Phoebe A. Cohen

Eukaryotic organisms in Proterozoic oceans

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.

Calibrating the Cryogenian

Aging Snowball Earth Earths glacial cycles have varied dramatically over time; at one point glaciers may have covered nearly the entire planet. Correlating various paleoclimate proxies such as fossil and isotope records from that time hinges on the ability to acquire precise age estimates of rocks deposited around the time of this so-called “Snowball Earth.” Macdonald et al. (p. 1241) report new high-precision U-Pb dates of Neoproterozoic strata in the Yukon and Northwest Territories, Canada, to calibrate the timing of carbon isotope variation in rocks from other locations around the globe. Based on the estimated past positions of where these rocks were deposited, glaciers probably extended to equatorial latitudes. The overlap with the survival and, indeed, diversification of some eukaryotes in the fossil record suggests that life survived in localized ecological niches during this global glaciation. A volcanic tuff dated to 716.5 million years ago calibrates the timing of a global glaciation event and eukaryotic survival. The Neoproterozoic was an era of great environmental and biological change, but a paucity of direct and precise age constraints on strata from this time has prevented the complete integration of these records. We present four high-precision U-Pb ages for Neoproterozoic rocks in northwestern Canada that constrain large perturbations in the carbon cycle, a major diversification and depletion in the microfossil record, and the onset of the Sturtian glaciation. A volcanic tuff interbedded with Sturtian glacial deposits, dated at 716.5 million years ago, is synchronous with the age of the Franklin large igneous province and paleomagnetic poles that pin Laurentia to an equatorial position. Ice was therefore grounded below sea level at very low paleolatitudes, which implies that the Sturtian glaciation was global in extent.

Large spinose microfossils in Ediacaran rocks as resting stages of early animals

Large (>100 μm), profusely ornamented microfossils comprise a distinctive paleontological component of sedimentary rocks deposited during the Ediacaran Period (635–542 million years ago). Smaller spinose fossils in Paleozoic rocks have commonly been interpreted as algal cysts or phycomata, but the Ediacaran populations differ from modern algal analogs in size, shape, ultrastructure, and internal contents. In contrast, cysts formed during the diapause egg-resting stages of many metazoans share features of size, ornamentation, and internal contents with large ornamented Ediacaran microfossils (LOEMs). Moreover, transmission electron microscopic observations of animal-resting cysts reveal a 3-layer wall ultrastructure comparable to that of LOEM taxa. Interpretation of these distinctive Ediacaran microfossils as resting stages in early metazoan life cycles offers additional perspectives on their functional morphology and stratigraphic distribution. Based on comparisons with modern marine invertebrates, the recalcitrant life stage represented by LOEMs is interpreted as an evolutionary response to prolonged episodes of bottom water anoxia in Ediacaran shelf and platform environments. As predicted by this hypothesis, the later Ediacaran disappearance of LOEM taxa coincides with geochemical evidence for a marked decline in the extent of oxygen-depleted waters impinging on continental shelves and platforms. Thus, the form, diversity, and stratigraphic range of LOEMs illuminate life cycle evolution in early animals as influenced by the evolving redox state of the oceans.

Phosphate biomineralization in mid-Neoproterozoic protists

The origin and expansion of biomineralization in eukaryotes played a critical role in Earth history, linking biological and geochemical processes. However, the onset of this phenomenon is poorly constrained due to a limited early fossil record of biomineralization. Although macroscopic evidence for biomineralization is not known until the late Ediacaran, we here report biologically controlled phosphatic biomineralization of scale microfossils from mid-Neoproterozoic (pre-Sturtian) strata of northwest Canada. Primary biological control on mineralization is supported by the identification of apatite in both chert-hosted and limestone-hosted specimens, the conspicuously rigid original morphology of the scale microfossils relative to co-occurring organic-walled cyanobacteria and acritarchs, and the microstructure of the constituent phosphate. Cell-enveloping mineralized scales occur in a wide range of extant protists, but the apparent restriction of phosphate scales to one modern taxon of green algae suggests a possible affiliation for these fossils. Documentation of primary phosphate biomineralization in Fifteenmile Group (Yukon Territory, Canada) microfossils greatly extends the known record of biologically controlled mineralization and provides a unique window into the diversity of early eukaryotes.

The Proterozoic Record of Eukaryotes

Abstract. Proterozoic strata host evidence of global “Snowball Earth” glaciations, large perturbations to the carbon cycle, proposed changes in the redox state of oceans, the diversification of microscopic eukaryotes, and the rise of metazoans. Over the past half century, the number of fossils described from Proterozoic rocks has increased exponentially. These discoveries have occurred alongside an increased understanding of the Proterozoic Earth system and the geological context of fossil occurrences, including improved age constraints. However, the evaluation of relationships between Proterozoic environmental change and fossil diversity has been hampered by several factors, particularly lithological and taphonomic biases. Here we compile and analyze the current record of eukaryotic fossils in Proterozoic strata to assess the effect of biases and better constrain diversity through time. Our results show that mean within assemblage diversity increases through the Proterozoic Eon due to an increase in high diversity assemblages, and that this trend is robust to various external factors including lithology and paleogeographic location. In addition, assemblage composition changes dramatically through time. Most notably, robust recalcitrant taxa appear in the early Neoproterozoic Era, only to disappear by the beginning of the Ediacaran Period. Within assemblage diversity is significantly lower in the Cryogenian Period than in the preceding and following intervals, but the short duration of the nonglacial interlude and unusual depositional conditions may present additional biases. In general, large scale patterns of diversity are robust while smaller scale patterns are difficult to discern through the lens of lithological, taphonomic, and geographic variability.

Early Neoproterozoic scale microfossils in the Lower Tindir Group of Alaska and the Yukon Territory

The Tindir Group is a <4-km-thick Neoproterozoic succession exposed in the Tatonduk inlier of east-central Alaska and the western Yukon Territory. The Tindir Group is informally divided into the Lower Tindir Group, which consists of <2 km of mixed carbonate and clastic rocks, and the overlying Upper Tindir Group, which contains two Cryogenian glacial deposits and an additional Ediacaran succession of mixed carbonate and clastic strata. Unique mineralized scale microfossils have been recovered from sections previously correlated with the Upper Tindir Group, and interpreted variously as Cryogenian to early Cambrian in age. Our remapping of the area indicates that these sections are stratigraphically below an early Cryogenian glacial diamictite, unit 2 of the Upper Tindir Group, and are actually part of the Lower Tindir Group. Carbon and strontium isotope correlations further suggest that the fossiliferous Lower Tindir Group is correlative with early Neoproterozoic strata of the northwestern Canadian Cordillera. This new age model is consistent with the accompanying microfossil assemblage and indicates that the diverse microfossils in the Lower Tindir Group can be added to the early Neoproterozoic record of eukaryotic evolution.

Tubular Compression Fossils from the Ediacaran Nama Group, Namibia

Abstract Abundant tubular macrofossils occur in finely laminated siltstones and shales of the 548–542 Ma Schwarzrand Subgroup, Nama Group, Namibia. The Nama tubes occur in both the Vingerbreek and Feldschuhhorn members commonly in dense populations and always in fine-grained, lower shore-face lithologies deposited below fair-weather wave base. The tubes are preserved mostly as compressed casts and molds that range in width from 0.6 to 2.1 mm; apparently incomplete specimens reach lengths up to 10 cm. All specimens show sinuous bending and occasional brittle fracture, indicating an original construction of strong but flexible organic matter. Feldschuhhorn specimens preserve fine longitudinal pleats or folds that record pliant organic walls, but the older Vingerbreek populations do not. Similarly, some specimens in the Feldschuhhorn Member display branching, while Vingerbreek tubes do not. The abundant Feldschuhhorn tubes are assigned to the widespread Ediacaran problematicum Vendotaenia antiqua; however, the distinctive Vingerbreek population remains in open nomenclature. The most abundant fossils in Nama rocks, these tubes resemble populations in Ediacaran successions from Russia, China, Spain, and elsewhere. Beyond their local importance, then, such tubes may turn out to be the most abundant record of Ediacaran life.

Snowball Earth climate dynamics and Cryogenian geology-geobiology

We review recent observations and models concerning the dynamics of Cryogenian global glaciation and their biological consequences. Geological evidence indicates that grounded ice sheets reached sea level at all latitudes during two long-lived Cryogenian (58 and ≥5 My) glaciations. Combined uranium-lead and rhenium-osmium dating suggests that the older (Sturtian) glacial onset and both terminations were globally synchronous. Geochemical data imply that CO2 was 102 PAL (present atmospheric level) at the younger termination, consistent with a global ice cover. Sturtian glaciation followed breakup of a tropical supercontinent, and its onset coincided with the equatorial emplacement of a large igneous province. Modeling shows that the small thermal inertia of a globally frozen surface reverses the annual mean tropical atmospheric circulation, producing an equatorial desert and net snow and frost accumulation elsewhere. Oceanic ice thickens, forming a sea glacier that flows gravitationally toward the equator, sustained by the hydrologic cycle and by basal freezing and melting. Tropical ice sheets flow faster as CO2 rises but lose mass and become sensitive to orbital changes. Equatorial dust accumulation engenders supraglacial oligotrophic meltwater ecosystems, favorable for cyanobacteria and certain eukaryotes. Meltwater flushing through cracks enables organic burial and submarine deposition of airborne volcanic ash. The subglacial ocean is turbulent and well mixed, in response to geothermal heating and heat loss through the ice cover, increasing with latitude. Terminal carbonate deposits, unique to Cryogenian glaciations, are products of intense weathering and ocean stratification. Whole-ocean warming and collapsing peripheral bulges allow marine coastal flooding to continue long after ice-sheet disappearance. The evolutionary legacy of Snowball Earth is perceptible in fossils and living organisms.

FOSSILS OF PUTATIVE MARINE ALGAE FROM THE CRYOGENIAN GLACIAL INTERLUDE OF MONGOLIA

ABSTRACT Neoproterozoic carbonate successions provide a new taphonomic window into the diversification of eukaryotes. We report recently discovered macroscopic organic warty sheets (MOWS) in macerates of limestone from the ca. 662–635 Ma Taishir Formation (Tsagaan Olom Group, Mongolia). Sheets are applanate. One surface contains raised ridges and conspicuous, ∼ 100-µm-tall warty protuberances with depressed tops that enclose internal cavities containing cellular structures. The Taishir MOWS may be the remains of unusual bacterial, protistan, or fungal biofilms, or a previously undocumented, extinct taxon. However, multiple lines of evidence including the morphology of warty protuberances and the presence of cellular architecture within protuberances support the interpretation of MOWS as marine algae, perhaps a member of the Rhodophyta. Regardless of their specific taxonomic affiliation, MOWS increase the diversity of biota reported from the Cryogenian glacial interlude and indicate the presence of macroscopic and morphologically complex multicellular organisms in the Cryogenian.

Controlled hydroxyapatite biomineralization in an ~810 million-year-old unicellular eukaryote

New analyses show that 811 million-year-old microfossils from the Yukon are the oldest evidence of eukaryotic biomineralization. Biomineralization marks one of the most significant evolutionary milestones among the Eukarya, but its roots in the fossil record remain obscure. We report crystallographic and geochemical evidence for controlled eukaryotic biomineralization in Neoproterozoic scale microfossils from the Fifteenmile Group of Yukon, Canada. High-resolution transmission electron microscopy reveals that the microfossils are constructed of a hierarchically organized interwoven network of fibrous hydroxyapatite crystals each elongated along the [001] direction, indicating biological control over microstructural crystallization. New Re-Os geochronological data from organic-rich shale directly below the fossil-bearing limestone constrain their age to <810.7 ± 6.3 million years ago. Mineralogical and geochemical variations from these sedimentary rocks indicate that dynamic global marine redox conditions, enhanced by local restriction, may have led to an increase in dissolved phosphate in pore and bottom waters of the Fifteenmile basin and facilitated the necessary geochemical conditions for the advent of calcium phosphate biomineralization.