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Open Access Highly Accessed Research article

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

Qiang Ou1, Simon Conway Morris2*, Jian Han3, Zhifei Zhang3, Jianni Liu3, Ailin Chen4, Xingliang Zhang3 and Degan Shu13*

Author affiliations

1 Early Life Evolution Laboratory, School of Earth Sciences and Resources, China University of Geosciences, Beijing 100083, China

2 Department of Earth Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EQ, UK

3 Early Life Institute and Key Laboratory of Continental Dynamics, Northwest University, Xi'an 710069, China

4 Chengjiang Fauna National Geopark of China, Chengjiang 652500, China

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Citation and License

BMC Biology 2012, 10:81  doi:10.1186/1741-7007-10-81

Published: 2 October 2012

Abstract

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 Lagerst├Ątte 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.