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Synchrotron X-ray tomographic microscopy of fossil embryos

Abstract

Fossilized embryos from the late Neoproterozoic and earliest Phanerozoic have caused much excitement because they preserve the earliest stages of embryology of animals that represent the initial diversification of metazoans1,2,3,4. However, the potential of this material has not been fully realized because of reliance on traditional, non-destructive methods that allow analysis of exposed surfaces only1,2,3,4, and destructive methods that preserve only a single two-dimensional view of the interior of the specimen5,6. Here, we have applied synchrotron-radiation X-ray tomographic microscopy (SRXTM)7, obtaining complete three-dimensional recordings at submicrometre resolution. The embryos are preserved by early diagenetic impregnation and encrustation with calcium phosphate, and differences in X-ray attenuation provide information about the distribution of these two diagenetic phases. Three-dimensional visualization of blastomere arrangement and diagenetic cement in cleavage embryos resolves outstanding questions about their nature, including the identity of the columnar blastomeres. The anterior and posterior anatomy of embryos of the bilaterian worm-like Markuelia confirms its position as a scalidophoran, providing new insights into body-plan assembly among constituent phyla. The structure of the developing germ band in another bilaterian, Pseudooides, indicates a unique mode of germ-band development. SRXTM provides a method of non-invasive analysis that rivals the resolution achieved even by destructive methods, probing the very limits of fossilization and providing insight into embryology during the emergence of metazoan phyla.

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Figure 1: Tomographic reconstructions of cleavage-stage embryos from the Lower Cambrian Kuanchuanpu Formation, Shizhonggou section, Kuanchuanpu, Ningqiang County, Shaanxi Province, Southern China.
Figure 2: The scalidophoran Markuelia from the Cambrian of China and Siberia.
Figure 3: Germ-band embryos of Pseudooides prima , same locality as for Fig. 1.

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Acknowledgements

We thank W. Guo for field assistance, and A. Groso for her support at the beamline, and K. Robson-Brown for her assistance in running the experiments. This work was funded by the Swiss Light Source (P.C.J.D. and S.B.), European Union FP6, as well as grants from the Natural Environment Research Council (P.C.J.D.), the Swedish Research Council (S.B.), Bristol University and the National Natural Science Foundation of China (X.-p.D.).

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Correspondence to Philip C. J. Donoghue.

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Supplementary information

Supplementary Notes

This file contains the Supplementary Figure Legends, Supplementary Methods. This file also contains additional figures and references. (DOC 154 kb)

Supplementary Figures

These are tomographic reconstructions of the divisions between compartments of blastoderm (dark infill) in the putative germ band of Pseudooides (MESIG 20064), and marginal furrow (light infill); 1 external view; 2 internal view provided by virtual sectioning away the opposite hemisphere of the embryo thus showing the division of the germ band penetrating to depth but not fully enclosing the compartments. (PDF 135 kb)

GMPKU_2011

Reconstructed slice data from SRXTM analysis of an embryo of Markuelia hunanensis from the Late Cambrian Bitiao Formation of Wangcun, Hunan, China. These data were used to produce the rendered tomographic models in Figure 2g-h (MOV 1150 kb)

GMPKU_2204

Reconstructed slice data from SRXTM analysis of a cleavage embryo from the Lower Cambrian Kuanchuanpu Formation of Shaanxi Province, China. These data were used to produce the rendered tomographic models in Figure 1e-g. (MOV 1139 kb)

GMPKU_2205

Reconstructed slice data from SRXTM analysis of an embryo of Markuelia hunanensis from the Late Cambrian Bitiao Formation of Wangcun, Hunan, China. These data were used to produce the rendered tomographic models in Figure 2a-f. (MOV 1135 kb)

MESIG_20061

Reconstructed slice data from SRXTM analysis of a cleavage embryo from the Lower Cambrian Kuanchuanpu Formation of Shaanxi Province, China. These data were used to produce the rendered tomographic models in Figure 1a-b. (MOV 1125 kb)

MESIG_20062

Reconstructed slice data from SRXTM analysis of a cleavage embryo from the Lower Cambrian Kuanchuanpu Formation of Shaanxi Province, China. These data were used to produce the rendered tomographic models in Figure 1c-d. (MOV 1149 kb)

MESIG_20063

Reconstructed slice data from SRXTM analysis of an embryo of Pseudooides prima from the Lower Cambrian Kuanchuanpu Formation of Shaanxi Province, China. These data were used to produce the rendered tomographic models in Figure 3. (MOV 1173 kb)

MESIG_20064

Reconstructed slice data from SRXTM analysis of an embryo of Pseudooides prima from the Lower Cambrian Kuanchuanpu Formation of Shaanxi Province, China. These data were used to produce the rendered tomographic models in Supplementary Figures 1 and 2. (MOV 1181 kb)

MESIG_20065

Reconstructed slice data from SRXTM analysis of an embryo of Pseudooides prima from the Lower Cambrian Kuanchuanpu Formation of Shaanxi Province, China. These data were used to produce the rendered tomographic models in Figure 3. (MOV 1248 kb)

SMNH_X2240

Reconstructed slice data from SRXTM analysis of an embryo of Markuelia secunda from the Lower Cambrian Pestrotsvet Formation, Dvortsy, Aldan River, Siberia. These data were used to produce the rendered tomographic models in Figure 2i-j. (MOV 1175 kb)

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Donoghue, P., Bengtson, S., Dong, Xp. et al. Synchrotron X-ray tomographic microscopy of fossil embryos. Nature 442, 680–683 (2006). https://doi.org/10.1038/nature04890

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