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Review
. 2006 Jun 29;361(1470):1023-38.
doi: 10.1098/rstb.2006.1843.

Eukaryotic organisms in Proterozoic oceans

A H Knoll  1 , E J Javaux, D Hewitt, P Cohen
Affiliations
Review

Eukaryotic organisms in Proterozoic oceans

A H Knoll et al. Philos Trans R Soc Lond B Biol Sci. .

Abstract

The geological record of protists begins well before the Ediacaran and Cambrian diversification of animals, but the antiquity of that history, its reliability as a chronicle of evolution and the causal inferences that can be drawn from it remain subjects of debate. Well-preserved protists are known from a relatively small number of Proterozoic formations, but taphonomic considerations suggest that they capture at least broad aspects of early eukaryotic evolution. A modest diversity of problematic, possibly stem group protists occurs in ca 1800-1300 Myr old rocks. 1300-720 Myr fossils document the divergence of major eukaryotic clades, but only with the Ediacaran-Cambrian radiation of animals did diversity increase within most clades with fossilizable members. While taxonomic placement of many Proterozoic eukaryotes may be arguable, the presence of characters used for that placement is not. Focus on character evolution permits inferences about the innovations in cell biology and development that underpin the taxonomic and morphological diversification of eukaryotic organisms.

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Figures

Figure 1
Figure 1
Shuiyousphaeridium macroreticulatum from the Mesoproterozoic Ruyang Group, China. (a) Light microphotograph showing specimen with numerous regularly spaced cylindrical processes that flare outward; (b, c, e–f) SEM images showing (b) whole specimen, with inset showing details of process morphology, (c) outer wall surface covered with ridges that delimit granular polygonal fields, (e) wall reticulation and (f) inner wall surface of closely packed, beveled hexagonal plates; (d) TEM image showing the two appressed walls of a single specimen—note multilayered wall comprising a thick electron-dense homogeneous layer of organic plates (ii) between an outer layer of debris and processes—note base of process at bottom left of centre (iii) and a thin electron-tenuous layer (i) that lines the inner side of plates. Scale bar in a=57 μm for a, 50 μm for b (20 μm for inset), 1.2 μm for c and e, 0.5 μm for d and 2.5 μm for f.
Figure 2
Figure 2
Diversity of Late Palaeoproterozoic to Early Mesoproterozoic eukaryotic fossils. (a) Tappania plana, from the Early Mesoproterozoic Roper Group, Australia; (b) Horodyskia moniliformis, from the Mesoproterozoic Bangemall Group, Western Australia; (c,f) Satka favosa, from the Roper Group, (c) showing the wall construction of hexagonal plates, shown under SEM in (f); (d, e) Valeria lophopstriata, showing ornamentation of closely spaced parallel ridges on the inner wall surface in SEM (d) and light microscopic (e) view; (g, h) Leiosphaeridia sp., an unornamented spheroidal acritarch, with a complex wall composed of two electron-dense, homogeneous layers (i) that sandwich a thick central layer with electron-dense, porous texture (ii) visible in TEM cross-section (h); Grypania spiralis, a coiled macrofossil compression from the Mesoproterozoic Gaoyuzhuang Formation, China (courtesy of M. Walter). Scale bar=40 μm for (a), 7.8 mm for (b), 35 μm for (c), 4 μm for (d), 15 μm for (e), 7.5 μm for f, 1 μm for (h), and 3 mm for (i).
Figure 3
Figure 3
Late Mesoproterozoic and Neoproterozoic eukaryotic fossils: (a, b) ‘Tappania plana’ from the Neoproterozoic Wynniatt Formation, arctic Canada, a complex form with septate, anastomosing processes, shown in detail in (b); (c) Bangiomorpha pubescens, from the Late Mesoproterozoic Hunting Formation, arctic Canada, showing radial division of cells within a discrete zone of uniseriate filaments; (d) Konglingiphyton erecta, a macroscopic, dichotomously branched alga from the Ediacaran Doushantou Formation, China; (e) Eosaccharomyces ramosa from the Late Mesoproterozoic Lakhanda succession, Siberia, showing net-like distribution on a bedding surface, with cells aligned along strands; (f) Segmentothallus asperus from the Lakhanda succession, a large uniseriate filament; (g) Appendisphaera grandis, a large acritarch with numerous, symmetrically arranged processes, from the Ediacaran Khamaka Formation, Siberia; (h) Kildinosphaera verrucata, an ornamented acritarch from the Neoproterozoic Miroyedikha Formation, Siberia; (i) Bonniea dacruchares, a vase-shaped protistan test from the Neoproterozoic Kwagunt Formation, Grand Canyon, USA; (j) preserved cast and mould of vase-shaped protist in silicified carbonates of the Neoproterozoic Ryssö Formation, Svalbard. Scale bar=100 μm in (a), 12 μm in (b), 40 μm in (c) 4 mm in (d) 150 μm in (e), 500 μm in (f), 70 μm in (g), 25 μm in (h), 43 μm in (i), and 75 μm in (j).
Figure 4
Figure 4
The composition and taxonomic richness of non-metazoan eukaryotes in Proterozoic to Early Cambrian fossil assemblages. (a) Total diversity of eukaryotic morphospecies for selected Proterozoic and Early Cambrian assemblages—in each column, a thin partition separates acritarchs from non-acritarchous protists; see legend in figure for compositions. Numbers refer to individual assemblages (principal references in parentheses; note that diversity estimates in the figure are the present authors' and do not in every case coincide with estimates in the primary references): (1) Changcheng Gr (Yan & Liu 1993); (2) Sarda Fm (Prasad & Asher 2001); (3) Avadh Fm (Prasad & Asher 2001); (4) Ruyang Gr (Xiao et al. 1997; Yin 1997); (5) Roper Gr (Javaux et al. 2001, 2003, 2004); (6) Chamberlin Fm (Horodyski 1982a,b); (7) Hunting Fm (Butterfield 2000, 2001); (8) Dundas Gr (Samuelsson et al. 1999); (9) Changlongshan Fm (Du & Tian 1985); (10) Lakhanda Fm (Jankauskas 1989; Herman 1990); (11) Miroyedikha Fm (Jankauskas 1989; Herman 1990); (12) Lower Visingsö Gr (Vidal 1976); (13) Båtsfjord Fm (Vidal & Siedlecka 1983); (14) Upper Visingsö Gr (Vidal 1976); (15) Wynniatt Fm (Butterfield & Rainbird 1998; Butterfield 2005a,b); (16) Svanbergfjellet Fm (Butterfield et al. 1994; Butterfield 2004); (17) Chuar Gr (Vidal & Ford 1985; Porter et al. 2003); (18) Ungoolya Gr (Grey 2005); (19) Doushantuo Fm (Yuan et al. 2002); (20) Pertatataka Fm (Zang & Walter 1992); (21) Yuryakh Fm (Moczydlowska et al. 1993); (22) Lantian Fm (Yuan et al. 2002); (23) Redkino Gr (Burzin et al. 1997); (24) Lower Nama Gr (Germs et al. 1986); (25) Vergale Horizon, Baltic drillcore (Volkova et al. 1983); (26) Radzyń and Kaplonosy Fms, lower part (Moczydlowska 1991); (27) Radzyń and Kaplonosy Fms, upper part (Moczydlowska 1991); (28) Baltic Depression drillcore, assemblage 1 (Hagenfelt 1989); (29) Baltic Depression drillcore, assemblage 2 (Hagenfelt 1989); Læså Fm (Moczydlowska & Vidal 1992); (30) Fucoid Beds (Downie 1982); Tokammane Fm (Knoll & Swett 1987). (b, c and d) show the taxonomic richness of assemblages through time for acritarchs (b), macrofossil compressions (c) and (d) multicellular microfossils and vase-shaped protists; width of rectangles indicates permissible age range for assemblages; C with arrow indicates position of Proterozoic–Cambrian boundary.
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