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A Cloudina-like fossil with evidence of asexual reproduction from the lowest Cambrian, South China

  • JIAN HAN (a1), YAOPING CAI (a1), JAMES D. SCHIFFBAUER (a2), HONG HUA (a1), XING WANG (a1), XIAOGUANG YANG (a1), KENTARO UESUGI (a3), TSUYOSHI KOMIYA (a4) and JIE SUN (a1)...

Abstract

The earliest fossil record of animal biomineralization occurs in the latest Ediacaran Period (c. 550 Ma). Cloudina and Sinotubulites are two important tubular taxa among these earliest skeletal fossils. The evolutionary fate of Cloudina-type fossils across the Ediacaran–Cambrian transition, however, remains poorly understood. Here we report a multi-layered tubular microfossil Feiyanella manica gen. et sp. nov. from a phosphorite interval of the lowest Cambrian Kuanchuanpu Formation, southern Shaanxi Province, South China. This newly discovered fossil is a conical tube with a ‘funnel-in-funnel’ construction, showing profound morphological similarities to Cloudina and Conotubus. On the other hand, the outer few layers, and particularly the outermost layer, of Feiyanella tubes are regularly to irregularly corrugated, a feature strikingly similar to the variably folded/wrinkled tube walls of Sinotubulites. The Feiyanella tubes additionally exhibit two orders of dichotomous branching, similar to branching structures reported occasionally in Cloudina and possibly indicative of asexual reproduction. Owing to broad similarities in tube morphology, tube wall construction and features presumably indicative of asexual reproduction, Cloudina, Conotubus, Sinotubulites and the here described Feiyanella may thus constitute a monophyletic group traversing the Ediacaran–Cambrian boundary. The tube construction and palaeoecological strategy of Feiyanella putatively indicate evolutionary continuity in morphology and palaeoecology of benthic metazoan communities across the Ediacaran–Cambrian transition.

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Corresponding author

Author for correspondence: yaopingcai@nwu.edu.cn

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Bengtson, S., Conway Morris, S., Cooper, B., Jell, P. & Runnegar, B. 1990. Early Cambrian fossils from South Australia. Memoirs of the Association of Australasian Palaeontologists 9, 1364.
Bereiter-Hahn, J., Matoltsy, A. G. & Richards, K. S. 1984. Biology of the Integument: Invertebrates. Berlin: Springer-Verlag.
Cai, Y., Hua, H., Schiffbauer, J. D., Sun, B. & Yuan, X. 2014. Tube growth patterns and microbial mat-related lifestyles in the Ediacaran fossil Cloudina, Gaojiashan Lagerstätte, South China. Gondwana Research 25, 1008–18.
Cai, Y., Hua, H., Xiao, S., Schiffbauer, J. D. & Li, P. 2010. Biostratinomy of the late Ediacaran pyritized Gaojiashan Lagerstätte from southern Shaanxi, South China: importance of event deposits. Palaios 25, 487506.
Cai, Y., Hua, H. & Zhang, X. 2013. Tube construction and life mode of the late Ediacaran tubular fossil Gaojiashania cyclus from the Gaojiashan Lagerstätte. Precambrian Research 224, 255–67.
Cai, Y., Schiffbauer, J. D., Hua, H. & Xiao, S. 2011. Morphology and paleoecology of the late Ediacaran tubular fossil Conotubus hemiannulatus from the Gaojiashan Lagerstätte of southern Shaanxi Province, South China. Precambrian Research 191, 4657.
Cai, Y., Xiao, S., Hua, H. & Yuan, X. 2015. New material of the biomineralizing tubular fossil Sinotubulites from the late Ediacaran Dengying Formation, South China. Precambrian Research 261, 1224.
Canfield, D. E. & Farquhar, J. 2009. Animal evolution, bioturbation, and the sulfate concentration of the oceans. Proceedings of the National Academy of Sciences 106, 8123–7.
Canfield, D. E., Poulton, S. W., Knoll, A. H., Narbonne, G. M., Ross, G., Goldberg, T. & Strauss, H. 2008. Ferruginous conditions dominated later Neoproterozoic deep-water chemistry. Science 321 (5891), 949–52.
Caron, J.-B. & Vannier, J. 2015. Waptia and the diversification of brood care in early arthropods. Current Biology 26, 16.
Chen, Z., Bengtson, S., Zhou, C. M., Hua, H. & Yue, Z. 2008. Tube structure and original composition of Sinotubulites: shelly fossils from the late Neoproterozoic in southern Shaanxi, China. Lethaia 41, 3745.
Conway Morris, S. & Chen, M. E. 1992. Carinachitids, hexaconulariids, and Punctatus: problematic metazoans from the Early Cambrian of South China. Journal of Paleontology 66, 384406.
Cortijo, I., Mus, M. M., Jensen, S. & Palacios, T. 2010. A new species of Cloudina from the terminal Ediacaran of Spain. Precambrian Research 176, 110.
Cortijo, I., Mus, M. M., Jensen, S. & Palacios, T. 2015. Late Ediacaran skeletal body fossil assemblage from the Navalpino anticline, central Spain. Precambrian Research 267, 186–95.
Darroch, S. A., Sperling, E. A., Boag, T. H., Racicot, R. A., Mason, S. J., Morgan, A. S., Tweedt, S., Myrow, P., Johnston, D. T. & Erwin, D. H. 2015. Biotic replacement and mass extinction of the Ediacara biota. In Proceedings of the Royal Society B: Biological Sciences 282, 20151003. doi: 10.1098/rspb.2015.1003.
Dong, X.-P., Cunningham, J. A., Bengtson, S., Thomas, C.-W., Liu, J., Stampanoni, M. & Donoghue, P. C. 2013. Embryos, polyps and medusae of the Early Cambrian scyphozoan Olivooides . Proceedings of the Royal Society B: Biological Sciences 280, 130071. doi: 10.1098/rspb.2013.0071.
Duan, Y., Han, J., Fu, D., Zhang, X., Yang, X., Komiya, T. & Shu, D. 2014. Reproductive strategy of the bradoriid arthropod Kunmingella douvillei from the Lower Cambrian Chengjiang Lagerstätte, South China. Gondwana Research 25, 983–90.
Erwin, D. H., Laflamme, M., Tweedt, S. M., Sperling, E. A., Pisani, D. & Peterson, K. J. 2011. The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334 (6059), 1091–7.
Fedonkin, M. A., Gehling, J. G., Grey, K., Narbonne, G. M. & Vickers-Rich, P. 2007. The Rise of Animals: Evolution and Diversification of the Kingdom Animalia. Baltimore: John Hopkins University Press.
Fike, D. A., Grotzinger, J. P., Pratt, L. M. & Summons, R. E. 2006. Oxidation of the Ediacaran ocean. Nature 444, 744–7.
Germs, J. G. B. 1972. New shelly fossils from the Nama Group, South West Africa. American Journal of Science 272, 752–61.
Glaessner, M. 1976. Early Phanerozoic annelid worms and their geological and biological significance. Journal of the Geological Society, London 132, 259–75.
Grant, S. 1990. Shell structure and distribution of Cloudina, a potential index fossil for the terminal Proterozoic. American Journal of Science 290, 261–94.
Grotzinger, J. P., Watters, W. A. & Knoll, A. H. 2000. Calcified metazoans in thrombolite–stromatolite reefs of the terminal Proterozoic Nama Group, Namibia. Paleobiology 26, 334–59.
Hagadorn, J. W. & Waggoner, B. M. 2000. Ediacaran fossils from the southwestern Great Basin, United States. Journal of Paleontology 74, 349–59.
Han, J., Kubota, S., Li, G., Ou, Q., Wang, X., Yao, X., Shu, D., Li, Y., Uesugi, K., Hoshino, M., Sasaki, O., Kano, H., Sato, T. & Komiya, T. 2016a. Divergent evolution of medusozoan symmetric patterns: evidence from the microanatomy of Cambrian tetramerous cubozoans from South China. Gondwana Research 31, 150–63.
Han, J., Kubota, S., Li, G., 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 (8), e70741. doi: 10.1371/journal.pone.0070741.
Han, J., Kubota, S., Uchida, H., Stanley, G. D. Jr, Yao, X. Y., Shu, D. G., Li, Y. & Yasui, K. 2010. Tiny sea anemone from the Lower Cambrian of China. PLoS One 5 (10), e13276. doi: 10.1371/journal.pone.0013276.
Han, J., Li, G. X., Kubota, S., Ou, Q., Toshino, S., Wang, X., Yang, X. G., Uesugi, K., Hoshino, M., Sasaki, O., Kano, H. & Komiya, T. 2016b. Internal microanatomy and zoological affinity of the early Cambrian Olivooides . Acta Geologica Sinica (English Edition) 90 (1), 3865.
Hofmann, H. J. & Mointjoy, E. W. 2001. Namacalathus–Cloudina assemblage in Neoproterozoic Miette Group (Byng Formation), British Columbia: Canada's oldest shelly fossils. Geology 29, 1091–4.
Hou, X. G., Siveter, D. J. & Aldridge, R. J. 2008. Collective behavior in an early Cambrian arthropod. Science 322 (5899), 224.
Hua, H., Chen, Z., Yuan, X. L., Zhang, L. Y. & Xiao, S. H. 2005. Skeletogenesis and asexual reproduction in the earliest biomineralizing animal Cloudina . Geology 33, 277–80.
Hua, H., Pratt, B. R. & Zhang, L.-Y. 2003. Borings in Cloudina shells: complex predator-prey dynamics in the terminal Neoproterozoic. Palaios 18, 454–9.
Hyman, L. H. 1940. The Invertebrates. New York: McGraw Hill.
Jarms, G. 1991. Taxonomic characters from the polyp tubes of coronate medusae (Scyphozoa, Coronatae). Hydrobiologia 216, 463–70.
Jensen, S., Gehling, J. G. & Droser, M. L. 1998. Ediacara-type fossils in Cambrian sediments. Nature 393, 567–9.
Komiya, T., Hirata, T., Kitajima, K., Yamamoto, S., Shibuya, T., Sawaki, Y., Ishikawa, T., Shu, D., Li, Y. & Han, J. 2008. Evolution of the composition of seawater through geologic time, and its influence on the evolution of life. Gondwana Research 14, 159–74.
Kouchinsky, A., Bengtson, S., Clausen, S. & Vendrasco, M. J. 2015. An early Cambrian fauna of skeletal fossils from the Emyaksin Formation, northern Siberia. Acta Palaeontologica Polonica 60, 421512.
Kouchinsky, A., Bengtson, S., Feng, W., Kutygin, R. & Val'kov, A. 2009. The Lower Cambrian fossil anabaritids: affinities, occurrences and systematics. Journal of Systematic Palaeontology 7, 241–98.
Laflamme, M., Darroch, S. A., Tweedt, S. M., Peterson, K. J. & Erwin, D. H. 2013. The end of the Ediacara biota: extinction, biotic replacement, or Cheshire Cat? Gondwana Research 23, 558–73.
Laflamme, M., Xiao, S. & Kowalewski, M. 2009. Osmotrophy in modular Ediacara organisms. Proceedings of the National Academy of Sciences 106, 14438–43.
Li, G. 2004. Early Cambrian Hyolithelminths – Torellella bisulcata sp. nov. from Zhenba, Southern Shaanxi. Acta Palaeontologica Sinica 43, 571–8.
Li, C., Love, G. D., Lyons, T. W., Fike, D. A., Sessions, A. L. & Chu, X. 2010. A stratified redox model for the Ediacaran ocean. Science 328 (5974), 80–3.
Liu, Y., Li, Y., Shao, T., Zhang, H., Wang, Q. & Qiao, J. 2014a. Quadrapyrgites from the lower Cambrian of South China: Growth pattern, post-embryonic development, and affinity. Chinese Science Bulletin 59 (31), 4086–95.
Liu, Y., Li, Y., Shao, T., Zheng, X., Zheng, J., Wang, G., Wang, H. & Qwang, K. 2011. A new genus and species of protoconulariids from the early Cambrian in the south Shaanxi, China. Acta Micropalaeontologica Sinica 28, 245–49.
Liu, Y. H., Xiao, S. H., Shao, T. Q., Broce, J. & Zhang, H. Q. 2014b. The oldest known priapulid-like scalidophoran animal and its implications for the early evolution of cycloneuralians and ecdysozoans. Evolution & Development 16, 155–65.
McIlroy, D., Green, O. R. & Brasier, M. D. 2001. Palaeobiology and evolution of the earliest agglutinated Foraminifera: Platysolenites, Spirosolenites and related forms. Lethaia 34, 1329.
Nutting, C. C. 1900. American Hydroids (II). Washington: US Government Printing Office.
Peterson, K. J. & Eernisse, D. J. 2001. Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences. Evolution and Development 3, 170205.
Qian, Y. 1977. Hyolitha and some problematica from the Lower Cambrian Meishucun Stage in central and SW China. Acta Palaeontologica Sinica 16, 255–75.
Qian, Y. 1999. Taxonomy and Biostratigraphy of Small Shelly Fossils in China. Beijing: Science Press (in Chinese with English summary).
Qian, Y. & Bengtson, S. 1989. Palaeontology and biostratigraphy of the Early Cambrian Meishucunian Stage in Yunnan Province, South China. Fossils and Strata 24, 1156.
Qian, Y., Van Iten, H., Cox, R. S., Zhu, M. & Zhou, E. 1997. A brief account of Emeiconularia trigemme, a new genus and species of protoconulariid. Acta Micropalaeontologica Sinica 14, 475–88.
Rahman, I. A., Darroch, S. A. F., Racicot, R. A. & Laflamme, M. 2015. Suspension feeding in the enigmatic Ediacaran organism Tribrachidium demonstrates complexity of Neoproterozoic ecosystems. Science Advances 1, e1500800. doi: 10.1126/sciadv.1500800.
Rogov, V. I., Karlova, G. A., Marusin, V. V., Kochnev, B. B., Nagovitsin, K. E. & Grazhdankin, D. V. 2015. Duration of the first biozone in the Siberian hypostratotype of the Vendian. Russian Geology and Geophysics 56, 573–83.
Schiffbauer, J. D., Huntley, J. W., O'Neil, G. R., Darroch, S. A. F., Laflamme, M. & Cai, Y. 2016. The latest Ediacaran Wormworld fauna: setting the ecological stage for the Cambrian Explosion. GSA Today 26, 411.
Schiffbauer, J. D., Wallace, A. F., Broce, J. & Xiao, S. 2014. Exceptional fossil conservation through phosphatization. The Paleontological Society Papers 20, 5982.
Seilacher, A. 1999. Biomat-related lifestyles in the Precambrian. Palaios 14, 8693.
Shu, D., Isozaki, Y., Zhang, X., Han, J. & Maruyama, S. 2014. Birth and early evolution of metazoans. Gondwana Research 25, 884–95.
Shu, D. G., Morris, S. C., Han, J., Li, Y., Zhang, X. L., Hua, H., Zhang, Z. F., Liu, J. N., Guo, J. F., Yao, Y. & Yasui, K. 2006. Lower Cambrian vendobionts from China and early diploblast evolution. Science 312 (5774), 731–4.
Signor, P. W., Mount, J. F. & Onken, B. R. 1987. A pre–trilobite shelly fauna from the White–Inyo region of eastern California and western Nevada. Journal of Paleontology 61, 425–38.
Skovsted, C. B. & Peel, J. S. 2011. Hyolithellus in life position from the Lower Cambrian of North Greenland. Journal of Paleontology 85, 3747.
Smith, E. F., Nelson, L. L., Strange, M. A., Eyster, A. E., Rowland, S. M., Schrag, D. P. & Macdonald, F. A. 2016. The end of the Ediacaran: two new exceptionally preserved body fossil assemblages from Mount Dunfee, Nevada, USA. Geology 44, 911–4.
Sperling, E. A., Frieder, C. A., Raman, A. V., Girguis, P. R., Levin, L. A. & Knoll, A. H. 2013. Oxygen, ecology, and the Cambrian radiation of animals. Proceedings of the National Academy of Sciences 110, 13446–51.
Steiner, M., Li, G. X., Qian, Y. & Zhu, M. Y. 2004a. Lower Cambrian Small Shelly Fossils of northern Sichuan and southern Shaanxi (China), and their biostratigraphic importance. Geobios 37, 259–75.
Steiner, M., Qian, Y., Li, G., Hagadorn, J. W. & Zhu, M. 2014. The developmental cycles of early Cambrian Olivooidae fam. nov. (?Cycloneuralia) from the Yangtze Platform (China). Palaeogeography, Palaeoclimatology, Palaeoecology 398, 97124.
Steiner, M., Zhu, M. Y., Li, G. X., Qian, Y. & Erdtmann, B. D. 2004b. New early Cambrian bilaterian embryos and larvae from China. Geology 32, 833–6.
Van Iten, H., Cox, R. S. & Mapes, R. H. 1992. New data on the morphology of Sphenothallus Hall: implications for its affinities. Lethaia 25, 135–44.
Van Iten, H., De Moraes Leme, J., Sim Es, M. G., Marques, A. C. & Collins, A. G. 2006. Reassessment of the phylogenetic position of conulariids (? Ediacaran–Triassic) within the subphylum Medusozoa (phylum Cnidaria). Journal of Systematic Palaeontology 4, 109–18.
Van Iten, H., Marques, A. C., Leme, J. D. M., Pacheco, M. L. & Sim Es, M. G. 2014. Origin and early diversification of the phylum Cnidaria Verrill: major developments in the analysis of the taxon's Proterozoic–Cambrian history. Palaeontology 57 (4), 114.
Vannier, J., Garc A-Bellido, D., Hu, S.-X. & Chen, A.-L. 2009. Arthropod visual predators in the early pelagic ecosystem: evidence from the Burgess Shale and Chengjiang biotas. Proceedings of the Royal Society of London B: Biological Sciences 276 (1667), 2567–74.
Vannier, J., Steiner, M., Renvoise, E., Hu, S. X. & Casanova, J. P. 2007. Early Cambrian origin of modern food webs: evidence from predator arrow worms. Proceedings of the Royal Society B: Biological Sciences 274 (1610), 627–33.
Vinn, O. 2006. Possible cnidarian affinities of Torellella (Hyolithelminthes, Upper Cambrian, Estonia). Paläontologische Zeitschrift 80, 384–9.
Vinn, O. & Zaton, M. 2012. Inconsistencies in proposed annelid affinities of early biomineralized organism Cloudina (Ediacaran): structural and ontogenetic evidences. Carnets de Geologie [Notebooks on Geology] CG2012 (A03), 3946.
Werner, B. 1973. New investigations on systematics and evolution of the class Scyphozoa and the phylum Cnidaria. Publications of the Seto Marine Biological Laboratory 20, 3561.
Wood, R. & Curtis, A. 2015. Extensive metazoan reefs from the Ediacaran Nama Group, Namibia: the rise of benthic suspension feeding. Geobiology 13, 112–22.
Yang, B., Steiner, M., Zhu, M., Li, G., Liu, J. & Liu, P. 2016. Transitional Ediacaran–Cambrian small skeletal fossil assemblages from South China and Kazakhstan: Implications for chronostratigraphy and metazoan evolution. Precambrian Research 285, 202–15.
Yochelson, E. L. & Stump, E. 1977. Discovery of early Cambrian fossils at Taylor Nunatak, 936 Antarctica. Journal of Paleontology 51, 872–5.
Yuan, X., Chen, Z., Xiao, S., Zhou, C. & Hua, H. 2011. An early Ediacaran assemblage of macroscopic and morphologically differentiated eukaryotes. Nature 470 (7334), 390–3.
Zhang, H., Xiao, S., Liu, Y., Yuan, X., Wan, B., Muscente, A., Shao, T., Gong, H. & Cao, G. 2015. Armored kinorhynch-like scalidophoran animals from the early Cambrian. Scientific Reports 5, 16521. doi: 10.1038/srep16521.
Zhu, M., Van Iten, H., Cox, R. S., Zhao, Y. & Erdtmann, B. D. 2000. Occurrence of Byronia Matthew and Sphenothallus Hall in the Lower Cambrian of China. Palaeontologische Zeitschrift 74, 227–38.
Zhuravlev, A. Y., Li, N, E., Vintaned, J. A. G., Debrenne, F. & Fedorov, A. B. 2012. New finds of skeletal fossils in the terminal Neoproterozoic of the Siberian Platform and Spain. Acta Palaeontologica Polonica 57, 205–24.

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