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      Canadia spinosa and the early evolution of the annelid nervous system

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      1 , 2 , * , 2 , 3 , 4
      Science Advances
      American Association for the Advancement of Science

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          Abstract

          Exceptional fossils reveal annelid nervous system evolution.

          Abstract

          Annelid worms are a disparate, primitively segmented clade of bilaterians that first appear during the early Cambrian Period. Reconstructing their early evolution is complicated by the extreme morphological diversity in early diverging lineages, rapid diversification, and sparse fossil record. Canadia spinosa, a Burgess Shale fossil polychaete, is redescribed as having palps with feeding grooves, a dorsal median antenna and biramous parapodia associated with the head and flanking a ventral mouth. Carbonaceously preserved features are identified as a terminal brain, circumoral connectives, a midventral ganglionated nerve cord and prominent parapodial nerves. Phylogenetic analysis recovers neuroanatomically simple extant taxa as the sister group of other annelids, but the phylogenetic position of Canadia suggests that the annelid ancestor was reasonably complex neuroanatomically and that reduction of the nervous system occurred several times independently in the subsequent 500 million years of annelid evolution.

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          Illuminating the base of the annelid tree using transcriptomics.

          Annelida is one of three animal groups possessing segmentation and is central in considerations about the evolution of different character traits. It has even been proposed that the bilaterian ancestor resembled an annelid. However, a robust phylogeny of Annelida, especially with respect to the basal relationships, has been lacking. Our study based on transcriptomic data comprising 68,750-170,497 amino acid sites from 305 to 622 proteins resolves annelid relationships, including Chaetopteridae, Amphinomidae, Sipuncula, Oweniidae, and Magelonidae in the basal part of the tree. Myzostomida, which have been indicated to belong to the basal radiation as well, are now found deeply nested within Annelida as sister group to Errantia in most analyses. On the basis of our reconstruction of a robust annelid phylogeny, we show that the basal branching taxa include a huge variety of life styles such as tube dwelling and deposit feeding, endobenthic and burrowing, tubicolous and filter feeding, and errant and carnivorous forms. Ancestral character state reconstruction suggests that the ancestral annelid possessed a pair of either sensory or grooved palps, bicellular eyes, biramous parapodia bearing simple chaeta, and lacked nuchal organs. Because the oldest fossil of Annelida is reported for Sipuncula (520 Ma), we infer that the early diversification of annelids took place at least in the Lower Cambrian. © The Author 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
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            Cladistics and polychaetes

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              A New Spiralian Phylogeny Places the Enigmatic Arrow Worms among Gnathiferans

              Chaetognaths (arrow worms) are an enigmatic group of marine animals whose phylogenetic position remains elusive, in part because they display a mix of developmental and morphological characters associated with other groups [1, 2]. In particular, it remains unclear whether they are a sister group to protostomes [1, 2], one of the principal animal superclades, or whether they bear a closer relationship with some spiralian phyla [3, 4]. Addressing the phylogenetic position of chaetognaths and refining our understanding of relationships among spiralians are essential to fully comprehend character changes during bilaterian evolution [5]. To tackle these questions, we generated new transcriptomes for ten chaetognath species, compiling an extensive phylogenomic dataset that maximizes data occupancy and taxonomic representation. We employed inference methods that consider rate and compositional heterogeneity across taxa to avoid limitations of earlier analyses [6]. In this way, we greatly improved the resolution of the protostome tree of life. We find that chaetognaths cluster together with rotifers, gnathostomulids, and micrognathozoans within an expanded Gnathifera clade and that this clade is the sister group to other spiralians [7, 8]. Our analysis shows that several previously proposed groupings are likely due to systematic error, and we propose a revised organization of Lophotrochozoa with three main clades: Tetraneuralia (mollusks and entoprocts), Lophophorata (brachiopods, phoronids, and ectoprocts), and a third unnamed clade gathering annelids, nemerteans, and platyhelminthes. Consideration of classical morphological, developmental, and genomic characters in light of this topology indicates secondary loss as a fundamental trend in spiralian evolution.
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                Author and article information

                Journal
                Sci Adv
                Sci Adv
                SciAdv
                advances
                Science Advances
                American Association for the Advancement of Science
                2375-2548
                September 2019
                11 September 2019
                : 5
                : 9
                : eaax5858
                Affiliations
                [1 ]Department of Natural History, Palaeobiology, Royal Ontario Museum, 100 Queen’s Park, Toronto, Ontario M5S 2C6, Canada.
                [2 ]Department of Geology and Geophysics, Yale University, New Haven, CT 06511, USA.
                [3 ]Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, Ontario M5S 3B2, Canada.
                [4 ]Department of Earth Sciences, University of Toronto, Toronto, Ontario M5S 3B1, Canada.
                Author notes
                [* ]Corresponding author. Email: luke.parry@ 123456yale.edu
                [†]

                Present address: Department of Geology and Geophysics, Yale University, New Haven, CT 06511, USA.

                Author information
                http://orcid.org/0000-0002-3910-0346
                http://orcid.org/0000-0002-1670-5502
                Article
                aax5858
                10.1126/sciadv.aax5858
                6739095
                31535028
                c373990f-3491-44c9-9d60-4bfb0f18ec25
                Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

                History
                : 05 April 2019
                : 09 August 2019
                Funding
                Funded by: NSERC;
                Award ID: 341944
                Categories
                Research Article
                Research Articles
                SciAdv r-articles
                Evolutionary Biology
                Paleontology
                Evolutionary Biology
                Custom metadata
                Nielsen Marquez

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