{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,18]],"date-time":"2026-05-18T17:22:37Z","timestamp":1779124957774,"version":"3.51.4"},"reference-count":43,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2017,6,2]],"date-time":"2017-06-02T00:00:00Z","timestamp":1496361600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2017,6,2]],"date-time":"2017-06-02T00:00:00Z","timestamp":1496361600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Past environmental conditions in the Mediterranean Sea have been proposed as main drivers of the current patterns of distribution of genetic structure of the seagrass <jats:italic>Posidonia oceanica<\/jats:italic>, the foundation species of one of the most important ecosystems in the Mediterranean Sea. Yet, the location of cold climate refugia (persistence regions) for this species during the Last Glacial Maximum (LGM) is not clear, precluding the understanding of its biogeographical history. We used Ecological Niche Modelling together with existing phylogeographic data to locate Pleistocene refugia in the Mediterranean Sea and to develop a hypothetical past biogeographical distribution able to explain the genetic diversity presently found in <jats:italic>P. oceanica<\/jats:italic> meadows. To do that, we used an ensemble approach of six predictive algorithms and two Ocean General Circulation Models. The minimum SST in winter and the maximum SST in summer allowed us to hindcast the species range during the LGM. We found separate glacial refugia in each Mediterranean basin and in the Central region. Altogether, the results suggest that the Central region of the Mediterranean Sea was the most relevant cold climate refugium, supporting the hypothesis that long-term persistence there allowed the region to develop and retain its presently high proportion of the global genetic diversity of <jats:italic>P. oceanica<\/jats:italic>.<\/jats:p>","DOI":"10.1038\/s41598-017-03006-2","type":"journal-article","created":{"date-parts":[[2017,5,26]],"date-time":"2017-05-26T11:57:19Z","timestamp":1495799839000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":37,"title":["Palaeoclimatic conditions in the Mediterranean explain genetic diversity of Posidonia oceanica seagrass meadows"],"prefix":"10.1038","volume":"7","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5031-4858","authenticated-orcid":false,"given":"Rosa M.","family":"Chefaoui","sequence":"first","affiliation":[]},{"given":"Carlos M.","family":"Duarte","sequence":"additional","affiliation":[]},{"given":"Ester A.","family":"Serr\u00e3o","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2017,6,2]]},"reference":[{"key":"3006_CR1","doi-asserted-by":"publisher","first-page":"e11842","DOI":"10.1371\/journal.pone.0011842","volume":"5","author":"M Coll","year":"2010","unstructured":"Coll, M. et al. The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats. PLoS One 5, e11842 (2010).","journal-title":"PLoS One"},{"key":"3006_CR2","doi-asserted-by":"publisher","unstructured":"Templado, J. In The Mediterranean Sea: Its History and Present Challenges 479\u2013498 (Springer Netherlands, 2014), doi:10.1007\/978-94-007-6704-1_28.","DOI":"10.1007\/978-94-007-6704-1_28"},{"key":"3006_CR3","first-page":"4426","volume-title":"Molecular Ecology","author":"T Patarnello","year":"2007","unstructured":"Patarnello, T., Volckaert, F. A. M. J. & Castilho, R. Pillars of Hercules: Is the Atlantic-Mediterranean transition a phylogeographical break? Molecular Ecology 16, 4426\u20134444 (2007)."},{"key":"3006_CR4","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1016\/S0079-6611(99)00030-0","volume":"44","author":"R Danovaro","year":"1999","unstructured":"Danovaro, R., Dinet, A., Duineveld, G. & Tselepides, A. Benthic response to particulate fluxes in different trophic environments: a comparison between the Gulf of Lions\u2013Catalan Sea (western-Mediterranean) and the Cretan Sea (eastern-Mediterranean). Prog. Oceanogr. 44, 287\u2013312 (1999).","journal-title":"Prog. Oceanogr."},{"key":"3006_CR5","doi-asserted-by":"publisher","first-page":"1279","DOI":"10.1111\/j.1365-2699.2007.01876.x","volume":"35","author":"F Alberto","year":"2008","unstructured":"Alberto, F. et al. Genetic differentiation and secondary contact zone in the seagrass Cymodocea nodosa across the Mediterranean-Atlantic transition region. J. Biogeogr 35, 1279\u20131294 (2008).","journal-title":"J. Biogeogr"},{"key":"3006_CR6","doi-asserted-by":"publisher","first-page":"929","DOI":"10.1098\/rspb.2000.1092","volume":"267","author":"L Bahri-Sfar","year":"2000","unstructured":"Bahri-Sfar, L., Lemaire, C., Ben Hassine, O. K. & Bonhomme, F. Fragmentation of sea bass populations in the western and eastern Mediterranean as revealed by microsatellite polymorphism. Proc. Biol. Sci 267, 929\u201335 (2000).","journal-title":"Proc. Biol. Sci"},{"key":"3006_CR7","doi-asserted-by":"publisher","first-page":"485","DOI":"10.1111\/maec.12156","volume":"36","author":"S Valente","year":"2015","unstructured":"Valente, S., Serr\u00e3o, E. A. & Gonz\u00e1lez-Wang\u00fcemert, M. West versus East Mediterranean Sea: origin and genetic differentiation of the sea cucumber Holothuria polii. Mar. Ecol. 36, 485\u2013495 (2015).","journal-title":"Mar. Ecol."},{"key":"3006_CR8","doi-asserted-by":"publisher","first-page":"771","DOI":"10.1111\/bij.12099","volume":"109","author":"L Ragionieri","year":"2013","unstructured":"Ragionieri, L. & Schubart, C. D. Population genetics, gene flow, and biogeographical boundaries of Carcinus aestuarii (Crustacea: Brachyura: Carcinidae) along the European Mediterranean coast. Biol. J. Linn. Soc. 109, 771\u2013790 (2013).","journal-title":"Biol. J. Linn. Soc."},{"key":"3006_CR9","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1007\/s00227-003-1088-6","volume":"143","author":"R Nikula","year":"2003","unstructured":"Nikula, R. & V\u00e4in\u00f6l\u00e4, R. Phylogeography of Cerastoderma glaucum (Bivalvia: Cardiidae) across Europe: A major break in the Eastern Mediterranean. Mar. Biol. 143, 339\u2013350 (2003).","journal-title":"Mar. Biol."},{"key":"3006_CR10","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1016\/j.marpolbul.2013.07.044","volume":"75","author":"P Vassallo","year":"2013","unstructured":"Vassallo, P. et al. The value of the seagrass Posidonia oceanica: A natural capital assessment. Mar. Pollut. Bull. 75, 157\u2013167 (2013).","journal-title":"Mar. Pollut. Bull."},{"key":"3006_CR11","doi-asserted-by":"publisher","first-page":"203","DOI":"10.3354\/meps137203","volume":"137","author":"N Marb\u00e0","year":"1996","unstructured":"Marb\u00e0, N. et al. Growth and population dynamics of Posidonia oceanica on the Spanish Mediterranean coast: elucidating seagrass decline. Mar. Ecol. Prog. Ser. 137, 203\u2013213 (1996).","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"3006_CR12","first-page":"328","volume":"7","author":"C-F Boudouresque","year":"2000","unstructured":"Boudouresque, C.-F. et al. A monitoring network based on the seagrass Posidonia oceanica in the northwestern Mediterranean Sea. Biol. Mar. Mediterr 7, 328\u2013331 (2000).","journal-title":"Biol. Mar. Mediterr"},{"key":"3006_CR13","doi-asserted-by":"publisher","first-page":"192","DOI":"10.1017\/S0376892902000127","volume":"29","author":"CM Duarte","year":"2002","unstructured":"Duarte, C. M. The future of seagrass meadows. Environ. Conserv. 29, 192\u2013206 (2002).","journal-title":"Environ. Conserv."},{"key":"3006_CR14","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1016\/j.biocon.2014.05.024","volume":"176","author":"N Marb\u00e0","year":"2014","unstructured":"Marb\u00e0, N., D\u00edaz-Almela, E. & Duarte, C. M. Mediterranean seagrass (Posidonia oceanica) loss between 1842 and 2009. Biol. Conserv. 176, 183\u2013190 (2014).","journal-title":"Biol. Conserv."},{"key":"3006_CR15","doi-asserted-by":"publisher","first-page":"963","DOI":"10.1111\/j.1365-2699.2006.01671.x","volume":"34","author":"S Arnaud-Haond","year":"2007","unstructured":"Arnaud-Haond, S. et al. Vicariance patterns in the Mediterranean Sea: East-west cleavage and low dispersal in the endemic seagrass Posidonia oceanica. J. Biogeogr. 34, 963\u2013976 (2007).","journal-title":"J. Biogeogr."},{"key":"3006_CR16","doi-asserted-by":"publisher","first-page":"18824","DOI":"10.1073\/pnas.0805571105","volume":"105","author":"AF Rozenfeld","year":"2008","unstructured":"Rozenfeld, A. F. et al. Network analysis identifies weak and strong links in a metapopulation system. Proc. Natl. Acad. Sci. USA 105, 18824\u20139 (2008).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"3006_CR17","doi-asserted-by":"publisher","first-page":"557","DOI":"10.1111\/j.1365-294X.2009.04462.x","volume":"19","author":"IA Serra","year":"2010","unstructured":"Serra, I. A. et al. Genetic structure in the Mediterranean seagrass Posidonia oceanica: Disentangling past vicariance events from contemporary patterns of gene flow. Mol. Ecol 19, 557\u2013568 (2010).","journal-title":"Mol. Ecol"},{"key":"3006_CR18","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1006\/ecss.1996.0116","volume":"44","author":"MA Mateo","year":"1997","unstructured":"Mateo, M. A., Romero, J., P\u00e9rez, M., Littler, M. M. & Littler, D. S. Dynamics of Millenary Organic Deposits Resulting from the Growth of the Mediterranean Seagrass Posidonia oceanica. Estuar. Coast. Shelf Sci. 44, 103\u2013110 (1997).","journal-title":"Estuar. Coast. Shelf Sci."},{"key":"3006_CR19","doi-asserted-by":"publisher","first-page":"e30454","DOI":"10.1371\/journal.pone.0030454","volume":"7","author":"S Arnaud-Haond","year":"2012","unstructured":"Arnaud-Haond, S. et al. Implications of extreme life span in clonal organisms: millenary clones in meadows of the threatened seagrass Posidonia oceanica. PLoS One 7, e30454 (2012).","journal-title":"PLoS One"},{"key":"3006_CR20","doi-asserted-by":"publisher","first-page":"1713","DOI":"10.1111\/j.1365-294X.2007.03228.x","volume":"16","author":"SS Jakob","year":"2007","unstructured":"Jakob, S. S., Ihlow, A. & Blattner, F. R. Combined ecological niche modelling and molecular phylogeography revealed the evolutionary history of Hordeum marinum (Poaceae) - Niche differentiation, loss of genetic diversity, and speciation in Mediterranean Quaternary refugia. Mol. Ecol 16, 1713\u20131727 (2007).","journal-title":"Mol. Ecol"},{"key":"3006_CR21","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1111\/j.1095-8312.1999.tb01160.x","volume":"68","author":"G Hewitt","year":"1999","unstructured":"Hewitt, G. Post-glacial re-colonization of European biota. Biol. J. Linn. Soc 68, 87\u2013112 (1999).","journal-title":"Biol. J. Linn. Soc"},{"key":"3006_CR22","doi-asserted-by":"publisher","first-page":"1137","DOI":"10.1111\/jbi.12278","volume":"41","author":"J Neiva","year":"2014","unstructured":"Neiva, J., Assis, J., Fernandes, F., Pearson, G. A. & Serr\u00e3o, E. A. Species distribution models and mitochondrial DNA phylogeography suggest an extensive biogeographical shift in the high-intertidal seaweed Pelvetia canaliculata. J. Biogeogr. 41, 1137\u20131148 (2014).","journal-title":"J. Biogeogr."},{"key":"3006_CR23","doi-asserted-by":"publisher","first-page":"e0131530","DOI":"10.1371\/journal.pone.0131530","volume":"10","author":"J Neiva","year":"2015","unstructured":"Neiva, J. et al. Genes left behind: Climate change threatens cryptic genetic diversity in the canopy-forming seaweed Bifurcaria bifurcata. PLoS One 10, e0131530 (2015).","journal-title":"PLoS One"},{"key":"3006_CR24","doi-asserted-by":"publisher","first-page":"833","DOI":"10.1111\/jbi.12677","volume":"43","author":"J Assis","year":"2016","unstructured":"Assis, J. et al. Deep reefs are climatic refugia for genetic diversity of marine forests. J. Biogeogr. 43, 833\u2013844 (2016).","journal-title":"J. Biogeogr."},{"key":"3006_CR25","doi-asserted-by":"publisher","first-page":"2797","DOI":"10.1111\/mec.12772","volume":"23","author":"J Assis","year":"2014","unstructured":"Assis, J., Serr\u00e3o, Ea, Claro, B., Perrin, C. & Pearson, G. Climate-driven range shifts explain the distribution of extant gene pools and predict future loss of unique lineages in a marine brown alga. Mol. Ecol. 23, 2797\u2013810 (2014).","journal-title":"Mol. Ecol."},{"key":"3006_CR26","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1016\/j.palaeo.2009.10.015","volume":"285","author":"I Rouis-Zargouni","year":"2010","unstructured":"Rouis-Zargouni, I. et al. Environmental and climatic changes in the central Mediterranean Sea (Siculo\u2013Tunisian Strait) during the last 30ka based on dinoflagellate cyst and planktonic foraminifera assemblages. Palaeogeogr. Palaeoclimatol. Palaeoecol 285, 17\u201329 (2010).","journal-title":"Palaeogeogr. Palaeoclimatol. Palaeoecol"},{"key":"3006_CR27","doi-asserted-by":"publisher","first-page":"12505","DOI":"10.1038\/srep12505","volume":"5","author":"L Telesca","year":"2015","unstructured":"Telesca, L. et al. Seagrass meadows (Posidonia oceanica) distribution and trajectories of change. Sci. Rep 5, 12505 (2015).","journal-title":"Sci. Rep"},{"key":"3006_CR28","doi-asserted-by":"crossref","unstructured":"Pergent, G. et al. Posidonia oceanica. The IUCN Red List of Threatened Species 2016: e.T153534A76571834, http:\/\/dx.doi.org\/10.2305\/IUCN.UK.2016-1.RLTS.T153534A76571834.en (2016).","DOI":"10.2305\/IUCN.UK.2016-1.RLTS.T153534A76571834.en"},{"key":"3006_CR29","first-page":"34","volume":"13","author":"B Celebi","year":"2006","unstructured":"Celebi, B., Gucu, A. C., Ok, M., Sakinan, S. & Akoglu, E. Hydrographic indications to understand the absence of Posidonia oceanica in the Levant Sea (Eastern Mediterranean). Biol. Mar. Mediterr 13, 34\u201338 (2006).","journal-title":"Biol. Mar. Mediterr"},{"key":"3006_CR30","doi-asserted-by":"publisher","first-page":"2366","DOI":"10.1111\/j.1365-2486.2009.02130.x","volume":"16","author":"N Marb\u00e0","year":"2010","unstructured":"Marb\u00e0, N. & Duarte, C. M. Mediterranean warming triggers seagrass (Posidonia oceanica) shoot mortality. Glob. Chang. Biol 16, 2366\u20132375 (2010).","journal-title":"Glob. Chang. Biol"},{"key":"3006_CR31","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1007\/s12237-015-9966-y","volume":"39","author":"RM Chefaoui","year":"2016","unstructured":"Chefaoui, R. M., Assis, J., Duarte, C. M. & Serr\u00e3o, E. A. Large-Scale Prediction of Seagrass Distribution Integrating Landscape Metrics and Environmental Factors: The Case of Cymodocea nodosa (Mediterranean\u2013Atlantic). Estuaries and Coasts 39, 123\u2013137 (2016).","journal-title":"Estuaries and Coasts"},{"key":"3006_CR32","doi-asserted-by":"publisher","first-page":"821","DOI":"10.1038\/nclimate1533","volume":"2","author":"G Jord\u00e0","year":"2012","unstructured":"Jord\u00e0, G., Marb\u00e0, N. & Duarte, C. M. Mediterranean seagrass vulnerable to regional climate warming. Nat. Clim. Chang 2, 821\u2013824 (2012).","journal-title":"Nat. Clim. Chang"},{"key":"3006_CR33","doi-asserted-by":"publisher","first-page":"919","DOI":"10.1038\/nclimate1958","volume":"3","author":"ES Poloczanska","year":"2013","unstructured":"Poloczanska, E. S. et al. Global imprint of climate change on marine life. Nat. Clim. Chang 3, 919\u2013925 (2013).","journal-title":"Nat. Clim. Chang"},{"key":"3006_CR34","doi-asserted-by":"publisher","first-page":"652","DOI":"10.1126\/science.1210288","volume":"334","author":"MT Burrows","year":"2011","unstructured":"Burrows, M. T. et al. The pace of shifting climate in marine and terrestrial ecosystems. Science 334, 652\u20135 (2011).","journal-title":"Science"},{"key":"3006_CR35","doi-asserted-by":"publisher","first-page":"492","DOI":"10.1038\/nature12976","volume":"507","author":"MT Burrows","year":"2014","unstructured":"Burrows, M. T. et al. Geographical limits to species-range shifts are suggested by climate velocity. Nature 507, 492\u2013495 (2014).","journal-title":"Nature"},{"key":"3006_CR36","unstructured":"Ruiz, J. M., Guill\u00e9n, E., Ramos Segura, A. & Otero, M. Atlas de las praderas marinas de Espa\u00f1a, http:\/\/www.ieo.es\/atlas-praderas-marinas (2015)."},{"key":"3006_CR37","doi-asserted-by":"publisher","unstructured":"Stark, J. D., Donlon, C. J., Martin, M. J. & McCulloch, M. E. OSTIA: An operational, high resolution, real time, global sea surface temperature analysis system. in OCEANS 2007 - Europe 1\u20134, doi:10.1109\/OCEANSE.2007.4302251 (IEEE, 2007).","DOI":"10.1109\/OCEANSE.2007.4302251"},{"key":"3006_CR38","unstructured":"Thuiller, W., Georges, D. & Engler, R. biomod2: Ensemble platform for species distribution modeling, http:\/\/cran.r-project.org\/package=biomod2 (2014)."},{"key":"3006_CR39","doi-asserted-by":"publisher","first-page":"478","DOI":"10.1016\/j.ecolmodel.2007.08.010","volume":"210","author":"RM Chefaoui","year":"2008","unstructured":"Chefaoui, R. M. & Lobo, J. M. Assessing the effects of pseudo-absences on predictive distribution model performance. Ecol. Modell 210, 478\u2013486 (2008).","journal-title":"Ecol. Modell"},{"key":"3006_CR40","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1017\/S0376892997000088","volume":"24","author":"AH Fielding","year":"1997","unstructured":"Fielding, A. H. & Bell, J. F. A review of methods for the assessment of prediction errors in conservation presence\/absence models. Ecol. Conserv 24, 38\u201349 (1997).","journal-title":"Ecol. Conserv"},{"key":"3006_CR41","doi-asserted-by":"publisher","first-page":"1223","DOI":"10.1111\/j.1365-2664.2006.01214.x","volume":"43","author":"O Allouche","year":"2006","unstructured":"Allouche, O., Tsoar, A. & Kadmon, R. Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). J. Appl. Ecol 43, 1223\u20131232 (2006).","journal-title":"J. Appl. Ecol"},{"key":"3006_CR42","unstructured":"Liaw, A. & Wiener, M. Classification and Regression by randomForest. 23 (2002)."},{"key":"3006_CR43","unstructured":"R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http:\/\/www.r-project.org\/ (2016)."}],"updated-by":[{"DOI":"10.1038\/s41598-020-62684-7","type":"correction","label":"Correction","source":"publisher","updated":{"date-parts":[[2020,4,3]],"date-time":"2020-04-03T00:00:00Z","timestamp":1585872000000}}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-03006-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-03006-2","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-03006-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,23]],"date-time":"2022-12-23T04:48:40Z","timestamp":1671770920000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-03006-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,6,2]]},"references-count":43,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2017,12]]}},"alternative-id":["3006"],"URL":"https:\/\/doi.org\/10.1038\/s41598-017-03006-2","relation":{"correction":[{"id-type":"doi","id":"10.1038\/s41598-020-62684-7","asserted-by":"object"}]},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,6,2]]},"assertion":[{"value":"18 January 2017","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 April 2017","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 June 2017","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 April 2020","order":4,"name":"change_date","label":"Change Date","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Correction","order":5,"name":"change_type","label":"Change Type","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"An amendment to this paper has been published and can be accessed via a link at the top of the paper.","order":6,"name":"change_details","label":"Change Details","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare that they have no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing Interests"}}],"article-number":"2732"}}