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Phylogeny of Nemertea with Special Interest in the Placement of Diversity from Far East Russia and Northeast Asia

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Phylogeny of Nemertea with Special Interest in the Placement of Diversity from Far East Russia and Northeast Asia Phylogeny of Nemertea with special interest in the placement of diversity from Far East Russia and northeast Asia Sebastian Kvist, Alexei V. Chernyshev & Gonzalo Giribet Hydrobiologia The International Journal of Aquatic Sciences ISSN 0018-8158 Hydrobiologia DOI 10.1007/s10750-015-2310-5 1 23 Your article is protected by copyright and all rights are held exclusively by Springer International Publishing Switzerland. 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 Hydrobiologia DOI 10.1007/s10750-015-2310-5 PRIMARY RESEARCH PAPER Phylogeny of Nemertea with special interest in the placement of diversity from Far East Russia and northeast Asia Sebastian Kvist . Alexei V. Chernyshev . Gonzalo Giribet Received: 13 February 2015 / Revised: 23 April 2015 / Accepted: 29 April 2015 Ó Springer International Publishing Switzerland 2015 Abstract Recent investigations, based mostly on COI and 16S rRNA, as well as nuclear 18S rRNA and molecular data, have unraveled the evolutionary 28S rRNA—finding that the current classification for history of several common ribbon worm (phylum most of these species is corroborated by their phylo- Nemertea) species and solidified the taxonomic status genetic placement. We then discuss the evolution of of many higher taxa within the group. However, a some unique morphological traits possessed by some large proportion of enigmatic species have yet to be of these species, using the molecular phylogeny as a placed in a phylogenetic framework. We investigated backbone for our general conclusions. the phylogenetic positions of 26 novel and/or per- plexing nemertean species from the Sea of Okhotsk, Keywords Nemertea Á Phylogeny Á Sea of Okhotsk Á the Sea of Japan, the Kuril–Kamchatka Trench, and Sea of Japan Á Vietnam Á Kuril–Kamchatka Trench Vietnam (including the first record of a reptant nemertean from the Far East seas of Russia). We conducted both maximum likelihood and parsimony Introduction analyses, utilizing four molecular loci—mitochondrial Notwithstanding the utility of morphological char- acters in delimiting and diagnosing ribbon worm Handling editor: Christian Sturmbauer S. Kvist (&) Á G. Giribet A. V. Chernyshev Museum of Comparative Zoology, Department of A.V. Zhirmunsky Institute of Marine Biology, Far East Organismic and Evolutionary Biology, Harvard Branch, Russian Academy of Sciences, University, 26 Oxford Street, Cambridge, MA 02138, Vladivostok 690059, Russia USA e-mail: [email protected] A. V. Chernyshev Far Eastern Federal University, Vladivostok 690600, Present Address: Russia S. Kvist Department of Natural History, Royal Ontario Museum, 100 Queen’s Park, Toronto, ON M5S 2C6, Canada S. Kvist Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, ON M5S 2B4, Canada 123 Author's personal copy Hydrobiologia (phylum Nemertea) species, molecular data seem to phylogeny. The oceanographic properties of these currently provide the most effective measure for semi-enclosed bodies of water are in stark contrast; inferring phylogenies (Schwartz & Norenburg, 2001; deep basins mainly represent the Sea of Japan, whereas Strand & Sundberg, 2005a; Sundberg et al., 2010; the Sea of Okhotsk also holds more shallow regions Sundberg & Strand, 2010; Strand et al., 2014; Leasi & (Preller & Hogan, 1998). Furthermore, palaeoenviron- Norenburg, 2014; see Turbeville, 2002 for a compre- mental studies have shown that the seas have undergone hensive review of nemertean phylogenetics). For major geomorphological shifts since the late Pleis- several nemertean taxa, this is due partly to the tocene (Ryu et al., 2005). These events have led to homoplastic nature of morphological characters, differences not only in oceanic currents (e.g., Hidaka, which impelled Sundberg et al. (2010) and Sundberg 1966; Kitamura et al., 2001), but also uniqueness in & Strand (2010) to propose that molecular data should micro-organismal diversity (e.g., Kojima, 2002)and accompany any modern species description within benthic faunal compositions (e.g., Sahling et al., 2003). Nemertea. In reply to the need for molecular ap- Indeed, the Sea of Okhotsk and the Sea of Japan have proaches, especially regarding more problematic taxa jointly been suggested as one of Earth’s most with few distinguishing morphological features, con- biologically valuable ecoregions, placing among the temporary nemertean systematics has seen a surge in top polar and sub-polar marine ecosystems in terms of contributions employing molecules to shed light on biological value (Olson & Dinerstein, 1998). Despite of long-reigning morphological phylogenetic hypotheses this importance, several major invertebrate groups and taxonomic classification systems (Sundberg et al., remain unsurveyed in this area of the Pacific Ocean. 2001; Thollesson & Norenburg, 2003; Andrade et al., To make matters worse, the depth and geomorpho- 2012, 2014; Kvist et al., 2014). Taken together, these logical complexity of the Kuril–Kamchatka Trench studies have allowed for robust tests of species ([10,000 m at the deepest), positioned slightly east of affiliations and evolutionary relationships among the the Sea of Okhotsk, makes sampling efforts within this most commonly sampled nemertean taxa. It remains, area particularly difficult. To partially alleviate this however, that several, perhaps more enigmatic, taxa situation, the present study aims to elucidate the general have yet to be placed in a phylogenetic framework and evolutionary relationships of several nemertean speci- that the body of undescribed diversity is likely large mens collected from the Sea of Okhotsk, the Sea of within Nemertea, much like most other phyla (e.g., Japan and the Kuril–Kamchatka Trench, as well as a May, 1988; Blaxter, 2003). Beyond the imbalance in few specimens from Vietnam. the distribution of scientific funding opportunities in opposing parts of the world, one of the principal reasons for the idleness towards groups of taxa is Materials and methods likely the logistic difficulty inherent in taxonomic sampling efforts in remote geographic regions. As a Specimen collection result, a disproportionate amount of the known nemertean diversity that has been firmly placed in a The specimens used in the present study were phylogenetic context inhabits the same general area collected by different methods during several expedi- around the western and southern European coastlines, tions to the Far East seas of Russia and northeastern as well as parts of the Americas. Asia. Intertidal nemerteans were collected without any Although over 300 nemertean species have been equipment; deeper dwelling species of nemerteans recorded from northeastern Asia, including about 120 (between 6 and 400 m depth) were collected by species from the Far East seas of Russia [the Sea of different kinds of dredges; the deepest-dwelling Okhotsk and the northern part of the Sea of Japan (also (abyssal) nemerteans were collected by Agassiz trawl known as the East Sea)] (Crandall et al., 2002; see also and epibenthic sledges during the German–Russian Gibson, 1995;Kajiharaetal.,2008;Chernyshev,2014), deep-sea expedition to the abyssal plain adjacent to the the full diversity of nemertean taxa in this geographic Kuril–Kamchatka Trench on board the R/V ‘‘Sonne’’ region is still largely unappreciated (e.g., Korotkevich, in the summer of 2012 (see Figs. 1, 2, 3 for some 1971; Chernyshev, 2013;Chernyshevetal.,2015), and representative taxa). Tissue samples from live ne- most of these taxa have yet to be solidly placed in a merteans were fixed in 95% ethanol for DNA 123 Author's personal copy Hydrobiologia Fig. 2 Live habitus of selected specimens. Photos by A. Chernyshev. A Hubrechtella juliae Chernyshev, 2003 IZ- Fig. 1 Live habitus of selected specimens. Photos by A. 45553 (Sea of Japan, Vostok Bay, Jul. 2013). B Carinina sp. Chernyshev. A Tubulanus sp. IZ-45552 (Sea of Japan, Vostok IZ-45550 (Sea of Japan, Vostok Bay, Jul. 2013). C Gonone- Bay, Aug. 2012). B Callinera kasyanovi Chernyshev, 2008 IZ- mertes sp. IZ-45558 (abyssal plain adjacent to the Kuril– 45551 (Sea of Japan, Peter the Great Bay, Aug. 2012). Kamchatka Trench, Aug. 2012). D Callinera sp. IZ-45635 (Sea C Cephalothrix iwatai Chernyshev, 2013 IZ-45650 (Sea of of Japan, Vostok Bay, Aug. 2007). E Tortus sp. IZ-45645 (Sea Japan, Nov. 2013). D Parahubrechtia sp. IZ-45554 (abyssal of Okhotsk, Iturup Island, Jul. 2011). F Tubulanus sp. IZ-45559 plain adjacent to the Kuril–Kamchatka Trench, Aug. 2012). (Sea of Okhotsk, Kuril Islands, Jul. 2011). Additional specimen E Monostilifera sp. IZ-45641 (Sea of Okhotsk, Kuril Islands, details can be found in MCZbase (http://mczbase.mcz.harvard. Jul. 2011). F Sacconemertidae sp. IZ-45649 (Sea of Okhotsk, edu/) near Magadan, Oct. 2008). Additional specimen details can be found in MCZbase (http://mczbase.mcz.harvard.edu/) and embedded in paraffin wax (m.p. 56–57°C). Serial extraction; in some instances, worms were
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