Hostname: page-component-76fb5796d-5g6vh Total loading time: 0 Render date: 2024-04-25T08:47:54.372Z Has data issue: false hasContentIssue false
  • English
  • Français

A vaucheriacean alga from the middle Neoproterozoic of Spitsbergen: implications for the evolution of Proterozoic eukaryotes and the Cambrian explosion

Published online by Cambridge University Press:  08 February 2016

Nicholas J. Butterfield
Nicholas J. Butterfield*
Affiliation:
Department of Earth Sciences, University of Cambridge, Cambridge CB2 3EQ, United Kingdom. E-mail: njb1005@esc.cam.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

A morphologically diverse assemblage of organic-walled fossils from the middle Neoproterozoic Svanbergfjellet Formation, Spitsbergen, is identified as a monospecific assemblage representing the Gongrosira-phase of a vaucheriacean xanthophyte alga. As such, it provides a range of additional criteria with which to identify fossil vaucheriaceans and confirms the identification of Palaeovaucheria in the Mesoproterozoic Lakhanda Formation. Pronounced taxonomic inflation, through the practice of form-taxonomy, suggests that overall estimates of eukaryotic diversity in the Proterozoic need to be adjusted downward. Combined with positive evidence for low levels of speciation and extended stasis, pre-Cambrian eukaryotes are seen to evolve at a fundamentally lower rate than their Phanerozoic counterparts. This slower turnover accounts for the “delayed” appearance of animals without appeal to external triggers or constraints. The Cambrian acceleration of evolutionary rates was a direct consequence of newly introduced animals, whereas the much slower overall rates of the Proterozoic imply an absence of earlier metazoans.

Type
Articles
Information
Paleobiology , Volume 30 , Issue 2 , Spring 2004 , pp. 231 - 252
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

Literature Cited

Adams, D. G., and Duggan, P. S. 1999. Tansley Review No. 107. Heterocyst and akinete differentiation in cyanobacteria. New Phytologist 144:3–33.CrossRefGoogle Scholar
Amthor, J. E., Grotzinger, J. P., Schröder, S., Bowring, S. A., Ramezani, J., Martin, M. W., and Matter, A. 2003. Extinction of Cloudina and Namacalathus at the Precambrian-Cambrian boundary in Oman. Geology 31:431–434.2.0.CO;2>CrossRefGoogle Scholar
Anbar, A. D., and Knoll, A. H. 2002. Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297:1137–1142.CrossRefGoogle ScholarPubMed
Bailey, J. C., and Andersen, R. A. 1998. Phylogenetic relationships among nine species of the Xanthophyceae inferred from rbcL and 18S rRNA gene sequences. Phycologia 37:458–466.CrossRefGoogle Scholar
Ben Ali, A., De Baere, R., De Wachter, R., and Van de Peer, Y. 2002. Evolutionary relationships among heterokont algae (the autotrophic stramenopiles) based on combined analyses of small and large subunit ribosomal RNA. Protist 153:123–132.CrossRefGoogle ScholarPubMed
Bloh, W. von, Bounama, C., and Franck, S. 2003. Cambrian explosion triggered by geosphere-biosphere feedbacks. Geophysical Research Letters 30:CLM 6-1-CLM 6-5 (doi: 10.1029/2003GL017928, 2003).Google Scholar
Brasier, M. D. 1992. Nutrient-enriched waters and the early skeletal fossil record. Journal of the Geological Society, London 149:621–629.CrossRefGoogle Scholar
Budd, G. E., and Jensen, S. 2000. A critical reappraisal of the fossil record of the bilaterian phyla. Biological Reviews 75:253–295.CrossRefGoogle ScholarPubMed
Butterfield, N. J. 1995. Secular distribution of Burgess Shale-type preservation. Lethaia 28:1–13.CrossRefGoogle Scholar
Butterfield, N. J. 1997. Plankton ecology and the Proterozoic-Phanerozoic transition. Paleobiology 23:247–262.CrossRefGoogle Scholar
Butterfield, N. J. 2000. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic-Neoproterozoic radiation of eukaryotes. Paleobiology 26:386–404.2.0.CO;2>CrossRefGoogle Scholar
Butterfield, N. J. 2001a. Explaining the Cambrian explosion: cause, consequence or coincidence? Earth System Processes, joint GSA/GSL meeting, Edinburgh, Programmes with Abstracts, p. 93–94.Google Scholar
Butterfield, N. J. 2001b. Paleobiology of the Mesoproterozoic Hunting Formation, Somerset Island, Canada. Precambrian Research 111:235–256.CrossRefGoogle Scholar
Butterfield, N. J. 2001c. Ecology and evolution of the Cambrian plankton. Pp. 200–216in Zhuravlev, A. Yu. and Riding, R., eds. Ecology of the Cambrian Radiation. Columbia University Press, New York.Google Scholar
Butterfield, N. J. 2003. Exceptional fossil preservation and the Cambrian Explosion. Integrative and Comparative Biology 43:166–177.CrossRefGoogle ScholarPubMed
Butterfield, N. J., and Chandler, F. W. 1992. Paleoenvironmental distribution of Proterozoic microfossils, with an example from the Agu Bay Formation, Baffin Island. Palaeontology 35:943–957.Google Scholar
Butterfield, N. J., Knoll, A. H., and Swett, K. 1994. Paleobiology of the Neoproterozoic Svanbergfjellet Formation, Spitsbergen. Fossils and Strata 34:1–84.CrossRefGoogle Scholar
Cavalier-Smith, T. 2002. The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. International Journal of Systematic and Evolutionary Microbiology 52:7–76.CrossRefGoogle ScholarPubMed
Ding, B., Itaya, A., and Woo, Y.-M. 1999. Plasmodesmata and cell-to-cell communication in plants. International Review of Cytology 190:251–316.CrossRefGoogle Scholar
Dunphy, M. E., McDevit, D. C., Lane, C. E., and Schneider, C. W. 2001. The survival of Vaucheria (Vaucheriaceae) propagules in desiccated New England riparian sediments. Rhodora 103:416–426.Google Scholar
Entwisle, T. J. 1987. An evaluation of taxonomic characters in the subsection Sessiles, section Corniculatae, of Vaucheria (Vaucheriaceae, Chrysophyta). Phycologia 26:297–321.CrossRefGoogle Scholar
Entwisle, T. J. 1988. An evaluation of taxonomic characters in the Vaucheria prona complex (Vaucheriaceae, Chrysophyta). Phycologia 27:183–200.CrossRefGoogle Scholar
Faizullin, M. Sh. 1998. New data on Baikalian microfossils of the Patom Upland. Russian Geology and Geophysics 39:338–347.Google Scholar
Fortey, R. A., Briggs, D. E. G., and Wills, M. A. 1996. The Cambrian evolutionary ‘explosion’: decoupling cladogenesis from morphological disparity. Biological Journal of the Linnean Society 57:13–33.Google Scholar
Fritsch, F. E. 1935. The structure and reproduction of the algae, Vol. 1. Cambridge University Press, London.Google Scholar
Golubic, S., and Hofmann, H. J. 1976. Comparison of Holocene and mid-Precambrian Entophysalidaceae (Cyanophyta) in stromatolitic algal mats: cell division and degradation. Journal of Paleontology 50:1074–1082.Google Scholar
Golubic, S., Sergeev, V. N., and Knoll, A. H. 1995. Mesoproterozoic Archaeoellipsoides: akinetes of heterocystous cyanobacteria. Lethaia 28:285–298.CrossRefGoogle ScholarPubMed
Grazhdankin, D. 2004. Patterns of distribution in the Ediacaran biotas: facies versus biogeography and evolution. Paleobiology 30:xx–xx. [this volume].2.0.CO;2>CrossRefGoogle Scholar
Halverson, G. P. 2000. A ‘phantom’ cap carbonate in the Neoproterozoic Grusdievbreen Formation, Akademikerbreen Group, northeastern Spitsbergen? Geological Society of America Abstracts with Programs 32:A144.Google Scholar
Harland, W. B. 1997. The geology of Svalbard. Geological Society of London, Memoir 17.Google Scholar
Hermann, T. N. 1981. Nitchatye mikroorganizmy Lakhandinskoi svity reki Mai. Paleontologicheskii Zhurnal 1981(2):126–131. [Filamentous microorganisms in the Lakhanda Formation on the Maya River. Paleontological Journal 1981(2):100–107.]Google Scholar
Hermann, T. N., and Timofeev, B. S. 1974. Mitoz i drevnikh vodoroslei. Pp. 5–6in Timofeev, B. V., ed. Mikrofitofossilii Proterozoia i Rannego Paleozoia SSSR. Nauka, Leningrad.Google Scholar
Hill, A. C., Cotter, K. L., and Grey, K. 2000. Mid-Neoproterozoic biostratigraphy and isotope stratigraphy in Australia. Precambrian Research 100:281–298.CrossRefGoogle Scholar
Hoffman, P. F., Kaufman, A. J., Halverson, G. P., and Schrag, D. P. 1998. A Neoproterozoic Snowball Earth. Science 281:1342–1346.CrossRefGoogle ScholarPubMed
Hofmann, H. J. 1985. The mid-Proterozoic Little Dal macrobiota, Mackenzie Mountains, north-west Canada. Palaeontology 28:331–354.Google Scholar
Hofmann, H. J. 1999. Global distribution of the Proterozoic sphaeromorph acritarch Valeria lophostriata (Jankauskas). Acta Micorpalaeontologica Sinica 16:215–224.Google Scholar
Holland, H. D. 2002. Volcanic gases, black smokers, and the Great Oxidation Event. Geochemica et Cosmochemica Acta 66:3811–3826.CrossRefGoogle Scholar
Horodyski, R. J., Bloeser, B., and Haar, S. Vonder 1977. Laminated algal mats from a coastal lagoon, Laguna Mormona, Baja California, Mexico. Journal of Sedimentary Petrology 47:680–696.Google Scholar
Jankauskas, T. V. 1980. Novye vodorocli iz verkhnego rifeia iuzhnogo Urala i Priuralia. Paleontologicheskii Zhurnal 1980(4):107–113. [New algae from the Upper Riphean of the southern Urals and the Ural forelands. Paleontological Journal 1980(4):113–121.]Google Scholar
Jankauskas, T. V., ed. 1989. Mikrofossilii Dokembriia SSSR. Nauka, Leningrad.Google Scholar
Javaux, E. J., Knoll, A. H., and Walter, M. R. 2001. Morphological and ecological complexity in early eukaryotic ecosystems. Nature 412:66–69.CrossRefGoogle ScholarPubMed
Jankauskas, T. V. 2003. Recognizing and interpreting the fossils of early eukaryotes. Origins of Life and Evolution of the Biosphere 33:75–94.Google Scholar
Kennedy, M. J., Runnegar, B., Prave, A. R., Hoffmann, K. H., and Arthur, M. 1998. Two or four Neoproterozoic glaciations? Geology 26:1059–1063.2.3.CO;2>CrossRefGoogle Scholar
Knoll, A. H. 1994. Proterozoic and Early Cambrian protists: evidence for accelerating evolutionary tempo. Proceedings of the National Academy of Sciences USA 91:6743–6750.CrossRefGoogle ScholarPubMed
Knoll, A. H. 1996. Archean and Proterozoic paleontology. Pp. 51–80in Jansonius, J. and McGregor, D. C., eds. Palynology: principles and applications, Vol. 1. American Association of Stratigraphic Palynologists Foundation, Dallas.Google Scholar
Knoll, A. H. 2000. Learning to tell Neoproterozoic time. Precambrian Research 100:3–20.CrossRefGoogle ScholarPubMed
Knoll, A. H., and Carroll, S. B. 1999. Early animal evolution: emerging views from comparative biology and geology. Science 284:2129–2137.CrossRefGoogle ScholarPubMed
Kumar, S. 2001. Mesoproterozoic megafossil Chuaria-Tawuia association may represent parts of a multicellular plant, Vindyan Supergroup, Central India. Precambrian Research 106:187–211.CrossRefGoogle Scholar
Nagovitsin, K. E. 2000. New Late Riphean composite microfossils from the Yenisei Ridge (East Siberia). Paleontologicheskii Zhurnal 2001(3):5–13.Google Scholar
Narbonne, G. M., and Gehling, J. G. 2003. Life after snowball: the oldest complex Ediacaran fossils. Geology 31:27–30.2.0.CO;2>CrossRefGoogle Scholar
Niklas, K. J. 2000. The evolution of plant body plans—a bio-mechanical perspective. Annals of Botany 85:411–438.CrossRefGoogle Scholar
Poole, A. M., Phillips, M. J., and Penny, D. 2003. Prokaryote and eukaryote evolvability. Biosystems 69:163–185.CrossRefGoogle ScholarPubMed
Porter, S. M., and Knoll, A. H. 2000. Testate amoebae in the Neoproterozoic era: evidence from vase-shaped microfossils in the Chuar Group, Grand Canyon. Paleobiology 26:360–385.2.0.CO;2>CrossRefGoogle Scholar
Porter, S. M., Meisterfeld, R., and Knoll, A. H. 2003. Vase-shaped microfossils from the Neoproterozoic Chuar Group, Grand Canyon: a classification guided by modern testate amoebae. Journal of Paleontology 77:409–429.2.0.CO;2>CrossRefGoogle Scholar
Potter, D., Saunders, G. W., and Andersen, R. A. 1997. Phylogenetic relationships of the Raphidophyceae and Xanthophyceae as inferred from nucleotide sequences of the 18S ribosomal RNA gene. American Journal of Botany 84:966–972.CrossRefGoogle ScholarPubMed
Puymaly, A. 1922. Reproduction de Vaucheria par zoospores amiboides. Comptes Rendus de l'Académie des Sciences, Paris 174:824–827.Google Scholar
Rainbird, R. H., Stern-Richard, A., Khudoley, A. K., Kropachev, A. P., Heaman, L. M., and Sukhorukov, V. Iu. 1998. U-Pb geochronology of Riphean sandstone and gabbro from Southeast Siberia and its bearing on the Laurentia-Siberia connection. Earth and Planetary Science Letters 164:409–420.CrossRefGoogle Scholar
Rasmussen, B., Bengtson, S., Fletcher, I. R., and McNaughton, N. J. 2002a. Discoidal impressions and trace-like fossils more than 1200 million years old. Science 296:1112–1115.CrossRefGoogle ScholarPubMed
Rasmussen, B., Bengtson, S., Fletcher, I. R., and McNaughton, N. J. 2002b. Ancient animals or something else entirely? Science 298:57–58.Google Scholar
Samuelsson, J., and Butterfield, N. J. 2001. Neoproterozoic fossils from the Franklin Mountains, northwestern Canada: stratigraphic, palaeoenvironmental and palaeobiological implications. Precambrian Research 107:235–251.CrossRefGoogle Scholar
Schluter, D. 2000. The ecology of adaptive radiation. Oxford University Press, Oxford.CrossRefGoogle Scholar
Seilacher, A., Pose, P. K., and Pflüger, F. 1998. Triploblastic animals more than 1 billion years ago: trace fossil evidence from India. Science 282:80–83.CrossRefGoogle ScholarPubMed
Sepkoski, J. J. Jr. 1993. 10 years in the library—new data confirm paleontological patterns. Paleobiology 19:43–51.CrossRefGoogle Scholar
Sepkoski, J. J. Jr., and Kendrick, D. C. 1993. Numerical experiments with model monophyletic and paraphyletic taxa. Paleobiology 19:168–184.CrossRefGoogle ScholarPubMed
Stahl, E. 1879. Ueber die Ruhezustände der Vaucheria geminata. Botanische Zeitung 37:129–137.Google Scholar
Stanley, S. M. 1973. An ecological theory for the sudden origin of multicellular life in the late Precambrian. Proceedings of the National Academy of Sciences, U.S.A. 70:1486–1489.CrossRefGoogle ScholarPubMed
Stanley, S. M. 1976. Ideas on the timing of metazoan diversification. Paleobiology 2:209–219.CrossRefGoogle Scholar
Stanley, S. M. 1979. Macroevolution: pattern and process. W. H. Freeman, San Francisco.Google Scholar
Summons, R. E., Jahnke, L. L., Hope, J. M., and Logan, G. A. 1999. 2-methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 400:554–557.CrossRefGoogle ScholarPubMed
Timofeev, B. V., and Hermann, T. N. 1974. Mitoz u rifeyskikh vodoroslei. Geologicky Sbornik 25:167–172.Google Scholar
Timofeev, B. V., and Hermann, T. N. 1979. Dokembriiiskaia mikrobiota Lakhandinskoi svity. Pp. 137–147in Sokolov, B. S., ed. Paleontologiia Dokembriia i Rannego Kembriia. Nauka, Leningrad.Google Scholar
Vermeij, G. J. 1995. Economics, volcanoes, and Phanerozoic revolutions. Paleobiology 21:125–152.CrossRefGoogle Scholar
Vermeij, G. J., and Lindberg, D. R. 2000. Delayed herbivory and the assembly of marine benthic ecosystems. Paleobiology 26:419–430.2.0.CO;2>CrossRefGoogle Scholar
Vidal, G., and Vidal, M. Moczydlowska 1997. Biodiversity, speciation, and extinction trends of Proterozoic and Cambrian phytoplankton. Paleobiology 23:230–246.CrossRefGoogle Scholar
Walter, M. R., Veever, J. J., Calver, C. R., Gorjan, P., and Hill, A. C. 2000. Dating the 840–544 Ma Neoproterozoic interval by isotopes of strontium, carbon, and sulfur in seawater, and some interpretive models. Precambrian Research 100:371–433.CrossRefGoogle Scholar
Wittrock, V., and Nordstedt, O. 1882. Algae aquae dulcis exsiccatae praecipue Scandinavicae, Vol. 10. P. A. Norstedt, Stockholm.Google Scholar
Woods, K. N., Knoll, A. H., and German, T. 1998. Xanthophyte algae from the Mesoproterozoic/Neoproterozoic transition: confirmation and evolutionary implications. Geological Society of America, Abstracts with Programm 30:232.Google Scholar
Wray, G. A., Levinton, J. S., and Shapiro, L. M. 1996. Molecular evidence for deep pre-Cambrian divergences among metazoan phyla. Science 214:568–573.CrossRefGoogle Scholar
Yoon, H. S., Hackett, J. D., Pinto, G., and Bhattacharya, D. 2002. The single, ancient origin of chromist plastids. Proceedings of the National Academy of Sciences USA 99:15507–15512.CrossRefGoogle ScholarPubMed