Frameworks for Interpreting the Early Fossil Record of Eukaryotes.

The origin of modern eukaryotes is one of the key transitions in life's history, and also one of the least understood. Although the fossil record provides the most direct view of this process, interpreting the fossils of early eukaryotes and eukaryote-grade organisms is not straightforward. We present two end-member models for the evolution of modern (i.e., crown) eukaryotes-one in which modern eukaryotes evolved early, and another in which they evolved late-and interpret key fossils within these frameworks, including where they might fit in eukaryote phylogeny and what they may tell us about the evolution of eukaryotic cell biology and ecology. Each model has different implications for understanding the rise of complex life on Earth, including different roles of Earth surface oxygenation, and makes different predictions that future paleontological studies can test.

Phosphatic scales in vase-shaped microfossil assemblages from Death Valley, Grand Canyon, Tasmania, and Svalbard.

Although biomineralized skeletal elements dominate the Phanerozoic fossil record, they did not become common until ~550-520 Ma when independent acquisitions of biomineralization appeared in multiple lineages of animals and a few protists (single-celled eukaryotes). Evidence of biomineralization preceding the late Ediacaran is spotty aside from the apatitic scale microfossils of the ~811 Ma Fifteenmile Group, northwestern Canada. Here, we describe scale-shaped microfossils from four vase-shaped microfossil (VSM)-bearing units of later Tonian age: the Togari Group of Tasmania, Chuar and Pahrump groups of southwestern United States, and the Roaldtoppen Group of Svalbard. These scale-shaped microfossils consist of thin, ~13 micron-long plates typically surrounded by a 1-3 micron-thick colorless envelope; they are found singly and in heterotypic and monotypic clusters of a few to >20 specimens. Raman spectroscopy and confocal laser scanning microscopy indicate these microfossils are composed of apatite and kerogen, just as is seen in the Fifteenmile Group scale microfossils. Despite compositional similarity, however, these scales are probably not homologous, representing instead, an independent acquisition of apatite mineralization. We propose that these apatite-kerogen scale-shaped microfossils are skeletal elements of a protistan cell. In particular, their consistent co-occurrence with VSMs, and similarities with scales of arcellinid testate amoebae, a group to which the VSMs are thought to belong, suggest the possibility that these microfossils may be test-forming scales of ancient arcellinid testate amoebae. The apparent apatite biomineralization in both these microfossils and the Fifteenmile scales is unexpected given its exceedingly rare use in skeletons of modern protists. This modern absence is attributed to the extravagance of using a limiting nutrient in a structural element, but multiple occurrences of apatite biomineralization in the Tonian suggest that phosphorus was not a limiting nutrient for these organisms, a suggestion consistent with the idea that dissolved seawater phosphate concentrations may have been higher at this time.

Evolution: Ancient Fossilized Amoebae Find Their Home in the Tree.

Ancestral test morphologies predicted from a new phylogeny of arcellinid amoebae show a striking resemblance to microscopic fossilized tests found worldwide in rocks 790-730 million years old.

It's a protist-eat-protist world: recalcitrance, predation, and evolution in the Tonian-Cryogenian ocean.

Predation, and how organisms respond to it, is an important ecological interaction across the tree of life. Much of our understanding of predation focuses on modern metazoa. However, predation is equally important in single-celled eukaryotes (commonly referred to as protists). In the fossil record, we see evidence of protists preying on other protists beginning in the Tonian Period (1000-720 Ma). In addition, the first evidence of eukaryotic biomineralization and the appearance of multiple unmineralized but recalcitrant forms are also seen in the Tonian and Cryogenian (720-635 Ma), potentially indirect evidence of predation. This fossil evidence, coupled with molecular clock analyses, is coincident with multiple metrics that show an increase in the diversity of eukaryotic clades and fossil assemblages. Predation, thus, may have played a critical role in the diversification of eukaryotes and the evolution of protistan armor in the Neoproterozoic Era. Here, we review the current understanding of predation in the Tonian and Cryogenian oceans as viewed through the fossil record, and discuss how the rise of eukaryotic predation upon other eukaryotes (eukaryovory) may have played a role in major evolutionary transitions including the origins of biomineralization.

Anoxic ecosystems and early eukaryotes.

Through much of the Proterozoic Eon (2.5-0.54 billion years ago, Ga), oceans were dominantly anoxic. It is often assumed that this put a brake on early eukaryote diversification because eukaryotes lived only in oxygenated habitats, which were restricted to surface waters and benthic environments near cyanobacterial mats. Studies of extant microbial eukaryotes show, however, that they are diverse and abundant in anoxic (including sulfidic) environments, often through partnerships with endo- and ectosymbiotic bacteria and archaea. Though the last common ancestor of extant eukaryotes was capable of aerobic respiration, we propose that at least some, and perhaps many, early eukaryotes were adapted to anoxic settings, and outline a way to test this with the microfossil and redox-proxy record in Proterozoic shales. This hypothesis might explain the mismatch between the record of eukaryotic body fossils, which extends back to >1.6 Ga, and the record of sterane biomarkers, which become diverse and abundant only after 659 Ma, as modern eukaryotes adapted to anoxic habitats do not make sterols (sterane precursors). In addition, an anoxic habitat might make sense for several long-ranging (>800 million years) and globally widespread eukaryotic taxa, which disappear in the late Neoproterozoic around the time oxic environments are thought to have become more widespread.