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Across the Antarctic Polar Front C.A Contrasting biogeographical patterns in Margarella (Gastropoda: Calliostomatidae: Margarellinae) across the Antarctic Polar Front C.A. González-Wevar, N.I. Segovia, S. Rosenfeld, Dominikus Noll, C.S. Maturana, M. Hüne, J. Naretto, K. Gérard, A. Díaz, H.G. Spencer, et al. To cite this version: C.A. González-Wevar, N.I. Segovia, S. Rosenfeld, Dominikus Noll, C.S. Maturana, et al.. Contrast- ing biogeographical patterns in Margarella (Gastropoda: Calliostomatidae: Margarellinae) across the Antarctic Polar Front. Molecular Phylogenetics and Evolution, Elsevier, 2021, 156, pp.107039. 10.1016/j.ympev.2020.107039. hal-03102696 HAL Id: hal-03102696 https://hal.archives-ouvertes.fr/hal-03102696 Submitted on 7 Jan 2021 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. Molecular Phylogenetics and Evolution (2021) 156: 107039. DOI: 10.1016/j.ympev.2020.107039 Contrasting biogeographical patterns in Margarella (Gastropoda: Calliostomatidae: Margarellinae) across the Antarctic Polar Front C.A. González-Wevar a, b,c, N.I. Segovia b, S. Rosenfeld b,d, D. Noll b, C.S. Maturana b, M. Hüne b, J. Naretto , K. Gerard´ , A.d Díaz , eH.G. Spencer , fT. Saucède , J.-P.g Féral´ , S.A. hMorley , i P. Bricklej , N.G. Wilsonk,l , E. Poulin b a Instituto de Ciencias Marinas y Limnol´ogicas (ICML), Facultad de Ciencias, Universidad Austral de Chile, Casilla 567, Valdivia, Chile b Instituto Milenio de Ecología y Biodiversidad (IEB), Las Palmeras 3425, ~Nu~noa, Santiago, Chile c Centro FONDAP de Investigaci´on en Din´amica de Ecosistemas Marinos de Altas Latitudes (IDEAL), Universidad Austral de Chile, Casilla 567, Valdivia, Chile d Laboratorio de Ecosistemas Marinos Ant´articos y Subant´articos, Universidad de Magallanes, Chile e Departamento de Zoología, Universidad de Concepci´on, Barrio Universitario s/n, Concepci´on, Chile f Department of Zoology, University of Otago, Dunedin, New Zealand g Biog´eosciences, UMR CNRS 6282, Universit´e de Bourgogne, 6, boulevard Gabriel, 21000, Dijon, France h AMU/CNRS/IRD/AU-IMBE-Institut M´editerran´een de Biodiversit´e et d’Ecologie marine et continentale, UMR 7263, Station Marine d’Endoume, Chemin de la Batterie des Lions, 13007 Marseille, France i British Antarctic Survey (BAS), Natural Environment Research Council. Madingley Road, High Cross, Cambridge CB30ET, UK j South Atlantic Environmental Research Institute (SAERI), PO Box 609, Stanley Cottage, Stanley, Falkland Islands, UK k Collections & Research, Western Australian Museum, 49 Kew St, Welshpool 6106, Perth, WA, Australia l University of Western Australia, 35 Stirling Highway, Crawley 6009, WA, Australia ABSTRACT Members of the trochoidean genus Margarella (Calliostomatidae) are broadly distributed across Antarctic and sub-Antarctic ecosystems. Here we used novel mitochondrial and nuclear gene sequences to clarify species boundaries and phylogenetic relationships among seven nominal species distributed on either side of the Ant-arctic Polar Front (APF). Molecular reconstructions and species-delimitation analyses recognized only four species: M. antarctica (the Antarctic Peninsula), M. achilles (endemic to South Georgia), M. steineni (South Georgia and Crozet Island) and the morphologically variable M. violacea (=M. expansa, M. porcellana and M. pruinosa), with populations in southern South America, the Falkland/Malvinas, Crozet and Kerguelen Islands. Margarella violacea and M. achilles are sister species, closely related to M. steineni, with M. antarctica sister to all these. This taxonomy reflects contrasting biogeographic patterns on either side of the APF in the Southern Ocean. Pop-ulations of Margarella north of the APF (M. violacea) showed significant genetic variation but with many shared haplotypes between geographically distant populations. By contrast, populations south of the APF (M. antarctica, M. steineni and M. achilles) exhibited fewer haplotypes and comprised three distinct species, each occurring across a separate geographical range. We hypothesize that the biogeographical differences may be the consequence of the presence north of the APF of buoyant kelps – potential long- distance dispersal vectors for these vetigastro-pods with benthic-protected development – and their near-absence to the south. Finally, we suggest that the low levels of genetic diversity within higher-latitude Margarella reflect the impact of Quaternary glacial cycles that exterminated local populations during their maxima. Keywords: Southern Ocean Antarctic Polar Front Long-distance dispersal Benthic-protected development Rafting Margarella 1. Introduction hard substrate inter- and shallow sub-tidal shores (Zelaya, 2004). Near- shore species of the genus are frequently found in ecosystems The genus Margarella Thiele, 1893 includes Antarctic and sub- dominated by macroalgae, on which they are commonly found grazing Antarctic small to medium-sized vetigastropods that are abundant on (Adami and Gordillo, 1999; Rosenfeld et al., 2011, 2017; Amsler et al., 2015). However, some species are restricted to deeper waters between 40 and development where free-crawling juveniles emerge from mature egg 1080 m (Hain, 1990). capsules (Picken, 1979; Zelaya, 2004; Rosenfeld et al., 2011). This key The taxonomy of Margarella has had a confused history and even life-history trait seems to have played a significant role in the biogeog- currently, specific identifications and relationships among Magellanic raphy of several marine groups by enhancing their respective and Antarctic species are poorly understood (Forcelli, 2000; Powell, speciation potential (Poulin and F´eral, 1996; Pearse et al., 2009; 1951; Williams, 2012a; Williams et al., 2010; Zelaya, 2004). Several Thatje, 2012). At the same time, the ecological association of some species were originally described in the genus Margarita Leach, 1819 species with buoyant macroalgae gives them a high potential for (not Leach, 1814) (=Margarites Gray, 1847), a group restricted to the rafting, which may explain their wide distributions across different Northern Hemisphere that is now placed in a separate family, Margar- sub-Antarctic provinces, in spite of their low dispersive potential itidae Thiele, 1924. Zelaya (2004), in a detailed morphological (Helmuth et al., 1994; Nikula et al., 2010; Cumming et al., 2014; revision of the group, confirmed that Antarctic, South American and Moon et al., 2017; Gonz´alez-Wevar et al., 2018). Other species, South Georgian species, previously identified as Margarites, should be lacking such associations are more narrowly distributed and indeed, placed in Margarella. More recently, Williams et al. (2010) used molecular comparisons might detect a series of unrecognized cryptic multilocus phy-logenies to show that Margarella antarctica (Strebel, species across the Southern Ocean, as has been the case in other 1908) was a cal-liostomatid. Moreover, Williams (2012a) confirmed groups of marine invertebrates (Hunter and Halanych, 2008; Leese et this placement for four further species and, in recognition, Williams al., 2008; Wilson et al., 2009; Janosik et al., 2011; Gonz´alez-Wevar et (2012b) established the new subfamily Margarellinae. Conversely, al., Here,2019). we present a molecular-genetic study of seven nominal several species from New Zealand, previously assigned to Margarella species collected at high-latitude Margarella populations from the have proved to belong to the genus Cantharidus Montfort, 1810 Antarctic Peninsula, southern South America, the Falkland/Malvinas (Trochidae: Cantharidinae) (Williams et al., 2010; Williams, 2012b; Islands, South Georgia, Crozet and Kerguelen Islands. We carried out Donald and Spencer, 2016), within a distinct clade, the subgenus phyloge-netic reconstructions based on mitochondrial and nuclear Pseudomargarella Donald and Spencer (2016). markers, species delimitation analyses, mitochondrial divergence-time The World Register of Marine Species database (http://www. estima-tions, as well as population-based analyses. Through the marinespecies.org) records 18 Margarella species distributed in Antarc- integration of these methodologies and the first molecular tic and sub-Antarctic areas. Five – M. antarctica, M. refulgens (E.A. investigation of the type species (M. expansa), we aim to further Smith, 1907) M. whiteana Linse, 2002, M. gunnerusensis Numanami, understand evolutionary re-lationships within Margarella in the 1996 and M. crebrilirulata (E.A. Smith, 1907) – occur around the Southern Ocean. Moreover, we elucidate the distribution of lineages of Antarctic Peninsula, the Ross Sea and East Antarctica. Three species this higher latitude calliosto-matid genus, as well as the taxonomic are recog-nized along southern South America – M. expansa (Sowerby, status of the various populations. Understanding these specific issues 1838), M. violacea (King, 1832) and M. pruinosa (Rochebrune and in Margarella provides new insights about the biogeography and Mabille, 1885) – and their shells differ primarily in external coloration evolution of the near-shore marine benthic biota in this important
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