Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-19T11:04:27.325Z Has data issue: false hasContentIssue false

Embryonic development of a Middle Cambrian (500 Myr old) scalidophoran worm

Published online by Cambridge University Press:  14 July 2015

Xi-Guang Zhang
Affiliation:
1Key Laboratory for Paleobiology, Yunnan University, Kunming, Yunnan 650091, China,
Brian R. Pratt
Affiliation:
2Department of Geological Sciences, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5E2, Canada
Cen Shen
Affiliation:
1Key Laboratory for Paleobiology, Yunnan University, Kunming, Yunnan 650091, China,

Abstract

Extraordinarily rare phosphatized embryos liberated from fossiliferous limestone of the Middle Cambrian (about 500 Myr old) Gaotai Formation of Duyun, southern China, are assigned to Markuelia qianensis n. sp. Several specimens with increasing numbers of blastomeres may represent four successive cleavage stages, seemingly exhibiting a radial holoblastic cleavage pattern. No subsequent stages showing gastrulation were observed. However, several specimens are late, pre-hatching stages, each with a vermiform shape coiled in either left-or right-handed directions within the fertilization envelope. These specimens indicate that the intuitively assumed difference in preservation potential between early cleavage and late pre-hatching stages is probably not valid. This new material clarifies the affinity of the first fossilized invertebrate embryos ever described, from the same rocks, which were originally attributed to arthropods, presumably trilobites. Instead, they belong to scalidophorans, and this finding infers likely diversified cleavage patterns for stem members of this group, and yields fresh insight into the embryogenesis of early metazoans as a whole.

Type
Research Article
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

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: 198201.Google Scholar
Bengtson, S. and Yue, Z. 1997. Fossilized metazoan embryos from the earliest Cambrian. Science, 277: 16451648.Google Scholar
Bengtson, S., Cunningham, J. A., Donoghue, P. C. J., Huldtgren, T., and Yin, C.-Y. 2010. A critical view of ‘animal embryos’ in the Ediacaran Doushantuo biota. Geological Society of America Annual Meeting, Paper 167-7.Google Scholar
Butterfield, N. J. 2002. Leanchoilia guts and the interpretation of three-dimensional structures in Burgess Shale-type fossils. Paleobiology, 28: 155171.Google Scholar
Chen, J.-Y., Schopf, J. W., Bottjer, D. J., Zhang, C.-Y., Kudryavtsev, A. B., Tripathi, A. B., Wang, X.-Q., Yang, Y.-H., Gao, X., and Yang, Y. 2007. Raman spectra of a Lower Cambrian ctenophore embryo from southwestern Shaanxi, China. Proceedings of the National Academy of Sciences, U.S.A., 104: 62896292.CrossRefGoogle ScholarPubMed
Davy, S. K. and Turner, J. R. 2003. Early development and acquisition of zooxanthellae in the temperate symbiotic sea anemone Anthopleura ballii (Cocks). The Biological Bulletin, 205: 6672.Google Scholar
Dong, X.-P. 2007. Developmental sequence of Cambrian embryo Markuelia. Chinese Science Bulletin, 52: 929935.Google Scholar
Dong, X.-P., Bengtson, S., Gostling, N. J., Cunninghan, J. A., and Donoghue, P. C. J. 2010. The anatomy, taphonomy, taxonomy and systematic affinity of Markuelia: Early Cambrian to Early Ordovician scalidophorans. Palaeontology, 53: 12911313.Google Scholar
Dong, X.-P., Donoghue, P. C. J., Cheng, H., and Liu, J.-B. 2004. Fossil embryos from the Middle and Late Cambrian period of Hunan, south China. Nature, 427: 237240.Google Scholar
Dong, X.-P., Donoghue, P. C. J., Cunningham, J. A., Liu, J.-B., and Cheng, H. 2005. The anatomy, affinity, and phylogenetic significance of Markuelia. Evolution and Development, 7: 468482.Google Scholar
Donoghue, P. C. J. 2007. Embryonic identity crisis. Nature, 445: 155156.Google Scholar
Donoghue, P. C. J., Kouchinsky, A., Waloszek, D., Bengtson, S., Dong, X.-P., Val'kov, A. K., Cunningham, J. A., and Repetski, J. E. 2006. Fossilized embryos are widespread but the record is temporally and taxonomically biased. Evolution and Development, 8: 232238.Google Scholar
Gostling, N. J., Thomas, C.-W., Greenwood, J. M., Dong, X., Bengtson, S., Raff, E. C., Raff, R., Degnan, B. M., Stampanoni, M., and Donoghue, P. C. J. 2008. Deciphering the fossil record of early bilaterian embryonic development in light of experimental taphonomy. Evolution and Development, 10: 339349.Google Scholar
Harvey, T. H. P., Dong, X.-P., and Donoghue, P. C. J. 2010. Are palaeoscolecids ancestral ecdysozoans? Evolution and Development, 12: 177200.Google Scholar
Haug, J. T., Maas, A., Waloszek, D., Donoghue, P. C. J., and Bengtson, S. 2009. A new species of Markuelia from the Middle Cambrian of Australia, p. 303313. In Laurie, J. R., Brock, G. A., and Paterson, J. R. (eds.), Cambro-Ordovician Studies III. Memoirs of the Association of Australasian Palaeontologists, 37.Google Scholar
Kouchinsky, A., Bengtson, S., and Gershwin, L. 1999. Cnidarian-like embryos associated with the first shelly fossils in Siberia. Geology, 27: 609612.Google Scholar
Li, C.-W., Chen, J.-Y., and Hua, T.-E. 1998. Precambrian sponges with cellular structures. Science, 279: 879882.Google Scholar
Müller, K. J. 1985. Exceptional preservation in calcareous nodules. Philosophical Transactions of the Royal Society B, 311: 6773.Google Scholar
Martin, D., Briggs, D. E. G., and Parkes, R. J. 2005. Decay and mineralization of invertebrate eggs. Palaios, 20: 562572.Google Scholar
Pyle, L. J., Narbonne, G. M., Nowlan, G. S., Xiao, S.-H., and James, N. P. 2006. Early Cambrian metazoan eggs, embryos, and phosphatic microfossils from northwestern Canada. Journal of Paleontology, 80: 811825.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.-P., 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, U.S.A., 105: 1936019365.Google Scholar
Steiner, M., Zhu, M.-Y., Li, G.-X., Qian, Y., and Erdtmann, B.-D. 2004. New Early Cambrian bilaterian embryos and larvae from China. Geology, 32: 833836.Google Scholar
Valentine, J. W. 1997. Cleavage patterns and the topology of the metazoan tree of life. Proceedings of the National Academy of Sciences, U.S.A., 94: 80018005.Google Scholar
Waloszek, D. 2003. The ‘orsten’ window—a three-dimensionally preserved Upper Cambrian meiofauna and its contribution to our understanding of the evolution of Arthropoda. Paleontological Research, 7: 7188.Google Scholar
Webster, B. L., Copley, R. R., Jenner, R. A., Mackenzie-Dodds, J. A., Bourlat, S. J., Rota-Stabelli, O., Littlewood, D. T. J., and Telford, M. J. 2006. Mitogenomics and phylogenomics reveal priapulid worms as extant models of the ancestral ecdysozoan. Evolution and Development, 8: 502510.Google Scholar
Wennberg, S. A., Janssen, R., and Budd, G. E. 2008. Early embryonic development of the priapulid worm Priapulus caudatus. Evolution and Development, 10: 326338.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: 553558.Google Scholar
Yin, C.-Y., Gao, L.-Z., and Xing, Y.-S. 2002. Advances in the study of permineralized biota of Doushantuo Stage in Weng'an, Guizhou Province and their geological significance. Acta Geoscientica Sinica, 23: 4754.Google Scholar
Yin, L.-M., Zhu, M.-Y., Knoll, A. H., Yuan, X.-L., Zhang, J.-M., and Hu, J. 2007. Doushantuo embryos preserved inside diapause egg cysts. Nature, 446: 661663.Google Scholar
Zhang, X.-G. and Pratt, B. R. 1994. Middle Cambrian arthropod embryos with blastomeres. Science, 266: 637639.Google Scholar
Zhang, X.-G. and Pratt, B. R. 2008. Microborings in Early Cambrian phosphatic and phosphatized fossils. Palaeogeography, Palaeoclimatology, Palaeoecology, 267: 185195.Google Scholar