Eocene animal trace fossils in 1.7-billion-year-old metaquartzites.

The Paleoproterozoic (1.7 Ga [billion years ago]) metasedimentary rocks of the Mount Barren Group in southwestern Australia contain burrows indistinguishable from ichnogenera Thalassinoides, Ophiomorpha, Teichichnus, and Taenidium, known from firmgrounds and softgrounds. The metamorphic fabric in the host rock is largely retained, and because the most resilient rocks in the sequence, the metaquartzites, are too hard for animal burrowing, the trace fossils have been interpreted as predating the last metamorphic event in the region. Since this event is dated at 1.2 Ga, this would bestow advanced animals an anomalously early age. We have studied the field relationships, petrographic fabric, and geochronology of the rocks and demonstrate that the burrowing took place during an Eocene transgression over a weathered regolith. At this time, the metaquartzites of the inundated surface had been weathered to friable sandstones or loose sands (arenized), allowing for animal burrowing. Subsequent to this event, there was a resilicification of the quartzites, filling the pore space with syntaxial quartz cement forming silcretes. Where the sand grains had not been dislocated during weathering, the metamorphic fabric was seemingly restored, and the rocks again assumed the appearance of hard metaquartzites impenetrable to animal burrowing.

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.

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.

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.

Modern optics in exceptionally preserved eyes of Early Cambrian arthropods from Australia.

Despite the status of the eye as an "organ of extreme perfection", theory suggests that complex eyes can evolve very rapidly. The fossil record has, until now, been inadequate in providing insight into the early evolution of eyes during the initial radiation of many animal groups known as the Cambrian explosion. This is surprising because Cambrian Burgess-Shale-type deposits are replete with exquisitely preserved animals, especially arthropods, that possess eyes. However, with the exception of biomineralized trilobite eyes, virtually nothing is known about the details of their optical design. Here we report exceptionally preserved fossil eyes from the Early Cambrian (∼ 515 million years ago) Emu Bay Shale of South Australia, revealing that some of the earliest arthropods possessed highly advanced compound eyes, each with over 3,000 large ommatidial lenses and a specialized 'bright zone'. These are the oldest non-biomineralized eyes known in such detail, with preservation quality exceeding that found in the Burgess Shale and Chengjiang deposits. Non-biomineralized eyes of similar complexity are otherwise unknown until about 85 million years later. The arrangement and size of the lenses indicate that these eyes belonged to an active predator that was capable of seeing in low light. The eyes are more complex than those known from contemporaneous trilobites and are as advanced as those of many living forms. They provide further evidence that the Cambrian explosion involved rapid innovation in fine-scale anatomy as well as gross morphology, and are consistent with the concept that the development of advanced vision helped to drive this great evolutionary event.

Ancestral state reconstruction of ontogeny supports a bilaterian affinity for Dickinsonia.

Despite numerous attempts, classification of the Precambrian fossil Dickinsonia has eluded scientific consensus. This is largely because Dickinsonia and its relatives are structurally simple, lacking morphological synapomorphies to clarify their relationship to modern taxa. However, there is increasing precedence for using ontogeny to constrain enigmatic fossils, and growth of the type species Dickinsonia costata is well understood. This study formalizes the connection between ontogeny in Dickinsonia-which grows by the addition of metameric units onto one end of its primary axis-with terminal addition, defined as growth and patterning from a posterior, subtermial growth zone. We employ ancestral state reconstruction and stochastic character mapping to conclude that terminal addition is a synapomorphy of bilaterian animals. Thus, terminal addition allies Dickinsonia with the bilaterians, providing evidence that large stem- or crown-group bilaterians made up a significant proportion of the Precambrian biota. This study also illustrates the potential for combining developmental and phylogenetic data in constraining the placement of ancient problematic fossil taxa on the evolutionary tree.

A new vetulicolian from Australia and its bearing on the chordate affinities of an enigmatic Cambrian group.

BACKGROUND: Vetulicolians are one of the most problematic and controversial Cambrian fossil groups, having been considered as arthropods, chordates, kinorhynchs, or their own phylum. Mounting evidence suggests that vetulicolians are deuterostomes, but affinities to crown-group phyla are unresolved. RESULTS: A new vetulicolian from the Emu Bay Shale Konservat-Lagerstätte, South Australia, Nesonektris aldridgei gen. et sp. nov., preserves an axial, rod-like structure in the posterior body region that resembles a notochord in its morphology and taphonomy, with notable similarity to early decay stages of the notochord of extant cephalochordates and vertebrates. Some of its features are also consistent with other structures, such as a gut or a coelomic cavity. CONCLUSIONS: Phylogenetic analyses resolve a monophyletic Vetulicolia as sister-group to tunicates (Urochordata) within crown Chordata, and this holds even if they are scored as unknown for all notochord characters. The hypothesis that the free-swimming vetulicolians are the nearest relatives of tunicates suggests that a perpetual free-living life cycle was primitive for tunicates. Characters of the common ancestor of Vetulicolia + Tunicata include distinct anterior and posterior body regions - the former being non-fusiform and used for filter feeding and the latter originally segmented - plus a terminal mouth, absence of pharyngeal bars, the notochord restricted to the posterior body region, and the gut extending to the end of the tail.

Pentaradial eukaryote suggests expansion of suspension feeding in White Sea-aged Ediacaran communities.

Suspension feeding is a key ecological strategy in modern oceans that provides a link between pelagic and benthic systems. Establishing when suspension feeding first became widespread is thus a crucial research area in ecology and evolution, with implications for understanding the origins of the modern marine biosphere. Here, we use three-dimensional modelling and computational fluid dynamics to establish the feeding mode of the enigmatic Ediacaran pentaradial eukaryote Arkarua. Through comparisons with two Cambrian echinoderms, Cambraster and Stromatocystites, we show that flow patterns around Arkarua strongly support its interpretation as a passive suspension feeder. Arkarua is added to the growing number of Ediacaran benthic suspension feeders, suggesting that the energy link between pelagic and benthic ecosystems was likely expanding in the White Sea assemblage (~ 558-550 Ma). The advent of widespread suspension feeding could therefore have played an important role in the subsequent waves of ecological innovation and escalation that culminated with the Cambrian explosion.

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.

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.

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.

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.

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.

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 Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records.

Unravelling the timing of the metazoan radiation is crucial for elucidating the macroevolutionary processes associated with the Cambrian explosion. Because estimates of metazoan divergence times derived from molecular clocks range from quite shallow (Ediacaran) to very deep (Mesoproterozoic), it has been difficult to ascertain whether there is concordance or quite dramatic discordance between the genetic and geological fossil records. Here, we show using a range of molecular clock methods that the major pulse of metazoan divergence times was during the Ediacaran, which is consistent with a synoptic reading of the Ediacaran macrobiota. These estimates are robust to changes in priors, and are returned with or without the inclusion of a palaeontologically derived maximal calibration point. Therefore, the two historical records of life both suggest that although the cradle of Metazoa lies in the Cryogenian, and despite the explosion of ecology that occurs in the Cambrian, it is the emergence of bilaterian taxa in the Ediacaran that sets the tempo and mode of macroevolution for the remainder of geological time.

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.