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

09:05-09:30 The transition from low-energy bacterial oceans to a highly productive eukaryotic world

Dr Jochen Brocks, Australian National University, Australia

Abstract

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.

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09:30-09:45 Discussion

09:45-10:15 Pumping and swimming through time - macroevolutionary control of oceanic expression

Dr Nicholas Butterfield, University of Cambridge, UK

Abstract

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.

10:15-10:30 Discussion

10:30-11:00 Coffee break

11:00-11:30 The evolution of complex life and the stabilization of the Earth system

Professor Jonathan Payne, Stanford University, USA

Abstract

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.

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11:30-11:45 Discussion

11:45-12:15 Multiple late origins of phagocytosis and the birth of modern food webs

Dr Daniel Mills, Stanford University, USA

Abstract

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.

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12:15-12:30 Discussion

13:30-14:00 The information encoded in Neoproterozoic sedimentary sulfide

Dr David Johnston, Harvard University, USA

Abstract

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)

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14:00-14:15 Discussion

14:15-14:45 The Tonian carbonate factory and the long-term evolution of the Precambrian CaCO3 cycle

Dr Nick Tosca, University of Oxford, UK

Abstract

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.

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14:45-15:00 Discussion

15:00-15:30 Coffee break

15:30-16:00 Effects of sulphur cycle imbalance on the emergence and radiation of complex life

Professor Graham Shields, University College London, UK

Abstract

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.

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16:00-16:15 Discussion

16:15-16:45 Late Ediacaran evolution of complex life and environment

Dr Shuhai Xiao, Virginia Tech, USA

Abstract

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.

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16:45-17:00 Discussion

09:00-09:30 Using organic carbon isotopes of single microfossils to illuminate Proterozoic eukaryotic ecosystems

Professor Phoebe A Cohen, Williams College, USA

Abstract

Major questions remain about the interplay between biology and the rise of atmospheric oxygen in the Proterozoic. One window into the biological record of this Eon is via organic carbon isotopes, which track the isotope systematics of fixed carbon. However, these measurements are almost always done on bulk samples that represent the entire biological community time averaged into a sedimentary sample, which limits our ability to reconstruct short-term carbon cycle dynamics and to probe the structure of ancient ecosystems. Recent advances in NanoEA-IRMS now allow us to reliably measure the carbon isotopic composition of a single organic microfossil (acritarch). We are working to use this new technique to explore how organic carbon isotopes can illuminate persistent unknowns in the Proterozoic Earth-life system including the habits and metabolisms of early eukaryotes and controls on bulk organic carbon isotopes in the Proterozoic stratigraphic record. Here, I will present data from our Late Devonian test case project which shows consistent offsets between fossil (heavier) and bulk organic carbon isotopes (lighter), potentially providing evidence of a strong biological pump. Then I will present our initial results from Ediacaran samples from the Officer Basin of Australia and Mesoproterozoic samples from the Velkerri Formation of Australia, which also display a consistent offset, and will discuss what these records can tell us about the Proterozoic Earth-life system.

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09:30-09:45 Discussion

09:45-10:15 Rethinking hypoxia as an evolutionary driver for large life

Dr Emma Hammarlund, Lund University, Sweden

Abstract

The appearance of complex multicellular life on Earth remains enigmatic. Since evolution and diversity of for example animals associate with oxic niches, the Cambrian explosion can be assumed the cascading result of the surpassing of a certain environmental threshold. However, the oxic niche can also be regarded as an impediment for the evolution of large life in general. A growing body of research in the medical and natural sciences demonstrate that the construction of animal and plant tissue is fundamentally sensitive to oxygen. The paradox of an oxygen-sensitive core within organisms that also require oxygen can be explained by certain tissue niches were oxygen concentrations are kept low (hypoxic) or by cellular machineries that respond as if conditions are hypoxic. Hypoxic tissue niches and cellular hypoxia-response machineries have been under selection, which suggest that biological ‘domestication’ of hypoxic conditions is of evolutionary importance. Indeed, the domestication of hypoxia can be argued critical for how multicellular evolution could (finally) leave the stable hypoxic niche for those where oxygen fluctuates. Dr Hammarlund will discuss the observations of oxygen-sensitive tissue construction, solutions that maintain hypoxic niches and responses and the potential evolutionary importance of the domestication of hypoxia. Dr Hammarlund hopes to demonstrate that if multicellular organisms could sustain oxic conditions first after internalizing hypoxic conditions, we must reconsider how changes of environmental oxygen concentrations has guided life history.

10:15-10:30 Discussion

10:30-11:00 Coffee break

11:00-11:30 Early metazoan evolution in a context of the changeable ocean (species, isotopes, elements)

Dr Andrey Yu. Zhuravlev, Lomonosov Moscow State University, Russia

Abstract

A relatively rapid metazoan diversification known since Charles Darwin (1859) as the “Sudden Appearance” or, nowadays, as the Cambrian Explosion took pace in two phases at least and embraced a relatively lengthy interval of over 30 million years. This process began from the very appearance and radiation of the first distinct skeletal metazoan species dominated mostly by stem groups at the end of the Ediacaran and the earliest Cambrian c. 545-530 million years ago (Ma), their following decline and extinction c. 513 Ma with a subsequent diversification of crown groups extending to the Ordovician Radiation. Integrated high-resolution isotope and elemental analyses of rocks yielding late Ediacaran – early Cambrian fossils, especially those of the Siberian Platform, revealed that these events occurred on the background of a highly unstable ocean composition including its oxygen and carbon dioxide contents, the magnesium to calcium ion ratio, phosphate and silica inputs among others which fluctuated in concert with the animal diversification phases. These drastic changes were influential for the fates of the evolution of different groups but, at the same time, the evolving organisms step by step took over abiotic process in maintaining a number of principal marine elemental cycles (calcium, phosphate, silica) as well as in the ocean oxygenation through coupling carbon and sulphur cycles and, probably, on the carbon dioxide output through carbonate sedimentation.

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11:30-11:45 Discussion

11:45-12:15 Microbial contribution to fossilization of soft animal tissues

Professor Tanja Bosak, Massachusetts Institute of Technology, USA

Abstract

Global Ediacaran sandstones preserve impressions and casts of soft-bodied organisms with unresolved taxonomic affinities. The taphonomic window in which these macroscopic organisms and tissues were preserved continues to inspire hypotheses about interactions among microbes, soft tissues and Ediacaran seawater chemistry. To understand how sediments can record the three-dimensional morphology of non-recalcitrant body parts in the absence of obvious replacive minerals, we characterize minerals in erniettomorph fossils and the rock matrix of the mass flow deposits from the Ediacaran Wood Canyon Formation, USA and conduct taphonomy experiments. Petrographic, compositional and mineral analyses reveal abundant clay mineral grains consistent with the former presence of smectite and kaolinite in the fossils and in the sediment matrix. These observations inform the design of experiments that compare the fossilization of scallop adductor muscles. The tissues are placed on bare sand or cyanobacterial mats and buried by sediments that contain different proportions of quartz sand and smectite/kaolinite. The least extensive decay occurs in the presence of clay minerals. When tissues are placed on top of mats, they also retain 10% more weight compared to muscles placed on bare sand. Clay minerals delay the early activity of heterotrophic microbes, including iron and sulfate reducers, and limit the extent of this activity. These observations highlight the need to better understand relationships between microbial metabolisms, clay minerals and delayed decay. Although challenging, taphonomy experiments provide opportunities to address these questions.

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12:15-12:30 Discussion

13:30-14:00 The embryo-like fossils from the Ediacaran Weng’an biota foreshadow the evolutionary origin of animal-like embryology

Zongjun Yin, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, China

Abstract

Origin and early evolution of animal development remains one of many deep, unresolved problems in evolutionary biology. As a compelling case for existence of pre-Cambrian animals, the Ediacaran embryo-like fossils from the Weng’an biota (~610 million-year-old, Doushantuo Formation, South China) have the great potential to cast light on the origin and early evolution of animal development. However, their biological implications can be fully realized only when their phylogenic positions are correctly established, and unfortunately, this is the key problem under debate. The debate on the affinities of the Ediacaran embryo-like fossils largely derives from a viewpoint that they were morphologically simple and yield very few phylogenetic signals, because they represent different developmental stages of the same organism since they share a similarly ornamented envelope. But recently, our new discoveries suggest that the biodiversity of the Ediacaran embryo-like fossils is likely higher than previously thought. To highlight this idea, in this talk, we are going to present a large number of new well-preserved fossil specimens reconstructed three-dimensionally by synchrotron X-ray microtomography and micro-CT. Our results show that the Ediacaran embryo-like fossils include different developmental stages of different taxa rather than different developmental stages of the same taxon. The high diversity of these embryo-like fossils and their developmental processes are not only helpful to constrain their affinities, but also crucial to understand the evolutionary origin of animal-like embryology.

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14:00-14:15 Discussion

14:15-14:45 Drivers of Ediacaran ecosystem dynamics

Dr Emily G Mitchell, University of Cambridge, UK

Abstract

The Ediacaran – Cambrian transition is one of the most dramatic periods in the history of life on Earth, changing from a microbially populated world to one with an abundance of large animals.  With this remarkable increase in body-size comes the ability to adapt and change their local environment, transforming the biosphere.  Determining the nature of the interactions between Ediacaran organisms and their environment can be undertaken in the Avalonian and White Sea Ediacaran assemblages because entire communities are preserved in-situ, so that the position of the fossil on the bedding plane reflects the organism’s life-history.  This community-level preservation means that statistical analyses can be used to reconstruct Ediacaran ecological dynamics, and so test different hypotheses of drivers for these ecosystems.  Such statistical analyses have revealed a wide variability of dynamics, with some communities exhibiting a complex network of interactions and associations, while others show little interaction between taxa. Analyses of communities from deep-water and shallow-water environments reveals a complex interplay of large-scale environmental influence on community ecology.  These ecological analyses demonstrate how different environments result in different ecological drivers of Ediacaran organisms, the consequently on the diversification of early animals.

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14:45-15:00 Discussion

15:00-15:30 Coffee break

15:30-16:00 Novelties in the early history of complex life and the environmental expansion of developmental opportunity

Dr Douglas Erwin, National Museum of Natural History, USA

Abstract

The ability for spatial and temporal differentiation of cell types and the generation of multicellular forms is shared among each of the major clades of holozoans: Icthysporea, Filastrea, Choanoflagellates and Metazoa.  This supports models for the emergence of aniamals based on a transition from temporal to spatial organisation of cell types, enabled in part by a suite of regulatory novelties, including distal enhancers, new types of promoters, regulatory RNA and expansion of transcription factors.  Further expansion of regulatory capacity arose at the split between protostomes and deuterostomes (including significant changes in chromatin structuring) and within vertebrates. The developmental evidence suggests that the earliest animals were small with diverse cell types, but largely lacking complex developmental patterning, which arose independently in bilaterian clades during the Cambrian explosion, enabling larger body size and more complex ecological networks. The independent intercalation of regulatory domains for segmentation, a tri-partite brain, sensory systems and appendages mirrors the well-accepted patter for biomineralization.  These developmental novelties and the resulting bodyplans can only be understood in the context of the environmental conditions of the time. In particular, the evidence for widespread, independent co-option and intercalation among bilaterian clades strongly implicates external, environmental controls as drivers. 

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16:00-16:15 Discussion

16:15-17:00 Panel discussion

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