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 Cambrian tommotiid preserving soft tissues reveals the metameric ancestry of lophophorates.

Among extant animals, Lophotrochozoa accounts for the majority of phyla.1 This bilaterian clade radiated rapidly during the Cambrian explosion, obfuscating its phylogenetic relationships and rendering many aspects of its early evolution uncertain. Many early lophotrochozoans are known only from isolated skeletal microfossils, "small shelly fossils," often derived from larger animals with complex multi-element skeletons.2 The discovery of articulated fossils has revealed surprising insights into the animals from which these skeletal pieces were derived, such as paired shells in the mollusc Halkieria.3 Tommotiids are a key group of phosphatic early skeletal fossils that first appear in the late early Cambrian.4,5 Although their affinities were previously obscure, discoveries of partial scleritomes and investigations of growth and microstructure6 provide links with Brachiopoda7,8 and Phoronida,9 two of the lophophorate phyla. By contrast, the body plan of camenellan tommotiids remains a palaeontological mystery, with hypothetical reconstructions representing motile, benthic, dorsally armored worms.4,10 Here, we describe an articulated camenellan (Wufengella bengtsoni gen. et sp. nov.) from the Cambrian Chengjiang Biota, China, revealing the morphology of the scleritome and the first soft tissues from an adult tommotiid. Wufengella carries two dorsal rows of sclerites in a highly asymmetric arrangement, flanked by smaller, cap-shaped sclerites. The scleritome was fringed by iterated fascicles of chaetae and two layers of flattened lobes. Phylogenetic analysis confirms that camenellans occupy a deep branch in lophophorate phylogeny, prior to the acquisition of a sessile lifestyle. Wufengella reveals direct evidence for a metameric body plan reminiscent of annelids early in the evolutionary history of lophophorates.11,12.

Symbiotic fouling of Vetulicola, an early Cambrian nektonic animal.

Here, we report the earliest fossil record to our knowledge of surface fouling by aggregates of small vermiform, encrusting and annulated tubular organisms associated with a mobile, nektonic host, the enigmatic Cambrian animal Vetulicola. Our material is from the exceptionally preserved early Cambrian (Epoch 2, Age 3), Chengjiang biota of Yunnan Province, southwest China, a circa 518 million-year old marine deposit. Our data show that symbiotic fouling relationships between species formed a component of the diversification of animal-rich ecosystems near the beginning of the Phanerozoic Eon, suggesting an early escalation of intimate ecologies as part of the Cambrian animal radiation.

Cambrian Sessile, Suspension Feeding Stem-Group Ctenophores and Evolution of the Comb Jelly Body Plan.

The origin of ctenophores (comb jellies) is obscured by their controversial phylogenetic position, with recent phylogenomic analyses resolving either sponges or ctenophores as the sister group of all other animals. Fossil taxa can provide morphological evidence that may elucidate the origins of derived characters and shared ancestries among divergent taxa, providing a means to "break" long branches in phylogenetic trees. Here we describe new fossil material from the early Cambrian Chengjiang Biota, Yunnan Province, China, including the putative cnidarian Xianguangia, the new taxon Daihua sanqiong gen et sp. nov., and Dinomischus venustus, informally referred to as "dinomischids" here. "Dinomischids" possess a basal calyx encircled by 18 tentacles that surround the mouth. The tentacles carry pinnules, each with a row of stiff filamentous structures interpreted as very large compound cilia of a size otherwise only known in ctenophores. Together with the Cambrian tulip animal Siphusauctum and the armored Cambrian scleroctenophores, they exhibit anatomies that trace ctenophores to a sessile, polypoid stem lineage. This body plan resembles the polypoid, tentaculate morphology of cnidarians, including a blind gastric cavity partitioned by mesenteries. We propose that comb rows are derived from tentacles with paired sets of pinnules that each bear a row of compound cilia. The scleroctenophores exhibit paired comb rows, also observed in Siphusauctum, in addition to an organic skeleton, shared as well by Dinomischus, Daihua, and Xianguangia. We formulate a hypothesis in which ctenophores evolved from sessile, polypoid suspension feeders, sharing similarities with cnidarians that suggest either a close relationship between these two phyla, a striking pattern of early convergent evolution, or an ancestral condition for either metazoans or eumetazoans.

Naked chancelloriids from the lower Cambrian of China show evidence for sponge-type growth.

Chancelloriids are an extinct group of spiny Cambrian animals of uncertain phylogenetic position. Despite their sponge-like body plan, their spines are unlike modern sponge spicules, but share several features with the sclerites of certain Cambrian bilaterians, notably halkieriids. However, a proposed homology of these 'coelosclerites' implies complex transitions in body plan evolution. A new species of chancelloriid, Allonnia nuda, from the lower Cambrian (Stage 3) Chengjiang Lagerstätte is distinguished by its large size and sparse spination, with modified apical sclerites surrounding an opening into the body cavity. The sclerite arrangement in A. nuda and certain other chancelloriids indicates that growth involved sclerite addition in a subapical region, thus maintaining distinct zones of body sclerites and apical sclerites. This pattern is not seen in halkieriids, but occurs in some modern calcarean sponges. With scleritome assembly consistent with a sponge affinity, and in the absence of cnidarian- or bilaterian-grade features, it is possible to interpret chancelloriids as sponges with an unusually robust outer epithelium, strict developmental control of body axis formation, distinctive spicule-like structures and, by implication, minute ostia too small to be resolved in fossils. In this light, chancelloriids may contribute to the emerging picture of high disparity among early sponges.

Host-specific infestation in early Cambrian worms.

Symbiotic relationships are widespread in terrestrial and aquatic animals today, but evidence of symbiosis in the fossil record between soft-bodied bilaterians where the symbiont is intimately associated with the integument of the host is extremely rare. The radiation of metazoan life apparent in the Ediacaran (~635-541 million years ago) and Cambrian (~541-488 million years ago) periods is increasingly accepted to represent ecological diversification resulting from earlier key genetic developmental events and other innovations that occurred in the late Tonian and Cryogenian periods (~850-635 million years ago). The Cambrian has representative animals in each major ecospace category, the early Cambrian in particular having witnessed the earliest known complex animal communities and trophic structures, including symbiotic relationships. Here we report on newly discovered Cricocosmia and Mafangscolex worms that are hosts to aggregates of a new species of tiny worm in the lower Cambrian (Series 2, Stage 3) Chengjiang Lagerstätte of Yunnan Province, southwest China. The worm associations suggest the earliest known record of aggregate infestation of the integument of a soft-bodied bilaterian, host specificity and host shift.

The functional head of the Cambrian radiodontan (stem-group Euarthropoda) Amplectobelua symbrachiata.

BACKGROUND: Segmental composition and homologies of the head of stem-group Euarthropoda have been the foci of recent studies on arthropod origins. An emerging hypothesis suggests that upper-stem group euarthropods possessed a three-segmented head/brain, including an ocular segment (protocerebrum) followed by the deutocerebrum with associated antennae/raptorial limbs and the tritocerebrum, while in the lower stem, head structures of Radiodonta are wholly associated with the protocerebrum and its preceding part. However, this hypothesis is incompletely tested because detailed knowledge on the head components of radiodontans is patchy, and informative articulated specimens are lacking for many taxa. Amplectobelua symbrachiata is the most common radiodontan species in the Chengjiang biota (ca. 520 Ma), normally known as isolated frontal appendages. Here we present detailed descriptions of new articulated specimens that elucidate the morphology and function of its head structures, and discuss their implications for hypotheses about euarthropod cephalic organisation. RESULTS: In addition to a central oval head shield, A. symbrachiata also bears a pair of P-elements connected by an elongated rod. The mouth consists of sets of smooth and tuberculate plates, in contrast to the typical radial oral cones of other radiodontans. Previously identified 'palm-like teeth' are located external to the mouth in the posterior head region, and are interpreted as segmental gnathobase-like structures (GLSs) associated with at least three reduced transitional flaps in a one (pair)-to-one (pair) pattern, consistent with an appendicular nature. Comparisons with other panarthropods show that GLSs are morphologically similar to the mandibles and other gnathobasic mouthparts of euarthropods, as well as to the jaws of onychophorans, indicating their functional integration into the feeding activities of A. symbrachiata. CONCLUSIONS: The functional head of A. symbrachiata must include the reduced transitional segments (and their associated structures), which have been identified in several other radiodontans. This functional view supports the idea that the integration of segments (and associated appendages) into the head region, probably driven by feeding, occurred along the euarthropod stem-lineage. However, the number of reduced transitional segments varies between different groups and it remains uncertain whether GLSs represent proximal or distal parts of appendages. Our study is the first description of appendicular structures other than the frontal appendages in the functional head region of radiodontans, revealing novel feeding structures in the morphological transition from the lower- to the upper- stem-group of Euarthropoda.

Arthropod eyes: The early Cambrian fossil record and divergent evolution of visual systems.

Four types of eyes serve the visual neuropils of extant arthropods: compound retinas composed of adjacent facets; a visual surface populated by spaced eyelets; a smooth transparent cuticle providing inwardly directed lens cylinders; and single-lens eyes. The first type is a characteristic of pancrustaceans, the eyes of which comprise lenses arranged as hexagonal or rectilinear arrays, each lens crowning 8-9 photoreceptor neurons. Except for Scutigeromorpha, the second type typifies Myriapoda whose relatively large eyelets surmount numerous photoreceptive rhabdoms stacked together as tiers. Scutigeromorph eyes are facetted, each lens crowning some dozen photoreceptor neurons of a modified apposition-type eye. Extant chelicerate eyes are single-lensed except in xiphosurans, whose lateral eyes comprise a cuticle with a smooth outer surface and an inner one providing regular arrays of lens cylinders. This account discusses whether these disparate eye types speak for or against divergence from one ancestral eye type. Previous considerations of eye evolution, focusing on the eyes of trilobites and on facet proliferation in xiphosurans and myriapods, have proposed that the mode of development of eyes in those taxa is distinct from that of pancrustaceans and is the plesiomorphic condition from which facetted eyes have evolved. But the recent discovery of enormous regularly facetted compound eyes belonging to early Cambrian radiodontans suggests that high-resolution facetted eyes with superior optics may be the ground pattern organization for arthropods, predating the evolution of arthrodization and jointed post-protocerebral appendages. Here we provide evidence that compound eye organization in stem-group euarthropods of the Cambrian can be understood in terms of eye morphologies diverging from this ancestral radiodontan-type ground pattern. We show that in certain Cambrian groups apposition eyes relate to fixed or mobile eyestalks, whereas other groups reveal concomitant evolution of sessile eyes equipped with optics typical of extant xiphosurans. Observations of fossil material, including that of trilobites and eurypterids, support the proposition that the ancestral compound eye was the apposition type. Cambrian arthropods include possible precursors of mandibulate eyes. The latter are the modified compound eyes, now sessile, and their underlying optic lobes exemplified by scutigeromorph chilopods, and the mobile stalked compound eyes and more elaborate optic lobes typifying Pancrustacea. Radical divergence from an ancestral apposition type is demonstrated by the evolution of chelicerate eyes, from doublet sessile-eyed stem-group taxa to special apposition eyes of xiphosurans, the compound eyes of eurypterids, and single-lens eyes of arachnids. Different eye types are discussed with respect to possible modes of life of the extinct species that possessed them, comparing these to extant counterparts and the types of visual centers the eyes might have served.

Brain structure resolves the segmental affinity of anomalocaridid appendages.

Despite being among the most celebrated taxa from Cambrian biotas, anomalocaridids (order Radiodonta) have provoked intense debate about their affinities within the moulting-animal clade that includes Arthropoda. Current alternatives identify anomalocaridids as either stem-group euarthropods, crown-group euarthropods near the ancestry of chelicerates, or a segmented ecdysozoan lineage with convergent similarity to arthropods in appendage construction. Determining unambiguous affinities has been impeded by uncertainties about the segmental affiliation of anomalocaridid frontal appendages. These structures are variably homologized with jointed appendages of the second (deutocerebral) head segment, including antennae and 'great appendages' of Cambrian arthropods, or with the paired antenniform frontal appendages of living Onychophora and some Cambrian lobopodians. Here we describe Lyrarapax unguispinus, a new anomalocaridid from the early Cambrian Chengjiang biota, southwest China, nearly complete specimens of which preserve traces of muscles, digestive tract and brain. The traces of brain provide the first direct evidence for the segmental composition of the anomalocaridid head and its appendicular organization. Carbon-rich areas in the head resolve paired pre-protocerebral ganglia at the origin of paired frontal appendages. The ganglia connect to areas indicative of a bilateral pre-oral brain that receives projections from the eyestalk neuropils and compound retina. The dorsal, segmented brain of L. unguispinus reinforces an alliance between anomalocaridids and arthropods rather than cycloneuralians. Correspondences in brain organization between anomalocaridids and Onychophora resolve pre-protocerebral ganglia, associated with pre-ocular frontal appendages, as characters of the last common ancestor of euarthropods and onychophorans. A position of Radiodonta on the euarthropod stem-lineage implies the transformation of frontal appendages to another structure in crown-group euarthropods, with gene expression and neuroanatomy providing strong evidence that the paired, pre-oral labrum is the remnant of paired frontal appendages.

An exceptionally preserved arthropod cardiovascular system from the early Cambrian.

The assumption that amongst internal organs of early arthropods only the digestive system withstands fossilization is challenged by the identification of brain and ganglia in early Cambrian fuxianhuiids and megacheirans from southwest China. Here we document in the 520-million-year-old Chengjiang arthropod Fuxianhuia protensa an exceptionally preserved bilaterally symmetrical organ system corresponding to the vascular system of extant arthropods. Preserved primarily as carbon, this system includes a broad dorsal vessel extending through the thorax to the brain where anastomosing branches overlap brain segments and supply the eyes and antennae. The dorsal vessel provides segmentally paired branches to lateral vessels, an arthropod ground pattern character, and extends into the anterior part of the abdomen. The addition of its vascular system to documented digestive and nervous systems resolves the internal organization of F. protensa as the most completely understood of any Cambrian arthropod, emphasizing complexity that had evolved by the early Cambrian.