A Silurian pseudocolonial pterobranch.

Pterobranchs, a major group of the phylum Hemichordata, first appear in the fossil record during the Cambrian,1 and there are more than 600 fossil genera dominated by the mainly planktic graptolites of the Paleozoic, which are widely used as zone fossils for correlating sedimentary rock sequences.2 Pterobranchs are rare today; they are sessile marine forms represented by Rhabdopleura, which is considered the only living graptolite, and Cephalodiscus. Unlike their sister taxon, the colonial graptolites, cephalodiscids are pseudocolonial.3,4 Here, we describe a problematic fossil from the Silurian (Pridoli) Bertie Group of Ontario (420 mya), a sequence of near-shore sediments well known for its remarkably preserved diversity of eurypterids (sea scorpions).5 The fossil, Rotaciurca superbus, a new genus and species, was familiarly known as Ezekiel's Wheel,5 with reference to the unusual circular arrangement of the tubes that compose it. The structure and arrangement of the tubes identify Rotaciurca as a pterobranch, and phylogenetic analysis groups it with the cephalodiscids. We place it in a new family Rotaciurcidae to distinguish it from Cephalodiscidae. A large structure associated with the tubes is interpreted as a float, which would distinguish Rotaciurca as the only known planktic cephalodiscid-thus cephalodiscids, like the graptolites, invaded the water column. This mode of life reflects the rarity of pseudocolonial macroinvertebrates in planktic ocean communities, a role occupied by the tunicates (Chordata) known as salps today. Our estimates of divergence times, the first using relaxed total-evidence clocks, date the origins of both hemichordates and pterobranchs to the earliest Cambrian (Fortunian).

A vicissicaudatan arthropod from the Silurian Herefordshire Lagerstätte, UK.

A new arthropod, Carimersa neptuni gen. et sp. nov., is described from the Silurian (Wenlock Series) Herefordshire Konservat-Lagerstätte, UK. The head bears pedunculate eyes and five pairs of appendages. Triflagellate antennae are followed by two pairs of uniramous limbs each with an endopod bearing a pronounced gnathobasic basipod. The posterior two pairs of head limbs and all trunk limbs bear an endopod, exopod and filamentous exite. The trunk consists of 10 appendage-bearing segments followed by an apodous abdomen of four segments. The arthropod resolves as sister taxon to Kodymirus and Eozetetes + Aglaspidida. It is the first representative of Vicissicaudata reported from the Herefordshire Lagerstätte and the first Silurian example with well-preserved appendages. The preservation of a cluster of radiolarians apparently captured by the trunk appendages is the first direct association of predator and prey discovered in the Herefordshire fauna, and suggests that Carimersa was a nektobenthic form that used its gnathobasic basipods in microdurophagy.

Fossilisation processes and our reading of animal antiquity.

Estimates for animal antiquity exhibit a significant disconnect between those from molecular clocks, which indicate crown animals evolved ∼800 million years ago (Ma), and those from the fossil record, which extends only ∼574 Ma. Taphonomy is often held culpable: early animals were too small/soft/fragile to fossilise, or the circumstances that preserve them were uncommon in the early Neoproterozoic. We assess this idea by comparing Neoproterozoic fossilisation processes with those of the Cambrian and its abundant animal fossils. Cambrian Burgess Shale-type (BST) preservation captures animals in mudstones showing a narrow range of mineralogies; yet, fossiliferous Neoproterozoic mudstones rarely share the same mineralogy. Animal fossils are absent where BST preservation occurs in deposits ≥789 Ma, suggesting a soft maximum constraint on animal antiquity.

Putting heads together.

Cambrian fossils reveal ancestry of the segmented brain in arthropods.

Fossil biomolecules reveal an avian metabolism in the ancestral dinosaur.

Birds and mammals independently evolved the highest metabolic rates among living animals1. Their metabolism generates heat that enables active thermoregulation1, shaping the ecological niches they can occupy and their adaptability to environmental change2. The metabolic performance of birds, which exceeds that of mammals, is thought to have evolved along their stem lineage3-10. However, there is no proxy that enables the direct reconstruction of metabolic rates from fossils. Here we use in situ Raman and Fourier-transform infrared spectroscopy to quantify the in vivo accumulation of metabolic lipoxidation signals in modern and fossil amniote bones. We observe no correlation between atmospheric oxygen concentrations11 and metabolic rates. Inferred ancestral states reveal that the metabolic rates consistent with endothermy evolved independently in mammals and plesiosaurs, and are ancestral to ornithodirans, with increasing rates along the avian lineage. High metabolic rates were acquired in pterosaurs, ornithischians, sauropods and theropods well before the advent of energetically costly adaptations, such as flight in birds. Although they had higher metabolic rates ancestrally, ornithischians reduced their metabolic abilities towards ectothermy. The physiological activities of such ectotherms were dependent on environmental and behavioural thermoregulation12, in contrast to the active lifestyles of endotherms1. Giant sauropods and theropods were not gigantothermic9,10, but true endotherms. Endothermy in many Late Cretaceous taxa, in addition to crown mammals and birds, suggests that attributes other than metabolism determined their fate during the terminal Cretaceous mass extinction.

The remarkable visual system of a Cretaceous crab.

True crabs (Brachyura) are one of the few groups of arthropods to evolve several types of compound eye, the origins and early evolution of which are obscure. Here, we describe details of the eyes of the Cretaceous brachyuran Callichimaera perplexa, which possessed remarkably large eyes and a highly disparate body form among brachyurans. The eyes of C. perplexa preserve internal optic neuropils and external corneal elements, and it is the first known post-Paleozoic arthropod to preserve both. Additionally, a series of specimens of C. perplexa preserve both the eyes and carapace, allowing for the calculation of the optical growth rate. C. perplexa shows the fastest optical growth rate compared with a sample of 14 species of extant brachyurans. The growth series of C. perplexa, in combination with the calculation of the interommatidial angle and eye parameter, demonstrates that it was a highly visual predator that inhabited well-lit environments.

Raman spectroscopy is a powerful tool in molecular paleobiology: An analytical response to Alleon et al. (https://doi.org/10.1002/bies.202000295).

A recent article argued that signals from conventional Raman spectroscopy of organic materials are overwhelmed by edge filter and fluorescence artefacts. The article targeted a subset of Raman spectroscopic investigations of fossil and modern organisms and has implications for the utility of conventional Raman spectroscopy in comparative tissue analytics. The inferences were based on circular reasoning centered around the unconventional analysis of spectra from just two samples, one modern, and one fossil. We validated the disputed signals with in situ Fourier-Transform Infrared (FT-IR) Spectroscopy and through replication with different lasers, filters, and operators in independent laboratories. Our Raman system employs a holographic notch filter which is not affected by edge filter or other artefacts. Multiple lines of evidence confirm that conventional Raman spectra of fossils contain biologically and geologically meaningful information. Statistical analyses of large Raman and FT-IR spectral data sets reveal patterns in fossil composition and yield valuable insights into the history of life.

Crab in amber reveals an early colonization of nonmarine environments during the Cretaceous.

Amber fossils provide snapshots of the anatomy, biology, and ecology of extinct organisms that are otherwise inaccessible. The best-known fossils in amber are terrestrial arthropods­principally insects­whereas aquatic organisms are rarely represented. Here, we present the first record of true crabs (Brachyura) in amber­from the Cretaceous of Myanmar [~100 to 99 million years (Ma)]. The new fossil preserves large compound eyes, delicate mouthparts, and even gills. This modern-looking crab is nested within crown Eubrachyura, or "higher" true crabs, which includes the majority of brachyuran species living today. The fossil appears to have been trapped in a brackish or freshwater setting near a coastal to fluvio-estuarine environment, bridging the gap between the predicted molecular divergence of nonmarine crabs (~130 Ma) and their younger fossil record (latest Cretaceous and Paleogene, ~75 to 50 Ma) while providing a reliable calibration point for molecular divergence time estimates for higher crown eubrachyurans.

Paleozoic ammonoid ecomorphometrics test ecospace availability as a driver of morphological diversification.

The early burst model suggests that disparity rises rapidly to fill empty ecospace following clade origination or in the aftermath of a mass extinction. Early bursts are considered common features of fossil data, but neontological studies have struggled to identify them. Furthermore, tests have proven difficult because factors besides ecology can drive changes in morphology. Here, we document the ecomorphometric evolution of the extinct Ammonoidea at 1-million-year resolution, from their origination in the Early Devonian (Emsian) to the Early Triassic (Induan), over ~156 million years. This time interval encompasses six global extinction events, including two of the Big Five, and incorporates multiple ammonoid radiations. However, we find no evidence for early bursts of ecomorphological disparity. This contradicts arguments that the temporal scope, or traits measured in genomic data, conceal evidence of early bursts. Rather, early bursts may be less prevalent in fossil data than is often assumed.

Arm waving in stylophoran echinoderms: three-dimensional mobility analysis illuminates cornute locomotion.

The locomotion strategies of fossil invertebrates are typically interpreted on the basis of morphological descriptions. However, it has been shown that homologous structures with disparate morphologies in extant invertebrates do not necessarily correlate with differences in their locomotory capability. Here, we present a new methodology for analysing locomotion in fossil invertebrates with a rigid skeleton through an investigation of a cornute stylophoran, an extinct fossil echinoderm with enigmatic morphology that has made its mode of locomotion difficult to reconstruct. We determined the range of motion of a stylophoran arm based on digitized three-dimensional morphology of an early Ordovician form, Phyllocystis crassimarginata. Our analysis showed that efficient arm-forward epifaunal locomotion based on dorsoventral movements, as previously hypothesized for cornute stylophorans, was not possible for this taxon; locomotion driven primarily by lateral movement of the proximal aulacophore was more likely. Three-dimensional digital modelling provides an objective and rigorous methodology for illuminating the movement capabilities and locomotion strategies of fossil invertebrates.

Phylogenetic and physiological signals in metazoan fossil biomolecules.

Proteins, lipids, and sugars establish animal form and function. However, the preservation of biological signals in fossil organic matter is poorly understood. Here, we used high-resolution in situ Raman microspectroscopy to analyze the molecular compositions of 113 Phanerozoic metazoan fossils and sediments. Proteins, lipids, and sugars converge in composition during fossilization through lipoxidation and glycoxidation to form endogenous N-, O-, and S-heterocyclic polymers. Nonetheless, multivariate spectral analysis reveals molecular heterogeneities: The relative abundance of glycoxidation and lipoxidation products distinguishes different tissue types. Preserved chelating ligands are diagnostic of different modes of biomineralization. Amino acid-specific fossilization products retain phylogenetic information and capture higher-rank metazoan relationships. Molecular signals survive in deep time and provide a powerful tool for reconstructing the evolutionary history of animals.

Aluminosilicate haloes preserve complex life approximately 800 million years ago.

Mudstone-hosted microfossils are a major component of the Proterozoic fossil record, particularly dominating the record of early eukaryotic life. Early organisms possessed no biomineralized parts to resist decay and controls on their fossilization in mudstones are poorly understood. Consequently, the Proterozoic fossil record is compromised-we do not know whether changing temporal/spatial patterns of microfossil occurrences reflect evolution or the distribution of favourable fossilization conditions. We investigated fossilization within the approximately 1000 Ma Lakhanda Group (Russia) and the approximately 800 Ma Svanbergfjellet and Wynniatt formations (Svalbard and Arctic Canada). Vertical sections of microfossils and surrounding matrices were extracted from thin sections by focused ion beam milling. Elemental mapping and synchrotron-based infrared microspectroscopy revealed that microfossils are surrounded by haloes rich in aluminium, probably hosted in kaolinite. Kaolinite has been implicated in Cambrian Burgess Shale-type (BST) fossilization and is known to slow the growth of degraders. The Neoproterozoic mudstone microfossil record may be biased to tropical settings conducive to kaolinite formation. These deposits lack metazoan fossils even though they share fossilization conditions with younger BST deposits that are capable of preserving non-mineralizing metazoans. Thus metazoans, at least those typically preserved in BST deposits, were probably absent from sedimentary environments before approximately 800 Ma.

Chemical signatures of soft tissues distinguish between vertebrates and invertebrates from the Carboniferous Mazon Creek Lagerstätte of Illinois.

The chemical composition of fossil soft tissues is a potentially powerful and yet underutilized tool for elucidating the affinity of problematic fossil organisms. In some cases, it has proven difficult to assign a problematic fossil even to the invertebrates or vertebrates (more generally chordates) based on often incompletely preserved morphology alone, and chemical composition may help to resolve such questions. Here, we use in situ Raman microspectroscopy to investigate the chemistry of a diverse array of invertebrate and vertebrate fossils from the Pennsylvanian Mazon Creek Lagerstätte of Illinois, and we generate a ChemoSpace through principal component analysis (PCA) of the in situ Raman spectra. Invertebrate soft tissues characterized by chitin (polysaccharide) fossilization products and vertebrate soft tissues characterized by protein fossilization products plot in completely separate, non-overlapping regions of the ChemoSpace, demonstrating the utility of certain soft tissue molecular signatures as biomarkers for the original soft tissue composition of fossil organisms. The controversial problematicum Tullimonstrum, known as the Tully Monster, groups with the vertebrates, providing strong evidence of a vertebrate rather than invertebrate affinity.

Three-dimensionally preserved soft tissues and calcareous hexactins in a Silurian sponge: implications for early sponge evolution.

Sponges (Porifera), as one of the earliest-branching animal phyla, are crucial for understanding early metazoan phylogeny. Recent studies of Lower Palaeozoic sponges have revealed a variety of character states and combinations unknown in extant taxa, challenging our views of early sponge morphology. The Herefordshire Konservat-Lagerstätte yields an abundant, diverse sponge fauna with three-dimensional preservation of spicules and soft tissue. Carduispongia pedicula gen. et sp. nov. possesses a single layer of hexactine spicules arranged in a regular orthogonal network. This spicule type and arrangement is characteristic of the reticulosans, which have traditionally been interpreted as early members of the extant siliceous Class Hexactinellida. However, the unusual preservation of the spicules of C. pedicula reveals an originally calcareous composition, which would be diagnostic of the living Class Calcarea. The soft tissue architecture closely resembles the complex sylleibid or leuconid structure seen in some modern calcareans and homoscleromorphs. This combination of features strongly supports a skeletal continuum between primitive calcareans and hexactinellid siliceans, indicating that the last common ancestor of Porifera was a spiculate, solitary, vasiform animal with a thin skeletal wall.

A new ophiocistioid with soft-tissue preservation from the Silurian Herefordshire Lagerstätte, and the evolution of the holothurian body plan.

Reconstructing the evolutionary assembly of animal body plans is challenging when there are large morphological gaps between extant sister taxa, as in the case of echinozoans (echinoids and holothurians). However, the inclusion of extinct taxa can help bridge these gaps. Here we describe a new species of echinozoan, Sollasina cthulhu, from the Silurian Herefordshire Lagerstätte, UK. Sollasina cthulhu belongs to the ophiocistioids, an extinct group that shares characters with both echinoids and holothurians. Using physical-optical tomography and computer reconstruction, we visualize the internal anatomy of S. cthulhu in three dimensions, revealing inner soft tissues that we interpret as the ring canal, a key part of the water vascular system that was previously unknown in fossil echinozoans. Phylogenetic analyses strongly suggest that Sollasina and other ophiocistioids represent a paraphyletic group of stem holothurians, as previously hypothesized. This allows us to reconstruct the stepwise reduction of the skeleton during the assembly of the holothurian body plan, which may have been controlled by changes in the expression of biomineralization genes.

The function of the ophiuroid nerve ring: how a decentralized nervous system controls coordinated locomotion.

Echinoderms lack a centralized nervous control system, yet each extant echinoderm class has evolved unique and effective strategies for locomotion. Brittle stars (Ophiuroidea) stride swiftly over the seafloor by coordinating motions of their five muscular arms. Their arms consist of many repeating segments, requiring them to use a complex control system to coordinate motions among segments and between arms. We conducted in vivo experiments with brittle stars to analyze the functional role of the nerve ring, which connects the nerves in each arm. These experiments were designed to determine how the ophiuroid nervous system performs complex decision making and locomotory actions under decentralized control. Our results show that brittle star arms must be connected by the nerve ring for coordinated locomotion, but information can travel bidirectionally around the nerve ring so that it circumvents the severance. Evidence presented indicates that ophiuroids rely on adjacent nerve ring connections for sustained periodic movements. The number of arms connected via the nerve ring is correlated positively with the likelihood that the animal will show coordinated locomotion, indicating that integrated nerve ring tissue is critical for control. The results of the experiments should provide a basis for the advancement of complex artificial decentralized systems.

A phylogenomic resolution of the sea urchin tree of life.

BACKGROUND: Echinoidea is a clade of marine animals including sea urchins, heart urchins, sand dollars and sea biscuits. Found in benthic habitats across all latitudes, echinoids are key components of marine communities such as coral reefs and kelp forests. A little over 1000 species inhabit the oceans today, a diversity that traces its roots back at least to the Permian. Although much effort has been devoted to elucidating the echinoid tree of life using a variety of morphological data, molecular attempts have relied on only a handful of genes. Both of these approaches have had limited success at resolving the deepest nodes of the tree, and their disagreement over the positions of a number of clades remains unresolved. RESULTS: We performed de novo sequencing and assembly of 17 transcriptomes to complement available genomic resources of sea urchins and produce the first phylogenomic analysis of the clade. Multiple methods of probabilistic inference recovered identical topologies, with virtually all nodes showing maximum support. In contrast, the coalescent-based method ASTRAL-II resolved one node differently, a result apparently driven by gene tree error induced by evolutionary rate heterogeneity. Regardless of the method employed, our phylogenetic structure deviates from the currently accepted classification of echinoids, with neither Acroechinoidea (all euechinoids except echinothurioids), nor Clypeasteroida (sand dollars and sea biscuits) being monophyletic as currently defined. We show that phylogenetic signal for novel resolutions of these lineages is strong and distributed throughout the genome, and fail to recover systematic biases as drivers of our results. CONCLUSIONS: Our investigation substantially augments the molecular resources available for sea urchins, providing the first transcriptomes for many of its main lineages. Using this expanded genomic dataset, we resolve the position of several clades in agreement with early molecular analyses but in disagreement with morphological data. Our efforts settle multiple phylogenetic uncertainties, including the position of the enigmatic deep-sea echinothurioids and the identity of the sister clade to sand dollars. We offer a detailed assessment of evolutionary scenarios that could reconcile our findings with morphological evidence, opening up new lines of research into the development and evolutionary history of this ancient clade.