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The fossil record of early eukaryotic diversification

Published online by Cambridge University Press:  21 July 2017

Susannah M. Porter
Susannah M. Porter*
Affiliation:
Department of Geological Sciences, University of California, Santa Barbara, CA 93106
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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.

Type
Research Article
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The Paleontological Society Papers , Volume 10: Neoproterozoic-Cambrian Biological Revolutions , November 2004 , pp. 35 - 50
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Copyright © 2004 by The Paleontological Society 

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References

Allison, C. W., and Hilgert, J. W. 1986. Scale microfossils from the Early Cambrian of Northwest Canada. Journal of Paleontology, 60:973–1015.CrossRefGoogle Scholar
Anbar, A. D., and Knoll, A. H. 2002. Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science, 297:1137–1142.CrossRefGoogle ScholarPubMed
Andersson, J. O., and Roger, A. J. 2002. A cyanobacterial gene in nonphotosynthetic protists — an early chloroplast acquisition in eukaryotes? Current Biology, 12:115–119.Google Scholar
Baldauf, S. L. 2003. The deep roots of eukaryotes. Science, 300:1703–1706.Google Scholar
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. 59–73. In Grotzinger, J. P. and James, N. P. (eds.), Carbonate Sedimentation and Diagenesis in the Evolving Precambrian World. SEPM special publication no. 67.Google Scholar
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, 111:165–202.CrossRefGoogle Scholar
Bartley, J. K., and Kah, L. 2004. Marine carbon reservoir, Corg-Ccarb coupling, and the evolution of the Proterozoic carbon cycle. Geology, 32:129–132.Google Scholar
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.Google Scholar
Bengtson, S. 1994. The advent of animal skeletons. In Bengtson, S. (ed.), Early Life on Earth. Columbia University Press, New York.Google Scholar
Boraas, M., Seale, D., and Boxhorn, J. 1998. Phagotrophy by a flagellate selects for colonial prey: a possible origin of multicellularity. Evolutionary Ecology, 12:153–164.Google Scholar
Bottjer, D. J., and Ausich, W. I. 1986. Phanerozoic development of tiering in soft substrata suspension-feeding communities. Paleobiology, 12:400–420.Google Scholar
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, 26:555–558.2.3.CO;2>CrossRefGoogle ScholarPubMed
Brocks, J. J., Logan, G. A., Buick, R., and Summons, R. E. 1999. Archean molecular fossils and the early rise of eukaryotes. Science, 285:1033–1036.CrossRefGoogle ScholarPubMed
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, 67:4321–4335.Google Scholar
Budd, G. E., and Jensen, S. 2000. A critical reappraisal of the fossil record of the bilaterian phyla. Biological Reviews, 75:253–295.Google Scholar
Buick, R., Des Marais, D. J., and Knoll, A. H. 1995. Stable isotopic compositions of carbonates from Mesoproterozoic Bangemall Group, northwestern Australia. Chemical Geology, 123:153–171.CrossRefGoogle ScholarPubMed
Butterfield, N., Knoll, A., and Swett, K. 1990. A bangiophyte red alga from the Proterozoic of arctic Canada. Science, 250:104–107.Google Scholar
Butterfield, N. J., and Chandler, F. W. 1992. Palaeoenvironmental distribution of Proterozoic microfossils, with an example from the Agu Bay Formation, Baffin Island. Palaeontology, 35:943–957.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.Google Scholar
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):386–404.Google Scholar
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, 30:231–252.Google Scholar
Butterfield, N. J. In press. Probable Proterozoic Fungi. Paleobiology.Google Scholar
Canfield, D. E. 1998. A new model for Proterozoic ocean chemistry. Nature, 396:450–453.CrossRefGoogle Scholar
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, 52:7–76.Google Scholar
Cavalier-Smith, T. 2002b. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. International Journal of Systematic and Evolutionary Microbiology, 52:297–354.Google Scholar
Conway Morris, S. 1986. The community structure of the Middle Cambrian Phyllopod Bed (Burgess Shale). Palaeontology, 29:423–467.Google Scholar
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, 18:418–426.CrossRefGoogle ScholarPubMed
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, 140:397–420.Google Scholar
German, T. 1981. Nitchatye mikroorganizmy Lakhandinskoi svity reki Mai [Filamentous microorganisms in the Lakhanda Formation on the Maya River]. Paleontologicheskii Zhurnal, 1981:100–107.Google Scholar
German, T. N. 1990. Organic World Billion Year Ago. Nauka, Leningrad.Google Scholar
Gibbs, S. 1992. The evolution of algal chloroplasts. In Lewin, R. (ed.), Origins of plastids. Chapman and Hall, New York.Google Scholar
Grey, K., and Williams, I. R. 1990. Problematic bedding-plane markings from the Middle Proterozoic Manganese Subgroup, Bangemall Basin, Western Australia. Precambrian Research, 46:307–327.Google Scholar
Grey, K., Walter, M., and Calver, C. 2003. Neoproterozoic biotic diversification: snowball Earth or aftermath of the Acraman impact? Geology, 31:459–462.2.0.CO;2>CrossRefGoogle Scholar
Grotzinger, J. P. 1989. Facies and evolution of Precambrian depositional systems: emergence of the modern platform archetype, p. 79–106. 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.Google Scholar
Han, T.-M., and Runnegar, B. 1992. Megascopic eukaryotic algae from the 2.1-billion-year-old Negaunee Iron-Formation, Michigan. Science, 257:232–235.Google Scholar
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, 55:3387–3390.Google Scholar
Hoffman, P. F., Kaufman, A. J., Halverson, G. P., Schrag, D. P. 1998. A Neoproterozoic snowball Earth. Science, 281:1342–1346.Google Scholar
Hoffman, P. F., and Schrag, D. P. 2002. The snowball Earth hypothesis: testing the limits of global change. Terra Nova, 14:129–155.CrossRefGoogle Scholar
Hofmann, H. J. 1994. Proterozoic carbonaceous compressions (“metaphytes” and “worms”). In Bengtson, S. (ed.), Early Life on Earth. Columbia University Press, New York.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
Javaux, E. J., Knoll, A. H., and Walter, M. 2003. Recognizing and interpreting the fossils of early eukaryotes. Origins of Life and the Biospshere, 33:75–94.CrossRefGoogle ScholarPubMed
Kah, L. C., and Knoll, A.H. 1996. Microbenthic distribution of Proterozoic tidal flats: environmental and taphonomic considerations. Geology, 24:79–82.2.3.CO;2>CrossRefGoogle ScholarPubMed
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, 36:313–332.Google Scholar
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), 11:120–125.Google Scholar
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, 111:5–30.Google Scholar
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, 20:181–185.Google Scholar
Kirschvink, J. L. 1992. Late Proterozoic low-latitude glaciation: the snowball Earth, p. 51–52. In Schopf, J. W. and Klein, C. (eds.), The Proterozoic Biosphere. Cambridge University Press, Cambridge.Google Scholar
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, 136:2551–2553.Google Scholar
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, 65:531–570.Google Scholar
Knoll, A. H. 1992. The early evolution of eukaryotes: a geological perspective. Science, 256:622–627.CrossRefGoogle ScholarPubMed
Knoll, A. H. 1994. Proterozoic and Early Cambrian protists: evidence for accelerating evolutionary tempo. Proceedings of the National Academy of Sciences, 91:6743–6750.Google Scholar
Knoll, A., and Carroll, S. 1999. Early animal evolution: emerging views from comparative biology and geology. Science, 284:2129–2137.CrossRefGoogle ScholarPubMed
Kumar, S. 1995. Megafossils from the Mesoproterozoic Rohtas Fromation (the Vindhyan Supergroup), Katni Area, central India. Precambrian Research, 72:171–184.CrossRefGoogle Scholar
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. 475–493. In Zhuravlev, A. Y. and Riding, R. (eds.), The Ecology of the Cambrian Radiation. Columbia University Press, New York.Google Scholar
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, 101:8066–8071.Google Scholar
Ourisson, G., Rohmer, M., and Poralla, K. 1987. Prokaryotic hopanoids and other polyterpenoid sterol surrogates. Annual Reviews of Microbiology, 41:301–333.Google Scholar
Paine, R. T. 1966. Food web complexity and species diversity. American Naturalist, 100:65–75.Google Scholar
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, 29:1321–1329.Google Scholar
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, 267:1213–1221.Google Scholar
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, 26:360–385.Google 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.Google 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.Google Scholar
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, 55:911–916.CrossRefGoogle Scholar
Runnegar, B. 2000. Loophole for snowball Earth. Nature, 405:403–404.Google Scholar
Schopf, J. W., Haugh, B. N., Molnar, R. E., and Satterthwait, D. F. 1973. On the development of metaphytes and metazoans. Journal of Paleontology, 47:1–9.Google Scholar
Schopf, J. W. 1992. Patterns of Proterozoic microfossil diversity: an initial, tentative, analysis, p. 529–552. In Schopf, J. W. and Klein, C. (eds.), The Proterozoic Biosphere. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Simpson, A. G. B., and Roger, A. J. 2002. Eukaryotic evolution: getting to the root of the problem. Current Biology, 12:R691–R693.Google Scholar
Sogin, M. L. 1991. Early evolution and the origin of eukaryotes. Current Opinion in Genetics and Development, 1:457–463.Google Scholar
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, 70:1486–1489.Google Scholar
Stechmann, A., and Cavalier-Smith, T. 2002. Rooting the eukaryote tree by using a derived gene fusion. Science, 297:89–91.Google Scholar
Stechmann, A., and Cavalier-Smith, T. 2003. The root of the eukaryote tree pinpointed. Current Biology, 13:R665–R666.Google Scholar
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, 52:2625–2637.Google Scholar
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:212–244.Google Scholar
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, 56:2437–2444.Google Scholar
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, 101:10368–10373.Google Scholar
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, 426:172–176.Google Scholar
Vidal, G., and Knoll, A. H. 1983. Proterozoic plankton. Geological Society of America Memoir, 161:265–277.Google Scholar
Vidal, G., and Moczydlowska-Vidal, M. 1997. Biodiversity, speciation, and extinction trends of Proterozoic and Cambrian phytoplankton. Paleobiology, 23:230–246.Google Scholar
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, 20:7–15.CrossRefGoogle Scholar
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, 266:163–171.CrossRefGoogle ScholarPubMed
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.Google Scholar
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, 72:1072–1086.Google Scholar
Xiao, S. H., Zhang, Y., and Knoll, A.H. 1998b. Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite. Nature, 391:553–558.CrossRefGoogle Scholar
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, 74:767–788.Google Scholar
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):347–376.Google Scholar
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, 91:214–227.Google 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.Google Scholar
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, 21:809–818.Google Scholar
Zander, J. M., Caspi, E., Pandey, G. N., and Mitra, C. 1969. The presence of tetrahymanol in Oleandra wallichii . Phytochemistry, 8:2265–2267.Google Scholar