With millions of extant species, ecdysozoans (Scalidophora, Nematoida and Panarthropoda) constitute a major portion of present-day biodiversity. All ecdysozoans secrete an exoskeletal cuticle which must be moulted periodically and replaced by a larger one. Although moulting (ecdysis) has been recognized in early Palaeozoic panarthropods such as trilobites and basal groups such as anomalocaridids and lobopodians, the fossil record lacks clear evidence of ecdysis in early scalidophorans, largely because of difficulties in recognizing true exuviae. Here, we describe two types of exuviae in microscopic scalidophoran worms from the lowermost Cambrian Kuanchuanpu Formation (ca535 Ma) of China and reconstruct their moulting process. These basal scalidophorans moulted in a manner similar to that of extant priapulid worms, extricating themselves smoothly from their old tubular cuticle or turning their exuviae inside out like the finger of a glove. This is the oldest record of moulting in ecdysozoans. We also discuss the origin of ecdysis in the light of recent molecular analyses and the significance of moulting in the early evolution of animals.

Background: The radiation of ecdysozoans (moulting animals) during the Cambrian gave rise to panarthropods and various groups of worms including scalidophorans, which played an important role in the elaboration of early marine ecosystems. Although most scalidophorans were infaunal burrowers travelling through soft sediment at the bottom of the sea,Selkirkialived inside a tube.Results: We explore the palaeobiology of these tubicolous worms, and more generally the origin and evolutionary significance of tube-dwelling in early animals, based on exceptionally preserved fossils from the early Cambrian Chengjiang Lagerstätte (Stage 3, China) including a new species,Selkirkia transitasp. nov. We find that the best phylogenetic model resolvesSelkirkiaas a stem-group priapulid.Selkirkiasecreted a protective cuticular thickening, the tube, inside which it was able to move during at least part of its life. Partly based on measured growth patterns, we construe that this tube was separated from the trunk during a moulting process that has no direct equivalent in other scalidophorans. Although the ontogeny ofSelkirkiais currently unknown, we hypothesize that its conical tube might have had the same ecological function and possibly even deep development origin as the lorica, a protective cuticular thickening found in larval priapulids and adult loriciferans.Selkirkiais seen as a semi-sedentary animal capable of very shallow incursions below the water/sediment interface, possibly for feeding or during the tube-secreting phase. Brachiopod epibionts previously reported from the Xiaoshiba Lagerstätte (ca. 514 Ma) also presumably occur inSelkirkia sinicafrom Chengjiang (ca. 518 Ma).Conclusions: Our critical and model-based approach provides a new phylogenetic framework for Scalidophora, upon which to improve in order to study the evolution of morphological characters in this group. Tube-dwelling is likely to have offeredSelkirkiabetter protection and anchoring to sediment and has developed simultaneously in other Cambrian animals such as hemichordates, annelids or panarthropods. Often lost in modern representatives in favour of active infaunal lifestyles, tube-dwelling can be regarded as an early evolutionary response of various metazoans to increasing environmental and biological pressure in Cambrian marine ecosystems.

The cuticle of ecdysozoans (Panarthropoda, Scalidophora, Nematoida) is secreted by underlying epidermal cells and renewed via ecdysis. We explore here the relationship between epidermis and external cuticular ornament in stem-group scalidophorans from the early Cambrian of China (Kuanchuanpu Formation;ca535 Ma) that had two types of microscopic polygonal cuticular networks with either straight or microfolded boundaries. Detailed comparisons with modern scalidophorans (priapulids) indicate that these networks faithfully replicate the cell boundaries of the epidermis. This suggests that the cuticle of early scalidophorans formed through the fusion between patches of extracellular material secreted by epidermal cells, as observed in various groups of present-day ecdysozoans, including arthropods. Key genetic, biochemical and mechanical processes associated with ecdysis and cuticle formation seem to have appeared very early (at least not later than 535 Ma) in the evolution of ecdysozoans. Microfolded reticulation is likely to be a mechanical response to absorbing contraction exerted by underlying muscles. The polygonal reticulation in early and extant ecdysozoans is clearly a by-product of the epidermal cell pavement and interacted with the sedimentary environment.

The vast majority of early Paleozoic ecdysozoan worms are often resolved as stem-group Priapulida based on resemblances with the rare modern representatives of the group, such as the structure of the introvert and the number and distribution of scalids (a spiny cuticular outgrowth) and pharyngeal teeth. In Priapulida, both scalids and teeth create symmetry patterns, and three major diagnostic features are generally used to define the group: 25 longitudinal rows of scalids (five-fold symmetry), 8 scalids around the first introvert circle and the pentagonal arrangement of pharyngeal teeth. Here we describe Ercaivermis sparios gen. et sp. nov., a new priapulid from the early Cambrian Chengjiang Lagerstätte, characterized by an annulated trunk lacking a sclerotized ornament, four pairs of anal hooks and 16 longitudinal rows of scalids along its introvert and eight scalids around each introvert circle, giving the animal an unusual octoradial symmetry. Cladistic analyses resolve Ercaivermis as a stem-group priapulid. Ercaivermis also suggests that several biradial symmetry patterns (e.g., pentagonal, octagonal) expressed in the cuticular ornament, may have co-existed among early Cambrian priapulids and that the pentaradial mode may have become rapidly dominant during the course of evolution, possibly via the standardization of patterning, i.e., the natural selection of one symmetry type over others.

Ecdysozoan worms (Nematoida + Scalidophora) are typified by disparate grades of neural organization reflecting a complex evolutionary history. The fossil record offers a unique opportunity to reconstruct the early character evolution of the nervous system via the exceptional preservation of extinct representatives. We focus on their nervous system as it appears in early and mid-Cambrian fossils. We show that some of the oldest known representatives of the group either preserved in carbonaceous compression (early and mid-Cambrian Burgess-type preservation) or secondarily phosphatized in three dimensions (e.g., basal Cambrian Kuanchuanpu Formation, ca. 535 million years) had an unpaired ventral nerve cord (VNC) that ran along the trunk in an eccentric position as in modern priapulids and nematodes. A phylogenetic analysis integrating these fossil data suggests that ancestral scalidophorans had an unpaired VNC and that paired nervous systems probably evolved independently in Kinorhyncha and Loricifera, and, more importantly, in panarthropods in possible relation with the rise of paired appendages and bilaterally coordinated motricity.

Extant ecdysozoans (moulting animals) are represented by a great variety of soft-bodied or articulated organisms that may or may not have appendages. However, controversies remain about the vermiform nature (i.e. elongated and tubular) of their ancestral body plan. We describe here Beretella spinosa gen. et sp. nov. a tiny (maximal length 3 mm) ecdysozoan from the lowermost Cambrian, Yanjiahe Formation, South China, characterized by an unusual sack-like appearance, single opening, and spiny ornament. Beretella spinosa gen. et sp. nov has no equivalent among animals, except Saccorhytus coronarius, also from the basal Cambrian. Phylogenetic analyses resolve both fossil species as a sister group (Saccorhytida) to all known Ecdysozoa, thus suggesting that ancestral ecdysozoans may have been non-vermiform animals. Saccorhytids are likely to represent an early off-shot along the stem-line Ecdysozoa. Although it became extinct during the Cambrian, this animal lineage provides precious insight into the early evolution of Ecdysozoa and the nature of the earliest representatives of the group.