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Abstract

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.

Chapter vignette artwork by Brigitte Baldrian. © Brigitte Baldrian and Andreas Wanninger.

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References

  • Bailey JV, Joye SB, Kalanetra KM, Flood BE, Corsetti FA (2007a) Evidence of giant sulfur bacteria in Neoproterozoic phosphorites. Nature 445:198–201

    Article  CAS  PubMed  Google Scholar 

  • Bailey JV, Joye SB, Kalanetra KM, Flood BE, Corsetti FA (2007b) Palaeontology – undressing and redressing ediacaran embryos – reply. Nature 446:E10–E11

    Article  CAS  Google Scholar 

  • Bengtson S (2003) Tracing metazoan roots in the fossil record. In: Legakis A, Sfenthourakis S, Polymeni R, Thessalou-Legaki M (eds) The new panorama of animal evolution. Pensoft, Moscow, pp 289–300

    Google Scholar 

  • Bengtson S (2005) Mineralized skeletons and early animal evolution. In: Briggs DEG (ed) Evolving form and function: fossils and development. Yale Peabody Museum, New Haven, pp 101–124

    Google Scholar 

  • Bengtson S, Budd G (2004) Comment on “Small Bilaterian Fossils from 40 to 55 Million Years Before the Cambrian”. Science 306:1291a

    Article  Google Scholar 

  • Bengtson S, Yue Z (1997) Fossilized metazoan embryos from the earliest Cambrian. Science 277:1645–1648

    Article  Google Scholar 

  • Briggs DEG (2003) The role of decay and mineralization in the preservation of soft-bodied fossils. Annu Rev Earth Planet Sci 31:275–301

    Article  CAS  Google Scholar 

  • Briggs DEG, Kear AJ, Martill DM, Wilby PR (1993) Phosphatization of soft-tissue in experiments and fossils. J Geol Soc Lond 150:1035–1038

    Article  Google Scholar 

  • Broce J, Schiffbauer JD, Sharma KS, Wang G, Xiao S (2014) Possible animal embryos from the Lower Cambrian (stage 3) Shuijingtuo Formation, Hubei Province, South China. J Paleontol 88:385–394

    Article  Google Scholar 

  • Butterfield NJ (2011) Terminal developments in Ediacaran embryology. Science 334:1655–1656

    Article  CAS  PubMed  Google Scholar 

  • Chen JY (2004) The dawn of animal world. Jiangsu Science and Technology Press, China

    Google Scholar 

  • Chen JY, Chi HM (2005) Precambrian phosphatized embryos and larvae from the Doushantuo Formation and their affinities, Guizhou (SW China). Chin Sci Bull 50:2193–2200

    Article  Google Scholar 

  • Chen J, Oliveri P, Li C-W, Zhou G-Q, Gao F, Hagadorn JW, Peterson KJ, Davidson EH (2000) Precambrian animal diversity: putative phosphatised embryos from the Doushantuo Formation of China. Proc Natl Acad Sci U S A 97:4457–4462

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen J, Oliveri P, Gao F, Dornbos SQ, Li CW, Bottjer DJ, Davidson EH (2002) Precambrian animal life: probable developmental and adult cnidarian forms from Southwest China. Dev Biol 248:182–196

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Braun A, Waloszek D, Peng Q-Q, Maas A (2004) Lower Cambrian yolk-pyramid embryos from southern Shaanxi, China. Prog Nat Sci 14:167–172

    Article  Google Scholar 

  • Chen JY, Bottjer DJ, Davidson EH, Dornbos SQ, Gao X, Yang YH, Li CW, Li G, Wang XQ, Xian DC, Wu HJ, Hwu YK, Tafforeau P (2006) Phosphatized polar lobe-forming embryos from the Precambrian of Southwest China. Science 312:1644–1646

    Article  CAS  PubMed  Google Scholar 

  • Chen J-Y, Schopf JW, Bottjer DJ, Zhang C-Y, Kudryavtsev AB, Tripathi AB, Wang X-Q, Yang Y-H, Gao X, Yang Y (2007) Raman spectra of a Lower Cambrian ctenophore embryo from southwestern Shaanxi, China. Proc Natl Acad Sci 104:6289–6292

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen J-Y, Bottjer DJ, Davidson EH, Li G, Gao F, Cameron RA, Hadfield MG, Xian D-C, Tafforeau P, Jia Q-J, Sugiyama H, Tang R (2009a) Phase contrast synchrotron X-ray microtomography of Ediacaran (Doushantuo) metazoan microfossils: phylogenetic diversity and evolutionary implications. Precambrian Res 173:191–200

    Article  CAS  Google Scholar 

  • Chen J-Y, Bottjer DJ, Li G, Hadfield MG, Gao F, Cameron AR, Zhang C-Y, Xian D-C, Tafforeau P, Liao X, Yin Z-J (2009b) Complex embryos displaying bilaterian characters from Precambrian Doushantuo phosphate deposits, Weng’an, Guizhou, China. Proc Natl Acad Sci U S A 106:19056–19060

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Conway Morris S (1998) Eggs and embryos from the Cambrian. BioEssays 20:676–682

    Article  Google Scholar 

  • Conway Morris S, Chen M (1992) Carinachitids, Hexangulaconulariids, and Punctatus: problematic metazoans from the Early Cambrian of South China. J Paleontol 66:384–406

    Google Scholar 

  • Cunningham JA (2012) Fossil focus: animal embryos. Palaeontology 2:1–4 (Online)

    Google Scholar 

  • Cunningham JA, Thomas C-W, Bengtson S, Kearns SL, Xiao S, Marone F, Stampanoni M, Donoghue PCJ (2012a) Distinguishing geology from biology in the Ediacaran Doushantuo biota relaxes constraints on the timing of the origin of bilaterians. Proc R Soc B Biol Sci 279:2369–2376

    Article  Google Scholar 

  • Cunningham JA, Thomas C-W, Bengtson S, Marone F, Stampanoni M, Turner FR, Bailey JV, Raff RA, Raff EC, Donoghue PCJ (2012b) Experimental taphonomy of giant sulphur bacteria: implications for the interpretation of the embryo-like Ediacaran Doushantuo fossils. Proc R Soc B Biol Sci 279:1857–1864

    Article  CAS  Google Scholar 

  • Cunningham JA, Donoghue PCJ, Bengtson S (2014) Distinguishing biology from geology in soft tissue preservation. In: Laflamme M, Schiffbauer JD, Darroch SAF (eds.), Reading and writing of the fossil record: preservational pathways to exceptional fossilization. Paleontol Soc 20: 275–287.

    Google Scholar 

  • Dong X-P (2007) Developmental sequence of the Cambrian embryo Markuelia. Chin Sci Bull 52:929–935

    Article  Google Scholar 

  • Dong X-P, Donoghue PCJ, Cheng H, Liu J (2004) Fossil embryos from the Middle and Late Cambrian period of Hunan, south China. Nature 427:237–240

    Article  CAS  PubMed  Google Scholar 

  • Dong X-P, Donoghue PCJ, Cunningham J, Liu J, Cheng H (2005) The anatomy, affinity and phylogenetic significance of Markuelia. Evol Dev 7:468–482

    Article  PubMed  Google Scholar 

  • Dong X-P, Bengtson S, Gostling NJ, Cunningham JA, Harvey THP, Kouchinsky A, Val’kov AK, Repetski JE, Stampanoni M, Donoghue PCJ (2010) The anatomy, taphonomy, taxonomy and systematic affinity of Markuelia: early Cambrian to early Ordovician scalidophorans. Palaeontology 53:1291–1314

    Article  Google Scholar 

  • Dong X-P, Cunningham JA, Bengtson S, Thomas CW, Liu J, Stampanoni M, Donoghue PCJ (2013) Embryos, polyps and medusae of the Early Cambrian scyphozoan Olivooides. Proc Biol Sci Royal Soc 280:20130071

    Article  Google Scholar 

  • Donoghue PCJ (2007) Palaeontology: embryonic identity crisis. Nature 445:155–156

    Article  CAS  PubMed  Google Scholar 

  • Donoghue PCJ, Dong X-P (2005) Embryos and ancestors. In: Briggs DEG (ed) Evolving form and function: fossils and development. Yale Peabody Museum of Natural History, Yale University, New Haven, pp 81–99

    Google Scholar 

  • Donoghue PCJ, Purnell MA (2009) Distinguishing heat from light in debate over controversial fossils. BioEssays 31:178–189

    Article  PubMed  Google Scholar 

  • Donoghue PCJ, Forey PL, Aldridge RJ (2000) Conodont affinity and chordate phylogeny. Biol Rev 75:191–251

    Article  CAS  PubMed  Google Scholar 

  • Donoghue PCJ, Bengtson S, Dong X-P, Gostling NJ, Huldtgren T, Cunningham JA, Yin C, Yue Z, Peng F, Stampanoni M (2006a) Synchrotron X-ray tomographic microscopy of fossil embryos. Nature 442:680–683

    Article  CAS  PubMed  Google Scholar 

  • Donoghue PCJ, Kouchinsky A, Waloszek D, Bengtson S, Dong X-P, Val’kov AK, Cunningham JA, Repetski JE (2006b) Fossilized embryos are widespread but the record is temporally and taxonomically biased. Evol Dev 8:232–238

    Article  PubMed  Google Scholar 

  • Duan B, Dong X-P, Donoghue PCJ (2012) New palaeoscolecid worms from the Furongian (upper Cambrian) of Hunan, South China: is Markuelia an embryonic palaeoscolecid? Palaeontology 55:613–622

    Article  Google Scholar 

  • Gostling NJ, Thomas C-W, Greenwood JM, Dong X-P, Bengtson S, Raff EC, Raff RA, Degnan BM, Stampanoni M, Donoghue PCJ (2008) Deciphering the fossil record of early bilaterian embryonic development in light of experimental taphonomy. Evol Dev 10:339–349

    Article  PubMed  Google Scholar 

  • Gostling NJ, Dong X-P, Donoghue PCJ (2009) Ontogeny and taphonomy: and experimental taphonomy study of the development of the brine shrimp Artemia salina. Palaeontology 52:169–186

    Article  Google Scholar 

  • Hagadorn JW, Xiao S, Donoghue PCJ, Bengtson S, Gostling NJ, Pawlowska M, Raff EC, Raff RA, Turner FR, Yin C, Zhou C, Yuan X, McFeely MB, Stampanoni M, Nealson KH (2006) Cellular and subcellular structure of Neoproterozoic animal embryos. Science 314:291–294

    Article  CAS  PubMed  Google Scholar 

  • Han J, Kubota S, Li G, Kubota S, Yao X, Yang X, Shu D, Li Y, Kinoshita S, Sasaki O, Komiya T, Yan G (2013) Early Cambrian pentamerous cubozoan embryos from South China. PLoS ONE 8:e70741

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Harvey THP, Dong X, Donoghue PCJ (2010) Are palaeoscolecids ancestral ecdysozoans? Evol Dev 12:177–200

    Article  PubMed  Google Scholar 

  • Haug JT, Maas A, Waloszek D, Donoghue PCJ, Bengtson S (2009) A new species of Markuelia from the Middle Cambrian of Australia. Mem Assoc Australas Palaeontol 37:303–313

    Google Scholar 

  • Huldtgren T, Cunningham JA, Yin C, Stampanoni M, Marone F, Donoghue PCJ, Bengtson S (2011) Fossilized nuclei and germination structures identify Ediacaran “animal embryos” as encysting protists. Science 334:1696–1699

    Article  CAS  PubMed  Google Scholar 

  • Huldtgren T, Cunningham JA, Yin C, Stampanoni M, Marone F, Donoghue PCJ, Bengtson S (2012) Response to comment on “fossilized nuclei and germination structures identify Ediacaran ‘animal embryos’ as encysting protists”. Science 335:1169

    Article  Google Scholar 

  • Jeppsson L, Fredholm D, Mattiasson B (1985) Acetic acid and phosphatic fossils – a warning. J Paleontol 59:952–956

    Google Scholar 

  • Kouchinsky A, Bengtson S, Gershwin L (1999) Cnidarian-like embryos associated with the first shelly fossils in Siberia. Geology 27:609–612

    Article  Google Scholar 

  • Li C, Chen JY, Hua TE (1998) Precambrian sponges with cellular structures. Science 279:879–882

    Article  CAS  PubMed  Google Scholar 

  • Lin J-P, Scott AC, Li C-W, Wu H-J, Ausich WI, Zhao Y-L, Hwu Y-K (2006) Silicified egg clusters from a Middle Cambrian Burgess Shale-type deposit, Guizhou, south China. Geology 34:1037–1040

    Article  CAS  Google Scholar 

  • Mathur VK, Shome S, Nath S, Babu R (2014) First record of metazoan eggs and embryos from early Cambrian Chert Member of Deo ka Tibba Formation, Tal Group, Uttarakhand Lesser Himalaya. J Geol Soc India 83:191–197

    Article  CAS  Google Scholar 

  • Pyle LJ, Narbonne GM, Nowlan GS, Xiao SH, James NP (2006) Early Cambrian metazoan eggs, embryos, and phosphatic microfossils from northwestern Canada. J Paleontol 80:811–825

    Article  Google Scholar 

  • Qian Y (1977) Hyolitha and some problematica from the Lower Cambrian Meischucunian Stage in central and southwestern China. Acta Palaeontol Sin 16:255–275

    Google Scholar 

  • Raff EC, Villinski JT, Turner FR, Donoghue PCJ, Raff RA (2006) Experimental taphonomy shows the feasibility of fossil embryos. Proc Natl Acad Sci U S A 103:5846–5851

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Raff EC, Schollaert KL, Nelson DE, Donoghue PCJ, Thomas C-W, Turner FR, Stein BD, Dong X-P, Bengtson S, Huldtgren T, Stampanoni M, Yin C, Raff RA (2008) Embryo fossilization is a biological process mediated by microbial biofilms. Proc Natl Acad Sci 105:19359–19364

    Article  Google Scholar 

  • Raff EC, Andrews ME, Turner FR, Toh E, Nelson DE, Raff RA (2013) Contingent interactions among biofilm-forming bacteria determine preservation or decay in the first steps toward fossilization of marine embryos. Evol Dev 15:243–256

    Article  PubMed  Google Scholar 

  • Steiner M, Li G, Zhu M (2004a) Lower Cambrian small shelly fossils of northern Sichuan and southern Shaanxi (China), and their biostratigraphic significance. Geobios 37:259–275

    Article  Google Scholar 

  • Steiner M, Zhu M, Li G, Qian Y, Erdtmann B-D (2004b) New early Cambrian bilaterian embryos and larvae from China. Geology 32:833–836

    Article  Google Scholar 

  • Steiner M, Qian Y, Li G, Hagadorn JW, Zhu M (2014) The developmental cycles of early Cambrian Olivooidae fam. nov. (?Cycloneuralia) from the Yangtze Platform (China). Palaeogeogr Palaeoclimatol Palaeoecol 398:97–124

    Article  Google Scholar 

  • Tang F, Yin C, Bengtson S, Liu P, Wang Z, Gao L (2008) Octoradiate spiral organisms in the Ediacaran of South China. Acta Geologica Sinica 82:27–34

    Google Scholar 

  • Val’kov AK (1983) Rasprostranenie drevnejshikh skeletnykh organizmov i korrelyatsiya nizhnej granitsy kembriya v yugo-vostochnoj chasti Sibirskoj platformy [Distribution of the oldest skeletal organisms and correlation of the lower boundary of the Cambrian in the southeastern part of the Siberian Platform]. In: Khomentovsky VV, Yakshin MS, Karlova GA (eds) Pozdnij dokembrij i rannij paleozoj Sibiri, Vendskie otlozheniya. Inst Geol Geofiz SO AN SSSR, Novosibirsk, pp 37–48

    Google Scholar 

  • Val’kov AK (1987) Biostratigrafiya nizhnego kembriya vostoka Sibirskoj Platformy (Yudoma-Olenyokskij region). [Lower Cambrian biostratigraphy of the eastern part of the Siberian Platform (Yudoma-Olenyok region)]. Nauka, Moscow

    Google Scholar 

  • Xiao S (2002) Mitotic topologies and mechanics of Neoproterozoic algae and animal embryos. Paleobiology 28:244–250

    Article  Google Scholar 

  • Xiao S, Knoll AH (2000) Fossil preservation in the Neoproterozoic Doushantuo phosphorite Lagerstätte, South China. Lethaia 32:219–240

    Article  Google Scholar 

  • Xiao S, Zhang Y, Knoll AH (1998) Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite. Nature 391:553–558

    Article  CAS  Google Scholar 

  • Xiao S, Yuan X, Knoll AH (2000) Eumetazoan fossils in terminal Proterozoic phosphorites? Proc Natl Acad Sci U S A 97:13684–13689

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xiao S, Zhou CM, Yuan XL (2007) Undressing and redressing Ediacaran embryos. Nature 446(7136):E9–E10

    Article  CAS  PubMed  Google Scholar 

  • Xiao S, Knoll AH, Schiffbauer JD, Zhou C, Yuan X (2012) Comment on “Fossilized nuclei and germination structures identify Ediacaran ‘animal embryos’ as ecysting protists”. Science 335:1169

    Article  PubMed  Google Scholar 

  • Xue Y-S, Tang T-F, Yu C-l, Z C-M (1995) Large spheroidal Chlorophyta fossils from Doushantuo Formation phosphoric sequence (late Sinian), central Guizhou, South China. Acta Palaeontol Sin 34:688–706, In Chinese

    Google Scholar 

  • Yasui K, Reimer JD, Liu Y, Yao X, Kubo D, Shu D, Li Y (2013) A diploblastic radiate animal at the dawn of Cambrian diversification with a simple body plan: distinct from Cnidaria? PLoS ONE 8:e65890

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yin C, Bengtson S, Zhao Y (2004) Silicified and phosphatized Tianzhushania, spheroidal microfossils of possible animal origin from the Neoproterozoic of South China. Acta Palaeontol Pol 49:1–12

    Google Scholar 

  • Yue Z, Bengtson S (1999) Embryonic and post-embryonic development of the Early Cambrian cnidarian Olivooides. Lethaia 32:181–195

    Google Scholar 

  • Zhang XG, Pratt BR (1994) Middle Cambrian arthropod embryos with blastomeres. Science 266:637–639

    Article  CAS  PubMed  Google Scholar 

  • Zhang X-G, Pratt BR (2014) Possible algal origin and life cycle of Ediacaran Doushantuo microfossils with dextral spiral structure. J Palaeontol 88:92–98

    Article  Google Scholar 

  • Zhang X-G, Pratt BR, Shen C (2011) Embryonic development of a middle Cambrian (500 Myr old) scalidophoran worm. J Paleontol 85:898–903

    Article  Google Scholar 

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Acknowledgments

We would like to thank the TOMCAT beamline scientists at the Swiss Light Source, Paul Scherrer Institut, Marco Stampanoni, Federica Marone, and Julie Fife, and the researchers at Beijing, Bristol, and Stockholm who have assisted in our research into fossil embryos over the years: Chen Fang, Cheng Gong, Duan Baichuan, Peng Fan, Zhi-kun Gai, Sam Giles, Neil Gostling, Jenny Greenwood, Guo Wei, Sandy Hetherington, Therese Huldtgren, David Jones, Joe Keating, Liu Jie, Liu Zheng, Duncan Murdock, Maria Pawlowska, Martin Rücklin, Ceri-Wynn Thomas, Zhao Yue, Chongyu Yin, and Zhang Huaqiao. We would also like to thank our colleagues with whom we have enjoyed fruitful discussions on embryology, fossilisation, and embryo fossils over the years. Finally, we thank Andreas Wanninger for inviting us to contribute to this wonderful and insightful volume on comparative embryology of invertebrates.

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Correspondence to Philip C. J. Donoghue .

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Donoghue, P.C.J., Cunningham, J.A., Dong, XP., Bengtson, S. (2015). Embryology in Deep Time. In: Wanninger, A. (eds) Evolutionary Developmental Biology of Invertebrates 1. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1862-7_3

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