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Molecular Data Reveal Cryptic Lineages Within the Northeastern Atlantic And bs_bs_banner Zoological Journal of the Linnean Society, 2013, 169, 389–407. With 4 figures Molecular data reveal cryptic lineages within the northeastern Atlantic and Mediterranean small mussel drills of the Ocinebrina edwardsii complex (Mollusca: Gastropoda: Muricidae) ANDREA BARCO1, ROLAND HOUART2, GIUSEPPE BONOMOLO3, FABIO CROCETTA4 and MARCO OLIVERIO1* 1Department of Biology and Biotechnology ‘C. Darwin’, University of Rome ‘La Sapienza’, Viale dell’Università 32, I-00185 Rome, Italy 2Belgian Royal Institute of Natural Sciences, Rue Vautier, 29, B-1000 Bruxelles, Belgium 3Via delle Terme 12, I-60035 Jesi, Italy 4Stazione Zoologica Anton Dohrn, Villa Comunale, I-80121 Napoli, Italy Received 27 March 2013; revised 2 July 2013; accepted for publication 9 July 2013 We used a molecular phylogenetic approach to investigate species delimitations and diversification in the mussel drills of the Ocinebrina edwardsii complex by means of a combination of nuclear (internal transcribed spacer 2, ITS2) and mitochondrial [cytochrome oxidase subunit I (COI) and 16S] sequences. Our sample included 243 specimens ascribed to seven currently accepted species from 51 sites. Five of the samples were from either the type locality of a nominal species or a close nearby locality (O. edwardsii from Corsica, O. carmelae and O. piantonii from the Kerkennah Islands, O. hispidula from the Gulf of Gabès and O. leukos from the Canary Islands), one from the inferred original locality (O. ingloria from Venice Lagoon), and specimens assigned in the recent literature to O. nicolai. We used a combination of distance- and tree-based species delimitation methods to identify Molecular Operational Taxonomic Units (MOTUs) to compare with the a priori species identifications. The consensus tree obtained by BEAST on the COI alignment allows the recognition of several distinct clades supported by the three species delimitation methods employed. The eight-MOTUs scenario, shared by the Automatic Barcode Gap Discovery (ABGD) and Generalized Mixed Yule-Coalescent (GMYC) methods, comprises the following major clades: clade A contains the south Tunisian species Ocinebrina piantonii Cecalupo, Buzzurro & Mariani from which the sympatric taxon O. carmelae Cecalupo, Buzzurro & Mariani (new synonym) cannot be separated; clades B and C bring together all populations from the Aegean Sea and some from the Ionian Sea, respectively; clade D groups, on the one hand, the south Tunisian samples morphologically assigned to O. hispidula Pallary and, on the other, Atlantic and Alboran Sea samples (including the Canarian taxon O. leukos Houart); clade E includes a sample from the type locality of O. edwardsii and several samples from the Tyrrhenian Sea; clades F and G correspond to a few samples from the Venice Lagoon and the Tyrrhenian Sea, respectively; clade H groups the bulk of samples from the Adriatic Sea, including samples from the Venice Lagoon morphologically identified as Ocinebrina ingloria (Crosse), and some from the Ionian Sea. No final conclusions could be reached to reconcile the currently recognized morphological taxa with the clades suggested by the COI data. The geographical structure proposed by the mitochondrial markers is similar to that found in other marine invertebrates and partially corresponds to the species defined by shell characters. We propose here a framework for the revision of the Ocinebrina edwardsii species complex, suggesting a geographical pattern for the diversification of this group in the studied area. © 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 169, 389–407. doi: 10.1111/zoj.12069 ADDITIONAL KEYWORDS: ABGD – cytochrome oxidase I – DNA-barcoding – GMYC – Mediterranean Sea – species delimitation. *Corresponding author. E-mail: [email protected] © 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 169, 389–407 389 390 A. BARCO ET AL. INTRODUCTION by Crocetta et al. (2012), includes O. aciculata (Lamarck, 1822), O. corallinoides Pallary, 1912 The existence of sibling species among marine and O. reinai Bonomolo and Crocetta, 2012. The invertebrates is a widely recognized phenomenon O. edwardsii complex includes the following species: (Knowlton, 1993), emphasized by the increasing use O. edwardsii (Payraudeau, 1826), O. carmelae of DNA-based methods for species delimitation Cecalupo, Buzzurro & Mariani, 2008, O. helleri (Vogler & Monaghan, 2007). These techniques are (Brusina, 1865), O. hispidula Pallary, 1904, contributing to the steady number of new marine O. hybrida (Aradas & Benoît, 1876), O. ingloria species described (Costello, Wilson & Houlding, 2012), (Crosse, 1865), O. inordinata (Houart & Abreu, 1994), allowing the recognition of unknown diversity (Caron O. leukos Houart, 2000, O. miscowichae Pallary, 1920, et al., 2012) and testing the status of known species O. nicolai Monterosato 1884, O. paddeui Bonomolo & (Templeton, 2001). Buzzurro, 2006, O. piantonii Cecalupo, Buzzurro & Cryptic diversity, however, does not surface exclu- Mariani, 2008 and O. purpuroidea Pallary, 1920 (see sively in poorly known lineages (Richards et al., 2012) Table 2 for a state of the art nomenclature). or in organisms from relatively unexplored areas Ocinebrina edwardsii is traditionally considered to (Goetze, 2003). Even within the well-known fauna of be a common species and one of the most variable the Mediterranean Sea, with its long-lasting tradition European muricids, as witnessed also by the exist- of taxonomic studies, many species have turned out to ence of numerous names established for the various be complexes of sibling lineages (Boisselier-Dubayle & morphotypes (see Table 2), whose status has been Gofas, 1999; Carreras-Carbonell, Macpherson & debated extensively (see, for example, Houart, 2001). Pascual, 2005; Calvo et al., 2009; Sá-Pinto et al., 2010; Its distribution spans the entire Mediterranean Sea Xavier et al., 2011). Molluscan taxonomy, in particu- and, in the Atlantic Ocean, it is recorded up to the lar, historically has been almost entirely based on Bay of Biscay and to the Canary Islands. The shell shell characters, which are still commonly used even reaches (and sometimes exceeds) 20 mm in length though morphological variation caused by adaptation with up to 5–5.5 teleoconch whorls, has a sealed to environmental pressures has been documented siphonal canal, five to six small denticles on the (Vermeij, 1978). Consequently, traditional shell-based internal part of the outer lip and variable coloration. taxonomic practice has proved to be problematic The protoconch is paucispiral (1.25–1.75 whorls) for molluscs, and particularly for morphologically and its morphology is similar to that of O. aciculata. diverse groups. Therefore, in several of the most Therefore, a development similar to that described for recent studies on marine molluscs, the combination of O. aciculata by Franc (1940) can be assumed, i.e. molecular and traditional approaches has proven to entirely intracapsular or with a very short pelagic be successful to resolve taxonomically doubtful groups phase. (e.g. Puillandre et al., 2009; Claremont et al., 2011; The combination of the high morphological variabil- Zou, Li & Kong, 2012). ity of the shell among and within species over a wide The genus Ocinebrina Jousseaume, 1880 is widely geographical range (see Supporting Information distributed in the Mediterranean Sea, northeastern Figs S4-S6) has contributed to the confused taxonomy Atlantic and northeastern Pacific, with species com- in the O. edwardsii complex. Here, we have applied monly called small mussel drills. It includes 23 cur- DNA-based methods to a sample including 243 speci- rently accepted living species: 16 in the northeastern mens from the northeastern Atlantic and the Medi- Atlantic and Mediterranean and seven in the north- terranean Sea (including the area of the type locality eastern Pacific (WoRMS: Appeltans et al., 2012, at of Purpura edwardsii, Corsica) in order to define the http://www.marinespecies.org – accessed on 13 March limits of this species and check for the presence 2013). The Pacific species are often attributed to other of cryptic lineages. We also included specimens mor- genera, such as Ocenebra Gray, 1847 and Urosalpinx phologically ascribed to some of the nominal species Stimpson, 1865 (two of the c. 29 genera in the of the same complex to investigate their relation- subfamily Ocenebrinae Cossmann, 1903: see, for ships with O. edwardsii: O. ingloria from the Venice example, Radwin & D’Attilio, 1976; Vermeij & Vokes, Lagoon, O. hispidula from the Gulf of Gabès, 1997; but see WoRMS – accessed on 13 March 2013 – O. carmelae and O. piantonii from the Kerkennah for an updated listing), and their relationships will be Islands, O. leukos from the Canary Islands and dealt with in an ongoing study on the phylogenetics of O. miscowichae from southern Morocco. In addition, the Ocenebrinae Cossmann, 1903. The northeastern we also processed specimens assigned in the recent Atlantic and Mediterranean species are traditionally literature to O. cf. nicolai and O. nicolai from Spain divided into two groups of morphological affinities: and Portugal (Rolán, 1983; Afonso et al., 2011; Gofas, the O. aciculata complex and the O. edwardsii 2011), although their morphology was not perfectly complex. The O. aciculata complex, recently revised matching that of the nominal taxon. Using three © 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 169, 389–407 CRYPTIC
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