Skip to main content
Log in

Mitochondrial DNA and electronic tracking reveal population structure of Atlantic bluefin tuna (Thunnus thynnus)

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

Abstract

Population subdivision was examined in Atlantic bluefin tuna (Thunnus thynnus) through sequencing of the control region of the mitochondrial genome. A total of 178 samples from the spawning grounds in the Gulf of Mexico, Bahamas and Mediterranean Sea were analyzed. Among the samples from these locations were 36 electronically tagged bluefin tuna that were tagged in the North Atlantic and subsequently traveled to one of these known spawning grounds during the spawning season. Bluefin tuna populations from the Gulf of Mexico and the Mediterranean Sea were found to be genetically distinct based on Φst, and sequence nearest neighbor analyses, showing that these two major spawning areas support independent stocks. Sequence nearest neighbor analysis indicated significant population subdivision among the Gulf of Mexico, western Mediterranean and eastern Mediterranean Sea. However, it was not possible to find significant pairwise differences between any sampling areas when using all samples. If only samples that had a high likelihood of assignment to a specific spawning site were used (young of the year, spawning adults), the differentiation increased among all sampling areas and the Western Mediterranean Sea was distinct from the Eastern Mediterranean Sea and the Gulf of Mexico. It was not possible to distinguish samples from the Bahamas from those collected at any of the other sampling sites. These data support tagging results that suggested distinctness of the Gulf of Mexico, Eastern and Western Mediterranean Sea spawning areas. This level of stock differentiation is only possible if Atlantic bluefin tuna show strong natal homing to individual spawning grounds.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alvarado-Bremer JR, Nasseri I, Ely B (1998) A provisional study of northern bluefin tuna populations. Coll Vol Sci Pap ICCAT SCRS 98(78):127–129

    Google Scholar 

  • 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. doi:https://doi.org/10.1016/j.ympev.2004.12.011

    Article  CAS  PubMed  Google Scholar 

  • Baglin RE Jr (1982) Reproductive biology of western Atlantic bluefin tuna (Thunnus thynnus). Fish Bull (Wash D C) 80:121–134

    Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

    Google Scholar 

  • Bentzen P, Taggart CT, Ruzzante DE, Cook D (1996) Microsatellite polymorphism and the population structure of Atlantic cod (Gadus morhua) in the northwest Atlantic. Can J Fish Aquat Sci 53:2706–2721. doi:https://doi.org/10.1139/cjfas-53-12-2706

    Article  Google Scholar 

  • Bermingham E, Forbes SH, Friedland K, Pla C (1991) Discrimination between Atlantic salmon (Salmo salar) of North-American and European origin using restriction analyses of mitochondrial-DNA. Can J Fish Aquat Sci 48:884–893. doi:https://doi.org/10.1139/f91-105

    Article  CAS  Google Scholar 

  • Block BA, Dewar H, Blackwell SB, Williams TD, Prince ED, Farwell CJ et al (2001) Electronic tags reveal migratory movements, depth preferences and thermal biology of Atlantic bluefin tuna. Science 293:1310–1314. doi:https://doi.org/10.1126/science.1061197

    Article  CAS  PubMed  Google Scholar 

  • Block BA, Teo SLH, Walli A, Boustany A, Stokesbury MJW, Farwell CJ et al (2005) Electronic tagging and population structure of Atlantic bluefin tuna. Nature 434:1121–1127. doi:https://doi.org/10.1038/nature03463

    Article  CAS  PubMed  Google Scholar 

  • Brodziak J, Bentley B, Bartley D, Gall GAE, Gomulkiewicz R, Mangel M (1992) Tests of genetic stock identification using coded wire tagged fish. Can J Fish Aquat Sci 49:1507–1517

    Article  Google Scholar 

  • Broughton RE, Gold JR (1997) Microsatellite development and survey of variation in northern bluefin tuna (Thunnus thynnus). Mol Mar Biol Biotechnol 6:308–314

    CAS  Google Scholar 

  • Carey FG, Teal JM (1969) Regulation of body temperature by the bluefin tuna. Comp Biochem Physiol 28A:205–213. doi:https://doi.org/10.1016/0010-406X(69)91336-X

    Article  Google Scholar 

  • Carlsson J, McDowell JR, Diaz-Jaimes P, Carlsson JEL, Boles SB, Gold JR et al (2004) Microsatellite and mitochondrial DNA analyses of Atlantic bluefin tuna (Thunnus thynnus thynnus) population structure in the Mediterranean Sea. Mol Ecol 13:3345–3356. doi:https://doi.org/10.1111/j.1365-294X.2004.02336.x

    Article  CAS  PubMed  Google Scholar 

  • Carlsson J, McDowell JR, Carlsson JEL, Graves JE (2007) Genetic identity of YOY bluefin tuna from the eastern and Western Atlantic spawning areas. J Hered 98:23–28. doi:https://doi.org/10.1093/jhered/esl046

    Article  CAS  PubMed  Google Scholar 

  • Collette BB, Reeb CA, Block BA (2001) Systematics of the tunas and mackerels (Scombridae). In: Block BA, Stevens ED (eds) Physiological ecology of tunas. Academic Press, San Diego, pp 5–33

    Google Scholar 

  • Chow S, Kishino H (1995) Phylogenetic relationships between tuna species of the genus Thunnus (Scombridae: Teleostei): inconsistent implications from morphology, nuclear and mitochondrial genomes. Natl Res Inst Far Seas Fish 41:741–748

    CAS  Google Scholar 

  • Chow S, Okamoto H, Miyabe N, Hiramatsu K, Barut N (2000) Genetic divergence between Atlantic and Indo-Pacific stocks of bigeye tuna (Thunnus obesus) and admixture around South Africa. Mol Ecol 9:221–227. doi:https://doi.org/10.1046/j.1365-294x.2000.00851.x

    Article  CAS  PubMed  Google Scholar 

  • Cort JJ, Loirzou B (1990) Reproduction-Eastern Atlantic and Mediterranean. In: Clay D (ed) World bluefin meeting, May 25–31, 1990. La Jolla, CA, pp 99–101

  • Cort JL (1991) Age and growth of the bluefin tuna Thunnus thynnus (L.) of the Northeast Atlantic. Col Vol Sci Pap ICCAT 35:213–230

    Google Scholar 

  • De Innocentiis S, Lesti A, Livi S, Rossi AR, Crosetti D, Sola L (2004) Microsatellite markers reveal population structure in gilthead sea bream Sparus auratus from the Atlantic Ocean and Mediterranean Sea. Fish Sci 70:852–859. doi:https://doi.org/10.1111/j.1444-2906.2004.00879.x

    Article  Google Scholar 

  • De Metrio G, Arnold GP, Block BA, de la Serna JM, Deflorio M, Cataldo M, Yannopoulos C, Megalofonou P, Beemer S, Farwell C, Seitz A (2002) Behaviour of post-spawning Atlantic bluefin tuna tagged with pop-up satellite tags in the Mediterranean and eastern Atlantic. Col Vol Sci Pap ICCAT 54:415–424

    Google Scholar 

  • Diaz GA, Turner SC (2007) Size frequency distribution analysis, age composition, and maturity of western bluefin tuna in the Gulf of Mexico from the U.S. (1981–2005) and Japanese (1975–1981) longline fleets. Col Vol Sci Pap ICCAT 6:1160–1170

    Google Scholar 

  • Edmonds PH, Sammons JI (1973) Similarity of genetic polymorphism of tetrazolium oxiidase in bluefin tuna (Thunnus thynnus) from the Atlantic coast of France and the western North Atlantic. J Fish Res Board Can 30:1031–1032

    Article  Google Scholar 

  • Ely B, Stoner DS, Dean JM, Alvarado-Bremer JR, Chow S, Tsuji S et al (2002) Genetic analysis of Atlantic northern bluefin tuna captured in the northwest Atlantic Ocean and the Mediterranean Sea. Col Vol Sci Pap ICCAT 54:372–376

    Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes:application of human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein J, Heppel S, Cooper A, Brault S, Lutcavage M (2007) Reproductive status and body condition of Atlantic bluefin tuna in the Gulf of Maine, 2000–2002. Mar Biol (Berl) 151:2063–2075. doi:https://doi.org/10.1007/s00227-007-0638-8

    Article  Google Scholar 

  • Gomes C, Oxenford HA, Dales RBG (1999) Mitochondrial DNA D-loop variation and implications for stock structure of the four-wing flyingfish, Hirundichthys affinis, in the central western Atlantic. Bull Mar Sci 64:485–500

    Google Scholar 

  • Graves JE (1996) Conservation genetics of fishes in the pelagic marine realm. In: Avise JC, Hamrick JL (eds) Conservation genetics: case histories from nature. Springer, Berlin, pp 335–366

    Chapter  Google Scholar 

  • Hudson RR (2000) A new statistic of detecting genetic differentiation. Genetics 155:2001–2014

    Google Scholar 

  • ICCAT (2003) Report of the 2002 Atlantic bluefin tuna stock assessment session. Col Vol Sci Pap ICCAT 55:710–937

    Google Scholar 

  • Jones WJ, Quattro JM (1999) Genetic structure of summer flounder (Paralichthys dentatus) populations north and south of Cape Hatteras. Mar Biol (Berl) 133:129–135. doi:https://doi.org/10.1007/s002270050451

    Article  CAS  Google Scholar 

  • Kimura DK, Shimada AM, Shaw FR (1998) Stock structure and movement of tagged sablefish, Anoplopoma fimbria, in offshore northeast Pacific waters and the effects of El Nino Southern Oscillation on migration and growth. Fish Bull (Wash D C) 96:462–481

    Google Scholar 

  • Kumar S, Tamura K, Nei M (1994) MEGA: molecular evolutionary genetics analysis software for microcomputers. Comput Appl Biosci 10:189–191

    CAS  PubMed  Google Scholar 

  • Laurs RM, Wetherall JA (1981) Growth-rates of North Pacific albacore, Thunnus alalunga, based on tag returns. Fish Bull (Wash D C) 79:293–302

    Google Scholar 

  • Lutcavage ME, Brill RW, Skomal GB, Chase BC, Howey PW (1999) Results of pop-up satellite tagging on spawning size class fish in the Gulf of Maine: do North Atlantic bluefin spawn in the mid-Atlantic? Can J Fish Aquat Sci 56:173–177. doi:https://doi.org/10.1139/cjfas-56-2-173

    Article  Google Scholar 

  • Magoulas A, Castilho R, Caetano S, Marcato S, Patarnello T (2006) Mitochondrial DNA reveals a mosaic pattern of phylogeographical structure in Atlantic and Mediterranean populations of anchovy (Engraulis encrasicolus). Mol Phylogenet Evol 39:734–746. doi:https://doi.org/10.1016/j.ympev.2006.01.016

    Article  CAS  PubMed  Google Scholar 

  • Mather FJ, Mason JM, Jones AC (1995) Life history and fisheries of Atlantic bluefin tuna. NOAA technical memorandum, NMFS–SFSC 370, 165 pp

  • McGowan MF, Richards WJ (1989) Bluefin tuna, Thunnus thynnus, larvae in the Gulf Stream off the southeastern USA: satellite and shipboard observations of their environment. Fish Bull (Wash D C) 87:615–632

    Google Scholar 

  • Nakadate M, Vinas J, Corriero A, Clarke S, Suzuki N, Chow S (2005) Genetic isolation between Atlantic and Mediterranean albacore populations inferred from mitochondrial and nuclear DNA markers. J Fish Biol 66:1545–1557. doi:https://doi.org/10.1111/j.0022-1112.2005.00705.x

    Article  CAS  Google Scholar 

  • National Research Council (1994) An assessment of Atlantic bluefin tuna. Natl Acad Press, Washington, 148 pp

  • Natoli A, Birkun A, Aguilar A, Lopez A, Hoelzel AR (2005) Habitat structure and the dispersal of male and female bottlenose dolphins (Tursiops truncatus). Proc R Soc B 272:1217–1226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nemerson D, Berkeley S, Safina C (2000) Spawning site fidelity in Atlantic bluefin tuna, Thunnus thynnus: the use of size-frequency analysis to test for the presence of migrant east Atlantic bluefin tuna on Gulf of Mexico spawning grounds. Fish Bull (Wash D C) 98:118–126

    Google Scholar 

  • Nishida T, Tsuji S, Segawa K (1998) Spatial data analyses of Atlantic bluefin tuna larval surveys in the 1994 ICCAT BYP. Coll Vol Sci Pap ICCAT 48:107–110

    Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinform Oxf 14:817–818. doi:https://doi.org/10.1093/bioinformatics/14.9.817

    Article  CAS  Google Scholar 

  • Pujolar JM, Pla C (2000) Genetic differentiation between north-west Atlantic and Mediterranean samples of bluefin tuna (Thunnus thynnus) using isozyme analysis. Coll Vol Sci Pap ICCAT 51:882–891

    Google Scholar 

  • Quinn JF, Hastings A (1987) Extinction in subdivided habitats. Conserv Biol 1:198–208. doi:https://doi.org/10.1111/j.1523-1739.1987.tb00033.x

    Article  Google Scholar 

  • 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 (Berl) 136:1123–1131. doi:https://doi.org/10.1007/s002270000291

    Article  Google Scholar 

  • Richards WJ (1976) Spawning of bluefin tuna in the Atlantic Ocean and adjacent seas. Coll Vol Sci Pap ICCAT 5:267–278

    Google Scholar 

  • Richards WJ (1990) Results of a review of the US bluefin tuna larval assessment with a brief response. Coll Vol Sci Pap ICCAT 32:240–247

    Google Scholar 

  • Rodriguez-Roda (1971) Investigations of tuna (Thunnus thynnus) in Spain. ICCAT Rep Biennal Period 1970–1971(Part 2), pp 110–113

  • Rozas J, Sánchez-DelBarrio JC, Messeguer-Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497. doi:https://doi.org/10.1093/bioinformatics/btg359

    Article  CAS  PubMed  Google Scholar 

  • Schaefer KM (2001) Reproductive biology of tunas. In: Block BA, Stevens ED (eds) Physiological ecology of tunas. Academic Press, San Diego, pp 225–270

    Chapter  Google Scholar 

  • Schneider S, Kueffer JM, Roessli D, Excoffier L (1997) ARLEQUIN version 1:1: a Software for Population Genetic Data Analysis Genetics and Biometry Laboratory. University of Geneva, Geneva

    Google Scholar 

  • Sharp GD (1978) Behavioral and physiological properties of tunas and their effects on vulnerability to fishing gear. In: Sharp GD, Dizon AE (eds) The physiological ecology of tunas. Academic Press, New York, pp 397–449

    Chapter  Google Scholar 

  • Simberloff DS, Abele LG (1976) Island bio-geography theory and conservation practice. Science 191:285–286. doi:https://doi.org/10.1126/science.191.4224.285

    Article  CAS  PubMed  Google Scholar 

  • Stokesbury MJW, Teo SLH, Seitz A, O’Dor RK, Block BA (2004) Movement of Atlantic bluefin tuna (Thunnus thynnus) as determined by satellite tagging experiments initiated off New England. Can J Fish Aquat Sci 61:1976–1987. doi:https://doi.org/10.1139/f04-130

    Article  Google Scholar 

  • Tajima F (1989) The effect of change in population size on DNA polymorphism. Genetics 123:597–602

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takagi M, Okamura T, Chow S, Taniguchi N (1999) PCR primers for microsatellite loci in tuna species of the genus Thunnus and its application for population genetic study. Fish Sci 65:571–576

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Teo SLH, Boustany AM, Blackwell S, Walli A, Weng KC, Block BA (2004) Validation of geolocation estimates based on light level and sea surface temperature from electronic tags. Mar Ecol Prog Ser 283:81–98. doi:https://doi.org/10.3354/meps283081

    Article  Google Scholar 

  • Teo SLH, Boustany AM, Dewar H, Stokesbury MJW, Weng KCM, Beemer S et al (2006) Annual migrations, diving behavior, and thermal biology of Atlantic bluefin tuna, Thunnus thynnus, on their Gulf of Mexico breeding grounds. Mar Biol (Berl) 151:1–18. doi:https://doi.org/10.1007/s00227-006-0447-5

    Article  Google Scholar 

  • Thompson HC, Contin RF (1980) Electrophoretic study of Atlantic bluefin tuna (Thunnus thynnus) from the eastern and western Atlantic Ocean. Bull Mar Sci 30:727–731

    CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. doi:https://doi.org/10.1093/nar/22.22.4673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Todd TN, Haas RC (1993) Genetic and tagging evidence for movement of walleyes between Lake Erie and Lake St-Clair. J Great Lakes Res 19:445–452

    Article  Google Scholar 

  • Vinas J, Alvarado-Bremer J, Pla C (2004) Phylogeography of the Atlantic bonito (Sarda sarda) in the northern Mediterranean: the combined effects of historical vicariance, population expansion, secondary invasion, and isolation by distance. Mol Phylogenet Evol 33:32–42. doi:https://doi.org/10.1016/j.ympev.2004.04.009

    Article  CAS  PubMed  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. doi:https://doi.org/10.1093/jhered/89.5.438

    Article  Google Scholar 

  • Ward RD, Elliott NG, Innes BH, Smolenski AJ, Grewe PM (1997) Global population structure of yellowfin tuna, Thunnus albacares, inferred from allozyme and mitochondrial DNA variation. Fish Bull (Wash D C) 95:566–575

    Google Scholar 

Download references

Acknowledgments

We wish to thank Gregorio De Metrio, Eric Prince, Steve Turner, Andy Seitz, Izumi Nakamura, Michael Stokesbury, Steven Teo, Shana Beemer, Steve Loga, Robert Schallert and Kevin Weng for collection of samples. We wish to thank Steve Palumbi, Kim Heiman, Heather Galindo and Michael Castleton for assistance with analysis and manuscript preparation. This study was made possible through grants from the Packard Foundation, the Monterey Bay Aquarium Foundation, the Meyers Trust and NOAA. All samples were collected and all experiments were performed in compliance with any and all laws governing them.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andre M. Boustany.

Additional information

Communicated by T. Reusch.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Boustany, A.M., Reeb, C.A. & Block, B.A. Mitochondrial DNA and electronic tracking reveal population structure of Atlantic bluefin tuna (Thunnus thynnus). Mar Biol 156, 13–24 (2008). https://doi.org/10.1007/s00227-008-1058-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-008-1058-0

Keywords

Navigation