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Population genetics of the nurse shark (Ginglymostoma cirratum) in the western Atlantic

Abstract

The nurse shark, Ginglymostoma cirratum, inhabits shallow, tropical, and subtropical waters in the Atlantic and the eastern Pacific. Unlike many other species of sharks, nurse sharks are remarkably sedentary. We assayed the mitochondrial control region and eight microsatellite loci from individuals collected primarily in the western Atlantic to estimate the degree of population subdivision. Two individuals from the eastern Atlantic and one from the Pacific coast of Panama also were genotyped. Overall, the mtDNA haplotype (h = 48 ± 5%) and nucleotide (π = 0.08 ± 0.06%) diversities were low. The microsatellite data mirror the mitochondrial results with the average number of alleles (\( \bar{N}_{A} \) = 9) and observed heterozygosity (\( \bar{H}_{O} \) = 0.58) both low. The low levels of diversity seen in both the mtDNA and the microsatellite may be due to historical sea level fluctuations and concomitant loss of shallow water habitat. Eight of the 10 pair-wise western Atlantic F ST estimates for mtDNA indicated significant genetic subdivision. Pair-wise F ST values for the microsatellite loci indicated a similar pattern as the mtDNA. The western Atlantic population of nurse sharks is genetically subdivided with the strongest separation seen between the offshore islands and mainland Brazil, likely due to deep water acting as a barrier to dispersal. The eastern and western Atlantic populations were closely related. The eastern Pacific individual is quite different from Atlantic individuals and may be a cryptic, sister species.

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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 

  • Briggs JC (1995) Marine zoogeography. McGraw-Hill, New York

    Google Scholar 

  • Castro JI (2000) The biology of the nurse shark, Ginglymostoma cirratum, off the Florida east coast and the Bahamas Islands. Environ Biol Fish 58:1–22

    Article  Google Scholar 

  • Castro ALF, Rosa RS (2005) Use of natural marks on population estimates of the nurse shark, Ginglymostoma cirratum, at Atol das Rocas Biological Reserve, Brazil. Environ Biol Fish 72:213–221

    Article  Google Scholar 

  • Castro JI, Naylor GJP, Marquez-Farias JF (2003) A new species of nurse shark from the Pacific Ocean. Proceeding of the annual meeting of the American elasmobranch society, Manaus, Brazil (abstract)

  • 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 

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

    Article  CAS  Google Scholar 

  • Coates AG, Jackson JBC, Collins LS, Cronin TM, Dowsett HJ, Bybell LM, Jung P, Obando JA (1992) Closure of the Isthmus of Panama: the near-shore marine record of Costa Rica and western Panama. Geo Soc Am Bull 104:814–828

    Article  Google Scholar 

  • Coates AG, Collins LS, Aubry MP, Berggren WA (2004) The geology of the Darien, Panama, and the late Miocene-Pliocene collision of the Panama arc with northwestern South America. Bull Geo Soc Am 116:11–12

    Google Scholar 

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

    Article  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  Google Scholar 

  • Corrigan S, Beheregaray LB (2009) A recent shark radiation: molecular phylogeny, biogeography and speciation of wobbegong sharks (family: Orectolobidae). Mol Phyl Evol 52:205–216

    Article  CAS  Google Scholar 

  • diRienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple sequence repeat loci in human populations. Proc Nat Acad Sci USA 91:3166–3170

    Article  CAS  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  CAS  Google Scholar 

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

    Article  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

    CAS  Google Scholar 

  • 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 10:295–303

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hasegawa M, Kishino H, Yano T (1985) Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  CAS  Google Scholar 

  • Hazin FHV, Wanderley JAM, Mattos SMC (2000) Distribuição e abundância relativa de tubarões no litoral do Estado de Pernambuco, Brasil. Arqui Ciênc Mar 33:33–42

    Google Scholar 

  • Hebert PDN, Cywinska A, Ball S, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lon Ser B Biol Sci 270:313–322

    Article  CAS  Google Scholar 

  • Heist EJ, Jenkot JL, Keeney DB, Lane RL, Moyer GR, Reading BJ, Smith NL (2003) Isolation and characterization of polymorphic microsatellite loci in nurse shark (Ginglymostoma cirratum). Mol Ecol Notes 3:59–61

    Article  CAS  Google Scholar 

  • Heithaus MR, Burkholder D, Hueter RE, Heithaus LI, Pratt HL Jr, 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, Carlson JK, Simfendorfer CA (2007) Shark nursery areas: concepts, definition, characterization and assumptions. Mar Ecol Prog Ser 337:287–297

    Article  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 Atl Fish Sci 35:239–247

    Google Scholar 

  • IUCN (2003) Guidelines for application of IUCN red list criteria at regional levels, version 3.0. IUCN species survival commission. IUCN. Gland, Switzerland

    Google Scholar 

  • Karl SA, Castro ALF, Lopez JA, Chavert 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 

  • Kato S, Carvallo AH (1967) Shark tagging in the eastern Pacific Ocean, 1962–65. In: Gilbert PW, Mathewson RF, Rall DP (eds) Sharks, skates, and rays. Johns Hopkins Press, Baltimore, pp 93–109

    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  CAS  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  Google Scholar 

  • Kocher TD, Thomas WK, Meyer A, Edward SV, Pääbo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:6196–6200

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Lee W, Conroy J, Howell WH, Kocher TD (1995) Structure and evolution of teleost mitochondrial control regions. J Mol Evol 41:54–66

    Article  CAS  Google Scholar 

  • Luikart G, Cornuet J (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Con Biol 12:228–237

    Article  Google Scholar 

  • Meyer CG, Clark TB, Papastamatiou YP, Whitney NM, Holland KN (2009) Long-term movements of the tiger shark (Galeocerdo cuvier) in Hawaii. Mar Ecol Prog Ser 381:223–235

    Article  Google Scholar 

  • Musick JA, Harbin MN, Compagno LJV (2004) Historical zoogeography of the Selachii. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 33–78

    Chapter  Google Scholar 

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

    Google Scholar 

  • Page RDM, Lydeard CL (1994) Towards a cladistic biogeography of the Caribbean. Cladistics 10:21–41

    Article  Google Scholar 

  • Pardini AT, Jones CS, Noble LR, Kreiser B, 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  CAS  Google Scholar 

  • Pillans R (2003) Negaprion acutidens. In: IUCN 2009. IUCN Red List of Threatened Species. Version 2009.2. http://www.iucnredlist.org. Downloaded on 1 June 2011

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

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) Model test: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  Google Scholar 

  • Pratt HL, Carrier JC (2001) A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum. Environ Biol Fish 60:157–188

    Article  Google Scholar 

  • Ratnasingham SR, Hebert PDN (2007) BOLD: the barcode of life data system (www.barcodinglife.org). Mol Ecol Notes 7:355–364

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

    Article  Google Scholar 

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

  • Swofford DL (2000) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  Google Scholar 

  • Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philos Trans R Soc B: Biol Sci 360:1847–1857

    Article  CAS  Google Scholar 

  • Ward RD, Holmes BH, White WT, Last PR (2008) DNA barcoding Australasian chondrichthyans: results and potential uses in conservation. Mar Fresh Res 59:57–71

    Article  CAS  Google Scholar 

  • Whitney N, Robbins W, Schultz J, Bowen BW, Holland K Oceanic dispersal in a sedentary reef shark (Triaenodon obesus): genetic evidence for extensive connectivity without a pelagic larval stage. J Biogeogr (accepted pending revision)

  • Wilcoxon F (1945) Individual comparisons by ranking methods. Biometr Bull 1:80–83

    Article  Google Scholar 

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Acknowledgments

We thank D. Chapman, K. Feldheim, S. Gruber, E. Heist, L Rocha, R. Rosa, M. Shivji for providing samples and A. Bass, B. Bowen, C. Curtis, K. Gorospe, C. Puchulutegui, C. Rocha, L. Rocha, R. Toonen, and J. Zamzow for general assistance and helpful comments on the manuscript. Nurse shark samples from Atol das Rocas Marine Reserve and Fernando de Noronha National Park were collected during the 1999–2001 international cooperative program between the University of Miami and Universidade Federal da Paraíba for the study of the natural history of the lemon shark in the Atol das Rocas Marine Reserve and Fernando de Noronha National Park and Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq. This study partially fulfilled the requirements for ALFC’s Ph.D. dissertation at University of South Florida and was supported, in part, by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior Fellowship BEX 1277-02-2 to ALFC. Funding for this project also was provided by National Science Foundation grants DEB 03-21924 and OCE 06-27299 to SAK. This is the University of Hawai‘i, Mānoa, School of Ocean and Earth Science and Technology contribution No. 8503 and the Hawai‘i Institute of Marine Biology contribution No. 1470.

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Correspondence to Stephen A. Karl.

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Communicated by M. I. Taylor.

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Karl, S.A., Castro, A.L.F. & Garla, R.C. Population genetics of the nurse shark (Ginglymostoma cirratum) in the western Atlantic. Mar Biol 159, 489–498 (2012). https://doi.org/10.1007/s00227-011-1828-y

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Keywords

  • Mitochondrial Control Region
  • Shark Species
  • Whale Shark
  • Lemon Shark
  • Nurse Shark