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Phylogeny and Systematics of Mitriform Gastropods

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Phylogeny and Systematics of Mitriform Gastropods bs_bs_banner Zoological Journal of the Linnean Society, 2015, 175, 336–359. With 8 figures Phylogeny and systematics of mitriform gastropods Downloaded from https://academic.oup.com/zoolinnean/article-abstract/175/2/336/2449786 by Ifremer, Bibliothèque La Pérouse user on 18 January 2019 (Mollusca: Gastropoda: Neogastropoda) ALEXANDER FEDOSOV1,2*, NICOLAS PUILLANDRE3, YURI KANTOR1,2 and PHILIPPE BOUCHET2 1A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninsky, Prospect 33, Moscow 119071, Russia 2Institut de Systématique, Évolution, Biodiversité ISYEB – UMR 7205 – CNRS, MNHN, UPMC, EPHE, Muséum National d’Histoire Naturelle, Sorbonne Universités, 55 rue Buffon, CP26, F-75005, Paris, France 3Institut de Systématique, Évolution, Biodiversité ISYEB – UMR 7205 – CNRS, MNHN, UPMC, EPHE, Muséum National d’Histoire Naturelle, Sorbonne Universités, 43 rue Cuvier, CP26, F-75005, Paris, France Received 26 January 2015; revised 21 March 2015; accepted for publication 25 March 2015 With about 800 Recent species, ‘miters’ are a widely distributed group of tropical and subtropical gastropods that are most diverse in the Indo-West Pacific. They include the two families Mitridae and Costellariidae, similar in shell morphology and traditionally treated as close relatives. Some genera of deep-water Ptychatractidae and Volutomitridae are close to miters in shell morphology, and the term ‘mitriform gastropods’ has been introduced to refer to Mitridae, Costellariidae, and this assortment of convergent forms. The present study aimed at the re- construction of phylogenetic relationships of mitriform gastropods based on representative taxon sampling. Four genetic markers [cytochrome c oxidase subunit I (COI), 16S and 12S rRNA mitochondrial genes, and H3 (Histone 3) nuclear gene] were sequenced for over 90 species in 20 genera, and the molecular data set was supplemented by studies of radula morphology. Our analysis recovered Mitridae as a monophyletic group, whereas the genus Mitra was found to be polyphyletic. Of 42 mitrid species included in the analysis, 37 formed a well-supported ‘core Mitridae’ consisting of four major clades, three of them consistent with the subfamilies Cylindromitrinae, Imbricariinae, and Mitrinae, and Strigatella paupercula standing out by itself. Basal to the ‘core Mitridae’ are four minor lineages, with the genus Charitodoron recognized as sister group to all other Mitridae. The deep- water family Pyramimitridae shows a sister relationship to the Mitridae, with high support for a Pyramimitridae + Mitridae clade. Our results recover the monophyly of the Costellariidae, which form a well- supported clade that also includes Ptychatractidae, Columbariinae, and Volutomitridae, but not Mitridae. Most derived and diverse amongst Costellariidae are species of Vexillum, characterized by a bow-shaped, multicuspidate rachidian tooth. Several previously unrecognized deep-water costellariid lineages are revealed. Their members retain some plesiomorphies – in particular a tricuspidate rachidian tooth – that makes them morphologically intermedi- ate between ptychatractids and Vexillum. The taxa of Ptychatractidae included in the analysis are not monophyletic, but form three well-supported, unrelated groupings, corresponding respectively to Ceratoxancus + Latiromitra, Exilia, and Exiliodea. None of them shows an affinity to Pseudolividae. © 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 175, 336–359. doi: 10.1111/zoj.12278 ADDITIONAL KEYWORDS: Costellariidae – marine molluscs – Mitra – Mitridae − Ptychatractidae – radula – Vexillum – Volutomitridae. *Corresponding author. E-mail: [email protected] 336 © 2015 The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 175, 336–359 PHYLOGENY OF MITRIFORM GASTROPODS 337 INTRODUCTION 2010; Zou, Li, & Kong, 2011). In fact, the close rela- tionship between Costellariidae and Ptychatractidae Almost one-quarter of the diversity of marine mol- was first suggested by Thiele (1929). However, a com- luscs is represented by the order Neogastropoda. With bination of plesiomorphies in the morphology of more than 12 000 Recent species classified in 40 fami- Ptychatractidae (the simple radula with tricuspidate Downloaded from https://academic.oup.com/zoolinnean/article-abstract/175/2/336/2449786 by Ifremer, Bibliothèque La Pérouse user on 18 January 2019 lies, these predatory and scavenging snails are one rachidian and sickle-shaped laterals; open seminal of the most evolutionary successful taxa of marine mol- groove) justified the later placement of this group in luscs, playing a key role in marine benthic ecosys- the family Turbinellidae (Bouchet & Warén, 1985; tems at all latitudes and depths. However, although Bouchet & Kantor, 2000). A recent morphological study, the superfamilies Conoidea (Puillandre et al., 2008, however, revealed a deep-water member of the family 2011) and Buccinoidea (Hayashi, 2005; Oliverio & Costellariidae that showed a remarkable similarity to Modica, 2010), and the families Muricidae (Barco et al., ptychatractids in foregut anatomy and radula mor- 2010) and Cancellaridae (Modica et al., 2011), have phology (Fedosov & Kantor, 2010); this discovery sup- been specifically targeted by recent molecular ports a close relationship between Costellariidae and phylogenies, a not inconsiderable fraction of the Ptychatractidae, and renders morphological differ- Neogastropoda – including some ancient and diverse ences between the two families quite subtle. With this lineages – has remained essentially outside the sphere background of contradictory morphological and mo- of molecular systematics. One such untouched group lecular data, the relationships of Mitridae, Costellariidae, is the so-called ‘miters’, a name that refers to members and other lineages of mitriform gastropods remain quite of the two families Mitridae and Costellariidae that uncertain and speculative, and require a fresh re- together encompass some 800 species (WoRMS, 2015). evaluation. The purposes of the present study were Miters are widely distributed in tropical and subtropi- to map precisely the phylogeny of mitriform gastro- cal waters and reach their highest diversity in the pods, with an emphasis on the two families of miters, Indo-West Pacific at depths of 0–100 m, where they and to describe their relationships within the form a characteristic element of soft-bottom benthic Neogastropoda. communities. Miter shells have long been popular amongst collectors, and many new species continue to be discovered by amateur taxonomists. Miters usually MATERIAL AND METHODS have high, fusiform shells, with an elongated aper- ture, strong columellar folds, and an adult size mostly TAXON SAMPLING in the 10–50 mm range. Based on this superficial re- The material used in the present study was collected semblance in shell morphology, a number of costellariid in a series of shore-based expeditions and deep- species was originally described under mitrid genera water cruises conducted by Museum National d’Histoire and vice versa. A similar shell is also found in Naturelle (MNHN), Institut de recherche pour le other neogastropod genera, such as Latiromitra Développement (IRD), and Joined Russian Vietnam- (Ptychatractidae) or Microvoluta (Volutomitridae), and ese Tropical Center in the tropical Indo-Pacific, West the term ‘mitriform gastropods’ (Ponder, 1972) infor- Africa, and the Mediterranean (Fig. 1, Table 1). In the mally refers to the miters as well as such miter- field, molluscs were either anaesthetized using mag- resembling forms. nesium chloride (MgCl2), or in some cases shells were The current miters systematics is still largely based drilled, or, in the most recent expeditions, were pro- on the work carried out by Walter Cernohorsky (1966, cessed using a microwave oven (Galindo et al., 2014); 1970, 1976, 1991). However, relationships within both a tissue clip was then cut and fixed in 95% ethanol. these families remain poorly understood, and the Voucher shells, kept intact for identification, have been monophyly of neither Costellariidae, nor Mitridae and deposited in MNHN (Table 1). Taxonomy of the family its subfamilies, has ever been tested. Despite Mitridae Mitridae follows Cernohorsky (1976, 1991), taxono- and Costellariidae having similar shell morphology, their my of the families Costellariidae, Ptychatractidae, and close relationship has been challenged based on radula Volutomitridae is based on several sources as indexed morphology and the anatomy of the digestive tract in World Register of Marine Species (WoRMS, 2015). (Iredale, 1929; Cernohorsky, 1966, 1970; Ponder, 1972; A number of mitriform species in the families Fedosov & Kantor, 2010). What little is available in Ptychatractidae (genera Exilia, Exilioidea, Ceratoxancus, terms of molecular data likewise suggests that the two and Latiromitra), Volutomitridae (genera Volutomitra families are not close relatives: the single mitrid species and Microvoluta), and Turbinellidae (subfamily Vasinae, sequenced so far clustered with the Muricidae and genus Vasum; subfamily Columbariinae, genera Coluzea Olividae, whereas the single costellariid species showed and Fustifusus) were included as putative sister groups a closer affinity to the deep-water families of the family Costellariidae. A suite of species from 17 Ptychatractidae and Volutomitridae (Oliverio & Modica, other neogastropod families in the superfamilies © 2015 The Linnean Society of London, Zoological Journal of
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