Paleobiological perspectives on early eukaryotic evolution

Abstract

Eukaryotic organisms radiated in Proterozoic oceans with oxygenated surface waters, but, commonly, anoxia at depth. Exceptionally preserved fossils of red algae favor crown group emergence more than 1200 million years ago, but older (up to 1600-1800 million years) microfossils could record stem group eukaryotes. Major eukaryotic diversification ~800 million years ago is documented by the increase in the taxonomic richness of complex, organic-walled microfossils, including simple coenocytic and multicellular forms, as well as widespread tests comparable to those of extant testate amoebae and simple foraminiferans and diverse scales comparable to organic and siliceous scales formed today by protists in several clades. Mid-Neoproterozoic establishment or expansion of eukaryophagy provides a possible mechanism for accelerating eukaryotic diversification long after the origin of the domain. Protists continued to diversify along with animals in the more pervasively oxygenated oceans of the Phanerozoic Eon.

Figure 1.

Late Paleo- and Mesoproterozoic fossils interpreted as eukaryotic. (A–D) Preserved spheroidal microfossils interpreted as the vegetative or resting walls of unicellular protists, arranged from lowest confidence (A) to highest (C and D). (A) Unornamented spheroidal vesicle, 1400–1500 Mya Roper Group, Australia. (B) Spheroidal vesicle with corduroy-like ornamentation of vesicle wall, Roper Group. (C) Spheroidal microfossil with surface divided into small fields and ornamented with cylindrical processes that expand distally; TEM of walls shows complex multilayered wall ultrastructure, >1600 Mya Ruyang Group, China. (D) Spheroidal vesicle with asymmetrically placed cylindrical processes; TEM shows complex wall ultrastructure, Roper Group (courtesy of Javaux et al. 2004). (E) Macroscopic compressions assigned to the form taxon Grypania, ∼1400 Mya Jixian Group, China (courtesy of M.R. Walter). Scale bars, 20 μm (A); 75 μm (B,D); 120 μm (C). Note 1-cm scale bar in E.

Figure 2.

Late Mesoproterozoic and Neoproterozoic fossils interpreted as eukaryotic. (A) Irregularly spheroidal microfossil with long cylindrical processes, 750–800 Mya Svanbergfjellet Formation, Spitsbergen. (B) Large microfossil with opaque inner wall bearing small spines and longer cylindrical processes, within encompassing smoothly spheroidal vesicle, Svanbergfjellet Formation. (C) Cladophora-like branching filamentous microfossil with apparently coenocytic subunits, Svanbergfjellet Formation. (D) Three-dimensionally (3D) preserved mineral replicate of testate eukaryote, Chuar Group, Grand Canyon (courtesy of Porter et al. 2003). (E) Bangiomorpha, interpreted as an early-branching red alga, 1100–1200 Mya Hunting Formation, Arctic Canada (courtesy of Butterfield 2000). (F–H). Scale microfossils preserved three-dimensionally in ∼800-Mya carbonate rocks of the Fifteenmile Group, Yukon Territory, Canada (courtesy of Cohen and Knoll 2013). Scale bars, 60 μm (A,C); 120 μm (B); 10 μm (F); 14 μm (G,H). Note scale bars in D and E.

Figure 3.

A summary of early eukaryotic evolution. Solid bars denote confident interpretation of geologic record; dashed bars indicate uncertain or controversial extensions of the record. Phan, Phanerozoic Eon (literally, the age of visible animal life). See text for references.