Temporal and spatial genetic variation in spawning grounds of European hake (Merluccius merluccius) in the Bay of Biscay

Polymorphism at five microsatellite loci were screened to determine the genetic variability and the temporal stability of population structure in natural populations of European hake (Merluccius merluccius, L.) within the Bay of Biscay. In addition, the control region (900 bp) and two protein coding genes (ATPase, subunits 6 and 8, 842 bp and a partial sequence of the ND1, 800 bp) of the mitochondrial DNA (mtDNA) were sequenced from geographically distant populations from the extremes of the species range. One hundred individuals from either side of a supposed stock boundary within the bay were collected in autumn 1997. This sampling strategy was repeated during hake spawning seasons in late spring of 1998 and 1999. Low levels of population subdivision were found between putative populations within years. Similarly, low levels of differentiation were found between autumn 1997 northern samples and spring 1998 southern samples which were collected 7 months later on spawning grounds. These results are discussed in relation to ecological, behavioural and oceanographic information. Sampling effects, which may influence these results, are also discussed. Theta (θ) estimates were significantly different from zero in every other pairwise comparison between geographical areas (north and south of the Bay of Biscay) and between years within the same area (P < 0.05). Hierarchical analysis of molecular variance (amova) does not confirm the temporal persistence of population structure. These results are discussed in relation to variance in reproductive success, and temporal spawning patterns, which may exist within the bay. mtDNA variability was very low between geographically distant samples from Norway and the Mediterranean Sea with only 10 variable sites found in a total of 2542 bp of mtDNA, these differences being exclusively in the d‐loop.

[1]  P. Cury.  Obstinate Nature: An Ecology of Individuals. Thoughts on Reproductive Behavior and Biodiversity , 1994 .

[2]  P. W. Webb,et al.  The energetics of migration by selective tidal stream transport: an analysis for plaice tracked in the southern North Sea , 1990, Journal of the Marine Biological Association of the United Kingdom.

[3]  L. Bernatchez,et al.  Ecological determinants and temporal stability of the within‐river population structure in Atlantic salmon (Salmo salar L.) * , 2000, Molecular ecology.

[4]  J. Castilla,et al.  The management of fisheries and marine ecosystems , 1997 .

[5]  T. Pitcher,et al.  Electrophoretic analysis of stock structure in Northern Mediterranean anchovies, Engraulis encrasicolus , 1996 .

[6]  D. Ruzzante,et al.  A nuclear DNA basis for shelf‐ and bank‐scale population structure in northwest Atlantic cod (Gadus morhua): Labrador to Georges Bank , 1998 .

[7]  M Slatkin,et al.  A measure of population subdivision based on microsatellite allele frequencies. , 1995, Genetics.

[8]  M. Dickey‐Collas,et al.  Does the western Irish Sea gyre influence the distribution of pelagic juvenile fish , 1997 .

[9]  B. Weir,et al.  ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE , 1984, Evolution; international journal of organic evolution.

[10]  François Rousset,et al.  GENEPOP (version 1.2): population genetic software for exact tests and ecumenicism , 1995 .

[11]  J. Avise.  Conservation genetics in the marine realm , 1998 .

[12]  S. Johansen,et al.  The complete mitochondrial DNA sequence of Atlantic cod (Gadus morhua): relevance to taxonomic studies among codfishes. , 1996, Molecular marine biology and biotechnology.

[13]  G. Hewitt,et al.  Isolation and characterization of microsatellite loci in European hake, Merlucius merlucius (Merlucidae, Teleostei) , 1999, Molecular ecology.

[14]  J. G..  The Hake and the Hake Fishery: , 1935, Nature.

[15]  D. Hedgecock,et al.  Genetic heterogeneity, detected by PCR-SSCP, among samples of larval Pacific oysters (Crassostrea gigas) supports the hypothesis of large variance in reproductive success , 1998 .

[16]  E. Thompson,et al.  Performing the exact test of Hardy-Weinberg proportion for multiple alleles. , 1992, Biometrics.

[17]  W. Rice.  ANALYZING TABLES OF STATISTICAL TESTS , 1989, Evolution; international journal of organic evolution.

[18]  G. Hewitt,et al.  Stock composition in North Atlantic populations of whiting using microsatellite markers , 1997 .

[19]  P. J. Smith,et al.  Stock discreteness in herrings: A conceptual revolution , 1986 .

[20]  G. Hewitt,et al.  Macrogeographical population differentiation in oceanic environments: a case study of European hake (Merluccius merluccius), a commercially important fish , 1999, Molecular ecology.

[21]  D. O. Evans,et al.  The Stock Concept, Discreteness of Fish Stocks, and Fisheries Management , 1981 .

[22]  H. Lessios,et al.  Massive gene flow across the world's most potent marine biogeographic barrier , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[23]  F. Bonhomme,et al.  Low genetic variability in a widely distributed and abundant clupeid species, Sardinella aurita. New empirical results and interpretations , 1998 .

[24]  D. Skagen,et al.  Phylogeography and population history of Atlantic mackerel (Scomber scombrus L.): a genealogical approach reveals genetic structuring among the eastern Atlantic stocks , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[25]  P. J. Smith,et al.  Electrophoretic studies and the stock concept in marine teleosts , 1990 .

[26]  T. Pitcher,et al.  What makes a hake? A review of the critical biological features that sustain global hake fisheries , 1995 .

[27]  L. Excoffier,et al.  Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. , 1992, Genetics.

[28]  D. H. Cushing,et al.  Plankton Production and Year-class Strength in Fish Populations: an Update of the Match/Mismatch Hypothesis , 1990 .

[29]  E. Nielsen,et al.  Improved primer sequences for the mitochondrial ND1, ND3/4 and ND5/6 segments in salmonid fishes : application to RFLP analysis of Atlantic salmon , 1998 .

[30]  J. Casey,et al.  European hake (M. merluccius) in the North-east Atlantic , 1995 .

[31]  M. Sinclair,et al.  Atlantic Herring: Stock Discreteness and Abundance , 1982, Science.

[32]  J. Ovenden.  Mitochondrial DNA and marine stock assessment: A review , 1990 .

[33]  S. Palumbi.  Genetic Divergence, Reproductive Isolation, and Marine Speciation , 1994 .

[34]  S. Goodman,et al.  RST Calc: a collection of computer programs for calculating estimates of genetic differentiation from microsatellite data and determining their significance , 1997 .

[35]  B. Bowen,et al.  Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation , 1998 .

[36]  L. R. Richardson,et al.  Mitochondrial DNA diversification and population structure in fishes from the Gulf of Mexico and Western Atlantic , 1998 .

[37]  C. Moritz.  Defining 'Evolutionarily Significant Units' for conservation. , 1994, Trends in ecology & evolution.

[38]  M Raymond,et al.  Testing differentiation in diploid populations. , 1996, Genetics.

[39]  J M Cornuet,et al.  Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. , 1996, Genetics.

[40]  G. Turner,et al.  Isolation and characterization of microsatellite loci in the cichlid fish Pseudotropheus zebra , 1997, Molecular ecology.

[41]  P. Stabeno,et al.  The role of larval retention and transport features in mortality and potential gene flow of walleye pollock , 1997 .

[42]  J. Avise.  Introduction : the scope of conservation genetics , 1996 .

[43]  S. Wright,et al.  Genetical Structure of Populations , 1950, Nature.

[44]  F. Bonhomme,et al.  Microsatellite polymorphism and population subdivision in natural populations of European sea bass Dicentrarchus labrax (Linnaeus, 1758) , 1997 .

[45]  J. M. McGlade,et al.  Stock Identification: Materials and Methods , 1981 .

[46]  R. Waples.  Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species , 1998 .

[47]  D. Ruzzante,et al.  Spatial and temporal variation in the genetic composition of a larval cod (Gadus morhua) aggregation: Cohort contribution and genetic stability , 1996 .

[48]  P. Hedrick.  PERSPECTIVE: HIGHLY VARIABLE LOCI AND THEIR INTERPRETATION IN EVOLUTION AND CONSERVATION , 1999, Evolution; international journal of organic evolution.

[49]  Marshall,et al.  Calcium regulation in the freshwater-adapted mummichog , 1997, Journal of fish biology.

[50]  L. Bernatchez,et al.  Stability of population structure and genetic diversity across generations assessed by microsatellites among sympatric populations of landlocked Atlantic salmon (Salmo salar L.) , 1999 .

[51]  J. García-Marín,et al.  Genetic structure of the European anchovy, Engraulis encrasicolus l., in the north-west Mediterranean , 1999 .

[52]  G. Carvalho,et al.  Microsatellite DNA analysis of population structure in Atlantic herring (Clupea harengus), with direct comparison to allozyme and mtDNA RFLP analyses , 1999, Heredity.

[53]  M. Sinclair,et al.  Population richness of marine fish species , 1988 .

[54]  G. Shields,et al.  Lack of geographic structure in mitochondrial DNA sequences of Bering Sea walleye pollock, Theragra chalcogramma. , 1995, Molecular marine biology and biotechnology.

[55]  G. Carvalho,et al.  Advances in the molecular analysis of fish population structure , 1998 .

[56]  F. Bonhomme,et al.  Genetic study of the Atlantic/Mediterranean transition in sea bass (Dicentrarchus labrax) , 1999 .

[57]  L. Bernatchez,et al.  DNA sequence variation of the mitochondrial control region among geographically and morphologically remote European brown trout Saltno trutta populations , 1992, Molecular ecology.