A late-Ediacaran crown-group sponge animal.

Sponges are the most basal metazoan phylum1 and may have played important roles in modulating the redox architecture of Neoproterozoic oceans2. Although molecular clocks predict that sponges diverged in the Neoproterozoic era3,4, their fossils have not been unequivocally demonstrated before the Cambrian period5-8, possibly because Precambrian sponges were aspiculate and non-biomineralized9. Here we describe a late-Ediacaran fossil, Helicolocellus cantori gen. et sp. nov., from the Dengying Formation (around 551-539 million years ago) of South China. This fossil is reconstructed as a large, stemmed benthic organism with a goblet-shaped body more than 0.4 m in height, with a body wall consisting of at least three orders of nested grids defined by quadrate fields, resembling a Cantor dust fractal pattern. The resulting lattice is interpreted as an organic skeleton comprising orthogonally arranged cruciform elements, architecturally similar to some hexactinellid sponges, although the latter are built with biomineralized spicules. A Bayesian phylogenetic analysis resolves H. cantori as a crown-group sponge related to the Hexactinellida. H. cantori confirms that sponges diverged and existed in the Precambrian as non-biomineralizing animals with an organic skeleton. Considering that siliceous biomineralization may have evolved independently among sponge classes10-13, we question the validity of biomineralized spicules as a necessary criterion for the identification of Precambrian sponge fossils.

Saccorhytus is an early ecdysozoan and not the earliest deuterostome.

The early history of deuterostomes, the group composed of the chordates, echinoderms and hemichordates1, is still controversial, not least because of a paucity of stem representatives of these clades2-5. The early Cambrian microscopic animal Saccorhytus coronarius was interpreted as an early deuterostome on the basis of purported pharyngeal openings, providing evidence for a meiofaunal ancestry6 and an explanation for the temporal mismatch between palaeontological and molecular clock timescales of animal evolution6-8. Here we report new material of S. coronarius, which is reconstructed as a millimetric and ellipsoidal meiobenthic animal with spinose armour and a terminal mouth but no anus. Purported pharyngeal openings in support of the deuterostome hypothesis6 are shown to be taphonomic artefacts. Phylogenetic analyses indicate that S. coronarius belongs to total-group Ecdysozoa, expanding the morphological disparity and ecological diversity of early Cambrian ecdysozoans.

Death march of a segmented and trilobate bilaterian elucidates early animal evolution.

The origin of motility in bilaterian animals represents an evolutionary innovation that transformed the Earth system. This innovation probably occurred in the late Ediacaran period-as evidenced by an abundance of trace fossils (ichnofossils) dating to this time, which include trails, trackways and burrows1-3. However, with few exceptions4-8, the producers of most of the late Ediacaran ichnofossils are unknown, which has resulted in a disconnection between the body- and trace-fossil records. Here we describe the fossil of a bilaterian of the terminal Ediacaran period (dating to 551-539 million years ago), which we name Yilingia spiciformis (gen. et sp. nov). This body fossil is preserved along with the trail that the animal produced during a death march. Yilingia is an elongate and segmented bilaterian with repetitive and trilobate body units, each of which consists of a central lobe and two posteriorly pointing lateral lobes, indicating body and segment polarity. Yilingia is possibly related to panarthropods or annelids, and sheds light on the origin of segmentation in bilaterians. As one of the few Ediacaran animals demonstrated to have produced long and continuous trails, Yilingia provides insights into the identity of the animals that were responsible for Ediacaran trace fossils.

A transient peak in marine sulfate after the 635-Ma snowball Earth.

SignificanceEarth system's response to major perturbations is of paramount interest. On the basis of multiple isotope compositions for pyrite, carbonate-associated sulfate, carbonates, and organics within, we inferred that the much-debated, enigmatic, extremely 13C-depleted calcite cements in the ∼635-Ma cap carbonates in South China preserve geochemical evidence for marine microbial sulfate reduction coupled to anaerobic oxidation of methane. This interpretation implies the existence of a brief interval of modern-level marine sulfate. We determined that this interval coincides with the earliest Ediacaran 17O-depletion episode, and both likely occurred within ∼50 ky since the onset of the 635-Ma meltdown, revealing an astonishing pace of transformation of the Earth system in the aftermath of Earth's latest snowball glaciation.

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.

Musculature of an Early Cambrian cycloneuralian animal.

Cycloneuralians are ecdysozoans with a fossil record extending to the Early Cambrian Fortunian Age and represented mostly by cuticular integuments. However, internal anatomies of Fortunian cycloneuralians are virtually unknown, hampering our understanding of their functional morphology and phylogenetic relationships. Here we report the exceptional preservation of cycloneuralian introvert musculature in Fortunian rocks of South China. The musculature consists of an introvert body-wall muscular grid of four circular and 36 radially arranged longitudinal muscle bundles, as well as an introvert circular muscle associated with 19 roughly radially arranged, short retractors. Collectively, these features support at least a scalidophoran affinity, and the absence of muscles associated with a mouth cone and scalids further indicates a priapulan affinity. As in modern scalidophorans, the fossil musculature, and particularly the introvert circular muscle retractors, may have controlled introvert inversion and facilitated locomotion and feeding. This work supports the evolution of scalidophoran-like or priapulan-like introvert musculature in cycloneuralians at the beginning of the Cambrian Period.

Earth Systems to Anthropocene Systems: An Evolutionary, System-of-Systems, Convergence Paradigm for Interdependent Societal Challenges.

Humans have made profound changes to the Earth. The resulting societal challenges of the Anthropocene (e.g., climate change and impacts, renewable energy, adaptive infrastructure, disasters, pandemics, food insecurity, and biodiversity loss) are complex and systemic, with causes, interactions, and consequences that cascade across a globally connected system of systems. In this Critical Review, we turn to our "origin story" for insight, briefly tracing the formation of the Universe and the Earth, the emergence of life, the evolution of multicellular organisms, mammals, primates, and humans, as well as the more recent societal transitions involving agriculture, urbanization, industrialization, and computerization. Focusing on the evolution of the Earth, genetic evolution, the evolution of the brain, and cultural evolution, which includes technological evolution, we identify a nested evolutionary sequence of geophysical, biophysical, sociocultural, and sociotechnical systems, emphasizing the causal mechanisms that first formed, and then transformed, Earth systems into Anthropocene systems. Describing how the Anthropocene systems coevolved, and briefly illustrating how the ensuing societal challenges became tightly integrated across multiple spatial, temporal, and organizational scales, we conclude by proposing an evolutionary, system-of-systems, convergence paradigm for the entire family of interdependent societal challenges of the Anthropocene.

Biomineralization by particle attachment in early animals.

Crystallization by particle attachment (CPA) of amorphous precursors has been demonstrated in modern biomineralized skeletons across a broad phylogenetic range of animals. Precisely the same precursors, hydrated (ACC-H2O) and anhydrous calcium carbonate (ACC), have been observed spectromicroscopically in echinoderms, mollusks, and cnidarians, phyla drawn from the 3 major clades of eumetazoans. Scanning electron microscopy (SEM) here also shows evidence of CPA in tunicate chordates. This is surprising, as species in these clades have no common ancestor that formed a mineralized skeleton and appear to have evolved carbonate biomineralization independently millions of years after their late Neoproterozoic divergence. Here we correlate the occurrence of CPA from ACC precursor particles with nanoparticulate fabric and then use the latter to investigate the antiquity of the former. SEM images of early biominerals from Ediacaran and Cambrian shelly fossils show that these early calcifiers used attachment of ACC particles to form their biominerals. The convergent evolution of biomineral CPA may have been dictated by the same thermodynamics and kinetics as we observe today.

Cell differentiation and germ-soma separation in Ediacaran animal embryo-like fossils.

Phosphorites of the Ediacaran Doushantuo Formation (∼600 million years old) yield spheroidal microfossils with a palintomic cell cleavage pattern. These fossils have been variously interpreted as sulphur-oxidizing bacteria, unicellular protists, mesomycetozoean-like holozoans, green algae akin to Volvox, and blastula embryos of early metazoans or bilaterian animals. However, their complete life cycle is unknown and it is uncertain whether they had a cellularly differentiated ontogenetic stage, making it difficult to test their various phylogenetic interpretations. Here we describe new spheroidal fossils from black phosphorites of the Doushantuo Formation that have been overlooked in previous studies. These fossils represent later developmental stages of previously published blastula-like fossils, and they show evidence for cell differentiation, germ-soma separation, and programmed cell death. Their complex multicellularity is inconsistent with a phylogenetic affinity with bacteria, unicellular protists, or mesomycetozoean-like holozoans. Available evidence also indicates that the Doushantuo fossils are unlikely crown-group animals or volvocine green algae. We conclude that an affinity with cellularly differentiated multicellular eukaryotes, including stem-group animals or algae, is likely but more data are needed to constrain further the exact phylogenetic affinity of the Doushantuo fossils.

Episode of intense chemical weathering during the termination of the 635 Ma Marinoan glaciation.

Cryogenian (∼720-635 Ma) global glaciations (the snowball Earth) represent the most extreme ice ages in Earth's history. The termination of these snowball Earth glaciations is marked by the global precipitation of cap carbonates, which are interpreted to have been driven by intense chemical weathering on continents. However, direct geochemical evidence for the intense chemical weathering in the aftermath of snowball glaciations is lacking. Here, we report Mg isotopic data from the terminal Cryogenian or Marinoan-age Nantuo Formation and the overlying cap carbonate of the basal Doushantuo Formation in South China. A positive excursion of extremely high δ26Mg values (+0.56 to +0.95)-indicative of an episode of intense chemical weathering-occurs in the top Nantuo Formation, whereas the siliciclastic component of the overlying Doushantuo cap carbonate has significantly lower δ26Mg values (<+0.40), suggesting moderate to low intensity of chemical weathering during cap carbonate deposition. These observations suggest that cap carbonate deposition postdates the climax of chemical weathering, probably because of the suppression of carbonate precipitation in an acidified ocean when atmospheric CO2 concentration was high. Cap carbonate deposition did not occur until chemical weathering had consumed substantial amounts of atmospheric CO2 and accumulated high levels of oceanic alkalinity. Our finding confirms intense chemical weathering at the onset of deglaciation but indicates that the maximum weathering predated cap carbonate deposition.

Sedimentology and chemostratigraphy of the terminal Ediacaran Dengying Formation at the Gaojiashan section, South China.

The late Ediacaran Dengying Formation (ca. 551.1-538.8 Ma) in South China is one of two successions where Ediacara-type macrofossils are preserved in carbonate facies along with skeletal fossils and bilaterian animal traces. Given the remarkable thickness of carbonate-bearing strata deposited in less than 12.3 million years, the Dengying Formation holds the potential for a relatively continuous chemostratigraphic profile for the terminal Ediacaran stage. In this study, a detailed sedimentological and chemostratigraphic (δ13Ccarb, δ18Ocarb, δ13Corg, δ34Spyrite, and 87Sr/86Sr) investigation was conducted on the Dengying Formation at the Gaojiashan section, Ningqiang County of the southern Shaanxi Province, South China. Sedimentological results reveal an overall shallow marine depositional environment. Carbonate breccia, void-filling botryoidal precipitates, and aragonite crystal fans are common in the Algal Dolomite Member of the Dengying Formation, suggesting that peritidal facies were repeatedly karstified. The timing of karstification was likely early, probably soon after the deposition of the dolomite sediments. The presence of authigenic aragonite cements suggests high alkalinity in the terminal Ediacaran ocean. Geochemical analysis of micro-drilled samples shows that distinct compositions are registered in different carbonate phases, which should be considered when constructing chemostratigraphic profiles representative of true temporal variations in seawater chemistry. Integrated chemostratigraphic data suggest enhanced burial of organic carbon and pyrite, and the occurrence of extensive marine anoxia (at least in the Gaojiashan Member). Rapid basinal subsidence and carbonate accumulation during a time of elevated seawater alkalinity and increased rates of pyrite burial may have facilitated the evolutionary innovation of early biomineralizing metazoans.

A problematic animal fossil from the early Cambrian Hetang Formation, South China.

The lower-middle Hetang Formation (Cambrian Stage 2-3) deposited in slope-basinal facies in South China is well-known for its preservation of the earliest articulated sponge fossils, providing an important taphonomic window into the Cambrian explosion. However, the Hetang Formation also hosts a number of problematic animal fossils that have not been systematically described. This omission results in an incomplete picture of the Hetang biota and limits its contribution to the understanding of the early evolution of animals. Here we describe a new animal taxon, Cambrowania ovata Tang and Xiao, new genus new species, from the middle Hetang Formation in the Lantian area of southern Anhui Province, South China. Specimens are preserved as carbonaceous compressions, although some are secondarily mineralized. A comprehensive analysis using reflected light microscopy, scanning electron microscopy, energy dispersive X-ray spectroscopy, and micro-CT reveals that the new species is characterized by a spheroidal to fusoidal truss-like structure consisting of rafter-like crossbars, some of which are secondarily baritized and may have been internally hollow. Some specimens have aperture-like structures that are broadly similar to oscula of sponges, whereas others show evidence of a medial split reminiscent of gaping carapaces. While the phylogenetic affinity of Cambrowania ovata Tang and Xiao, new genus new species remains problematic, we propose that it may represent carapaces of bivalved arthropods or more likely sponges in early life stages. Along with other problematic metazoan fossils such as hyolithids and sphenothallids, Cambrowania ovata Tang and Xiao, new genus new species adds to the diversity of the sponge-dominated Hetang biota in an early Cambrian deep-water slope-basinal environment.

An early Ediacaran assemblage of macroscopic and morphologically differentiated eukaryotes.

The deep-water Avalon biota (about 579 to 565 million years old) is often regarded as the earliest-known fossil assemblage with macroscopic and morphologically complex life forms. It has been proposed that the rise of the Avalon biota was triggered by the oxygenation of mid-Ediacaran deep oceans. Here we report a diverse assemblage of morphologically differentiated benthic macrofossils that were preserved largely in situ as carbonaceous compressions in black shales of the Ediacaran Lantian Formation (southern Anhui Province, South China). The Lantian biota, probably older than and taxonomically distinct from the Avalon biota, suggests that morphological diversification of macroscopic eukaryotes may have occurred in the early Ediacaran Period, perhaps shortly after the Marinoan glaciation, and that the redox history of Ediacaran oceans was more complex than previously thought.

The oldest known priapulid-like scalidophoran animal and its implications for the early evolution of cycloneuralians and ecdysozoans.

Morphological phylogenetic analyses suggest that scalidophorans (priapulids, loriciferans, and kinorhynchs) and nematoids (nematodes and nematomorphs) form the ecdysozoan clade Cycloneuralia, which is a sister group to panarthropods. It has been proposed that extant priapulids and Cambrian priapulid-like scalidophorans, because of their conserved evolution, have the potential to illuminate the ancestral morphology, ecology, and developmental biology of highly derived ecdysozoans such as nematods and arthropods. As such, Cambrian fossils, particularly Markuelia and possibly olivooids, can inform the early evolution of scalidophorans, cycloneuralians, and ecdysozoans. However, the scalidophoran Markuelia is known exclusively as embryo fossils, and the olivooids have been alternatively interpreted as cnidarians or cycloneuralians. Here, we describe a post-embryonic scalidophoran fossil Eopriapulites sphinx new genus and species, which represents the oldest known scalidophoran, from the early Cambrian Period (∼535 Ma) in South China. E. sphinx is similar to modern scalidophorans in having an introvert armed with hollow scalids, a collar with coronal scalids, and a pharynx with pharyngeal teeth, but its scalids and pharyngeal teeth are arranged in a hexaradial pattern. Phylogenetically resolved as a stem-group scalidophoran, E. sphinx shares a hexaradial pattern with the hexaradial arrangement of certain anatomical structures in kinorhynchs, loriciferans, nematoids, and Cambrian fossils such as Eolympia pediculata, which could also be a scalidophoran. Thus, the bodyplan of ancestral cycloneuralians may have had a component of hexaradial symmetry (i.e., some but not necessarily all anatomical parts are hexaradially arranged). If panarthropods are nested within paraphyletic cycloneuralians, as several molecular phylogenetic analyses suggest, the ancestral ecdysozoans may have been a legless worm possibly with a component of hexaradial symmetry.

Ordovician origin and subsequent diversification of the brown algae.

Brown algae are the only group of heterokont protists exhibiting complex multicellularity. Since their origin, brown algae have adapted to various marine habitats, evolving diverse thallus morphologies and gamete types. However, the evolutionary processes behind these transitions remain unclear due to a lack of a robust phylogenetic framework and problems with time estimation. To address these issues, we employed plastid genome data from 138 species, including heterokont algae, red algae, and other red-derived algae. Based on a robust phylogeny and new interpretations of algal fossils, we estimated the geological times for brown algal origin and diversification. The results reveal that brown algae first evolved true multicellularity, with plasmodesmata and reproductive cell differentiation, during the late Ordovician Period (ca. 450 Ma), coinciding with a major diversification of marine fauna (the Great Ordovician Biodiversification Event) and a proliferation of multicellular green algae. Despite its early Paleozoic origin, the diversification of major orders within this brown algal clade accelerated only during the Mesozoic Era, coincident with both Pangea rifting and the diversification of other heterokont algae (e.g., diatoms), coccolithophores, and dinoflagellates, with their red algal-derived plastids. The transition from ancestral isogamy to oogamy was followed by three simultaneous reappearances of isogamy during the Cretaceous Period. These are concordant with a positive character correlation between parthenogenesis and isogamy. Our new brown algal timeline, combined with a knowledge of past environmental conditions, shed new light on brown algal diversification and the intertwined evolution of multicellularity and sexual reproduction.

Palaeontology: undressing and redressing Ediacaran embryos.

Bailey et al. propose that the Ediacaran microfossils Megasphaera and Parapandorina, previously interpreted as animal resting eggs and blastula embryos, represent Thiomargarita-like sulphide-oxidizing bacteria, claiming that this interpretation better explains their abundance and taphonomy. Here we highlight important observations that significantly weaken the authors' conclusions.

Nitrate limitation in early Neoproterozoic oceans delayed the ecological rise of eukaryotes.

The early Neoproterozoic Era witnessed the initial ecological rise of eukaryotes at ca. 800 Ma. To assess whether nitrate availability played an important role in this evolutionary event, we measured nitrogen isotope compositions (δ15N) of marine carbonates from the early Tonian (ca. 1000 Ma to ca. 800 Ma) Huaibei Group in North China. The data reported here fill a critical gap in the δ15N record and indicate nitrate limitation in early Neoproterozoic oceans. A compilation of Proterozoic sedimentary δ15N data reveals a stepwise increase in δ15N values at ~800 Ma. Box model simulations indicate that this stepwise increase likely represents a ~50% increase in marine nitrate availability. Limited nitrate availability in early Neoproterozoic oceans may have delayed the ecological rise of eukaryotes until ~800 Ma when increased nitrate supply, together with other environmental and ecological factors, may have contributed to the transition from prokaryote-dominant to eukaryote-dominant marine ecosystems.

Tonian carbonaceous compressions indicate that Horodyskia is one of the oldest multicellular and coenocytic macro-organisms.

Macrofossils with unambiguous biogenic origin and predating the one-billion-year-old multicellular fossils Bangiomorpha and Proterocladus interpreted as crown-group eukaryotes are quite rare. Horodyskia is one of these few macrofossils, and it extends from the early Mesoproterozoic Era to the terminal Ediacaran Period. The biological interpretation of this enigmatic fossil, however, has been a matter of controversy since its discovery in 1982, largely because there was no evidence for the preservation of organic walls. Here we report new carbonaceous compressions of Horodyskia from the Tonian successions (~950-720 Ma) in North China. The macrofossils herein with bona fide organic walls reinforce the biogenicity of Horodyskia. Aided by the new material, we reconstruct Horodyskia as a colonial organism composed of a chain of organic-walled vesicles that likely represent multinucleated (coenocytic) cells of early eukaryotes. Two species of Horodyskia are differentiated on the basis of vesicle sizes, and their co-existence in the Tonian assemblage provides a link between the Mesoproterozoic (H. moniliformis) and the Ediacaran (H. minor) species. Our study thus provides evidence that eukaryotes have acquired macroscopic size through the combination of coenocytism and colonial multicellularity at least ~1.48 Ga, and highlights an exceptionally long range and morphological stasis of this Proterozoic macrofossils.