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.

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.

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.

The origin and evolution of cell types.

Cell types are the basic building blocks of multicellular organisms and are extensively diversified in animals. Despite recent advances in characterizing cell types, classification schemes remain ambiguous. We propose an evolutionary definition of a cell type that allows cell types to be delineated and compared within and between species. Key to cell type identity are evolutionary changes in the 'core regulatory complex' (CoRC) of transcription factors, that make emergent sister cell types distinct, enable their independent evolution and regulate cell type-specific traits termed apomeres. We discuss the distinction between developmental and evolutionary lineages, and present a roadmap for future research.

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.

Rarity in mass extinctions and the future of ecosystems.

The fossil record provides striking case studies of biodiversity loss and global ecosystem upheaval. Because of this, many studies have sought to assess the magnitude of the current biodiversity crisis relative to past crises-a task greatly complicated by the need to extrapolate extinction rates. Here we challenge this approach by showing that the rarity of previously abundant taxa may be more important than extinction in the cascade of events leading to global changes in the biosphere. Mass rarity may provide the most robust measure of our current biodiversity crisis relative to those past, and new insights into the dynamics of mass extinction.

Earth's oxygen cycle and the evolution of animal life.

The emergence and expansion of complex eukaryotic life on Earth is linked at a basic level to the secular evolution of surface oxygen levels. However, the role that planetary redox evolution has played in controlling the timing of metazoan (animal) emergence and diversification, if any, has been intensely debated. Discussion has gravitated toward threshold levels of environmental free oxygen (O2) necessary for early evolving animals to survive under controlled conditions. However, defining such thresholds in practice is not straightforward, and environmental O2 levels can potentially constrain animal life in ways distinct from threshold O2 tolerance. Herein, we quantitatively explore one aspect of the evolutionary coupling between animal life and Earth's oxygen cycle-the influence of spatial and temporal variability in surface ocean O2 levels on the ecology of early metazoan organisms. Through the application of a series of quantitative biogeochemical models, we find that large spatiotemporal variations in surface ocean O2 levels and pervasive benthic anoxia are expected in a world with much lower atmospheric pO2 than at present, resulting in severe ecological constraints and a challenging evolutionary landscape for early metazoan life. We argue that these effects, when considered in the light of synergistic interactions with other environmental parameters and variable O2 demand throughout an organism's life history, would have resulted in long-term evolutionary and ecological inhibition of animal life on Earth for much of Middle Proterozoic time (∼1.8-0.8 billion years ago).

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'.

When and how did the terrestrial mid-Permian mass extinction occur? Evidence from the tetrapod record of the Karoo Basin, South Africa.

A mid-Permian (Guadalupian epoch) extinction event at approximately 260 Ma has been mooted for two decades. This is based primarily on invertebrate biostratigraphy of Guadalupian-Lopingian marine carbonate platforms in southern China, which are temporally constrained by correlation to the associated Emeishan Large Igneous Province (LIP). Despite attempts to identify a similar biodiversity crisis in the terrestrial realm, the low resolution of mid-Permian tetrapod biostratigraphy and a lack of robust geochronological constraints have until now hampered both the correlation and quantification of terrestrial extinctions. Here we present an extensive compilation of tetrapod-stratigraphic data analysed by the constrained optimization (CONOP) algorithm that reveals a significant extinction event among tetrapods within the lower Beaufort Group of the Karoo Basin, South Africa, in the latest Capitanian. Our fossil dataset reveals a 74-80% loss of generic richness between the upper Tapinocephalus Assemblage Zone (AZ) and the mid-Pristerognathus AZ that is temporally constrained by a U-Pb zircon date (CA-TIMS method) of 260.259 ± 0.081 Ma from a tuff near the top of the Tapinocephalus AZ. This strengthens the biochronology of the Permian Beaufort Group and supports the existence of a mid-Permian mass extinction event on land near the end of the Guadalupian. Our results permit a temporal association between the extinction of dinocephalian therapsids and the LIP volcanism at Emeishan, as well as the marine end-Guadalupian extinctions.

Biotic replacement and mass extinction of the Ediacara biota.

The latest Neoproterozoic extinction of the Ediacara biota has been variously attributed to catastrophic removal by perturbations to global geochemical cycles, 'biotic replacement' by Cambrian-type ecosystem engineers, and a taphonomic artefact. We perform the first critical test of the 'biotic replacement' hypothesis using combined palaeoecological and geochemical data collected from the youngest Ediacaran strata in southern Namibia. We find that, even after accounting for a variety of potential sampling and taphonomic biases, the Ediacaran assemblage preserved at Farm Swartpunt has significantly lower genus richness than older assemblages. Geochemical and sedimentological analyses confirm an oxygenated and non-restricted palaeoenvironment for fossil-bearing sediments, thus suggesting that oxygen stress and/or hypersalinity are unlikely to be responsible for the low diversity of communities preserved at Swartpunt. These combined analyses suggest depauperate communities characterized the latest Ediacaran and provide the first quantitative support for the biotic replacement model for the end of the Ediacara biota. Although more sites (especially those recording different palaeoenvironments) are undoubtedly needed, this study provides the first quantitative palaeoecological evidence to suggest that evolutionary innovation, ecosystem engineering and biological interactions may have ultimately caused the first mass extinction of complex life.

The evolution of hierarchical gene regulatory networks.

Comparative developmental evidence indicates that reorganizations in developmental gene regulatory networks (GRNs) underlie evolutionary changes in animal morphology, including body plans. We argue here that the nature of the evolutionary alterations that arise from regulatory changes depends on the hierarchical position of the change within a GRN. This concept cannot be accomodated by microevolutionary nor macroevolutionary theory. It will soon be possible to investigate these ideas experimentally, by assessing the effects of GRN changes on morphological evolution.

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.

Highlights from the Science family of journals.

Evolutionary uniformitarianism.

I present a new compilation of the distribution of the temporal distribution of new morphologies of marine invertebrates associated with the Ediacaran-Cambrian (578-510 Ma) diversification of Metazoa. Combining this data with previous work on the hierarchical structure of gene regulatory networks, I argue that the distribution of morphologies may be, in part, a record of the time-asymmetric generation of variation. Evolution has been implicitly viewed as a uniformitarian process where the rates may vary but the underlying processes, including the types of variation, are essentially invariant through time. Recent studies demonstrate that this uniformitarian assumption is false, suggesting that the types of variation may vary through time.

Novelties that change carrying capacity.

Comparative developmental studies have revealed a rich array of details about the patterns and processes of morphological change in animals and increasingly in plants. But, applying these insights to the study of major episodes of evolutionary innovation requires understanding how these novel morphologies become established and sufficiently abundant (either as individuals within a species or as a clade of species) to be preserved in the fossil record, and, in many cases, to influence ecological processes. Evolutionary novelties may: (1) disappear without changing the species; (2) be associated with the generation (through selection or drift) of a new species; and if the latter (3) may or may not become ecologically significant. Only the latter are commonly preserved in the fossil record. These alternatives mirror the distinction among historians of technology between innovation and invention. Here, I argue that specific sorts of evolutionary inventions drive ecological transformation, essentially constructing an environment for themselves and ancillary organisms through ecological spillover effects, increasing the "carrying capacity" of an ecosystem.

Compilation and network analyses of cambrian food webs.

A rich body of empirically grounded theory has developed about food webs--the networks of feeding relationships among species within habitats. However, detailed food-web data and analyses are lacking for ancient ecosystems, largely because of the low resolution of taxa coupled with uncertain and incomplete information about feeding interactions. These impediments appear insurmountable for most fossil assemblages; however, a few assemblages with excellent soft-body preservation across trophic levels are candidates for food-web data compilation and topological analysis. Here we present plausible, detailed food webs for the Chengjiang and Burgess Shale assemblages from the Cambrian Period. Analyses of degree distributions and other structural network properties, including sensitivity analyses of the effects of uncertainty associated with Cambrian diet designations, suggest that these early Paleozoic communities share remarkably similar topology with modern food webs. Observed regularities reflect a systematic dependence of structure on the numbers of taxa and links in a web. Most aspects of Cambrian food-web structure are well-characterized by a simple "niche model," which was developed for modern food webs and takes into account this scale dependence. However, a few aspects of topology differ between the ancient and recent webs: longer path lengths between species and more species in feeding loops in the earlier Chengjiang web, and higher variability in the number of links per species for both Cambrian webs. Our results are relatively insensitive to the exclusion of low-certainty or random links. The many similarities between Cambrian and recent food webs point toward surprisingly strong and enduring constraints on the organization of complex feeding interactions among metazoan species. The few differences could reflect a transition to more strongly integrated and constrained trophic organization within ecosystems following the rapid diversification of species, body plans, and trophic roles during the Cambrian radiation. More research is needed to explore the generality of food-web structure through deep time and across habitats, especially to investigate potential mechanisms that could give rise to similar structure, as well as any differences.

Colloquium paper: extinction as the loss of evolutionary history.

Current plant and animal diversity preserves at most 1-2% of the species that have existed over the past 600 million years. But understanding the evolutionary impact of these extinctions requires a variety of metrics. The traditional measurement is loss of taxa (species or a higher category) but in the absence of phylogenetic information it is difficult to distinguish the evolutionary depth of different patterns of extinction: the same species loss can encompass very different losses of evolutionary history. Furthermore, both taxic and phylogenetic measures are poor metrics of morphologic disparity. Other measures of lost diversity include: functional diversity, architectural components, behavioral and social repertoires, and developmental strategies. The canonical five mass extinctions of the Phanerozoic reveals the loss of different, albeit sometimes overlapping, aspects of loss of evolutionary history. The end-Permian mass extinction (252 Ma) reduced all measures of diversity. The same was not true of other episodes, differences that may reflect their duration and structure. The construction of biodiversity reflects similarly uneven contributions to each of these metrics. Unraveling these contributions requires greater attention to feedbacks on biodiversity and the temporal variability in their contribution to evolutionary history. Taxic diversity increases after mass extinctions, but the response by other aspects of evolutionary history is less well studied. Earlier views of postextinction biotic recovery as the refilling of empty ecospace fail to capture the dynamics of this diversity increase.