Abstract
Current taxonomy indicates a single global species of the Great Barracuda (Sphyraena barracuda) despite differences in color and behavior between Atlantic and Pacific forms. To investigate these differences and qualify the dispersal characteristics of this unique coastal–pelagic teleost (bony fish), we conducted a global phylogeographic survey of 246 specimens from thirteen sampling locations using a 629-base pair fragment of mtDNA cytochrome b. Data indicate high overall gene flow in the Indo-Pacific over large distances (>16,500 km) bridging several biogeographic barriers. The West Atlantic population contains an mtDNA lineage that is divergent from the Indo-Pacific (d = 1.9%), while the East Atlantic (N = 23) has two mutations (d = 0.6%) apart from the Indo-Pacific. While we cannot rule out distinct evolutionary partitions among ocean basins based on behavior, coloration, and near-monophyly between Atlantic and Indo-Pacific subpopulations, more investigation is required before taxonomic status is revised. Overall, the pattern of high global dispersal and connectivity in S. barracuda more closely resembles those reported for large oceanic predators than reef-associated teleosts.
Similar content being viewed by others
References
Alvarado Bremer JR, Mejuto J, Greig TW, Ely B (1996) Global population structure of the swordfish (Xiphias gladius L.) as revealed by analysis of the mitochondrial DNA control region. J Exp Mar Biol Ecol 197:295–310
Alvarado Bremer JR, Vinas J, Mejuto J, Ely B, Pla C (2005) Comparative phylogeography of Atlantic bluefin tuna and swordfish: the combined effects of vicariance, secondary contact, introgression, and population expansion on the regional phylogenies of two highly migratory pelagic fishes. Mol Phylogenet Evol 36:169–187
Barber PH, Erdmann MV, Palumbi SR (2006) Comparative phylogeography of three codistributed stomatopods: origins and timing of regional diversification in the coral triangle. Evolution 60:1825–1839
Bienfang P, Oben B, DeFelice P, Moeller K, Huncik P, Oben R, Toonen R, Daly-Engel T, Bowen B (2008) Ciguatera: the detection of neurotoxins in carnivorous reef fish from the coast of Cameroon, West Africa. Afr J Mar Sci 30:533–540
Bourjea J, Lapegue S, Gagnevin L, Broderick D, Mortimer JA, Ciccione S, Roos D, Taquet C, Grizel H (2007) Phylogeography of the green turtle, Chelonia mydas, in the Southwest Indian Ocean. Mol Ecol 16:175–186
Bowen BW, Karl SA (2007) Population genetics and phylogeography of sea turtles. Mol Ecol 16:4886–4907
Bowen BW, Kamezaki N, Limpus CJ, Hughes GR, Meylan AB, Avise JC (1994) Global phylogeography of the loggerhead turtle (Caretta caretta) as indicated by mitochondrial DNA haplotypes. Evolution 48:1820–1828
Bowen BW, Bass AL, Rocha LA, Grant WS, Robertson DR (2001) Phylogeography of the trumpetfishes (Aulostomus): ring species complex on a global scale. Evolution 55:1029–1039
Bowen BW, Bass AL, Muss AJ, Carlin J, Robertson DR (2006a) Phylogeography of two Atlantic squirrelfishes (family Holocentridae): exploring pelagic larval duration and population connectivity. Mar Biol 149:899–913
Bowen BW, Muss A, Rocha LA, Grant WS (2006b) Shallow mtDNA coalescence in Atlantic pygmy angelfishes (Genus Centropyge) indicates a recent invasion from the Indian Ocean. J Hered 97:1–12
Briggs JC (1960) Fishes of worldwide (Circumtropical) distribution. Copeia 3:171–180
Briggs JC (1974a) Marine zoogeography. McGraw-Hill, New York
Briggs JC (1974b) Operation of zoogeographic barriers. Syst Zool 23:248–256
Briggs JC, Bowen BW (2012) A realignment of marine biogeographic provinces with particular reference to fish distributions. J Biogeogr 39:12–30
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
Chow S, Ushiama H (1995) Global population structure of albacore (Thunnus alalunga) inferred by RFLP analysis of the mitochondrial ATPase gene. Mar Biol 123:39–45
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660
Collette BB, McDowell JR, Graves JE (2006) Phylogeny of recent billfishes (Xiphioidei). Bull Mar Sci 79:455–468
Daly-Engel TS, Duncan KM, Holland KN, Coffey JP, Nance HA, Toonen RJ, Bowen BW (2012) Global molecular phylogeography reveals male-mediated dispersal in the endangered scalloped hammerhead shark (Sphyrna lewini). PLoS ONE 7(1):e29986
de Sylva DP (1963) Systematics and life history of the great barracuda Sphyraena barracuda Walbaum. University of Miami Press, Coral Gables
de Sylva DP (1968) Systematics and life history of the great barracuda Sphyraena barracuda (Walbaum). Toxicon 5:227
DiBattista JD, Wilcox C, Craig MT, Rocha CR, Bowen BW (2011) Phylogeography of the Pacific blueline surgeonfish Acanthurus nigroris reveals a cryptic species in the Hawaiian archipelago. J Mar Biol, Article ID 839134
Drew JA, Barber PH (2009) Sequential cladogenesis of Pomacentrus moluccensis (Bleeker, 1853) supports the peripheral origin of marine biodiversity in the Indo-Australian archipelago. Mol Phylogenet Evol 53:355–359
Duncan KM, Martin AP, Bowen BW, De Couet HG (2006) Global phylogeography of the scalloped hammerhead (Sphyrna lewini). Mol Ecol 15:2239–2251
Durand JD, Collet A, Chow S, Guinand B, Borsa P (2005) Nuclear and mitochondrial DNA markers indicate unidirectional gene flow of Indo-Pacific to Atlantic bigeye tuna (Thunnus obesus) populations, and their admixture off southern Africa. Mar Biol 147:313–322
Eble JA, Rocha LA, Craig MT, Bowen BW (2011a) Not all larvae stay close to home: insights into marine population connectivity with a focus on the brown surgeonfish (Acanthurus nigrofuscus). J Mar Biol, Article ID 518516
Eble JA, Sorenson LS, Papastamatiou YP, Basch L, Toonen RJ, Bowen BW (2011b) Escaping paradise: larval export from Hawaii in an Indo-Pacific reef fish, the yellow tang. Mar Ecol Prog Ser 426:245–258
Edwards A (1980) Fish and Fisheries of Saint Helena Island. Center for Tropical Coastal Management Studies, University of Newcastle upon Tyne, U.K.
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 Resour 10:564–567
Faunce CH, Serafy JE (2008) Selective use of mangrove shorelines by snappers, grunts, and great barracuda. Mar Ecol Prog Ser 356:153–162
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
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
Gaither MR, Bowen BW, Bordenave T-R, Rocha CR, Newman SJ, Gomez JA, Van Herwerden L, Craig MT (2011) Phylogeography of the reef fish Cephalopholus argus (Epinephelidae) indicates Pleistocene isolation across the Indo-Pacific barrier with contemporary overlap in the Coral Triangle. BMC Evol Biol 11:89
Graves JE, McDowell JR (1995) Inter-ocean genetic divergence of istiophorid billfishes. Mar Biol 122:193–203
Graves JE, McDowell JR (2003) Stock structure of the world’s istiophorid billfishes: a genetic perspective. Mar Freshw Res 54:287–298
Horne JB, Van Herwerden L, Choat JH, Robertson DR (2008) High population connectivity across the Indo-Pacific: congruent lack of phylogeographic structure in three reef fish congeners. Mol Phylogenet Evol 49:629–638
Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
Hughes GR (1974) The sea turtles of southeast Africa. I. Status, morphology, and distributions. Oceanographic Research Institute Investigational Report 35:1–144
Johns GC, Avise JC (1998) A comparative summary of genetic distances in the vertebrates from the mitochondrial cytochrome b gene. Mol Biol Evol 15:1481–1490
Jorgensen SJ, Reeb CA, Chapple TK, Anderson S, Perle C, Van Sommeran SR, Fritz-Cope C, Brown AC, Klimley AP, Block BA (2010) Philopatry and migration of Pacific white sharks. Proc R Soc B 277:679–688
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
Lessios HA (2008) The great American schism: divergence of marine organisms after the rise of the Central American isthmus. Annu Rev Ecol Evol Syst 39:63–91
Muss A, Robertson DR, Stepien CA, Wirtz P, Bowen BW (2001) Phylogeography of the genus Ophioblennius: the role of ocean currents and geography in reef fish evolution. Evolution 55:561–572
Nakamura I (1985) FAO species catalogue, vol 5. Billfishes of the world: an annotated and illustrated catalogue of marlins, sailfishes, spearfishes and swordfishes known to date FAO Fisheries Synopsis, Rome
Oremus M, Gales R, Dalebout ML, Funahashi N, Endo T, Kage T, Steel D, Baker SC (2009) Worldwide mitochondrial DNA diversity and phylogeography of pilot whales (Globicephala spp.). Biol J Linn Soc 98:729–744
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
Pauly D (1978) A preliminary compilation of fish length growth parameters. Ber Inst Meereskd Christian-Albrechts-Univ Kiel 55:1–200
Peeters FJC, Acheson R, Brummer GJA, de Ruijter WPM, Schneider RR, Ganssen GM, Ufkes E, Kroon D (2004) Vigorous exchange between the Indian and Atlantic Oceans at the end of the past five glacial periods. Nature 430:661–665
Rambaut A, Drummond AJ (2003) Tracer version 1.3. http://evolve.zoo.ox.ac.uk/
Randall JE (1967) Food habits of reef fishes of the West Indies. Stud Trop Oceanogr 5:665–847
Randall JE (1998) Zoogeography of shore fishes of the Indo-Pacific region. Zool Stud 37:227–268
Randall JE (2007) Reef and shore fishes of the Hawaiian Islands. University of Hawaii Press, Honolulu
Reeb CA, Arcangeli L, Block BA (2000) Structure and migration corridors in Pacific populations of the Swordfish Xiphius gladius, as inferred through analyses of mitochondrial DNA. Mar Biol 136:1123–1131
Reece JS, Bowen BW, Joshi K, Goz V, Larson AF (2010a) Phylogeography of two moray eels indicates high dispersal throughout the Indo-Pacific. J Hered 101:391–402
Reece JS, Bowen BW, Smith DG, Larson AF (2010b) Molecular phylogenetics of moray eels (Murenidae) demonstrates multiple origins of a shell-crushing jaw (Gymnomuraena, Echidna) and multiple colonizations of the Atlantic Ocean. Mol Phylogenet Evol 57:829–835
Robertson DR, Grove JS, Jack S, McCosker JE (2004) Tropical transpacific shore fishes. Pac Sci 58:507–565
Rocha LA, Robertson DR, Rocha CR, Van Tassel JL, Craig MT, Bowen BW (2005) Recent invasion of the tropical Atlantic by an Indo-Pacific coral reef fish. Mol Ecol 14:3921–3928
Rocha LA, Craig MT, Bowen BW (2007) Phylogeography and the conservation genetics of coral reef fishes. Coral Reefs 26:501–512
Rogers AR, Harpending H (1992) Population-growth makes waves in the distribution of pairwise genetic-differences. Mol Biol Evol 9:552–569
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Ronquist F, Huelsenbeck JP, van der Mark P (2005) MrBayes 3.1 manual. pp 1–69
Schultz JK, Feldheim KA, 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
Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90
Shannon LV (1985) The Benguela ecosystem. I. Evolution of the Benguela physical features and processes. Oceanogr Mar Biol Annu Rev 23:105–182
Song CB, Near TJ, Page JM (1998) Phylogenetic relations among Percid fishes as inferred from mitochondrial cytochrome b DNA sequence data. Mol Phylogenet Evol 10:343–353
Strathmann RR (1993) Hypotheses on the origins of marine larvae. Ann Rev Ecol Syst 24:89–117
Sunnucks P, Hales DF (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol Biol Evol 13:510–524
Swofford DL (2000) PAUP*. Phylogeny analysis using parsimony (*and Other Methods), Version 4. Sinauer Associates, Sunderland
Taberlet P, Meyer A, Bouvet J (1992) Unusually large mitochondrial variation in populations of the blue tit, Parus caeruleus. Mol Ecol 1:27–36
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tamura K, Nei M (1993) Estimation of the number of nucelotide substitutions in the control region of mitiochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
Taylor MS, Hellberg ME (2005) Marine radiations at small geographic scales: speciation in neotropical reef gobies (Elacatinus). Evolution 59:374–385
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
Van Herwerden L, Choat JH, Newman SJ, Leray M, Hillersoy G (2009) Complex patterns of population structure and recruitment of Plectropomus leopardus (Pisces: Epinephelidae) in the Indo-West Pacific: implications for fisheries management. Mar Biol 156:1595–1607
Weersing KA, Toonen RJ (2009) Population genetics, larval dispersal, and demographic connectivity in marine systems. Mar Ecol Prog Ser 393:1–12
Acknowledgments
The authors gratefully acknowledge Jeff Eble, Greg Concepcion, Marc Crepeau, Paul Marek, and Rob Toonen for laboratory support and help with genetic analyses. For help with sample collection, we thank Kim Holland, Dean Grubbs, Robert Kikuta, Paul Bienfang, Benedicta Oben, David Itano, Michelle Gaither, Mindy Mizobe, Lori O’Hara, Zoltan Szabo, Luiz Rocha, Matt Craig, Ross Newton and Tracey Rushford of Reel Teaser Charters in Western Australia, Anne Gasc of EnCoRe inc, David Rowat and the Marine Conservation Society of the Seychelles, Mike Trevor, Lenore Litherland, Monica Mwale, Ross Robertson, Ben Victor, Ross Langston, Barry Alty, Junior Sasis, Samuel Gruber, Charles Sheppard, Bill Signs, Craig Henn, Jimmy Bijoux, Tom Vely, Jon Puritz, Tristan Guttridge, Johann Mourier, John Coffey, Carl Meyer, Yannis Papastamatiou, Nick Whitney, R. Newton, Jeff Johnson, R. Charles Anderson, J. Beets, Hannelore Waska, Emily Marcus, Sean Williams, Bill Signs, the Guam Fisherman’s Cooperative Association, British Indian Ocean Territory Administration, and the Toonen, Bowen, and Holland Labs at the Hawaii Institute of Marine Biology. Funding came from the Graduate Student Organization at the University of Hawaii, National Science Foundation (OCE-0453167, OCE-0623678, and OCE-0929031 to B.W.B. and R.J. Toonen, and EPSCoR EPS-0554657 to University of Hawaii). We thank Sarah Daley, Rajesh Shrestha, and Mindy Mizobe and the HIMB EPSCoR core facility for assistance with DNA sequencing. The lead author is supported by grant No. 2 K12 GM000708 to the PERT Program at the University of Arizona from the National Institute of General Medical Sciences division of NIH. This is contribution #1454 from the Hawaii Institute of Marine Biology and contribution #8211 from the School of Ocean and Earth Science and Technology at the University of Hawaii.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. I. Taylor.
Rights and permissions
About this article
Cite this article
Daly-Engel, T.S., Randall, J.E. & Bowen, B.W. Is the Great Barracuda (Sphyraena barracuda) a reef fish or a pelagic fish? The phylogeographic perspective. Mar Biol 159, 975–985 (2012). https://doi.org/10.1007/s00227-012-1878-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-012-1878-9