Advertisement

Marine Biology

, Volume 162, Issue 3, pp 515–538 | Cite as

From the laboratory to the wild: salinity-based genetic differentiation of the European sea bass (Dicentrarchus labrax) using gene-associated and gene-independent microsatellite markers

  • Bruno GuinandEmail author
  • Nolwenn Quéré
  • Erick Desmarais
  • Jacques Lagnel
  • Costas S. Tsigenopoulos
  • François Bonhomme
Original Paper

Abstract

Convincing evidence reporting adaptive variation for physiologically and/or ecologically important traits in marine taxa is often derived from studies comparing field and laboratory observations and based on candidate-gene markers, mainly allozymes, responding to habitat selection. Likewise, patterns of genetic differentiation between sea and lagoon populations of the euryhaline European sea bass (Dicentrarchus labrax) were shown to correlate with changes in allele frequencies recorded during experimental salinity challenges, suggesting potential role for local adaptation. However, there has been criticism of these past approaches, causing a need for further investigation. We reinvestigated this correlation in European sea bass using a set of 20 micro- and one minisatellite markers, some of which are associated with candidate genes. We used rigorous experimental settings to demonstrate that only one single gene-associated marker consistently reported significant genetic differentiation between fish raised in seawater compared to fish acclimated to freshwater (locus EIF3E; F ST = 0.060; p = 0.007, n = 268). A few other loci were shown to be false positive and did not respond to selection. Furthermore, a field study of sea–lagoon differentiation in wild European sea bass (n = 144) using the same loci reported marginally significant genetic differentiation at locus EIF3E (F ST = 0.0114, p = 0.068). This locus was identified as putatively under selection. Two other microsatellite loci associated with genes (DLA0070 and DLA0060, respectively) were found to significantly participate to sea–lagoon differentiation and deviate from neutral expectation. The evidence for sea–lagoon local adaptation in sea bass remains faint if not highly elusive.

Keywords

Genetic Differentiation Significant Genetic Differentiation Before Present Allozymic Locus Lagoon Sample 
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.

Notes

Acknowledgments

Authors wish to thank G. Charmantier and D.M. Rand for constructive advices on results presented in this paper, and M. Cantou and M. Benezech for participating in sea bass sampling. G. Esposito provided help during the acclimation experiment. A. Escalas provided the graphical basis necessary to Fig. 1. We are grateful to J. Bohling for English language editing. Genetic data were produced at facilities of the HCMR and of the LabEx CeMEB (Centre Méditerranéen Environnement Biodiversité).

Supplementary material

227_2014_2602_MOESM1_ESM.pdf (17 kb)
Supplementary material 1 (PDF 17 kb)

References

  1. Addison JA, Ort BS, Mesa KA, Pogson GH (2008) Range-wide genetic homogeneity in the California sea mussel (Mytilus californianus): a comparison of allozymes, nuclear DNA markers, and mitochondrial DNA sequences. Mol Ecol 17:4222–4232Google Scholar
  2. Allegrucci G, Fortunato C, Cataudella S, Sbordoni V (1994) Acclimation to fresh water of the sea bass: evidence of selective mortality and allozyme genotypes. In: Beaumont AR (ed) Genetics and evolution of marine organisms. Chapman and Hall, London, pp 486–502Google Scholar
  3. Allegrucci G, Caccone A, Cataudella S, Powell J, Sbordoni V (1995) Acclimation of the European sea bass to freshwater: monitoring genetic changes by RAPD polymerase chain reaction to detect DNA polymorphisms. Mar Biol 121:591–599Google Scholar
  4. 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 128:347–358Google Scholar
  5. Almuly R, Poleg-Danin Y, Gorshkov S, Gorshkova G, Rapoport B, Soller M, Kashi Y, Funkenstein B (2005) Characterization of the 5′ flanking region of the growth hormone gene of the marine teleost, gilthead sea bream Sparus aurata: analysis of a polymorphic microsatellite in the proximal promoter. Fish Sci 71:479–490Google Scholar
  6. Almuly R, Skopal F, Funkenstein B (2008) Regulatory regions in the promoter and first intron of Sparus aurata growth hormone gene: repression of gene activity by a polymorphic minisatellite. Comp Biochem Physiol D3:43–50Google Scholar
  7. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410Google Scholar
  8. Andersen Ø (2012) Hemoglobin polymorphisms in Atlantic cod—a review of 50 years of studies. Mar Genomics 8:59–65Google Scholar
  9. Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a F st-outlier method. BMC Bioinf 9:323Google Scholar
  10. Barnabé G (1980) Exposé synoptique des données biologiques sur le loup ou bar (Dicentrarchus labrax). Synopsis FAO sur les Pêches. FAO, RomeGoogle Scholar
  11. Barnes RSK (1980) Coastal lagoons. Cambridge University Press, CambridgeGoogle Scholar
  12. Barrett RDH, Hoekstra HE (2011) Molecular spandrels: tests of adaptation at the genetic levels. Nat Rev Genet 12:767–780Google Scholar
  13. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Biol Sci 263:1619–1626Google Scholar
  14. Behrmann-Godel J, Gerlach G, Eckmann R (2006) Kin and population recognition in sympatric Lake Constance perch (Perca fluviatilis L.): can assortative shoaling drive population divergence? Behav Ecol Sociobiol 59:451–468Google Scholar
  15. Bekkevold D, André C, Dahlgren TG, Clause LAW, Torstesen E, Moegaard H, Carvalho GR, Christensen TB, Norlinder E, Ruzzante DE (2005) Environmental correlates of population differentiation in Atlantic herring. Evolution 59:2656–2668Google Scholar
  16. Belkhir K, Castric V, Bonhomme F (2002) IDENTIX, a software to test for relatedness in a population using permutation methods. Mol Ecol Notes 2:611–614Google Scholar
  17. Bell TM, Strand AE, Sotka EE (2014) The adaptive cline at LDH (lactate dehydrogenase) in killifish Fundulus heteroclitus remains stationary after 40 years of warming estuaries. J Hered 105:566–571Google Scholar
  18. Benjamini Y, Yukitieli D (2001) The control of false discovery rate under dependency. Ann Stat 29:1165–1188Google Scholar
  19. Bierne N, Bonhomme F, David P (2003) Habitat preference and the marine speciation paradox. Proc R Soc Biol Sci 270:1399–1406Google Scholar
  20. Bierne N, Gagnaire PA, David P (2013) The geography of introgression in a patchy environment and the thorn in the side of ecological speciation. Curr Zool 59:72–86Google Scholar
  21. Blaber SJM, Blaber TG (1980) Factors affecting the distribution of juvenile estuarine and inshore fishes. J Fish Biol 17:143–162Google Scholar
  22. Blel H, Panfili J, Guinand B, Berrebi P, Said K, Durand JD (2010) S election 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 210:60–67Google Scholar
  23. Borsa P, Millet B (1992) Recruitment of the clam Ruditapes decussatus in the lagoon of Thau, Mediterranean. Estuar Coast Shelf Sci 35:289–300Google Scholar
  24. Bouchereau JL, Guélorget O (1998) Comparison of three Gobiidae (Teleostei) life history strategies over their geographical range. Oceanol Acta 21:503–516Google Scholar
  25. Boutet I, Ky CL, Bonhomme F (2006) A transcriptomic approach of salinity response in the euryhaline teleost, Dicentrarchus labrax. Gene 379:40–50Google Scholar
  26. Boutet I, Lorin-Nebel C, De Lorgeril J, Guinand B (2007) Molecular characterisation of prolactin and analysis of extrapituitary expression in the European sea bass Dicentrarchus labrax under various salinity conditions. Comp Biochem Physiol D2:74–83Google Scholar
  27. Boutet I, Quéré N, Lecomte F, Agnèse JF, Guinand B (2008) Putative transcription factor binding sites and polymorphisms in the proximal promoter of the PRL—a gene in percomorphs and European sea bass (Dicentrarchus labrax). Mar Ecol 29:354–364Google Scholar
  28. Bradbury IR, Hubert S, Higgins B, Borza T, Bowman S, Paterson IG, Snelgrove PVR, Morris CJ, Gregory RS, Hardie DC, Hutchings JA, Ruzzante DE, Taggart CT, Bentzen P (2010) Parallel adaptive evolution of Atlantic cod on both side of the Atlantic Ocean in response to temperature. Proc R Soc Biol Sci 277:3725–3734Google Scholar
  29. Brind’Amour A, Bourget E, Tremblay R (2002) Fecundity, growth rate and survivorship at the interface between two contiguous genetically distinct groups of Semibalanus balanoides. Mar Ecol Progr Ser 229:173–184Google Scholar
  30. Buehler D, Holderegger R, Brodbeck S, Schnyder E, Gugerli F (2014) Validation of outlier loci through replication of independent data sets: a test on Arabis alpina. Ecol Evol. doi: 10.1002/ece3.1300 Google Scholar
  31. Burton RS, Ellison CK, Harrison JS (2006) The sorry state of F2 hybrids: consequences of rapid mitochondrial DNA evolution in allopatric populations. Am Nat 168:S14–S24Google Scholar
  32. Caccone A, Allegrucci G, Fortunato C, Sbordoni V (1997) Genetic differentiation within the European sea bass (D. labrax) as revealed by RAPD–PCR assays. J Hered 88:316–324Google Scholar
  33. Carvalho GR (1993) Evolutionary aspects of fish distribution—genetic variability and adaptation. J Fish Biol 43:53–73Google Scholar
  34. Castric V, Bernatchez L, Belkhir K, Bonhomme F (2002) Heterozygote deficiencies in small lacustrine populations of brook charr Salvelinus fontinalis Mitchill (Pisces, Salmonidae): a test of alternative hypotheses. Heredity 89:27–35Google Scholar
  35. Chaoui L, Gagnaire PA, Guinand B, Quignard JP, Tsigenopoulos C, Kara MH, Bonhomme F (2012) Microsatellite length variation in candidate genes correlates with habitat in the gilthead sea bream Sparus aurata. Mol Ecol 21:5497–5511Google Scholar
  36. Cimmaruta R, Bondanelli P, Nascetti G (2005) Genetic structure and environmental heterogeneity in the European hake (Merluccius merluccius). Mol Ecol 14:2577–2591Google Scholar
  37. Conover DO, Clarke LM, Munch SB, Wagner GN (2006) Spatial and temporal scales of adaptive divergence in marine fishes and the implications for conservation. J Fish Biol 69:S21–S47Google Scholar
  38. Coyer JA, Hoarau B, Pearson G, Mota C, Jüterbock A, Alpermann T, John U, Olsen JL (2011) Genomic scans detect signatures of selection along a salinity gradient in populations of the intertidal seaweed Fucus serratus on a 12 km scale. Mar Genomics 4:41–49Google Scholar
  39. Cui CY, Childress V, Piao Y, Michel M, Johnson AA, Kunisada M, Ko MSH, Kaestner KH, Marmorstein AD, Schlessinger D (2012) Forkhead transcription factor FoxA1 regulates sweat secretion through Bestrophin 2 anion channel and Na–K–Cl cotransporter 1. Proc Natl Acad Sci USA 109:1199–1203Google Scholar
  40. David P, Perdieu MA, Pernot AF, Jarne P (1997) Fine-grained spatial and temporal population genetic structure in the marine bivalve Spisula ovalis L. Evolution 51:1318–1322Google Scholar
  41. Day AJ (1990) Microgeographic variation in allozyme frequencies in relation to the degree of exposure to wave action in the dogwelk Nucella lapillus (L) (Prosobranchia, Muricacea). Biol J Linn Soc 40:245–261Google Scholar
  42. DeFaveri J, Shikano T, Shimada Y, Merilä J (2013) High degree of genetic differentiation in marine three-spined sticklebacks (Gasterosteus aculeatus). Mol Ecol 22:4811–4828Google Scholar
  43. Dufour V, Cantou M, Lecomte F (2009) Identification of sea bass (Dicentrarchus labrax) nursery areas in the north-western Mediterranean Sea. J Mar Biol Assoc UK 89:1367–1374Google Scholar
  44. Dufresne F, Bourget E, Bernatchez L (2002) Differential patterns of spatial divergence in microsatellite and allozyme alleles: further evidence for locus-specific selection in the acorn barnacle, Semibalanus balanoides? Mol Ecol 11:113–123Google Scholar
  45. Flight PA, Rand DM (2012) Genetic variation in the acorn barnacle from allozymes to population genomics. Integr Comp Biol 52:418–429Google Scholar
  46. Flight PA, Schoepfer SD, Rand DM (2010) Physiologial stress and the fitness effects of Mpi genotypes in the acorn barnacle Semibalanus balanoïdes. Mar Ecol Progr Ser 404:139–149Google Scholar
  47. Fourcade Y, Chaput-Bardy A, Secondi J, Fleurant C, Lemaire C (2013) Is local selection so widespread in river organisms? Fractal geometry of river networks leads to high bias in outlier detection. Mol Ecol 22:2065–2073Google Scholar
  48. Gagnaire PA, Normandeau E, Côté C, Hansen MM, Bernatchez L (2012) The genetic consequences of spatially varying selection in the panmictic American eel (Anguilla rostrata). Genetics 190:725–736Google Scholar
  49. Galindo J, Morán P, Rolán-Alvarez E (2009) Comparing geographical genetic differentiation between candidate and noncandidate loci for adaptation strengthens support for parallel ecological divergence in the marine snail Littorina saxatilis. Mol Ecol 18:919–930Google Scholar
  50. García F, Zalba G, Páez G, Encío I, de Miguel C (1998) Molecular cloning and characterization of the human p44 mitogen-activated protein kinase gene. Genomics 50:69–78Google Scholar
  51. Gemayel R, Vinces MD, Legendre M, Verstrepen KJ (2010) Variable tandem repeats accelerate evolution of coding and regulatory sequences. Ann Rev Genet 44:445–477Google Scholar
  52. González-Wangüemert G, Pérez-Ruzafa Á (2012) In two waters: contemporary evolution of lagoonal and marine white seabream (Diplodus sargus) populations. Mar Ecol 33:337–349Google Scholar
  53. González-Wangüemert M, Vergara-Chen C (2014) Environmental variables, habitat discontinuity and life history shaping the genetic structure of Pomatoschistus minutus. Helgol Mar Res 68:357–371Google Scholar
  54. Gosling E, Astanei I, Was A (2008) Genetic variability in Irish populations of the invasive zebra mussel, Dreissena polymorpha: discordant estimates of population differentiation from allozymes and microsatellites. Freshw Biol 53:1303–1315Google Scholar
  55. Gouttenoire J, Valcourt U, Bougault C, Aubert-Foucher E, Arnaud E, Giraud L, Mallein-Gerin L (2007) Knockdown of the intraflagellar transport protein IFT46 stimulates selective gene expression in mouse chondrocytes and affects early development in zebrafish. J Biol Chem 282:30960–30973Google Scholar
  56. Green EM, Barrett CF, Bultynck G, Shamah SM, Dolmetsch RE (2007) The tumor suppressor eIF3e mediates calcium-dependent internalization of the L-type calcium channel CaV1.2. Neuron 55:615–632Google Scholar
  57. Guinand B, Dujardin E, Dufour V, Tsigenopoulos C (2008) Characterisation of genetic structure of Dicentrarchus labrax larvae in two nurseries of the Gulf of Lions (NW Mediterranean). Aquat Living Resour 21:81–87Google Scholar
  58. Guinand B, Quéré N, Desmarais E, Cerqueira F, Bonhomme F (2014) Fitness difference between cryptic salinity-related phenotypes of sea bass (Dicentrarchus labrax). Sci Mar 78:493–503Google Scholar
  59. Hauser L, Carvalho GR (2008) Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish Fish 9:333–362Google Scholar
  60. Hellberg ME (2009) Gene flow and isolation among populations of marine animals. Ann Rev Ecol Evol Syst 40:310–491Google Scholar
  61. Hemmer-Hansen J, Nielsen EE, Frydenberg J, Loeschcke V (2007) Adaptive divergence in a high gene flow environment: Hsc70 variation in the European flounder (Platichthys flesus L.). Heredity 99:592–600Google Scholar
  62. Hilbish TJ, Koehn RK (1985) Dominance in physiological phenotypes and fitness at an enzyme locus. Science 229:52–54Google Scholar
  63. Hinnesbush AG (2006) eIF3: a versatile scaffold for translation initiation complexes. Trends Biochem Sci 31:553–562Google Scholar
  64. Hofer T, Ray N, Wegmann D, Excoffier L (2009) Large allele frequency differences between human continental groups are more likely to have occurred by drift during range expansions than by selection. Ann Hum Genet 73:95–108Google Scholar
  65. Ifremer (2005) Réseau de Suivi Lagunaire du Languedoc-Roussillon: Bilan des Résultats 2005. Rapport RSL-06/2006Google Scholar
  66. Ifremer (2008) Réseau de Suivi Lagunaire du Languedoc-Roussillon: Bilan des résultats 2007. Rapport RSL-08/2008Google Scholar
  67. Ishida N, Yoshioka S, Chiba Y, Takeuchi M, Kawakita M (1999) Molecular cloning and functional expression of the human Golgi UDP-N-acetylglucosamine transporter. J Biochem 126:68–77Google Scholar
  68. Janssens V, Goris J (2001) Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 353:417–439Google Scholar
  69. Johannesson K, Johannesson B (1989) Differences in allele frequencies of Aat between high-rocky and mid-rocky shore populations of Littorina saxatilis (Olivi) suggest selection in this enzyme locus. Genet Res 54:7–11Google Scholar
  70. Jones O, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Res 10:551–555Google Scholar
  71. Kelley DF (1988) The importance of estuaries for sea bass, Dicentrarchus labrax (L.). J Fish Biol 33:25–33Google Scholar
  72. Kirby RR, Bayne BL, Berry RJ (1994) Phenotypic variation along a cline in allozyme and karyotype frequencies, and its relationship with habitat, in the dogwhelk Nucella lapillus, L. Biol J Linn Soc 53:255–275Google Scholar
  73. Koehn RK, Newell RI, Immermann F (1980) Maintenance of an aminopeptidase allele frequency cline by natural selection. Proc Natl Acad Sci USA 77:5385–5389Google Scholar
  74. Kuhl H, Beck A, Wozniak G, Canario A, Volckaert F, Reinhardt R (2010) The European sea bass Dicentrarchus labrax genome puzzle: comparative BAC-mapping and low coverage shotgun sequencing. BMC Genomics 11:68Google Scholar
  75. Kultz D (1998) Phylogenetic and functional classification of mitogen- and stress-activated protein kinases. J Mol Evol 46:571–588Google Scholar
  76. Ky C, de Lorgeril J, Hirtz C, Sommerer N, Rossignol M, Bonhomme F (2007) The effect of environmental salinity on the proteome of the sea bass (Dicentrarchus labrax L.). Anim Genet 38:601–608Google Scholar
  77. Larmuseau MHD, Raeymaekers JAM, Ruddick KG, Van Houdt JKJ, Volckaert FAM (2009) To see in different seas: spatial variation in the rhodopsin gene of the sand goby (Pomatoschistus minutus). Mol Ecol 18:4227–4239Google Scholar
  78. Lefebvre AK, Korneeva NL, Trutschl M, Cvek U, Duzan RD, Bradley CA, Hershey JWB, Rhoads RE (2006) Translation initiation factor eIF4G-1 binds to eIF3 through the eIF3e subunit. J Biol Chem 281:22917–22932Google Scholar
  79. Lemaire C, Allegrucci G, Naciri M, Bahri-Sfar L, Kara H, Bonhomme F (2000) Do discrepancies between microsatellite and allozyme variation reveal differential selection between sea and lagoon in the sea bass (Dicentrarchus labrax)? Mol Ecol 9:457–467Google Scholar
  80. Li X, Bai J, Ye X, Hu Y, Li S, Yu L (2009) Polymorphisms in the 5′ flanking region of the insulin-like growth factor I gene are associated with growth traits in largemouth bass Micropterus salmoides. Fish Sci 75:351–358Google Scholar
  81. Li L, Dong X, Leong MC, Zhou W, Yang Z, Cheng F, Bao Y, Jia W, Hu R (2010) Identification of the novel protein FAM172A, and its up-regulation by high glucose in human aortic smooth muscle cells. Int J Mol Med 26:483–490Google Scholar
  82. Limborg MT, Helyar SJ, De Bruyn M, Taylor MI, Nielsen EE, Ogden R, Carvalho G, FPT Consortium, Bekkevold D (2012) Environmental selection on transcriptome-derived SNPs in a high gene flow marine fish, the Atlantic herring (Clupea harengus). Mol Ecol 21:3686–3703Google Scholar
  83. Lorin-Nebel C, Boulot V, Bodinier C, Charmantier G (2006) The Na+/K+/2Cl cotransporter in the sea bass Dicentrarchus labrax ontogeny: involvement in osmoregulation. J Exp Biol 209:4908–4922Google Scholar
  84. Lotterhos KE, Whitlock MC (2014) Evaluation of demographic history and neutral parameterization on the performance of F ST outlier tests. Mol Ecol 23:2178–2192Google Scholar
  85. Magnanou E, Klopp C, Noirot C, Besseau L, Falcón J (2014) Generation and characterization of the sea bass Dicentrarchus labrax brain and liver transcriptomes. Gene 544:56–66Google Scholar
  86. Mäkinen HS, Cano JM, Merilä J (2008) Identifying footprints of directional and balancing selection in marine and freshwater three-spined stickleback (Gasterosteus aculeatus) populations. Mol Ecol 17:3565–3582Google Scholar
  87. Marino G, Cataldi E, Pucci P, Bronzi P, Cataudella S (1994) Acclimation trials of wild and hatchery sea bass (Dicentrarchus labrax) fry at different salinities. J Appl Ichthyol 10:57–63Google Scholar
  88. Marino IAM, Barbisan F, Gennari M, Giomi F, Beltramini M, Biol PM, Zane L (2010) Genetic heterogeneity in populations of the Mediterranean shore crab, Carcinus aestuarii (Decapoda, Portunidae), from the Venice Lagoon. Estuar Coast Shelf Sci 87:135–144Google Scholar
  89. McCairns RJS, Bernatchez L (2008) Landscape genetic analyses reveal cryptic population structure and putative selection gradients in a large-scale estuarine environment. Mol Ecol 17:3901–3916Google Scholar
  90. Milano I, Babbucci M, Cariani A, Atanassova M, Bekkevold D, Carvalho GR, Espiñeira M, Fiorentino F, Garofalo G, Geffen AJ, Hansen JH, Helyar SJ, Nielsen EE, Ogden R, Patarnello T, Stagioni M, FishPopTrace Consortium, Tinti F, Bargelloni L (2014) Outlier SNP markers reveal fine-scale genetic structuring across European hake populations (Merluccius merluccius). Mol Ecol 23:118–135Google Scholar
  91. Nebel C, Romestand B, Nègre-Sadargues G, Grousset E, Aujoulat F, Bacal J, Bonhomme F, Charmantier G (2005) Differential freshwater adaptation in juvenile sea-bass Dicentrarchus labrax: involvement of gills and urinary system. J Exp Biol 208:3859–3871Google Scholar
  92. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  93. Nielsen EE, Hemmer-Hansen J, Larsen PF, Bekkevold D (2009) Population genomics of marine fishes: identifying adaptive variation in space and time. Mol Ecol 18:3128–3150Google Scholar
  94. Nordeide JT, Johansen SD, Jørgensen TE, Karlsen BO, Moum T (2011) Population connectivity among migratory and stationary cod Gadus morhua in the Northeast Atlantic—a review of 80 years of study. Mar Ecol Progr Ser 435:269–283Google Scholar
  95. Nosil P, Funk DJ, Ortiz-Barrientos D (2009) Divergent selection and heterogeneous genomic divergence. Mol Ecol 18:375–402Google Scholar
  96. O’Driscoll KE, Hatton WJ, Burkin HR, Leblanc N, Britton FC (2008) Expression, localization, and functional properties of Bestrophin 3 channel isolated from mouse heart. Am J Physiol Cell Physiol 295:C1610–C1624Google Scholar
  97. Oleksiak MF (2010) Genomic approaches with natural fish populations. J Fish Biol 76:1067–1093Google Scholar
  98. Olsen MT, Pampoulie C, Daníelsdóttir AK, Lidh E, Bérubé M, Víkingsson GA, Palsbøll PJ (2014) Fin whale MDH-1 and MPI allozyme variation is not reflected in the corresponding DNA sequences. Ecol Evol 4:1787–1803Google Scholar
  99. Pampoulie C, Gysels ES, Maes GE, Hellemans B, Leentjes V, Jones AG, Volckaert FAM (2004) Evidence for fine-scale genetic structure and estuarine colonisation in a potential high gene flow marine goby (Pomatoschistus minutus). Heredity 92:434–445Google Scholar
  100. Pampoulie C, Jakobsdóttir KB, Marteinsdóttir G, Thorsteinsson V (2008) Are vertical behaviour patterns related to the Pantophysin locus in the Atlantic cod (Gadus morhua L.)? Behav Genet 38:76–81Google Scholar
  101. Pascoal S, Carvalho G, Creer S, Rock J, Kawaii K, Mendo S, Hughes R (2012) Plastic and heritable components of phenotypic variation in Nucella lapillus: an assessment using reciprocal transplant and common garden experiments. PLoS One 7:e30289Google Scholar
  102. Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855Google Scholar
  103. Queller D, Goodnight K (1989) Estimating relatedness using genetic markers. Evolution 43:258–275Google Scholar
  104. Quéré N, Guinand B, Kuhl H, Reinhardt R, Bonhomme F, Desmarais E (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 23:285–296Google Scholar
  105. Quéré N, Desmarais E, Tsigenopoulos CS, Belkhir K, Bonhomme F, Guinand B (2012) Gene flow at major transitional areas in sea bass (Dicentrarchus labrax) and the possible emergence of a hybrid swarm. Ecol Evol 2:3061–3078Google Scholar
  106. Quignard JP, Man-Wai R, Vianet R (1984) Les poissons de l’Etang de Mauguio (Hérault, France) inventaire, structure du peuplement, croissance et polymorphisme des tailles. Vie Milieu 34:173–183Google Scholar
  107. Raeymaekers JAM, Joost AM, Van Houdt JKJ, Larmuseau MHD, Geldof S, Volckaert FAM (2007) Divergent selection as revealed by PST and QTL-based FST in three-spined stickleback (Gasterosteus aculeatus) populations along a coastal-inland gradient. Mol Ecol 16:891–905Google Scholar
  108. Roesti M, Hendry AP, Salzburger W, Berner D (2012) Genome divergence during evolutionary diversification as revealed in replicate lake-stream stickleback population pairs. Mol Ecol 21:2852–2862Google Scholar
  109. Sabatier P, Dezileau L, Barbier M, Raynal O, Lofi J, Briqueu L, Condomines M, Bouchette F, Certain R, Van Grafenstein U, Jorda C, Blanchemanche P (2010) Late-Holocene evolution of coastal lagoon system in the Gulf of Lions (South of France). Bull Soc Géol Fr 181:7–36Google Scholar
  110. Sánchez-Ramos I, Cross I, Mácha J, Martínez-Rodríguez G, Krylov V, Rebordinos L (2012) Assessment of tools for marker-assisted selection in a marine commercial species: significant association between MSTN-1 gene polymorphism and growth traits. Sci World J 2012:369802Google Scholar
  111. Sanford E, Kelly MW (2011) Local adaptation in the sea. Ann Rev Mar Sci 3:509–535Google Scholar
  112. Savolainen O, Lacoux M, Merilä J (2013) Ecological genomics of local adaptation. Nat Rev Genet 14:807–820Google Scholar
  113. Schmidt PS, Rand DM (1999) Intertidal microhabitat and selection at MPI: interlocus contrasts in the northern acorn barnacle, Semibalanus balanoides. Evolution 53:135–146Google Scholar
  114. Schmidt PS, Bertness MD, Rand DM (2000) Environmental heterogeneity and balancing selection in the acorn barnacle Semibalanus balanoides. Proc R Soc Biol Sci 267:379–384Google Scholar
  115. Schoville SD, Flowers JM, Burton RS (2012) Diversifying selection underlies the origin of allozyme polymorphism at the phosphoglucose isomerase locus in Tigriopus californicus. PLoS One 7:e40035Google Scholar
  116. Schulte PM, Glémet HC, Fiebig AA, Powers DA (2000) Adaptive variation in the lactate dehydrogenase-B gene expression: role of a stress-responsive regulatory element. Proc Natl Acad Sci USA 97:6597–6602Google Scholar
  117. 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 27:2775–2789Google Scholar
  118. Shimada Y, Shikano T, Merilä J (2011) A high incidence of selection on physiologically important genes in the three-spined stickleback, Gasterosteus aculeatus. Mol Biol Evol 28:181–193Google Scholar
  119. Siridechadilok B, Fraser CS, Hall RJ, Doudna JA, Nogales E (2005) Structural roles for human translation factor eIF3 in initiation of protein synthesis. Science 310:1513–1515Google Scholar
  120. Streelman JT, Kocher TD (2002) Microsatellite variation associated with prolactin expression and growth of salt-challenged tilapia. Physiol Genom 9:1–4Google Scholar
  121. Tao WJ, Boulding EG (2003) Associations between single nucleotide polymorphisms in candidate genes and growth rate in Arctic charr (Salvelinus alpinus L.). Heredity 91:60–69Google Scholar
  122. Tine M, Kuhl H, Gagnaire PA, Louro B, Desmarais E, Martins RST, Hecht J, Knaust F, Belkhir K, Klages S, Dieterich R, Stueber K, Pfiferrer F, Guinand B, Bierne N, Volckaert FAM, Bargelloni L, Power DM, Bonhomme F, Canario AVM, Reinhardt R (2014) The European sea bass genome and its variation provide insights into adaptation to euryhalinity and marine speciation. Nat Commun. doi: 10.1038/ncomms6770 Google Scholar
  123. Vandamme SG, Maes GE, Raeymaekers JAM, Cottnie K, Imsland AK, Hellemans B, Lacroix G, Mac Aoidh E, Martinsohn JT, Martínez P, Robbens J, Vilas R, Volckaert FAM (2014) Regional environmental pressure influences population differentiation in turbot (Scophthalmus maximus). Mol Ecol 23:618–636Google Scholar
  124. Varsamos S, Xuereb B, Commes T, Flik G, Spanings-Pierrot C (2006) Pituitary hormone mRNA expression in European sea bass Dicentrarchus labrax in seawater and following acclimation to fresh water. J Endocrinol 191:473–480Google Scholar
  125. Vasemägi A, Nilsson J, Primmer CR (2005) Expressed sequence tag-linked microsatellites as a source of gene-associated polymorphisms for detecting signatures of divergent selection in Atlantic salmon (Salmo salar L.). Mol Biol Evol 22:1067–1076Google Scholar
  126. Vasioukhin V (2006) Lethal giant puzzle of Lgl. Dev Neurosci 28:13–24Google Scholar
  127. Vergara-Chen C, González-Wangüemert M, Marcos C, Pérez-Ruzafa Á (2010) Genetic diversity and connectivity remain high in Holothuria polii (Delle Chiaje 1823) across a coastal lagoon-open sea environmental gradient. Genetica 138:895–906Google Scholar
  128. Vergara-Chen C, González-Wangüemert M, Marcos C, Pérez-Ruzafa Á (2013) Small-scalegenetic structure of Cerastoderma glaucum in a lagoonal environment: potential significance of habitat discontinuity and unstable population dynamics. J Moll Stud 79:230–240Google Scholar
  129. Vitalis R, Dawson K, Boursot P (2001) Interpretation of variation across marker loci as evidence of selection. Genetics 158:1811–1823Google Scholar
  130. Vitalis R, Dawson K, Boursot P, Belkhir K (2003) DetSel 1.0: a computer program to detect markers responding to selection. J Hered 94:429–431Google Scholar
  131. Vizzini S, Savona B, Do Chi T, Mazzola A (2005) Spatial variability of stable carbon and nitrogen isotope ratios in a Mediterranean coastal lagoon. Hydrobiologia 550:73–82Google Scholar
  132. Volckaert FAM, Hellemans B, Batargias C, Louro B, Massault C, Van Houdt JKJ, Haley C, de Koning DJ, Canario AVM (2012) Heritability of cortisol response to confinement stress in European sea bass Dicentrarchus labrax. Genet Sel Evol 44:15Google Scholar
  133. Wang J (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166:1963–1979Google Scholar
  134. Wang J (2010) Effects of genotyping errors on parentage exclusion analysis. Mol Ecol 19:5061–5078Google Scholar
  135. Wang L, Liu S, Zhuang Z, Guo G, Meng Z, Lin H (2013) Population genetic studies revealed local adaptation in a high gene-flow marine fish, the small yellow croaker (Larimichthys polyactis). PLoS One 8:e83493Google Scholar
  136. Ward RD, Woodwark M, Skibinski DOF (1994) A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. J Fish Biol 44:213–232Google Scholar
  137. Weir BS (1979) Inferences about linkage disequilibrium. Biometrics 35:235–254Google Scholar
  138. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370Google Scholar
  139. Williams LM, Oleksiak MF (2011) Evolutionary and functional analyses of cytochrome P4501A promoter polymorphisms in natural populations. Mol Ecol 20:5236–5247Google Scholar
  140. Wilson RW, Wilson JM, Grosell M (2002) Intestinal bicarbonate secretion by marine teleost fish—why and how? Bioch Biophys Acta 1566:182–193Google Scholar
  141. Wodarz A (2000) Tumor suppressors: linking cell polarity and growth control. Curr Biol 10:R624–R626Google Scholar
  142. Yeaman S, Otto SP (2011) Establishment and maintenance of adaptive genetic divergence under migration, selection, and drift. Evolution 65:2123–2129Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Bruno Guinand
    • 1
    • 2
    • 5
    Email author
  • Nolwenn Quéré
    • 1
    • 2
  • Erick Desmarais
    • 1
    • 3
  • Jacques Lagnel
    • 4
  • Costas S. Tsigenopoulos
    • 4
  • François Bonhomme
    • 1
    • 2
  1. 1.CNRS-UMR 5554, Institut des Sciences de l’EvolutionUniversité Montpellier 2Montpellier Cedex 5France
  2. 2.Station Méditerranéenne de l’Environnement LittoralUniversité Montpellier 2SèteFrance
  3. 3.Montpellier Environnement BiodiversitéUniversité Montpellier 2Montpellier Cedex 5France
  4. 4.Institute of Marine Biology and GeneticsHellenic Center for Marine ResearchHeraklion, CreteGreece
  5. 5.CNRS-UMR 5554, Institut des Sciences de l’Evolution de MontpellierUniversité Montpellier 2Montpellier Cedex 5France

Personalised recommendations