PUBLISHED VERSION Diego C García-Bellido, Michael S Y Lee, Gregory D Edgecombe, James B Jago, James G Gehling, and John R Paterson A new vetulicolian from Australia and its bearing on the chordate affinities of an enigmatic Cambrian group BMC Evolutionary Biology, 2014; 14(1):214-1-214-13 © 2014 Garcia-Bellido et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Originally published at: http://doi.org/10.1186/s12862-014-0214-z PERMISSIONS http://creativecommons.org/licenses/by/4.0/ http://hdl.handle.net/2440/97396 Drawing by Katrina Kenny A new vetulicolian from Australia and its bearing on the chordate affinities of an enigmatic Cambrian group García-Bellido et al. García-Bellido et al. BMC Evolutionary Biology 2014, 14:214 http://www.biomedcentral.com/1471-2148/14/214 García-Bellido et al. BMC Evolutionary Biology 2014, 14:214 http://www.biomedcentral.com/1471-2148/14/214 RESEARCH ARTICLE Open Access A new vetulicolian from Australia and its bearing on the chordate affinities of an enigmatic Cambrian group Diego C García-Bellido1,2*†, Michael S Y Lee1,2†, Gregory D Edgecombe3†, James B Jago4, James G Gehling1,2 and John R Paterson5*† Abstract Background: Vetulicolians are one of the most problematic and controversial Cambrian fossil groups, having been considered as arthropods, chordates, kinorhynchs, or their own phylum. Mounting evidence suggests that vetulicolians are deuterostomes, but affinities to crown-group phyla are unresolved. Results: A new vetulicolian from the Emu Bay Shale Konservat-Lagerstätte, South Australia, Nesonektris aldridgei gen. et sp. nov., preserves an axial, rod-like structure in the posterior body region that resembles a notochord in its morphology and taphonomy, with notable similarity to early decay stages of the notochord of extant cephalochordates and vertebrates. Some of its features are also consistent with other structures, such as a gut or a coelomic cavity. Conclusions: Phylogenetic analyses resolve a monophyletic Vetulicolia as sister-group to tunicates (Urochordata) within crown Chordata, and this holds even if they are scored as unknown for all notochord characters. The hypothesis that the free-swimming vetulicolians are the nearest relatives of tunicates suggests that a perpetual free-living life cycle was primitive for tunicates. Characters of the common ancestor of Vetulicolia + Tunicata include distinct anterior and posterior body regions – the former being non-fusiform and used for filter feeding and the latter originally segmented – plus a terminal mouth, absence of pharyngeal bars, the notochord restricted to the posterior body region, and the gut extending to the end of the tail. Keywords: Deuterostomes, Chordata, Vetulicolia, Tunicata, Cambrian, Emu Bay Shale Background context, vetulicolians were suggested to be either stem- The enigmatic Cambrian vetulicolians have been allied to group chordates [4] or crown-group chordates most closely various protostome and deuterostome animal lineages over allied to tunicates [5]. Phylogenetic analyses coding for the decades since their discovery. They were initially de- characters in all known vetulicolians using both protostome scribed as bivalved arthropods because their bipartite body anddeuterostometaxa[6]didnotresolvethesystematic was interpreted as an anterior carapace with a segmented position of the group, but suggested kinorhynchs and tuni- abdomen extending beyond the carapace margins [1,2]. No cates to be likely relatives under either a protostome or a segmental appendages have been found in any vetulicolian, deuterostome model, respectively. and closest affinities to deuterostomes were instead pro- The presence of pharyngeal gill slits, pouches, plus posedbecauseofthepresenceofgillslits,apurported possible circular and longitudinal body-wall musculature mesodermal skeleton and a possible endostyle [3,4]. In this ally vetulicolians with deuterostomes [7-10], but their systematic position relative to the crown-group phyla * Correspondence: [email protected]; [email protected] has remained uncertain. The monophyly of Vetulicolia † Equal contributors has been regarded as an open question [8], and most 1School of Earth and Environmental Sciences & Environment Institute, University of Adelaide, Adelaide, SA 5005, Australia debate discusses whether they are either stem-group 5Division of Earth Sciences, School of Environmental and Rural Science, deuterostomes [8,9] or stem-group chordates [11]. University of New England, Armidale, NSW 2351, Australia Vetulicolia is now known from 14 species classified as Full list of author information is available at the end of the article © 2014 Garcia-Bellido et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. García-Bellido et al. BMC Evolutionary Biology 2014, 14:214 Page 2 of 13 http://www.biomedcentral.com/1471-2148/14/214 nine genera, four families and two orders (Additional file 1). Description Most species have been described from Cambrian Series Anterior and posterior body regions are often found dis- 2,Stages3and4inSouthChina(theChengjiangand articulated, with the most complete specimen 125 mm Guanshan biotas), supplemented by taxa from Sirius in length. Extrapolation from incomplete specimens, Passet (Stage 3) in Greenland and the Burgess Shale however, suggests maximum sizes of over 170 mm in (Stage 5) in western Canada. length. The anterior region is up to 70 mm long and Abundant, well-preserved material of a new vetulicolian 42 mm high, subquadrate anteriorly and slightly dorso- from the early Cambrian of Australia extends the group’s ventrally asymmetrical, tapering backwards. An oral distribution to East Gondwana, and a new phylogenetic marginal zone is of constant width, extending dorsally analysis provides evidence that Vetulicolia are crown- and ventrally into marginal keels that widen posteriorly, group chordates, most closely related to tunicates. especially the ventral one, which reaches the axial pos- terior region. The anterior region is generally smooth, Results with some specimens showing a dimpled surface, and Systematics occasional wrinkles due to burial and compaction of This published work and the nomenclatural acts it the cuticularized body-wall (Figure 1C). A thin lateral contains have been registered in Zoobank: http://zoo- groove (Figures 1A, C, G, 3A, C-F) extends longitudin- bank.org/urn:lsid:zoobank.org:pub:D9915A7D-DD12-4031- ally from the oral marginal zone to the posterior portion AA36-D1879A96B6D0. of the anterior body, but no openings (slits, gills or pouches) can be recognized in association. The internal Class Vetulicolida Chen & Zhou, 1997. cavity is occasionally filled by sediment (Figures 1A-C, Nesonektris aldridgei gen. et sp. nov. 3E), and several specimens (Figure 3C, D, F) preserve a ventral food gutter (compare [9], their Figures six A, D, E). LSID The posterior region (tail) is up to 90 mm long and urn:lsid:zoobank.org:act:31858511-031A-4098-9852-18B 40 mm high, and displaced towards the dorsal part of the 42757C847. animal (Figure 1G), but not as much as in Vetulicola ([9], their Figure seven A). It is divided into 7 segments, con- Etymology nected by intersegmental membranes that become shorter Nesos (f.), Greek for island; nektris (f.), for swimmer. and narrower distally (Figures 1D, G, 4). The anterior and Specific epithet in memory of Dick Aldridge, who led a posterior boundaries of the first segment (S1) are at an ap- pioneering effort to resolve vetulicolian affinities. proximate angle of 10–15° to one another, so S1 is nar- rower ventrally (Figures 4A, B, but also 1D, G). Length Holotype and width slightly increase caudally up to S4 and taper SAM P45212a,b (Figure 1A-C, Figure 2B). after S5. S6 is consistently the shortest, while S7 is the lon- gest but narrowest dorso-ventrally, tapering considerably Referred material and presenting a distal notch. Dorsal flanges are present in Fifteen figured paratypes and c. 150 additional unfigured alltailsegments. specimens (Additional file 2). A three-dimensional axial rod-like structure is re- stricted to the posterior region of Nesonektris. It has a Locality and horizon relatively constant width of about 20% the width of the Buck Quarry, the wave-cut platform and coastal cliffs, Big whole tail – including the dorsal and ventral flanges – Gully, Kangaroo Island, South Australia; Emu Bay Shale, but fills a high proportion of the tail cavity. It reaches Pararaia janeae Zone (Cambrian Series 2, Stage 4). the distal end of the posteriormost segment, terminating in the caudal notch. It occasionally shows partition into Diagnosis sections that are offset or separated and frequently Large vetulicolian with