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Genetic structure in species with shallow evolutionary lineages: a case study of the rare flatfish Verasper variegatus

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Abstract

We examined the genetic population divergence of the spotted halibut Verasper variegatus. A previous report suggested two conservation units for this species along the Japanese Pacific coast. Extending the coverage of the genomes (29 microsatellites and three mitochondrial DNA segments) revealed hitherto-undetected genetic population boundaries. We screened population samples from the major habitats along the Japanese coast and the Yellow Sea coast (East Asian Continent). Significant genetic differentiation was found in every comparison between the habitats. In most cases, the nuclear and mitochondrial population divergences were incongruent, most likely caused by differences between the two genomes in the effects of genetic drift after recent population isolation and bottleneck events. We discuss the ecological and evolutionary mechanisms of the genetic structure as well as the units of conservation. The present study illustrates the merits of wider coverage of genomes in genetic population analysis especially for species with a shallow population history.

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References

  • Anonymous (2002) Report on the technical development and promotion of stock enhancement for the spotted halibut. Japan Sea Farming Association, Tokyo (in Japanese)

    Google Scholar 

  • Aris-Brosou S, Excoffier L (1996) The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism. Mol Biol Evol 13:494–504

    CAS  PubMed  Google Scholar 

  • Aritaki M, Ohta K, Hotta Y, Tanaka M (2001) Morphological development and growth of laboratory-reared spotted halibut Verasper variegatus. Nippon Suisan Gakkaishi 67:58–66 (in Japanese with English abstract)

    Google Scholar 

  • Aritaki M, Ohta K, Hotta Y, Tagawa M, Tanaka M (2004) Temperature effects on larval development and occurrence of metamorphosis-related morphological abnormalities in hatchery-reared spotted halibut Verasper variegatus juveniles. Nippon Suisan Gakkaishi 70:8–15 (in Japanese with English abstract)

    Article  Google Scholar 

  • Ballard JWO, Kreitman M (1994) Unraveling selection in the mitochondrial genome of Drosophila. Genetics 138:757–772

    CAS  PubMed  Google Scholar 

  • Ballard LW, Adams PS, Bao Y et al (2002) Strategies for genotyping: effectiveness of tailing primers to increase accuracy in short tandem repeat determinations. J Biomol Tech 13:20–29

    PubMed  Google Scholar 

  • Bay LK, Crozier RH, Caley MJ (2006) The relationship between population genetic structure and pelagic larval duration in coral reef fishes on the Great Barrier Reef. Mar Biol 149:1247–1256

    Article  Google Scholar 

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

    Google Scholar 

  • Bernatchez L (1995) A role for molecular systematics in defining evolutionary significant units in fishes. In: Nielsen JL, Powers GA (eds) Evolution and the aquatic ecosystem: defining units in population conservation, American Fisheries Society Symposium 17. American Fisheries Society, Bethesda, Maryland, pp 114–132

    Google Scholar 

  • Bernatchez L, Wilson CC (1998) Comparative phylogeography of Nearctic and Palearctic fishes. Mol Ecol 7:431–452

    Article  Google Scholar 

  • Bowen BW, Bass AL, Muss A, Carlin J, Robertson DR (2006) Phylogeography of two Atlantic squirrelfishes (Family Holocentridae): exploring links between pelagic larval duration and population connectivity. Mar Biol 149:899–913

    Article  Google Scholar 

  • Chen D, Liu C, Dou S (1992) The biology of flatfish (Pleuronectinae) in the coastal waters of China. Neth J Sea Res 29:25–33

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295

    Article  PubMed  Google Scholar 

  • Crochet P-A (2000) Genetic structure of avian populations: allozymes revisited. Mol Ecol 9:1463–1469

    Article  CAS  PubMed  Google Scholar 

  • Crochet P-A, Chen JZ, Pons J-M et al (2003) Genetic differentiation at nuclear and mitochondrial loci among large white-headed gulls: sex-biased interspecific gene flow? Evolution 57:2865–2878

    CAS  PubMed  Google Scholar 

  • Desalle R, Templeton A, Mori I, Pletscher S, Johnston JS (1987) Temporal and spatial heterogeneity of mtDNA polymorphisms in natural populations of Drosophila mercatorum. Genetics 116:215–223

    CAS  PubMed  Google Scholar 

  • Di Rienzo A, Peterson AC, Garza JC et al (1994) Mutational processes of simple sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170

    Article  PubMed  Google Scholar 

  • Donnelly MJ, Licht MC, Lehman T (2001) Evidence for recent population expansion in the evolutionary history of the malaria vectors Anopheles arabiensis and Anopheles gambiae. Mol Biol Evol 18:1353–1364

    CAS  PubMed  Google Scholar 

  • Dowling DK, Friberg U, Lindell J (2008) Evolutionary implications of non-neutral mitochondrial genetic variation. Trends Ecol Evol 23:546–554

    Article  PubMed  Google Scholar 

  • El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839

    Article  Google Scholar 

  • Ellegren H (2000) Microsatellite mutations in the germline: implications for evolutionary inference. Trends Genet 16:551–558

    Article  CAS  PubMed  Google Scholar 

  • Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5:435–445

    Article  CAS  PubMed  Google Scholar 

  • Emery KO, Niino H, Sullivan B (1971) Post-Pleistocene levels of East China Sea. In: Turekian KK (ed) Late Cenozoic glacial ages. Yale University Press, New Haven, pp 381–390

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Ray N (2008) Surfing during population expansions promotes genetic revolutions and structuration. Trends Ecol Evol 23:347–351

    Article  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetic data analysis. Evol Bioinform Online 1:47–50

    CAS  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  Google Scholar 

  • Farris JS, Kallersjo M, Kluge AG, Bult C (1994) Testing significance of congruence. Cladistics 10:315–319

    Article  Google Scholar 

  • Ferguson MM, Danzmann RG (1998) Role of genetic markers in fisheries and aquaculture: useful tools or stamp collecting? Can J Fish Aquat Sci 55:1553–1563

    Article  Google Scholar 

  • Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Fu YX, Li WH (1993) Statistical test of neutrality of mutations. Genetics 133:693–709

    CAS  PubMed  Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  CAS  PubMed  Google Scholar 

  • Goudet J (1995) FSTAT version 1.2: a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insight from sardines and anchovies and lessons for conservation. J Hered 89:415–426

    Article  Google Scholar 

  • Hancock JM (1999) Microsatellites and other simple sequences: genomic context and mutational mechanisms. In: Goldstein DB, Schlötterer C (eds) Microsatellites—evolution and applications. Oxford University Press, New York, pp 1–9

    Google Scholar 

  • Haond-Arnaud S, Teixeira S, Massa SI et al (2006) Genetic structure at range edge: low diversity and high inbreeding in Southeast Asian mangrove (Avicennia marina) populations. Mol Ecol 15:3515–3525

    Article  CAS  Google Scholar 

  • Hauser L, Ward RD (1998) Population identification in pelagic fish: the limits of molecular markers. In: Carvalho GR (ed) Advances in molecular ecology. IOS Press, Amsterdam, pp 191–224

    Google Scholar 

  • He C, Han J, Ge L et al (2008) Sequence and organization of the complete mitochondrial genomes of spotted halibut (Verasper variegatus) and barfin flounder (Verasper moseri). DNA Seq 19:246–255

    CAS  PubMed  Google Scholar 

  • Hedgecock D (1994) Does variance in reproductive success limit effective population sizes of marine organisms? In: Beaumont AR (ed) Genetics and evolution of aquatic organisms. Chapman & Hall, New York, pp 122–134

    Google Scholar 

  • Hedrick PW (2000) Genetics of populations. Jones and Bartlett Publishers, Sudbury

    Google Scholar 

  • Ichikawa K, Fujita Y, Shimazu M (1970) The geological development of the Japanese islands. Tsukiji Shokan, Tokyo (in Japanese)

    Google Scholar 

  • Iles TD, Sinclair M (1982) Atlantic herring: stock discreteness and abundance. Science 215:627–633

    Article  CAS  PubMed  Google Scholar 

  • Isobe A (2008) Recent advances in ocean-circulation research on the Yellow Sea and East China Sea shelves. J Oceanogr 64:569–584

    Article  Google Scholar 

  • Kijima A, Fujio Y (1990) Genetic analysis of population structure in marine teleosts around Japan. In: Ogita Z, Markert CL (eds) Isozymes: structure function and use in biology and medicine. Wiley-Liss, New York, pp 177–206

    Google Scholar 

  • Kijima A, Park J (1989) Genetic differentiation and population structure within species of brown sole and marbled sole in the genus Limanda. In: Board of Genetic Assessment Project (ed) Allozyme-based genetic population analysis for fish and shellfish. Japan Fisheries Resource Conservation Association, Tokyo, pp 436–444 (in Japanese)

    Google Scholar 

  • Kimmel M, Chakraborty R, King JP et al (1998) Signatures of population expansion in microsatellite repeat data. Genetics 148:1921–1930

    CAS  PubMed  Google Scholar 

  • Kruskal JB (1964) Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29:1–27

    Article  Google Scholar 

  • Laikre L, Palm S, Ryman N (2005) Genetic population structure of fishes: implications for coastal zone management. Ambio 34:111–119

    PubMed  Google Scholar 

  • Lesica P, Allendorf FW (1995) When are peripheral populations valuable for conservation? Conserv Biol 9:753–760

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Liu J-X, Gao T-X, Yokogawa K, Zhang Y-P (2006a) Differential population structuring and demographic history of two closely related fish species, Japanese sea bass (Lateolabrax japonicus) and spotted sea bass (Lateolabrax maculatus) in Northwestern Pacific. Mol Phylogenet Evol 39:799–811

    Article  CAS  PubMed  Google Scholar 

  • Liu J-X, Gao T-X, Zhuang Z-M et al (2006b) Late Pleistocene divergence and subsequent population expansion of two closely related fish species, Japanese anchovy (Engraulis japonicus) and Australian anchovy (Engraulis australis) in Northwestern Pacific. Mol Phylogenet Evol 40:712–723

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Matsushima Y (1984) Shallow marine molluscan assemblages of postglacial period in the Japanese Islands: its historical and geographical changes induced by the environmental changes. Bull Kanagawa Prefect Mus 15:37–109 (in Japanese with English abstract)

    Google Scholar 

  • Minami T, Nakamura I (1978) Seasonal occurrence of pelagic stages of flatfishes (Pleuronectiformes) in the coastal water of western Wakasa Bay, the Japan Sea. Mem Coll Agric Kyoto Univ 112:29–47

    Google Scholar 

  • Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Biol 51:238–254

    Article  PubMed  Google Scholar 

  • Nakamura Y, Yamada A, Terui M (1997) Seeding of artificial juveniles of spotted halibut (Verasper variegatus Temminck et Schlegel) in Tokyo Bay. Bull Kanagawa Prefect Fish Res Inst 2:55–63 (in Japanese)

    Google Scholar 

  • NAPPS (2006) Statistics on production, procurement and release of seedlings for stock enhancement (in 2004). National Association for the Promotion of Productive Seas, Tokyo (in Japanese)

    Google Scholar 

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

    Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  • Nemoto Y, Fujita T, Watanabe M (1999) Studies on spotted halibut (Verasper variegatus Temminck & Schlegel)–I. Bull Fukushima Prefect Fish Exp Station 8:5–16 (in Japanese)

    Google Scholar 

  • Nielsen EE, Kenchington E (2001) A new approach to prioritizing marine fish and shellfish populations for conservation. Fish Fish 2:328–343

    Google Scholar 

  • Noichi T, Subiyanto, Hirata I (2006) Occurrence and feeding habit of the settled larval and juvenile spotted halibut Verasper variegatus at sandy beaches on the western coast of Kyushu, Japan. Nippon Suisan Gakkaishi 72:366–373 (in Japanese with English abstract)

    Article  Google Scholar 

  • Norman JR (1934) A systematic monograph of the flatfishes (Heterosomata), vol 1. Trustees of the British Museum, London

    Google Scholar 

  • Ortega-Villaizán Romo M, Nakajima M, Taniguchi N (2003) Isolation and characterization of microsatellite DNA markers in the rare species barfin flounder (Verasper moseri) and its closely related species spotted halibut (Verasper variegatus). Mol Ecol Notes 3:629–631

    Article  CAS  Google Scholar 

  • Ortega-Villaizán Romo M, Aritaki M, Suzuki S et al (2006) Genetic population evaluation of two closely related flatfish species, the rare barfin flounder and spotted halibut, along the Japanese coast. Fish Sci 72:556–567

    Article  Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  • Pimm SL, Gittleman JL, McCracken GF, Gilpin M (1989) Plausible alternatives to bottlenecks to explain reduced genetic diversity. Trends Ecol Evol 4:176–178

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Porter AH (1999) Refugees from lost habitat and reorganization of genetic population structure. Conserv Biol 13:850–859

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  Google Scholar 

  • Ramstad KM, Woody CA, Sage GK, Allendorf FW (2004) Founding events influence genetic population structure of sockeye salmon (Oncorhynchus nerka) in Lake Clark, Alaska. Mol Ecol 13:277–290

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Rohlf FJ (1998) NTSYSpc: numerical taxonomy system, version 2.0. Exeter Publishing, Setauket

    Google Scholar 

  • Rosenbaum HC, Deinard AS (1998) Caution before claim: an overview of microsatellite analysis in ecology and evolutionary biology. In: DeSalle R, Schierwater B (eds) Molecular approaches to ecology and evolution. Birkhäuser, Basel, pp 87–106

    Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386

    Google Scholar 

  • Savolainen P, Zhang Y-P, Luo J, Lundeberg J, Leitner T (2002) Genetic evidence for an East Asian origin of domestic dogs. Science 298:1610–1613

    Article  CAS  PubMed  Google Scholar 

  • Schneider S, Excoffier L (1999) Estimation of 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  Google Scholar 

  • Sekino M (2009) In search of the Kumamoto oyster Crassostrea sikamea (Amemiya, 1928) based on molecular markers: is the natural resource at stake? Fish Sci 75:819–831

    Article  CAS  Google Scholar 

  • Sekino M, Hara M (2001) Application of microsatellite markers to population genetics studies of Japanese flounder Paralichthys olivaceus. Mar Biotechnol 3:572–589

    Article  CAS  PubMed  Google Scholar 

  • Sekino M, Saitoh K, Aritaki M (2008) Microsatellite markers for a rare species of right-eye flounder Verasper variegatus (Pleuronectiformes, Pleuronectidae). Conserv Genet 9:761–765

    Article  CAS  Google Scholar 

  • Shigenobu Y, Hayashizaki K, Asahida T, Ida H, Saitoh K (2007) Stock structure of Japanese flounder inferred from morphological and genetic analyses. Fish Sci 73:1104–1112

    Article  CAS  Google Scholar 

  • Shimamura S, Yasuoka S, Mizuno T, Sasaki K, Nemoto Y (2007) The study on the spotted halibut, Verasper variegatus—II: aspects of fishery utilization and life history in coastal waters of Fukushima Prefecture. Bull Fukushima Prefect Fish Exp Station 14:69–90 (in Japanese)

    Google Scholar 

  • Sinclair M (1988) Marine populations: an essay on population regulation and speciation. University of Washington Press, Seattle

    Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (* and other methods) version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460

    CAS  PubMed  Google Scholar 

  • Tanaka M (2007) Relict estuarine ecosystem isolated from the continental coastal waters. Aquabiology 29:3–9 (in Japanese with English abstract)

    Google Scholar 

  • Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109

    Article  CAS  PubMed  Google Scholar 

  • Tsuzaki T (1995) Present status and problems of seedling production of spotted halibut, Verasper variegatus. Suisanzoshoku 43:273–276 (in Japanese)

    Google Scholar 

  • Wada T, Aritaki M, Tanaka M (2004) Effects of low-salinity on the growth and development of spotted halibut Verasper variegatus in the larva-juvenile transformation period with reference to pituitary prolactin and gill chloride cells responses. J Exp Mar Biol Ecol 308:113–126

    Article  CAS  Google Scholar 

  • Wada T, Mitsunaga N, Suzuki H, Yamashita Y, Tanaka M (2006) Growth and habitat of spotted halibut Verasper variegatus in the shallow coastal nursery area, Shimabara Peninsula in Ariake Bay, Japan. Fish Sci 72:603–611

    Article  CAS  Google Scholar 

  • Wang P (1999) Response of Western Pacific marginal seas to glacial cycles: paleoceanographic and sedimentological features. Mar Geol 156:5–39

    Article  Google Scholar 

  • Wang J, Wang P (1980) Relationship between sea-level changes and climatic fluctuations in East China since late Pleistocene. Acta Geogr Sin 35:299–312 (in Chinese with English abstract)

    Google Scholar 

  • Waples RS (1987) A multispecies approach to the analysis of gene flow in marine shore fishes. Evolution 41:385–400

    Article  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

    Article  Google Scholar 

  • Ward RD, Woodward M, Skibinski DOF (1994) A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. J Fish Biol 44:213–232

    Article  Google Scholar 

  • Weber JL (1990) Informativeness of human (dC-dA) n ·(dG-dT) n polymorphisms. Genomics 7:524–530

    Article  CAS  PubMed  Google Scholar 

  • Weber JL, Wong C (1993) Mutation of human short tandem repeats. Hum Mol Genet 2:1123–1128

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • William J, Ballard O, Kreitman M (1995) Is mitochondrial DNA a strictly neutral marker? Trends Ecol Evol 10:485–488

    Article  Google Scholar 

  • Williamson-Natesan EG (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv Genet 6:551–562

    Article  Google Scholar 

  • Xu X, Oda M (1999) Surface-water evolution of the eastern East China Sea during the last 36, 000 years. Mar Geol 156:285–304

    Article  CAS  Google Scholar 

  • Yamaguchi S, Yoneda M, Ohta K, Miyaki K, Arakawa T, Matsuyama M (2001) Reproductive biology of spotted halibut, Verasper variegatus, in Tachibana Bay, Nagasaki Prefecture. Sci Bull Fac Agric Kyushu Univ 55:179–184 (in Japanese with English abstract)

    Google Scholar 

  • Yanagi T, Aida K (1998) Nature and environment of Seto Inland Sea. Kobe Shinbun Sougou Syuppan Center, Kobe (in Japanese)

    Google Scholar 

  • Yatsu A (2008) Impacts of climate and climate change on the key species in the fisheries in the North Pacific (country report of Japan). PICES Sci Rep 35:57–84

    Google Scholar 

  • Zhang D-X, Hewitt GM (2003) Nuclear DNA analysis in genetic studies of populations: practice, problems and prospects. Mol Ecol 12:563–584

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Takeshi Onodera for his assistance in collecting fish samples from Miyagi Prefecture. Professor Qi Li and his graduate students helped MS’s expedition in China to procure the Yellow Sea sample. Many constructive comments provided by three anonymous reviewers and editors helped improve the manuscript significantly. We conducted this study in the research project ‘Research and Development Projects for Application in Promoting New Policy of Agriculture, Forestry, and Fisheries’, funded by the Ministry of Agriculture, Forestry, and Fisheries, Japan. This study is a scientific contribution from the Fisheries Research Agency of Japan (FRA-TNFRI-B125).

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Table 6 Per locus estimates of microsatellite variability

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Table 7 Polymorphic sites in CR, Cytb and ND2 segments of spotted halibut mtDNA

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Sekino, M., Saitoh, K., Shimizu, D. et al. Genetic structure in species with shallow evolutionary lineages: a case study of the rare flatfish Verasper variegatus . Conserv Genet 12, 139–159 (2011). https://doi.org/10.1007/s10592-010-0128-2

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