Journal of Ichthyology

, Volume 59, Issue 1, pp 65–77 | Cite as

Inter- and Intra-Species Relationships of Greenland Halibut Reinhardtius hippoglossoides (Pleuronectidae) Based on the Analysis of Nuclear and Mitochondrial Genetic Markers

  • S. Yu. Orlova
  • A. A. Volkov
  • D. M. Shcepetov
  • O. A. Maznikova
  • N. V. Chernova
  • E. A. Chikurova
  • I. I. Glebov
  • A. M. OrlovEmail author


Samples of Greenland halibut Reinhardtius hippoglossoides (Jordan and Snyder, 1901) from the Atlantic, Arctic, and Pacific Oceans were compared using eight microsatellite loci and the Cyt b mtDNA gene. The data obtained revealed a population connectivity of the Greenland halibut from the Laptev Sea to those from the Atlantic Ocean that is result of considerable eastward range extension due to recent climate change. Genetic differences between the Greenland halibut groupings of the Atlantic and Pacific Oceans, according to Fst values (0.141–0.197), reach a high level. Given the genetic differences revealed by both nuclear and mitochondrial markers, the taxonomic status of the Greenland halibut inhabiting the Pacific Ocean requires reevaluation at least to the rank of subspecies. It is suggested that the Greenland halibut populations of the Atlantic Ocean basin originated from those of the North Pacific. The time and conditions of Greenland halibut penetration from the North Pacific to the Atlantic Ocean are discussed.


microsatellite markers Cyt b mtDNA connectivity differentiation isolation taxonomic status Atlantic Ocean Bering Sea 


  1. 1.
    Andryashev, A.P., Ocherk zoogegrafii i proiskhozhdeniya fauny ryb Beringova morya i sopredel’nykh vod (The Fishes of the Bering Sea and Adjacent Waters: Origin and Zoogeography), Leningrad: Leningr. Gos. Univ., 1939.Google Scholar
  2. 2.
    Andryashev, A.P. and Chernova, N.V., Annotated list of fish-like vertebrates and fish of the Arctic seas and adjacent waters, J. Ichthyol., 1994, vol. 35, no. 1, pp. 81–123.Google Scholar
  3. 3.
    Bulatov, O.A., Distribution of eggs and larvae of Greenland halibut Reinhardtius hippoglossoides (Pleuronectidae) in the eastern Bering Sea, J. Ichthyol., 1983, vol. 23, pp. 157–159.Google Scholar
  4. 4.
    Catalog of Fishes: Genera, Species, and References, Eschmeyer, W.N., Fricke, R., and van der Laan, R., Eds., 2017. Accessed March 10, 2017.Google Scholar
  5. 5.
    Chereshnev, I.A. and Kirillov, A.F., Fish-like animals and fishes of marine and fresh waters of the Laptev Sea and East Siberian Sea basins, Vestn. Sev.-Vost. Nauchn. Tsentra, Dal’nevost. Otd., Ross. Akad. Nauk, 2007, vol. 2, pp. 95–106.Google Scholar
  6. 6.
    Chernova, N.V., Distribution patterns and chorological analysis of fish fauna of the Arctic region, J. Ichthyol., 2011, vol. 51, no. 10, pp. 825–924. CrossRefGoogle Scholar
  7. 7.
    Chernova, N.V., Marine fish fauna of the Novosibirskie Islands area (protected zone of the Ust’-Lenskiy Reserve), Nauchn. Tr. Gos. Prirodn. Zap. Prisurskiy, 2015, vol. 30, pp. 271–276.Google Scholar
  8. 8.
    Chernova, N.V., Catching of Greenland halibut Reinhardtius hippoglossoides (Pleuronectidae) on the shelf edge of the Laptev and East Siberian seas, J. Ichthyol., 2017, vol. 57, no. 2, pp. 219–227. CrossRefGoogle Scholar
  9. 9.
    Chernova, N.V. and Neyelov, A.V., Fish caught in the Laptev Sea during the cruise of RV “Polarstern” in 1993, Ber. Polarforsch., 1995, vol. 176, pp. 222–227.Google Scholar
  10. 10.
    Coughlan, J., Stefansson, M., Galvin, P., et al., Isolation and characterization of 11 microsatellite loci in Atlantic halibut (Hippoglossus hippoglossus L.), Mol. Ecol., 2000, vol. 9, pp. 817–829. CrossRefGoogle Scholar
  11. 11.
    De Vliet van, M.S., Diekmann, O.E., and Serrão, E.T.A., Highly polymorphic microsatellite markers for the short-snouted seahorse (Hippocampus hippocampus), including markers from a closely related species the longsnouted seahorse (Hippocampus guttulatus), Conserv. Genet. Resour., 2009, vol. 1, pp. 93–96.
  12. 12.
    Diakov, Y.P., Population structure of the Pacific black halibut Reinhardtius matsuurae Jordan et Snyder, J. Sea Res., 1998, vol. 40, pp. 109–116.CrossRefGoogle Scholar
  13. 13.
    D’yakov, Y.P., Distribution of Greenland halibut juveniles in the Bering Strait and Chukchi Sea, in Biologicheskie resursy shel’fovykh i okrainnykh morei (Biological Resources of Shelf and Marginal Seas), Skarlato, O.A. and Alekseev, A.P., Eds., Moscow: Nauka, 1990, pp. 177–180.Google Scholar
  14. 14.
    Ding, H., Shao, C., Liao, X., et al., Ten polymorphic microsatellite loci for the Atlantic halibut (Hippoglossus hippoglossus) and cross-species application in related species, Conserv. Genet., 2009, vol. 10, pp. 611–614.Google Scholar
  15. 15.
    Dominguez-Petit, R., Ouellet, P., and Lambert, Y., Reproductive strategy, egg characteristics and embryonic development of Greenland halibut (Reinhardtius hippoglossoides), ICES J. Mar. Sci., 2013, vol. 70, pp. 342–351.
  16. 16.
    Drummond, A.J., Ashton, B., Buxton, S., et al., Geneious v. 5.5, 2011. Scholar
  17. 17.
    Earl, D.A. and von Holdt, B.M., STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method, Conserv. Genet. Resour., 2012, vol. 4, no. 2. pp. 359–361. CrossRefGoogle Scholar
  18. 18.
    Excoffier, L. and Lischer, H.E.L. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows, Mol. Ecol. Resour., 2010, vol. 10, no. 3, pp. 564–567. CrossRefGoogle Scholar
  19. 19.
    Fairbairn, D.J., Biochemical genetic analysis of population differentiation in Greenland halibut (Reinhardtius hippoglossoides) from the Northwest Atlantic, Gulf of St. Lawrence, and Bering Sea, Can. J. Fish. Aquat. Sci., 1981, vol. 38, no. 6, pp. 669–677. CrossRefGoogle Scholar
  20. 20.
    Fierstine, H.L., Huddleston, R.W., and Takeuchi, G.T., Catalog of the Neogene bony fishes of California: a systematic inventory of all published accounts, Occas. Pap. Calif. Acad. Sci., 2012, vol. 159, pp. 1–206.Google Scholar
  21. 21.
    Filina, E.A. and Budanova, L.K., On the finding of mature individuals of the Greenland halibut Reinhardtius hippoglossoides (Pleuronectidae) in the Kara Sea, J. Ichthyol., 2015, vol. 55, no. 1, pp. 138–142. CrossRefGoogle Scholar
  22. 22.
    Glebov, I.I., Nadtochii, V.A., Savin, A.B., et al., Results of multidisciplinary survey in the Laptev Sea in August–September 2015, Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 2016a, vol. 187, pp. 72–88.Google Scholar
  23. 23.
    Glebov, I.I., Nadtochii, V.A., Savin, A.B., et al., Results of complex surveys in the East Siberian Sea in August 2015, Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 2016b, vol. 186, pp. 81–92.Google Scholar
  24. 24.
    Hubbs, C.L. and Willimovsky, N.J., Distribution and synonymy in the Pacific Ocean, and variation, of the Greenland halibut Reinhardtius hippoglossoides (Walbaum), J. Fish. Res. Board Can., 1964, vol. 21, no. 5, pp. 1129–1154. CrossRefGoogle Scholar
  25. 25.
    Igland, O.T. and Nævdal, G. Allozyme studies of Greenland halibut, Reinhardtius hippoglossoides Walbaum 1792, from the North Atlantic, Sarsia, 2001, vol. 86, no. 3, pp. 237–240. CrossRefGoogle Scholar
  26. 26.
    Kartavtsev, Y.P., Sharina, S.N., Saitoh, K.J., et al., Phylogenetic relationships of Russian far eastern flatfish (Pleuronectiformes, Pleuronectidae) based on two mitochondrial gene sequences, Co-1 and Cyt-b, with inferences in order phylogeny using complete mitogenome data, Mitochondrial DNA, Part A, 2016, vol. 27, no. 1, pp. 667–678. CrossRefGoogle Scholar
  27. 27.
    Kirillov, A.F. and Chereshnev, I.A., Annotated list of fish-like species and fishes of marine and fresh waters of Yakutia, Vestn. Yakut. Gos. Univ., 2006, vol. 3, pp. 5–14.Google Scholar
  28. 28.
    Knutsen, H., Jorde, P.E., Albert, O.T., et al., Population genetic structure in the North Atlantic Greenland halibut (Reinhardtius hippoglossoides): influenced by oceanic current systems? Can. J. Fish. Aquat. Sci., 2007, vol. 64, pp. 857–866. CrossRefGoogle Scholar
  29. 29.
    Lahrech, Z., Kishioka, C., Morishima, K., et al., Genetic verification of induced gynogenesis and microsatellite-centromere mapping in the barfin flounder, Verasper moseri, Aquaculture, 2007, vol. 272, suppl. 1, pp. S115–S124. CrossRefGoogle Scholar
  30. 30.
    Leigh, J.W. and Bryant, D., POPART: Full-feature software for haplotype network construction, Methods Ecol. Evol., 2015, vol. 6, no. 9, pp. 1110–1116. CrossRefGoogle Scholar
  31. 31.
    Lyle, M., Barron, J., Bralower, T., et al., Pacific Ocean and Cenozoic evolution of climate, Rev. Geophys., 2008, vol. 46, no. 2, art. ID RG2002. CrossRefGoogle Scholar
  32. 32.
    Marincovich, L., Jr., Central American paleogeography controlled Pliocene Arctic Ocean molluscan migrations, Geology, 2000, vol. 28, no. 6, pp. 551–554.<551:CAPCPA>2.0.CO;2 CrossRefGoogle Scholar
  33. 33.
    Matthiessen, J., Knies, J., Vogt, C., and Stein, R. Pliocene palaeoceanography of the Arctic Ocean and subarctic seas, Philos. Trans. R. Soc. A, 2009, vol. 367, no. 1886, pp. 21–48.
  34. 34.
    McGowan, C. and Reith, M.E., Polymorphic microsatellite markers for Atlantic halibut, Hippoglossus hippoglossus, Mol. Ecol., 1999, vol. 8, no. 10, pp. 1761–1763. CrossRefGoogle Scholar
  35. 35.
    Mecklenburg, C.W., Mecklenburg, T.A., Sheiko, B.A., and Steinke, D. Pacific Arctic Marine Fishes, CAFF Monitoring Series Report No. 23, Akureyri: Arctic Council, 2016.Google Scholar
  36. 36.
    Mecklenburg, C.W., Møller, P.R., and Steinke, D., Biodiversity of Arctic marine fishes: taxonomy and zoogeography, Mar. Biodiversity, 2011, vol. 41, no. 1, pp. 109–140. CrossRefGoogle Scholar
  37. 37.
    Minami, T. and Tanaka, M., Life history cycles in flatfish from the northwestern Pacific, with particular reference to their early life histories, Neth. J. Sea Res., 1992, vol. 29, nos. 1–3, pp. 35–48. CrossRefGoogle Scholar
  38. 38.
    Nazarkin, M.V., A new late Miocene flounder from Agnevo Svita, Sakhalin Island, J. Ichthyol., 1997, vol. 37, no. 5, pp. 547–553.Google Scholar
  39. 39.
    Nazarkin, M.V., Large flatfishes from the Miocene of the Agnev formation of the Sakhalin Island, J. Ichthyol., 2002, vol. 42, no. 1, pp. 7–18.Google Scholar
  40. 40.
    Norman, J.R., A Systematic Monograph of the Flatfishes (Heterosomata), London: Br. Mus., 1934.CrossRefGoogle Scholar
  41. 41.
    Ohe, F., Deep fish assemblage from the Middle Miocene Morozaki Group, southern part of Chita Peninsula, Aichi Prefecture, central Japan, in Fossils from the Miocene Morozaki Group, Nagoya: Tokai Fossil Soc., 1993, pp. 169–262.Google Scholar
  42. 42.
    Orlova, S.Yu., Volkov, A.A., Maznikova, O.A., et al., Population status of Greenland halibut Reinhardtius hippoglossoides (Walbaum, 1793) of the Laptev Sea, Dokl. Biochem. Biophys., 2017, vol. 477, no. 1, pp. 349–353. CrossRefGoogle Scholar
  43. 43.
    Parin, N.V., Evseenko, S.A., and Vasil’eva, E.D., Ryby morei Rossii: Annotirovannyi katalog (Fishes of Russian Seas: Annotated Catalogue), Moscow: KMK, 2014.Google Scholar
  44. 44.
    Peakall, R. and Smouse, P.E., GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research, Mol. Ecol. Notes, 2006, vol. 6, no. 1, pp. 288–295. CrossRefGoogle Scholar
  45. 45.
    Pomilla, C., Treble, M.A., Postma, L.D., et al., Initial genetic evidence of population structure of Greenland halibut (Reinhardtius hippoglossoides) in the Northwest Atlantic, J. Northw. Atl. Fish. Sci., 2008, vol. 40, pp. 1–15.Google Scholar
  46. 46.
    Pritchard, J.K., Stephens, M., and Donnelly, P., Inference of population structure using multilocus genotype data, Genetics, 2000, vol. 155, no. 2, pp. 945–959.
  47. 47.
    Raymond, M. and Rousset, F., GENEPOP (version 1.2): Population genetics software for exact tests and ecumenicism, J. Hered., 1995, vol. 86, no. 3, pp. 248–249. CrossRefGoogle Scholar
  48. 48.
    Reid, D. P., Smith, C.A., Rommens, M., et al., A genetic linkage map of Atlantic halibut (Hippoglossus hippoglossus L.), Genetics, 2007, vol. 177, no. 2, pp. 1193–1205.CrossRefGoogle Scholar
  49. 49.
    Roje, D.M., Incorporating molecular phylogenetics with larval morphology while mitigating the effects of substitution saturation on phylogeny estimation: A new hypothesis of relationships for the flatfish family pleuronectidae (Percomorpha: Pleuronectiformes), Mol. Phylogen. Evol., 2010, vol. 56, no. 2, pp. 586–600. CrossRefGoogle Scholar
  50. 50.
    Schmidt, P.Y., Fishes of the Sea of Okhotsk, Tr. Tikhookean. Kom. Akad. Nauk SSSR, 1950, vol. 6, pp. 1–370.Google Scholar
  51. 51.
    Silva, W.A., Jr., Costa, M.C., Valente, V., et al., PCR template preparation for capillary DNA sequencing, BioTechniques, 2001, vol. 30, no. 3, pp. 537, 540–542.CrossRefGoogle Scholar
  52. 52.
    Soldatov, V.K. and Lindberg, G.U., Review of fishes of Far East seas, Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 1930, vol. 5, pp. 1–576.Google Scholar
  53. 53.
    Suzuki, N., Nishida, M., and Amaoka, K., The phylogenetic position of the genus Atheresthes (Pleuronectidae) and its classification: A molecular phylogenetic approach using mitochondrial sequence data, Bull. Fac. Fish. Sci. Hokkaido Univ., 2001, vol. 52, pp. 39–46.Google Scholar
  54. 54.
    Taranetz, A.Yu., Handbook for identification of fishes of Soviet Far East and adjacent waters, Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 1937, vol. 11, pp. 1–200.Google Scholar
  55. 55.
    Tsukamoto, Y., Ueno, Y., Minami, T., and Okiyama, M., Transforming specimens of two right flounders, Atheresthes evermanni and Reinhardtius hippoglossoides, Jpn. J. Ichthyol., 1995, vol. 41, pp. 469–473.Google Scholar
  56. 56.
    Vernidub, M.F. and Panin, K.I., Systematic position and biology of a Pacific representative of Reinhardtius Gill., Uch. Zap. Leningr. Gos. Univ., 1937, vol. 15, pp. 250–272.Google Scholar
  57. 57.
    Vinnikov, K.A., Thomson, R.C., and Munroe, T.A., Revised classification of the righteye flounders (Teleostei: Pleuronectidae) based on multilocus phylogeny with complete taxon sampling, Mol. Phylogen. Evol., 2018, vol. 125, pp. 147–162. CrossRefGoogle Scholar
  58. 58.
    Voronina, E.P., Specific features of the seismosensory system and their use in the systematics of five families of the order Pleuronectiformes, J. Ichthyol., 2009, vol. 49, no. 5, pp. 349–361. CrossRefGoogle Scholar
  59. 59.
    Wang, J., The computer program structure for assigning individuals to populations: easy to use but easier to misuse, Mol. Ecol. Resour., 2016, vol. 17, no. 5, pp. 981–990. CrossRefGoogle Scholar
  60. 60.
    Wesgaard, J-I., Saha, A., Kent, M., et al., Genetic population structure in Greenland halibut (Reinhardtius hippoglossoides) and its relevance to fishery management, Can. J. Fish. Aquat. Sci., 2017, vol. 74, no. 4, pp. 475–485. CrossRefGoogle Scholar
  61. 61.
    Yabumoto, Y. and Uyeno, T., Late Mesozoic and Cenozoic fish faunas of Japan, Island Arc, 1994, vol. 3, pp. 255–269.CrossRefGoogle Scholar
  62. 62.
    Zhivotovskii, L.A., Populyatsionnaya biometriya (Population Biometrics), Moscow: Nauka, 1991.Google Scholar

Copyright information

© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  • S. Yu. Orlova
    • 1
  • A. A. Volkov
    • 1
  • D. M. Shcepetov
    • 1
    • 2
  • O. A. Maznikova
    • 1
  • N. V. Chernova
    • 3
  • E. A. Chikurova
    • 1
    • 5
  • I. I. Glebov
    • 4
  • A. M. Orlov
    • 1
    • 5
    • 6
    • 7
    • 8
    Email author
  1. 1.Russian Federal Research Institute of Fisheries and OceanographyMoscowRussia
  2. 2.Koltzov Institute of Developmental Biology of the Russian Academy of SciencesMoscowRussia
  3. 3.Zoological Institute of the Russian Academy of SciencesSt. PetersburgRussia
  4. 4.Pacific Fisheries Science CenterVladivostokRussia
  5. 5.Severtsov Institute of Ecology and Evolution of the Russian Academy of SciencesMoscowRussia
  6. 6.Dagestan State UniversityMakhachkalaRussia
  7. 7.Tomsk State UniversityTomskRussia
  8. 8.Caspian Institute of Biological Resources, Dagestan Scientific Center of the Russian Academy of SciencesMakhachkalaRussia

Personalised recommendations