Genetic structure and connectivity of the critically endangered deep-sea octocoral Isidella elongata: implications for marine biodiversity conservation in the Mediterranean Sea
Resumen
The protection of the Vulnerable Marine Ecosystem identified by the presence of the critically endangered bamboo coral Isidella elongata has been recognized as an urgent task. Although some research has focused on the spatial distribution of this species, there is no information available on its connectivity and genetic structure. This is the first study to examine the genetic diversity pattern and inter-population connectivity of I. elongata at the Mediterranean scale. The DNA-based approach for assessing the genetic diversity of 33 I. elongata samples collected in six different areas involved two mitochondrial markers (COI and MutS) and one nuclear marker (ITS2). Molecular results confirmed that all samples belonged to I. elongata and showed a scarce level of intra- and inter-population mtDNA differentiation, whereas nuDNA data revealed genetic structuring. Furthermore, a Lagrangian model (forward-in-time simulations) was used to investigate the species larval connectivity under different sea current conditions. Our results suggest the presence of persistent pathways, supporting the self-sustaining nature of the populations, especially in the central Mediterranean Sea. This study identifies the main corridors of connectivity for I. elongata in the Mediterranean Sea, highlighting the importance of including such information in the implementation of fishery management measures.
Article Details
- Cómo citar
-
LAURIA, V., GARGANO, F., ARCULEO, M., BONO, G., FIORENTINO, F., FLOT, J.-F., COLLARD, O., FOLLESA, M. C., GAROFALO, G., GEORGES, V., MAIORANO, P., MASSI, D., STAMOULI, C., VAZ, S., VITALE, S., & VECCHIONI, L. (2025). Genetic structure and connectivity of the critically endangered deep-sea octocoral Isidella elongata: implications for marine biodiversity conservation in the Mediterranean Sea. Mediterranean Marine Science, 26(4), 1050–1067. https://doi.org/10.12681/mms.40883
- Sección
- Research Article
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution Non-Commercial License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g. post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (preferably in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
Descargas
Los datos de descargas todavía no están disponibles.
Citas
Angiolillo, M., Di Lorenzo, B., Izzi, A., Giusti, M., Nonnis, O. et al. 2024. Healthy assemblages of Isidella elongata unintentionally protected from trawling offshore of Asinara Island (northwestern Sardinia, NW Mediterranean Sea). Scientific Reports, 14 (1), 12813.
Aurelle, D., Pivotto, I.D., Malfant, M., Topçu, N.E., Masmoudi, M.B. et al., 2017. Fuzzy species limits in Mediterranean gorgonians (Cnidaria, Octocorallia): Inferences on speciation processes. Zoologica Scripta, 46 (6), 767-778.
Bandelt, H.J., Forster, P., Röhl, A., 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16 (1), 37-48.
Bayer, F., Stefani, J., 1987. Isididae (Gorgonacea) de Nouvelle- Calédonie. Nouvelle clé des genres de la famille. Bulletin du Mus é um National d’Histoire Naturelle de Paris, 4 (9), 47-106.
Bongiorni, L., Mea, M., Gambia, C., Pusceddu, A., Taviani, Μ. et al. 2010. Deep-water scleractinian corals promote higher biodiversity in deep-sea meiofaunal assemblages along continental margins. Biological Consrvation, 143 (7), 1687-1700.
Brugler, M.R., France, S.C., 2008. The mitochondrial genome of a deep-sea bamboo coral (Cnidaria, Anthozoa, Octocorallia, Isididae): genome structure and putative origins of replication are not conserved among octocorals. Journal of Molecular Evolution, 67 (2), 125-136.
Buhl-Mortensen, L., Vanreusel, A., Gooday, A.J., Levin, L.A., Priede, I.G. et al., 2010. Biological structures as a source of habitat heterogeneity and biodiversity on the deep ocean margins. Marine Ecology, 31 (1), 21-50.
Calderón, I., Garrabou, J., Aurelle, D., 2006. Evaluation of the utility of COI and ITS markers as tools for population genetic studies of temperate gorgonians. Journal of Experimental Marine Biology and Ecology, 336 (2), 184-197.
Carbonara, P., Zupa, W., Follesa, M. C., Cau, A., Capezzuto, F. et al., 2020. Exploring a deep-sea vulnerable marine ecosystem: Isidella elongata (Esper, 1788) species assemblages in the Western and Central Mediterranean. Deep Sea Research Part I: Oceanographic Research Papers, 166, 103406.
Carbonara, P., Zupa, W., Follesa, M.C., Cau, A., Donnaloia, M. et al., 2022. Spatio-temporal distribution of Isidella elongata, a vulnerable marine ecosystem indicator species, in the southern Adriatic Sea. Hydrobiologia, 849 (21), 4837-4855.
Carpine, C., Grasshoff, M., 1975. Les gorgonaires de la Méditerranée occidentale. Bulletin de l’Institut Océanographique de Monaco, 71 (1430), 140 p.
Cartes, J.E., Díaz-Viñolas, D., González-Irusta, J.M., Serrano, A., Mohamed, S. et al., 2022. The macrofauna associated to the bamboo coral Isidella elongata: To what extent the impact on isideidae affects diversification of deep-sea fauna. Coral Reefs, 41 (4), 1273-1284.
CBD/COP/15/L.25 Kunming-Montreal Global biodiversity framework, 18 Dec. 2022, Chimienti, G., Bo, M., Taviani, M., Mastrototaro, F., 2019. 19 occurrence and biogeography of Mediterranean cold-water corals. In: Mediterranean Cold-Water Corals: Past, Present and Future, C. Orejas, C. Jiménez (Eds.) Understanding the Deep-Sea Realms of Coral (pp. 213-243). Cham: Springer International Publishing.
Chimienti, G., Mastrototaro, F., D’Onghia, G., 2020. Mesophotic and deep-sea vulnerable coral habitats of the Mediterranean sea: overview and conservation perspectives. In L. A. Soto (Ed.), Advances in the Studies of the Benthic Zone. IntechOpen.
Coelho, M.A.G., Pearson, G.A., Boavida, J.R.H., Paulo, D., Aurelle, D. et al., 2023. Not out of the Mediterranean: Atlantic populations of the gorgonian Paramuricea clavata are a separate sister species under further lineage diversification. Ecology and Evolution, 13 (1), e9740.
Coll, M., Piroddi, C., Steenbeek, J., Kaschner, K., Ben Rais Lasram, F. et al., 2010. The biodiversity of the Mediterranean sea: estimates, patterns, and threats. PLoS ONE, 5 (8), e11842.
Coma, R., Ribes, M., Zabala, M., Giti, J., 1995. Reproduction and cycle of gonadal development in the Mediterranean gorgonian Paramuricea clavata. Marine Ecology Progresses Series, 117, 173-183.
Danovaro, R., Pusceddu, A., 2007.Ecomanagement of biodiversity and ecosystem functioning in the Mediterranean Sea: concerns and strategies. Chemistry and Ecology 23, 347-360.
Doyle, J.J., 1995. The irrelevance of allele tree topologies for species delimitation, and a non-topological alternative. Systematic Botany, 20 (4), 574-588. European Commission, 2023. Improving environmental sustainability of deep sea fisheries with emphasis on the conservation of Vulnerable Marine Ecosystems (VMEs): Final report. Publications Office.
Fabri, M.C., Pedel, L., Beuck, L., Galgani, F., Hebbeln, D. et al., 2014. Megafauna of vulnerable marine ecosystems in French mediterranean submarine canyons: Spatial distribution and anthropogenic impacts. Deep-Sea Research Part II: Topical Studies in Oceanography, 104, 184-207.
Fiorentino, F., Garofalo, G., Bono, G.,Vitale, S., 2024. Learning from the history of red shrimp fisheries in the Mediterranean to improve sustainability of deep-water bottom trawling. ICES Journal of Marine Science, 81 (4), 652-664. Flot, J.F., 2007. Champuru 1.0: A computer software for unraveling mixtures of two DNA sequences of unequal lengths. Molecular Ecology Notes, 7 (6), 974-977.
Flot, J.F., Couloux, A., Tillier, S., 2010. Haplowebs as a graphical tool for delimiting species: a revival of Doyle’s “field for recombination” approach and its application to the coral genus Pocillopora in Clipperton. BMC Evolutionary Biology, 10, 372.
Flot, J.F., 2010. SeqPHASE: A web tool for interconverting phase input/output files and fasta sequence alignments. Molecular Ecology Resources, 10 (1), 162-166.
Flot, J.F., Magalon, H., Cruaud, C., Couloux, A., Tillier, S., 2008. Patterns of genetic structure among Hawaiian corals of the genus Pocillopora yield clusters of individuals that are compatible with morphology. Comptes Rendus Biologies, 331 (3), 239-247.
Flot, J.F., Tillier, S., 2006. Molecular phylogeny and systematics of the scleractinian coral genus Pocillopora in Hawaii. Proceedings of the 10th International Coral Reef Symposium, 1, 24-29.
Folmer, O., Black, M., Hoeh, W., Lutz, R., Vrijenhoek, R., 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3 (5), 294-299.
Fontaneto, D., Flot, J.F., Tang, C. Q., 2015. Guidelines for DNA taxonomy, with a focus on the meiofauna. Marine Biodiversity, 45 (3), 433-451.
Gargano, F., Garofalo, G., Fiorentino, F., 2017. Exploring connectivity between spawning and nursery areas of Mullus barbatus (L., 1758) in the Mediterranean through a dispersal model. Fisheries Oceanography, 26 (4), 476-497.
Gargano, F., Garofalo, G., Quattrocchi, F., Fiorentino, F., 2022. Where do recruits come from? Backward Lagrangian simulation for the deep water rose shrimps in the Central Mediterranean Sea. Fisheries Oceanography, 31 (4), 369-383.
Georges, V., Vaz, S., Carbonara, P., Fabri, M.C., Fanelli, E. et al., 2024. Mapping the habitat refugia of Isidella elongata under climate change and trawling impacts to preserve Vulnerable Marine Ecosystems in the Mediterranean. Scientific Reports, 14 (1), 6246.
Gerovasileiou, V., Smith, C. J., Kiparissis, S., Stamouli, C., Dounas, C. et al., 2019. Updating the distribution status of the critically endangered bamboo coral Isidella elongata (Esper, 1788) in the deep Eastern Mediterranean Sea. Regional Studies in Marine Science, 28, 100610.
Getis, A., Ord, J.K., 1992. The analysis of spatial association by use of distance statistics. Geographical Analysis, 24 (3), 189-206.
González-Irusta, J.M., Cartes, J.E., Punzón, A., Díaz, D., de Sola, L.G. et al., 2022. Mapping habitat loss in the deepsea using current and past presences of Isidella elongata (Cnidaria: Alcyonacea). ICES Journal of Marine Science, 79 (6), 1888-1901.
Gori, A., Bramanti, L., López-González, P., Thoma, J.N., Gili, J.M. et al., 2012. Characterization of the zooxanthellate and azooxanthellate morphotypes of the Mediterranean gorgonian Eunicella singularis . Marine Biology, 159, 1485-1496.
Grilli, F., Pinardi, N., 1998. The computation of Rossby radii of deformation for the Mediterranean Sea. MTP News, 4-5.
Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W. et al., 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance PhyML 3.0. Systematic Biology, 59 (3), 307321.
Guizien, K., Bramanti, L., 2014. Modelling ecological complexity for marine species conservation: The effect of variable connectivity on species spatial distribution and age-structure. Theoretical Biology Forum, 107, 47-56.
Hebert, P.D.N., Cywinska, A., Ball, S. L., deWaard, J.R., 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270 (1512), 313-321.
Hellberg, M.E., Burton, R.S., Neigel, J.E., Palumbi, S.R., 2002. Genetic assessment of connectivity among marine populations. Bulletin of Marine Science, 70 (1), 273-290.
Hilário, A., Metaxas, A., Gaudron, S.M., Howell, K.L., Mercier, A. et al., 2015. Estimating dispersal distance in the deep sea: Challenges and applications to marine reserves. Frontiers in Marine Science, 2, 6.
Huang, D., Meier, R., Todd, P.A., Chou, L.M., 2008. Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA Barcoding. Journal of Molecular Evolution, 66 (2), 167-174.
Huret, M., Runge, J., Chen, C., Cowles, G., Xu, Q., et al. 2007. Dispersal modeling of fish early life stages: Sensitivity with application to Atlantic cod in the western Gulf of Maine. Marine Ecology Progress Series, 347, 261-274.. ICES, 2020. Workshop on EU regulatory area options for VME protection.
Katoh, K., Rozewicki, J., Yamada, K.D., 2019. MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, 20 (4), 1160-1166.
Kenchington, E., Wang, Z., Lirette, C., Murillo, F.J., Guijarro, J. et al., 2019. Connectivity modelling of areas closed to protect vulnerable marine ecosystems in the northwest Atlantic. Deep Sea Research Part I: Oceanographic Research Papers, 143, 85-103.
Korfhage, S.A., Rossel, S., Brix, S., McFadden, C.S., Ólafsdóttir, S.H. et al., 2022. Species delimitation of Hexacorallia and Octocorallia around Iceland using nuclear and mitochondrial DNA and proteome fingerprinting. Frontiers in Marine Science, 9, 838201.
Lacorata, G., Mazzino, A., Rizza, U., 2008. 3D chaotic model for sub-grid turbulent dispersion in large eddy simulations. Journal of the Atmospheric Sciences, 65 (7), 2389-2401.
Lacorata, G., Palatella, L., Santoleri, R., 2014. Lagrangian predictability characteristics of an Ocean Model. Journal of Geophysical Research: Oceans, 119 (11), 8029-038.
Laubier, L., Emig, C.C., 1993. La faune benthique profonde de Méditerranée, 397-428.
Lauria, V., Garofalo, G., Fiorentino, F., Massi, D., Milisenda, G. et al., 2017. Species distribution models of two critically endangered deep-sea octocorals reveal fishing impacts on vulnerable marine ecosystems in central Mediterranean Sea. Scientific Reports, 7 (1), 1-14.
Ledoux, J.B., Mokhtar-Jamaï, K., Roby, C., Féral, J.P., Garrabou, J. et al., 2010a. Genetic survey of shallow populations of the Mediterranean red coral [Corallium rubrum (Linnaeus, 1758)]: new insights into evolutionary processes shaping nuclear diversity and implications for conservation. Molecular Ecology, 19 (4), 675-90.
Ledoux, J.B., Garrabou, J., Bianchimani, O., Drap, P., Féral, J.P. et al., 2010b. Fine-scale genetic structure and inferences on population biology in the threatened Mediterranean red coral, Corallium rubrum. Molecular Ecology, (19), 4204-4216.
Le Goff-Vitry, M.C., Pybus, O. G., Rogers, A.D., 2004. Genetic structure of the deep-sea coral Lophelia pertusa in the northeast Atlantic revealed by microsatellites and internal transcribed spacer sequences. Molecular Ecology, 13 (3), 537-549.
Lejeusne, C., Chevaldonné, P., Pergent-Martini, C., Boudouresque, C.F., Pérez, T., 2010. Climate change effects on a miniature ocean: The highly diverse, highly impacted Mediterranean Sea. Trends in Ecology & Evolution, 25 (4), 250-260.
Leis, J.M., 2021. Perspectives on larval behaviour in biophysical modelling of larval 588 dispersal in marine, demersal fishes. Oceans, 2 (1),1 -25.
Liao, D., 1999. Concerted evolution: molecular mechanism and biological implications. American Journal of Human Genetics, 64, 24-30.
Linares, C., Coma, R., Mariani, S., Díaz, D., Hereu, B. et al., 2008. Early life history of the Mediterranean gorgonian Paramuricea clavata: implications for population dynamics. Invertebrate Biology, 127, 1-11.
Mackenzie, C.L., Kent, F.E.A., Baxter, J.M., Gormley, K.S.G., Cassidy, A.J. et al., 2022. Genetic connectivity and diversity of a protected, habitat-forming species: evidence demonstrating the need for wider environmental protection and integration of the marine protected area network. Frontiers in Marine Science, 9, 772259.
Martínez-Quintana, A., Bramanti, L., Viladrich, N., Rossi, S., Guizien, K., 2015. Quantification of larval traits driving connectivity: The case of Corallium rubrum (L. 1758). Marine Biology, 162 (2), 309-318.
Mastrototaro, F., Chimienti, G., Acosta, J., Blanco, J., Garcia, S. et al., 2017. Isidella elongata (Cnidaria: Alcyonacea) facies in the western Mediterranean Sea: Visual surveys and descriptions of its ecological role. The European Zoological Journal, 84 (1), 209-225.
Maynou, F., Cartes, J.E., 2012. Effects of trawling on fish and invertebrates from deep-sea coral facies of Isidella elongata in the western Mediterranean. Journal of the Marine Biological Association of the United Kingdom, 92, 1501-1507.
Metaxas, A., Lacharité, M., de Mendonça, S.N., 2019. Hydrodynamic connectivity of habitats of deep-water corals in Corsair Canyon, northwest Atlantic: a case for cross-boundary conservation. Frontiers in Marine Science, 6, 159.
Millot, J., Georges, V., Lauria, V., Hattab, T., Dominguez-Carrió, C. et al. 2024. Habitat shifts of the vulnerable crinoid Leptometra phalangium under climate change scenarios. Progress in Oceanography, 229, 103355.
Mokthar-Jamai, K., Pascual, M., Ledoux, J.B., Coma, R., Féral, J.P. et al., 2011. From global to local genetic structuring in the red gorgonian Paramuricea clavata: the interplay between oceanographic conditions and limited larval dispersal. Molecular Ecology, 20, 3291-3305.
Mokhtar-Jamai, K., Coma, R., Wang, J., Zuberer F., Féral, J.P. et al., 2013. Role of evolutionary and ecological factors in the reproductive success and the spatial genetic structure of the temperate gorgonian Paramuricea clavata. Ecology and Evolution, 3 (6), 1765-1779.
Mulla, A.J., Lin, C.-H., Takahashi, S., Nozawa, Y., 2020. Species-specific phototaxis of coral larvae causes variation in vertical positioning during dispersal. bioRxiv, 2020.07.31.230235.
Mytilineou, C., Smith, C.J., Anastasopoulou, A., Papadopoulou, K.N., Christidis, G., 2014. New cold-water coral occurrences in the Eastern Ionian Sea: Results from experimental long line fishing. Deep-Sea Research Part I: Oceanographic Research Papers, 99, 146-157.
Otero, M.M., Numa, M., Orejas, C., Garrabou, J., Cerrano, C. et al., 2017. Overview of the conservation status of Mediterranean anthozoans. IUCN International Union for Conservation of Nature.
Palatella, L., Bignami, F., Falcini, F., Lacorata, G., Lanotte, A.S. et al., 2014. Lagrangian simulations and interannual variability of anchovy egg and larva dispersal in the Sicily Channel. Journal of Geophysical Research: Oceans, 119 (2), 1306-1323.
Pineda, J., Hare, J.A., Sponaugle, S., 2007. Larval transport and dispersal in the coastal ocean and consequences for population connectivity. Oceanography, 20, 22-39.
Pont-Kingdon, G.A., Okada, N.A., Macfarlane, J.L., Beagley, C.T., Wolstenholme, D.R. et al., 1995. A coral mitochondrial mutS gene. Nature, 375 (6527), 109-111.
Quattrocchi, G., Sinerchia, M., Colloca, F., Fiorentino, F., Garofalo, G. et al., 2019. Hydrodynamic controls on connectivity of the high commercial value shrimp Parapenaeus longirostris (Lucas, 1846) in the Mediterranean Sea. Scientific Reports, 9 (1), 16935.
Queiroga, H., Cruz, T., Santos, A. dos, Dubert, J., González-Gordillo, et al., 2007. Oceanographic and behavioural processes affecting invertebrate larval dispersal and supply in the western Iberia upwelling ecosystem. Progress in Oceanography, 74 (2), 174-191.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A. et al., 2012. MrBayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61 (3), 539-542. Rossi, L., 1971. Cnidari e ctenofori d’Italia (2; pp. 77-92). Quaderni della Civica Stazione Idrobiologica di Milano.
Rueda, J. L., Urra, J., Aguilar, R., Angeletti, L., Bo, M. et al., 2019. Cold-Water Coral Associated Fauna in the Mediterranean Sea and Adjacent Areas. In C. Orejas, C. Jiménez (Eds.), Mediterranean Cold-Water Corals: Past, Present and Future. Springer International Publishing.
Sánchez, J.A., McFadden, C.S., France, S.C., Lasker, H.R., 2003. Molecular phylogenetic analyses of shallow-water Caribbean octocorals. Marine Biology, 142 (5), 975-987.
Saucier, E.H., 2016. Phylogenetic studies of the deep-sea bamboo corals (Octocorallia: Isididae: Keratoisidinae). Doctor of Philosophy Dissertation]. Graduate Faculty of the University of Louisiana at Lafayette.
Sciascia, R., Guizien, K., Magaldi, M.G., 2022. Larval dispersal simulations and connectivity predictions for Mediterranean gorgonian species: Sensitivity to flow representation and biological traits. ICES Journal of Marine Science, 79 (7), 2043-2054.
Shearer, T.L., van Oppen, M.J.H., Romano, S.L., Wörheide, G., 2002. Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Molecular Ecology, 11(12), 2475-2487.
Spöri, Y., Flot, J.F., 2020. HaplowebMaker and CoMa: Two web tools to delimit species using haplowebs and conspecificity matrices. Methods in Ecology and Evolution, 11 (11), 1434-1438.
Spöri, Y., Flot, J.F., 2024. Champuru 2: Improved scoring of alignments and a user-friendly graphical interface. arXiv preprint arXiv:2405.06032.
Tamura, K., Stecher, G., Kumar, S., 2021. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution, 38 (7), 3022-3027.
Terrana, L., Flot, J.F., Eeckhaut, I., 2021. ITS1 variation among Stichopathes cf. maldivensis (Hexacorallia: Antipatharia) whip black corals unveils conspecificity and population connectivity at local and global scales across the Indo-Pacific. Coral Reefs, 40 (2), 521-533.
Thompson, J. D., Higgins, D. G., Gibson, T. J., 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position- specific gap penalties and weight matrix choice. Nucleic Acids Research, 22 (22), 4673-4680.
Torri, M., Russo, S., Falcini, F., De Luca, B., Colella, S. et al., 2023. Coupling Lagrangian simulation models and remote sensing to explore the environmental effect on larval growth rate: The Mediterranean case study of round sardinella (Sardinella aurita) early life stages. Frontiers in Marine Science, 9, 1065514.
Wang, S., Murillo, F.J., Kenchington, E., 2022. Climate-change refugia for the bubblegum coral Paragorgia arborea in the Northwest Atlantic. Frontiers in Marine Science, 9, 863693.
White, C., Selkoe, K.A., Watson, J., Siegel, D.A., Zacherl, D.C. et al., 2010. Ocean currents help explain population genetic structure. Proceedings of the Royal Society B: Biological Sciences, 277 (1688), 1685-1694.
