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Post-Glacial Colonisation Pathways Varied Among Cold-Water Coral Out of the Mediterranean? Post-glacial colonisation pathways varied among cold-water coral species Joana Ruela Heimbürger Boavida, Ronan Becheler, Marvin Choquet, Norbert Frank, Marco Taviani, Jean-François Bourillet, Anne-Leila Meistertzheim, Anthony Grehan, Alessandra Savini, Sophie Arnaud-Haond To cite this version: Joana Ruela Heimbürger Boavida, Ronan Becheler, Marvin Choquet, Norbert Frank, Marco Taviani, et al.. Out of the Mediterranean? Post-glacial colonisation pathways varied among cold-water coral species. Journal of Biogeography, Wiley, 2019, 46 (5), pp.915-931. 10.1111/jbi.13570. hal-03043708 HAL Id: hal-03043708 https://hal.archives-ouvertes.fr/hal-03043708 Submitted on 7 Dec 2020 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. Journal of Biogeography Out of the Mediterranean? Post-glacial colonisation pathways varied among cold-water coral species Journal: Journal of Biogeography Manuscript ID JBI-18-0133.R1 Manuscript Type:ForResearch Peer Paper Review Date Submitted by the n/a Author: Complete List of Authors: boavida, joana; Ifremer Centre de Mediterranee, MARBEC; Centro de Ciencias do Mar, Biogeography Ecology and Evolution Lab Becheler, Ronan; Ifremer Centre de Mediterranee, MARBEC; UPMC Univ Paris 6, CNRS, UMI 3614 Evolutionary Biology and Ecology of Algae, Sorbonne Université; Station Biologique de Roscoff, Station Biologique de Roscoff Choquet, Marvin; Ifremer Centre de Mediterranee, MARBEC; Nord University, Faculty of Biosciences and Aquaculture Frank, Norbert; Heidelberg University, Institute of Environmental Physics Taviani, Marco; Institute of Marine Science - National Research Council ISMAR-CNR, Institute of Marine Science - National Research Council ISMAR-CNR; Woods Hole Oceanographic Institution, Biology Department; Stazione Zoologica Anton Dohrn, Stazione Zoologica Anton Dohrn Bourillet, Jean Francois ; ifremer, Physical resources and sea floor ecosystems Department Meistertzheim, Anne Leila; Sorbonne Universités, Laboratoire d’Ecogéochimie des Environnements Benthiques (LECOB), Observatoire Océanologique de Banyuls Grehan, Anthony; NUI Galway, NUI Savini, Alessandra; Università degli Studi di Milano-Bicocca, Dept. of Earth and Environmental Sciences Arnaud-Haond, Sophie; Ifremer Centre de Mediterranee, MARBEC Cold-water corals, Lophelia pertusa, Madrepora oculata, Marine Key Words: phylogeography, Deep-sea, Last Glacial Maximum, Glacial marine refugia Page 27 of 114 Journal of Biogeography 1 2 3 1 i. Out of the Mediterranean? Post-glacial colonisation pathways varied among cold-water coral 4 2 species 5 6 3 ii. Running title: Contrasting deep corals recolonisation paths 7 8 4 iii. Joana Ruela Heimbürger Boavida1*±, Ronan Becheler1,2,3,*§, Marvin Choquet1,4, Norbert Frank5, 9 5 Marco Taviani6,7,8, Jean-François Bourillet9, Anne Leila Meistertzheim10, Anthony Grehan11, 10 6 Alessandra Savini12, Sophie Arnaud-Haond1 11 12 7 *Equal contribution 13 14 8 Correspondance: Joana Boavida Institut Français de Recherche pour l'Exploitation de la Mer, Marine 15 16 9 Biodiversity Exploitation and Conservation - Marbec, Station de Sète - Avenue Jean Monnet - CS 17 10 30171, 34203 Sète Cedex, France 18 19 11 [email protected] | +33 7 69 41 12 79 20 21 12 iv. The author's institutionalFor affiliations Peer Review 22 23 13 1 Institut Français de Recherche pour l'Exploitation de la Mer, Marine Biodiversity Exploitation and 24 14 Conservation - Marbec, Station de Sète - Avenue Jean Monnet - CS 30171, 34203 Sète Cedex, France 25 26 27 15 2 CNRS, UMI 3614 Evolutionary Biology and Ecology of Algae, Sorbonne Université, UPMC Univ 28 16 Paris 6 29 30 17 3 Station Biologique de Roscoff, CS 90074, Place Georges Teissier, 29688 Roscoff cedex, France. 31 32 33 18 4 Faculty of Biosciences and Aquaculture, Nord University, Bodø, Norway 34 35 19 5 Heidelberg University, Institute of Environmental Physics, Im Neuenheimer Feld 229, 69120 36 20 Heidelberg, Germany 37 38 21 6 Institute of Marine Science - National Research Council ISMAR-CNR, Via Gobetti 101, 40129 39 22 Bologna, Italy 40 41 23 7 Biology Department, Woods Hole Oceanographic Institution, 266 Woods Hole Road, Woods Hole, 42 43 24 MA 02543, USA 44 8 45 25 Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy 46 47 26 9 Institut Français de Recherche pour L'Exploitation de la Mer, Physical resources and sea floor 48 27 ecosystems Department, Centre de Brest BP 70, F-29280, Brest - France 49 50 10 51 28 Sorbonne Universités, CNRS, UPMC Univ Paris 06, Laboratoire d’Ecogéochimie des 52 29 Environnements Benthiques (LECOB), Observatoire Océanologique de Banyuls, Banyuls sur mer, 53 30 France 54 55 31 11 Dept. of Earth & Ocean Sciences, Quadrangle Bldg, NUI Galway, Ireland 56 57 32 12 Università degli Studi di Milano-Bicocca, Dept. of Earth and Environmental Sciences, Italy 58 59 60 1 Journal of Biogeography Page 28 of 114 1 2 3 33 § Present address: Centro de Conservación Marina, Departamento de Ecología, Facultad de Ciencias 4 34 Biológicas, Pontificia Universidad Católica de Chile, Casilla 114-D, Chile 5 6 35 ± Present address: Centro de Ciências do Mar, Universidade do Algarve, Campus de Gambelas, 8005- 7 8 36 139 Faro, Portugal 9 10 37 v. Acknowledgements 11 12 38 We are thankful to the teams involved in multiple oceanographic cruises: EU CoralFish's: ROV team, 13 39 captain and crew of BOBECO, IceCTD, and CE98. We thank Franck Lartaud and Nadine Le Bris 14 40 (chair ‘Extreme environment, biodiversity and global change’ Fondation TOTAL and UPMC; Coord.: 15 41 N. Le Bris) for providing Mediterranean samples. Thanks to Lars-Eric Heimbürger for english edits. 16 42 JB was supported by the European Union's H2020 research and innovation program under grant 17 43 agreement Number: 678760 (ATLAS). This work is a contribution to the European Union’s FP7 and 18 44 Horizon 2020 projects, respectively CoralFISH (under grant agreement no. 213144) and ATLAS 19 45 (under grant agreement no. 678760), samples from the Adriatic Sea through the EU Coconet program. 20 46 This is Ismar-CNR, Bologna scientific contribution n. 1960. This contribution reflects the authors’ 21 47 views and the European UnionFor is not Peerresponsible forReview any use that may be made of the information it 22 48 contains. 23 24 49 vi. Abstract and keywords: 25 26 50 Aim. To infer cold-water corals post-glacial phylogeography and assess the role of Mediterranean Sea 27 51 glacial refugia as the origin for the recolonisation of the North-eastern Atlantic Ocean. 28 29 52 Location. North-eastern Atlantic Ocean and Mediterranean Sea. 30 31 53 Taxon. Lophelia pertusa, Madrepora oculata. 32 33 54 Methods. We sampled cold-water corals using remotely operated vehicles and performed one 34 55 geological corer for coral and sediment dating. We characterized spatial genetic patterns 35 56 (microsatellites and a nuclear gene fragment) using networks, clustering and measures of genetic 36 57 differentiation. 37 38 58 Results. Microsatellite and sequence data were congruent, and showed a contrast between the two 39 59 cold-water coral species. Populations of L. pertusa are not genetically structured across the North- 40 60 eastern Atlantic, present a dominant pioneer haplotype, local haplotype radiations and a majority of 41 61 endemic variation in lower latitudes. M. oculata populations are differentiated across the North-eastern 42 62 Atlantic, and genetic lineages are poorly admixed even along neighbouring sites. 43 44 63 Conclusions. Our study shows contrasting post-glacial colonisation pathways for two key habitat- 45 64 forming species in the deep-sea. The cold-water coral L. pertusa has likely undertaken a long-range 46 65 (post-glacial) recolonisation of the North-eastern Atlantic directly from refugia located along southern 47 66 Europe (Mediterranean Sea or Gulf of Cadiz). Contrastingly, the stronger genetic differentiation of 48 67 M. oculata populations mirrors the effects of long-term isolation in multiple refugia. We suggest that 49 68 the distinct and genetically diverged, refugial populations initiated the post-glacial recolonisation of 50 69 North-eastern Atlantic margins, leading to a secondary contact in the northern range and reaching 51 70 higher latitudes much later, in the late Holocene. This study highlights the need to disentangle the 52 71 influence of present day dispersal and evolutionary processes on the distribution of genetic 53 72 polymorphism, to unravel the influence of past and future environmental changes on connectivity in 54 73 the cosmopolitan deep-sea ecosystems associated to cold-water corals. Marine phylogeography, Deep- 55 74 sea, Cold-water corals, Last Glacial Maximum, Lophelia pertusa, Madrepora oculata, Glacial marine 56 75 refugia 57 58 76 vii. Main text 59 60 77 Introduction 2 Page 29 of 114 Journal of Biogeography 1 2 3 78 Cold-water corals (CWC) are amongst the most charismatic marine ecosystems in the deep ocean 4 79 (>200 m), supporting abundant and diverse biomass (Milligan et al., 2016). Deep-reef habitats rely 5 6 80 upon the frame-building capability of several coral species, notably Lophelia pertusa and 7 81 Madrepora oculata (Linnaeus, 1758). The two species intermingle and anastomose in reefs in the 8 82 North-eastern Atlantic Ocean (NE Atlantic; Arnaud-Haond et al., 2017). Yet, ever rising 9 83 anthropogenic pressures in the deep-sea, like fisheries (Pusceddu et al., 2014), oil and gas exploitation 10 84 (Cordes et al., 2016) and deep-sea mining (Wedding et al., 2015), threaten vulnerable CWC. 11 12 85 Protection of key deep-sea ecosystems is, therefore, an urgent priority, particularly in the face of 13 86 global change, and strategic Marine Protected Areas, thoroughly assessed for their genetic 14 87 connectivity, need to be established.
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