Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

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

    Article  CAS  Google Scholar 

  • 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 19:732–748

    Article  CAS  Google Scholar 

  • 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 93:789–795

    Article  CAS  Google Scholar 

  • 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, Dordrecht

    Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  Google Scholar 

  • Beebee T, Rowe G (2008) An introduction to molecular ecology, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • 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 64:40–49

    Google Scholar 

  • 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 14:13–22

    Article  Google Scholar 

  • 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):289–300

    Google Scholar 

  • 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. http://www.iucnredlist.org/details/39370/0. Accessed 28 Oct 2014

  • 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 114–127

    Chapter  Google Scholar 

  • 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 55:1029–1039

    Article  CAS  Google Scholar 

  • 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 97:1–12

    Article  CAS  Google Scholar 

  • 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 90:13–46

    Article  Google Scholar 

  • Briggs JC, Bowen BW (2012) A realignment of marine biogeographic provinces with particular reference to fish distributions. J Biogeogr 39:12–31

    Article  Google Scholar 

  • Briggs JC, Bowen BW (2013) Marine shelf habitat: biogeography and evolution. J Biogeogr 40:1023–1035

    Article  Google Scholar 

  • 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 + 78p

  • 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 16:5183–5192

    Article  CAS  Google Scholar 

  • 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 9:221–228

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 9:1115–1126

    Article  Google Scholar 

  • 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 62:668–675

    Article  Google Scholar 

  • 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):197–209

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) tcs: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  Google Scholar 

  • 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 23:25–34

    Article  Google Scholar 

  • 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 280:20131541

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 40:1170–1181

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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 428:245–258

    Article  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  • 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 10:295–303

    Article  CAS  Google Scholar 

  • Ferretti F, Myers RA, Serena F, Lotze HK (2008) Loss of large predatory sharks from the Mediterranean Sea. Conserv Biol 22:952–964

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 24:45–60

    Article  Google Scholar 

  • 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 90:427–454

    Article  Google Scholar 

  • Habel JC, Schmitt T (2012) The burden of genetic diversity. Biol Conserv 147:270–274

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155:2011–2014

    CAS  Google Scholar 

  • ICCAT (2011) Recommendation by ICCAT on the conservation of silky sharks caught in association with ICCAT fisheries, 11-08 BYC. http://www.ccsbt.org/userfiles/file/other_rfmo_measures/iccat/ICCAT_2011-08.pdf. Accessed 28 Oct 2014

  • 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 12:371–382

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Karl SA, Toonen RJ, Grant WS, Bowen BW (2012b) Common misconceptions in molecular ecology: echoes of the modern synthesis. Mol Ecol 21:4171–4189

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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 14:1911–1923

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • 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 60:1–87

    Google Scholar 

  • Librado P, Rozas J (2009) dnasp v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  Google Scholar 

  • 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 19:2005–2021

    Article  CAS  Google Scholar 

  • MigraMar (2011) Silky shark tagged in Galapagos is detected at Clipperton Atoll. http://migramar.org/hi/home/silky-shark-tagged-in-galapagos-is-detected-at-clipperton-atoll/. Accessed 28 Oct 2014

  • 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

    Article  Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  Google Scholar 

  • Pérez-Jiménez JC (2014) Historical records reveal potential extirpation of four hammerhead sharks (Sphyrna spp.) in Mexican Pacific waters. Rev Fish Biol Fish 24:671–683

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 19:1994–2010

    Article  CAS  Google Scholar 

  • 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 57:829–835

    Article  CAS  Google Scholar 

  • 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 100:273–283

    Article  CAS  Google Scholar 

  • 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 166:1857–1870

    Article  CAS  Google Scholar 

  • Rocha LA, Robertson DR, Roman J, Bowen BW (2005a) Ecological speciation in tropical reef fishes. Proc R Soc B Biol Sci 272:573–579

    Article  Google Scholar 

  • 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 14:3921–3928

    Article  Google Scholar 

  • 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 27:20–24

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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 593–610

    Chapter  Google Scholar 

  • 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 423:853–858

    Article  CAS  Google Scholar 

  • 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 35:752–760

    Article  Google Scholar 

  • Villesen P (2007) FaBox: an online toolbox for fasta sequences. Mol Ecol Notes 7(6):965–968

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 23:626–635

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Yokota L, Lessa RP (2006) A nursery area for sharks and rays in northeastern Brazil. Environ Biol Fishes 75:349–360

    Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Danah Divers Marine Research Facility, Beach Palace, P.O. Box 10646, Jeddah, 21443, Saudi Arabia

    Christopher R. Clarke & James S. Lea

  2. Hawai‘i Institute of Marine Biology, University of Hawai‘i, Mānoa, P.O. Box 1346, Kāne‘ohe, HI, 96744, USA

    Stephen A. Karl

  3. Save Our Seas Shark Research Center USA, Nova Southeastern University, 8000 North Ocean Drive, Dania Beach, FL, 33004, USA

    Rebekah L. Horn, Andrea M. Bernard & Mahmood S. Shivji

  4. Guy Harvey Research Institute, Nova Southeastern University, 8000 North Ocean Drive, Dania Beach, FL, 33004, USA

    Mahmood S. Shivji

  5. Departamento de Pesca e Aquicultura, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros, s/n, Dois Irmãos, Recife, PE, 52171-032, Brazil

    Fabio H. Hazin

  6. Medical Biology Centre, School of Biological Sciences, Institute for Global Food Security, Queen’s University Belfast, 97 Lisburn Road, Belfast, BT9 7BL, Ireland

    Paulo A. Prodöhl

Authors
  1. Christopher R. Clarke
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen A. Karl
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rebekah L. Horn
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andrea M. Bernard
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. James S. Lea
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fabio H. Hazin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Paulo A. Prodöhl
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mahmood S. Shivji
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mahmood S. Shivji.

Additional information

Communicated by T. Reusch.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Clarke, C.R., Karl, S.A., Horn, R.L. et al. Global mitochondrial DNA phylogeography and population structure of the silky shark, Carcharhinus falciformis . Mar Biol 162, 945–955 (2015). https://doi.org/10.1007/s00227-015-2636-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-015-2636-6

Keywords

Search

Navigation