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Download (2MB) Molecular Phylogenetics and Evolution 158 (2021) 107081 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Eight new mitogenomes clarify the phylogenetic relationships of Stromboidea within the caenogastropod phylogenetic framework Alison R. Irwin a,b,*, Ellen E. Strong c, Yasunori Kano d, Elizabeth M. Harper e, Suzanne T. Williams a a Department of Life Sciences, Natural History Museum, Cromwell Rd, London SW7 5BD, United Kingdom b School of Biological Sciences, University of Bristol, 24 Tyndall Ave, Bristol BS8 1TQ, United Kingdom c Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, 10th St. & Constitution Ave. NW, Washington, D.C. 20560, United States d Department of Marine Ecosystems Dynamics, Atmosphere and Ocean Research Institute, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan e Department of Earth Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EQ, United Kingdom ARTICLE INFO ABSTRACT Keywords: Members of the gastropod superfamily Stromboidea (Littorinimorpha) are characterised by their elaborate shell Stromboidea morphologies, distinctive mode of locomotion, and often large and colourful eyes. This iconic group comprises Strombidae over 130 species, including many large and charismatic species. The family Strombidae is of particular interest, Xenophoroidea largely due to its commercial importance and wide distribution in tropical and subtropical waters. Although a Mitochondrial genome few strombid mitochondrial genomes have been sequenced, data for the other four Recent families in Strom­ Systematics Phylogenetics boidea are lacking. In this study we report seven new stromboid mitogenomes obtained from transcriptomic and genomic data, with taxonomic representation from each Recent stromboid family, including the first mitoge­ nomes for Aporrhaidae, Rostellariidae, Seraphsidae and Struthiolariidae. We also report a new mitogenome for the family Xenophoridae. We use these data, along with published sequences, to investigate the relationships among these and other caenogastropod groups. All analyses undertaken in this study support monophyly of Stromboidea as redefined here to include Xenophoridae, a finding consistent with morphological and behav­ ioural data. Consistent with previous morphological and molecular analyses, including those based on mitoge­ nomes, monophyly of Hypsogastropoda is confirmed but monophyly of Littorinimorpha is again rejected. 1. Introduction n/im/2007-36711). By comparison, the other four stromboidean fam­ ilies are represented in the Recent fauna by only a handful of species The superfamily Stromboidea is a highly diverse group within the with restricted distributions, although fossil records show they were largest and most successful clade of living gastropods, the Caenogas­ more diverse and geographically widespread until the end-Cretaceous tropoda (Bouchet and Rocroi, 2005; Bouchet et al., 2017). Stromboidea (K/Pg) mass extinction (Morton, 1951; Roy, 1996; Nielsen, 2005). is currently understood to comprise five Recent families: Aporrhaidae, Despite their diverse shell morphologies (Savazzi, 1991), extensive fossil Rostellariidae, Seraphsidae, Strombidae and Struthiolariidae (Bouchet record (Roy, 1996), and recognition as a commercially important group et al., 2017). By far the largest of these is the family Strombidae, which is (within the shell trade and fishing industry; Aiken et al., 2006; Dias widespread in tropical and subtropical seas, and comprises more than 90 et al., 2011; Stoner et al., 2019), strombids have been the focus of few species currently considered valid (Abbott, 1960, 1961; Kreipl and morphological or molecular systematic studies (Stone, 2001; Simone, Poppe, 1999; Liverani, 2013; WoRMS, 2020). Strombids inhabit mostly 2005; Latiolais et al., 2006; Maxwell et al., 2020). shallow waters, but some have been found in deeper habitats; for Extreme differences in shell morphology exist among stromboid example, Dolomena labiosa has been collected at depths in excess of 780 families (Savazzi, 1991; Bandel, 2007), yet equally striking is the vari­ m (MNHN IM-2007-36711; http://coldb.mnhn.fr/catalognumber/mnh ation in eye morphology. Rostellariidae, Seraphsidae, and Strombidae * Corresponding author at: Department of Life Sciences, Natural History Museum, Cromwell Rd, London SW7 5BD, United Kingdom. E-mail addresses: [email protected] (A.R. Irwin), [email protected] (E.E. Strong), [email protected] (Y. Kano), [email protected] (E.M. Harper), s. [email protected] (S.T. Williams). https://doi.org/10.1016/j.ympev.2021.107081 Received 5 October 2020; Received in revised form 18 December 2020; Accepted 12 January 2021 Available online 20 January 2021 1055-7903/Crown Copyright © 2021 Published by Elsevier Inc. All rights reserved. A.R. Irwin et al. Molecular Phylogenetics and Evolution 158 (2021) 107081 possess large and colourful camera-type eyes (which probably impart genome skimming). Type species were used for Strombidae and Stru­ excellent vision; Seyer, 1994) on the ends of long, mobile eyestalks thiolariidae; (Strombus pugilis and Struthiolaria papulosa; Table 1); how­ (ommatophores), and are characterised by a u-shaped “stromboid ever, appropriately preserved specimens of type species were not notch” near the anterior end of the shell outer lip which accommodates available for the other families. Therefore, specimens were chosen from the right ommatophore (Woodward, 1894; D.P. Abbott, 1962; Berg, the type genus (Aporrhais serresiana, Aporrhaidae; Xenophora japonica, 1974; Simone, 2005). By contrast, Aporrhaidae and Struthiolariidae Xenophoridae), or in Rostellariidae, where samples were limited, the have small, darkly pigmented eyes near the base of cephalic tentacles, species with the highest quality extracted DNA (Varicospira cancellata; and no stromboid notch (Simone, 2005). Despite this diversity, the Table 1). The type genus of Seraphsidae, Seraphs, is extinct, however the incorporation of these five families within Stromboidea is widely name Seraphsidae was introduced by Jung (1974) as a replacement for accepted due to a number of unreversed synapomorphies, including a the name Terebellidae (Bouchet and Rocroi, 2005; Bouchet et al., 2017) foot with a sub-terminal, projecting operculum (Woodward, 1894; so we used the type species of Terebellum (Terebellum terebellum) to Simone, 2005). represent the family (Table 1). Complete mitogenomes were also From cladistic analysis of morphological characters, Simone (2005) assembled from the transcriptomes of two additional strombid species also assigned Xenophoridae to Stromboidea, a decision not widely which have been sequenced for another project: Ministrombus variabilis accepted; Xenophoridae is currently assigned to a separate superfamily, (formerly Dolomena variabilis; Bandel, 2007; Dekkers and Maxwell, Xenophoroidea (WoRMS, 2020). The systematic relationship between 2020), and Tridentarius dentatus (Table 1). Stromboidea and Xenophoridae has long been problematic, with the latter variably included in Xenophoroidea (Boss, 1982; Ponder, 1983; 2.2. DNA extractions Ponder and De Keyzer, 1998; Bouchet et al., 2005, 2017; Ponder et al., 2020), Stromboidea (Wenz, 1940; Berg, 1974, 1975; Kiel and Perrilliat, Tissue samples taken from the foot were cut into small pieces and 2001; Simone, 2005, 2011; Kronenberg and Wieneke, 2020; also DNA was extracted according to the manufacturer’s instructions for the tentatively by Bandel, 2007), or Calyptraeoidea (Morton, 1958; Ponder, E.Z.N.A.® Mollusc DNA extraction kit (Omega Bio-tek; Terebellum ter­ 1983). Stromboidea differ from the Xenophoroidea principally in the ebellum, Strombus pugilis, Xenophora japonica and Struthiolaria papulosa), fusiform shell shape (as opposed to the flattened, conical xenophorid or High Pure PCR Template Preparation kit (Roche; Aporrhais serresiana shell, which is arbitrarily termed ‘trochiform’) and in the presence of a and Varicospira cancellata), with the minor modifications that tissue ◦ siphonal canal extending from the anterior edge of the aperture (Ponder samples in proteinase K and tissue lysis buffer were incubated at 50 C and De Keyzer, 1998; Simone, 2005). Nevertheless, all studies suggest a overnight whilst rotated at 15 rpm. DNA was quantified with a Nano­ close relationship between Stromboidea and Xenophoroidea, which Drop™ 8000 spectrophotometer (Thermo Fisher Scientific),and further were united by Ponder et al. (2020) in the Strombida, and the two su­ purifiedwhen necessary by precipitation with absolute ethanol and 3 M perfamilies share numerous morphological characters, including the sodium acetate. Final DNA concentrations were within the range projecting operculum (Simone, 2005). However, to date, neither 14.3–41.7 ng/mL. morphological nor molecular phylogenetic analyses have fully tested the relationship between these two superfamilies, or among the currently 2.3. RNA extractions recognised stromboid families. Both Stromboidea and Xenophoroidea belong to the gastropod group Transcriptomic data were obtained from RNA extracted from Hypsogastropoda, which includes all living caenogastropods other than strombid eyes (Ministrombus variabilis and Tridentarius dentatus) using Architaenioglossa and Cerithioidea (Bouchet et al., 2017; Ponder et al., the E.Z.N.A.® Mollusc RNA Kit protocol (Omega Bio-tek) following the 2020). Within the hypsogastropods, these two superfamilies are
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