Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-22T18:44:57.279Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular Genetic Analysis of Atlanto-Scandian Herring (Clupea Harengus) Populations Using Allozymes and Mitochondrial Dna Markers

Published online by Cambridge University Press:  11 May 2009

Cemal Turan ,
Gary R. Carvalho  and
Jarle Mork
Cemal Turan
Affiliation:
Molecular Ecology & Fisheries Genetics Laboratory, Department of Biological Sciences, University of Hull, Hull, HU6 7RX.
Gary R. Carvalho*
Affiliation:
Molecular Ecology & Fisheries Genetics Laboratory, Department of Biological Sciences, University of Hull, Hull, HU6 7RX.
Jarle Mork
Affiliation:
Trondheim Biological Station, Bynesveien 46 N-7018, Trondheim, Norway.
*
‡ For correspondence (G.R.C.)
Get access Rights & Permissions [Opens in a new window]

Extract

Allozymes and restriction fragment length polymorphisms (RFLP's) in genes of the NADH dehydrogenase complex (ND 5/6 genes) of mitochondrial DNA (mtDNA) were used to investigate the spatial genetic structure of Atlanto-Scandian herring (Clupea harengus). Samples (sample size=46–50/site) comprised Icelandic summer spawners, Norwegian spring spawners, and two fjord populations, Balsfjord and Trondheimsfjord, on the Norwegian coast. Fifty enzymes were assayed, and samples were routinely examined at 18 enzymes comprising 28 putative allozyme loci. Significant genetic differentiation (P < 0.001) was detected between Trondheimsfjord herring and all other samples, with apparent genetic homogeneity among remaining samples, including the Balsfjord; a region shown previously to contain an allozymically distinct population. Herring from the Balsfjord were shown allozymically to represent the Norwegian spring spawning group, suggesting the presence of two stocks, a deeper resident spawning (Balsfjord) and a shallower, non-native feeding population (Norwegian spring spawning). Variation at the ND5/6 genes using six restriction enzymes revealed 96 composite haplotypes in 196 fish. Mean haplotype diversity was high (0.92), though nucleotide divergence between samples was small (highest=0.00029, between Trondheimsfjord and Balsfjord samples; lowest=0.00003, between Icelandic summer and Balsfjord samples). Monte-Carlo %2 analysis of haplotype frequencies revealed no significant geographic heterogeneity among samples, thus revealing a discordant pattern of genetic differentiation produced by allozymes and mtDNA markers. The detection of a genetically divergent population in deeper waters of the Trondheimsfjord supports the existence of distinct deep-water resident populations in the Norwegian fjords.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 78 , Issue 1 , February 1998 , pp. 269 - 283
Copyright
Copyright © Marine Biological Association of the United Kingdom 1998

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, L., Ryman, N., Rosenberg, R. & Stahl, G., 1981. Genetic variability in Atlantic herring (Clupea harengus harengus): description of protein loci and population data. Hereditas, 95, 69–78.CrossRefGoogle Scholar
Bembo, D.G., Carvalho, G.R., Cingolani, N. & Pitcher, T.J., 1996. Electrophoretic analysis of stock structure in Northern Mediterranean anchovies, Engraulis encrasicolus L. ICES Journal of Marine Science, 53, 115–128.CrossRefGoogle Scholar
Bembo, D.G., Carvalho, G.R., Snow, M., Cingolani, N. & Pitcher, T.J., 1995. Stock discrimination among European anchovies, Engraulis encrasicolus, by means of PCR-amplified mitochondrial DNA analysis. Fishery Bulletin. National Oceanic and Atmospheric Administration. Washington, DC, 94, 31–40.Google Scholar
Birky, C.W., Fuerst, P. & Maruyama, T., 1989. Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics, 21, 613–627.CrossRefGoogle Scholar
Brown, B.E., Darcy, G.H. & Overholtz, W., 1987. Stock assessment/stock identification: an interactive process. In Proceedings of the Stock Identification Workshop, NOAA-TM-NMFSSEFC-199 (ed. H.E., Kumpf et al.), pp. 1–24. Washington, DC: US Department of Commerce.Google Scholar
Carvalho, G.R., Bembo, D.G., Carone, A., Giesbrecht, G., Cingolani, N., & Pitcher, T.J., 1994. Stock discrimination in relation to assessment of Adriatic anchovy and sardine fisheries. Final Project Report to the Commission of the European Communities, EC XIV-1 /MED/91001 /A.Google Scholar
Carvalho, G.R. & Hauser, L., 1994. Molecular genetics and the stock concept in fisheries. Reviews in Fish Biology and Fisheries, 4, 326–350.CrossRefGoogle Scholar
Cronin, M.A., Spearman, W.J., Wilmot, R.L., Patton, J.C. & Bickham, J.W., 1993. Mitochondrial DNA variation in chinook (Oncorhynchus tshawytscha) and chum salmon (Oncorhynchus keta) detected by restriction enzyme analysis of polymerase chain reaction (PCR) products. Canadian Journal of Fisheries and Aquatic Sciences, 50, 708–715.CrossRefGoogle Scholar
Dahle, G. & Eriksen, A.G., 1990. Spring and autumn spawners of herring (Clupea harengus) in the North Sea, Skagerrak and Kattegat; population genetic analysis. Fisheries Research, 9, 131–141.CrossRefGoogle Scholar
Ferguson, A., 1989. Genetic differences among brown trout, Salmo trutta, stocks and their importance for the conservation and management of the species. Freshwater Biology, 21, 35–46.CrossRefGoogle Scholar
Ferguson, M.M., Danzmann, R.G. & Hutchings, J.A., 1991. Incongruent estimates of population differentiation among brook charr, Salvelinus fontinalis, from Cape Race, Newfoundland, Canada, based upon allozyme and mitochondrial DNA variation. Journal of Fish Biology, 39A, 79–85.CrossRefGoogle Scholar
Fridriksson, A., 1944. The herring of the north coast of Iceland. Rit Fiskideildar, no. 1, 390 pp.Google Scholar
Fridriksson, A., 1958. The tribes of the north coast herring of Iceland with special reference to the period 1948–1955. Rapports et Procès-verbaux des Reunions. Conseil International pour l'Exploration de la Mer. Copenhague, 143, 36–44.Google Scholar
Fridriksson, A. & Aasen, O., 1952. The Norwegian-Icelandic herring tagging experiments. Report no. 2. Rit Fiskideildar, 1, 1–54.Google Scholar
Grant, W.S., 1984. Biochemical population genetics of Atlantic herring, Clupea harengus. Copeia, Report no. 2. Rit Fiskideildar, 1, 355–362.Google Scholar
Haegele, C.W. & Schweigert, J.F., 1985. Distribution and characteristics of herring spawning grounds and description of spawning behaviour. Canadian Journal of Fisheries and Aquatic Sciences, 42, supplement 1, 39–55.CrossRefGoogle Scholar
Hall, H., 1992. The genetics of brown trout (Salmo trutta L.) populations in Wales. PhD thesis, University of Wales, Swansea, Wales.Google Scholar
Hansen, M.M. & Loeschcke, V., 1996. Genetic differentiation among Danish brown trout populations, as detected by RFLP analysis of PCR amplified mitochondrial DNA segments. Journal of Fish Biology, 48, 422–436.Google Scholar
Harris, H. & Hopkinson, D., 1976. Handbook of enzyme electrophoresis in human genetics. New York: Elsevier.Google Scholar
Hauser, L., Carvalho, G.R. & Pitcher, T.J., 1995. Morphological and genetic differentiation of the African clupeid Limnothrissa miodon 34 years after its introduction to Lake Kivu. Journal of Fish Biology, 47A, 127–144.CrossRefGoogle Scholar
Henry, F. & Ferguson, A., 1985. Kinetic studies on the lactate dehydrogenase (LDH-5) isozymes of brown trout, Salmo trutta L. Comparative Biochemistry and Physiology, 82B, 95–98.Google ScholarPubMed
Jakobsson, J., 1963. The Icelandic herring fishery in 1961. Annals in Biology. Copenhagen, 18, 142–147.Google Scholar
Jakobsson, J., 1965. The Icelandic herring fishery in 1963. Annals in Biology. Copenhagen, 20, 155–160.Google Scholar
Johansen, A.C., 1926. Investigations on Icelandic herring in 1924 and 1925. Rapports Conseil pour l'Exploration de la Mer, 39, 114–138.Google Scholar
Johansen, A.C., 1927. On the migration of the herring. Journal du Conseil, 2, 3–27.CrossRefGoogle Scholar
JØrstad, K.E., Dahle, G. & Paulsen, O.I., 1994. Genetic comparison between Pacific herring (Clupea pallasi) and a Norwegian fjord stock of Atlantic herring (Clupea harengus). Canadian Journal of Fisheries and Aquatic Sciences, 51, supplement 1, 233–239.CrossRefGoogle Scholar
JØrstad, K.E., King, D.P.F. & Nævdal, G., 1991. Population structure of Atlantic herring, Clupea harengus. Journal of Fish Biology, 39, supplement A, 43–52.CrossRefGoogle Scholar
JØrstad, K.E. & Nævdal, G., 1981. Significance of population genetics on the management of herring stocks. Conseil International pour l'Exploration de la Mer, 1981/H, 64.Google Scholar
JØrstad, K.E. & Nævdal, G., 1983. Genetically distinct populations of herring. Contribution to XI International Congress of Genetics, New Delhi, India, 24–36.Google Scholar
JØrstad, K.E. & Pederson, S.A., 1986. Discrimination of herring populations in a Northern Norwegian fjord: genetic and biological aspects. International Council for the Exploration of the Sea (CM Papers and Reports), M: 63.Google Scholar
King, D.P.F., Fergusson, A. & Moffett, I.J.J., 1987. Aspects of the population genetics of herring, Clupea harengus, around the British Isles and in the Baltic Sea. Fisheries Research, 6, 35–52.CrossRefGoogle Scholar
Kornfield, I. & Bogdanowicz, S.M., 1987. Differentiation of mitochondrial DNA in Atlantic herring, Clupea harengus. Fishery Bulletin. National Oceanic and Atmospheric Administration. Washington, DC, 85, 561–568.Google Scholar
Kornfield, I., Sidell, B.D. & Gagnon, P.S., 1982. Stock definition in Atlantic herring (Clupea harengus): genetic evidence for discrete fall and spring spawning populations. Canadian journal of Fisheries and Aquatic Sciences, 39, 1610–1621.CrossRefGoogle Scholar
Liamin, K.A., 1959. Trudy PINRO (In Russian); Translation in Special Science Report. US Fish and Wildlife Service. Fisheries, no. 327, 166–202. [In Russian.]Google Scholar
Martin, A.P., Naylor, G.J.P. & Palumbi, S.R., 1992. Rates of mitochondrial evolution in sharks are slow compared with mammals. Nature, London, 357, 153–155.CrossRefGoogle ScholarPubMed
McElroy, D., Moran, P., Bermingham, E. & Kornfield, I., 1992. REAP: an integrated environment for the manipulation and phylogenetic analysis of restriction data, journal of Heredity, 83, 157–158.CrossRefGoogle ScholarPubMed
Messieh, S.N., 1972. Use of otoliths in identifying herring stocks in the southern Gulf of St. Lawrence and adjacent waters, journal of Fisheries Research Board, 29, 1113–1118.CrossRefGoogle Scholar
Moritz, C., Dowling, T.E. & Brown, W.M., 1987. Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Annual Review of Ecology and Systematics, 18, 269–292.CrossRefGoogle Scholar
Nei, M., 1987. Molecular evolutionary genetics. New York: Columbia University Press.CrossRefGoogle Scholar
Nei, M. & Li, W.-H., 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings of the National Academy of Sciences of the United States of America, 76, 5269–5273.CrossRefGoogle ScholarPubMed
O'connell, M., 1993. Population genetics of Atlantic salmon in Wales. PhD thesis, University of Wales, Swansea, Wales.Google Scholar
Parrish, B.B. & Saville, A., 1965. The biology of the north-east Atlantic herring populations. Oceanography and Marine Biology. Annual Review, 3, 323–373.Google Scholar
Parrish, B.B. & Saville, A., 1967. Changes in the fisheries of North Sea and Atlanto-Scandian herring stocks and their causes. Oceanography and Marine Biology. Annual Review, 5, 409–47.Google Scholar
Raymond, M. & Rousset, F., 1995. GENEPOP (v. 1.2): A population genetics software for exact test and ecumenicism. Journal of Heredity, 86, 248–249.CrossRefGoogle Scholar
Reeb, C.A. & Avise, J.C., 1990. A genetic discontinuity in a continuously distributed species: mitochondrial DNA in the American oyster, Crassostrea virginica. Genetics, 124, 397–406.CrossRefGoogle Scholar
Rice, W.R., 1989. Analysing tables of statistical tests. Evolution, 43, 223–225.CrossRefGoogle Scholar
Roff, D.A. & Bentzen, P., 1989. The statistical analysis of mtDNA polymorphisms:x 2 and the problem of small samples. Molecular Biology and Evolution, 6, 539–545.Google Scholar
Runström, S., 1936. Investigations on Icelandic herrings in 1929–1935. Rapports Conseil pour l'Exploration de la Mer, 99, 1–11.Google Scholar
Ryman, N.U., Lagercrantz, L., Andersson, R., Chakraborty, R. & Rosenberg, R., 1984. Lack of correspondence between genetic and morphological variability patterns in Atlantic herring (Clupea harengus). Journal of Heredity, 53, 687–704.CrossRefGoogle Scholar
Sambrook, J., Fritsch, E.F. & Maniatis, T., 1989. Molecular cloning: a laboratory manual, 2nd ed. New York: Cold Spring Harbor Press.Google Scholar
Smith, P.J. & Jamieson, A., 1986. Stock discreteness in herrings: a conceptual revolution. Fisheries Research, 4, 223–234.CrossRefGoogle Scholar
Svetovidov, A.N., ed., 1963. Fauna of USSR Fishes. Vol. 2. Clupeidae. Jerusalem: Israel Programme for Scientific Translations.Google Scholar
Swofford, D.L. & Selander, R.B., 1989. BIOSYS-1. A computer program for the analyses of allelic variation in population genetics and biochemical systematics. Release 1.7.Google Scholar
Ward, R.D., Billington, N. & Hebert, P.D.N., 1989. Comparison of allozyme and mitochondrial variation in populations of walleye, Stizostedion vitreum. Canadian journal of Fisheries and Aquatic Sciences, 46, 2074–2084.CrossRefGoogle Scholar
Ward, R.D., Elliott, N.G., Grewe, P.M. & Smolenski, A.J., 1994. Allozyme and mitochondrial DNA variation in yellowfin tuna (Thunnus albacares) from the Pacific Ocean. Marine Biology, 118, 531–539.CrossRefGoogle Scholar
Ward, R.D. & Grewe, P., 1994. Appraisal of molecular genetic techniques in fisheries. Reviews in Fish Biology and Fisheries, 4, 300–325.CrossRefGoogle Scholar
Wright, J. & Bentzen, P., 1994. Microsatellites: genetic markers for the future. Reviews in Fish Biology and Fisheries, 4, 384–388.CrossRefGoogle Scholar