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Genetic population structure of the Pacific bluefin tuna Thunnus orientalis and the yellowfin tuna Thunnus albacares in the North Pacific Ocean

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Abstract

The genetic population structure of the Pacific bluefin tuna (PBF) Thunnus orientalis and the yellowfin tuna (YFT) T. albacares in the North Pacific Ocean was investigated. The polymorphism of microsatellite (SSR) loci and sequences of mitochondrial DNA control region (mtCR) were analyzed for 71 samples of PBF from Japan and Mexico and 45 samples of YFT from Japan and Panama. In the SSR analyses, both single-locus (−0.010 to 0.008 in PBF and −0.023 to 0.020 in YFT) and global multilocus (0.003 in PBF and −0.002 in YFT) F ST values among the geographic populations were low and not significant in these species. In the mtCR analyses, neither the neighbor-joining tree nor the minimum spanning network showed genetic differentiation among the geographic populations in each species. The pairwise F ST values among the geographic populations of them (−0.005 in PBF and −0.020 to −0.014 in YFT) were low and not significant. Our SSR and mtCR data suggested that genetic differentiations were not evident among the eastern and western populations in the North Pacific Ocean either in PBF or in YFT. Mismatch distributions, demographic parameters, and neutrality tests suggested that sudden population expansion of PBF and YFT in the North Pacific Ocean occurred 628,000–731,000 and 450,000–525,000 years ago, respectively.

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References

  1. Collette BB, Smith BR (1981) Bluefin tuna, Thunnus thynnus orientalis, from the Gulf of Papua. Japan J Ichthyol 28:166–168

    Google Scholar 

  2. Honda N (2012) The situation connecting tuna (in Japanese). National Diet Library-Issue Brief-Number 738:1–12

    Google Scholar 

  3. Fisheries Research Agency (2013a) Pacific bluefin tuna in the Pacific Ocean (in Japanese). Present condition of international fisheries stock in 2013.:1–8

  4. ISC Pacific bluefin tuna Working Group (2013) Scientific committee ninth regular session. Stock Assessment of Pacific Bluefin Tuna in 2012. WCPFC-SC9-2013/SA-WP-10 (Rev 1): 1–67

  5. Collette BB, Nauen CE (1983) Scombrids of the world–an annotated and illustrated catalogue of tunas, mackerels, bonitos and related species known to date. FAO Fisher Syn no. 125(2), FAO, Rome

  6. International Seafood Sustainability Foundation (2012) ISSF status of the world fisheries for tuna, management of tuna stocks and fisheries. ISSF Technical Report 2012–07:1–21

    Google Scholar 

  7. Inter-American Tropical Tuna Commission (2013) Tunas and billfishes in the eastern Pacific Ocean in 2012. Fishery Status Report No. 11: 1–171

  8. Langley A, Holey S, Hampton J (2011) Scientific committee seventh regular session. Stock assessment of yellowfin tuna in the western and central Pacific Ocean. WCPFC-SC7-2011/SA-WP-03 (Rev.1-03Aug2011): 1–132

  9. Fisheries Research Agency (2013b) Yellowfin tuna in the East Pacific Ocean (in Japanese). Present condition of international fisheries stock in 2013.:1–2

  10. Sawada Y, Okada T, Miyashita S, Murata O, Kumai H (2005) Completion of the Pacific bluefin tuna Thunnus orientalis (Temminck et Schlegel) life cycle. Aquac Res 36:413–421

    Article  Google Scholar 

  11. Inagake D, Yamada H, Segawa K, Okazaki M, Nitta A, Itoh T (2001) Migration of young bluefin tuna, Thunnus orientalis Temminck et Schlegel, through archival tagging experiments and its relation with oceanographic condition in the western North Pacific. Bull Nat Res Inst Far Seas Fish 38:53–81

    Google Scholar 

  12. Itoh T, Tsuji S, Nitta A (2003) Migration patterns of young Pacific bluefin tuna (Thunnus orientalis) determined with archival tags. Fish Bull 101:514–534

    Google Scholar 

  13. Schaefer KM, Fuller DW, Block BA (2007) Movements, behavior, and habitat utilization of yellowfin tuna (Thunnus albacares) in the northeastern Pacific Ocean, ascertained through archival tag data. Mar Biol 152:503–525

    Article  Google Scholar 

  14. 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 

  15. Ward RD, Elliott NG, Grewe PM, Smolenski AJ (1994) Allozyme and mitochondrial DNA variation in yellowfin tuna (Thunnus albacares) from the Pacific Ocean. Mar Biol 118:531–539

    Article  CAS  Google Scholar 

  16. 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 95:566–575

    Google Scholar 

  17. Scoles DR, Graves JE (1993) Genetic analysis of the population structure of yellowfin tuna, Thunnus albacares, from the Pacific Ocean. Fish Bull 91:690–698

    Google Scholar 

  18. Appleyard SA, Grewe PM, Innes BH, Ward RD (2001) Population structure of yellowfin tuna (Thunnus albacares) in the western Pacific Ocean, inferred from microsatellite loci. Mar Biol 139:383–393

    Article  CAS  Google Scholar 

  19. Díaz-Jaimes P, Uribe-Alcocer M (2006) Spatial differentiation in the eastern Pacific yellowfin tuna revealed by microsatellite variation. Fish Sci 72:590–596

    Article  Google Scholar 

  20. 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

    CAS  Google Scholar 

  21. 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

    Article  CAS  Google Scholar 

  22. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  24. 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 

  25. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  26. Weir BS, Cockerham CC (1984) Estimating F-Statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  27. Alvarado Bremer JR, Stequert B, Robertson NW, Ely B (1998) Genetic evidence for inter-oceanic subdivision of bigeye tuna (Thunnus obesus) populations. Mar Biol 132:547–557

    Article  Google Scholar 

  28. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X ver. 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  29. Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York

    Google Scholar 

  30. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  32. Felsenstein J (1997) PHYLIP (Phylogeny Inference Package), ver. 3.65. University of Washington, Seattle, WA

  33. Felsenstein J (1985) Confidence limits on phylogenies: an approach using bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  34. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  PubMed  Google Scholar 

  35. Rogers AR (1995) Genetic evidence for a Pleistocene population explosion. Evolution 49:608–615

    Article  Google Scholar 

  36. Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600

    CAS  PubMed  Google Scholar 

  37. Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089

    CAS  PubMed Central  PubMed  Google Scholar 

  38. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  PubMed  Google Scholar 

  39. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed Central  PubMed  Google Scholar 

  40. Tajima F (1989) The effect of change in population size on DNA polymorphism. Genetics 123:597–601

    CAS  PubMed Central  PubMed  Google Scholar 

  41. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed Central  PubMed  Google Scholar 

  42. 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

    Article  CAS  PubMed  Google Scholar 

  43. Alvarado Bremer JR, Viñas 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

    Article  CAS  PubMed  Google Scholar 

  44. Ely B, Viñas J, Alvarado Bremer JR, 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

    Article  PubMed Central  PubMed  Google Scholar 

  45. Wu GC-C, Chiang H-C, Chou Y-W, Wong Z-R, Hsu C–C, Chen C-Y, Yang H-Y (2010) Phylogeography of yellowfin tuna (Thunnus albacares) in the Western Pacific and the Western Indian Oceans inferred from mitochondria DNA. Fish Res 105:248–253

    Article  Google Scholar 

  46. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100

    Article  CAS  PubMed  Google Scholar 

  47. Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562

    CAS  PubMed Central  PubMed  Google Scholar 

  48. Maslin, M. A. and A. J. Ridgwell (2005) Mid-Pleistocene revolution and the ‘eccentricity myth’. In: Head MJ, Gibbard PL (eds) Early-Middle Pleistocene Transitions: The Land-Ocean Evidence. Geological Society, London, Special Publication, 247, pp 19–34

  49. Huybers P (2006) Early Pleistocene glacial cycles and the integrated summer isolation forcing. Science 313:508–511

    Article  CAS  PubMed  Google Scholar 

  50. Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conservation Biol 10:1500–1508

    Article  Google Scholar 

  51. International Commission for the conservation of Atlantic tunas (2012) Report of the standing committee on research and statistics (SCRS). PLE-104/2012: 1–300

  52. Fisheries Research Agency (2011) Yellowfin tuna in the western and central Pacific Ocean (in Japanese). Present condition of international fisheries stock in 2011:1–2

    Google Scholar 

  53. Schaefer KM (1998) Reproductive biology of yellowfin tuna (Thunnus albacares) in the eastern Pacific Ocean. Inter-Am Trop Tuna Comm, Bull 21:201–272

    Google Scholar 

  54. Margulies D, Suter JM, Hunt SL, Olson RJ, Scholey VP, Wexler JB, Nakazawa A (2007) Spawning and early development of captive yellowfin tuna (Thunnus albacares). Fish Bull 105:249–265

    Google Scholar 

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Acknowledgments

We thank Mr. Ryuichi Kojima at the Tsukiji Market, Tokyo, Japan, Mr. Seiji Sakamoto at the Osaka Municipal Wholesale Market Honjo, Osaka, Japan, Mr. Asanari Gima in Nanjo-city, Okinawa Pref., Japan, Mr. Yousuke Matsumoto and Dr. Rui Matsumoto at Okinawa Churaumi Aquarium, Japan, and Ms. Susana Cusatti at IATTC, USA for their help in collecting the samples of the Pacific bluefin tuna and the yellowfin tuna. This research was supported in part by a Grant-in-Aid for the SATREPS program in Japan.

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Authors and Affiliations

  1. Laboratory for Aquatic Biology, Graduate School of Agriculture, Kinki University, Nakamachi, Nara, 631-8505, Japan

    Shohei Nomura, Toru Kobayashi & Naoki Yagishita

  2. Fisheries Laboratories, Kinki University, Kushimoto, Wakayama, 649-3633, Japan

    Yasuo Agawa & Yoshifumi Sawada

  3. Inter-American Tropical Tuna Comission, La Jolla, CA, 92037-1508, USA

    Daniel Margulies & Vernon Scholey

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  1. Shohei Nomura
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  2. Toru Kobayashi
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  3. Yasuo Agawa
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  6. Yoshifumi Sawada
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  7. Naoki Yagishita
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Correspondence to Naoki Yagishita.

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Nomura, S., Kobayashi, T., Agawa, Y. et al. Genetic population structure of the Pacific bluefin tuna Thunnus orientalis and the yellowfin tuna Thunnus albacares in the North Pacific Ocean. Fish Sci 80, 1193–1204 (2014). https://doi.org/10.1007/s12562-014-0789-8

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  • DOI: https://doi.org/10.1007/s12562-014-0789-8

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