In defence of the calcichordates

The cornutes and mitrates, collectively known as stylophorans or calcichordates, are the most controversial members of the traditional group of the 'carpoid echinoderms'. In a recent review, Philip has rejected Ubaghs' interpretation of them as aberrant echinoderms with a single feeding arm, has also rejected my own interpretation of diem as primitive chordates, and has made some tentative proposals of his own. The present paper answers Philip's criticisms of the calcichordate interpretation and discusses his own proposals and his comments on Ubaghs' views.     

Exceptionally preserved soft parts in fossils from the Lower Ordovician of Morocco clarify stylophoran affinities within basal deuterostomes

The extinct echinoderm clade Stylophora consists of some of the strangest known deuterostomes. Stylophorans are known from complete, fully articulated skeletal remains from the middle Cambrian to the Pennsylvanian, but remain difficult to interpret. Their bizarre morphology, with a single appendage extending from a main body, has spawned vigorous debate over the phylogenetic significance of stylophorans, which were long considered modified but bona fide echinoderms with a feeding appendage. More recent interpretation of this appendage as a posterior “tail-like” structure has literally turned the animal back to front, leading to consideration of stylophorans as ancestral chordates, or as hemichordate-like, early echinoderms. Until now, the data feeding the debate have been restricted to evaluations of skeletal anatomy. Here, we apply novel elemental mapping technologies to describe, for the first time, soft tissue traces in stylophorans in conjunction with skeletal molds. The single stylophoran appendage contains a longitudinal canal with perpendicular, elongate extensions projecting beyond hinged biserial plates. This pattern of soft tissues compares most favorably with the hydrocoel, including a water vascular canal and tube feet found in all typical echinoderms. Presence of both calcite stereom and now, an apparent water vascular system, supports echinoderm and not hemichordate-like affinities.     

A defence of the calcichordates

Peterson (1994, Short Courses in Paleontology 7, Pal. Soc. & Univ. Tennessee; 1995, Lethaia 28 ) has claimed that the calcichordate theory of the origin of chordates can be dismissed on purely methodological grounds, without evaluating the anatomy of the calcichordates. He claimed this on the basis of his finding that the interrelationships for extant deuterostomes obtained by a PAUP analysis were not altered by including calcichordate fossils in the analysis, allegedly coded according to the anatomical interpretations of the calcichordate theory. This result, however, was due (1) to acceptance of dubious homologies among extant deuterostomes, (2) to reliance, when asserting that the fossils made no difference, on a majority-rule tree based on 13 equal-shortest trees; and (3) to the use of numerous multi-state characters in coding, which had the effect of denying, a priori , many of the homologies claimed by the calcichordate theory between fossil and extant forms. When these errors are corrected, a new PAUP analysis yields a tree consistent with the calcichordate theory. Peterson's claim therefore fails.     

The Early Phylogeny of Chordates and Echinoderms and the Origin of Chordate Left–Right Asymmetry and Bilateral Symmetry

Abstract Left–right asymmetry in Dexiothetica (= echinoderms + chordates) results mainly from dexiothetism—an episode in their ancestry when an animal resembling the Recent pterobranch Cephalodiscus lay right-side-downwards on the sea floor. Castericystis sprinklei belongs to the dexiothete stem group. The history of the echinoderm stem group is reconstructed. Chordate bilateral symmetry evolved by six successive steps. Tail–head overlap occurred independently in craniates and acraniates. The neural crest would have existed in the latest common ancestor of extant chordates, or even earlier. Gross asymmetries occur in extant chordates in organs derived from the calcichordate head, but not in those derived from the calcichordate tail. The anterior boundary of hox gene expression in vertebrates corresponds to the anterior end of the calcichordate tail. Left–right organ pairing (an important step in the origin of chordate bilateral symmetry) may have involved the interaction of a symmetrizing morphogen, produced from the anterior end of the tail, with a lateral morphogen (Wilhelmi's morphogen), produced in ontogeny at first from the left and later from the right. This mechanism may still act in the metamorphosis of amphioxus and in mirror-imaging in vertebrate twins. Wilhelmi's morphogen may be related to one or more members of the dorsal cascade of Drosophila.     

What are the 'Calcichordata'? and the larger question of the origin of Ghordates

Argument around the question of the validity of the 'Calcichordata' emphasizes the need for a more functional and utilitarian view of the origin of the chordates. The calcichordate question is reviewed and 'tested' in terms of our usual ideas of biological reality. The concept is rejected and the Stylophora are viewed as aberrant and still largely unknown echinoderms. Rejection of the calcichordate concept turns us once more to the question of the origin of the chordates. A number of competing hypotheses are compared: the tunicate, dipleuruloid and archicoelomate models. The conclusion is that the dipleuruloid, a simple metazoan, offers the least explanatory difficulties. Also it is concluded that discussion of such a subject as this refines and improves our thinking concerning it.     

A cladistic analysis of the cornutes (stem chordates)

At the root of the calcichordate controversy is the problem of recognizing homologous similarity. Only when a criterion or set of criteria for hypothesizing homologies is established can the calcichordate theory be tested against its main rival—the Stylophoran theory—by applying the principle of parsimony. The criterion of topological similarity is applied to a three-laxon problem involving a mitrate, the crown-group Echinodermata and the crown-group Chordata. The mitrate shares more features with extant chordates than with extant echinoderms and the calcichordate theory is supported by a simple parsimony analysis. In a cladistic analysis of the cornutes, four monophyletic families are recognized (Cothurnocystidae, Scotiaecystidae, Phyllocystidae and Hanusiidae) and their interrelationships resolved using Hennig86 and the successive-weighting procedure of Farris. Because the known fossil record of cornutes and mitrates is very poor, the correlation between the cladogram produced for cornutes and their order of appearance in the geological record is weak. All of the cornute families must have originated in the Lower Cambrian at the latest.     

A new calcichordate from the Ordovician of Bohemia and its anatomy, adaptations and relationships

The paper describes a new member of a group of Lower Palaeozoic marine fossils which partly bridge the gap between echinoderms and chordates. Evidence suggests that this group included the ancestors of the vertebrates. Its members are traditionally regarded as primitive echinoderms, but are better seen as primitive chordates with echinoderm affinities. They form a basal subphylum of chordates-the Calcichordata Jefferies 1967. The Calcichordata, in accordance with an early suggestion by Gislén, are probably ancestral to all living chordates. The new calcichordate is named Reticulocarpos hanusi gen et sp. nov. It comes from the Lower Ordovician ?árka Formation (Llanvirn) of ?árka near Prague, Czechoslovakia and is placed in the family Amygdalothecidae Ubaghs 1970. It is important because of its position in the Calcichordata. This group is divided into two very different orders–the Cornuta and the Mitrata. The Cornuta are the more primitive order and gave rise to the Mitrata, which had the structure of giant, calcite-plated tunicate tadpoles. Many features show that the new species is a very advanced cornute, closely related to the stock that gave rise to the mitrates. For this reason it is important in the general history of the chordates, since some primitive mitrate was probably the latest common ancestor of the living chordate subphyla i.e. of tunicates, of amphioxus and its allies and of the vertebrates. Being a mitrate-like cornute, the new species allows the cornutes and mitrates to be compared more confidently than before. Four results are especially important. Firstly it is likely that the stem (=tail) of mitrates is equivalent only to the anterior part of the stem of cornutes. This is significant, because traditional views as to which was the upper surface in mitrates have been based on stem homologies now seen as false. Secondly Reticulocarpos hanusi is adapted to stay up on very soft mud, using only the strength of the mud for support. The mitrates, on the other hand, supported themselves on soft mud by a much more reliable method resembling buoyancy. Thirdly, the new form had paired transpharyngeal eyes which are otherwise known only in mitrates, and which are the earliest type of paired eyes in chordates. Fourthly, it becomes possible to homologize the thecal plates of cornutes with those of mitrates. Reticulocarpos hanusi represents an important phase in chordate evolution dominated by the necessity of staying up on mud by a very precarious method. During this phase many pre-adaptations for swimming were acquired. Primitive mitrates, descended from a very similar form, were probably the first chordates that could swim.     

A phylogenetic test of the calcichordate scenario

The calcichordate scenario of Jefferies and colleagues purports to explain the origin and early evolution of the phyla Echinodermata and Chordata. Calcichordate proponents have argued that echinoderms are the sister group of the chordates and urochordates are the sister group of the craniates. These phylogenetic hypotheses, which differ from the traditional groupings, are derived primarily from morphological interpretations of carpoids (solutes, cornutes, and mitrates), an enigmatic fossil group usually held to be primitive stem-group echinoderms. Although the scenario has received only limited support, it has yet to be falsified. The difficulty with falsifying the calcichordate scenario is proving that the morphological interpretations, for example, that carpoids possessed notochords, dorsal hollow nerve cords, and other typical chordate or craniate characters, are incorrect. Here, rather than argue over the interpretation of fossils, the phylogenetic hypotheses embedded within the scenario are tested. It is found that the calcichordate scenario fails such a test, even if both the Recent and fossils forms are coded according to the calcichordate scenario. It is argued that: (1) the erection of scenarios must follow the construction of a cladogram; and (2) fossils are unable to dictate the relationships among phyla. □ Calcichordate scenario, Carpoidea, Deuterostomia, Echinodermata, Chordata, phylogeny, cladistics.     

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.     

Radial Glia in Echinoderms

Radial glial cells are crucial in vertebrate neural development and regeneration. It has been recently proposed that this neurogenic cell type might be older than the chordate lineage itself and might have been present in the last common deuterostome ancestor. Here, we summarize the results of recent studies on radial glia in echinoderms, a highly regenerative phylum of marine invertebrates with shared ancestry to chordates. We discuss the involvement of these cells in both homeostatic neurogenesis and post‐traumatic neural regeneration, compare the features of radial glia in echinoderms and chordates to each other, and review the molecular mechanisms that control differentiation and plasticity of the echinoderm radial glia. Overall, studies on echinoderm radial glia provide a unique opportunity to understand the fundamental biology of this cell type from evolutionary and comparative perspectives.     

Evaluating phylogenetic hypotheses of carpoids using stratigraphic congruence indices

Fossil carpoids possess a unique anatomy that is difficult to interpret; as a result, there are a number of competing phylogenetic hypotheses for carpoid taxa. Stratigraphic congruence indices provide a quantitative means of evaluating alternative cladograms where character coding is contentious; trees that show a statistically significant fit between stratigraphy and phylogeny are better supported by the fossil record. We here test the agreement between stratigraphic and cladistic data for 27 carpoid cladograms (24 have previously been published, three are novel). The results demonstrate that in analyses of subsets of carpoid taxa, the stratigraphic congruence of trees is not strongly affected by the interpretative model followed. However, when studying the relationships of carpoids with other deuterostomes, assuming that carpoids should be interpreted by reference to chordates/hemichordates (rather than echinoderms) leads to a poorer fit with the known stratigraphic ranges of taxa. Thus, the disputed calcichordate hypothesis (carpoids interpreted as stem and crown-group chordates and stem-group hemichordates) is much less congruent with stratigraphy than alternative models interpreting carpoids as stem or crown-group echinoderms.     

Ichnological evidence on the behaviour of mitrates: two trails associated with the Devonian mitrate Rhenocystis

The mitrates are controversial marine Palaeozoic fossils, assigned either to the chordates or to the echinoderms. This paper describes two trails associated with the mitrate Rhenocystis from the Lower Devonian Hunsrück Slate, Bundenbach, Germany. They indicate that, just before death, the animals were moving tail-first with the flat dorsal surface of the head upward. This behaviour is consistent with the chordate theory of mitrates, rather than with either of the two current echinoderm interpretations.     

Early development of coelomic structures in an echinoderm larva and a similarity with coelomic structures in a chordate embryo

Early coelomic development in the abbreviated development of the sea urchin Holopneustes purpurescens is described and then used in a comparison with coelomic development in chordate embryos to support homology between a single arm of the five-armed radial body plan of an echinoderm and the single bilateral axis of a chordate. The homology depends on a positional similarity between the origin of the hydrocoele in echinoderm development and the origin of the notochord in chordate development, and a positional similarity between the respective origins of the coelomic mesoderm and chordate mesoderm in echinoderm and chordate development. The hydrocoele is homologous with the notochord and the secondary podia are homologous with the somites. The homology between a single echinoderm arm and the chordate axis becomes clear when the aboral to oral growth from the archenteron in the echinoderm larva is turned anteriorly, more in line with the anterior–posterior axis of the early zygote. A dorsoventral axis inversion in chordates is not required in the proposed homology.     

Hemichordates and deuterostome evolution: robust molecular phylogenetic support for a hemichordate + echinoderm clade

SUMMARY Hemichordates were traditionally allied to the chordates, but recent molecular analyses have suggested that hemichordates are a sister group to the echinoderms, a relationship that has important consequences for the interpretation of the evolution of deuterostome body plans. However, the molecular phylogenetic analyses to date have not provided robust support for the hemichordate + echinoderm clade. We use a maximum likelihood framework, including the parametric bootstrap, to reanalyze DNA data from complete mitochondrial genomes and nuclear 18S rRNA. This approach provides the first statistically significant support for the hemichordate + echinoderm clade from molecular data. This grouping implies that the ancestral deuterostome had features that included an adult with a pharynx and a dorsal nerve cord and an indirectly developing dipleurula-like larva.     

Conserved expression pattern of BMP-2/4 in hemichordate acorn worm and echinoderm sea cucumber embryos

The auricularia larva of sea cucumbers and tornaria larva of acorn worms share striking developmental and morphological similarities. They are regarded as not only an archetype of the nonchordate deuterostome larva, but also an archetype of the origin of chordates. Here we report the characterization and spatial expression patterns of the BMP-2/4 genes of a hemichordate acorn worm (Pf-bmp2/4) and an echinoderm sea cucumber (Sj-bmp2/4). Both the Pf-bmp2/4 and Sj-bmp2/4 genes exhibited apparently conserved expression in the region of the coelomopore complex. This is in agreement with the homology between their basic larval body plans with respect to coelomogenesis and allows us to discuss the evolutionary counterparts of the coelomopore complex in chordates.     

The evolutionary origin of chordate segmentation: revisiting the enterocoel theory

One of the definitive characteristics of chordates (cephalochordates, vertebrates) is the somites, which are a series of paraxial mesodermal blocks exhibiting segmentation. The presence of somites in the basal chordate amphioxus and in vertebrates, but not in tunicates (the sister group of vertebrates), suggests that the tunicates lost the somites secondarily. Somites are patterned from anterior to posterior during embryogenesis. How such a segmental pattern evolved from deuterostome ancestors is mysterious. The classic enterocoel theory claims that chordate mesoderm evolved from the ancestral deuterostome mesoderm that organizes the trimeric body parts seen in extant hemichordates. Recent progress in molecular embryology has been tremendous, which has enabled us to test this classic theory. In this review, the history of the study on the evolution of the chordate mesoderm is summarized. This is followed by a review of the current understanding of genetic mapping on anterior/posterior (A/P) mesodermal patterning between chordates (cephalochordates, vertebrates) and a direct developing hemichordate (Saccoglossus kowalevskii). Finally, a possible scenario about the evolution of the chordate mesoderm from deuterostome ancestors is discussed.     

Modularity of gene-regulatory networks revealed in sea-star development

Evidence that conserved developmental gene-regulatory networks can change as a unit during deutersostome evolution emerges from a study published in BMC Biology. This shows that genes consistently expressed in anterior brain patterning in hemichordates and chordates are expressed in a similar spatial pattern in another deuterostome, an asteroid echinoderm (sea star), but in a completely different developmental context (the animal-vegetal axis). This observation has implications for hypotheses on the type of development present in the deuterostome common ancestor.     

A calcichordate interpretation of the new mitrateeumitrocystella savilli from the ordovician of Morocco

A new mitrate (stem-group craniate sensuJefferies 1979) is described from the Ordovician (Llandeilo) of Morocco and an anatomical and functional interpretation on the basis of the calcichordate theory is given. It is characterized by its small size, marked asymmetry of the anterior part of the head, and extensive resorption of the skeleton.