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Restricted connectivity and population genetic fragility in a globally endangered Hammerhead Shark

Abstract

Vagile, large-bodied marine organisms frequently have wide range dispersion but also dependence on coastal habitats for part of their life history. These characteristics may induce complex population genetic structure patterns, with resulting implications for the management of exploited populations. The scalloped hammerhead, Sphyrna lewini, is a cosmopolitan, migratory shark in tropical and warm temperate waters, inhabiting coastal bays during parturition and juvenile development, and the open ocean as adults. Here, we investigated the genetic connectivity and diversity of S. lewini in the western Atlantic using large sample coverage (N = 308), and data from whole mitochondrial control region (mtCR) sequences and ten nuclear microsatellite markers We detected significant population genetic structure with both mtCR and microsatellites markers (mtCR: ΦST = 0.60; p < 0.001; microsatellites: Dest 0.0794, p = 0.001, FST = 0.046, p < 0.05), and isolation by distance (mtCR r = 0.363, p = 0.009; microsatellites markers r = 0.638, p = 0.007). Migration and gene flow patterns were asymmetric and female reproductive philopatry is postulated to explain population subdivisions. The notable population differentiation at microsatellites markers indicates low-levels of male-mediated gene flow in the western Atlantic. The overall effective population size was estimated as 299 (215–412 CI), and there was no evidence of strong or recent bottleneck effects. Findings of at least three management units, moderate genetic diversity, and low effective population size in the context of current overfishing calls for intensive management aimed at short and long-term conservation for this endangered species in the western Atlantic Ocean.

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Data accessibility

The sequencing data and microsatellite dataset of Sphyrna lewini in this study are archived in GenBank (accession numbers: MK636839-MK636863) and Dryad database (https://doi.org/10.5061/dryad.pp8js50), respectively.

References

  1. Abercrombie DL, Clarke SC, Shivji MS (2005) Global-scale genetic identification of hammerhead sharks: application to assessment of the international fin trade and law enforcement. Conserv Genet 6:775–788

    CAS  Google Scholar 

  2. Alcala N, Goudet J, Vuilleumier S (2014) On the transition of genetic differentiation from isolation to panmixia: what we can learn from GST and D. Theor Popul Biol 93:75–84

    PubMed  Google Scholar 

  3. Andreotti S, Rutzen M, van Der Walt S, Von der Heyden S, Henriques R, Meÿer M, Oosthuizen H, Matthee 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

    CAS  Google Scholar 

  4. Ashe JL, Feldheim 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

    Google Scholar 

  5. Barker AM, Adams DH, Driggers WB, Frazier BS, Portnoy DS (2019) Hybridization between sympatric hammerhead sharks in the Western North Atlantic Ocean. Biol Lett 15(4):1–5

    Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  8. 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

    CAS  PubMed  Google Scholar 

  9. 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 Biog 44:2488–2500

    Google Scholar 

  10. Cao Y, Wadell PJ, Okada N, Hasegawa M (1998) The complete mitochondrial DNA sequence of the shark Mustelus manazo: evaluating rooting contradictions to living bony vertebrates. Mol Biol Evol 15:1637–1646

    CAS  PubMed  Google Scholar 

  11. Carmo CB, Ferrette BLS, Camargo SM, Roxo FF, Garla RC, Oliveira C, Piercy AN, Bornatowski H, Foresti F, Burgess GH, Mendonça FF (2019) A new map of the tiger shark (Galeocerdo cuvier) genetic population structure in the western Atlantic Ocean: hypothesis of an equatorial convergence centre. Aquat Conserv Mar Freshw Ecosyst 29:760–772

    Google Scholar 

  12. 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

    Google Scholar 

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

    PubMed  Google Scholar 

  14. 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

    PubMed  Google Scholar 

  15. Cockerham CC, Weir BS (1993) Estimation of gene flow from F-statistics. Evolution 47:855–863

    PubMed  Google Scholar 

  16. Cortés E, Arocha F, Beerkircher L, Carvalho F, Domingos A, Heupel M, Holtzhausen H, Santos MN, Ribera M, Simpfendorfer C (2010) Ecological risk assessment of pelagic sharks caught in Atlantic pelagic longline fisheries. Aquat Living Resour 23:25–34

    Google Scholar 

  17. Crandall KA, Bininda-Emonds ORR, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295

    CAS  Google Scholar 

  18. 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

    CAS  Google Scholar 

  19. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Devloo-Delva F, Maes GE, Hernández SI, Mcallister JD, Gunasekera RM, Grewe PM, Thomson RB, Feutry P (2019) Accounting for kin sampling reveals genetic connectivity in Tasmanian and New Zealand school sharks, Galeorhinus galeus. Ecol Evol 9:4465–4472

    PubMed  PubMed Central  Google Scholar 

  21. Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: Re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214

    CAS  PubMed  Google Scholar 

  22. Domingues RR, Hilsdorf AWS, Gadig OBF (2018a) The importance of considering genetic diversity in shark and ray conservation policies. Conserv Genet 19:501–525

    CAS  Google Scholar 

  23. Domingues RR, Hilsdorf AWS, Shivji MS, Hazin FVH, Gadig OBF (2018b) 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 28:213–227

    Google Scholar 

  24. Domingues RR, Bruels CC, Gadig OBF, Chapman DD, Hilsdorf AWS, Shivji MS (2019) Genetic connectivity and phylogeography of the night shark (Carcharhinus signatus) in the western Atlantic Ocean: implications for conservation management. Aquat Conserv Mar Freshw Ecosyst 29:102–114

    Google Scholar 

  25. 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 Genet 16:1443–1454

    Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  28. Ebert D, Fowler S, Compagno L (2013) Sharks of the World: a fully illustrated guide. Wild Nature Press, Plymouth

    Google Scholar 

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

    CAS  Google Scholar 

  30. Excoffier L, Lischer H (2010) Arlequin ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resourc 10:564–567

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1787

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Ferrette BL, Mendonça FF, Coelho R, Oliveira PGV, Hazin FHV, Romanov EV, Oliveira C, Santos MN, Foresti F (2015) High connectivity of the crocodile shark between the Atlantic and southwest Indian oceans: highlights for conservation. PLoS ONE 10:e0117549

    Google Scholar 

  34. Ferrette BL, Domingues RR, Ussami LHF, Moraes L, Magalhães CO et al (2019) DNA-based species identification of shark finning seizures in Southwest Atlantic: implications for wildlife trade surveillance and law enforcement. Biodivers Conserv 28:4007–4025

    Google Scholar 

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

    PubMed  Google Scholar 

  36. Floeter SR, Rocha LA, Robertson DR, Joyeux JC, Smith-Vaniz WF, Wirtz P, Edwards AJ, Barreiros JP, Ferreira CEL, Gasparini JL, Brito A, Falcon JM, Bowen BW, Bernardi G (2008) Atlantic reef fish biogeography and evolution. J Biogeogr 35:22–47

    Google Scholar 

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

    Google Scholar 

  38. Funk WC, McKay JK, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27:489–494

    PubMed  PubMed Central  Google Scholar 

  39. Gallagher AJ, Klimley AP (2018) The biology and conservation status of the large hammerhead shark complex: the great, scalloped, and smooth hammerheads. Rev Fish Biol Fish 28:777–794

    Google Scholar 

  40. Gallagher AJ, Orbesen ES, Hammerschlag N, Serafy JE (2014) Vulnerability of oceanic sharks as pelagic longline bycatch. Glob Ecol Conserv 1:50–59

    Google Scholar 

  41. Graves JE (1998) Molecular insights into the population structures of cosmopolitan marine fishes. J Hered 89:427–437

    CAS  Google Scholar 

  42. Hare MP, Nunney L, Schwartz MK, Ruzzante DE, Burford M, Waples RS, Ruegg K, Palstra F (2011) Understanding and estimating effective population size for practical application in marine species management. Conserv Biol 25:438–449

    PubMed  Google Scholar 

  43. 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 99:11742–11747

    CAS  PubMed  Google Scholar 

  44. Hayes CG, Jiao Y, Cortés E (2009) Stock assessment of scalloped hammerheads in the western north Atlantic Ocean and Gulf of Mexico. N Am J Fish Manag 29:1406–1417

    Google Scholar 

  45. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  46. Jombart T (2008) Adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94

    PubMed  PubMed Central  Google Scholar 

  48. Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  51. Keenan K, Mcginnity P, Cross TF, Crozier WW, Prodöhl PA (2013) DiveRsity: An R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol Evol 4:782–788

    Google Scholar 

  52. Kohler NE, Turner PA (2001) Shark tagging: a review of conventional methods and studies. Environ Biol Fishes 60:191–223

    Google Scholar 

  53. Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Kulbicki M, Parravicini V, Bellwood DR, Arias-Gonzalez E, Chabanet P, Floeter SR, Friedlander A, McPherson J, Myers RE, Vigliola L, Mouillot D (2013) Global biogeography of reef fishes: a hierarchical quantitative delineation of regions. PLoS ONE 8:e81847

    PubMed  PubMed Central  Google Scholar 

  55. Lowe WH, Allendorf FW (2010) What can genetics tell us about population connectivity? Mol Ecol 19:3038–3051

    PubMed  Google Scholar 

  56. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Morales MJA, Mendonça FF, Magalhães CO, Oliveira C, Coelho R, Santos MSN, Cruz VP, Piercy A, Burgess G, Hazin FVH, Foresti F (2018) Population genetics of the bigeye thresher shark Alopias superciliosus in the Atlantic and Indian Oceans: implications for conservation. Rev Fish Biol Fish 28:941–951

    Google Scholar 

  58. Nachtigall PG, Rodrigues-Filho LFS, Sodré DCA et al (2017) A multiplex PCR approach for the molecular identification and conservation of the critically endangered daggernose shark. Endanger Species Res 32:169–175

    Google Scholar 

  59. Nance HA, Daly-Engel TS, Marko PB (2009) New microsatellite loci for the endangered scalloped hammerhead shark, Sphyrna lewini. Mol Ecol Notes 9:955–957

    CAS  Google Scholar 

  60. Nance HA, Klimley P, Galván-Magaña F, Martínez-Ortíz J, Marko PB (2011) Demographic processes underlying subtle patterns of population structure in the scalloped hammerhead shark. Sphyrna lewini. PLoS One 6:e21459

    PubMed  Google Scholar 

  61. 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

    Google Scholar 

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

    Google Scholar 

  63. 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

    PubMed  PubMed Central  Google Scholar 

  64. Ovenden JR, Morgan JAT, Street R, Tobin A, Simpfendorfer C, Macbeth W, Welch D (2011) Negligible evidence for regional genetic population structure for two shark species Rhizoprionodon acutus (Rüppell, 1837) and Sphyrna lewini (Griffith & Smith, 1834) with contrasting biology. Mar Biol 158:1497–1509

    Google Scholar 

  65. Palsbøll PJ, Bérubé M, Allendorf FW (2007) Identification of management units using population genetic data. Trends Ecol Evol 22:12–16

    Google Scholar 

  66. Pew J, Muir PH, Wang J, Frasier TR (2015) related: An R package for analysing pairwise relatedness from codominant molecular markers. Mol Ecol Resour 15:557–561

    PubMed  Google Scholar 

  67. Pinhal D, Gadig OBF, Wasko AP, Oliveira C, Ron E, Foresti F, Martins C (2008) Discrimination of shark species by simple PCR of 5S rDNA repeats. Genet Mol Biol 31:361–365

    CAS  Google Scholar 

  68. Pinhal D, Gadig OBF, Martins C (2009) Genetic identification of the sharks Rhizoprionodon porosus and R. lalandii by PCR-RFLP and nucleotide sequence analyses of 5S rDNA. Conserv Genet Resour 1:35

    Google Scholar 

  69. Pinhal D, Shivji MS, Vallinoto M, Chapman DD, Gadig OBF, Martins C (2012) Cryptic hammerhead shark lineage occurrence in the western South Atlantic revealed by DNA analysis. Mar Biol 159:829–836

    CAS  Google Scholar 

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

    PubMed  Google Scholar 

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

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Putman AI, Carbone I (2014) Challenges in analysis and interpretation of microsatellite data for population genetic studies. Ecol Evol 4:4399–4428

    PubMed  PubMed Central  Google Scholar 

  75. Quattro JM, Driggers WB, Grady JM, Ulrich GF, Roberts MA (2013) Sphyrna gilberti sp. Nov., a new hammerhead shark (Carcharhiniformes, Sphyrnidae) from the western Atlantic Ocean. Zootaxa 3702:159–178

    PubMed  Google Scholar 

  76. Quintanilla 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 of Colombia. J Hered 106:448–458

    CAS  PubMed  Google Scholar 

  77. R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. R Found Stat Comput Vienna, Austria

  78. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Raymond M, Rousset F (1995) GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  80. Rigby CL, Dulvy NK, Barreto R, Carlson J, Fernando D, Fordham S, Francis MP, Herman K, Jabado RW, Liu KM, Marshall A, Pacoureau N, Romanov E, Sherley RB, Winker H (2019) Sphyrna lewini. The IUCN red list of threatened species 2019: e.T39385A2918526. Downloaded on 18 March 2020

  81. 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

    CAS  Google Scholar 

  82. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    CAS  PubMed  Google Scholar 

  83. 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

    CAS  Google Scholar 

  84. 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

    PubMed  PubMed Central  Google Scholar 

  85. Spalding MD, Fox HE, Allen GR, Davidson N, Ferdana ZA, Finlayson M, Halpern BS, Jorge MA, Lombana A, Lourie SA, Martin KD, Mcmanus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioSci 57:573–583

    Google Scholar 

  86. Sundqvist L, Keenan K, Zackrisson M, Prodöhl P, Kleinhans D (2016) Directional genetic differentiation and relative migration. Ecol Evol 6:3461–3475

    PubMed  PubMed Central  Google Scholar 

  87. Theisen TC, Bowen BW, Lanier W, Baldwin JD (2008) High connectivity on a global scale in the pelagic wahoo, Acanthocybium solandri (tuna family Scombridae). Mol Ecol 17:4233–4247

    CAS  PubMed  Google Scholar 

  88. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Google Scholar 

  89. 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

    PubMed  PubMed Central  Google Scholar 

  90. Villesen P (2007) FaBox: an online toolbox for FASTA sequences. Mol Ecol Notes 7:965–968

    CAS  Google Scholar 

  91. Wang J (2002) An estimator for pairwise relatedness using molecular markers. Genetics 160:1203–1215

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262

    PubMed  Google Scholar 

  93. Weersing K, Toonen RJ (2009) Population genetics, larval dispersal, and connectivity in marine systems. Mar Ecol Prog Ser 393:1–12

    Google Scholar 

  94. Wells RJD, TinHan TC, Dance MA, Drymon JM, Falterman B, Ajemian MJ, Stunz GW, Mohan JA, Hoffmayer ER, Driggers WB III, McKinney JA (2018) Movement, behavior, and habitat use of a marine apex predator, the scalloped hammerhead. Front Mar Sci. https://doi.org/10.3389/fmars.2018.00321

    Article  Google Scholar 

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Acknowledgements

We thank Alexandre Azevedo, Silas C. Souza and several fishermen for providing scalloped hammerhead samples. We are grateful to Rebekah L. Horn and Andrea M. Bernard (Save Our Seas Shark Research Center) for laboratory assistance.

Funding

This research was supported by grants from São Paulo Research Foundation – FAPESP to D. Pinhal (#2007/03067-8), R. Domingues (#2017/02420-8) and C. Martins (#2007/03065-5), and the Save Our Seas Foundation and Guy Harvey Ocean Foundation to M. Shivji.

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DP, CM, MS designed the study; DP, OBFG, MS collected data; DP and CB performed lab work; RRD, DP, BF analyzed the data; RRD and DP wrote the manuscript; all authors edited and revised the manuscript.

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Correspondence to Danillo Pinhal.

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Pinhal, D., Domingues, R.R., Bruels, C.C. et al. Restricted connectivity and population genetic fragility in a globally endangered Hammerhead Shark. Rev Fish Biol Fisheries 30, 501–517 (2020). https://doi.org/10.1007/s11160-020-09607-x

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Keywords

  • elasmobranch conservation
  • Endangered species
  • Genetic connectivity
  • Genetic diversity