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Distinguishing Biology from Geology in Soft-Tissue Preservation

Published online by Cambridge University Press:  21 July 2017

John A. Cunningham ,
Philip C. J. Donoghue  and
Stefan Bengtson
John A. Cunningham
Affiliation:
School of Earth Sciences, University of Bristol, Bristol BS8 1RJ UK Department of Paleobiology and Nordic Centre for Earth Evolution, Swedish Museum of Natural History, 10405 Stockholm, Sweden
Philip C. J. Donoghue
Affiliation:
School of Earth Sciences, University of Bristol, Bristol BS8 1RJ UK
Stefan Bengtson
Affiliation:
Department of Paleobiology and Nordic Centre for Earth Evolution, Swedish Museum of Natural History, 10405 Stockholm, Sweden
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Abstract

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.

Type
Research Article
Information
The Paleontological Society Papers , Volume 20: Reading and Writing of the Fossil Record: Preservational Pathways to Exceptional Fossilization , October 2014 , pp. 275 - 288
Copyright
Copyright © 2014 by The Paleontological Society 

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References

Bailey, J. V., Joye, S. B., Kalanetra, K. M., Flood, B. E., and Corsetti, F.A. 2007. Evidence of giant sulphur bacteria in Neoproterozoic phosphorites. Nature, 445:198–201.Google Scholar
Bengtson, S. 2003. Tracing metazoan roots in the fossil record, p. 289–300. In Legakis, A., Sfenthourakis, S., Polymeni, R., and Thessalou-Legaki, M. (eds.), The New Panorama of Animal Evolution. Proceedings of the XVIII International Congress of Zoology, Athens, Greece, September, 2000. Pensoft Publishers, Sofia, Bulgaria.Google Scholar
Bengtson, S., and Budd, G. 2004. Comment on “Small bilaterian fossils from 40 to 55 million years before the Cambrian.” Science, 306:1291a.Google Scholar
Bengtson, S., Cunningham, J. A., Yin, C., and Donoghue, P. C. J. 2012. A merciful death for the “earliest bilaterian,” Vernanimalcula . Evolution & Development, 14:421–427.Google Scholar
Benton, M. J., Donoghue, P. C. J., and Asher, R. J. 2009. Calibrating and constraining the molecular clock, p. 35–86. In Hedges, B. and Kumar, S. (eds.), Dating the Tree of Life. Oxford University Press.Google Scholar
Bergmann, U., Morton, R. W., Manning, P. L., Sellers, W. I., Farrar, S., Huntley, K. G., Wogelius, R. A., and Larson, P. 2010. Archaeopteryx feathers and bone chemistry fully revealed via synchrotron imaging. Proceedings of the National Academy of Sciences of the United States of America, 107:9060–9065.Google Scholar
Brasier, M. D., Green, O. R., Jephcoat, A. P., Kleppe, A. K., Van Kranendonk, M. J., Lindsay, J. F., Steele, A., and Grassineau, N. V. 2002. Questioning the evidence for Earth's oldest fossils. Nature, 416:76–81.Google Scholar
Briggs, D. E. G. 2003. The role of decay and mineralization in the preservation of soft-bodied fossils. Annual Review of Earth and Planetary Sciences, 31:275–301.Google Scholar
Chen, J. Y., Bottjer, D. J., Davidson, E. H., Dornbos, S. Q., Gao, X., Yang, Y. H., Li, C. W., Li, G., Wang, X. Q., Xian, D. C., Wu, H. J., Hwu, Y. K., and Tafforeau, P. 2006. Phosphatized polar lobe-forming embryos from the Precambrian of southwest China. Science, 312:1644–1646.Google Scholar
Chen, J. Y., Bottjer, D. J., Davidson, E. H., Li, G., Gao, F., Cameron, R. A., Hadfield, M. G., Xian, D. C., Tafforeau, P., Jia, Q. J., Sugiyama, H., and Tang, R. 2009a. Phase contrast synchrotron X-ray microtomography of Ediacaran (Doushantuo) metazoan microfossils: Phylogenetic diversity and evolutionary implications. Precambrian Research, 173:191–200.CrossRefGoogle Scholar
Chen, J. Y., Bottjer, D. J., Li, G., Hadfield, M. G., Gao, F., Cameron, A. R., Zhang, C. Y., Xian, D. C., Tafforeau, P., Liao, X., and Yin, Z. J. 2009b. Complex embryos displaying bilaterian characters from Precambrian Doushantuo phosphate deposits, Weng'an, Guizhou, China. Proceedings of the National Academy of Sciences of the United States of America, 106:19056–19060.Google Scholar
Chen, J. Y., Bottjer, D. J., Oliveri, P., Dornbos, S. Q., Gao, F., Ruffins, S., Chi, H., Li, C. W., and Davidson, E. H. 2004. Small bilaterian fossils from 40 to 55 million years before the Cambrian. Science, 305:218–222.Google Scholar
Chen, J. Y., Oliveri, P., Gao, F., Dornbos, S. Q., Li, C. W., Bottjer, D. J., and Davidson, E. H. 2002. Precambrian animal life: Probable developmental and adult cnidarian forms from southwest China. Developmental Biology, 248:182–196.Google Scholar
Chen, J. Y., Oliveri, P., Li, C. W., Zhou, G. Q., Gao, F., Hagadorn, J. W., Peterson, K. J., and Davidson, E. H. 2000. Precambrian animal diversity: Putative phosphatized embryos from the Doushantuo Formation of China. Proceedings of the National Academy of Sciences of the United States of America, 97:4457–4462.Google Scholar
Conway Morris, S. 1986. The community structure of the Middle Cambrian Phyllopod Bed (Burgess Shale). Palaeontology, 29:423–467.Google Scholar
Conway Morris, S. 2003. The Cambrian “explosion” of metazoans and molecular biology: would Darwin be satisified? International Journal of Developmental Biology, 47:505–515.Google Scholar
Cunningham, J. A., Thomas, C.-W., Bengtson, S., Kearns, S. L., Xiao, S., Marone, F., Stampanoni, M., and Donoghue, P. C. J. 2012. Distinguishing geology from biology in the Ediacaran Doushantuo biota relaxes constraints on the timing of the origins of bilaterians. Proceedings of the Royal Society B-Biological Sciences, 1737:2369–2376.CrossRefGoogle Scholar
Donoghue, P. C. J., Bengtson, S., Dong, X. P., Gostling, N. J., Huldtgren, T., Cunningham, J. A., Yin, C., Yue, Z., Peng, F., and Stampanoni, M. 2006. Synchrotron X-ray tomographic microscopy of fossil embryos. Nature, 442:680–683.CrossRefGoogle ScholarPubMed
Donoghue, P. C. J., and Purnell, M. A. 2009. Distinguishing heat from light in debate over controversial fossils. BioEssays, 31:178–189.Google Scholar
Edwards, N. P., Barden, H. E., van Dongen, B. E., Manning, P. L., Larson, P. L., Bergmann, U., Sellers, W. I., and Wogelius, R. A. 2011. Infrared mapping resolves soft tissue preservation in 50 million year-old reptile skin. Proceedings of the Royal Society B-Biological Sciences, 278:3209–3218.Google Scholar
Friis, E. M., Crane, P. R., Pedersen, K. R., Bengtson, S., Donoghue, P. C. J., Grimm, G. W., and Stampanoni, M. 2007. Phase-contrast X-ray microtomography links Cretaceous seeds with Gnetales and Bennettitales. Nature, 450:549–552.Google Scholar
Golden, D. C., Ming, D. W., Schwandt, C. S., Morris, R. V., Yang, S. V., and Lofgren, G. E. 2000. An experimental study on kinetically-driven precipitation of calcium-magnesium-iron carbonates from solution: Implications for the low-temperature formation of carbonates in Martian meteorite Allan Hills 84001. Meteoritics & Planetary Science, 35:457–465.CrossRefGoogle Scholar
Hagadorn, J. W., Xiao, S., Donoghue, P. C. J., Bengtson, S., Gostling, N. J., Pawlowska, M., Raff, E. C., Raff, R. A., Turner, F. R., Chongyu, Y., Zhou, C., Yuan, X., McFeely, M. B., Stampanoni, M., and Nealson, K. H. 2006. Cellular and subcellular structure of Neoproterozoic animal embryos. Science, 314:291–294.CrossRefGoogle ScholarPubMed
Huldtgren, T., Cunningham, J. A., Yin, C., Stampanoni, M., Marone, F., Donoghue, P. C. J., and Bengtson, S. 2011. Fossilized nuclei and germination structures identify Ediacaran ‘animal embryos’ as encysting protists. Science, 334:1696–1699.Google Scholar
Huldtgren, T., Cunningham, J. A., Yin, C., Stampanoni, M., Marone, F., Donoghue, P. C. J., and Bengtson, S. 2012. Response to Comment on “Fossilized nuclei and germination structures identify Ediacaran ‘animal embryos’ as encysting protists.” Science, 335:1169 Google Scholar
Kaye, T. G., Gaugler, G., and Sawlowwicz, Z. 2008. Dinosaurian soft tissues interpreted as bacterial biofilms. PLoS ONE, 3:e2808: doi:10.1371/journal.pone.0002808 Google Scholar
Lak, M., Neraudeau, D., Nel, A., Cloetens, P., Perrichot, V., and Tafforeau, P. 2008. Phase contrast X-ray synchrotron imaging: Opening access to fossil inclusions in opaque amber. Microscopy and Microanalysis, 14:251–259.CrossRefGoogle ScholarPubMed
Lindgren, J., Uvdal, P., Sjövall, P., Nilsson, D. E., Engdahl, A., Pagh Schultz, B., and Thiel, V. 2011. Molecular preservation of the pigment melanin in fossil melanosomes. Nature Communications, 3:824. doi:10.1038/ncomms1819 Google Scholar
Manning, P. L., Edwards, N. P., Wogelius, R. A., Bergmann, U., Barden, H. E., Larson, P. L., Schwarz-Wings, D., Egerton, V. M., Sokaras, D., Mori, R. A., and Sellers, W. I. 2013. Synchrotron-based chemical imaging reveals plumage patterns in a 150 million year old early bird. Journal of Analytical Atomic Spectrometry, 28:1024–1030.CrossRefGoogle Scholar
Marshall, A. O., and Marshall, C. P. 2013. Comment on “Biogenicity of Earth's earliest fossils: a resolution of the controversy” by Schopf, J. W. and Kudryavtsev, A. B., Gondwana Research, Volume 22, Issue 3–4, Pages 761–777. Gondwana Research, 23:1654–1655.Google Scholar
Martill, D. M., and Unwin, D. M. 1997. Small spheres in fossil bones: Blood corpuscles or diagenetic products? Palaeontology, 40:619–624.Google Scholar
McKay, D. S., Gibson, E. K., Thomas-Keprta, K. L., Vali, H., Romanek, C. S., Clemett, S. J., Chillier, X. D. F, Maechling, C. R., and Zare, R. N. 1996. Search for past life on Mars: Possible relic biogenic activity in Martian meteorite ALH84001. Science, 273:924–930.CrossRefGoogle ScholarPubMed
Orlando, L., Ginolhac, A., Zhang, G. J., Froese, D., Albrechtsen, A., Stiller, M., Schubert, M., Cappellini, E., Petersen, B., Moltke, I., Johnson, P. L. F., Fumagalli, M., Vilstrup, J. T., Raghavan, M., Korneliussen, T., Malaspinas, A. S., Vogt, J., Szklarczyk, D., Kelstrup, C. D., Vinther, J., Dolocan, A., Stenderup, J., Velazquez, A. M. V., Cahill, J., Rasmussen, M., Wang, X. L., Min, J. M., Zazula, G. D., Seguin-Orlando, A., Mortensen, C., Magnussen, K., Thompson, J. F., Weinstock, J., Gregersen, K., Roed, K. H., Eisenmann, V., Rubin, C. J., Miller, D. C., Antczak, D. F., Bertelsen, M. F., Brunak, S., Al-Rasheid, K. A. S., Ryder, O., Andersson, L., Mundy, J., Krogh, A., Gilbert, M. T. P., Kjaer, K., Sicheritz-Ponten, T., Jensen, L. J., Olsen, J. V., Hofreiter, M., Nielsen, R., Shapiro, B., Wang, J., and Willerslev, E. 2013. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature, 499:74–78.Google Scholar
Orr, P. J., Briggs, D. E. G., and Kearns, S. L. 1998. Cambrian Burgess Shale animals replicated in clay minerals. Science, 281:1173–1175.Google Scholar
Orr, P. J., and Kearns, S. L. 2011. X-ray microanalysis of Burgess Shale and similarly preserved fossils, p. 271–299. In Laflamme, M., Schiffbauer, J. D., and Dornbos, S. Q. (eds.), Quantifying the Evolution of Early Life. Topics in Geobiology 36, Springer, Dordrecht.Google Scholar
Orr, P. J., Kearns, S. L., and Briggs, D. E. G. 2002. Backscattered electron imaging of fossils exceptionally-preserved as organic compressions. PALAIOS, 17:110–117.2.0.CO;2>CrossRefGoogle Scholar
Petryshyn, V. A., Bottjer, D. J., Chen, J.-Y., and Gao, F. 2013. Petrographic analysis of new specimens of the putative microfossil Vernanimalcula guizhouena (Doushantuo Formation, South China). Precambrian Research, 225:58–66.CrossRefGoogle Scholar
Pevzner, P. A., Kim, S., and Ng, J. 2008. Comment on “Protein sequences from Mastodon and Tyrannosaurus rex revealed by mass spectrometry.” Science, 321:1040.CrossRefGoogle Scholar
Pinti, D. L., Mineau, R., and Clement, V. 2013. Comment on “Biogenicity of Earth's earliest fossils: a resolution of the controversy” by J. William Schopf and Anatoliy B. Kudryavtsev, Gondwana Research 22 (2012), 761–771. Gondwana Research, 23:1652–1653.Google Scholar
Raff, E. C., Schollaert, K. L., Nelson, D. E., Donoghue, P. C. J., Thomas, C. W., Turner, F. R., Stein, B. D., Dong, X., Bengtson, S., Huldtgren, T., Stampanoni, M., Yin, C. Y., and Raff, R. A. 2008. Embryo fossilization is a biological process mediated by microbial biofilms. Proceedings of the National Academy of Sciences of the United States of America, 105:19360–19365.Google Scholar
Schiffbauer, J. D., and Xiao, S. H. 2009. Novel application of Focused Ion Beam Electron Microscopy (FIB-EM) in preparation and analysis of microfossil ultrastructures: A new view of complexity in early Eukaryotic organisms. PALAIOS, 24:616–626.Google Scholar
Schiffbauer, J. D., and Xiao, S. 2011. Paleobiological applications of focused ion beam electron microscopy (FIB-EM): an ultrastructural approach to the (micro)fossil record, p. 321–354. In Laflamme, M., Schiffbauer, J. D., and Dornbos, S. Q. (eds.), Quantifying the Evolution of Early Life. Topics in Geobiology 36, Springer, Dordrecht.Google Scholar
Schiffbauer, J. D., Xiao, S. H., Sen Sharma, K., and Wang, G. 2012. The origin of intracellular structures in Ediacaran metazoan embryos. Geology, 40:223–226.Google Scholar
Schopf, J. W. 1993. Microfossils of the Early Archean Apex Chert: new evidence of the antiquity of life. Science, 260:640–646.Google Scholar
Schopf, J. W., and Kudryavtsev, A. B. 2011. Confocal laser scanning microscopy and Raman (and fluorescence) spectroscopic imagery of permineralized Cambrian and Neoproterozoic fossils, p. 241–270. In Laflamme, M., Schiffbauer, J. D., and Dornbos, S. Q. (eds.), Quantifying the Evolution of Early Life. Topics in Geobiology 36, Springer, Dordrecht.Google Scholar
Schopf, J. W., and Kudryavtsev, A. B. 2012. Biogenicity of Earth's earliest fossils: A resolution of the controversy. Gondwana Research, 22:761–771.Google Scholar
Schopf, J. W., and Kudryavtsey, A. B. 2013. Reply to the comments of D. L. Pinti, R. Mineau and V. Clement, and of A. O. Marshall and C. P. Marshall on “Biogenicity of Earth's earliest fossils: A resolution of the controversy” by William Schopf, J. and Kudryavtsev, Anatoliy B., Gondwana Research 22 (2012), 761–77. Gondwana Research, 23:1656–1658.Google Scholar
Schopf, J. W., Kudryavtsev, A. B., Agresti, D. G., Wdowiak, T. J., and Czaja, A. D. 2002. Laser-Raman imagery of Earth's earliest fossils. Nature, 416:73–76.CrossRefGoogle ScholarPubMed
Schweitzer, M. H. 2011. Soft tissue preservation in terrestrial Mesozoic vertebrates. Annual Review of Earth and Planetary Sciences, 39:187–216.Google Scholar
Schweitzer, M. H., Suo, Z., Avci, R., Asara, J. M., Allen, M. A., Arce, F. T., and Horner, J. R. 2007. Analyses of soft tissue from Tyrannosaurus rex suggest the presence of protein. Science, 316:277–280.Google Scholar
Schweitzer, M. H., Wittmeyer, J. L., Horner, J. R., and Toporski, J. K. 2005. Soft-tissue vessels and cellular preservation in Tyrannosaurus rex . Science, 307:1952–1955.Google Scholar
Scott, A. C., and Collinson, M. E. 2003. Nondestructive multiple approaches to interpret the preservation of plant fossils: implications for calcium-rich permineralizations. Journal of the Geological Society, 160:857–862.Google Scholar
Selden, P., and Nudds, J. R. 2012. Evolution of Fossil Ecosystems (Second Edition). Academic Press, London.Google Scholar
Tafforeau, P., Boistel, R., Boller, E., Bravin, A., Brunet, M., Chaimanee, Y., Cloetens, P., Feist, M., Hoszowska, J., Jaeger, J. J., Kay, R. F., Lazzari, V., Marivaux, L., Nel, A., Nemoz, C., Thibault, X., Vignaud, P., and Zabler, S. 2006. Applications of X-ray synchrotron microtomography for non-destructive 3D studies of paleontological specimens. Applied Physics A-Materials Science & Processing, 83:195–202.Google Scholar
Taylor, P. D., Kudryavtsev, A. B., and Schopf, J. W. 2008. Calcite and aragonite distributions in the skeletons of bimineralic bryozoans as revealed by Raman spectroscopy. Invertebrate Biology, 127:87–97.Google Scholar
Thomas, D. B., McGoverin, C. M., Fordyce, R. E., Frew, R. D., and Gordon, K. C. 2011. Raman spectroscopy of fossil bioapatite—A proxy for diagenetic alteration of the oxygen isotope composition. Palaeogeography, Palaeoclimatology, Palaeoecology, 310:62–70.Google Scholar
Wacey, D., Gleeson, D., and Kilburn, M. R. 2010. Microbialite taphonomy and biogenicity: new insights from NanoSIMS. Geobiology, 8:403–416.Google Scholar
Wacey, D., Menon, S., Green, L., Gerstmann, D., Kong, C., McLoughlin, N., Saunders, M., and Brasier, M. 2012. Taphonomy of very ancient microfossils from the ∼3400 Ma Strelley Pool Formation and ∼1900 Ma Gunflint Formation: New insights using a focused ion beam. Precambrian Research, 220:234–250.Google Scholar
Xiao, S. H., Knoll, A. H., Schiffbauer, J. D., Zhou, C. M., and Yuan, X. L. 2012. Comment on “Fossilized nuclei and germination structures identify Ediacaran ‘animal embryos’ as encysting protists.” Science, 335:1169.Google Scholar
Xiao, S. H., Schiffbauer, J. D., McFadden, K. A., and Hunter, J. 2010. Petrographic and SIMS pyrite sulfur isotope analyses of Ediacaran chert nodules: Implications for microbial processes in pyrite rim formation, silicification, and exceptional fossil preservation. Earth and Planetary Science Letters, 297:481–495.Google Scholar
Xiao, S. H., Yuan, X. L., and Knoll, A. H. 2000. Eumetazoan fossils in terminal Proterozoic phosphorites? Proceedings of the National Academy of Sciences of the United States of America, 97:13684–13689.Google Scholar
Xiao, S. H., Zhang, Y., and Knoll, A. H. 1998. Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite. Nature, 391:553–558.Google Scholar
Yin, Z., Zhu, M., Tafforeau, P., Chen, J.-Y., Liu, P., and Li, G. 2013. Early embryogenesis of potential bilaterian animals with polar lobe formation from the Ediacaran Weng'an Biota, South China. Precambrian Research, 225:44–57.Google Scholar