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Phylogeography and conservation of the bull shark (Carcharhinus leucas) inferred from mitochondrial and microsatellite DNA

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Abstract

The bull shark (Carcharhinus leucas) is a widely distributed, large coastal shark species known to travel long distances. These characteristics, coupled with the species’ long life span and late age of maturity, would lead one to predict significant global genetic exchange among bull shark populations. By contrast, data show localized depletion in some areas of large coastal shark fisheries, indicating some geographic isolation may exist. We examined genetic variation in the control region of mitochondrial DNA and at five nuclear microsatellite loci in bull sharks sampled from the western Atlantic to investigate the degree of population subdivision. The average per sample haplotype and nucleotide diversity in the mtDNA (0.51 ± 0.26 and 0.12% ± 0.12, respectively) and expected heterozygosity (0.84) in the microsatellite loci contrast sharply in having lower and higher values (respectively) relative to many other shark species. Significant structure exists between the Brazilian and all northern populations at the mtDNA control region (pairwise ΦST > 0.8, P < 0.001), but not at the nuclear microsatellite loci. Adjacent northern populations show weak to no genetic differentiation for both markers. These results are congruent with restricted maternal gene flow between populations caused by female site fidelity to nursery areas. We estimate the current effective population size to be around 160,000 and 221,000 individuals for the southern and northern Atlantic populations, respectively. The philopatric habits and the relatively low levels of mtDNA genetic diversity observed in bull sharks must be considered in the conservation of this species. Our results indicate that effective bull shark management strategies will require local, regional, and international attention and cooperation.

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References

  • Almeida OT, McGrath DG, Ruffino ML (2001) The commercial fisheries of the lower Amazon: an economic analysis. Fish Manag Ecol 8:253–269

    Article  Google Scholar 

  • Avise JC (2004) Molecular markers, natural history, and evolution. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744

    Article  PubMed  Google Scholar 

  • Barker JS, Frydenberg J, Gonzalez J, Davies HI, Ruiz A, Sorensen JG, Loeschcke V (2009) Bottlenecks, population differentiation and apparent selection at microsatellite loci in Australian Drosophila buzzatti. Heredity 102:389–401

    Article  PubMed  CAS  Google Scholar 

  • Baum JK, Myers RA (2004) Shifting baselines and the decline of pelagic sharks in the Gulf of Mexico. Ecol Lett 7:135–145

    Article  Google Scholar 

  • Baum JK, Myers RA, Kehler DG, Worm B, Harley SJ, Doherty PA (2003) Collapse and conservation of shark populations in the northwest Atlantic. Science 299:389–392

    Article  PubMed  CAS  Google Scholar 

  • Bazin E, Glemin S, Galtier N (2006) Population size does not influence mitochondrial genetic diversity in animals. Science 312:570–572

    Google Scholar 

  • Bowen BW, Karl SA (2007) Population genetics and phylogeography of sea turtles. Mol Ecol 16:4886–4907

    Article  PubMed  CAS  Google Scholar 

  • Bowen BW, Grant WS, Hillis-Starr ZD, Bjorndal KA, Bolten AB, Bass AL (2007) Mixed stock analysis reveals the migrations of juvenile hawksbill turtles (Eretmochelys imbricata) in the Caribbean Sea. Mol Ecol 16:49–60

    Article  PubMed  CAS  Google Scholar 

  • Branstetter S, Stiles R (1987) Age and growth-estimates of the bull shark, Carcharhinus leucas, from the northern Gulf of Mexico. Environ Biol Fishes 20:169–181

    Article  Google Scholar 

  • Burgess GH, Beerkircher LR, Cailliet GM, Carlson JK, Cortes E, Goldman KJ, Grubbs RD, Musick JA, Musyl MK, Simpfendorfer CA (2005) Is the collapse of shark populations in the northwest Atlantic Ocean and Gulf of Mexico real? Fisheries 30:20–26

    Article  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Compagno LJV (1984) FAO species catalogue. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. II. Carcharhiniformes. FAO Fisheries Synopsis, Rome, Italy

  • Dallas JF (1992) Estimations of microsatellite mutation-rates in recombinant inbred strains of mouse. Mamm Genome 3:452–456

    Article  PubMed  CAS  Google Scholar 

  • Dankel DJ, Skagen DW, Ulltang Ø (2008) Fisheries management in practice: review of 13 commercially important fish stocks. Rev Fish Biol Fish 18:201–233

    Article  Google Scholar 

  • Dib C, Faure S, Fizames C, Samson D, Drouot N, Vignal A, Millasseau P, Marc S, Hazan J, Seboum E, Lathrop M, Gyapay G, Morissette J, Weissenback J (1996) A comprehensive genetic map of the human genome based on 5,264 microsatellites. Nature 380:152–154. Note: the extended reprint is available at www.genoscope.cns.fr/spip/Human-genetic-map-supplementary.html but, as of 9/15/2010, the mutation rate information is missing

    Google Scholar 

  • DiBattista JD, Feldheim KA, Thibert-Plante X, Gruber SH, Hendry AP (2008) A genetic assessment of polyandry and breeding-site fidelity in lemon sharks. Mol Ecol 17:3337–3351

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dupuy BM, Stenersen M, Egeand T, Olaisen B (2004) Y-chromosomal microsatellite mutation rates: differences in mutation rate between and within loci. Hum Mutat 23:117–124

    Article  PubMed  CAS  Google Scholar 

  • Ellegren H (2000) Microsatellite mutations in the germline: implications for evolutionary inference. TIG 16:551–558

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Feldheim KA, Gruber SH, Ashley MV (2002) Breeding biology of lemon shark at a tropical nursery lagoon. Proc R Soc B: Biol Sci 269:1655–1661

    Article  Google Scholar 

  • Feldheim KA, Gruber SH, Ashley MV (2004) Reconstruction of parental microsatellite genotypes reveals female polyandry and philopatry in the lemon shark, Negaprion brevirostris. Evolution 58:2332–2342

    PubMed  CAS  Google Scholar 

  • Felsenstein J (2006) Accuracy of coalescent likelihood estimates: do we need more sites, more sequences, or more loci. Mol Biol Evol 23:691–700

    Article  PubMed  CAS  Google Scholar 

  • Gaither MR, Toonen RJ, Robertson DR, Planes S, Bowen BW (2010) Genetic evaluation of marine biogeographical barriers: perspectives from two widespread Indo-Pacific snappers (Lutjanus kasmira and Lutjanus fulvus). J Biogeogr 37:133–147

    Article  Google Scholar 

  • Grant WS, Bowen BW (1998) Shallow population history in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:425–426

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometals 48:361–372

    CAS  Google Scholar 

  • Handley LJL, Perrin N (2007) Advances in our understanding of mammalian sex-biased dispersal. Mol Ecol 16:1559–1578

    Article  Google Scholar 

  • Heithaus MR, Burkholder D, Hueter RE, Heithaus LI, Pratt HL, Carrier JC (2007) Spatial and temporal variation in shark communities of the lower Florida Keys and evidence for historical population declines. Can J Fish Aquat Sci 64:1302–1313

    Article  Google Scholar 

  • Heupel MR, Simpfendorfer CA (2008) Movement and distribution of young bull sharks Carcharhinus leucas in a variable estuarine environment. Aquat Biol 1:277–289

    Article  Google Scholar 

  • Heupel MR, Semmens JM, Hobday AJ (2006) Automated acoustic tracking of aquatic animals: scales, designs and deployment of listening station arrays. Mar Freshw Res 57:1–13

    Article  Google Scholar 

  • Heupel MR, Carlson JK, Simpfendorfer CA (2007) Shark nursery areas: concepts, definition, characterization and assumptions. Mar Ecol Prog Ser 337:287–297

    Article  Google Scholar 

  • Heupel MR, Simpfendorfer CA, Fitzpatrick R (2010) Large-scale movement and reef fidelity of grey reef sharks. PLoS ONE 5:e9650. doi:10.1371/journal.pone.0009650

    Article  PubMed  Google Scholar 

  • Hey J (2010) Isolation with migration models for more than two populations. Mol Biol Evol 27:905–920

    Article  PubMed  CAS  Google Scholar 

  • Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved markov chain Monte Carlo methods in population genetics. Proc Natl Acad Sci 104:2785–27900

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Huang QY, Xu FH, Shen H, Deng HY, Liu YJ, Liu YZ, Li JL, Recker RR, Deng HW (2002) Mutation patters at dinucleotide microsatellite loci in humans. Am J Hum Genet 70:625–654

    Article  PubMed  CAS  Google Scholar 

  • Hueter RE, Heupel MR, Heist EJ, Keeney DB (2005) Evidence of philopatry in sharks and implications for the management of shark fisheries. J Northwest At Fish Sci 35:239–247

    Google Scholar 

  • Kashi Y, Soller M (1999) Functional roles of microsatellites and minisatellites. In: Goldstein DB, Schlotterer C (eds) Microsatellites: evolution, applications. Oxford University Press, New York, NY

    Google Scholar 

  • Keeney DB, Heist EJ (2003) Characterization of microsatellite loci isolated from the blacktip shark and their utility in requiem and hammerhead sharks. Mol Ecol Notes 3:501–504

    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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kitamura T, Takemura A, Watabe S, Taniuchi T, Shimizu M (1996) Mitochondrial DNA analysis for the cytochrome b gene and D-loop region from the bull shark Carcharhinum leucas. Fish Sci 62:21–27

    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 

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

    Article  Google Scholar 

  • Martin AP (1995) Mitochondrial DNA sequence evolution in sharks: rates, patterns and phylogenetic inferences. Mol Biol Evol 12:1114–1123

    PubMed  CAS  Google Scholar 

  • Martin RA (2005) Conservation of freshwater and euryhaline elasmobranchs: a review. J Mar Biolog Assoc U K 85:1049–1073

    Article  Google Scholar 

  • Martin AP, Naylor GJP, Palumbi SR (1992) Rates of mitochondrial DNA are slow in sharks compared to mammals. Nature 357:153–155

    Article  PubMed  CAS  Google Scholar 

  • Montoya RV, Thorson TB (1982) The bull shark (Carcharhinus leucas) and the largetooth sawfish (Pristis perotteti) in Lake Bayano, a tropical man-made impoundment in Panama. Environ Biol Fishes 7:341–347

    Article  Google Scholar 

  • Morgan A, Cooper P, Curtis T, Burgess G (2009) An overview of the United States east coast bottom longline shark-fishery, 1994–2003. Mar Fish Rev 71:23–38

    Google Scholar 

  • Müller J, Henle FGJ (1839) Systematische Beschreibung der Plagiostomen., Berlin. Veit 2:29–102

    Google Scholar 

  • Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315:1846–1850

    Article  PubMed  CAS  Google Scholar 

  • Neer JA, Thompson BA, Carlson JK (2005) Age and growth of Charcharhinus leucas in the northern Gulf of Mexico: incorporating variability in size at birth. J Fish Biol 67:370–383

    Article  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York, NY

    Google Scholar 

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

    Article  Google Scholar 

  • Nóbrega MF, Lessa RP (2007) Descrição e composição das capturas da frota pesqueira artesanal da região nordeste do Brasil. Arq Ciên Mar 40:64–74

    Google Scholar 

  • O’Connell MT, Shepherd TD, O’Connell AMU, Myers RA (2007) Long-term declines in two apex predators, bull sharks (Carcharhinus leucas) and alligator gar (Atractosteus spatula), in lake Pontchartrain, an oligohaline estuary in southeastern Louisiana. Estu Coa 30:567–574

    Google Scholar 

  • Ortega LA (2008) Movement and distribution of juvenile bull sharks, Carcharhinus leucas, in response to water quality and quantity modifications in a Florida nursery. M.Sc. Thesis, University of South Florida, Tampa, USA

  • Ortega LA, Heupel MR, van Beynen P, Motta P (2009) Movement patterns and water quality preferences of juvenile bull sharks (Carcharhinus leucas) in a Florida estuary. Environ Biol Fishes 84:361–373

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Pillans RD, Franklin CE (2004) Plasma osmolyte concentrations and rectal gland mass of bull sharks Carcharhinus leucas, captured along a salinity gradient. Comp Biochem Physiol Mol Integr Physiol 138:363–371

    Article  Google Scholar 

  • Pluzhnikov A, Donnelly P (1996) Optimal sequencing strategies for surveying molecular genetic diversities. Genetics 144:1247–1262

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283

    Google Scholar 

  • Rocha LA, Rocha CR, Robertson DR, Bowen BW (2008) Comparative phylogeography of Atlantic reef fishes indicates both origin and accumulation of diversity in the Caribbean. BMC Evol Biol 8:157–173

    Article  PubMed  Google Scholar 

  • Sadowsky V (1971) Note on bull shark, Carcharhinus leucas, in the lagoon region of Cananéia, Brazil. Bol Inst Oceano 20:71–78

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York, NY

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zoo 69:82–90

    Article  CAS  Google Scholar 

  • Simpfendorfer CA, Milward NE (1993) Utilization of a tropical bay as a nursery area by sharks of the families Carcharhinidae and Sphyrnidae. Environ Biol Fishes 37:337–345

    Article  Google Scholar 

  • Simpfendorfer CA, Freitas GG, Wiley TR, Heupel MR (2005) Distribution and habitat partitioning of immature bull sharks (Carcharhinus leucas) in a southwest Florida estuary. Estuaries 28:78–85

    Article  Google Scholar 

  • Simpfendorfer CA, Heupel MR, Collins AB (2008) Variation in the performance of acoustic receivers and its implication for positioning algorithms in a riverine setting. Can J Fish Aquat Sci 65:482–492

    Article  Google Scholar 

  • Snelson FF, Mulligan TJ, Williams SE (1984) Food habits, occurrence and population structure of the bull shark, Carcharhinus leucas, in Florida coastal lagoons. Bull Mar Sci 34:71–80

    Google Scholar 

  • Soto JMR, Nisa-Castro-Neto (1998) Revisão dos registros de tubarão-touro, Carcharhinus leucas (Valenciennes, 1839) (Chondrichthyes, Carcharhinidae), em rios e lagunas brasileiras. In: Resumos Expandidos da 11ª Semana Nacional de Oceanografia. FURG, Rio Grande, RS, Brasil, pp 314–316

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of the mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    PubMed  CAS  Google Scholar 

  • 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 19:4233–4247

    Article  Google Scholar 

  • Thomerson JE, Thorson TB, Hempel RL (1977) The bull shark, Carcharhinus leucas, from the upper Mississippi River near Alton, Illinois. Copeia 1977:166–168

    Article  Google Scholar 

  • Thorson TB (1971) Movements of bull sharks, Carcharhinus leucas, between the Caribbean Sea and Lake Nicaragua demonstrated by tagging. Copeia 1971:336–338

    Article  Google Scholar 

  • Thorson TB (1972) Status of bull shark, Carcharhinus leucas, in Amazon River. Copeia 1971:601–605

    Article  Google Scholar 

  • Thorson TB, Watson DE, Cowan CM (1966) The status of the freshwater shark of Lake Nacaragua. Copeia 1966:385–402

  • Walsh PS, Metzger DA, Higuchi R (1991) Chelex medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513

    PubMed  CAS  Google Scholar 

  • Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89:438–450

    Article  Google Scholar 

  • Weber JL, Wong C (1993) Mutation of short tandem repeats. Hum Mol Genet 2:1123–1128

    Article  PubMed  CAS  Google Scholar 

  • Wintner SP, Dudley SFJ, Kistnasamy N, Everett B (2002) Age and growth estimates for the Zambezi shark, Carcharhinus leucas, from the east coast of South Africa. Mar Fresh Res 53:557–566

    Article  Google Scholar 

  • Yeiser BG, Heupel MR, Simpfendorfer CA (2008) Occurrence, home range and movement patterns of juvenile bull (Carcharhinus leucas) and lemon (Negaprion brevirostris) sharks within a Florida estuary. Mar Fresh Res 59:489–501

    Article  Google Scholar 

  • Zhivotovsky LA, Bennett L, Bowcock AM, Feldman MW (2000) Human population expansion and microsatellite variation. Mol Biol Evol 17:757–767

    PubMed  CAS  Google Scholar 

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Acknowledgments

We thank the major contributors to this study including the organizations and people that assisted collecting tissue samples: CSFOP observer coordinator A. Morgan and all the hardworking CSFOP fishery observers. We also thank those individuals who provided laboratory and data analysis assistance: A. Bass, C. Curtis, K. Gorospe, C. Puchulutegui, C. Rocha, and L. Rocha. Part of this work was carried out by using the resources of the Computational Biology Service Unit from Cornell University, which is partially funded by Microsoft Corporation. Two anonymous reviewers provided helpful suggestions that improved the manuscript. Much of the laboratory research was conducted in the Department of Biology, University of South Florida (Tampa, FL) in partial fulfillment of doctoral research of ALFC who was supported, in part, by CAPES Fellowship BEX 1277-02-2. Funding for this project also was provided by NSF grants DEB 98-06905 and DEB 03-21924 to SAK and National Marine Fisheries Service funding of the National Shark Research Consortium. This is SOEST contribution No. 8014 and HIMB contribution No. 1404.

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Karl, S.A., Castro, A.L.F., Lopez, J.A. et al. Phylogeography and conservation of the bull shark (Carcharhinus leucas) inferred from mitochondrial and microsatellite DNA. Conserv Genet 12, 371–382 (2011). https://doi.org/10.1007/s10592-010-0145-1

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