The Weng'an Biota is a fossil Konservat-Lagerstätte in South China that is c. 570 – 609 myr old and provides an unparalleled snapshot of marine life during the interval in which molecular clocks estimate that animal clades were diversifying. It yields fossils that are three-dimensionally preserved in calcium phosphate with cellular and sometimes subcellular fidelity. The biota includes candidates for the oldest animals in the fossil record, including embryonic, larval and adult forms. We argue that, although the Weng'an Biota includes forms that could be animals, none can currently be assigned to this group with confidence. Nonetheless, the biota offers a rare and valuable window on the evolution of multicellular and soft-bodied organisms in the prelude to the Cambrian radiation.
Fossilized embryos afford direct insight into the pattern of development in extinct organisms, providing unique tests of hypotheses of developmental evolution based in comparative embryology. However, these fossils can only be effective in this role if their embryology and phylogenetic affinities are well constrained. We elucidate and interpret the development of Olivooides from embryonic and adult stages and use these data to discriminate among competing interpretations of their anatomy and affinity. The embryology of Olivooides is principally characterized by the development of an ornamented periderm that initially forms externally and is subsequently formed internally, released at the aperture, facilitating the direct development of the embryo into an adult theca. Internal anatomy is known only from embryonic stages, revealing two internal tissue layers, the innermost of which is developed into three transversally arranged walls that partly divide the lumen into an abapertural region, interpreted as the gut of a polyp, and an adapertural region that includes structures that resemble the peridermal teeth of coronate scyphozoans. The anatomy and pattern of development exhibited by Olivooides appears common to the other known genus of olivooid, Quadrapyrgites, which differs in its tetraradial, as opposed to pentaradial symmetry. We reject previous interpretations of the olivooids as cycloneuralians, principally on the grounds that they lack a through gut and introvert, in embryo and adult. Instead we consider the affinities of the olivooids among medusozoan cnidarians; our phylogenetic analysis supports their classification as totalgroup Coronata, within crown-Scyphozoa. Olivooides and Quadrapyrgites evidence a broader range of life history strategies and bodyplan symmetry than is otherwise commonly represented in extant Scyphozoa specifically, and Cnidaria more generally.Key words: development, embryo, Cnidaria, Scyphozoa, Kuanchuanpu, Cambrian. et al. 2015), the tempo of early animal evolution is astonishing given the scale of innovation achieved (Erwin et al. 2011): the establishment of all phylum-level body plans that are sufficiently distinct that they are effectively defined by the limits of comparative anatomy (Bengtson 1986). Insights into the processes that brought about this remarkable episode in evolutionary history are afforded through comparative embryology of living animals, facilitating inference of the embryology of ancient ancestors and, indeed, into the evolution of development that brought about the origin of animal bodyplans. Inevitably, this approach is confused by the subsequent developmental evolution that serves to conflate homologies and convergences. Hence, the discovery of a fossil record of embryology from early in animal evolutionary history affords a more direct insight into the embryology of ancient ancestors, free from the confounding effects of half a billion years of subsequent evolutionary history. T H O U G H there remains considerable debate over the timing of ori...
General rightsThis document is made available in accordance with publisher policies. Please cite only the published version using the reference above. Full terms of use are available: http://www.bristol.ac.uk/pure/about/ebr-terms A R T I C L E I N F OKeywords: Fossil embryo Doushantuo Animal Evolution Ediacaran A B S T R A C TThe embryo-like microfossils from the Ediacaran Weng'an Biota (ca. 609 million years old) are among the oldest plausible claims of animals in the fossil record. Fossilization frequently extends beyond the cellular, to preserve subcellular structures including contentious Large Intracellular Structures (LISs) that have been alternately interpreted as eukaryote nuclei or organelles, degraded remains, or abiological structures. Here we present new data on the structure, morphology, and development of the LISs in these embryo-like fossils, based on Synchrotron Radiation X-ray Tomographic Microscopy (SRXTM) and quantitative computed tomographic analysis. All the lines of evidence, including consistency in the number, shape, position, and relative size (LIS-tocytoplasm ratio) of the LISs, as well as their occurrence within preserved cytoplasm, support their interpretation as cell nuclei. Our results allow us to reject the view that nuclei cannot be preserved in early eukaryote fossils, offering new potential for interpreting the fossil record of early eukaryote evolution.
Early Cambrian Pseudooides prima has been described from embryonic and post-embryonic stages of development, exhibiting long germ-band development. There has been some debate about the pattern of segmentation, but this interpretation, as among the earliest records of ecdysozoans, has been generally accepted. Here, we show that the ‘germ band’ of P. prima embryos separates along its mid axis during development, with the transverse furrows between the ‘somites’ unfolding into the polar aperture of the ten-sided theca of Hexaconularia sichuanensis, conventionally interpreted as a scyphozoan cnidarian; co-occurring post-embryonic remains of ecdysozoans are unrelated. We recognize H. sichuanensis as a junior synonym of P. prima as a consequence of identifying these two form-taxa as distinct developmental stages of the same organism. Direct development in P. prima parallels the co-occuring olivooids Olivooides, and Quadrapyrgites and Bayesian phylogenetic analysis of a novel phenotype dataset indicates that, despite differences in their tetra-, penta- and pseudo-hexa-radial symmetry, these hexangulaconulariids comprise a clade of scyphozoan medusozoans, with Arthrochites and conulariids, that all exhibit direct development from embryo to thecate polyp. The affinity of hexangulaconulariids and olivooids to extant scyphozoan medusozoans indicates that the prevalence of tetraradial symmetry and indirect development are a vestige of a broader spectrum of body-plan symmetries and developmental modes that was manifest in their early Phanerozoic counterparts.
The Ediacaran Weng'an Biota (Doushantuo Formation, 609 million years 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 the 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. Maternal investment in the embryonic development of Caveasphaera and co-occuring 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. RESULTS 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, 9-12], but all remain contentious [3, 13-18]. 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. These fossils include Caveasphaera costata (Figure 1) which has been described as a spherical hollow cage (Figure 1A-C) [4] to a more solid sphere (Figure 1D) [5] of unknown nature and affinity, though superficial comparison has been drawn to embryos of an octocoral [4]. Analysis of the structure and development of Caveasphaera is challenging because of its small size and complex morphology. We employed Synchrotron Radiation X-ray Tomographic Microscopy (srXTM) [19] and High resolution Xray microtomography [20] to analyse 233 specimens of Caveasphaera that encompass its morphological and size range, based on a rich fossil assemblage from '54' and Datang quarries in the
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