Framing an agenda for understanding the origin and rise of complex life

Eukaryotes appear in the fossil record about 1.6 billion years (Ga) ago, and most molecular clocks place the last common ancestor of all extant eukaryotes broadly into the late Paleoproterozoic to early Mesoproterozoic (~1.9 to 1.3 Ga). The oldest fossil alga, a benthic rhodophyte, has been dated to 1.05 Ga. Yet, sedimentary rocks of the interval 1.6 to 1.0 Ga are devoid of molecular fossils that are diagnostic for Eukarya, suggesting that eukaryotes, including algae, were not an abundant component of most marine environments at that time. The first eukaryotic steranes emerge across supercontinent Rodinia 900 to 750 Ma ago, and they first become diverse and abundant in the brief interval between the Sturtian and Marinoan Snowball Earth glaciations, 659 to ~640 Ma ago. The aftermath of the Marinoan glacials at 635 Ma saw a brief return to a primitive sterane pattern before algae permanently took over as dominant primary producers in the oceans. During melting of the Sturtian Snowball, massive volumes of meltwater flowed into the global ocean, forming a ~1 km thick, hot freshwater lid atop cold, dense brines. Dr Brocks will investigate how the biomarker record unfolded in this unusual freshwater ocean, and test the hypothesis that algae replaced cyanobacteria as dominant phototrophs when the oceans eventually returned to normal marine conditions.

Animals have an unparalleled capacity to pump and swim through water, but these hydrodynamic properties have been largely overlooked as a factor in early animal evolution.  By collectively driving water currents and compressing corresponding diffusion gradients, even the simplest colonies of flagellated cells gain significant gas-exchange and feeding advantage.  These advective effects multiply at larger length scales, particularly in combination with differentiated muscle tissue.  At a cnidarian grade of organisation, they introduced animals to inertial and turbulent fluid dynamic regimes with negligible metabolic investment.  In concert with hydrodynamically tuned morphologies they also led to the phenomenon of swimming and the metazoan take-over of pelagic ecology.  Swimming animals actively mix and ventilate much of the modern oceans as a by-product of their feeding activities.  In addition to the repackaging of dispersed surface-generated productivity as sedimenting faecal pellets, a significant fraction is transported actively to depth via diurnal vertical migration (DVM), a behavioural consequence of visual predation, muscular swimming and the size-structured tiering of pelagic food webs.  Such activity both aerates the surface ocean and concentrates biological oxygen demand at depth in the form of oxygen minimum zones – independently of atmospheric oxygen concentration or net carbon burial.  In this light, it is clear that the depth of DVM and the nature of OMZs must have changed systematically through time, in concert with escalatory innovations in the size and speed and of marine predators.  This alone may account for the step-wise changes observed in marine redox signatures through the later Neoproterozoic and early Palaeozoic, as well as intervals experiencing mass extinction.

The half-billion-year history of animal evolution is characterized by decreasing rates of background extinction. Earth’s increasing habitability for animals could result from several processes: (1) a decrease in the intensity of interactions among species that lead to extinctions; (2) a decrease in the prevalence or intensity of geological triggers such as flood basalt eruptions and bolide impacts; (3) a decrease in the sensitivity of animals to environmental disturbance; or (4) an increase in the strength of stabilizing feedbacks within the climate system and biogeochemical cycles. There is no evidence that the prevalence or intensity of interactions among species or geological extinction triggers have decreased over time. There is, however, evidence from paleontology, geochemistry, and comparative physiology that animals have become more resilient to environmental change and that the evolution of complex life has, on the whole, strengthened stabilizing feedbacks in the climate system. The differential success of certain phyla and classes appears to result, at least in part, from the anatomical solutions to the evolution of macroscopic size that were arrived at largely during Ediacaran and Cambrian time. Larger-bodied animals, enabled by increased anatomical complexity, were increasingly able to mix the marine sediment and water columns, thus promoting stability in biogeochemical cycles. In addition, body plans that also facilitated ecological differentiation have tended to be associated with lower rates of extinction. In this sense, Cambrian solutions to Cambrian problems have had a lasting impact on the trajectory of complex life and, in turn, fundamental properties of the Earth system.

Phagocytosis, or cell eating, is a eukaryote-specific process where particulate matter is engulfed via invaginations of the plasma membrane. The temporal origin of phagocytosis has been central to discussions on eukaryogenesis for decades – phagocytosis is argued either as being a prerequisite for, or consequence of, the acquisition of the ancestral mitochondrion. In recent years, genomic, bioenergetic, and cytological evidence have increasingly supported the view that the pre-mitochondrial host cell – a bona fide archaeon closely related to the Asgardarchaeota – was incapable of phagocytosis and used alternative mechanisms to assimilate the alphaproteobacterial ancestor of mitochondria. Indeed, the diversity and variability of proteins used in phagocytosis across the eukaryotic tree suggest that phagocytosis may have evolved independently several times. Since phagocytosis is so essential to the functioning of modern marine food webs (without it, there would be no microbial loop or animal life), multiple late origins of phagocytosis might help explain why many of the ecological and evolutionary innovations of the late Proterozoic (e.g. the advent of eukaryotic biomineralization, the ‘rise of algae’, and the origin of animals) happened when they did. While the compatibility of phagocytosis with anaerobiosis and anoxia suggests that biospheric oxygenation was unlikely to have controlled the evolutionary origins of phagocytosis, the sensitivity of phagocytosis to both high and low temperatures suggests a potential thermal driver for the origin of cell eating and the birth of modern ecosystems.

The sulfur isotopic composition of sedimentary sulfides, especially when paired with similar metrics in the carbon cycle, anchor interpretations of Earth history. These reconstructions are predicated on having a quantitative understanding of how microbial / geochemical / environmental information is transferred to mineral phases like pyrite.  Much of this focus has in the past fallen on the microbial metabolisms that both drive redox transformations (largely in marine sediments) and consequently impart much of the observed isotopic effect.  Therefore, variance in geological isotope records – for instance through the Ediacaran and across the Shuram excursion - could be and are inverted to tell stories of microbial evolution / innovation and/or Earth surface change.  In parallel was an attempt to understand how boundary conditions (like sulfate concentrations) might come to influence the isotope record preserved in marine sediments.  The obvious goal is to construct and apply an interpretative framework that accounts for both approaches, while also including the physics of sediment diagenesis. In working toward this goal, we first developed a quantitative context for understanding early diagenetic sulfur isotope signals through reaction-transport modelling.  As a case study, we provide results from a geochemically well-characterized system (Aarhus Bay, Denmark). Importantly, a major result of that work was the requirement for large and invariant intrinsic fractionations associated with sulfate reduction (approximating an equilibrium effect of 70‰).  These predictions for near equilibrium behavior apply over a range of different depositional environments (e.g., the California borderland basins). Together, these conclusions now stand in opposition to geological storylines calling upon evolving biogeochemistry as the root of changing historical isotope records.  This new interpretive context allows for alternative explanations for Neoproterozoic records.

D.T. Johnston¹, J. Hemingway¹, B.C. Gill², I. Halevy³

¹Harvard University ²Virginia Tech, ³Weitzmann Institute)

Numerous hypotheses have sought to identify what perturbations to the global carbon cycle fueled Earth system change during the Neoproterozoic Era (1000–541 million years ago, Ma). Nevertheless, a lack of constraints on ocean-atmosphere carbon chemistry has precluded mechanistic links between biology, climate, and the lithosphere. Field observations, combined with microanalytical data and new experimental constraints, show that early Neoproterozoic seawater featured elevated alkalinity in the presence of high atmospheric pCO2, which sustained excessive marine CaCO3 supersaturation. These data also show that between ~800–750 Ma, this inorganic carbon reservoir was halved. Without pelagic calcification, marine CaCO3 supersaturation and pCO2 would have been modulated principally by CaCO3 precipitation kinetics; thus, secular changes in kinetic inhibitors to CaCO3 deposition may have destabilized the global carbon cycle, facilitating extreme Neoproterozoic climatic instability.

The Neoproterozoic Era witnessed a succession of biological innovations that culminated in diverse animal body plans and behaviours during the Ediacaran-Cambrian radiations. Intriguingly, this interval is also marked by perturbations to the global carbon cycle, as evidenced by anomalous fluctuations in climate and carbon isotopes. The Neoproterozoic isotope record has defied parsimonious explanation because sustained ¹²C-enrichment (low δ¹³C) in seawater seems to imply that substantially more oxygen was consumed by organic carbon oxidation than could possibly have been available. We propose a solution to this problem, in which carbon and oxygen cycles maintained dynamic equilibrium during negative excursions because surplus oxidant could be generated through bacterial reduction of sulfate that originated from evaporite weathering. Coupling of evaporite dissolution with pyrite burial drove a positive feedback loop whereby net oxidation of marine organic carbon could sustain greenhouse forcing of chemical weathering, nutrient input and ocean margin euxinia. Our proposed framework is particularly applicable to the late Ediacaran ‘Shuram’ isotope excursion that directly preceded the emergence of energetic metazoan metabolisms during the Ediacaran-Cambrian transition. However, in this discussion, we outline how sulfur cycle imbalance might potentially have affected the global carbon cycle at other times, too, leading to climatic, ocean redox and biotic changes on a global scale.

The development of controlled motility among bilaterian animals is a manifestation of morphological, neural, and behavioral complexity. It is also a transformative innovation that redefined animals in ecological engineering and geobiological interactions (e.g., substrate and agronomic revolutions). It has been hypothesized that heterogenous distribution of food may have been an evolutionary stimulus for the evolution of bilaterian motility. Here I would like to explore the possibility that dynamic and heterogeneous redox conditions in late Ediacaran oceans may have been an alternative or additional driving force leading to the evolution of bilaterian motility.

Trace fossils indicate that the earliest motile bilaterians appeared in late Ediacaran (ca. 560-540 Ma), and ichnofossil diversity increased terminal Ediacaran (ca. 550-540 Ma) when many Ediacara-type organisms went extinct. Geochemical data indicate that the late Ediacaran is characterized by a major expansion of oceanic anoxia, resulting in temporally dynamic and spatially heterogeneous redox conditions in shallow shelves where animals lived. While such an expansion of anoxia may have driven some organisms to extinction, it may have also stimulated others to develop evolutionary innovations.

The observation that Ediacaran ichnofossils are closely associated with cyanobacterial mats offers insights into the possible relationship between animal motility and redox conditions. Because of the dynamic redox conditions in the water column and in the cyanobacterial mats, animals exploring localized oxygen oases must also be able to maneuver in and out these oases. This may have been an environmental stimulus that drove the evolution of motility among early benthic bilaterian animals.