Marine Biology

, Volume 162, Issue 5, pp 945–955 | Cite as

Global mitochondrial DNA phylogeography and population structure of the silky shark, Carcharhinus falciformis

  • Christopher R. Clarke
  • Stephen A. Karl
  • Rebekah L. Horn
  • Andrea M. Bernard
  • James S. Lea
  • Fabio H. Hazin
  • Paulo A. Prodöhl
  • Mahmood S. ShivjiEmail author
Original Paper


Globally, sharks are under enormous pressure from fishing efforts. One such species is the silky shark, Carcharhinus falciformis, which occurs in all the Earth’s tropical oceans and is captured in large numbers in pelagic fisheries. Regionally, the silky shark is listed as Vulnerable to Near Threatened by the International Union for the Conservation of Nature due to high levels of direct and bycatch exploitation. Despite major conservation concerns about this species, little is known about its genetic status and level of demographic or evolutionary connectivity among its regional distributions. We report a genetic assessment of silky sharks sampled across a major portion of the species’ global range. We sequenced the complete mitochondrial DNA control region from 276 individuals taken from the western Atlantic and Indo-Pacific Oceans and the Red Sea. Overall, haplotype and nucleotide diversities were relatively large (0.93 ± 0.01 and 0.61 ± 0.32 %, respectively). Nucleotide diversity in Indo-Pacific sharks, however, was significantly lower and about half that in Atlantic sharks. Strong phylogeographic partitioning occurred between ocean basins. Furthermore, shallow but significant pairwise statistical differentiation occurred among most regional samples within the Indo-Pacific, but not the western Atlantic. Overall, at least five mitochondrial DNA populations of silky sharks were identified globally. Despite historically large population sizes, silky sharks appear to be isolated on relatively small spatial scales, at least in the Indo-Pacific, indicating that conservation and management efforts will need to be exerted at relatively small scales in a pelagic and highly vagile species.


Population Subdivision Eastern Pacific Shark Species Lemon Shark Nurse Shark 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Funding for this study was provided by the Save Our Seas Foundation, Save Our Seas Shark Research Center, Danah Divers, the Guy Harvey Ocean Foundation and Nova Southeastern University. We thank S. Gulak and D. Bethea (NMFS Panama City Laboratory), and D. McCauley and C. Wilson for contributing shark samples. We are grateful to C. Galván-Tirado and colleagues for providing additional silky shark sequences from their paper, which allowed us to extend our shark assessment to the EP. We specially thank the founder of Save Our Seas Foundation for his vision, passion and efforts in supporting shark research to help understand, preserve and protect these dwindling species around the world.

Supplementary material

227_2015_2636_MOESM1_ESM.pdf (98 kb)
Supplementary material 1 (PDF 98 kb)
227_2015_2636_MOESM2_ESM.pdf (68 kb)
Supplementary material 2 (PDF 68 kb)
227_2015_2636_MOESM3_ESM.pdf (32 kb)
Supplementary material 3 (PDF 31 kb)
227_2015_2636_MOESM4_ESM.pdf (32 kb)
Supplementary material 4 (PDF 31 kb)


  1. Ahonen H, Harcourt RG, Stow AJ (2009) Nuclear and mitochondrial DNA reveals isolation of imperiled grey nurse shark populations (Carcharias taurus). Mol Ecol 18:4409–4421CrossRefGoogle Scholar
  2. Andrews KR, Karczmarski L, Au WWL, Rickards SH, Vanderlip CA, Bowen BW, Grau EG, Toonen RJ (2010) Rolling stones and stable homes: social structure, habitat diversity and population genetics of the Hawaiian spinner dolphin (Stenella longirostris). Mol Ecol 19:732–748CrossRefGoogle Scholar
  3. Aoki M, Wada K (2013) Genetic structure of the wide-ranging fiddler crab Uca crassipes in the west Pacific region. J Mar Biol Assoc UK 93:789–795CrossRefGoogle Scholar
  4. Bailey G (2009) The Red Sea, coastal landscapes, and hominin dispersals. In: Petyraglia M, Rose J (eds) The evolution of human populations in Arabia. Springer, DordrechtGoogle Scholar
  5. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefGoogle Scholar
  6. Beebee T, Rowe G (2008) An introduction to molecular ecology, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  7. Beerkircher L, Cortes E, Shivji MS (2004) Characteristics of shark bycatch observed on pelagic longlines off the southeastern United States, 1992–2000. Mar Fish Rev 64:40–49Google Scholar
  8. Benavides MT, Horn RL, Feldheim KA, Shivji MS, Clarke SC, Wintner S, Natanson L, Braccini M, Boomer JJ, Gulak SJB, Chapman DD (2011) 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
  9. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57(1):289–300Google Scholar
  10. Bonfil R, Amorim A, Anderson C, Arauz R, Baum J, Clarke SC, Graha, RT, Gonzalez M, Jolón M, Kyne PM, Mancini P, Márquez F, Ruí C, Smith W (2009) Carcharhinus falciformis. Version 2014.3. The IUCN Red List of Threatened Species. Accessed 28 Oct 2014
  11. Bonfil R (2008) The biology and ecology of the silky shark, Carcharhinus falciformis. In: Camhi MD, Pikitch EK, Babcock EA (eds) Sharks of the open ocean: biology, fisheries and conservation. Fish and aquatic resources series 13. Blackwell Publishing Ltd., UK, pp 114–127CrossRefGoogle Scholar
  12. Bowen BW, Bass AL, Rocha LA, Grant WS, Robertson DR (2001) Phylogeography of the trumpetfish, genus Aulostomus: ring species complex on a planetary scale. Evolution 55:1029–1039CrossRefGoogle Scholar
  13. Bowen BW, Muss A, Rocha LA, Grant WS (2006) Shallow mtDNA coalescence in Atlantic pygmy anglefishes (genus Centropyge) indicates a recent invasion from the Indian Ocean. J Hered 97:1–12CrossRefGoogle Scholar
  14. Bowen BW, Shanker K, Yasuda N, Malay MCD, von der Heyden S, Paulay G, Rocha LA, Selkoe KA, Barber PH, Williams ST, Lessios HA, Crandall ED, Bernardi G, Meyer CP, Carpenter KE, Toonen RJ (2014) Phylogeography unplugged: comparative surveys in the genomic era. Bull Mar Sci 90:13–46CrossRefGoogle Scholar
  15. Briggs JC, Bowen BW (2012) A realignment of marine biogeographic provinces with particular reference to fish distributions. J Biogeogr 39:12–31CrossRefGoogle Scholar
  16. Briggs JC, Bowen BW (2013) Marine shelf habitat: biogeography and evolution. J Biogeogr 40:1023–1035CrossRefGoogle Scholar
  17. Camhi MD, Valenti SV, Fordham SV, Fowler SL, Gibson C (2009) The conservation status of pelagic sharks and rays: report of the IUCN Shark Specialist Group Pelagic Shark Red List Workshop. IUCN Species Survival Commission Shark Specialist Group. Newbury, UK. x + 78pGoogle Scholar
  18. Castro ALF, Stewart BS, Wilson SG, Hueter RE, Meekan MG, Motta PJ, Bowen BW, Karl SA (2007) Population genetic structure of Earth’s largest fish, the whale shark (Rhincodon typus). Mol Ecol 16:5183–5192CrossRefGoogle Scholar
  19. Chapman DD, Pinhal D, Shivji MS (2009) Tracking the fin trade: genetic stock identification in Western Atlantic scalloped hammerheads sharks (Sphyrna lewini). Endanger Species Res 9:221–228CrossRefGoogle Scholar
  20. 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 102:643–652CrossRefGoogle Scholar
  21. Chow S, Jeffs A, Miyake Y, Konishi K, Okazaki M, Suzuki N, Abdullah MF, Imai H, Wakabayasi T, Sakai M (2011) Genetic isolation between the western and eastern Pacific populations of Pronghorn spiny lobster Panulirus penicillatus. PLoS One 6:e29280. doi: 10.1371/journal.pone.0029280 CrossRefGoogle Scholar
  22. Clarke SC, McAllister MK, Milner-Gulland EJ, Kirkwood GP, Michielsens CGJ, Agnew DJ, Pikitch EK, Nakano H, Shivji MS (2006) Global estimates of shark catches using trade records from commercial markets. Ecol Lett 9:1115–1126CrossRefGoogle Scholar
  23. Clarke C, Lea JSE, Ormond RFG (2011) Reef-use and residency patterns of a baited population of silky sharks, Carcharhinus falciformis, in the Red Sea. Mar Freshw Res 62:668–675CrossRefGoogle Scholar
  24. Clarke SC, Harley SJ, Hoyle SD, Rice JS (2012) Population trends in Pacific oceanic sharks and the utility of regulations on shark finning. Conserv Biol 27(1):197–209CrossRefGoogle Scholar
  25. Clement M, Posada D, Crandall KA (2000) tcs: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660CrossRefGoogle Scholar
  26. Cortés E, Arocha F, Beerkircher L, Carvalho F, Domingo A, Heupel M, Holtzhausen H, Santos MN, Ribera M, Simpfendorfer C (2008) Ecological risk assessment of pelagic sharks caught in Atlantic pelagic longline fisheries. Aquat Living Resour 23:25–34CrossRefGoogle Scholar
  27. Cowman PF, Bellwood DR (2013) Vicariance across major marine biogeographic barriers: temporal concordance and the relative intensity of hard versus soft barriers. Proc R Soc B Biol Sci 280:20131541CrossRefGoogle Scholar
  28. Daly-Engel TS, Seraphin KD, Holland KN, Coffey JP, Nance HA, Toonen RT, 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. doi: 10.1371/journal.pone.0029986 CrossRefGoogle Scholar
  29. DiBattista JD, Berumen ML, Gaither MR, Rocha LA, Eble JA, Choat JH, Craig MT, Skillings DJ, Bowen BW (2013) After continents divide: comparative phylogeography of reef fishes from the Red Sea and Indian Ocean. J Biogeogr 40:1170–1181CrossRefGoogle Scholar
  30. Duncan KM, Martin AP, Bowen BW, de Couet G (2006) Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini). Mol Ecol 15:2239–2251CrossRefGoogle Scholar
  31. Eble JA, Toonen RJ, Sorenson L, Basch LB, Papastamatiou YP, Bowen BW (2011) Escaping paradise: larval export form Hawaii in an Indo-Pacific reef fish, the yellow tang Zebrasoma flavescens. Mar Ecol Prog Ser 428:245–258CrossRefGoogle Scholar
  32. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  33. Feldheim KA, Gruber SH, Ashley V (2001) Population genetic structure of the lemon shark (Negaprion brevirostris) in the western Atlantic: DNA microsatellite variation. Mol Ecol 10:295–303CrossRefGoogle Scholar
  34. Ferretti F, Myers RA, Serena F, Lotze HK (2008) Loss of large predatory sharks from the Mediterranean Sea. Conserv Biol 22:952–964CrossRefGoogle Scholar
  35. 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
  36. Geraghty PT, Williamson JE, Macbeth WG, Wintner SP, Harry AV, Ovenden JR, Gillings MR (2013) Population expansion and genetic structure in Carcharhinus brevipinna in the Southern Indo-Pacific. PLoS One 8(9):e75169. doi: 10.1371/journal.pone.0075169 CrossRefGoogle Scholar
  37. Geraghty PT, Williamson JE, Macbeth WG, Blower MJ, 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
  38. Giles JL, Ovenden JR, Dharmadi AD, 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
  39. Habel JC, Schmitt T (2012) The burden of genetic diversity. Biol Conserv 147:270–274CrossRefGoogle Scholar
  40. Hoelzel AR, Shivji MS, Magnussen J, Francis MP (2006) Low worldwide genetic diversity in the basking shark (Cetorhinus maximus). Biol Lett 2:639–642CrossRefGoogle Scholar
  41. Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155:2011–2014Google Scholar
  42. ICCAT (2011) Recommendation by ICCAT on the conservation of silky sharks caught in association with ICCAT fisheries, 11-08 BYC. Accessed 28 Oct 2014
  43. Karl SA, Castro ALF, Lopez JA, Charvet P, Burgess GH (2011) Phylogeography and conservation of the bull shark (Carcharhinus leucas) inferred from mitochondrial and microsatellite DNA. Conserv Genet 12:371–382CrossRefGoogle Scholar
  44. Karl SA, Castro ALF, Garla RC (2012a) Population genetics of the nurse shark (Ginglymostoma cirratum) in the western Atlantic. Mar Biol 159:489–498CrossRefGoogle Scholar
  45. Karl SA, Toonen RJ, Grant WS, Bowen BW (2012b) Common misconceptions in molecular ecology: echoes of the modern synthesis. Mol Ecol 21:4171–4189CrossRefGoogle Scholar
  46. 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 15:3669–3679CrossRefGoogle Scholar
  47. Keeney DB, Heupel MR, Hueter RE, Heist EJ (2005) Microsatellite and mitochondrial DNA analyses of the genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the northwestern Atlantic, Gulf of Mexico, and Caribbean Sea. Mol Ecol 14:1911–1923CrossRefGoogle Scholar
  48. Kohler NE, Turner PA (2001) Shark tagging: a review of conventional methods and studies. Environ Biol Fishes 60:191–223CrossRefGoogle Scholar
  49. Kohler NE, Casey JG, Turner PA (1998) NMFS cooperative shark tagging program, 1962–1993: an atlas of shark tag and recapture data. Mar Fish Rev 60:1–87Google Scholar
  50. Librado P, Rozas J (2009) dnasp v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefGoogle Scholar
  51. Marko PB (2002) Fossil calibration of molecular clocks and the divergence times of geminate species pairs separated by the Isthmus of Panama. Mol Biol Evol 19:2005–2021CrossRefGoogle Scholar
  52. MigraMar (2011) Silky shark tagged in Galapagos is detected at Clipperton Atoll. Accessed 28 Oct 2014
  53. Nance HA, Klimley P, Galván-Magan M-OJ, Marko PB (2011) Demographic processes underlying subtle patterns of population structure in the scalloped hammerhead shark, Sphyrna lewini. PLoS One 6:e21459. doi: 10.1371/journal.pone.0021459 CrossRefGoogle Scholar
  54. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefGoogle Scholar
  55. Pérez-Jiménez JC (2014) Historical records reveal potential extirpation of four hammerhead sharks (Sphyrna spp.) in Mexican Pacific waters. Rev Fish Biol Fish 24:671–683CrossRefGoogle Scholar
  56. Pinsky ML, Palumbi SR (2014) Meta-analysis reveals lower genetic diversity in overfished populations. Mol Ecol 23:29–39CrossRefGoogle Scholar
  57. Portnoy DS, McDowell JR, Heist EJ, Musick JA, Graves JA (2010) World phylogeography and male-mediated gene flow in the sandbar shark, Carcharhinus plumbeus. Mol Ecol 19:1994–2010CrossRefGoogle Scholar
  58. Reece JS, Bowen BW, Smith DG, Larson AF (2010) Molecular phylogenetics of moray eels (Muraenidae) demonstrates multiple origins of shell-crushing jaw (Gymnomuraena, Echidna) and multiple colonization of the Atlantic Ocean. Mol Phylogenet Evol 57:829–835CrossRefGoogle Scholar
  59. Richards VP, Henning M, Witzell W, Shivji MS (2009) Species delineation and evolutionary history of the globally distributed spotted eagle ray (Aetobatus narinari). J Hered 100:273–283CrossRefGoogle Scholar
  60. Roberts MA, Schwartz TS, Karl SA (2004) Global population genetic structure and male-mediated gene flow in the green sea turtle (Chelonia mydas): analysis of microsatellite loci. Genetics 166:1857–1870CrossRefGoogle Scholar
  61. Rocha LA, Robertson DR, Roman J, Bowen BW (2005a) Ecological speciation in tropical reef fishes. Proc R Soc B Biol Sci 272:573–579CrossRefGoogle Scholar
  62. Rocha LA, Robertson DR, Rocha CR, Van Tassell JL, Craig MT, Bowen BW (2005b) Recent invasion of the tropical Atlantic by an Indo-Pacific coral reef fish. Mol Ecol 14:3921–3928CrossRefGoogle Scholar
  63. Sánchez-de Ita JA, Quiñónez-Velázquez C, Galván-Magaña F, Bocanegra-Castillo N, Félix-Uraga R (2011) Age and growth of the silky shark Carcharhinus falciformis from the west coast of Baja California Sur, Mexico. J App Ichthyol 27:20–24CrossRefGoogle Scholar
  64. Schmidt JV, Schmidt CL, Ozer F, Ernst RE, Feldheim KA, Ashley M, Levine M (2009) Low genetic differentiation across three major ocean populations of the Whale shark, Rhincodon typus. PLoS One 4:e4988. doi: 10.1371/journal.pone.0004988 CrossRefGoogle Scholar
  65. 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
  66. Schultz JK, Feldehim K, Gruber SH, Ashley MV, McGovern TM, Bowen BW (2008) Global phylogeography and seascape genetics of the lemon sharks (genus Negaprion). Mol Ecol 17:5336–5348CrossRefGoogle Scholar
  67. Shivji MS (2010) DNA forensic applications in shark management and conservation. In: Carrier JC, Heithaus MR, Musick JA (eds) Sharks and their relatives II: biodiversity, adaptive physiology, and conservation. CRC Press, Boca Raton, pp 593–610CrossRefGoogle Scholar
  68. Siddall M, Rohling EJ, Almogi-Labin A, Hemleben C, Meischner D, Schmelzer I, Smeed DA (2003) Sea-level fluctuations during the last glacial cycle. Nature 423:853–858CrossRefGoogle Scholar
  69. Sodré D, Rodrigues-Filho LFS, Souza RFC, Rêgo PS, Schneider H, Sampaio I, Vallinoto M (2012) Inclusion of South American samples reveals new population structuring of the blacktip shark (Carcharhinus limbatus) in the western Atlantic. Genet Mol Biol 35:752–760CrossRefGoogle Scholar
  70. Villesen P (2007) FaBox: an online toolbox for fasta sequences. Mol Ecol Notes 7(6):965–968CrossRefGoogle Scholar
  71. Ward-Paige CA, Mora C, Lotze HK, Pattengill-Semmens C, McClenachan L, Arias-Castro E, Myers RA (2010) Large-scale absence of sharks on reefs in the greater-Caribbean: a footprint of human pressures. PLoS One 5:e11968. doi: 10.1371/journal.pone.0011968 CrossRefGoogle Scholar
  72. Watson JT, Essington TE, Lennert-Cody CE, Hall MA (2008) Trade-offs in the design of fishery closures: management of silky shark bycatch in the eastern Pacific ocean tuna fishery. Conserv Biol 23:626–635CrossRefGoogle Scholar
  73. 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
  74. Yokota L, Lessa RP (2006) A nursery area for sharks and rays in northeastern Brazil. Environ Biol Fishes 75:349–360CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Christopher R. Clarke
    • 1
  • Stephen A. Karl
    • 2
  • Rebekah L. Horn
    • 3
  • Andrea M. Bernard
    • 3
  • James S. Lea
    • 1
  • Fabio H. Hazin
    • 5
  • Paulo A. Prodöhl
    • 6
  • Mahmood S. Shivji
    • 3
    • 4
    Email author
  1. 1.Danah Divers Marine Research FacilityJeddahSaudi Arabia
  2. 2.Hawai‘i Institute of Marine BiologyUniversity of Hawai‘iKāne‘oheUSA
  3. 3.Save Our Seas Shark Research Center USANova Southeastern UniversityDania BeachUSA
  4. 4.Guy Harvey Research InstituteNova Southeastern UniversityDania BeachUSA
  5. 5.Departamento de Pesca e AquiculturaUniversidade Federal Rural de PernambucoRecifeBrazil
  6. 6.Medical Biology Centre, School of Biological Sciences, Institute for Global Food SecurityQueen’s University BelfastBelfastIreland

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