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RESEARCH ARTICLE

Genetic characterisation of the spiny dogfish Squalus acanthias in the Adriatic Sea: evidence for high genetic diversity and an Atlantic–South Pacific origin

Romana Gračan A , Bojan Lazar B C , Sara Zupan B and Elena Bužan https://orcid.org/0000-0003-0714-5301 B D E
+ Author Affiliations
- Author Affiliations

A University of Zagreb, Faculty of Science, Department of Biology, Division of Zoology, Roosevelt Square 6, HR-10000 Zagreb, Croatia.

B University of Primorska, Faculty of Mathematics, Natural Sciences and Information Technologies, Department of Biodiversity, Glagoljaška 8, SI-6000 Koper, Slovenia.

C Juraj Dobrila University of Pula, Marine Science Program, Zagrebačka 30, HR-52100 Pula, Croatia.

D Environmental Protection College, Trg mladosti 7, SI-3320 Velenje, Slovenia.

E Corresponding author. Email: elena.buzan@upr.si

Marine and Freshwater Research 72(1) 131-139 https://doi.org/10.1071/MF20046
Submitted: 12 February 2020  Accepted: 19 March 2020   Published: 19 May 2020

Abstract

Spiny dogfish Squalus acanthias is a widely distributed, highly migratory mesopredatory shark that is extremely sensitive to overexploitation. Because of unregulated targeted and incidental capture and a lack of enforceable management in the Mediterranean Sea, the spiny dogfish subpopulation has declined by at least 50% in the Mediterranean Sea over the past 75–105 years, and is regionally classified as endangered. In this study we sampled 124 spiny dogfish in the northern-most part of the Mediterranean (i.e. the Adriatic Sea) to: (1) assess levels of genetic diversity using 13 microsatellite loci and mitochondrial (mt)DNA (NADH dehydrogenase subunit 2 (ND2) gene); and (2) infer its evolutionary placement while assessing further possible genetic divergence across the Atlantic and Pacific Ocean basins based on ND2. Analysis of mtDNA revealed 12 unique haplotypes and a high level of genetic variation in the Mediterranean region, whereas results from microsatellite markers showed significant genetic heterogeneity and a fine-scale stock structuring involving both sexes. The findings support an Atlantic–South Pacific origin for the spiny dogfish in the Adriatic Sea, with little or no present-day connectivity with the Atlantic population. Consequently, this commercially exploited and regionally endangered coastal shark in the Adriatic Sea should be considered as a separate management unit, with implementation of regional protective management plans.

Additional keywords: conservation, elasmobranchs, population connectivity.


References

Alvarado Bremer, J. R., Viñas, J., Mejuto, J., Ely, B., and Pla, C. (2005). Comparative phylogeography of Atlantic bluefin tuna and swordfish: the combined effects of vicariance, secondary contact, introgression, and population expansion on the regional phylogenies of two highly migratory pelagic fishes. Molecular Phylogenetics and Evolution 36, 169–187.
Comparative phylogeography of Atlantic bluefin tuna and swordfish: the combined effects of vicariance, secondary contact, introgression, and population expansion on the regional phylogenies of two highly migratory pelagic fishes.Crossref | GoogleScholarGoogle Scholar | 15904864PubMed |

Andrews, C. A. (2010). Natural selection, genetic drift, and gene flow do not act in isolation in natural populations. Nature Education Knowledge 3, 5.

Avise, J. C. (1994). ‘Molecular Markers, Natural History and Evolution.’ (Chapman & Hall: New York, NY, USA.)

Bandelt, H. J., Forster, P., and Rohl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.
Median-joining networks for inferring intraspecific phylogenies.Crossref | GoogleScholarGoogle Scholar | 10331250PubMed |

Barausse, A., Michieli, A., Riginella, E., Palmeri, L., and Mazzoldi, C. (2011). Long-term changes in community composition and life history traits in a highly exploited basin (northern Adriatic Sea): the role of environment and anthropogenic pressures. Journal of Fish Biology 79, 1453–1486.
Long-term changes in community composition and life history traits in a highly exploited basin (northern Adriatic Sea): the role of environment and anthropogenic pressures.Crossref | GoogleScholarGoogle Scholar | 22136236PubMed |

Barausse, A., Correale, V., Ćurković, A., Finotto, L., Riginella, E., Visentin, E., and Mazzoldi, C. (2014). The role of fisheries and the environment in driving the decline of elasmobranchs in the northern Adriatic Sea. ICES Journal of Marine Science 71, 1593–1603.
The role of fisheries and the environment in driving the decline of elasmobranchs in the northern Adriatic Sea.Crossref | GoogleScholarGoogle Scholar |

Campana, S. E., Gibson, J. F., Marks, L., Joyce, W., Rulifson, R., and Dadswell, M. (2007). Stock structure, life history, fishery and abundance indices for spiny dogfish (Squalus acanthias) in Atlantic Canada. Canadian Science Advisory Secretariat, Research Document, 2007/089. (Fisheries and Oceans, Canada.) Available at https://waves-vagues.dfo-mpo.gc.ca/Library/334817.pdf [Verified xx XXX xxxx].

Capetta, H. (2006). Elasmobranchii post-Triadici (index generum et specierum). In ‘Fossilium Catalogus I: Animalia 142’. (Ed. W. Riegraf.) pp. 1–472. (Backhuys Publishers: Leiden, Netherlands.)

Carlson, A. E., Hoffmayer, E. R., Tribuzio, C. A., and Sulikowski, J. A. (2014). The use of satellite tags to redefine movement patterns of spiny dogfish (Squalus acanthias) along the U.S. East Coast: implications for fisheries management. PLoS One 9, e103384.
The use of satellite tags to redefine movement patterns of spiny dogfish (Squalus acanthias) along the U.S. East Coast: implications for fisheries management.Crossref | GoogleScholarGoogle Scholar | 25068584PubMed |

Cavanagh, R. D., and Gibson, C. (2007). ‘Overview of the Conservation Status of Cartilaginous Fishes (Chondrichthyans) in the Mediterranean Sea.’ (IUCN: Gland, Switzerland.)

Chapuis, M. P., and Estoup, A. (2007). Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24, 621–631.
Microsatellite null alleles and estimation of population differentiation.Crossref | GoogleScholarGoogle Scholar | 17150975PubMed |

Chatzispyrou, A., and Megalofonou, P. (2005). Sexual maturity, fecundity and embryonic development of the spiny dogfish, Squalus acanthias, in the eastern Mediterranean Sea. Journal of the Marine Biological Association of the United Kingdom 85, 1155–1161.
Sexual maturity, fecundity and embryonic development of the spiny dogfish, Squalus acanthias, in the eastern Mediterranean Sea.Crossref | GoogleScholarGoogle Scholar |

Chevolot, M. H., Hoarau, G., Rijnsdorp, A. D., Stam, W. T., and Olsen, J. L. (2006). Phylogeography and population structure of thornback rays (Raja clavata L., Rajidae). Molecular Ecology 15, 3693–3705.
Phylogeography and population structure of thornback rays (Raja clavata L., Rajidae).Crossref | GoogleScholarGoogle Scholar |

Collette, B. B., and Klein-MacPhee, G. (2002). ‘Bigelow and Schroeder’s Fishes of the Gulf of Maine’, 3rd edn. (Smithsonian Institution Press: Washington, DC, USA.)

Compagno, L. J. V. (1984). ‘FAO Species Catalogue, Volume 4, Sharks of the World. An Annotated and Illustrated Catalogue of Shark Species Known to Date. Part I. Hexanchiformes to Lamniformes. FAO Fisheries Synopsis (125) 4, Part 1.’ (Food and Agriculture Organization of the United Nations: Rome, Italy.)

Corander, J., Marttinen, P., Siren, J., and Tang, J. (2008). Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9, 539.
Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations.Crossref | GoogleScholarGoogle Scholar | 19087322PubMed |

Crandall, K. A., Bininda-Emonds, O. R. P., Mace, G. M., and Wayne, R. K. (2000). Considering evolutionary processes in conservation biology. Trends in Ecology & Evolution 15, 290–295.
Considering evolutionary processes in conservation biology.Crossref | GoogleScholarGoogle Scholar |

Dulvy, N. K., and Forrest, R. E. (2010). Life histories, population dynamics and extinction risks in chondrichthyans. In ‘Sharks and Their Relatives II. Biodiversity, Adaptive Physiology and Conservation’. (Eds J. C. Carrier, J. A. Musick, and M. R. Heithaus.) pp. 639–679. (CRC Press: Boca Raton, FL, USA.)

Earl, D. A., and von Holdt, B. (2012). Structure Harvester: a website and program for visualizing structure output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.
Structure Harvester: a website and program for visualizing structure output and implementing the Evanno method.Crossref | GoogleScholarGoogle Scholar |

Ellis, J. R., Soldo, A., Dureuil, M., and Fordham, S. (2015). Spiny dogfish Squalus acanthias. In ‘The IUCN Red List of Threatened Species 2015’. e.T91209505A48910866. (International Union for Conservation of Nature and Natural Resources.) Available at https://www.iucnredlist.org/species/91209505/48910866 [Verified 15 April 2020].

Engelhaupt, D., Hoelzel, A. R., Nicholson, C., Fratzis, A., Mesnick, S., Gero, S., Whitehead, H., Rendell, L., Miller, P., De Stefanis, R., Cañadas, A., Airoldi, S., and Mignucci-Giannoni, A. A. (2009). Female philopatry in coastal basins and male dispersion across the North Atlantic in a highly mobile marine species, the sperm whale (Physeter macrocephalus). Molecular Ecology 18, 4193–4205.
Female philopatry in coastal basins and male dispersion across the North Atlantic in a highly mobile marine species, the sperm whale (Physeter macrocephalus).Crossref | GoogleScholarGoogle Scholar | 19769692PubMed |

Ewing, B., Hillier, L., Wendl, M. C., and Green, P. (1998). Base-calling of automated sequencer traces using Phred. I. Accuracy assessment. Genome Research 8, 175–185.
Base-calling of automated sequencer traces using Phred. I. Accuracy assessment.Crossref | GoogleScholarGoogle Scholar | 9521921PubMed |

Excoffier, L., and Lischer, H. E. L. (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.
Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar | 21565059PubMed |

Excoffier, L., Smouse, P. E., and Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial-DNA restriction data. Genetics 131, 479–491.
| 1644282PubMed |

Falush, D., Stephens, M., and Pritchard, J. K. (2003). Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587.
| 12930761PubMed |

Feldheim, K. A., Gruber, S. H., and Aschley, M. V. (2001). Population genetic structure of the lemon shark (Negaprion brevirostris) in the western Atlantic: DNA microsatellite varioation. Molecular Ecology 10, 295–303.
Population genetic structure of the lemon shark (Negaprion brevirostris) in the western Atlantic: DNA microsatellite varioation.Crossref | GoogleScholarGoogle Scholar | 11298946PubMed |

Franks, J. (2006). Phylogeography and population genetics of spiny dogfish (Squalus acanthias). M.Sc. Thesis, University of Washington, Seattle, WA, USA.

Fraser, D. J., and Bernatchez, L. (2001). Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Molecular Ecology 10, 2741–2752.
Adaptive evolutionary conservation: towards a unified concept for defining conservation units.Crossref | GoogleScholarGoogle Scholar | 11903888PubMed |

Funk, W. C., McKay, J. K., Hohenlohe, P. A., and Allendorf, F. W. (2012). Harnessing genomics for delineating conservation units. Trends in Ecology & Evolution 27, 489–496.
Harnessing genomics for delineating conservation units.Crossref | GoogleScholarGoogle Scholar |

Gračan, R., Lazar, B., Posavec, I., Gregorović, G., and Lacković, G. (2013). Maturation, fecundity and reproductive cycle of spiny dogfish, Squalus acanthias, in the Adriatic Sea. Marine Biology Research 9, 198–207.
Maturation, fecundity and reproductive cycle of spiny dogfish, Squalus acanthias, in the Adriatic Sea.Crossref | GoogleScholarGoogle Scholar |

Gračan, R., Heppell, S. A., Lacković, G., and Lazar, B. (2016). Age and growth dynamics of spiny dogfish, Squalus acanthias, in the Adriatic Sea (eastern Mediterranean Sea). Marine and Freshwater Research 67, 357–367.
Age and growth dynamics of spiny dogfish, Squalus acanthias, in the Adriatic Sea (eastern Mediterranean Sea).Crossref | GoogleScholarGoogle Scholar |

Grant, W. S., and Bowen, B. W. (1998). Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. The Journal of Heredity 89, 415–426.
Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation.Crossref | GoogleScholarGoogle Scholar |

Gubili, C., Bilgin, R., Kalkan, E., and Karhan, S. U. (2011). Antipodean white sharks on a Mediterranean walkabout? Historical dispersal leads to genetic discontinuity and an endangered anomalous population. Proceedings of the Royal Society of London – B. Biological Sciences 278, 1679–1686.
Antipodean white sharks on a Mediterranean walkabout? Historical dispersal leads to genetic discontinuity and an endangered anomalous population.Crossref | GoogleScholarGoogle Scholar |

Gubili, C., Macleod, K., Perry, W., Hanel, P., Batzakas, I., Farrell, E. D., Lynghammar, A., Mancusi, C., Mariani, S., Menezes, G. M., Neat, F., Scarcella, G., and Griffiths, A. M. (2016). Connectivity in the deep: phylogeography of the velvetbelly lanternshark. Deep-sea Research – I. Oceanographic Research Papers 115, 233–239.
Connectivity in the deep: phylogeography of the velvetbelly lanternshark.Crossref | GoogleScholarGoogle Scholar |

Heist, E. J. (2008). Molecular markers and genetic population structure of pelagic sharks. In ‘Sharks of the Open Ocean: Biology, Fisheries and Conservation’. (Eds M. D. Camhi, E. K. Pikitch, and E. A. Babcock.) pp. 323–333. (Blackwell Publishing: Oxford, UK.)

Henderson, C. A., Flannery, K., and Dunne, J. (2002). Growth and reproduction in spiny dogfish Squalus acanthias L. (Elasmobranchii: Squalidae), from the west coast of Ireland. Sarsia 87, 350–361.
Growth and reproduction in spiny dogfish Squalus acanthias L. (Elasmobranchii: Squalidae), from the west coast of Ireland.Crossref | GoogleScholarGoogle Scholar |

Hoelzel, A. R., Shivji, M. S., Magnussen, J., and Francis, M. P. (2006). Low worldwide genetic diversity in the basking shark (Cetorhinus maximus). Biology Letters 2, 639–642.
Low worldwide genetic diversity in the basking shark (Cetorhinus maximus).Crossref | GoogleScholarGoogle Scholar | 17148309PubMed |

Jardas, I. (1996). ‘Adriatic Ichthyofauna.’ (Školska knjiga dd: Zagreb, Croatia.) [In Croatian].

Jardas, I., Pallaoro, A., Vrgoč, N., Jukić-Peladić, S., and Dadić, V. (2008). ‘Red Book of Sea Fishes of Croatia.’ (Ministry of Culture, State Institution for Nature Protection: Zagreb, Croatia.) [In Croatian].

Keeney, D. B., Heupel, M. R., Hueter, R. E., and Heist, E. J. (2005). Microsatellite and mitochondrial DNA analyses of the genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the nothwestern Atlantic, Gulf of Mexico, and Caribbean Sea. Molecular Ecology 14, 1911–1923.
Microsatellite and mitochondrial DNA analyses of the genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the nothwestern Atlantic, Gulf of Mexico, and Caribbean Sea.Crossref | GoogleScholarGoogle Scholar | 15910315PubMed |

Ketchen, K.S. (1986). The spiny dogfish (Squalus acanthias) in the northeast Pacific and a history of its utilization. Canadian Special Publication of Fisheries and Aquatic Sciences number 88, Department of Fisheries and Oceans, Ottawa, ON, Canada.

Klein, J. D., Bester-van der Merwe, A. E., Dicken, M. L., Mmonwa, K. L., and Teske, P. R. (2019). Reproductive philopatry in a coastal shark drives age-related population structure. Marine Biology 166, 26.
Reproductive philopatry in a coastal shark drives age-related population structure.Crossref | GoogleScholarGoogle Scholar |

Klimley, A. P. (1987). The determinants of sexual segregation in the scalloped hammerhead shark, Sphyrna lewini. Environmental Biology of Fishes 18, 27–40.
The determinants of sexual segregation in the scalloped hammerhead shark, Sphyrna lewini.Crossref | GoogleScholarGoogle Scholar |

Kousteni, V., Kasapidis, P., Kotoulas, G., and Megalofonou, P. (2015). Strong population genetic structure and contrasting demographic histories for the small-spotted catshark (Scyliorhinus canicula) in the Mediterranean Sea. Heredity 114, 333–343.
Strong population genetic structure and contrasting demographic histories for the small-spotted catshark (Scyliorhinus canicula) in the Mediterranean Sea.Crossref | GoogleScholarGoogle Scholar | 25469687PubMed |

Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 27004904PubMed |

Leone, A., Urso, I., Damalas, D., Martinsohn, J., Zanzi, A., Mariani, S., Sperone, E., Micarelli, P., Garibaldi, F., Megalofonou, P., Bargelloni, L., Franch, R., Macias, D., Prodöhl, P., Fitzpatrick, S., Stagioni, M., Tinti, F., and Cariani, A. (2017). Genetic differentiation and phylogeography of Mediterranean–north eastern Atlantic blue shark (Prionace glauca, L. 1758) using mitochondrial DNA: panmixia or complex stock structure? PeerJ 5, e4112.
Genetic differentiation and phylogeography of Mediterranean–north eastern Atlantic blue shark (Prionace glauca, L. 1758) using mitochondrial DNA: panmixia or complex stock structure?Crossref | GoogleScholarGoogle Scholar | 29230359PubMed |

Librado, P., and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.
DnaSP v5: a software for comprehensive analysis of DNA polymorphism data.Crossref | GoogleScholarGoogle Scholar | 19346325PubMed |

Lipej, L., De Maddalena, A., and Soldo, A. (2004). ‘Sharks of the Adriatic Sea.’ (Knjižnica Annales Majora: Koper, Slovenia.)

Martin, A. P. (1999). Substitution rates of organelle and nuclear genes in sharks: implicating metabolic rate (again). Molecular Biology and Evolution 16, 996–1002.
Substitution rates of organelle and nuclear genes in sharks: implicating metabolic rate (again).Crossref | GoogleScholarGoogle Scholar | 10406116PubMed |

McCauley, L., Goecker, C., Parker, P., Rudolph, T., Goetz, F., and Gerlach, G. (2004). Characterization and isolation of DNA microsatellite primers in the spiny dogfish (Squalus acanthias). Molecular Ecology Notes 4, 494–496.
Characterization and isolation of DNA microsatellite primers in the spiny dogfish (Squalus acanthias).Crossref | GoogleScholarGoogle Scholar |

McFarlane, G. A., and King, J. R. (2003). Migration patterns of spiny dogfish (Squalus acanthias) in the North Pacific Ocean. Fish Bulletin 101, 358–367.

Moritz, C. (2002). Strategies to protect biological diversity and the evolutionary processes that sustain it. Systematic Biology 51, 238–254.
Strategies to protect biological diversity and the evolutionary processes that sustain it.Crossref | GoogleScholarGoogle Scholar | 12028731PubMed |

Musick, J. A., Harbin, M. M., and Compagno, L. J. V. (2004). Historical zoogeography of the Selachii. In ‘Biology of Sharks and Their Relatives’. (Eds J. C. Carrier, J. A. Musick, and M. R. Heithaus.) pp. 33–78. (CRC Press: Boca Raton, FL, USA.)

Muths, D., Le Couls, S., Evano, H., Grewe, P., and Bourjea, J. (2013). Multi-genetic marker approach and spatio-temporal analysis suggest there is a single panmictic population of swordfish Xiphias gladius in the Indian Ocean. PLoS One 8, e63558.
Multi-genetic marker approach and spatio-temporal analysis suggest there is a single panmictic population of swordfish Xiphias gladius in the Indian Ocean.Crossref | GoogleScholarGoogle Scholar | 23717447PubMed |

Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590.
| 17248844PubMed |

Patarnello, T., Volckaert, F. A., and Castilho, R. (2007). Pillars of Hercules: is the Atlantic–Mediterranean transition a phylogeographical break? Molecular Ecology 16, 4426–4444.
Pillars of Hercules: is the Atlantic–Mediterranean transition a phylogeographical break?Crossref | GoogleScholarGoogle Scholar | 17908222PubMed |

Portnoy, D. S., Puritz, J. B., Hollenbeck, C. M., Gelsleichter, J., Chapman, D., and Gold, J. R. (2015). Selection and sex-biased dispersal in a coastal shark: the influence of philopatry on adaptive variation. Molecular Ecology 24, 5877–5885.
Selection and sex-biased dispersal in a coastal shark: the influence of philopatry on adaptive variation.Crossref | GoogleScholarGoogle Scholar | 26518727PubMed |

Riccioni, G., Stagioni, M., Landi, M., Ferrara, G., Barbujani, G., and Tinti, F. (2013). Genetic structure of bluefin tuna in the Mediterranean sea correlates with environmental variables. PLoS One 8, e80105.
Genetic structure of bluefin tuna in the Mediterranean sea correlates with environmental variables.Crossref | GoogleScholarGoogle Scholar | 24260341PubMed |

Rodrigues-Filho, L. F., Pinhal, D., Vallinoto, M., and Sodré, D. (2012). Shark DNA forensics: applications and impacts on genetic diversity. In ‘Analysis of Genetic Variation in Animals’. (Ed. M. Caliskan.) pp. 269–286. (InTech: Rijeka, Croatia.)

Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian inference of phylogenetic trees. Bioinformatics 19, 1572–1574.
MrBayes 3: Bayesian inference of phylogenetic trees.Crossref | GoogleScholarGoogle Scholar | 12912839PubMed |

Rousset, F. (2008). Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources 8, 103–106.
Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux.Crossref | GoogleScholarGoogle Scholar | 21585727PubMed |

Schrey, A. W., and Heist, E. J. (2003). Microsatellite analysis of population structure in the shortfin mako (Isurus oxyrinchus). Canadian Journal of Fisheries and Aquatic Sciences 60, 670–675.
Microsatellite analysis of population structure in the shortfin mako (Isurus oxyrinchus).Crossref | GoogleScholarGoogle Scholar |

Slatkin, M., and Hudson, R. R. (1991). Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129, 555–562.
| 1743491PubMed |

Stenberg, C. (2005). Life history of the piked dogfish (Squalus acanthias L.) in Swedish waters. Journal of Northwest Atlantic Fishery Science 35, 155–164.
Life history of the piked dogfish (Squalus acanthias L.) in Swedish waters.Crossref | GoogleScholarGoogle Scholar |

Thorburn, J., Neat, F., Bailey, D., Noble, L. R., and Jones, C. S. (2015). Winter residency and site association in the critically endangered North East Atlantic spurdog (Squalus acanthias). Marine Ecology Progress Series 526, 113–124.
Winter residency and site association in the critically endangered North East Atlantic spurdog (Squalus acanthias).Crossref | GoogleScholarGoogle Scholar |

Thorburn, J., Jones, R., Neat, F., Pinto, C., Bendall, V., Hetherington, S., Bailey, D. M., Noble, L., and Jones, C. (2018). Spatial versus temporal structure: implications of inter-haul variation and relatedness in the North East Atlantic spurdog Squalus acanthias. Aquatic Conservation 28, 1167–1180.
Spatial versus temporal structure: implications of inter-haul variation and relatedness in the North East Atlantic spurdog Squalus acanthias.Crossref | GoogleScholarGoogle Scholar |

Veríssimo, A., McDowell, J. R., and Graves, J. E. (2010). Global population structure of the spiny dogfish Squalus acanthias, a temperate shark with an antitropical distribution. Molecular Ecology 19, 1651–1662.
Global population structure of the spiny dogfish Squalus acanthias, a temperate shark with an antitropical distribution.Crossref | GoogleScholarGoogle Scholar | 20345677PubMed |

Veríssimo, A., Sampaio, Í., McDowell, J. R., Alexandrino, P., Mucientes, G., Queiroz, N., da Silva, C., Jones, C. S., and Noble, L. R. (2017). World without borders – genetic population structure of a highly migratory marine predator, the blue shark (Prionace glauca). Ecology and Evolution 7, 4768–4781.
World without borders – genetic population structure of a highly migratory marine predator, the blue shark (Prionace glauca).Crossref | GoogleScholarGoogle Scholar | 28690806PubMed |

Waples, R. S. (1998). Separating the wheat from the chaff: pattern of genetic differentiation in high gene flow species. The Journal of Heredity 89, 438–450.
Separating the wheat from the chaff: pattern of genetic differentiation in high gene flow species.Crossref | GoogleScholarGoogle Scholar |

Ward, R. D., Holmes, B. H., Zemlak, T. S., and Smith, P. J. (2007). DNA barcoding discriminates spurdogs of the genus Squalus. In ‘Descriptions of New Dogfishes of the Genus Squalus (Squaloidea: Squalidae)’. (Eds P. R. Last, W. T. White and J. J. Pogonoski.) Research Paper 014, pp. 117–130. (CSIRO Marine and Atmospheric: Hobart, Tas., Australia.)