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

Abstract

BackgroundVetulicolians 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.ResultsNew 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.ConclusionsIf 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.

The Emu Bay Shale Konservat-Lagerstätte: a view of Cambrian life from East Gondwana

“…Arthropod affinities were challenged by the absence of limbs and by the discovery of features that were more consistent with alternative (specifically deuterostome) affinities. Based especially on a series of openings in the anterior part of the body interpreted as gill slits , the deuterostome hypothesis has generally found favour (Aldridge et al 2007;Vinther et al 2011;Ou et al 2012;Smith 2012). Nonetheless, the question of whether vetulicolians belong to the deuterostome stem-group or are more closely related to one of the extant deuterostome subgroups (thus making them crown-group Deuterostomia) remains unclear.…”

New data on the palaeobiology of the enigmatic yunnanozoans from theChengjiangBiota,LowerCambrian,China

“…b) considered by Bergström () to be preserved in the act of splitting is not, in itself, definitive evidence for ecdysis, as noted by Ou et al . (); the partial separation of the body parts of this specimen might well be the product of decomposition. The fact that small specimens of Yunnanozoon have a similar number of dorsal units to large specimens suggests that segments were not added during growth stages in the manner commonly shown by ecdysozoans.…”

“…Structures that have previously been interpreted as gill filaments in Vetulicola have now been shown by careful preparation to be a zone of striations and folds around the pharyngeal openings (Ou et al . ). Although the similarities between the two animals are intriguing, the differences mean that the identification of homologies is somewhat speculative, and some caution should be maintained when assessing whether they have a close relationship.…”

Cambrian Chordates and Vetulicolians

“…These enigmatic creatures, typified by the eponymous genus Vetulicola, have the general appearance of a segmented tadpole. They were originally identified as arthropods due to the apparently segmented character of the 'tail' in some genera, but the complete absence of jointed appendages plus the recognition of a series of five pairs of gill structures [45] in the anterior part of the animal led to a revised placement with the deuterostomes. They are best known from Lagerstätten such as Chengjiang [13] and have recently been reported from the newly discovered Qingjiang biota [16].…”