Decoding the fossil record of embryology at the dawn of animal evolution

Lead Research Organisation: University of Bristol
Department Name: Earth Sciences

Abstract

Embryology, the study of development, is pivotal to unravelling the evolutionary history of animals, and how changes to patterns of development have produced the branching events in the Tree of Life. Palaeontology can provide the only direct tests of such hypotheses but, traditionally, it has been silent in such debates because of a dearth of embryological data preserved in the fossil record. The outlook for evolutionary biology and for palaeontology was changed at once with the discovery of rich and diverse assemblages of fossil embryos in rocks deposited at the time that major animal groups were first emerging. These fossils have a huge potential for understanding developmental evolution at this critical episode of evolutionary history, but it is largely unrealised because of difficulties in distinguishing preserved biological structure from later geological mineralization, and because it is difficult to understand the 3D anatomy of an individual fossil embryo let alone the changes that took place during development from one embryological stage to another. These challenges have led to wildly differing interpretations of which animal group the fossil embryos belong to - a debate that must be concluded before evolutionary conclusions can be made. In fact the situation is so bad that although the fossil embryos are often beautifully preserved, including cellular and sub-cellular details, some scientists even doubt they belong to animals, preferring instead to interpret them as giant bacteria. Our interpretation of the fossils will be aided by analysis using a high resolution version of a medical CT scanner, which is powered by a particle accelerator and allows us to analyse the 3D anatomy of a fossil embryo, including its internal structure, based on a virtual computer model. This allows us to analyse details of an embryo's anatomy that are less than a millionth of a millimetre, revealing details of cell movements and even sub-cellular structure that are necessary to determine the embryology, affinity and, ultimately, the evolutionary importance of these half billion year old fossils. Our CT scans also reveal differences in the chemical composition of preserved biological and geological structures, aiding the interpretation of the fossils. We will determine the basis of these chemical differences and use the results to judge between conflicting interpretations of controversial fossil embryos and adults from the same geological layers. These experiments will be conducted to better understand known fossil embryos, but also to uncover the anatomy of fossil embryos and larvae that are completely new to science, in the collections of our international team which includes almost every leading scientist in the field of fossil embryos. We will also undertake rotting experiments to understand the decay of (i) giant bacteria and, (ii) the subcellular structures in animal embryos. These data will be used to guide our interpretation of the biological structure in the fossils, allowing us to decide whether the bacteria or animal-embryo model of interpretation fits best. Ultimately, our aim is to uncover the embryology of fossil embryos as a way of working out their closest living relatives, and whether the pattern of embryology has evolved between the fossil embryos and their living relatives. Collectively, these answers will reveal the role of embryological evolution in one of the most fundamental and most-debated episodes in animal evolutionary history: the establishment of the modern animal groups that we see about us today.

Publications

10 25 50
publication icon
Bengtson S (2012) A merciful death for the "earliest bilaterian," Vernanimalcula. in Evolution & development

publication icon
Cunningham JA (2017) The origin of animals: Can molecular clocks and the fossil record be reconciled? in BioEssays : news and reviews in molecular, cellular and developmental biology

 
Description Fossil embryos are a new class of fossils that have the potential to provide fundamental new insights into the pattern and processes underpinning the emergence of animal bodyplans in the Neoproterozoic and Cambrian. However, realising this potential requires an understanding of the processes that lead to the fossilization of animal embryos, a means of discriminating mineral replication of biological structure from later diagenetic mineralization of no biological significance, resolution of phylogenetic affinities in this light, and the reconstruction of meaningful patterns of embryology. We have sought to meet these challenges:



1. Established a new protocol to characterise chemically and physically the different phases of mineralization that replicate biological structure versus infill voids left after biological structures have rotted away. We applied this to the Neoproterozoic Doushantuo fossil deposit and discriminated among competing interpretations of phylogenetic affinity.



2. We tested the hypothesis that the Doushantuo fossils represented giant sulphur reducing bacteria through experimental taphonomy, showing ultimately that the fossils are compatible with animal embryos but not sulphur reducing bacteria.



3. We elucidated the later embryological stages of the Doushantuo fossils, revealing stages that are entirely incompatible with the prevailing interpretation that they represent animal embryos. Rather, we conclude that they represent encysting protists, perhaps akin to the mseomycetozoans, not animal relatives of animals.



4. We analysed and refuted claims of a minute bilaterian, Vernanimalcula, in the Doushantuo deposit.



5. We elucidated the embryology of Olivooides and arbitrated among competing interpretations of its phylogenetic affinity.
Exploitation Route none obvious These outcomes were exploited through academic publication, presentation to public and academic audiences at meetings, conferences, etc.
Sectors Education,Culture/ Heritage/ Museums and Collections

 
Description Swiss Light Source, non PX Beamlines
Amount SFr. 448,000 (CHF)
Organisation Paul Scherrer Institute 
Sector Public
Country Switzerland
Start 01/2015 
End 07/2016
 
Title Tomographic data of tubular fossils from the Ediacaran Weng'an Doushantuo biota 
Description X-ray tomographic data of tubular fossils from the Ediacaran Weng'an Doushantuo biota. Data collected to examine internal anatomy of these fossils, which have previously been interpreted as animals similar to tabulate corals. 
Type Of Material Database/Collection of data 
Year Produced 2015 
Provided To Others? Yes  
 
Title Tomographic data on the developmental biology of the Early Cambrian cnidarian Olivooides 
Description Three dimensional micro-CT and SRXTM data of various specimens of Olivooides including tomographic slices, segmentation data and 3D models 
Type Of Material Database/Collection of data 
Year Produced 2016 
Provided To Others? Yes