The history of life on Earth progressed in parallel with the evolving oxygen state of the atmosphere and oceans, but the details of that relationship remain poorly known and debated. There is, however, general agreement that the first appreciable and persistent accumulation of oxygen in the oceans and atmosphere occurred around 2.3 to 2.4 billion years ago. Following this Great Oxidation Event, biospheric oxygen remained at relatively stable intermediate levels for more than a billion years. Much current research focuses on the transition from the intermediate conditions of this middle chapter in Earth history to the more oxygenated periods that followed — often emphasizing whether increasing and perhaps episodic oxygenation drove fundamental steps in the evolution of complex life and, if so, when. These relationships among early organisms and their environments are the thematic threads that stitch together the papers in this collection. Expert authors bring a mix of methods and opinions to their leading-edge reviews of the earliest proliferation and ecological impacts of eukaryotic life, the subsequent emergence and ecological divergence of animals, and the corresponding causes and consequences of environmental change.

The history of life on Earth is written in many chapters, and the first 90% are the most difficult to read. These sedimentary archives are rare and often altered through eons of heating and tectonic deformation. So elusive are those primary details that Darwin famously struggled to understand how rocky layers rich with animal fossils beginning ∼540 million years ago — an event now known as the Cambrian explosion [1] — sprung out of a seemingly lifeless past. The preceding 4 billion years of the Precambrian were dubbed the Cryptozoic in the late 19th century and defined as the time period ‘in which rocks contain no, or only slight, traces of living organisms [2].’

Generations of additional study have resolved Darwin's dilemma by revealing that the record of life before the Cambrian, from microbes to metazoans, is rich and diverse — captured in microfossils, organo-sedimentary structures such as stromatolites, the imprints of soft-bodied animals, and the earliest burrows and skeletons. Other signs lie with organic molecules, phylogenetic trees captured in the genes of extant organisms and given temporal context through molecular clocks, and isotopic signatures of microbial metabolisms. Moreover, many researchers have devoted careers to the cause-and-effect relationship between evolving life and coevolving environments at Earth's surface — recognizing that environments and their variations drive evolution but also that life can be a first-order agent of environmental change. We might think of the earliest photosynthetic production of oxygen (O2) perhaps 3 billion years ago and the concomitant oxidation of Earth's surface (reviewed in ref. [3].) as our best example of the latter.

In light of all this research, we can imagine an early world with a warming sun and cooling interior; continents first appearing, growing, and then colliding and ripping apart; evolving atmospheres with remarkably diverse compositions; and temperatures and climates from steamy to the icy expanses of snowball Earths. Yet through it all, mostly temperate climates and liquid oceans conceivably teeming with life first hit the scene more than 4 billion years ago and persisted from that point forward. This path led much later to the earliest animals roughly 700 million years ago. But it is the relationship among these physical and chemical processes and the parallel oxygenation of the early atmosphere and oceans that lies at the heart of most stories about the beginnings of complex life and its ecological consequences.

Dickinsonia costata, an extinct soft-bodied organism representing one of the first complex metazoans in the fossil record.

Dickinsonia costata, an extinct soft-bodied organism representing one of the first complex metazoans in the fossil record.

Total length 53.5 mm. This image was taken and provided by Scott Evans.

Dickinsonia costata, an extinct soft-bodied organism representing one of the first complex metazoans in the fossil record.

Total length 53.5 mm. This image was taken and provided by Scott Evans.

In this special issue devoted to early Earth and the rise of complex life, we use ‘complex’ to imply eukaryotes and multicellularity, culminating with metazoans. Our specific target is the earliest beginnings of ecosystems wherein eukaryotic populations first showed great diversity, ecological innovation, the emergence of diverse crown groups, and appreciable contributions to global primary production along with cycling and burial of the resulting organic matter. In this regard, the focus shifts from first appearances to ecological impact. The key question then is whether some or all of these milestones — perhaps initiating only ∼800 million years ago as led by algae and followed soon after by animals — were driven by or instead drove biospheric oxygenation. Furthermore, what were the coincident environmental transitions in the oceans, atmosphere, and solid Earth?

The first traces of eukaryotic life are microfossils observed in rocks from 1.7 to 1.6 billion years ago. There is general agreement within the research community that oxygen levels in the oceans and atmosphere at that time and for hundreds of millions of years following were stabilized at intermediate levels between a virtually anoxic earlier world and the oxygen-rich conditions that characterized much of the last half a billion years [3]. But far less a point of agreement is how high oxygen concentrations were during that middle chapter of Earth history — with estimates for the atmosphere ranging from 10% of the present atmospheric level to less than 1% or even 0.1%.

Another point of disagreement is when big changes in ocean–atmosphere oxygenation occurred, along with other environmental transformations often coupled to surface redox conditions that could have impacted life — such as climate and nutrient availability. The debate distils down to whether oxygen levels in the surface ocean remained low enough after the initial appearance of eukaryotes to stifle their ecological impact for many millions of years and whether fundamental environmental change was required to break through that ceiling and permit the emergence of animals. Or might the rise of animals have had nothing to do with oxygen triggers, as some suggest?

The papers in this volume reflect a diversity of opinion. Readers will not leave this collection with a clear single answer, but they will get an up-to-date view of the debates about evolving early complex life and its environments, the full context that lies behind the questions and uncertainties, and the work left to do. Some of the seeds for this volume were first sown back in 2014 during a NASA-NSF joint workshop — Beyond Habitability: Coevolution of Life and the Early Earth — held at the Smithsonian Institution and organized by Editor Lyons, Doug Erwin of the Smithsonian, and NASA's Lindsay Hays. Over the span of a week, topics covered began with Earth's earliest habitability more than 4 billion years ago and extended billions of years forward to the emergence of complex life and its ecosystem relationships. We have chosen to narrow the focus here to the latter.

The eighteen papers included in this special issue span the full range of approaches available in studies of early life and its environments. Among those, novel stratigraphic evaluations of the sediments hosting records of biotic and environmental evolution broaden the context and hint at the possibility that creation and destruction of the sedimentary record itself may be the ultimate geologic driver of oxygenation [4]. New perspectives offered on age relationships reveal the tempo and pattern of evolution while providing a robust framework for global correlation and for the possible relationships between biotic and environmental change [5].

Discussions about oxygen in the oceans and atmosphere occupy many of the pages. Among the crucial considerations are the possibilities of still low levels of O2 during the so-called ‘boring billion’ roughly 1.8–0.8 billion years ago [6] and subsequent dramatic changes in eukaryotic life and perhaps oxygenation between the boring billion and global glaciations that initiated ∼720 million years ago [7]. Cohen and Riedman [8] link predation among single-celled eukaryotes (protists) to patterns of diversification and innovation in the same time period. Organic biomarkers speak to increasing algal contributions leading up to and during the glacial period [9], while the complementary review of Gold [10] speaks to the time gap between the first appearance of eukaryotes (expressed in fossils and genomic data) and their later rise to ecological significance recorded in biomarkers. Others make a connection between younger O2 increases suggested ∼550 million years ago and animal activities and characteristics that may have demanded increased oxygenation, such as biomineralization [11] and advances in motility and predation expressed in burrowing and scavenging traces [12]. Also at ∼560–550 million years ago, morphological trends suggest patterns of variation in the number of cells in diffusive contact with seawater that may have scaled inversely with dynamic (rising and falling) O2 levels in seawater [13].

The prospect of short-term dynamics in oxygen contents of the oceans and atmosphere against a backdrop of long-term O2 increases is a theme in other contributions. For example, Diamond and Lyons [14] explore the possibility of transient oxygenation events during the boring billion that could have driven eukaryotic evolution despite overall low background O2 levels. Perhaps consistent with these observations, Loron et al. [15] propose that patterns of pre-800-million-year eukaryotic diversification may be underappreciated, including early predation pressure as a possible driver.

Other authors look at environmental variability beyond these earlier chapters of our history to ∼800 million years ago and the 200+ million years that followed. In one case, Shields [16] envisions dynamic environments tied to accumulation and remineralization of a vast pool of dissolved organic matter. This waxing and waning may have modulated biospheric oxygenation, climate, and related radiations of life — including the snowball glaciations and the early emergence of animals. Similarly, Lenton and Daines [17] give us new modeling solutions tied to evolving organic and nutrient recycling to explain possible oxygenation dynamics (events) during the Cyrogenian snowball glacial episodes (∼720–635 million years ago), the Ediacaran (∼635–540 million years ago), and the Cambrian immediately following. Trends in South China implying animal evolution coupled to spatially heterogeneous and temporally dynamic oxygenation on marine shelves support these calculations [18].

Some authors place less emphasis on the biological benefits of rising oxygen levels in the oceans and atmosphere. Mills et al. [19], for example, suggest that relationships between the timing of fundamental biotic change and increasing oxygenation remain open to question and specifically that the emergence of animals was decoupled from environmental transitions — instead reflecting ‘internal, developmental constraints.’ Porter et al. [20] note that many early eukaryotes may have been well adapted to low O2 conditions, and rising oxygen for them could have been deleterious. Sperling et al. [21] draw a line connecting exceptional preservation of animal remains to the likely persistence of widespread anoxia in the oceans even during the Cambrian — despite the likelihood of earlier increases in marine O2.

Our priority was to solicit overviews of the known pages in these crucial chapters and those awaiting discovery — all viewed through the critical eyes of expert witnesses. We encouraged presentations designed to capture, in a balanced way, a broadly accessible big picture that collectively would expose controversies. To further sharpen that cutting edge, we asked authors for their particular spins on long-standing questions. These papers are largely analytical reviews of existing data, but some offer new results to bolster the arguments made. If we have succeeded, readers new to the questions and related data will join those deep in the same trenches as the authors in learning something new about old life.

We are grateful to the staff of Portland Press and Emerging Topics in Life Sciences in particular for their many layers of expert support and to the Biochemical Society and Royal Society of Biology for catalyzing this special issue. NASA and the U.S. National Science Foundation provided financial and intellectual support for the initial workshops and for this volume specifically. We especially call out Sonia Esperanca, the late Rich Lane, Lindsay Hays Michael New, and Mary Voytek for their contributions and encouragement throughout.

Competing Interests

The Authors declare that there are no competing interests associated with the manuscript.

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