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  • 1. Butler, Aodhán
    et al.
    Cunningham, John
    Swedish Museum of Natural History, Department of Paleobiology.
    Budd, Graham
    Donoghue, Philip
    Experimental taphonomy of Artemia reveals the role of endogenous microbes in mediating decay and fossilization2015In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 282, p. 20150476-Article in journal (Refereed)
    Abstract [en]

    Exceptionally preserved fossils provide major insights into the evolutionary

    history of life. Microbial activity is thought to play a pivotal role in both the

    decay of organisms and the preservation of soft tissue in the fossil record,

    though this has been the subject of very little experimental investigation.

    To remedy this, we undertook an experimental study of the decay of the

    brine shrimp Artemia, examining the roles of autolysis, microbial activity,

    oxygen diffusion and reducing conditions. Our findings indicate that

    endogenous gut bacteria are the main factor controlling decay. Following

    gut wall rupture, but prior to cuticle failure, gut-derived microbes spread

    into the body cavity, consuming tissues and forming biofilms capable of

    mediating authigenic mineralization, that pseudomorph tissues and structures

    such as limbs and the haemocoel. These observations explain patterns

    observed in exceptionally preserved fossil arthropods. For example, guts

    are preserved relatively frequently, while preservation of other internal anatomy

    is rare. They also suggest that gut-derived microbes play a key role in the

    preservation of internal anatomy and that differential preservation between

    exceptional deposits might be because of factors that control autolysis and

    microbial activity. The findings also suggest that the evolution of a through

    gut and its bacterial microflora increased the potential for exceptional fossil

    preservation in bilaterians, providing one explanation for the extreme rarity

    of internal preservation in those animals that lack a through gut.

  • 2.
    Cunningham, John A.
    et al.
    Swedish Museum of Natural History, Department of Paleobiology. University of Bristol.
    Liu, Alexander G.
    University of Cambridge.
    Bengtson, Stefan
    Swedish Museum of Natural History, Department of Paleobiology.
    Donoghue, Philip C.J.
    University of Bristol.
    The origin of animals: Can molecular clocks and the fossil record be reconciled?2016In: Bioessays, ISSN 0265-9247, E-ISSN 1521-1878, Vol. 38, p. 1-12Article in journal (Refereed)
    Abstract [en]

    The evolutionary emergence of animals is one of the most significant episodes in the history of life, but its timing remains poorly constrained. Molecular clocks estimate that animals originated and began diversifying over 100 million years before the first definitive metazoan fossil evidence in the Cambrian. However, closer inspection reveals that clock estimates and the fossil record are less divergent than is often claimed. Modern clock analyses do not predict the presence of the crown-representatives of most animal phyla in the Neoproterozoic. Furthermore, despite challenges provided by incomplete preservation, a paucity of phylogenetically informative characters, and uncertain expectations of the anatomy of early animals, a number of Neoproterozoic fossils can reasonably be interpreted as metazoans. A considerable discrepancy remains, but much of this can be explained by the limited preservation potential of early metazoans and the difficulties associated with their identificationin the fossil record. Critical assessment of both recordsmay permitbetter resolutionof the tempo and mode of early animal evolution.

  • 3.
    Cunningham, John
    et al.
    Swedish Museum of Natural History, Department of Paleobiology.
    Donoghue, Philip C.J.
    University of Bristol.
    Bengtson, Stefan
    Swedish Museum of Natural History, Department of Paleobiology.
    Distinguishing biology from geology in soft-tissue preservation.2014In: Reading and Writing of the Fossil Record: Preservational Pathways to Exceptional Fossilization / [ed] Marc Laflamme, James D. Schiffbauer, Simon A. F. Darroch, The Paleontological Society , 2014, p. 275-287Chapter in book (Refereed)
    Abstract [en]

    Knowledge of evolutionary history is based extensively on relatively rare fossils that preserve soft tissues. These fossils record a much greater proportion of anatomy than would be known solely from mineralized remains and provide key data for testing evolutionary hypotheses in deep time. Ironically, however, exceptionally preserved fossils are often among the most contentious because they are difficult to interpret. This is because their morphology has invariably been affected by the processes of decay and diagenesis, meaning that it is often difficult to distinguish preserved biology from artifacts introduced by these processes. Here we describe how a range of analytical techniques can be used to tease apart mineralization that preserves biological structures from unrelated geological mineralization phases. This approach involves using a series of X-ray, ion, electron and laser beam techniques to characterize the texture and chemistry of the different phases so that they can be differentiated in material that is difficult to interpret. This approach is demonstrated using a case study of its application to the study of fossils from the Ediacaran Doushantuo Biota.

  • 4.
    Cunningham, John
    et al.
    Swedish Museum of Natural History, Department of Paleobiology.
    Vargas, Kelly
    Liu, Pengju
    Belivanova, Veneta
    Swedish Museum of Natural History, Department of Paleobiology.
    Marone, Federica
    Martínez-Pérez, Carlos
    Guizar-Sicairos, Manuel
    Holler, Mirko
    Bengtson, Stefan
    Swedish Museum of Natural History, Department of Paleobiology.
    Donoghue, Philip C.J.
    Critical appraisal of tubular putative eumetazoans from the Ediacaran Weng’an Doushantuo biota2015In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 282, p. 1-9, article id 2151169Article in journal (Refereed)
    Abstract [en]

    Molecular clock analyses estimate that crown-group animals began diversifying hundreds of millions of years before the start of the Cambrian period. However, the fossil record has not yielded unequivocal evidence for animals during this interval. Some of the most promising candidates for Precambrian animals occur in theWeng’an biota of South China, including a suite of tubular fossils assigned to Sinocyclocyclicus, Ramitubus, Crassitubus and Quadratitubus, that have been interpreted as soft-bodied eumetazoans comparable to tabulate corals. Here, we present new insights into the anatomy, original composition and phylogenetic affinities of these taxa based on data from synchrotron radiation X-ray tomographic microscopy, ptychographic nanotomography, scanning electron microscopy and electron probe microanalysis. The patterns of deformation observed suggest that the cross walls of Sinocyclocyclicus and Quadratitubus were more rigid than those of Ramitubus and Crassitubus. Ramitubus and Crassitubus specimens preserve enigmatic cellular clusters at terminal positions in the tubes. Specimens of Sinocyclocyclicus and Ramitubus have biological features that might be cellular tissue or subcellular structures filling the spaces between the crosswalls. These observations are incompatible with a cnidarian interpretation, in which the spaces between cross walls are abandoned parts of the former living positions of the polyp. The affinity of the Weng’an tubular fossils may lie within the algae.

  • 5.
    Dong, Xi-ping
    et al.
    Peking University.
    Vargas, Kelly
    University of Bristol.
    Cunningham, John
    Swedish Museum of Natural History, Department of Paleobiology. University of Bristol.
    Zhang, Huaqiao
    Nanjing Institute of Geology and Palaeontology.
    Liu, Teng
    Peking University.
    Chen, Fang
    Peking University.
    Liu, Jianbo
    Peking University.
    Bengtson, Stefan
    Swedish Museum of Natural History, Department of Paleobiology.
    Donoghue, Philip C.J.
    Developmental biology of the early Cambrian cnidarian Olivooides.2016In: Palaeontology, ISSN 0031-0239, E-ISSN 1475-4983, Vol. 59, no 3, p. 387-407Article in journal (Refereed)
    Abstract [en]

    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.

  • 6. Donoghue, Philip C.J.
    et al.
    Cunningham, John
    Swedish Museum of Natural History, Department of Paleobiology.
    Dong, Xi-ping
    Peking University.
    Bengtson, Stefan
    Swedish Museum of Natural History, Department of Paleobiology.
    Embryology in deep time.2015In: Evolutionary Developmental Biology of Invertebrates 1 / [ed] Wanninger, Andreas, Wien: Springer Science+Business Media B.V., 2015, p. 45-63Chapter in book (Refereed)
    Abstract [en]

    For anyone who has cared for animal embryos, it beggars belief that these squishy cellular aggregates could be fossilised. Hence, with hindsight, it is possible to empathise with palaeontologists who found such fossils and, in their naming of Olivooides, Pseudooides, etc., drew attention to their likeness to animal eggs and embryos but without going so far as to propose such an interpretation. However, in 1994, Zhang Xi-guang and Brian Pratt described microscopic balls of calcium phosphate from Cambrian rocks of China, one or two of which preserved polygonal borders that resembled blastomeres on the surface of an early cleaving animal embryo. In retrospect, these fossils are far from remarkable, some of them may not be fossils at all, and it is not as if anyone ever conceived Cambrian animals as having lacked an embryology. But Zhang Xi-guang and Brian Pratt dared the scientific world, not least their fellow palaeontologists, to believe that the fragile embryonic stages of invertebrate animals could be fossilised, that there was a fossil record of animal embryology, that this record hailed from the interval of time in which animal body plans were first established, and that it had been awaiting discovery in the rocks, for want of looking. The proof of this concept came a few years later, when phosphatised Cambrian fossils from China and Siberia were shown to display indisputable features of animal embryonic morphologies. In the case of Olivooides, a series of developmental stages from cleavage to morphogenesis through hatching and juvenile growth could be tentatively identified; in Markuelia, the coiled-up body of an annulated worm-like animal could be clearly seen within its fertilisation envelope.

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