Skip to main content Accessibility help
×
Home

The fossil record of early eukaryotic diversification

  • Susannah M. Porter (a1)

Abstract

The Cambrian explosion can be thought of as the culmination of a diversification of eukaryotes that had begun several hundred million years before. Eukaryotes - one of the three domains of life — originated by late Archean time, and probably underwent a long period of stem group evolution during the Paleoproterozoic Era. A suite of taxonomically resolved body fossils and biomarkers, together with estimates of acritarch and compression fossil diversity, suggest that while divergences among major eukaryotic clades or 'super-groups' may have occurred as early as latest Paleoproterozoic through Mesoproterozoic time, the main phase of eukaryotic diversification took place several hundred million years later, during the middle Neoproterozoic Era. Hypotheses for Neoproterozoic diversification must therefore explain why eukaryotic diversification is delayed several hundred million years after the origin of the eukaryotic crown group, and why diversification appears to have occurred independently within several eukaryotic super-groups at the same time. Evolutionary explanations for eukaryotic diversification (the evolution of sex; the acquisition of plastids) fail to account for these patterns, but ecological explanations (the advent of microbial predators) and environmental explanations (changes in ocean chemistry) are both consistent with them. Both ecology and environment may have played a role in triggering or at least fueling Neoproterozoic eukaryotic diversification.

Copyright

References

Hide All
Allison, C. W., and Hilgert, J. W. 1986. Scale microfossils from the Early Cambrian of Northwest Canada. Journal of Paleontology, 60:9731015.
Anbar, A. D., and Knoll, A. H. 2002. Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science, 297:11371142.
Andersson, J. O., and Roger, A. J. 2002. A cyanobacterial gene in nonphotosynthetic protists — an early chloroplast acquisition in eukaryotes? Current Biology, 12:115119.
Baldauf, S. L. 2003. The deep roots of eukaryotes. Science, 300:17031706.
Bartley, J. K., Knoll, A. H., Grotzinger, J. P., and Sergeev, V. N. 2000. Lithification and fabric genesis in precipitated stromatolites and associated peritidal carbonates, Mesoproterozoic Billyakh Group, Siberia, p. 5973. In Grotzinger, J. P. and James, N. P. (eds.), Carbonate Sedimentation and Diagenesis in the Evolving Precambrian World. SEPM special publication no. 67.
Bartley, J. K., Semikhatov, M. A., Kaufman, A. J., Knoll, A. H., Pope, M. C., and Jacobsen, S. B. 2001. Global events across the Mesoproterozoic-Neoproterozoic boundary: C and Sr isotopic evidence from Siberia. Precambrian Research, 111:165202.
Bartley, J. K., and Kah, L. 2004. Marine carbon reservoir, Corg-Ccarb coupling, and the evolution of the Proterozoic carbon cycle. Geology, 32:129132.
Bengtson, S., and Morris, S. C. 1992. Early radiation of biomineralizing phyla. In Lipps, J. and Signor, P. (eds.), Origin and Early Evolution of the Metazoa. Plenum Press, New York.
Bengtson, S. 1994. The advent of animal skeletons. In Bengtson, S. (ed.), Early Life on Earth. Columbia University Press, New York.
Boraas, M., Seale, D., and Boxhorn, J. 1998. Phagotrophy by a flagellate selects for colonial prey: a possible origin of multicellularity. Evolutionary Ecology, 12:153164.
Bottjer, D. J., and Ausich, W. I. 1986. Phanerozoic development of tiering in soft substrata suspension-feeding communities. Paleobiology, 12:400420.
Brasier, M. D., and Lindsay, J. F. 1998. A billion years of environmental stability and the emergence of eukaryotes: new data from northern Australia. Geology, 26:555558.
Brocks, J. J., Logan, G. A., Buick, R., and Summons, R. E. 1999. Archean molecular fossils and the early rise of eukaryotes. Science, 285:10331036.
Brocks, J. J., Buick, R., Summons, R. E., and Logan, G. A. 2003. A reconstruction of Archean biological diversity based on molecular fossils from the 2.78 to 2.45 billion-year-old Mount Bruce Supergroup, Hamersley Basin, Western Australia. Geochimica et Cosmochimica Acta, 67:43214335.
Budd, G. E., and Jensen, S. 2000. A critical reappraisal of the fossil record of the bilaterian phyla. Biological Reviews, 75:253295.
Buick, R., Des Marais, D. J., and Knoll, A. H. 1995. Stable isotopic compositions of carbonates from Mesoproterozoic Bangemall Group, northwestern Australia. Chemical Geology, 123:153171.
Butterfield, N., Knoll, A., and Swett, K. 1990. A bangiophyte red alga from the Proterozoic of arctic Canada. Science, 250:104107.
Butterfield, N. J., and Chandler, F. W. 1992. Palaeoenvironmental distribution of Proterozoic microfossils, with an example from the Agu Bay Formation, Baffin Island. Palaeontology, 35:943957.
Butterfield, N. J., Knoll, A. H., and Swett, K. 1994. Paleobiology of the Neoproterozoic Svanbergfjellet Formation, Spitsbergen. Fossils and Strata, 34:184.
Butterfield, N. 2000. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic-Neoproterozoic radiation of eukaryotes. Paleobiology, 26(3):386404.
Butterfield, N. J. 2004. A vaucheriacean alga from the middle Neoproterozoic of Spitsbergen: implications for the evolution of Proterozoic eukaryotes and the Cambrian explosion. Paleobiology, 30:231252.
Butterfield, N. J. In press. Probable Proterozoic Fungi. Paleobiology.
Canfield, D. E. 1998. A new model for Proterozoic ocean chemistry. Nature, 396:450453.
Cavalier-Smith, T. 2002a. The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. International Journal of Systematics, Evolution, and Microbiology, 52:776.
Cavalier-Smith, T. 2002b. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. International Journal of Systematic and Evolutionary Microbiology, 52:297354.
Conway Morris, S. 1986. The community structure of the Middle Cambrian Phyllopod Bed (Burgess Shale). Palaeontology, 29:423467.
Fast, N. M., Kissinger, J. C., Roos, D. S., and Keeling, P. J. 2001. Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Molecular Biology and Evolution, 18:418426.
Frank, T. D., Kah, L. C., and Lyons, T. W. 2003. Changes in organic matter production and accumulation as a mechanism for isotopic evolution in the Mesoproterozoic ocean. Geological Magazine, 140:397420.
German, T. 1981. Nitchatye mikroorganizmy Lakhandinskoi svity reki Mai [Filamentous microorganisms in the Lakhanda Formation on the Maya River]. Paleontologicheskii Zhurnal, 1981:100107.
German, T. N. 1990. Organic World Billion Year Ago. Nauka, Leningrad.
Gibbs, S. 1992. The evolution of algal chloroplasts. In Lewin, R. (ed.), Origins of plastids. Chapman and Hall, New York.
Grey, K., and Williams, I. R. 1990. Problematic bedding-plane markings from the Middle Proterozoic Manganese Subgroup, Bangemall Basin, Western Australia. Precambrian Research, 46:307327.
Grey, K., Walter, M., and Calver, C. 2003. Neoproterozoic biotic diversification: snowball Earth or aftermath of the Acraman impact? Geology, 31:459462.
Grotzinger, J. P. 1989. Facies and evolution of Precambrian depositional systems: emergence of the modern platform archetype, p. 79106. In Crevello, P. D., Wilson, J. J., Sarg, J. F., and Read, J. F. (eds.), Controls on Carbonate Platform and Basin Development. SEPM Special Publication no. 44.
Han, T.-M., and Runnegar, B. 1992. Megascopic eukaryotic algae from the 2.1-billion-year-old Negaunee Iron-Formation, Michigan. Science, 257:232235.
Harvey, H. R., and Mcmanus, G. B. 1991. Marine ciliates as a widespread source of tetrahymanol and hopan-3-beta-ol in sediments. Geochimica et Cosmochimica Acta, 55:33873390.
Hoffman, P. F., Kaufman, A. J., Halverson, G. P., Schrag, D. P. 1998. A Neoproterozoic snowball Earth. Science, 281:13421346.
Hoffman, P. F., and Schrag, D. P. 2002. The snowball Earth hypothesis: testing the limits of global change. Terra Nova, 14:129155.
Hofmann, H. J. 1994. Proterozoic carbonaceous compressions (“metaphytes” and “worms”). In Bengtson, S. (ed.), Early Life on Earth. Columbia University Press, New York.
Javaux, E. J., Knoll, A. H., and Walter, M. R. 2001. Morphological and ecological complexity in early eukaryotic ecosystems. Nature, 412:6669.
Javaux, E. J., Knoll, A. H., and Walter, M. 2003. Recognizing and interpreting the fossils of early eukaryotes. Origins of Life and the Biospshere, 33:7594.
Kah, L. C., and Knoll, A.H. 1996. Microbenthic distribution of Proterozoic tidal flats: environmental and taphonomic considerations. Geology, 24:7982.
Kah, L. C., Sherman, A. G., Narbonne, G. M., Knoll, A. H., and Kaufman, A. J. 1999. 13C stratigraphy of the Proterozoic Bylot Supergroup, Baffin Island, Canada: implications for regional lithostratigraphic correlations. Canadian Journal of Earth Sciences, 36:313332.
Kamaya, R., Mori, T., Shoji, H., Ageta, H., Chang, H. C., and Hsu, H. Y. 1991. Fern constituents: triterpenes from Oleandra wallichii . Yakugaku Zasshi (Journal of the Pharmaceutical Society of Japan), 11:120125.
Karlstrom, K. E., åhäll, K.-I., Harlan, S. S., Williams, M. L., Mclelland, J., and Geissman, J. W. 2001. Long-lived (1.8-1.0 Ga) convergent orogen in southern Laurentia, its extensions to Australia and Baltica, and implications for refining Rodinia. Precambrian Research, 111:530.
Kaufman, A. J., Knoll, A. H., and Awramik, S. M. 1992. Biostratigraphic and chemostratigraphic correlation of Neoproterozoic sedimentary successions: Upper Tindir Group, northwestern Canada, as a test case. Geology, 20:181185.
Kirschvink, J. L. 1992. Late Proterozoic low-latitude glaciation: the snowball Earth, p. 5152. In Schopf, J. W. and Klein, C. (eds.), The Proterozoic Biosphere. Cambridge University Press, Cambridge.
Kleemann, G., Poralla, K., Englert, G., Kjosen, H., Liaaen-Jensen, N., Neunlist, S., and Rohmer, M. 1990. Tetrahymanol from the phototrophic bacterium Rhodopseudomonas palustris: first report of a gammacerane triterpene from a prokaryote. Journal of General Microbiology, 136:25512553.
Knoll, A. H., Swett, K., and Mark, J. 1991. Paleobiology of a Neoproterozoic tidal flat/lagoonal complex: the Draken Conglomerate Formation, Spitsbergen. Journal of Paleontology, 65:531570.
Knoll, A. H. 1992. The early evolution of eukaryotes: a geological perspective. Science, 256:622627.
Knoll, A. H. 1994. Proterozoic and Early Cambrian protists: evidence for accelerating evolutionary tempo. Proceedings of the National Academy of Sciences, 91:67436750.
Knoll, A., and Carroll, S. 1999. Early animal evolution: emerging views from comparative biology and geology. Science, 284:21292137.
Kumar, S. 1995. Megafossils from the Mesoproterozoic Rohtas Fromation (the Vindhyan Supergroup), Katni Area, central India. Precambrian Research, 72:171184.
Moldowan, J. M., Jacobsen, S. R., Dahl, J., Al-Hajji, A., Huizinga, B. J., and Fago, F. J. 2001. Molecular fossils demonstrate Precambrian origins of dinoflagellates, p. 475493. In Zhuravlev, A. Y. and Riding, R. (eds.), The Ecology of the Cambrian Radiation. Columbia University Press, New York.
Nikolaev, S. I., Berney, C., Fahrni, J. F., Bolivar, I., Polet, S., Mylnikov, A. P., Aleshin, V. V., Petrov, N. B., and Pawlowski, J. 2004. The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes. Proceedings of the National Academy of Sciences USA, 101:80668071.
Ourisson, G., Rohmer, M., and Poralla, K. 1987. Prokaryotic hopanoids and other polyterpenoid sterol surrogates. Annual Reviews of Microbiology, 41:301333.
Paine, R. T. 1966. Food web complexity and species diversity. American Naturalist, 100:6575.
Peng, P., Sheng, G., Fu, J., and Yan, Y. 1998. Biological markers in 1.7 billion year old rock from the Tuanshanzi Formation, Jixian strata section, North China. Organic Geochemistry, 29:13211329.
Philippe, H., Lopez, P., Brinkmann, H., Budin, K., Germot, A., Laurent, J., Moreira, D., Müller, M., and Guyader, H. L. 2000. Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions. Proceedings of the Royal Society of London, Series B, 267:12131221.
Porter, S. M., and Knoll, A. H. 2000. Testate amoebae in the Neoproterozoic Era: evidence from vase-shapes microfossils in the Chuar Group, Grand Canyon. Paleobiology, 26:360385.
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, 77:409429.
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, 84:966972.
Pratt, L. M., Summons, R. E., and Hieshima, G. B. 1991. Sterane and triterpane biomarkers in the Precambrian Nonesuch Formation, North American Midcontinent Rift. Geochimica et Cosmochimica Acta, 55:911916.
Runnegar, B. 2000. Loophole for snowball Earth. Nature, 405:403404.
Schopf, J. W., Haugh, B. N., Molnar, R. E., and Satterthwait, D. F. 1973. On the development of metaphytes and metazoans. Journal of Paleontology, 47:19.
Schopf, J. W. 1992. Patterns of Proterozoic microfossil diversity: an initial, tentative, analysis, p. 529552. In Schopf, J. W. and Klein, C. (eds.), The Proterozoic Biosphere. Cambridge University Press, Cambridge.
Simpson, A. G. B., and Roger, A. J. 2002. Eukaryotic evolution: getting to the root of the problem. Current Biology, 12:R691R693.
Sogin, M. L. 1991. Early evolution and the origin of eukaryotes. Current Opinion in Genetics and Development, 1:457463.
Stanley, S. M. 1973. Ecological theory for the sudden origin of multicellular life in the late Precambrian. Proceedings of the National Academy of Sciences USA, 70:14861489.
Stechmann, A., and Cavalier-Smith, T. 2002. Rooting the eukaryote tree by using a derived gene fusion. Science, 297:8991.
Stechmann, A., and Cavalier-Smith, T. 2003. The root of the eukaryote tree pinpointed. Current Biology, 13:R665R666.
Summons, R. E., Brassell, S. C., Eglinton, G., Evans, E., Horodyski, R. J., Robinson, N., and Ward, D. M. 1988. Distinctive hydrocarbon biomarkers from fossiliferous sediment of the Late Proterozoic Walcott Member, Chuar Group, Grand Canyon, Arizona. Geochimica et Cosmochimica Acta, 52:26252637.
Summons, R. E., and Walter, M. R. 1990. Molecular fossils and microfossils of prokaryotes and protists from Proterozoic sediments. Amercian Journal of Science, 290-A:212244.
Summons, R. E., Thomas, J., Maxwell, J. R., and Boreham, C. J. 1992. Secular and environmental constraints on the occurrence of dinosterane in sediments. Geochimica et Cosmochimica Acta, 56:24372444.
Sutak, R., Dolezal, P., Fiumera, H., Hrdy, I., Dancis, A., Delgadillo-Correa, M., Johnson, P., Müller, M., and Tachezy, J. 2004. Mitochondrial-type aseembly of FeS centers in the hydrogenosomes of the amitochondriate eukaryote Trichomonas vaginalis . Proceedings of the National Academy of Sciences USA, 101:1036810373.
Tovar, J., León-Avila, G., Sánchez, L. B., Sutak, R., Tachezy, J., Van Der Giezen, M., Hernández, M., Müller, M., and Lucocq, J. M. 2003. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature, 426:172176.
Vidal, G., and Knoll, A. H. 1983. Proterozoic plankton. Geological Society of America Memoir, 161:265277.
Vidal, G., and Moczydlowska-Vidal, M. 1997. Biodiversity, speciation, and extinction trends of Proterozoic and Cambrian phytoplankton. Paleobiology, 23:230246.
Volkman, J. K., Barrett, S. M., Dunstan, G. A., and Jeffrey, S. W. 1993. Geochemical significance of the occurrence of dinosterol and other 4-methylsterols in a marine diatom. Organic Geochemistry, 20:715.
Wang, D., Kumar, S., and Hedges, S. 1999. Divergence time estimates for the early history of animal phyla and the origin of plants, animals and fungi. Proceedings of the Royal Society of London, Series B, 266:163171.
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 Programs, 30:A232.
Xiao, S. H., Knoll, A.H., and Yuan, X., 1998a. Morphological reconstruction of Miaohephyton bifurcatum, a possible brown alga from the Neoproterozoic Doushantuo Formation, South China. Journal of Paleontology, 72:10721086.
Xiao, S. H., Zhang, Y., and Knoll, A.H. 1998b. Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite. Nature, 391:553558.
Xiao, S. H., and Knoll, A.H., 2000. Phosphatized animal embryos from the Neoproterozoic Doushantuo Formation at Weng-An, Guizhou, South China. Journal of Paleontology, 74:767788.
Xiao, S., Yuan, X., Steiner, M., and Knoll, A. H. 2002. Macroscopic carbonaceous compressions in a terminal Proterozoic shale: a systematic reassessment of the Miaohe biota, South China. Journal of Paleontology, 76(2):347376.
Xiao, S. H., Knoll, M. A. H., Yuan, X., and Pueschel, C.M. 2004. Phosphatized multicellular algae in the Neoproterozoic Doushantuo Formation, China, and the early evolution of florideophyte red algae. American Journal of Botany, 91:214227.
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, 99:1550715512.
Yoon, H., Hackett, J., Ciniglia, C., Pinto, G., and Bhattacharya, D. 2004. A molecular timeline for the origin of photosynthetic eukaryotes. Molecular Biology and Evolution, 21:809818.
Zander, J. M., Caspi, E., Pandey, G. N., and Mitra, C. 1969. The presence of tetrahymanol in Oleandra wallichii . Phytochemistry, 8:22652267.

The fossil record of early eukaryotic diversification

  • Susannah M. Porter (a1)

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed