Facts and uncertainties about the genetic population structure of Atlantic bluefin tuna (Thunnus thynnus) in the Mediterranean. Implications for fishery management

Reviews in Fish Biology and Fisheries

Volumn 21, Issue 3, 2011, Pages 527-541

  Viñas, Jordi ^a   Gordoa, Ana ^b   Fernández Cebrián, Raquel ^a   Pla, Carles ^a   Vahdet, Ünal ^c   Araguas, Rosa M ^a  

^a UNIVERSITY OF GIRONA   (Spain)

^b CENTRE D ESTUDIS AVANÇATS DE BLANES CEAB CSIC   (Spain)

^c EGE UNIVERSITY   (Turkey)

Author keywords

Atlantic bluefin tuna; Fishery management; Genetic population structure; Mediterranean Sea; Thunnus thynnus

Indexed keywords

FISHERY MANAGEMENT; GENETIC DIFFERENTIATION; GENETIC STRUCTURE; MITOCHONDRIAL DNA; PERCIFORM; POPULATION STRUCTURE;

ATLANTIC OCEAN; ATLANTIC OCEAN (EAST); ATLANTIC OCEAN (WEST); MEDITERRANEAN SEA;

SCOMBRIDAE; THUNNUS THYNNUS;

EID: 79961025855     PISSN: 09603166     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11160-010-9174-6     Document Type: Article

References (97)

1. Allendorf FW, Phelps SR (1981) Use of allelic frequencies to describe population-structure. Can J Fish Aquat Sci 38: 1507-1514.
2. Alvarado Bremer J, Mejuto J, Gómez-Márquez J, Boan F, Carpintero P, Rodríguez JM, Viñas J, Greig TW, Ely B (2005a) Hierarchical analyses of genetic variation of samples from breeding and feeding grounds confirm the genetic partitioning of northwest Atlantic and south Atlantic populations of swordfish (Xiphias gladius L.). J Exp Mar Biol Ecol 327: 167-182.
3. Alvarado Bremer JR, Viñas J, Mejuto J, Ely B, Pla C (2005b) 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.
4. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge.
5. Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraespecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18: 489-522.
6. Block BA, Teo SL, Walli A, Boustany A, Stokesbury MJ, Farwell CJ, Weng KC, Dewar H, Williams TD (2005) Electronic tagging and population structure of Atlantic bluefin tuna. Nature 434: 1121-1127.
7. Boustany AM, Reeb CA, Block BA (2008) Mitochondrial DNA and electronic tracking reveal population structure of Atlantic bluefin tuna (Thunnus thynnus). Mar Biol 156: 13-24.
8. Broughton RE, Gold JR (1997) Microsatellite development and survey of variation in northern bluefin tuna (Thunnus thynnus). Mol Mar Biol Biotechnol 6: 308-314.
9. Carlsson J, McDowell JR, Díaz-Jaimes P, Carlsson JEL, Boles SB, Gold JR, Graves JE (2004) Microsatellite and mitochondrial DNA analyses of Atlantic bluefin tuna (Thunnus thynnus thynnus) population structure in the Mediterranean sea. Mol Ecol 13: 3345-3356.
10. Carlsson J, McDowell JR, Carlsson JEL, Olasdottir D (2006) Genetic heterogeneity of Atlantic bluefin tuna caught in the eastern North Atlantic Ocean south of Iceland. ICES J Mar Sci 63: 1111-1117.
11. 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.
12. Carvalho GR, Hauser L (1994) Molecular-genetics and the stock concept in fisheries. Rev Fish Biol Fish 4: 326-350.
13. Corriero A, Desantis S, Deflorio M, Acone F, Bridges CR, De Serna JM, Megalofonou P, De Metrio G (2003) Histological investigation on the ovarian cycle of the bluefin tuna in the western and central Mediterranean. J Fish Biol 63: 108-119.
14. Corriero A, Karakulak S, Santamaria N, Deflorio M, Spedicato D, Addis P, Desantis S, Cirillo F, Fenech-Farrugia A, Vassallo-Agius R, de la Serna JM, Oray Y, Cau A, Megalofonou P, De Metrio G (2005) Size and age at sexual maturity of female bluefin tuna (Thunnus thynnus L. 1758) from the Mediterranean sea. J Appl Ichthyol 21: 483-486.
15. de la Serna JM, Alot E (1992) Análisis del sex-ratio por clase de talla y otros datos sobre la madurez sexual del atún rojo (Thunnus thynnus L.) en el Atlántico este y Mediterráneo. ICAAT Coll Vol Sci Pap 52: 784-792.
16. De Metrio G, Arnold GP, de la Serna JM, Block BA, Megalofonou P, Lutcavage M, Oray IK, Deflorio M (2005) Movements of bluefin tuna (Thunnus thynnus L.) tagged in the Mediterranean sea with pop-up satellite tags. ICAAT Coll Vol Sci Pap 58: 1337-1340.
17. DeWoody JA, Avise JC (2000) Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J Fish Biol 56: 461-473.
18. Di Natale A, Mangano A, Asaro B, Bacone B, Celona A, Valastro M (2005) Bluefin tuna (Thunnus thynnus L.) catch composition in the Tyrrhenian sea and in the straits of Sicily in 2002 and 2003. ICAAT Coll Vol Sci Pap 58: 1296-1336.
19. Dicenta A (1977) Zonas de puesta del atún (Thunnus thynnus L.) y otros túnidos en el mediterráneo occidental y primer intento de evaluación del stock de reproductores de atún. Bol Instit Esp Oceano 234: 109-135.
20. Duclerc J, Piccinetti-Manfrin G, Piccinetti C, Dicenta A, Barrois JM (1974) New data on the reproduction of the red tunny and other species of thunnidae in the mediterranean. Rapport Procès-Verbaux des Réunions de la Commission International de l'Exploration Scientifique de la Mer Mediterrané 22: 7-37.
21. Edmunds PH, Sammons JI (1971) Genic polymorphism of tetrazolium oxidase in bluefin tuna, Thunnus thynnus, from western north Atlantic. J Fish Res Board Can 28: 1053-1055.
22. Edmunds PH, Sammons JI (1973) Similarity of genic polymorphism of tetrazolium oxidase in bluefin tuna (Thunnus thynnus) from Atlantic coast of France and western north Atlantic. J Fish Res Board Can 30: 1031-1032.
23. Ely B, Stoner DS, Alvarado Bremer JR, Dean JM, Addis P, Cau A, Thelen EJ, Jones WJ, Black DE, Smith L, Scott K, Naseri I, Quattro JM (2002) Analyses of nuclear ldha gene and MtDNA control region sequences of atlantic northern bluefin tuna populations. Mar Biotechnol 4: 583-588.
24. Ely B, Viñas J, Bremer JRA, Black D, Lucas L, Covello K, Labrie AV, Thelen E (2005) Consequences of the historical demography on the global population structure of two highly migratory cosmopolitan marine fishes: The yellowfin tuna (Thunnus albacares) and the skipjack tuna (Katsuwonus pelamis). BMC Evol Biol 5: 19.
25. Estoup A, Angers B (1998) Microsatellites and minisatellites for molecular ecology: theoretical and empirical considerations. In: Carvalho GR (ed) Advances in molecular ecology p. IOS Press, Amsterdam, pp 55-86.
26. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14: 2611-2620.
27. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479-491.
28. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3. 0): an integrated software package for population genetics data analysis. Evol Bioinform 1: 47-50.
29. FAO (1996) Precautionary approach to capture fisheries and species introductions, elaborated by the technical consultation on the precautionary approach to capture fisheries (including species introductions) (6 13 June 1995, lysekil, sweden). (Fisheries FTGfR, ed.). Food and Agriculture Organization of the United Nations, Rome.
30. Fromentin JM (2009) Lessons from the past: investigating historical data from bluefin tuna fisheries. Fish Fish 10: 197-216.
31. Fromentin JM, Powers JE (2005) Atlantic bluefin tuna: population dynamics, ecology, fisheries and management. Fish Fish 6: 281-306.
32. Gordoa A, Olivar MP, Arevalo R, Vinas J, Moli B, Illas X (2009) Determination of atlantic bluefin tuna (Thunnus thynnus) spawning time within a transport cage in the western Mediterranean. ICES J Mar Sci 66: 2205-2210.
33. Goudet J (1995) FSTAT (version 1. 2): a computer program to calculate F-statistics. J Hered 86: 485-486.
34. Grant WS, Garcia-Marin JL, Utter F (1999) Defining populations boundaries for fishery management. In: Mustafa S (ed) Management. Blackwell Science, Oxford, pp 27-72.
35. Graves JE (1998) Molecular insights into the population structures of cosmopolitan marine fishes. J Hered 89: 427-437.
36. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
37. Hall TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/nt. Nucl Acids Symp Ser 41: 95-98.
38. Hauser L, Carvalho GR (2008) Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish Fish 9: 333-362.
39. Hauser L, Adcock GJ, Smith PJ, Ramírez JHB, Carvalho GR (2002) Loss of microsatellite diversity and low effective population size in an overexploited population of new Zealand snapper (Pagrus auratus). Proc Natl Acad Sci USA 99: 11742-11747.
40. Heinisch G, Corriero A, Medina A, Abascal FJ, de la Serna JM, Vassallo-Agius R, Rios AB, Garcia A, de la Gandara F, Fauvel C, Bridges CR, Mylonas CC, Karakulak SF, Oray I, De Metrio G, Rosenfeld H, Gordin H (2008) Spatial-temporal pattern of bluefin tuna (Thunnus thynnus L. 1758) gonad maturation across the Mediterranean sea. Mar Biol 154: 623-630.
41. ICCAT (2008) Report of the 2008 Atlantic bluefin stock assessment session (scrs/2008/019). International Commission for the Conservation of Atlantic Tunas, Madrid, p 161.
42. Karakulak S, Oray I, Corriero A, Deflorio M, Santamaria N, Desantis S, De Metrio G (2004) Evidence of a spawning area for the bluefin tuna (Thunnus thynnus L.) in the eastern Mediterranean. J Appl Ichthyol 20: 318-320.
43. Latch EK, Dharmarajan G, Glaubitz JC, Rhodes OE (2006) Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Conserv Genet 7: 295-302.
44. Lutcavage ME, Brill RW, Skomal GB, Chase BC, Howey PW (1999) Results of pop-up satellite tagging of spawning size class fish in the gulf of Maine: do north Atlantic bluefin tuna spawn in the mid-Atlantic? Can J Fish Aquat Sci 56: 173-177.
45. MacKenzie BR, Mosegaard H, Rosenberg AA (2009) Impending collapse of bluefin tuna in the northeast Atlantic and Mediterranean. Con Let 2: 26-35.
46. Magoulas A, Tsimenides N, Zouros E (1996) Mitochondrial DNA phylogeny and the reconstruction of the population history of a species: the case of the European anchovy (Engraulis encrasicolus). Mol Biol Evol 13: 178-190.
47. 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.
48. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27: 209-220.
49. McDowell JR, Díaz-Jaimes P, Graves JE (2002) Isolation and characterization of seven tetranucleotide microsatellite loci from Atlantic northern bluefin tuna Thunnus thynnus thynnus. Mol Ecol Notes 2: 214-216.
50. Medina A, Abascal FJ, Megina C, Garcia A (2002) Stereological assessment of the reproductive status of female atlantic northern bluefin tuna during migration to Mediterranean spawning grounds through the strait of Gibraltar. J Fish Biol 60: 203-217.
51. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York.
52. Nei M, Tajima F (1981) DNA polymorphism detectable by restriction endonucleases. Genetics 97: 145-163.
53. O'Reilly PT, Canino MF, Bailey KM, Bentzen P (2004) Inverse relationship between Fst and microsatellite polymorphism in the marine fish, walleye Pollock (Theragra chalcogramma): implications for resolving weak population structure. Mol Ecol 13: 1799-1814.
54. Olsen JB, Merkouris SE, Seeb JE (2002) An examination of spatial and temporal genetic variation in walleye pollock (Theragra chalcogramma) using allozyme, mitochondrial DNA, and microsatellite data. Fish Bull 100: 752-764.
55. Oray IK, Karakulak FS (1997) Some remarks of the bluefin tuna (Thunnus thynnus) fishery in Turkish waters in 1993, 1994, 1995. ICAAT Coll Vol Sci Pap 46: 357-362.
56. Oray IK, Karakulak FS (2005) Further evidence of spawning of bluefin tuna (Thunnus thynnus L., 1758) and the tuna species (Auxis rochei Ris., 1810, Euthynnus alletteratus Raf., 1810) in the eastern Mediterranean sea: preliminary results of tunalev larval survey in 2004. J Appl Ichthyol 21: 236-240.
57. Palumbi SR (1994) Genetic-divergence, reproductive isolation, and marine speciation. Ann Rev Ecol Syst 25: 547-572.
58. Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13: S146-S158.
59. Patarnello T, Volckaert FAMJ, Castilho R (2007) Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Mol Ecol 16: 4426-4444.
60. Pearse DE, Crandall KA (2004) Beyond Fst: analysis of population genetic data for conservation. Conserv Genet 5: 585-602.
61. Posada D (2003) Using modeltest and PAUP* to select a model of nucleotide substitution. In: Baxevanis AD, Davison RD, Page RDM, Petsko GA, Stein LD, Stormo GD (eds) Current protocols in bioinformatics. Wiley, Londan, pp 6. 5. 1-6. 5. 14.
62. Posada D (2008) jModeltest: phylogenetic model averaging. Mol Biol Evol 25: 1253-1256.
63. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
64. Pujolar JM, Roldán MI, Pla C (2003) Genetic analysis of tuna populations Thunnus thynnus thynnus and T. alalunga. Mar Biol 143: 613-621.
65. Punt AE (2006) The FAO precautionary approach after almost 10 years: have we progressed towards implementing simulation-tested feedback-control management systems for fisheries management? Nat Resour Model 19: 441-464.
66. Ravier C, Fromentin JM (2001) Long-term fluctuations in the eastern Atlantic and Mediterranean bluefin tuna population. ICES J Mar Sci 58: 1299-1317.
67. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49: 1280-1283.
68. Reeb CA (2010) Genetic discontinuity of big fish in a small sea. Proc Natl Acad Sci USA 107: 2377-2378.
69. Reiss H, Hoarau G, Dickey-Collas M, Wolff WJ (2009) Genetic population structure of marine fish: mismatch between biological and fisheries management units. Fish Fish 10: 361-395.
70. Riccioni G, Landi M, Ferrara G, Milano I, Cariani A, Zane L, Sella M, Barbujani G, Tinti F (2010) Spatio-temporal population structuring and genetic diversity retention in depleted Atlantic bluefin tuna of the Mediterranean sea. Proc Natl Acad Sci USA 107: 2102-2107.
71. Rice WR (1989) Analyzing tables of statistical test. Evolution 43: 223-225.
72. Rooker JR, Bremer JRA, Block BA, Dewar H, De Metrio G, Corriero A, Kraus RT, Prince ED, Rodriguez-Marin E, Secor DH (2007) Life history and stock structure of Atlantic bluefin tuna (Thunnus thynnus). Rev Fish Sci 15: 265-310.
73. Rooker JR, Secor DH, De Metrio G, Schloesser R, Block BA, Neilson JD (2008) Natal homing and connectivity in Atlantic bluefin tuna populations. Science 322: 742-744.
74. Ryman N, Utter F (1987) Population genetics and fishery management. University of Washington Press, Seatlle.
75. Sanz N, Garcia-Marin JL, Vinas J, Roldán M, Pla C (2008) Spawning groups of European anchovy: population structure and management implications. ICES J Mar Sci 65: 1635-1644.
76. Sará R (1973) Sulla biologia dei tinni, Thunnus thynnus (L.). Bollettino di Pesca, Piscicoltura e Idrobiologia 28: 217-243.
77. Sarasquete C, Cardenas S, de Canales MLG, Pascual E (2002) Oogenesis in the bluefin tuna, Thunnus thynnus L.: a histological and histochemical study. Histol Histopathol 17: 775-788.
78. Schuelke M (2000) An economic method for the fluorescent labelling of PCR fragments. Nat Biotechnol 18: 233-234.
79. Slatkin M (1993) Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47: 264-279.
80. Susca V, Corriero A, Bridges CR, De Metrio G (2001) Study of the sexual maturity of female bluefin tuna: purification and partial characterization of vitellogenin and its use in an enzyme-linked immunosorbent assay. J Fish Biol 58: 815-831.
81. Takagi M, Okamura T, Chow S, Taniguchi N (1999) PCR primers for microsatellite loci in tuna species of genus thunnus and its application for population genetic study. Fisheries Sci 65: 571-576.
82. Teo SLH, Boustany A, Dewar H, Stokesbury MJW, Weng KC, Beemer S, Seitz AC, Farwell CJ, Prince ED, Block BA (2007) Annual migrations, diving behavior, and thermal biology of Atlantic bluefin tuna, Thunnus thynnus, on their Gulf of Mexico breeding grounds. Mar Biol 151: 1-18.
83. Thompson HC, Contin RF (1980) Electrophoretic study of Atlantic bluefin tuna (Thunnus thynnus) from the eastern and western north Atlantic ocean. Bull Mar Sci 30: 727-731.
84. van Oosterhout C, Hutchinson B, Wills D, Shipley P (2004) Micro-checker: Software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4: 535-538.
85. Viñas J, Tudela S (2009) A validated methodology for genetic identification of tuna species (genus Thunnus). PLoS ONE 4: e7606.
86. Viñas J, Alvarado Bremer J, Pla C (2004a) 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.
87. Viñas J, Alvarado Bremer JR, Pla C (2004b) Inter-oceanic genetic differentiation among albacore (Thunnus alalunga) populations. Mar Biol 145: 225-232.
88. Viñas J, Pérez-Serra A, Vidal O, Alvarado Bremer JR, Pla C (2010) Genetic differentiation between eastern and western Mediterranean swordfish revealed by phylogeographic analysis of the mitochondrial DNA control region. ICES J Mar Sci 67: 1222-1229.
89. Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89: 438-450.
90. Waples RS, Gaggiotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15: 1419-1439.
91. Waples RS, Punt AE, Cope JM (2008) Integrating genetic data into management of marine resources: how can we do it better? Fish Fish 9: 423-449.
92. Ward RD (2000) Genetics in fisheries management. Hydrobiologia 420: 191-201.
93. Ward RD, Woodwark M, Skibinski DOF (1994) A comparison of genetic diversity levels in marine, fresh-water, and anadromous fishes. J Fish Biol 44: 213-232.
94. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population-structure. Evolution 38: 1358-1370.
95. Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Jackson JBC, Lotze HK, Micheli F, Palumbi SR, Sala E, Selkoe KA, Stachowicz JJ, Watson R (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314: 787-790.
96. Wright S (1951) The genetical structure of populations. Ann Eugen 15: 323-354.
97. Zardoya R, Castilho R, Grande C, Favre-Krey L, Caetano S, Marcato S, Krey G, Patarnello T (2004) Differential population structuring of two closely related fish species, the mackerel (Scomber scombrus) and the chub mackerel (Scomber japonicus), in the Mediterranean Sea. Mol Ecol 13: 1785-1798.