Summary
The Atlantic herring (Clupea harengus) stock complex is confusing from the perspectives of both evolutionary biology and systematics. There are numerous ecologically and morphologically divergent stocks classified as species, subspecies, races, tribes, etc. with an unknown degree of genetic differentiation and reproductive isolation between them. The genetic population structure of herring from the Scandinavian waters was analysed electrophoretically. The pattern for distribution of genetic variation was compared to that of the morphological characters most frequently used for stock classification, i.e., the number of vertebrae and keeled scales.
Fish were collected from 17 locations distributed from the northern Gulf of Bothnia to the north-east Atlantic off the west coast of Norway. The genetic analysis was based on 17 electrophoretic loci, 13 of which were variable. There are statistically significant allele frequency heterogeneities, but there is a conspicuously small amount of genetic differentiation, even between stocks classified as representing different subspecies. More than 99 per cent of the total gene diversity was found within populations, and genetic distances are typically of the order of 0ยท001. The genotypic distribution of the total material is very similar to the one expected if all the samples had been drawn from a single panmictic population. There appears to be no association between the variation of morphological characters and that at electrophoretic loci, and this is true for the variation between as well as within samples. Data suggest that stocks either diverged rather recently or that the amount of gene flow between groups of fish classified as stocks has been large enough to prevent substantial differentiation, and that morphologic and ecologic divergence may to a large extent be environmentally induced.
Similar content being viewed by others
Article PDF
References
Ackefors, H. 1977a. The meristic characters and the maturity cycle of the Skagerrak spring spawners. Medd Havsfiskelab, Lysekil, 227, 12 p.
Ackefors, H. 1977b. The life-cycle of Kattegat spring spawners in relation to growth rate, the development of gonads and the fat content. Medd Havsfiskelab, Lysekil, 228, 7 p.
Andersson, L, Ryman, N, Rosenberg, R, and Stรฅhl, G. 1981. Genetic variability in Atlantic herring (Clupea harengus harengus): description of protein loci and population data. Hereditas, 95, 69โ78.
Aneer, G. 1979. On the ecology of the Baltic herring with special reference to the Askรถ-Landsort area. Ph.D. thesis Univ. Stockholm, Sweden.
Anokhina, L. 1971. Maturation of Baltic and White Sea herring with special reference to variations in fecundity and egg diameter. Rapp Cons Explor Mer, 160, 12โ17.
Blaxter, J H S. 1958. The racial problem in Herring from the viewpoint of recent physiological, evolutionary, and genetical theory. Rapp Cons Explor Mer, 143, 10โ19.
Bรผckman, A, and Parrish, B B. 1958. Conclusions reached at special scientific meeting on โHerring racesโ held at Charlottenlund on 25โ27 September 1956. Rapp Cons Explor Mer, 143, 8โ9.
Chakraborty, R. 1980. Gene diversity analysis in nested subdivided populations. Genetics, 96, 721โ726.
Chakraborty, R. 1981. The distribution of the number of heterozygous loci in an individual in natural populations. Genetics, 98, 461โ466.
Chakraborty, R, Fuerst, P A, and Nei, M. 1980. Statistical studies on protein polymorphism in natural populations. III. Distribution of allele frequencies and the number of alleles per locus. Genetics, 94, 1039โ1063.
Chakraborty, R, Haag, M, Ryman, N, and Stahl, G. 1982. Hierarchical gene diversity analysis and its application to brown trout population data. Hereditas, 97, 17โ21.
Chakraborty, R, and Ryman, N. 1983. Relationship of mean and variance of genotypic values with heterozygosity per individual in a natural population. Genetics, 103, 149โ152.
Emigh, T H. 1980. A comparison of tests for Hardy-Weinberg equilibrium. Biometrics, 36, 627โ642.
Endler, J A. 1977. Geographic variation, speciation, and clines Princeton Univ. Press, Princeton, New Jersey.
Felsenstein, J. 1982. Numerical methods for inferring evolutionary trees. The Quarterly Review of Biology, 57, 379โ404.
Gartner-Kepkay, K E, Zouros, E, Dickie, L M, and Freeman, K R. 1983. Genetic differentiation in the face of gene flow: a study of mussel populations from a single Nova Scotian embayment. Can J Fish Aquat Sci, 40, 443โ451.
Grant, W S. 1981. Biochemical genetic variation, population structures, and evolution of Atlantic and Pacific herring. Ph.D. thesis Univ. Washington, Seattle, USA.
Heincke, F. 1898. Naturgeschichte des Herings. Teil I. Die Lokalformen und die Wanderungen des Herings in den Europรคischen Meeren. Abh dtsch Seefisch Ver, 2.
Hempel, G, and Blaxter, J H. 1961. The experimental modification of meristic characters in herring (Clupea harengus L.). Rapp Cons Explor Mer, 26, 336โ346.
Hill, W G. 1974. Estimation of linkage disequilibrium in randomly mating populations. Heredity, 33, 229โ239.
Ihssen, P E, Booke, H E, Casselman, J M, McGlade, J M, Payne, N R, and Utter, F M. 1981. Stock identification: materials and methods. Can J Fish Aquat Sci, 38, 1838โ1855.
Iles, T D, and Sinclair, M. 1982. Atlantic herring: stock discreteness and abundance. Science, 215, 627โ633.
Koehn, R K, Newell, R I E, and Immerman, F. 1980. Maintenance of an aminopeptidase allele frequency cline by natural selection. Proc Natl Acad Sci, 77, 5385โ5389.
Kornfield, I, Gagnon, P S, and Sidell, B D. 1981. Inheritance of allozymes in Atlantic herring (Clupea harengus harengus). Can J Genet Cytol, 23, 715โ720.
Kornfield, I, Sidell, B D, and Gagnon, P S. 1982a. Stock definition in Atlantic herring (Clupea harengus harengus): genetic evidence for discrete fall and spring spawning populations. Can J Fish Aquat Sci, 39, 1610โ1621.
Kornfield, I, Smith, D C, Gagnon, P S, and Taylor, J N. 1982b. The Cichlid fish of Cuatro Ciรฉnegas, Mexico: direct evidence of conspecificity among distinct trophic morphs. Evolution, 36, 658โ664.
McAndrew, B J, Ward, R D, and Beardmore, J A. 1982. Lack of relationship between morphological variance and enzyme heterozygosity in the plaice, Pleuronectes platessa. Heredity, 48, 117โ125.
Nei, M. 1973. Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci, 70, 3321โ3323.
Nei, M. 1975. Molecular population genetics and evolution North-Holland, Amsterdam.
Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89, 583โ590.
Nei, M, and Li, W-H. 1973. Linkage disequilibrium in subdivided populations. Genetics, 75, 213โ219.
Nevo, E. 1978. Genetic variation in natural populations: patterns and theory. Theor Popul Biol, 13, 121โ177.
Parrish, B B, and Saville, A. 1965. The biology of the north-east Atlantic herring populations. Oceanogr Mar Biol Ann Rev, 3, 323โ373.
Petursson, P M, and Rosenberg, R. 1982. Maturity and growth of the spring spawning herring in the Kattegat-Skagerrak. Ophelia, 21, 195โ204.
Rosenberg, R, and Palmรฉn, L E. 1982. Composition of herring stocks in the Skagerrak-Kattegat and the relations of these stocks with those of the North Sea and adjacent waters. Fish Res, 1, 83โ104.
Slatkin, M. 1981. Estimating levels of gene flow in natural populations. Genetics, 99, 323โ335.
Sneath, P H, and Sokal, R R. 1973. Numerical taxonomy W. H. Freeman and Co., San Francisco.
Sokal, R R, and Rohlf, F J. 1981. Biometry, 2nd ed. W. H. Freeman and Co., San Francisco.
Svรคrdson, G. 1966. Young sibling fish species in northwestern Europe, P. 498โ513. In W. F. Blair (ed.), Vertebrate speciation Univ. Texas Press, Austin.
Turner, B J, and Grosse, D J. 1980. Trophic differentiation in Ilyodon, a genus of stream-dwelling goodeid fishes: speciation versus ecological polymorphism. Evolution, 34, 259โ270.
Utter, F M. 1981. Biological criteria for definition of species and distinct intraspecific populations of anadromous salmonids under the U.S. Endangered Species Act of 1973 Can. J Fish Aquat Sci, 38, 1626โ1635.
Vithayasai, C. 1973. Exact critical values of the Hardy-Weinberg test statistic for two alleles. Commun, in Stat, 1, 229โ242.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Ryman, N., Lagercrantz, U., Andersson, L. et al. Lack of correspondence between genetic and morphologic variability patterns in Atlantic herring (Clupea harengus). Heredity 53, 687โ704 (1984). https://doi.org/10.1038/hdy.1984.127
Received:
Issue Date:
DOI: https://doi.org/10.1038/hdy.1984.127
This article is cited by
-
The life aquatic: advances in marine vertebrate genomics
Nature Reviews Genetics (2016)
-
Introgressive hybridization between the Atlantic and Pacific herrings (Clupea harengus and C. pallasii) in the north of Europe
Marine Biology (2015)
-
RETRACTED ARTICLE: Advancements in morphometric differentiation: a review on stock identification among fish populations
Reviews in Fish Biology and Fisheries (2013)
-
Detecting population structure in a high gene-flow species, Atlantic herring (Clupea harengus): direct, simultaneous evaluation of neutral vs putatively selected loci
Heredity (2011)
-
Identification of subpopulations in pelagic marine fish species using amino acid composition
Hydrobiologia (2011)