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SRXTM and BSE images of (a–c) Doushantuo algae and (d–f ) acritarchs. (a) SRXTM image; arrow indicates carbon-rich fluorapatite replicating algal morphology. (b– c) BSE images of the same specimen; arrow in (b) indicates encrusting carbon-poor fluorapatite; arrow in (c) indicates coarse, surface-normal carbon-poor fluorapatite crystals. (d ) SRXTM image; arrow indicates a region where laminae are absent owing to lack of space where structures abut. (e–f) BSE images; box in (e) indicates region shown in ( f ); arrow in ( f ) indicates geoidal apatite growth. Scale bar, (a) 39 mm; (b) 36 mm; (c) 20 mm; (d) 75 mm; (e) 67 mm and (f) 22 mm.
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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 o...
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... are two distinct phases of mineralization in the specimens of the alga Sarcinophycus that we have exam- ined. The first of these (figure 1a, black arrow), a carbon-rich fluorapatite, has lower X-ray attenuation (appearing less bright in the figured SRXTM images; figure 2a) and lower atomic number (appearing less bright in BSE images; figure 2b,c). This phase defines the outline of the cells and is composed of very fine crys- tals that are difficult to distinguish in BSE analysis and show no evidence for preferred orientation. ...
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... with algae, there are two phases of mineralization. The regions with high X-ray attenuation ( figure 2d) in acritarchs correspond to regions of high atomic number (figure 2e, f ) and high relative abundances of Ca, P and F and relatively low abundances of C (figure 1b, white arrow). Quantitative elemental compositions for these two phases in acritarchs are presented in the electronic supplementary material, table S1. ...
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... elemental compositions for these two phases in acritarchs are presented in the electronic supplementary material, table S1. The acritarchs studied have irregular layered tex- ture in the interior, with variable X-ray attenuation and atomic number ( figure 2d-f ). In some instances, these layers, which are composed principally of surface-normal crystals, run concentrically around the margin of voids that still exist (figure 2f ). ...
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... outer portion of the specimen has a thick region that preserves the acanthomorphic surface morphology of the acritarch cyst; there is evidence of layer- ing in this region of some specimens (figure 2d). A similar layered region surrounds the shrunken internal body, with a phase of high attenuation and high atomic number filling the intervening space ( figure 2d). ...
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... bright in BSE images). Regions with high X-ray attenuation and high atomic number have high relative elemental abundances of Ca, P and F, but low abundances of C. The inverse pattern is observed in low-attenuation regions ( figure 2; electronic supplementary material, table S1; [23,24]); -preserved soft tissue in these specimens is replicated in a low-attenuation cryptocrystalline carbon-rich fluora- patite phase (figure 2a, arrow). However, carbon-rich fluorapatite alone does not necessarily indicate soft tissue preservation: it can occasionally be void filling, in which case it can be identified as such on the basis of its texture; -geoidal textures and relatively large (greater than 1 mm) crystals with long axes perpendicular to the surface are associated with diagenetic crystal growth; these regions are associated with variation in attenuation that results in a distinctly laminated texture; this presumably reflects alternation between carbon-rich and carbon- poor fluorapatite (figures 1b and 2f, arrow). ...
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... are indistinguishable from mineral fabrics that are demonstrably void filling in other taxa in the same biota (e.g. acritarchs, figure 2e, f ). This strengthens the case that the published thin sections of Vernanimalcula represent organic substrates that contain heavily decayed tissue with several phases of diagenetic cements [9,17] and not bilaterian animals preserved to a subcellular level [12,13]. ...
Citations
... The indistinctness or lack of the cell-boundary structures between cells is relatively common in the Zhenba embryo-like fossils and has frequently been reported for the Weng'an specimens as well (Sun et al., 2020;Xiao & Knoll, 2000). Such a phenomenon has been explained as taphonomic variations resulting from different degrees of overgrowth of apatite (Xiao & Knoll, 1999) or decay (Cunningham et al., 2012). The paired small cells in both specimens are approximately equivalent in size and overall morphology and are distributed symmetrically against each other at one pole, with the underlying large cell at the opposite pole. ...
Ediacaran embryo-like spherical fossils exhibit diverse cell adhesion patterns resembling partial cleavage-stage embryos of living animals. Two three-celled specimens characterized by a pair of small cells overlying a large cell have been recovered from the Ediacaran Zhenba microfossil assemblage. Their cell adhesion pattern is highly comparable to a phenomenon reported from the Weng'an biota that was interpreted as fossil embryos undergoing discoidal cleavage. However, our specimens contain fewer cells and thus probably represent developmental precursors of the Weng'an counterparts. Additionally, new material shows several anatomical features that are inconsistent with an embryo interpretation, including (1) an unusually large volume of “blastomeres,” (2) a putative nucleus preserved within the large “yolk cell,” and (3) completely separated cells. Collectively, the Zhenba embryo-like specimens permit a reconstruction of the consecutive developmental sequence from single-celled individuals to the three-celled individuals, leading us to interpret the newly found specimens as products of abnormal development of Ediacaran embryo-like organisms whose affinity remains unresolved.
... A distinct school of the embryo-like microfossils (Fig. 9l-o) and sponge (Fig. 9p) preserved in the phosphorites of the Doushantuo Formation in the Weng'an area, such as Megasphaera (Fig. 9l), Helicoforamina (Fig. 9m), Spiralicellula (Fig. 9n) and Caveasphaera (Fig. 9o), were considered as a unique window to understand the origin of animals. However, it is challenging to ascertain the phylogenetic classification of these ornamented spheroidal fossils, and hence, their affinities are still controversial Chen et al., 2000;Cunningham et al., 2012;Hagadorn et al., 2006;Huldtgren et al., 2011). Taking the enigmatic Helicoforamina wenganica with a helical structure as an example (Fig. 9m), there were several disparate explanations of its phylogenetic position due to the obvious lack of awareness of internal biological structure. ...
The emergence and diversity of eukaryotes that occurred in the Proterozoic Eon (2.5–0.541 Ga) are the most important parts of life’s evolution on the Earth. However, the critical time and key environmental factor(s) are still controversial. Herein, we systematically compiled the reported fossils and convinced biomarkers of Proterozoic eukaryotes. The Proterozoic eukaryotic evolutionary timeline was proposed to be divided into four stages: (1) ambiguous origin (2.3–1.8 Ga), (2) slow evolution (1.8–0.8 Ga), (3) diversity fluctuation (0.8–0.635 Ga), and (4) first radiation (0.635–0.541 Ga). As aerobic organisms, the emergence and evolution of eukaryotes have been proposed to be hindered by low oxygen levels during the Proterozoic Eon. However, increasing evidence suggests that the Proterozoic oxygen content might have been higher than 1% PAL (present atmospheric level) since 2.3 Ga, allowing eukaryotes, including early animals, to survive. The Great Oxygenation Event (GOE) did not wake up eukaryotes. The Mesoproterozoic Oxygenation Event (MOE) did not accelerate the evolution of eukaryotes. The first and rapid radiation of eukaryotes after the Neoproterozoic Oxygenation Event (NOE) and global glaciations acted like the opening of Pandora's box. Hence atmospheric oxygen alone cannot be invoked as the only control on the evolution of eukaryotes. Instead, we suggest that oceanic temperature may have been an important environmental factor that limited eukaryotic physiology until the end-Proterozoic.
... Nearly all of the phosphatized EELFs from the Weng'an Biota have undergone taphonomic and diagenetic processes [44]. ...
The origin and early evolution of animal development remain among the many deep, unresolved problems in evolutionary biology. As a compelling case for the existence of pre-Cambrian animals, the Ediacaran embryo-like fossils (EELFs) from the Weng'an Biota (approx. 609 Myr old, Doushantuo Formation, South China) have great potential to cast light on the origin and early evolution of animal development. However, their biological implications can be fully realized only when their phylogenetic positions are correctly established, and unfortunately, this is the key problem under debate. As a significant feature of developmental biology, the cell division pattern (CDP) characterized by the dynamic spatial arrangement of cells and associated developmental mechanisms is critical to reassess these hypotheses and evaluate the diversity of the EELFs; however, their phylogenetic implications have not been fully realized. Additionally, the scarcity of fossil specimens representing late developmental stages with cell differentiation accounts for much of this debate too. Here, we reconstructed a large number of EELFs using submicron resolution X-ray tomographic microscopy and focused on the CDPs and associated developmental mechanisms as well as features of cell differentiation. Four types of CDPs and specimens with cell differentiation were identified. Contrary to the prevailing view, our results together with recent studies suggest that the diversity and complexity of developmental mechanisms documented by the EELFs are much higher than is often claimed. The diverse CDPs and associated development features including palintomic cleavage, maternal nutrition, asymmetric cell divisions, symmetry breaking, establishment of polarity or axis, spatial cell migration and differentiation constrain some, if not all, EELFs as total-group metazoans.
This article is part of the theme issue ‘The impact of Chinese palaeontology on evolutionary research’.
... In previous studies, the Weng'an embryoids are described under various genus and species name include Megasphaera, Parapandorina, Megaclonophycus, and Tianzhushania because of the different taxonomic interpretations (Xiao and Knoll 2000;Huldtgren et al. 2011;Cunningham et al. 2012a;Chen et al. 2014;Xiao et al. 2014a, b). While Xiao and Knoll have argued that Megasphaera is a form taxon, likely encompassing many biological species (Xiao and Knoll 2000), the majority of studies of the Weng'an biota have treated it as a coherent biological taxon (Bailey et al. 2007;Huldtgren et al. 2011;Chen et al. 2014;Zhang and Pratt 2014) and, indeed, many researchers have interpreted the diverse components of the Weng'an Biota as stages in the life cycle of just one or a smaller number of taxa (Xiao et al. 2007a;Huldtgren et al. 2011;Zhang and Pratt 2014). ...
Embryo-like fossils from the early Ediacaran Weng’an biota provide a window of exceptional fossil preservation onto the period of life history in which molecular clocks estimate the fundamental animal lineages to have diverged. However, their diversity and biological affinities have proven controversial, because they are morphologically simple and, consequently, their interpretation lacks phylogenetic constraint. The subcellular structures preserved in these embryo-like fossils might help to understand their cytology, biology, and diversity, but the potential of these structures has not been fully realized, because detailed microscale physical and chemical investigations are lacking. Here, to remedy this deficiency, we performed a comprehensive study to characterize their micro- and ultra-structures as well as in-situ chemical components. Our results reveal three types of subcellular structure that differ in size, shape, and mineral components: (1) relatively small and spheroidal granules in embryo-like fossils with equal cell division pattern; (2) relatively large, spheroidal, or polygonal granules in embryo-like fossils with unequal and asynchronous cell division pattern; and (3) irregular multi-layered rim-bounded granules in embryo-like fossils with unequal and asynchronous cell division pattern. We propose that the three types may be rationalized to a single taphonomic pathway of preferential mineralization of the cell cytoplasm, preserving an external mould of subcellular granules. We followed the previous interpretation that the spheroidal and polygonal granules should be fossilized lipid droplets or yolk platelets. The distinction between these subcellular structures are largely the result of postmortem degradation processes such as autolysis. The widely preserved lipid droplets or yolk platelets within these Ediacaran embryo-like fossils are compatible with the interpretion of large yolky embryos with maternal nourishment and direct development.
... Since the mid-1990s, 'Orsten'-type preservations have been continuously documented globally, and their age has been further expanded to include the early Ordovician, lower Cambrian, and even the Ediacaran (Zhang and Pratt, 1994;Walossek, 1999;Dong et al., 2005aDong et al., , 2005bMaas et al., 2006;. With the discovery of fossil metazoan embryos from the Doushantuo and Kuanchuanpu formations of China, embryology became a new topic in palaeontology (Bengtson and Yu, 1997;Bailey et al., 2007;Cohen et al., 2009;Huldtgren et al., 2011;Cunningham et al., 2012;Yin and Zhu, 2012;Zhang et al., 2014;Yin et al., 2018). ...
Our understanding of the early Cambrian bioradiation is largely driven by the contrasting information obtained from small skeletal fossils (SSF) and various types of exceptionally preserved fossils from different parts of the world. In this study, a new ‘Orsten’-type fossil Lagerstätte is reported from the Cambrian Series 2 upper Shuijingtuo Formation in the eastern Three Gorges area, South China. The Shuijingtuo Formation yielded a range of microscopic fragments of metazoan cuticles as well as fragments of possible epithelial tissue. Seventeen different types of micro-ornamentation patterns are recognized on the surface of these cuticular fragments. Based on comparisons with fossil organisms recorded from coeval strata elsewhere, as well as extant relatives, possible affinities with arthropods, palaeoscolecids, acrotretid brachiopods and mollusks are discussed. This ‘Orsten’-type fossil assemblage was deposited in offshore environments, and the lack of evidence for long-distance transportation indicates that a highly diverse fauna was present in, or very close to, the relatively deep shelf settings in the Three Gorges area during the early Cambrian (Epoch 2, Age 3). The invasion of metazoans into deeper, offshore environments could have closely followed, or even been coeval, with their radiation in relatively shallow water settings. Thus, albeit highly fragmented, such cuticular fossils can aid in providing a more complete picture of the Cambrian bioradiation.
... Beneath the outer wall, the specimens are invariably solid and almost always show evidence of multiple phases of void-filling cement, manifest as mineral phases with different x-ray attenuation profiles. These vary from fine-grained and largely homogenous ( Some specimens show evidence of inner bodies smaller than the inner volume of the outer wall, but which trace its shape, reflecting postmortem shrinkage [e.g., Figs. 1 (K, L, P to R) and 4 (I to K)]; the intervening volume is occupied by coarse void-filling cement, while the inner body is more finely crystalline, characteristic of mineralization of an original biological substrate ( Fig. 1, P, Q, and U) (19). In some specimens, centrifugal lining of the void beneath the inner surface of the outer wall can create the impression of a thickened outer wall, but this is a diagenetic void-filling mineral artifact (e.g., Fig. 1, N and S). ...
... These large cells are of equal size within each specimen and fill more or less fully the space enclosed by the outer wall. A couple of specimens preserve small spheroids in a manner akin to the cells in specimens of "Megaclonophycus-stage" Megasphaera (e.g., Fig. 4, A to D), where the cell membrane exhibits evidence of centripetal and/or centrifugal mineralization (19). The spheroidal morphology of the cells and their discrete distribution suggest that if they were once associated, they have been disaggregated. ...
The exceptional fossil preservation of the early Ediacaran Weng’an biota provides a unique window on the interval of Earth history in which animal lineages emerged. It preserves a diversity of similarly ornamented encysted developmental stages previously interpreted as different developmental stages of one taxon. Although Helicoforamina wenganica is distinguished from other forms by a helical groove or canal, it has been interpreted as a developmental stage of cooccurring metazoan, nonmetazoan holozoan, or green algal taxa. Using x-ray microtomography, we show that Helicoforamina developed through one-, four-, and eight-cell stages, to hundreds and thousands of cells. Putative hatchlings are artifacts of incompletely preserved cyst walls. Our results preclude inclusion of Helicoforamina into life cycles assembled from other components of the Weng’an biota but support a holozoan affinity. The similarly ornamented encysted forms shared among the diverse Weng’an biota represent parallel adaptations to the temporally and spatially heterogeneous Ediacaran shallow marine environments.
... The Weng'an biota provides a unique insight into multicellular life in the early Ediacaran period, during which molecular clocks estimate the fundamental animal lineages to have diverged [6]. Indeed, there are numerous claims of animal remains from the biota, including miniature adult eumetazoans [7] and bilaterians [8], and embryonic animals [2,[9][10][11][12], but all remain contentious [3,[13][14][15][16][17][18]. However, there is a broader diversity of fossil remains from this deposit that have been the subject of little attention, some of which may have a greater claim on animal affinity. ...
The Ediacaran Weng'an Biota (Doushantuo Formation, 609 Ma old) is a rich microfossil assemblage that preserves biological structure to a subcellular level of fidelity and encompasses a range of developmental stages [1]. However, the animal embryo interpretation of the main components of the biota has been the subject of controversy [2, 3]. Here, we describe the development of Caveasphaera, which varies in morphology from lensoid to a hollow spheroidal cage [4] to a solid spheroid [5] but has largely evaded description and interpretation. Caveasphaera is demonstrably cellular and develops within an envelope by cell division and migration, first defining the spheroidal perimeter via anastomosing cell masses that thicken and ingress as strands of cells that detach and subsequently aggregate in a polar region. Concomitantly, the overall diameter increases as does the volume of the cell mass, but after an initial phase of reductive palinotomy, the volume of individual cells remains the same through development. The process of cell ingression, detachment, and polar aggregation is analogous to gastrulation; together with evidence of functional cell adhesion and development within an envelope, this is suggestive of a holozoan affinity. Parental investment in the embryonic development of Caveasphaera and co-occurring Tianzhushania and Spiralicellula, as well as delayed onset of later development, may reflect an adaptation to the heterogeneous nature of the early Ediacaran nearshore marine environments in which early animals evolved.
... Synchrotron sources allow other contrast modalities to be explored, such as the phase contrast. Phasecontrast µ-CT has become critical for paleobiological studies in the last decades (Tafforeau et al., 2006;Cunningham et al., 2012;Maldanis et al., 2016), due to its capacity of extracting 3D information from these homogeneously dense specimens non-invasively, revealing even the preservation of soft tissues. Recently, the limit of resolution of X-ray microscopy has been pushed forward by the development of techniques based on Coherent Diffraction Imaging (CDI), specially Ptychography. ...
The biogenicity problem of geological materials is one of the most challenging ones in the field of paleo and astrobiology. As one goes deeper in time, the traces of life become feeble and ambiguous, blending with the surrounding geology. Well-preserved metasedimentary rocks from the Archaean are relatively rare, and in very few cases contain structures resembling biological traces or fossils. These putative biosignatures have been studied for decades and many biogenicity criteria have been developed, but there is still no consensus for many of the proposed structures. Synchrotron-based techniques, especially on new generation sources, have the potential for contributing to this field of research, providing high sensitivity and resolution that can be advantageous for different scientific problems. Exploring the X-ray and matter interactions on a range of geological materials can provide insights on morphology, elemental composition, oxidation states, crystalline structure, magnetic properties, and others, which can measurably contribute to the investigation of biogenicity of putative biosignatures. Here, we provide an overview of selected synchrotron-based techniques that have the potential to be applied in different types of questions on the study of biosignatures preserved in the geological record. The development of 3rd and recently 4th generation synchrotron sources will favor a deeper understanding of the earliest records of life on Earth and also bring up potential analytical approaches to be applied for the search of biosignatures in meteorites and samples returned from Mars in the near future.
... The biostratinomy of the Weng'an Biota has been considered previously (Cunningham et al., 2012;Schiffbauer et al., 2012;Yin et al., 2014, discriminating early phases of mineralization which preserve biological structure from later void-filling mineralization and late diagenetic mineral phases. Mineral phases preserving biological structure are invariably microcrystalline and randomly oriented, reflecting growth on and within an organic template; later phases unrelated to the original biological structure are usually more coarsely crystalline and polarized, reflecting centripetal and centrifugal void-filling growth relative to existing mineral substrates (Cunningham et al., 2012). ...
... The biostratinomy of the Weng'an Biota has been considered previously (Cunningham et al., 2012;Schiffbauer et al., 2012;Yin et al., 2014, discriminating early phases of mineralization which preserve biological structure from later void-filling mineralization and late diagenetic mineral phases. Mineral phases preserving biological structure are invariably microcrystalline and randomly oriented, reflecting growth on and within an organic template; later phases unrelated to the original biological structure are usually more coarsely crystalline and polarized, reflecting centripetal and centrifugal void-filling growth relative to existing mineral substrates (Cunningham et al., 2012). ...
... Most of the fossils otherwise exhibit a structureless and homogeneous interior which reflects mineralization of a structureless, extensively decayed cyst interior (Fig. 3). The low contrast, low-attenuation mineral microspheres that characterize the mineralization of the interior of some cysts (e.g., Fig. 2H-J), is characteristic of mineral-replicated biological structure in other Weng'an fossils (Cunningham et al., 2012). Their consistent shape and distribution is compatible with preservation of original biological structure, as component cells as in Megaclonophycus (Cunningham et al., 2012), or as small lipid droplets (Hagadorn et al., 2006;Raff et al., 2006). ...
... The biostratinomy of the Weng'an Biota has been considered previously (Cunningham et al., 2012;Schiffbauer et al., 2012;Yin et al., 2014Yin et al., , 2017, discriminating early phases of mineralization which preserve biological structure from later void-filling mineralization and late diagenetic mineral phases. Mineral phases preserving biological structure are invariably microcrystalline and randomly oriented, reflecting growth on and within an organic template; later phases unrelated to the original biological structure are usually more coarsely crystalline and polarized, reflecting centripetal and centrifugal void-filling growth relative to existing mineral substrates (Cunningham et al., 2012). ...
... The biostratinomy of the Weng'an Biota has been considered previously (Cunningham et al., 2012;Schiffbauer et al., 2012;Yin et al., 2014Yin et al., , 2017, discriminating early phases of mineralization which preserve biological structure from later void-filling mineralization and late diagenetic mineral phases. Mineral phases preserving biological structure are invariably microcrystalline and randomly oriented, reflecting growth on and within an organic template; later phases unrelated to the original biological structure are usually more coarsely crystalline and polarized, reflecting centripetal and centrifugal void-filling growth relative to existing mineral substrates (Cunningham et al., 2012). ...
... Most of the fossils otherwise exhibit a structureless and homogeneous interior which reflects mineralization of a structureless, extensively decayed cyst interior (Fig. 3). The low contrast, low-attenuation mineral microspheres that characterize the mineralization of the interior of some cysts (e.g., Fig. 2H-J), is characteristic of mineral-replicated biological structure in other Weng'an fossils (Cunningham et al., 2012). Their consistent shape and distribution is compatible with preservation of original biological structure, as component cells as in Megaclonophycus (Cunningham et al., 2012), or as small lipid droplets (Hagadorn et al., 2006;Raff et al., 2006). ...
The Ediacaran Weng’an Biota provides a unique window on marine diversity during the interval in which the fundamental animal body plans were being established. Here we describe a previously unreported component of the assemblage, millimeter-scale encysted spheres that exhibit a characteristic but simple slit-shaped excystment mechanism (Sporosphaera guizhouensis n. gen. n. sp.), reminiscent of acritarchs. The cysts contain a large inner body or numerous small discrete membrane-bounded bodies. It is possible that the inner bodies represent disaggregated cells of a multicellular body, like an embryo, but there is no evidence to support this interpretation and the occurrence of the excystment structure is not readily compatible with an embryo interpretation. Rather, we interpret the encysted organisms as multicellular stages within the lifecycle of otherwise probably unicellular eukaryotes. The developmental mode exhibited by Sporosphaera, incorporating a resting stage, implies an adaptation to adverse environmental conditions. This parallels the appearance of Large Ornamented Ediacaran Microfossils (LOEMs) which have been interpreted as diapause stages in the embryology of early animals. Sporosphaera is distinct from LOEMs by ornamentation instead of size, which may implicate that not all LOEMs are animal embryos, if any.
