Marine Biology

, Volume 156, Issue 9, pp 1869–1880 | Cite as

Population differentiation in megrim (Lepidorhombus whiffiagonis) and four spotted megrim (Lepidorhombus boscii) across Atlantic and Mediterranean waters and implications for wild stock management

  • Delphine DanancherEmail author
  • Eva Garcia-Vazquez
Original Paper


Megrim, Lepidorhombus whiffiagonis, and four spot megrim, Lepidorhombus boscii, are two marine fish species of high commercial interest. Despite their quite heavy exploitation little is known on the genetic structure of their populations. The present work aimed at characterizing the first seven microsatellites markers available for the two megrim species. These new markers were in a second step employed to describe the population structure of the two species among their almost entire habitat range (Atlantic and Mediterranean samples). Our study confirmed the existence of a strong genetic difference between Atlantic and Mediterranean megrim species already described in the literature for L. whiffiagonis on the basis of variations at ribosomal genes. Additionally our analysis gave the first evidences of a strong genetic differentiation among Atlantic populations in both megrim species (within Atlantic global FST in L. whiffiagonis and L. boscii were respectively 0.158 and 0.145). When describing megrim population structure, the comparison between allele-frequency-based tests (FST comparisons) and genotype-based inferences (Bayesian approach) gave evidences of a hierarchical structure of the populations. In conclusion, our work enlighten the existence of two different stocks within the Atlantic Ocean and one in the Mediterranean Sea that will clearly need to be managed separately. As the present results do not fully support the current megrim stock boundaries they will surely help to rethink megrim management policies in the future.


Mediterranean Population Atlantic Population Population Genetic Differentiation Flatfish Species Genotypic Linkage Disequilibrium 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We are indebted to Francisco Sanchez (IEO at Santander, Spain), Paula Alvarez (AZTI at the Basque Country, Spain), Placida Lopes (IPIMAR at Lisbon, Portugal), for kindly providing biological samples in the context of the EU 5FP Research Project MARINEGGS. The RTD Asturian Regional Project FICYT IB-105 and the Central Directorate of Fisheries (Asturias, Spain) provided financial support for this study. We are also grateful to anonymous colleague for his welcome language corrections.


  1. Azevedo MFC, Oliveira C, Pardo BG, Martinez P, Foresti F (2008) Phylogenetic analysis of the order Pleuronectiformes (Teleostei) based on sequences 12S and 16S mitochondrial genes. Genet Mol Biol 31:284–292. doi: CrossRefGoogle Scholar
  2. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier (France).
  3. Blanquer A, Alayse JP, Berrada-Rkhami O, Berrebi R (1992) Allozyme variation in turbot (Psetta maxima) and brill (Scophthalmus rhombus) (Osteichthyes, Pleuronectiformes, Scophthalmidae) throughout their range in Europe. J Fish Biol 41:725–736. doi: CrossRefGoogle Scholar
  4. Bloor PA, Barker FS, Watts PC, Noyes HA, Kemp SJ (2001) Microsatellite libraries by enrichment version 1.0.
  5. Borsa P, Blanquer A, Berrebi P (1997a) Genetic structure of the flounders Platichtys flesus and P. stellatus at different geographic scales. Mar Biol (Berl) 129:233–246. doi: CrossRefGoogle Scholar
  6. Borsa P, Naciri M, Bahri L, Chikhi L, Garcia de Léon FJ, Kotoulas G, Bonhomme F (1997b) Zoogéographie infra-spécifique de la mer Méditerranée : analyse des données génétiques populationnelles sur seize espèces atlanto-méditerranéennes (Poissons et Invertébrés). Vie Milieu 47:295–305Google Scholar
  7. Bouza C, Presa P, Castro J, Sánchez L, Martínez P (2002) Allozyme and microsatellite diversity in natural and domestic populations of turbot (Scophthalmus maximus) in comparison with other Pleuronectiformes. Can J Fish Aquat Sci 59:1460–1473. doi: CrossRefGoogle Scholar
  8. Burrows MT, Gibson RN, Robb L, Maclean A (2004) Alongshore dispersal and site fidelity of juvenile plaice from tagging and transplants. J Fish Biol 65:620–634. doi: CrossRefGoogle Scholar
  9. Carvalho GR, Hauser L (1994) Molecular genetics and the stock concept in fisheries. Rev Fish Biol Fish 4:326–350CrossRefGoogle Scholar
  10. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evolut Int J Org Evolut 21:550–570. doi: CrossRefGoogle Scholar
  11. Coughlan JP, Imsland AK, Galvin PT, Fitzgerald RD, Naevdal G, Cross TF (1998) Microsatellite DNA variation in wild populations and farmed strains of turbot from Ireland and Norway: a preliminary study. J Fish Biol 52:916–922. doi: CrossRefGoogle Scholar
  12. Estoup A, Largiader CR, Perrot E, Chourrout D (1996) Rapid one-tube DNA extraction for reliable PCR detection of fish polymorphic marker and transgenes. Mol Mar Biol Biotechnol 5:295–298Google Scholar
  13. Evanno G, Regnault S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. doi: CrossRefGoogle Scholar
  14. Felsenstein J (1995) PHYLIP (Phylogeny Inference Package) Version 3.572. Department of Genetics, University of Washington, SeattleGoogle Scholar
  15. Gaggiotti OE, Lange O, Rassmann K, Gliddons C (1999) A comparison of two indirect methods for estimating average levels of gene flow using microsatellites data. Mol Ecol 8:1513–1520. doi: CrossRefGoogle Scholar
  16. Garcia de Léon FJ, Chikhi L, Bonhomme F (1997) Microsatellite polymorphism and population subdivision in natural populations of European sea bass Dicentrarchus labrax (Linnaeus, 1758). Mol Ecol 6:51–62. doi: CrossRefGoogle Scholar
  17. Garcia-Vazquez E, Izquierdo JI, Perez J (2006) Genetic variation at ribosomal genes supports the existence of two different European subspecies in the megrim Lepidorhombus whiffiagonis. J Sea Res 56:59–64. doi: CrossRefGoogle Scholar
  18. Goldstein DB, Schlötterer C (eds) (1999) Microsatellites: evolution and applications. Oxford University Press, OxfordGoogle Scholar
  19. Goldstein DB, Ruiz Linares A, Cavalli-Sforza LL, Feldman MW (1995) Genetic absolute dating based on microsatellites and the origin of modern humans. Proc Natl Acad Sci USA 92:6723–6727. doi: CrossRefGoogle Scholar
  20. Goudet J (1995) Fstat version 1.2: a computer program to calculate Fstatistics. J Hered 86:485–486CrossRefGoogle Scholar
  21. Goudet J, Raymond M, de Meeus T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940PubMedPubMedCentralGoogle Scholar
  22. 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 89:415–426. doi: CrossRefGoogle Scholar
  23. Harding D, Nichols JH, Tungate DS (1978) The spawning of the plaice (Pleuronectes platessa L.) in the southern North Sea and English Channel. Rapp P-V Reun Cons Int Explor Mer 172:102–113Google Scholar
  24. Hoarau G, Rijnsdorp AD, Van der Veer HW, Stam WT, Olsen JL (2002) Population structure of plaice (Pleuronectes platessa L.) in northern Europe: microsatellites revealed large-scale spatial and temporal homogeneity. Mol Ecol 11:1165–1176. doi: CrossRefGoogle Scholar
  25. Hoarau G, Piqueta AMT, van der Veerb HW, Rijnsdorpc AD, Stama WT, Olsena JL (2004) Population structure of plaice (Pleuronectes platessa L.) in northern Europe: a comparison of resolving power between microsatellites and mitochondrial DNA data. J Sea Res 51:183–190. doi: CrossRefGoogle Scholar
  26. Jennings S, Greenstreet SPR, Reynolds JD (1999) Structural change in an exploited fish community: a consequence of differential fishing effects on species with contrasting life histories. J Anim Ecol 68:617–627. doi: CrossRefGoogle Scholar
  27. Kinlan BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020. doi: CrossRefGoogle Scholar
  28. Landa J, Piñeiro C (2000) Megrim (Lepidorhombus whiffiagonis) growth in the north-eastern atlantic based on back-calculation of otolith rings. ICES J Mar Sci 57:1077–1090. doi: CrossRefGoogle Scholar
  29. Landa J, Perez N, Piñeiro C (2002) Growth patterns of the four spot megrim (Lepidorhombus boscii) in the northeast Atlantic. Fish Res 55:141–152. doi: CrossRefGoogle Scholar
  30. Langella O (2002) POPULATIONS, a free population genetics software. URL
  31. Lester SE, Ruttenberg BI (2005) The relationship between pelagic larval duration and range size in tropical reef fishes: a synthetic analysis. Proc R Soc B Biol Sci 272:585–591CrossRefGoogle Scholar
  32. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220Google Scholar
  33. Marques JF, Teixeira CM, Cabral HN (2006) Differentiation of commercially important flatfish populations along the Portuguese coast: evidence from morphology and parasitology. Fish Res 81:293–305. doi: CrossRefGoogle Scholar
  34. Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283. doi: CrossRefGoogle Scholar
  35. Nielsen EE, Nielsen PH, Meldrup D, Hansen MM (2004) Genetic population structure of turbot (Scophthalmus maximus L.) supports the presence of multiple hybrid zones for marine fishes in the transition zone between the Baltic Sea and the North Sea. Mol Ecol 13:585–595. doi: CrossRefGoogle Scholar
  36. Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358Google Scholar
  37. Palumbi SR (1994) Genetic divergence, reproductive isolation and marine speciation. Annu Rev Ecol Evol Syst 25:547–572CrossRefGoogle Scholar
  38. Pardo BG, Machordom A, Foresti F, Porto-Foresti F, Azevedo MFC, Banon R, Sanchez L, Martinez P (2005) Phylogenetic analysis of flatfish (order Pleuronectiformes) based on mitochondrial 16 s rDNA sequences. Sci Mar 69:531–543. doi: CrossRefGoogle Scholar
  39. Perez J, Alvarez P, Martinez JL, Garcia-Vazquez E (2005) Genetic identification of hake and megrim eggs in formaldehyde-fixed plankton samples. ICES J Mar Sci 62:908–914. doi: CrossRefGoogle Scholar
  40. Poulard JC, Peronnet I, Rivoalen JJ (1993) Depth and spatial distribution of Lepidorhombus whiffiagonis (Walbaum, 1792) by age group in the Celtic sea and Bay of Biscay. ICES CM 1993/G:43Google Scholar
  41. Pritchard JK, Stephens M, Donnelly P (2000) Inferences of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  42. Reid DP, Pongsomboon S, Jackson T, McGowan C, Murphy C, Martin-Robichaud D, Reith M (2005) Microsatellite analysis indicates an absence of population structure among Hippoglossus hippoglossus in the north-west Atlantic. J Fish Biol 67:570–576. doi: CrossRefGoogle Scholar
  43. Rice J, Cooper JA (2003) Management of flatfish fisheries: what factor matter? J Sea Res 50:227–243. doi: CrossRefGoogle Scholar
  44. Rolland JL, Bonhomme F, Lagardère F, Hassan M, Guinand B (2007) Population structure of the common sole (Solea solea) in the Northeastern Atlantic and Mediterranean Sea: revisiting the divide with EPIC Markers. Mar Biol (Berl) 151:27–341. doi: CrossRefGoogle Scholar
  45. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228PubMedPubMedCentralGoogle Scholar
  46. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  47. Sanchez F, Perez N, Landa J (1998) Distribution and abundance of megrim (Lepidorhombus boscii and Lepidorhombus wiffiagonis) on the northern Spanish shelf. ICES J Mar Sci 55:494–514. doi: CrossRefGoogle Scholar
  48. Sanjuan A, Comesaña AS (2002) Molecular identification of nine commercial flatfish species by polymerase chain reaction-restriction fragment length polymorphism analysis of a segment of the cytochrome b region. J Food Prot 65:1016–1023CrossRefGoogle Scholar
  49. Shanks AL, Grantham BA, Carr MH (2003) Propagule dispersal distance and the size and spacing of marine reserves. Ecol Appl 13(Supplement):S159–S169. doi:[0159:PDDATS]2.0.CO;2 CrossRefGoogle Scholar
  50. Shaw PW, Pierce GJ, Boyle PR (1999) Subtle population structuring within a highly vagile marine invertebrate, the veined squid Loligo forbesi, demonstrated with microsatellite DNA markers. Mol Ecol 8:407–417. doi: CrossRefGoogle Scholar
  51. Slatkin M (1995) A measure of population subdivision based on microsatellite allele unbiased estimates of genetic differentiation and determining their significance for microsatellite data. Mol Ecol 6:881–885Google Scholar
  52. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. doi: CrossRefGoogle Scholar
  53. Vassilopoulou V (2000) Abundance and distribution of four-spotted megrim (Lepidorhombus boscii) in the Aegean Sea. Belg J Zool 130:81–85Google Scholar
  54. Ward RD, Woodwark M, Skibinski DOF (1994) A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. J Fish Biol 44:213–232. doi: CrossRefGoogle Scholar
  55. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolut Int J Org Evolut 38:1358–1370. doi: Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Laboratoire d’Ecologie des Hydrosystèmes Fluviaux, équipe biodiversité des écosystèmes lotiquesUniversité de LyonVilleurbanne cedexFrance
  2. 2.Department of Functional BiologyUniversity of OviedoOviedoSpain

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