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.

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. 

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?

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.

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.

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.

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.

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.