Competition and mimicry: the curious case of chaetae in brachiopods from the middle Cambrian Burgess Shale.

BACKGROUND: One of the first phyla to acquire biomineralized skeletal elements in the Cambrian, brachiopods represent a vital component in unraveling the early evolution and relationships of the Lophotrochozoa. Critical to improving our understanding of lophotrochozoans is the origin, evolution and function of unbiomineralized morphological features, in particular features such as chaetae that are shared between brachiopods and other lophotrochozoans but are poorly understood and rarely preserved. Micromitra burgessensis and Paterina zenobia from the middle Cambrian Burgess Shale are among the most remarkable examples of fossilized chaetae-bearing brachiopods. The form, functional morphology, evolutionary and ecological significance of their chaetae are studied herein. RESULTS: Like in Recent forms, the moveable but semi-rigid chaetae fringe both the dorsal and ventral mantle margins, but in terms of length, the chaetae of Burgess Shale taxa can exceed twice the maximum length of the shell from which it projects. This is unique amongst Recent and fossil brachiopod taxa and given their size, prominence and energy investment to the organism certainly had an important functional significance. Micromitra burgessensis individuals are preserved on hard skeletal elements, including conspecific shells, Tubulella and frequently on the spicules of the sponge Pirania muricata, providing direct evidence of an ecological association between two species. Morphological analysis and comparisons with fossil and extant brachiopod chaetae point to a number of potential functions, including sensory, defence, feeding, defouling, mimicry and spatial competition. CONCLUSIONS: Our study indicates that it is feasible to link chaetae length to the lack of suitable substrate in the Burgess Shale environment and the increased intraspecific competition associated with this. Our results however, also lend support to the elongated chaetae as an example of Batesian mimicry, of the unpalatable sponge Pirania muricata. We also cannot discount brachiopod chaetae acting as a sensory grille, extending the tactile sensitivity of the mantle into the environment, as an early warning system to approaching predators.

Evolution and diversity of biomineralized columnar architecture in early Cambrian phosphatic-shelled brachiopods.

Biologically-controlled mineralization producing organic-inorganic composites (hard skeletons) by metazoan biomineralizers has been an evolutionary innovation since the earliest Cambrian. Among them, linguliform brachiopods are one of the key invertebrates that secrete calcium phosphate minerals to build their shells. One of the most distinct shell structures is the organo-phosphatic cylindrical column exclusive to phosphatic-shelled brachiopods, including both crown and stem groups. However, the complexity, diversity, and biomineralization processes of these microscopic columns are far from clear in brachiopod ancestors. Here, exquisitely well-preserved columnar shell ultrastructures are reported for the first time in the earliest eoobolids Latusobolus xiaoyangbaensis gen. et sp. nov. and Eoobolus acutulus sp. nov. from the Cambrian Series 2 Shuijingtuo Formation of South China. The hierarchical shell architectures, epithelial cell moulds, and the shape and size of cylindrical columns are scrutinised in these new species. Their calcium phosphate-based biomineralized shells are mainly composed of stacked sandwich columnar units. The secretion and construction of the stacked sandwich model of columnar architecture, which played a significant role in the evolution of linguliforms, is highly biologically controlled and organic-matrix mediated. Furthermore, a continuous transformation of anatomic features resulting from the growth of diverse columnar shells is revealed between Eoobolidae, Lingulellotretidae, and Acrotretida, shedding new light on the evolutionary growth and adaptive innovation of biomineralized columnar architecture among early phosphatic-shelled brachiopods during the Cambrian explosion.

Tubule system of earliest shells as a defense against increasing microbial attacks.

The evolutionary mechanism behind the early Cambrian animal skeletonization was a complex and multifaceted process involving environmental, ecological, and biological factors. Predation pressure, oxygenation, and seawater chemistry change have frequently been proposed as the main drivers of this biological innovation, yet the selection pressures from microorganisms have been largely overlooked. Here we present evidence that calcareous shells of the earliest mollusks from the basal Cambrian (Fortunian Age, ca. 539-529 million years ago) of Mongolia developed advanced tubule systems that evolved primarily as a defensive strategy against extensive microbial attacks within a microbe-dominated marine ecosystem. These high-density tubules, comprising approximately 35% of shell volume, enable nascent mineralized mollusks to cope with increasing microbial bioerosion caused by boring endolithic cyanobacteria, and hence represent an innovation in shell calcification. Our finding demonstrates that enhanced microboring pressures played a significant role in shaping the calcification of the earliest mineralized mollusks during the Cambrian Explosion.

Fibrous or Prismatic? A Comparison of the Lamello-Fibrillar Nacre in Early Cambrian and Modern Lophotrochozoans.

The Precambrian-Cambrian interval saw the first appearance of disparate modern metazoan phyla equipped with a wide array of mineralized exo- and endo-skeletons. However, the current knowledge of this remarkable metazoan skeletonization bio-event and its environmental interactions is limited because uncertainties have persisted in determining the mineralogy, microstructure, and hierarchical complexity of these earliest animal skeletons. This study characterizes in detail a previously poorly understood fibrous microstructure-the lamello-fibrillar (LF) nacre-in early Cambrian mollusk and hyolith shells and compares it with shell microstructures in modern counterparts (coleoid cuttlebones and serpulid tubes). This comparative study highlights key differences in the LF nacre amongst different lophotrochozoan groups in terms of mineralogical compositions and architectural organization of crystals. The results demonstrate that the LF nacre is a microstructural motif confined to the Mollusca. This study demonstrates that similar fibrous microstructure in Cambrian mollusks and hyoliths actually represent a primitive type of prismatic microstructure constituted of calcitic prisms. Revision of these fibrous microstructures in Cambrian fossils demonstrates that calcitic shells are prevalent in the so-called aragonite sea of the earliest Cambrian. This has important implications for understanding the relationship between seawater chemistry and skeletal mineralogy at the time when skeletons were first acquired by early lophotrochozoan biomineralizers.

Evolutionary contingency in lingulid brachiopods across mass extinctions.

Morphology usually serves as an effective proxy for functional ecology,1,2,3,4,5 and evaluating morphological, anatomical, and ecological changes permits a deeper understanding of the nature of diversification and macroevolution.5,6,7,8,9,10,11,12 Lingulid (order Lingulida) brachiopods are both diverse and abundant during the early Palaeozoic but decrease in diversity over time, with only a few genera of linguloids and discinoids present in modern marine ecosystems, resulting in them frequently being referred to as "living fossils."13,14,15 The dynamics that drove this decline remain uncertain, and it has not been determined if there is an associated decline in morphological and ecological diversity. Here, we apply geometric morphometrics to reconstruct global morphospace occupation for lingulid brachiopods through the Phanerozoic, with results showing that maximum morphospace occupation was reached by the Early Ordovician. At this time of peak diversity, linguloids with a sub-rectangular shell shape already possessed several evolutionary features, such as the rearrangement of mantle canals and reduction of the pseudointerarea, common to all modern infaunal forms. The end Ordovician mass extinction has a differential effect on linguloids, disproportionally wiping out those forms with a rounded shell shape, while forms with sub-rectangular shells survived both the end Ordovician and the Permian-Triassic mass extinctions, leaving a fauna predominantly composed of infaunal forms. For discinoids, both morphospace occupation and epibenthic life strategies remain consistent through the Phanerozoic. Morphospace occupation over time, when considered using anatomical and ecological analyses, suggests that the limited morphological and ecological diversity of modern lingulid brachiopods reflects evolutionary contingency rather than deterministic processes.

Hyolithid-like hyoliths without helens from the early Cambrian of South China, and their implications for the evolution of hyoliths.

BACKGROUND: A small hyolith, with a triangular operculum and a conical-pyramidal conch with a sharp apex, originally documented as Ambrolinevitus ventricosus, is revised based on new material from the Chengjiang biota. The operculum of 'Ambrolinevitus' ventricosus displays strong morphological similarities with the operculum of Paramicrocornus from the Shuijingtuo Formation (Cambrian Series 2), indicating that the species should be reassigned to Paramicrocornus. RESULTS: Based on the unusual morphology of Paramicrocornus, we herein propose a new family Paramicrocornidae fam. nov. A cladistic analysis of Cambrian and Ordovician hyoliths clearly delineates hyolithids as a monophyletic group which evolved from the paraphyletic orthothecids in the early Cambrian and with Paramicrocornidae as its closest relative. CONCLUSIONS: The phylogenetic analysis, together with the distribution of hyoliths from the Cambrian to the Ordovician, reveals the presumptive evolution model of both the skeleton and soft-part anatomy of hyoliths. The Family Paramicrocornidae plays an intermediate role in hyolith evolution, representing the transitional stage in the evolution from orthothecids to hyolithids.

A fresh look at the Hyolithid Doliutheca from the Early Cambrian (Stage 4) Shipai Formation of the Three Gorges Area, Hubei, South China.

New hyolith specimens from the early Cambrian (Stage 4) of the Three Gorges area, western Hubei Province are described and assigned to the species Doliutheca orientalis. Doliutheca are preserved in two taphonomic modes: casts in silty mudstone revealing gross morphology and some soft parts, and internal molds in calcareous pelites, which exhibit new morphological details of the conch and operculum. SEM and Micro-CT analyses show that Doliutheca preserve well-developed platy clavicles and cardinal processes on the interior of the operculum composed of rod-shaped tubular elements. This observation and the distinct cardinal and conical shields of the operculum indicate that Doliutheca could be placed within the Family Paramicrocornidae, most recently established as a group of hyoliths closely related to hyolithids.

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.

An encrusting kleptoparasite-host interaction from the early Cambrian.

Parasite-host systems are pervasive in nature but are extremely difficult to convincingly identify in the fossil record. Here we report quantitative evidence of parasitism in the form of a unique, enduring life association between tube-dwelling organisms encrusted to densely clustered shells of a monospecific organophosphatic brachiopod assemblage from the lower Cambrian (Stage 4) of South China. Brachiopods with encrusting tubes have decreased biomass (indicating reduced fitness) compared to individuals without tubes. The encrusting tubes orient tightly in vectors matching the laminar feeding currents of the host, suggesting kleptoparasitism. With no convincing parasite-host interactions known from the Ediacaran, this widespread sessile association reveals intimate parasite-host animal systems arose in early Cambrian benthic communities and their emergence may have played a key role in driving the evolutionary and ecological innovations associated with the Cambrian radiation.

The scleritome of Paterimitra: an Early Cambrian stem group brachiopod from South Australia.

Early Cambrian tommotiids are problematic fossil metazoans with external organophosphatic sclerites that have been considered to be basal members of the lophophorate stem group. Tommotiids are almost exclusively known from isolated or rarely fused individual sclerites, which made previous reconstructions of the actual organism highly conjectural. However, the recent discovery of the first articulated specimens of the tommotiid Eccentrotheca revealed a tubular sclerite arrangement (scleritome) that limited the possible life habit to sessile filter feeding and thus further supported a lophophorate affinity. Here, we report the first articulated specimens of a second tommotiid taxon, Paterimitra from the Early Cambrian of the Arrowie Basin, South Australia. Articulated specimens of Paterimitra are composed of two bilaterally symmetrical sclerite types and an unresolved number of small, asymmetrical and irregular crescent-shaped sclerites that attached to the anterior margin of the symmetrical sclerites. Together, the sclerites form an open cone in which the symmetrical sclerites are joined together and form a small posterior opening near the base of the scleritome, while the irregular crescent-shaped sclerites defined a broad anterior opening. The coniform scleritome of Paterimitra is interpreted to have attached to hard substrates via a pedicle that emerged through the small posterior opening (sometimes forming a tube) and was probably a sessile filter feeder. The scleritome of Paterimitra can be derived from the tubular scleritome of Eccentrotheca by modification of basal sclerites and reduction in tube height, and probably represents a more derived member of the brachiopod stem group with the paired symmetrical sclerites possibly homologous to brachiopod valves.

A stem group echinoderm from the basal Cambrian of China and the origins of Ambulacraria.

Deuterostomes are a morphologically disparate clade, encompassing the chordates (including vertebrates), the hemichordates (the vermiform enteropneusts and the colonial tube-dwelling pterobranchs) and the echinoderms (including starfish). Although deuterostomes are considered monophyletic, the inter-relationships between the three clades remain highly contentious. Here we report, Yanjiahella biscarpa, a bilaterally symmetrical, solitary metazoan from the early Cambrian (Fortunian) of China with a characteristic echinoderm-like plated theca, a muscular stalk reminiscent of the hemichordates and a pair of feeding appendages. Our phylogenetic analysis indicates that Y. biscarpa is a stem-echinoderm and not only is this species the oldest and most basal echinoderm, but it also predates all known hemichordates, and is among the earliest deuterostomes. This taxon confirms that echinoderms acquired plating before pentaradial symmetry and that their history is rooted in bilateral forms. Yanjiahella biscarpa shares morphological similarities with both enteropneusts and echinoderms, indicating that the enteropneust body plan is ancestral within hemichordates.

Brachiopods hitching a ride: an early case of commensalism in the middle Cambrian Burgess Shale.

Ecological interactions, including symbiotic associations such as mutualism, parasitism and commensalism are crucial factors in generating evolutionary novelties and strategies. Direct examples of species interactions in the fossil record generally involve organisms attached to sessile organisms in an epibiont or macroboring relationship. Here we provide support for an intimate ecological association between a calcareous brachiopod (Nisusia) and the stem group mollusc Wiwaxia from the Burgess Shale. Brachiopod specimens are fixed to Wiwaxia scleritomes, the latter showing no signs of decay and disarticulation, suggesting a live association. We interpret this association as the oldest unambiguous example of a facultative ectosymbiosis between a sessile organism and a mobile benthic animal in the fossil record. The potential evolutionary advantage of this association is discussed, brachiopods benefiting from ease of attachment, increased food supply, avoidance of turbid benthic conditions, biofoul and possible protection from predators, suggesting commensalism (benefiting the symbiont with no impact for the host). While Cambrian brachiopods are relatively common epibionts, in particular on sponges, the association of Nisusia with the motile Wiwaxia is rare for a brachiopod species, fossil or living, and suggests that symbiotic associations were already well established and diversified by the "middle" (Series 3, Stage 5) Cambrian.