The terrestrial end-Permian mass extinction in the paleotropics postdates the marine extinction.

The end-Permian mass extinction was the most severe ecological event during the Phanerozoic and has long been presumed contemporaneous across terrestrial and marine realms with global environmental deterioration triggered by the Siberian Traps Large Igneous Province. We present high-precision zircon U-Pb geochronology by the chemical abrasion-isotope dilution-thermal ionization mass spectrometry technique on tuffs from terrestrial to transitional coastal settings in Southwest China, which reveals a protracted collapse of the Cathaysian rainforest beginning after the onset of the end-Permian marine extinction. Integrated with high-resolution geochronology from coeval successions, our results suggest that the terrestrial extinction occurred diachronously with latitude, beginning at high latitudes during the late Changhsingian and progressing to the tropics by the early Induan, spanning a duration of nearly 1 million years. This latitudinal age gradient may have been related to variations in surface warming with more degraded environmental conditions at higher latitudes contributing to higher extinction rates.

In Science Journals.

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Ediacara growing pains: Modular addition and development in Dickinsonia costata.

Constraining patterns of growth using directly observable and quantifiable characteristics can reveal a wealth of information regarding the biology of the Ediacara Biota - the oldest macroscopic, complex community forming organisms in the fossil record. However, these rely on individuals captured at an instant in time at various growth stages, and so different interpretations can be derived from the same material. Here we leverage newly discovered and well-preserved Dickinsonia costata Sprigg 1947 from South Australia, combined with hundreds of previously described specimens, to test competing hypotheses for the location of module addition. We find considerable variation in the relationship between the total number of modules and body size that cannot be explained solely by expansion and contraction of individuals. Patterns derived assuming new modules differentiated at the anterior result in numerous examples where the oldest module(s) must decrease in size with overall growth, potentially falsifying this hypothesis. Observed polarity as well as the consistent posterior location of defects and indentations support module formation at this end in D. costata. Regardless, changes in repeated units with growth share similarities with those regulated by morphogen gradients in metazoans today, suggesting that these genetic pathways were operating in Ediacaran animals.

Felsic volcanism as a factor driving the end-Permian mass extinction.

The Siberian Traps large igneous province (STLIP) is commonly invoked as the primary driver of global environmental changes that triggered the end-Permian mass extinction (EPME). Here, we explore the contributions of coeval felsic volcanism to end-Permian environmental changes. We report evidence of extreme Cu enrichment in the EPME interval in South China. The enrichment is associated with an increase in the light Cu isotope, melt inclusions rich in copper and sulfides, and Hg concentration spikes. The Cu and Hg elemental and isotopic signatures can be linked to S-rich vapor produced by felsic volcanism. We use these previously unknown geochemical data to estimate volcanic SO2 injections and argue that this volcanism would have produced several degrees of rapid cooling before or coincident with the more protracted global warming. Large-scale eruptions near the South China block synchronous with the EPME strengthen the case that the STLIP may not have been the sole trigger.

Developmental processes in Ediacara macrofossils.

The Ediacara Biota preserves the oldest fossil evidence of abundant, complex metazoans. Despite their significance, assigning individual taxa to specific phylogenetic groups has proved problematic. To better understand these forms, we identify developmentally controlled characters in representative taxa from the Ediacaran White Sea assemblage and compare them with the regulatory tools underlying similar traits in modern organisms. This analysis demonstrates that the genetic pathways for multicellularity, axial polarity, musculature, and a nervous system were likely present in some of these early animals. Equally meaningful is the absence of evidence for major differentiation of macroscopic body units, including distinct organs, localized sensory machinery or appendages. Together these traits help to better constrain the phylogenetic position of several key Ediacara taxa and inform our views of early metazoan evolution. An apparent lack of heads with concentrated sensory machinery or ventral nerve cords in such taxa supports the hypothesis that these evolved independently in disparate bilaterian clades.

Tempos and modes of collectivity in the history of life.

Collective integration and processing of information have increased through the history of life, through both the formation of aggregates in which the entities may have very different properties and which jointly coarse-grained environmental variables (ranging from widely varying metabolism in microbial consortia to the ecological diversity of species on reefs) and through collectives of similar entities (such as cells within an organism or social groups). Such increases have been implicated in significant transitions in the history of life, including aspects of the origin of life, the generation of pangenomes among microbes and microbial communities such as stromatolites, multicellularity and social insects. This contribution provides a preliminary overview of the dominant modes of collective information processing in the history of life, their phylogenetic distribution and extent of convergence, and the effects of new modes for integrating and acting upon information on the tempo of evolutionary change.

A conceptual framework of evolutionary novelty and innovation.

Since 1990 the recognition of deep homologies among metazoan developmental processes and the spread of more mechanistic approaches to developmental biology have led to a resurgence of interest in evolutionary novelty and innovation. Other evolutionary biologists have proposed central roles for behaviour and phenotypic plasticity in generating the conditions for the construction of novel morphologies, or invoked the accessibility of new regions of vast sequence spaces. These approaches contrast with more traditional emphasis on the exploitation of ecological opportunities as the primary source of novelty. This definitional cornucopia reflects differing stress placed on three attributes of novelties: their radical nature, the generation of new taxa, and ecological and evolutionary impact. Such different emphasis has led to conflating four distinct issues: the origin of novel attributes (genes, developmental processes, phenotypic characters), new functions, higher clades and the ecological impact of new structures and functions. Here I distinguish novelty (the origin of new characters, deep character transformations, or new combinations) from innovation, the ecological and evolutionary success of clades. Evidence from the fossil record of macroevolutionary lags between the origin of a novelty and its ecological success demonstrates that novelty may be decoupled from innovation, and only definitions of novelty based on radicality (rather than generativity or consequentiality) can be assessed without reference to the subsequent history of the clade to which a novelty belongs. These considerations suggest a conceptual framework for novelty and innovation, involving: (i) generation of the potential for novelty; (ii) the formation of novel attributes; (iii) refinement of novelties through adaptation; (iv) exploitation of novelties by a clade, which may coincide with a new round of ecological or environmental potentiation; followed by (v) the establishment of innovations through ecological processes. This framework recognizes that there is little empirical support for either the dominance of ecological opportunity, nor abrupt discontinuities (often caricatured as 'hopeful monsters'). This general framework may be extended to aspects of cultural and social innovation.

Evolutionary dynamics of gene regulation.

The long controversy over the importance of changes in the regulatory genome has been resolved with the recognition that such changes are a fundamental component of evolutionary dynamics. Comparative studies have revealed four dominant modes of change as the regulatory genome evolved: (1) the origin of regulatory novelties such as distal enhancers and new types of promoters at the origin of Metazoa; (2) the expansion of regulatory capacity, most notably with diversification of transcription factors. Together these changes expanded the available combinatoric complexity of regulatory interactions and allow an increase in the variety of cell types. There are two more common modes of regulatory evolution: (3) Repatterning of gene regulatory networks. Such repatterning largely involves the introduction of transposons, promoter switching, co-option of regulatory genes or subcircuits, recombination, and the de novo generation of new regulatory sequences. Finally, (4) changes in enhancer and promoter specificity enable fine-scale adaptive changes. One of the outstanding issues at the intersection of evolutionary and developmental biology is how these various modes of regulatory evolution translate to morphological change, and particularly macro- and microevolutionary patterns and whether evolutionary novelties are associated with distinctive patterns of regulatory change.

On the co-evolution of surface oxygen levels and animals.

Few topics in geobiology have been as extensively debated as the role of Earth's oxygenation in controlling when and why animals emerged and diversified. All currently described animals require oxygen for at least a portion of their life cycle. Therefore, the transition to an oxygenated planet was a prerequisite for the emergence of animals. Yet, our understanding of Earth's oxygenation and the environmental requirements of animal habitability and ecological success is currently limited; estimates for the timing of the appearance of environments sufficiently oxygenated to support ecologically stable populations of animals span a wide range, from billions of years to only a few million years before animals appear in the fossil record. In this light, the extent to which oxygen played an important role in controlling when animals appeared remains a topic of debate. When animals originated and when they diversified are separate questions, meaning either one or both of these phenomena could have been decoupled from oxygenation. Here, we present views from across this interpretive spectrum-in a point-counterpoint format-regarding crucial aspects of the potential links between animals and surface oxygen levels. We highlight areas where the standard discourse on this topic requires a change of course and note that several traditional arguments in this "life versus environment" debate are poorly founded. We also identify a clear need for basic research across a range of fields to disentangle the relationships between oxygen availability and emergence and diversification of animal life.

The origin of animal body plans: a view from fossil evidence and the regulatory genome.

The origins and the early evolution of multicellular animals required the exploitation of holozoan genomic regulatory elements and the acquisition of new regulatory tools. Comparative studies of metazoans and their relatives now allow reconstruction of the evolution of the metazoan regulatory genome, but the deep conservation of many genes has led to varied hypotheses about the morphology of early animals and the extent of developmental co-option. In this Review, I assess the emerging view that the early diversification of animals involved small organisms with diverse cell types, but largely lacking complex developmental patterning, which evolved independently in different bilaterian clades during the Cambrian Explosion.

A high-resolution summary of Cambrian to Early Triassic marine invertebrate biodiversity.

One great challenge in understanding the history of life is resolving the influence of environmental change on biodiversity. Simulated annealing and genetic algorithms were used to synthesize data from 11,000 marine fossil species, collected from more than 3000 stratigraphic sections, to generate a new Cambrian to Triassic biodiversity curve with an imputed temporal resolution of 26 ± 14.9 thousand years. This increased resolution clarifies the timing of known diversification and extinction events. Comparative analysis suggests that partial pressure of carbon dioxide (Pco2) is the only environmental factor that seems to display a secular pattern similar to that of biodiversity, but this similarity was not confirmed when autocorrelation within that time series was analyzed by detrending. These results demonstrate that fossil data can provide the temporal and taxonomic resolutions necessary to test (paleo)biological hypotheses at a level of detail approaching those of long-term ecological analyses.

EvoChromo: towards a synthesis of chromatin biology and evolution.

Over the past few years, interest in chromatin and its evolution has grown. To further advance these interests, we organized a workshop with the support of The Company of Biologists to debate the current state of knowledge regarding the origin and evolution of chromatin. This workshop led to prospective views on the development of a new field of research that we term 'EvoChromo'. In this short Spotlight article, we define the breadth and expected impact of this new area of scientific inquiry on our understanding of both chromatin and evolution.

Prospects for a General Theory of Evolutionary Novelty.

Novelty is a topic of broad interest, with two distinct approaches within evolutionary biology. The dominant approach since Darwin has been transformationist, with novelty arising through gradual changes in morphology. The Modern Synthesis emphasized the importance of ecological opportunity rather than the source of variation, and this view has many adherents today. Yet, since well before Darwin, an alternative view has held that novelties could arise by rapid changes and many not necessarily be connected to ecological opportunity. The rise of comparative evolutionary developmental biology since 1990 has led to a resurgence of these arguments. Many case studies have documented novelties and there have been rigorous efforts to define the attributes of novelty, but there have been few attempts at a more general model. In contrast, studies of technological innovation have been replete with qualitative models since the 1930s. In this article I consider several possibilities for constructing a general model of novelty and innovation: (1) A general formal theory. (2) Commonalities between different levels, such as genes and morphology, but with sufficient differences between domains that any formal theory would be level specific. (3) Commonalities across levels but for various reasons developing a formal theory even within domains is improbable. A final alternative is that novelty and innovation may be so deeply historical that any general framework is impossible. I conclude that a common conceptual framework can be developed and serve as the foundation for simulation studies, but the importance of feedbacks and potentiating factors renders a formal model implausible.

Ediacaran Extinction and Cambrian Explosion.

The Ediacaran-Cambrian (E-C) transition marks the most important geobiological revolution of the past billion years, including the Earth's first crisis of macroscopic eukaryotic life, and its most spectacular evolutionary diversification. Here, we describe competing models for late Ediacaran extinction, summarize evidence for these models, and outline key questions which will drive research on this interval. We argue that the paleontological data suggest two pulses of extinction - one at the White Sea-Nama transition, which ushers in a recognizably metazoan fauna (the 'Wormworld'), and a second pulse at the E-C boundary itself. We argue that this latest Ediacaran fauna has more in common with the Cambrian than the earlier Ediacaran, and thus may represent the earliest phase of the Cambrian Explosion.

Innovation not recovery: dynamic redox promotes metazoan radiations.

Environmental fluctuations in redox may reinforce rather than hinder evolutionary transitions, such that variability in near-surface oceanic oxygenation can promote morphological evolution and novelty. Modern, low-oxygen regions are heterogeneous and dynamic habitats that support low diversity and are inhabited by opportunistic and non-skeletal metazoans. We note that several major radiation episodes follow protracted or repeating intervals (>1 million years) of persistent and dynamic shallow marine redox (oceanic anoxic events). These are also often associated with short-lived mass-extinction events (<0.5 million years) where skeletal benthic incumbents are removed, and surviving or newly evolved benthos initially inhabit transient oxic habitats. We argue that such intervals create critical opportunities for the generation of evolutionary novelty, followed by innovation and diversification. We develop a general model for redox controls on the distribution and structure of the shallow marine benthos in a dominantly anoxic world, and compile data from the terminal Ediacaran-mid-Cambrian (∼560-509 Ma), late Cambrian-Ordovician (∼500-445 Ma), and Permo-Triassic (∼255-205 Ma) to test these predictions. Assembly of phylogenetic data shows that prolonged and widespread anoxic intervals indeed promoted morphological novelty in soft-bodied benthos, providing the ancestral stock for subsequently skeletonized lineages to appear as innovations once oxic conditions became widespread and stable, in turn promoting major evolutionary diversification. As a result, we propose that so-called 'recovery' intervals after mass extinctions might be better considered as 'innovation' intervals.

The role of public goods in planetary evolution.

Biological public goods are broadly shared within an ecosystem and readily available. They appear to be widespread and may have played important roles in the history of life on Earth. Of particular importance to events in the early history of life are the roles of public goods in the merging of genomes, protein domains and even cells. We suggest that public goods facilitated the origin of the eukaryotic cell, a classic major evolutionary transition. The recognition of genomic public goods challenges advocates of a direct graph view of phylogeny, and those who deny that any useful phylogenetic signal persists in modern genomes. Ecological spillovers generate public goods that provide new ecological opportunities.This article is part of the themed issue 'Reconceptualizing the origins of life'.

Snowball Earth climate dynamics and Cryogenian geology-geobiology.

Geological evidence indicates that grounded ice sheets reached sea level at all latitudes during two long-lived Cryogenian (58 and ≥5 My) glaciations. Combined uranium-lead and rhenium-osmium dating suggests that the older (Sturtian) glacial onset and both terminations were globally synchronous. Geochemical data imply that CO2 was 102 PAL (present atmospheric level) at the younger termination, consistent with a global ice cover. Sturtian glaciation followed breakup of a tropical supercontinent, and its onset coincided with the equatorial emplacement of a large igneous province. Modeling shows that the small thermal inertia of a globally frozen surface reverses the annual mean tropical atmospheric circulation, producing an equatorial desert and net snow and frost accumulation elsewhere. Oceanic ice thickens, forming a sea glacier that flows gravitationally toward the equator, sustained by the hydrologic cycle and by basal freezing and melting. Tropical ice sheets flow faster as CO2 rises but lose mass and become sensitive to orbital changes. Equatorial dust accumulation engenders supraglacial oligotrophic meltwater ecosystems, favorable for cyanobacteria and certain eukaryotes. Meltwater flushing through cracks enables organic burial and submarine deposition of airborne volcanic ash. The subglacial ocean is turbulent and well mixed, in response to geothermal heating and heat loss through the ice cover, increasing with latitude. Terminal carbonate deposits, unique to Cryogenian glaciations, are products of intense weathering and ocean stratification. Whole-ocean warming and collapsing peripheral bulges allow marine coastal flooding to continue long after ice-sheet disappearance. The evolutionary legacy of Snowball Earth is perceptible in fossils and living organisms.

Developmental push or environmental pull? The causes of macroevolutionary dynamics.

Have the large-scale evolutionary patterns illustrated by the fossil record been driven by fluctuations in environmental opportunity, by biotic factors, or by changes in the types of phenotypic variants available for evolutionary change? Since the Modern Synthesis most evolutionary biologists have maintained that microevolutionary processes carrying on over sufficient time will generate macroevolutionary patterns, with no need for other pattern-generating mechanisms such as punctuated equilibrium or species selection. This view was challenged by paleontologists in the 1970s with proposals that the differential sorting and selection of species and clades, and the effects of biotic crises such as mass extinctions, were important extensions to traditional evolutionary theory. More recently those interested in macroevolution have debated the relative importance of abiotic and biotic factors in driving macroevolutionary patterns and have introduced comparative phylogenetic methods to analyze the rates of change in taxonomic diversity. Applying Peter Godfrey-Smith's distinction between distributional explanations and explanations focusing on the origin of variation, most macroevolutionary studies have provided distributional explanations of macroevolutionary patterns. Comparative studies of developmental evolution, however, have implicated the origin of variants as a driving macroevolution force. In particular, the repatterning of gene regulatory networks provides new insights into the origins of developmental novelties. This raises the question of whether macroevolution has been pulled by the generation of environmental opportunity, or pushed by the introduction of new morphologies. The contrast between distributional and origination scenarios has implications for understanding evolutionary novelty and innovation and how macroevolutionary process may have evolved over time.

The topology of evolutionary novelty and innovation in macroevolution.

Sewall Wright's fitness landscape introduced the concept of evolutionary spaces in 1932. George Gaylord Simpson modified this to an adaptive, phenotypic landscape in 1944 and since then evolutionary spaces have played an important role in evolutionary theory through fitness and adaptive landscapes, phenotypic and functional trait spaces, morphospaces and related concepts. Although the topology of such spaces is highly variable, from locally Euclidean to pre-topological, evolutionary change has often been interpreted as a search through a pre-existing space of possibilities, with novelty arising by accessing previously inaccessible or difficult to reach regions of a space. Here I discuss the nature of evolutionary novelty and innovation within the context of evolutionary spaces, and argue that the primacy of search as a conceptual metaphor ignores the generation of new spaces as well as other changes that have played important evolutionary roles.This article is part of the themed issue 'Process and pattern in innovations from cells to societies'.