Conceived and designed the experiments: JBC SCM. Analyzed the data: JBC SCM. Contributed reagents/materials/analysis tools: JBC DS. Wrote the paper: JBC SCM DS.
The authors have declared that no competing interests exist.
Molecular and morphological evidence unite the hemichordates and echinoderms as the Ambulacraria, but their earliest history remains almost entirely conjectural. This is on account of the morphological disparity of the ambulacrarians and a paucity of obvious stem-groups. We describe here a new taxon
An understanding of the Cambrian “explosion” arguably provides one of the best avenues to tackling two major questions in evolutionary biology: How are metazoan bodyplans assembled and what, if any, role do macroevolutionary processes play? In addition, this event provides a crucial test as to the relevance of the fossil record either to decide between conflicting phylogenetic hypotheses or to determine the actual course of events. Given the crucial contributions of the fossil record to understanding such key episodes as the terrestrialization of the sarcopterygian fish or the capacity of theropod dinosaurs to engage in flight, then it might seem paradoxical that equivalent material is of ambiguous status when it comes to the interpretation of the Cambrian “explosion”. The reason largely revolves around the fact that a significant number of these early animal fossils have very unfamiliar, if not bizarre, anatomies, exhibiting a combination of characters not encountered in any extant phyla
What then is the best line of approach when it comes to establishing their evolutionary position? One procedure is to treat these ostensibly strange fossils as extinct bodyplans. In the literature these are often equated with the level of phylum, and the idea of a plethora of extinct Cambrian phyla has played a significant role in evolutionary interpretations of the Cambrian “explosion”
It is important to recall that not only is the concept of phyla essentialist but it serves to place problematic taxa in a phylogenetic limbo, rendering them effectively immune to further evolutionary analysis. An alternative strategy is to assign a supposedly enigmatic taxa to one or other extant group, that is somewhere within a given crown-group. This, however, is often a procrustean process. This is because it generally relies on comparisons between various structures in the fossil material (the preservation of which may be less than perfect) and extant material, a procedure that may be based on pre-suppositions that are not necessarily spelt out unequivocally. So too by placing these enigmatic Cambrian taxa in crown-groups, it can presuppose a deeper origin of phyla than appears to be consistent with the fossil record. A third way is to assign these fossils to various stem-groups of either a major phylum (e.g., an echinoderm) or some more embracive super-clade (e.g., the ambulacrarians). This procedure has, however, its own difficulties. This is because of the need to homologize morphologically disparate structures, a procedure which is effectively the converse of attempting to accommodate these taxa in crown-groups. The advantage of this approach is that it has the potential to explain how key characters evolved in the emerging bodyplans within a functional and ecological context. These characters can then be placed in a series of paraphyletic stem-groups
In principle, by testing various evolutionary scenarios a cladistic methodology will be able to impart a rigorous approach when dealing with the evolution of bodyplans and the interpretation of Problematica. In practice, however, this ideal remains somewhat elusive. The fact remains that the available fossil record is very patchy and as often as not, there is a dearth of very well-preserved material and characters available.
Despite these difficulties there does appear to be some progress in the identification of metazoan groups amongst various Cambrian taxa. Here we aim both to extend this process, but also provide a model example of the difficulties that emerge as the comparisons are extended to higher taxonomic levels. In brief, on the basis of conspicuous morphological similarities we demonstrate that a new soft-bodied fossil from the Middle Cambrian Burgess Shale (
A, lectotype, National Museum of Natural History (USNM) 57540 Part, overall view. B–C, USNM 188552; B, Part, overall view; C, detail of the tentacles. D, USNM 201692 Part, overall view, arrows pointing to triangular projections representing evidence of possible segmental mesenteries. Scale bars: 10 mm. an, anus; in, intestine; ph, pharynx; stom, stomach; te, tentacle. (Photos D. Collins).
?Superphylum Ambulacraria
Cambroernids, in reference to the stratigraphic age and prominent branched tentacles (Greek,
Metazoans with prominent feeding tentacles and conspicuous gut housed in a coiled coelomic sac suspended by mesenterial elements, body form ranging from pedunculate to discoidal.
urn:lsid:zoobank.org:act:F9124AEB-1937-4570-881D-6068AE78A62E
The genetic name refers to the collectors' nick-name “creeposaurus” [creeping aspect of the animal] (Greek,
ROM 58051. 100 additional specimens: ROM 57164, 57167, 58022-58090, 58158-58160, 58928-58930, 59850, 59852-59854.
Burgess Shale and Stephen Shale Formations; Middle Cambrian, Yoho and Kootenay National Parks, British Columbia, Canada.
Segmented body, coiled dextrally. Short head bearing prominent anterior dendritic tentacles and pharyngeal structures, possibly lateral pores. Trunk, sub-cylindrical, divided into two sub-sections, narrowing posteriorly. Ventral and contractile adhesive stolon, sometimes with terminal disc. Digestive tract with anterior mouth, pharynx, voluminous stomach, and narrow intestine with terminal anus. Stomach and intestine of sub-equal lengths, un-looped, with triangular mesenterial insertions.
urn:lsid:zoobank.org:act:2759BD4E-6ACA-4C5D-92A2-29DF511E3071
Head with bilateral tentacles in basal two plus two arrangement, sub-equal length, monopodial, fractal-like branching. At least 13 trunk segments, well developed on dorsal anterior.
Whilst we present evidence for a relationship between
A–B, Locality maps. C, specimen occurrences.
The body of
All specimens are preserved dorso-ventrally, except F. In each photographic figure anterior is indicated by a wide white arrow. A–C, Royal Ontario Museum (ROM) 58051 Holotype. A, Part, overall view; B, Counterpart, detail of tentacles with hydrostatic canal and/or vascular system emphasized by white arrows; C, Camera-lucida drawing of part and counterpart emphasizing the presence of putative segment boundaries and triangular projections along the stomach. D, ROM 58046 Part, with symmetrical tentacles and pharyngeal pores. E, ROM 58039 Counterpart, intestine with putative enclosing tube emphasized by small arrows. F, G, ROM 58037 Part. F, Part, lateral view; G, Detail of terminal disc. H, I, ROM 58047 Part. H, extended stolon and terminal disc; I, Detail of the stolon, small arrows point to a darker central area representing a possible coelomic cavity. Scale bars: A–F, H, 5 mm; G,I, 1 mm. an, anus; hy?, putative hydrostatic canal and/or vascular system; in, intestine; p?, putative pharyngeal pores; ph, pharynx; seg, segment boundary?; st, stolon; stom, stomach; td, terminal disc; te, tentacle.
© 2010 - Marianne Collins.
The tentacles (
In dorso-ventral specimens the frontal margin of the head is straight and broad (
The mouth is assumed to have been located on the anterior margin and between the tentacles. A central darker area, which in dorso-ventral view occupies much of the head, is interpreted as a pharynx (
An elongate structure, termed here the stolon, extends from approximately the ninth trunk segment. It evidently arises from the ventral mid-line (
The somewhat older
A, ELI-Phl-07-001 lateral view, complete specimen with the stolon attached to a fragment of trilobite exoskeleton. B, ELI-Phl-07-002 oral view, specimen showing four tentacles (the broken area suggests the possibility of a fifth set) and three preserved lobes. C–D, ELI-Phl-07-003 lateral view; C, overall view of the gut; D, detail of the anus. Scale bars: A–C, 5 mm; D, 1 mm. Legend, see
The best known eldoniids come from various Cambrian fossil Lagerstätten:
The overall similarities between
Accepting our arguments for significant homologies that unite
As noted above in the introduction, the problems of assigning apparently problematic taxa (which are by no means confined to the Cambrian
With respect to the lophotrochozoans an affinity to either the annelids or sipunculans seems unlikely, not least because the tentacles in annelids (notably the serpulids and sabellids) originate from multiple segments. In addition, the sipunculans may well nest within the annelids themselves
Any attempt at a comparison between extant lophotrochozoans, notably the tentaculate ectoprocts (and by implication possibly the entoprocts
In principle, however, a comparison with the entoprocts
A possible relationship between
In addition, extant pterobranchs are miniaturized and colonial, live in tubes and their U-shaped gut is probably a consequence of this miniaturization and sessile lifestyle. These characters probably evolved early on in the history of this clade as is evident from the graptolites
A = stem-group hemichordate, B = stem-group echinoderm, C = stem-group ambulacrarian.
A relationship to crown-group echinoderms has received attention on account of comparisons between
We should also note that Chen
Unfortunately these ideas are difficult to test in much detail because of: a) important but disputed inferences concerning the soft-bodied anatomy of the pre-radial echinoderms, b) the considerable disparity of this assemblage, and correspondingly c) the controversial nature of their earliest evolution
Importantly, however, in the context of a possible relationship to the cambroernids, the cinctans are hypothesized to have possessed a water vascular system with right and left-hand hydrocoels presumably extending into two tentacular elements of unequal size
Based on molecular phylogenies, fossils and detailed developmental studies, the last common ancestor of hemichordates and echinoderms is predicted to have been bilaterally symmetrical, a filter feeder with a paired water vascular system constructed from right and left hydrocoels, and with a muscular post-anal stalk (
Any discussion of the stem-group ambulacrarians must also in principle consider the somewhat problematic xenoturbellans, a group of modern free-living worm-like animals. In
Arriving at a precise phylogenetic position for the cambroernids, therefore, has proved difficult. On balance a place amongst the tentaculate lophotrochozoans seems to be less persuasive. Given a place within the ecdysozoans is even less plausible, then the final possibility must be to look to the deuterostomes. Here, as noted the options revolve around a series of possibilities, including a stem-group echinoderm, a hemichordate or an ambulacrarian. Whilst this list of possibilities might seem to leave the matter largely unconstrained, it is important to stress that from a Cambrian perspective the morphological differences between these various alternatives were probably insignificant. If, for the sake of the argument, the position of the cambroernids does indeed lie near the branching point of the two main ambulacrarian clades that led ultimately to the echinoderms and hemichordates, then we should not be surprised that it seems reminiscent of both pterobranchs and pre-radial echinoderms.
Finally, if accepted as some sort of deuterostome then these fossils have some further interesting implications. For example, consider the possible segmentation in
Most specimens of
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A, camera lucida of the holotype of
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Camera-lucida drawings of
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We thank G. Giribet and M. Zhu for their constructive reviews, A. Smith and K. Peterson for many helpful comments on earlier versions of this manuscript, and M. Reitner, C. Cameron for respective discussions on holothurians and hemichordates. Secretarial assistance by V. Brown, and collection assistance by P. Fenton is also greatly appreciated. We thank Parks Canada for granting successive collection permits to Royal Ontario Museum field crews.