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Strong genetic isolation despite wide distribution in a commercially exploited coastal shark

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Abstract

The common smoothhound, Mustelus mustelus, is an epibenthic species targeted by fisheries around the world driven by the increasing demand for shark products. Given the wide-spread occurrence of this species and corresponding lack of molecular data in many areas of said distribution, baseline molecular assessments of this commercially important shark may contribute to finer-scale analyses in areas in which this species is targeted. Therefore, population genetic analyses were conducted along the East Atlantic, from the Mediterranean Sea to the south-east coast of Africa, using microsatellite markers and the mitochondrial control region (mtCR). Overall, M. mustelus displayed low to moderate genetic diversity, with the Mediterranean populations appearing to exhibit the lowest mitochondrial diversity, and the west African populations displaying the lowest nuclear diversity. Microsatellite analysis indicated strong genetic differentiation between the three regions, with finer-scale population structure in each region, without correlation between genetic and geographical distance. For the mtCR sequences, a total of 18 haplotypes were identified, with a high degree of divergence discernable between the regions, largely in accordance with the microsatellite data. The study documents a remarkable level of population isolation across a vast area, suggesting little or no present-day connectivity among extant populations. The findings may serve as an essential baseline for global population management and commercial traceability of this threatened shark.

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References

  • Amaral, A. R., L. B. Beheregaray, K. Bilgmann, D. Boutov, L. Freitas, K. M. Robertson, M. Sequeira, K. A. Stockin, M. M. Coelho & L. M. Möller, 2012. Seascape genetics of a globally distributed, highly mobile marine mammal: the short-beaked common dolphin (genus Delphinus). PloS ONE 7: e31482.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avise, J. C., 2012. Molecular Tools. In Avise, J. C. (ed.), Molecular Markers, Natural History and Evolution. Springer, New York: 44–91.

    Google Scholar 

  • Avise, J. C., J. E. Neigel & J. Arnold, 1984. Demographic influences on mitochondrial DNA lineage survivorship in animal populations. Journal of Molecular Evolution 20: 99–105.

    Article  CAS  PubMed  Google Scholar 

  • Bandelt, H. J., F. Peter & A. Röhl, 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology 16: 37–48.

    Article  CAS  Google Scholar 

  • Barker, M. J. & V. Schluessel, 2005. Managing global shark fisheries: suggestions for prioritizing management strategies. Aquatic Conservation: Marine and Freshwater Ecosystems 15: 325–347.

    Article  Google Scholar 

  • Barker, A. M., A. P. Nosal, E. A. Lewallen & R. S. Burton, 2015. Genetic structure of leopard shark (Triakis semifasciata) populations along the Pacific coast of North America. Journal of Experimental Marine Biology and Ecology 472: 151–157.

    Article  Google Scholar 

  • Beerli, P. & M. Palczewski, 2010. Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185: 313–326.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bester-van der Merwe, A. E., D. N. Bitalo, J. M. Cuevas, J. Ovenden, S. Hernández, C. da Silva, M. E. McCord & R. Roodt-Wilding, 2017. Population genetics of southern hemisphere tope shark (Galeorhinus galeus): intercontinental divergence and constrained gene flow at different geographical scales. PLoS ONE 12: e0184481.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bitalo, D. N., S. N. Maduna, C. da Silva, R. Roodt-Wilding & A. E. Bester-van der Merwe, 2015. Differential gene flow patterns for two commercially exploited shark species, tope (Galeorhinus galeus) and common smoothhound (Mustelus mustelus) along the south-west coast of South Africa. Fisheries Research 172: 190–196.

    Article  Google Scholar 

  • Bonfil, R., 2008. The Biology and Ecology of the Silky Shark, Carcharhinus falciformis. In Camhi, M. D., E. K. Pikitch & E. A. Babcock (eds), Sharks of the Open Ocean: Biology, Fisheries and Conservation. Fish and Aquatic Resources Series 13. Blackwell Publishing Ltd., Hoboken: 114–127.

    Chapter  Google Scholar 

  • Boomer, J. J., R. G. Harcourt, M. P. Francis & A. J. Stow, 2012. Genetic divergence, speciation and biogeography of Mustelus (sharks) in the central Indo-Pacific and Australasia. Molecular Phylogenetics and Evolution 64: 697–703.

    Article  PubMed  Google Scholar 

  • Cavanagh, R. D. & C. Gibson, 2007. Overview of the Conservation Status of Cartilaginous Fishes (Chondrichthyans) in the Mediterranean Sea. IUCN, Gland, Switzerland and Malaga: 8–27.

    Book  Google Scholar 

  • Chabot, C. L. & L. G. Allen, 2009. Global population structure of the tope (Galeorhinus galeus) inferred by mitochondrial control region sequence data. Molecular Ecology 18: 545–552.

    Article  CAS  PubMed  Google Scholar 

  • Chabot, C. L., M. Espinoza, I. Mascareñas-Osorio & A. Rocha-Olivares, 2015. The effect of biogeographic and phylogeographic barriers on gene flow in the brown smoothhound shark, Mustelus henlei, in the northeastern Pacific. Ecology and Evolution 5: 1585–1600.

    Article  PubMed  PubMed Central  Google Scholar 

  • Charif, D. & J. R. Lobry, 2007. Seqin R 1.0-3: a contributed package to the R project for statistical computing devoted to biological sequences retrieval and analysis. Structural approaches to sequence evolution. Springer, Berlin, Heidelberg: 207–232.

    Chapter  Google Scholar 

  • Clarke, S. C., M. K. McAllister, E. J. Milner-Gulland, G. P. Kirkwood, C. G. J. Michielsens, D. J. Agnew, E. K. Pikitch, H. Nakano & M. S. Shivji, 2006. Global estimates of shark catches using trade records from commercial markets. Ecology Letters 9: 1115–1126.

    Article  PubMed  Google Scholar 

  • Clarke, C. C., S. A. Karl, R. L. Horn, A. M. Bernard, J. S. Lea, F. H. Hazin, P. A. Prodöhl & M. S. Shivji, 2015. Global mitochondrial DNA phylogeography and population structure of the silky shark, Carcharhinus falciformis. Marine Biology 162: 945–955.

    Article  CAS  Google Scholar 

  • Colloca, F., M. Enea, S. Ragonese & M. Di Lorenzo, 2017. A century of fishery data documenting the collapse of smoothhounds (Mustelus spp.) in the Mediterranean Sea. Aquatic Conservation: Marine and Freshwater Ecosystems 27: 1145–1155.

    Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • da Silva C., 2018. Biology, movement behaviour and spatial dynamics of an exploited population of smoothhound shark Mustelus mustelus around a coastal Marine Protected Area in South Africa. PhD Thesis, University of Cape Town.

  • da Silva, C., S. E. Kerwath, C. G. Attwood, E. B. Thorstad, P. D. Cowley, F. Økland, C. G. Wilke & T. F. Næsje, 2013. Quantifying the degree of protection afforded by a no-take marine reserve on an exploited shark. African Journal of Marine Science 35: 57–66.

    Article  Google Scholar 

  • da Silva, C., A. J. Booth, S. F. J. Dudley, S. E. Kerwath, S. J. Lamberth, R. W. Leslie, M. E. McCord, W. H. H. Sauer & T. Zweig, 2015. The current status and management of South Africa’s chondrichthyan fisheries. African Journal of Marine Science 37: 233–248.

    Article  Google Scholar 

  • Darriba, D., G. L. Taboada, R. Doallo & D. Posada, 2012. JMODELTEST 2: more models, new heuristics and parallel computing. Nature Methods 9: 772.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dent, F. & S. Clarke, 2015. State of the global market for shark products. Food and Agriculture Organization of the United Nations, Rome.

    Google Scholar 

  • Diop, M. & J. Dossa, 2011. 30 years of shark fishing in West Africa: development of fisheries, catch trends, and their conservation status in sub-regional fishing commission member countries. Report to FIBA. http://www.iucnssg.org/tl_files/Assets/Regional%20files/West%20Africa/30years_eng.pdf. Accessed 17 Dec 2017.

  • Djakouré, S., P. Penven, B. Bourlès, V. Koné & J. Veitch, 2017. Respective roles of the Guinea Current and local winds on the coastal upwelling in the northern Gulf of Guinea. Journal of Physical Oceanography 47: 1367–1387.

    Article  Google Scholar 

  • Dudgeon, C. L., D. Broderick & J. R. Ovenden, 2009. IUCN classification zones concord with, but underestimate, the population genetic structure of the zebra shark Stegostoma fasciatum in the Indo-West Pacific. Molecular Ecology 18: 248–261.

    Article  CAS  PubMed  Google Scholar 

  • Dulvy, N. K., S. L. Fowler, J. A. Musick, R. D. Cavanagh, P. M. Kyne, L. R. Harrison, J. K. Carlson, L. N. K. Davidson, S. V. Fordham & M. P. Francis, 2014. Extinction risk and conservation of the world’s sharks and rays. eLife 3: e00590.

    Article  PubMed  PubMed Central  Google Scholar 

  • Duncan, K. M., A. P. Martin, B. W. Bowen & H. G. De Couet, 2006. Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini). Molecular Ecology 15: 2239–2251.

    Article  CAS  PubMed  Google Scholar 

  • Evanno, G., S. Regnaut & J. Goudet, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620.

    Article  CAS  PubMed  Google Scholar 

  • Excoffier, L. & H. E. L. Lischer, 2010. ARLEQUIN suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.

    Article  PubMed  Google Scholar 

  • Farrell, E. D., M. Clarke & S. Mariani, 2009. A simple genetic identification method for north-east Atlantic smoothhound sharks (Mustelus spp.). ICES Journal of Marine Science 66: 561–565.

    Article  Google Scholar 

  • Ferrer I., S. Bonanomi, F. Colloca, M. Di Lorenzo, I.A.M. Marino, A. Sala, L. Zane & C. Mazzoldi, 2017. Genetic ID and preliminary population genetics of two threatened smoothhound sharks: insights for conservation. In: Euromarine Workshop, 23–25 May 2017, Venice, Italy.

  • Graves, J. E., 1998. Molecular insight into the population structure of cosmopolitan marine fishes. Journal of Heredity 89: 427–437.

    Article  CAS  Google Scholar 

  • Hoelzel, A. R., M. S. Shivji, J. Magnussen & M. P. Francis, 2006. Low worldwide genetic diversity in the basking shark (Cetorhinus maximus). Biology Letters 2: 639–642.

    Article  CAS  PubMed  Google Scholar 

  • Jost, L., 2008. GST and its relatives do not measure differentiation. Molecular Ecology 17: 4015–4026.

    Article  PubMed  Google Scholar 

  • Kalinowski, S. T., 2005. HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Notes 5: 187–189.

    Article  CAS  Google Scholar 

  • Keeney, D. B., M. R. Heupel, R. E. Hueter & E. J. Heist, 2005. Microsatellite and mitochondrial DNA analyses of the genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the northwestern Atlantic, Gulf of Mexico, and Caribbean Sea. Molecular Ecology 14: 1911–1923.

    Article  CAS  PubMed  Google Scholar 

  • Kopelman, N. M., J. Mayzel, M. Jakobsson, N. A. Rosenberg & I. Mayrose, 2015. CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources 15: 1179–1191.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kousteni, V., P. Kasapidis, G. Kotoulas & P. Megalofonou, 2015. Strong population genetic structure and contrasting demographic histories for the small-spotted catshark (Scyliorhinus canicula) in the Mediterranean Sea. Heredity 114: 333–343.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, S., G. Stecher & K. Tamura, 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870–1874.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, Y. L. & J. X. Liu, 2018. STRUCTURESELECTOR: a web-based software to select and visualize the optimal number of clusters using multiple methods. Molecular Ecology Resources 18: 176–177.

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Maduna, S. N., C. da Silva, S. P. Wintner, R. Roodt-Wilding & A. E. Bester-van der Merwe, 2016. When two oceans meet: regional population genetics of an exploited coastal shark, Mustelus mustelus. Marine Ecology Progress Series 544: 183–196.

    Article  CAS  Google Scholar 

  • Maduna, S. N., C. Rossouw, C. da Silva, M. Soekoe & A. E. Bester-van der Merwe, 2017. Species identification and comparative population genetics of four coastal houndsharks based on novel NGS-mined microsatellites. Ecology and Evolution 7: 1462–1486.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mann, B. Q. & E. M. Bullen, 2009. ORI/WWF-SA Tagging Project: Summary of Tag and Recapture Data for Smoothhoundsharks (Mustelus mustelus) Caught Along the Southern African Coast from 1984 to 2008. Oceanographic Research Institute, Durban.

    Google Scholar 

  • Mantel, N., 1967. The detection of disease clustering and a generalized regression approach. Cancer Research 27: 1183–1185.

    Google Scholar 

  • Marino, I. A. M., E. Riginella, A. Cariani, F. Tinti, E. D. Farrell, C. Mazzoldi & L. Zane, 2014. New molecular tools for the identification of 2 endangered smoothhound sharks, Mustelus mustelus and Mustelus punctulatus. Journal of Heredity 106: 123–130.

    Article  PubMed  Google Scholar 

  • Marino, I. A. M., L. Finotto, F. Colloca, M. Di Lorenzo, M. Gristina, E. D. Farrell, L. Zane & C. Mazzoldi, 2017. Resolving the ambiguities in the identification of two smooth-hound sharks (Mustelus mustelus and Mustelus punctulatus) using genetics and morphology. Marine Biodiversity 48: 1551–1562.

    Article  Google Scholar 

  • Mazzoldi, C., A. Sambo & E. Riginella, 2014. The Clodia database: a long time series of fishery data from the Adriatic Sea. Science Data 1: 140018.

    Article  Google Scholar 

  • Meeuwis, J. & J. Lutjeharms, 1990. Surface thermal characteristics of the Angola-Benguela front. South African Journal of Marine Science 9: 261–279.

    Article  Google Scholar 

  • Momigliano, P., R. Harcourt, W. D. Robbins, V. Jaiteh, G. N. Mahardika, A. Sembiring & A. Stow, 2017. Genetic structure and signatures of selection in grey reef sharks (Carcharhinus amblyrhynchos). Heredity 119: 142.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orlic, M., M. Gacic & P. Laviolette, 1992. The currents and circulation of the Adriatic Sea. Oceanologica Acta 15: 109–124.

    Google Scholar 

  • Ovenden, J. R., 2013. Crinkles in connectivity: combining genetics and other types of biological data to estimate movement and interbreeding between populations. Marine Freshwater Research 64: 201–207.

    Article  Google Scholar 

  • Paradis, E., J. Claude & K. Strimmer, 2004. Ape: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290.

    Article  CAS  PubMed  Google Scholar 

  • Park S., 2001. The Excel Microsatellite toolkit (version 3.1.1). Animal Genomics Laboratory: University College, Dublin.

  • Peakall, R. & P. E. Smouse, 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288–295.

    Article  Google Scholar 

  • Pennings, P. S., A. Achenbach & S. Foitzik, 2011. Similar evolutionary potentials in an obligate ant parasite and its two host species. Journal of Evolutionary Biology 24: 871–886.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereyra, S., G. García, P. Miller, S. Oviedo & A. Domingo, 2010. Low genetic diversity and population structure of the narrownose shark (Mustelus schmitti). Fisheries Research 106: 468–473.

    Article  Google Scholar 

  • Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Puechmaille, S. J., 2016. The program STRUCTURE does not reliably recover the correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem. Molecular Ecology Resources 16: 608–627.

    Article  PubMed  Google Scholar 

  • Ronquist, F., M. Teslenko, P. Van Der Mark, D. L. Ayres, A. Darling, S. Höhna, B. Larget, L. Liu, M. A. Suchard & J. P. Huelsenbeck, 2012. MRBAYES 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rousset, F., 2008. GENEPOP’007: a complete re-implementation of the genepop software for Windows and Linux. Molecular Biology and Evolution 8: 103–106.

    Google Scholar 

  • Saidi, B., M. N. Bradaï & A. Bouaïn, 2008. Reproductive biology of the smooth-hound shark Mustelus mustelus (L.) in the Gulf of Gabès (south-central Mediterranean Sea). Journal of Fish Biology 72: 1343–1354.

    Article  Google Scholar 

  • Sambrook, J. & D. W. Russell, 2001. Molecular cloning: a laboratory manual. Cold Spring Harbour Laboratory Press, New York.

    Google Scholar 

  • Schmidt, J. V., C. L. Schmidt, F. Ozer, R. E. Ernst, K. A. Feldheim, M. V. Ashley & M. Levine, 2009. Low genetic differentiation across three major ocean populations of the whale shark, Rhincodon typus. PLoS ONE 4: e4988.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schultz, J. K., K. A. Feldheim, S. H. Gruber, M. V. Ashley, T. M. McGovern & B. W. Bowen, 2008. Global phylogeography and seascape genetics of the lemon sharks (genus Negaprion). Molecular Ecology 17: 5336–5348.

    Article  CAS  PubMed  Google Scholar 

  • Serena F., C. Mancusi, S. Clò, J. Ellis & S.V. Valenti, 2009. Mustelus mustelus (Common smoothhound). The IUCN Red List of Threatened Species. http://www.iucnredlist.org/details/39358/0. Accessed 6 Feb 2017.

  • Simpfendorfer, C. & M. Heupel, 2004. Assessing Habitat Use and Movement. In Carrier, J. C., J. A. Musick & M. R. Heithaus (eds), Biology of Sharks and Their Relatives. CRC Press, Boca Raton: 553–572.

    Chapter  Google Scholar 

  • Smale, M. J. & L. J. V. Compagno, 1997. Life history and diet of two southern African smoothhound sharks, Mustelus mustelus (Linnaeus, 1758) and Mustelus palumbes Smith, 1957 (Pisces: Triakidae). South African Journal of Marine Science 18: 229–248.

    Article  Google Scholar 

  • Stevens, J. D., R. Bonfil, N. K. Dulvy & P. A. Walker, 2000. The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES Journal of Marine Science 57: 476–494.

    Article  Google Scholar 

  • Teske, P. R., T. R. Golla, J. Sandoval-Castillo, A. Emami-Khoyi, C. D. van der Lingen, S. von der Heyden, B. Chiazzari, B. J. van Vuuren & L. B. Beheregaray, 2018. Mitochondrial DNA is unsuitable to test for isolation by distance. Scientific Reports 8: 8448.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ukwe, C. N., C. A. Ibe & K. Sherman, 2006. A sixteen-country mobilization for sustainable fisheries in the Guinea current large marine ecosystem. Ocean and Coastal Management 49: 385–412.

    Article  Google Scholar 

  • Van Oosterhout, C., W. F. Hutchinson, D. P. M. Will & P. Shipley, 2004. MICROCHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.

    Article  Google Scholar 

  • Veríssimo, A., Í. Sampaio, J. R. McDowell, P. Alexandrino, G. Mucientes, N. Queiroz, C. da Silva, C. S. Jones & L. R. Noble, 2017. World without borders—genetic population structure of a highly migratory marine predator, the blue shark (Prionace glauca). Ecology and Evolution 7: 4768–4781.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vignaud, T. M., E. Clua, J. Mourier, J. A. Maynard & S. Planes, 2013. Microsatellite analyses of blacktip reef sharks (Carcharhinus melanopterus) in a fragmented environment show structured clusters. PloS ONE 8: e61067.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vignaud, T. M., J. Mourier, J. A. Maynard, R. Leblois, J. L. Spaet, E. Clua, V. Neglia & S. Planes, 2014. Blacktip reef sharks, Carcharhinus melanopterus, have high genetic structure and varying demographic histories in their Indo-Pacific range. Molecular Ecology 23: 5193–5207.

    Article  PubMed  Google Scholar 

  • White, C., K. A. Selkoe, J. Watson, D. A. Siegel, D. C. Zacherl & R. J. Toonen, 2010. Ocean currents help explain population genetic structure. Proceedings of the Royal Society B: Biological Sciences 277: 1685–1694.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wright, S., 1943. Isolation by distance. Genetics 28: 114–138.

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors would like to thank the Central Analytical Facility at Stellenbosch University, South Africa, for sequencing conducted. This project was partly funded by the National Research Foundation of South Africa.

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Authors and Affiliations

  1. Molecular Breeding and Biodiversity Group, Department of Genetics, Stellenbosch University, Private Bag X1, Stellenbosch, Western Cape, 7602, South Africa

    Kelvin L. Hull, Tamaryn A. Asbury, Simo N. Maduna & Aletta E. Bester-van der Merwe

  2. Department of Agriculture, Forestry and Fisheries, Fisheries Research, Rogge Bay, Cape Town, South Africa

    Charlene da Silva

  3. KwaZulu-Natal Sharks Board, Umhlanga Rocks, 4320, South Africa

    Matthew Dicken

  4. Department of Development Studies, School of Economics, Development and Tourism, Nelson Mandela Metropolitan University, PO Box 77000, Port Elizabeth, 6031, South Africa

    Matthew Dicken

  5. CIBIO – U.P. – Research Center for Biodiversity and Genetic Resources, Vairão, Portugal

    Ana Veríssimo

  6. Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, VA, USA

    Ana Veríssimo

  7. School of Biology and Environmental Science, Science Centre West, University College Dublin, Belfield, Dublin 4, Ireland

    Edward D. Farrell

  8. School of Environment and Life Sciences, University of Salford, Greater Manchester, England, UK

    Stefano Mariani

  9. Department of Biology, University of Padova, Via U. Bassi 58/B, 35131, Padua, Italy

    Carlotta Mazzoldi, Ilaria A. M. Marino & Lorenzo Zane

  10. Consorzio Nazionale Interuniversitario per le Scienze delMare (CoNISMa), Piazzale Flaminio 9, 00196, Rome, Italy

    Lorenzo Zane

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Hull, K.L., Asbury, T.A., da Silva, C. et al. Strong genetic isolation despite wide distribution in a commercially exploited coastal shark. Hydrobiologia 838, 121–137 (2019). https://doi.org/10.1007/s10750-019-03982-8

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