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Population genetics of Cerastoderma edule in Ria Formosa (southern Portugal): the challenge of understanding an intraspecific hotspot of genetic diversity

Published online by Cambridge University Press:  07 October 2014

Carlos Vergara-Chen ,
Fernanda Rodrigues  and
Mercedes González-Wangüemert
Carlos Vergara-Chen*
Affiliation:
Instituto de Investigaciones Científicas y Servicios de Alta Tecnología (INDICASAT-AIP), Apartado 0843-01103 Panamá, Panamá
Fernanda Rodrigues
Affiliation:
Übersee-Museum Bremen, Bahnhofsplatz 13, 28195 Bremen, Germany
Mercedes González-Wangüemert
Affiliation:
Centro de Ciências do Mar (CCMAR), Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal
*
Correspondence should be addressed to: C. Vergara-Chen, Instituto de Investigaciones Científicas y Servicios de Alta Tecnología (INDICASAT-AIP), Apartado 0843-01103 Panamá, Panamá email: [email protected]
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Abstract

Coastal lagoons are highly variable environments that may act as hotspots of genetic diversity as a consequence of their ecological role as nursery habitats of marine species with both ecological and fisheries importance. The edible cockle (Cerastoderma edule) is a commercially important shellfish resource inhabiting coastal lagoons in Europe and their fisheries management urgently needs genetic studies to design appropriate strategies to promote the recovery of exploited populations. The aim of this study was to assess the C. edule genetic diversity and population structure at a small geographic scale, inside Ria Formosa coastal lagoon (southern Portugal) using mitochondrial cytochrome oxidase I sequences in six locations. Outcomes pointed to a common pattern of high haplotype diversity and non-significant genetic structuring inside the Ria Formosa lagoon. A high level of gene flow was detected between all localities and the presence of a single stock from a genetic point of view may be considered for fisheries management purposes. The existence of a high number of haplotypes and high values of haplotype diversity of C. edule in Ria Formosa lagoon could be consistent with the hypothesis that higher genetic diversity is expected in populations occurring in coastal lagoons, suggesting that lagoons could increase standing genetic variation and an adaptive potential of lagoon populations as an ecological response to a highly variable environment.

Keywords

connectivitygene flowshellfishtransitional coastal watersstock
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 95 , Issue 2 , March 2015 , pp. 371 - 379
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

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References

REFERENCES

Abbiati, M. and Maltagliati, F. (1992) Genetic population structure of Neanthes succinea (Polychaeta: Nereididae). Journal of the Marine Biological Association of the United Kingdom 72, 511–517.CrossRefGoogle Scholar
Águas, M. (1986) Simulação da circulação hidrodinâmica na Ria Formosa. Os sistemas lagunares do Algarve. Faro: Universidade do Algarve, pp. 78–90.Google Scholar
Aguirre, J.D. and Marshall, D.J. (2012) Genetic diversity increases population productivity in a sessile marine invertebrate. Ecology 93, 1134–1142.CrossRefGoogle Scholar
Allendorf, F.W., England, P.R., Luikart, G., Ritchie, P.A. and Ryman, N. (2008) Genetic effects of harvest on wild animal populations. Trends in Ecology and Evolution 23, 327–337.CrossRefGoogle ScholarPubMed
Angeletti, D., Cimmaruta, R. and Nascetti, G. (2010) Genetic diversity of the killifish Aphanius fasciatus paralleling the environmental changes of Tarquinia Salterns habitat. Genetica 138, 1011–1021.CrossRefGoogle ScholarPubMed
Arnaud-Haond, S., Vonau, V., Rouxel, C., Bonhomme, F., Prou, J., Goyard, E. and Boudry, P. (2008) Genetic structure at different spatial scales in the pearl oyster (Pinctada margaritifera cumingii) in French Polynesian lagoons: beware of sampling strategy and genetic patchiness. Marine Biology 155, 147–157.CrossRefGoogle Scholar
Avise, J.C. (2000). Phylogeography: the history and formation of species. Cambridge, MA: Harvard University Press.CrossRefGoogle Scholar
Avise, J.C., Neigel, J.E. and Arnold, J. (1984) Demographic influences on mitochondrial DNA lineage survivorship in animal populations. Journal of Molecular Evolution 20, 99–105.CrossRefGoogle ScholarPubMed
Barnes, R.S.K. (1980) Coastal lagoons. Cambridge: Cambridge University Press.Google Scholar
Beaumont, A.R. and Pether, S.M.J. (1996) Allozyme variation and gene flow between cockle Cerastoderma edule populations in southern United Kingdom. Fisheries Research 28, 263–275.CrossRefGoogle Scholar
Beaumont, A.R., Day, T.R. and Gade, G. (1980) Genetic variation at the octopine dehydrogenase locus in the adductor muscle of Cerastoderma edule (L) and 6 other bivalve species. Marine Biology Letters 1, 137–148.Google Scholar
Becquet, V., Lasota, R., Pante, E., Sokolowski, A., Wolowicz, M. and Garcia, P. (2013) Effects of fine-scale environmental heterogeneity on local genetic structure in Macoma balthica from the Gulf of Gdañsk (southern Baltic Sea). Hydrobiologia 714, 61–70.CrossRefGoogle Scholar
Beer, N.A. and Joyce, C.B. (2013) North Atlantic coastal lagoons: conservation, management and research challenges in the twenty-first century. Hydrobiologia 701, 1–11.CrossRefGoogle Scholar
Beverton, R.J.H. (1990) Small marine pelagic fish and the threat of fishing – are they endangered? Journal of Fish Biology 37(Suppl. A), 5–16.CrossRefGoogle Scholar
Bezuidenhout, K., Nel, R. and Hauser, L. (2014) Demographic history, marker variability and genetic differentiation in sandy beach fauna: what is the meaning of low FSTs? Estuarine, Coastal and Shelf Science. doi: 10.1016/j.ecss.2014.03.009.CrossRefGoogle Scholar
Canestrelli, D., Aloise, G., Cecchetti, S. and Nascetti, G. (2010) Birth of a hotspot of intraspecific genetic diversity: notes from the underground. Molecular Ecology 19, 5432–5451.CrossRefGoogle ScholarPubMed
Canu, D.M., Solidoro, C., Umgiesser, G., Cucco, A. and Ferrarin, C. (2012) Assessing confinement in coastal lagoons. Marine Pollution Bulletin 64, 2391–2398.CrossRefGoogle ScholarPubMed
Casu, M., Maltagliati, F., Cossu, P., Lai, T., Curini Galletti, M., Castelli, A. and Commito, J.A. (2005) Fine-grained spatial genetic structure in the bivalve Gemma gemma from Maine and Virginia (USA), as revealed by Inter-Simple Sequence Repeat markers. Journal of Experimental Marine Biology and Ecology 325, 46–54.CrossRefGoogle Scholar
Chícharo, L. and Chícharo, M.A. (2001) Effects of environmental conditions on planktonic abundances, benthic recruitment and growth rates of the bivalve mollusc Ruditapes decussatus in a Portuguese coastal lagoon. Fisheries Research 53, 235–250.CrossRefGoogle Scholar
Chust, G., Albaina, A., Aranburu, A., Borja, Á., Diekmann, O.E., Estonba, A., Franco, J., Garmendia, J.M., Iriondo, M., Muxika, I., Rendo, F., Rodríguez, J.G., Ruiz-Larrañaga, O., Serrão, E.A. and Valle, M. (2013) Connectivity, neutral theories and the assessment of species vulnerability to global change in temperate estuaries. Estuarine, Coastal and Shelf Science 131, 52–63.CrossRefGoogle Scholar
Cimmaruta, R., Angeletti, D., Pontremolesi, A. and Nascetti, G. (2011) Low microsatellite variation in Aphanius fasciatus from the Tarquinia Salterns. Transitional Waters Bulletin 4, 83–93.Google Scholar
Clement, M., Posada, D. and Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.CrossRefGoogle ScholarPubMed
Coscia, I., Robins, P.E., Porter, J.S., Malham, S.K. and Ironside, J.E. (2013) Modelled larval dispersal and measured gene flow: seascape genetics of the common cockle Cerastoderma edule in the southern Irish Sea. Conservation Genetics 14, 451–466.CrossRefGoogle Scholar
Crawford, K.M. and Whitney, K.D. 2010. Population genetic diversity influences colonization success. Molecular Ecology 19, 1253–1263.CrossRefGoogle ScholarPubMed
Dabouineau, L. and Ponsero, A. (2009) Synthesis on biology of common European cockle Cerastoderma edule. 2nd edition. Hillion: Université Catholique de l'Ouest-Réserve Naturelle Nationale Baie de St-Brieuc.Google Scholar
Dare, P.J., Bell, M.C., Walker, P. and Bannister, R.C.A. (2004). Historical and current status of cockle and mussel stocks in The Wash. Lowestoft: CEFAS, pp. 85.Google Scholar
Dodson, J.J., Tremblay, S., Colombani, F., Carscadden, J.E. and Lecomte, F. (2007) Trans-Arctic dispersals and the evolution of a circumpolar marine fish species complex, the capelin (Mallotus villosus). Molecular Ecology 16, 5030–5043.CrossRefGoogle ScholarPubMed
Excoffier, L. and Lischer, H.E. (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.CrossRefGoogle ScholarPubMed
Falcão, M. and Vale, C. (1990) Study of the Ria Formosa ecosystem: benthic nutrient remineralization and tidal variability of nutrients in the water. Hydrobiologia 207, 137–146.CrossRefGoogle Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Fu, Y.-X. (1997) Statistical test of neutrality of mutation against population growth, hitchhiking and background selection. Genetics 147, 915–925.CrossRefGoogle Scholar
Gamfeldt, L. and Källström, B. (2007) Increasing intraspecific diversity increases predictability in population survival in the face of perturbations. Oikos 116, 700–705.Google Scholar
Gamito, S., Gilabert, S., Marcos, C. and Pérez-Ruzafa, A. (2005) Effects of changing environmental conditions on lagoon ecology. In Gönenç, I.E. and Wolflin, J.P. (eds) Coastal lagoons: ecosystem processes and modeling for sustainable use and development. Boca Raton, FL: CRC Press, pp. 193–229.Google Scholar
Garant, D., Forde, S.E. and Hendry, A.P. (2007) The multifarious effects of dispersal and gene flow on contemporary adaptation. Functional Ecology 21, 434–443.CrossRefGoogle Scholar
Garrido, J., Pe'rez-Bilbao, A. and Benetti, C.J. (2011) Biodiversity and conservation of coastal lagoons. In Grillo, O. (ed.). Ecosystems biodiversity. InTech. Available from: http://www.intechopen.com/books/ecosystems-biodiversity/biodiversity-and-conservation-ofcoastal-lagoons.Google Scholar
Gharbi, A., Chatti, N., Said, K. and Van Wormhoudt, A. (2010). Genetic variation and population structure of the carpet shell clam Ruditapes decussatus along the Tunisian coast inferred from mtDNA and ITS1 sequence analysis. Biologia 65, 688–696.CrossRefGoogle Scholar
González-Wangüemert, M. and Pérez-Ruzafa, Á. (2012) In two waters: contemporary evolution of lagoonal and marine white seabream (Diplodus sargus) populations. Marine Ecology 33, 337–349.CrossRefGoogle Scholar
González-Wangüemert, M. and Vergara-Chen, C. (2014) Environmental variables, habitat discontinuity and life history shaping the genetic structure of Pomatoschistus marmoratus. Helgoland Marine Research 68, 357–371.CrossRefGoogle Scholar
González-Wangüemert, M., Giménez-Casalduero, F. and Pérez-Ruzafa, Á. (2006) Genetic differentiation of Elysia timida (Risso, 1818) populations in Southwest Mediterranean and Mar Menor coastal lagoon. Biochemical Systematics and Ecology 34, 514–527.CrossRefGoogle Scholar
González-Wangüemert, M., Cánovas, F., Marcos, C. and Pérez-Ruzafa, A. (2009) Phosphoglucose isomerase variability of Cerastoderma glaucum as a model for testing the influence of environmental conditions and dispersal patterns through quantitative ecology approaches. Biochemical Systematics and Ecology 37, 325–333.CrossRefGoogle Scholar
González-Wangüemert, M., Fernández, T.V., Pérez-Ruzafa, A., Giacalone, M., D'Anna, G. and Badalamenti, F. (2012) Genetic considerations on the introduction of farmed fish in marine protected areas: the case of study of white seabream restocking in the Gulf of Castellammare (Southern Tyrrhenian Sea). Journal of Sea Research 68, 41–48.CrossRefGoogle Scholar
González-Wangüemert, M., Domínguez-Godino, J., Giménez-Casalduero, F. and Serrão, E.A. (2014) Genetic signature of a recent invasion: the ragged sea hare Bursatella leachii in Mar Menor (SE Spain). Biochemical Systematics and Ecology 54, 123–129.CrossRefGoogle Scholar
Gouy, M., Guindon, S. and Gascuel, O. (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27, 221–224.CrossRefGoogle ScholarPubMed
Grant, W.S. and Bowen, B.W. (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. Journal of Heredity 89, 415–426.CrossRefGoogle Scholar
Hauser, L., Adcock, G.J., Smith, P.J., Bernal Ramírez, J.H. and Carvalho, G.R. (2002) Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus). Proceedings of the National Academy of Sciences USA 99, 11742–11747.CrossRefGoogle Scholar
Hummel, H., Wolowicz, M. and Bogaards, R.H. (1994) Genetic variability and relationships for populations of Cerastoderma edule and of the C. glaucum complex. Netherland Journal of Sea Research 33, 81–89.CrossRefGoogle Scholar
Kenchington, E. (2003) The effects of fishing on species and genetic diversity. In Sinclair, M. and Valdimarsson, G. (eds) Responsible fisheries in the marine ecosystem. Rome and Wallingford: FAO and CAB International, pp. 235–253.CrossRefGoogle Scholar
Kenchington, E., Heino, M. and Nielsen, E.E. (2003) Managing marine genetic diversity: time for action. ICES Journal of Marine Science 60, 1172–1176.CrossRefGoogle Scholar
Kjerfve, B. (1994) Coastal lagoons. In Kjerfve, B. (ed.) Coastal lagoon processes, Volume 60. Amsterdam: Elsevier Oceanography Series, pp. 1–8.CrossRefGoogle Scholar
Krakau, M., Jacobsen, S., Jensen, K.T. and Reise, K. (2012) The cockle Cerastoderma edule at Northeast Atlantic shores: genetic signatures of glacial refugia. Marine Biology 159, 221–230.CrossRefGoogle Scholar
Ladhar-Chaabouni, R., Hamza-Chaffai, A., Hardivillier, Y., Chénais, B. and Denis, F. (2010) A pilot study of genetic differentiation between two phenotypes of a Mediterranean population of the bivalve Cerastoderma glaucum and genetic discrimination with other Cerastoderma glaucum and Cerastoderma edule populations outside the Mediterranean. Marine Ecology 31, 355–363.CrossRefGoogle Scholar
Luttikhuizen, P.C., Drent, J., van Delden, W. and Piersma, T. (2003) Spatially structured genetic variation in a broadcast spawning bivalve: quantitative vs. molecular traits. Journal of Evolutionary Biology 16, 260–272.CrossRefGoogle Scholar
Mahidol, C., Na-Nakorn, U., Sukmanomon, S., Taniguchi, N. and Nguyen, T.T. (2007) Mitochondrial DNA diversity of the Asian moon scallop, Amusium pleuronectes (Pectinidae), in Thailand. Marine Biotechnology 9, 352–359.CrossRefGoogle ScholarPubMed
Malham, S.K., Hutchinson, T.H. and Longshaw, M. (2012) A review of the biology of European cockles (Cerastoderma spp.). Journal of the Marine Biological Association of the United Kingdom 92, 1563–1577.CrossRefGoogle Scholar
Marín, A., Fujimoto, T. and Arai, K. (2013) Genetic structure of the Peruvian scallop Argopecten purpuratus inferred from mitochondrial and nuclear DNA variation. Marine Genomics 9, 1–8.CrossRefGoogle ScholarPubMed
Marino, I.A.M., Barbisan, F., Gennari, M., Giomi, F., Beltramini, M., Bisol, P.M. and Zane, L. (2010) Genetic heterogeneity in populations of the Mediterranean shore crab, Carcinus aestuarii (Decapoda, Portunidae), from the Venice Lagoon. Estuarine, Coastal and Shelf Science 87, 135–144.CrossRefGoogle Scholar
Martínez, L., Méndez, J., Insua, A., Arias-Pérez, A. and Freire, R. (2013) Genetic diversity and population differentiation in the cockle Cerastoderma edule estimated by microsatellite markers. Helgoland Marine Research 67, 179–189.CrossRefGoogle Scholar
Milana, V., Franchini, P., Sola, L., Angiulli, E. and Rossi, A.R. (2012) Genetic structure in lagoons: the effects of habitat discontinuity and low dispersal ability on populations of Atherina boyeri. Marine Biology 159, 399–411.CrossRefGoogle Scholar
Newton, A. and Mudge, S.M. (2003) Temperature and salinity regimes in a shallow, mesotidal lagoon, the Ria Formosa, Portugal. Estuarine, Coastal and Shelf Science 56, 1–13.Google Scholar
Owen, E.F. and Rawson, P.D. (2013) Small-scale spatial and temporal genetic structure of the Atlantic sea scallop (Placopecten magellanicus) in the inshore Gulf of Maine revealed using AFLPs. Marine Biology 160, 3015–3025.CrossRefGoogle Scholar
Pacheco, A., Ferreira, Ó., Williams, J.J., Garel, E., Vila-Concejo, A. and Dias, J.A. (2010) Hydrodynamics and equilibrium of a multiple-inlet system. Marine Geology 274, 32–42.CrossRefGoogle Scholar
Pampoulie, C., Gysels, E.S., Maes, G.E., Hellemans, B., Leentjes, V., Jones, A.G. and Volckaert, F.A.M. (2004) Evidence for fine-scale genetic structure and estuarine colonisation in a potential high gene flow marine goby (Pomatoschistus minutus). Heredity 92, 434–445.CrossRefGoogle Scholar
Pérez-Ruzafa, Á., González-Wangüemert, M., Lenfant, P., Marcos, C. and García-Charton, J.A. (2006) Effects of fishing protection on the genetic structure of fish populations. Biological Conservation 129, 244–255.CrossRefGoogle Scholar
Pilkey, O. Jr, Neal, W., Monteiro, J. and Dias, J. (1989) Algarve barrier islands: a noncoastal-plain system in Portugal. Journal of Coastal Research 5, 239–261.Google Scholar
Pinsky, M.L. and Palumbi, S.R. (2014) Meta-analysis reveals lower genetic diversity in overfished populations. Molecular Ecology 23, 29–39.CrossRefGoogle ScholarPubMed
Posada, D. and Crandall, K.A. (2001) Intraspecific phylogenetics: trees grafting into networks. Trends in Ecology and Evolution 16, 37–45.CrossRefGoogle ScholarPubMed
R Development Core Team (2008) R: A language and environment for statistical computing. Vienna: R Foundation Statistical Computing.Google Scholar
Ribeiro, J., Monteiro, C.C., Monteiro, P., Bentes, L., Coelho, R., Gonçalves, J.M.S., Lino, P.G. and Erzini, K. (2008) Long-term changes in fish communities of the Ria Formosa coastal lagoon (southern Portugal) based on two studies made 20 years apart. Estuarine, Coastal and Shelf Science 76, 57–68.CrossRefGoogle Scholar
Rice, W.R. (1989) Analyzing tables of statistical tests. Evolution 43, 223–225.CrossRefGoogle ScholarPubMed
Richards, C.L., Wares, J.P- and Mackie, J.A. (2010) Evaluating adaptive processes for conservation and management of estuarine and coastal resources. Estuaries and Coasts 33, 805–810.CrossRefGoogle Scholar
Ridgway, G. (2001) Interpopulation variation in blue mussels, Mytilus edulis L., over short distances. Sarsia 86, 157–161.CrossRefGoogle Scholar
Rozas, J., Sánchez-DelBarrio, J.C., Messeguer, X. and Rozas, R. (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.CrossRefGoogle ScholarPubMed
Russell, P.J. (1971) A reappraisal of the geographical distributions of the cockles Cardium edule L. and C. glaucum Bruguière. Journal of Conchology 27, 225–234.Google Scholar
Ryman, N., Utter, F. and Laikre, L. (1995) Protection of intraspecific biodiversity of exploited fishes. Review of Fish Biology and Fisheries 5, 417–446.CrossRefGoogle Scholar
Sambrook, J. and Russell, D.W. (2001) Molecular cloning: a laboratory manual. 3rd edition. New York, NY: Cold Spring Harbor Press.Google Scholar
Santos, S., Cruzeiro, C., Olsen, J.L., Van der Veer, H.W. and Luttikhuizen, P.C. (2012) Isolation by distance and low connectivity in the peppery furrow shell Scrobicularia plana (Bivalvia). Marine Ecology Progress Series 462, 111–124.CrossRefGoogle Scholar
Smith, P.J. (1994) Genetic diversity of marine fisheries resources: possible impacts of fishing. FAO Fisheries Technical Paper No. 344. Rome: FAO.Google Scholar
Sousa-Leitão, F.M. and Baptista-Gaspar, M. (2007) Immediate effect of intertidal non-mechanised cockle harvesting on macrobenthic communities: a comparative study. Scientia Marina 71, 723–733.CrossRefGoogle Scholar
Stamatis, C., Triantafyllidis, A., Moutou, K.A. and Mamuris, Z. (2004) Mitochondrial DNA variation in North East Atlantic and Mediterranean populations of Norway lobster, Nephrops norvegicus. Molecular Ecology 13, 1377–1390.CrossRefGoogle Scholar
Tajima, F. (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.CrossRefGoogle ScholarPubMed
Tarnowska, K., Chenuil, A., Nikula, R., Féral, J.P. and Wolowicz, M. (2010) Complex genetic population structure of the bivalve Cerastoderma glaucum in a highly fragmented lagoon habitat. Marine Ecology Progress Series 406, 173–184.CrossRefGoogle Scholar
Tarnowska, K., Krakau, M., Jacobsen, S., Wołowicz, M., Féral, J.P. and Chenuil, A. (2012) Comparative phylogeography of two sister (congeneric) species of cardiid bivalve: strong influence of habitat, life history and post-glacial history. Estuarine, Coastal and Shelf Science 107, 150–158.CrossRefGoogle Scholar
Vânia, B., Ullah, H., Teixeira, C.M., Range, P., Erzini, K. and Leitão, F. (2014) Influence of environmental variables and fishing pressure on bivalve fisheries in an inshore lagoon and adjacent nearshore coastal area. Estuaries and Coasts 37, 191–205.CrossRefGoogle Scholar
Vasileiadou, K., Sarropoulou, E., Tsigenopoulos, C., Reizopoulou, S., Nikolaidou, A., Orfanidis, S., Simboura, M. and Kotoulas, G. (2012) Genetic vs community diversity patterns of macrobenthic species: preliminary results from the lagoonal ecosystem. Transitional Waters Bulletin 6, 20–33.Google Scholar
Vergara-Chen, C., González-Wangüemert, M., Marcos, C. and Pérez-Ruzafa, A. (2010a) Genetic diversity and connectivity remain high in Holothuria polii (Delle Chiaje 1823) across a coastal lagoon–open sea environmental gradient. Genetica 138, 895–906.CrossRefGoogle ScholarPubMed
Vergara-Chen, C., González-Wangüemert, M., Marcos, C. and Pérez-Ruzafa, A. (2010b) High gene flow promotes the genetic homogeneity of Pomatoschistus marmoratus (Risso 1810) from Mar Menor coastal lagoon and adjacent marine waters (Spain). Marine Ecology 31, 270–275.CrossRefGoogle Scholar
Vergara-Chen, C., González-Wangüemert, M., Marcos, C. and Pérez-Ruzafa, A. (2013) Small-scale genetic structure of Cerastoderma glaucum in a lagoonal environment: potential significance of habitat discontinuity and unstable population dynamics. Journal of Molluscan Studies 79, 230–240.CrossRefGoogle Scholar
Winkler, G., Souissi, S., Poux, C. and Castric, V. (2011) Genetic heterogeneity among Eurytemora affinis populations in Western Europe. Marine Biology 158, 1841–1856.CrossRefGoogle Scholar
Zainal Abidin, D.H., Mustaffa, S., Rahim, M.A., Nair, D.M., Naim, D.Md. and Nor, A.M. (2014) Population genetics of the black scar oyster, Crassostrea iredalei: repercussion of anthropogenic interference. Mitochondrial DNA. doi: 10.3109/19401736.2014.913137.Google ScholarPubMed
Zhan, A., Hu, J., Hu, X., Zhou, Z., Hui, M., Wang, S., Peng, W., Wang, M. and Bao, Z. (2009) Fine-scale population genetic structure of Zhikong scallop (Chlamys farreri): do local marine currents drive geographical differentiation? Marine Biotechnology 11, 223–235.CrossRefGoogle ScholarPubMed
Zhang, H., Geller, J.B. and Vrijenhoek, R.C. (2014) Genetic diversity in native and introduced populations of the amethyst gem clam Gemma gemma (Totten, 1834) from the US east and west coasts. Biological Invasions. doi: 10.1007/s10530-014-0699-9.CrossRefGoogle Scholar