Meiofaunal deuterostomes from the basal Cambrian of Shaanxi (China).

Deuterostomes include the group we belong to (vertebrates) as well as an array of disparate forms that include echinoderms, hemichordates and more problematic groups such as vetulicolians and vetulocystids. The Cambrian fossil record is well-populated with representative examples, but possible intermediates are controversial and the nature of the original deuterostome remains idealized. Here we report millimetric fossils, Saccorhytus coronarius nov. gen., nov. sp., from an Orsten-like Lagerstätte from the earliest Cambrian period of South China, which stratigraphically are amongst the earliest of deuterostomes. The bag-like body bears a prominent mouth and associated folds, and behind them up to four conical openings on either side of the body as well as possible sensory structures. An anus may have been absent, and correspondingly the lateral openings probably served to expel water and waste material. This new form has similarities to both the vetulicolians and vetulocystids and collectively these findings suggest that a key step in deuterostome evolution was the development of lateral openings that subsequently were co-opted as pharyngeal gills. Depending on its exact phylogenetic position, the meiofaunal habit of Saccorhytus may help to explain the major gap between divergence times seen in the fossil record and estimates based on molecular clocks.

Three Cambrian fossils assembled into an extinct body plan of cnidarian affinity.

The early Cambrian problematica Xianguangia sinica, Chengjiangopenna wangii, and Galeaplumosus abilus from the Chengjiang biota (Yunnan, China) have caused much controversy in the past and their phylogenetic placements remain unresolved. Here we show, based on exceptionally preserved material (85 new specimens plus type material), that specimens previously assigned to these three species are in fact parts of the same organism and propose that C. wangii and G. abilus are junior synonyms of X. sinica Our reconstruction of the complete animal reveals an extinct body plan that combines the characteristics of the three described species and is distinct from all known fossil and living taxa. This animal resembled a cnidarian polyp in overall morphology and having a gastric cavity partitioned by septum-like structures. However, it possessed an additional body cavity within its holdfast, an anchoring pit on the basal disk, and feather-like tentacles with densely ciliated pinnules arranged in an alternating pattern, indicating that it was a suspension feeder rather than a predatory actiniarian. Phylogenetic analyses using Bayesian inference and maximum parsimony suggest that X. sinica is a stem-group cnidarian. This relationship implies that the last common ancestor of X. sinica and crown cnidarians was probably a benthic, polypoid animal with a partitioned gastric cavity and a single mouth/anus opening. This extinct body plan suggests that feeding strategies of stem cnidarians may have been drastically different from that of their crown relatives, which are almost exclusively predators, and reveals that the morphological disparity of total-group Cnidaria is greater than previously assumed.

Anamorphic development and extended parental care in a 520 million-year-old stem-group euarthropod from China.

BACKGROUND: Extended parental care is a complex reproductive strategy in which progenitors actively look after their offspring up to - or beyond - the first juvenile stage in order to maximize their fitness. Although the euarthropod fossil record has produced several examples of brood-care, the appearance of extended parental care within this phylum remains poorly constrained given the scarcity of developmental data for Palaeozoic stem-group representatives that would link juvenile and adult forms in an ontogenetic sequence. RESULTS: Here, we describe the post-embryonic growth of Fuxianhuia protensa from the early Cambrian Chengjiang Lagerstätte in South China. Our data demonstrate anamorphic post-embryonic development for F. protensa, in which new tergites were sequentially added from a posterior growth zone, the number of tergites varies from eight to 30. The growth of F. protensa is typified by the alternation between segment addition, followed by the depletion of the anteriormost abdominal segment into the thoracic region. The transformation of abdominal into thoracic tergite is demarcated by the development of laterally tergopleurae, and biramous walking legs. The new ontogeny data leads to the recognition of the rare Chengjiang euarthropod Pisinnocaris subconigera as a junior synonym of Fuxianhuia. Comparisons between different species of Fuxianhuia and with other genera within Fuxianhuiida suggest that heterochrony played a prominent role in the morphological diversification of fuxianhuiids. Functional analogy with the flexible trunk ontogeny of Cambrian and Silurian olenimorphic trilobites suggests an adaptation to sporadic low oxygen conditions in Chengjiang deposits for F. protensa. Finally, understanding the growth of F. protensa allows for the interpretation of an exceptional life assemblage consisting of a sexually mature adult alongside four ontogenetically coeval juveniles, which constitutes the oldest occurrence of extended parental care by prolonged cohabitation in the panarthropod fossil record. CONCLUSIONS: Our findings constitute the most detailed characterization of the post-embryonic development in a soft-bodied upper stem-group euarthropod available to date. The new ontogeny data illuminates the systematics, trunk segmentation and palaeoecology of F. protensa, offers insights on the macroevolutionary processes involved in the diversification of this clade, and contributes towards an improved understanding of complex post-embryonic reproductive ecology in Cambrian euarthropods.

Microbial decay analysis challenges interpretation of putative organ systems in Cambrian fuxianhuiids.

The Chengjiang fossil Lagerstätte (Cambrian Stage 3) from Yunnan, southern China is renowned for its soft-tissue preservation. Accordingly structures in fuxianhuiids, radiodontans and great appendage arthropods have been interpreted as the nervous and cardiovascular systems, including brains, hearts and blood vessels. That such delicate organ systems survive the fossilization process seems remarkable; given that this mode of preservation involves major taphonomic changes, such as flattening, microbial degradation, chemical alteration and replacement. Here, we document a range of taphonomic preservation states in numerous articulated individuals of Fuxianhuia protensa We suggest that organic (partly iron mineral-replaced) bulbous structures in the head region, previously interpreted as brain tissue, along with sagittally located organic strands interpreted as part of the cardiovascular system or as nerve cords, may be better explained as microbial biofilms that developed following decomposition of the intestine, muscle and other connective tissues, forming halos surrounding the original organic remains.

An armoured Cambrian lobopodian from China with arthropod-like appendages.

Cambrian fossil Lagerstätten preserving soft-bodied organisms have contributed much towards our understanding of metazoan origins. Lobopodians are a particularly interesting group that diversified and flourished in the Cambrian seas. Resembling 'worms with legs', they have long attracted much attention in that they may have given rise to both Onychophora (velvet worms) and Tardigrada (water bears), as well as to arthropods in general. Here we describe Diania cactiformis gen. et sp. nov. as an 'armoured' lobopodian from the Chengjiang fossil Lagerstätte (Cambrian Stage 3), Yunnan, southwestern China. Although sharing features with other typical lobopodians, it is remarkable for possessing robust and probably sclerotized appendages, with what appear to be articulated elements. In terms of limb morphology it is therefore closer to the arthropod condition, to our knowledge, than any lobopodian recorded until now. Phylogenetic analysis recovers it in a derived position, close to Arthropoda; thus, it seems to belong to a grade of organization close to the point of becoming a true arthropod. Further, D. cactiformis could imply that arthropodization (sclerotization of the limbs) preceded arthrodization (sclerotization of the body). Comparing our fossils with other lobopodian appendage morphologies--see Kerygmachela, Jianshanopodia and Megadictyon--reinforces the hypothesis that the group as a whole is paraphyletic, with different taxa expressing different grades of arthropodization.

Evidence for gill slits and a pharynx in Cambrian vetulicolians: implications for the early evolution of deuterostomes.

BACKGROUND: Vetulicolians are a group of Cambrian metazoans whose distinctive bodyplan continues to present a major phylogenetic challenge. Thus, we see vetulicolians assigned to groups as disparate as deuterostomes and ecdysozoans. This divergence of opinions revolves around a strikingly arthropod-like body, but one that also bears complex lateral structures on its anterior section interpreted as pharyngeal openings. Establishing the homology of these structures is central to resolving where vetulicolians sit in metazoan phylogeny. RESULTS: New material from the Chengjiang Lagerstätte helps to resolve this issue. Here, we demonstrate that these controversial structures comprise grooves with a series of openings. The latter are oval in shape and associated with a complex anatomy consistent with control of their opening and closure. Remains of what we interpret to be a musculature, combined with the capacity for the grooves to contract, indicate vetulicolians possessed a pumping mechanism that could process considerable volumes of seawater. Our observations suggest that food captured in the anterior cavity was transported to dorsal and ventral gutters, which then channeled material to the intestine. This arrangement appears to find no counterpart in any known fossil or extant arthropod (or any other ecdysozoan). Anterior lateral perforations, however, are diagnostic of deuterostomes. CONCLUSIONS: If the evidence is against vetulicolians belonging to one or other group of ecdysozoan, then two phylogenetic options seem to remain. The first is that such features as vetulicolians possess are indicative of either a position among the bilaterians or deuterostomes but apart from the observation that they themselves form a distinctive and recognizable clade current evidence can permit no greater precision as to their phylogenetic placement. We argue that this is too pessimistic a view, and conclude that evidence points towards vetulicolians being members of the stem-group deuterostomes; a group best known as the chordates (amphioxus, tunicates, vertebrates), but also including the ambulacrarians (echinoderms, hemichordates), and xenoturbellids. If the latter, first they demonstrate that these members of the stem group show few similarities to the descendant crown group representatives. Second, of the key innovations that underpinned deuterostome success, the earliest and arguably most seminal was the evolution of openings that define the pharyngeal gill slits of hemichordates (and some extinct echinoderms) and chordates.

Gill function in an early arthropod and the widespread adoption of the countercurrent exchange mechanism.

Rising but fluctuating oxygen levels in the Early Palaeozoic provide an environmental context for the radiation of early metazoans, but little is known about how mechanistically early animals satisfied their oxygen requirements. Here we propose that the countercurrent gaseous exchange, a highly efficient respiratory mechanism, was effective in the gills of the Late Ordovician trilobite Triarthrus eatoni. In order to test this, we use computational fluid dynamics to simulate water flow around its gills and show that water velocity decreased distinctly in front of and between the swollen ends, which first encountered the oxygen-charged water, and slowed continuously at the mid-central region, forming a buffer zone with a slight increase of the water volume. In T. eatoni respiratory surface area was maximized by extending filament height and gill shaft length. In comparison with the oxygen capacity of modern fish and crustaceans, a relatively low weight specific area in T. eatoni may indicate its low oxygen uptake, possibly related to a less active life mode. Exceptionally preserved respiratory structures in the Cambrian deuterostome Haikouella are also consistent with a model of countercurrent gaseous exchange, exemplifying the wide adoption of this strategy among early animals.

Comment on "Ultrastructure reveals ancestral vertebrate pharyngeal skeleton in yunnanozoans".

Tian et al. (Research Articles, 8 July 2022, abm2708) hypothesized that yunnanozoans are stem-group vertebrates on the basis of "cellular cartilage", "fibrillin microfibers", and "subchordal rod" associated with the branchial arches of yunnanozoans. However, we reject the presence of cellular cartilage, fibrillin, and the phylogenetic proposal of vertebrate affinities based on ultrastructure and morphology of yunnanozoans from more than 8000 specimens.

Dawn of complex animal food webs: A new predatory anthozoan (Cnidaria) from Cambrian.

Cnidarians diverged very early in animal evolution; therefore, investigations of the morphology and trophic levels of early fossil cnidarians may provide critical insights into the evolution of metazoans and the origin of modern marine food webs. However, there has been a lack of unambiguous anthozoan cnidarians from Ediacaran assemblages, and undoubted anthozoans from the Cambrian radiation of metazoans are very rare and lacking in ecological evidence. Here, we report a new polypoid cnidarian, Nailiana elegans gen. et sp. nov., represented by multiple solitary specimens from the early Cambrian Chengjiang biota (∼520 Ma) of South China. These specimens show eight unbranched tentacles surrounding a single opening into the gastric cavity, which may have born multiple mesenteries. Thus, N. elegans displays a level of organization similar to that of extant cnidarians. Phylogenetic analyses place N. elegans in the stem lineage of Anthozoa and suggest that the ancestral anthozoan was a soft-bodied, solitary polyp showing octoradial symmetry. Moreover, one specimen of the new polyp preserves evidence of predation on an epifaunal lingulid brachiopod. This case provides the oldest direct evidence of macrophagous predation, the advent of which may have triggered the emergence of complex trophic/ecological relationships in Cambrian marine communities and spurred the explosive radiation of animal body plans.

Epibionts on the lingulate brachiopod Diandongia from the Early Cambrian Chengjiang Lagerstatte, South China.

The classic Chengjiang Lagerstätte (Lower Cambrian, Atdabanian stage: Yu'anshan Formation) Yunnan, southwestern China, has yielded, besides the exceptional and often controversial soft-bodied fossils, a fauna of primitive/early lingulid brachiopods. Diandongia pista (Rong 1974) is one of the commonest and most strongly mineralized of the phosphatic brachiopods from the Lagerstätte. The shells of this species have been found to commonly serve as a basibiont host. Epibionts comprise the coeval brachiopod Longtancunella chengjiangensis and the cone-shaped cnidarian-related Archotuba conoidalis, as well as rounded smaller-sized epizoans (lesser than 2 mm). A principle morphological analysis demonstrates that the ovoid and rounded organisms that often occur along the commissure of D. pista resemble small juvenile or immature brachiopods. Epibiont-bearing shells of D. pista with soft-tissue preservation demonstrate that the host brachiopods were overgrown while alive, and provide an argument for D. pista having a semi-infaunal life style with only the slim pedicle embedded in sediment. The epibiotic association sheds direct light on the ecology of Cambrian brachiopods in soft-substrate marine environments. The Chengjiang fossils demonstrate that the Early Cambrian brachiopods, as compared with recent lingulids, occupied different and a wider spectrum of ecological niches and tiers of space.

Are hyoliths Palaeozoic lophophorates?

The phylogenetic position of hyoliths has long been unsettled, with recent discoveries of a tentaculate feeding apparatus ('lophophore') and fleshy apical extensions from the shell ('pedicle') suggesting a lophophorate affinity. Here, we describe the first soft parts associated with the feeding apparatus of an orthothecid hyolith, Triplicatella opimus from the Chengjiang biota of South China. The tuft-like arrangement of the tentacles of T. opimus differs from that of hyolithids, suggesting they collected food directly from the substrate. A reassessment of the feeding organ in hyolithids indicates that it does not represent a lophophore and our analysis of the apical structures associated with some orthothecids show that these represent crushed portions of the shell and are not comparable to the brachiopod pedicle. The new information suggests that hyoliths are more likely to be basal members of the lophotrochozoans rather than lophophorates closely linked with the Phylum Brachiopoda.

Evolutionary trade-off in reproduction of Cambrian arthropods.

Trade-offs play a crucial role in the evolution of life-history strategies of extant organisms by shaping traits such as growth pattern, reproductive investment, and lifespan. One important trade-off is between offspring number and energy (nutrition, parental care, etc.) allocated to individual offspring. Exceptional Cambrian fossils allowed us to trace the earliest evidence of trade-offs in arthropod reproduction. †Chuandianella ovata, from the early Cambrian Chengjiang biota of China, brooded numerous (≤100 per clutch), small (Ø, ~0.5 mm) eggs under carapace flaps. The closely related †Waptia fieldensis, from the middle Cambrian Burgess Shale of Canada, also brooded young, but carried fewer (≤ 26 per clutch), larger (Ø, ~2.0 mm) eggs. The notable differences in clutch/egg sizes between these two species suggest an evolutionary trade-off between quantity and quality of offspring. The shift toward fewer, larger eggs might be an adaptive response to marine ecosystem changes through the early-middle Cambrian. We hypothesize that reproductive trade-offs might have facilitated the evolutionary success of early arthropods.

Sclerite-bearing annelids from the lower Cambrian of South China.

Cambrian annelids are strikingly diverse and reveal important details of annelid character acquisition. Their contribution, however, to a wider understanding of the evolution of the trochozoans (encompassing the annelids as well as such groups as the brachiopods and molluscs) remains limited. Thus the early annelids had been linked to a variety of cataphract Cambrian metazoans, notably Wiwaxia and the halkieriids, but recent work assigns such fossils to stem-group molluscs. Here we report two new annelids from the Lower Cambrian Chengjiang Lagerstätte, South China. Ipoliknus avitus n. gen., n. sp. is biramous with neurochaetae and notochaetae, but significantly also bears dorsal spinose sclerites and dorso-lateral dentate sclerites. Adelochaeta sinensis n. gen., n. sp. is unique amongst Cambrian polychaetes in possessing the rod-like supports of the parapodia known as aciculae. This supports phylogenetic placement of Adelochaeta as sister to some more derived aciculate Palaeozoic taxa, but in contrast Ipoliknus is recovered as the most basal of the stem-group annelids. Sclerites and chaetae of I. avitus are interpreted respectively as the remnants and derivatives of a once more extensive cataphract covering that was a characteristic of more primitive trochozoans. The two sets of chaetae (noto- and neurochaetae) and two sets of sclerites (spinose and dentate) suggest that in a pre-annelid an earlier and more complete scleritome may have consisted of four zones of sclerites. Other cataphract taxa from the Lower Palaeozoic show a variety of scleritome configurations but establishing direct links with such basal annelids as Ipoliknus at present must remain conjectural.

Gut glands illuminate trunk segmentation in Cambrian fuxianhuiids.

The euarthropod body consists of serially repeated segments with various degrees of functional specialization and regionalization [1]. Some representatives exhibit deviant metameric patterns expressed as an indirect correspondence between components of the exoskeleton, usually the number or position of dorsoventral sclerotized plates and walking legs (Supplemental Information) [1-3]. Segmental mismatch in the form of supernumerary walking legs per tergite (i.e. dorsal exoskeletal plate) is characteristic of fuxianhuiids, Cambrian euarthropods widely regarded as critical for understanding the origin of this phylum [4,5]. The broader significance of this organization remains obscure, however, due to the difficulty of distinguishing which components of the fuxianhuiid trunk reflect ancestral or derived traits. Here, we describe for the first time the presence of metameric midgut diverticulae in Fuxianhuia protensa from the Chengjiang Konservat-Lagerstätte and demonstrate that these digestive structures follow the segmentation pattern of the dorsal exoskeleton. Midgut diverticulae signal a predatory or scavenging ecology [6,7], falsifying the view of fuxianhuiids as simple mud-feeders [4]. Comparison with other euarthropods [1-3,5] indicates that fuxianhuiids possessed a unique mode of exoskeletal and visceral segmental mismatch, in which the tergites and midgut were segmentally patterned independently from the walking legs and ventral nerve cord. Our findings provide direct evidence of substantial developmental flexibility among stem-group euarthropods during the Cambrian.

New reconstruction of the Wiwaxia scleritome, with data from Chengjiang juveniles.

Wiwaxiids are a problematic group of scale-covered lophotrochozoans known from Cambrian Stages 3-5. Their imbricating dorsal scleritome of leaf-like scales has prompted comparison with various annelids and molluscs, and has been used as a template to reconstruct the articulation pattern of isolated Small Shelly Fossils. The first articulated specimens of Wiwaxia from the Cambrian Stage 3 Chengjiang Konservat-Lagerstätte show that the Wiwaxia scleritome comprised nine equivalent transverse rows associated with outgrowths of soft tissue, but did not possess a separate zone of anterior sclerites. This serial construction is fundamentally incompatible with the circumferential disposition of sclerites in early molluscs, but does closely resemble the armature of certain annelids. A deep homology with the annelid scleritome must be reconciled with Wiwaxia's mollusc-like mouthparts and foot; together these point to a deep phylogenetic position, close to the common ancestor of annelids and molluscs.

A vanished history of skeletonization in Cambrian comb jellies.

Ctenophores are traditionally regarded as "lower" metazoans, sharing with cnidarians a diploblastic grade of organization. Unlike cnidarians, where skeletonization (biomineralization and sclerotization) evolved repeatedly among ecologically important taxa (for example, scleractinians and octocorals), living ctenophores are characteristically soft-bodied animals. We report six sclerotized and armored ctenophores from the early Cambrian period. They have diagnostic ctenophore features (for example, an octamerous symmetry, oral-aboral axis, aboral sense organ, and octaradially arranged ctene rows). Unlike most modern counterparts, however, they lack tentacles, have a sclerotized framework, and have eight pairs of ctene rows. They are resolved as a monophyletic group (Scleroctenophora new class) within the ctenophores. This clade reveals a cryptic history and sheds new light on the early evolution of this basal animal phylum. Skeletonization also occurs in some other Cambrian animal groups whose extant members are exclusively soft-bodied, suggesting the ecological importance of skeletonization in the Cambrian explosion.

A diploblastic radiate animal at the dawn of cambrian diversification with a simple body plan: distinct from Cnidaria?

BACKGROUND: Microfossils of the genus Punctatus include developmental stages such as blastula, gastrula, and hatchlings, and represent the most complete developmental sequence of animals available from the earliest Cambrian. Despite the extremely well-preserved specimens, the evolutionary position of Punctatus has relied only on their conical remains and they have been tentatively assigned to cnidarians. We present a new interpretation of the Punctatus body plan based on the developmental reconstruction aided by recent advances in developmental biology. RESULTS: Punctatus developed from a rather large egg, gastrulated in a mode of invagination from a coeloblastura, and then formed a mouth directly from the blastopore. Spiny benthic hatchlings were distinguishable from swimming or crawling ciliate larvae found in cnidarians and sponges. A mouth appeared at the perihatching embryonic stage and was renewed periodically during growth, and old mouths transformed into the body wall, thus elongating the body. Growing animals retained a small blind gut in a large body cavity without partitioning by septa and did not form tentacles, pedal discs or holdfasts externally. A growth center at the oral pole was sufficient for body patterning throughout life, and the body patterning did not show any bias from radial symmetry. CONCLUSIONS: Contrary to proposed cnidarian affinity, the Punctatus body plan has basic differences from that of cnidarians, especially concerning a spacious body cavity separating ectoderm from endoderm. The lack of many basic cnidarian characters in the body patterning of Punctatus leads us to consider its own taxonomic group, potentially outside of Cnidaria.

Early Cambrian pentamerous cubozoan embryos from South China.

BACKGROUND: Extant cubozoans are voracious predators characterized by their square shape, four evenly spaced outstretched tentacles and well-developed eyes. A few cubozoan fossils are known from the Middle Cambrian Marjum Formation of Utah and the well-known Carboniferous Mazon Creek Formation of Illinois. Undisputed cubozoan fossils were previously unknown from the early Cambrian; by that time probably all representatives of the living marine phyla, especially those of basal animals, should have evolved. METHODS: Microscopic fossils were recovered from a phosphatic limestone in the Lower Cambrian Kuanchuanpu Formation of South China using traditional acetic-acid maceration. Seven of the pre-hatched pentamerous cubozoan embryos, each of which bears five pairs of subumbrellar tentacle buds, were analyzed in detail through computed microtomography (Micro-CT) and scanning electron microscopy (SEM) without coating. RESULTS: The figured microscopic fossils are unequivocal pre-hatching embryos based on their spherical fertilization envelope and the enclosed soft-tissue that has preserved key anatomical features arranged in perfect pentaradial symmetry, allowing detailed comparison with modern cnidarians, especially medusozoans. A combination of features, such as the claustrum, gonad-lamella, suspensorium and velarium suspended by the frenula, occur exclusively in the gastrovascular system of extant cubozoans, indicating a cubozoan affinity for these fossils. Additionally, the interior anatomy of these embryonic cubozoan fossils unprecedentedly exhibits the development of many new septum-derived lamellae and well-partitioned gastric pockets unknown in living cubozoans, implying that ancestral cubozoans had already evolved highly specialized structures displaying unexpected complexity at the dawn of the Cambrian. The well-developed endodermic lamellae and gastric pockets developed in the late embryonic stages of these cubozoan fossils are comparable with extant pelagic juvenile cubomedusae rather than sessile cubopolyps, whcih indicates a direct development in these fossil taxa, lacking characteristic stages of a typical cnidarian metagenesis such as planktonic planula and sessile polyps.

A sclerite-bearing stem group entoproct from the early Cambrian and its implications.

The Lophotrochozoa includes disparate tentacle-bearing sessile protostome animals, which apparently appeared in the Cambrian explosion, but lack an uncontested fossil record. Here we describe abundant well preserved material of Cotyledion tylodes Luo et Hu, 1999, from the Cambrian (Series 2) Chengjiang deposits, reinterpreted here as a stem-group entoproct. The entoproct affinity is supported by the sessile body plan and interior soft anatomy. The body consists of an upper calyx and a lower elongate stalk with a distal holdfast. The soft anatomy includes a U-shaped gut with a mouth and aboral anus ringed by retractable marginal tentacles. Cotyledion differs from extant entoprocts in being larger, and having the calyx and the stalk covered by numerous loosely-spaced external sclerites. The description of entoprocts from the Chengjiang biota traces the ancestry of yet another lophotrochozoan phylum back to the Cambrian radiation, and has important implications for the earliest evolution of lophotrochozoans.