Conservation Genetics

, Volume 11, Issue 3, pp 999–1012 | Cite as

Fine-scale population genetic structure in Alaskan Pacific halibut (Hippoglossus stenolepis)

  • Jennifer L. Nielsen
  • Sara L. Graziano
  • Andrew C. Seitz
Research Article

Abstract

Pacific halibut collected in the Aleutian Islands, Bering Sea and Gulf of Alaska were used to test the hypothesis of genetic panmixia for this species in Alaskan marine waters. Nine microsatellite loci and sequence data from the mitochondrial (mtDNA) control region were analyzed. Eighteen unique mtDNA haplotypes were found with no evidence of geographic population structure. Using nine microsatellite loci, significant heterogeneity was detected between Aleutian Island Pacific halibut and fish from the other two regions (FST range = 0.007–0.008). Significant FST values represent the first genetic evidence of divergent groups of halibut in the central and western Aleutian Archipelago. No significant genetic differences were found between Pacific halibut in the Gulf of Alaska and the Bering Sea leading to questions about factors contributing to separation of Aleutian halibut. Previous studies have reported Aleutian oceanographic conditions at deep inter-island passes leading to ecological discontinuity and unique community structure east and west of Aleutian passes. Aleutian Pacific halibut genetic structure may result from oceanographic transport mechanisms acting as partial barriers to gene flow with fish from other Alaskan waters.

Keywords

Pacific halibut Alaska Population genetics Microsatellites mtDNA 

References

  1. Able KW, Neuman MJ, Wennhage H (2005) Ecology of juvenile and adult stages of flatfishes: distribution and dynamics of habitat associations. In: Gibson RN (ed) Flatfishes biology and exploitation. Blackwell Science, Oxford, UK, pp 164–184Google Scholar
  2. Ådlandsvik B, Gundersen AC, Nedreaas KH, Stene A, Albert OT (2004) Modeling the advection and diffusion of eggs and laevae of Greenland halibut (Reinhardtius hippoglossoides) in the north-east Arctic. Fish Oceanogr 13:403–415. doi:10.1111/j.1365-2419.2004.00303.x CrossRefGoogle Scholar
  3. Allen MJ, Smith GB (1988) Atlas and zoogeography of common fishes in the Bering Sea and northeastern Pacific. US Dept Comm NOAA Tech Rep NMFS 66Google Scholar
  4. Avise JC, Lansman RA, Shade RO (1979) The use of restriction endonucleases to measure mitochondrial DNA sequence relatedness in natural populations I. Population structure and evolution in the genus Peromyscus. Genetics 92:279–295PubMedGoogle Scholar
  5. Avise JC, Arnold J, Ball RM et al (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematic. Annu Rev Ecol Syst 18:489–522Google Scholar
  6. Bailey KM, Picquelle SJ (2002) Larval distribution of offshore spawning flatfish in the Gulf of Alaska: potential transport pathways and enhanced onshore transport during ENSO events. Mar Ecol Prog Ser 236:205–217. doi:10.3354/meps236205 CrossRefGoogle Scholar
  7. Bailey KM, Nakata H, Van der Veer H (2005) The plankton stages of flatfishes: physical and biological interactions in transport processes. In: Gibson RN (ed) Flatfishes biology and exploitation. Blackwell Science, Oxford, UK, pp 94–119Google Scholar
  8. Bailey KM, Abookire AA, Duffy-Anderson JT (2008) Ocean transport paths for the early life history stages of offshore-spawning flatfishes: a case study in the Gulf of Alaska. Fish Fish 9:44–66. doi:10.1111/j.1467-2979.2007.00268.x Google Scholar
  9. Bentzen P, Taggart CT, Ruzzante DE, Cook D (1996) Microsatellite polymorphism and population structure of Atlantic cod (Gadus morhua) in the Northwest Atlantic. Can J Fish Aquat Sci 53:2706–2721. doi:10.1139/cjfas-53-12-2706 CrossRefGoogle Scholar
  10. Bentzen P, Britt J, Kwon J (1998) Genetic variation in Pacific halibut (Hippoglossus stenolepis) detected with novel microsatellite markers. IPHC Rep Assess Res Act 229–241. Seattle, WAGoogle Scholar
  11. Bernardi G, Findley L, Rocha-Olivares A (2003) Vicariance and dispersal across Baja California in disjunct marine fish populations. Evolution 57(7):1599–1609PubMedGoogle Scholar
  12. Best EA (1981) Halibut ecology. In: Hood DW, Calder JA (eds) The Eastern Bering Sea Shelf: oceanography and resources, vol 1. US Dept Comm NOAA, Washington DC, pp 495–508Google Scholar
  13. Blaylock RB, Margolis L, Holmes JC (2003) The use of parasites in discriminating stocks of Pacific halibut (Hippoglossus stenolepis) in the northeast Pacific. Fish Bull (Wash DC) 101:1–9Google Scholar
  14. Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45. doi:10.1086/392950 CrossRefPubMedGoogle Scholar
  15. Botsford LW, Brumbaugh D, Grimes C, Kellner JB, Largier J, O’Farrell MR, Ralson S, Soulanille E, Wespestad V (2008) Connectivity, sustainability, and yield: bridging the gap between conventional fisheries management and marine protected areas. Rev Fish Fish Biol. doi 10.1007/s1160-008-9092-z
  16. Bouza C, Presa P, Castro J, Sanchez L, Martinez P (2002) Allozyme and microsatellite diversity in natural and domestic populations of turbot (Scophthalmus maximus) in comparison to other Pleuronectiformes. Can J Fish Aquat Sci 59:1460–1473. doi:10.1139/f02-114 CrossRefGoogle Scholar
  17. Brown JE, Stepien CA (2008) Ancient divisions, recent expansions: phylogeography and population structure of the round goby Apollonia melanostoma. Mol Ecol 17:2598–2615. doi:10.1111/j.1365-294X.2008.03777.x CrossRefPubMedGoogle Scholar
  18. Clark WG, Hare SR (2000) Assessment of the Pacific halibut stock in 2000. IPHC Rep Assess Res Act 85–118. Seattle, WAGoogle Scholar
  19. Clement M, Posada D, Crandall D (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657. http://darwin.uvigo.es/software/tcs.html. doi:10.1046/j.1365-294x.2000.01020.x Google Scholar
  20. Coughlan J, Stefansson M, Galvin P, Dillane E, Fitzgerald R, Cross TF (2000) Isolation and characterization of 11 microsatellite loci in Atlantic halibut (Hippoglossus hippoglossus L.). Mol Ecol 9:817–829. doi:10.1046/j.1365-294x.2000.00915-3.x CrossRefGoogle Scholar
  21. Cowen RK, Kmm Lwiza, Sponaugle S, Paris CB, Olson DB (2006) Connectivity of marine populations open or closed? Science 287:857–859. doi:10.1126/science.287.5454.857 CrossRefGoogle Scholar
  22. Cox DG, Kraft P (2006) Quantification of the power of Hardy–Weinberg equilibrium testing to detect genotyping error. Hum Hered 61:10–14. doi:10.1159/000091787 CrossRefPubMedGoogle Scholar
  23. Coyle KO (2005) Zooplankton distribution, abundance and biomass relative to water mass in eastern and central Aleutian Island passes. Fish Oceanogr 14(Suppl. 1):77–92. doi:10.1111/j.1365-2419.2005.00367.x CrossRefGoogle Scholar
  24. Coyle KO, Weingartner TJ, Hunt GL (1998) Distribution of acoustically determined biomass and major zooplankton taxa in the upper mixed layer relative to water masses in the western Aleutian Islands. Mar Ecol Prog Ser 165:95–108. doi:10.3354/meps165095 CrossRefGoogle Scholar
  25. Cunningham KM, Canino MF, Spies IB, Hauser L (2009) Genetic isolation by distance and localized fjord population structure in Pacific cod (Gadus macrocephalus): limited effective dispersal in the northeastern Pacific Ocean. Can J Fish Aquat Sci 66:153–166. doi:10.1139/F08-199 CrossRefGoogle Scholar
  26. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581. doi:10.1046/j.1365-294X.2002.01650.x CrossRefPubMedGoogle Scholar
  27. Eckert CG, Samis KE, Lougheed C (2008) Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond. Mol Ecol 17:1170–1188. doi:10.1111/j.1365-294X.2007.03659.x CrossRefPubMedGoogle Scholar
  28. Excoffier L, Laval G, Schneider S (2005) ARLEQUIN version 3.0: an integrated software package for population genetics data analysis. Evol Bioinfo Online 1:47–50Google Scholar
  29. Florin A-B, Höglund J (2007) Absence of population structure of turbot (Psetta maxima) in the Baltic Sea. Mol Ecol 16:115–126. doi:10.1111/j.1365-294X.2006.03120.x CrossRefPubMedGoogle Scholar
  30. Foss A, Imsland K, Nævdal G (1998) Population genetic studies of the Atlantic halibut in the North Atlantic Ocean. J Fish Biol 53:901–905CrossRefGoogle Scholar
  31. Fujii T, Nishida M (1997) High sequence variability in the mitochondrial DNA control region of the Japanese flounder Paralichthys olivaceus. Fish Sci 63:906–910Google Scholar
  32. Galarza JA, Carreras-Carbonell J, Macpherson E, Pascual M, Roques S, Turner GF, Rico C (2009) The influence of oceanographic fronts and early-life-history traits on connectivity among littoral fish species. Proc Natl Acad Sci USA 106:1473–1478. doi:10.1073/pnas.0806804106 CrossRefPubMedGoogle Scholar
  33. Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89(5):415–426. doi:10.1093/jhered/89.5.415 CrossRefGoogle Scholar
  34. Grant WS, Bakkala R, Utter FM, Teel DJ, Kobayashi T (1983) Biochemical genetic population structure of yellowfin sole, Limanda aspera, of the North Pacific Ocean and Bering Sea. Fish Bull (Wash DC) 81:667–677Google Scholar
  35. Grant WS, Teel DJ, Kobayashi T (1984) Biochemical population genetics of Pacific halibut (Hippoglossus stenolepis) and comparison with Atlantic halibut (H. hippoglossus). Can J Fish Aquat Sci 41:1083–1088. doi:10.1139/f84-127 CrossRefGoogle Scholar
  36. Hare SR (2004) The role of fishing in the Area 4C CPUE decline. Int Pac Halibut Comm Rep Assess Res Act 185–198Google Scholar
  37. Haug T, Fevolden SE (1986) Morphology and biochemical genetics of Atlantic halibut, Hippoglossus hippoglossus (L.) from various spawning grounds. J Fish Biol 28:367–378. doi:10.1111/j.1095-8649.1986.tb05173.x CrossRefGoogle Scholar
  38. Hauser L, Spies I, Loher T (2006) Microsatellite screening in Pacific halibut (Hippoglossus stenolepis) and a preliminary examination of population structure based on observed DNA variation. IPHC Sci Rpt No 81. Seattle, WAGoogle Scholar
  39. Hemmer-Hansen J, Nielsen EE, Grønkjær LoeschckeV (2007) Evolutionary mechanisms shaping the genetic population structure of marine fishes; lessons from the European flounder (Platichthys flesus L.). Mol Ecol 16:3104–3118. doi:10.1111/j.1365-294X.2007.03367.x CrossRefPubMedGoogle Scholar
  40. Hoarau G, Cook D, Stam WT, Olsen JL (2002a) New microsatellite primers for plaice, Pleuronectes platessa L. (Teleostei: Pleuronectidae). Mol Ecol Notes 2:60–61. doi:10.1046/j.1471-8286.2002.00149.x CrossRefGoogle Scholar
  41. Hoarau G, Rijnsdorp AD, Van Der Veer HW, Stam WT, Olsen JL (2002b) Population structure of plaice (Pleuronrctes platessa L.) in northern Europe: microsatellites revealed large-scale spatial and temporal homogeneity. Mol Ecol 11:1165–1176. doi:10.1046/j.1365-294X.2002.01515.x CrossRefPubMedGoogle Scholar
  42. Hoarau G, Piquet AM-T, Van der Veer HW, Rijnsdorp AD, Stam WT, Olsen JL (2004) Population structure of plaice (Pleuronectes platessa L.) in northern Europe: a comparison of resolving power between microsatellites and mitochondrial DNA data. J Sea Res 51:183–190. doi:10.1016/j.seares.2003.12.002 CrossRefGoogle Scholar
  43. Hunt GL Jr, Stabeno PJ (2005) Oceanography and ecology of the Aleutian Archipelago: spatial and temporal variation. Fish Oceanogr 14(Suppl. 1):292–306. doi:10.1111/j.1365-2419.2005.00378.x CrossRefGoogle Scholar
  44. IPHC (2001) Pacific halibut commercial catch tables. Available at: http://www.iphc.washington.edu/halcom/commerc/catchheader.htm
  45. IPHC (International Pacific Halibut Commission) (1998) The Pacific halibut: biology, fishery and management. Int Pac Halibut Comm Tech Rep 40. Seattle, WAGoogle Scholar
  46. Irwin DE (2002) Phylogeographic breaks without geographic barriers to gene flow. Evol Int J Org Evol 56:2383–2394Google Scholar
  47. Kaimmer S (2000) Pacific halibut tag release programs and tag release and recovery data, 1925-1998. IPHC Tech Rep 41. Seattle, WAGoogle Scholar
  48. Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Cons Gen 5:539–543. doi:10.1023/B:COGE.0000041021.91777.1a CrossRefGoogle Scholar
  49. Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189. doi:10.1111/j.1471-8286.2004.00845.x CrossRefGoogle Scholar
  50. Kandpal RJ, Kandpa G, Weissman SM (1994) Construction of libraries enriched for sequence repeats and jumping clones, and hybridization selection for region-specific markers. Proc Natl Acad Sci USA 91:88–92. doi:10.1073/pnas.91.1.88 CrossRefPubMedGoogle Scholar
  51. Knutsen H, Jorde PE, Albert OT, Hoelzel AR, Stenseth NC (2007) Population genetic structure in the North Atlantic Greenland halibut (Reinhardtius hippoglossoides): influenced by ocean current systems? Can J Fish Aquat Sci 64:857–866. doi:10.1139/F07-070 CrossRefGoogle Scholar
  52. Koutsikopoulos C, Fortier L, Gagne JA (1991) Cross-shelf dispersion of Dover sole (Solea solea) eggs and larvae in Biscay Bay and recruitment to inshore nurseries. J Plankton Res 13:923–945. doi:10.1093/plankt/13.5.923 CrossRefGoogle Scholar
  53. Ladd C, Hunt GW Jr, Mordy CW, Salo SA, Stabeno PJ (2005) Marine environment of the eastern and central Aleutian Islands. Fish Oceanogr 14(Suppl.1):22–38. doi:10.1111/j.1365-2419.2005.00373.x CrossRefGoogle Scholar
  54. Larsen PF, Nielsen EE, Williams TD, Hemmer-Hansen J, Chipman JK, Kruhøffer M, Grønkjær P, George SC, Dyrskjøt L, Loeschcke V (2007) Adaptive differences in gene expression in European flounder (Platichthys flesus). Mol Ecol 16:4674–4683. doi:10.1111/j.1365-294X.2007.03530.x CrossRefPubMedGoogle Scholar
  55. Logerwell EA, Stabeno PJ, Wilson CD, Hollowed AB (2007) The effect of oceanographic variability and interspecific competition on juvenile Pollock (Theragra chalcogamma) and capelin (Mallotus villosus) distributions on the Gulf of Alaska shelf. Deep Sea Res Part II Top Stud Oceanogr 54:2849–2868. doi:10.1016/j.dsr2.2007.08.008 CrossRefGoogle Scholar
  56. Loher T, Seitz A (2006a) Seasonal migration and environmental conditions of Pacific halibut Hippoglossus stenolepis, elucidated from pop-up archival transmitting (PAT) tags. Mar Ecol Prog Ser 317:259–271. doi:10.3354/meps317259 CrossRefGoogle Scholar
  57. Loher T, Seitz A (2006b) Assessing seasonal migration of adult Pacific halibut (Hippoglossus stenopelis) along the Aleutian Chain using Pop-up Archival Transmitting (PAT) tags. Int Pac Halibut Comm Rep Assess Res Activ 2005:293–299Google Scholar
  58. Loher T, Seitz A (2008) Characterization of active spawning season and depth for eastern Pacific halibut (Hippoglossus stenolepis) and evidence of probably skipped-spawning. J Northwest Atl Fish Sci 41:23–36. doi:10.2960/J.v41.m617 CrossRefGoogle Scholar
  59. Lundy CJ, Moran P, Rico C, Milner RS, Hewitt GM (1999) Macrogeographical population differentiation in oceanic environments: a case study of European hake (Merluccius merluccius), a commercially important fish. Mol Ecol 8:1889–1898. doi:10.1046/j.1365-294x.1999.00789.x CrossRefPubMedGoogle Scholar
  60. McLean JE, Taylor EB (2001) Resolution of population structure in a species with high gene flow: microsatellite variation in the eulachon (Osmeridae: Thaleichthys pacificus). Mar Biol (Berl) 139:411–420. doi:10.1007/s002270100483 CrossRefGoogle Scholar
  61. Mecklenburg CW, Mecklenburg TA, Thorsteinson LK (2002) Fishes of Alaska. AFS Bethesda, MDGoogle Scholar
  62. Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special interest to microsatellite loci. Genetics 142:1061–1064PubMedGoogle Scholar
  63. Mordy CW, Stabeno PJ, Ladd C, Zeeman S, Wisegarver DP, Ssalo SA, Hunt GL Jr (2005) Nutrients and primary production along the eastern Aleutian Island Archipelago. Fish Oceanogr 14(Suppl. 1):55–76. doi:10.1111/j.1365-2419.2005.00364.x CrossRefGoogle Scholar
  64. Mork J, Haug T (1983) Genetic variation in halibut Hippoglossus hippoglossus (L.) from Norwegian waters. Hereditas 98:167–174. doi:10.1111/j.1601-5223.1983.tb00591.x CrossRefPubMedGoogle Scholar
  65. Nielsen E, Bagge O, MacKenzie BR (1998) Wind induced transport of plaice (Pleuronectes platessa) early life history stages in the Skagerrak-Kattegat. J Sea Res 39:11–28. doi:10.1016/S1385-1101(97)00014-2 CrossRefGoogle Scholar
  66. Norcross BL, Shaw RF (1984) Oceanic and estuarine transport of fish eggs and larvae: a review. Trans Am Fish Soc 113:153–165. doi:10.1577/1548-8659(1984)113<153:OAETOF>2.0.CO;2 CrossRefGoogle Scholar
  67. Norcross BL, Blanchard A, Holladay BA (1999) Comparison of models for defining nearshore flatfish nursery areas in Alaskan waters. Fish Oceanogr 8:50–67. doi:10.1046/j.1365-2419.1999.00087.x CrossRefGoogle Scholar
  68. Nunney L (1999) The effective size of a hierarchically structured population. Evol Int J Org Evol 53:1–10. doi:10.2307/2640915 Google Scholar
  69. O’Connell M, Dillon MC, Wright JM, Bentzen P, Merkouris S, Seeb J (1998) Genetic structure among Alaskan Pacific herring populations identified using microsatellite variation. J Fish Biol 53:150–163. doi:10.1111/j.1095-8649.1998.tb00117.x CrossRefGoogle Scholar
  70. 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 (V. variegatus). Mol Ecol Notes 3:629–631. doi:10.1046/j.1471-8286.2003.00536.x CrossRefGoogle Scholar
  71. Ortega-Villaizán Romo M, Aritaki M, Suzuki S, Ikeda M, Asahida T, Taniguchi N (2006) Genetic population evaluation of two closely related flatfish species, the rare barfin flounder and spotted halibut, along the Japanese coast. Fish Sci 72(3):556–567. doi:10.1111/j.1444-2906.2006.01184.x CrossRefGoogle Scholar
  72. Palumbi SR (1992) Marine speciation on a small planet. Trends Ecol Evol 7:114–118. doi:10.1016/0169-5347(92)90144-Z CrossRefGoogle Scholar
  73. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572. doi:10.1146/annurev.es.25.110194.002555 CrossRefGoogle Scholar
  74. Park SDE (2001) Trypano tolerance in West African cattle and the population genetic effects of selection. Dissertation, University of Dublin, IrelandGoogle Scholar
  75. Parker KS (1989) Influence of oceanographic and meteorological processes on the recruitment of Pacific halibut, Hippoglossus stenolepis, in the Gulf of Alaska. Can Sp Pub Fish Aquat Sci 108:221–237Google Scholar
  76. Raymond M, Rousset F (1997) GENEPOP version 3.4. Laboratiore de Genetique et Environment, Montpellier, France. Available at http://wbiomed.curtin.edu.au/genepop/index.html cited 10 June 2008
  77. Reid DP, Pongsomboon S, Jackson T, McGowan C, Murphy C, Marting-Robichaud D, Reith M (2005) Microsatellite analysis indicates an absence of population structure among Hippoglossus hippoglossus in the north-west Atlantic. J Fish Biol 67:570–576. doi:10.1111/j.0022-1112.2005.00733.x CrossRefGoogle Scholar
  78. Rice WR (1989) Analyzing tables of statistical tests. Evol Int J Org Evol 43:223–225. doi:10.2307/2409177 Google Scholar
  79. Ringinos C, Nachman MW (2001) Population subdivision in marine environments: the contributions of biogeography, geographical distance and discontinuous habitat to genetic differentiation in a blennioid fish, Axoclinus nigricaudus. Mol Ecol 10:1439–1453. doi:10.1046/j.1365-294X.2001.01294.x CrossRefGoogle Scholar
  80. Rooper CN, Gunderson DR, Hickey BM (2006) An examination of the feasibility of passive transport from coastal spawning grounds to estuarine nursery areas for English sole. Estuar Coast Shelf Sci 68:609–618. doi:10.1016/j.ecss.2006.03.009 CrossRefGoogle Scholar
  81. Rozen S, Skaletsky HJ (1998) Primer3. Code available at http://www-genome.wi.mit.edu/genome_software/other/primer3.html
  82. Ruzzant DE, Mariani S, Bekkevold D, Andre C, Mosegaard H, Clausen LAW, Dahlgren TG, Hutchinson WF, Hatfield EMC, Torstensen E, Brigham J, Simmonds EJ, Laikre L, Larsson LC, Stet RJM, Ryman N, Carvalho GR (2006) Biocomplexity in a highlt migratory pelagic marine fish Atlantic herring. Proc R Soc Lond B Biol Sci 273:1459–1464. doi:10.1098/rspb.2005.3463 CrossRefGoogle Scholar
  83. Salanti G, Amountza G, Ntzani EE, Ioannidis JPA (2005) Hardy-Weinberg equilibrium in genetic association studies: an empirical evaluation of reporting, deviations, and power. Eur J Hum Genet 13:840–848. doi:10.1038/sj.ejhg.5201410 CrossRefPubMedGoogle Scholar
  84. Seitz AC (2006) Population structure and behavior of Pacific halibut. PhD Dissertation University of Alaska FairbanksGoogle Scholar
  85. Seitz A, Wilson D, Norcross BL, Nielsen JL (2003) Pop-up archival transmitting (PAT) tags: a method to investigate the migration and behavior of Pacific halibut Hippoglossus stenolepis in the Gulf of Alaska. Alsk Fish Res Bull 10(2):124–136Google Scholar
  86. Seitz AC, Norcross BL, Wilson D, Nielsen JL (2005) Identifying spawning behavior in Pacific halibut, Hippoglossus stenolepis, using electronic tags. Environ Biol Fishes 73:445–451. doi:10.1007/s10641-005-3216-2 CrossRefGoogle Scholar
  87. Seitz AC, Loher T, Nielsen JL (2007) Seasonal movements and environmental conditions experienced by Pacific halibut in the Bering Sea, examined by pop-up satellite tags. Int Pac Halibut Comm Sci Rep 84Google Scholar
  88. Sekino M, Saitoh K, Yamada T, Kumagai A, Hara M, Yamashita Y (2003) Microsatellite-based pedigree tracing in a Japanese flounder Paralichthys olivaceus hatchery strain; implications for hatchery management related to stock enhancement program. Aquaculture 221:255–263. doi:10.1016/S0044-8486(02)00667-1 CrossRefGoogle Scholar
  89. Selkoe KA, Henzler CM, Gaines SD (2008) Seascape genetics and the spatial ecology of marine populations. Fish Fish 9:363–377. doi:10.1111/j.1467-2979.2008.00300.x Google Scholar
  90. Shaw PW, Pierce GJ, Boyle PR (1999) Subtle population structure within a highly vagile marine invertebrate, the veined squid Loligo forbesi, demonstrated with microsatellite DNA markers. Mol Ecol 8:407–418. doi:10.1046/j.1365-294X.1999.00588.x CrossRefGoogle Scholar
  91. Skud BE (1977) Drift, migration, and intermingling of Pacific halibut stocks. IPHC Tech Rpt 63Google Scholar
  92. Spencer PD (2008) Density-independent and density-dependent factors affecting temporal changes in spatial distributions of eastern Bering Sea flatfish. Fish Oceanogr 17:396–410. doi:10.1111/j.1365-2419.2008.00486.x CrossRefGoogle Scholar
  93. St. Pierre G (1984) Spawning locations and season for Pacific halibut. Int Pac Halibut Comm Sci Rep 70Google Scholar
  94. St. Pierre G (1989) Recent studies of Pacific halibut postlarvae in the Gulf of Alaska and eastern Bering Sea. Int Pac Halibut Comm Sci Rpt 73Google Scholar
  95. Stabeno P, Schumacher JD, Ohtani K (1999) The physical oceanography of the Bering Sea. In: Loughlin TS, Ohtani K (eds) Dynamics of the Bering Sea. Fairbanks, University of Alaska Sea Grant, pp 1–28Google Scholar
  96. Stabeno PJ, Reed RK, Napp JM (2002) Transport through Unimak Pass, Alaska. Deep Sea Res Part II Top Stud Oceanogr 49:5919–5930. doi:10.1016/S0967-0645(02)00326-0 CrossRefGoogle Scholar
  97. Stabeno PJ, Bond NA, Hermann AJ, Kachel NB, Mordy CW, Overland JE (2004) Meteorology and oceanography of the northern Gulf of Alaska. Cont Shelf Res 24:859–897. doi:10.1016/j.csr.2004.02.007 CrossRefGoogle Scholar
  98. Stabeno PJ, Kachel DG, Kachel NB, Sullivan ME (2005) Observations from moorings in the Aleutian Passes: temperature, salinity and transport. Fish Oceanogr 14(Suppl. 1):39–54. doi:10.1111/j.1365-2419.2005.00362.x CrossRefGoogle Scholar
  99. Stepien CA (1999) Phylogeographical structure of the Dover sole Microstomus pacificus: the larval retention hypothesis and genetic divergence along the deep continental slope of the northeastern Pacific Ocean. Mol Ecol 8:923–939. doi:10.1046/j.1365-294x.1999.00643.x CrossRefPubMedGoogle Scholar
  100. Thompson WF, Van Cleve R (1936) Life history of the Pacific halibut. Rpt Inter Fish Comm No.9. pp 1–184Google Scholar
  101. Thornhill DJ, Mahon AR, Norenburg JL, Halanych KM (2008) Open-ocean barriers to dispersal: a test case with the Antarctic Polar Front and the ribbon worm Parborlasia corrugates (Nemertea:Lineidae). Mol Ecol 17:5104–5117. doi:10.1111/j.1365-294X.2008.03970.x CrossRefPubMedGoogle Scholar
  102. Tsuyuki H, Roberts E, Best EA (1969) Serum transferring systems and the hemoglobins of the Pacific halibut (Hippoglossus stenolepus). J Fish Res Bd Can 26:2351–2362Google Scholar
  103. 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. doi:10.1111/j.1471-8286.2004.00684.x CrossRefGoogle Scholar
  104. Vis ML, Carr SM, Bowering WR, Davidson WS (1997) Greenland halibut (Reinhardtius hippoglossoides) in the North Atlantic are genetically homogeneous. Can J Fish Aquat Sci 54:1813–1821. doi:10.1139/cjfas-54-8-1813 CrossRefGoogle Scholar
  105. Walpes RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Res 8:753–756. doi:10.1111/j.1755-0998.2007.02061.x CrossRefGoogle Scholar
  106. Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Cons Gene 7:167–184. doi:10.1007/s10592-005-9100-y CrossRefGoogle Scholar
  107. Waters JM, Dijkstra LH, Wallis GP (2000) Biogeography of a southern hemisphere freshwater fish: how important is marine dispersal? Mol Ecol 9:1815–1821CrossRefPubMedGoogle Scholar
  108. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evol Int J Org Evol 38(6):1358–1370. doi:10.2307/2408641 Google Scholar
  109. Werner FE, Quinlan JA, Blanton BO, Luettich RA Jr (1997) The role of hydrodynamics in explaining variability in fish populations. J Sea Res 37:195–212. doi:10.1016/S1385-1101(97)00024-5 CrossRefGoogle Scholar
  110. Wilderbuer TK, Hollowed AB, Ingraham WJ Jr, Spencer PD, Conners ME, Bond NA, Walters GE (2002) Flatfish recruitment response to decadal climate variability and ocean condition in the eastern Bering Sea. Prog Oceanogr 55:235–247. doi:10.1016/S0079-6611(02)00081-2 CrossRefGoogle Scholar
  111. Wilderbuer TW, Leaman B, Zhang CI, Fargo J, Paul L (2005) Pacific flatfish fisheries. In: Gibson RN (ed) Flatfishes biology and exploitation. Blackwell Science, Oxford, UK, pp 272–291Google Scholar
  112. Wilkins JF (2004) A separation-of-timescales approach to the coalescent in a continuous population. Genetics 168:2227–2244. doi:10.1534/genetics.103.022830 CrossRefPubMedGoogle Scholar
  113. Wilson NG, Schrodl M, Halanych KM (2009) Ocean barriers and glaciation: evidence for explosive radiation of mitochondrial lineages in the Antarctic sea slug Doris kerguelenensis (Mollusca, Nudibranchia). Mol Ecol 18:965–984. doi:10.1111/j.1365-294X.2008.04071.x CrossRefGoogle Scholar

Copyright information

© US Government 2009

Authors and Affiliations

  • Jennifer L. Nielsen
    • 1
  • Sara L. Graziano
    • 2
  • Andrew C. Seitz
    • 3
  1. 1.U.S. Geological Survey, Alaska Science CenterAnchorageUSA
  2. 2.AnchorageUSA
  3. 3.School of Fisheries and Ocean Sciences, University of Alaska FairbanksFairbanksUSA

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