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A Molecular Phylogeny of Raphitomidae

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A Molecular Phylogeny of Raphitomidae Where the snails have no name: a molecular phylogeny of Raphitomidae (Neogastropoda: Conoidea) uncovers vast unexplored diversity in the deep seas of temperate southern and eastern Australia Francesco Criscione, Anders Hallan, Nicolas Puillandre, Alexander Fedosov To cite this version: Francesco Criscione, Anders Hallan, Nicolas Puillandre, Alexander Fedosov. Where the snails have no name: a molecular phylogeny of Raphitomidae (Neogastropoda: Conoidea) uncovers vast unexplored diversity in the deep seas of temperate southern and eastern Australia. Zoological Journal of the Linnean Society, Linnean Society of London, In press, 10.1093/zoolinnean/zlaa088. hal-02970382 HAL Id: hal-02970382 https://hal.archives-ouvertes.fr/hal-02970382 Submitted on 22 Oct 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Where the snails have no name: A molecular phylogeny of the Raphitomidae (Neogastropoda: Conoidea) uncovers vast unexplored diversity in the deep seas of temperate southern and eastern Australia. Francesco Criscione A*, Anders Hallan A, Nicolas Puillandre B, Alexander Fedosov C A - Australian Museum, 1 William Street, Sydney NSW 2010, Australia B - Institut Systématique Evolution Biodiversité (ISYEB), Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles. 57 rue Cuvier, CP 26, 75005 Paris, France C - A.N. Severtsov Institute of Ecology and Evolution of Russian Academy of Sciences, Leninski Prospect 33, Moscow 119071, Russia * Corresponding author: [email protected] Running Head: Molecular phylogeny of SE Australian Raphitomidae Zoological Journal of the Linnean Society Where the snails have no name: A molecular phylogeny of Raphitomidae (Neogastropoda: Conoidea) uncovers vast unexplored diversity in the deep seas of temperate southern and eastern Australia. Journal: Zoological Journal of the Linnean Society ManuscriptFor ID ZOJ-04-2020-4102.R1 Review Only Manuscript Type: Original Article shell characters < Anatomy, comparative anatomy < Anatomy, mtDNA < Keywords: Genetics, convergence < Evolution, endemic < Geography, Taxonomy Although raphitomid snails are a dominant component of gastropod communities in deep seas worldwide, their systematics is still largely tentative. We assembled the most complete sampling of south-eastern Australia Raphitomidae to date. Based on morphological and molecular data from this material, we produced a robust phylogenetic framework and applied it to genus delimitation. Our results for the focus area show a large proportion of undescribed species- and genus-level taxa, eleven of which are formally described herein. We demonstrate that the examination of purely morphological characters rarely suffices for the purpose of accurate genus delimitation. As a result, some traditionally Abstract: highly diverse raphitomid genera (such as Gymnobela) are in fact artificial assemblages of several unrelated, mostly undescribed genus- level lineages. Our data suggests that comparable configurations of shell and radular features, observed at the genus level, commonly do not reflect true phylogenetic relationships. However, our results are inconclusive as to whether homoplasy or conservatism are the drivers of this phenomenon. Accommodating for the inevitable sampling biases, south-eastern Australia appears as a possible hotspot for both raphitomid diversity and endemism, when compared with adjacent areas. Page 1 of 86 Zoological Journal of the Linnean Society 1 2 3 1 Introduction 4 5 6 2 Over a century after the expeditions of the Challenger, Albatross and Siboga (Watson, 1886; 7 8 3 Dall, 1908; Schepman, 1913), deep-sea exploration remains one of the major frontiers for 9 10 11 4 the discovery of marine mollusc biodiversity (Bouchet et al., 2016). 12 13 5 Over the last 35 years, deep-sea expeditions have been conducted across the Indo-Pacific 14 15 16 6 under the Tropical Deep-Sea Benthos (TDSB) programme, led by the Muséum national 17 18 7 d'Histoire naturelle (MNHN) (https://expeditions.mnhn.fr). These expeditions have revealed 19 20 8 a significant molluscan diversity, roughly projected to be in the order of 25-30,000 species 21 For Review Only 22 23 9 for the south Pacific (Bouchet et al., 2008). An estimated 5,000 of these comprise the group 24 25 10 commonly referred to as turriform conoidean gastropods. Turriform Conoidea, or simply 26 27 28 11 ‘turrids’, is a conventional name used for the heterogenous assemblage including all but two 29 30 12 (Conidae and Terebridae) of the 18 currently recognised families in the neogastropod 31 32 33 13 superfamily Conoidea Fleming, 1822 (Bouchet et al., 2009; Abdelkrim et al., 2018a). 34 35 14 Turriform Conoidea is the most diverse group of marine molluscs, with current estimates of 36 37 38 15 354 valid Recent genera and 3776 named Recent species (Horton et al., 2019). Maximum 39 40 16 species diversity within turrids is found in offshore and deep-sea gastropod assemblages 41 42 17 where, however, many species exhibit low abundance (Sysoev, 1997; Kantor et al., 2008; 43 44 45 18 Bouchet et al., 2009). In general, turriform conoideans are characterised by considerable 46 47 19 morphological homoplasy, with numerous cases where distantly related taxa exhibit almost 48 49 50 20 identical shell shape and sculpture (Sysoev, 1997; Kantor et al., 2008; Bouchet et al., 2009). 51 52 21 Because of their high diversity, low abundance and morphological complexity combined, the 53 54 55 22 systematics of deep-sea turriform conoideans below family level remains tentative. Genera 56 57 23 and species are diagnosed primarily based on morphology (e.g. Bouchet & Warén, 1980; 58 59 24 60 Sysoev & Kantor, 1990; Sysoev, 1996a; Sysoev, 1996b; Sysoev, 1997; Bouchet & Sysoev, Zoological Journal of the Linnean Society Page 2 of 86 1 2 3 25 2001; Sysoev & Bouchet, 2001) and comparatively few genetic studies are available (e.g. 4 5 6 26 Puillandre et al., 2009; Puillandre et al., 2010; Fedosov & Puillandre, 2012; Kantor et al. 7 8 27 2012; Kantor et al., 2016; Abdelkrim et al., 2018b; Kantor et al., 2018; Fassio et al. 2019; 9 10 11 28 Hallan et al., 2019). However, such studies have challenged current species delimitations 12 13 29 and highlighted pervasive genus-level paraphyly (e.g. Bouchet & Warén, 1980; Sysoev & 14 15 16 30 Kantor, 1990; Sysoev, 1996a; Sysoev, 1996b; Sysoev, 1997; Bouchet & Sysoev, 2001; Sysoev 17 18 31 & Bouchet, 2001; Puillandre et al., 2010; Kantor et al., 2018). Furthermore, a comparatively 19 20 32 large proportion of deep-sea turriform conoideans still await description. For many areas, 21 For Review Only 22 23 33 the number of undescribed species far outnumbers that of described species. For instance, 24 25 34 it has been estimated that in New Caledonia, about 80% of deep-sea turriform conoideans 26 27 28 35 are undescribed (Bouchet et al., 2008). 29 30 36 The family Raphitomidae Bellardi, 1875 (Bouchet et al., 2011), notably in the deep sea, are 31 32 33 37 among the most poorly studied families of the group (Bouchet et al., 2011). The family 34 35 38 comprises a total of 795 Recent accepted species in 65 Recent accepted genera (source 36 37 38 39 WORMS, Horton et al., 2019). Nearly two-thirds of these genera (39), accounting for more 39 40 40 than half of the overall raphitomid diversity (418 species), are found below the continental 41 42 41 shelf. These figures are based on the notion that bathymetric preferences of turriform 43 44 45 42 conoidean genera are exclusive of either deep- or shallow seas (Bouchet et al., 2009). The 46 47 43 type species of almost half of the deep-sea raphitomid genera were described in the 19th 48 49 50 44 century, with only four named after 2000. No molecular data has accompanied these 51 52 45 descriptions, with anatomical data provided only occasionally (e.g. Sysoev & Kantor, 1986; 53 54 55 46 Sysoev, 1988; Kantor & Sysoev, 1989; Sysoev & Bouchet, 2001). For the vast majority of 56 57 47 these genera, shell features are the only source of taxonomic information accessible from 58 59 48 60 their type species. In addition, descriptions of most deep-sea raphitomids species have been Page 3 of 86 Zoological Journal of the Linnean Society 1 2 3 49 provided in faunistic studies, aiming primarily to present the results of sampling campaigns 4 5 6 50 in a given region and not necessarily to resolve the systematics. Consequently, generic 7 8 51 attributions have been almost exclusively based on shell features and are therefore 9 10 11 52 influenced by problems with character interpretation and undetected homoplasies. This 12 13 53 issue has resulted in the current situation whereby only three genera contain approximately 14 15 16 54 half of all accepted deep-sea raphitomid species. These genera (Pleurotomella Verril, 1872, 17 18 55 100 species; Gymnobela Verril, 1884, 75 and Xanthodaphne Powell, 1942, 33) have 19 20 56 subsequently been colloquially addressed as “dumpsters”, acting as provisional containers 21 For Review Only 22 23 57 for newly described species of problematic generic attribution. For instance, Sysoev & 24 25 58 Bouchet (2001, p. 305) state: “we somewhat arbitrarily include the yoshidai complex of 26 27 28 59 species in Gymnobela”. 29 30 60 Among the consequences of such unresolved systematics is a tentative status of the current 31 32 33 61 biogeography of deep-sea raphitomids. A search of the Global Biodiversity Information 34 35 62 Facility (GBIF - https://www.gbif.org) for the eight most speciose genera (>10 species), 36 37 38 63 reveals that they all occur outside the marine realm for which their type species was 39 40 64 described.
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