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The importance of considering genetic diversity in shark and ray conservation policies

Conservation Genetics volume 19, pages 501–525 (2018)Cite this article

Abstract

Many populations of elasmobranchs (sharks and rays) are experiencing severe declines due to the high demand for shark fins in Asia, the activities of unregulated fisheries, and increases in shark and ray catches. Recently, the effects of the decline in the populations of marine fish species on genetic diversity have drawn increasing attention; however, only a few studies have addressed the genetic diversity of shark and ray populations. Here, we report the results of a quantitative analysis of the genetic diversity of shark and ray species over the past 20 years and discuss the importance and utility of this genetic information for fisheries management and conservation policies. Furthermore, we suggest future actions important for minimizing the gaps in our current knowledge of the genetic diversity of shark and ray species and to minimize the information gap between genetic scientists and policymakers. We suggest that shark and ray fisheries management and conservation policies consider genetic diversity information, such as the management unit, effective population size (Ne), haplotype and nucleotide diversity, observed heterozygosity, and allelic richness, because the long-term survival of a species is strongly dependent on the levels of genetic diversity within and between populations. In addition, sharks and rays are a group of particular interest for genetic conservation due to their remarkable life histories.

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References

  • Ahonen H, Harcourt RG, Stow AJ (2009) Nuclear and mitochondrial DNA reveals isolation of imperiled grey nurse shark populations (Carcharias taurus). Mol Ecol 18:4409–4421

    Article  PubMed  CAS  Google Scholar 

  • Allendorf FW, England PR, Ritchie PA, Ryman N (2008) Genetic effects of harvest on wild animal populations. Trends Ecol Evol 23:327–337

    Article  PubMed  Google Scholar 

  • Allendorf FW, Luikart G, Aitken SN (2013) Conservation and the genetics of population. Blackwell, Oxford

    Google Scholar 

  • Andreotti S, von der Heyden S, Henriques R, Rutzen M, Meÿer M, Oosthuizen H, Metthee CA (2015) New insights into the evolutionary history of white sharks, Carcharodon carcharias. J Biogeogr 43:328–339

    Article  Google Scholar 

  • Andreotti S, Rutzen M, van der Walt, von der Heyden S, Henriques R, Meÿer M, Oosthuizen H, Metthee CA (2016) An integrated mark-recapture and genetic approach to estimate the population size of white sharks in South Africa. Mar Ecol Prog Ser 552:241–253

    Article  CAS  Google Scholar 

  • Arlyza IS, Shen KN, Durand JD, Borsa P (2013) Mitochondrial haplotypes indicate parapatric-like phylogeographic structure in blue-spotted maskray (Neotrygon kuhlii) from the coral Triangle Region. J Hered 4:725–733

    Article  CAS  Google Scholar 

  • Ashe JL, Feldhei KA, Fields AT, Reyier EA, Brooks EJ, O’Connell MT, Skomal G, Gruber SH, Chapman DD (2015) Local population structure and context-dependent isolation by distance in a large coastal shark. Mar Ecol Prog Ser 520:203–216

    Article  Google Scholar 

  • Barker AM, Nosal AP, Lewallen EA, Burton RS (2015) Genetic structure of leopard shark (Triakis semifasciata) populations along the Pacific coast of North America. J Exp Mar Biol Ecol 472:151–157

    Article  Google Scholar 

  • Barreto R, Ferretti F, Flemming JM, Amorim A, Andrade H, Worm B, Lessa R (2016) Trends in the exploitation of South Atlantic shark populations. Cons Biol 30:792–804

    Article  Google Scholar 

  • Belgrano A, Fowler CW (2013) How fisheries affect evolution. Science 342:1176

    Article  PubMed  Google Scholar 

  • Benavides MT, Feldheim KA, Duffy CA et al (2011a) Phylogeography of the copper shark (Carcharhinus brachyurus) in the southern hemisphere: implications for the conservation of a coastal apex predator. Mar Freshw Res 62:861–869

    Article  Google Scholar 

  • Benavides MT, Horn RL, Feldheim KA et al (2011b) Global phylogeography of the dusky shark Carcharhinus obscurus: implications for fisheries management and monitoring the shark fin trade. Endanger Species Res 14:13–22

    Article  Google Scholar 

  • Bernal MA, Sinai NL, Rocha C, Gaither MR, Dunker F, Rocha LA (2015) Long-term sperm storage in the brownbanded bamboo shark Chiloscyllium punctatum. J Fish Biol 86:1171–1176

    Article  PubMed  CAS  Google Scholar 

  • Bernard AM, Feldheim KA, Heithaus MR, Wintner SP, Wetherbee BM, Shivji MS (2016) Global population genetic dynamics of a highly migratory, apex predator shark. Mol Ecol 25:5312–5329

    Article  PubMed  CAS  Google Scholar 

  • Bernard AM, Rebekah LH, Chapman DD, Feldheim KA, Garla RC, Brooks EJ, Gore MA, Shivji MS (2017) Genetic connectivity of a coral reef ecosystem predator: the population genetic structure and evolutionary history of the Caribbean reef shark (Carcharhinus perezi). J Biogeogr 44:2488–2500

    Article  Google Scholar 

  • Bitalo DN, Maduna SN, da Silva C, Roodt-Wilding R, van der Merwe AE (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. Fish Res 172:190–196

    Article  Google Scholar 

  • Blower DC, Pandolfi JM, Bruce BD, Gomez-Cabrera MD, Ovenden JR (2012) Population genetics of Australian white sharks reveals fine-scale spatial structure, transoceanic dispersal events and low effective population sizes. Mar Ecol Prog Ser 455:229–244

    Article  CAS  Google Scholar 

  • Bonamoni S, Therkildsen NO, Retzel A et al (2016) Historial DNA documents long distance natal homing in marine fish. Mol Ecol 25:2727–2734

    Article  CAS  Google Scholar 

  • Boomer JJ, Harcourt RG, Francis M, Stow AJ (2012) Genetic divergence, speciation and biogeography of Mustelus (sharks) in the central Indo-Pacific and Australasia. Mol Phylogenet Evol 64:697–703

    Article  PubMed  Google Scholar 

  • Booth W, Schuett GW (2011) Molecular genetic evidence for alternative reproductive strategies in North American pitvipers (Serpentes: Viperidae): long-term sperm storage and facultative parthenogenesis. Biol J Linn Soc 104:934–942

    Article  Google Scholar 

  • Bowen BW, Shanker K, Yasuda N et al (2014) Phylogeography unplugged: comparative surveys in the genome era. Bull Mar Sci 90:13–46

    Article  Google Scholar 

  • Bräutigam A, Callow M, Campbell IR, Camhi MD, Cornish AS, Dulvy NK, Fordham SV, Fowler SL, Hood AR, McClennen C, Reuter EL, Sant G, Simpfendorfer CA, Welch DJ (2015) Global priorities for conserving sharks and rays: a 2015–2025 Strategy

  • Byrne RJ, Avise JC (2012) Genetic mating system of the brown smoothhound shark (Mustelus henlei), including a literature review of multiple paternity in other elasmobranch species. Mar Biol 159:749–756

    Article  Google Scholar 

  • Camargo SM, Coelho R, Chapman D, Howey-Jordan L et al (2016) Structure and genetic variability of the oceanic whitetip shark, Carcharhinus longimanus, determined using mitochondrial DNA. PLoS ONE 11:e0155623. https://doi.org/10.1371/journal.pone.0155623

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cardeñosa D, Hyde J, Caballero S (2014) Genetic diversity and population structure of the pelagic shark (Alopias pelagicus) in the Pacific Ocean: evidence for two evolutionary significant units. PLoS ONE 9:e110193. https://doi.org/10.1371/journal.pone.0110193

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Castillo-Olguín E, Uribe-Alcocer M, Díaz-Jaimes P (2012) Assessment of the population genetic structure of Sphyrna lewini to identify conservation units in the Mexican Pacific. Cienc Mar 38:635–652

    Article  Google Scholar 

  • Castillo-Páez A, Sosa-Nishizaki O, Sandoval-Castillo J, Galván-Magaña F, Blanco-Parra MD, Rocha-Olivares A (2014) Strong population structure and shallow mitochondrial phylogeny in the banded guitarfish, Zapteryx exasperate (Jordan y Gilbert, 1880), from the Northen Mexican Pacific. J Hered 105:91–100

    Article  PubMed  CAS  Google Scholar 

  • Castro ALF, Stewart BS, Wilson SG, Hueter RE, Meekan MG, Motta PJ (2007) Population genetic structure of Earth’s largest fish, the whale shark (Rhincodon typus). Mol Ecol 16:5183–5192

    Article  PubMed  CAS  Google Scholar 

  • Catarino D, Knutsen H, Veríssimo A et al (2015) The pillars of Hercules as a bathymetric barrier to gene flow promoting isolation in a global deep-sea shark (Centroscymnus coelolepis). Mol Ecol 24:6061–6079

    Article  PubMed  Google Scholar 

  • Chabot CL (2015) Microsatellite loci confirm a lack of population connectivity among globally distributed populations of the tope shark Galeorhinus galeus (Triakidae). J Fish Biol 87:371–385

    Article  PubMed  CAS  Google Scholar 

  • Chabot CL, Allen LG (2009) Global population structure of the tope (Galeorhinus galeus) inferred by mitochondrial control region sequence data. Mol Ecol 18:545–552

    Article  PubMed  CAS  Google Scholar 

  • Chabot CL, Espinoza M, Mascareñas-Osorio I, Rocha-Olivares A (2015) The effect of biogeographic and phylogeographic barriers on gene flow in the brown smoothhound shark, Mustelus henlei, in the northeastern Pacific. Ecol Evol 5:1585–1600

    Article  PubMed  PubMed Central  Google Scholar 

  • Chapman DD, Prodöhl PA, Gelsleichter J, Manire CA, Shivji MS (2004) Predominance of genetic monogamy by females in a hammerhead shark, Sphyrna tiburo: implications for shark conservation. Mol Ecol 13:1965–1974

    Article  PubMed  CAS  Google Scholar 

  • Chapman DD, Shivji MS, Louis E, Sommer J, Fletcher H, Prodöhl PA (2007) Virgin birth in a hammerhead shark. Biol Lett 3:425–427

    Article  PubMed  PubMed Central  Google Scholar 

  • Chapman DD, Pinhal D, Shivji MM (2009) Tracking the fin trade: genetic stock identification in western Atlantic scalloped hammerhead sharks Sphyrna lewini. Endanger Species Res 9:221–228

    Article  Google Scholar 

  • Chapman DD, Simpfendorfer C, Wiley TR, Poulakis GR, Curtis C, Tringali M, Carlson J, Feldheim K (2011) Genetic diversity despite population collapse in a critically endangered marine fish: the smalltooth sawfish (Pristis pectinata). J Hered 102:643–652

    Article  PubMed  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. Ann Rev Mar Sci 7:547–570

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chevolot M, Wolfs PH, Pálsson K, Riijnsdorp AD, Wytze TS, Olsen JL (2007a) Population structure and historical demography of the thorny skate (Amblyraja radiata, Rajidae) in the North Atlantic. Mar Biol 151:1275–1286

    Article  Google Scholar 

  • Chevolot M, Ellis JR, Rijnsdorp AD, Stam WT, Olsen JL (2007b) Multiple paternity analysis in the thornback ray Raja clavata L. J Hered 98:712–715

    Article  PubMed  CAS  Google Scholar 

  • Chevolot M, Ellis JR, Rijnsdorp AD, Stam WT, Olsen JL (2008) Temporal changes in allele frequencies but stable genetic diversity over the past 40 years in the Irish Sea population of thornback ray, Raja clavata. Heredity 101:120–126

  • Clarke SC, Magnussen JE, Abercrombie DL, McAllister MK, Shivji MS (2006) Identification of shark species composition and proportion in the Hong Kong shark fin market based on molecular genetics and trade records. Conserv Biol 20:201–211

    Article  PubMed  Google Scholar 

  • Clarke SC, Harley SJ, Hoyle SD, Rice JS (2013) Population trends in pacific oceanic sharks and the utility of regulations on shark finning. Conserv Biol 27:197–209

    Article  PubMed  Google Scholar 

  • Clarke CR, Karl SA, Horn RL, Bernard AM, Lea JS, Hazin FHZ, Prodöhl PA, Shivji MS (2015) Global mitochondrial DNA phylogeography and population structure of the silky shark, Carcharhinus falciformis. Mar Biol 162:945–955

    Article  CAS  Google Scholar 

  • Conrath CL, Musick JA (2012) Reproductive biology of elasmobranchs. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives, 2rd edn. CRC Press, Boca Raton, pp 291–312

    Chapter  Google Scholar 

  • Corrigan S, Delser PM, Eddy C, Duffy C, Yang L, Chenhong L, Bazinet AL, Mona S, Naylor GJP (2017) Historical introgression drivers pervasive mitochondrial admixture between two species of pelagic sharks. Mol Phylogenet Evol 110:122–126

    Article  PubMed  Google Scholar 

  • Cortés E (2002) Incorporating uncertainty into demographic modeling: application to shark populations and their conservation. Conser Biol 16:1048–1062

    Article  Google Scholar 

  • Daly-Engel TS, Grubbs RD, Feldheim KA, Bowen B, Toonen RJ (2010) Is multiple mating beneficial or unavoidable? Low multiple paternity and genetic diversity in the shortspine spurdog Squalus mitsukurii. Mar Ecol Prog Ser 403:255–267

    Article  CAS  Google Scholar 

  • Daly-Engel TS, Seraphin KD, Holland KN, Coffey JP, Nance HA, Toonen RJ, Bowen BW (2012) Global phylogeography with mixed-marker analysis reveals male-mediated dispersal in the endangered scalloped hammerhead shark (Sphyrna lewini). PLoS ONE 7:e29986. https://doi.org/10.1371/journal.pone.0029986

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Davey JW, Blaxter ML (2011) RADSeq: next-generation population genetics. Brief Funct Genomics 5:416–423

    Google Scholar 

  • Delser PM, Corrigan S, Hale M, Li C, Veuille M, Planes S, Naylor G, Mona S (2016) Population genomics of C. melanopterus using target gene capture data: demographic inferences and conservation perspectives. Sci Rep 6:33753

    Article  CAS  Google Scholar 

  • DiBattista J (2008) Pattern of genetic variation in anthropogenically impacted populations. Conserv Genet 9:141–156

    Article  Google Scholar 

  • Domingues RR, Hilsdorf AWS, Mahmood MS, Hazin FVH, Gadig OBF (2017) Effects of the pleistocene on the mitochondrial population genetic structure and demographic history of the silky shark (Carcharhinus falciformis) in the western Atlantic Ocean. Rev Fish Biol Fish. https://doi.org/10.1007/s11160-017-9504-z

    Article  Google Scholar 

  • Dudgeon CL, Ovenden JR (2015) The relationship between abundance and genetic effective population size in elasmobranchs: an example from the globally threatened zebra shark Stegostoma fasciatum within its protected range. Conserv Gen 16:1443–1454

    Article  Google Scholar 

  • Dudgeon CL, Broderick D, Ovenden JR (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  PubMed  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  PubMed  CAS  Google Scholar 

  • Dulvy NK, Fowler SL, Musick JA, Cavanagh RD et al (2014) Extinction risk and conservation of the world’s sharks and rays. eLife 3:e00590

    Article  PubMed  PubMed Central  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  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Escatel-Luna E, Adams DH, Uribe-Alcocer M, Islas-Villanueva V, Díaz-Jaimes P (2015) Population genetic structure of the bonnethead shark, Sphyrna tiburo, from the Western North Atlantic Ocean based on mtDNA sequences. J Hered 106:355–365

    Article  PubMed  CAS  Google Scholar 

  • Federal Register Volume 80, Issue 221 (Nov 17, 2015)

  • Feldheim KA, Gruber SH, Ashley MV (2001) Population genetic structure of the lemon shark (Negaprion brevirostris) in the western Atlantic: DNA microsatellite variation. Mol Ecol 10:295–303

    Article  PubMed  CAS  Google Scholar 

  • Feldheim KA, Gruber SH, Dibattista JD et al (2014) Two decades of genetic profiling yields first evidence of natal philopatry and long-term fidelity to parturition sites in sharks. Mol Ecol 23:110–117

    Article  PubMed  Google Scholar 

  • Ferretti F, Worm B, Britten GL, Heithaus MR, Lotze HK (2010) Patters and ecosystem consequences of shark declines in the ocean. Ecol Lett 13:1055–1071

    PubMed  Google Scholar 

  • Ferretti BLS, Mendonça FF, Coelho R, Vasconcelos PG, Hazin FVH, Romanov EV, Oliveira C, Santos MN, Foresti F (2015) High connectivity of the crocodile shark between Atlantic and Southwest Indian Oceans: highlights for conservation. PLoS ONE 10:e0117549. https://doi.org/10.1371/journal.pone.0117549

    Article  CAS  Google Scholar 

  • Feutry P, Kyne PM, Pillans RD, Chen X, Marthick JR, Morgan DL, Grewe PM (2015) Whole mitogenome sequencing population structure of the critically endangered sawfish Pristis pristis. Mar Ecol Prog Ser 533:237–244

    Article  CAS  Google Scholar 

  • Fields AT, Feldheim KA, Poulakis GR, Chapman DD (2015) Facultative parthenogenesis in a critically endangered wild vertebrate. Curr Biol 25:446–447

    Article  CAS  Google Scholar 

  • Flanagan SP, Forester BR, Latch EK, Aitken SN, Hoban S (2017) Guidelines for planning genomic assessment and monitoring of locally adaptive variation to inform species conservation. Evol Appl. https://doi.org/10.1111/eva.12569

    Article  PubMed  PubMed Central  Google Scholar 

  • Forselledo R, Pons M, Miller P, Domingos A (2008) Distribution and population structure of the pelagic stingray, Pteroplatytrygon violacea (Dasyatidae), in the south-western Atlantic. Aquat Living Resour 21:357–363

    Article  Google Scholar 

  • Frankham R (2010) Challenges and opportunities of genetic approaches to biological conservation. Biol Cons 143:1919–1927

    Article  Google Scholar 

  • Frankham R (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv 170:56–63

    Article  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Frederico RG, Farias I, Araújo MLG, Charvet-Almeida P, Alves-Gomes JA (2012) Phylogeography and conservation genetics of the Amazonian freshwater stingray Paratrygon aiereba Müller & Henle, 1841 (Chondrichthyes: Potamotrygonidae). Neotrop Ichtyol 10:71–80

    Article  Google Scholar 

  • Frodella N, Cannas R, Velonà A et al (2016) population connectivity and phylogeography of the Mediterranean endemic skate Raja polystigma and evidence of its hybridization with the parapatric sibling R. montagui. Mar Ecol Prog Ser 554:99–113

    Article  Google Scholar 

  • Fu M, Wnag J, Ding S, Du J, Su Y (2010) Studies on the genetic structure and genetic subdividion of white spotted bamboo shark, Chiloscyllium plagiosum, by analyzing mitochondrial Cyt b genes. J Trop Ocean 29:86–91

    CAS  Google Scholar 

  • Fung HC, Waples RS (2017) Perfomance of IUCN proxies for generation length. Cons Biol 31:739–961

    Article  Google Scholar 

  • Gaida IH (1997) Population structure of the pacific angel shark, Squatina californica (Squatiniformes: Squatinidae), around the California Channel Islands. Copeia 4:738–744

    Article  Google Scholar 

  • Gallagher AJ, Hammerschlag N, Shiffman DS, Giert S (2014) Evolved for extinction: the cost and conservation implications of specialization in hammerhead sharks. Bioscience 67:619–624

    Article  Google Scholar 

  • Galván-Tirado C, Díaz-Jaimes P, García-de León FJ, Galván-Magaña FG, Uribe-Alcocer M (2013) Historical demography and genetic differentiation inferred from the mitochondrial DNA of the silky shark (Carcharhinus falciformis) in the Pacific Ocean. Fish Res 147:36–46

    Article  Google Scholar 

  • Garber AF, Tringali EM, Franks EJS (2005) Population genetic and phylogeographic structure of wahoo, Acanthocybium solandri, from the western central Atlantic and central Pacific Oceans. Mar Biol 147:205–214

    Article  Google Scholar 

  • Garcia G, Pereyra S, Gutierrez V, Oviedo S, Miller P, Domingo A (2015) Population structure of Squatina guggenheim (Squatiniformes, Squatinidae) from the south-western Atlantic Ocean. J Fish Biol 86:186–202

    Article  PubMed  CAS  Google Scholar 

  • Gardner MG, Ward RD (1998) Taxonomic affinities within Australian and New Zealand Mustelus sharks (Chondrichthyes: Triakidae) inferred from allozymes, mitochondrial DNA and precaudal vertebrae counts. Copeia 2:356–363

    Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  PubMed  CAS  Google Scholar 

  • Geraghty PT, Williamson JE, Macbeth WG, Wintner SP, Harry AV, Ovenden JR, Gillings MR (2013) Population expansion genetic structure in Carcharhinus brevipinna in the southern Indo-Pacific. PLoS ONE 8:e75169

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Geraghty PT, Williamson JE, Macbeth WG, Blower DC, Morgan JAT, Johnson G, Ovenden JR, Gillings MR (2014) Genetic structure and diversity of two highly vulnerable Carcharhinids in Australian waters. Endanger Species Res 24:45–60

    Article  Google Scholar 

  • Giles JL, Ovenden JR, Almojil D, Garvilles E, Khampetch K, Manjebrayakath H, Riginos C (2014) Extensive genetic population structure in the Indo-West Pacific spot-tail shark, Carcharhinus sorrah. Bull Mar Sci 90:427–454

    Article  Google Scholar 

  • Giles JL, Riginos C, Naylor GJP, Ovenden JR (2016) Genetic and phenotypic diversity in the wedgefish Rhynchobatus australiae, a threatened ray of high value in the shark fin trade. Mar Ecol Prog Ser 548:165–180

    Article  CAS  Google Scholar 

  • Goodwin S, McPherson JD, McCombie WR (2016) Coming of age: ten years of next-generation sequencing technologies. Nat Rev Genet 17:333–351

    Article  PubMed  CAS  Google Scholar 

  • Grant WS, Cheng W (2012) Incorporating deep and shallow components of genetic structure into the management of Alaskan red king crab. Evol Appl 5:820–837

    Article  PubMed  PubMed Central  Google Scholar 

  • Grogan ED, Lund R, Greenfest-Allen E (2012) The origin and relationship of early Chondrichthyes. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives, 2nd edn. CRC Press, Boca Raton, pp 3–29

    Chapter  Google Scholar 

  • Gubili C, Robinson CEC, Cliff G et al (2015) DNA from historical and trophy samples provides insights into white shark population origins and genetic diversity. Endang Species Res 27:233–241

  • Haig SM, Miller MP, Bellinger R, Draheim HM, Mercer DM, Mullins TD (2016) The conservation genetics juggling act: integrating genetics and ecology, science and policy. Evol Appl 9:181–195

    Article  PubMed  CAS  Google Scholar 

  • Hare MT, Nunney L, Schwartz MK, Ruzzante DE, Burford M, Waples RS, Palstra F (2011) Understanding and estimating effective population size for practical application in marine species management. Conserv Biol 3:438–449

    Article  Google Scholar 

  • Hauser L, Carvalho GR (2008) Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish Fish 9:333–362

    Article  Google Scholar 

  • Hauser L, Adcock GJ, Smith PJ, Ramírez JHB, Carvalho GR (2002) Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus). Proc Natl Acad Sci USA 99:11742–11747

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Heino M, Pauli DB, Dieckmann U (2015) Fisheries-induced evolution. Annu Rev Ecol Evol Syst 46:461–480

    Article  Google Scholar 

  • Heist EJ, Graves JE, Musick JA (1995) Population genetics of the sandbar shark (Carcharhinus plumbeus) in the Gulf of Mexico and Mid-Atlantic Bight. Copeia 3:555–562

    Article  Google Scholar 

  • Heist EJ, Musick JA, Graves JE (1996a) Genetic population structure of the shortfin mako (Isurus oxyrinchus) inferred from restriction fragment length polymorphism analysis of mitochondrial DNA. Can J Fish Aquat 53:583–588

    Article  CAS  Google Scholar 

  • Heist EJ, Musick JA, Graves JE (1996b) Mitochondrial DNA diversity and divergence among sharpnose sharks, Rhizoprionodon terraenovae, from the Gulf of Mexico and Mid-Atlantic Bight. Fish Bull 94:664–668

    Google Scholar 

  • Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23:202–210

    Article  PubMed  Google Scholar 

  • Hernández S, Daley R, Walker T, Braccini M, Varela A, Francis MP, Ritchie (2015) Demographic history and the South Pacific dispersal barrier for school shark (Galeorhinus galeus) inferred by mitochondrial DNA and microsatellite DNA mark. Fish Res 176:132–142

    Article  Google Scholar 

  • Herndon A, Gallucci VF, DeMaster D, Burke W (2010) The case for an international commission for the conservation and management of sharks (ICCMS). Mar Policy 34:1239–1248

    Article  Google Scholar 

  • Hindrikson M, Remm J, Pilot M et al (2017) Wolf population in Europe: a systematic review, meta-analysis and suggestions for conservation and management. Biol Rev 92:1601–1629

    Article  PubMed  Google Scholar 

  • Hobab SM, Arntzen W, Bertorelle G et al (2013c) Conservation genetic for effective species survival (ConGRESS): bridging the divide between conservation research and practice. J Nat Conserv 21:433–437

    Article  Google Scholar 

  • Hoban SM, Hauffe HC, Pérez-Espona S et al (2013a) Bringing genetic diversity to the forefront of conservation policy and management. Conserv Genet Resour 5:593–598

    Article  Google Scholar 

  • Hoban S, Gaggiotti O, Bertorelle G (2013b) Sample planning optimization tool for conservation and population genetics (SPOTG): a software for choosing the appropriate number of markers and samples. Methods Ecol Evol 4:299–303

    Article  Google Scholar 

  • Hoban S, Kelley JL, Lotterhos KE et al (2016) Finding the genomic basis of local adaptation: pitfalls, practical solutions, and future directions. Am Nat 188:379–397

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hoffman M, Hilton-Taylor C, Angulo A et al (2010) The impact of conservation on the status of the world’s vertebrates. Science 330:1503–1509

    Article  CAS  Google Scholar 

  • Jorgensen SJ, Reeb CA, Chapple TK, Anderson S, Perle C, Van Sommeran SR, Fritz-Cope C, Brown AC, Klimley AP, Block BA (2009) Philopatry and migration of Pacific white sharks. Proc R Soc B 277:679–688

    Article  PubMed  PubMed Central  Google Scholar 

  • Karl SA (2008) The effect of multiple paternity on the genetically effective size of a population. Mol Ecol 17:3973–3977

    Article  PubMed  Google Scholar 

  • Karl SA, Castro ALF, Garla RC, Lopez JA, Charvet P, Burgess GH (2011) Phylogeography and conservation of the bull shark (Carcharhinus leucas) inferred from mitochondrial and microsatellite DNA. Conserv Gen 12:371–382

    Article  Google Scholar 

  • Karl SA, Castro ALF, Garla RC (2012) Population genetics of the nurse shark (Ginglymostoma cirratum) in the western Atlantic. Mar Biol 159:489–498

    Article  Google Scholar 

  • Kashiwagi T, Maxwell EA, Marshall AD, Christensen AB (2015) Evaluating manta ray mucus as an alternative DNA source for population genetics study: underwater-sampling, dry-storage and PCR success. PeerJ 3:e1188. https://doi.org/10.7717/peerj.1188

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Keeney DB, Heist EJ (2006) Worldwide phylogeography of the blacktip shark (Carcharhinus limbatus) inferred from mitochondrial DNA reveals isolation of western Atlantic populations coupled with recent Pacific dispersal. Mol Ecol 15:3669–3679

    Article  PubMed  CAS  Google Scholar 

  • Keeney DB, Heupel ME, Hueter RE, Heist EJ (2003) Genetic heterogeneity among blacktip shark, Carcharhinus limbatus, continental nurseries along the U.S. Atlantic and Gulf of Mexico. Mar Biol 143:1039–1046

    Article  Google Scholar 

  • Keeney DB, Heupel M, Hueter RE, Heist EJ (2005) Microsatellite and mitochondrial analyses of the genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the northwestern Atlantic, Gulf of Mexico, and Caribbean Sea. Mol Ecol 14:1911–1923

    Article  PubMed  CAS  Google Scholar 

  • Kenchington E, Heino M, Nielsen EE (2003) Managing marine genetic diversity: time for action? ICES J Mar Sci 60:1172–1176

    Article  Google Scholar 

  • King JR, Wetklo M, Supernaul J, Taguchi M, Yokawa K, Sosa-Nishizaki O, Withler RE (2015) Genetic analysis of stock structure of blue shark (Prionace glauca) in the north Pacific. Fish Res 172:181–189

    Article  Google Scholar 

  • Kousteni V, Kasapidis P, Kotoulas G, Megalofonou P (2015) Strong population genetic structure and contrasting histories for the small-spotted catshark (Scyliorhinus canicula) in the Mediterranean Sea. Heredity 114:1–11

  • Laikre L (2010) Genetic diversity is overlooked in international conservation policy implementation. Conserv Genet 11:349–354

    Article  Google Scholar 

  • Laikre L, Larsson LC, Palmé A, Charlier J, Josefsson M, Ryman N (2008) Potentials for monitoring gene level biodiversity: using Sweden as an example. Biodivers Conserv 17:893–910

    Article  Google Scholar 

  • Laikre L, Schwartz MK, Waples RS et al (2010b) Compromising genetic diversity in the wild: unmonitored large-scale release of plants and animals. Trends Ecol Evol 25:520–529

    Article  PubMed  Google Scholar 

  • Larson S, Farrer D, Lowry D, Ebert DA (2015) Preliminary observations of population genetics and relatedness of the broadnose sevengill shark, Notorynchus cepedianus, in two Northeast Pacific estuaries. PLoS ONE 10:e0129278. https://doi.org/10.1371/journal.pone.0129278

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Larson SE, Daly-Engel TS, Phillips NM (2017) Review of current conservation genetic analyses of Northeast Pacific sharks. Adv Mar Biol 77:79–110

  • Last PR, White WT, Carvalho MR, Séret B, Stehmann MFW, Naylor GJP (2016) Rays of the world. Cornell University Press, Ithaca

    Google Scholar 

  • Lavery S, Shaklee JB (1989) Population genetics of two tropical sharks, Carcharhinus tilstoni and C. sorrah in Northern Australia. Mar Freshw Res 40:541–547

    Article  Google Scholar 

  • Le Port A, Lavery S (2012) Population structure and phylogeography of the short-tailed stingray, Dasyatis brevicaudata (Hutton 1875), in the southern Hemisphere. J Hered 103:1–12

    Article  Google Scholar 

  • Leberg P (2005) Genetic approaches for estimating the effective size of populations. J Wildl Res 69:1385–1399

    Article  Google Scholar 

  • Lessa R, Batista VS, Santana FM (2016) Close to extinction? The collapse of the endemic daggernose shark (Isogomphodon oxyrhynchus) off Brazil. Global Ecol Evol 7:70–81

    Google Scholar 

  • Letessier TB, Bouchet PJ, Meeuwig JJ (2017) Sampling mobile oceanic fishes and sharks: implications for fisheries and conservation planning. Biol Rev 92:627–646

    Article  PubMed  Google Scholar 

  • Lewallen EA, Anderson TW, Bohonak AJ (2007) Genetic structure of leopard shark (Triakis semifasciata) populations in California waters. Mar Biol 152:599–609

    Article  Google Scholar 

  • Li N, Song N, Cheng G, Gao T (2013) Genetic diversity and population structure of the red stingray, Dasyatis akajei inferred by AFLP marker. Biochem Syst Ecol 51:130–137

    Article  CAS  Google Scholar 

  • Li N, Chen X, Sun D, Song N, Lin Q, Gao T (2015) Phylogeography and population structure of the red stingray, Dasyatis akajei inferred by mitochondrial control region. Mitochondr DNA 26:505–513

    Article  CAS  Google Scholar 

  • Li W, Dai X, Zhu J, Tian S, He S, Wu F (2016) Genetic differentiation in blue shark, Prionace glauca, from the central Pacific Ocean, as inferred by mitochondrial cytochrome b region. Mitochondr DNA 28:575–578

    Article  CAS  Google Scholar 

  • Lieber L, Berrow S, Johnston E, Graham H, Hall J, Gubili C, Sims DW, Jones CS, Noble LR (2013) Mucus: aiding elasmobranch conservation through non-invasive genetic sampling. Endanger Species Res 21:215–222

    Article  Google Scholar 

  • Lucifora LO, García VB, Worm B (2011) Global diversity hotspots and conservation priorities for sharks. PLoS ONE 6:e19356

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maduna SN, da Silva C, Wintner SP, Roodt-Wilding R, van der Merwe AE (2016) When two oceans meet: regional population genetics of an exploited coastal shark, Mustelus mustelus. Mar Ecol Prog Ser 544:183–196

    Article  CAS  Google Scholar 

  • Martin AP, Naylor GJP, Palumbi SR (1992) Rate of mitochondrial evolution is low in sharks compared to mammals. Nature 357:153–155

    Article  PubMed  CAS  Google Scholar 

  • Massa A, Hozbor N, Chiaramonte GE, Balestra AD, Vooren CM (2006) Mustelus schmitti. The IUCN Red List of threatened species 2006: e.T60203A12318268. http://dx.doi.org/10.2305/IUCN.UK.2006.RLTS.T60203A12318268.en. Accessed 07 Nov 2016

  • McClenachan L, Cooper AB, Dulvy NK (2016) Rethinking trade-driven extinction risk in marine and terrestrial megafauna. Curr Biol 26:1–7

    Article  CAS  Google Scholar 

  • McCusker MR, Bentzen P (2010) Positive relationships between genetic diversity and abundance in fishes. Mol Ecol 19:4852–4862

    Article  PubMed  Google Scholar 

  • MacDonald CM (1988) Genetic variation, breeding structure and taxonomic status of the gummy shark Mustelus antarticus in Southern Australian waters. Mar Freshw Res 39:641–648

    Article  Google Scholar 

  • McNelly JA, Miller KR, Reid WV, Mittermeier RA, Werner TB (1990) World Conservation Union. World Resources Institute, Conservation International, World Wildlife Fund–US, and the World Bank, Washington, D.C

    Google Scholar 

  • Mendonça FF, Oliveira C, Gadig OBF, Foresti F (2011) Phylogeography and genetic population structure of Caribben sharpnose shark Rhizoprionodon porosus. Rev Fish Biol Fish 21:799–814

    Article  Google Scholar 

  • Mendonça FF, Oliveira C, Gadig OBF, Foresti F (2013) Diversity and genetic population of the Brazilian sharpnose shark Rhizoprionodon lalandii. Aquat Conserv Mar Fresh Ecosyst 23:850–9857

    Article  Google Scholar 

  • Miller MH, Carlson J, Cooper P, Kobayashi D, Wilson J (2013) Status review report: scalloped hammerhead shark (Sphyrna lewini). Report to National Marine Fisheries Service, Office of Protected Resources, p 131

  • Momigliano P, Harcourt R, Robbins WD, Stow A (2015) Connectivity in grey reef sharks (Carcharhinus amblyrhynchos) determined using empirical and simulated genetic data. Sci Rep 5:13229

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mourier J, Planes S (2013) Direct genetic evidence for reproductive philopatry and associated fine-scale migration in female blacktip reef sharks (Carcharhinus melanopterus) in French Polynesia. Mol Ecol 22:201–214

    Article  PubMed  Google Scholar 

  • Mourier J, Burray J, Schultz JK, Clua E, Planes S (2013) Genetic network and breeding of a sicklefin lemon shark (Negaprion acutidens) population in the Society Islands, French Polynesia. PLoS ONE 8:e73899. https://doi.org/10.1371/journal.pone.0073899

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Murray BW, Wang JY, Yang SC, Stevens JD, Fisk A, Svavarsson J (2008) Mitochondrial cytochrome b variation in sleeper sharks (Squaliformes: Somniosidae). Mar Biol 153:1015–1022

    Article  CAS  Google Scholar 

  • Musick JA, Burgess G, Cailliet G, Camhi M, Fordham S (2000) Management of sharks and their relatives (Elasmobranchii). Fisheries 25:9–13

    Article  Google Scholar 

  • Nance HA, Klimley P, Galván-Magaña F, Martínez-Ortíz J, Marko PB (2011) Demographic process underlying subtle pattern of population structure in the scalloped hammerhead shark, Sphyrna lewini. PLoS ONE 6:e21459. https://doi.org/10.1371/journal.pone.0021459

    Article  PubMed  PubMed Central  Google Scholar 

  • Narun SR, Hess JE (2011) Comparison of F ST outlier tests for SNP loci under selection. Mol Ecol Resour 11:184–194

    Article  Google Scholar 

  • Nelson JS, Grande TC, Wilson MHV (2016) Fishes of the world. Wiley, Hoboken

    Book  Google Scholar 

  • Newby JN, Darden T, Shedlock AM (2014) Population genetic structure of spotted eagle rays, Aetobatus narinari, off Sarasota, Florida and the Southeastern United States. Copeia 3:503–512

    Article  Google Scholar 

  • Nielsen EE, Hansen MM (2008) Waking the dead: the value of population genetic analyses of historical samples. Fish Fish 9:450–461

    Article  Google Scholar 

  • Nielsen EE, Hemmer-Hansen J, Larsen PF, Bekkevold D (2009) Population genomics of marine fishes: identifying adaptive variation in space and time. Mol Ecol 18:3128–3150

  • Nielsen EE, Morgan JAT, Maher SL, Edson J, Gauthier M, Pepperell J, Holmes BJ, Bennett MB, Ovenden JR (2016) Extracting DNA from ‘jaws’: high yield and quality from archived tiger shark (Galeocerdo cuvier) skeletal material. Mol Ecol Res 17:431–442

    Article  CAS  Google Scholar 

  • O’Leary SJ, Feldheim KA, Fields AT, Natanson LJ, Wintner S, Hussey N, Shivji MS, Chapman DD (2015) Genetic diversity of white sharks, Carcharodon carcharias, in the Northwest Atlantic and Southern Africa. J Hered 106:1–8

    Article  Google Scholar 

  • Oñate-González EC, Rocha-Olivares A, Saavedra-Sotelo N, Sosa-Nishizaki O (2015) Mitochondrial genetic structure and matrilineal origin of white sharks, Carcharodon carcharias in the Northeastern Pacific: implications for their conservation. J Hered 106:347–354

    Article  PubMed  Google Scholar 

  • Ovenden JR, Kashiwagi T, Broderick D, Giles J, Salini J (2009) The extent of population genetic subdivision differs among four co-distributed shark species in the Indo-Australian archipelago. BMC Evol Biol 9:40

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ovenden JR, Morgan JA, Street R, Tobin A, Simpfendorfer C, Macbeth W, Welch D (2011) Negligible evidence species Rhizoprionodon acutus (Rüppell, 1837) and Sphyrna lewini (Griffith & Smith, 1834) with contrasting biology. Mar Biol 158:1497–1509

    Article  Google Scholar 

  • Ovenden JR (2013) Crinkles in connectivity: combining genetics and other types of biological data to estimate movement and interbreeding between populations. Mar Freshwater Res 64:201–207

  • Ovenden JR, Berry O, Welch DJ, Buckworth R, Dichmont CM (2013) 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 

  • Ovenden JR, Blower DC, Jones AT, Moore A, Bustamante C, Buckworth RC, Bennett MB, Dudgeon CL (2016) Can estimates of genetic effective population size contribute to fisheries stock assessments? J Fish Biol 89:2505–2518

    Article  PubMed  CAS  Google Scholar 

  • O’Brien SM, Gallucci VF, Hauser L (2013) Effects of species biology on the historical demography of sharks and their implications for likely consequences of contemporary climate change. Conserv Genet 14:125–144

  • Pardini AT, Jones CS, Noble LR, Kreiser B, Malcolm H, Bruce BD, Stevens JD, Cliff G, Scholl MC, Francis M, Clinton CAJ, Duffy P, Martin AP (2001) Sex-biased dispersal of great white sharks. Science 412:139–140

    CAS  Google Scholar 

  • Parsolini P, Ragazzini C, Zaccaro Z, Cariani A, Ferrara G, Gonzalez EG, Landi M (2011) Quartenary geographical sibling speciation and population structuring in the eastern Atlantic skates (suborder Rajoidea) Raja clavata and R. straeleni. Mar Biol 158:2173–2186

    Article  Google Scholar 

  • Pazmiño Da, Maes GE, Simpfendorfer CA, Salinas-de-León P, van Herwerden L (2017) Genome-wide SNPs reveal low effective population size within confined management units of the highly vagile Galapagos shark (Carcharhinus galapagensis). Conserv Genet 18:1151–1163

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

    Article  Google Scholar 

  • Phillips NM, Chaplin JA, Morgan DL, Peverell SC (2011) Population genetic structure and genetic diversity of three critically endangered Pristis sawfishes in Australian waters. Mar Biol 158:903–915

    Article  Google Scholar 

  • Pichler FB, Baker CS (2000) Loss of genetic diversity in the endemic Hector’s dolphin due to fisheries-related mortality. Proc Biol Sci 267:97–102

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pinsky ML, Palumbi SR (2014) Meta-analysis reveals lower genetic diversity in overfished populations. Mol Ecol 23:29–39

    Article  PubMed  Google Scholar 

  • Plank SM, lowe CG, Feldheim KA, Wilson RR Jr, Brusslan JA (2010) Population genetic structure of the round stingray Urobatis halleri (Elasmobranchii: Rajiformes) in southern California and the Gulf of California. J Fish Biol 77:329–340

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Portnoy DS, McDowell JR, McCandless CT, Musick JA, Graves JE (2009) Effective size closely approximates the census size in the heavily exploited western Atlantic population of the sandbar shark, Carcharhinus plumbeus. Conserv Genet 10:1697–1705

    Article  Google Scholar 

  • Portnoy DS, McDowell JR, Heist EJ, Musick JA, Graves JE (2010) World phylogeography and male-mediated gene flow in the sandbar shark, Carcharhinus plumbeus. Mol Ecol 19:1994–2010

    Article  PubMed  CAS  Google Scholar 

  • Portnoy DS, Hollenbeck CM, Johnston JS, Casman HM, Gold JR (2014a) Parthenogenesis in a whitetip reef shark Triaenodon obesus involves a reduction in ploidy. J Fish Biol 85:502–508

    Article  PubMed  CAS  Google Scholar 

  • Portnoy DS, Hollenbeck CM, Belcher CN, Driggers WB III, Frazier BS, Gelsleichter J, Grubbs RD, Gold JR (2014b) Contemporary population structure and post-glacial genetic demography in a migratory marine species, the blacknose shark, Carcharhinus acronotus. Mol Ecol 23:5480–5495

    Article  PubMed  CAS  Google Scholar 

  • Portnoy DS, Puritz JB, Hollenbeck CM, Gelsleichter J, Chapman D, Gold JR (2015) Selection and sex-biased dispersal in a coastal shark: the influence of philopatry on adaptive variation. Mol Ecol 24:5877–5885

    Article  PubMed  CAS  Google Scholar 

  • Portnoy DS, Hollenbeck CM, Bethe DM, Frazier BS, Gelsleichter J, Gold JR (2016) Population structure, gene flow, and historical demography of a small coastal shark (Carcharhinus isodon) in US waters of the Western Atlantic Ocean. ICES J Mar Sci 73:2322–2332

    Article  Google Scholar 

  • Puckett EE (2017) Variability in total project and per sample genotyping costs under varying study designs including with microsatellites or SNPs to answer conservation genetic questions. Conserv Genet Resour 9:289–304

    Article  Google Scholar 

  • Quintanilha S, Gómez A, Mariño-Ramírez C, Sorzano C, Bessudo S, Soler G, Bernal JE, Caballero S (2015) Conservation genetics of the scalloped hammerhead shark in the Pacific coast od Colombia. J Hered 106:448–458

    Article  CAS  Google Scholar 

  • Ramakrishnan U, Storz JF, Taylor BL, Lande R (2004) Estimation of genetically effective breeding numbers using a rejection algorithm approach. Mol Ecol 13:3283–3292

    Article  PubMed  CAS  Google Scholar 

  • Richards VP, Suzuki H, Stanhope MJ, Shivji MS (2013) Characterization of the heart transcriptome of the shark (Carcharodon carcharias). BMC Genom 4:697

    Article  CAS  Google Scholar 

  • Rivers MC, Brummitt NA, Lughadha EN, Meagher TR (2014) Do species conservation assessments capture genetic diversity? Global Ecol Evol 2:81–87

    Google Scholar 

  • Rocha L, Bernal MA, Gaither MR, Alfaro ME (2013) Massively parallel DNA sequencing: the new frontier in biogeography. Front Biogeogr 5:67–77

    Google Scholar 

  • Rosa RS, Castro ALF, Furtado M, Monzini J, Grubbs RD (2006) Ginglymostoma cirratum. The IUCN Red List of Threatened Species 2006: e.T60223A12325895. http://dx.doi.org/10.2305/IUCN.UK.2006.RLTS.T60223A12325895.en. Acessed 14 April 2016

  • Ryman N, Palm S (2006) POWSIM: a computer for assessing statistical power when testing for genetic differentiation. Mol Ecol Resour 6:600–602

    Article  Google Scholar 

  • Ryman N, Utter F, Laikre L (1995) Protection of intraspecific biodiversity of exploited fishes. Rev Fish Biol Fish 5:417–446

    Article  Google Scholar 

  • Sandoval-Castillo J, Beheregaray LB (2015) Metapopulation structure informs conservation management in a heavily exploited coastal shark (Mustelus henlei). Mar Ecol Prog Ser 533:191–203

    Article  CAS  Google Scholar 

  • Sandoval-Castillo J, Rocha-Olivares A (2011) Deep mitochondrial divergence in Baja California populations of an aquilopelagic elasmobranch: the golden cownose ray. J Hered 102:269–274

    Article  PubMed  CAS  Google Scholar 

  • Sandoval-Castillo J, Rocha-Olivares A, Villavicencio-Garayzar C, Balart E (2004) Cryptic isolation of Gulf of California shovelnose guitarfish evidence by mitochondrial DNA. Mar Biol 145:983–988

    Article  CAS  Google Scholar 

  • Schluessel V, Broderick D, Collin SP, Ovenden JR (2010) Evidence for extensive population structure in the white-spotted eagle ray within the Indo-Pacific inferred from mitochondrial DNA gene sequences. J Zool 281:46–55

    Article  Google Scholar 

  • Schmidt JV, Schmidt CL, Ozer F, Ernst RE, Feldheim KA, Ashley MV, Levine M (2009) Low genetic differentiation across three major ocean populations of the whale shark, Rhincodon typus. PLoS ONE 4:e4988. https://doi.org/10.1371/journal.pone.0004988

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schrey AW, Heist EJ (2003) Microsatellite analysis of population structure in the shortfin mako (Isurus oxyrinchus). Can J Fish Aquat Sci 60:670–675

    Article  CAS  Google Scholar 

  • Schultz JK, Feldheim KA, Gruber SH, Ashley MV, McGovern TM, Bowen BW (2008) Global phylogeography and seascape genetics of the lemon sharks (genus Negaprion). Mol Ecol 17:5336–5348

    Article  PubMed  CAS  Google Scholar 

  • Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33

  • Seitz JC, Poulakis GR (2006) anthropogenic effects on the smalltooth sawfish (Pristis pectinata) in the United States. Mar Pollut Bull 52:1533–1540

    Article  PubMed  CAS  Google Scholar 

  • Sellas AB, Bassos-Hull K, Pérez-Jiménez JC, Angulo-Valdés JA, Bernal MA, Hueter RE (2015) Population structure and seasonal migration of the spotted eagle ray, Aetobatus narinari. J Hered 106:266–275

    Article  PubMed  CAS  Google Scholar 

  • Simpfendorfer CA, Heupel MR, White WT, Dulvy NK (2011) The importance of research and public opinion to conservation management of sharks and rays: a synthesis. Mar Freshw Res 62:518–527

    Article  CAS  Google Scholar 

  • Sodré D, Rodrigues-Filho LFS, Souza RFC, Rêgo PS, Schneider H, Sampaio I, Vallinoto (2012) Inclusion of South American samples reveals new population structuring of the blacktip shark (Carcharhinus limbatus) in the western Atlantic. Genet Mol Biol 4:752–760

    Article  Google Scholar 

  • Solé-Cava AM, Vooren CM, Levy JA (1983) Isozymic differentiation of two sibling species of Squatina (Condrichthyes) in southern Brazil. Comp Biochem Physiol 75:355–358

    Google Scholar 

  • Spaet JLY, Jabado RW, Henderson AC, Moore ABM, Berumen ML (2015) Population genetics of four heavily exploited shark species around the Arabian Peninsula. Ecol Evol 5:2317–2332

    Article  PubMed  PubMed Central  Google Scholar 

  • Stapley J, Reger J, Feulner PGD, Smadja C, Galindo J, Ekblom R, Bennison C, Ball AD, Beckerman AP, Slate J (2010) Adaptation genomics: the next generation. Trends Ecol Evol 25:705–712

    Article  PubMed  Google Scholar 

  • Stevens JD, Bonfil R, Dulvy NK, Walker PA (2000) The effects of fishing on sharks, rays, and chimaeras (Chondrichthyans), and the implications for marine ecosystems. ICES J Mar Sci 57:476–494

    Article  Google Scholar 

  • Stow A, Zenger K, Briscoe D, Gillings M, Peddemors V, Otway N, Harcourt R (2006) Isolation and genetic diversity of endangered grey nurse shark (Carcharias taurus) populations. Biol Lett 2:308–311

    Article  PubMed  PubMed Central  Google Scholar 

  • Suárez-Moo J, Rocha-Olivares A, Zapata-Pérez O, Quiroz-Moreno A, Sánchez-Teyer F (2013) High genetic connectivity in the Atlantic sharpnose shark, Rhizoprionodon terraenovae, from the southeast Gulf of Mexico inferred from AFLP fingerprinting. Fish Res 147:338–343

    Article  Google Scholar 

  • Taguchi M, King JR, Wetklo M, Withler RE, Yokawa (2015) Population genetic structure and demographic history of Pacific blue sharks (Prionace glauca) inferred from mitochondrial DNA analysis. Mar Freshw Res 66:267–275

    Article  CAS  Google Scholar 

  • Tavares W, Rodrigues-Filho LFS, Sodré D, Souza RFC, Schneider H, Sampaio I (2013) Multiple substitutions and reduced genetic variability in sharks. Biochem Syst Ecol 49:21–29

    Article  CAS  Google Scholar 

  • Tiffin P, Ross-Ibarra (2014) Advances and limits of using population genetics to understand local adaptation. Trends Ecol Evol 29:673–680

    Article  PubMed  Google Scholar 

  • Tillet BJ, Meekan MG, Broderick D, Field IC, Cliff G, Ovenden JR (2012a) Pleistocene isolation, secondary introgression and restricted contemporary gene flow in the pig-eye shark, Carcharhinus amboinensis across northern Australia. Conserv Genet 13:99–115

    Article  Google Scholar 

  • Tillet BJ, Meekan MG, Field IC, Thorburn DC, Ovenden JR (2012b) Evidence fro reproductive philopatry in the bull shark Carcharhinus leucas. J Fish Biol 80:2140–2158

    Article  Google Scholar 

  • Tolotti MT, Filmalter JD, Bach P, Travassos P, Seret B, Dagorn L (2015) Banning is not enough: the complexities of oceanic shark management by tuna regional fisheries management organizations. Glob Ecol Evol 4:1–7

    Google Scholar 

  • Uzans AJ, Lucas Z, McLeod BA, Frasier TR (2015) Small Ne of the isolated and unmanaged horse population on Sable Island. J Hered 106:660–665

    Article  PubMed  CAS  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  PubMed  CAS  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 

  • Veríssimo A, McDowell JR, Graves JE (2012) Genetic population structure and connectivity in a commercially exploited and wide-ranging deepwater shark, the leafscale gulper (Centrophorus squamosus). Mar Freshw Res 63:505–512

    Article  CAS  Google Scholar 

  • Veríssimo A, Sampaio Í, McDowell JR, Alexandrino P, Mucientes G, Queiroz N, da Silva C, Jones CS, Noble LR (2017) World without borders—genetic population structure of a highly migratory marine predator, the blue shark (Prionace glauca). Ecol Evol 7:4768–4781

    Article  PubMed  PubMed Central  Google Scholar 

  • Vignaud T, Clua E, Mourier J, Maynard J, Planes S (2013) Microsatellite analyses of blacktip reef sharks (Carcharhinus melanopterus) in a fragmented environment show structured clusters. PLoS ONE 8:e61067. https://doi.org/10.1371/journal.pone.0061067

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vignaud TM, Mourier J, Maynard J, Leblois R, Azquez-Juárez RV, Ramírez-Macías D, Pierce SJ, Rowat D, Berumen ML, Beeravolu C, Baksay S, Planes S (2014a) 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  PubMed  CAS  Google Scholar 

  • Vignaud TM, Maynard J, Leblois R, Meekan M, Spaet JLY, Clua E, Neglia V, Planes S (2014b) Blacktip reef sharks, Carcharhinus melanopterus, have high genetic structure and varying demographic histories in their Indo-Pacific range. Mol Ecol 23:5193–5207

    Article  PubMed  Google Scholar 

  • Vooren CM, Lessa RP, Klippel S (2005) Biologia e status de conservação da viola Rhinobatos horkelli. In: Vooren CM, Klippel S (eds) Ações para a conservação de tubarões e raias no sul do Brasil. Igaré, Porto Alegre, pp 32–56

    Google Scholar 

  • Walker TI, Taylor BL, Russell JH, Cottier JP (1998) The phenomenon of apparent change of growth rate in gummy shark (Mustelus antarcticus) harvested off southern Australia. Fish Res 39:139–163

    Article  Google Scholar 

  • Waples R (1995) Evolutionary significant units and the conservation of biological diversity under the endangered’s species. Am Fish Soc Symp 17:8–27

    Google Scholar 

  • Waples RS, Gaggiotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439

    Article  PubMed  CAS  Google Scholar 

  • Wasko AP, Martins C, Oliveira C, Foresti F (2003) Non-destructive genetic sampling in fish. An improved DNA extraction from fish fins and scales. Hereditas 138:161–165

    Article  PubMed  Google Scholar 

  • Watts PC, Buley KR, Sanderson S, Boardman W, Ciofi C, Gibson R (2006) Parthenogenesis in Komodo dragons. Nature 444:1021–1022

    Article  PubMed  CAS  Google Scholar 

  • Weigmann S (2016) Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with focus on biogeographical diversity. J Fish Biol 88:837–1037

    Article  PubMed  CAS  Google Scholar 

  • Whitney NM, Robbins WD, Schultz JK, Bowen BW, Holland KN (2012) Oceanic dispersal in a sedentary reef shark (Triaenodon obesus): genetic evidence for extensive connectivity without a pelagic larval stage. J Biogeogr 39:1144–1156

    Article  Google Scholar 

  • Willette DA, Allendorf FW, Barber PH et al (2014) So, you want to use next-generation sequencing in marine systems? Insight from the Pan-Pacific Advanced Studies Institute. Bull Mar Sci 90:79–122

    Article  Google Scholar 

  • Willoughby JR, Sundaram M, Wijayawardena BK, Kimble SJA, Yanzhu J, Fernandez NB, Antonides JD, Lamb MC, Marra NJ, DeWoody JA (2015) The reduction of genetic diversity in threatened vertebrates and new recommendations regarding IUCN conservation rankings. Biol Cons 191:495–503

    Article  Google Scholar 

  • Worm B, Davis B, Kettemer L, Ward-Paige CA, Chapman D, Heithaus MR, Kessel S, Gruber S (2013) Global catches, exploitation rates, and rebuilding options for sharks. Mar Policy 40:194–204

    Article  Google Scholar 

  • Zeh JA, Zeh DW (2003) Toward a new sexual selection paradigm: polyandry, conflict and incompatibility. Ethology 109:929–950

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank three anonymous reviewers and the editors of Conservation Genetics for their valuable suggestions for strengthening the manuscript during peer review. This work was supported by the São Paulo Research Foundation (FAPESP #2009/54660-6 and #2013/08675-7) and by a grant from the Brazilian National Council for Scientific and Technological Development to OBFG (CNPq #308430-8).

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Authors and Affiliations

  1. Instituto de Biociências de Rio Claro, Universidade Estadual Paulista, UNESP, Av. 24-A, 1515, Rio Claro, São Paulo, 113506-900, Brazil

    Rodrigo Rodrigues Domingues

  2. Núcleo Integrado de Biotecnologia, Universidade de Mogi das Cruzes, Mogi das Cruzes, São Paulo, 08701-970, Brazil

    Alexandre Wagner Silva Hilsdorf

  3. Laboratório de Pesquisa de Elasmobrânquios, Instituto de Biociências, Universidade Estadual Paulista, Campus do Litoral Paulista, São Vicente, São Paulo, 11330-900, Brazil

    Rodrigo Rodrigues Domingues & Otto Bismarck Fazzano Gadig

Authors
  1. Rodrigo Rodrigues Domingues
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  2. Alexandre Wagner Silva Hilsdorf
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  3. Otto Bismarck Fazzano Gadig
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Correspondence to Rodrigo Rodrigues Domingues.

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Domingues, R.R., Hilsdorf, A.W.S. & Gadig, O.B.F. The importance of considering genetic diversity in shark and ray conservation policies. Conserv Genet 19, 501–525 (2018). https://doi.org/10.1007/s10592-017-1038-3

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  • DOI: https://doi.org/10.1007/s10592-017-1038-3

Keywords

  • Conservation
  • Elasmobranch
  • Evolution
  • Fisheries management
  • Genetic variability
  • Molecular marker