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Tabelliscolex (Cricocosmiidae: Palaeoscolecidomorpha) from the Early Cambrian Chengjiang Biota, and the Evolution of Seriation in Ecdysozoa

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Tabelliscolex (Cricocosmiidae: Palaeoscolecidomorpha) from the Early Cambrian Chengjiang Biota, and the Evolution of Seriation in Ecdysozoa Accepted Manuscript Journal of the Geological Society Tabelliscolex (Cricocosmiidae: Palaeoscolecidomorpha) from the early Cambrian Chengjiang Biota, and the evolution of seriation in Ecdysozoa Xiaomei Shi, Richard J. Howard, Gregory D. Edgecombe, Xianguang Hou & Xiaoya Ma DOI: https://doi.org/10.1144/jgs2021-060 To access the most recent version of this article, please click the DOI URL in the line above. When citing this article please include the above DOI. This article is part of the Advances in the Cambrian Explosion collection available at: https://www.lyellcollection.org/cc/advances-cambrian-explosion Received 26 May 2021 Revised 2 August 2021 Accepted 7 August 2021 © 2021 The Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution 4.0 License (http://creativecommons.org/licenses/by/4.0/). Published by The Geological Society of London. Publishing disclaimer: www.geolsoc.org.uk/pub_ethics Supplementary material at https://doi.org/10.6084/m9.figshare.c.5551565 Manuscript version: Accepted Manuscript This is a PDF of an unedited manuscript that has been accepted for publication. The manuscript will undergo copyediting, typesetting and correction before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Although reasonable efforts have been made to obtain all necessary permissions from third parties to include their copyrighted content within this article, their full citation and copyright line may not be present in this Accepted Manuscript version. Before using any content from this article, please refer to the Version of Record once published for full citation and copyright details, as permissions may be required. Downloaded from http://pubs.geoscienceworld.org/jgs/article-pdf/doi/10.1144/jgs2021-060/5378998/jgs2021-060.pdf by guest on 30 September 2021 Tabelliscolex (Cricocosmiidae: Palaeoscolecidomorpha) from the early Cambrian Chengjiang Biota, and the evolution of seriation in Ecdysozoa Xiaomei Shi1,2,5, Richard J. Howard2,3,4,5, Gregory D. Edgecombe2,4*, Xianguang Hou1,2, Xiaoya Ma1,2,3* 1. Yunnan Key Laboratory for Palaeobiology, Institute of Palaeontology, Yunnan University, Chenggong Campus, Kunming 650504, China 2. MEC International Joint Laboratory for Palaeobiology and Palaeoenvironment, Yunnan University, Chenggong Campus, Kunming 650504, China 3. Centre for Ecology and Conservation, University of Exeter, Penryn Campus, Cornwall TR10 9TA, UK 4. Department of Earth Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK MANUSCRIPT 5. These authors contributed equally *Correspondence: [email protected]; [email protected] ACCEPTED Downloaded from http://pubs.geoscienceworld.org/jgs/article-pdf/doi/10.1144/jgs2021-060/5378998/jgs2021-060.pdf by guest on 30 September 2021 Abstract Cricocosmiidae is a clade of palaeoscolecid-like worms from the Chengjiang Biota, China (Cambrian Stage 3). In contrast to palaeoscolecids sensu stricto, which exhibit tessellating micro-plate trunk ornamentation, cricocosmiids possess larger, serially repeated sets of trunk sclerites bearing resemblance to lobopodian trunk sclerites (e.g., Microdictyon spp.). Cricocosmiidae were therefore proposed as stem-group Panarthropoda in some studies but are recovered as stem-group Priapulida in most phylogenetic analyses. The affinity of cricoscosmiids within Ecdysozoa is therefore of much interest, as is testing the homology of these seriated structures. We report four new specimens of the rare cricocosmiid Tabelliscolex hexagonus, yielding new details of the ventral trunk projections, sclerites and proboscis. New data confirm T. hexagonus possessed paired ventral trunk projections in a consistent seriated pattern, which is also reported from new material of Cricocosmia jinningensis (Cricocosmiidae) and Mafangscolex yunnanensis (Palaeoscolecida sensu stricto). Even when the seriated sclerites and ventral projections of cricocosmiids are coded as homologous with the seriated trunk sclerites and paired appendages, respectively, of lobopodian panarthropods, our tree searches indicate they are convergent. Cricocosmiidae is nested within a monophyletic ―Palaeoscolecida sensu lato‖ clade (Palaeoscolecidomorpha nov.) in stem-group Priapulida. Our study indicates that morphological seriation has independent origins inMANUSCRIPT Scalidophora and Panarthropoda. Keywords: Cambrian, Ecdysozoa, palaeoscolecids, Cricocosmiidae, phylogenetics, palaeobiology ACCEPTED Downloaded from http://pubs.geoscienceworld.org/jgs/article-pdf/doi/10.1144/jgs2021-060/5378998/jgs2021-060.pdf by guest on 30 September 2021 Palaeoscolecida Conway Morris and Robinson, 1986 is a group of marine benthic ecdysozoan worms with a spiny anterior proboscis, an elongate trunk with striking ornamentation of small, annular- arranged, tessellating polymorphic plates, and bilaterally orientated terminal posterior hooks (Harvey et al. 2010). Cricocosmiidae Hou et al. 1999 are otherwise morphologically similar to palaeoscolecids, but exhibit a different, though also highly characteristic trunk ornamentation. The cricocosmiids Cricocosmia jinningensis Hou and Sun, 1988 and Tabelliscolex hexagonus Han et al. 2003a possess larger sclerites that are serially repeated in groups along the length of the trunk, with a striking similarity in structure, position and composition to the trunk sclerites of some lobopodian panarthropods such as Onychodictyon spp. and Microdictyon spp. (Han et al. 2007a). Cricocosmiids and a few other vermiform taxa such as Maotianshania cylindrica Sun and Hou, 1987 and Tylotites petiolaris Luo et al. 1999 have been informally grouped with palaeoscolecids as ―Palaeoscolecida sensu lato‖; in this framework, ―Palaeoscolecida sensu stricto” is reserved exclusively for those taxa bearing the distinctive polymorphic tessellating plate ornament (see Harvey et al. 2010). Palaeoscolecida sensu stricto has a broad biogeographic and stratigraphic range from the early Cambrian to the late Silurian, whereas Cricocosmiidae, Maotianshania and Tylotites (i.e., Palaeoscolecida sensu lato) are known only from the Cambrian Stage 3 Chengjiang Biota of Yunnan, China. MANUSCRIPT Individual plates of Palaeoscolecida sensu stricto comprise the form-genera Milaculum, Hadimopanella, Kaimenella and Utahphospha (see Hinz et al. 1990). These small shelly fossils (SSFs) are known from the Cambrian to Silurian across a wide geographic distribution and are sometimes recovered in association with the sclerotome (Hinz et al. 1990; Müller and Hinz- Schallreuter 1993; Brock and Cooper 1993; Zhang and Pratt 1996; Conway Morris 1997; Topper et al. 2010; Harvey et al. 2010; Duan et al. 2012; Streng et al. 2017). Individual plates of the form-genus Hadimopanella have also been identified as small carbonaceous fossils (SCFs), alongside possibly conspecificACCEPTED pharyngeal teeth, introvert scalids and terminal posterior hooks from the early Cambrian of Scandinavia (Slater et al. 2017). Some SSF cuticle fragments even preserve in-situ the posterior terminal hooks of Palaeoscolecida sensu stricto (e.g., Harvey et al. 2010, Fig. 2E-G). Cricocosmiids remain unidentified from microfossil assemblages. Articulated two-dimensional compression fossils from Konservat-Lagerstätten demonstrate the complete cuticular morphology and partial soft-tissue anatomy of both groups however, revealing many similarities. Palaeoscolecida sensu stricto Downloaded from http://pubs.geoscienceworld.org/jgs/article-pdf/doi/10.1144/jgs2021-060/5378998/jgs2021-060.pdf by guest on 30 September 2021 described in detail from such articulated material include Scathascolex minor (Smith 2015), Wronascolex antiquus (García-Bellido et al. 2013) and W. yichangensis (Yang and Zhang, 2016), Mafangscolex yunnanensis (Hou et al. 1988; Luo et al. 2014; Yang et al. 2020); Guanduscolex minor (Hu et al. 2008), and Utahscolex ratcliffei (Whittaker et al. 2020). The best preserved of these Palaeoscolecida sensu stricto exhibit a three-part proboscis divisible into the traditional zonation system common to extant and fossil priapulans (Conway Morris 1977). Zone I is represented by an introvert with rings of scalids, Zone II is the collar – representing a diastema between introvert and pharynx, and Zone III is the eversible pharynx with rings of teeth. This is mirrored by the sometimes exquisitely preserved proboscis morphology of Cricocosmia jinningensis and Maotianshania cylindrica (Huang 2005), and in addition is partially known in Tabelliscolex hexagonus (Han et al. 2003a) and Tylotites petiolaris (Han et al. 2003b, 2007b). Palaeoscolecid-like worms have an interesting and varied history of phylogenetic interpretation. Palaeoscolecida was originally attributed to Annelida when first described (Whittard 1953), but later authors favoured an affinity among the cycloneuralian phyla due to the annulated trunk region (Dzik and Krumbiegel 1989; Conway Morris 1993), especially after the discovery of the anterior proboscis (Hou and Bergström 1994). Alternative cycloneuralian interpretations of palaeoscolecids have been postulated, the group being allied to either nematomorphsMANUSCRIPT (Hou and Bergström 1994) or priapulans (Conway Morris 1997), or as stem-group Cycloneuralia (Zhurvalev et al. 2011). Another interpretation is that palaeoscolecids represent a basal branch within Ecdysozoa, which was popularized by the influential hypothesis of
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