Revisiting the Lepetodrilus elevatus species complex (Vetigastropoda: Lepetodrilidae), using samples from the Galápagos and Guaymas hydrothermal vent systems Marjolaine Matabos, Didier Jollivet To cite this version: Marjolaine Matabos, Didier Jollivet. Revisiting the Lepetodrilus elevatus species complex (Vetigas- tropoda: Lepetodrilidae), using samples from the Galápagos and Guaymas hydrothermal vent systems. Journal of Molluscan Studies, Oxford University Press (OUP), 2019, 85 (1), pp.154-165. 10.1093/mol- lus/eyy061. hal-02354593 HAL Id: hal-02354593 https://hal.archives-ouvertes.fr/hal-02354593 Submitted on 7 Nov 2019 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. 1 Revisiting the Lepetodrilus elevatus species complex (Vetigastropoda: 2 Lepetodrilidae), using samples from the Galápagos and Guaymas 3 hydrothermal vent systems 4 Marjolaine Matabos1 and Didier Jollivet2 5 6 1IFREMER, Centre de Bretagne, REM/EEP, Laboratoire Environnement Profond, 7 29280 Plouzané, France; and 8 2Sorbonne Université, UPMC Univ. Paris 06, CNRS UMR 7144, Adaptation et 9 Diversité en Milieu Marin, Equipe ABICE, Station Biologique de Roscoff, 29688 10 Roscoff, France 11 Correspondence: M. Matabos; e-mail: [email protected] 12 (Received 7 June 2018 ; editorial decision 9 November 2018) 13 Running head: LEPETODRILUS ELEVATUS SPECIES COMPLEX 14 15 1 16 ABSTRACT 17 The current distribution ranges of vent species result from the complex tectonic history 18 of oceanic ridges. A growing number of DNA barcode studies report the presence of 19 cryptic species across geological discontinuities that offset ridge systems and have 20 gradually helped to draw a more precise picture of the historical migration pathways of 21 vent fauna. We reexamined the phylogeny of species within the Lepetodrilus elevatus 22 complex along the East Pacific Rise (EPR) ridge system in the light of new samples 23 from the Galápagos Rift and the Guaymas Basin. Our analyses of mitochondrial 24 cytochrome c oxidase subunit I gene sequences, coupled with morphological data, 25 highlight the occurrence of a distinct lineage along the Galápagos Rift and offer new 26 insight into the current distribution range of this species complex. Due to the absence of 27 clear morphological diagnostic criteria and the potential overlap of these lineages at key 28 locations, we recommend reassigning the taxon L. galriftensis to the subspecies level 29 and maintaining the name L. elevatus for all clades along the EPR/Galápagos Rift 30 system. 31 2 32 INTRODUCTION 33 Biodiversity conservation represents the most challenging issue for scientists and policy 34 makers today, therefore determining current species’ ranges is of utmost importance 35 (Hendry et al., 2010). Understanding hydrothermal vent biogeography is, however, 36 often hindered by the lack of samples at key areas along ridge systems. The growing 37 literature on vent phylogeography reveals a complex history of lineages at hydrothermal 38 vents, where the constant reorganization of ridges and geodynamics affect gene flow 39 over time (Vrijenhoek, 1997; Jollivet, Chevaldonné & Planque, 1999). Continuous 40 changes in ocean floor geomorphology, such as ridge reorganization/fossilization 41 (Mammerickx & Klitgord, 1982), or their subduction under volcanic arcs or continental 42 plates (Tunnicliffe & Fowler, 1996), make identifying biogeographical patterns 43 difficult, simply because species’ ranges evolve with the creation and subsequent 44 removal of physical barriers to gene flow (Plouviez et al., 2013). The present 45 distribution of vent fauna is a result of these historical events, modulated by the life- 46 history traits of each species, which determine the potential for colonization of more or 47 less distant territories through larval dispersal (Marsh et al., 2001; Mullineaux et al., 48 2002, 2010; McGillicuddy et al., 2010). In addition, geographical distances between 49 neighboring vents and habitat density mainly depend on the ridge spreading rate 50 (Hannington et al., 1995) and the convection of heat, according to the oscillations of the 51 magmatic chamber beneath the ridge (Watremez & Kervevan, 1990). Hydrothermal 52 fluid circulation, directly determined by magmatic and tectonic activity, controls the 53 rate of appearance and disappearance of vent sites (Vrijenhoek, 1997; Jollivet et al., 54 1999). These local dynamics influence the temporal dynamics in communities through 55 ecological succession patterns (Shank et al., 1998; Marcus, Tunnicliffe & Butterfield, 56 2009). In highly unstable portions of ridges (i.e. segments with the highest accretionary 3 57 rates), vent communities rarely reach the climax state. Thus, position in the ecological 58 succession order (i.e. early, mid and late successional colonizers) strongly influences 59 species’ distributions. It also influences the number and size of populations, and 60 therefore the effective population size (number of reproductive adults) of species and 61 the number of offspring able to colonize new sites (Vrijenhoek, 2010). 62 There is a need for knowledge on biodiversity and distribution of vent species, 63 in order to describe and understand biogeographical patterns and the history of vent 64 colonization. Over the last decade, a growing number of DNA-barcoding studies have 65 reported the presence of well-separated cryptic species across physical geological 66 discontinuities that offset ridge systems, particularly along the well-studied East Pacific 67 Rise (EPR) (Johnson et al., 2008; Plouviez et al., 2009; Matabos et al., 2011) or in the 68 northeastern Pacific Ocean on both sides of the Blanco Transform Fault Zone (Johnson 69 et al., 2006). The occurrence of cryptic species able to migrate over great distances and 70 hybridize at some locations, impedes our ability to define clear-cut biogeographical 71 provinces along the EPR (Matabos et al., 2011). Species’ distributions along the EPR 72 are thus far from being understood and clarifying them may change our perception of 73 East Pacific biogeography. 74 Based on biogeographical studies using species presence/absence, the EPR was 75 originally considered as a single biogeographical province (Tunnicliffe, 1988; 76 Tunnicliffe & Fowler, 1996; Bachraty, Legendre & Desbruyères, 2009). However, 77 Matabos et al. (2011) recently demonstrated that the southern EPR represents a 78 transition zone between the northern EPR and the Pacific-Antarctic Ridge, where 79 several physical barriers prevent larval dispersal and promote species partitioning. In 80 this specific context, tectonic events, creating physical barriers such as transform faults 4 81 or the Easter/Bauer microplates, may have played a crucial role in the allopatric 82 isolation of species. A large number of taxa, including gastropods, polychaetes and 83 bivalves, indeed display population divergence on either side of the Equator and/or the 84 Easter microplate, generating cryptic species complexes along the 5000 km of the EPR 85 (Won et al., 2003; Hurtado, Lutz & Vrijenhoek, 2004; Matabos et al., 2008; Plouviez et 86 al., 2009). Several geological events related to the major reorganization and re- 87 orientation of the EPR over the last 20 Myr likely coincided with the timing of the 88 estimated genetic divergences. Population divergences in the majority of taxa likely 89 occurred during two distinct events about 11 and 1.3 Ma, respectively (Plouviez et al., 90 2009), corresponding to the rotation of the Bauer microplate, the reorganization of the 91 Mathematician Ridge (for the older date) and the setting up of the most pronounced 92 transform faults that offset the ridge between 9°50'N and 7°25'S (for the more recent 93 date). Estimations of divergence dates (0.7 to 3.5 Ma) from a multilocus approach also 94 indicate that part of the observed genetic divergences between the southern and northern 95 populations of the vent mussel Bathymodiolus thermophilus at the Equator may derive 96 from the formation of the Easter microplate, about 3 to 5 Ma, via allele introgression 97 through this older, but semipermeable barrier (Plouviez et al., 2013). 98 Among taxa exhibiting cryptic species, the Lepetodrilus elevatus species 99 complex is one of the most genetically diversified, with at least three distinct genetic 100 units emerging from the ridge-system reorganization. Species in this complex, similar to 101 all species of Lepetodrilus, possess planktonic, presumably lecithotrophic, larvae (Berg, 102 1985; Tyler et al., 2008). As originally described, Lepetodrilus elevatus contained two 103 morphologically distinct subspecies: L. e. elevatus from the EPR and L. e. galriftensis 104 from the Galapagos Rift (McLean, 1988). These limpets are very abundant on the tubes 105 of the tubeworm Riftia pachyptila and on mussel shells, along the EPR and the 5 106 Galápagos Rift. On the EPR, the species is composed of at least two cryptic lineages 107 between 21°N and 21°S, which co-occur at 9°50'N where they are likely to hybridize 108 (Matabos et al., 2008). This population