Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-10T12:01:37.542Z Has data issue: false hasContentIssue false

Very high genetic fragmentation in a large marine fish, the meagre Argyrosomus regius (Sciaenidae, Perciformes) : impact of reproductive migration, oceanographic barriers and ecological factors

Published online by Cambridge University Press:  16 July 2012

Pierrick Haffray*
Affiliation:
SYSAAF, Station SCRIBE/INRA, Campus de Beaulieu, 35042 Rennes, France
Rachid Malha
Affiliation:
LABOGENA, INRA, Domaine de Vilvert, 78350 Jouy-en-Josas, France
Mahfoud Ould Taleb Sidi
Affiliation:
IMROP, BP 22, Nouadhibou, Mauritania
Nuno Prista
Affiliation:
Centro de Oceanografia, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal
Moshira Hassan
Affiliation:
Reef Check, Wachmannstr. 25, 28209 Bremen, Germany
Gérard Castelnaud
Affiliation:
IRSTEA (ex-CEMAGREF), 50 av. de Verdun, 33612 Cestas, France
Bilge Karahan-Nomm
Affiliation:
Ege University, Fisheries Faculty, Aquaculture Dep., 35100 Izmir, Turkey
Kutsal Gamsiz
Affiliation:
Ege University, Fisheries Faculty, Aquaculture Dep., 35100 Izmir, Turkey
Sherif Sadek
Affiliation:
FMD, BP 4, 17840 La Brée les Bains, France
Jean-Sébastien Bruant
Affiliation:
Les Poissons du Soleil, BP 10, 34540 Balaruc-les-Bains, France
Philippe Balma
Affiliation:
CNRS UMR 5554, Institut des Sciences de l’Evolution, Université de Montpellier II, 2 rue des Chantiers, 34200 Sète, France
François Bonhomme
Affiliation:
CNRS UMR 5554, Institut des Sciences de l’Evolution, Université de Montpellier II, 2 rue des Chantiers, 34200 Sète, France
*
a Corresponding author : haffray@rennes.inra.fr
Get access

Abstract

The meagre Argyrosomus regius is a large Sciaenid fish known to reproduce in the eastern Atlantic and Mediterranean Sea in just five distinct and restricted geographic areas: along the Mauritanian coast and at estuary openings (Gironde, Tagus, Guadalquivir and Nile). The biological traits of A. regius (high dispersal capabilities, high fecundity, long larval phase, overlapping generations, reproduction until 40 years of age) are, in principle, favourable to high gene flow, which should lead to genetic homogeneity over large geographic scales. Nevertheless, the high geographic distances between the few reproductive areas leads one ask whether there is genetic differentiation in this species. In the present study, the genetic differentiation of the wild A. regius was investigated across most of its natural range from the Atlantic Ocean (France, Portugal, Spain, Mauritania) to the Mediterranean Sea (Egypt, Turkey), using 11 microsatellite markers previously identified in another Sciaenid, the red drum Sciaenops ocellatus. At least two very distinct groups could be identified, separated by the Gibraltar Strait. Genetic divergences (FST values) were intermediate between the Atlantic samples (0.012–0.041), high between Egypt and the Atlantic (0.06–0.107) or Aegean Sea (0.081) and extremely high between the Aegean Sea and the Atlantic (0.098–0.168). A. regius exhibited a very high level of genetic differentiation rarely reported in marine fishes. These results also demonstrate the existence of a sixth independent spawning area in the Menderes delta (Turkey). Factors potentially involved in this very high genetic fragmentation are discussed, including physical barriers, glaciation pulses and biological traits.

Type
Research Article
Copyright
© EDP Sciences, IFREMER, IRD 2012

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

Alarcón, J.A., Magoulas, A., Georgakopoulos, T., Zouros, E., Alvarez, M.C., 2004, Genetic comparison of wild and cultivated European populations of the gilthead sea bream (Sparus aurata). Aquaculture 230, 6580. CrossRefGoogle Scholar
Archangi B., 2008, Levels and patterns of genetic diversity in wild and cultured populations of mulloway (Argyrosomus japonicus) using mitochondrial DNA and microsatellites. Thesis, School of Natural Resources Sciences, Brisbane, Queensland University of Technology.
Ball, A.O., Beal, M.G., Chapman, R.W., Sedberry, G.R., 2007, Population structure of red porgy, Pagrus pagrus, in the Atlantic Ocean. Mar. Biol. 150, 13211332. CrossRefGoogle Scholar
Bahri-Sfar, L., Lemaire, C., Ben Hassine, O.K., Bonhomme, F., 2000, Fragmentation of the sea bass populations in the western and eastern Mediterranean as revealed by microsatellites polymorphism. Proc. R. Soc. Lond. B 267, 929935. CrossRefGoogle Scholar
Bebars, M.L., Lassere, G., Lam Hoai, T., 1997, Analyse des captures des pêcheries marines et lagunaires d’Egypte en liaison avec la construction de haut barrage d’Assouan. Oceanol. Acta 20, 421436. Google Scholar
Belkhir K., Borsa P., Goudet J., Chikhi L., Bonhomme F., 2004, Genetix v4.05. Logiciel sous WindowsTM pour la génétique des populations. Laboratoire Génome et Populations, Univ. Montpellier 2, Montpellier.
Bianchi, C.N., Morri, C., 2000, Marine biodiversity of the Mediterranean Sea : situation, problems and prospects for future research. Mar. Pollut. Bull. 40, 367376. CrossRefGoogle Scholar
Bonhomme, F., Naciri, M., Barhi-Sfa, L., Lemaire, C., 2002, Analyse comparée de la structure génétique de deux espèces de poissons marins apparentés et sympatriques Dicentrarchus labrax et Dicentrarchus punctatus. C.R. Biol. 325, 213220. CrossRefGoogle Scholar
Borsa, P., Naciri, M., Bahri, M., Chikhi, L., Garcia de Leon, F.J., Kotoulas, G., Bonhomme, F., 1997, Zoogéographie infra-spécifique de la mer Méditerranée : analyse des données génétiques populationnelles sur seize espèces atlanto-méditerranéennes (poissons et invertébrés). Vie Milieu 47, 295305. Google Scholar
Chakroun, N., Ktari, M.H., Kamoun, M.N., 1982, Production de Sciaenidae (Poisson, Téléostéens) des côtes tunisiennes. Bull. Inst. Natl. Scient. Tech. Océanogr. Pêches, Salammbô 9, 121126. Google Scholar
Champagnat, C., Domain, F., 1978, Migrations des poissons démersaux le long des côtes ouest-africaines de 10 à 24° de latitude Nord. Cah. ORSTOM, Sér. Océanogr. 16, 239261. Google Scholar
Cisneros-Mata, M.A., Montemayor-López, G., Román-Rodriguez, M.J., 1995, Life history and conservation of Totoaba macdonaldi. Conserv. Biol. 9, 806814. CrossRefGoogle Scholar
Costa, M.J., 1986, Les poissons de l’estuaire du Tage. Cybium 10, 5775. Google Scholar
Crowley, T.J., 1981, Temperature and circulation changes in the eastern north Atlantic during the last 150,000 years : evidence from the planktonic foraminiferal record. Mar. Micropaleontol. 6, 97129. CrossRefGoogle Scholar
Dieuzeide, R., 1929, Les Sciaenidés des côtes algériennes. Bull. Stat. Aquic. Pêche Castiglione 1, 133161. Google Scholar
El-Hehyawi M.L.E., 1974, Changes in salinity and landing of six fish species in the shelf, North to the Nile Delta. Bull. Inst. Ocean. Fish. Cairo, 437–458.
Ergin M., Kadir S., Keskin S., Turhan-Akyüz N., Yaşar D., 2007, Late Quaternary climate and sea-level changes recorded in the sediment composition off the Büyük Menderes river delta (eastern Aegean Sea, Turkey). Quat. Int. 167–176.
Franklin, I.R., Frankham, R., 1998, How large must populations be to retain evolutionary potential? Anim. Conserv. 1, 6973. Google Scholar
Galarza, J.A., Carreras-Carbonell, J., Macpherson, E., Pascual, M., Roques, S., Turner, G.F., Rico, C., 2009, The influence of oceanographic fronts and early-life-history traits on connectivity among littoral fish species. Proc. Natl. Acad. Sci. 106, 14731478. CrossRefGoogle ScholarPubMed
Gold, J.R., Burridge, C.P., Turner, T.F., 2001, A modified stepping-stone model of population structure in red drum. Sciaenops ocellatus (Sciaenidae), from the northern Gulf of Mexico. Genetica 111, 305317. CrossRefGoogle Scholar
González-Wangüemert, M., Cánovas, F., Pérez-Ruzafa, A., Marcos, C., Alexandrino, P., 2010, Connectivity patterns inferred from the genetic structure of white seabream (Diplodus sargus L.). J. Exp. Mar. Biol. Ecol. 383, 2331. CrossRefGoogle Scholar
González-Quirós, R., del Árbol, J., García-Pacheco, M.M., Silva-García, A.J., Naranjo, J.M.Morales-Nin, B., 2011, Life-history of the meagre Argyrosomus regius in the Gulf of Cadiz (SW Iberian Peninsula). Fish. Res. 109, 140149. CrossRefGoogle Scholar
Goudet, J., 1995, Fstat version 1.2 : a computer program to calculate Fstatistics. J. Hered. 86, 485486. CrossRefGoogle Scholar
Gyllensten, U., 1985, The genetic structure of fish : differences in intraspecific distribution of biochemical genetic variation between marine, anadromous and freshwater species. J. Fish Biol. 26, 691699. CrossRefGoogle Scholar
Han, Z.Q., Gao, T.X., Zhuang, Z., Tang, Q.H., 2008, Genetic variation among white croaker populations. J. Ocean, Univ China. 7, 7276. CrossRefGoogle Scholar
Hedgecock D., 1994, Does variance in reproductive success limit effective population sizes of marine organisms? In : Beaumont A.R. (ed.), Genetics and evolution of aquatic organisms,Chapman and Hall, London, pp. 122–134.
Hedrick, P.W., 2005, Large variance in reproductive success and the Ne/N ratio. Evolution 59, 15961599. CrossRefGoogle ScholarPubMed
Hermas J., 1995, Contribution à l’étude la biologie du maigre Argyrosomus regius (Asso, 1801) débarqué au port d’Agadir. Univ. Ibnou Zohr, Faculté des Sciences Agadir, Thesis.
Kazanci, N., Dündar, S., Alçicek, M.C., Gürbüz, A., 2009, Quaternary deposit of the Büyük Menderes Braben in western Anatolia, Turkey : Implication for river capture and the longest Holocene estuary in the Aegean Sea. Mar. Geol. 264, 165176. CrossRefGoogle Scholar
Kotoulas, G., Mejuto, J., Antoniou, A., Kasapidis, P., Tserpes, G., Piccinetti, C., Peristeraki, P., García-Cortés, B., Oikonomaki, K., de la Serna, J.M., Magoulas, A., 2006, Global genetic structure of the swordfish (Xiphias gladius) as revealed by microsatellites DNA markers. Col. Vol. Sci. Pap. ICCAT, 61, 7988. Google Scholar
Lankford, T.E., Targett, T.E., Gaffney, P.M., 1999, Mitochondrial analysis of populations structure in Micropogonias undulates (Perciform, Sciaenidae). Fish. Bull. 97, 884990. Google Scholar
Liu, M., Sadovy de Mitcheson, Y., 2008, Profile of a fishery collapse : why mariculture failed to save the large yellow croaker. Fish Fish. 9, 219242. CrossRefGoogle Scholar
Maggio, T., Lo Brutto, S., Garoia, F., Tinti, F., Arculeo, M., 2009, Microsatellite analysis of red mullet Mullus barbatus (Perciformes, Mullidae) reveals the isolation of the Adriatic Basin in the Mediterranean Sea. ICES J. Mar. Sci. 66, 18831891. CrossRefGoogle Scholar
Morales-Nin, B., Geffen, A.J., Pérez-Mayol, S., Palmer, M., González-Quirós, R., Grau, A., 2012, Seasonal and ontogenic migrations of the meagre (Argyrosomus regius) determined by otolith geochemical signatures. Fish. Res. 127–128, 154155. CrossRefGoogle Scholar
Naciri, M., Lemaire, C., Borsa, P., Bonhomme, F., 1999, Genetic study of the Atlantic/Mediterranean transition in sea bass (Dicentrarchus labrax). J. Hered. 90, 591596. CrossRefGoogle Scholar
Nei, M., 1978, Estimation of average heretozygosity and genetic distance from a small number of individuals. Genetics 89, 583590. Google Scholar
Nielsen, E.E., Hansen, M.M., Ruzzante, D.E., Meldrup, D., Grønkjær, P., 2003, Evidence of a hybrid-zone in Atlantic cod (Gadus morhua) in the Baltic and the Danish Belt Sea, revealed by individual admixture analysis. Mol. Ecol. 12, 14971508. CrossRefGoogle Scholar
Nielsen, E.E., Hemmer-Hansen, J., Meldrup, D., Hansen, M.M., 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, 585595. CrossRefGoogle Scholar
Oczkowski, A., Nixon, S., 2008, Increasing nutrient concentrations and the rise and fall of coastal fishery; a review of data from the Nile Delta, Egypt. Estuar. Coast. Shelf Sci. 77, 309319. CrossRefGoogle Scholar
Patarnello, T., Volkaert, F.A.M.J., Castilho, R., 2007, Pillars of Hercules : is the Atlantic-Mediterranean transition a phylogeographical break? Mol. Ecol. 16, 44264444. Google Scholar
Prista N., Costa J.L., Costa M.J., Jones C.M., 2009, Age determination in meagre Argyrosomus regius. In : Ruano F., Campos A., Batista I., Falcão M., Brohueira M.J., Martins M.M., Martins R. (eds.), Relat. Cient. Téc. Inst. Invest. Pescas Mar. IPIMAR, Lisboa, Ser. Digital, 49.
Quéro, J.C., Vayne, J.J., 1987, Le maigre, Argyrosomus regius (Asso 1801) (Pisces, Perciforme, Sciaenidae) du golfe de Gascogne et des eaux plus septentrionales. Rev. Trav. Inst. Pêches Marit. 49, 3566. Google Scholar
Quéro, J.C., 1989a, Sur la piste des maigres Argyrosomus regius (Poisson, Sciaenidae) du golfe de Gascogne et de Mauritanie. Océanis 15, 161179. Google Scholar
Quéro, J.C., 1989b, Le maigre Argyrosomus regius (Asso 1801) (Poisson, Perciforme, Sciaenidae) en Méditerranée occidentale. Bull. Soc. Zool. France 114, 8189. Google Scholar
Renshaw, M.A., Saillant, E., Bradfield, C.S., Gold, J., 2006, Microsatellite multiplex panels for genetic studies of three species of marine fishes : red drum (Scianops ocellatus), red snapper (Lutjanus campechanus), and cobia (Rachycentron canadum). Aquaculture 253, 731735. CrossRefGoogle Scholar
Rice, W.R., 1989, Analyzing tables of statistical tests. Evolution 43, 223225. CrossRefGoogle ScholarPubMed
Ruzzante, D.E., 1997, A comparison of several measures of genetic distance and population structure with microsatellite data : bias and sampling variance. Can. J. Fish. Aquat. Sci. 55, 114. CrossRefGoogle Scholar
Sadek, S., Sabry, A.M., Asfoor, S.M., 2009, Meagre, a new candidate in Egyptian aquaculture. Aquac. Eur. 34, 1317. Google Scholar
Sadovy, Y., Cheung, W.L., 2003, Near extinction of a highly fecund fish : the one that nearly got away. Fish Fish. 4, 8699. CrossRefGoogle Scholar
Saillant, E., Renshaw, M.A., Gatlin III, D.M., Neill, W.H., Vega, R.R., Gold, J.R., 2009, An experimental assessment of genetic tagging and founder representation in hatchery-reared red drum (Sciaenops ocellatus) used in stock enhancement. J. Appl. Ichthyol. 25, 108113. CrossRefGoogle Scholar
Saitou, N., Nei, M., 1987, The neighbor-joining method : a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406425. Google Scholar
Sourget Q., Biais G., 2009, Ecologie, biologie et exploitationdu maigre du golfe de Gascogne. Rapp. final convention SMIDDEST-IFREMER-CNRS.
Tamura, K., Dudley, J., Nei, M., Kumar, S., 2007, MEGA4 : Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 15961599. CrossRefGoogle ScholarPubMed
Tixerant G., 1974, Contribution à l’étude de la biologie du maigre ou courbine Argyrosomus regius (Asso 1801) ( =  Sciaena aquila Lacép.) sur la côte mauritanienne. Thèse Université, Univ. Aix-Marseille.
Turner, T.F., Richardson, L.R., Gold, J.R., 1998, Polymorphic microsatellite DNA markers in red drum (Sciaenops ocellatus). Mol. Ecol. 7, 17711773. CrossRefGoogle Scholar
Turner, T.F., Wares, J.P., Gold, J.R., 2002, Genetic effective size is three orders of magnitude smaller than adult census size in an abundant, estuarine-dependent marine fish (Sciaenops ocellatus). Genetics 162, 13291339. Google Scholar
Van Oosterhout, C., Hutchinson, W.F., Derek, P., Wills, D.P.M., Shipley, P., 2004, MICRO-CHECKER : software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4, 535538. CrossRefGoogle Scholar
Waples, R.S., 2005, Genetic estimates of contemporary effective population size : to what time periods do the estimates apply? Mol. Ecol. 14, 33353352. Google Scholar
Waples, R.S., Do, C., 2008, LDNE : a program for estimating effective population size from data on linkage disequilibrium. Mol. Ecol. Res. 8, 753756. CrossRefGoogle ScholarPubMed
Ward, R.D., Woodwark, M., Skibinski, D.O.F., 1994, A comparison of genetic diversity levels in marine, freshwater and anadromous fishes. J. Fish Biol. 44, 213232. CrossRefGoogle Scholar
Ward R.D., Bowers K., Hensley R., Mobley B., Belouski E., 2007, Genetic variability in spotted seatrout (Cynoscion nebulosus), determined with microsatellite DNA markers Fish. Bull. 105–197.
Weir, B.S., Cockerham, C.C., 1984, Estimating F-statistics for the analysis of population structure. Evolution 38, 13581370. Google Scholar
Wilson, A.B., Veraguth, I.E., 2010, The impact of Pleistocene glaciation across the range of a widespread European coastal species. Mol. Ecol. 19, 45354553. CrossRefGoogle Scholar
Xiao, Y., Zhang, Y., Gao, K., Yanagimoto, T., Yabe, M., Sakurai, Y., 2009, Genetic diversity in the mtDNA control region and population structure in the small yellow croaker Larimichthys polyactis. Environ. Biol. Fishes 85, 303314. CrossRefGoogle Scholar