Jul 4, 2013 - Cambrian spiral-plated echinoderms from Gondwana reveal the earliest pentaradial body plan rspb.royalsocie...
Cambrian spiral-plated echinoderms from Gondwana reveal the earliest pentaradial body plan rspb.royalsocietypublishing.org
Andrew B. Smith1 and Samuel Zamora2 1
Department of Earth Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012, USA 2
Research Cite this article: Smith AB, Zamora S. 2013 Cambrian spiral-plated echinoderms from Gondwana reveal the earliest pentaradial body plan. Proc R Soc B 280: 20131197. http://dx.doi.org/10.1098/rspb.2013.1197
Echinoderms are unique among animal phyla in having a pentaradial body plan, and their fossil record provides critical data on how this novel organization came about by revealing intermediate stages. Here, we report a spiralplated animal from the early Cambrian of Morocco that is the most primitive pentaradial echinoderm yet discovered. It is intermediate between helicoplacoids (a bizarre group of spiral-bodied echinoderms) and crown-group pentaradiate echinoderms. By filling an important gap, this fossil reveals the common pattern that underpins the body plans of the two major echinoderm clades (pelmatozoans and eleutherozoans), showing that differential growth played an important role in their divergence. It also adds to the striking disparity of novel body plans appearing in the Cambrian explosion.
Received: 13 May 2013 Accepted: 4 June 2013
1. Introduction Subject Areas: evolution, palaeontology, taxonomy and systematics Keywords: phylogeny, body plans, Echinodermata, evolution, Cambrian explosion
Author for correspondence: Andrew B. Smith e-mail: [email protected]
All living echinoderms share a body plan that shows pentaradial symmetry, yet they start out as larvae with bilateral symmetry [1,2]. This ontogenetic transformation reflects an evolutionary history in which originally bilaterian ancestors evolved into pentaradiate forms [3,4]. The fossil record captures a partial record of these long-extinct transitional forms, and is thus important for establishing the precise pathway followed in assembling this highly derived body plan [5–7] and for estimating rates of transformation . However, there remain many gaps and uncertainties. One of these concerns the origin of pentaradiality and the morphology of the latest common ancestor of crown-group echinoderms. Specifically, drawing convincing homologies between helicoplacoids (the oldest echinoderms with ambulacra) and crown-group echinoderms (with their fivefold pattern of ambulacra) has been highly problematic, because their respective body plans appeared so distinct [9–12]. The new spirally plated echinoderm from the Cambrian of Morocco, described here as Helicocystis moroccoensis, is the most primitive known form with pentaradial symmetry, and now resolves these problems. Crown-group echinoderms split very early in their history into two major clades: the Pelmatozoa (represented today by the Crinoidea), usually with cup and stem living attached and mouth upward with free feeding appendages; and the Eleutherozoa (represented today by echinoids, asteroids, ophiuroids and holothurians), free-living and living mouth downwards. Helicocystis shows how these two clades diverged initially through differential growth and development.
2. Material and methods Electronic supplementary material is available at http://dx.doi.org/10.1098/rspb.2013.1197 or via http://rspb.royalsocietypublishing.org.
(a) Geological setting and stratigraphy In the Alnif region of the eastern Anti-Atlas mountains, Morocco, shallow marine siliciclastics of the Cambrian Jbel Wawrmast Formation are widely developed [8,13 – 15]. The Formation commences with episodic hiatal shell accumulation layers capped with stromatolitic crusts and interbedded with mudstone—the Bre`che a` Micmacca Member—and passes upwards into the muddier Tarhoucht
& 2013 The Author(s) Published by the Royal Society. All rights reserved.
Eastern Anti-Atlas Alnif
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EL Graara massif
Anti-Atlas Zagora Jbel ani
Silurian to Permian
studied sections close to Alnif
Figure 1. Geological setting of the studied sections (adapted from A´lvaro et al. ). (Online version in colour.) Member. The lower member encompasses the classic lowermiddle Cambrian boundary and base of Global series 3, and is dated to approximately 517 Ma [8,16]. Helicocystis moroccoensis was collected from the Jbel Wawrmast Formation at the following three localities (figure 1): — Near Alnif, at Assemame 3 (coordinates 31.287688 N, 004.984938 W). Here, a level close to the base of the Bre`che a` Micmacca Member contains the articulated trilobites Paradoxides (Accadoparadoxides) mureroensis, Hamatolenus (Hamatolenus) vincenti, Protolenus (Protolenus) densigranulatus, Myopsolenites boutiouiti and Kingaspis sp., all characteristic of the basal Cephalopyge notabilis Zone . — In a creek bed, close to the primary school of Tarhia, where local collectors quarry the Bre`che a` Micmacca Member (coordinates 31.394598 N, 005.019778 W). The fauna here includes common trilobites Accaparadoxides sp., Hamatolenus sp. and Cambropallas telesto, indicative of Cephalopyge notabilis Zone and probably slightly younger than the level at locality 1. — At Tizi n’Telgane [13,14], a section close to the road north from Alnif that intersects with the road from Tinejdad to Ouarzazate (coordinates 31.302408 N, 005.262668 W). Here, a level low in the Tarhoucht Member has provided very rare trilobites indicative of Cephalopyge notabilis–Ornamentaspis frequens Zones. Levels providing H. moroccoensis correspond to the global Cambrian stage 4 –5 boundary and the base of stage 5 and are thus dated to 515 – 510 Ma.
200 km Ouarzazate
Western Plateau High Atlas Anti-Atlas
(b) Methods summary Specimens are preserved as moulds or with original calcite preserved. In the latter case, specimens were submerged in a solution of HCl (10%) before casting. Latex casts were made in order to reproduce the original morphology and whitened with NH4Cl prior to photography.
3. Results (a) Morphology of Helicocystis Helicocystis is 5 –20 mm in length, excluding the holdfast. The body is divided into three parts (figure 2; electronic supplementary material, figures S1 –S3): a polyplated stem, a short cup of tessellated plates, and a spiral-plated part that includes ambulacra and the main body openings. In juveniles, the spiral region is only slightly larger than the cup (figure 2c; electronic supplementary material, figure S2), but as growth proceeds, the spiral part becomes proportionally much larger. The spiral part is composed of ambulacral and interambulacral rows of plates arranged helically. The mouth is at the apex, framed by seven oral plates, five of which extend deep into the theca (figures 2a and 3a,b; electronic supplementary material, figures S3 and S4). Oral plates are arranged exactly as in other pentaradiate echinoderms [19,20], with one interambulacrum (C/D) having three oral plates, framing a small pore that we interpret as
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1 mm (g) (f)
(h) Amb 1 mm cup 1 mm ( j)
Figure 2. Helicocystis moroccoensis n. gen. n. sp. from the Cambrian of Morocco. (a, d – f ) Holotype (NHM UK EE15373; locality 3): (a) general view, (d) detail showing periproct plating, (e) detail of ambulacrum showing exposed flooring plates, (f ) detail of ambulacral and interambulacral areas in an expanded state. (b, j ) Paratype (NHM UK EE14847; locality 3): (b) general view, ( j ) detail of theca showing interambulacral spines. (c) Paratype (NHM UK EE15375; locality 3): a wellpreserved juvenile. (g) Paratype (NHM UK EE14848ii; locality 1): a juvenile. (h) Paratype (NHM UK EE15374; locality 3): detail of the polyplated stem. (i) Paratype (NHM UK EE14848i; locality 1): cup and stem of a juvenile. Images (a – c, e, f, h) are latex casts whitened with NH4Cl; images (g, i, j ) are SEM images. Amb, ambulacral zone; cp, cover plate; fp, flooring plate; Iamb, interambulacral zone; ppt, periproct; pst, peristome; sp, interambulacral spine.
the gonopore/hydropore (figure 3b). The ambulacra enter the mouth between these elements. Cover plates in this region are missing. The periproct is a conical structure and opens on the side about half-way down (figure 2d ). Interambulacra are composed of a mosaic of polygonal plates that are largest medially and become progressively smaller towards the ambulacra (figure 2f ). We infer that these zones were able to expand and contract, concertina-like. Among the larger plates, some are spine-like and project perpendicularly from the body (figure 2f,j; electronic supplementary material, figure S2C). Interambulacral plates have a deep groove (articulation facet) on their narrow abutment face. Ambulacra run spirally from the peristome, ending in the lower part of the theca before the cup is reached (see the electronic supplementary material, figures S3 and S4). Each ambulacrum is
composed of flooring plates and cover plates. Flooring plates are biserially arranged, irregular in size (though generally as wide as long) and lack perforations (figure 2e). The food groove is roofed by a sheet of cover plates. Primary cover plates are polygonal, ending in a short projection (figure 2f; electronic supplementary material, figure S4B), and correlate 1 : 1 with flooring plates. Secondary cover plates are small and rarely preserved. Aborally, the theca takes the form of a rigid cup composed of two or three irregular circlets of large, relatively thick polygonal plates that are sutured together (figure 2). The junction between the spiral part and the cup is abrupt. The base of the cup is connected directly to a short polyplated stem composed of small circular plates without apparent organization (figure 2h,i). These are neither strongly imbricate nor sutured together but appear to loosely abut.
03 04 02
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(d) A E A
03 01 D
04 06 07
06 07 C
Figure 3. Oral plating in (a, b) Helicocystis (NHM UK EE15373; locality 3), (c) the edrioasteroid Cambraster (adapted from Zamora et al. ) and (d) a glyptocystitid rhombiferan (adapted from Sumrall ). Oral plates lightly shaded (green in online version) and numbered O1 – O7; ambulacral cover plates shaded dark grey ( purple in online version) ( peristomial cover plates missing in Helicocystis); ambulacra labelled A – E; gp, gonopore. (Online version in colour.)
(b) Phylogenetic position of Helicocystis A phylogenetic analysis of the major Cambrian echinoderm groups (see the electronic supplementary material for details) places Helicocystis as the immediate sister group to crowngroup echinoderms, and intermediate in position between helicoplacoids and typical pentaradiate echinoderms (figure 4).
4. Discussion Helicocystis shows a novel and unexpected mix of echinoderm characters. It has the spiral body plating of a helicoplacoid but has a terminal mouth and five recumbent ambulacra like crown-group echinoderms, and the cup and stem of a pelmatozoan. It is interpreted as close to the latest common ancestor of all crown-group echinoderms and, for the first time, allows plausible homologies to be drawn between helicoplacoids and crown-group echinoderms. Several important conclusions emerge. First, Helicocystis and helicoplacoids have a spirally plated theca that is constructed in an identical manner, with sheets of polygonal interambulacral plates that can open flat or become folded, concertina-like. However, the sense of spirality differs, being clockwise in Helicocystis and anticlockwise in Helicoplacus. This implies that the entire theca of helicoplacoids is homologous to only the spiralled region of Helicocystis. This is significant because crowngroup echinoderms have two distinct partitions to their body derived embryologically from rudiment and larval tissues, respectively [4,21,22], and referred to as axial and
extraxial. Helicocystis, with its clear differentiation between its spiralled region and cup plus stem, thus helps pinpoint when this bimodal tissue origin first arose in echinoderm evolution. Second, helicocystids, like helicoplacoids, have recumbent ambulacra constructed of biserial flooring plates and sheets of cover plates [9,12]. However, whereas the mouth is lateral and the periproct apical in helicoplacoids, torsion has brought the mouth to the apical position and the periproct to a lateral position (see the electronic supplementary material, figure S5). This shows that torsion, an important step in echinoderm evolution related to migrating the mouth to an apical position following larval fixation at metamorphosis , evolved progressively. Third, helicocystids have oral plates arranged in a pattern that matches that found in many early eleutherozoan and pelmatozoan taxa (stromatocystitids, edrioasteroids, most eocrinoids, glyptocystitids, diploporans and crinoids), and so conforms to the universal homology system [19,20]. This pattern therefore represents the plesiomorphic state for crown-group echinoderms. Fourth, helicocystitids had a theca and stem like that of primitive pelmatozoans (i.e. Gogia [23 –25]) and were clearly attached throughout much, if not all, of their lives. As this region becomes progressively reduced during growth, attachment was clearly less important to adults, suggesting that adult attachment arose through retention of a larval trait associated with settlement. In pelmatozoans, cup and stem are retained and developed, but in primitive eleutherozoans, they are reduced and modified, probably corresponding to the basal zone of tessellated plates in Stromatocystites (figure 5). Finally, helicocystitids appear to
Figure 4. Evolutionary tree of Cambrian echinoderms based on our cladistic analysis. (Online version in colour.)
spiral region axial zone extraxial zone Stromatocystites
Figure 5. Diagram indicating the homology and relative development of body regions in Cambrian echinoderms. (Online version in colour.) lack pores connecting the food grooves with the internal part of the body and so presumably lacked well-developed ampullae associated with its tube-feet. Both edrioasteroids ( primitive eleutherozoans) and helicoplacoids have such pores [12,23,26], suggesting multiple evolutionary gain or loss of this trait has occurred. Figure 5 summarizes the homologies that can now be drawn between Helicocystis, primitive pelmatozoans (Gogia) and primitive eleutherozoans (Stromatocystites). The evolutionary divergence of pelmatozoans and eleutherozoans thus involved the differential growth of the axial and extraxial regions observed in Helicocystis, and the evolutionary innovation of free appendages in the former. With the
discovery of Helicocystis, a major gap between helicoplacoids and crown-group echinoderms is finally filled.
5. Systematic palaeontology Stem group Echinodermata Family Helicocystitidae nov. Etymology. For the spiral organization of the ambulacral region combined with the cystoid-like cup and stem. Diagnosis. Stem polyplated; basal cup of large sutured plates; theca above the cup with five recumbent ambulacra spiralling clockwise away from an apical peristome.
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Type genus. Helicocystis gen. nov. Occurrence. Base of Cambrian series 3, Morocco Genus Helicocystis nov. Diagnosis. As for family.
Acknowledgements. We appreciate the support of Isabel Pe´rez (Zaragoza University, Spain) for her assistance with photographs, figures and digital reconstruction of Helicocystis. Three reviewers provided comments that improved the resulting manuscript. We appreciate discussions with Colin Sumrall and Thomas Kammer on oral homologies in pentaradial echinoderms. Both authors contributed equally to the fieldwork, description and interpretation of the fossils. Funding statement. S.Z. was funded by the Smithsonian Institution (Springer fund) and project CGL2011-24516. Fieldwork was supported by National Geographic Project grant no. GEFNE5-11.
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Type species. Helicocystis moroccoensis sp. nov. Occurrence. As for family. Helicocystis moroccoensis sp. nov. Holotype. Specimens are housed in the Natural History Museum (London). The holotype is NHM UK EE15373, paratypes are EE15374–EE15376, EE14847, EE14848 and EE15329.
Diagnosis. As for family. Occurrence. The holotype comes from the Jbel Wawrmast Formation, Cephalopyge notabilis to Ornamentaspis frequens Zones, base of Cambrian Series 3, at Tizi n’Telgane, north of Alnif, Anti-Atlas mountains, Morocco. Paratypes are from the Jbel Wawrmast Formation of Tarhia and Assemame (see above).
Ambulacra composed of biserial flooring plates lacking direct connection with the body chamber, and sheets of primary cover plates and very small secondary cover plates. Interambulacral zones are also spiral, composed of sheets of plates that could be expanded and contracted concertina-like.