Cloudina shows

Martynov, Alexander V. & Korshunova, Tatiana A., 2022, Review Renewed perspectives on the sedentary-pelagic last common bilaterian ancestor, Contributions to Zoology 91 (2), pp. 285-352 : 311-316

Terminal Ediacaran Cloudina shows afFinities to both Deuterostomia and

Lophotrochozoa

There is a strong similarity between the fusellar tube structure of the recent pterobranchs Cephalodiscus (fig. 3A, B), Rhabdopleura ( Maletz et al., 2005) , the fossil pterobranch Graptolithina (Urbanek & Dilly, 2000; Maletz & Steiner, 2015) (fig. 3C), and the oblique annulations near the apical/posterior part and other parts of the tubes of the late Ediacaran fossils Cloudina (fig. 3D; Cortijo et al., 2015: fig. 3f; Cai et al.,

2017). This similarity is evident (fig. 3A–D) and cannot be ignored, although cloudinids were never definitely considered as belonging to Pterobranchia. Both Cephalodiscus and cloudinids also possess a multi-layered structure of the tubes (compare fig. 3 A and Cai et al., 2017: Figs. 3b, 7d). Considering that the age of the pterobranchs can now be extended to the earliest Cambrian ( Maletz, 2019), this provides evidence that semi-sedentary/sedentary bilaterian organisms may already have existed in the terminal Ediacaran (thus preceding all modern motile bilaterian phyla) (fig. 1), and that they built their tubes using a special differentiated secretory cephalic shield, like modern Pterobranchia (fig. 3G, H).

In a recent study, a gut and the general organization comparable with the sedentary siboglinid polychaetes were indicated for Cloudina , although not without reservations (Schiffbauer et al., 2020). For example, presence in the recent siboglinids of the tube-secreted vestimentum (Jones, 1985) supports the assessment of a secretory shield for Cloudina (fig. 3; Martynov, 2013). However, it is implausible to infer a straight gut for Cloudina (Schiffbauer et al., 2020) because its tube has a closed apex ( Cortijo et al., 2015: Fig. 2). Furthermore, organization of Cloudina tubes does not exactly match with annelids (Vinn & Zaton, 2012a; Cai et al., 2017). It was also noted that Cloudinidae / Cloudinomorpha may represent a heterogeneous assemblage that includes both cnidarian- and bilaterian-related forms (Selly et al., 2020; Shore et al., 2020; Yang et al., 2020a; Park et al., 2021). These recent considerations not only approve, but instead further support for the sedentary(adult)-pelagic(larva) model of LCBA. Despite assessments of some cnidarian features in cloudinomorphs (Park et al., 2021), the strong bilaterian affinity of Cloudinidae is supported by the presence of the initial tube structure, which is similar to both the primary zooid of pterobranchs and the molluscan protoconch (fig. 2, supplementary fig. S1; Cortijo et al., 2015). Importantly, it is not similar to the initial apical parts of cnidarians (Yang et al., 2020a). Furthermore, while discussing the potential annelid affinity of Cloudinidae , it was remarkably highlighted that “The coincidence of tube morphologies and pseudo-orthogonal organization of fibrillar compounds in graptolites and polychaetes is remarkable …” (Yang et al., 2020a: 8–9). Next, the authors make a reservation: “There are, of course, morphological differences in their construction, as pterobranch tubes are constructed by fusellar half-rings, but such features are absent in cloudinid tubes”. However, here we confirm that tubes of Cloudina may possess oblique annulations ( Cortijo et al., 2015), which are highly similar to the diagnostic fusellar structures for Pterobranchia, including graptolites (figs. 2 and 3). Taking the presence of other significant similarities in the multilayered morphology of tubes (figs. 2 and 3; Cai et al., 2017) and tube microstructure (Yang et al., 2020a) into the consideration, we cannot consider these multiple similarities just a convergence among “heterogenous cloudinomorphs”. In this respect, the recent inclusion into cloudinomorphs of the previously assessed Cambrian potential octocorals (Park et al., 2021) is not necessarily well founded. Therefore, this apparent “heterogeneity” should be not interpreted that cloudinomorphs include an assemblage of completely unrelated forms which are similar due to a convergence. Instead, the basic similarity between various cloudinomorphs (fig. 2) implies that the different, apparently “heterogenous” taxa represent various lineages of evolutionary transitions between semi-sedentary cnidarian-like and bilaterian-like, both with protostomiens and deuterostomiens ancestral organizations.

Thus,at least several Ediacaran Cloudinidae have a closed apical part (the proximal portion according to Moczydłowska et al., 2021: 446) and a distinct protoconch-like terminal structure (figs. 2 and 3, supplementary fig. S1). Zhuravlev (2015: 424) claims that “no protoconch has been found in Cloudina , but that a basal opening is present”, which is in disagreement with available data (figs. 2 and 3, supplementary fig. S1; Cortijo et al., 2015). Also, in the same paper the bases of the tubes in Cloudina were described as “closed” (Zhuravlev, 2015: 424). This is well confirmed by the recently updated taxonomic diagnosis of the type genus of the family Cloudinidae , where the “apical end closed” for the genus Cloudina is explicitly indicated ( Cai et al., 2017). Thus, the presence of a protoconch-like structure within several members of the genus Cloudina and the family Cloudinidae is currently strongly supported and can be directly compared with protoconchs of the earliest Cambrian hyoliths and molluscs, as well as with the initial zooid structures of the later Ordovician graptholites, i.e. with Pterobranchia (figs. 2 and 3). The fossil records of pterobranchs are extended to the early Cambrian ( LoDuca et al., 2015; Slater et al., 2018; Maletz, 2019) and thus are almost conjoined with the preceding Cloudinidae from the terminal Ediacaran. Therefore, there is little doubt that early Cambrian pterobranchs possessed essentially similar initial parts of tubes with the Ordovician graptolites (figs. 2 and 3).

In support of the non-occasional similarities between both general and detailed tube patterns of the terminal Ediacaran Cloudinidae and various bilaterian phyla is the earliest Cambrian single-shelled tubular fossil of the genus Pseudorthotheca (fig. 2). It can be taxonomically assigned either to “tubular problematics” listed near hyoliths ( Devaere et al., 2013), or directly with the annelids (Read & Fauchald, 2022)! As a reservation for annelid affinity, such a considerably molluscan-looking shell as in Pseudorthotheca (fig. 2) is unlikely to have housed a homonomously segmented body and a straight gut, which is consistent with the presence of a basically U-shaped gut among the all Hyolitha and Pterobranchia, as in many molluscs. This conclusion finds further support in the recent taxonomic reassessment of “ Pelagiella ”, an early Cambrian genus with a molluscan-like shell. The majority of species previously included into that genus were re-assigned to the benthic sabellid-like annelid polychaetes (despite the misleading genus name “ Pelagiella ”), whose members fundamentally represent an adult sedentary mode of life and a heteronomous segmentation (fig. 2; Thomas et al., 2020; Landing et al., 2021).

The hyoliths possess a well-defined, distinct protoconch ( Bengtson 2004; Zhuravlev & Wood, 2018; Liu et al., 2020), comparable with both the protoconchs of molluscs and protoconch-like structures of Cloudinidae (fig. 2, supplementary fig. S1). The assessment for Cloudinidae of both organic and biomineralized tubes ( Murdock, 2020; Shore et al., 2020; Park et al., 2021) does not contradict this evaluation. In the mineralization pathways of the apparently disparate cnidarians, cloudinids, echinoderms and molluscs, the same precursor phases to aragonite and calcite biominerals were confirmed and considered as an indication of independent biomineralization events ( Gilbert et al., 2022). However, this does not preclude the presence of these mineralization pathways as a common ancestral feature shared between cnidarians and bilaterians.

Therefore, it is incorrect to assume an exclusively cnidarian affinity for Cloudinidae using clonal reproduction (Park et al., 2021) because, for example, Pterobranchia have extremely well-defined clonal reproduction generally comparable with that of Cnidaria and Cloudinidae (fig. 3). It was also noted that cnidarians have a broad array of clonal reproduction strategies (Zhuravlev, 2012: 214) and therefore a particular form of clonality found in serpulid polychaets (Pernet, 2001) does not necessarely disprove bilaterian affinity of some cloudinids. A protoconch is absent in cnidarians and other features of the benthic cnidarian tube-bearing polyps, as in Coronatae , are also significantly different from Cloudinidae (Werner, 1971; Jarms, 1991; Morandini & Jarms, 2012). The well-defined clonal reproduction in Cnidaria, the terminal Ediacaran Cloudinidae ( Hua et al., 2005; Shore et al., 2021) and early Cambrian and modern pterobranchs, indeed represent that other case of deep developmental similarity, which is underestimated in current studies and will be further addressed in more detail below.

Thus, in contrast to the supposed motile vendobionts with a completely uncertain phylum attribution (fig. 2A, B), for the Ediacaran sedentary/semi-sedentary group Cloudinomorpha it is possible to indicate several particular characters of tube morphology that can be assigned to both particular extinct and modern bilaterian phyla, such as Hyolitha, Mollusca, Annelida and Pterobranchia (figs. 2 and 3). Indeed, we cannot provide an exhaustive set of characters for cloudinomorphs that are diagnosable for each of these particular phyla, e.g., molluscan radula or pterobranch small gill slits, which cannot yet be differentiated in the ancestral cloudinid-like group, and we are also aware of possible additional complications. However, in comparison with the supposed motile Ediacaran taxa (fig. 2), for Cloudinomorpha we may provide such essential features for molluscs and hyoliths as the protoconch, as well as morphological details of the shared microstructure of annelid and pterobranch tubes (Yang et al., 2020a). The significant similarities in the tube structures may in turn imply homological similarity in the respective soft tissue morphologies, responsible for the tube secretion in the form of cephalic shields of pterobranchs and vestimental wings of annelids (fig. 3).

To summarize the multidisciplinary evidence provided above, and as further support, the key developmental features of the protoconch, shell and initial structures of the tubes are also briefly compared here between Cloudinidae , hyoliths, molluscs, annelids, and Pterobranchia (fig. 2C). This ontogenetic (phylotypic)reconstruction is based on the data and an ontogenetic model presented for the apical parts of Cloudina tubes by Cortijo et al. (2015), and the data for several shelled or tubicolous bilaterian phyla (figs. 2 and 3, supplementary fig. S1). Importantly, the relationship within the pseudosegmented Ediacaran taxa is well corroborated by an ontogenetic model (fig. 2B), and it is possible to construct a consistent series (fig. 2C) for these protoconch-bearing Ediacaran, Cambrian and recent representatives of Cloudinidae, Hyolitha , Mollusca, Annelida, and Pterobranchia, despite potential differences in some details of microstructure. It may imply the deeper relationship of all the apparently disparate bilaterian phyla mentioned at the level of ancestral sedentary/ semi-sedentary organization (figs. 2–5).

Segmentation in the sedentary siboglinids is heteronomous and evident only at the posterior part of the body (Rouse, 2001). Therefore, although the bilaterian affinity of Cloudina is compelling, the presence of a homonomous segmentation is not. According to recent paleontological and phylogenetic data, the stem group of at least modern annelids consisted of tube-dwelling sedentary organisms with heteronomous segmentation similar to the recent Magelonidae and Oweniidae ( Beckers et al., 2019; Chen et al., 2020), in spite of the presence of apparently motile annelids at ca. 521 Ma ( Han et al., 2019). For oweniids, the deuterostome features are well known (Smart & Von Dassow, 2009), including at the genomic level ( Martín-Durán et al., 2022). Presence of the deuterostomian characters in the sedentary/semi-sedentary Oweniidae (fig. 2), which are placed among the most basal annelids (and hence members of the traditional “protostomiens”) further confirms the previously mentioned case of morphological and ontogenetic similarities and apparent molecular phylogenetic disparity between non-segmented Lophophorata and Pterobranchia, as evidence of common ancestral organization. According to a number of the available data reviewed here, such an ancestor was unlikely to represent a simple segmented worm, however, this is still commonly indicated on the reconstructions ( Carroll et al., 2001; Chen et. al., 2019; Evans et al., 2020).

In this respect, a peculiar semi-sedentary group, which is still recognized as a separate phylum Sipuncula (Saiz, 2022) with an unsegmented body, tentacle crown, spacious coeloms and U-shaped gut, also recalls both Lophophorata and Pterobranchia, but at the same time, sipunculans can be placed among the basal annelids ( Capa & Hutchings, 2021). According to another analysis the non-segmented Sipuncula retains a sister position to all other annelids( Chen et al., 2020).This intricate combination of characters in the phylum Sipuncula from apparently disparate bilaterian phyla well corroborates the above-mentioned possibility of a deeper ancestral relationship between Cloudinidae, Hyolitha , Mollusca, Annelida and Pterobranchia (fig. 2).

This is also the case of the molecularly defined lophotrochozoans Lophophorata and Oweniidae , but with deuterostomian developmental features ( Martín-Durán et al., 2022). Being related to basal annelids, however, the sipunculans remarkably “do not exhibit any signs of morphological segmentation during development” ( Carrillo-Baltodano et al., 2019: 1628). Furthermore, the segmented origin of deuterostomian hemichordates is also not supported ( Fritzenwanker et al., 2019). For sipunculans and other lophotrochozoans a single-shelled tubular ancestral organization has been recently reconstructed(Smith, 2020). Whilst Cloudinidae were unlikely homonomously segmented, the partition of its tubes into separate tube modules, after a reduction of the ancestral tube, could contribute to further evolution of homonomous segmentation within annelids and other phyla (figs. 2 and 5).

The consolidated data reviewed here therefore refute the motile annelid-like homonomously segmented LCBA (Balavoine & Adoutte, 1998, 2003; Carroll et al., 2001, 2005) and disprove a plainly reconstructed origin of modern bilaterians on the basis of the Ediacaran pseudosegmented problematic taxa ( Evans et al., 2021). This creates special perspectives for the semi-sedentary/sedentary adult bilaterian ancestral organization, since Cloudinidae is the earliest complex sedentary metazoan group, which combines similarities of both major bilaterian clades – protostomes and deuterostomes, and at the same time, still demonstrates some cnidarian features (figs. 2 and 3; Vinn & Zaton, 2012 a, Cortijo et al., 2015; Shore at al., 2020; Yang et al., 2020a; Park et al., 2021).

Applying these data, it is possible to formulate a significant controversy: if, for example, lophotrochozoans and deuterostomians have diverged from an ancestral microscopic or macroscopic shelled motile ancestral group, then fossil records must occur at least at a similar age with the known occurrence of Cloudinomorpha, no later than 551 Ma. However, the motile small shelly fauna appears only towards the early Cambrian (ca. 540 Ma) (Maloof et al., 2010). If we in turn will hypothesize that lophotrochozoans and deuterostomians have diverged from an ancestral microscopic or macroscopic soft-bodied, non-shelled, motile ancestral group, then we must explain the significant similarities in tube patterns and microstructures between Cloudinomorpha, Pterobranchia, Annelida and Mollusca as a pure convergence. However, there is enough detailed similarity (even with potential reservations) and the geological precedence of the cloudinomorphs over any shelled lophotrochozoans as well as tube-bearing deuterostomians (fig. 2; Cortijo et al., 2015; Schiffbauer et al., 2020; Yang et al., 2020a) to prevent us from considering this case as a plain convergence. Additionally, the continued popular assignment of Kimberella as a representative of a motile shell-less ancestral group of at least lophotrochozoans is strongly hampered by the absence of any reliable characters that can help taxonomically assign Kimberella to a particular bilaterian phylum (fig. 2; Vinther, 2015; Wanninger & Wollesen, 2019; Kocot et al., 2020; Runnegar, 2021).

Ultimately, we may explain the absence of any reliable fossils due to preservation and taphonomic bias. Taphonomic bias was presented as one of the explanations of the strong controversy in the presence of significant similarity between the microstructures of sclerites of the sedentary chancelloriids and apparently motile halkieriids (Porter, 2008). However, despite a considerable number of studies, no shelled mollscan-like fossils have been described below the early Cambrian, where tubular Cloudinidae with distinct protoconch-like structures were highly abundant instead (fig. 2). Thus, in that case the significant similarity between tubes of the clonally reproducing sedentary/semi-sedentary Cloudinidae and tubes of the clonal sedentary/semi-sedentary Pterobranchia and Annelida, and also the shells of the semi-sedentary Hyolitha, and those of the motile molluscs is supported by the fossil record. The shelled hyoliths, molluscs, as well as the colonial graptolites appear in the fossil record only after the appearance of cloudinomorphs (figs. 1–3, supplementary fig. S1; Parkhaev, 2008; Kouchinsky et al., 2012; Li et al., 2021b). All this implies that our general understanding of the patterns of the metazoan and bilaterian evolution suffers from significant theoretical and practical restraints and therefore needs to be revised.

Larvae and adults reconciled: an ontogeny-based model of bilaterian origin