Scientia Marina, Vol 78, No 4 (2014)

Fitness difference between cryptic salinity-related phenotypes of sea bass (Dicentrarchus labrax)


https://doi.org/10.3989/scimar.03992.02C

Bruno Guinand
Institut des Sciences de l’Evolution de Montpellier, CNRS-UMR 5554 (Université Montpellier 2) - Station Méditerranéenne de l’Environnement Littoral, France

Nolwenn Quéré
Institut des Sciences de l’Evolution de Montpellier, CNRS-UMR 5554 (Université Montpellier 2) - Station Méditerranéenne de l’Environnement Littoral, France

Frédérique Cerqueira
Institut des Sciences de l’Evolution de Montpellier, CNRS-UMR 5554 (Université Montpellier 2) - LabEx CeMEB (Centre Méditerranéen Environnement Biodiversité), Université Montpellier II, France

Erick Desmarais
Institut des Sciences de l’Evolution de Montpellier, CNRS-UMR 5554 (Université Montpellier 2) - LabEx CeMEB (Centre Méditerranéen Environnement Biodiversité), Université Montpellier II, France

François Bonhomme
Institut des Sciences de l’Evolution de Montpellier, CNRS-UMR 5554 (Université Montpellier 2) - Station Méditerranéenne de l’Environnement Littoral, France

Abstract


The existence of cryptic salinity-related phenotypes has been hypothesized in the “euryhaline” sea bass (Dicentrarchus labrax). How differential osmoregulation costs between freshwater and saltwater environments affect fitness and phenotypic variation is misunderstood in this species. During an experiment lasting around five months, we investigated changes in the whole body mass and in the expression of growth-related genes (insulin-like growth factor 1 [IGF-1]; growth hormone receptor [GHR]) in the intestine and the liver of sea bass thriving in sea water (SSW), successfully acclimated to freshwater (SFW), and unsuccessfully acclimated to freshwater (UFW). Albeit non-significant, a trend toward change in body mass was demonstrated among SSW, UFW and SFW fish, suggesting that SSW fish were a mixture of the other phenotypes. Several mortality peaks were observed during the experiment, with batches of UFW fish showing higher expression in the osmoregulatory intestine due to down-regulation of genes in the liver and significant up-regulation of GHR in the intestine compared with SFW fish. Energy investment toward growth or ion homeostasis hence partly mediates the fitness difference between cryptic SFW and UFW phenotypes. The use of a genetic marker located within the IGF-1 gene showed no genotype-phenotype relationship with levels of gene expression.

Keywords


phenotype; gene expression; growth hormone receptor; insulin-like growth factor 1; sea bass

Full Text:


HTML PDF XML

References


Allegrucci G., Fortunato C., Cataudella S., et al. 1994. Acclimation to fresh water of the sea bass: evidence of selective mortality and allozyme genotypes. In: Beaumont A.R. (ed.), Genetics and evolution of marine organisms. Chapman and Hall, London, pp. 486-502.

Allegrucci G., Fortunato C., Sbordoni V. 1997. Genetic structure and allozyme variation of sea bass (Dicentrarchus labrax and D. punctatus) in the Mediterranean Sea. Mar. Biol. 128: 347-358. http://dx.doi.org/10.1007/s002270050100

Alliot E., Pastoureaud A., Thébault H. 1983. Influence de la température et de la salinité sur la croissance et la composition corporelle d'alevins de Dicentrarchus labrax. Aquaculture 31: 181-194. http://dx.doi.org/10.1016/0044-8486(83)90312-5

Andersen C.L., Jensen J.L., Ørntoft T.F. 2004. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64: 5245–5250. http://dx.doi.org/10.1158/0008-5472.CAN-04-0496 PMid:15289330

Angers B., Castonguay E., Massicotte R. 2010. Environmentally induced phenotypes and DNA methylation: how to deal with unpredictable conditions until the next generation and after. Mol. Ecol. 19: 1283-1295. http://dx.doi.org/10.1111/j.1365-294X.2010.04580.x PMid:20298470

Avarre J.C., Dugué R., Alonso P., et al. 2014. Analysis of the black-chinned tilapia Sarotherodon melanotheron heudelotii reproducing under a wide range of salinities: from RNA-seq to candidate genes. Mol. Ecol. Res. 19: 1283-1295.

Barnabé G. 1973. Étude morphologique du loup, Dicentrarchus labrax (L.) de la région de Sète. Rev. Trav. Instit. Pêches Marit. 37: 397-410.

Bahri-Sfar L., Ben Hassine O.K. 2009. Clinal variations of discriminative meristic characters of sea bass, Dicentrarchus labrax (Moronidae, Perciformes) populations on Tunisian coasts. Cybium 33: 211-218.

Blel H., Panfili J., Guinand B., et al. 2010. Selection footprint at the first intron of the Prl gene in natural populations of the flathead mullet (Mugil cephalus, L. 1758). J. Exp. Mar. Biol. Ecol. 387: 60-67. http://dx.doi.org/10.1016/j.jembe.2010.02.018

Bodinier C., Lorin-Nebel C., Charmantier G., Boulo V. 2009. Influence of salinity on the localization and expression of the CFTR chloride channel in the ionocytes of juvenile Dicentrarchus labrax exposed to seawater and freshwater. Comp. Biochem. Physiol. A153: 345-351. http://dx.doi.org/10.1016/j.cbpa.2009.03.011 PMid:19328865

Boeuf G., Payan P. 2001. How should salinity influence fish growth? Comp. Biochem. Physiol. C130: 411-423.

Boutet I., Lorin-Nebel C., De Lorgeril J., et al. 2007. Molecular characterisation of prolactin and analysis of extrapituitary expression in the European sea bass Dicentrarchus labrax under various salinity conditions. Comp. Biochem. Physiol. D2: 74-83.

Bustin S.A., Benes V., Garson J.A., et al. 2009. The MIQE Guidelines: minimum information for publication of quantitative real-Time PCR experiments. Clin. Chem. 55: 611-622. http://dx.doi.org/10.1373/clinchem.2008.112797 PMid:19246619

Calduch-Giner J.A., Mingarro M., de Celis S.V.R., et al. 2003. Molecular cloning and characterization of gilthead sea bream, (Sparus aurata) growth hormone receptor (GHR). Assessment of alternative splicing. Comp. Biochem. Physiol. B136: 1-13. http://dx.doi.org/10.1016/S1096-4959(03)00150-7

Cataudella S., Allegrucci G., Bronzi P., et al. 1991. Multidisciplinary approach to the optimisation of sea bass (Dicentrarchus labrax) rearing in freshwater – Basic morpho-physiology and osmoregulation. In: De Pauw N. and Joyce J. (eds), Aquaculture and the environment. European Aquaculture Society - Special Publication n° 14. Bredene, Belgium, pp. 55-57.

Chaoui L., Gagnaire P.A., Guinand B., et al. 2012. Microsatellite length variation in candidate genes correlates with habitat in the gilthead sea bream Sparus aurata. Mol. Ecol. 21: 5497-5515. http://dx.doi.org/10.1111/mec.12062 PMid:23061421

Chatain B., Chavanne H. 2009. La génétique du bar (Dicentrarchus labrax, L.). Cah. Agric. 18: 249-255.

Chervinski J. 1974. Sea bass, Dicentrarchus labrax L. (Pisces, Serranidae) a "police fish" in freshwater ponds and its adaptability to various saline condition. Isr. J. Aquacult. - Bamidgeh 26: 110-113.

Chervinski J. 1975. Sea basses Dicentrarchus labrax (Linné) and D. punctatus (Boch) (Pisces: Serranidae), a control fish in fresh-water. Aquaculture 6: 249-256. http://dx.doi.org/10.1016/0044-8486(75)90045-9

Claireaux G., Lagardère J.P. 1999. Influence of temperature, oxygen and salinity on the metabolism of the European sea bass. J. Sea Res. 42: 157-168. http://dx.doi.org/10.1016/S1385-1101(99)00019-2

Conides A.J., Glamuzina B. 2006. Laboratory simulation of the effects of environmental salinity on acclimation, feeding and growth of wild-caught juveniles of European sea bass Dicentrarchus labrax and gilthead sea bream, Sparus aurata. Aquaculture 256: 235-245. http://dx.doi.org/10.1016/j.aquaculture.2006.02.029

Corti M., Loy A., Cataudella S. 1996. Form changes in the sea bass, Dicentrarchus labrax (Moronidae: Teleostei), after acclimation to freshwater: an analysis using shape coordinates. Env. Biol. Fishes 47: 165-175. http://dx.doi.org/10.1007/BF00005039

Côté G., Perry G., Blier P., et al. 2007. The influence of gene-environment interactions on GHR and IGF-1 expression and their association with growth in brook charr, Salvelinus fontinalis (Mitchill). BMC Genet. 8: 87. http://dx.doi.org/10.1186/1471-2156-8-87 PMid:18154679 PMCid:PMC2257973

Costa C., Vandeputte M., Antonucci F., et al. 2010. Genetic and environmental influences on shape variation in the European sea bass (Dicentrarchus labrax). Biol. J. Linn. Soc. 101: 427-436. http://dx.doi.org/10.1111/j.1095-8312.2010.01512.x

Dendrinos P., Thorpe J.P. 1985. Effects of reduced salinity on growth and body composition in the European bass Dicentrarchus labrax (L.). Aquaculture 49: 333-358. http://dx.doi.org/10.1016/0044-8486(85)90090-0

Duan C. 1997. The insulin-like growth factor system and its biological actions in fish. Am. Zool. 37: 491-503.

Dufour V., Cantou M., Lecomte F. 2009. Identification of sea bass (Dicentrarchus labrax) nursery areas in the north-western Mediterranean Sea. J. Mar. Biol. Ass. UK 89: 1367-1374. http://dx.doi.org/10.1017/S0025315409000368

Eroldogan O.T., Kumlu M. 2002. Growth performance, body traits and fillet composition of the European sea bass (Dicentrarchus labrax) reared in various salinities and freshwater. Turk. J. Vet. Anim. Sci. 26: 993-1001.

Ferraresso S., Milan M., Pellizzari C., et al. 2010. Development of an oligo DNA microarray for the European sea bass and its application to expression profiling of jaw deformity. BMC Genomics 11 : 354. http://dx.doi.org/10.1186/1471-2164-11-354 PMid:20525278 PMCid:PMC2889902

Fox B.K., Breves J.P., Davis L.K., et al. 2010. Tissue-specific regulation of the growth hormone/insulin-like growth factor axis during fasting and re-feeding: Importance of muscle expression of IGF-I and IGF-II mRNA in the tilapia. Gen. Comp. Endocrinol. 166: 573-580. http://dx.doi.org/10.1016/j.ygcen.2009.11.012 PMid:19932110

Fukamachi S., Meyer A. 2007. Evolution of receptors for growth hormone and somatolactin in fish and land vertebrates: lessons from the lungfish and sturgeon orthologues. J. Mol. Evol. 65: 359-372. http://dx.doi.org/10.1007/s00239-007-9035-7 PMid:17917757

Gabriel W., Luttbeg B., Sih A., et al. 2005. Environmental tolerance, heterogeneity, and the evolution of reversible plastic responses. Am. Nat. 166: 339-353. http://dx.doi.org/10.1086/432558 PMid:16224689

Gemayel R., Vinces M.D., Legendre M., et al.2010. Variable tandem repeats accelerate evolution of coding and regulatory sequences. Ann. Rev. Genet. 44: 445-477. http://dx.doi.org/10.1146/annurev-genet-072610-155046 PMid:20809801

Ghalambor C.K., McKay J.K., Carroll S.P., et al. 2007. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21: 394-407. http://dx.doi.org/10.1111/j.1365-2435.2007.01283.x

Gienapp P., Teplitsky C., Alho J.S., et al. 2008. Climate change and evolution: disentangling environmental and genetic responses. Mol. Ecol. 17: 167-178. http://dx.doi.org/10.1111/j.1365-294X.2007.03413.x PMid:18173499

Giffard-Mena I., Lorin-Nebel C., Charmantier G., et al. 2008. Adaptation of the sea-bass (Dicentrarchus labrax) to fresh water: Role of aquaporins and Na+/K+-ATPases. Comp. Biochem. Physiol. A150: 332-338. http://dx.doi.org/10.1016/j.cbpa.2008.04.004 PMid:18485772

González-Wangüemert G, Pérez-Ruzafa Á. 2012. In two waters: contemporary evolution of lagoonal and marine white seabream (Diplodus sargus) populations. Mar. Ecol. 33: 337-349. http://dx.doi.org/10.1111/j.1439-0485.2011.00501.x

González-Wangüemert M, Vergara-Chen C. 2014. Environmental variables, habitat discontinuity and life history shaping the genetic structure of Pomatoschistus minutus. Helgol. Mar. Res. 68: 357-371. http://dx.doi.org/10.1007/s10152-014-0396-1

Guderley H., Pörtner H.O. 2010. Metabolic power budgeting and adaptive strategies in zoology: examples from scallops and fish. Can. J. Zool. 88: 753-763. http://dx.doi.org/10.1139/Z10-039

Havird J.C., Henry R.P., Wilson A.E. 2013. Altered expression of Na+/K+–ATPase and other osmoregulatory genes in the gills of euryhaline animals in response to salinity transfer: A meta-analysis of 59 quantitative PCR studies over 10 years. Comp. Biochem. Physiol. D8: 131-140.

Hoffmann A.A., Parsons P.A. 1991. Evolutionary genetics and environmental stress. Oxford University Press, Oxford, 296 pp.

Jensen K., Madsen S.S., Kristiansen K. 1998. Osmoregulation and salinity effects on the expression and activity of Na+,K+-ATPase in the gills of European sea bass, Dicentrarchus labrax (L.). J. Exp. Zool. 282: 290-300. http://dx.doi.org/10.1002/(SICI)1097-010X(19981015)282:3<290::AID-JEZ2>3.0.CO;2-H

Kuhl H., Beck A., Wozniak G., et al. 2010. The European sea bass Dicentrarchus labrax genome puzzle: comparative BAC-mapping and low coverage shotgun sequencing. BMC Genomics 11: 68. http://dx.doi.org/10.1186/1471-2164-11-68 PMid:20105308 PMCid:PMC2837037

Larsen P.F., Schulte P.M., Nielsen E.E. 2011. Gene expression analysis for the identification of selection and local adaptation in fishes. J. Fish Biol. 78:1-22. http://dx.doi.org/10.1111/j.1095-8649.2010.02834.x PMid:21235543

Lasserre P, Gallis JL. 1975. Osmoregulation and differential penetration of two grey mullets, Chelon labrosus (Risso) and Liza ramada (Risso) in estuarine fish ponds. Aquaculture 5: 323-344. http://dx.doi.org/10.1016/0044-8486(75)90053-8

Lemaire C., Allegrucci G., Naciri M., et al. 2000. Do discrepancies between microsatellite and allozyme variation reveal differential selection between sea and lagoon in the sea bass (Dicentrar chus labrax)? Mol. Ecol. 9: 457-467. http://dx.doi.org/10.1046/j.1365-294x.2000.00884.x PMid:10736048

Lerner D.T., Sheridan M.A., McCormick S.D. 2012. Estrogenic compounds decrease growth hormone receptor abundance and alter osmoregulation in Atlantic salmon. Gen. Comp. Endocrinol. 179: 196-204. http://dx.doi.org/10.1016/j.ygcen.2012.08.001 PMid:22906423

Link K., Berishvili G., Shved N., et al. 2010: Seawater and freshwater challenges affect the insulin-like growth factors IGF-I and IGF-II in liver and osmoregulatory organs of the tilapia. Mol. Cell. Endocrinol. 327: 40-46. http://dx.doi.org/10.1016/j.mce.2010.05.011 PMid:20621706

Loy A, Corti M., Cataudella S. 1999. Variation in gill rakers number during growth of the sea bass, Dicentrarchus labrax (Perciformes: Moronidae), reared at different salinities. Env. Biol. Fishes 55: 391-398. http://dx.doi.org/10.1023/A:1007548102060

Magdeldin S., Uchida K., Hirano T., et al. 2007. Effects of environmental salinity on somatic growth and growth hormone/insulin-like growth factor-I axis in juvenile tilapia (Oreochromis mossambicus). Fish. Sci. 73: 1025-1034. http://dx.doi.org/10.1111/j.1444-2906.2007.01432.x

Magnanou E., Klopp C., Noirot C., et al. 2014. Generation and characterization of the sea bass Dicentrarchus labrax brain and liver transcriptomes. Gene 544:56-66. http://dx.doi.org/10.1016/j.gene.2014.04.032 PMid:24768179

Marino G., Cataldi E., Pucci P., et al. 1994. Acclimation trials of wild and hatchery sea bass (Dicentrarchus labrax) fry at different salinities. J. Appl. Ichthyol. 10: 57-63. http://dx.doi.org/10.1111/j.1439-0426.1994.tb00142.x

Marshall D.J., Monro K., Bode M., et al. 2010. Phenotype-environment mismatches reduce connectivity in the sea. Ecol. Lett. 13: 128-140. http://dx.doi.org/10.1111/j.1461-0248.2009.01408.x PMid:19968695

Mazurais D., Darias M.J., Gouillou-Coustans M.F., et al. 2008. Dietary vitamin mix levels influence the ossification process in European sea bass (Dicentrarchus labrax) larvae. Am. J. Physiol. – Regul. Integr. Comp. Physiol. 294: R520-R527. http://dx.doi.org/10.1152/ajpregu.00659.2007 PMid:18032465

McCairns R.J.S., Bernatchez L. 2010. Adaptive divergence between freshwater and marine sticklebacks: insights into the role of phenotypic plasticity from an integrated analysis of candidate gene expression. Evolution 64: 1029-1047. http://dx.doi.org/10.1111/j.1558-5646.2009.00886.x PMid:19895556

Montserrat N., Gabillard J.C., Capilla E., et al. 2007. Role of insulin, insulin-like growth factors, and muscle regulatory factors in the compensatory growth of the trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 150: 462-472. http://dx.doi.org/10.1016/j.ygcen.2006.11.009 PMid:17196198

Moriyama S., Ayson F.G., Kawauchi H., 2000. Growth regulation by insulin-like growth factor-I in fish. Biosci. Biotech. Biochem. 64: 1553-1562. http://dx.doi.org/10.1271/bbb.64.1553 PMid:10993139

Nebel C., Romestand B., Nègre-Sadargues G., et al. 2005. Differential freshwater adaptation in juvenile sea-bass Dicentrarchus labrax: involvement of gills and urinary system. J. Exp. Biol. 208: 3859-3871. http://dx.doi.org/10.1242/jeb.01853 PMid:16215214

Norman J.D., Danzmann R.G., Glede B., et al. 2011. The genetic basis of salinity tolerance traits in Arctic charr (Salvelinus alpinus). BMC Genet. 12: 81. http://dx.doi.org/10.1186/1471-2156-12-81 PMid:21936917 PMCid:PMC3190344

Palaima A. 2007. The fitness cost of generalization: present limitations and future possible solutions. Biol. J. Linn. Soc. 90: 583-590. http://dx.doi.org/10.1111/j.1095-8312.2007.00745.x

Pfaffl M. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nuc. Acids Res. 29: e45. http://dx.doi.org/10.1093/nar/29.9.e45 PMid:11328886 PMCid:PMC55695

Pfennig D.W., Wund M.A., Snell-Rodd E.C., et al. 2010. Phenotypic plasticity's impact on diversification and speciation. Trends Ecol. Evol. 25: 459-467. http://dx.doi.org/10.1016/j.tree.2010.05.006 PMid:20557976

Pickett G.D., Pawson M.G. 1994. Sea bass biology, exploitation and conservation. Fish and fisheries series, Chapman and Hall, London, 337 pp.

Plaut I. 1998. Comparison of salinity tolerance and osmoregulation in two closely related species of blennies from different habitats. Fish Physiol. Biochem. 19: 181-188. http://dx.doi.org/10.1023/A:1007798712727

Quéré N., Guinand B., Kuhl H., etal. 2010. Genomic sequences and genetic differentiation at associated tandem repeat markers in growth hormone, somatolactin and insulin-like growth factor 1 genes of the sea bass, Dicentrarchus labrax. Aquat. Living Resour. 23: 285-296. http://dx.doi.org/10.1051/alr/2010021

Räsänen K, Hendry A.P. 2008. Disentangling interactions between adaptive divergence and gene flow when ecology drives diversification. Ecol. Lett. 11: 624-636. http://dx.doi.org/10.1111/j.1461-0248.2008.01176.x PMid:18384363

Reindl K.L., Sheridan M.A. 2012. Peripheral regulation of the growth hormone-insulin-like growth factor system in fish and other vertebrates. Gene Comp. Endocrinol. 163: 231-245.

Reinecke M. 2010. Influences of the environment on the endocrine and paracrine fish growth hormone–insulin-like growth factor-I system. J. Fish Biol. 76:1233-1254. http://dx.doi.org/10.1111/j.1095-8649.2010.02605.x PMid:20537012

Rigal F., Chevalier T., Lorin-Nebel C., et al. 2008. Osmoregulation as a potential factor for the differential distribution of two cryptic gobiid species, Pomatoschistus microps and P. marmoratus in French Mediterranean lagoons. Sci. Mar. 72: 469-476.

Riley L.G., Hirano T., Gray E.G. 2003. Effects of transfer from seawater to fresh water on the growth hormone/insulin-like growth factor-I axis and prolactin in the tilapia, Oreochromis mossambicus. Comp. Biochem. Physiol. B136: 647-655. http://dx.doi.org/10.1016/S1096-4959(03)00246-X

Roff D.A., 1992. The evolution of life histories. Chapman and Hall, New York, 595 pp.

Rubio V.C., Sánchez-Vázquez F.J., Madrid J.A. 2005. Effects of salinity on food intake and macronutrient selection in European sea bass. Physiol. Behav. 85: 333-339. http://dx.doi.org/10.1016/j.physbeh.2005.04.022 PMid:15932763

Saillant A., Fostier E., Haffray P., et al. 2003. Saline preferendum for the European sea bass, Dicentrarchus labrax, larvae and juveniles: effect of salinity on early development and sex determination. J. Exp. Mar. Biol. Ecol. 287: 103-117. http://dx.doi.org/10.1016/S0022-0981(02)00502-6

Sakamoto T., Hirano T. 1991. Growth hormone receptors in the liver and osmoregulatory organs of rainbow trout: characterization and dynamics during adaptation to seawater. J. Endocrinol. 130: 425-433. http://dx.doi.org/10.1677/joe.0.1300425 PMid:1940716

Sánchez Vázquez F.J., Muñoz-Cueto J.A. 2014. Biology of European sea bass. CRC Press, Cambridge, 436 pp.

Scott G.R., Baker D.W., Schulte P.M., et al. 2008. Physiological and molecular mechanisms of osmoregulatory plasticity in killifish after seawater transfer. J. Exp. Biol. 211: 2450-2459. http://dx.doi.org/10.1242/jeb.017947 PMid:18626079

Shikano T., Ramadevi J., Merilä J. 2010. Identification of local- and habitat-dependent selection: scanning functionally important genes in nine-spined sticklebacks (Pungitius pungitius). Mol. Biol. Evol. 27: 2775-2789. http://dx.doi.org/10.1093/molbev/msq167 PMid:20591843

Sotka E.E. 2012. Natural selection, larval dispersal, and the geography of phenotypes in the sea. Integr. Comp. Biol. 52: 538-545. http://dx.doi.org/10.1093/icb/ics084 PMid:22634357

Streelman J., Kocher T. 2002. Microsatellite variation associated with prolactin expression and growth of salt-challenged tilapia. Physiol. Genomics 9: 1-4. PMid:11948285

Tine M., De Lorgeril J., D'Cotta H., et al. 2008. Transcriptional responses of the black-chinned tilapia Sarotherodon melanotheron to salinity extremes. Mar. Genomics 1: 37-46. http://dx.doi.org/10.1016/j.margen.2008.06.001 PMid:21798152

Terova G., Rimoldi S., Chini V., et al. 2007. Cloning and expression analysis of insulin-like growth factor I and II in liver and muscle of sea bass (Dicentrarchus labrax, L.) during long-term fasting and refeeding. J. Fish Biol. 70: 219-233. http://dx.doi.org/10.1111/j.1095-8649.2007.01402.x

Venturini G., Cataldi E., Marino G., et al. 1992. Serum ions concentration and ATPase activity in gills, kidney and oesophagus of European sea bass (Dicentrarchus labrax, Pisces, Perciformes) during acclimation trials to fresh water. Comp. Biochem. Physiol. A103: 451-454. http://dx.doi.org/10.1016/0300-9629(92)90271-Q

Van Valen L. 1965. Morphological variation and width of ecological niche. Am. Nat. 99: 377-390. http://dx.doi.org/10.1086/282379

Varsamos S., Diaz J.P., Charmantier G., et al. 2002. Branchial chlo ride cells in sea bass (Dicentrarchus labrax) adapted to fresh water, seawater, and doubly concentrated seawater. J. Exp. Zool. 293: 12-26. http://dx.doi.org/10.1002/jez.10099 PMid:12115915

Varsamos S., Xuereb B., Commes T., et al. 2006. Pituitary hormone mRNA expression in European sea bass Dicentrarchus labrax in seawater and following acclimation to fresh water. J. Endocrinol. 191: 473-480. http://dx.doi.org/10.1677/joe.1.06847 PMid:17088417

Vasconcelos R.P., Reis-Santos P., Maia A., et al. 2010. Nursery use patterns of commercially important marine fish species in estuarine systems along the Portuguese coast. Estuar. Coast. Shelf Sci. 86: 613-624. http://dx.doi.org/10.1016/j.ecss.2009.11.029

Wang Z., Gerstein M, Snyder M. 2009. RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10: 57-63 http://dx.doi.org/10.1038/nrg2484 PMid:19015660 PMCid:PMC2949280

Weir B.S., Cockerham C.C. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370. http://dx.doi.org/10.2307/2408641

Wood A.W., Duan C., Bern H.A. 2005. Insulin-like growth factor signaling in fish. Internat. Rev. Cytol. 243: 215-285. http://dx.doi.org/10.1016/S0074-7696(05)43004-1




Copyright (c) 2014 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.


Contact us scimar@icm.csic.es

Technical support soporte.tecnico.revistas@csic.es