Quantifying the effects of exceptional fossil preservation on the global availability of phylogenetic data in deep time.

Fossil deposits with exceptional preservation ("lagerstätten") provide important details not typically preserved in the fossil record, such that they hold an outsized influence on our understanding of biodiversity and evolution. In particular, the potential bias imparted by this so-called "lagerstätten effect" remains a critical, but underexplored aspect of reconstructing evolutionary relationships. Here, we quantify the amount of phylogenetic information available in the global fossil records of 1,327 species of non-avian theropod dinosaurs, Mesozoic birds, and fossil squamates (e.g., lizards, snakes, mosasaurs), and then compare the influence of lagerstätten deposits on phylogenetic information content and taxon selection in phylogenetic analyses to other fossil-bearing deposits. We find that groups that preserve a high amount of phylogenetic information in their global fossil record (e.g., non-avian theropods) are less vulnerable to a "lagerstätten effect" that leads to disproportionate representation of fossil taxa from one geologic unit in an evolutionary tree. Additionally, for each taxonomic group, we find comparable amounts of phylogenetic information in lagerstätten deposits, even though corresponding morphological character datasets vary greatly. Finally, we unexpectedly find that ancient sand dune deposits of the Late Cretaceous Gobi Desert of Mongolia and China exert an anomalously large influence on the phylogenetic information available in the squamate fossil record, suggesting a "lagerstätten effect" can be present in units not traditionally considered lagerstätten. These results offer a phylogenetics-based lens through which to examine the effects of exceptional fossil preservation on biological patterns through time and space, and invites further quantification of evolutionary information in the rock record.

Contrasting terrestrial and marine ecospace dynamics after the end-Triassic mass extinction event.

Mass extinctions have fundamentally altered the structure of the biosphere throughout Earth's history. The ecological severity of mass extinctions is well studied in marine ecosystems by categorizing marine taxa into functional groups based on 'ecospace' approaches, but the ecological response of terrestrial ecosystems to mass extinctions is less well understood due to the lack of a comparable methodology. Here, we present a new terrestrial ecospace framework that categorizes fauna into functional groups as defined by tiering, motility and feeding traits. We applied the new terrestrial and traditional marine ecospace analyses to data from the Paleobiology Database across the end-Triassic mass extinction-a time of catastrophic global warming-to compare changes between the marine and terrestrial biospheres. We found that terrestrial functional groups experienced higher extinction severity, that taxonomic and functional richness are more tightly coupled in the terrestrial, and that the terrestrial realm continued to experience high ecological dissimilarity in the wake of the extinction. Although signals of extinction severity and ecological turnover are sensitive to the quality of the terrestrial fossil record, our findings suggest greater ecological pressure from the end-Triassic mass extinction on terrestrial ecosystems than marine ecosystems, contributing to more prolonged terrestrial ecological flux.

Colonial coral resilience by decreasing size: reaction to increased detrital influx during onset of the late Palaeozoic Ice Age.

Modern coral reefs and associated biodiversity are severely threatened by increasing terrestrial runoff. Similar scenarios could be suspected for geological times, but reef coral resilience is still an enigma. In late Visean-Serpukhovian (Mississippian foraminiferal zones/MFZ 14-16) times, a major glaciation phase of the late Palaeozoic Ice Age (LPIA) associated with enhanced terrestrial weathering and runoff coincides with a biodiversity crisis and coral reef decline. In this study, the impact of enhanced terrestrial runoff is tested on size variations of colonial corals Aulina rotiformis and Lithostrotion decipiens along a gradient of contemporaneous (Serpukhovian) open marine carbonate to near-shore siliciclastic facies in South China. Along this gradient, their sizes decrease from carbonate, through intermediate carbonate-siliciclastic, to siliciclastic facies. This is consistent with increasing abundance of terrestrial materials of high silicon, aluminium and phosphorus values. On a larger million-year-long interval (MFZ14-16) and for several palaeocontinents, size data of Lithostrotion decipiens and Siphonodendron pauciradiale show a distinct decline in late Visean, when enhanced terrestrial weathering occurred commonly with palaeosols developed during regression. This suggests that terrestrial sediment and nutrient input may have mainly controlled phenotypic plasticity in Mississippian reef corals, with a decrease in size as a component of resilience across the LPIA onset.

Ediacaran-Cambrian bioturbation did not extensively oxygenate sediments in shallow marine ecosystems.

The radiation of bioturbation during the Ediacaran-Cambrian transition has long been hypothesized to have oxygenated sediments, triggering an expansion of the habitable benthic zone and promoting increased infaunal tiering in early Paleozoic benthic communities. However, the effects of bioturbation on sediment oxygen are underexplored with respect to the importance of biomixing and bioirrigation, two bioturbation processes which can have opposite effects on sediment redox chemistry. We categorized trace fossils from the Ediacaran and Terreneuvian as biomixing or bioirrigation fossils and integrated sedimentological proxies for bioturbation intensity with biogeochemical modeling to simulate oxygen penetration depths through the Ediacaran-Cambrian transition. Ultimately, we find that despite dramatic increases in ichnodiversity in the Terreneuvian, biomixing remains the dominant bioturbation behavior, and in contrast to traditional assumptions, Ediacaran-Cambrian bioturbation was unlikely to have resulted in extensive oxygenation of shallow marine sediments globally.

Resilience of infaunal ecosystems during the Early Triassic greenhouse Earth.

The Permian-Triassic mass extinction severely depleted biodiversity, primarily observed in the body fossil of well-skeletonized animals. Understanding how whole ecosystems were affected and rebuilt following the crisis requires evidence from both skeletonized and soft-bodied animals; the best comprehensive information on soft-bodied animals comes from ichnofossils. We analyzed abundant trace fossils from 26 sections across the Permian-Triassic boundary in China and report key metrics of ichnodiversity, ichnodisparity, ecospace utilization, and ecosystem engineering. We find that infaunal ecologic structure was well established in the early Smithian. Decoupling of diversity between deposit feeders and suspension feeders in carbonate ramp-platform settings implies that an effect of trophic group amensalism could have delayed the recovery of nonmotile, suspension-feeding epifauna in the Early Triassic. This differential reaction of infaunal ecosystems to variable environmental controls thus played a substantial but heretofore little appreciated evolutionary and ecologic role in the overall recovery in the hot Early Triassic ocean.

Diverse and complex developmental mechanisms of early Ediacaran embryo-like fossils from the Weng'an Biota, southwest China.

The origin and early evolution of animal development remain among the many deep, unresolved problems in evolutionary biology. As a compelling case for the existence of pre-Cambrian animals, the Ediacaran embryo-like fossils (EELFs) from the Weng'an Biota (approx. 609 Myr old, Doushantuo Formation, South China) have great potential to cast light on the origin and early evolution of animal development. However, their biological implications can be fully realized only when their phylogenetic positions are correctly established, and unfortunately, this is the key problem under debate. As a significant feature of developmental biology, the cell division pattern (CDP) characterized by the dynamic spatial arrangement of cells and associated developmental mechanisms is critical to reassess these hypotheses and evaluate the diversity of the EELFs; however, their phylogenetic implications have not been fully realized. Additionally, the scarcity of fossil specimens representing late developmental stages with cell differentiation accounts for much of this debate too. Here, we reconstructed a large number of EELFs using submicron resolution X-ray tomographic microscopy and focused on the CDPs and associated developmental mechanisms as well as features of cell differentiation. Four types of CDPs and specimens with cell differentiation were identified. Contrary to the prevailing view, our results together with recent studies suggest that the diversity and complexity of developmental mechanisms documented by the EELFs are much higher than is often claimed. The diverse CDPs and associated development features including palintomic cleavage, maternal nutrition, asymmetric cell divisions, symmetry breaking, establishment of polarity or axis, spatial cell migration and differentiation constrain some, if not all, EELFs as total-group metazoans. This article is part of the theme issue 'The impact of Chinese palaeontology on evolutionary research'.

Intensified continental chemical weathering and carbon-cycle perturbations linked to volcanism during the Triassic-Jurassic transition.

Direct evidence of intense chemical weathering induced by volcanism is rare in sedimentary successions. Here, we undertake a multiproxy analysis (including organic carbon isotopes, mercury (Hg) concentrations and isotopes, chemical index of alteration (CIA), and clay minerals) of two well-dated Triassic-Jurassic (T-J) boundary sections representing high- and low/middle-paleolatitude sites. Both sections show increasing CIA in association with Hg peaks near the T-J boundary. We interpret these results as reflecting volcanism-induced intensification of continental chemical weathering, which is also supported by negative mass-independent fractionation (MIF) of odd Hg isotopes. The interval of enhanced chemical weathering persisted for ~2 million years, which is consistent with carbon-cycle model results of the time needed to drawdown excess atmospheric CO2 following a carbon release event. Lastly, these data also demonstrate that high-latitude continental settings are more sensitive than low/middle-latitude sites to shifts in weathering intensity during climatic warming events.

Dental replacement in Mesozoic birds: evidence from newly discovered Brazilian enantiornithines.

Polyphyodonty-multiple tooth generations-in Mesozoic birds has been confirmed since the nineteenth century. Their dental cycle had been assessed through sparse data from tooth roots revealed through broken jawbones and disattached teeth. However, detailed descriptions of their tooth cycling are lacking, and the specifics of their replacement patterns remain largely unknown. Here we present unprecedented µCT data from three enantiornithine specimens from the Upper Cretaceous of southeastern Brazil. The high resolution µCT data show an alternating dental replacement pattern in the premaxillae, consistent with the widespread pattern amongst extinct and extant reptiles. The dentary also reveals dental replacement at different stages. These results strongly suggest that an alternating pattern was typical of enantiornithine birds. µCT data show that new teeth start lingually within the alveoli, resorb roots of functional teeth and migrate labially into their pulp cavities at an early stage, similar to modern crocodilians. Our results imply that the control mechanism for tooth cycling is conserved during the transition between non-avian reptiles and birds. These first 3D reconstructions of enantiornithine dental replacement demonstrate that 3D data are essential to understand the evolution and deep homology of archosaurian tooth cycling.

Complex marine bioturbation ecosystem engineering behaviors persisted in the wake of the end-Permian mass extinction.

The end-Permian mass extinction was the most severe mass extinction event of the Phanerozoic and was followed by a several million-year delay in benthic ecosystem recovery. While much work has been done to understand biotic recovery in both the body and trace fossil records of the Early Triassic, almost no focus has previously been given to analyzing patterns in ecosystem engineering complexity as a result of the extinction drivers. Bioturbation is a key ecosystem engineering behavior in marine environments, as it results in changes to resource flows and the physical environment. Thus, the trace fossil record can be used to examine the effect of the end-Permian mass extinction on bioturbating ecosystem engineers. We present a dataset compiled from previously published literature to analyze burrowing ecosystem engineering behaviors through the Permian-Triassic boundary. We report two key observations: first, that there is no loss in bioturbation ecosystem engineering behaviors after the mass extinction, and second, that these persisting behaviors include deep tier, high-impact, complex ecosystem engineering. These findings suggest that while environmental conditions may have limited deeper burrowing, complex ecosystem engineering behaviors were able to persist in the Early Triassic. Furthermore, the persistence of deep tier bioirrigated three-dimensional network burrows implies that benthic biogeochemical cycling could have been maintained at pre-extinction states in some local environments, stimulating ecosystem productivity and promoting biotic recovery in the Early Triassic.

Mid-Cretaceous amber inclusions reveal morphogenesis of extinct rachis-dominated feathers.

We describe three-dimensionally preserved feathers in mid-Cretaceous Burmese amber that share macro-morphological similarities (e.g., proportionally wide rachis with a "medial stripe") with lithic, two-dimensionally preserved rachis-dominated feathers, first recognized in the Jehol Biota. These feathers in amber reveal a unique ventrally concave and dorsoventrally thin rachis, and a dorsal groove (sometimes pigmented) that we identify as the "medial stripe" visible in many rachis-dominated rectrices of Mesozoic birds. The distally pennaceous portion of these feathers shows differentiated proximal and distal barbules, the latter with hooklets forming interlocking barbs. Micro-CT scans and transverse sections demonstrate the absence of histodifferentiated cortex and medullary pith of the rachis and barb rami. The highly differentiated barbules combined with the lack of obvious histodifferentiation of the barb rami or rachis suggests that these feathers could have been formed without the full suite and developmental interplay of intermediate filament alpha keratins and corneous beta-proteins that is employed in the cornification process of modern feathers. This study thus highlights how the development of these feathers might have differed from that of their modern counterparts, namely in the morphogenesis of the ventral components of the rachis and barb rami. We suggest that the concave ventral surface of the rachis of these Cretaceous feathers is not homologous with the ventral groove of modern rachises. Our study of these Burmese feathers also confirms previous claims, based on two-dimensional fossils, that they correspond to an extinct morphotype and it cautions about the common practice of extrapolating developmental aspects (and mechanical attributes) of modern feathers to those of stem birds (and their dinosaurian outgroups) because the latter need not to have developed through identical pathways.

Uppermost Triassic phosphorites from Williston Lake, Canada: link to fluctuating euxinic-anoxic conditions in northeastern Panthalassa before the end-Triassic mass extinction.

The end-Triassic mass extinction (ETE) is associated with a rise in CO2 due to eruptions of the Central Atlantic Magmatic Province (CAMP), and had a particularly dramatic effect on the Modern Fauna, so an understanding of the conditions that led to the ETE has relevance to current rising CO2 levels. Here, we report multiple phosphorite deposits in strata that immediately precede the ETE at Williston Lake, Canada, which allow the paleoenvironmental conditions leading up to the mass extinction to be investigated. The predominance of phosphatic coated grains within phoshorites indicates reworking in shallow water environments. Raman spectroscopy reveals that the phosphorites contain organic carbon, and petrographic and scanning electron microscopic analyses reveal that the phosphorites contain putative microfossils, potentially suggesting microbial involvement in a direct or indirect way. Thus, we favor a mechanism of phosphogenesis that involves microbial polyphosphate metabolism in which phosphatic deposits typically form at the interface of euxinic/anoxic and oxic conditions. When combined with data from deeper water deposits (Kennecott Point) far to the southwest, it would appear a very broad area of northeastern Panthalassa experienced anoxic to euxinic bottom water conditions in the direct lead up to the end-Triassic mass extinction. Such a scenario implies expansion and shallowing of the oxygen minimum zone across a very broad area of northeastern Panthalassa, which potentially created a stressful environment for benthic metazoan communities. Studies of the pre-extinction interval from different sites across the globe are required to resolve the chronology and spatial distribution of processes that governed before the major environmental collapse that caused the ETE. Results from this study demonstrate that fluctuating anoxic and euxinic conditions could have been potentially responsible for reduced ecosystem stability before the onset of CAMP volcanism, at least at the regional scale.

Echinoids from the Tesero Member (Werfen Formation) of the Dolomites (Italy): implications for extinction and survival of echinoids in the aftermath of the end-Permian mass extinction.

The end-Permian mass extinction (∼252 Ma) was responsible for high rates of extinction and evolutionary bottlenecks in a number of animal groups. Echinoids, or sea urchins, were no exception, and the Permian to Triassic represents one of the most significant intervals of time in their macroevolutionary history. The extinction event was responsible for significant turnover, with the Permian-Triassic representing the transition from stem group echinoid-dominated faunas in the Palaeozoic to Mesozoic faunas dominated by crown group echinoids. This turnover is well-known, however, the environmental and taxonomic distribution of echinoids during the latest Permian and Early Triassic is not. Here we report on an echinoid fauna from the Tesero Member, Werfen Formation (latest Permian to Early Triassic) of the Dolomites (northern Italy). The fauna is largely known from disarticulated ossicles, but consists of both stem group taxa, and a new species of crown group echinoid, Eotiaris teseroensis n. sp. That these stem group echinoids were present in the Tesero Member indicates that stem group echinoids did not go extinct in the Dolomites coincident with the onset of extinction, further supporting other recent work indicating that stem group echinoids survived the end-Permian extinction. Furthermore, the presence of Eotiaris across a number of differing palaeoenvironments in the Early Triassic may have had implications for the survival of cidaroid echinoids during the extinction event.

A new stem group echinoid from the Triassic of China leads to a revised macroevolutionary history of echinoids during the end-Permian mass extinction.

The Permian-Triassic bottleneck has long been thought to have drastically altered the course of echinoid evolution, with the extinction of the entire echinoid stem group having taken place during the end-Permian mass extinction. The Early Triassic fossil record of echinoids is, however, sparse, and new fossils are paving the way for a revised interpretation of the evolutionary history of echinoids during the Permian-Triassic crisis and Early Mesozoic. A new species of echinoid, Yunnanechinus luopingensis n. sp. recovered from the Middle Triassic (Anisian) Luoping Biota fossil Lagerstätte of South China, displays morphologies that are not characteristic of the echinoid crown group. We have used phylogenetic analyses to further demonstrate that Yunnanechinus is not a member of the echinoid crown group. Thus a clade of stem group echinoids survived into the Middle Triassic, enduring the global crisis that characterized the end-Permian and Early Triassic. Therefore, stem group echinoids did not go extinct during the Palaeozoic, as previously thought, and appear to have coexisted with the echinoid crown group for at least 23 million years. Stem group echinoids thus exhibited the Lazarus effect during the latest Permian and Early Triassic, while crown group echinoids did not.

Paleogenomics of echinoids reveals an ancient origin for the double-negative specification of micromeres in sea urchins.

Establishing a timeline for the evolution of novelties is a common, unifying goal at the intersection of evolutionary and developmental biology. Analyses of gene regulatory networks (GRNs) provide the ability to understand the underlying genetic and developmental mechanisms responsible for the origin of morphological structures both in the development of an individual and across entire evolutionary lineages. Accurately dating GRN novelties, thereby establishing a timeline for GRN evolution, is necessary to answer questions about the rate at which GRNs and their subcircuits evolve, and to tie their evolution to paleoenvironmental and paleoecological changes. Paleogenomics unites the fossil record and all aspects of deep time, with modern genomics and developmental biology to understand the evolution of genomes in evolutionary time. Recent work on the regulatory genomic basis of development in cidaroid echinoids, sand dollars, heart urchins, and other nonmodel echinoderms provides an ideal dataset with which to explore GRN evolution in a comparative framework. Using divergence time estimation and ancestral state reconstructions, we have determined the age of the double-negative gate (DNG), the subcircuit which specifies micromeres and skeletogenic cells in Strongylocentrotus purpuratus We have determined that the DNG has likely been used for euechinoid echinoid micromere specification since at least the Late Triassic. The innovation of the DNG thus predates the burst of post-Paleozoic echinoid morphological diversification that began in the Early Jurassic. Paleogenomics has wide applicability for the integration of deep time and molecular developmental data, and has wide utility in rigorously establishing timelines for GRN evolution.

Mercury anomalies and the timing of biotic recovery following the end-Triassic mass extinction.

The end-Triassic mass extinction overlapped with the eruption of the Central Atlantic Magmatic Province (CAMP), and release of CO2 and other volcanic volatiles has been implicated in the extinction. However, the timing of marine biotic recovery versus CAMP eruptions remains uncertain. Here we use Hg concentrations and isotopes as indicators of CAMP volcanism in continental shelf sediments, the primary archive of faunal data. In Triassic-Jurassic strata, Muller Canyon, Nevada, Hg levels rise in the extinction interval, peak before the appearance of the first Jurassic ammonite, remain above background in association with a depauperate fauna, and fall to pre-extinction levels during significant pelagic and benthic faunal recovery. Hg isotopes display no significant mass independent fractionation within the extinction and depauperate intervals, consistent with a volcanic origin for the Hg. The Hg and palaeontological evidence from the same archive indicate that significant biotic recovery did not begin until CAMP eruptions ceased.

A microbial carbonate response in synchrony with the end-Triassic mass extinction across the SW UK.

The eruption of the Central Atlantic Magmatic Province (CAMP)-the largest igneous province known-has been linked to the end-Triassic mass extinction event, however reconciling the response of the biosphere (at local and nonlocal scales) to potential CAMP-induced geochemical excursions has remained challenging. Here we present a combined sedimentary and biological response to an ecosystem collapse in Triassic-Jurassic strata of the southwest United Kingdom (SW UK) expressed as widely distributed carbonate microbialites and associated biogeochemical facies. The microbialites (1) occur at the same stratigraphic level as the mass extinction extinction, (2) host a negative isotope excursion in δ(13)Corg found in other successions around the world, and (3) co-occur with an acme of prasinophyte algae 'disaster taxa' also dominant in Triassic-Jurassic boundary strata of other European sections. Although the duration of microbialite deposition is uncertain, it is likely that they formed rapidly (perhaps fewer than ten thousand years), thus providing a high-resolution glimpse into the initial carbon isotopic perturbation coincident with the end-Triassic mass extinction. These findings indicate microbialites from the SW UK capture a nonlocal biosedimentary response to the cascading effects of massive volcanism and add to the current understanding of paleoecology in the aftermath of the end-Triassic extinction.

Reorganization of sea urchin gene regulatory networks at least 268 million years ago as revealed by oldest fossil cidaroid echinoid.

Echinoids, or sea urchins, are rare in the Palaeozoic fossil record, and thus the details regarding the early diversification of crown group echinoids are unclear. Here we report on the earliest probable crown group echinoid from the fossil record, recovered from Permian (Roadian-Capitanian) rocks of west Texas, which has important implications for the timing of the divergence of crown group echinoids. The presence of apophyses and rigidly sutured interambulacral areas with two columns of plates indicates this species is a cidaroid echinoid. The species, Eotiaris guadalupensis, n. sp. is therefore the earliest stem group cidaroid. The occurrence of this species in Roadian strata pushes back the divergence of cidaroids and euechinoids, the clades that comprise all living echinoids, to at least 268.8 Ma, ten million years older than the previously oldest known cidaroid. Furthermore, the genomic regulation of development in echinoids is amongst the best known, and this new species informs the timing of large-scale reorganization in echinoid gene regulatory networks that occurred at the cidaroid-euechinoid divergence, indicating that these changes took place by the Roadian stage of the Permian.

Early Triassic wrinkle structures on land: stressed environments and oases for life.

Wrinkle structures in rocks younger than the Permian-Triassic (P-Tr) extinction have been reported repeatedly in marine strata, but rarely mentioned in rocks recording land. Here, three newly studied terrestrial P-Tr boundary rock succession in North China have yielded diverse wrinkle structures. All of these wrinkles are preserved in barely bioturbated shore-shallow lacustrine siliciclastic deposits of the Liujiagou Formation. Conversely, both the lacustrine siliciclastic deposits of the underlying Sunjiagou Formation and the overlying Heshanggou Formation show rich bioturbation, but no wrinkle structures or other microbial-related structures. The occurrence of terrestrial wrinkle structures in the studied sections reflects abnormal hydrochemical and physical environments, presumably associated with the extinction of terrestrial organisms. Only very rare trace fossils occurred in the aftermath of the P-Tr extinction, but most of them were preserved together with the microbial mats. This suggests that microbial mats acted as potential oases for the surviving aquatic animals, as a source of food and oxygen. The new finds suggests that extreme environmental stresses were prevalent both in the sea and on land through most of the Early Triassic.