Fossil preservation in the Neoproterozoic Doushantuo phosphorite Lagerstätte, South China

Phosphorites of the late Neoproterozoic Doushantuo Formation exposed in the vicinity of Weng'an, Guizhou Province, and Chadian, Shaanxi Province, South China, contain exceptionally well-preserved algal thalli, acritarchs, and globular microfossils interpreted as animal embryos. Combined optical microscopic and SEM observations provide insights into the taphonomy of phosphatized fossils. Algal cells and tissues are variably resistant to decay, and within preserved populations permineralization began at varying stages of degradation. In consequence, there is a spectrum of quality in cellular preservation. Algal cell walls, acritarch vesicles, and embryo envelopes are commonly encrusted by an isopachous rim of apatite, with cell interiors filled by collophane and later diagenetic dolomite. In contrast, blastomere surfaces of animal embryos are encrusted primarily by minute phosphatic spherules and filaments, possibly reflecting an immediately postmortem infestation of bacteria that provided nucleation sites for phosphate crystal growth. Thus, the same processes that gave rise to Phanerozoic phosphatized Lagerstätten - phosphatic encrustation, and impregnation, probably mediated by microbial activity - effected soft-tissue preservation in the Doushantuo Lagerstätte. It remains unclear how phosphatic ions and organic macro-molecules interact at the molecular level and to what extent specific microbial metabolisms or microenvironmental conditions control the phosphatization of soft tissues. New observations of phosphatized Doushantuo fossils include: a second locality (Chadian) for Wengania globosa , interpreted as an algal thallus and previously known only from Weng'an; microtunnels in Weng'an phosphorites interpreted as pyrite trails; and new taxa described from Weng'an: Meghystrichosphaeridium reticulatum (acritarch), Sarcinophycus radiatus (algal thallus), and one unnamed problematic form.     

Fossil preservation in the Neoproterozoic Doushantuo phosphorite Lagerstatte, South China.

Phosphorites of the late Neoproterozoic Doushantuo Formation exposed in the vicinity of Weng'an, Guizhou Province, and Chadian, Shaanxi Province, South China, contain exceptionally well-preserved algal thalli, acritarchs, and globular microfossils interpreted as animal embryos. Combined optical microscopic and SEM observations provide insights into the taphonomy of phosphatized fossils. Algal cells and tissues are variably resistant to decay, and within preserved populations permineralization began at varying stages of degradation. In consequence, there is a spectrum of quality in cellular preservation. Algal cell walls, acritarch vesicles, and embryo envelopes are commonly encrusted by an isopachous rim of apatite, with cell interiors filled by collophane and later diagenetic dolomite. In contrast, blastomere surfaces of animal embryos are encrusted primarily by minute phosphatic spherules and filaments, possibly reflecting an immediately postmortem infestation of bacteria that provided nucleation sites for phosphate crystal growth. Thus, the same processes that gave rise to Phanerozoic phosphatized Lagerstatten--phosphatic encrustation, and impregnation, probably mediated by microbial activity--effected soft-tissue preservation in the Doushantuo Lagerstatte. It remains unclear how phosphatic ions and organic macromolecules interact at the molecular level and to what extent specific microbial metabolisms or microenvironmental conditions control the phosphatization of soft tissues. New observations of phosphatized Doushantuo fossils include: a second locality (Chadian) for Wengania globosa, interpreted as an algal thallus and previously known only from Weng'an; microtunnels in Weng'an phosphorites interpreted as pyrite trails; and new taxa described from Weng'an: Meghystrichosphaeridium reticulatum (acritarch), Sarcinophycus radiatus (algal thallus), and one unnamed problematic form.     

Are the new Ediacaran Doushantuo Megasphaera-like acritarchs early metazoans?

A recent report by Chen et al. (2014) describes the new Ediacaran Doushantuo acritarchs with fascinating features. Nested within Megaclonophycus-like fossils that exhibit palintomic cell division are multicellular spheroid structures termed matryoshkas, which are interpreted to be germ cells. Such distinctive features of cellular differentiation and germ-soma separation suggest affinities of these with early stem group metazoans. In this commentary, I suggest some alternative interpretations to those elaborated by Chen et al. (2014).     

A multi-locus time-calibrated phylogeny of the siphonous green algae

The siphonous green algae are an assemblage of seaweeds that consist of a single giant cell. They comprise two sister orders, the Bryopsidales and Dasycladales. We infer the phylogenetic relationships among the siphonous green algae based on a five-locus data matrix and analyze temporal aspects of their diversification using relaxed molecular clock methods calibrated with the fossil record. The multi-locus approach resolves much of the previous phylogenetic uncertainty, but the radiation of families belonging to the core Halimedineae remains unresolved. In the Bryopsidales, three main clades were inferred, two of which correspond to previously described suborders (Bryopsidineae and Halimedineae) and a third lineage that contains only the limestone-boring genus Ostreobium. Relaxed molecular clock models indicate a Neoproterozoic origin of the siphonous green algae and a Paleozoic diversification of the orders into their families. The inferred node ages are used to resolve conflicting hypotheses about species ages in the tropical marine alga Halimeda.     

Multicellular thallophytes with differentiated tissues from Late Proterozoic phosphate rocks of South China

An assemblage of megascopic, multicellular thallophytes with well-preserved tissues and microstructures was discovered in phosphate rocks of the Late Proterozoic Doushantuo Formation (approximately 680 Ma old) at the Wengan-Fuquan Phosphate Mines, Guizhou Province, South China. Two new genera and three new species are erected: Thallophyca ramosa n. gen. et n. sp., Thallophyca simplica n. gen. et n. sp. and Wengania globosa n. gen. et n. sp. The thalli of Thallophyca are embedded in amorphous collophane and consist of differentiated tissues interpreted as cortex and medulla, and distinct structures (conceptacle-like cavities and special cell-groups or 'cell-islands'). Tissue differentiation and megascopic (millimetric to centrimetric) size of the thalli suggest that the new genus Thallophyca may represent a primitive metaphyte. The new genus Wengania is assigned to the Paleozoic algal group Solenoporaceae Pia. This study provides reliable fossil evidence of Late Proterozoic metaphytes and leads to the following conclusions: (1) diverse multicellular thallophytes had evolved during Late Proterozoic Ediacaran time; (2) adaptive radiations possibly took place more or less contemporaneously in both metazoans and metaphytes, and (3) Precambrian phosphate rocks can preserve megafossils with delicate microstructures.     

Experimental taphonomy of giant sulphur bacteria: implications for the interpretation of the embryo-like Ediacaran Doushantuo fossils

The Ediacaran Doushantuo biota has yielded fossils interpreted as eukaryotic organisms, either animal embryos or eukaryotes basal or distantly related to Metazoa. However, the fossils have been interpreted alternatively as giant sulphur bacteria similar to the extant Thiomargarita. To test this hypothesis, living and decayed Thiomargarita were compared with Doushantuo fossils and experimental taphonomic pathways were compared with modern embryos. In the fossils, as in eukaryotic cells, subcellular structures are distributed throughout cell volume; in Thiomargarita, a central vacuole encompasses approximately 98 per cent cell volume. Key features of the fossils, including putative lipid vesicles and nuclei, complex envelope ornament, and ornate outer vesicles are incompatible with living and decay morphologies observed in Thiomargarita. Microbial taphonomy of Thiomargarita also differed from that of embryos. Embryo tissues can be consumed and replaced by bacteria, forming a replica composed of a three-dimensional biofilm, a stable fabric for potential fossilization. Vacuolated Thiomargarita cells collapse easily and do not provide an internal substrate for bacteria. The findings do not support the hypothesis that giant sulphur bacteria are an appropriate interpretative model for the embryo-like Doushantuo fossils. However, sulphur bacteria may have mediated fossil mineralization and may provide a potential bacterial analogue for other macroscopic Precambrian remains.     

A new look at saponite formation and its implications for early animal records in the Ediacaran of South China

Acanthomorphic acritarch fossils, including some interpreted to be the fossils of the earliest animal embryos, first appear in the lower Doushantuo Formation of the Yangtze Gorges area (YGA). Further, the complete paleontological and geochemical record for the YGA has played a central role in defining the global biological and geochemical backdrop that presaged and witnessed the dawn of diverse animal life. Despite the importance of the YGA in our understanding of Neoproterozoic Earth history, basic aspects about its depositional history remain debated. Foremost among the controversies, extensively studied sections in the YGA were recently tied to deposition in an alkaline lake, casting new but contentious light on the environments of early animal evolution and the broader significance of geochemical records from the YGA. Arguments for a lacustrine setting hinged on the presence of trioctahedral clays (saponite–corrensite). However, this clay type commonly forms in other environments, including the weathering profiles of mafic and ultramafic volcanics. Using a coupled geochemical and sedimentological approach, we argue that the trioctahedral clays in the lower Doushantuo of the YGA are better explained as weathering products from a regional mafic‐to‐ultramafic hinterland delivered by rivers to a shelf or lagoon in the Yangtze Gorges Basin. These novel provenance relationships for YGA sediments and associated clays are consistent with a marine setting for the early animal records and must factor in our current understanding of the broader geochemical fabric of the Doushantuo Formation.     

Origin and early diversification of the phylum Cnidaria Verrill: major developments in the analysis of the taxon's Proterozoic–Cambrian history

Diploblastic eumetazoans of the phylum Cnidaria originated during the Neoproterozoic Era, possibly during the Cryogenian Period. The oldest known fossil cnidarians occur in strata of Ediacaran age and consist of polypoid forms that were either nonbiomineralizing or weakly so. The oldest possible anthozoans, including the genus Ramitubus, may be related to tabulate corals and occur in the Doushantuo Lagerstätte (upper Doushantuo Formation, South China), the age of which is poorly constrained (approximately 585 Ma?). Conulariid scyphozoans may first appear as early as 635–577 Ma (Lantian Formation, South China). A definite conulariid, most similar to Palaeozoic species assigned to the genus Paraconularia, occurs in association with the possible scyphozoan, Corumbella werneri, in the latest Ediacaran (c. 543 Ma) Tamengo Formation of Brazil. Basal Cambrian (c. 540 Ma) phosphorites in the upper Kuanchuanpu Formation (South China) yield solitary polyps of the oldest probable anthozoan (Eolympia pediculata), which appears to have been a stem hexacorallian. This same formation contains fossils interpreted by some authors as pentaradial cubozoan polyps; however, both the oldest known cubozoans and the oldest hydrozoans, all medusae, may actually occur in the Cambrian (Series 3, c. 505 Ma) Marjum Formation (Utah, USA). Although these recently published palaeontological data tend to corroborate the hypothesis that Cnidaria has a relatively deep Neoproterozoic history, the timing of major internal branching events remains poorly constrained, with, for example, the results of some molecular clock analyses indicating that the two cnidarian subphyla (Anthozoaria and Medusozoa) may have originated as many as one billion years ago. Further progress towards elucidating the evolution and early fossil record of cnidarians may accrue from: (1) an intensive search for phosphatized soft parts in possible anthozoans from the Ediacaran Doushantuo Formation; (2) an expanded search for Ediacaran conulariids; and (3) additional detailed analyses of the taphonomy and preservation of Ediacaran and Cambrian cnidarians, including possible pentaradial cubozoan polyps from the Fortunian upper Kuanchuanpu Formation.     

Distinguishing geology from biology in the Ediacaran Doushantuo biota relaxes constraints on the timing of the origin of bilaterians

The Ediacaran Doushantuo biota has yielded fossils that include the oldest widely accepted record of the animal evolutionary lineage, as well as specimens with alleged bilaterian affinity. However, these systematic interpretations are contingent on the presence of key biological structures that have been reinterpreted by some workers as artefacts of diagenetic mineralization. On the basis of chemistry and crystallographic fabric, we characterize and discriminate phases of mineralization that reflect: (i) replication of original biological structure, and (ii) void-filling diagenetic mineralization. The results indicate that all fossils from the Doushantuo assemblage preserve a complex mélange of mineral phases, even where subcellular anatomy appears to be preserved. The findings allow these phases to be distinguished in more controversial fossils, facilitating a critical re-evaluation of the Doushantuo fossil assemblage and its implications as an archive of Ediacaran animal diversity. We find that putative subcellular structures exhibit fabrics consistent with preservation of original morphology. Cells in later developmental stages are not in original configuration and are therefore uninformative concerning gastrulation. Key structures used to identify Doushantuo bilaterians can be dismissed as late diagenetic artefacts. Therefore, when diagenetic mineralization is considered, there is no convincing evidence for bilaterians in the Doushantuo assemblage.     

现代丰年虾卵的腐解实验——对早期化石胚胎研究的启示

早寒武世和埃迪卡拉纪中的球状化石,一些已被归入可能的后生动物胚胎化石,由于具较为完好的三维保存方式以及近乎完美的胚胎发育序列,为早期后生动物的起源、分类、谱系演化及发育生物学提供了难得的实证材料。然而随着研究的深入,多数寒武纪胚胎的生物学分类位置未定;而数量异常巨大、又有独自的保存方式的晚元古代陡山沱组胚胎的真伪和生物学归属,更是争议未消。通过对现生生物胚胎的实验埋藏研究,可以揭示出各类生物胚胎在腐解、埋藏各阶段的保存潜力,而现代胚胎在各实验埋藏阶段形态、结构的变化,也能为化石胚胎的研究提供重要的实证材料。本文就是通过对虾卵胚胎各发育阶段腐解保存潜力的实验模拟研究,试图为球状化石的形成机制和化石归属提供一些实验室依据。     

A new paleozoic Symmoriiformes (Chondrichthyes) from the late Carboniferous of Kansas (USA) and cladistic analysis of early chondrichthyans

Background

The relationships of cartilaginous fishes are discussed in the light of well preserved three-dimensional Paleozoic specimens. There is no consensus to date on the interrelationship of Paleozoic chondrichthyans, although three main phylogenetic hypotheses exist in the current literature: 1. the Paleozoic shark-like chondrichthyans, such as the Symmoriiformes, are grouped along with the modern sharks (neoselachians) into a clade which is sister group of holocephalans; 2. the Symmoriiformes are related to holocephalans, whereas the other Paleozoic shark-like chondrichthyans are related to neoselachians; 3. many Paleozoic shark-like chondrichthyans, such as the Symmoriiformes, are stem chondrichthyans, whereas stem and crown holocephalans are sister group to the stem and crown neoselachians in a crown-chondrichthyan clade. This third hypothesis was proposed recently, based mainly on dental characters.

Methodology/Principal Findings

On the basis of two well preserved chondrichthyan neurocrania from the Late Carboniferous of Kansas, USA, we describe here a new species of Symmoriiformes, Kawichthys moodiei gen. et sp. nov., which was investigated by means of computerized X-ray synchrotron microtomography. We present a new phylogenetic analysis based on neurocranial characters, which supports the third hypothesis and corroborates the hypothesis that crown-group chondrichthyans (Holocephali+Neoselachii) form a tightly-knit group within the chondrichthyan total group, by providing additional, non dental characters.

Conclusions/Significance

Our results highlight the importance of new well preserved Paleozoic fossils and new techniques of observation, and suggest that a new look at the synapomorphies of the crown-group chondrichthyans would be worthwhile in terms of understanding the adaptive significance of phylogenetically important characters.     

贵州瓮安新元古代陡山沱组磷酸盐化管柱状微体化石新材料

在用醋酸浸泡处理采自贵州瓮安新元古代陡山沱组磷酸质岩石样品时,获得大量微体动物骨骼化石。文中重点报道部分管柱状微体化石,即：Sinoquadraticus poratus gen.et sp.nov和Sinoquadraticus wenganensis gen. et sp.nov.。并对Sinocyclocylicus的部分特征进行补充。     

Precambrian animal life: Taphonomy of phosphatized metazoan embryos from southwest China

Phosphatized fossils from the Neoproterozoic Doushantuo Formation have provided valuable insight into the early evolution of metazoans, but the preservation of these spectacular fossils is not yet fully understood. This research begins to address this issue by performing a detailed specimen-based taphonomic analysis of the Doushantuo Formation phosphatized metazoan embryos. A total of 206 embryos in 65 thin sections from the Weng'an Phosphorite Member of the Doushantuo Formation were examined and their levels of pre-phosphatization decay estimated. The data produced from this examination reveal a strong taphonomic bias toward earlier (2-cell and 4-cell) cleavage stages, which tend to be well-preserved, and away from later (8-cell and 16-cell) cleavage stages, which tend to exhibit evidence for slight to intense levels of organic decay. In addition, the natural abundances of these embryos tend to decrease with advancement in cleavage stage, and no evidence of more advanced (beyond 16-cell) cleavage stages or eventual adult forms were found in this study. One possible explanation for this taphonomic bias toward early cleavage stages is that later cleavage stages and adult forms were more physically delicate, allowing them to be more easily damaged during burial and reworking, allowing for more rapid decay. The spectacular preservation of these embryos was probably aided by their likely internal enrichment in phosphate-rich yolk, which would have caused their internal dissolved phosphate levels to reach critical levels with only miniscule organic decay, thereby hastening phosphatization. If internal sources of phosphate did indeed play a role in the phosphatization of these embryos, it may explain their prolific abundance in these rocks compared to other phosphatized fossils as well as indicating that metazoans lacking such internal phosphate sources were likely much more difficult to preserve. The phosphatic fossils of the Doushantuo Formation, therefore, provide an indispensable, yet restricted, window into Neoproterozoic life and metazoan origins.     

Are the new Ediacaran Doushantuo embryo-like fossils early metazoans? A reply

Chen et al. (2014) described a suite of one-celled, Parapandorina-stage, Megaclonophycus-stage (some with dyads and tetrads), and matryoshka-stage fossils from the Doushantuo Formation, and interpreted them as representing a sequence of ontogenetic stages of the animal embryo-like fossil Megasphaera. Tang (2015) argues that the matryoshkas might have been parasites or symbionts, rather than developmental products of dyads and tetrads in Megaclonophycus-stage fossils. Assessing Tang's (2015) arguments against available evidence, we conclude that the matryoshkas likely represent an ontogenetic stage of Megasphaera. As such, they have the potential to illuminate the developmental biology, life cycle, and phylogenetic affinity of the enigmatic fossil Megasphaera.     

New early crown-group asteroids (Echinodermata; Triassic of Germany)

Migmaster angularis n. gen. n. sp. (Trichasteropsiidae, Forcipulatacea, Asteroidea) is described from the German Triassic Lower Muschelkalk of Anisian (Pelsonian) age, and new specimens ofTrichasteropsis bielertorum broaden understanding of this species. Phylogenetic events linking the stem groups, known only from Paleozoic rocks, with the crown group, known only from post-Paleozoic rocks, are problematic; the new fossils partially constrain phylogenetic changes associated with emergence of crown-group asteroids.      

Devonian climate change, breathing, and the origin of the tetrapod stem group

The diversification of the tetrapod stem group occurred duringthe late Middle through the Late Devonian, that is from theGivetian to Famennian stages about 385–365 million yearsago. The relationships between the known taxa representing thisradiation have currently reached a reasonable consensus so thatinterpretations of the order of appearance of tetrapod charactersis possible. The immediate fish relatives of the earliest limbedtetrapods show what is interpreted as a progressive increasein the spiracular chamber and its opening to the outside. Here,this is inferred to be associated with an increased capacityfor air-breathing. Lungs are thought to have been present inmost early bony fishes, and were most likely ventilated by air-gulping.This could have brought about a facultative capacity for air-breathing,which the tetrapod stem group exploited to the greatest degree.These adaptations are shown not only in freshwater forms butalso in estuarine and marginal marine forms. Estimates of oxygenlevels during this period suggest that they were unprecedentedlylow during the Givetian and Frasnian periods. At the same time,plant diversification was at its most rapid, changing the characterof the landscape and contributing, via soils, soluble nutrients,and decaying plant matter, to anoxia in all water systems. Theco-occurrence of these global events may explain the evolutionof air-breathing adaptations in at least two lobe-finned groups,contributing directly to the rise of the tetrapod stem group.In contrast to recent studies, low atmospheric oxygen is notconsidered to be a causal factor in the lack of fossils documentingthe evolution of Early Carboniferous tetrapods.     

Dating the Dipsacales: comparing models, genes, and evolutionary implications

Dipsacales is an asterid angiosperm clade of ca. 1100 species, with most of its lineages occupying temperate regions of the Northern Hemisphere. A recent phylogenetic analysis based on 7593 nucleotides of chloroplast DNA recovered a well-resolved and strongly supported phylogenetic hypothesis, which we use here to estimate divergence times within the group. A molecular clock is strongly rejected, regardless of data partition. We used recently proposed methods that relax the assumption of rate constancy among lineages (local clocks, nonparametric rate smoothing, penalized likelihood, and Bayesian relaxed clock) to estimate the ages of major lineages. Age estimates for Dipsacales varied widely among markers and codon positions, and depended on the fossils used for calibration and method of analysis. Some methods yielded dates for the Dipsacales diversification that appear to be too old (prior to the presumed 125 my [million years] age of eudicots), and others suggested ages that are too young based on well-documented Dipsacales fossils. Concordant penalized likelihood and Bayesian studies imply that Dipsacales originated in the Cretaceous, as did its two major lineages, Adoxaceae and Caprifoliaceae. However, diversification of crown Adoxaceae and Caprifoliaceae mainly occurred in the Tertiary, with the origin of major lineages within these clades mainly occurring during the Eocene. Another round of diversification appears to have occurred in the Miocene. Several radiations, such as Valerianaceae in South America and Dipsacaceae around the Mediterranean, are even more recent. This study demonstrates the wide range of divergence times that can be obtained using different methods and data sets, and cautions against reliance on age estimates based on only a single gene or methodology. Despite this variance, significant conclusions can be made about the timing of Dipsacales evolution.     

Sexual reproductive structures of Latest Proterozoic multicellular rhodophytes (red algae) from South China

Carposporangium- and spermatangium-like reproductive structures associated with differentiated vegetative tissues have been observed in the multicellular rhodophyte fossils, which were well preserved in the 650-Ma-old phosphate rocks of Doushantuo Formation in Guizhou Province, South China. The fossils show details of cellular structures that are comparable to the female and male reproductive organs of some extant rhodophytes. The first fossil-histological evidence for sexuality of Precambrian non-vascular plants is provided.     

Sexual reproductive structures in the green alga Ivanovia triassica

Ivanovia triassica is a new species of calcified Codiaceae from Triassic rocks of the Yukon Stikine Terrane in Canada. The genus was known previously only from the late Paleozoic. Stalked outgrowths of the thalli are interpreted as oogonia and dome-shaped outpocketings as male gametangia. These represent the first sexual reproductive structures observed in Ivanovia. Sectional views of the thalli indicate the species was cyathiform and that the inner and outer cortices of the membranes comprising the thallus were dimorphic.