumed ctenophores and Maotianoas- no. 1212011120140, 1212010611802), and the National Natural Sci- cus. Shu et al. (2006) downplayed the comparison with ence Foundation of China (grant no. 40672022). SB’s work is sup- ported by the Swedish Science Research Council (grant no. 2007- Thaumaptilon but brought in another Cambrian frond-like 4484). fossil, , in the discussion, suggesting homology between the fine transverse stripes along the branches of the frond and the comb rows of ctenophores. The transverse REFERENCES stripes in Stromatoveris average about 0.15-mm apart (mea- Arai, M. N. 2005. Predation on pelagic coelenterates: a review. J. Mar. sured from the images in Shu et al. 2006), which is finer than Biol. Assoc. 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