Deciphering the early evolution of echinoderms with Cambrian fossils

Echinoderms are a major group of invertebrate deuterostomes that have been an important component of marine ecosystems throughout the Phanerozoic. Their fossil record extends back to the Cambrian, when several disparate groups appear in different palaeocontinents at about the same time. Many of these early forms exhibit character combinations that differ radically from extant taxa, and thus their anatomy and phylogeny have long been controversial. Deciphering the earliest evolution of echinoderms therefore requires a detailed understanding of the morphology of Cambrian fossils, as well as the selection of an appropriate root and the identification of homologies for use in phylogenetic analysis. Based on the sister‐group relationships and ontogeny of modern species and new fossil discoveries, we now know that the first echinoderms were bilaterally symmetrical, represented in the fossil record by Ctenoimbricata and some early ctenocystoids. The next branch in echinoderm phylogeny is represented by the asymmetrical cinctans and solutes, with an echinoderm‐type ambulacral system originating in the more crownward of these groups (solutes). The first radial echinoderms are the helicoplacoids, which possess a triradial body plan with three ambulacra radiating from a lateral mouth. Helicocystoids represent the first pentaradial echinoderms and have the mouth facing upwards with five radiating recumbent ambulacra. Pentaradial echinoderms diversified rapidly from the beginning of their history, and the most significant differences between groups are recorded in the construction of the oral area and ambulacra, as well as the nature of their feeding appendages. Taken together, this provides a clear narrative of the early evolution of the echinoderm body plan.     

Crypto-helical body plan in partially disarticulated gogiids from the Cambrian of South China

All living echinoderms have a pentaradial symmetry that is unique within the Bilateria. However, the Cambrian origin of echinoderm radial/pentaradiate symmetry is a long-standing problem. During the Cambrian (542–488 Ma), gogiids were the most common stalked echinoderm characterized by an “irregularly” plated body. Based on recently discovered material from the Balang Formation (Cambrian Series 2), eastern Guizhou, China, three unusual, partially disarticulated specimens of Guizhoueocrinus have clear evidence for a helical body plan. This helical plating is only evident in partially disarticulated specimens, thus a crypto-helical body construction is present. Crypto-helical construction in a gogiid raises the possibility of a phylogenetic connection among helicoplacoids, gogiids, and Helicocystis. The crypto-helical body construction may be an important evolutionary innovation among pre-radiate echinoderms.     

Cambrian stalked echinoderms show unexpected plasticity of arm construction

Feeding arms carrying coelomic extensions of the theca are thought to be unique to crinoids among stemmed echinoderms. However, a new two-armed echinoderm from the earliest Middle Cambrian of Spain displays a highly unexpected morphology. X-ray microtomographic analysis of its arms shows they are polyplated in their proximal part with a dorsal series of uniserial elements enclosing a large coelomic lumen. Distally, the arm transforms into the more standard biserial structure of a blastozoan brachiole. Phylogenetic analysis demonstrates that this taxon lies basal to rhombiferans as sister-group to pleurocystitid and glyptocystitid blastozoans, drawing those clades deep into the Cambrian. We demonstrate that Cambrian echinoderms show surprising variability in the way their appendages are constructed, and that the appendages of at least some blastozoans arose as direct outgrowths of the body in much the same way as the arms of crinoids.     

A re‐interpretation of the ambulacral system of Eumorphocystis (Blastozoa,Echinodermata) and its bearing on the evolution of early crinoids

Recent debates over the evolutionary relationships of early echinoderms have relied heavily on morphological evidence from the feeding ambulacral system. Eumorphocystis, a Late Ordovician diploporitan, has been a focus in these debates because it bears ambulacral features that show strong morphological similarity to early crinoid arms. Undescribed and well‐preserved specimens of Eumorphocystis from the Bromide Formation (Oklahoma, USA) provide new data illustrating that composite arms supported by a radial plate that bear a triserial arrangement of axial and extraxial components encasing a coelomic extension can also be found in blastozoans. Previous reports have considered these arm structures to be restricted to crinoids; these combined features have not been previously observed in blastozoan echinoderms. Phylogenetic analyses suggest that Eumorphocystis and crinoids are sister taxa and that shared derived features of these taxa are homologous. The evidence from the arms of Eumorphocystis suggests that crinoid arms were derived from a specialized blastozoan ambulacral system that lost feeding brachioles and strongly suggests that crinoids are nested within blastozoans.     

Revision of Echmatocrinus from the Middle Cambrian Burgess Shale of British Columbia

Echmatocrinus from the Middle Cambrian Burgess Shale of British Columbia was originally described as the earliest crinoid(?) known from the fossil record. Recently, Conway Morris and Ausich & Babcock have questioned whether Echmatocrinus is in fact an echinoderm, comparing it instead to cnidarians with a polyp-like body and pinnate tentacles, and other authors are beginning to use this reinterpretation. We studied the well-preserved holotype of Echmatocrinus brachiatus, two paratypes, and 18 new specimens recovered from different levels in the Burgess Shale sequence at three localities. All are preserved as pyrite films in dark shale with relatively little relief, suggesting a lightly skeletized body. Complete specimens have a long, slightly tapering, large-plated attachment stalk, a conical cup or calyx with numerous small to medium-sized irregular plates, and 7–10 short arms with heavier plating and (in the holotype) soft appendages alternating from opposite sides of several arms. Several morphologic features indicate that Echmatocrinus is an echinoderm and has crinoid affinities: (1) Sutured plates, shown by darker depressed sutures, slightly raised plate centers, and oriented plate ornament, cover all major parts of the body; (2) reticulate surface ornament in the pyrite film on the plates of all specimens matches the ornament in the Burgess Shale edrioasteroid Walcottidiscus, an undoubted echinoderm, but not the pyritized surfaces of other metazoans in the fauna; (3) this distinctive ornament may represent the surface expression of microporous stereom; (4) possible ligament or muscle pads are present between the arm ossicles to fold and unfurl the more heavily plated arms. Within the echinoderms, only crinoids commonly have a calyx attached by a stalk or stem to the substrate and bear erect, moveable, uniserial arms for feeding. Although Echmatocrinus shows some resemblance to octocorals in overall body shape as an attached suspension feeder, almost all the details are different, indicating that Echmatocrinus is most likely unrelated to this group. All complete specimens of Echmatocrinus are attached to hard substrates, either another fossil or skeletal debris. The new specimens indicate that Echmatocrinus was twice as common (about 0.02%) in the Burgess Shale fauna as previously recorded and represents one of the earliest attached, medium-level, skeletized, suspension feeders or microcarnivores in the fossil record.     

Cambrian spiral-plated echinoderms from Gondwana reveal the earliest pentaradial body plan

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 spiral-plated 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.     

Ordovician Paracrinoids from the Baltic: Key Problems of Comparative Morphology of Pelmatozoan Echinoderms

The erect feeding appendages of paracrinoids, brachioles of typical blastozoans and arms of crinoids are morphologically similar in their terminal growth, biserial cover plates, and pinnulation. This is attributed to the inducing effect of the radial ambulacral canal on their growth mode. The uniserial brachioles of Laurentian paracrinoids are homologous to the biserial brachioles of the Baltic Achradocystites and Heckerites, and those of other blastozoans. Based on this assumption, the two Baltic genera, which have a brachiole system plesiomorphic for paracrinoids, and a similar morphology of the theca, are assigned to this class. Brachiolars in brachioles are a new development, homologous to the flooring plates of the food groove and, where present, are the continuations of these plates beyond the theca. The uniserial brachioles of Laurentian paracrinoids evolved from the biserial brachioles as a result of a gradual shift of brachiolars in the neighboring rows and their subsequent fusion in pairs. Brachials in crinoidal arms are a new development that evolved as distal serial growth of radial plates under the induced influence of the incipient radial canals emerging from the closed vestibular cavity, which was an ontogenetic innovation in crinoids. The transformation of a nonorganized small-plated theca into a large-plated, and completely or partly symmetrized theca, or vice versa is possible and results from accelerated or retarded growth of some plate generation in relation to the growth rate of the theca.     

Redescription of Macurdablastus and redefinition of Eublastoidea as a clade of Blastoidea (Echinodermata)

Eublastoids are a large clade of blastoids; stemmed blastozoan echinoderms diagnosed by their conservative body plan (three basals, four deltoid plates and five radial plates), lancet plate supporting the ambulacra, and hydrospire respiratory structures. Although Eublastoidea was a highly successful clade in the middle and late Palaeozoic it is absent from early echinoderm radiations seen in the Cambrian and Ordovician record. Here we provide a re‐evaluation of Macurdablastus uniplicatus Broadhead from the Ordovician, using detailed morphological assessment based on advanced synchrotron tomography and phylogenetic analysis. Macurdablastus uniplicatus falls outside Eublastoidea because of the morphological differences in lancet plate and respiratory structures. The oldest recorded eublastoid is thus middle Silurian in age. The re‐evaluation of the morphology of Macurdablastus provides a basis for revising blastoid phylogeny and classification.     

Arms versus brachioles: Morphogenetic basis of similarity and differences in food-gathering appendages of pelmatozoan echinoderms

The similarity in the skeleton model of the brachiolar food-gathering system of Blastozoa and the arm system of Crinozoa, including the apical growth with enantomorphous displacement of skeletal ele-ments, is explained by the primary organizing role of the radial ambulacral canals, which have the same branching model for ambulacral tentacles. The difference in the positions of brachioles and arms relative to the theca (exothecal and endothecal) is associated with the formation of the primary ambulacral tentacles directly on the body surface of the majority of Blastozoa, particularly, the closed vestibular cavity of crinoids. The supporting skeleton of brachioles arose as a branch of the plates covering the floor of the ambulacrum, if they were present, or formed similarly as a new formation outside the theca. The supporting skeleton of arms, brachials, developed as a result of the serial growth of plates positioned radially at the boundary of the aboral skeleton and tegmen formed due to the appearance of the vestibulum. The hypothesis of the inductive role of hydrocoel and its radial ambulacral appendages, which organize the arrangement of skeletal elements in the morphogenesis of echinoderms, enables the refinement of the principle of skeleton division into the axial and extraxial parts. The axial skeleton has a developmental model formed under the control of the radial ambu-lacral canals. Remaining skeleton is extraxial, subdivided into the symmetrized part arranged under direct or indirect organizing effect of the hydrocoel and unregulated, nonsymmetrized part, which is not connected initially with the influence of the hydrocoel.     

A unique edrioasteroid from the upper Middle Cambrian of Iran,its phylogenetic implications and paleoecology

One of the earliest isorophid edrioasteroids from the upper Middle Cambrian-lower Upper Cambrian (upper part of Series 3-lower part of the Furongian Series) of northern Iran is described. It has unusual branched ambulacra, which extend beyond the theca almost to the marginal rim. These unusual features reflect the latent possibility of appearance of separated from the theca and even branching food-gathering appendages, such as arms in crinoids and brachials in blastozoans, in common ancestor of all radially symmetrical echinoderms.     

Plated Cambrian bilaterians reveal the earliest stages of echinoderm evolution

Echinoderms are unique in being pentaradiate, having diverged from the ancestral bilaterian body plan more radically than any other animal phylum. This transformation arises during ontogeny, as echinoderm larvae are initially bilateral, then pass through an asymmetric phase, before giving rise to the pentaradiate adult. Many fossil echinoderms are radial and a few are asymmetric, but until now none have been described that show the original bilaterian stage in echinoderm evolution. Here we report new fossils from the early middle Cambrian of southern Europe that are the first echinoderms with a fully bilaterian body plan as adults. Morphologically they are intermediate between two of the most basal classes, the Ctenocystoidea and Cincta. This provides a root for all echinoderms and confirms that the earliest members were deposit feeders not suspension feeders.     

Middle Cambrian cystoid (sensu lato) stem columnals from Bornholm, Denmark

A rich material of echinoderm fragments from two Middle Cambrian stratigraphical levels on Bornholm are preserved due to phosphatization of the original calcitic stereom. Preservation of echinoderms in this way - not previously recorded from the Middle Cambrian - permits detailed analysis of the three-dimensional stereom structure. Identifiable are fragments of stylophorans and eocrinoids. Stem columnals, most likely from eocrinoids, show a wide and advanced morphological variation indicating articulation similar to that of crinoids. The material from the Exsulans Limestone/Kalby marl ( Ptychagnostus gibbus Zone) represents stem-bearing cystoids older than Akadocrinus from Bohemia. The Andrarum Limestone ( Sole-nopleura brachymetopa Zone) contains echinoderm fragments from a higher stratigraphical level, a level correlatable with that from which the oldest North American stem–bearing cystoid, Eustypocystis , has been recorded.     

Reduction in the number of Early Cambrian helicoplacoid species

Helicoplacoid echinoderms occur in Lower Cambrian shales and mudstones along the northern coast of Laurentia, now western North America. The group originally contained four genera and nine species, diagnosed by differing ambulacra, plate length-to-width ratios, and plate ornament. Ambulacra are identical in all specimens except for the single example of Waucobella nelsoni, and the remaining morphologic differences are caused by ontogeny. The characters used to diagnose seven of the original nine species are therefore invalid, reducing the group to three genera and three species. These are: Helicoplacus gilberti Durham and Caster, 1963, Waucobella nelsoni Durham, 1967, and Polyplacus kilmeri Durham, 1967, which has a test composed of ambulacra, and likely represents a developmental oddity.     

Disarticulation patterns in Ordovician crinoids: Implications for the evolutionary history of connective tissue in the Crinoidea

Taphonomic information is examined to evaluate the early history of connective tissues in the Crinoidea. The pattern of stalk segmentation of Middle and Late Ordovician crinoids is consistent with the two-ligament (intercolumnal and through-going ligaments) pattern present in living isocrinid crinoids and interpreted for fossil isocrinids, holocrinids, and Lower Mississippian crinoids. A single rhombiferan was also examined; its taphonomic pattern is also indicative of this style of tissue organization. Furthermore, the taphonomy of all Middle and Late Ordovician crinoids may reflect that they lacked discretely organized muscles between arm brachials, which is consistent with the hypothesis that muscles evolved as a connective tissue between plates only once within the Crinoidea, during the Early Devonian. These data indicate that the two-ligament organization of the stalk is a primitive feature among the Crinoidea and perhaps even among stalked echinoderms. Therefore, the autotomy function of this column-tissue organization among living crinoids is an exaptation. On the other hand, discretely organized muscles as connective tissue in crinoid arms is a derived trait that first appeared during the middle Paleozoic; this adaptation proved very successful for the advanced cladid crinoids.     

First report of Gogia (Eocrinoidea, Echinodermata) from the Early-Middle Cambrian of Sonora (Mexico), with biostratigraphical and palaeoecological comments

The blastozoan echinoderm genus Gogia is reported for the first time in the Early and the Middle Cambrian of Mexico. Reports in different members of the section of San José de Gracia (Sonora State, northwestern Mexico) extend the palaeogeographical range of the genus to the South Laurentia, and the stratigraphic range of Gogia granulosa to the whole first half of middle Middle Cambrian. Isolated plates occur in rocks deposited in detrital inner platform and complete specimens, in carbonate outer platform, confirming their ability to live in diverse environments. Their presence in these different environments through the Early-Middle Cambrian on Laurentia agrees with the onshore-offshore expansion of echinoderms during Cambrian.     

Site Selectivity of the Pit Oichnus excavatus Donovan and Jagt Infesting Hemipneustes striatoradiatus (Leske) (Echinoidea) in the Type Maastrichtian (Upper Cretaceous,The Netherlands)

Two tests of the holasteroid echinoid Hemipneustes striatoradiatus (Leske) from the type area of the Maastrichtian Stage (Upper Cretaceous) bear a varied infestation of episkeletozoans (oysters, bryozoan colony, and serpulids), borings (probable Caulostrepsis isp., Oichnus simplex Bromley), surface abrasion (Gnathichnus? isp.), and pits (O. excavatus Donovan and Jagt). Only O. excavatus represents a premortem infestation. In one specimen, the four individual pits of this ichnospecies are each associated with a different ambulacrum and pore pairs that, in life, bore respiratory tube feet; the anterior ambulacrum, of different gross morphology, is not infested. In the second test, three out of four of the same ambulacra are infested, although there are also O. excavatus in the interambulacra. The association between O. excavatus and the ambulacra of the echinoid, and thus its tube feet, is open to several plausible explanations, but most likely provided some form of feeding or protective advantage to the pit-forming organism.     

Arrays in rays: terminal addition in echinoderms and its correlation with gene expression

The echinoderms are deuterostomes that superimpose radial symmetry upon bilateral larval morphology. Consequently, they are not the first animals that come to mind when the concepts of segmentation and terminal addition are being discussed. However, it has long been recognized that echinoderms have serial elements along their radii formed in accordance with the ocular plate rule (OPR). The OPR is a special case of terminal growth, forming elements of the ambulacra that define the rays in echinoderms. New elements are added at the terminus of the ray, which may or may not be marked by a calcified element called the terminal plate (the "ocular" of sea urchins). The OPR operates in every echinoderm, from the occasionally bizarre fossils of the Cambrian to the most familiar extant taxa. Using the OPR and other criteria of recognition, echinoderm body wall can be divided into two main regions: extraxial components are associated with the somatocoels, axial components (formed in accordance with the OPR) with the hydrocoel. We compare patterns of development in axial regions of echinoderms with those found in the anterior-posterior axes of the earliest echinoderms as well as other invertebrates. Although axial and extraxial skeletons appear to be composed of the same biomineral matrix, the genes involved in patterning these two skeletal components are likely distinct. During development of the axial skeleton, for instance, the genes engrailed and orthodenticle are expressed in spatial and temporal patterns consistent with the OPR. Other genes such as distal-less seem to demarcate early ontogenetic boundaries between the axial rudiment and the extraxial larval body. There is a complex and pervasive reorganization of gene expression domains to produce the highly divergent morphologies seen in the Echinodermata. We integrate morphological and genetic information, particularly with respect to the origins of radial symmetry in the rudiment, and the concomitant development of the rays.     

SOFT-TISSUE PRESERVATION OF THE HIND GUT IN A NEW GENUS OF CLADID CRINOID FROM THE MISSISSIPPIAN (VISEAN, ASBIAN) AT ST ANDREWS, SCOTLAND

Abstract:  Soft-tissue preservation of the hind gut, or anal sac, in the tegmen of Tubulusocrinus (gen. nov.) doliolus (Wright) from the Mississippian (Visean, Asbian) Pittenweem Formation at St Andrews, Scotland, is the first of its kind known in crinoids; it sheds important new light on the nature of the cladid tegmen. Many cladid crinoids had a calcite-plated anal sac that may have functioned like a chimney to prevent fouling of the ambulacra. The tubular, uncalcified anal sac of Tubulusocrinus may have functioned like a hose by pointing down current between the arms to avoid fouling of the ambulacra. Its smaller size may also have required less energy to produce than a heavy-plated sac. The hind gut is apparently preserved by haematite replacement, which was probably altered from original authigenic pyrite that formed soon after catastrophic burial.     

Morphology,ontogeny, and heterochrony in lower and middle Cambrian Gogiids (Eocrinoidea,Echinodermata) from Guizhou Province,China

Gogiid eocrinoids from the Lower Cambrian (Balang Formation — Guizhoueocrinus) and basal Middle Cambrian (Kaili Formation — Sinoeocrinus, Globoeocrinus) in Guizhou Province, China are found in great numbers and are extremely well preserved as high fidelity molds in shale/mud sized siliciclastics. Because of their numbers, complete ontogenetic growth sequences have been observed. Significant differences in growth patterns (heterochrony) are present between Lower and Middle Cambrian genera: thecal plates tend to be paedomorphic in development, while the sutural pores developed between them are peramorphic in their development. Because of the large surface area of theca and brachioles relative to the size of the attachment area, considerable drag in ambient currents would necessitate a strong attachment medium. Anchoring by “biogluing”, possibly by collagen, directly to the substrate or to biodetritus is proposed as the method of attachment.