New insight into the global record of the Ediacaran tubular morphotype: a common solution to early multicellularity.

The tubular morphogroup is a common component of Earth's first complex, multicellular communities-the Ediacaran biota-and offers valuable insight into biological traits that are fundamental to animal life because they have intriguing links to metazoan phyla and are highly abundant in Ediacaran ecosystems. Biomineral tubes (e.g. Cloudina) are well described from the Nama assemblage (~550-538 Myr), yielding a relatively detailed understanding of this subset of the morphogroup. Conversely, the non-biomineral tubular taxa of the Nama assemblage, as well as of the older White Sea assemblage (~560-550 Myr), are poorly understood. As a result, the variability of characters that define non-biomineral tubular organisms is unknown and their diversity dynamics throughout the terminal Ediacaran are unconstrained. To test hypotheses related to the diversity, morphological variability and temporal distribution of non-biomineral tubes, a comprehensive database of non-biomineral Ediacaran tubular taxa was compiled. Results demonstrate previously unrecognized morphological disparity in the non-biomineral tubular morphogroup and reveal that it comprises a higher number of genera than all other non-tubular morphogroups in the White Sea and the Nama. Thus, it illustrates that a tubular form dominated Ediacaran ecosystems for considerably longer than previously appreciated and, importantly, was the most common solution to early multicellularity.

Environmental drivers of the first major animal extinction across the Ediacaran White Sea-Nama transition.

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.

Ediacara growing pains: Modular addition and development in Dickinsonia costata.

Constraining patterns of growth using directly observable and quantifiable characteristics can reveal a wealth of information regarding the biology of the Ediacara Biota - the oldest macroscopic, complex community forming organisms in the fossil record. However, these rely on individuals captured at an instant in time at various growth stages, and so different interpretations can be derived from the same material. Here we leverage newly discovered and well-preserved Dickinsonia costata Sprigg 1947 from South Australia, combined with hundreds of previously described specimens, to test competing hypotheses for the location of module addition. We find considerable variation in the relationship between the total number of modules and body size that cannot be explained solely by expansion and contraction of individuals. Patterns derived assuming new modules differentiated at the anterior result in numerous examples where the oldest module(s) must decrease in size with overall growth, potentially falsifying this hypothesis. Observed polarity as well as the consistent posterior location of defects and indentations support module formation at this end in D. costata. Regardless, changes in repeated units with growth share similarities with those regulated by morphogen gradients in metazoans today, suggesting that these genetic pathways were operating in Ediacaran animals.

Developmental processes in Ediacara macrofossils.

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.

Biostratinomy of the Ediacara Member (Rawnsley Quartzite, South Australia): implications for depositional environments, ecology and biology of Ediacara organisms.

The Precambrian Ediacara Biota-Earth's earliest fossil record of communities of macroscopic, multicellular organisms-provides critical insights into the emergence of complex life on our planet. Excavation and reconstruction of nearly 300 m2 of fossiliferous bedding planes in the Ediacara Member of the Rawnsley Quartzite, at the National Heritage Ediacara fossil site Nilpena in South Australia, have permitted detailed study of the sedimentology, taphonomy and palaeoecology of Ediacara fossil assemblages. Characterization of Ediacara macrofossils and textured organic surfaces at the scale of facies, bedding planes and individual specimens has yielded unprecedented insight into the manner in which the palaeoenvironmental settings inhabited by Ediacara communities-particularly hydrodynamic conditions-influenced the aut- and synecology of Ediacara organisms, as well as the morphology and assemblage composition of Ediacara fossils. Here, we describe the manner in which environmental processes mediated the development of taphofacies hosting Ediacara fossil assemblages. Using two of the most common Ediacara Member fossils, Arborea and Dickinsonia, as examples, we delineate criteria that can be used to distinguish between ecological, environmental and biostratinomic signals and reconstruct how interactions between these processes have distinctively shaped the Ediacara fossil record.

Discovery of the oldest bilaterian from the Ediacaran of South Australia.

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.

Slime travelers: Early evidence of animal mobility and feeding in an organic mat world.

Mobility represents a key innovation in the evolution of complex animal life. The ability to move allows for the exploration of new food sources, escapes from unfavorable environmental conditions, enhanced ability to exchange genetic material, and is one of the major reasons for the diversity and success of animal life today. The oldest widely accepted trace fossils of animal mobility are found in Ediacaran-aged rocks (635-539 Ma). The earliest definitive evidence for movement associated with exploitation of resources for feeding occurs in the White Sea assemblage of the Ediacara Biota-macroscopic, soft-bodied fossils of Ediacaran age. Here, we evaluate potential support for mobility in dickinsoniomorphs, presenting new data regarding abundant Dickinsonia and associated trace fossils from the Ediacara Member, South Australia. Results quantitatively demonstrate that Dickinsonia was capable of mobility on relatively short, ecological timescales. This organism was bilaterally symmetrical, likely moved via muscular peristalsis, and left trace fossils due to active removal of the organic mat related to feeding. Analogous structures associated with Yorgia indicate that it was also mobile and fed in a similar manner. Morphological evidence suggests that two other modular taxa, Andiva and Spriggina, were able to move but did not feed in a manner that impacted the organic mat. Together, these data suggest that mobility was present in multiple disparate bilaterally symmetrical Ediacaran taxa.

A stable and productive marine microbial community was sustained through the end-Devonian Hangenberg Crisis within the Cleveland Shale of the Appalachian Basin, United States.

The end-Devonian Hangenberg Crisis constituted one of the greatest ecological and environmental perturbations of the Paleozoic Era. To date, however, it has been difficult to precisely constrain the occurrence of the Hangenberg Crisis in the Appalachian Basin of the United States and thus to directly assess the effects of this crisis on marine microbial communities and paleoenvironmental conditions. Here, we integrate organic and inorganic chemostratigraphic records compiled from two discrete outcrop locations to characterize the onset and paleoenvironmental transitions associated with the Hangenberg Crisis within the Cleveland Shale member of the Ohio Shale. The upper Cleveland Shale records both positive carbon (δ13 Corg ) and nitrogen (δ15 Ntotal ) isotopic excursions, and replenished trace metal inventories with links to eustatic rise. These dual but apparently temporally offset isotope excursions may be useful for stratigraphic correlation with other productive end-Devonian epeiric marine locations. Deposition of the black shale succession occurred locally beneath a redox-stratified water column with euxinic zones, with signs of strengthening denitrification during the Hangenberg Crisis interval, but with an otherwise stable and algal-rich marine microbial community structure sustained in the surface mixed layer as ascertained by lipid biomarker assemblages. Discernible trace fossil signals in some horizons suggest, however, that bioturbation and seafloor oxygenation occurred episodically throughout this succession and highlight that geochemical proxies often fail to capture these rapid and sporadic redox fluctuations in ancient black shales. The paleoenvironmental conditions, source biota, and accumulations of black shale are consistent with expressions of the Hangenberg Crisis globally, suggesting this event is likely captured within the uppermost strata of the Cleveland Shale in North America.

Ecological Expansion and Extinction in the Late Ediacaran: Weighing the Evidence for Environmental and Biotic Drivers.

The Ediacara Biota, Earth's earliest communities of complex, macroscopic, multicellular organisms, appeared during the late Ediacaran Period, just prior to the Cambrian Explosion. Ediacara fossil assemblages consist of exceptionally preserved soft-bodied forms of enigmatic morphology and affinity which nonetheless represent a critical stepping-stone in the evolution of complex animal ecosystems. The Ediacara Biota has historically been divided into three successive Assemblages-the Avalon, the White Sea, and the Nama. Although the oldest (Avalon) Assemblage documents the initial appearance of several groups of Ediacara taxa, the two younger (White Sea and Nama) Assemblages record a particularly striking suite of ecological innovations, including the appearance of diverse Ediacara body plans-in tandem with the rise of bilaterian animals-as well as the emergence of novel ecological strategies such as movement, sexual reproduction, biomineralization, and the development of dense, heterogeneous benthic communities. Many of these ecological innovations appear to be linked to adaptations to heterogeneous substrates and shallow and energetic marine settings. In spite of these innovations, the majority of Ediacara taxa disappear by the end of the Ediacaran, with interpretations for this disappearance historically ranging from the closing of preservational windows to environmentally or biotically mediated extinction. However, in spite of the unresolved affinity and eventual extinction of individual Ediacara taxa, these distinctive ecological strategies persist across the Ediacaran-Cambrian boundary and are characteristic of younger animal-dominated communities of the Phanerozoic. The late Ediacaran emergence of these strategies may, therefore, have facilitated subsequent radiations of the Cambrian. In this light, the Ediacaran and Cambrian Periods, although traditionally envisioned as separate worlds, are likely to have been part of an ecological and evolutionary continuum.

Early Earth and the rise of complex life.

The history of life on Earth progressed in parallel with the evolving oxygen state of the atmosphere and oceans, but the details of that relationship remain poorly known and debated. There is, however, general agreement that the first appreciable and persistent accumulation of oxygen in the oceans and atmosphere occurred around 2.3 to 2.4 billion years ago. Following this Great Oxidation Event, biospheric oxygen remained at relatively stable intermediate levels for more than a billion years. Much current research focuses on the transition from the intermediate conditions of this middle chapter in Earth history to the more oxygenated periods that followed - often emphasizing whether increasing and perhaps episodic oxygenation drove fundamental steps in the evolution of complex life and, if so, when. These relationships among early organisms and their environments are the thematic threads that stitch together the papers in this collection. Expert authors bring a mix of methods and opinions to their leading-edge reviews of the earliest proliferation and ecological impacts of eukaryotic life, the subsequent emergence and ecological divergence of animals, and the corresponding causes and consequences of environmental change.

Dynamic oxygen and coupled biological and ecological innovation during the second wave of the Ediacara Biota.

Animal life on Earth is generally accepted to have risen during a period of increasingly well-oxygenated conditions, but direct evidence for that relationship has previously eluded scientists. This gap reflects both the enigmatic nature of the early animal fossil record and the coarse temporal resolution of Precambrian environmental change. Here, we combine paleontological data from the Ediacara Biota, the earliest fossil animals, with geochemical evidence for fluctuating redox conditions. Using morphological and ecological novelties that broadly reflect oxygen demand, we show that the appearance of abundant oxygen-demanding organisms within the Ediacara Biota corresponds with a period of elevated global oxygen concentrations. This correlation suggests that a putative rise in oxygen levels may have provided the necessary environments for the diversification of complex body plans and energetically demanding ecologies. The potential loss of organisms with relatively high oxygen requirements in the latest Ediacaran coupled with an apparent return to low oxygen concentrations further supports the availability of oxygen as a control on early animal evolution. While the advent of animal life was probably the product of a variety of factors, the recognition of a possible connection between changing environmental conditions and the diversification of animal morphologies suggests that the availability of oxygen played a significant role in the evolution of animals on Earth.

Ediacaran scavenging as a prelude to predation.

Predation is one of the most fundamental ecological and evolutionary drivers in modern and ancient ecosystems. Here, we report the discovery of evidence of the oldest scavenging of shallowly buried bodies of iconic soft-bodied members of the Ediacara Biota by cryptic seafloor mat-burrowing animals that produced the furrow and levee trace fossil, Helminthoidichnites isp. These mat-burrowers were probably omnivorous, stem-group bilaterians that largely grazed on microbial mats but when following mats under thin sands, they actively scavenged buried Dickinsonia, Aspidella, Funisia and other elements of the Ediacara Biota. These traces of opportunistic scavengers of dead animals from the Ediacaran of South Australia represent a fundamental ecological innovation and a possible pathway to the evolution of macrophagous predation in the Cambrian. While the Ediacaran oceans may have had oxygen levels too low to support typical large predators, the Helminthoidichnites maker lived in and grazed on microbial mats, which may have provided a localized source of oxygen.

Highly regulated growth and development of the Ediacara macrofossil Dickinsonia costata.

The Ediacara Biota represents the oldest fossil evidence for the appearance of animals but linking these taxa to specific clades has proved challenging. Dickinsonia is an abundant, apparently bilaterally symmetrical Ediacara fossil with uncertain affinities. We identified and measured key morphological features of over 900 specimens of Dickinsonia costata from the Ediacara Member, South Australia to characterize patterns in growth and morphology. Here we show that development in Dickinsonia costata was surprisingly highly regulated to maintain an ovoid shape via terminal addition and the predictable expansion of modules. This result, along with other characters found in Dickinsonia suggests that it does not belong within known animal groups, but that it utilized some of the developmental gene networks of bilaterians, a result predicted by gene sequencing of basal metazoans but previously unidentified in the fossil record. Dickinsonia thus represents an extinct clade located between sponges and the last common ancestor of Protostomes and Deuterostomes, and likely belongs within the Eumetazoa.

Rheotaxis in the Ediacaran epibenthic organism Parvancorina from South Australia.

Diverse interpretations of Ediacaran organisms arise not only from their enigmatic body plans, but also from confusion surrounding the sedimentary environments they inhabited and the processes responsible for their preservation. Excavation of Ediacaran bedding surfaces of the Rawnsley Quartzite in South Australia has provided the opportunity to study the community structure of the Ediacara biota, as well as the autecology of individual organisms. Analysis of two bedding surfaces preserving large numbers of Parvancorina illustrates that individuals display a preferred, unidirectional orientation aligned with current, as indicated by the identified current proxies: tool marks, overfolded edges of Dickinsonia, felled fronds and drag structures generated by uprooted frond holdfasts. Taphonomic and morphological evidence suggests that the preferred orientations of Parvancorina individuals are not the result of passive current alignment, but represent a rheotactic response at some stage during their life cycle. These results illustrate a previously unrecognized life mode for an Ediacaran organism and arguably the oldest known example of rheotaxis in the fossil record. The morphology and previously suggested phylogenetic affinities of Parvancorina are also re-evaluated. Apart from possessing a bilaterally symmetrical body, there are no unequivocal morphological characters to support placement of Parvancorina within the Euarthropoda or even the Bilateria.

The advent of animals: The view from the Ediacaran.

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.

Mineralogical constraints on the paleoenvironments of the Ediacaran Doushantuo Formation.

Assemblages of clay minerals are routinely used as proxies for paleoclimatic change and paleoenvironmental conditions in Phanerozoic rocks. However, this tool is rarely applied in older sedimentary units. In this paper, the clay mineralogy of the Doushantuo Formation in South China is documented, providing constraints on depositional conditions of the Ediacaran Yangtze platform that host the earliest animal fossils in the geological record. In multiple sections from the Yangtze Gorges area, trioctahedral smectite (saponite) and its diagenetic products (mixed-layer chlorite/smectite, corrensite, and chlorite) are the dominant clays through the lower 80 m of the formation and constitute up to 30 wt% of the bulk rock. Saponite is interpreted as an in situ early diagenetic phase that formed in alkaline conditions (pH > or = 9). The absence of saponite in stratigraphically equivalent basin sections, 200-400 km to the south, indicates that alkaline conditions were localized in a nonmarine basin near the Yangtze Gorges region. This interpretation is consistent with crustal abundances of redox-sensitive trace elements in saponitic mudstones deposited under anoxic conditions, as well as a 10 per thousand difference in the carbon isotope record between Yangtze Gorges and basin sections. Our findings suggest that nonmarine environments may have been hospitable for the fauna preserved in the Yangtze Gorges, which includes the oldest examples of animal embryo fossils and acanthomorphic acritarchs.

Synchronous aggregate growth in an abundant new Ediacaran tubular organism.

The most abundant taxon of the Neoproterozoic soft-bodied biota near Ediacara, South Australia, occurs as clusters of similarly sized individuals, which suggests synchronous aggregate growth by spatfall. Tubes of Funisia dorothea gen. et sp. nov. were anchored within the shallow, sandy sea bed and lived in dense, typically monospecific concentrations. Tubes were composed of modular, serially repeating elements. Individuals grew by adding serial elements to the tubular body and by branching of tubes. Their construction and close-packed association imply likely affinity within the Porifera or Cnidaria. These data suggest that several of the most successful marine invertebrate ecological strategies known today were in place in Earth's oldest known metazoan ecosystems before the advent of skeletonization and widespread predation.

The Ordovician Radiation: A Follow-up to the Cambrian Explosion?

There was a major diversification known as the Ordovician Radiation, in the period immediately following the Cambrian. This event is unique in taxonomic, ecologic and biogeographic aspects.While all of the phyla but one were established during the Cambrian explosion, taxonomic increases during the Ordovician were manifest at lower taxonomic levels although ordinal level diversity doubled. Marine family diversity tripled and within clade diversity increases occurred at the genus and species levels. The Ordovician radiation established the Paleozoic Evolutionary Fauna; those taxa which dominated the marine realm for the next 250 million years. Community structure dramatically increased in complexity. New communities were established and there were fundamental shifts in dominance and abundance.Over the past ten years, there has been an effort to examine this radiation at different scales. In comparison with the Cambrian explosion which appears to be more globally mediated, local and regional studies of Ordovician faunas reveal sharp transitions with timing and magnitudes that vary geographically. These transitions suggest a more episodic and complex history than that revealed through synoptic global studies alone.Despite its apparent uniqueness, we cannot exclude the possibility that the Ordovician radiation was an extension of Cambrian diversity dynamics. That is, the Ordovician radiation may have been an event independent of the Cambrian radiation and thus requiring a different set of explanations, or it may have been the inevitable follow-up to the Cambrian radiation. Future studies should focus on resolving this issue.

Trace fossils and substrates of the terminal Proterozoic-Cambrian transition: implications for the record of early bilaterians and sediment mixing.

The trace fossil record is important in determining the timing of the appearance of bilaterian animals. A conservative estimate puts this time at approximately equal 555 million years ago. The preservational potential of traces made close to the sediment-water interface is crucial to detecting early benthic activity. Our studies on earliest Cambrian sediments suggest that shallow tiers were preserved to a greater extent than typical for most of the Phanerozoic, which can be attributed both directly and indirectly to the low levels of sediment mixing. The low levels of sediment mixing meant that thin event beds were preserved. The shallow depth of sediment mixing also meant that muddy sediments were firm close to the sediment-water interface, increasing the likelihood of recording shallow-tier trace fossils in muddy sediments. Overall, trace fossils can provide a sound record of the onset of bilaterian benthic activity.