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

Part of: From Snowball Earth to the Cambrian Explosion: Evidence from China

Published online by Cambridge University Press:  09 January 2017

JIAN HAN Open the ORCID record for JIAN HAN [Opens in a new window] ,
YAOPING CAI ,
JAMES D. SCHIFFBAUER ,
HONG HUA ,
XING WANG ,
XIAOGUANG YANG ,
KENTARO UESUGI ,
TSUYOSHI KOMIYA  and
JIE SUN
JIAN HAN
Affiliation:
Early Life Institute and Department of Geology and State Key Laboratory of Continental Dynamics, Northwest University, No. 229 Taibai Road, Xi'an 710069, China
YAOPING CAI*
Affiliation:
Early Life Institute and Department of Geology and State Key Laboratory of Continental Dynamics, Northwest University, No. 229 Taibai Road, Xi'an 710069, China
JAMES D. SCHIFFBAUER
Affiliation:
Department of Geological Sciences, University of Missouri, 101 Geology Building, Columbia, MO, 65211, USA
HONG HUA
Affiliation:
Early Life Institute and Department of Geology and State Key Laboratory of Continental Dynamics, Northwest University, No. 229 Taibai Road, Xi'an 710069, China
XING WANG
Affiliation:
Early Life Institute and Department of Geology and State Key Laboratory of Continental Dynamics, Northwest University, No. 229 Taibai Road, Xi'an 710069, China
XIAOGUANG YANG
Affiliation:
Early Life Institute and Department of Geology and State Key Laboratory of Continental Dynamics, Northwest University, No. 229 Taibai Road, Xi'an 710069, China
KENTARO UESUGI
Affiliation:
Japan Synchrotron Radiation Research Institute (JASRI), 1-1-1 Kouto, Sayo-cho, Sayo-gun, Hyogo, Japan
TSUYOSHI KOMIYA
Affiliation:
Department of Earth Science and Astronomy, Graduate School of Arts and Sciences, University of Tokyo, Tokyo 153–8902, Japan
JIE SUN
Affiliation:
Early Life Institute and Department of Geology and State Key Laboratory of Continental Dynamics, Northwest University, No. 229 Taibai Road, Xi'an 710069, China
*
†Author for correspondence: yaopingcai@nwu.edu.cn
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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.

Keywords

CloudinaSinotubulitesasexual reproductionearly CambrianKuanchuanpu Formation.
Type
Original Articles
Information
Geological Magazine , Volume 154 , Issue 6: THEMATIC ISSUE: From Snowball Earth to the Cambrian Explosion: Evidence from China , November 2017 , pp. 1294 - 1305
Copyright
Copyright © Cambridge University Press 2017 

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References

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, 1–364.Google Scholar
Bereiter-Hahn, J., Matoltsy, A. G. & Richards, K. S. 1984. Biology of the Integument: Invertebrates. Berlin: Springer-Verlag.Google Scholar
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.Google Scholar
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, 487–506.Google Scholar
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.Google Scholar
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, 46–57.Google Scholar
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, 12–24.Google Scholar
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.Google Scholar
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.Google Scholar
Caron, J.-B. & Vannier, J. 2015. Waptia and the diversification of brood care in early arthropods. Current Biology 26, 1–6.Google Scholar
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, 37–45.Google Scholar
Conway Morris, S. & Chen, M. E. 1992. Carinachitids, hexaconulariids, and Punctatus: problematic metazoans from the Early Cambrian of South China. Journal of Paleontology 66, 384–406.CrossRefGoogle Scholar
Cortijo, I., Mus, M. M., Jensen, S. & Palacios, T. 2010. A new species of Cloudina from the terminal Ediacaran of Spain. Precambrian Research 176, 1–10.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
Fike, D. A., Grotzinger, J. P., Pratt, L. M. & Summons, R. E. 2006. Oxidation of the Ediacaran ocean. Nature 444, 744–7.Google Scholar
Germs, J. G. B. 1972. New shelly fossils from the Nama Group, South West Africa. American Journal of Science 272, 752–61.CrossRefGoogle Scholar
Glaessner, M. 1976. Early Phanerozoic annelid worms and their geological and biological significance. Journal of the Geological Society, London 132, 259–75.Google Scholar
Grant, S. 1990. Shell structure and distribution of Cloudina, a potential index fossil for the terminal Proterozoic. American Journal of Science 290, 261–94.Google Scholar
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.Google Scholar
Hagadorn, J. W. & Waggoner, B. M. 2000. Ediacaran fossils from the southwestern Great Basin, United States. Journal of Paleontology 74, 349–59.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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), 38–65.Google Scholar
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.Google Scholar
Hou, X. G., Siveter, D. J. & Aldridge, R. J. 2008. Collective behavior in an early Cambrian arthropod. Science 322 (5899), 224.Google Scholar
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.Google Scholar
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.Google Scholar
Hyman, L. H. 1940. The Invertebrates. New York: McGraw Hill.Google Scholar
Jarms, G. 1991. Taxonomic characters from the polyp tubes of coronate medusae (Scyphozoa, Coronatae). Hydrobiologia 216, 463–70.Google Scholar
Jensen, S., Gehling, J. G. & Droser, M. L. 1998. Ediacara-type fossils in Cambrian sediments. Nature 393, 567–9.Google Scholar
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.CrossRefGoogle Scholar
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, 421–512.Google Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
Laflamme, M., Xiao, S. & Kowalewski, M. 2009. Osmotrophy in modular Ediacara organisms. Proceedings of the National Academy of Sciences 106, 14438–43.Google Scholar
Li, G. 2004. Early Cambrian Hyolithelminths – Torellella bisulcata sp. nov. from Zhenba, Southern Shaanxi. Acta Palaeontologica Sinica 43, 571–8.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
McIlroy, D., Green, O. R. & Brasier, M. D. 2001. Palaeobiology and evolution of the earliest agglutinated Foraminifera: Platysolenites, Spirosolenites and related forms. Lethaia 34, 13–29.Google Scholar
Nutting, C. C. 1900. American Hydroids (II). Washington: US Government Printing Office.Google Scholar
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, 170–205.Google Scholar
Qian, Y. 1977. Hyolitha and some problematica from the Lower Cambrian Meishucun Stage in central and SW China. Acta Palaeontologica Sinica 16, 255–75.Google Scholar
Qian, Y. 1999. Taxonomy and Biostratigraphy of Small Shelly Fossils in China. Beijing: Science Press (in Chinese with English summary).Google Scholar
Qian, Y. & Bengtson, S. 1989. Palaeontology and biostratigraphy of the Early Cambrian Meishucunian Stage in Yunnan Province, South China. Fossils and Strata 24, 1–156.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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, 4–11.Google Scholar
Schiffbauer, J. D., Wallace, A. F., Broce, J. & Xiao, S. 2014. Exceptional fossil conservation through phosphatization. The Paleontological Society Papers 20, 59–82.Google Scholar
Seilacher, A. 1999. Biomat-related lifestyles in the Precambrian. Palaios 14, 86–93.Google Scholar
Shu, D., Isozaki, Y., Zhang, X., Han, J. & Maruyama, S. 2014. Birth and early evolution of metazoans. Gondwana Research 25, 884–95.Google Scholar
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.Google Scholar
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.Google Scholar
Skovsted, C. B. & Peel, J. S. 2011. Hyolithellus in life position from the Lower Cambrian of North Greenland. Journal of Paleontology 85, 37–47.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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, 97–124.Google Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
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), 1–14.Google Scholar
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.Google Scholar
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.Google Scholar
Vinn, O. 2006. Possible cnidarian affinities of Torellella (Hyolithelminthes, Upper Cambrian, Estonia). Paläontologische Zeitschrift 80, 384–9.Google Scholar
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), 39–46.Google Scholar
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, 35–61.Google Scholar
Wood, R. & Curtis, A. 2015. Extensive metazoan reefs from the Ediacaran Nama Group, Namibia: the rise of benthic suspension feeding. Geobiology 13, 112–22.Google Scholar
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.Google Scholar
Yochelson, E. L. & Stump, E. 1977. Discovery of early Cambrian fossils at Taylor Nunatak, 936 Antarctica. Journal of Paleontology 51, 872–5.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar