Evolution Of Complex Life Research Articles

The emerging view on the origin and early evolution of eukaryotic cells.

The origin of the eukaryotic cell, with its compartmentalized nature and generally large size compared with bacterial and archaeal cells, represents a cornerstone event in the evolution of complex life on Earth. In a process referred to as eukaryogenesis, the eukaryotic cell is believed to have evolved between approximately 1.8 and 2.7 billion years ago from its archaeal ancestors, with a symbiosis with a bacterial (proto-mitochondrial) partner being a key event. In the tree of life, the branch separating the first from the last common ancestor of all eukaryotes is long and lacks evolutionary intermediates. As a result, the timing and driving forces of the emergence of complex eukaryotic features remain poorly understood. During the past decade, environmental and comparative genomic studies have revealed vital details about the identity and nature of the host cell and the proto-mitochondrial endosymbiont, enabling a critical reappraisal of hypotheses underlying the symbiotic origin of the eukaryotic cell. Here we outline our current understanding of the key players and events underlying the emergence of cellular complexity during the prokaryote-to-eukaryote transition and discuss potential avenues of future research that might provide new insights into the enigmatic origin of the eukaryotic cell.

Assessing the Influence of HGT on the Evolution of Stress Responses in Microbial Communities from Shark Bay, Western Australia.

Pustular microbial mats in Shark Bay, Western Australia, are modern analogs of microbial systems that colonized peritidal environments before the evolution of complex life. To understand how these microbial communities evolved to grow and metabolize in the presence of various environmental stresses, the horizontal gene transfer (HGT) detection tool, MetaCHIP, was used to identify the horizontal transfer of genes related to stress response in 83 metagenome-assembled genomes from a Shark Bay pustular mat. Subsequently, maximum-likelihood phylogenies were constructed using these genes and their most closely related homologs from other environments in order to determine the likelihood of these HGT events occurring within the pustular mat. Phylogenies of several stress-related genes-including those involved in response to osmotic stress, oxidative stress and arsenic toxicity-indicate a potentially long history of HGT events and are consistent with these transfers occurring outside of modern pustular mats. The phylogeny of a particular osmoprotectant transport gene reveals relatively recent adaptations and suggests interactions between Planctomycetota and Myxococcota within these pustular mats. Overall, HGT phylogenies support a potentially broad distribution in the relative timing of the HGT events of stress-related genes and demonstrate ongoing microbial adaptations and evolution in these pustular mat communities.

An Absentological Analysis of the Trace: Pre-Cambrian Arche-Writing, and Jacques Derrida’s Realism

The first trace-fossil in the history of terrestrial life dates to the pre-Cambrian era. Left by an unknown species around 542 million years ago, Treptichnus are fossilized mud burrows, remaining as a geological testament to the early stages of complex life on Earth. Because of the impossibility of any empirical knowledge relating to these unfossilizable creatures, which presumably lacked a skeletal structure, any philosophical treatment of this paleobiological matter of fact must necessarily engage in speculation. Absentology as a speculative epistemontological register allows us to conceptualize these strange burrows as a key event. Following Jacques Derrida’s concept of"arche-writing", our essay presents an absentological reading of the forever unknowable unfossilized animal species. Arche-writing for Derrida is an abstract mode of writing that precedes speech and actual written language, hence this constitutes a concept that can be used for prelinguistic modes of expression. The trace fossils left by these unknown creatures constitute a type of prewriting, as well as the dawn of work, representing a crucial step in the evolution of complex life on this planet. A fossil that is not the animal itself, but rather a trace referring to an unknown organic singularity, this is the absent scene of arche-writing. A more realist Derrida emerges from this encounter, for whom extra-textual elements are even more relevant than explicit language.

Biostratinomy of the enigmatic tubular organism Aulozoon soliorum, the Rawnsley Quartzite, South Australia

The Ediacaran fauna (574–539 Ma) are the first macroscopic community forming organisms on Earth, thus providing unique insight into the origins and evolution of complex life. However, the assignment of most Ediacaran organisms to specific phyla and kingdoms remains difficult due to their commonly non-analogous body plans and soft-bodied nature, which often results in the loss of diagnostic features through the processes of death and fossilization. Notably, this taphonomic overprint is not imparted equally to all Ediacaran organisms and is particularly exaggerated for the morphotypic grouping of tubular organisms. This morphogroup is comprised of macroscopic organisms with elongate, hollow, and simple body plans and is the most abundant Ediacaran morphogroup. However, the simple and hollow morphology of tubular organisms results in a broadly low preservation potential. In turn, this commonly limits the reconstruction of in vivo morphology, muddles taxonomic assignment, obfuscates phylogenetic affinities, and inhibits understanding of their broader significance. Fortunately, previous studies of abundant tubular taxa have demonstrated that taxon-level biostratinomic investigations can, in part, account for this low preservation potential. Such studies inform a more complete understanding of the morphogroup, providing novel insight into the paleobiology, paleoecology, and biomaterials of tubular taxa. To contribute to this biostratinomically-geared assessment of Ediacaran tubular organisms, this study analyzes the preservation of Aulozoon soliorum, an abundant tubular organism from the Rawnsley Quartzite of South Australia. This investigation demonstrates that Aulozoon is preserved via five preservational modes, which inform a novel in vivo reconstruction of Aulozoon as a sessile, fluid-filled, cylindrical organism with a holdfast and a thin, organic, and featureless body wall. The preservational modes identified here additionally inform a taphonomic framework under which Aulozoon fossils can be interpreted, thus furthering holistic understanding of the morphogroup-specific preservational variability of Ediacaran tubular organisms.

Chromium evidence for protracted oxygenation during the Paleoproterozoic

It has commonly been proposed that the development of complex life is tied to increases in atmospheric oxygenation. However, there is a conspicuous gap in time between the oxygenation of the atmosphere 2.4 billion years ago (Ga) and the first widely-accepted fossil evidence for complex eukaryotic cells <1.7Ga. At present the gap could either represent poor sampling, poor preservation, and/or difficulties in recognizing early eukaryote fossils, or it could be real and the evolution of complex cells was delayed due to relatively low and/or variable O2 levels in the Paleoproterozoic. To assess the extent and stability of Paleoproterozoic O2 levels, we measured chromium-based oxygen proxies in a >2400-m core from the Onega Basin (NW-Russia), deposited ∼2.1–2.0 billion years ago—a few hundred million years prior to the oldest definitive fossil evidence for eukaryotes. Fractionated chromium isotopes are documented throughout the section (max. 1.63±0.10‰δ53Cr), suggesting a long interval (possibly >100 million years) during which oxygen levels were higher and more stable than in the billion years before or after. This suggests that, if it is the case that complex cells did not evolve until after 1.7 Ga, then this delay was not due to O2-limitation. Instead, it could reflect other limiting factors—ecological or environmental—or could indicate that it simply takes a long time—more than the tens to >100 million years recorded in Onega Basin sediments—for such biological innovations to evolve.

The tempo of Ediacaran evolution.

The rise of complex macroscopic life occurred during the Ediacaran Period, an interval that witnessed large-scale disturbances to biogeochemical systems. The current Ediacaran chronostratigraphic framework is of insufficient resolution to provide robust global correlation schemes or test hypotheses for the role of biogeochemical cycling in the evolution of complex life. Here, we present new radio-isotopic dates from Ediacaran strata that directly constrain key fossil assemblages and large-magnitude carbon cycle perturbations. These new dates and integrated global correlations demonstrate that late Ediacaran strata of South China are time transgressive and that the 575- to 550-Ma interval is marked by two large negative carbon isotope excursions: the Shuram and a younger one that ended ca. 550 Ma ago. These data calibrate the tempo of Ediacaran evolution characterized by intervals of tens of millions of years of increasing ecosystem complexity, interrupted by biological turnovers that coincide with large perturbations to the carbon cycle.

The oxygen cycle and a habitable Earth

As an important contributor to the habitability of our planet, the oxygen cycle is interconnected with the emergence and evolution of complex life and is also the basis to establish Earth system science. Investigating the global oxygen cycle provides valuable information on the evolution of the Earth system, the habitability of our planet in the geologic past, and the future of human life. Numerous investigations have expanded our knowledge of the oxygen cycle in the fields of geology, geochemistry, geobiology, and atmospheric science. However, these studies were conducted separately, which has led to one-sided understandings of this critical scientific issue and an incomplete synthesis of the interactions between the different spheres of the Earth system. This review presents a five-sphere coupled model of the Earth system and clarifies the core position of the oxygen cycle in Earth system science. Based on previous research, this review comprehensively summarizes the evolution of the oxygen cycle in geological time, with a special focus on the Great Oxidation Event (GOE) and the mass extinctions, as well as the possible connections between the oxygen content and biological evolution. The possible links between the oxygen cycle and biodiversity in geologic history have profound implications for exploring the habitability of Earth in history and guiding the future of humanity. Since the Anthropocene, anthropogenic activities have gradually steered the Earth system away from its established trajectory and had a powerful impact on the oxygen cycle. The human-induced disturbance of the global oxygen cycle, if not controlled, could greatly reduce the habitability of our planet.

A model of developmental canalization, applied to human cranial form.

Developmental mechanisms that canalize or compensate perturbations of organismal development (targeted or compensatory growth) are widely considered a prerequisite of individual health and the evolution of complex life, but little is known about the nature of these mechanisms. It is even unclear if and how a “target trajectory” of individual development is encoded in the organism’s genetic-developmental system or, instead, emerges as an epiphenomenon. Here we develop a statistical model of developmental canalization based on an extended autoregressive model. We show that under certain assumptions the strength of canalization and the amount of canalized variance in a population can be estimated, or at least approximated, from longitudinal phenotypic measurements, even if the target trajectories are unobserved. We extend this model to multivariate measures and discuss reifications of the ensuing parameter matrix. We apply these approaches to longitudinal geometric morphometric data on human postnatal craniofacial size and shape as well as to the size of the frontal sinuses. Craniofacial size showed strong developmental canalization during the first 5 years of life, leading to a 50% reduction of cross-sectional size variance, followed by a continual increase in variance during puberty. Frontal sinus size, by contrast, did not show any signs of canalization. Total variance of craniofacial shape decreased slightly until about 5 years of age and increased thereafter. However, different features of craniofacial shape showed very different developmental dynamics. Whereas the relative dimensions of the nasopharynx showed strong canalization and a reduction of variance throughout postnatal development, facial orientation continually increased in variance. Some of the signals of canalization may owe to independent variation in developmental timing of cranial components, but our results indicate evolved, partly mechanically induced mechanisms of canalization that ensure properly sized upper airways and facial dimensions.

Calibrating the coevolution of Ediacaran life and environment

The rise of animals occurred during an interval of Earth history that witnessed dynamic marine redox conditions, potentially rapid plate motions, and uniquely large perturbations to global biogeochemical cycles. The largest of these perturbations, the Shuram carbon isotope excursion, has been invoked as a driving mechanism for Ediacaran environmental change, possibly linked with evolutionary innovation or extinction. However, there are a number of controversies surrounding the Shuram, including its timing, duration, and role in the concomitant biological and biogeochemical upheavals. Here we present radioisotopic dates bracketing the Shuram on two separate paleocontinents; our results are consistent with a global and synchronous event between 574.0 ± 4.7 and 567.3 ± 3.0 Ma. These dates support the interpretation that the Shuram is a primary and synchronous event postdating the Gaskiers glaciation. In addition, our Re-Os ages suggest that the appearance of Ediacaran macrofossils in northwestern Canada is identical, within uncertainty, to similar macrofossils from the Conception Group of Newfoundland, highlighting the coeval appearance of macroscopic metazoans across two paleocontinents. Our temporal framework for the terminal Proterozoic is a critical step for testing hypotheses related to extreme carbon isotope excursions and their role in the evolution of complex life.

The evolution of complex life and the stabilization of the Earth system.

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: (i) a decrease in the intensity of interactions among species that lead to extinctions; (ii) a decrease in the prevalence or intensity of geological triggers such as flood basalt eruptions and bolide impacts; (iii) a decrease in the sensitivity of animals to environmental disturbance; or (iv) 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 palaeontology, geochemistry and comparative physiology that animals have become more resilient to an 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.

Just a Bit of Physics Can Tell So Much: A Unique Story of the Start of the Earth-Moon System

The start of the Earth-Moon system has been studied to show that this was an exceptionally violent event. One result was that Earth became the terrestrial planet with the highest average density. Another result was that Earth acquired enough mass and radioactive elements that it is expected to maintain a molten core region and magnetic field for the expected life of the Earth. Earth alone of the terrestrial planets was then able to develop plate tectonics as a long term energy release mechanism. The dipole magnetic field of the Sun reverses periodically, currently at the rate of about every 11 years, so that there was a magnetic braking action acting on the core of Venus that accounts for the slow rotation of that planet. A key result is that the impact event that resulted in the Earth-Moon system led to long term stability on Earth that allowed the eventual development of complex life forms on the Earth.

The fate of a Neoproterozoic intracratonic marine basin: Trace elements, TOC and IRON speciation geochemistry of the Bambuí Basin, Brazil

Neoproterozoic marine systems are associated with major paleoecological changes that took place in the Ediacaran and during the Ediacaran-Cambrian transition. During this timespan, the Bambuí basin located on east Brazil held a peculiar paleoenvironmental scenario. Due to its intracratonic evolution, the basin was partially disconnected from neighboring open marine systems. This setting raises a very interesting opportunity to understand how an isolated Neoproterozoic marine system evolved in contrast with typical (globally connected) open marine systems. To understand the paleoenvironmental changes that took place in the Bambuí basin, we investigate the pre-glaciogenic deposits of the Carrancas Fm and the post-glaciogenic mixed (shale-carbonate) successions of the Bambuí Group. Through the analysis of iron speciation, TOC, trace element and C-O isotope systematics, our study suggests a very complex environmental evolution. Firstly, our samples are marked by strong contamination of detrital continental material that can be related to an increased bioproductivity on both the Carrancas Fm. and lower Bambuí group stratigraphic units, and provenance data show that all studied sediments probably shared common source areas. Iron speciation data, Ce anomalies and RSE enrichments shows that lower Bambuí Group stratigraphic units were likely deposited in an open marine scenario featuring high bioproductivity in shallow waters and euxinic incursions in predominant anoxic/ferruginous bottom waters. On the other hand, upper Bambuí stratigraphic units register a marine evolution in a restricted scenario, where anoxic ferruginous conditions probably reached surface waters. Finally, our data show that the lack of oceanic connection prevented the re-supply of marine sulfate, RSE, bionutrients and ultimately of dissolved oxygen which may have decreased biological activity and probably hindered biological evolution, preventing the rise of a typical modern-like Cambrian ecosystem. In this sense, our data suggest that oceanic connectivity and proper re-supply of inorganic marine input were important features in the development of complex life in the Ediacaran-Cambrian environment.

A sluggish mid-Proterozoic biosphere and its effect on Earth's redox balance.

The possibility of low but nontrivial atmospheric oxygen (O2) levels during the mid‐Proterozoic (between 1.8 and 0.8 billion years ago, Ga) has important ramifications for understanding Earth's O2 cycle, the evolution of complex life and evolving climate stability. However, the regulatory mechanisms and redox fluxes required to stabilize these O2 levels in the face of continued biological oxygen production remain uncertain. Here, we develop a biogeochemical model of the C‐N‐P‐O2‐S cycles and use it to constrain global redox balance in the mid‐Proterozoic ocean–atmosphere system. By employing a Monte Carlo approach bounded by observations from the geologic record, we infer that the rate of net biospheric O2 production was 3.5−1.1+1.4 Tmol year−1 (1σ), or ~25% of today's value, owing largely to phosphorus scarcity in the ocean interior. Pyrite burial in marine sediments would have represented a comparable or more significant O2 source than organic carbon burial, implying a potentially important role for Earth's sulphur cycle in balancing the oxygen cycle and regulating atmospheric O2 levels. Our statistical approach provides a uniquely comprehensive view of Earth system biogeochemistry and global O2 cycling during mid‐Proterozoic time and implicates severe P biolimitation as the backdrop for Precambrian geochemical and biological evolution.

Early Earth and the rise of complex life

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 slow rise of complex life as revealed through biomarker genetics.

Organic molecules preserved in ancient rocks can function as 'biomarkers', providing a unique window into the evolution of life. While biomarkers demonstrate intriguing patterns through the Neoproterozoic, it can be difficult to constrain particular biomarkers to specific organisms. The goal of the present paper is to demonstrate the utility of biomarkers when we focus less on which organisms produce them, and more on how their underlying genetic pathways evolved. Using this approach, it becomes clear that there are discrepancies between the biomarker, fossil, and molecular records. However, these discrepancies probably represent long time periods between the diversification of eukaryotic groups through the Neoproterozoic and their eventual rise to ecological significance. This 'long fuse' hypothesis contrasts with the adaptive radiations often associated with the development of complex life.

The Boring Billion, a slingshot for Complex Life on Earth

The period 1800 to 800 Ma (“Boring Billion”) is believed to mark a delay in the evolution of complex life, primarily due to low levels of oxygen in the atmosphere. Earlier studies highlight the remarkably flat C, Cr isotopes and low trace element trends during the so-called stasis, caused by prolonged nutrient, climatic, atmospheric and tectonic stability. In contrast, we suggest a first-order variability of bio-essential trace element availability in the oceans by combining systematic sampling of the Proterozoic rock record with sensitive geochemical analyses of marine pyrite by LA-ICP-MS technique. We also recall that several critical biological evolutionary events, such as the appearance of eukaryotes, origin of multicellularity & sexual reproduction, and the first major diversification of eukaryotes (crown group) occurred during this period. Therefore, it appears possible that the period of low nutrient trace elements (1800–1400 Ma) caused evolutionary pressures which became an essential trigger for promoting biological innovations in the eukaryotic domain. Later periods of stress-free conditions, with relatively high nutrient trace element concentration, facilitated diversification. We propose that the “Boring Billion” was a period of sequential stepwise evolution and diversification of complex eukaryotes, triggering evolutionary pathways that made possible the later rise of micro-metazoans and their macroscopic counterparts.

Reactive Oxygen Species: Radical Factors in the Evolution of Animal Life: A molecular timescale from Earth's earliest history to the rise of complex life.

Introduction of O2 to Earth's early biosphere stimulated remarkable evolutionary adaptations, and a wide range of electron acceptors allowed diverse, energy-yielding metabolic pathways. Enzymatic reduction of O2 yielded a several-fold increase in energy production, enabling evolution of multi-cellular animal life. However, utilization of O2 also presented major challenges as O2 and many of its derived reactive oxygen species (ROS) are highly toxic, possibly impeding multicellular evolution after the Great Oxidation Event. Remarkably, ROS, and especially hydrogen peroxide, seem to play a major part in early diversification and further development of cellular respiration and other oxygenic pathways, thus becoming an intricate part of evolution of complex life. Hence, although harnessing of chemical and thermo-dynamic properties of O2 for aerobic metabolism is generally considered to be an evolutionary milestone, the ability to use ROS for cell signaling and regulation may have been the first true breakthrough in development of complex life.

Evolutionary exobiology: towards the qualitative assessment of biological potential on exoplanets

AbstractA planet may be defined as habitable if it has an atmosphere and is warm enough to support the existence of liquid water on its surface. Such a world has the basic set of conditions that allow it to develop life similar to ours, which is carbon-based and has water as its universal solvent. While this definition is suitably vague to allow a fairly broad range of possibilities, it does not address the question as to whether any life that does form will become either complex or intelligent. In this paper, we seek to synthesize a qualitative definition of which subset of these ‘habitable worlds’ might develop more complex and interesting life forms. We identify two key principles in determining the capacity of life to breach certain transitions on route to developing intelligence. The first is the number of potential niches a planet provides. Secondly, the complexity of life will reflect the information density of its environment, which in turn can be approximated by the number of available niches. We seek to use these criteria to begin the process of placing the evolution of terrestrial life in a mathematical framework based on environmental information content. This is currently testable on Earth and will have clear application to the worlds that we are only beginning to discover. Our model links the development of complex life to the physical properties of the planet, something which is currently lacking in all evolutionary theory.

Algal light sensing and photoacclimation in aquatic environments.

Anoxygenic photosynthetic prokaryotes arose in ancient oceans ~3.5 billion years ago. The evolution of oxygenic photosynthesis by cyanobacteria followed soon after, enabling eukaryogenesis and the evolution of complex life. The Archaeplastida lineage dates back ~1.5 billion years to the domestication of a cyanobacterium. Eukaryotic algae have subsequently radiated throughout oceanic/freshwater/terrestrial environments, adopting distinctive morphological and developmental strategies for adaptation to diverse light environments. Descendants of the ancestral photosynthetic alga remain challenged by a typical diurnally fluctuating light supply ranging from ~0 to ~2000μEm-2 s-1 . Such extreme changes in light intensity and variations in light quality have driven the evolution of novel photoreceptors, light-harvesting complexes and photoprotective mechanisms in photosynthetic eukaryotes. This minireview focuses on algal light sensors, highlighting the unexpected roles for linear tetrapyrroles (bilins) in the maintenance of functional chloroplasts in chlorophytes, sister species to streptophyte algae and land plants.

Towards a Unified View of Inhomogeneous Stellar Winds in Isolated Supergiant Stars and Supergiant High Mass X-Ray Binaries

Massive stars, at least $\sim$ 10 times more massive than the Sun, have two key properties that make them the main drivers of evolution of star clusters, galaxies, and the Universe as a whole. On the one hand, the outer layers of massive stars are so hot that they produce most of the ionizing ultraviolet radiation of galaxies; in fact, the first massive stars helped to re-ionize the Universe after its Dark Ages. Another important property of massive stars are the strong stellar winds and outflows they produce. This mass loss, and finally the explosion of a massive star as a supernova or a gamma-ray burst, provide a significant input of mechanical and radiative energy into the interstellar space. These two properties together make massive stars one of the most important cosmic engines: they trigger the star formation and enrich the interstellar medium with heavy elements, that ultimately leads to formation of Earth-like rocky planets and the development of complex life. The study of massive star winds is thus a truly multidisciplinary field and has a wide impact on different areas of astronomy. [...] This detailed review summarises the current knowledge on the theory and observations of winds from massive stars, as well as on observations and accretion processes in wind-fed high mass X-ray binaries. The aim is to combine in the near future all available theoretical diagnostics and observational measurements to achieve a unified picture of massive star winds in isolated objects and in binary systems.