New observations of the ornamented Doushantuo embryo fossils from the Ediacaran Weng’an Biota, South China

 

Authors: Yin ZJ, Zhu MY

Published in: Bulletin of Geosciences, volume 87, issue 1; pages: 171 - 181; Received 12 September 2010; Accepted in revised form 7 October 2011; Online 2 February 2012

Keywords: Ediacaran, Doushantuo, fossil, embryos, resting eggs, Weng’an Biota,

full text (PDF, 3.51 MB)

Export to RIS

 

Abstract

Phosphatized Weng’an embryo fossils from the Ediacaran Doushantuo Formation in Guizhou, South China are dominated by various ornamented spheroidal fossils, with one internal body or several blastomeres enclosed within a single or multiple layered envelope, which have been interpreted as the resting eggs or diapause embryos of metazoans. Based on the microstructure of the envelope, we separated these ornamented spheroidal fossils into two groups: 1) group one, represented by typical Megasphaera ornata and characterized by an envelope consisting of at least two thick capsules with various surface ornaments and a single internal body, which can be interpreted as resting eggs; 2) another group, exhibiting an envelope consisting of a thin capsule with cell-like surface structure and internal blastomeres (amount is equal to 2n, n = 0, 1, 2, 3…), which are probably not diapause embryos but developing blastulae at various holoblastic cleavage stages.

References

Belk, D. 1989. Identification of species in the conchostracan genus Eulimnadia by egg shell morphology. Journal of Crustacean Biology 9(1), 115-125. View article

Belmonte, G.,Miglietta, A., Rubino, F.&Boero, F. 1997. Morphological convergence of resting stage of planktonic organisms: a review. Hydrobiologia 355, 159-165. View article

Belmonte, G. & Pati, C.A. 2007. Hatching rate and diapause duration in eggs of Paracartia latisetosa (Copepoda: Calanoida). Journal of Plankton Research 29, i39-i47. View article

Belmonte, G. & Puce, M. 1994. Morphological aspects of subitaneous and resting eggs from Acartia josephinae (Calanoida). Hydrobiologia 292/293, 131-135. View article

Bengtson, S. & Budd, G. 2004. Comment on “small bilaterian fossils from 40 to 55 million years before the Cambrian”. Science 306, 1291a. View article

Blades-Eckelbarger, P.I. & Marcus, N.H. 1992. The origin of cortical vesicles and their role in egg envelope formation in the “spiny” eggs of a calanoid copepod, Centropages velificatus. Biology Bulletin 182, 41-52. View article

Britz, R., Kokoscha, M. & Riehl, R. 1995. The anabantoid genera Ctenops, Luciocephalus, Parasphaerichthys, and Sphaerichthys (Teleostei: Perciformes) as a monophyletic group: evidence from egg surface structure and reproductive behaviour. Japan Journal of Ichthyology 42(1), 71-79.

Buckland-Nicks, J. & Hodgson, A.N. 2000. Fertilization in Callochiton castaneus (Mollusca). Biology Bulletin 199, 59-67. View article

Cáceres, C.E. 1997. Dormancy in invertebrates. Invertebrate Biology 116(4), 371-383. View article

Castro-Longoria, E. 2001. Comparative observations on the external morphology of subitaneous and diapause eggs of acartia species from Southampton Water. Crustaceana 74(3), 225-236. View article

Chen, J.Y. 2004. The dawn of animal world. 104 pp. Jiangsu Press of Science and Technology, Nanjing. [in Chinese]

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. & Tafforeau, P. 2006. Phosphatized polar lobe-forming embryos from the Precambrian of Southwest China. Science 312, 1644-1646. View article

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. & Tang, R. 2009a. Phase contrast synchrotron X-ray microtomography of Ediacaran (Doushantuo) metazoan microfossils: phylogenetic diversity and evolutionary implications. Precambrian Research 173, 191-200. View article

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. & Yin, Z.J. 2009b. Complex embryos displaying bilaterian characters from Precambrian Doushantuo phosphate deposits, Weng’an, Guizhou, China. Proceedings of National Academy of Sciences of the United States of America 106, 19056-19060. View article

Chen, J.Y., Bottjer, D.J., Oliveri, P., Dornbos, S.Q., Gao, F., Ruffins, S., Chi, H.M., Li, C.W. & Davidson, E.H. 2004a. Small bilaterian fossils from 40 to 55 million years before the Cambrian. Science 305, 218-222. View article

Chen, J.Y. & Chi, H.W. 2005. Precambrian phosphatized embryos and larvae from the Doushantuo Formation and their affinities, Guizhou (SW China). Chinese Science Bulletin 50, 1750-1757.View article

Chen, J.Y., Oliveri, P., Davidson, E.H. & Bottjer, D.J. 2004b. Response to comment on “Small bilaterian fossils from 40 to 55 million years before the Cambrian”. Science 306, 129lb.

Chen, J.Y., Oliveri, P., Gao, F., Dornbos, S.Q., Li, C.W., Bottjer, D.J. & Davidson, E.H. 2002. Precambrian animal life: Probable developmental and adult cnidarian forms from Southwest China. Developmental Biology 248, 182-196. View article

Chen, J.Y., Oliveri, P., Li, C.W., Zhou, G.Q., Gao, F., Hagadorn, J.W., Peterson, K.J.&Davidson, E.H. 2000. Precambrian animal diversity: Putative phosphatized embryos from the Doushantuo Formation of China. Proceedings of National Academy of Sciences of the United States of America 97, 4457-4462. View article

Chi, H.M., Chen, J.Y. & Li, C.W. 2003. Early developmental eggs with perivitelline space from Precambrian Weng’an Fauna, Weng’an, central Guizhou (South China). Acta Palaeontologica Sinica 42(3), 448-451. [in Chinese with English abstract]

Cohen, P.A., Knoll, A.H. & Kodnerc, R.B. 2009. Large spinose microfossils in Ediacaran rocks as resting stages of early animals. Proceedings of National Academy of Sciences of the United States of America 106, 6519-6524. View article

Condon, D., Zhu, M.Y., Bowring, S., Wang, W., Yang, A.H. & Jin, Y.G. 2005. U-Pb ages from the Neoproterozoic Doushantuo Formation, China. Science 308, 95-98. View article

Conn, D.B. 1991. Atlas of Invertebrate Reproduction and Development. 252 pp. Wiley-Liss, New York.

Couch, K.M., Downes, M. & Burns, C.W. 2001. Morphological differences between subitaneous and diapause eggs of Boeckella triarticulata (Copepoda: Calanoida). Freshwater Biology 46, 925-933. View article

Dharani, G. & Altaff, K. 2004. Ultra structure of subitaneous and diapausing eggs of planktonic copepod Sinodiaptomus (Rhinediaptomus) indicus. Current Science 87(1), 109-112.

Dornbos, Q.S., Bottjer, D.J., Chen, J.Y., Gao, F., Oliveri, P. & Li, C.W. 2006. Environmental controls on the taphonomy of phosphatized animals and animal embryos from the Neoproterozoic Doushantuo Formation, southwest China. Palaios 21, 3-14. View article

Dornbos, Q.S., Bottjer, D.J., Chen, J.Y., Oliveri, P., Gao, F. & Li, C.W. 2005. Precambrian animal life: Taphonomy of phosphatized metazoan embryos from southwest China. Lethaia 38, 101-109. View article

Engel, M. & Hirche, H.-J. 2004. Seasonal variability and interspecific differences in hatching of calanoid copepod resting eggs from sediments of the German Bight (North Sea). Journal of Plankton Research 26(9), 1083-1093. View article

Gilbert, J.J. & Wurdak, E.S. 1978. Species-specific morphology of resting eggs in the rotifer Asplanchna. Transactions of the American Microscopical Society 97(3), 330-339. View article

Gilbert, S.F. & Raunio, A.M. 1997. Embryology: constructing the organism. 537 pp. Sinauer Associates, Sunderland.

Gilchrist, B.M. 1978. Scanning electron microscope studies of the egg shell in some Anostraca (Crustacea: Branchiopoda). Cell Tissue Research 193, 337-351. View article

Hagadorn, J.W., Xiao, S.H., Donoghue, P.C.J., Bengtson, S., Gostling, N.J., Pawlowska, M., Raff, E.C., Raff, R.A., Turner, F.R., Yin, C.Y., Zhou, C.M., Yuan, X.L., McFeely, M.B., Stampanoni, M. & Nealson, K.H. 2006. Cellular and subcellular structure of Neoproterozoic animal embryos. Science 314, 291-294. View article

Hairston, N.G., Van Brunt, R.A., Kearns, C.M. & Engstrom, D.R. 1995. Age and survivorship of diapause eggs in a sediment egg bank. Ecology 76(6), 1706-1711.View article

Hrbek, T. & Larson, A. 1999. The evolution of diapause in the killifish family Rivulidae (Atherinomorpha, Cyprinodotiformes): a molecular phylogenetic and biogeographic perspective. Evolution 53(4), 1200-1216.View article

Ianora, A. & Santella, L. 1991. Diapause embryos in the neustonic copepod Anomalocera patersoi. Marine Biology 108, 387-394.View article

Li, C.W., Chen, J.Y. & HUA, T.E. 1998. Precambrian sponges with cellular structures. Science 279, 879-882.View article

Liu, P.J., Xiao, S.H., Yin, C.Y., Zhou, C.M., Gao, L.Z. & Tang, F. 2008. Systematic description and phylogenetic affinity of tubular microfossils from the Ediacaran Doushantuo Formation at Weng’an, South China. Palaeontology 51, 339-366.View article

Liu, Y.L., Zhao, Y., Dai, Z.M., Chen, H.M. & Yang, W.J. 2009. Formation of diapause cyst shell in brine shrimp Artemia parthenogenetica, and its resistance role in environmental stresses. Journal of Biological Chemistry 284(25), 16931-16938.View article

Marcus, N.H. 1996. Ecological and evolutionary significance of resting eggs in marine copepods: past, present, and future studies. Hydrobiologia 320, 141-152.View article

Martin, D., Briggs, D.E.G. & Parkes, R.J. 2003. Experimental mineralization of invertebrate eggs and the preservation of Neoproterozoic embryos. Geology 31, 39-42.View article

Martin, D., Briggs, D.E.G. & Parkes, R.J. 2005. Decay and mineralization of invertebrate eggs. Palaios 20, 562-572.View article

Mura, G. 2001. Morphological diversity of the resting eggs in the anostracan genus Chirocephalus (Crustacea, Branchiopoda). Hydrobiologia 450, 173-185.View article

Murphy, W.J. & Collier, G.E. 1997. A molecular phylogeny for aplocheiloid fishes (Atherinomorpha, Cyprinodotiformes): the role of vicariance and the origins of annualism. Molecular Biology and Evolution 14(8), 790-799.View article

Pennington, J.T., Tamburri, M.N. & Barry, J.P. 1999. Development, temperature tolerance, and settlement preference of embryos and larvae of the articulate brachiopod Laqueus californianus. Biology Bulletin 196, 245-256.View article

Raff, E.C., Villinski, J.T., Turner, R.T., Donoghue, P.C.J. & Raff, R.A. 2006. Experimental taphonomy shows the feasibility of fossil embryos. Proceedings of National Academy of Sciences of the United States of America 103, 5846-5851. View article

Santella, L. & Ianora, A. 1990. Subitaneous and diapause eggs in Mediterranean populations of Pontella mediterranea (Copepoda: Calanoida): a morphological study. Marine Biology 105, 83-90. View article

Schoenwolf, G.C. 2009. Laboratory studies of vertebrate and invertebrate embryos: guide and atlas of descriptive and experimental development. 388 pp. Benjamin Cummings, San Francisco.

Shen, Y.B. & Huang, D.Y. 2008. Extant clam shrimp egg morphology: taxonomy and comparison with other fossil branchiopod eggs. Journal of Crustacean Biology 28(2), 352-360. View article

Villa, L. & Patricolo, E. 1987. A scanning electron microscope study of Ascidia malaca egg (Tunicate), changes in the cell surface morphology at fertilization. Biology Bulletin 173, 355-366. View article

Xiao, S.H., Hagadorn, J.W., Zhou, C.M. & Yuan, X.L. 2007. Rare helical spheroidal fossils from the Doushantuo Lagerstätte: Ediacaran animal embryos come of age? Geology 35, 115-118. View article

Xiao, S.H. & Knoll, A.H. 1999. Fossil preservation in the Neoproterozoic Doushantuo phosphorite Lagerstätte, South China. Lethaia 32, 219-240. View article

Xiao, S.H. & Knoll, A.H. 2000. Phosphatized animal embryos from the Neoproterozoic Doushantuo Formation at Weng’an, Guizhou, South China. Journal of Paleontology 74(5), 767-788. View article

Xiao, S.H. & Schiffbauer, J.D. 2009. Microfossils phosphatization and its astrobiological implications, 89-117. In Seckbach, J. & Walsh, M. (eds) From Fossils to Astrobiology. Springer, Berlin.

Xiao, S.H., Yuan, X.L. & Knoll, A.H. 2000. Eumetazoan fossils in terminal Proterozoic phosphorites? Proceedings of National Academy of Sciences of the United States of America 97, 13684-13689. View article

Xiao, S.H., Zhang, Y. & Knoll, A.H. 1998. Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite. Nature 391, 553-558. View article

Xiao, S.H., Zhou, C.M. & Yuan, X.L. 2007b. Undressing and redressing Ediacaran embryos. Nature 446, E9. View article

Yin, C.Y., Bengtson, S. & Yue, Z. 2004. Silicified and phosphatized Tianzhushania from the Neoproterozoic Doushantuo phosphorites at Weng’an, Guizhou, South China. Acta Palaeontologica Polonica 49(1), 1-12.

Yin, L.M., Zhu, M.Y., Knoll, A.H., Yuan, X.L., Zhang, J.M. & Hu, J. 2007. Doushantuo embryos preserved inside diapause egg cysts. Nature 446, 661-663. View article

Yin, L.M., Zhou, C.M. & Yuan, X.L. 2008. New data on Tianzhushania: an Ediacaran diapauses egg cyst from Yichang, Huibei. Acta Palaeontologica Sinica 47(2), 129-140. [in Chinese with English abstract]

Yuan, X.L., Xiao, S.H., Yin, L.M., Knoll, A.H., Zhou, C.M. & Mu, X.N. 2002. Doushantuo fossils: life on the eve of animal radiation. 171 pp. University of Science and Technology of China Press, Heifei, China. [in Chinese with English summary]

Zhu, M.Y., Zhang, J.M. & Yang, A.H. 2007. Integrated Ediacaran (Sinian) chronostratigraphy of South China. Palaeogeography, Palaeoclimatology, Palaeoecology 254, 7-61. View article