Abstract
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.
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References
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:https://doi.org/10.1590/S1415-47572008000200023
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).http://www.genetix.univ-montp2.fr/genetix/genetix.htm
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:https://doi.org/10.1111/j.1095-8649.1992.tb02702.x
Bloor PA, Barker FS, Watts PC, Noyes HA, Kemp SJ (2001) Microsatellite libraries by enrichment version 1.0. http://www.genomics.liv.ac.uk/animal/MICROSAT.PDF
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:https://doi.org/10.1007/s002270050164
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 47:295–305
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:https://doi.org/10.1139/f02-114
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:https://doi.org/10.1111/j.0022-1112.2004.00467.x
Carvalho GR, Hauser L (1994) Molecular genetics and the stock concept in fisheries. Rev Fish Biol Fish 4:326–350
Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evolut Int J Org Evolut 21:550–570. doi:https://doi.org/10.2307/2406616
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:https://doi.org/10.1111/j.1095-8649.1998.tb00592.x
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 5:295–298
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:https://doi.org/10.1111/j.1365-294X.2005.02553.x
Felsenstein J (1995) PHYLIP (Phylogeny Inference Package) Version 3.572. Department of Genetics, University of Washington, Seattle
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:https://doi.org/10.1046/j.1365-294x.1999.00730.x
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:https://doi.org/10.1046/j.1365-294X.1997.t01-1-00151.x
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:https://doi.org/10.1016/j.seares.2006.04.001
Goldstein DB, Schlötterer C (eds) (1999) Microsatellites: evolution and applications. Oxford University Press, Oxford
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:https://doi.org/10.1073/pnas.92.15.6723
Goudet J (1995) Fstat version 1.2: a computer program to calculate Fstatistics. J Hered 86:485–486
Goudet J, Raymond M, de Meeus T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940
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:https://doi.org/10.1093/jhered/89.5.415
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 172:102–113
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:https://doi.org/10.1046/j.1365-294X.2002.01515.x
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:https://doi.org/10.1016/jseares.2003.12.002
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:https://doi.org/10.1046/j.1365-2656.1999.00312.x
Kinlan BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020. doi:https://doi.org/10.1890/01-0622
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:https://doi.org/10.1006/jmsc.2000.0702
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:https://doi.org/10.1016/S0165-7836(01)00302-2
Langella O (2002) POPULATIONS, a free population genetics software. URL http://www.legs.cnrs-gif.fr
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 272:585–591
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
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:https://doi.org/10.1016/j.fishres.2006.05.021
Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283. doi:https://doi.org/10.1038/nature01610
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:https://doi.org/10.1046/j.1365-294X.2004.02097.x
Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
Palumbi SR (1994) Genetic divergence, reproductive isolation and marine speciation. Annu Rev Ecol Evol Syst 25:547–572
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:https://doi.org/10.3989/scimar.2005.69n4531
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:https://doi.org/10.1016/j.icesjms.2005.04.001
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:43
Pritchard JK, Stephens M, Donnelly P (2000) Inferences of population structure using multilocus genotype data. Genetics 155:945–959
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:https://doi.org/10.1111/j.0022-1112.2005.00733.x
Rice J, Cooper JA (2003) Management of flatfish fisheries: what factor matter? J Sea Res 50:227–243. doi:https://doi.org/10.1016/j.seares.2003.07.001
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:https://doi.org/10.1007/s00227-006-0484-0
Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
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:https://doi.org/10.1006/jmsc.1997.0279
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 65:1016–1023
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:https://doi.org/10.1890/1051-0761(2003)013[0159:PDDATS]2.0.CO;2
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:https://doi.org/10.1046/j.1365-294X.1999.00588.x
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 6:881–885
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:https://doi.org/10.1111/j.1471-8286.2004.00684.x
Vassilopoulou V (2000) Abundance and distribution of four-spotted megrim (Lepidorhombus boscii) in the Aegean Sea. Belg J Zool 130:81–85
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:https://doi.org/10.1111/j.1095-8649.1994.tb01200.x
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolut Int J Org Evolut 38:1358–1370. doi:https://doi.org/10.2307/2408641
Acknowledgments
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.
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Danancher, D., Garcia-Vazquez, E. Population differentiation in megrim (Lepidorhombus whiffiagonis) and four spotted megrim (Lepidorhombus boscii) across Atlantic and Mediterranean waters and implications for wild stock management. Mar Biol 156, 1869–1880 (2009). https://doi.org/10.1007/s00227-009-1219-9
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DOI: https://doi.org/10.1007/s00227-009-1219-9