Just, 2014 wrote:IntroductionThe aim of this paper is to present a group of non-bilaterian metazoan organisms that cannot at present be placed in an existing phylum. The two species described,
D. enigmatica and
D. discoides (Figs 1–7) in new genus
Dendrogramma of the new family Dendrogrammatidae were collected at 400 and 1000 metres on the Australian continental slope off eastern Bass Strait and Tasmania during a cruise in 1986. The first author subsequently worked up the entire material at Museum Victoria, Melbourne, Australia. The specimens in question were not recognised in the field, but were extracted from bulk samples in the laboratory during sorting (see further under Material and Methods below).
Fig. 1: Figure 1.
Dendrogramma gen. nov., all 15 paratypes of
D. enigmatica and (with *)
D. discoides.
Image visible hereFig. 2:
Dendrogramma enigmatica sp. n., A, holotype, ‘lateral’ view. B, same, aboral view.
Image visible hereFig. 3:
Dendrogramma enigmatica sp. nov., holotype.
Imaage visible here<See article for other image>
For reasons given in the Discussion we cannot refer these specimens to Ctenophora or Cnidaria, two phyla that are often considered diploblastic [1] and bear some resemblance to
Dendrogramma. We therefore place the new genus as
incertae sedis in the Metazoa, pending the collection of more material. We do, however, discuss some possible phylogenetic implications and draw attention to similarities between
Dendrogramma and some fossil medusoids from the Precambrian Ediacara (Vendian) fauna [2].
ResultsMetazoaIt has been suggested during review that Dendrogramma could represent a new non-bilaterian phylum. While we may agree, we refrain from erecting such a high-level taxon for the time being, because new material is needed to resolve many pertinent outstanding questions.
Dendrogrammatidae, new familyurn:lsid:zoobank.org:act:73DFB28C-EF41-48F7-B324-09503D79B382.
Diagnosis.Multicellular, mesogleal, apparently diploblastic animal. Body divided into cylindrical stalk and broad, flat disc (Figs 2A, B, 3, 4, 5A, 7). Simple round mouth opening situated in slightly depressed lobed field on rounded apex of stalk. With gastrovascular system comprising a simple tube centrally in stalk (pharynx) running from mouth to base of disc, then branching dichotomously, including first branching node (Fig. 6B), in disc at right angles to stalk. Epidermis composed of single layer of low, uniform cells; gastrodermis composed of single layer of elongate, vacuolated cells tapering towards narrow gastrovascular canal (pharynx) (Fig. 2C); epidermis of mouth-field lobes with thickened, elongate, apparently vacuolated/glandular cells (Fig. 2D). Dense mesoglea milky translucent when formalin fixed except for refractive sheath of spongiose mesoglea surrounding gastrodermis of gastrovascular canal in stalk (pharynx) (Figs 2C, 5C). Mesoglea criss-crossed by fibrils including cylindrical sheet under epidermis (Fig. 2C, D).
Component genus.Dendrogramma, new genus.
Dendrogramma, new genusurn:lsid:zoobank.org:act:4D13A8A6-8768-4103-AA81-9772D0D0F39E.
Diagnosis.With the characters of the family.
Etymology.The name of the genus alludes to the branching pattern of the gastrovascular system of the disc.
Type-species.Dendrogramma enigmatica new species.
Additional species.Dendrogramma discoides new species.
Dendrogramma enigmatica new speciesurn:lsid:zoobank.org:act:9BBD1C77-4B5B-4248-8B0D-79D598F07E05.
Holotype.Australia, Victoria, S of Pt. Hicks, 38° 21.9′S 149° 20.0′E–38° 21.40′S 149°20.90′E, 1000 m, WHOI epibenthic sled, RV Franklin Stn SLOPE 32, 23 July 1986, G.C.B. Poore et al., NMV F65709.
Paratypes.9 specimens, same data as holotype, NMV F60459. 2 specimens, same data as holotype, ZMUC-DEN-01. 1 specimen used for SEM, same data as holotype, ZMUC-DEN-02. 1 specimen [fragments], Australia, Tasmania, off Freycinet Peninsula, 41° 57.50′S 148° 37.90′E, 400 m, coarse shell, WHOI epibenthic sled, RV Franklin Stn SLOPE 48, 27 July 1986, M.F. Gomon et al., NMV F60458.
Description (holotype).Tapering stalk elongate, about 7/10 as long as disc diameter; length approximately 1.5 width at base of disc. Disc diameter approximately 11 mm (2.8 mm after shrinkage), stalk length approximately 7.8 mm (cf. Fig. 2) (2 mm after shrinkage). Disc nearly circular with single marginal notch and small rounded hump on each side of notch on disc surface. Mouth-field asymmetrically bilobed, reaching farther up one side of the stalk than the other. Disc with 37 terminals of the gastrovascular branches.
Remarks.Dendrogramma enigmatica sp. nov. differs from the following species by its much longer stalk with a bilobed mouth field, and a marginal notch in the disc.
Etymology.This species has been and still is a great enigma.
Dendrogramma discoides new speciesurn:lsid:zoobank.org:act:4EDB8115-4138-4682-9A79-76D8DFB19650.
Holotype.Australia, Victoria, S of Pt. Hicks, 38° 21.9′S 149° 20.0′E–38° 21.40′S 149°20.90′E, 1000 m, WHOI epibenthic sled, RV Franklin Stn SLOPE 32, 23 July 1986, G.C.B. Poore et al., NMV F65710.
Paratypes.2 specimens, data as holotype, NMV F65711. 1 specimen, data as holotype, ZMUC-DEN-03.
Description (holotype).Stem short, length approximately 1/10 disc diameter; not longer than wide at base of disc. Disc diameter approximately 17 mm (3 mm after shrinkage), stalk length approximately 4.5 mm (cf. Fig. 6 C). Disc circular with entire margin. Mouth-field of three lobes, two lobes of equal length both longer than the third lobe. Disc with 63 terminals of the gastrovascular branches.
Remarks.Dendrogramma discoides sp. nov. differs from
D. enigmatica by its much shorter stalk and entire disc.
Etymology.This species is named for the shape of the disc.
DiscussionThe two
Dendrogramma species are multicellular (metazoans), non-bilaterian, apparently diploblastic animals with a dense mesoglea between an outer epidermis and an inner gastrodermis. The animals are composed of a body divided into a stalk with a mouth opening terminally, and a flattened disc. The mouth is set in a specialised, lobed epidermis field, leading into a gastrodermis-lined gastrovascular canal (pharynx) in the stalk which aborally branches dichotomously into numerous radiating canals in the disc. While the animals are certainly multicellular, the precise structural identity of the epithelia lining the gastrovascular canal and the external remain to be studied and compared to that of other metazoans.
Dendrogramma shares a number of similarities in general body organisation with the two phyla, Ctenophora and Cnidaria, but cannot be placed inside any of these as they are recognised currently. We can state with considerable certainty that the organisms do not possess cnidocytes, tentacles, marginal pore openings for the radiating canals, ring canal, sense organs in the form of e.g., statocysts or the rhopalia of Scyphozoa and Cubozoa, or colloblasts, ctenes, or an apical organ as seen in Ctenophora. No cilia have been located. We have not found evidence that the specimens may represent torn-off parts of colonial Siphonophora (e.g., gastrozooids). Neither have we observed any traces of gonads, which may indicate immaturity or seasonal changes. No biological information on
Dendrogramma is available. To judge from their construction, both species appear unable to swim (the ‘disc’ appears inflexible in preserved specimens). With their small, simple mouth opening it would seem likely that they feed on micro-organisms, perhaps trapped by mucus from the specialised lobes surrounding the mouth opening.
Although
Dendrogramma cannot at present be referred to Ctenophora or Cnidaria, those two phyla share more characteristics with Dendrogramma than does any other phylum. These include the presence of apparently only two germ layers (diploblastic) with a mesoglea in between (but see [3] for discussion of a third germ layer in Ctenophora), and the presence of a single mouth opening through which food is ingested and waste is released, leading into a gastrovasular cavity becoming highly branched terminally. It is therefore possible that
Dendrogramma may eventually find a phylogenetic position as closely related to one of these phyla (e.g., as sister group), but at present no unique characters suggesting close affinity to any of these has been found (see above).
The question of the phylogenetic position of
Dendrogramma also depends on how the basal metazoan lineages are related to each other, a question which can be reduced to considering the relationship between Porifera, Placozoa, Cnidaria, Ctenophora, and Bilateria [4], [5]. In theory 105 possibilities exist for grouping five taxa, but only few have in this case actually been suggested [5]. The traditional view is that Porifera is sister group to all other animals, a view based on their lack of tissue organisation, lack of nervous system, and the similarities of choanocytes to choanoflagellates [3] (Fig. 8). However, a recent finding, supported by much molecular data (incl. genomic data for all major taxa), proposes that Ctenophora, rather than Porifera, is sister group to all other metazoans [6], [7], [8], [9]. Due to this significant conflict regarding deep metazoan phylogeny, we have chosen to illustrate possible positions of
Dendrogramma on a phylogeny with two different positions of Ctenophora (Fig. 8). Regardless of the position of Ctenophora, we suggest that the most likely position of
Dendrogramma is before Bilateria, being related to either Ctenophora and/or Cnidaria based on the general similarities in body organisation (e.g., presence of mesoglea and gastrovascular system). If indeed Porifera is the sister group to the remaining metazoans as traditionally perceived and recently supported by a re-analysis [10], [11] of a major molecular dataset from [6], [7], and if Ctenophora and Cnidaria are sister taxa ( = Coelenterata), as was the result of the same re-analysis [10], [11], then
Dendrogramma may be related to Coelenterata.
Ctenophora positioned as sister group to the remaining Metazoa (‘Ctenophora-first’ hypothesis) has recently been supported by adding the genome of a second ctenophore as well as the transcriptome of several other ctenophores [9]. In the same study it was suggested that neural systems in ctenophores evolved independently from those in other animals. If indeed Ctenophora and Cnidaria are placed widely separated (see Fig. 8), it is likely that also the general body organisation of Ctenophora and Cnidaria has evolved in parallel from a poriferan or placozoan-like ancestor. Then the most likely position of
Dendrogramma would be as sister group to either Ctenophora or Cnidaria based on the similarities in general body organisation. In this way the lack of tissue organisation and nervous system (etc.) in Porifera would be original attributes. However, if the similarities between Ctenophora and Cnidaria regarding general body organisation are homologous (but symplesiomorphic), then this significantly broadens the spectrum of possible phylogenetic positions of the mesogleal
Dendrogramma. Then, all that can be said is that
Dendrogramma should be placed somewhere before the Bilateria (yellow area in phylogeny in Fig. 8). In this scenario a multitude of possible positions exist, including sister group to any of the involved taxa (incl. Ctenophora or Cnidaria), and even a position as sister group to the remaining Metazoa is possible.
In summary, the available information about
Dendrogramma does not allow for a more precise phylogenetic position than being before the Bilateria, possibly on either the lineage leading to the Ctenophora and/or Cnidaria. A more robust phylogeny between the five basal metazoan lineages (Ctenophora, Placozoa, Porifera, Cnidaria, Bilateria) is needed before strong conclusions on the evolution of important characters (such as number of germ layers and presence of nervous system) can be made. In addition, fresh material of
Dendrogramma appropriately fixed for molecular (genomic) studies, ultra structure, and histology together with additional biological information, if possible, should be obtained before a proper phylogenetic placement can be made. From a morphological point of view, detailed information about the epithelial structure, composition of the mesoglea, nervous system, and muscles fibres (if present) are particularly wanted for comparison with other non-bilaterians.
It is widely thought that bilateral symmetry evolved in the common ancestor of Bilateria, but it has long been known that some members of Cnidaria also exhibit bilateral symmetry [12]. Based on studies of Hox genes it has been suggested that bilateral symmetry already evolved before the Cnidaria diverged from Bilateria [12], [13]. The considerable difference in global symmetry between the two species of
Dendrogramma is additional evidence that symmetry is highly plastic. Both species of
Dendrogramma exhibit bilateral aspects notably in the lobed field surrounding the mouth opening and in the initial dichotome branching node of the radiating canals. The disc of
D. enigmatica is clearly bilateral as indicated by the disc notch. The distal extremity of the stalk of
D. discoides can be interpreted as triradial in which case the unequal length of the lobes of the mouth field is just localised bilateral symmetry. The disc of
D. discoides may be interpreted as radial symmetric. Considering the differences in symmetry pattern between the two species, even in different parts of the body, the issue of the origin of bilateralism may add additional interest to the study of new material of
Dendrogramma.
Finally, we would like to point to an interesting similarity between
Dendrogramma and a small group of Precambrian Ediacara (Vendian) trilobozoid medusoids. In particular we draw attention to taxa such as
Albumares, Anfesta, and
Rugoconites (the last mentioned is not included in the Trilobozoida by all authors). All three have dichotomously branching radiating canals in a disc.
Rugoconites tenuirugosus Wade, 1972 (Figs 6 E and F3; size range in the two richest
Rugoconites beds: 9–29 mm, see [14) appears to be seen in aboral view with a presumed triradiate initial central branching node. This may well be an artefact. If
Dendrogramma were to be fossilised in the same position it would most probably exhibit the same pattern, in spite of the central (first) branching node being actually dichotomous.
Albumares brunsae Fedonkin, 1976 (Fig. 6 D, F1; size range 8–15 mm) and
Anfesta stankovskii Fedonkin, 1984 (Fig. 6 E2; size range 5–18 mm) both possess a trilobed field radiating from the centre, similar to the adoral lobed field of
Dendrogramma discoides. In view of the considerable depth at which the
Dendrogramma species were collected we note that the Ediacaran fauna (including some medusoids) of several Canadian locations, e.g. Newfoundland and the Mackenzie Mountains, appear to have lived at bathyal depth to more than 1000 meters [2]. We are aware that the similarities to some of the Ediacaran forms may be independent responses to the same environmental necessities, rather than being evidence of homology. But, if indeed the similarities between
Dendrogramma and Ediacaran forms such as
Albumares, Anfesta, and
Rugoconites (Fig. 6E–F) are indicators of close relationship, it has interesting phylogenetic implications and may throw light on the origin of these Ediacaran taxa. Then, if
Dendrogramma is an off split of either the lineage leading to Ctenophora and/or to Cnidaria (Fig. 8), as suggested by us,
Albumares, Anfesta, and
Rugoconites would also be in such a position and should therefore be considered ingroup metazoans rather than being a member of a monophyletic extinct kingdom ‘Vendozoa’. The latter taxon has been suggested to be a failed experiment with multicellularity independent of that of the ‘true’ Metazoa [15]. A metazoan affinity of many Ediacaran forms was suggested already early (e.g., as cnidarians or echinoderms, see [16]), a notion that have been supported lately for a number of taxa such as
Tribrachidium (as a sponge or ctenophore-type organism),
Kimberella (mollusc), or
Dickinsonia (early placozoan) [17,18,19,20,21 22]. The possibility of the Ediacaran taxa
Albumares, Anfesta, and
Rugoconites being true metazoans as mentioned above, based indirectly on the presumed position of
Dendrogramma is therefore in line with this more recent phylogenetic treatment of various Precambrian Ediacaran forms.