Conservation Genetics

, Volume 19, Issue 3, pp 501–525 | Cite as

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

  • Rodrigo Rodrigues DominguesEmail author
  • Alexandre Wagner Silva Hilsdorf
  • Otto Bismarck Fazzano Gadig
Review Article


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.


Conservation Elasmobranch Evolution Fisheries management Genetic variability Molecular marker 



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).


  1. Ahonen H, Harcourt RG, Stow AJ (2009) Nuclear and mitochondrial DNA reveals isolation of imperiled grey nurse shark populations (Carcharias taurus). Mol Ecol 18:4409–4421PubMedCrossRefGoogle Scholar
  2. Allendorf FW, England PR, Ritchie PA, Ryman N (2008) Genetic effects of harvest on wild animal populations. Trends Ecol Evol 23:327–337PubMedCrossRefGoogle Scholar
  3. Allendorf FW, Luikart G, Aitken SN (2013) Conservation and the genetics of population. Blackwell, OxfordGoogle Scholar
  4. 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 43:328–339CrossRefGoogle Scholar
  5. 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 552:241–253CrossRefGoogle Scholar
  6. 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 4:725–733CrossRefGoogle Scholar
  7. 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 520:203–216CrossRefGoogle Scholar
  8. 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 472:151–157CrossRefGoogle Scholar
  9. 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 30:792–804CrossRefGoogle Scholar
  10. Belgrano A, Fowler CW (2013) How fisheries affect evolution. Science 342:1176PubMedCrossRefGoogle Scholar
  11. 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 62:861–869CrossRefGoogle Scholar
  12. 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 14:13–22CrossRefGoogle Scholar
  13. 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 86:1171–1176PubMedCrossRefGoogle Scholar
  14. 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 25:5312–5329PubMedCrossRefGoogle Scholar
  15. 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 44:2488–2500CrossRefGoogle Scholar
  16. 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 172:190–196CrossRefGoogle Scholar
  17. 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 455:229–244CrossRefGoogle Scholar
  18. Bonamoni S, Therkildsen NO, Retzel A et al (2016) Historial DNA documents long distance natal homing in marine fish. Mol Ecol 25:2727–2734CrossRefGoogle Scholar
  19. 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 64:697–703PubMedCrossRefGoogle Scholar
  20. 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 104:934–942CrossRefGoogle Scholar
  21. Bowen BW, Shanker K, Yasuda N et al (2014) Phylogeography unplugged: comparative surveys in the genome era. Bull Mar Sci 90:13–46CrossRefGoogle Scholar
  22. 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 StrategyGoogle Scholar
  23. 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 159:749–756CrossRefGoogle Scholar
  24. 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. PubMedPubMedCentralCrossRefGoogle Scholar
  25. 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. PubMedPubMedCentralCrossRefGoogle Scholar
  26. 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 38:635–652CrossRefGoogle Scholar
  27. 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 105:91–100PubMedCrossRefGoogle Scholar
  28. 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 16:5183–5192PubMedCrossRefGoogle Scholar
  29. 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 24:6061–6079PubMedCrossRefGoogle Scholar
  30. 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 87:371–385PubMedCrossRefGoogle Scholar
  31. Chabot CL, Allen LG (2009) Global population structure of the tope (Galeorhinus galeus) inferred by mitochondrial control region sequence data. Mol Ecol 18:545–552PubMedCrossRefGoogle Scholar
  32. 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 5:1585–1600PubMedPubMedCentralCrossRefGoogle Scholar
  33. 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 13:1965–1974PubMedCrossRefGoogle Scholar
  34. Chapman DD, Shivji MS, Louis E, Sommer J, Fletcher H, Prodöhl PA (2007) Virgin birth in a hammerhead shark. Biol Lett 3:425–427PubMedPubMedCentralCrossRefGoogle Scholar
  35. 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 9:221–228CrossRefGoogle Scholar
  36. 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 102:643–652PubMedCrossRefGoogle Scholar
  37. 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 7:547–570PubMedCrossRefGoogle Scholar
  38. Chevolot M, Hoarau G, Stam WT, Olsen J (2006) Phylogeography and population structure of thornback rays (Raja clavata L., Rajidae). Mol Ecol 15:3693–3705PubMedCrossRefGoogle Scholar
  39. 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 151:1275–1286CrossRefGoogle Scholar
  40. Chevolot M, Ellis JR, Rijnsdorp AD, Stam WT, Olsen JL (2007b) Multiple paternity analysis in the thornback ray Raja clavata L. J Hered 98:712–715PubMedCrossRefGoogle Scholar
  41. 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 101:120–126Google Scholar
  42. 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 20:201–211PubMedCrossRefGoogle Scholar
  43. 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 27:197–209PubMedCrossRefGoogle Scholar
  44. 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 162:945–955CrossRefGoogle Scholar
  45. 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 291–312CrossRefGoogle Scholar
  46. 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 110:122–126PubMedCrossRefGoogle Scholar
  47. Cortés E (2002) Incorporating uncertainty into demographic modeling: application to shark populations and their conservation. Conser Biol 16:1048–1062CrossRefGoogle Scholar
  48. 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 403:255–267CrossRefGoogle Scholar
  49. 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. PubMedPubMedCentralCrossRefGoogle Scholar
  50. Davey JW, Blaxter ML (2011) RADSeq: next-generation population genetics. Brief Funct Genomics 5:416–423Google Scholar
  51. 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 6:33753CrossRefGoogle Scholar
  52. DiBattista J (2008) Pattern of genetic variation in anthropogenically impacted populations. Conserv Genet 9:141–156CrossRefGoogle Scholar
  53. 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. CrossRefGoogle Scholar
  54. 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 16:1443–1454CrossRefGoogle Scholar
  55. 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 18:248–261PubMedCrossRefGoogle Scholar
  56. 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 80:1789–1843PubMedCrossRefGoogle Scholar
  57. Dulvy NK, Fowler SL, Musick JA, Cavanagh RD et al (2014) Extinction risk and conservation of the world’s sharks and rays. eLife 3:e00590PubMedPubMedCentralCrossRefGoogle Scholar
  58. Duncan KM, Martin AP, Bowen BW, Couet HG (2006) Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini). Mol Ecol 15:2239–2251PubMedCrossRefGoogle Scholar
  59. Ebert DA, Fowler S, Compagno L (2013) Sharks of the world: a fully illustrated guide. Wild Nature Press, PlymouthGoogle Scholar
  60. 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 106:355–365PubMedCrossRefGoogle Scholar
  61. Federal Register Volume 80, Issue 221 (Nov 17, 2015)Google Scholar
  62. 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 10:295–303PubMedCrossRefGoogle Scholar
  63. 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 23:110–117PubMedCrossRefGoogle Scholar
  64. Ferretti F, Worm B, Britten GL, Heithaus MR, Lotze HK (2010) Patters and ecosystem consequences of shark declines in the ocean. Ecol Lett 13:1055–1071PubMedGoogle Scholar
  65. 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. CrossRefGoogle Scholar
  66. 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 533:237–244CrossRefGoogle Scholar
  67. Fields AT, Feldheim KA, Poulakis GR, Chapman DD (2015) Facultative parthenogenesis in a critically endangered wild vertebrate. Curr Biol 25:446–447CrossRefGoogle Scholar
  68. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  69. 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 21:357–363CrossRefGoogle Scholar
  70. Frankham R (2010) Challenges and opportunities of genetic approaches to biological conservation. Biol Cons 143:1919–1927CrossRefGoogle Scholar
  71. Frankham R (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv 170:56–63CrossRefGoogle Scholar
  72. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  73. 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 10:71–80CrossRefGoogle Scholar
  74. 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 554:99–113CrossRefGoogle Scholar
  75. 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 29:86–91Google Scholar
  76. Fung HC, Waples RS (2017) Perfomance of IUCN proxies for generation length. Cons Biol 31:739–961CrossRefGoogle Scholar
  77. Gaida IH (1997) Population structure of the pacific angel shark, Squatina californica (Squatiniformes: Squatinidae), around the California Channel Islands. Copeia 4:738–744CrossRefGoogle Scholar
  78. Gallagher AJ, Hammerschlag N, Shiffman DS, Giert S (2014) Evolved for extinction: the cost and conservation implications of specialization in hammerhead sharks. Bioscience 67:619–624CrossRefGoogle Scholar
  79. 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 147:36–46CrossRefGoogle Scholar
  80. 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 147:205–214CrossRefGoogle Scholar
  81. 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 86:186–202PubMedCrossRefGoogle Scholar
  82. 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 2:356–363Google Scholar
  83. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318PubMedCrossRefGoogle Scholar
  84. 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:e75169PubMedPubMedCentralCrossRefGoogle Scholar
  85. 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 24:45–60CrossRefGoogle Scholar
  86. 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 90:427–454CrossRefGoogle Scholar
  87. 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 548:165–180CrossRefGoogle Scholar
  88. Goodwin S, McPherson JD, McCombie WR (2016) Coming of age: ten years of next-generation sequencing technologies. Nat Rev Genet 17:333–351PubMedCrossRefGoogle Scholar
  89. Grant WS, Cheng W (2012) Incorporating deep and shallow components of genetic structure into the management of Alaskan red king crab. Evol Appl 5:820–837PubMedPubMedCentralCrossRefGoogle Scholar
  90. 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 3–29CrossRefGoogle Scholar
  91. 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 27:233–241Google Scholar
  92. 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 9:181–195PubMedCrossRefGoogle Scholar
  93. 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 3:438–449CrossRefGoogle Scholar
  94. Hauser L, Carvalho GR (2008) Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish Fish 9:333–362CrossRefGoogle Scholar
  95. 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 99:11742–11747PubMedPubMedCentralCrossRefGoogle Scholar
  96. Heino M, Pauli DB, Dieckmann U (2015) Fisheries-induced evolution. Annu Rev Ecol Evol Syst 46:461–480CrossRefGoogle Scholar
  97. 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 3:555–562CrossRefGoogle Scholar
  98. 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 53:583–588CrossRefGoogle Scholar
  99. 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 94:664–668Google Scholar
  100. Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23:202–210PubMedCrossRefGoogle Scholar
  101. 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 176:132–142CrossRefGoogle Scholar
  102. 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 34:1239–1248CrossRefGoogle Scholar
  103. 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 92:1601–1629PubMedCrossRefGoogle Scholar
  104. 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 21:433–437CrossRefGoogle Scholar
  105. Hoban SM, Hauffe HC, Pérez-Espona S et al (2013a) Bringing genetic diversity to the forefront of conservation policy and management. Conserv Genet Resour 5:593–598CrossRefGoogle Scholar
  106. 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 4:299–303CrossRefGoogle Scholar
  107. Hoban S, Kelley JL, Lotterhos KE et al (2016) Finding the genomic basis of local adaptation: pitfalls, practical solutions, and future directions. Am Nat 188:379–397PubMedPubMedCentralCrossRefGoogle Scholar
  108. Hoelzel AR, Shivji MS, Magnussen J, Francis MP (2006) Low worldwide genetic diversity in the basking sharks (Cetorhinus maximus). Biol Lett 2:639–642PubMedCrossRefGoogle Scholar
  109. Hoffman M, Hilton-Taylor C, Angulo A et al (2010) The impact of conservation on the status of the world’s vertebrates. Science 330:1503–1509CrossRefGoogle Scholar
  110. 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 277:679–688PubMedPubMedCentralCrossRefGoogle Scholar
  111. Karl SA (2008) The effect of multiple paternity on the genetically effective size of a population. Mol Ecol 17:3973–3977PubMedCrossRefGoogle Scholar
  112. 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 12:371–382CrossRefGoogle Scholar
  113. Karl SA, Castro ALF, Garla RC (2012) Population genetics of the nurse shark (Ginglymostoma cirratum) in the western Atlantic. Mar Biol 159:489–498CrossRefGoogle Scholar
  114. 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. PubMedPubMedCentralCrossRefGoogle Scholar
  115. 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 15:3669–3679PubMedCrossRefGoogle Scholar
  116. 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 143:1039–1046CrossRefGoogle Scholar
  117. 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 14:1911–1923PubMedCrossRefGoogle Scholar
  118. Kenchington E, Heino M, Nielsen EE (2003) Managing marine genetic diversity: time for action? ICES J Mar Sci 60:1172–1176CrossRefGoogle Scholar
  119. 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 172:181–189CrossRefGoogle Scholar
  120. 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 114:1–11Google Scholar
  121. Laikre L (2010) Genetic diversity is overlooked in international conservation policy implementation. Conserv Genet 11:349–354CrossRefGoogle Scholar
  122. 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 17:893–910CrossRefGoogle Scholar
  123. 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 25:520–529PubMedCrossRefGoogle Scholar
  124. 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. PubMedPubMedCentralCrossRefGoogle Scholar
  125. Larson SE, Daly-Engel TS, Phillips NM (2017) Review of current conservation genetic analyses of Northeast Pacific sharks. Adv Mar Biol 77:79–110Google Scholar
  126. Last PR, White WT, Carvalho MR, Séret B, Stehmann MFW, Naylor GJP (2016) Rays of the world. Cornell University Press, IthacaGoogle Scholar
  127. Lavery S, Shaklee JB (1989) Population genetics of two tropical sharks, Carcharhinus tilstoni and C. sorrah in Northern Australia. Mar Freshw Res 40:541–547CrossRefGoogle Scholar
  128. 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 103:1–12CrossRefGoogle Scholar
  129. Leberg P (2005) Genetic approaches for estimating the effective size of populations. J Wildl Res 69:1385–1399CrossRefGoogle Scholar
  130. Lessa R, Batista VS, Santana FM (2016) Close to extinction? The collapse of the endemic daggernose shark (Isogomphodon oxyrhynchus) off Brazil. Global Ecol Evol 7:70–81Google Scholar
  131. Letessier TB, Bouchet PJ, Meeuwig JJ (2017) Sampling mobile oceanic fishes and sharks: implications for fisheries and conservation planning. Biol Rev 92:627–646PubMedCrossRefGoogle Scholar
  132. Lewallen EA, Anderson TW, Bohonak AJ (2007) Genetic structure of leopard shark (Triakis semifasciata) populations in California waters. Mar Biol 152:599–609CrossRefGoogle Scholar
  133. 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 51:130–137CrossRefGoogle Scholar
  134. 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 26:505–513CrossRefGoogle Scholar
  135. 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 28:575–578CrossRefGoogle Scholar
  136. 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 21:215–222CrossRefGoogle Scholar
  137. Lucifora LO, García VB, Worm B (2011) Global diversity hotspots and conservation priorities for sharks. PLoS ONE 6:e19356PubMedPubMedCentralCrossRefGoogle Scholar
  138. 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 544:183–196CrossRefGoogle Scholar
  139. Martin AP, Naylor GJP, Palumbi SR (1992) Rate of mitochondrial evolution is low in sharks compared to mammals. Nature 357:153–155PubMedCrossRefGoogle Scholar
  140. Massa A, Hozbor N, Chiaramonte GE, Balestra AD, Vooren CM (2006) Mustelus schmitti. The IUCN Red List of threatened species 2006: e.T60203A12318268. Accessed 07 Nov 2016
  141. McClenachan L, Cooper AB, Dulvy NK (2016) Rethinking trade-driven extinction risk in marine and terrestrial megafauna. Curr Biol 26:1–7CrossRefGoogle Scholar
  142. McCusker MR, Bentzen P (2010) Positive relationships between genetic diversity and abundance in fishes. Mol Ecol 19:4852–4862PubMedCrossRefGoogle Scholar
  143. MacDonald CM (1988) Genetic variation, breeding structure and taxonomic status of the gummy shark Mustelus antarticus in Southern Australian waters. Mar Freshw Res 39:641–648CrossRefGoogle Scholar
  144. 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.CGoogle Scholar
  145. Mendonça FF, Oliveira C, Gadig OBF, Foresti F (2011) Phylogeography and genetic population structure of Caribben sharpnose shark Rhizoprionodon porosus. Rev Fish Biol Fish 21:799–814CrossRefGoogle Scholar
  146. 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 23:850–9857CrossRefGoogle Scholar
  147. 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 131Google Scholar
  148. 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 5:13229PubMedPubMedCentralCrossRefGoogle Scholar
  149. 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 22:201–214PubMedCrossRefGoogle Scholar
  150. 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. PubMedPubMedCentralCrossRefGoogle Scholar
  151. Murray BW, Wang JY, Yang SC, Stevens JD, Fisk A, Svavarsson J (2008) Mitochondrial cytochrome b variation in sleeper sharks (Squaliformes: Somniosidae). Mar Biol 153:1015–1022CrossRefGoogle Scholar
  152. Musick JA, Burgess G, Cailliet G, Camhi M, Fordham S (2000) Management of sharks and their relatives (Elasmobranchii). Fisheries 25:9–13CrossRefGoogle Scholar
  153. 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. PubMedPubMedCentralCrossRefGoogle Scholar
  154. Narun SR, Hess JE (2011) Comparison of F ST outlier tests for SNP loci under selection. Mol Ecol Resour 11:184–194CrossRefGoogle Scholar
  155. Nelson JS, Grande TC, Wilson MHV (2016) Fishes of the world. Wiley, HobokenCrossRefGoogle Scholar
  156. 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 3:503–512CrossRefGoogle Scholar
  157. Nielsen EE, Hansen MM (2008) Waking the dead: the value of population genetic analyses of historical samples. Fish Fish 9:450–461CrossRefGoogle Scholar
  158. Nielsen EE, Hemmer-Hansen J, Larsen PF, Bekkevold D (2009) Population genomics of marine fishes: identifying adaptive variation in space and time. Mol Ecol 18:3128–3150Google Scholar
  159. 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 17:431–442CrossRefGoogle Scholar
  160. 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 106:1–8CrossRefGoogle Scholar
  161. 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 106:347–354PubMedCrossRefGoogle Scholar
  162. 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 9:40PubMedPubMedCentralCrossRefGoogle Scholar
  163. 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 158:1497–1509CrossRefGoogle Scholar
  164. Ovenden JR (2013) Crinkles in connectivity: combining genetics and other types of biological data to estimate movement and interbreeding between populations. Mar Freshwater Res 64:201–207Google Scholar
  165. 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 16:125–159CrossRefGoogle Scholar
  166. 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 89:2505–2518PubMedCrossRefGoogle Scholar
  167. 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 14:125–144Google Scholar
  168. 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 412:139–140Google Scholar
  169. 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 158:2173–2186CrossRefGoogle Scholar
  170. 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 18:1151–1163Google Scholar
  171. 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 106:468–473CrossRefGoogle Scholar
  172. 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 158:903–915CrossRefGoogle Scholar
  173. Pichler FB, Baker CS (2000) Loss of genetic diversity in the endemic Hector’s dolphin due to fisheries-related mortality. Proc Biol Sci 267:97–102PubMedPubMedCentralCrossRefGoogle Scholar
  174. Pinsky ML, Palumbi SR (2014) Meta-analysis reveals lower genetic diversity in overfished populations. Mol Ecol 23:29–39PubMedCrossRefGoogle Scholar
  175. 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 77:329–340PubMedPubMedCentralCrossRefGoogle Scholar
  176. 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 10:1697–1705CrossRefGoogle Scholar
  177. 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 19:1994–2010PubMedCrossRefGoogle Scholar
  178. 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 85:502–508PubMedCrossRefGoogle Scholar
  179. 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 23:5480–5495PubMedCrossRefGoogle Scholar
  180. 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 24:5877–5885PubMedCrossRefGoogle Scholar
  181. 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 73:2322–2332CrossRefGoogle Scholar
  182. 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 9:289–304CrossRefGoogle Scholar
  183. 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 106:448–458CrossRefGoogle Scholar
  184. Ramakrishnan U, Storz JF, Taylor BL, Lande R (2004) Estimation of genetically effective breeding numbers using a rejection algorithm approach. Mol Ecol 13:3283–3292PubMedCrossRefGoogle Scholar
  185. Richards VP, Suzuki H, Stanhope MJ, Shivji MS (2013) Characterization of the heart transcriptome of the shark (Carcharodon carcharias). BMC Genom 4:697CrossRefGoogle Scholar
  186. Rivers MC, Brummitt NA, Lughadha EN, Meagher TR (2014) Do species conservation assessments capture genetic diversity? Global Ecol Evol 2:81–87Google Scholar
  187. Rocha L, Bernal MA, Gaither MR, Alfaro ME (2013) Massively parallel DNA sequencing: the new frontier in biogeography. Front Biogeogr 5:67–77Google Scholar
  188. Rosa RS, Castro ALF, Furtado M, Monzini J, Grubbs RD (2006) Ginglymostoma cirratum. The IUCN Red List of Threatened Species 2006: e.T60223A12325895. Acessed 14 April 2016
  189. Ryman N, Palm S (2006) POWSIM: a computer for assessing statistical power when testing for genetic differentiation. Mol Ecol Resour 6:600–602CrossRefGoogle Scholar
  190. Ryman N, Utter F, Laikre L (1995) Protection of intraspecific biodiversity of exploited fishes. Rev Fish Biol Fish 5:417–446CrossRefGoogle Scholar
  191. Sandoval-Castillo J, Beheregaray LB (2015) Metapopulation structure informs conservation management in a heavily exploited coastal shark (Mustelus henlei). Mar Ecol Prog Ser 533:191–203CrossRefGoogle Scholar
  192. Sandoval-Castillo J, Rocha-Olivares A (2011) Deep mitochondrial divergence in Baja California populations of an aquilopelagic elasmobranch: the golden cownose ray. J Hered 102:269–274PubMedCrossRefGoogle Scholar
  193. 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 145:983–988CrossRefGoogle Scholar
  194. 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 281:46–55CrossRefGoogle Scholar
  195. 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. PubMedPubMedCentralCrossRefGoogle Scholar
  196. Schrey AW, Heist EJ (2003) Microsatellite analysis of population structure in the shortfin mako (Isurus oxyrinchus). Can J Fish Aquat Sci 60:670–675CrossRefGoogle Scholar
  197. 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 17:5336–5348PubMedCrossRefGoogle Scholar
  198. Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33Google Scholar
  199. Seitz JC, Poulakis GR (2006) anthropogenic effects on the smalltooth sawfish (Pristis pectinata) in the United States. Mar Pollut Bull 52:1533–1540PubMedCrossRefGoogle Scholar
  200. 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 106:266–275PubMedCrossRefGoogle Scholar
  201. 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 62:518–527CrossRefGoogle Scholar
  202. 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 4:752–760CrossRefGoogle Scholar
  203. Solé-Cava AM, Vooren CM, Levy JA (1983) Isozymic differentiation of two sibling species of Squatina (Condrichthyes) in southern Brazil. Comp Biochem Physiol 75:355–358Google Scholar
  204. 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 5:2317–2332PubMedPubMedCentralCrossRefGoogle Scholar
  205. 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 25:705–712PubMedCrossRefGoogle Scholar
  206. 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 57:476–494CrossRefGoogle Scholar
  207. 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 2:308–311PubMedPubMedCentralCrossRefGoogle Scholar
  208. 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 147:338–343CrossRefGoogle Scholar
  209. 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 66:267–275CrossRefGoogle Scholar
  210. 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 49:21–29CrossRefGoogle Scholar
  211. Tiffin P, Ross-Ibarra (2014) Advances and limits of using population genetics to understand local adaptation. Trends Ecol Evol 29:673–680PubMedCrossRefGoogle Scholar
  212. 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 13:99–115CrossRefGoogle Scholar
  213. Tillet BJ, Meekan MG, Field IC, Thorburn DC, Ovenden JR (2012b) Evidence fro reproductive philopatry in the bull shark Carcharhinus leucas. J Fish Biol 80:2140–2158CrossRefGoogle Scholar
  214. 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 4:1–7Google Scholar
  215. Uzans AJ, Lucas Z, McLeod BA, Frasier TR (2015) Small Ne of the isolated and unmanaged horse population on Sable Island. J Hered 106:660–665PubMedCrossRefGoogle Scholar
  216. 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 19:1651–1662PubMedCrossRefGoogle Scholar
  217. Veríssimo A, McDowell JR, Graves JE (2011) Population structure of a deep-water squaloid shark, the Portuguese dogfish (Centroscymnus coelolepis). ICES J Mar Sci 68:555–563CrossRefGoogle Scholar
  218. 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 63:505–512CrossRefGoogle Scholar
  219. 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 7:4768–4781PubMedPubMedCentralCrossRefGoogle Scholar
  220. 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. PubMedPubMedCentralCrossRefGoogle Scholar
  221. 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 23:2590–2601PubMedCrossRefGoogle Scholar
  222. 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 23:5193–5207PubMedCrossRefGoogle Scholar
  223. 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 32–56Google Scholar
  224. 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 39:139–163CrossRefGoogle Scholar
  225. Waples R (1995) Evolutionary significant units and the conservation of biological diversity under the endangered’s species. Am Fish Soc Symp 17:8–27Google Scholar
  226. 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 15:1419–1439PubMedCrossRefGoogle Scholar
  227. 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 138:161–165PubMedCrossRefGoogle Scholar
  228. Watts PC, Buley KR, Sanderson S, Boardman W, Ciofi C, Gibson R (2006) Parthenogenesis in Komodo dragons. Nature 444:1021–1022PubMedCrossRefGoogle Scholar
  229. Weigmann S (2016) Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with focus on biogeographical diversity. J Fish Biol 88:837–1037PubMedCrossRefGoogle Scholar
  230. 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 39:1144–1156CrossRefGoogle Scholar
  231. 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 90:79–122CrossRefGoogle Scholar
  232. 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 191:495–503CrossRefGoogle Scholar
  233. 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 40:194–204CrossRefGoogle Scholar
  234. Zeh JA, Zeh DW (2003) Toward a new sexual selection paradigm: polyandry, conflict and incompatibility. Ethology 109:929–950CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2017

Authors and Affiliations

  • Rodrigo Rodrigues Domingues
    • 1
    • 3
    Email author
  • Alexandre Wagner Silva Hilsdorf
    • 2
  • Otto Bismarck Fazzano Gadig
    • 3
  1. 1.Instituto de Biociências de Rio ClaroUniversidade Estadual Paulista, UNESPRio ClaroBrazil
  2. 2.Núcleo Integrado de BiotecnologiaUniversidade de Mogi das CruzesMogi das CruzesBrazil
  3. 3.Laboratório de Pesquisa de Elasmobrânquios, Instituto de BiociênciasUniversidade Estadual Paulista, Campus do Litoral PaulistaSão VicenteBrazil

Personalised recommendations