The origin and rise of complex life: integrating models, geochemical and palaeontological data

The link between global environmental change and the rise of complex life during the late Precambrian remains uncertain. The time period in question contains two massive 'Snowball Earth' glacial events, and also contains abundant but sporadic evidence for atmospheric and marine oxygenation, but forming a more precise picture of Earth's surface environment through the Neoproteorzoic Era is essential in order to understand whether these conditions might have spurred evolutionary advances, or alternatively may have been a direct result of 'bioengineering' of the environment by new organisms. The evidence for surface system evolution comes from a fantastic suite of geochemical analyses, but these are necessarily limited in time and often tell an incomplete and inherently local story. We can strengthen these analyses by introducing global biogeochemical models: these systems take information about past tectonic and biological processes and produce independent and detailed estimates for changes to the surface environment, which can then be related to the existing analytical databases. Professor Mills will introduce our latest results for the changes in surface temperature and atmospheric oxygen through the Neoproterozoic, question how we might expect marine oxygen levels to change, and discuss the coupling between marine oxygenation and biodiversity.

Benjamin Mills, University of Leeds, UK

Benjamin Mills, University of Leeds, UK

Ben is an Academic Fellow at the University of Leeds. He is a mathematician and biogeochemical modeller whose research focuses on the dynamics of the Earth system over geological timescales. He designs and builds computer models to make quantitative predictions for changes in climate and surface geochemistry that relate to both the evolution of the biosphere, and to the planet’s internal geodynamic processes. His key contributions are reconstructions of long-term Phanerozoic climate change, evaluation of the processes by which the atmosphere and oceans have become oxygenated, and determining the causes and consequences of severe ‘Snowball Earth’ glaciations.

It is generally accepted that animals first evolved during the Ediacaran Period when the oceans were just becoming fully oxygenated. The best evidence of the first animals include in situ trace fossils that are commonly associated with microbially induced sedimentary structures. The trace fossils generally were formed parallel to the surface of the seabed, at or below the sediment–water interface. This evidence suggests that the earliest mobile animals inhabited settings with high microbial populations, and may have mined microbially bound sediments for food resources, and possibly O2 if the mats were comprised of cyanobacteria. Numerous studies of modern cyanobactertially-dominated mats have further documented that during the day O2 levels in the mats are several times higher than in the overlying water column, in effect serving as oxygen-rich oases. These findings raise the possibility that animal evolution during the Ediacaran could have arisen in similarly O2-rich microbial mats that inhabited an otherwise poorly oxygenated or even anoxic environments. If true, then oxygen availability in sea water may not have played a direct role in the appearance of the first animals, especially considering the apparent existence of cyanobacterial mats as far back in time as 3.2 billion years ago. 

Dr Kurt Konhauser, University of Alberta, Canada

Dr Kurt Konhauser, University of Alberta, Canada

Kurt Konhauser is a Professor in Geochemistry and Geomicrobiology at the University of Alberta. His research focuses on mineral-metal-microbe interactions through time, including surface reactivity, biomineralization and biochemical weathering. His current interests are understanding how Earth and photosynthetic life co-evolved in the distant past, specifically the role of bacteria in the precipitation of banded iron formations and the causes for the rise of oxygen on the early Earth. He is a Fellow of the Geochemical Society and the Royal Society of Canada, and was previously a Canada Research Chair in Geomicrobiology. He is the Editor-in-Chief of the journal Geobiology, co-editor of the book Fundamentals of Geobiology, and sole author of the textbook Introduction to Geomicrobiology.

Sponges, morphologically simple animals and likely descendants of the oldest surviving animal lineage, are the key phylum to study the origin of animal multicellularity. Sponge body plan is based on a system of chambers built of collared cells (choanocytes), which propel water and capture food particles. Water, entering the canal system through small pores, is expelled by a larger apical opening (osculum). The outermost epithelium is composed of flat pinacocytes, with diverse motile cells inhabiting the space between the two layers. Morphology and function of choanocytes are reminiscent of choanoflagellates, colonial and single-cell protists, which are the nearest relatives of animals. The combination of similarity and phylogeny implies a choanoflagellate-like ancestor of all animals, and a sponge-like ancestor of all complex animals. The bi-layered body plan of sponges, with the major apical opening, is similar to cnidarian polyps, suggesting transition between poriferan and cnidarian grades of organization, with the endoderm derived from choanoderm, the ectoderm from pinacoderm, and the polyp mouth from the osculum. Recently, gene expression studies – initially of candidate genes, then involving massive single cell transcriptome sequencing – have been used to test these long-standing hypotheses. These studies produced unprecedented insights into cell and developmental biology of sponges, as well as several lineages of protists closely related to animals. However, interpretations of these insights vary widely, and we are far from understanding the events leading to emergence of complex animal multicellularity. Will improvement of sequencing technologies and inclusion of additional model species help shed light on our beginnings?

Professor Maja Adamska, Australian National University, Australia

Professor Maja Adamska, Australian National University, Australia

Maja Adamska studied biology in Poland and carried doctoral and postdoctoral research on vertebrate development in Germany and the USA.To gain insight into the origin of the complex developmental mechanisms in vertebrates, she moved to Queensland to analyse developmental signalling pathways in the first sequenced sponge, Amphimedon queenslandica. This work revealed surprising similarities in patterning of sponge and other animal embryos. From 2007 to 2015 Maja was a group leader at the Sars International Centre for Marine Molecular Biology in Norway; and in 2015 moved her lab to the Australian National University. Her group uses calcareous sponges and corals to investigate a variety of biological processes, including segregation of germ layers, axial patterning, skeleton formation, regeneration and symbiosis. Maja is also interested in major transitions in animal evolution, such as emergence of multicellularity and morphological complexity and their relationship to genomic complexity.

Sterane biomarkers preserved in immature ancient sedimentary rocks hold promise for tracking the diversification and ecological expansion of eukaryotes. Bacterial markers dominate biomarker assemblages until the early Neoproterozoic and eukaryotic steranes do not leave a detectable record till ca. 800 Ma and younger, probably due to low environmental abundance of microbial eukaryotes in most marine settings. The earliest proposed animal biomarkers from demosponges (Demospongiae) are recorded in a ca. 100-Myr-long sequence of Neoproterozoic-Cambrian marine sedimentary strata from the Huqf Supergroup, South Oman Salt Basin (Love et al., 2009). This C30 sterane biomarker, informally known as 24-isopropylcholestane (24-ipc), possesses the same carbon skeleton as sterols found in some modern-day demosponges. However, this evidence is controversial because 24-ipc is not exclusive to demosponges since 24-ipc sterols are found in trace amounts in some pelagophyte algae. We recently detected a new fossil sterane biomarker that co-occurs with 24-ipc in a suite of late Neoproterozoic-Cambrian sedimentary rocks and oils, which possesses a rare hydrocarbon skeleton that is uniquely found within extant demosponge taxa. This sterane is informally designated as 26-methylstigmastane (26-mes), reflecting the very unusual methylation at the terminus of the steroid side-chain. These new findings strongly suggest that demosponges, and hence multicellular animals, were prominent in some late Neoproterozoic marine environments at least extending back to the Cryogenian Period.

Professor Gordon Love, University of California, Riverside, USA

Professor Gordon Love, University of California, Riverside, USA

A focus of Dr Love's research program is molecular organic geochemistry, particularly the analysis of stable organic compounds preserved in ancient sedimentary rocks, oils and meteorites.  Additionally, he uses a range of complementary stable isotope and inorganic geochemical approaches for understanding carbon and other element biogeochemical cycling in the modern and ancient biosphere. Dr Love continued to use and refine novel analytical approaches that I helped develop with applications in geobiology, astrobiology and organic geochemistry. His degrees were in Chemistry but he developed a curiosity about the environmental and evolutionary history of our planet during his PhD research. After his PhD degree, he was awarded a NERC Fellowship to conduct lipid biomarker research at University of Newcastle then he spent three years at MIT as a Research Fellow. He joined the faculty at University of California, Riverside in 2007 and is currently Professor of Biogeochemistry in the Department of Earth Sciences.

A hypothesised rise in oxygen levels around the Neoproterozoic–Palaeozoic Boundary has been repeatedly linked to the origin and radiation of early animals. Given that oxygen is required by all extant animals, this hypothesis seems intuitive and has proved rather attractive. But a large body of recent work has shown that the role of oxygen in early animal ecosystems is more complex and dynamic than previously thought. One issue is that geochemical proxies often don’t provide the information needed to address ecologically relevant questions. For example, it is perhaps more important to know which regions of the ocean were anoxic, than how much of the ocean was anoxic. It is also important to know how much oxygen was available in the oxygenated parts of the ocean. Waters containing 100 µM or 1 µM O₂ would be indistinguishable in many proxy systems, but the first could host a complex ecosystem containing skeletal animals and motile predators, and the second would be largely uninhabitable. These issues can be partly resolved by considering the systematics of each geochemical proxy, and exactly what information it provides about the redox structure of ancient environments. This talk will focus on the questions we are able to ask using geochemical proxies, and evaluate our current ability to assess the role of oxygen in early animal evolution.

Dr Rosalie Tostevin, University of Cape Town, South Africa

Dr Rosalie Tostevin, University of Cape Town, South Africa

Dr Tostevin is a new lecturer in the Department of Geological Sciences at the University of Cape Town. Previously, she has worked as a postdoc at the University of Oxford and the University of Otago. She completed her PhD at University College London in 2015. She is interested in interactions between life and the environment on the early Earth. Dr Tostevin has worked on tracking major shifts in oceanic redox that occurred in the Precambrian using a variety of geochemical proxies, working closely with paleo-ecologists to tie together the chemical and ecological records.

Species do not live in isolation, but adapt and ultimately, evolve, in relationship with other species as well as with their chemical and physical environment. In the ocean, the surface biogeochemical environment modulates the makeup of the pelagic ecosystem, while the ecological assemblage, in turn, regulates the carbon and nutrient cycles in the ocean and concentration of CO2 in the atmosphere, thus influencing the environment. Evolutionary feedbacks, both negative and positive, must therefore exist between plankton, and global biogeochemical cycles and climate. This has important implications for understanding the rise of complex life and presents a significant challenge to understanding the rock record (what is the geological chicken vs. the egg?).

In this talk, Professor Ridgwell will illustrate a theoretical way forward via toy (‘fake’) worlds – aka, numerical models. Specifically, he will present some initial results of some contrasting modelling philosophies, both based on what happens if you incorporate a diverse marine ecology in an Earth system model. In the first example, idealized evolutionary changes in ecosystem structure are prescribed, and the attendant impacts on the marine environment are then simulated – (the chicken is prescribed and the eggs follow?). In the second, the structure and diversity of the ecosystem is allowed to ‘evolve’ in association with the environment. The resulting ecological successions exhibit some real world behavior, and in fact mimic observations of planktic evolutionary recovery in the aftermath of the end Cretaceous impact. The technical challenge is to apply such an approach to ~720-520 million years ago.

Professor Andy Ridgwell, University of California Riverside, USA

Professor Andy Ridgwell, University of California Riverside, USA

Andy Ridgwell is currently Professor of Earth System Science at the University of California, Riverside and Professorial Research Fellow at the University of Bristol, and in a prior incarnation, a Royal Society University Research Fellow. He writes computer models of global carbon cycling and climate, focusing on both past and future controls on the concentration of CO₂ in the atmosphere its interaction with life on this planet. His interests span questions of evolution and extinction, causes and consequences of changes in ocean chemistry, and geoengineering of the Earths’ climate. He is a great proponent of computer (programming) literacy and greater accessibility of tools (models) to help understand the complexities (and uncertainties) in the dynamics and evolution of the Earth system. He lives in the Southern Californian mountains where he collects cats and Pokémon.

Eukaryogenesis—the steps by which the eukaryotic cell emerged—has long intrigued scientists. The recent discovery of the closely related Asgard archaea has provided new insights into how this might have occurred, but fossils are the only way to reconstruct evolutionary transitions in clades now extinct. Though many cell characters are not preserved, there are at least four crown group characters for which proxy records exist: sterol synthesis (steranes), mitochondria (occurrences of fossils in different redox habitats), the cytoskeleton (fossils with spiny ornamentation), and the capacity to form resistant-walled cysts (the body fossils themselves). We could thus use these records to infer the relative order in which these characters evolved, and the environmental context of their evolution. In this talk I review these records and propose a different scenario for early eukaryote evolution than what is widely assumed. Rather than crown group eukaryotes originating in the late Paleoproterozoic and remaining ecologically minor components for more than half a billion years in a prokaryote-dominated world, the fossil record may point instead to a late emergence of the eukaryote crown group, with cyst formation and the cytoskeleton appearing early, and sterol synthesis evolving late. The origin of mitochondria cannot as easily be pinned down, in part because it’s difficult to reconstruct redox habitats of ancient eukaryotes. However, it is clear from the handful of studies we have that it cannot be assumed early Proterozoic eukaryotes were aerobic.

Professor Susannah Porter, University of California, Santa Barbara, USA

Professor Susannah Porter, University of California, Santa Barbara, USA

Susannah received her bachelor's degree in Mathematics from Yale University in 1995 and her Ph.D. in Biology at Harvard University in 2002. After completing a one-year NASA Astrobiology Post-Doctoral Fellowship at UCLA, she moved to the University of California at Santa Barbara, where she is Professor and Vice Chair in the Department of Earth Science. She studies the early fossil record of animals and their protistan relatives and has worked on problems relating to the evolution of skeletal biomineralization, the influence of snowball Earth glaciations on the biosphere, the early evolution of eukaryotes, and the Cambrian diversification of animals. She lives in Carpinteria, California, with her husband, Jamie, and her two sons, Willie and Sam.

Deciphering the role—if any—that oxygen levels played in controlling the timing and tempo of the radiation of complex life is one of the most fundamental questions in Earth and life sciences. Accurately reconstructing Earth’s redox history is an essential part of tackling this question.  Over the past few decades, there has been a flood of research applying geochemical redox proxies in an effort to tell the story of Earth’s oxygenation. However, many of these studies have led to conflicting interpretations of the timing and intensity of oxygenation events, even when considering the same isotopic systems. There are two potential explanations for conflicting redox reconstructions—1) that oxygen levels were incredibly dynamic in both time and space or 2) that as a community we have often studied rocks affected by secondary alteration (particularly secondary oxidation). It is an unpopular view to suggest that as a community we have failed to police our own work and it is even more unpopular to directly question the fidelity of individual studies. However, I will make a case that we—researchers interested in understanding the factors controlling the rise of complex life—are currently facing a quality control crisis. I will make a case that secondary alteration is likely widespread in previously published geochemical studies and highlight examples were other communities have faced similar quality control calamities. Lastly, I will argue that proper sample archiving in publicly assessable museums needs to be a prerequisite for publication in all paleoredox studies.

Dr Noah Planavsky, Yale University, USA

Dr Noah Planavsky, Yale University, USA

Noah Planavsky is an Assistant Professor in the Department of Geology and Geophysics at Yale University. He studies the connections between the evolution of Earth-system processes, biological innovation, and ecosystem change—foremost in Earth’s early history. His research integrates field, petrographic, and geochemical work. A central theme of his research has been trying to piece together the history and effects of Earth’s oxygenation. He has also worked on reconstructing the evolution of atmospheric carbon dioxide levels through Earth’s history. Current projects include coupling paleoredox proxies, calibrating novel metal isotope systems in modern aqueous systems and disentangling the distribution and diagenetic history of traces metals in sedimentary rocks.