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The Phylogenetic Position and Taxonomic Status of Sterechinus Bernasconiae Larrain, 1975 (Echinodermata, Echinoidea), an Enigmatic Chilean Sea Urchin

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The Phylogenetic Position and Taxonomic Status of Sterechinus Bernasconiae Larrain, 1975 (Echinodermata, Echinoidea), an Enigmatic Chilean Sea Urchin The phylogenetic position and taxonomic status of Sterechinus bernasconiae Larrain, 1975 (Echinodermata, Echinoidea), an enigmatic Chilean sea urchin Thomas Saucède, Angie Díaz, Benjamin Pierrat, Javier Sellanes, Bruno David, Jean-Pierre Féral & Elie Poulin Polar Biology ISSN 0722-4060 Volume 38 Number 8 Polar Biol (2015) 38:1223-1237 DOI 10.1007/s00300-015-1689-9 1 23 Your article is protected by copyright and all rights are held exclusively by Springer- Verlag Berlin Heidelberg. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Polar Biol (2015) 38:1223–1237 DOI 10.1007/s00300-015-1689-9 ORIGINAL PAPER The phylogenetic position and taxonomic status of Sterechinus bernasconiae Larrain, 1975 (Echinodermata, Echinoidea), an enigmatic Chilean sea urchin 1 2,3 1 4 Thomas Sauce`de • Angie Dı´az • Benjamin Pierrat • Javier Sellanes • 1 5 3 Bruno David • Jean-Pierre Fe´ral • Elie Poulin Received: 17 September 2014 / Revised: 28 March 2015 / Accepted: 31 March 2015 / Published online: 5 May 2015 Ó Springer-Verlag Berlin Heidelberg 2015 Abstract Sterechinus is a very common echinoid genus subclade and a subclade composed of other Sterechinus in benthic communities of the Southern Ocean. It is widely species. The three nominal species Sterechinus antarcticus, distributed across the Antarctic and South Atlantic Oceans Sterechinus diadema, and Sterechinus agassizi cluster to- and has been the most frequently collected and intensively gether and cannot be distinguished. The species Ster- studied Antarctic echinoid. Despite the abundant literature echinus dentifer is weakly differentiated from these three devoted to Sterechinus, few studies have questioned the nominal species. The elucidation of phylogenetic rela- systematics of the genus. Sterechinus bernasconiae is the tionships between G. multidentatus and species of Ster- only species of Sterechinus reported from the Pacific echinus also allows for clarification of respective Ocean and is only known from the few specimens of the biogeographic distributions and emphasizes the putative original material. Based on new material collected during role played by biotic exclusion in the spatial distribution of the oceanographic cruise INSPIRE on board the R/V species. Melville, the taxonomy and phylogenetic position of the species are revised. Molecular and morphological analyses Keywords Sterechinus bernasconiae Á Gracilechinus show that S. bernasconiae is a subjective junior synonym multidentatus Á Echinoidea Á Antarctic Á Phylogeny Á of Gracilechinus multidentatus (Clark). Results also show Biogeography the existence of two genetically distinct subclades within the so-called Sterechinus clade: a Sterechinus neumayeri Introduction & Thomas Sauce`de For more than a century, species of the genus Sterechinus [email protected] have been among the most frequently collected and com- 1 UMR CNRS 6282 Bioge´osciences, Universite´ de Bourgogne, monly studied Antarctic echinoids (Agassiz 1869, 1881; 6 bd Gabriel, 21000 Dijon, France Studer 1876, 1880; Meissner 1900, Koehler 1901, 1906, 2 Laboratorio de Macroalgas Anta´rticas y Subanta´rticas, 1926;Do¨derlein 1906; Mortensen 1910). The genus in- Departamento de Ciencias y Recursos Naturales, Facultad de cludes six nominal species that were treated in many eco- Ciencias, Universidad de Magallanes, Av. Bulnes #01855, logical and biogeographic studies devoted to Antarctic Punta Arenas, Chile marine life (Brey and Gutt 1991; Arnaud et al. 1998; 3 Departamento de Ciencias Ecolo´gicas, Facultad de Ciencias, Barnes and Brockington 2003; Lee et al. 2004; David et al. ´ Instituto de Ecologıa y Biodiversidad, Universidad de Chile, 2005; Brandt et al. 2007; Linse et al. 2008;Dı´az et al. Las Palmeras 3425, N˜ un˜oa, Santiago, Chile ´ 4 2011; Gonzalez-Wevar et al. 2012a; Pierrat et al. 2012a, b). Departamento de Biologı´a Marina, Facultad de Ciencias del The genus Sterechinus is widely distributed across the Mar, Universidad Cato´lica del Norte, Larrondo 1281, Coquimbo, Chile Southern Ocean and extends northward along the coasts of Argentina until 35°S latitude (David et al. 2005; Pierrat 5 UMR 7263 Institut Me´diterrane´en de Biodiversite´ et d’Ecologie marine et continentale, Aix Marseille Universite´- et al. 2012b; Sauce`de et al. 2014). In the Antarctic, Ster- CNR-IRD-Avignon Universite´, Marseille, France echinus neumayeri (Meissner, 1900), Sterechinus 123 Author's personal copy 1224 Polar Biol (2015) 38:1223–1237 antarcticus (Koehler, 1901), and Sterechinus dentifer species, among which specimens of S. bernasconiae were (Koehler, 1926) inhabit the inner (0–800 m depth), outer collected. Based on these newly collected specimens along (200–1500 m depth), and deep shelf and slope with original samples including the type material (Larrain (500–2400 m depth) of the Antarctic continent, respec- 1975), the present work aims to revise the systematics of S. tively. Sterechinus diadema (Studer, 1876) is restricted to bernasconiae, clarify phylogenetic relationships with other sub-Antarctic islands (Marion and Prince Edward Islands, species of Sterechinus, and re-examine the biogeographic Crozet and the Kerguelen Plateau), and the distribution distribution of the genus Sterechinus in the Southern range of Sterechinus agassizi (Mortensen, 1910) extends Ocean. from sub-Antarctic islands (Falkland Islands, South Geor- gia, Shag Rocks, Bouvet Island, and Marion and Prince Edward Islands) to the coasts of Argentina as far northward Materials and methods as the mouth of Rio de la Plata at ca. 35°S latitude (David et al. 2005; Pierrat et al. 2012b). Finally, Sterechinus Material studied bernasconiae (Larrain, 1975) was only described from few localities off the coasts of southern Chile. It is the only New specimens of S. bernasconiae were collected off the species of Sterechinus recorded from the Pacific Ocean coasts of Chile during the oceanographic cruise INSPIRE (Larrain 1975). aboard the R/V Melville along the Chilean continental Despite the abundant literature devoted to Sterechinus, margin (Fig. 1; Table 1). Eight specimens were caught by recent molecular and morphological results have shown trawling at six stations, between about 600 and 1100 m that the three nominal species S. diadema, S. agassizi, and depth (Tables 1, 2). They are housed at the Biological S. antarcticus cannot be distinguished (David et al. 2005; Collection of Universidad Cato´lica del Norte (CBUCN, Dı´az et al. 2011). In the past, the distinction between Coquimbo, Chile). The analysis of specimens was com- species often relied on the geographic origin of specimens plemented by the examination of specimens of S. ber- as well as on subtle differences in morphology. However, nasconiae formerly collected in Patagonia during the Hero most of the morphological characters show a wide range of 72, 4b cruise (Larrain 1975). They are housed at the Mu- within-species variation that tend to overlap among species seum of Zoology, Universidad de Concepcio´n, Chile and make the distinctions between them unclear (Morten- (Table 1). To perform the phylogenetic analysis, specimens sen 1943; David et al. 2005). of S. bernasconiae were sequenced along with specimens In this context, S. bernasconiae has attracted our attention belonging to the five other nominal species of Sterechinus as it is the only species of Sterechinus reported from the that were collected in six areas of the Southern Ocean Pacific Ocean. It is recorded from a narrow area off the coast (Ade´lie Land, South Shetland Islands, Antarctic Peninsula, of southern Chile. In contrast, S. agassizi is much more Weddell/Bellingshausen seas, and around the Kerguelen widely distributed on the Atlantic side of southern South Islands) and off the coasts of Argentina (Table 2). This America; it extends from sub-Antarctic islands to the coasts material is housed at the Molecular Ecology Laboratory, and continental shelf of Argentina. Considering the few Faculty of Ecology Sciences at Universidad de Chile, specimens of S. bernasconiae ever collected as compared Santiago, Chile. with the numerous samples available for other Sterechinus species (Larrain 1975), the taxonomic status and distribution Morphological study range of the species were not revised in studies devoted to the systematics and biogeography of Austral echinoids (David New material was fixed in 96 % ethanol, the old specimens et al. 2005;Dı´az et al. 2011; Gonza´lez-Wevar et al. 2012a; housed at the University of Concepcio´n being preserved in Pierrat et al. 2012b, 2013). In light of the taxonomic issues formaldehyde. Morphological observations were per- raised in a recent study (Dı´az et al. 2011), the taxonomic formed with a binocular microscope, test measurements status of S. bernasconiae and its phylogenetic relationships were taken with a digital caliper to the nearest 0.1 mm. with S. agassizi and other species of Sterechinus had to be Statistical tests were performed with PAST v. 1.93 clarified. (Hammer et al. 2001). Echinoid test plating was drawn The oceanographic cruise INSPIRE was led off the using a binocular microscope equipped with a camera lu- coasts of Chile (February–March 2010, R/V Melville)to cida. Secondary spines and pedicellariae were removed explore chemosynthetic systems (i.e. hydrothermal vents from tests of the newly collected specimens and placed into and methane seeps) and study the associated marine life 96 % ethanol. They were bleached with a 10 % solution of (Zapata-Herna´ndez et al. 2014). The sampling effort was sodium hypochlorite to remove soft tissue and to separate led between 400 and 3300 m depth and from * 33°S individual valves of pedicellariae.
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