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The Ediacara Biota—the oldest communities of complex, macroscopic fossils—consists of three temporally distinct assemblages: the Avalon (ca. 575–560 Ma), White Sea (ca. 560–550 Ma), and Nama (ca. 550–539 Ma). Generic diversity varies among assemblages, with a notable decline at the transition from White Sea to Nama. Preservation and sampling biases, biotic replacement, and environmental perturbation have been proposed as potential mechanisms for this drop in diversity. Here, we compile a global database of the Ediacara Biota, specifically targeting taphonomic and paleoecological characters, to test these hypotheses. Major ecological shifts in feeding mode, life habit, and tiering level accompany an increase in generic richness between the Avalon and White Sea assemblages. We find that ∼80% of White Sea taxa are absent from the Nama interval, comparable to loss during Phanerozoic mass extinctions. The paleolatitudes, depositional environments, and preservational modes that characterize the White Sea assemblage are well represented in the Nama, indicating that this decline is not the result of sampling bias. Counter to expectations of the biotic replacement model, there are minimal ecological differences between these two assemblages. However, taxa that disappear exhibit a variety of morphological and behavioral characters consistent with an environmentally driven extinction event. The preferential survival of taxa with high surface area relative to volume may suggest that this was related to reduced global oceanic oxygen availability. Thus, our data support a link between Ediacaran biotic turnover and environmental change, similar to other major mass extinctions in the geologic record.

Analysis of modern animals and Ediacaran trace fossils predicts that the oldest bilaterians were simple and small. Such organisms would be difficult to recognize in the fossil record, but should have been part of the Ediacara Biota, the earliest preserved macroscopic, complex animal communities. Here, we describe Ikaria wariootia gen. et sp. nov. from the Ediacara Member, South Australia, a small, simple organism with anterior/posterior differentiation. We find that the size and morphology of Ikaria match predictions for the progenitor of the trace fossil Helminthoidichnites—indicative of mobility and sediment displacement. In the Ediacara Member, Helminthoidichnites occurs stratigraphically below classic Ediacara body fossils. Together, these suggest that Ikaria represents one of the oldest total group bilaterians identified from South Australia, with little deviation from the characters predicted for their last common ancestor. Further, these trace fossils persist into the Phanerozoic, providing a critical link between Ediacaran and Cambrian animals.

The latest Neoproterozoic extinction of the Ediacara biota has been variously attributed to catastrophic removal by perturbations to global geochemical cycles, ‘biotic replacement’ by Cambrian-type ecosystem engineers, and a taphonomic artefact. We perform the first critical test of the ‘biotic replacement’ hypothesis using combined palaeoecological and geochemical data collected from the youngest Ediacaran strata in southern Namibia. We find that, even after accounting for a variety of potential sampling and taphonomic biases, the Ediacaran assemblage preserved at Farm Swartpunt has significantly lower genus richness than older assemblages. Geochemical and sedimentological analyses confirm an oxygenated and non-restricted palaeoenvironment for fossil-bearing sediments, thus suggesting that oxygen stress and/or hypersalinity are unlikely to be responsible for the low diversity of communities preserved at Swartpunt. These combined analyses suggest depauperate communities characterized the latest Ediacaran and provide the first quantitative support for the biotic replacement model for the end of the Ediacara biota. Although more sites (especially those recording different palaeoenvironments) are undoubtedly needed, this study provides the first quantitative palaeoecological evidence to suggest that evolutionary innovation, ecosystem engineering and biological interactions may have ultimately caused the first mass extinction of complex life.

Significance Patterns of evolution, origination, and extinction of early animal life on this planet are largely interpreted from fossils of the soft-bodied Ediacara Biota, Earth’s earliest multicellular communities preserved globally. The record of these organisms predates the well-known Cambrian Explosion by nearly 40 million years and provides critical information concerning early experimentation with complex life-forms on Earth. Here we show that, although in appearance, these organisms look very strange and unfamiliar, many of them may have had a biology and/or ecology similar to animals today, and some were most certainly bilaterians, cnidarians, and poriferans. Patterns of origination and evolution of early complex life on this planet are largely interpreted from the fossils of the Precambrian soft-bodied Ediacara Biota. These fossils occur globally and represent a diverse suite of organisms living in marine environments. Although these exceptionally preserved fossil assemblages are typically difficult to reconcile with modern phyla, examination of the morphology, ecology, and taphonomy of these taxa provides keys to their relationships with modern taxa. Within the more than 30 million y range of the Ediacara Biota, fossils of these multicellular organisms demonstrate the advent of mobility, heterotrophy by multicellular animals, skeletonization, sexual reproduction, and the assembly of complex ecosystems, all of which are attributes of modern animals. This approach to these fossils, without the constraint of attempting phylogenetic reconstructions, provides a mechanism for comparing these taxa with both living and extinct animals.

Marine dissolved organic carbon (DOC), the largest pool of reduced carbon in the oceans, plays an important role in the global carbon cycle and contributes to the regulation of atmospheric oxygen and carbon dioxide abundances. Despite its importance in global biogeochemical cycles, the long-term history of the marine DOC reservoir is poorly constrained. Nonetheless, significant changes to the size of the oceanic DOC reservoir through Earth’s history have been commonly invoked to explain changes to ocean chemistry, carbon cycling, and marine ecology. Here, we present a revised view of the evolution of marine DOC concentrations using a mechanistic carbon cycle model that can reproduce DOC concentrations in both oxic and anoxic modern environments. We use this model to demonstrate that the overall size of the marine DOC reservoir has likely undergone very little variation through Earth’s history, despite major changes in the redox state of the ocean–atmosphere system and the nature and efficiency of the biological carbon pump. A relatively static marine DOC reservoir across Earth’s history renders it unlikely that major changes in marine DOC concentrations have been responsible for driving massive repartitioning of surface carbon or the large carbon isotope excursions observed in Earth’s stratigraphic record and casts doubt on previously hypothesized links between marine DOC levels and the emergence and radiation of early animals.

The Ediacara Biota preserves the oldest fossil evidence of abundant, complex metazoans. Despite their significance, assigning individual taxa to specific phylogenetic groups has proved problematic. To better understand these forms, we identify developmentally controlled characters in representative taxa from the Ediacaran White Sea assemblage and compare them with the regulatory tools underlying similar traits in modern organisms. This analysis demonstrates that the genetic pathways for multicellularity, axial polarity, musculature, and a nervous system were likely present in some of these early animals. Equally meaningful is the absence of evidence for major differentiation of macroscopic body units, including distinct organs, localized sensory machinery or appendages. Together these traits help to better constrain the phylogenetic position of several key Ediacara taxa and inform our views of early metazoan evolution. An apparent lack of heads with concentrated sensory machinery or ventral nerve cords in such taxa supports the hypothesis that these evolved independently in disparate bilaterian clades.

Owing to the lack of temporally well-constrained Ediacaran fossil localities containing overlapping biotic assemblages, it has remained uncertain if the latest Ediacaran (ca 550–541 Ma) assemblages reflect systematic biological turnover or environmental, taphonomic or biogeographic biases. Here, we report new latest Ediacaran fossil discoveries from the lower member of the Wood Canyon Formation in Nye County, Nevada, including the first figured reports of erniettomorphs, Gaojiashania, Conotubus and other problematic fossils. The fossils are spectacularly preserved in three taphonomic windows and occur in greater than 11 stratigraphic horizons, all of which are below the first appearance of Treptichnus pedum and the nadir of a large negative δ13C excursion that is a chemostratigraphic marker of the Ediacaran–Cambrian boundary. The co-occurrence of morphologically diverse tubular fossils and erniettomorphs in Nevada provides a biostratigraphic link among latest Ediacaran fossil localities globally. Integrated with a new report of Gaojiashania from Namibia, previous fossil reports and existing age constraints, these finds demonstrate a distinctive late Ediacaran fossil assemblage comprising at least two groups of macroscopic organisms with dissimilar body plans that ecologically and temporally overlapped for at least 6 Myr at the close of the Ediacaran Period. This cosmopolitan biotic assemblage disappeared from the fossil record at the end of the Ediacaran Period, prior to the Cambrian radiation.

Recent geochemical data from Oman, Newfoundland, and the western United States suggest that long-term oxidation of Ediacaran oceans resulted in progressive depletion of a large dissolved organic carbon (DOC) reservoir and potentially triggered the radiation of acanthomorphic acritarchs, algae, macroscopic Ediacara organisms, and, subsequently, motile bilaterian animals. However, the hypothesized coupling between ocean oxidation and evolution is contingent on the reliability of continuous geochemical and paleontological data in individual sections and of intercontinental correlations. Here we report high-resolution geochemical data from the fossil-rich Doushantuo Formation (635-551 Ma) in South China that confirm trends from other broadly equivalent sections and highlight key features that have not been observed in most sections or have received little attention. First, samples from the lower Doushantuo Formation are characterized by remarkably stable $\\delta {}^{13}{\\rm C}{}_{\\text{org}}$ (carbon isotope composition of organic carbon) values but variable $\\delta {}^{34}{\\rm S}{}_{{\\rm CAS}}$ (sulfur isotope composition of carbonate-associated sulfate) values, which are consistent with a large isotopically buffered DOC reservoir and relatively low sulfate concentrations. Second, there are three profound negative $\\delta {}^{13}{\\rm C}{}_{\\text{carb}}$ (carbon isotope composition of carbonate) excursions in the Ediacaran Period. The negative $\\delta {}^{13}{\\rm C}{}_{\\text{carb}}$ excursions in the middle and upper Doushantuo Formation record pulsed oxidation of the deep oceanic DOC reservoir. The oxidation events appear to be coupled with eukaryote diversity in the Doushantuo basin. Comparison with other early Ediacaran basins suggests spatial heterogeneity of eukaryote distribution and redox conditions. We hypothesize that the distribution of early Ediacaran eukaryotes likely tracked redox conditions and that only after ≈551 Ma (when Ediacaran oceans were pervasively oxidized) did evolution of oxygen-requiring taxa reach global distribution.

The mid-late Ediacaran Period (~579–541 Ma) is characterized by globally distributed marine soft-bodied organisms of unclear phylogenetic affinities colloquially called the “Ediacara biota.” Despite an absence of systematic agreement, previous workers have tested for underlying factors that may control the occurrence of Ediacaran macrofossils in space and time. Three taxonomically distinct “assemblages,” termed the Avalon, White Sea, and Nama, were identified and informally incorporated into Ediacaran biostratigraphy. After ~15 years of new fossil discoveries and taxonomic revision, we retest the validity of these assemblages using a comprehensive database of Ediacaran macrofossil occurrences. Using multivariate analysis, we also test the degree to which taphonomy, time, and paleoenvironment explain the taxonomic composition of these assemblages. We find that: (1) the three assemblages remain distinct taxonomic groupings; (2) there is little support for a large-scale litho-taphonomic bias present in the Ediacaran; and (3) there is significant chronostratigraphic overlap between the taxonomically and geographically distinct Avalonian and White Sea assemblages ca. 560–557 Ma. Furthermore, both assemblages show narrow bathymetric ranges, reinforcing that they were paleoenvironmental–ecological biotopes and spatially restricted in marine settings. Meanwhile, the Nama assemblage appears to be a unique faunal stage, defined by a global loss of diversity, coincident with a noted expansion of bathymetrically unrestricted, long-ranging Ediacara taxa. These data reinforce that Ediacaran biodiversity and stratigraphic ranges of its representative taxa must first statistically account for varying likelihood of preservation at a local scale to ultimately aggregate the Ediacaran macrofossil record into a global biostratigraphic context.

For almost 150 years, megascopic structures in siliciclastic sequences of terminal Precambrian age have been frustratingly difficult to characterize and classify. As with all other areas of human knowledge, progress with exploration, documentation and understanding is growing at an exponential rate. Nevertheless, there is much to be learned from following the evolution of the logic behind the biological interpretations of these enigmatic fossils. Here, I review the history of discovery as well as some long-established core members of widely recognized clades that are still difficult to graft on to the tree of life. These ‘orphan plesions’ occupy roles that were once held by famous former Problematica, such as archaeocyaths, graptolites and rudist bivalves. In some of those cases, taxonomic enlightenment was brought about by the discovery of new characters; in others it required a better knowledge of their living counterparts. Can we use these approaches to rescue the Ediacaran orphans? Five taxa that are examined in this context are Arborea (Arboreomorpha), Dickinsonia (Dickinsoniomorpha), Pteridinium plus Ernietta (Erniettomorpha) and Kimberella (Bilateria?). With the possible exception of Dickinsonia, all of these organisms may be coelenterate grade eumetazoans.