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.

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.

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.

Phylotranscriptomics unveil a Paleoproterozoic-Mesoproterozoic origin and deep relationships of the Viridiplantae.

The Viridiplantae comprise two main clades, the Chlorophyta (including a diverse array of marine and freshwater green algae) and the Streptophyta (consisting of the freshwater charophytes and the land plants). Lineages sister to core Chlorophyta, informally refer to as prasinophytes, form a grade of mainly planktonic green algae. Recently, one of these lineages, Prasinodermophyta, which is previously grouped with prasinophytes, has been identified as the sister lineage to both Chlorophyta and Streptophyta. Resolving the deep relationships among green plants is crucial for understanding the historical impact of green algal diversity on marine ecology and geochemistry, but has been proven difficult given the ancient timing of the diversification events. Through extensive taxon and gene sampling, we conduct large-scale phylogenomic analyses to resolve deep relationships and reveal the Prasinodermophyta as the lineage sister to Chlorophyta, raising questions about the necessity of classifying the Prasinodermophyta as a distinct phylum. We unveil that incomplete lineage sorting is the main cause of discordance regarding the placement of Prasinodermophyta. Molecular dating analyses suggest that crown-group green plants and crown-group Prasinodermophyta date back to the Paleoproterozoic-Mesoproterozoic. Our study establishes a plausible link between oxygen levels in the Paleoproterozoic-Mesoproterozoic and the origin of Viridiplantae.

Recurrent photic zone euxinia limited ocean oxygenation and animal evolution during the Ediacaran.

The Ediacaran Period (~635-539 Ma) is marked by the emergence and diversification of complex metazoans linked to ocean redox changes, but the processes and mechanism of the redox evolution in the Ediacaran ocean are intensely debated. Here we use mercury isotope compositions from multiple black shale sections of the Doushantuo Formation in South China to reconstruct Ediacaran oceanic redox conditions. Mercury isotopes show compelling evidence for recurrent and spatially dynamic photic zone euxinia (PZE) on the continental margin of South China during time intervals coincident with previously identified ocean oxygenation events. We suggest that PZE was driven by increased availability of sulfate and nutrients from a transiently oxygenated ocean, but PZE may have also initiated negative feedbacks that inhibited oxygen production by promoting anoxygenic photosynthesis and limiting the habitable space for eukaryotes, hence abating the long-term rise of oxygen and restricting the Ediacaran expansion of macroscopic oxygen-demanding animals.

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.

Mid-latitudinal habitable environment for marine eukaryotes during the waning stage of the Marinoan snowball glaciation.

During the Marinoan Ice Age (ca. 654-635 Ma), one of the 'Snowball Earth' events in the Cryogenian Period, continental icesheets reached the tropical oceans. Oceanic refugia must have existed for aerobic marine eukaryotes to survive this event, as evidenced by benthic phototrophic macroalgae of the Songluo Biota preserved in black shales interbedded with glacial diamictites of the late Cryogenian Nantuo Formation in South China. However, the environmental conditions that allowed these organisms to thrive are poorly known. Here, we report carbon-nitrogen-iron geochemical data from the fossiliferous black shales and adjacent diamictites of the Nantuo Formation. Iron-speciation data document dysoxic-anoxic conditions in bottom waters, whereas nitrogen isotopes record aerobic nitrogen cycling perhaps in surface waters. These findings indicate that habitable open-ocean conditions were more extensive than previously thought, extending into mid-latitude coastal oceans and providing refugia for eukaryotic organisms during the waning stage of the Marinoan Ice Age.

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.

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.

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.

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.

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.

Preservation of early Tonian macroalgal fossils from the Dolores Creek Formation, Yukon.

The rise of eukaryotic macroalgae in the late Mesoproterozoic to early Neoproterozoic was a critical development in Earth's history that triggered dramatic changes in biogeochemical cycles and benthic habitats, ultimately resulting in ecosystems habitable to animals. However, evidence of the diversification and expansion of macroalgae is limited by a biased fossil record. Non-mineralizing organisms are rarely preserved, occurring only in exceptional environments that favor fossilization. Investigating the taphonomy of well-preserved macroalgae will aid in identifying these target environments, allowing ecological trends to be disentangled from taphonomic overprints. Here we describe the taphonomy of macroalgal fossils from the Tonian Dolores Creek Formation (ca. 950 Ma) of northwestern Canada (Yukon Territory) that preserves cm-scale macroalgae. Analytical microscopy, including scanning electron microscopy and tomographic x-ray microscopy, was used to investigate fossil preservation, which was the result of a combination of pyritization and aluminosilicification, similar to accessory mineralization observed in Paleozoic Burgess Shale-type fossils. These new Neoproterozoic fossils help to bridge a gap in the fossil record of early algae, offer a link between the fossil and molecular record, and provide new insights into evolution during the Tonian Period, when many eukaryotic lineages are predicted to have diversified.

Phylotranscriptomic insights into a Mesoproterozoic-Neoproterozoic origin and early radiation of green seaweeds (Ulvophyceae).

The Ulvophyceae, a major group of green algae, is of particular evolutionary interest because of its remarkable morphological and ecological diversity. Its phylogenetic relationships and diversification timeline, however, are still not fully resolved. In this study, using an extensive nuclear gene dataset, we apply coalescent- and concatenation-based approaches to reconstruct the phylogeny of the Ulvophyceae and to explore the sources of conflict in previous phylogenomic studies. The Ulvophyceae is recovered as a paraphyletic group, with the Bryopsidales being a sister group to the Chlorophyceae, and the remaining taxa forming a clade (Ulvophyceae sensu stricto). Molecular clock analyses with different calibration strategies emphasize the large impact of fossil calibrations, and indicate a Meso-Neoproterozoic origin of the Ulvophyceae (sensu stricto), earlier than previous estimates. The results imply that ulvophyceans may have had a profound influence on oceanic redox structures and global biogeochemical cycles at the Mesoproterozoic-Neoproterozoic transition.

Cracking the superheavy pyrite enigma: possible roles of volatile organosulfur compound emission.

The global deposition of superheavy pyrite (pyrite isotopically heavier than coeval seawater sulfate in the Neoproterozoic Era and particularly in the Cryogenian Period) defies explanation using the canonical marine sulfur cycle system. Here we report petrographic and sulfur isotopic data (δ34Spy) of superheavy pyrite from the Cryogenian Datangpo Formation (660-650 Ma) in South China. Our data indicate a syndepositional/early diagenetic origin of the Datangpo superheavy pyrite, with 34S-enriched H2S supplied from sulfidic (H2S rich) seawater. Instructed by a novel sulfur-cycling model, we propose that the emission of 34S-depleted volatile organosulfur compounds (VOSC) that were generated via sulfide methylation may have contributed to the formation of 34S-enriched sulfidic seawater and superheavy pyrite. The global emission of VOSC may be attributed to enhanced organic matter production after the Sturtian glaciation in the context of widespread sulfidic conditions. These findings demonstrate that VOSC cycling is an important component of the sulfur cycle in Proterozoic oceans.

Cryptic terrestrial fungus-like fossils of the early Ediacaran Period.

The colonization of land by fungi had a significant impact on the terrestrial ecosystem and biogeochemical cycles on Earth surface systems. Although fungi may have diverged ~1500-900 million years ago (Ma) or even as early as 2400 Ma, it is uncertain when fungi first colonized the land. Here we report pyritized fungus-like microfossils preserved in the basal Ediacaran Doushantuo Formation (~635 Ma) in South China. These micro-organisms colonized and were preserved in cryptic karstic cavities formed via meteoric water dissolution related to deglacial isostatic rebound after the terminal Cryogenian snowball Earth event. They are interpreted as eukaryotes and probable fungi, thus providing direct fossil evidence for the colonization of land by fungi and offering a key constraint on fungal terrestrialization.

Putative fossil blood cells reinterpreted as diagenetic structures.

Red to red-orange spheres in the vascular canals of fossil bone thin sections have been repeatedly reported using light microscopy. Some of these have been interpreted as the fossilized remains of blood cells or, alternatively, pyrite framboids. Here, we assess claims of blood cell preservation within bones of the therizinosauroid theropod Beipiaosaurus inexpectus from the Jehol Lagerstätte. Using Raman spectroscopy, Energy Dispersive X-ray Spectrometry, and Time of Flight Secondary Ion Mass Spectroscopy, we found evidence of high taphonomic alteration of the bone. We also found that the vascular canals in the bone, once purported to contain fossil red blood cell, are filled with a mix of clay minerals and carbonaceous compounds. The spheres could not be analyzed in isolation, but we did not find any evidence of pyrite or heme compounds in the vessels, surrounding bone, or matrix. However, we did observe similar spheres under light microscopy in petrified wood found in proximity to the dinosaur. Consequently, we conclude that the red spheres are most likely diagenetic structures replicated by the clay minerals present throughout the vascular canals.

The influence of environmental setting on the community ecology of Ediacaran organisms.

The broad-scale environment plays a substantial role in shaping modern marine ecosystems, but the degree to which palaeocommunities were influenced by their environment is unclear. To investigate how broad-scale environment influenced the community ecology of early animal ecosystems, we employed spatial point process analyses (SPPA) to examine the community structure of seven late Ediacaran (558-550 Ma) bedding-plane assemblages drawn from a range of environmental settings and global localities. The studied palaeocommunities exhibit marked differences in the response of their component taxa to sub-metre-scale habitat heterogeneities on the seafloor. Shallow-marine (nearshore) palaeocommunities were heavily influenced by local habitat heterogeneities, in contrast to their deeper-water counterparts. The local patchiness within shallow-water communities may have been further accentuated by the presence of grazers and detritivores, whose behaviours potentially initiated a propagation of increasing habitat heterogeneity of benthic communities from shallow to deep-marine depositional environments. Higher species richness in shallow-water Ediacaran assemblages compared to deep-water counterparts across the studied time-interval could have been driven by this environmental patchiness, because habitat heterogeneities increase species richness in modern marine environments. Our results provide quantitative support for the 'Savannah' hypothesis for early animal diversification-whereby Ediacaran diversification was driven by patchiness in the local benthic environment.

A one-billion-year-old multicellular chlorophyte.

Chlorophytes (representing a clade within the Viridiplantae and a sister group of the Streptophyta) probably dominated marine export bioproductivity and played a key role in facilitating ecosystem complexity before the Mesozoic diversification of phototrophic eukaryotes such as diatoms, coccolithophorans and dinoflagellates. Molecular clock and biomarker data indicate that chlorophytes diverged in the Mesoproterozoic or early Neoproterozoic, followed by their subsequent phylogenetic diversification, multicellular evolution and ecological expansion in the late Neoproterozoic and Palaeozoic. This model, however, has not been rigorously tested with palaeontological data because of the scarcity of Proterozoic chlorophyte fossils. Here we report abundant millimetre-sized, multicellular and morphologically differentiated macrofossils from rocks approximately 1,000 million years ago. These fossils are described as Proterocladus antiquus new species and are interpreted as benthic siphonocladalean chlorophytes, suggesting that chlorophytes acquired macroscopic size, multicellularity and cellular differentiation nearly a billion years ago, much earlier than previously thought.