Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-27T14:02:51.779Z Has data issue: false hasContentIssue false
  • English
  • Français

Ediacara growing pains: modular addition and development in Dickinsonia costata

Published online by Cambridge University Press:  13 September 2021

Scott D. Evans Open the ORCID record for Scott D. Evans [Opens in a new window] ,
James G. Gehling ,
Douglas H. Erwin  and
Mary L. Droser
Scott D. Evans*
Affiliation:
Department of Geosciences, Virginia Tech, Blacksburg, Virginia 24061, U.S.A. E-mail: [email protected]
James G. Gehling
Affiliation:
South Australia Museum, Adelaide, South Australia 5000, Australia. E-mail: [email protected]
Douglas H. Erwin
Affiliation:
Department of Paleobiology MRC-121, National Museum of Natural History, Washington, D.C. 20013-7012, U.S.A. E-mail: [email protected]
Mary L. Droser
Affiliation:
Department of Earth and Planetary Sciences, University of California, Riverside, California 92521, USA. E-mail: [email protected]
*
*Corresponding author.
Get access Rights & Permissions [Opens in a new window]

Abstract

Constraining patterns of growth using directly observable and quantifiable characteristics can reveal a wealth of information regarding the biology of the Ediacara biota—the oldest macroscopic, complex community-forming organisms in the fossil record. However, these rely on individuals captured at an instant in time at various growth stages, and so different interpretations can be derived from the same material. Here we leverage newly discovered and well-preserved Dickinsonia costata Sprigg, 1947 from South Australia, combined with hundreds of previously described specimens, to test competing hypotheses for the location of module addition. We find considerable variation in the relationship between the total number of modules and body size that cannot be explained solely by expansion and contraction of individuals. Patterns derived assuming new modules differentiated at the anterior result in numerous examples in which the oldest module(s) must decrease in size with overall growth, potentially falsifying this hypothesis. Observed polarity as well as the consistent posterior location of defects and indentations support module formation at this end in D. costata. Regardless, changes in repeated units with growth share similarities with those regulated by morphogen gradients in metazoans today, suggesting that these genetic pathways were operating in Ediacaran animals.

Type
Articles
Information
Paleobiology , Volume 48 , Issue 1 , February 2022 , pp. 83 - 98
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of 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

Literature Cited

Adamska, M., Degnan, S. M., Green, K. M., Adamski, M., Craigie, A., Larroux, C., and Degnan, B. M.. 2007. Wnt and TGF-ß expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning. PLoS ONE 10:e1031.CrossRefGoogle Scholar
Aulehla, A., and Pourquié, O.. 2010. Signal gradients during paraxial mesoderm development. Cold Spring Harbor Perspectives in Biology 2:a000869.CrossRefGoogle ScholarPubMed
Averbukh, I., Ben-Zvi, D., Mishra, S., and Barkai, N.. 2014. Scaling morphogen gradients during tissue growth by a cell division rule. Development 141:2150–2156.CrossRefGoogle ScholarPubMed
Babonis, L. S., and Martindale, M. Q.. 2016. Phylogenetic evidence for the modular evolution of metazoan signalling pathways. Philosophical Transactions of the Royal Society of London 372:20150477.CrossRefGoogle Scholar
Boag, T. H., Darroch, S. A., S. A., and Laflamme, M.. 2016. Ediacaran distributions in space and time: testing assemblage concepts of earliest macroscopic body fossils. Paleobiology 42:574–594.CrossRefGoogle Scholar
Bobrovskiy, I., Hope, J. M., Ivantsov, A., Nettersheim, B. J., Hallmann, C., and Brocks, J. J.. 2018. Ancient steroids establish the Ediacaran fossil Dickinsonia as one of the earliest animals. Science 361:1246–1249.CrossRefGoogle ScholarPubMed
Bobrovskiy, I. A. Krasnova, A. Ivantsov, E. Luzhnaya, and J. J. Brocks, . 2019. Simple sediment rheology explains the Ediacara biota preservation. Nature Ecology and Evolution 3:582–589.CrossRefGoogle ScholarPubMed
Brasier, M. D., and Antcliffe, J. B.. 2008. Dickinsonia from Ediacara: a new look at morphology and body construction. Palaeogeography, Palaeoclimatology, Palaeoecology 270:311–323.CrossRefGoogle Scholar
Degnan, B. M., Leys, S. P., and Larroux, C.. 2005. Sponge development and antiquity of animal pattern formation. Integrative and Comparative Biology. 45:335–341.CrossRefGoogle ScholarPubMed
Droser, M. L., Gehling, J. G., Tarhan, L. G., Evans, S. D., Hall, C. M., Hughes, I. V., Hughes, E. B., et al. 2019. Piecing together the puzzle of the Ediacara Biota: excavation and reconstruction at the Ediacara National Heritage site Nilpena (South Australia). Palaeogeography, Palaeoclimatology, Palaeoecology 513:132–145.CrossRefGoogle Scholar
DuBuc, T. Q., Ryan, J. F., and Martindale, M. Q.. 2019. “Dorsal–ventral” genes are part of an ancient axial patterning system: evidence from Trichoplax adhaerens (Placozoa). Molecular Biology and Evolution. 36:966–973.CrossRefGoogle Scholar
Dunn, F. S., Liu, A. G., and Donoghue, P. C. J.. 2018. Ediacaran developmental biology, Biological Reviews, 93:914–932.CrossRefGoogle ScholarPubMed
Erwin, D. H. 2020. The origin of animal body plans: a view from fossil evidence and the regulatory genome. Development 147:dev182899.CrossRefGoogle ScholarPubMed
Evans, S. D., Droser, M. L., and Gehling, J. G.. 2015. Dickinsonia liftoff: evidence of current derived morphologies. Palaeogeography, Palaeoclimatology, Palaeoecology 434:28–33.CrossRefGoogle Scholar
Evans, S. D., Droser, M. L., and Gehling, J. G.. 2017. Highly regulated growth and development of the Ediacara macrofossil Dickinsonia costata. PLoS ONE 12:e0176874.CrossRefGoogle ScholarPubMed
Evans, S. D., Dzaugis, P. W., Droser, M. L., and Gehling, J. G.. 2018. You can get anything you want from Alice's Restaurant Bed: exceptional preservation and an unusual fossil assemblage from a newly excavated bed (Ediacara Member, Nilpena, South Australia). Australian Journal of Earth Sciences 67:873–883.CrossRefGoogle Scholar
Evans, S. D., Gehling, J. G., and Droser, M. L.. 2019a. Slime travelers: early evidence of animal mobility and feeding in an organic mat world. Geobiology 17:490–509.CrossRefGoogle Scholar
Evans, S. D., Huang, W., Gehiling, J. G., Kisailus, D., and Droser, M. L.. 2019b. Stretched, mangled, and torn: responses of the Ediacaran fossil Dickinsonia to variable forces. Geology 47:1049–1053.CrossRefGoogle Scholar
Finnerty, J. R. 2005. Did internal transport, rather than locomotion, favor the evolution of bilateral symmetry in animals? BioEssays 27:1174–1180.CrossRefGoogle ScholarPubMed
Finnerty, J. R., Pang, K., Burton, P., Paulson, D., and Martindale, M. Q.. 2004. Origins of bilateral symmetry: Hox and Dpp expression in a sea anemone. Science 304:1335–1337.CrossRefGoogle Scholar
Fischer, A., and Dorresteijn, A.. 2004. The polychaete Platynereis dumerilii (Annelida): a laboratory animal with spilarian cleavage, lifelong segment proliferation and a mixed benthic/pelagic life cycle. BioEssays 26:314–325.CrossRefGoogle Scholar
Fischer, A. H. L., Henrich, T., and Arendt, D.. 2010. The normal development of Platynereis dumerilii (Nereididae, Annelida). Frontiers in Zoology 7:31.CrossRefGoogle Scholar
Gehling, J. G. 1999. Microbial mats in terminal Proterozoic siliciclastics; Ediacaran death masks. Palaios 14:40–57.CrossRefGoogle Scholar
Gehling, J. G. 2000. Environmental interpretation and a sequence stratigraphic framework for the terminal Proterozoic Ediacara Member within the Rawnsley Quartzite, South Australia. Precambrian Research 100:65–95.CrossRefGoogle Scholar
Gehling, J. G., and Droser, M. L.. 2009. Textured organic surfaces associated with the Ediacara biota in South Australia. Earth-Science Reviews 96:196–206.CrossRefGoogle Scholar
Gehling, J. G., and Droser, M. L.. 2013. How well do fossil assemblages of the Ediacara Biota tell time? Geology 41:447–450.CrossRefGoogle Scholar
Gehling, J. G., Droser, M. L., Jensen, S., and Runnegar, B. N.. 2005. Ediacaran organisms: relating form to function. Pp. 43–66 in Briggs, D. E. G., ed. Evolving form and function: fossils and development, proceedings of a symposium honoring Adolf Seilacher for his contributions to palaeontology in celebration of his 80th birthday. Peabody Museum of Natural History, New Haven, Conn.Google Scholar
Glaessner, M. F., and Wade, M.. 1966. The late Precambrian fossils from Ediacara, South Australia. Palaeontology 9:599–628.Google Scholar
Gold, D. A., Runnegar, B., Gehling, J. G., and Jacobs, D. K.. 2015. Ancestral state reconstruction of ontogeny supports a bilaterian affinity for Dickinsonia. Evolution and Development 17:315–324.CrossRefGoogle ScholarPubMed
Grazhdankin, D. 2014. Patterns of evolution of the Ediacaran soft-bodied biota. Journal of Paleontology 88:269–283.CrossRefGoogle Scholar
Gurdon, J. B., and Bourillot, P.-Y.. 2001. Morphogen gradient interpretation. Nature 413:797–803.CrossRefGoogle ScholarPubMed
Hannibal, R. L., and Patel, N. H.. 2013. What is a segment? EvoDevo 4:35.CrossRefGoogle ScholarPubMed
Hoekzema, R. S., Brasier, M. D., Dunn, F. S., and Liu, A. G.. 2017. Quantitative study of developmental biology confirms Dickinsonia as a metazoan. Proceedings of the Royal Society of London 284:20171348.Google ScholarPubMed
Holley, S. A., Jackson, P. D., Sasai, Y., Lu, B., De Robertis, E. M., Hoffmann, F. M., and Ferguson, E. L.. 1995. A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature 376:249–253.CrossRefGoogle ScholarPubMed
Ivanstov, A. Y. 2007. Small Vendian transversely articulated fossils. Paleontological Journal 41:113–122.Google Scholar
Ivantsov, A. Y., and Malakhovskaya, Y. E.. 2002. Giant traces of Vendian animals. Doklady Earth Sciences 385:618–622.Google Scholar
Ivantsov, A. Y., Zakrevskaya, M. A., and Nagovitsyn, A. L.. 2019. Morphology of integuments of the Precambrian animals, Proarticulata. Invertebrate Zoology 16:19–26.CrossRefGoogle Scholar
Ivantsov, A. Y., Zakrevskaya, M. A., Nagovitsyn, A. L., Krasnova, A., Bobrovskiy, I., and Luzhnaya, E.. 2020. Intravital damage to the body of Dickinsonia (Metazoa of the late Ediacaran). Journal of Paleontology 94:1019–1033.CrossRefGoogle Scholar
Jacobs, D. K., Hughes, N. C., Fitz-Gibbon, S. T., and Winchell, C. J.. 2005. Terminal addition, the Cambrian radiation and the Phanerozoic evolution of bilaterian form. Evolution and Development 7:498–514.CrossRefGoogle ScholarPubMed
Jenkins, R. J. F. 1992. Functional and ecological aspects of Ediacaran assemblages. Pp. 131–176 in Lipps, J. H. and Signor, P.W., eds. Origin and evolution of the Metazoa. Springer Science, Business Media, New York.CrossRefGoogle Scholar
Keller, B. M., and Fedonkin, M. A.. 1977. New organic fossil finds in the Precambrian Valday series along the Syuz'ma River. International Geology Review 19:924–930.CrossRefGoogle Scholar
Kusserow, A., Pang, K., Sturm, C., Hrouda, M., Lentfer, J., Schmidt, H. A., Technau, U., et al. 2005. Unexpected complexity of the Wnt gene family in a sea anemone. Nature 433:156–160.CrossRefGoogle Scholar
McMahon, W. J., Liu, A. G., Tindal, B. H., and Kleinhans, M. G.. 2020. Ediacaran life close to land: coastal and shoreface habitats of the Ediacaran macrobiota, the Central Flinders ranges, South Australia. Journal of Sedimentary Research 90:1463–1499.CrossRefGoogle Scholar
Minelli, A., and Fusco, G.. 2004. Evo-devo perspectives on segmentation: model organisms, and beyond. Trends in Ecology and Evolution 19:423–429.CrossRefGoogle ScholarPubMed
Niehrs, C. 2010. On growth and form: a Cartesian coordinate system of Wnt and BMP signaling specifies bilaterian body axes. Development 137:845–857.CrossRefGoogle ScholarPubMed
Nielsen, C., Brunet, T., and Arendt, D.. 2018. Evolution of the bilaterian mouth and anus. Nature Ecology & Evolution 2:1358–1376.CrossRefGoogle ScholarPubMed
Pang, K., Ryan, J. F., NISC Comparative Sequencing Program, Mullikin, J. C., Baxevanis, A. D., and Martindale, M. Q.. 2010. Genomic insights into Wnt signaling in an early diverging metazoan, the ctenophore Mnemiopsis leidyi. EvoDevo 1:10.CrossRefGoogle Scholar
Reid, L. M., Holmes, J. D., Payne, J. L., García-Bellido, D. C., and Jago, J. B.. 2020. Taxa, turnover and taphofacies: a preliminary analysis of facies-assemblage relationships in the Ediacara Member (Flinders Ranges, South Australia). Australian Journal of Earth Sciences 67:905–914.CrossRefGoogle Scholar
Rentzsch, F., and Technau, U.. 2016. Genomics and development of Nematostella vectensis and other anthozoans. Current Opinions in Genetics & Development 39:63–70.CrossRefGoogle ScholarPubMed
Retallack, G. J. 2007. Growth, decay and burial compaction of Dickinsonia, an iconic Ediacaran fossil. Alcheringa 31:215–240.CrossRefGoogle Scholar
Runnegar, B. 1982. Oxygen requirements, biology and phylogenetic significance of the late Precambrian worm Dickinsonia, and the evolution of the burrowing habit. Alcheringa 6:223–239.CrossRefGoogle Scholar
Schwank, G., and Basler, K.. 2010. Regulation of organ growth by morphogen gradients. Cold Spring Harbor Perspectives in Biology 2:a001669.CrossRefGoogle ScholarPubMed
Seilacher, A., Grazhdankin, D., and Legouta, A.. 2003. Ediacaran biota: the dawn of animal life in the shadow of giant protists. Paleontological Research 7:43–54.CrossRefGoogle Scholar
Sperling, E. A., and Vinther, J.. 2010. A placozoan affinity for Dickinsonia and the evolution of late Proterozoic metazoan feeding modes. Evolution and Development 12:201–209.CrossRefGoogle ScholarPubMed
Sprigg, R. 1947. Early Cambrian (?) jellyfishes from the Flinders Ranges, South Australia. Transactions of the Royal Society, South Australia 71:212–224.Google Scholar
Sprigg, R. 1949. Early Cambrian “jellyfishes” of Ediacara, South Australia and Mount John, Kimberley District, Western Australia. Transactions of the Royal Society, South Australia 73:72–99.Google Scholar
Tarhan, L. G., Hood, A., Droser, M. L., Gehling, J. G., and Briggs, D. E. G.. 2016. Exceptional preservation of soft-bodied Ediacara Biota promoted by silica-rich oceans. Geology 44:951–954.CrossRefGoogle Scholar
Tarhan, L. G., Droser, M. L., Gehling, J. G., and Dzaugis, M. P.. 2017. Microbial mat sandwiches and other anactualistic sedimentary features of the Ediacara Member (Rawnsley Quartzite, South Australia): implications for interpretation of the Ediacaran sedimentary record. Palaios 32:181–194.CrossRefGoogle Scholar
Wade, M. 1972. Dickinsonia: polychaete worms from the late Precambrian Ediacaran fauna, South Australia. Memoirs of the Queensland Museum 16:171–190.Google Scholar
Zakrevskaya, M. A., and Ivantsov, A. Y.. 2017. Dickinsonia costata—the first evidence of neoteny in Ediacaran organisms. Invertebrate Zoology 14:92–98.CrossRefGoogle Scholar