Molecular and Morphometric Variations in the Sea Raven, Hemitripterus villosus from Korea, with its Implication on Fisheries Management

  • Seo-Ha Jang
  • Jang-Won Lee
  • Jin-Koo KimEmail author


To understand and clarify the geographic variations of the Korean sea raven, Hemitripterus villosus, we investigated the molecular and morphometric characteristics of 147 individuals (in morphs) and 175 individuals (in molecules) collected from three locations in the Yellow Sea (Incheon, Boryeong, and Heuksando), one location in the Korea Strait (Busan), and two locations in the East Sea (Goseong and Pohang), around the Korean peninsula. The Kruskal-Wallis test showed there were no significant differences in meristic characteristics among locations, except for the number of vertebrae (mean, 39.7 in Goseong vs. and 38.4–38.8 in the remaining locations). A canonical discriminant analysis based on 25 morphometric characters showed that two groups were separated by the center value “0” of CAN1: Yellow Sea and Korea Strait individuals had positive values, whereas East Sea individuals had negative values. An analysis of molecular variance (AMOVA) based on 801 base-pair sequences of the mitochondrial DNA cytochrome b gene showed that two lineages were separated by fixation (FST) index. A pairwise FST test revealed moderate genetic differentiation between the Goseong individuals (middle East Sea) and the individuals at the remaining locations except for the Pohang individuals (southern East Sea). Our molecular and morphometric analysis results indicate that there exists two populations in the Korean sea raven, and their admixture zone may be located near Pohang. Population subdivision might be associated with sea level change during last glacial period, and this may have been subsequently maintained by the hydrographic and oceanic current heterogeneity of each sea around the Korean peninsula. Accordingly, different management measures should be adopted with regard to the two groups, the East Sea group and the Yellow Sea + Korea Strait group.


Hemitripterus villosus cytochrome b amova morphometric characters fisheries management 


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We are grateful to anonymous reviewers for their valuable comments. This research was supported by the Marine Biotechnology Program of the Korea Institute of Marine Science and Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (MOF) (No. 20170431) and supported by a grant from the National Institute of Fisheries Science of Korea (R2019020).


  1. Avise JC (1994) Molecular markers, natural history and evolution. Chapman and Hall Press, New York, 511 pCrossRefGoogle Scholar
  2. Bartlett SE, Davidson WS (1991) Identification of Thunnus tuna species by the polymerase chain reaction and direct sequence analysis of mitochondrial cytochrome b genes. Can J Fish Aquat Sci 48:309–317CrossRefGoogle Scholar
  3. Begg GA, Hare JA, Sheehan DD (1999) The role of life history parameters as indicators of stock structure. Fish Res 43:141–163CrossRefGoogle Scholar
  4. Bowen BW, Muss A, Rocha LA, Grant WS (2006) Shallow mtDNA coalescence in Atlantic pygmy angelfishes (Genus Centropyge) indicates a recent invasion from the Indian Ocean. J Hered 97:1–12CrossRefGoogle Scholar
  5. Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial DNA sequences of primates: tempo and mode of evolution. J Mol Evol 18:225–239CrossRefGoogle Scholar
  6. Buonaccorsi VP, McDowell JR, Graves JE (2001) Reconciling patterns of inter-ocean molecular variance from four classes of molecular markers in blue marlin (Makaira nigricans). Mol Ecol 10:1179–1196CrossRefGoogle Scholar
  7. Byun SG, Kim JD, Go CJ (1997) Development testing of seed production techniques of Hemitripterus villosus (I). National Fisheries Research and Development Institute, Busan, 356 pGoogle Scholar
  8. Choi Y (2007) Edible sea fishes. Kyo-Hak Publishing, Seoul, 314 pGoogle Scholar
  9. Chyung MK (1977) The fishes of Korea. Ilchisa Publishing Co., Seoul, 727 pGoogle Scholar
  10. Clement M, Posada DCKA, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefGoogle Scholar
  11. Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefGoogle Scholar
  12. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925Google Scholar
  13. 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. P Natl A Sci USA 106:1473–1478CrossRefGoogle Scholar
  14. 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 89:415–426CrossRefGoogle Scholar
  15. Grant WS, Utter FM (1984) Biochemical population genetics of Pacific herring (Clupea pallasi). Can J Fish Aquat Sci 41:856–864CrossRefGoogle Scholar
  16. Habib M, Lakra WS, Mohindra V, Khare P, Barman AS, Singh A, Lal KK, Punia P, Khan AA (2011) Evaluation of cytochrome b mtDNA sequences in genetic diversity studies of Channa marulius (Channidae: Perciformes). Mol Biol Rep 38:841–846CrossRefGoogle Scholar
  17. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid S 41:95–98Google Scholar
  18. Han ZQ, Gao TX, Yanagimoto T, Sakurai Y (2008) Deep phylogeographic break among white croaker Pennahia argentata (Sciaenidae, Perciformes) populations in North-western Pacific. Fisheries Sci 74:770–780CrossRefGoogle Scholar
  19. Harpending RC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600Google Scholar
  20. Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913CrossRefGoogle Scholar
  21. Hilborn R, Walters CJ (1992) Quantitative fisheries stock assessment: choice, dynamics and uncertainty. Rev Fish Biol Fisher 2:177–178CrossRefGoogle Scholar
  22. Hsu KC, Shih NT, Ni HI, Shao KT (2007) Genetic variation in Trichiurus lepturus (Perciformes: Trichiuridae) in water of Taiwan: several species or cohort distribution? Raffles Bull Zool 14:215–220Google Scholar
  23. Ihssen PE, Booke HE, Casselman JM, McGlade JM, Payne NR, Utter FM (1981) Stock identification: materials and methods. Can J Fish Aquat Sci 3:1838–1855CrossRefGoogle Scholar
  24. Im YJ, Jo HS, Ji HS, Myoung SH, Kim JK (2017) Geographic variations of the mottled skate, Beringraja pulchra (Liu, 1932) (Rajidae) in the Yellow and East seas based on molecular and morphometric data. J Appl Ichthyol 33:950–956CrossRefGoogle Scholar
  25. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. Version 3.23. Accessed 17 Nov 2017
  26. Joseph J, Jayasankar P (2001) Morphometric and genetic variations in the threadfin bream Nemipterus mesoprion. J Mar Biol Ass India 43:217–221Google Scholar
  27. Kai Y, Nakabo T (2002) Morphological differences among three color morphotypes of Sebastes inermis (Scorpaenidae). Ichthyol Res 49:260–266CrossRefGoogle Scholar
  28. Kaiser TS, Neumann D, Heckel DG, Berendonk TU (2010) Strong genetic differentiation and postglacial origin of populations in the marine midge Clunio marinus (Chironomidae, Diptera). Mol Ecol 19:2845–2857CrossRefGoogle Scholar
  29. Kelly RP, Palumbi SR (2010) Genetic structure among 50 species of the Northeastern Pacific intertidal community. PLoS One 5(1):e8594. doi: CrossRefGoogle Scholar
  30. Khim BK, Bahk JJ, Hyun S, Lee GH (2007) Late pleistocene dark laminated mud layers from the Korea Plateau, western East Sea/Japan Sea and their paleoceanographic implications. Palaeogeogr Palaeocl 247:74–87CrossRefGoogle Scholar
  31. Kim IS, Choi Y, Lee CL, Lee YJ, Kim BJ, Kim JH (2005) Illustrated book of Korean fishes. Kyo-Hak Pub Co, Seoul, 615 pGoogle Scholar
  32. Kim JK, Park JH, Kim YS, Kim YH, Hwang HJ, Hwang SJ, Lee SI, Kim TI (2008) Geographic variations in Pacific sand eels Ammodytes personatus (Ammodytidae) from Korea and Japan using multivariate morphometric analysis. J Ichthyol 48:904–910CrossRefGoogle Scholar
  33. Kim JK (2009) Diversity and conservation of Korean marine fishes. Korean J Ichthyol 21:52–62Google Scholar
  34. Kim JK, Bae SE, Lee SJ, Yoon MG (2017) New insight into hybridization and unindirectional introgression between Ammodyetes japonicus and Ammodytes heian (Trachiniformes, Ammodytidae). PLoS One 12(6):e0178001. doi: CrossRefGoogle Scholar
  35. Kim JK, Ryu JW (2016) Distribution map of sea fishes in Korea. Maple Publishing, Busan, 667 p (in Korean)Google Scholar
  36. Kim WJ, Kim KK, Han HS, Nam BH, Kim YO, Kong HJ, Noh JK, Yoon M (2010) Population structure of the olive flounder (Paralichthys olivaceus) in Korea inferred from microsatellite marker analysis. J Fish Biol 77:1958–1971CrossRefGoogle Scholar
  37. Kitamura A, Kimoto K (2006) History of the inflow of the warm Tsushima Current into the Sea of Japan between 3.5 and 0.8 Ma. Palaeogeogr Palaeocl 236:355–366CrossRefGoogle Scholar
  38. Kyushin K (1968) The embryonic development and larval stages of Hemitripterus villosus (Pallas). Bull Fac Fish Hokkaido Univ 18:277–289Google Scholar
  39. Lambeck K, Esat TM, Potter EK (2002) Links between climate and sea levels for the past three million years. Nature 419:199–206CrossRefGoogle Scholar
  40. Lecomte F, Grant WS, Dodson JJ, Rodriguez-Sanchez R, Bowen BW (2004) Living with uncertainty: genetic imprints of climate shifts in east Pacific anchovy (Engraulis mordax) and sardine (Sardinops sagax). Mol Ecol 13:2169–2182CrossRefGoogle Scholar
  41. Li WH (1997) Molecular evolution. Sinauer Associates, Massachusetts, 487 pGoogle Scholar
  42. Lindberg GU, Krasyukova ZV (1987) Fishes of the sea of Japan and adjacent parts of the Sea of Okhotsk and the Yellow Sea (Nauka, Leningrad), Part 5. SILNSF, Washington DCGoogle Scholar
  43. Lindsey CC (1988) Factors controlling meristic variation. In: Hoar WS, Randall DJ (eds) Fish physiology. Academic Press, San Diego, pp 197–274Google Scholar
  44. Liu JX, Gao TX, Yokogawa K, Zhang YP (2006) 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 39:799–811CrossRefGoogle Scholar
  45. Liu JX, Gao TX, Wu SF, Zhang YP (2007) Pleistocene isolation in the Northwestern Pacific marginal seas and limited dispersal in a marine fish, Chelon haematocheilus (Temminck & Schlegel, 1845). Mol Ecol 16:275–288CrossRefGoogle Scholar
  46. Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76:173–190CrossRefGoogle Scholar
  47. Masuda H, Amaoka K, Araga C, Uyeno T, Yoshino T (1984) The fishes of the Japanese archipelago. Tokai University Press, Tokyo, 837 pGoogle Scholar
  48. McDowall RM (2008) Jordan’s and other ecogeographical rules, and the vertebral number in fishes. J Biogeogr 35:501–508CrossRefGoogle Scholar
  49. Murray WB, Wang JY, Yang SC, Stevens JD, Fisk A, Svavarsson J (2008) Mitochondrial cytochrome b variation in sleeper sharks (Squaliformes: Somniosidae). Mar Biol 153:1015–1022CrossRefGoogle Scholar
  50. Murta AG (2000) Morphological variation of horse mackerel (Trachurus trachurus) in the Iberian and North African Atlantic: implications for stock identification. ICES J Mar Sci 57:1240–1248CrossRefGoogle Scholar
  51. Murta AG, Pinto AL, Abaunza P (2008) Stock identification of horse mackerel (Trachurus trachurus) through the analysis of body shape. Fish Res 89:152–158CrossRefGoogle Scholar
  52. Myoung SH, Ban TW, Kim JK (2016) Population structure of Liparis tanakae (PISCES, Liparidae) from Korea based on morphological and molecular traits. Korean J Fish Aquat Sci 49:198–207Google Scholar
  53. Myoung SH, Kim JK (2016) Population structure of the Korean gizzard shad, Konosirus punctatus (Clupeiformes, Clupeidae) using multivariate morphometric analysis. Ocean Sci J 51:33–41CrossRefGoogle Scholar
  54. Novikov NP, Sokolovskii AS, Sokolovskaya TG, Yakovlev YM (2002) RybyPrimor’ya (Fishes of Primorye). Dal’rybvtuz, Vladivostok, 552 pGoogle Scholar
  55. Okiyama M, Sando H (1976) Early life history of the sea raven, Hemitripterus villosus (Hemitripterinae, cottidae) in the Japan sea. Bull Japan Sea Rgnl Fish Res Lab 27:1–10Google Scholar
  56. Pack AJ, Han KH, Lee SH, Kim HJ, Kim SY, Lim IH (2014) Embryonic development of eggs, larvae, and juveniles of the Hemitripterus villosus. Korean J Ichthyol 26:34–11Google Scholar
  57. Park JH (2014) Community structure of demersal fish and its relation to marine environments in the coastal waters of middle and southern East Sea, Korea. Ph.D. Thesis, Pukyong National University, 150 pGoogle Scholar
  58. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Evol S 25:547–572CrossRefGoogle Scholar
  59. Palumbi SR (1996) Nucleic acids II: the polymerase chain reaction. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics. Sinauer Associates, Massachusetts, pp 205–247Google Scholar
  60. Pickart RS, Spall MA, Lazier JRN (1997) Mid-depth ventilation in the western boundary current system of the sub-polar gyre. Deep-Sea Res Pt I 44:1025–1054CrossRefGoogle Scholar
  61. Quddus MMA, Shimizu M, Nose Y (1984) Meristic and morphometric differences between two types of Hilsa ilisha in Bangladesh waters. Nippon Suisan Gakk 50:43–49CrossRefGoogle Scholar
  62. Ricker WE (1973) Linear regressions in fishery research. J Fish Res Board Can 30:409–434CrossRefGoogle Scholar
  63. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569Google Scholar
  64. 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 152:1079–1089Google Scholar
  65. Shen KN, Jamandre BW, Hsu CC, Tzeng WN, Durand JD (2011) Plio-Pleistocene sea level and temperature fluctuations in the northwestern Pacific promoted speciation in the globally-distributed flathead mullet Mugil cephalus. BMC Evol Biol 11(1):83. doi: CrossRefGoogle Scholar
  66. Silva A (2003) Morphometric variation among sardine (Sardina pilchardus) populations from the northeastern Atlantic and the western Mediterranean. ICES J Mar Sci 60:1352–1360CrossRefGoogle Scholar
  67. Sun P, Tang BJ (2018) Low mtDNA variation and shallow population structure of the Chinese pomfret Pampus chinensis along the China coast. J Fish Biol 92:214–228CrossRefGoogle Scholar
  68. Sun P, Yin F, Gao Q, Shi Z (2013) Genetic diversity and population structure of silver pomfret (Pampus argenteus) in the Indo-West Pacific revealed by mitochondrial control region sequences. Biochem Syst Ecol 51:28–36CrossRefGoogle Scholar
  69. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595Google Scholar
  70. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526Google Scholar
  71. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  72. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  73. Tokranov AM, Orlov AM (2006) Biological features of the sea raven Hemitripterus villosus (Hemitripteridae) in Pacific waters off the northern Kuril Islands and southeastern Kamchatka. J Ichthyol 46:743–751CrossRefGoogle Scholar
  74. Turan C, Oral M, Öztürk B, Dzgünes E (2006) Morphometric and meristic variation between stocks of bluefish (Pomatomus saltatrix) in the Black, Marmara, Aegean and northeastern Mediterranean Seas. Fish Res 79:139–147CrossRefGoogle Scholar
  75. Tzeng TD (2004) Morphological variation between populations of spotted mackerel (Scomber australasicus) off Taiwan. Fish Res 68:45–55CrossRefGoogle Scholar
  76. Walpes RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89:438–450CrossRefGoogle Scholar
  77. Wang P (1999) Response of western pacific marginal seas to glacial cycles: paleoceanographic and sedimentological features. Mar Geol 156:5–39CrossRefGoogle Scholar
  78. Wang L, Liu S, Zhuang Z, Guo L, Meng Z, Lin H (2013) Population genetic studies revealed local adaptation in a high gene-flow marine fish, the small yellow croaker (Larimichthys polyactis). PLoS One 8(12):e83493. doi: CrossRefGoogle Scholar
  79. Wilson AC, Cann RL, Carr SM, George M, Gyllensten UB, Helm-Bychowski KM, Higuchi RG, Palumbi SR, Prager EM, Sage RD, Stoneking M (1985) Mitochondrial DNA and two perspectives on evolutionary genetics. Biol J Linn Soc 26:375–100CrossRefGoogle Scholar
  80. Wright S (1978) Evolution and the genetics of populations: variability within and among natural populations. The University of Chicago Press, Chicago, 590 pGoogle Scholar
  81. Xiao Y, Gao T, Zhang Y, Yanagimoto T (2010) Demographic history and population structure of blackfin flounder (Glyptocephalus stelleri) in Japan revealed by mitochondrial control region sequences. Biochem Genet 48:402–417CrossRefGoogle Scholar
  82. Yu HJ, Kai Y, Kim JK (2016) Genetic diversity and population structure of Hyporhamphus sajori (Beloniformes: Hemiramphidae) inferred from mtDNA control region and msDNA markers. J Fish Biol 89:2607–2624. doi: CrossRefGoogle Scholar
  83. Yu HJ, Kim JK 2018 Upwelling and eddies affect connectivity among local populations of the goldeye rockfish, Sebastes thompsoni (Pisces, Scorpaenoidei). Ecol Evol 8(9):4387–4402. doi: CrossRefGoogle Scholar
  84. Zar JH (1999) Biostatistical analysis. Pearson Prentice Hall, New Jersey, 960 pGoogle Scholar

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© KSO, KIOST and Springer 2019

Authors and Affiliations

  1. 1.Department of Marine Biology, College of Fisheries SciencesPukyong National UniversityBusanKorea
  2. 2.Department of Integrative Bio-industrial EngineeringSejong UniversitySeoulKorea

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