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.

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.

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.

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.

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.

An edrioasteroid from the Silurian Herefordshire Lagerstätte of England reveals the nature of the water vascular system in an extinct echinoderm.

Echinoderms are unique in having a water vascular system with tube feet, which perform a variety of functions in living forms. Here, we report the first example of preserved tube feet in an extinct group of echinoderms. The material, from the Silurian Herefordshire Lagerstätte, UK, is assigned to a new genus and species of rhenopyrgid edrioasteroid, Heropyrgus disterminus The tube feet attach to the inner surface of compound interradial plates and form two sets, an upper and a lower, an arrangement never reported previously in an extant or extinct echinoderm. Cover plates are absent and floor plates are separated creating a large permanent entrance to the interior of the oral area. The tube feet may have captured food particles that entered the oral area and/or enhanced respiration. The pentameral symmetry of the oral surface transitions to eight columns in which the plates are vertically offset resulting in a spiral appearance. This change in symmetry may reflect flexibility in the evolutionary development of the axial and extraxial zones in early echinoderm evolution.

Open data and digital morphology.

Over the past two decades, the development of methods for visualizing and analysing specimens digitally, in three and even four dimensions, has transformed the study of living and fossil organisms. However, the initial promise that the widespread application of such methods would facilitate access to the underlying digital data has not been fully achieved. The underlying datasets for many published studies are not readily or freely available, introducing a barrier to verification and reproducibility, and the reuse of data. There is no current agreement or policy on the amount and type of data that should be made available alongside studies that use, and in some cases are wholly reliant on, digital morphology. Here, we propose a set of recommendations for minimum standards and additional best practice for three-dimensional digital data publication, and review the issues around data storage, management and accessibility.

Inference of facultative mobility in the enigmatic Ediacaran organism Parvancorina.

Establishing how Ediacaran organisms moved and fed is critical to deciphering their ecological and evolutionary significance, but has long been confounded by their non-analogue body plans. Here, we use computational fluid dynamics to quantitatively analyse water flow around the Ediacaran taxon Parvancorina, thereby testing between competing models for feeding mode and mobility. The results show that flow was not distributed evenly across the organism, but was directed towards localized areas; this allows us to reject osmotrophy, and instead supports either suspension feeding or detritivory. Moreover, the patterns of recirculating flow differ substantially with orientation to the current, suggesting that if Parvancorina was a suspension feeder, it would have been most efficient if it was able to re-orient itself with respect to current direction, and thus ensure flow was directed towards feeding structures. Our simulations also demonstrate that the amount of drag varied with orientation, indicating that Parvancorina would have greatly benefited from adjusting its position to minimize drag. Inference of facultative mobility in Parvancorina suggests that Ediacaran benthic ecosystems might have possessed a higher proportion of mobile taxa than currently appreciated from trace fossil studies. Furthermore, this inference of movement suggests the presence of musculature or appendages that are not preserved in fossils, but which would noneltheless support a bilaterian affinity for Parvancorina.

Cambrian cinctan echinoderms shed light on feeding in the ancestral deuterostome.

Reconstructing the feeding mode of the latest common ancestor of deuterostomes is key to elucidating the early evolution of feeding in chordates and allied phyla; however, it is debated whether the ancestral deuterostome was a tentaculate feeder or a pharyngeal filter feeder. To address this, we evaluated the hydrodynamics of feeding in a group of fossil stem-group echinoderms (cinctans) using computational fluid dynamics. We simulated water flow past three-dimensional digital models of a Cambrian fossil cinctan in a range of possible life positions, adopting both passive tentacular feeding and active pharyngeal filter feeding. The results demonstrate that an orientation with the mouth facing downstream of the current was optimal for drag and lift reduction. Moreover, they show that there was almost no flow to the mouth and associated marginal groove under simulations of passive feeding, whereas considerable flow towards the animal was observed for active feeding, which would have enhanced the transport of suspended particles to the mouth. This strongly suggests that cinctans were active pharyngeal filter feeders, like modern enteropneust hemichordates and urochordates, indicating that the ancestral deuterostome employed a similar feeding strategy.

Experimental reduction of intromittent organ length reduces male reproductive success in a bug.

It is now clear in many species that male and female genital evolution has been shaped by sexual selection. However, it has historically been difficult to confirm correlations between morphology and fitness, as genital traits are complex and manipulation tends to impair function significantly. In this study, we investigate the functional morphology of the elongate male intromittent organ (or processus) of the seed bug Lygaeus simulans, in two ways. We first use micro-computed tomography (micro-CT) and flash-freezing to reconstruct in high resolution the interaction between the male intromittent organ and the female internal reproductive anatomy during mating. We successfully trace the path of the male processus inside the female reproductive tract. We then confirm that male processus length influences sperm transfer by experimental ablation and show that males with shortened processi have significantly reduced post-copulatory reproductive success. Importantly, male insemination function is not affected by this manipulation per se. We thus present rare, direct experimental evidence that an internal genital trait functions to increase reproductive success and show that, with appropriate staining, micro-CT is an excellent tool for investigating the functional morphology of insect genitalia during copulation.

Early post-metamorphic, Carboniferous blastoid reveals the evolution and development of the digestive system in echinoderms.

Inferring the development of the earliest echinoderms is critical to uncovering the evolutionary assembly of the phylum-level body plan but has long proven problematic because early ontogenetic stages are rarely preserved as fossils. Here, we use synchrotron tomography to describe a new early post-metamorphic blastoid echinoderm from the Carboniferous (approx. 323 Ma) of China. The resulting three-dimensional reconstruction reveals a U-shaped tubular structure in the fossil interior, which is interpreted as the digestive tract. Comparisons with the developing gut of modern crinoids demonstrate that crinoids are an imperfect analogue for many extinct groups. Furthermore, consideration of our findings in a phylogenetic context allows us to reconstruct the evolution and development of the digestive system in echinoderms more broadly; there was a transition from a straight to a simple curved gut early in the phylum's evolution, but additional loops and coils of the digestive tract (as seen in crinoids) were not acquired until much later.

A new interpretation of Pikaia reveals the origins of the chordate body plan.

Our understanding of the evolutionary origin of Chordata, one of the most disparate and ecologically significant animal phyla, is hindered by a lack of unambiguous stem-group relatives. Problematic Cambrian fossils that have been considered as candidate chordates include vetulicolians,1Yunnanozoon,2 and the iconic Pikaia.3 However, their phylogenetic placement has remained poorly constrained, impeding reconstructions of character evolution along the chordate stem lineage. Here we reinterpret the morphology of Pikaia, providing evidence for a gut canal and, crucially, a dorsal nerve cord-a robust chordate synapomorphy. The identification of these structures underpins a new anatomical model of Pikaia that shows that this fossil was previously interpreted upside down. We reveal a myomere configuration intermediate between amphioxus and vertebrates and establish morphological links between Yunnanozoon, Pikaia, and uncontroversial chordates. In this light, we perform a new phylogenetic analysis, using a revised, comprehensive deuterostome dataset, and establish a chordate stem lineage. We resolve vetulicolians as a paraphyletic group comprising the earliest diverging stem chordates, subtending a grade of more derived stem-group chordates comprising Yunnanozoon and Pikaia. Our phylogenetic results reveal the stepwise acquisition of characters diagnostic of the chordate crown group. In addition, they chart a phase in early chordate evolution defined by the gradual integration of the pharyngeal region with a segmented axial musculature, supporting classical evolutionary-developmental hypotheses of chordate origins4 and revealing a "lost chapter" in the history of the phylum.

Ediacaran marine animal forests and the ventilation of the oceans.

The rise of animals across the Ediacaran-Cambrian transition marked a step-change in the history of life, from a microbially dominated world to the complex macroscopic biosphere we see today.1,2,3 While the importance of bioturbation and swimming in altering the structure and function of Earth systems is well established,4,5,6 the influence of epifaunal animals on the hydrodynamics of marine environments is not well understood. Of particular interest are the oldest "marine animal forests,"7 which comprise a diversity of sessile soft-bodied organisms dominated by the fractally branching rangeomorphs.8,9 Typified by fossil assemblages from the Ediacaran of Mistaken Point, Newfoundland,8,10,11 these ancient communities might have played a pivotal role in structuring marine environments, similar to modern ecosystems,7,12,13 but our understanding of how they impacted fluid flow in the water column is limited. Here, we use ecological modeling and computational flow simulations to explore how Ediacaran marine animal forests influenced their surrounding environment. Our results reveal how organism morphology and community structure and composition combined to impact vertical mixing of the surrounding water. We find that Mistaken Point communities were capable of generating high-mixing conditions, thereby likely promoting gas and nutrient transport within the "canopy." This mixing could have served to enhance local-scale oxygen concentrations and redistribute resources like dissolved organic carbon. Our work suggests that Ediacaran marine animal forests may have contributed to the ventilation of the oceans over 560 million years ago, well before the Cambrian explosion of animals.

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.

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.

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.