Taphonomy And Biology Of Problematic Fossils From The Ediacaran Weng’an Biota

The Weng’an biota from the early Ediacaran Doushantuo Formation(Guizhou Province,Southwest China)encompasses an assemblage of phosphatic microfossils that have exquisitely preserved to cellular and subcellular levels of fidelity.Among the fossil assemblage,which includes diverse multicellular algae,occur the remains of animal embryo-like organisms,preserving a record of development.As such,these fossils have the potential to inform on the origin and evolution of animal development.However,the phylogenetic affinities of the embryo-like fossils are controversial.The main competing hypotheses for their biological interpretation are crown group animals,stem group animals,or the single-celled relatives of animals.Interpretation of the fossils is controversial because of the challenging of discriminating between different developmental stages of the same organism versus different developmental stages of different organisms.It is likely that in either instance,the developmental sequence of the fossil organisms is incompletely preserved.Furthermore,the preserved anatomy of the fossils is difficult to distinguish from later diagenetic mineralization.To make progress,it is necessary to establish the taphonomic pathways through which these organisms were fossilized.To resolve these key issues,we undertook synchrotron radiation x-ray tomographic microscopy,X-ray microscopic tomography,scanning electron microscopy transmission electron microscopy to characterize the micro-and ultra-structure of the embryo-like fossils.We also employed elemental mapping and confocal Raman spectroscopy to characterize the in-situ chemistry of the fossils.On this basis,we have reconstructed the taphonomic pathway of subcellular structures in the embryo-like fossils and reinterpreted the biological affinity of these and other problematic fossils(including associated micro tubular fossils).The conclusions are as follows:(1)The nuclei of the embryo-like fossils exhibit diverse preservational modes that differ in shape,presence or absence of an inner body and the chemistry of the associated mineralization.The fossil and experimental evidence may be rationalized by a single taphonomic pathway of selective mineralization of the cell cytoplasm,preserving an external mould of the nucleus that is itself resistant to both decay and mineral replication.(2)Subcellular granules that occur in the embryo-like fossils exhibit a diversity of sizes,shapes,and mineral components,but they fall into two broad groupings.The first type are spheroidal granules which occur in embryo-like fossils with equal cell division pattern.The second type are polygonal and irregular granules that occur in embryo-like fossils with an unequal and asynchronous cell division pattern.The subcellular granules exhibit a similar taphonomic pathway and mechanism of mineralization to the nuclei.We interpret these subcellular granules as fossilized lipid or yolk granules,based on their size,morphology,distribution,and number within the cell.In addition,the correlation between subcellular granule types and cell division patterns also suggests that the Weng’an embryo-like fossils may be more taxonomically diverse than conventionally thought.(3)The four taxa of tubular fossils from the Weng’an biota were not biomineralized,as has previously been thought.Crassitubulus,Quadratitubus,and Sinocyclocylcicus,may be grouped on the basis that they exhibit alternating complete and incomplete cross walls,and bipolar growth;this makes them comparable to filamentous cyanobacteria.In contrast,Ramitubulus exhibits only complete cross walls,unipolar growth and dichotomous branching.These features are difficult to reconcile with a cyanobacterial interpretation.They are,instead,more comparable to the Cambrian multicellular alga-like Epiphyton.Thus,the Weng’an tubular microfossils constitute a disparate assemblage of cyanobacteria and algae,but none of these fossils can be interpreted as animals.(4)We found Helicoforamina developed through one-,four-,and eight-cell stages,to hundreds and thousands of cells,followed by apoptosis to form branching cell masses.Our results preclude the affinities between Helicoforamina,Spiralicellula and Sinocyclocylcicus,and proved that it is not a unicellular protist or green alga.We interpret Helicoforamina as a holozoa,but with a more complex envelope structure and developmental processes than the unicellular relatives of animals.(5)We provide a systematic description of the biological structure of Spiralicellula,finding a single-layered outer envelope with no more than 32 internal cells.There is no correlation between the extent of development of the eponymous spiral and the number of component cells.We regarded the Spiralicellula as an independent taxon;there is no evidence supporting a developmental relationship with Megasphaera or Helicoforamina,as has been proposed previously.We interpret Spiralicellula as holozoa based on its general similarity in development and structure,to Megasphaera and Helicoforamina.Spiralicellula may represent a unicellular relative of animals similar to Ichthyosporeans.(6)We found a new species of embryo-like fossil,Ostiosphaera,from the Ediacaran Weng’an Biota.These specimens exhibit a spherical morphology,a thick ornamented envelope with a circular opening and a membrane-bound,multicellular,inner body.We assume a holozoa affinity for these fossils because they share the same grade of complexity with co-occurring embryo-like fossils.Ostiosphaera resembles asexual reproductive gemmules of fossil and living demosponges,in terms of size,morphology,circular opening,and cellular anatomy.