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Cnidarians form a disparate phylum of animals and their diploblastic body plan represents a key step in animal evolution. Cnidarians are split into two main classes; anthozoans (sea anemones, corals) are benthic polyps, while medusozoans (hydroids, jellyfishes) generally have alternating life cycle stages of polyps and medusae. A sessile polyp is present in both groups and is widely regarded as the ancestral form of their last common ancestor. However, the nature and anatomy of the ancestral polyp, particularly of medusozoans, is controversial, owing to the divergent body plans of the extant lineages and the scarcity of medusozoan soft tissues in the fossil record. Here, we redescribe Conicula striata Luo & Hu from the early Cambrian Chengjiang biota, south China, which has previously been interpreted as a polyp, lophophorate or deuterostome. Through re-examination of the holotype and 51 exceptionally preserved specimens, we show that C. striata possessed features of both anthozoans and medusozoan polyps. A conical, annulated organic skeleton (periderm) fully encasing a polyp is found in fossil and living medusozoans, while a tubular pharynx extending from the mouth into a gut partitioned by c. 28 mesenteries, resembling the actinopharynx of anthozoans. Our phylogenetic analyses recover C. striata as a stem-group medusozoan, implying that the wealth of medusozoan diversity derived, ultimately, from an anemone-like ancestor.

Pteridinium simplex is an iconic erniettomorph taxon best known from late Ediacaran successions in South Australia, Russia, and Namibia. Despite nearly 100 years of study, there remain fundamental questions surrounding the paleobiology and paleoecology of this organism, including its life position relative to the sediment–water interface, and how it fed and functioned within benthic communities. Here, we combine a redescription of specimens housed at the Senckenberg Forschungsinstitut und Naturmuseum Frankfurt with field observations of fossiliferous surfaces, to constrain the life habit of Pteridinium and gain insights into the character of benthic ecosystems shortly before the beginning of the Cambrian. We present paleontological and sedimentological evidence suggesting that Pteridinium was semi-infaunal and lived gregariously in aggregated communities, preferentially adopting an orientation with the long axis perpendicular to the prevailing current direction. Using computational fluid dynamics simulations, we demonstrate that this life habit could plausibly have led to suspended food particles settling within the organism's central cavity. This supports interpretation of Pteridinium as a macroscopic suspension feeder that functioned similarly to the coeval erniettomorph Ernietta, emblematic of a broader paleoecological shift toward benthic suspension-feeding strategies over the course of the latest Ediacaran. Finally, we discuss how this new reconstruction of Pteridinium provides information concerning its potential relationships with extant animal groups and state a case for reconstructing Pteridinium as a colonial metazoan.

Extant cnidarians are a disparate phylum of non-bilaterians and their diploblastic body plan represents a key step in animal evolution. Anthozoans (anemones, corals) are benthic polyps, while adult medusozoans (jellyfishes) are dominantly pelagic medusae. A sessile polyp is present in both groups and is widely conceived as the ancestral form of their last common ancestor. However, the nature and anatomy of this ancestral polyp, particularly of medusozoans, are controversial, owing to the divergent body plans of both groups in the extant lineages and the rarity of medusozoan soft tissues in the fossil record. Here we redescribe the enigmatic Conicula striata Luo et Hu from the early Cambrian Chengjiang biota, south China, which has previously been interpreted as a polyp, lophophorate or deuterostome. We show that C. striata possessed features of both anthozoans and medusozoans. Its stalked polyp and fully encasing conical, annulated organic skeleton (periderm) are features of medusozoans. However, the gut is partitioned by ∼28 mesenteries, and has a tubular pharynx, resembling anthozoans. Our phylogenetic analysis recovers C. striata as a stem medusozoan, indicating that the enormously diverse medusozoans were derived from an anemone-like ancestor, with the pharynx lost and number of mesenteries reduced prior to the origin of crown group Medusozoa.

Molecular timescales estimate that early animal lineages diverged tens of millions of years before their earliest unequivocal fossil evidence. The Ediacaran macrobiota (~574–538 million years ago) are largely eschewed from this debate, primarily due to their extreme phylogenetic uncertainty, but they remain germane. We characterize the development of Charnia masoni and establish the phylogenetic affinity of rangeomorphs, among the oldest and most enigmatic components of the Ediacaran macrobiota. We provide the first direct evidence for the internal interconnected nature of rangeomorphs, and show Charnia was constructed of repeated branches that derived successively from pre-existing branches. We find homology and rationalise morphogenesis between disparate rangeomorph taxa, before producing a new phylogenetic analysis, resolving Charnia as a stem-eumetazoan and expanding the anatomical disparity of that group to include a long-extinct bodyplan. These data bring competing records of early animal evolution into closer agreement, reformulating our understanding of the evolutionary emergence of animal bodyplans.

Rangeomorphs represent a long-extinct group of eumetazoans with a bodyplan unlike anything alive today., Molecular timescales estimate that early animal lineages diverged tens of millions of years before their earliest unequivocal fossil evidence. The Ediacaran macrobiota (~574 to 538 million years ago) are largely eschewed from this debate, primarily due to their extreme phylogenetic uncertainty, but remain germane. We characterize the development of Charnia masoni and establish the affinity of rangeomorphs, among the oldest and most enigmatic components of the Ediacaran macrobiota. We provide the first direct evidence for the internal interconnected nature of rangeomorphs and show that Charnia was constructed of repeated branches that derived successively from pre-existing branches. We find homology and rationalize morphogenesis between disparate rangeomorph taxa, before producing a phylogenetic analysis, resolving Charnia as a stem-eumetazoan and expanding the anatomical disparity of that group to include a long-extinct bodyplan. These data bring competing records of early animal evolution into closer agreement, reformulating our understanding of the evolutionary emergence of animal bodyplans.

Summary Fossils of the Ediacaran macrobiota (∼571–539 mya) record phylogenetically diverse marine palaeocommunities, including early animals, which pre-date the "Cambrian Explosion" [1–4]. Benthic forms with a frondose gross morphology, assigned to the morphogroups Rangeomorpha [5] and Frondomorpha (see also Arboreomorpha) [6–8], are among the most temporally wide-ranging and environmentally tolerant members of the Ediacaran macrobiota [6] and dominated deep-marine ecosystems ∼571–560 mya [9–11]. Investigations into the morphology [12–14], palaeoecology [10, 15, 16], reproductive strategies [17, 18], feeding methods [9, 19], and morphogenesis of frondose taxa together constrain their phylogenetic position to the metazoan (for Rangeomorpha) or eumetazoan (e.g., Arborea) total groups [14, 20], but tighter constraint is currently lacking. Here, we describe fossils of abundant filamentous organic structures preserved among frond-dominated fossil assemblages in Newfoundland (Canada). The filaments constitute a prominent component of the ecosystems, and exhibit clear physical associations with at least seven frondose taxa. Individual specimens of one uniterminal rangeomorph taxon appear to be directly connected by filaments across distances of centimeters to meters. Such physical linkages are interpreted to reflect evidence for stolonic connections: a conclusion with potential implications for the phylogenetic placement and palaeoecology of frondose organisms. Consideration of extant stoloniferous organisms suggests that Ediacaran frondose taxa were likely clonal and resurrects the possibility that they may have been colonial (e.g., [21, 22]). Video Abstract

Rocks of the Ediacaran System (635–541 Ma) preserve fossil evidence of some of the earliest complex macroscopic organisms, many of which have been interpreted as animals. However, the unusual morphologies of some of these organisms have made it difficult to resolve their biological relationships to modern metazoan groups. Alternative competing phylogenetic interpretations have been proposed for Ediacaran taxa, including algae, fungi, lichens, rhizoid protists, and even an extinct higher‐order group (Vendobionta). If a metazoan affinity can be demonstrated for these organisms, as advocated by many researchers, they could prove informative in debates concerning the evolution of the metazoan body axis, the making and breaking of axial symmetries, and the appearance of a metameric body plan. Attempts to decipher members of the enigmatic Ediacaran macrobiota have largely involved study of morphology: comparative analysis of their developmental phases has received little attention. Here we present what is known of ontogeny across the three iconic Ediacaran taxa Charnia masoni, Dickinsonia costata and Pteridinium simplex, together with new ontogenetic data and insights. We use these data and interpretations to re‐evaluate the phylogenetic position of the broader Ediacaran morphogroups to which these taxa are considered to belong (rangeomorphs, dickinsoniomorphs and erniettomorphs). We conclude, based on the available evidence, that the affinities of the rangeomorphs and the dickinsoniomorphs lie within Metazoa.

Macroscopic organisms from the late Ediacaran period have often been described as failed experiments in the history of life. We argue that the field of Ediacaran palaeobiology should dispense with unhelpful historical classification schemes and embrace phylogenetic systematics if we are to establish the evolutionary relevance of these fossils.\ud \ud The Ediacaran macrobiota — an assortment of macroscopic, largely soft-bodied organisms that lived during the ~30 Myr interval prior to the Cambrian period — have long been considered a palaeontological conundrum. Many fossils of these organisms exhibit unusual body plans that are unlike anything seen among living taxa (Fig. 1a–d) and it has proved difficult to resolve their relationships to extant groups. Individually and collectively, members of the Ediacaran macrobiota have been both allied with extant clades and deliberately set apart from them by suggestions that they were either ‘failed experiments’ in the history of life, or members of long-extinct higher-order clades1. Despite the role they have played in stimulating debate around these taxa, we argue that these latter viewpoints have hampered Ediacaran research. They have also created confusion within the wider community as to the placement of the Ediacaran macrobiota in the tree of life, forming a barrier to their incorporation within biological and developmental discussions. We advocate abandoning the failed experiment perspective and embracing phylogenetic thinking in order to make progress in determining the phylogenetic positions of these organisms and realizing their evolutionary significance.

The ‘Cambrian Explosion’ describes the rapid increase in animal diversity and abundance, as manifest in the fossil record, between ~ 540 and 520 million years ago (Ma). This event, however, is nested within a far more ancient record of macrofossils extending at least into the late Ediacaran, ~571 Ma. The evolutionary events documented during the Ediacaran–Cambrian interval coincide with geochemical evidence for the modernisation of Earth’s biogeochemical cycles. Holistic integration of fossil and geochemical records leads us to challenge the notion that the Ediacaran and Cambrian worlds were markedly distinct, and places biotic and environmental change within a longer-term narrative. We propose that the evolution of metazoans may have been facilitated by a series of dynamic and global changes in redox conditions and nutrient supply, which, together with potential biotic feedbacks, enabled turnover events that sustained phases of radiation. \ud In this synthesis, we argue that early metazoan diversification should be recast as a series of successive, transitional radiations that extended from the late Ediacaran and continued through the early Palaeozoic. We conclude that while the Cambrian Explosion represents a radiation of crown-group bilaterians, it was simply one phase amongst several older, and younger, metazoan radiations.

The Ediacaran macrofossil Charnia masoni Ford is perhaps the most iconic member of the Rangeomorpha: a group of seemingly sessile, frondose organisms that dominates late Ediacaran benthic, deep‐marine fossil assemblages. Despite C. masoni exhibiting broad palaeogeographical and stratigraphical ranges, there have been few morphological studies that consider the variation observed among populations of specimens derived from multiple global localities. We present an analysis of C. masoni that evaluates specimens from the UK, Canada and Russia, representing the largest morphological study of this taxon to date. We describe substantial morphological variation within C. masoni and present a new morphological model for this species that has significant implications both for interpretation of rangeomorph architecture, and potentially for existing taxonomic schemes. Previous reconstructions of Charnia include assumptions regarding the presence of structures seen in other rangeomorphs (e.g. an internal stalk) and of homogeneity in higher order branch morphology; observations that are not borne out by our investigations. We describe variation in the morphology of third and fourth order branches, as well as variation in gross structure near the base of the frond. The diagnosis of Charnia masoni is emended to take account of these new features. These findings highlight the need for large‐scale analyses of rangeomorph morphology in order to better understand the biology of this long‐enigmatic group.

The first known diverse, complex, macroscopic benthic marine ecosystems (late\ud Ediacaran, ca. 571-541 Ma) were dominated by the Rangeomorpha, an enigmatic\ud group of extinct frondose eukaryotes that are candidate early metazoans[1,2]. The\ud group is characterised by a self-similar branching architecture that was likely optimised\ud for exchange, but nearly every other aspect of their biology is contentious[2-4]. We\ud report locally-enhanced, aberrant growth ("eccentric branching") in a stalked,\ud multifoliate rangeomorph - Hylaecullulus fordi n. gen., n. sp. - from Charnwood Forest\ud (UK), confirming the presence of true biological modularity within the group. Random\ud branches achieve unusually large proportions and mimic the architecture of their\ud parent branch, rather than that of their neighbours (the norm). Their locations indicate\ud exceptional growth at existing loci, rather than insertion at new sites. Analogous over-\ud compensatory branching in extant modular organisms requires the capacity to\ud orchestrate growth at specific sites, and occurs most frequently in response to damage\ud or environmental stress, allowing regeneration towards optimum morphology[e.g. 5-7].\ud Its presence in rangeomorphs indicates a hitherto unappreciated level of control to\ud their growth plan, a previously unrecognised form of morphological plasticity within the\ud group, and an ability to actively respond to external physical stimuli. The trait would\ud have afforded rangeomorphs resilience to fouling and abrasion, partially accounting for\ud their wide environmental tolerance, and may have pre-adapted them to withstand\ud predation, weakening this argument for their extinction. Our findings highlight that\ud multiple, phylogenetically disparate, clades first achieved large size through modularity.

The late Ediacaran soft-bodied macroorganism Dickinsonia (age range approx. 560–550 Ma) has often been interpreted as an early animal, and is increasingly invoked in debate on the evolutionary assembly of eumetazoan body plans. However, conclusive positive evidence in support of such a phylogenetic affinity has not been forthcoming. Here we subject a collection of Dickinsonia specimens interpreted to represent multiple ontogenetic stages to a novel, quantitative method for studying growth and development in organisms with an iterative body plan. Our study demonstrates that Dickinsonia grew via pre-terminal ‘deltoidal’ insertion and inflation of constructional units, followed by a later inflation-dominated phase of growth. This growth model is contrary to the widely held assumption that Dickinsonia grew via terminal addition of units at the end of the organism bearing the smallest units. When considered alongside morphological and behavioural attributes, our developmental data phylogenetically constrain Dickinsonia to the Metazoa, specifically the Eumetazoa plus Placozoa total group. Our findings have implications for the use of Dickinsonia in developmental debates surrounding the metazoan acquisition of axis specification and metamerism.

The late Ediacaran soft-bodied macroorganism Dickinsonia (age range approx. 560–550 Ma) has often been interpreted as an early animal, and is increasingly invoked in debate on the evolutionary assembly of eumetazoan body plans. However, conclusive positive evidence in support of such a phylogenetic affinity has not been forthcoming. Here we subject a collection of Dickinsonia specimens interpreted to represent multiple ontogenetic stages to a novel, quantitative method for studying growth and development in organisms with an iterative body plan. Our study demonstrates that Dickinsonia grew via pre-terminal ‘deltoidal’ insertion and inflation of constructional units, followed by a later inflation-dominated phase of growth. This growth model is contrary to the widely held assumption that Dickinsonia grew via terminal addition of units at the end of the organism bearing the smallest units. When considered alongside morphological and behavioural attributes, our developmental data phylogenetically constrain Dickinsonia to the Metazoa, specifically the Eumetazoa plus Placozoa total group. Our findings have implications for the use of Dickinsonia in developmental debates surrounding the metazoan acquisition of axis specification and metamerism.

Rocks of the Ediacaran System (635–541 Ma) preserve fossil evidence of some of the earliest complex macroscopic organisms, many of which have been interpreted as animals. However, the unusual morphologies of some of these organisms have made it difficult to resolve their biological relationships to modern metazoan groups. Alternative competing phylogenetic interpretations have been proposed for Ediacaran taxa, including algae, fungi, lichens, rhizoid protists, and even an extinct higher‐order group (Vendobionta). If a metazoan affinity can be demonstrated for these organisms, as advocated by many researchers, they could prove informative in debates concerning the evolution of the metazoan body axis, the making and breaking of axial symmetries, and the appearance of a metameric body plan. Attempts to decipher members of the enigmatic Ediacaran macrobiota have largely involved study of morphology: comparative analysis of their developmental phases has received little attention. Here we present what is known of ontogeny across the three iconic Ediacaran taxa Charnia masoni, Dickinsonia costata and Pteridinium simplex, together with new ontogenetic data and insights. We use these data and interpretations to re‐evaluate the phylogenetic position of the broader Ediacaran morphogroups to which these taxa are considered to belong (rangeomorphs, dickinsoniomorphs and erniettomorphs). We conclude, based on the available evidence, that the affinities of the rangeomorphs and the dickinsoniomorphs lie within Metazoa.

In the version of this article initially published, the reference “Mitchell, E. G., & Kenchington, C. G. The utility of height for the Ediacaran organisms of Mistaken Point. Nat. Ecol. Evol. 2, 1218–1222 (2018).” was missing. A callout to the reference should have been placed at the end of this sentence: “For biotic replacement to occur, taxa must be both spatially collocated and have similar resource requirements, yet spatial analyses of contemporary communities find only very limited instances of resource competition.” The reference has been added to the list, and the error has been corrected in the PDF and HTML versions of the article.