2.a. The rangeomorph skeleton

Whatever the particular habits of Ediacaran macrofossils, they were clearly supported by some sort of skeletal superstructure, an anatomical feature that is likely to illuminate other aspects of their biology. In the absence of obvious biomineralization, this has been widely envisaged as a hydrostatic endoskeleton, comparable to the coelomic system of annelid worms (Runnegar, Reference Runnegar1982), the syncytia of giant ‘unicellular’ protists (Seilacher, Reference Seilacher1989, Reference Seilacher1992; Seilacher et al. Reference Seilacher, Grazhdankin and Legouta2003) or a sponge-grade mesenchyme-like mass (Dufour & McIlroy, Reference Dufour and McIlroy2017). More generally, Laflamme et al. (Reference Laflamme, Xiao and Kowalewski2009) have argued that ‘much of the internal body cavity… may have been filled by metabolically inactive material (inorganic, organic, or fluid).’

The key to resolving the nature of the rangeomorph skeleton lies in its taphonomic dissection. Although most rangeomorphs are preserved as more or less 2D bedding-plane imprints – a product of felling, degradational collapse and early diagenetic ‘death-mask’ cementation – there is a notable subset of specimens that have been preserved as conspicuously 3D casts and moulds (Jenkins, Reference Jenkins1985; Fedonkin, Reference Fedonkin and Bengtson1994; Dzik, Reference Dzik2002; Grazhdankin & Seilacher, Reference Grazhdankin and Seilacher2005; Vickers-Rich et al. Reference Vickers-Rich, Yu Ivantsov, Trusler, Narbonne, Hall, Wilson, Greentree, Fedonkin, Elliott, Hoffmann and Schneider2013; Sharp et al. Reference Sharp, Evans, Wilson and Vickers-Rich2017). Such sedimentary infilling points to the presence not only of large internalized chambers, but also chamber walls of sufficient integrity to act as the containing form. In Charnia specimens from the Winter Mountains of the White Sea, for example, substantial parts of the fronds have been infilled with silt early and rapidly enough to capture their full 3D profile (Fedonkin, Reference Fedonkin and Bengtson1994; Grazhdankin, Reference Grazhdankin2004; Dunn et al. Reference Dunn, Wilby, Kenchington, Grazhdankin, Donoghue and Liu2018), even as adjacent unfilled areas collapsed to yield a more typical 2D death-mask (Fig. 2).

Fig. 2. Partially cast 3D specimens of Charnia from the Verkhovka Formation (Winter Mountains, White Sea, Russia), demonstrating the previous presence of water-filled chambers. (a, b) ‘Upper’ and ‘lower’ surfaces of PIN 3993-7018 (with differential transfer of the primary branch casts between the two parts); note that only some parts of this specimen have been infilled with sediment (roughly the left-hand side of (a) and the right-hand side of (b)), with the remainder experiencing a more typical ‘collapse and death-mask’ type of preservation. The three serially repeated lensoid structures preserved on the upper side of the cast (arrows in (a)) potentially represent openings into the chambers; they are not present on the lower ‘fractally’ divided side (b), and are not preserved in collapsed parts of the frond. (c) Cross-section through a silt-cast primary branch of PIN 3993-7018, locally buried in mud and showing anatomical continuity between the chambers and serially repeated lensoid structures (arrowed); line of section indicated by the dotted line in (b). (d) Cross-section through a silt-cast primary branch of PIN 3993-7018, locally buried in cross-laminated silt and showing clear evidence of erosive breaching and loss of the upper body wall; line of section indicated by asterisks in (b). (e) Detail of a further silt-cast, mud-buried specimen (PIN 3992-7020) preserving serially repeated lensoid structures on the upper, non-fractally divided surface (arrows); the full specimen is figured in Fedonkin (Reference Fedonkin and Bengtson1994). Scale bar: (a, b, e) 1 cm; (c) 2.5 mm; and (d) 5 mm. PIN – Palaeontological Institute, Moscow. Photo credits: (a, b, c, e) Dima Grazhdankin; and (d) Alex Liu.

Casting is a common mode of preservation in biomineralized or heavily lignified organisms, but is less expected in ‘soft-bodied’ Ediacaran forms (Seilacher, Reference Seilacher1970; Rex, Reference Rex1985; Retallack, Reference Retallack1994; Maeda et al. Reference Maeda, Kumagae, Matsuoka and Yamazaki2010). Where it does occur, the process will be similarly dependent on chambers with self-supporting walls, but proceeding on fundamentally shorter timescales. Given the rapidly collapsing 2D habit of rangeomorphs in general, it follows that the original contents of the chambers must have been correspondingly fluid. The effectively instantaneous casting of Charnia compartments (Fig. 2) is inconsistent with the original contents having the viscosity of syncytial cytoplasm (cf. Seilacher, Reference Seilacher1989, Reference Seilacher1992), mesenchyme (cf. Dufour & McIlroy, Reference Dufour and McIlroy2017) or coelomic fluids (cf. Runnegar, Reference Runnegar1982), particularly given the rapid wound-repair systems associated with these fully isolated hydrostatic skeletons (e.g. Menzel, Reference Menzel1988; Duckworth, Reference Duckworth2003; Kamran et al. Reference Kamran, Zellner, Kyriazes, Kraus, Reynier and Malamy2017). By far the most likely material filling the compartments of rangeomorphs – and conferring their primary skeletal support – is locally contained low-viscosity seawater.

In the absence of obvious openings in the body wall (Narbonne, Reference Narbonne2004), the route by which such water entered rangeomorph chambers has yet to be identified. One likely possibility is that the conduits were simply too small or ephemeral to fossilize under the associated taphonomic regimes. Even with the fundamentally greater levels of resolution seen in Burgess Shale-type preservation, for example, the ostia and associated aquiferous system of sponges have never been directly preserved (Butterfield, Reference Butterfield2003). The external openings of water-pumping siphonozooids in colonial octocorals can be similarly cryptic, even in living specimens (Fig. 3d) (Hickson, Reference Hickson1883; Brafield, Reference Brafield1969; Nonaka et al. Reference Nonaka, Nakamura, Tsukahara and Reimer2012; Williams et al. Reference Williams, Hoeksema and Van Ofwegen2012), and it is notable that the millimetre-sized siphonozooids of certain pennatulaceans fail to preserve even under the most optimized laboratory burial conditions (Norris, Reference Norris1989).

Fig. 3. Extant anthozoan cnidarians exhibiting features of relevance to the interpretation of Ediacaran rangeomorphs. (a) The modern actiniarian Metridium, demonstrating the disparate range of forms possible by a single specimen depending on the retention and deployment of seawater within the gastrovascular cavity. In the absence of muscle, such an organism would be unable to operate tentacles or a central mouth, although it could still (in principle) function as a suspension-feeding extra-cellular digestion chamber. (b) Scanning electron micrograph (SEM) of the colonial alcyonacean Corallium, showing the surface expression of retracted autozooids (muscle-powered micro-predatory feeding polyps) and cryptically embedded siphonozooids (cilia-powered atentaculate polyps specialized for circulating seawater); the latter are unlikely to be recognizably preserved in the fossil record, even under the most exceptional taphonomic circumstances. (c) Schematic transverse section through a single siphonozooid of the colonial alcyonacean Paragorgia, showing its ciliated water-pumping siphonoglyph (shaded dark blue) and interconnecting gastrovascular canal system (light blue). (d) Schematic longitudinal section of Paragorgia, showing multiple water-pumping siphonozooids with cryptically small external openings (siphonoglyphs shaded dark blue, gastrovascular canals light blue). Scale bar: (a) 2 cm; (b, d) 1 mm; and (c) 0.25 mm. (a) From Batham & Pantin (Reference Batham and Pantin1950), reproduced with permission of the Journal of Experimental Biology. (b) Modified from Nonaka et al. (Reference Nonaka, Nakamura, Tsukahara and Reimer2012). (c, d) Modified from Hickson (Reference Hickson1883).

Considering that such features are only expected under the most exceptional taphonomic circumstances, it is worth revisiting Grazhdankin’s (Reference Grazhdankin2004) original documentation of the 3D Winter Mountains Charnia. Intriguingly, the upwards-facing surfaces of at least two specimens bear serially repeated lensoid structures (Fig. 2a, e, arrows) that are not preserved in corresponding 2D fossils. The continuity of fossil-casting silt through these millimetre-sized structures (Fig. 2c, arrows) points to their likely function as anatomical conduits connecting the internal chambers to surrounding seawater. Taphonomic merger of the ‘upper’ and ‘lower’ surfaces during more typical death-mask preservation readily accounts for their absence in most Charnia fossils (Fig. 4c, d), as well as the misleading impression that the two sides of Charnia fronds were morphologically identical (cf. Dunn et al. Reference Dunn, Wilby, Kenchington, Grazhdankin, Donoghue and Liu2018). Indeed, the preservation of original spatial relationships in these exceptional specimens demonstrates that much of the underlying ‘fractal’ architecture was associated exclusively with the ‘lower’ surface (Fig. 2a, b). In view of their conspicuously mouldic expression, the ‘third-order branches’ of Charnia also appear not to define external morphology, but rather internalized mesentery-like structures – presumably with a primary purpose in expanding internalized surface area (Fig. 4).

Fig. 4. Schematic reconstruction of the constructional and functional anatomy of rangeomorphs, alongside possible taphonomic pathways. (a) Chambered construction with a central mesoglea-like layer (black) supporting a ciliated epithelium; external epidermis (brown) serves as an important locus of high Re/Pe gas exchange, whereas the internalized ‘gastrodermis’ (orange) is optimized for feeding at macroscopic length scales. Overall support is provided by transiently contained seawater (grey). (b) Suspended DOC and POC is cycled through the internalized system via ciliary transport and siphonoglyph-like pumping. Chamber walls are likely to have hosted a diverse, mostly anaerobic microbiome (coloured dots), contributing to gut-like extracellular digestion. (c) Three-dimensional casting of rangeomorph chambers following high-energy erosive breaching of the body wall. (d) Collapse and 2D ‘death-mask’ preservation where the body wall remains intact; the telescoping of spatially separated features onto a single surface yields specimens that appear similar on both surfaces, and obscures key aspects of the original anatomy.

Whether or not the serially repeated lensoid structures represent biological openings in the Charnia integument, it is unlikely that they provided the primary conduit for the infilling sediment. Comparable structures are not recorded in similarly preserved Rangea specimens (e.g. Jenkins, Reference Jenkins1985; Grazhdankin & Seilacher, Reference Grazhdankin and Seilacher2005; Vickers-Rich et al. Reference Vickers-Rich, Yu Ivantsov, Trusler, Narbonne, Hall, Wilson, Greentree, Fedonkin, Elliott, Hoffmann and Schneider2013; Sharp et al. Reference Sharp, Evans, Wilson and Vickers-Rich2017), and such openings in living organisms are almost universally guarded by ciliated and/or contractile cells. Full 3D preservation also requires sufficient ‘draft-through’ flow to deliver the casting sediment prior to degradational collapse (cf. Seilacher, Reference Seilacher1970; Rex, Reference Rex1985; Maeda et al. Reference Maeda, Kumagae, Matsuoka and Yamazaki2010), suggesting substantially larger-scale access to the internalized chambers. Given the high-energy tempestite conditions under which the Winter Mountains Charnia were buried (Grazhdankin, Reference Grazhdankin2004), the most likely route of silt-entraining currents would have been through abrasive breaches in the thin body wall (cf. de Bettignies et al. Reference de Bettignies, Thomsen and Wernberg2012). Indeed, the depositional continuity from fossil-casting silts to overlying cross-laminated horizons in PIN 3993-7018 (Fig. 2d) demonstrates the localized erosion of upwards-facing portions of the frond; it is only where the casts are locally succeeded by low-energy muddy laminae that the differentiated anatomy of this surface is preserved (Figs 2a, e, 4c). In a similar vein, Brasier et al. (Reference Brasier, Liu, Menon, Matthews, McIlroy and Wacey2013) have interpreted features of the high-relief rangeomorphs at Spaniard’s Bay as the consequence of body-wall rupture and/or removal during hydraulic scouring events, and it is notable that the majority of three-dimensionally cast rangeomorphs occur in conspicuously more abrasion- and transport-prone ‘Nama-type’ facies (Grazhdankin, Reference Grazhdankin2004; Grazhdankin & Seilacher, Reference Grazhdankin and Seilacher2005; Vickers-Rich et al. Reference Vickers-Rich, Yu Ivantsov, Trusler, Narbonne, Hall, Wilson, Greentree, Fedonkin, Elliott, Hoffmann and Schneider2013; Sharp et al. Reference Sharp, Evans, Wilson and Vickers-Rich2017).

Rapid sedimentary casting of bag-like compartments is also documented in a range of co-occurring non-rangeomorph Ediacaran taxa. Among the most spectacular examples are in situ, vertically oriented populations of Charniodiscus in Zimnie Gory sections of the White Sea (Grazhdankin, Reference Grazhdankin2014; Ivantsov, Reference Ivantsov2016), reclined but similarly frondose Pambikalbae and Arborea from Nilpena in South Australia (Jenkins & Nedin, 2007; Laflamme et al. Reference Laflamme, Gehling and Droser2018; Dunn et al. Reference Dunn, Liu and Gehling2019; Droser et al. Reference Droser, Tarhan, Evans, Surprenant and Gehling2020) and globular tripartite Ventogyrus from the Onega River area of the White Sea (Ivantsov & Grazhdankin, Reference Ivantsov and Grazhdankin1997; Fedonkin & Ivantsov, Reference Fedonkin and Ivantsov2007). All of these fossils have been variably infilled during event-bed sedimentation, yielding a taphonomic continuum from fully inflated 3D casts through to essentially 2D death-mask imprints. As with rangeomorphs, the form of the casts directly mirrors that of the external moulds, attesting to the thin deformable nature of the chamber walls (Jenkins & Nedin, 2007; Sharp et al. Reference Sharp, Evans, Wilson and Vickers-Rich2017) and the presence of a rapidly displaceable, chamber-filling fluid. Also like rangeomorphs, there is little direct evidence of the openings through which seawater may have entered in life but, similarly, no expectation that these should be recognizably preserved. Again, the infilling sediment was most likely introduced via abrasional breaches in thin body walls. Regardless of any phylogenetic connection to rangeomorphs, the localized 3D casting of these arboreomorphs and other problematica point to a similar grade of chambered construction and hydrostatic support.

2.b. Functional morphology of hydrostatic exoskeletons

The recognition of rangeomorph chambers with direct conduits to the external environment means that the contained seawater was topologically on the outside of the organism, that is, within a bag-like hydrostatic (exo)skeleton. There is nothing particularly exotic about such a system; indeed, it is the primary means of structural support among basal eumetazoans. In actiniarian (sea anemones) and pennatulacean (sea pens, etc.) anthozoans, for example, it is transiently retained seawater in the gastrovascular system that provides the antagonist against which epithelial muscle acts to generate overall form and movement (Fig. 3a) (Batham & Pantin, Reference Batham and Pantin1950; Chapman, Reference Chapman1958). At a more fundamental level, even the muscle can be dispensed with since the flow and containment of seawater within the system is based on embedded ciliary pumps, typically expressed in the form of channelized siphonoglyphs (Fig. 3c, d). This self-supporting bag-like construction offers an exceptionally parsimonious means of assembling a macroscopic organism, not based on costly biominerals, differentiated tissue systems or coelomic fluids, but on environmental water that comes for free. The only substantial costs are a mesoglea-like internal layer that defines the overall form of the inflated chamber (cf. Batham & Pantin, Reference Batham and Pantin1951; Tucker et al. Reference Tucker, Shibata and Blankenship2011) and an enveloping epithelial layer to ensure its integrity (Fig. 4a) (cf. Tyler, Reference Tyler2003; Jonusaite et al. Reference Jonusaite, Donini and Kelly2016). With a charging mechanism based on the plesiomorphic capacity of eukaryotes to pump water (Butterfield, Reference Butterfield2018), such an apparatus provides access to most of the fluid dynamic advantages of large size without the metabolic trade-offs accompanying more complex, carbon-rich body plans (Thingstad et al. Reference Thingstad, Øvreås, Egge, Løvdal and Heldal2005; Acuña et al. Reference Acuña, López-Urrutia and Colin2011; Pitt et al. Reference Pitt, Duarte, Lucas, Sutherland, Condon, Mianzan, Purcell, Robinson and Uye2013).

Most significantly, the middle Ediacaran invention of this bag-like habit solved the problem of conducting extracellular digestion at macroscopic length scales. By containing the process within an essentially impermeable integument, hydrolytic exo-enzymes could now be freely released without advective loss to the environment or competing organisms, even under the turbulent conditions associated with centimetre- to metre-length scales (cf. Sher et al. Reference Sher, Fishman, Melamed-Book, Zhang and Zlotkin2008; Agostini et al. Reference Agostini, Suzuki, Higuchi, Casareto, Yoshinaga, Nakano and Fujimura2012; Raz-Bahat et al. Reference Raz-Bahat, Douek, Moiseeva, Peters and Rinkevich2017; Goldberg, Reference Goldberg, Kloc and Kubiak2018; Steinmetz, Reference Steinmetz2019). Combined with organismal control over the cycling of seawater, the presence of a large-scale holding and mixing vessel provided both the time and hydrodynamic conditions necessary for optimal uptake and digestion, particularly in the presence of substantially expanded mesentery-like surface area (Fig. 4a, b). In modern industrial applications such structures are known as chemical reactors; in biology, they are regularly employed as guts (Penry & Jumars, Reference Penry and Jumars1987).

The most basic type of gut among living animals is the single-opening ‘batch reactor’ of predatory cnidarians, where individual prey items are processed within a (transiently closed) gastrovascular cavity, followed by the regurgitation of undigested remains (Schick, Reference Schick1991; Sher et al. Reference Sher, Fishman, Melamed-Book, Zhang and Zlotkin2008; Schlesinger et al. Reference Schlesinger, Zlotkin, Kramarsky-Winter and Loya2009; Raz-Bahat et al. Reference Raz-Bahat, Douek, Moiseeva, Peters and Rinkevich2017; Steinmetz, Reference Steinmetz2019). Such behaviour, however, is predicated on the availability of suitable prey and a muscle-based means of capturing and manipulating it, for which there is no direct evidence in middle Ediacaran deposits. In this context, the more appropriate model for extracellular digestion is a continuous-flow stirred-tank reactor (CSTR), involving the continuous processing of dissolved or suspended substrate as it passes through a reaction chamber (Penry & Jumars, Reference Penry and Jumars1986). This type of unidirectional water cycling is widely employed by extant cnidarians, where cilia- and siphonoglyph-based pumping is capable of marshalling complex flow paths, even within blind-ended chambers and canals (Southward, Reference Southward1955; Holley & Shelton, Reference Holley and Shelton1984; Schick, Reference Schick1991; Parrin et al. Reference Parrin, Netherton, Bross, McFadden and Blackstone2010; Harmata et al. Reference Harmata, Parrin, Morrison, McConnell, Bross and Blackstone2013; Goldberg, Reference Goldberg, Kloc and Kubiak2018). Fully open-ended unidirectional processing has also been achieved secondarily in colonial pennatulacean and alcyonacean octocorals, through the differentiation and interconnection of water-pumping siphonozooids and stolon systems (Fig. 3c, d) (Hickson, Reference Hickson1883; Brafield, Reference Brafield1969; Williams et al. Reference Williams, Hoeksema and Van Ofwegen2012; Nonaka et al. Reference Nonaka, Nakamura, Tsukahara and Reimer2012), as well as in the atentaculate solitary coral Leptoseris fragilis via the formation of micrometre-scale gastrovascular pores (Schlicter, Reference Schlicter1991). Significantly, active gastrovascular cycling of seawater proceeds even where its skeletal function has been largely superseded by hard skeleton, demonstrating a primary purpose in feeding and internal transport. The ‘fractally’ partitioned hydrostatic exoskeleton of rangeomorphs was similarly suited to such CSTR-like processing.

The Ediacaran introduction of large, gently stirred, semi-enclosed, reaction vessels would have been equally revolutionary from a microbial point of view. Along with the massively expanded area for surface attachment, microbial residence within the rangeomorph chamber system offered both a continuously buffered habitat and essentially unlimited levels of host-delivered resources (Fig. 4b). At the same time, localized containment allowed the direct physiological coupling of otherwise incompatible modes of life. In the bilaterian gut, for example, it is clear that the anaerobic conditions necessary for optimal digestion are maintained both by and for the resident microbiome (Plante, Reference Plante1990; Friedman et al. Reference Friedman, Bittinger, Esipova, Hou, Chau, Jiang, Mesaros, Lund, Liang, FitzGerald, Goulian, Lee, Garcia, Blair, Vinogradov and Wu2018; Litvak et al. Reference Litvak, Byndloss and Bäumler2018), even as the collective ‘holobiome’ takes advantage of a fully oxygenated existence. Comparably steep redox gradients are found in the gastrovascular cavities of extant cnidarians (Agostini et al. Reference Agostini, Suzuki, Higuchi, Casareto, Yoshinaga, Nakano and Fujimura2012), offering similar opportunities for such catabolic partnerships (Viver et al. Reference Viver, Orellana, Hatt, Urdiain, Díaz, Richter, Antón, Avian, Amann, Konstantinidis and Rosselló-Móra2017; Goldberg, Reference Goldberg, Kloc and Kubiak2018). In the case of actiniarian and pennatulacean anthozoans, rhythmic cycling between hypoxic and anoxic conditions within the gastrovascular system (Brafield & Chapman, Reference Brafield and Chapman1967; Chapman, Reference Chapman1972; Jones et al. Reference Jones, Pickthall and Nesbitt1977; Brafield, Reference Brafield1980) reflects the active suppression of oxygen levels, even in the presence of regularly transiting oxygenated seawater (Penry & Jumars, Reference Penry and Jumars1987; Smith & Waltman, Reference Smith and Waltman1995; Agostini et al. Reference Agostini, Suzuki, Higuchi, Casareto, Yoshinaga, Nakano and Fujimura2012). Given the ubiquity of metabolically diverse microbes in the marine realm, the Ediacaran appearance of bag-like rangeomorphs can be viewed as the original evolutionary experiment linking high-Re oxygen-respiring multicellular eukaryotes to a low-Re, hypoxic to anoxic, microbial digester. Such symbioses will have dramatically expanded the capacity of Ediacaran eukaryotes to feed on dilute and/or recalcitrant DOC, while also tapping into the rich physiological, immunological and developmental potential of such redox-sensitive relationships (e.g. McFall-Ngai et al. Reference McFall-Ngai, Hadfield, Bosch, Carey, Domazet-Lošo, Douglas, Dubilier, Eberl, Fukami, Gilbert, Hentschel, King, Kjelleberg, Knoll, Kremer, Mazmanian, Metcalf, Nealson, Pierce, Rawls, Reid, Ruby, Rumpho, Sanders, Tautz and Wernegreen2013; Dishaw et al. Reference Dishaw, Cannon, Litman and Parker2014; Hammarlund, Reference Hammarlund2020).

In addition to optimizing digestion, a large-scale chemical reactor requires reliable delivery of reactants. Although rangeomorphs preserve little direct evidence of their water-processing habits, simply the turbulence generated by the elevated canopy and background currents will have ensured a continuous supply of food and gas exchange (Larsen & RiisgÅrd, Reference Larsen and RiisgÅrd1997; Lassen et al. Reference Lassen, Kortegrd, RiisgÅrd, Friedrichs, Graf and Larsen2006; Singer et al. Reference Singer, Plotnik and Laflamme2012; Ghisalberti et al. Reference Ghisalberti, Gold, Laflamme, Clapham, Narbonne, Summons, Johnston and Jacobs2014). By capitalizing on both the active hydrodynamics of their exposed mostly turbulent outsides, and the unique chemical and microbial milieu of their semi-contained ‘insides’, chamber-forming rangeomorphs invented a fundamentally new way of feeding, breathing and making a living.

2.c. Rangeomorph affiliations

A cnidarian grade of construction does not mean that rangeomorphs were necessarily cnidarians, but it usefully rules out a number of the usual suspects. There is, for example, no feasible means by which the cytoplasmic contents of coenocytic or syncytial eukaryotes could be replaced with sediment on timescales compatible with the 3D preservation of these soft-bodied organisms. Moreover, the absence of any known seaweeds using this sort of chambered, taphonomically castable construction makes an algal interpretation unlikely, even in photic-zone settings. Any convincing case for metazoan affiliation, however, requires the positive identification of diagnostically metazoan features, set in a phylogenetic context. Ignoring problematic ctenophores, there are currently three principal hypotheses for where rangeomorphs might reasonably be positioned within total-group Metazoa: (1) the sister-group of all extant animals (stem-group Metazoa) (Xiao & Laflamme, Reference Xiao and Laflamme2009; Budd & Jensen, Reference Budd and Jensen2017; Dunn et al. Reference Dunn, Liu and Donoghue2017; Darroch et al. Reference Darroch, Smith, Laflamme and Erwin2018); (2) the sister-group of all extant animals minus sponges (stem-group Eumetazoa) (Buss & Seilacher, Reference Buss and Seilacher1994; Dunn et al. Reference Dunn, Liu and Donoghue2017; Hoyal Cuthill & Han, Reference Hoyal Cuthill and Han2018); or (3) the sister-group of all extant cnidarians (stem-group Cnidaria) (Dunn et al. Reference Dunn, Liu and Donoghue2017).

Despite the potential for confusing non-preservation with a true absence of derived characters (Sansom et al. Reference Sansom, Gabbott and Purnell2010), it is clear that rangeomorphs lacked a number of key crown-cnidarian attributes, not least an ability to move or respond usefully to sedimentary inundation. Under comparable levels of event-bed sedimentation, modern actiniarian and pennatulacean cnidarians engage in pronounced whole-organism or whole-colony contraction, an escape response that both fluidizes surrounding sediments and precludes any infilling of gastrovascular compartments (Batham & Pantin, Reference Batham and Pantin1950; Kastendiek, Reference Kastendiek1976; Norris, Reference Norris1989; Holst & Jarms, Reference Holst and Jarms2006; Chimienti et al. Reference Chimienti, Angeletti and Mastrototaro2018). The conspicuously unresponsive habit of rangeomorphs reliably demonstrates their lack of cnidarian-grade muscle. It is also consistent with a lack of (muscle-activated) tentacles and a localized mouth, which in turn implies absence of a cnidarian-grade nerve net, predatory cnidae or predation-based feeding.

In the absence of muscle and associated systems, there appears to be little more to rangeomorphs than perforated bags of water charged by ciliary pumps. But even this represents a fundamental departure from protistan or sponge-grade multicellularity (Arendt et al. Reference Arendt, Benito-Gutierrez, Brunet and Marlow2015). At macroscopic length scales, such a membranous structure can only be realistically achieved with the mechanical reinforcement afforded by specialized intercellular adhesion molecules and a collectivized, extracellular, basement membrane (Tyler, Reference Tyler2003; Nielsen, Reference Nielsen2008; Jonusaite et al. Reference Jonusaite, Donini and Kelly2016). This type of differentiated epithelium is a uniquely eumetazoan feature, and its (inferred) identification in thin-walled rangeomorphs convincingly places these problematic fossils within total-group Eumetazoa (Budd & Jensen, Reference Budd and Jensen2017). The degree to which they can be more precisely resolved depends on the identification of additional phylogenetically informative characters. As pre-muscular, epithelial, tank-based digesters, they offer a compelling model for stem-group eumetazoans. To the extent that macroscopically responsive striated muscle appears to have evolved independently in cnidarians and bilaterians (cf. Steinmetz et al. Reference Steinmetz, Kraus, Larroux, Hammel, Amon-Hassenzahl, Houliston, Wörheide, Nickel, Degnan and Technau2012), they might further be viewed as pre-muscular, pre-predatory, stem-group cnidarians (cf. Marcum & Campbell, Reference Marcum and Campbell1978; Dunn et al. Reference Dunn, Liu and Donoghue2017).

There is much discussion over the nature of the ancestral (eu)metazoan, but the development of a gastrula phase – where the outside surface of a spherical blastula becomes sufficiently invaginated to act as an ‘inside’ – was undoubtedly a key innovation (Nielsen, Reference Nielsen2008; Arendt et al. Reference Arendt, Benito-Gutierrez, Brunet and Marlow2015). Although topologically equivalent to a solitary bag-like cnidarian, neither the gastrula nor its hypothetical ‘gastraea’ counterpart in early metazoan evolution is obviously comparable to macroscopic rangeomorphs, presumably because a large centralized mouth has no function in the absence of muscle, tentacles or, indeed, any food particles large enough to require such an apparatus. In this context, there is a compelling argument for viewing these macroscopic fossils not as single organisms, but as integrated suspension-feeding colonies, broadly analogous to those of extant pennatulacean and alcyonacean octocorals. The serially repeated pore-like structures in three-dimensionally preserved Charnia (Fig. 2) certainly point to colony-like modularity (cf. Dewel, Reference Dewel2000; Dewel et al. Reference Dewel, Dewel and McKinney2001; Hoyal Cuthill & Conway Morris, Reference Hoyal Cuthill and Conway Morris2014; Dececchi et al. Reference Dececchi, Narbonne, Greentree and Laflamme2017; Kenchington et al. Reference Kenchington, Dunn and Wilby2018), while the quantum increase in length scales associated with coloniality would have provided fundamentally enhanced access to water-borne resources without the costs of developing a more sophisticated body plan (cf. Acuña et al. Reference Acuña, López-Urrutia and Colin2011; Pitt et al. Reference Pitt, Duarte, Lucas, Sutherland, Condon, Mianzan, Purcell, Robinson and Uye2013). Unlike predatory octocorals, however, all of the constituent individuals or modules of this hypothetical pre-muscular, colonial rangeomorph would have been deployed as cilia-powered, broadly gastraea-like ‘siphonozooids’, with a primary purpose in circulating water (Figs 3c, d, 4). This does not mean that they are homologous with the siphonozooids of crown-group cnidarians of course (cf. Landing et al. Reference Landing, Antcliffe, Geyer, Kouchinsky, Bowser and Andreas2018). A colonial or modular suspension feeding habit is likely to have evolved independently in any number of stem-group metazoan lineages, just as it has among extant groups (Ryland & Warner, Reference Ryland and Warner1986).