Reconstructing the feeding ecology of Cambrian sponge reefs: the case for active suspension feeding in Archaeocyatha.

Sponge-grade Archaeocyatha were early Cambrian biomineralizing metazoans that constructed reefs globally. Despite decades of research, many facets of archaeocyath palaeobiology remain unclear, making it difficult to reconstruct the palaeoecology of Cambrian reef ecosystems. Of specific interest is how these organisms fed; previous experimental studies have suggested that archaeocyaths functioned as passive suspension feeders relying on ambient currents to transport nutrient-rich water into their central cavities. Here, we test this hypothesis using computational fluid dynamics (CFD) simulations of digital models of select archaeocyath species. Our results demonstrate that, given a range of plausible current velocities, there was very little fluid circulation through the skeleton, suggesting obligate passive suspension feeding was unlikely. Comparing our simulation data with exhalent velocities collected from extant sponges, we infer an active suspension feeding lifestyle for archaeocyaths. The combination of active suspension feeding and biomineralization in Archaeocyatha may have facilitated the creation of modern metazoan reef ecosystems.

Raptorial appendages of the Cambrian apex predator Anomalocaris canadensis are built for soft prey and speed.

The stem-group euarthropod Anomalocaris canadensis is one of the largest Cambrian animals and is often considered the quintessential apex predator of its time. This radiodont is commonly interpreted as a demersal hunter, responsible for inflicting injuries seen in benthic trilobites. However, controversy surrounds the ability of A. canadensis to use its spinose frontal appendages to masticate or even manipulate biomineralized prey. Here, we apply a new integrative computational approach, combining three-dimensional digital modelling, kinematics, finite-element analysis (FEA) and computational fluid dynamics (CFD) to rigorously analyse an A. canadensis feeding appendage and test its morphofunctional limits. These models corroborate a raptorial function, but expose inconsistencies with a capacity for durophagy. In particular, FEA results show that certain parts of the appendage would have experienced high degrees of plastic deformation, especially at the endites, the points of impact with prey. The CFD results demonstrate that outstretched appendages produced low drag and hence represented the optimal orientation for speed, permitting acceleration bursts to capture prey. These data, when combined with evidence regarding the functional morphology of its oral cone, eyes, body flaps and tail fan, suggest that A. canadensis was an agile nektonic predator that fed on soft-bodied animals swimming in a well-lit water column above the benthos. The lifestyle of A. canadensis and that of other radiodonts, including plausible durophages, suggests that niche partitioning across this clade influenced the dynamics of Cambrian food webs, impacting on a diverse array of organisms at different sizes, tiers and trophic levels.

A new species of Nanhsiungchelys (Testudines: Cryptodira: Nanhsiungchelyidae) from the Upper Cretaceous of Nanxiong Basin, China.

Nanhsiungchelyidae are a group of large turtles that lived in Asia and North America during the Cretaceous. Here we report a new species of nanhsiungchelyid, Nanhsiungchelys yangi sp. nov., from the Upper Cretaceous of Nanxiong Basin, China. The specimen consists of a well-preserved skull and lower jaw, as well as the anterior parts of the carapace and plastron. The diagnostic features of Nanhsiungchelys include a large entire carapace length (∼55.5 cm), a network of sculptures consisting of pits and ridges on the surface of the skull and shell, shallow cheek emargination and temporal emargination, deep nuchal emargination, and a pair of anterolateral processes on the carapace. However, Nanhsiungchelys yangi differs from the other species of Nanhsiungchelys mainly in having a triangular-shaped snout (in dorsal view) and wide anterolateral processes on the carapace. Additionally, some other characteristics (e.g., the premaxilla is higher than wide, the maxilla is unseen in dorsal views, a small portion of the maxilla extends posterior and ventral of the orbit, and the parietal is bigger than the frontal) are strong evidence to distinguish Nanhsiungchelys yangi from Nanhsiungchelys wuchingensis. A phylogenetic analysis of nanhsiungchelyids places Nanhsiungchelys yangi and Nanhsiungchelys wuchingensis as sister taxa. Nanhsiungchelys yangi and some other nanhsiungchelyids bear distinct anterolateral processes on the carapace, which have not been reported in any extant turtles and may have played a role in protecting the head. The Nanxiong Basin was extremely hot during the Late Cretaceous, and so we suggest that nanhsiungchelyids might have immersed themselves in mud or water to avoid the heat, similar to some extant tortoises. If they were capable of swimming, our computer simulations of fluid flow suggest the anterolateral processes could have reduced drag during locomotion.

Cambrian stem-group ambulacrarians and the nature of the ancestral deuterostome.

Deuterostomes are characterized by some of the most widely divergent body plans in the animal kingdom. These striking morphological differences have hindered efforts to predict ancestral characters, with the origin and earliest evolution of the group remaining ambiguous. Several iconic Cambrian fossils have been suggested to be early deuterostomes and hence could help elucidate ancestral character states. However, their phylogenetic relationships are controversial. Here, we describe new, exceptionally preserved specimens of the discoidal metazoan Rotadiscus grandis from the early Cambrian Chengjiang biota of China. These reveal a previously unknown double spiral structure, which we interpret as a chordate-like covering to a coelomopore, located adjacent to a horseshoe-shaped tentacle complex. The tentacles differ in key aspects from those seen in lophophorates and are instead more similar to the tentacular systems of extant pterobranchs and echinoderms. Thus, Rotadiscus exhibits a chimeric combination of ambulacrarian and chordate characters. Phylogenetic analyses recover Rotadiscus and closely related fossil taxa as stem ambulacrarians, filling a significant morphological gap in the deuterostome tree of life. These results allow us to reconstruct the ancestral body plans of major clades of deuterostomes, revealing that key traits of extant forms, such as a post-anal region, gill bars, and a U-shaped gut, evolved through convergence.

The rangeomorph Pectinifrons abyssalis: Hydrodynamic function at the dawn of animal life.

Rangeomorphs are among the oldest putative eumetazoans known from the fossil record. Establishing how they fed is thus key to understanding the structure and function of the earliest animal ecosystems. Here, we use computational fluid dynamics to test hypothesized feeding modes for the fence-like rangeomorph Pectinifrons abyssalis, comparing this to the morphologically similar extant carnivorous sponge Chondrocladia lyra. Our results reveal complex patterns of flow around P. abyssalis unlike those previously reconstructed for any other Ediacaran taxon. Comparisons with C. lyra reveal substantial differences between the two organisms, suggesting they converged on a similar fence-like morphology for different functions. We argue that the flow patterns recovered for P. abyssalis do not support either a suspension feeding or osmotrophic feeding habit. Instead, our results indicate that rangeomorph fronds may represent organs adapted for gas exchange. If correct, this interpretation could require a dramatic reinterpretation of the oldest macroscopic animals.

Heterochrony and parallel evolution of echinoderm, hemichordate and cephalochordate internal bars.

Deuterostomes comprise three phyla with radically different body plans. Phylogenetic bracketing of the living deuterostome clades suggests the latest common ancestor of echinoderms, hemichordates and chordates was a bilaterally symmetrical worm with pharyngeal openings, with these characters lost in echinoderms. Early fossil echinoderms with pharyngeal openings have been described, but their interpretation is highly controversial. Here, we critically evaluate the evidence for pharyngeal structures (gill bars) in the extinct stylophoran echinoderms Lagynocystis pyramidalis and Jaekelocarpus oklahomensis using virtual models based on high-resolution X-ray tomography scans of three-dimensionally preserved fossil specimens. Multivariate analyses of the size, spacing and arrangement of the internal bars in these fossils indicate they are substantially more similar to gill bars in modern enteropneust hemichordates and cephalochordates than to other internal bar-like structures in fossil blastozoan echinoderms. The close similarity between the internal bars of the stylophorans L. pyramidalis and J. oklahomensis and the gill bars of extant chordates and hemichordates is strong evidence for their homology. Differences between these internal bars and bar-like elements of the respiratory systems in blastozoans suggest these structures might have arisen through parallel evolution across deuterostomes, perhaps underpinned by a common developmental genetic mechanism.

Cambrian edrioasteroid reveals new mechanism for secondary reduction of the skeleton in echinoderms.

Echinoderms are characterized by a distinctive high-magnesium calcite endoskeleton as adults, but elements of this have been drastically reduced in some groups. Herein, we describe a new pentaradial echinoderm, Yorkicystis haefneri n. gen. n. sp., which provides, to our knowledge, the oldest evidence of secondary non-mineralization of the echinoderm skeleton. This material was collected from the Cambrian Kinzers Formation in York (Pennsylvania, USA) and is dated as ca 510 Ma. Detailed morphological observations demonstrate that the ambulacra (i.e. axial region) are composed of flooring and cover plates, but the rest of the body (i.e. extraxial region) is preserved as a dark film and lacks any evidence of skeletal plating. Moreover, X-ray fluorescence analysis reveals that the axial region is elevated in iron. Based on our morphological and chemical data and on taphonomic comparisons with other fossils from the Kinzers Formation, we infer that the axial region was originally calcified, while the extraxial region was non-mineralized. Phylogenetic analyses recover Yorkicystis as an edrioasteroid, indicating that this partial absence of skeleton resulted from a secondary reduction. We hypothesize that skeletal reduction resulted from lack of expression of the skeletogenic gene regulatory network in the extraxial body wall during development. Secondary reduction of the skeleton in Yorkicystis might have allowed for greater flexibility of the body wall.

The locomotion of extinct secondarily aquatic tetrapods.

The colonisation of freshwater and marine ecosystems by land vertebrates has repeatedly occurred in amphibians, reptiles, birds and mammals over the course of 300 million years. Functional interpretations of the fossil record are crucial to understanding the forces shaping these evolutionary transitions. Secondarily aquatic tetrapods have acquired a suite of anatomical, physiological and behavioural adaptations to locomotion in water. However, much of this information is lost for extinct clades, with fossil evidence often restricted to osteological data and a few extraordinary specimens with soft tissue preservation. Traditionally, functional morphology in fossil secondarily aquatic tetrapods was investigated through comparative anatomy and correlation with living functional analogues. However, in the last two decades, biomechanics in palaeobiology has experienced a remarkable methodological shift. Anatomy-based approaches are increasingly rigorous, informed by quantitative techniques for analysing shape. Moreover, the incorporation of physics-based methods has enabled objective tests of functional hypotheses, revealing the importance of hydrodynamic forces as drivers of evolutionary innovation and adaptation. Here, we present an overview of the latest research on the locomotion of extinct secondarily aquatic tetrapods, with a focus on amniotes, highlighting the state-of-the-art experimental approaches used in this field. We discuss the suitability of these techniques for exploring different aspects of locomotory adaptation, analysing their advantages and limitations and laying out recommendations for their application, with the aim to inform future experimental strategies. Furthermore, we outline some unexplored research avenues that have been successfully deployed in other areas of palaeobiomechanical research, such as the use of dynamic models in feeding mechanics and terrestrial locomotion, thus providing a new methodological synthesis for the field of locomotory biomechanics in extinct secondarily aquatic vertebrates. Advances in imaging technology and three-dimensional modelling software, new developments in robotics, and increased availability and awareness of numerical methods like computational fluid dynamics make this an exciting time for analysing form and function in ancient vertebrates.

Vertically migrating Isoxys and the early Cambrian biological pump.

The biological pump is crucial for transporting nutrients fixed by surface-dwelling primary producers to demersal animal communities. Indeed, the establishment of an efficient biological pump was likely a key factor enabling the diversification of animals over 500 Myr ago during the Cambrian explosion. The modern biological pump operates through two main vectors: the passive sinking of aggregates of organic matter, and the active vertical migration of animals. The coevolution of eukaryotes and sinking aggregates is well understood for the Proterozoic and Cambrian; however, little attention has been paid to the establishment of the vertical migration of animals. Here we investigate the morphological variation and hydrodynamic performance of the Cambrian euarthropod Isoxys. We combine elliptical Fourier analysis of carapace shape with computational fluid dynamics simulations to demonstrate that Isoxys species likely occupied a variety of niches in Cambrian oceans, including vertical migrants, providing the first quantitative evidence that some Cambrian animals were adapted for vertical movement in the water column. Vertical migration was one of several early Cambrian metazoan innovations that led to the biological pump taking on a modern-style architecture over 500 Myr ago.

Lack of support for Deuterostomia prompts reinterpretation of the first Bilateria.

The bilaterally symmetric animals (Bilateria) are considered to comprise two monophyletic groups, Protostomia (Ecdysozoa and the Lophotrochozoa) and Deuterostomia (Chordata and the Xenambulacraria). Recent molecular phylogenetic studies have not consistently supported deuterostome monophyly. Here, we compare support for Protostomia and Deuterostomia using multiple, independent phylogenomic datasets. As expected, Protostomia is always strongly supported, especially by longer and higher-quality genes. Support for Deuterostomia, however, is always equivocal and barely higher than support for paraphyletic alternatives. Conditions that cause tree reconstruction errors-inadequate models, short internal branches, faster evolving genes, and unequal branch lengths-coincide with support for monophyletic deuterostomes. Simulation experiments show that support for Deuterostomia could be explained by systematic error. The branch between bilaterian and deuterostome common ancestors is, at best, very short, supporting the idea that the bilaterian ancestor may have been deuterostome-like. Our findings have important implications for the understanding of early animal evolution.

Pentaradial eukaryote suggests expansion of suspension feeding in White Sea-aged Ediacaran communities.

Suspension feeding is a key ecological strategy in modern oceans that provides a link between pelagic and benthic systems. Establishing when suspension feeding first became widespread is thus a crucial research area in ecology and evolution, with implications for understanding the origins of the modern marine biosphere. Here, we use three-dimensional modelling and computational fluid dynamics to establish the feeding mode of the enigmatic Ediacaran pentaradial eukaryote Arkarua. Through comparisons with two Cambrian echinoderms, Cambraster and Stromatocystites, we show that flow patterns around Arkarua strongly support its interpretation as a passive suspension feeder. Arkarua is added to the growing number of Ediacaran benthic suspension feeders, suggesting that the energy link between pelagic and benthic ecosystems was likely expanding in the White Sea assemblage (~ 558-550 Ma). The advent of widespread suspension feeding could therefore have played an important role in the subsequent waves of ecological innovation and escalation that culminated with the Cambrian explosion.

Functional assessment of morphological homoplasy in stem-gnathostomes.

Osteostraci and Galeaspida are stem-gnathostomes, occupying a key phylogenetic position for resolving the nature of the jawless ancestor from which jawed vertebrates evolved more than 400 million years ago. Both groups are characterized by the presence of rigid headshields that share a number of common morphological traits, in some cases hindering the resolution of their interrelationships and the exact nature of their affinities with jawed vertebrates. Here, we explore the morphological and functional diversity of osteostracan and galeaspid headshields using geometric morphometrics and computational fluid dynamics to constrain the factors that promoted the evolution of their similar morphologies and informing on the ecological scenario under which jawed vertebrates emerged. Phylomorphospace, Mantel analysis and Stayton metrics demonstrate a high degree of homoplasy. Computational fluid dynamics reveals similar hydrodynamic performance among morphologically convergent species, indicating the independent acquisition of the same morphofunctional traits and, potentially, equivalent lifestyles. These results confirm that a number of the characters typically used to infer the evolutionary relationships among galeaspids, osteostracans and jawed vertebrates are convergent in nature, potentially obscuring understanding of the assembly of the gnathostome bodyplan. Ultimately, our results reveal that while the jawless relatives of the earliest jawed vertebrates were ecologically diverse, widespread convergence on the same hydrodynamic adaptations suggests they had reached the limits of their potential ecological diversity-overcome by jawed vertebrates and their later innovations.

Ancient life and moving fluids.

Over 3.7 billion years of Earth history, life has evolved complex adaptations to help navigate and interact with the fluid environment. Consequently, fluid dynamics has become a powerful tool for studying ancient fossils, providing insights into the palaeobiology and palaeoecology of extinct organisms from across the tree of life. In recent years, this approach has been extended to the Ediacara biota, an enigmatic assemblage of Neoproterozoic soft-bodied organisms that represent the first major radiation of macroscopic eukaryotes. Reconstructing the ways in which Ediacaran organisms interacted with the fluids provides new insights into how these organisms fed, moved, and interacted within communities. Here, we provide an in-depth review of fluid physics aimed at palaeobiologists, in which we dispel misconceptions related to the Reynolds number and associated flow conditions, and specify the governing equations of fluid dynamics. We then review recent advances in Ediacaran palaeobiology resulting from the application of computational fluid dynamics (CFD). We provide a worked example and account of best practice in CFD analyses of fossils, including the first large eddy simulation (LES) experiment performed on extinct organisms. Lastly, we identify key questions, barriers, and emerging techniques in fluid dynamics, which will not only allow us to understand the earliest animal ecosystems better, but will also help to develop new palaeobiological tools for studying ancient life.

Computational Fluid Dynamics Suggests Ecological Diversification among Stem-Gnathostomes.

The evolutionary assembly of the vertebrate bodyplan has been characterized as a long-term ecological trend toward increasingly active and predatory lifestyles, culminating in jawed vertebrates that dominate modern vertebrate biodiversity [1-8]. This contrast is no more stark than between the earliest jawed vertebrates and their immediate relatives, the extinct jawless, dermal armor-encased osteostracans, which have conventionally been interpreted as benthic mud-grubbers with poor swimming capabilities and low maneuverability [9-12]. Using computational fluid dynamics, we show that osteostracan headshield morphology is compatible with a diversity of hydrodynamic efficiencies including passive control of water flow around the body; these could have increased versatility for adopting diverse locomotor strategies. Hydrodynamic performance varies with morphology, proximity to the substrate, and angle of attack (inclination). Morphotypes with dorsoventrally oblate headshields are hydrodynamically more efficient when swimming close to the substrate, whereas those with dorsoventrally more prolate headshields exhibit maximum hydrodynamic efficiency when swimming free from substrate effects. These results suggest different hydrofoil functions among osteostracan headshield morphologies, compatible with ecological diversification and undermining the traditional view that jawless stem-gnathostomes were ecologically constrained [9-12] with the origin of jaws as the key innovation that precipitated the ecological diversification of the group [13, 14].

Evolution and Development at the Origin of a Phylum.

Quantifying morphological evolution is key to determining the patterns and processes underlying the origin of phyla. We constructed a hierarchical morphological character matrix to characterize the radiation and establishment of echinoderm body plans during the early Paleozoic. This showed that subphylum-level clades diverged gradually through the Cambrian, and the distinctiveness of the resulting body plans was amplified by the extinction of transitional forms and obscured by convergent evolution during the Ordovician. Higher-order characters that define these body plans were not fixed at the origin of the phylum, countering hypotheses regarding developmental processes governing the early evolution of animals. Instead, these burdened characters were flexible, enabling continued evolutionary innovation throughout the clades' history.

Gregarious suspension feeding in a modular Ediacaran organism.

Reconstructing Precambrian eukaryotic paleoecology is pivotal to understanding the origins of the modern, animal-dominated biosphere. Here, we combine new fossil data from southern Namibia with computational fluid dynamics (CFD) to test between competing feeding models for the Ediacaran taxon Ernietta. In addition, we perform simulations for multiple individuals, allowing us to analyze hydrodynamics of living communities. We show that Ernietta lived gregariously, forming shallow marine aggregations in the latest Ediacaran, 548 to 541 million years (Ma) ago. We demonstrate enhanced vertical mixing of the water column above aggregations and preferential redirection of current into body cavities of downstream individuals. These results support the reconstruction of Ernietta as a macroscopic suspension feeder and also provide a convincing paleoecological advantage to feeding in aggregations analogous to those recognized in many extant marine metazoans. These results provide some of the oldest evidence of commensal facilitation by macroscopic eukaryotes yet recognized in the fossil record.

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.

Effects of body plan evolution on the hydrodynamic drag and energy requirements of swimming in ichthyosaurs.

Ichthyosaurs are an extinct group of fully marine tetrapods that were well adapted to aquatic locomotion. During their approximately 160 Myr existence, they evolved from elongate and serpentine forms into stockier, fish-like animals, convergent with sharks and dolphins. Here, we use computational fluid dynamics (CFD) to quantify the impact of this transition on the energy demands of ichthyosaur swimming for the first time. We run computational simulations of water flow using three-dimensional digital models of nine ichthyosaurs and an extant functional analogue, a bottlenose dolphin, providing the first quantitative evaluation of ichthyosaur hydrodynamics across phylogeny. Our results show that morphology did not have a major effect on the drag coefficient or the energy cost of steady swimming through geological time. We show that even the early ichthyosaurs produced low levels of drag for a given volume, comparable to those of a modern dolphin, and that deep 'torpedo-shaped' bodies did not reduce the cost of locomotion. Our analysis also provides important insight into the choice of scaling parameters for CFD applied to swimming mechanics, and underlines the great influence of body size evolution on ichthyosaur locomotion. A combination of large bodies and efficient swimming modes lowered the cost of steady swimming as ichthyosaurs became increasingly adapted to a pelagic existence.

Whole-body photoreceptor networks are independent of 'lenses' in brittle stars.

Photoreception and vision are fundamental aspects of animal sensory biology and ecology, but important gaps remain in our understanding of these processes in many species. The colour-changing brittle star Ophiocoma wendtii is iconic in vision research, speculatively possessing a unique whole-body visual system that incorporates information from nerve bundles underlying thousands of crystalline 'microlenses'. The hypothesis that these might form a sophisticated compound eye-like system regulated by chromatophores has been extensively reiterated, with investigations into biomimetic optics and similar supposedly 'visual' structures in living and fossil taxa. However, no photoreceptors or visual behaviours have ever been identified. We present the first evidence of photoreceptor networks in three Ophiocoma species, both with and without microlenses and colour-changing behaviour. High-resolution microscopy, immunohistochemistry and synchrotron tomography demonstrate that putative photoreceptors cover the animals' oral, lateral and aboral surfaces, but are absent at the hypothesized focal points of the microlenses. The structural optics of these crystal 'lenses' are an exaptation and do not fulfil any apparent visual role. This contradicts previous studies, yet the photoreceptor network in Ophiocoma appears even more widespread than previously anticipated, both taxonomically and anatomically.