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Contrasting evolutionary patterns in populations of demersal sharks throughout the western Mediterranean

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Abstract

The spotted catshark (Scyliorhinus canicula) and the blackmouth catshark (Galeus melastomus) are demersal sharks showing a distinct bathymetric distribution in the western Mediterranean. Together, both species represent more than 85% of the total abundance of demersal chondrichthyans in this Mediterranean basin. Our study provides a complete analysis of the genetic population structure, connectivity and demographic history of both species. Sampling was performed across four geographical subareas (GSAs) established by the General Fisheries Commission for the Mediterranean in the western Mediterranean: the northern Alboran Sea (GSA01), Alboran Island (GSA02), Balearic Islands (GSA05) and northern Spain (GSA06). Three mitochondrial fragments were analyzed for both species, and 12 microsatellite loci for S. canicula. We found contrasting patterns of population structure and connectivity in both species. Scyliorhinus canicula displayed significant genetic differences and low connectivity between some GSAs corresponding to different sub-basins (Alboran vs. Balearic). In contrast, G. melastomus showed absence of a population structure and high connectivity between GSAs. These findings are in accordance with the fact that both species exhibit different dispersal behaviors, which leads to distinct bathymetric distributions. Contrasting demographic histories were also identified: Scyliorhinus canicula revealed a recent stable population, with evidence of bottlenecks in the past, which may be related to Pleistocene glacial periods; whereas G. melastomus showed a recent population expansion. Altogether, our findings indicate a mismatch between fishery subareas and population structure for both sharks, which must be considered for fisheries management purposes.

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References

  • Alcántara-Carrió J, Albarracín S, Montoya-Montes I, Flor-Blanco G, Fontán-Bouzas A, Rey-Salgado J (2013) An indurated Pleistocene coastal barrier on the inner shelf on the Gulf of Valencia (western Mediterranean): evidence for a prolonged relative sea-level stillstand. Geo Mar Lett 33:209–216

    Article  Google Scholar 

  • Arenas M, Ray N, Currat M, Excoffier L (2012) Consequences of range contractions and range shifts on molecular diversity. Mol Biol Evol 29:207–218

    Article  CAS  Google Scholar 

  • Arenas M, Mona S, Trochet A, Sramkova Hanulova A, Currat M, Ray N, Chikhi L, Rasteiro R, Schmeller DS, Excoffier L (2014) The scaling of genetic diversity in a changing and fragmented world. In: Henle K, Potts SG, Kunin WE, Matsinos YG, Similä J, Pantis JD, Grobelnik V, Penev L, Settele J (eds) Scaling in ecology and biodiversity conservation. Pensoft Publishers, Sofia, pp 55–60

    Google Scholar 

  • Barbieri M, Maltagliati F, Roldán MI, Castelli A (2014) Molecular contribution to stock identification in the small-spotted catshark, Scyliorhinus canicula (Chondrichthyes, Scyliorhinidae). Fish Res 154:11–16

    Article  Google Scholar 

  • Bargelloni L, Alarcon JA, Alvarez MC, Penzo E, Magoulas A, Reis C, Patarnello T (2003) Discord in the family Sparidae (Teleostei): divergent phylogeographic patterns across the Atlantic–Mediterranean divide. J Evol Biol 16:1149–1158

    Article  CAS  Google Scholar 

  • Baro J, Rueda JL, Díaz del Río V (2012) South Iberian submarine canyons in the Alborán sea: geohabitats, associated communities and fisheries resources. In: Würtz M (ed) Mediterranean submarine canyons: ecology and governance. IUCN, Malaga, pp 145–156

    Google Scholar 

  • Bertrand JA, Gil de Sola L, Papaconstantinou C, Relini G, Souplet A (2002) The general specifications of the MEDITS surveys. Sci Mar 66:9–17

    Article  Google Scholar 

  • Botsford LW, Hastings A, Gaines SD (2001) Dependence of sustainability on the configuration of marine reserves and larval dispersal distance. Ecol Lett 4:144–150

    Article  Google Scholar 

  • Camhi M, Fowler S, Musick J, Bräutigam A, Fordham S (1998) Sharks and their relatives: ecology and conservation. IUCN/SSC Shark Specialist Group, Cambridge

    Google Scholar 

  • Capapé C, Mnasri-Sioudi N, Kamel-Moutalibi O, Boumaïza M, Ben Amor MM, Reynaud C (2014) Production, maturity, reproductive cycle and fecundity of small-spotted catshark, Scyliorhinus canicula (Chondrichthyes: Scyliorhinidae) from the northern coast of Tunisia (Central Mediterranean). J Ichthyol 54:111–126

    Article  Google Scholar 

  • Carbonell A, Alemany F, Merella P, Quetglas A, Román E (2003) The by-catch of sharks in the western Mediterranean (Balearic Islands) trawl fishery. Fish Res 61:7–18

    Article  Google Scholar 

  • Cardinale M, Osio GC (2013) State of fish stocks and fisheries in European waters: status of Mediterranean and Black Sea resources in European waters in 2013. European Commission Joint Research Center, Ispra

    Google Scholar 

  • Chapman DD, Feldheim KA, Papastamatiou YP, Hueter RE (2015) There and back again: a review of residency and return migrations in sharks, with implications for population structure and management. Annu Rev Mar Sci 7:547–570

    Article  Google Scholar 

  • Chevolot M, Hoarau G, Rijnsdorp AD, Stam WT, Olsen JL (2006) Phylogeography and population structure of thornback rays (Raja clavata L., Rajidae). Mol Ecol 15:3693–3705

    Article  CAS  Google Scholar 

  • Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E, Plymouth

    Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  Google Scholar 

  • Corrigan S, Huveneers C, Stow A, Beheregaray B (2016) A multilocus comparative study of dispersal in three codistributed demersal sharks from eastern Australia. Can J Fish Aquat Sci 73:1–10

    Article  Google Scholar 

  • Cowen RK, Lwiza KMM, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: open or closed? Science 287:857–859

    Article  CAS  Google Scholar 

  • Cunha RL, Coscia I, Madeira C, Mariani S, Stefanni S, Castilho R (2012) Ancient divergence in the trans-oceanic deep-sea shark Centroscymnus crepidater. PLoS One 7:e49196

    Article  CAS  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  CAS  Google Scholar 

  • Drummond A, Rambaut A (2007) BEAST: bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  Google Scholar 

  • Dudgeon CL, Broderick D, Ovenden R (2009) IUCN classification zones concord with, but underestimate, the population genetic structure of the zebra shark Stegostoma fasciatum in the Indo-West Pacific. Mol Ecol 18:248–261

    Article  CAS  Google Scholar 

  • Dudgeon CL, Blower DC, Broderick D, Giles JL, Holmes BJ, Kashiwagi T, Krück NC, Morgan JAT, Tillett BJ, Ovenden JR (2012) A review of the application of molecular genetics for fisheries management and conservation of sharks and rays. J Fish Biol 80:1789–1843

    Article  CAS  Google Scholar 

  • Duncan KM, Martin AP, Bowen BW, Couet HG (2006) Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini). Mol Ecol 15:2239–2251

    Article  CAS  Google Scholar 

  • Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Ebert DA, Fowler S, Compagno L (2013) Sharks of the world. Wild Nature Press, Plymouth

    Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) ARLEQUIN ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinf Online 1:47–50

    Article  CAS  Google Scholar 

  • Frankham R, Lees K, Montgomery ME, England PR, Lowe EH, Briscoe DA (1999) Do population size bottlenecks reduce evolutionary potential? Anim Conserv 2:255–260

    Article  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  Google Scholar 

  • Gaida IH (1997) Population structure of the Pacific angel shark, Squatina californica (Squatiniformes: Squatinidae), around the California Channel Islands. Copeia 1:738–744

    Article  Google Scholar 

  • Gaines SD, White C, Carr MH, Palumbi SR (2010) Designing marine reserve networks for both conservation and fisheries management. Proc Natl Acad Sci 107:18286–18293

    Article  CAS  Google Scholar 

  • Goudet J, Perrin N, Waser P (2002) Tests for sex-biased dispersal using bi-parentally inherited genetic markers. Mol Ecol 11:1103–1114

    Article  CAS  Google Scholar 

  • Griffiths AM, Casane D, McHugh M, Wearmounth VJ, Sims DW, Genner MJ (2011) Characterisation of polymorphic microsatellite loci in the small-spotted catshark (Scyliorhinus canicula). Conserv Genet Resour 3:705–709

    Article  Google Scholar 

  • Griffiths AM, Jacoby DMP, Casane D, McHugh M, Croft DP, Genner MJ, Sims DW (2012) First analysis of multiple paternity in an oviparous shark species, the small-spotted catshark (Scyliorhinus canicula L.). J Hered 103:166–173

    Article  Google Scholar 

  • Gubili C, Sims DW, Veríssimo A, Domenici P, Ellis J, Grigoriou P, Johnson AF, McHugh M, Neat F, Satta A, Scarcella G, Serra-Pereira B, Soldo A, Genner MJ, Griffiths AM (2014) A tale of two seas: contrasting patterns of population structure in the small-spotted catshark across Europe. R Soc Open Sci 1:140175

    Article  Google Scholar 

  • Gubili C, Macleod K, Perry W, Hanel P, Batzakas I, Farrell ED, Lynghammar A, Mancusi C, Mariani S, Menezes GM, Neat F, Scarcella G, Griffiths AM (2016) Connectivity in the deep: phylogeography of the velvet belly lanternshark. Deep Sea Res I 115:233–239

    Article  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hanski I (1998) Metapopulation dynamics. Nature 396:41–49

    Article  CAS  Google Scholar 

  • Harpending RC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600

    CAS  Google Scholar 

  • Hoelzel AR, Shivji MS, Magnussen J, Francis MP (2006) Low worldwide genetic diversity in the basking shark (Cetorhinus maximus). Biol Lett 2:639–642

    Article  CAS  Google Scholar 

  • Kousteni V, Kontopoulou M, Megalofonou P (2010) Sexual maturity and fecundity of Scyliorhinus canicula (Linnaeus, 1758) in the Aegean Sea. Mar Biol Res 6:390–398

    Article  Google Scholar 

  • Kousteni V, Kasapidis P, Kotoulas G, Megalofonou P (2014) Strong population genetic structure and contrasting demographic histories for the small-spotted catshark (Scyliorhinus canicula) in the Mediterranean Sea. Heredity 114:333–343

    Article  Google Scholar 

  • Kuhner MK (2006) LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22:768–770

    Article  CAS  Google Scholar 

  • Le Port A, Lavery S (2012) Population structure and phylogeography in the short-tailed stingray, Dasyatis brevicaudata (Hutton 1875), in the Southern hemisphere. J Hered 103:174–185

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  Google Scholar 

  • Lleonart J, Maynou F (2003) Fish stock assessments in the Mediterranean: state of the art. Sci Mar 67:37–49

    Article  Google Scholar 

  • Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237

    Article  Google Scholar 

  • Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247

    Article  CAS  Google Scholar 

  • Lykousis V (2009) Sea-level changes and shelf break prograding sequences during the last 400 ka in the Aegean margins: subsidence rates and palaeogeographic implications. Cont Shelf Res 29:2037–2044

    Article  Google Scholar 

  • Magoulas A, Castilho R, Caetano S, Marcato S, Patarnello T (2006) Mitochondrial DNA reveals a mosaic pattern of phylogeographical structure in Atlantic and Mediterranean populations of anchovy (Engraulis encrasicolus). Mol Phylogenet Evol 39:734–746

    Article  CAS  Google Scholar 

  • Malak DA, Livingstone SR, Pollard D, Polidoro BA, Cuttelod A, Bariche M, Bilecenoglu M, Carpenter KE, Collette BB, Francour P, Goren M, Kara MH, Massutí E, Papaconstantinou C, Tunesi L (2011) Overview of the conservation status of the marine fishes of the Mediterranean Sea. IUCN, Gland

    Google Scholar 

  • Manolopoulou I, Emerson BC (2012) Phylogeographic ancestral inference using the coalescent model on haplotype trees. J Comput Biol 19:745–755

    Article  CAS  Google Scholar 

  • Manolopoulou I, Legarreta L, Emerson BC, Brooks S, Tavaré S (2011) A Bayesian approach to phylogeographic clustering. Interface Focus 1:909–921

    Article  Google Scholar 

  • Massutí E, Olivar MP, Monserrat S, Rueda L, Oliver P (2014) Towards understanding the influence of environmental conditions on demersal resources and ecosystems in the western Mediterranean: motivations, aims and methods of the IDEADOS project. J Mar Syst 138:3–19

    Article  Google Scholar 

  • Millot C (1999) Circulation in the western Mediterranean Sea. J Mar Syst 20:423–442

    Article  Google Scholar 

  • Mona S, Ray N, Arenas M, Excoffier L (2014) Genetic consequences of habitat fragmentation during a range expansion. Heredity 11:291–299

    Article  Google Scholar 

  • Monserrat S, López-Jurado JL, Marcos M (2008) A mesoscale index to describe the regional circulation around the Balearic Islands. J Mar Syst 71:413–420

    Article  Google Scholar 

  • Moranta J, Stefanescu C, Massutí E, Morales-Nin B, Lloris D (1998) Fish community structure and depth-related trends on the continental slope of the Balearic Islands (Algerian basin, western Mediterranean). Mar Ecol Prog Ser 171:247–259

    Article  Google Scholar 

  • Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:373–375

    Article  CAS  Google Scholar 

  • Musick JA, Harbin MM, Compagno LJV (2004) Historical zoogeography of the Selachii. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 33–78

    Chapter  Google Scholar 

  • Nielsen EE, Nielsen PH, Meldrup D, Hansen M (2004) Genetic population structure of turbot (Scophthalmus maximus L.) supports the presence of multiple hybrid zones for marine fishes in the transition zone between the Baltic Sea and the North Sea. Mol Ecol 13:585–595

    Article  Google Scholar 

  • Ordines F, Bauzá M, Sbert M, Roca P, Gianotti M, Massutí E (2014) Red algal beds increase the condition of nekton-benthic fish. J Sea Res 95:115–123

    Article  Google Scholar 

  • Ovenden JR, Berry O, Welch DJ, Buckworth R, Dichmont M (2015) Ocean’s eleven: a critical evaluation of the role of population, evolutionary and molecular genetics in the management of wild fisheries. Fish Fish 16:125–159

    Article  Google Scholar 

  • Padrón M, Guizien K (2016) Modelling the effect of demographic traits and connectivity of the genetic structuration of marines metapopulations of sedentary benthic invertebrates. ICES J Mar Sci 73(7):1935–1945

    Article  Google Scholar 

  • Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    Article  CAS  Google Scholar 

  • Pinot JM, López-Jurado JL, Riera M (2002) The CANALES experiment (1996–1998). Interannual, seasonal and mesoscale variability of the circulation in the Balearic Channels. Prog Oceanogr 55:335–370

    Article  Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Portnoy DS, Heist EJ (2012) Molecular markers: progress and prospects for understanding reproductive ecology in elasmobranchs. J Fish Biol 80:1120–1140

    Article  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  Google Scholar 

  • Rambaut A, Drummond AJ (2009) Tracer version 1.5. [computer program] http://beast.bio.ed.ac.uk/Tracer

  • Ramírez-Amaro S, Ordines F, Terrasa B, Esteban A, García C, Guijarro B, Massutí E (2015) Demersal chondrichthyans in the western Mediterranean: assemblages and biological parameters of their main species. Mar Freshw Res 67:636–652

    Article  Google Scholar 

  • Ramón M, Abelló P, Ordines F, Massutí E (2014) Deep epibenthic communities in two contrasting areas of the Balearic Islands (western Mediterranean). J Mar Syst 138:182–193

    Article  Google Scholar 

  • Reiss H, Hoarau G, Dickey-Collas M, Wolff WJ (2009) Genetic population structure of marine fish: mismatch between biological and fisheries management units. Fish Fish 10:361–395

    Article  Google Scholar 

  • Rey J, Massutí E, Gil de Sola L (2005) Distribution and biology of the blackmouth catshark Galeus melastomus in the Alborán Sea (southwestern Mediterranean). J Northwest Atl Fish Sci 35:215–223

    Article  Google Scholar 

  • Rodríguez-Cabello C, Sánchez F, Fernández A, Olaso I (2004) Is the lesser spotted dogfish (Scyliorhinus canicula) from the Cantabrian Sea a unique stock? Fish Res 69:57–71

    Article  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  Google Scholar 

  • Rohling EJ, Foster GL, Grant KM, Marino G, Roberts AP, Tamisiea ME, Williams F (2014) Sea-level and deep-sea temperature variability over the past 5.3 million years. Nature 508:432–477

    Article  Google Scholar 

  • Rozenfeld AF, Arnaud-Haond S, Hernández-García E, Eguíluz VM, Serrão EA, Duarte CM (2008) Network analysis identifies weak and strong links in a metapopulation system. Proc Natl Acad Sci 105:18824–18829

    Article  Google Scholar 

  • Scacco U, La Messa G, Vacchi M (2010) Body morphometrics, swimming diversity and niche in demersal sharks: a comparative case study from the Mediterranean Sea. Sci Mar 74:37–53

    Article  Google Scholar 

  • Simpfendorfer CA, Kyne PM (2009) Limited potential to recover from overfishing raises concerns for deep-sea sharks, rays and chimaeras. Environ Conserv 36:97–103

    Article  Google Scholar 

  • Sims DW, Nash JP, Morritt D (2001) Movements and activity of male and female dogfish in a tidal sea lough: alternative behavioural strategies and apparent sexual segregation. Mar Biol 139:1165–1175

    Article  Google Scholar 

  • Soria G, Torre-Cosio J, Munguia-Vega A, Marinone SG, Lavín MF, Cinti A, Moreno-Báez M (2014) Dynamic connectivity patterns from an insular marine protected area in the Gulf of California. J Mar Syst 129:248–258

    Article  Google Scholar 

  • Stefanescu C, Lloris D, Rucabado J (1992) Deep-living demersal fishes in the Catalan Sea (western Mediterranean) below a depth of 1000 m. J Nat Hist 26:197–213

    Article  Google Scholar 

  • Tajima F (1989) Statistical methods for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  Google Scholar 

  • Terrasa B, Pérez-Mellado V, Brown RP, Picornell A, Castro JA, Ramon MM (2009) Foundations for conservation of intraspecific genetic diversity revealed by analysis of phylogeographical structure in the endangered endemic lizard Podarcis lilfordi. Divers Distrib 15:207–221

    Article  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  • Treml EA, Halpin PN (2012) Marine population connectivity indentifies ecological neighbors for conservation planning in the Coral Triangle. Conserv Lett 5:441–449

    Article  Google Scholar 

  • Veríssimo A, McDowell JR, Graves JE (2010) Global population structure of the spiny dogfish Squalus acanthias, a temperate shark with an antitropical distribution. Mol Ecol 19:1651–1662

    Article  Google Scholar 

  • Veríssimo A, McDowell JR, Graves JE (2011) Population structure of a deep-water squaloid shark, the Portuguese dogfish (Centroscymnus coelolepis). ICES J Mar Sci 68:555–563

    Article  Google Scholar 

  • Vignaud T, Maynard JA, Leblois R, Meekan MG, Vázquez-Juárez R, Ramírez-Macías D, Pierce S, Rowat D, Berumen ML, Beeravolu C, Baksay S, Planes S (2014) Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline. Mol Ecol 23:2590–2601

    Article  CAS  Google Scholar 

  • Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Jackson JBC, Lotze HK, Micheli F, Palumbi SR, Sala E, Selkoe KA, Stachowicz JJ, Watson R (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314:787–790

    Article  CAS  Google Scholar 

  • Würtz M (2012) Mediterranean submarine canyons: ecology and governance. IUCN, Gland

    Google Scholar 

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Acknowledgements

The authors wish to thank all participants in the MEDITS surveys, as well as the crew of R/V Cornide de Saavedra and the Genetics Laboratory team of the Universitat de les Illes Balears. We also thank Dr. Ioanna Manolopoulou for extensive help with the BPEC analyses and Prof. Antonio Amorim for helpful comments. Three anonymous reviewers and the Editor are also greatly acknowledged for their constructive comments in improving the quality of the manuscript.

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Correspondence to Sergio Ramírez-Amaro.

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This research was supported in part by the Consejo Nacional de Ciencia y Tecnología (CONACyT) of Mexico, through the FPI Fellowship of SRA, the Direcció General de Innovació i Recerca del Govern de les Illes Balears and the European Regional Development Fund (FEDER), through the Special Actions “Introducción de las técnicas moleculares en la identificación de stocks y conectividad de poblaciones marinas” (AAEE030/2012) and “Mejora de los estudios de diversidad íctica en las Islas Baleares mediante técnicas morfológicas y moleculares” (AAEE7/2015), the project DEMBAGOL funded by the European Commission and the Instituto Español de Oceanografía through the Data Collection Framework and the projects ECLIPSAME and CLIFISH funded by the Spanish Ministry of Economy and Competitiveness (Plan Estatal I + D + I; CTM2012-37701 and CTM2015-66400-C3-1R, respectively). MA was supported by the Fundação para a Ciência e a Tecnologia (FCT) of the Portuguese Government through the FCT Starting Grant IF/00955/2014 and by the Spanish Government through the fellowship “Ramón y Cajal” RYC-2015-18241.

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Ramírez-Amaro, S., Picornell, A., Arenas, M. et al. Contrasting evolutionary patterns in populations of demersal sharks throughout the western Mediterranean. Mar Biol 165, 3 (2018). https://doi.org/10.1007/s00227-017-3254-2

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