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Phylogeography of the Brittle Star Ophiura Sarsii Lütken, 1855 (Echinodermata: Ophiuroidea) from the Barents Sea and East Atlantic

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Phylogeography of the Brittle Star Ophiura Sarsii Lütken, 1855 (Echinodermata: Ophiuroidea) from the Barents Sea and East Atlantic diversity Article Phylogeography of the Brittle Star Ophiura sarsii Lütken, 1855 (Echinodermata: Ophiuroidea) from the Barents Sea and East Atlantic Evgeny Genelt-Yanovskiy 1,* , Yixuan Li 2, Ekaterina Stratanenko 3, Natalia Zhuravleva 3, Natalia Strelkova 4, Qinzeng Xu 2 and Sophia Nazarova 3,* 1 Department of Molecular Systematics, Zoological Institute Russian Academy of Sciences, 199034 Saint Petersburg, Russia 2 MNR Key Laboratory of Marine Eco-Environmental Science and Technology, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China; [email protected] (Y.L.); xuqinzeng@fio.org.cn (Q.X.) 3 Laboratory of Marine Research, Zoological Institute Russian Academy of Sciences, 199034 Saint Petersburg, Russia; [email protected] (E.S.); [email protected] (N.Z.) 4 Laboratory of Hydrobiology, Polar Branch of Russian Federal Research Institute of Fisheries and Oceanography (PINRO Named after N.M.Knipovich), 183038 Murmansk, Russia; [email protected] * Correspondence: [email protected] or [email protected] (E.G.-Y.); [email protected] (S.N.) Abstract: Ophiura sarsii is a common brittle star species across the Arctic and Sub-Arctic regions of the Atlantic and the Pacific oceans. Ophiura sarsii is among the dominant echinoderms in the Barents Sea. We studied the genetic diversity of O. sarsii by sequencing the 548 bp fragment of the mitochondrial COI gene. Ophiura sarsii demonstrated high genetic diversity in the Barents Sea. Both major Atlantic mtDNA lineages were present in the Barents Sea and were evenly distributed between Citation: Genelt-Yanovskiy, E.; Li, Y.; the northern waters around Svalbard archipelago and the southern part near Murmansk coast of Kola Stratanenko, E.; Zhuravleva, N.; Peninsula. Both regions, and other parts of the O. sarsii range, were characterized by high haplotype Strelkova, N.; Xu, Q.; Nazarova, S. diversity with a significant number of private haplotypes being mostly satellites to the two dominant Phylogeography of the Brittle Star haplotypes, each belonging to a different mtDNA clade. Demographic analyses indicated that the Ophiura sarsii Lütken, 1855 demographic and spatial expansion of O. sarsii in the Barents Sea most plausibly has started in the (Echinodermata: Ophiuroidea) from the Barents Sea and East Atlantic. Bølling–Allerød interstadial during the deglaciation of the western margin of the Barents Sea. Diversity 2021, 13, 40. https://doi.org/10.3390/d13020040 Keywords: mtDNA; barcoding; echinoderms; demographic expansion Received: 24 December 2020 Accepted: 18 January 2021 Published: 21 January 2021 1. Introduction Marine communities of the Northern Atlantic experienced remarkable changes during Publisher’s Note: MDPI stays neutral the quaternary sea level oscillations when ranges of species were contracting during the with regard to jurisdictional claims in advances of glaciations and expanding during warmer periods [1]. A number of taxa published maps and institutional affil- migrated from the Pacific to the Atlantic by trans-Arctic migrations after the first opening iations. of the Bering Strait in the Pliocene [2]. The recent glacial cycle culminating in the last glacial maximum 21 kyr BP (thousands of years before present) lead to the southward retreat of boreal species, yet many populations survived in the northern unglaciated areas known as periglacial refugia [3–12]. Demographic expansions between the glacial cycles and after the Copyright: © 2021 by the authors. retreat of the LGM ice sheets resulted in secondary contacts between previously isolated Licensee MDPI, Basel, Switzerland. populations [6]. This article is an open access article The Barents Sea is a marginal sea of the Arctic Ocean (Figure1) and a biogeographic distributed under the terms and transition zone between East Atlantic and typical Arctic faunas. The sea is highly pro- conditions of the Creative Commons ductive with the pronounced spatial variation in productivity of benthic communities. Attribution (CC BY) license (https:// Southern and central parts of the Barents Sea are characterized by higher abundance and creativecommons.org/licenses/by/ biomass of benthic species compared to the northern regions around Svalbard and Franz 4.0/). Diversity 2021, 13, 40. https://doi.org/10.3390/d13020040 https://www.mdpi.com/journal/diversity Diversity 2021, 13, x FOR PEER REVIEW 2 of 12 glacial cycles and after the retreat of the LGM ice sheets resulted in secondary contacts between previously isolated populations [6]. The Barents Sea is a marginal sea of the Arctic Ocean (Figure 1) and a biogeographic transition zone between East Atlantic and typical Arctic faunas. The sea is highly pro- Diversity 2021, 13, 40 ductive with the pronounced spatial variation in productivity of benthic communities.2 of 11 Southern and central parts of the Barents Sea are characterized by higher abundance and biomass of benthic species compared to the northern regions around Svalbard and Franz JosefJosef Land Land [13] [13. ].The The Northern Northern Barents Barents Sea Sea is isoften often considered considered as asthe the Arctic Arctic warming warming hotspot,hotspot, where where the the sharp sharp increase increase of of water water temperatures andand salinitysalinity isis observed observed since since the themid-2000s mid-2000s [14 [14]]. Studies. Studies of theof the population population structure structure of species of species distributed distributed across across the Barents the BarentsSea shelf Sea are shelf thus are important thus important for understanding for understanding the current the and current long-term and changes long-term in this changesdynamic in this marine dynamic ecosystem. marine ecosystem. FigureFigure 1. 1.MapMap of ofOphiuraOphiura sarsii sarsii samplingsampling locations. locations. The The Barents Barents Sea Sea is highlighted is highlighted on onthe the map. map. IDID—locations—locations codes: codes: HUD—HudsonHUD—Hudson Bay, Bay, LAW—St. LAW— LawrenceSt. Lawrence Bay, BAF—Baffin Bay, BAF Bay,—Baffin ICE—Iceland, Bay, ICENS—the—Iceland, North NS Sea,—the SVD—Svalbard, North Sea, SVD BAR—Southern—Svalbard, partBAR of—Southern the Barents part Sea, of BC—British the Barents Columbia. Sea, BC—British Columbia. Ophiuroidea are important components of marine benthic communities in the North- ernOphiuroidea Hemisphere, are often important dominating components vast areas of of marine shelvesbenthic [15communities–17]. The brittle in the star NorthernOphiura Hemisphere, sarsii Lütken, often 1855 isdominating a circumpolar vast cold-water areas of marine species shelves widely [15 distributed–17]. The through-brittle starout Ophiura the North sarsii Pacific, Lütken, the 1855 North is Atlantic,a circumpolar and the cold Arctic-water oceans, species where widely it can distributed reach maxi- throughoutmum depths the ofNorth ca. 3000 Pacific, m [18 the,19 ].North In the Atlantic, Barents Sea,and O.the sarsii Arcticrepresents oceans, upwhere to 4% it ofcan the reachtotal maximum echinoderm depths biomass, of ca. typically 3000 m occurring[18,19]. In at the muddy Barents and Sea, muddy O. sarsii fine represent sand communitiess up to 4%at of a the depth total range echinoderm between biomass, 3 and 500 typically m [19]. Ophiura occurring sarsii at muddyis a predator–scavenger and muddy fine species,sand communitiesand an important at a depth food itemrange for between many fish 3 and species 500 [20m ].[19] It is. Ophiura also a typical sarsii marineis a predator broadcast– scavengerspawner, species, releasing and eggs an andimportant sperm food in the item Barents for many Sea in fish May–June species [[20]21]. and It is then alsohaving a typ- a icalfeeding marine larval broadcast stage spawner, (ophiopluteus) releasing with eggs planktonic and sperm existence in the ofBarents up to 30Sea days in May [22].–June [21] andRecently, then having the genetic a feeding structure larval of stageO. sarsii (ophiopluteus)was broadly evaluatedwith planktonic across theexistence Pacific of [23 ]. Here we present analysis of the mitochondrial cytochrome c oxidase subunit I (COI) gene up to 30 days [22]. to examine the genetic diversity of O. sarsii in the Barents Sea and to make a pilot estimate Recently, the genetic structure of O. sarsii was broadly evaluated across the Pacific of population structuring across the Atlantic using the previously published sequences [23]. Here we present analysis of the mitochondrial cytochrome c oxidase subunit I (COI) from the barcoding studies of Echinoderms [24–26]. gene to examine the genetic diversity of O. sarsii in the Barents Sea and to make a pilot estimate2. Materials of population and Methods structuring across the Atlantic using the previously published sequences2.1. Samples from the barcoding studies of Echinoderms [24–26]. Sampling was conducted in the Barents Sea during the 17th joint Barents Sea Ecosys- tem Survey (BESS) cruise of the Institute of Marine Research (IMR, Bergen, Norway) and the Polar branch of VNIRO (PINRO, Murmansk, Russia) [27] in September 2019 and 114th cruise of RV “Vilnyus” (Polar branch of the VNIRO) (Figure1, Supplementary Table S1). Samples were collected using the bottom trawl from the depth range between 84 and 325 m. Individuals from the trawl were washed in seawater from sediments and preserved in 96% ethanol. Specimens of O. sarsii from the Barents Sea were deposited in the Zoological Diversity 2021, 13, 40 3 of 11 Institute (ZIN RAS) in St. Petersburg with voucher numbers 964/25547–973/25556
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