The finding of pharyngeal teeth and circumoral mouthparts in fossils of the Cambrian lobopodian animal Hallucigenia sparsa improves our understanding of the deep evolutionary links between moulting animals. See Letter p.75
Fossils provide direct evidence of evolutionary history, and their unique morphological combinations can reveal crucial evolutionary links between extant taxa1. Most major animal phyla first appear in the fossil record during the Cambrian period, 541 million to 485 million years ago, and this early flowering of animal life has been termed the Cambrian explosion. Therefore, Cambrian fossils are particularly important for understanding the origin and early evolution of major animal groups. In this issue, Smith and Caron2 (page 75) redescribe one of the most celebrated Cambrian animals, Hallucigenia sparsa, and document several new features of this species, including its pharyngeal teeth and circumoral elements, which are suggested to be two of the few morphological characters uniting all groups within the Ecdysozoa.
The Ecdysozoa is far and away the richest animal group3. It is composed of eight extant phyla that shed their cuticle periodically to accommodate growth4 — nematode worms and crustaceans are familiar examples. The two commonly recognized subgroupings of ecdysozoans, Cycloneuralia and Panarthropoda, have distinctly different body plans (Fig. 1). Cycloneuralia unites worm-like organisms (Nematoda, Nematomorpha, Priapulida, Kinorhyncha and Loricifera) that have a non-segmented body terminating in a mouth that can turn inside out (eversible) and has a ring of nerves behind it — their brain. By contrast, panarthropods (Arthropoda, Onychophora and Tardigrada) are all segmented, with paired legs, and have a dorsal (upper side) brain in front of the mouth. These great morphological disparities have made it difficult to illuminate the last common ancestor of the Ecdysozoa and to fully understand the evolutionary relationships between its phyla, particularly between Cycloneuralia and Panarthropoda. Early ecdysozoan fossils are crucial for addressing these questions.
Among the earliest Cambrian fossils, ecdysozoans are the most diverse and abundant group. They are best shown in exceptionally preserved Cambrian fossil localities, such as the Chengjiang biota in China (around 518 million years old) and the Burgess Shale in Canada (about 508 million years old). The body plans of some of the organisms represented have not changed much over 500 million years of evolution, such as priapulids (commonly known as penis worms) and arthropods (jointed-legged invertebrates with an exoskeleton and a segmented body, such as insects and spiders). Other Cambrian groups are extinct but represent crucial evolutionary stages, such as lobopodians (an informal group of worm-like animals with non-jointed legs) and radiodontans (a group of animals characterized by possessing a pair of frontal appendages at the anterior part of the head and a ventral (lower side) mouth surrounded by radial tooth plates).
Cambrian lobopodians are assigned to Panarthropoda on the basis of their segmented body and paired legs, but they also share a worm-shaped soft body and a terminal mouth with cycloneuralians. These unusual character combinations make Cambrian lobopodians particularly relevant for understanding the evolutionary links between the two major ecdysozoan groups.
Hallucigenia sparsa from the Burgess Shale is certainly the most famous Cambrian lobopodian animal. It was originally reconstructed upside down5 and considered to be one of the most bizarre Cambrian creatures until it was recognized as a lobopodian animal armed with dorsal spines6. However, owing to lack of evidence of clear head structures, the front and rear ends of H. sparsa have been a subject of debate. Smith and Caron's redescription includes a new set of anatomical features that once and for all clarifies the anterior–posterior orientation of H. sparsa. They show that the animal had an elongated head with a pair of dorsal eyes. It also had hardened, lamellae-like structures surrounding its mouth opening (circumoral elements), and the front part of its foregut (its pharynx) was lined with teeth.
Although pharyngeal teeth and circumoral mouthparts have been reported in other Cambrian lobopodians7,8, Smith and Caron have provided the most convincing evidence yet of equivalent structures in this extinct group. These findings amplify the transitional status of Cambrian lobopodians, because the pharyngeal teeth of H. sparsa most closely resemble those of Cambrian priapulids, whereas circumoral structures are also a key characteristic of Cambrian radiodontans. More crucially, H. sparsa is now regarded2,9 as an ancestor of living onychophorans (commonly known as velvet worms), so the finding of H. sparsa mouthparts suggests that the absence of circumoral elements and pharyngeal teeth in extant onychophorans is probably the result of secondary loss. Thus, this combined structure is now reported for all major ecdysozoan groups.
Smith and Caron further notice the similarities of ecdysozoan mouthparts (see Supplementary Note 1, transformation series 9 and 13 of the paper2), and suggest that all pharyngeal teeth and circumoral structures across ecdysozoan groups share a single origin from the last common ancestor of ecdysozoans. This provides new anatomical features to unite the Cycloneuralia and Panarthropoda.
However, this conclusion is bound to provoke some controversy. Limited by the vagaries of preservation, it is difficult to determine the detailed morphology and symmetry of the pharyngeal teeth and circumoral elements of H. sparsa — such details are essential for further comparative studies. Although the homology of ecdysozoan pharynxes lined with teeth is well accepted, the evolutionary links between the circumoral structures of Cycloneuralia and Panarthropoda are less clear, because these differ substantially in their structure, relative position, construction and symmetry10. Therefore, a more complete understanding of the evolutionary origin and transformation sequence of these mouthparts depends on a more thorough comparison of their morphology, development and innervation across all ecdysozoan groups. For this, new fossil evidence showing transitional features of the mouthparts between cycloneuralians and panarthropods would be particularly enlightening.Footnote 1
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