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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

Published online by Cambridge University Press:  04 October 2010

Nolwenn Quéré ,
Bruno Guinand ,
Heiner Kuhl ,
Richard Reinhardt ,
François Bonhomme  and
Erick Desmarais
Nolwenn Quéré
Affiliation:
Université Montpellier 2, Biologie intégrative, Institut des Sciences de l’Evolution de Montpellier, CNRS-UMR 5554, CC 63, 34095 Montpellier Cedex 5, France
Bruno Guinand*
Affiliation:
Université Montpellier 2, Biologie intégrative, Institut des Sciences de l’Evolution de Montpellier, CNRS-UMR 5554, CC 63, 34095 Montpellier Cedex 5, France Station Méditerranéenne de l’Environnement Littoral, 1 quai de la Daurade, 34200 Sète, France
Heiner Kuhl
Affiliation:
Max-Planck-Institute Molecular Genetics , Ihnestrasse 63-73, 14195 Berlin-Dahlem, Germany
Richard Reinhardt
Affiliation:
Max-Planck-Institute Molecular Genetics , Ihnestrasse 63-73, 14195 Berlin-Dahlem, Germany
François Bonhomme
Affiliation:
Université Montpellier 2, Biologie intégrative, Institut des Sciences de l’Evolution de Montpellier, CNRS-UMR 5554, CC 63, 34095 Montpellier Cedex 5, France Station Méditerranéenne de l’Environnement Littoral, 1 quai de la Daurade, 34200 Sète, France
Erick Desmarais
Affiliation:
Université Montpellier 2, Biologie intégrative, Institut des Sciences de l’Evolution de Montpellier, CNRS-UMR 5554, CC 63, 34095 Montpellier Cedex 5, France
*
a Corresponding author: bruno.guinand@univ-montp2.fr
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Abstract

The completion of genomic sequences of physiologically important genes frequently reveals non-coding genetic elements such as tandem repeats (micro- and minisatellites) that are often more polymorphic than nearby coding sequences. We obtained the complete genomic sequences of three hormone genes in sea bass Dicentrarchus labrax: growth hormone (dlGH), somatolactin (dlSL) and insulin-like growth factor-1 (dlIGF-1), including 5′- and 3′-untranslated regions. Mini- and microsatellites were discovered in both flanking and intron regions. Some were partially conserved across Perciformes. To assess the usefulness and relevance of these gene-associated markers for understanding population structure, an investigation was made on genetic diversity and differentiation at four of them in (i) five wild populations from the North Sea, the Bay of Biscay and the Western Mediterranean, and (ii) two samples of hatchery-bred individuals from a freshwater-acclimation experiment. Gene and allelic diversities were lower in cultured individuals than in wild ones. Significant genetic differentiation was demonstrated between Bay of Biscay + North Sea and Mediterranean populations (Fst > 0.06, p < 0.001), primarily due to dlGH-associated markers. Significant genetic differentiation was also detected among the Atlantic and North Sea samples, but restricted to the locus associated with dlSL. Significant genetic differentiation was also found among experimental individuals before and after a salinity challenge (Fst ≈ 0.05, p < 0.001), but was due to dlSL and dlIGF-1 loci. Gene-associated markers proved to be more efficient than formerly used anonymous microsatellite markers in providing a clear picture of genetic differentiation.

Keywords

Growth hormoneSomatolactinInsulin-like growth factor-1Non-coding regionsEuropean sea bassMicrosatellitesMinisatellites
Type
Research Article
Information
Aquatic Living Resources , Volume 23 , Issue 3 , July 2010 , pp. 285 - 296
Copyright
© EDP Sciences, IFREMER, IRD 2010

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References

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, 591–599. CrossRefGoogle Scholar
Allegrucci G., Fortunato C., Cataudella S., Sbordoni V., 1994, Acclimation to fresh water of the sea bass: evidence of selective motality and allozyme genotypes. In: Beaumont A.R. (ed.) Genetics and evolution of marine organisms, London, Chapman and Hall, pp. 486–502.
Allegrucci, G., Fortunato, C., Sbordoni, V., 1997, Genetic structure and allozyme variation of seabass (Dicentrarchus labrax and D. punctatus) in the Mediterranean Sea. Mar. Biol. 128, 347–358. CrossRefGoogle Scholar
Almuly, R., Cavari, B., Ferstman, H., Kolodny, O., Funkenstein, B., 2000, Genomic structure and sequence of the gilthead seabream (Sparus aurata) growth hormone-encoding gene: identification of minisatellite polymorphism in intron I. Genome 43, 836–845. CrossRefGoogle ScholarPubMed
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, 479–490. CrossRefGoogle Scholar
Almuly, R., Skopal, T., 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, 43–50. Google Scholar
Bahri-Sfar, L., Lemaire, C., Ben Hassine, O.K., Bonhomme, F., 2000, Fragmentation of seabass populations in the western and eastern Mediterranean as revealed by microsatellite polymorphism. Proc. R. Soc. Lond. B Biol. Sci. 267, 929–935. CrossRefGoogle Scholar
Barnett K.R., Hopkins II R.L., Peyton D.K. 2007, A minisatellite in the growth hormone gene of Esocidae is derived from a single copy element in the salmonid genome. Copeia 2007, 205–211.
Benson, G., 1999, Tandem repeats finder: a program to analyze DNA sequences. Nucl. Acids Res. 27, 573–580. CrossRefGoogle ScholarPubMed
Blel, H., Panfili, J., Guinand, B., Berrebi, P., Said, K., Durand, J.-D., 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. CrossRefGoogle Scholar
Bonhomme, F., Naciri, M., Bahri-Sfar, L., Lemaire, C. 2002, Analyse comparée de la structure génétique de deux espèces de poissons marins apparentées et sympatriques Dicentrarchus labrax et Dicentrarchus punctatus . C. R. Biol. 325, 213–220. CrossRefGoogle Scholar
Bouck, A., Vision, T., 2007, The molecular ecologist’s guide to expressed sequence tags. Mol. Ecol. 16, 907–924. CrossRefGoogle ScholarPubMed
Chaoui, L., Kara, M.H., Quignard, J.P., Faure, E., Bonhomme, F., 2009, Forte différenciation génétique de la daurade Sparus aurata (L., 1758) entre les deux rives de la Méditerranée occidentale. C. R. Biol. 332, 329–335. CrossRefGoogle Scholar
Chatain, B., Chavanne, H., 2009, La génétique du bar (Dicentrarchus labrax, L.). Cah. Agric. 18: 249–255. Google Scholar
Chervinski, J., 1974, Sea Bass, Dicentrarchus labrax L. (Pisces, Serranidae), a “police fish” in fresh water ponds and its adaptability to various saline conditions. Bamidgeh 2, 110–113. Google Scholar
Chistiakov, D.A., Hellemans, B., Haley, C.S., Law, A.S., Tsigenopoulos, C.S., Kotoulas, G., Bertotto, D., Libertini, A., Volckaert, F.A.M., 2005, A microsatellite linkage map of the European sea bass Dicentrarchus labrax L. Genetics 170, 1821–1826. CrossRefGoogle ScholarPubMed
Chistiakov, D., Tsigenopoulos, C., Lagnel, J., Guo, Y., Hellemans, B., Haley, C., Volckaert, F.A.M., Kotoulas, G., 2008, A combined AFLP and microsatellite linkage map and pilot comparative genomic analysis of European sea bass Dicentrarchus labrax L. Anim. Genet. 39, 623–634. CrossRefGoogle Scholar
Company, R., Calduch-Giner, J.A., Mingarro, M., Pérez-Sánchez, J., 2000, CDNA cloning and sequence of European sea bass (Dicentrarchus labrax) somatolactin. Comp. Biochem. Physiol. B127, 183–192. CrossRefGoogle Scholar
Cossins, A.R., Crawford, D.L., 2005, Fish as models for environmental genomics. Nat. Rev. Genet. 6, 324–340. CrossRefGoogle Scholar
Dalziel, A.C., Rogers, S.M., Schulte, P.M., 2009, Linking genotypes to phenotypes and fitness: how mechanistic biology can inform molecular ecology. Mol. Ecol. 18, 4997–5017. CrossRefGoogle Scholar
Deane, E.E., Woo, N.Y.S., 2009, Modulation of fish growth hormone levels by salinity, temperature, pollutants and aquaculture related stress: a review. Rev. Fish. Biol. Fish. 19, 97–120. CrossRefGoogle Scholar
De-Santis, C., Jerry, D.R., 2007, Candidate growth genes in finfish - where should we be looking? Aquaculture 272, 22–38. CrossRefGoogle Scholar
DiMichele, L., Powers, D.A., 1982, Physiological-basis for swimming endurance differences between Ldh-B genotypes of Fundulus heteroclitus . Science 216, 1014–1016. CrossRefGoogle ScholarPubMed
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, 1367–1374. CrossRefGoogle Scholar
Feder, M.E., Mitchell-Olds, T., 2003, Evolutionary and ecological functional genomics. Nat. Rev. Genet. 4, 649–655. CrossRefGoogle ScholarPubMed
Fritsch, M., Morizur, Y., Lambert, E., Bonhomme, F., Guinand, B., 2007, Assessment of sea bass (Dicentrarchus labrax, L.) stock delimitation in the Bay of Biscay and the English Channel based on mark-recapture and genetic data. Fish. Res. 83, 123–132. CrossRefGoogle Scholar
Fromme, T., Hoffmann, C., Nau, K., Rozman, J., Reichwald, K., Utting, M., Platzer, M., Klingenspor, M., 2009, An intronic single base exchange leads to a brown adipose tissue-specific loss of Ucp3 expression and an altered body mass trajectory. Physiol. Genomics 38, 54–62. CrossRefGoogle Scholar
Giffard-Mena, I., Lorin-Nebel, C., Charmantier, G., Castille, R., Boulo, V., 2008, Adaptation of the sea-bass (Dicentrarchus labrax) to fresh water: role of aquaporins and Na+/K+-ATPases. Comp. Biochem. Physiol. A150, 332–338. CrossRefGoogle Scholar
Hall, T.A., 1999, BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 41, 95–98. Google Scholar
Hancock J.M., 1999, Microsatellites and other simple sequences: genomic context and mutational mechanisms. In: D.B. Goldstein, Schlötterer C. (Eds). Micosatelittes: evolution and applications, Oxford, Oxford University Press, pp. 1–9.
Huising, M.O., Kruiswijk, M., Flik, G., 2006, Phylogeny and evolution of class-I helical cytokines. J. Endocrinol. 189, 1–25. CrossRefGoogle Scholar
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. 3.0.CO;2-H>CrossRefGoogle Scholar
Kashi Y., Soller M., 1999, Functional roles of microsatellites and minisatellites. In: Micosatelittes: evolution and applications. In: D.B. Goldstein, Schlötterer C. (Eds). Micosatelittes: evolution and applications, Oxford, Oxford University Press, pp. 10–23.
Kelley, D.F., 1988, The importance of estuaries for sea-bass, Dicentrarchus labrax (L.). J. Fish Biol. 33, 25–33. CrossRefGoogle Scholar
Koehn, R.K., Bayne, B.L., Moore, M.N.,Siebenaller, J.F., 1980, Salinity related physiological and genetic differences between populations of Mytilus edulis . Biol. J. Linn. Soc. 14, 319–334. CrossRefGoogle Scholar
Kuhl, H., Beck, A., Wozniak, G., Canario, A., Volckaert, F., Reinhardt, R., 2010a, The European sea bass Dicentrarchus labrax genome puzzle: comparative BAC-mapping and low coverage shotgun sequencing. BMC Genomics 11, 68. CrossRefGoogle Scholar
Kuhl H., Tine M., Hecht J., Knaust F., Reinhardt R., 2010b, Analysis of single nucleotide polymorphisms in three chromosomes of European sea bass Dicentrarchus labrax. Comp. Biochem. Physiol. D [doi: 10.1016/j.cbd.2010.04.003]
Laiz-Carrión, R., Fuentes, J., Redruello, B., Guzmán, J.M., Martín del Río, M.P., Power, D., Mancera, J.M., 2009, Expression of pituitary prolactin, growth hormone and somatolactin is modified in response to different stressors (salinity, crowding and food-deprivation) in gilthead sea bream Sparus auratus . Gen. Comp. Endocrinol. 162, 293–300. CrossRefGoogle Scholar
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, 457–467. Google Scholar
Lemaire, C., Versini, J.J., Bonhomme, F., 2005, Maintenance of genetic differentiation across a transition zone in the sea: discordance between nuclear and cytoplasic markers. J. Evol. Biol. 18, 70–80. CrossRefGoogle Scholar
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, 351-358. CrossRefGoogle Scholar
Li, Y., Korol, A., Fahima, T., Nevo, E., 2004, Microsatellites within genes: structure, function, and evolution. Mol. Biol. Evol. 21, 991–1007. CrossRefGoogle ScholarPubMed
Mancera, J.M., McCormick, S.D., 1998a, Osmoregulatory actions of the GH/IGF axis in nonsalmonid teleosts. Comp. Biochem. Physiol. B 121, 43–48. CrossRefGoogle Scholar
Mancera, J.M., McCormick, S.D., 1998b, Evidence for growth hormone/insulin-like growth factor I axis regulation of seawater acclimation in the euryhaline teleost Fundulus heteroclitus . Gen. Comp. Endocrinol. 11, 103–112. CrossRefGoogle Scholar
Mancera J.M., McCormick S.D., 2007, Role of prolactin, growth hormone, insuline-like growth factor and cortisol in teleost osmoregulation. In: Baldisserotto B., Mancera J.M., Kapoor B.G. (Eds.) Fish osmoregulation, Enfield, Science Publishers Inc., pp. 497–515.
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, 57–63. CrossRefGoogle Scholar
Moen, T., Hayes, B., Nilsen, F., Delghandi, M., Fjalestad, K.T., Fevolden, S.-E., Berg, P.R., Lien, S., 2008, Identification and characterisation of novel SNP markers in Atlantic cod: evidence for directional selection. BMC Genomics 9, 18. Google Scholar
Naciri, M., Lemaire, C., Borsa, P., Bonhomme, F., 1999, Genetic study of the Atlantic/Mediterranean transition in seabass (Dicentrarchus labrax). J. Hered. 90, 591–596. CrossRefGoogle Scholar
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, 3859–3871. CrossRefGoogle ScholarPubMed
Nei M., 1987, Molecular evolutionary genetics, New York, Columbia University Press.
Nielsen, E.E., Hemmer-Hansen, J., Larsen, P.F., Bekkevold, D., 2009a, Population genomics of marine fishes: identifying adaptive variation in space and time. Mol. Ecol. 18, 3128–3150. CrossRefGoogle ScholarPubMed
Nielsen, E.E., Hemmer-Hanssen, J., Poulsen, N.A., Loeschke, V., Moen, T., Johansen, T., Mittelholzer, T., Taranger, G.L., Ogden, R., Carvalho, G.R., 2009b, Genomic signatures of local directional selection in a high gene flow marine organism; the Atlantic cod (Gadus morhua). BMC Evol. Biol. 9, 276. CrossRefGoogle Scholar
Patarnello, T., Volckaert, F.A.M.J., Castilho,, R., 2007, Pillars of Hercules: is the Atlantic–Mediterranean transition a phylogeographical break? Mol. Ecol. 16, 4426–4444. CrossRefGoogle ScholarPubMed
Pickett G.D., Pawson M.G. 1994, Sea bass biology, exploitation and conservation. Chapman and Hall, London, Fish and Fisheries Series.
Pradet-Balade, B., Salmon, C., Hardy, A., Querat, B., 1998, Heterogeneity of eel thyrotropin β mRNAs is due to a minisatellite in the 3′untranslated region of the gene. Gene 215, 251–257. CrossRefGoogle Scholar
Poulter, R., Butler, M., Ormandy, J., 1999, A LINE element from the pufferfish (fugu) Fugu rubripes which shows similarity to the CR1 family of non-LTR retrotransposons. Gene 227, 169–179. CrossRefGoogle ScholarPubMed
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. CrossRefGoogle ScholarPubMed
Rise, M.L., Hall, J.R., Rise, M., Hori, T.S., Browne, M.J., Gamperl, A.K., Hubert, S., Kimball, J., Bowman, S., Johnson, S.C., 2010, Impact of asymptomatic nodavirus carrier state and intraperitoneal viral mimic injection on brain transcript expression in Atlantic cod (Gadus morhua). Physiol. Genomics, 42, 266–280. CrossRefGoogle Scholar
Ryynänen, H., Primmer, C., 2004, Distribution of genetic variation in the growth hormone 1 gene in Atlantic salmon (Salmo salar) populations from Europe and North America. Mol. Ecol. 13, 3857–3869. CrossRefGoogle ScholarPubMed
Sakamoto, T., Hirano, T., 1993, Expression of insulin-like growth factor I gene in osmoregulatory organs during seawater adaptation of the salmonid fish: possible mode of osmoregulatory action of growth hormone. Proc. Natl. Acad. Sci. USA 90, 1912–1916. CrossRefGoogle ScholarPubMed
Sakamoto, T., McCormick, S.D., 2006, Prolactin and growth hormone in fish osmoregulation. Gen. Comp. Endocrinol. 147, 24–30. CrossRefGoogle Scholar
Schulte, P.M., Glémet, H.C., Fiebig, A.A., Powers, D.A., 2000, Adaptive variation in lactate dehydrogenase-B gene expression: Role of a stress-responsive regulatory element. Proc. Natl. Acad. Sci. USA 97, 6597–6602. CrossRefGoogle ScholarPubMed
Smith, W.L., Craig, M.T., 2007, Casting the Percomorph net widely: the importance of broad taxonomic sampling in the search for the placement of Serranid and Percid fishes. Copeia 2007, 35–55. CrossRefGoogle Scholar
Streelman, J., Kocher, T., 2002, Microsatellite variation associated with prolactin expression and growth of salt-challenged tilapia. Physiol. Genomics 9, 1–4. CrossRefGoogle ScholarPubMed
Taniyama,, S., Kitahashi,, T., Ando,, H., Ban, M., Ueda,, H., Urano,, A., 1999, Changes in the levels of mRNAs for growth hormone/prolactin/somatolactin family and Pit-1/GHF-1 in the pituitaries of pre-spawning chum salmon. J. Mol. Endocrinol. 23, 189–198. CrossRefGoogle Scholar
Tao, W.J., Boulding, E.G., 2003, Associations between single nucleotide polymorphisms in candidate genes and growth rate in Arctic charr (Salvelinus alpinus L.). Heredity 91, 60–69. CrossRefGoogle Scholar
Terova, G., Rimoldi, S., Chini, V., Gornati, R., Bernardini, G., Saroglia, M., 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. CrossRefGoogle Scholar
Uchida, K., Moriyama, S., Breves, J.P., Fox, B.K., Pierce, A.L., Borski, R.J., Hirano, T., Grau, E.G., 2009, cDNA cloning and isolation of somatolactin in Mozambique tilapia and effects of seawater acclimation, confinement stress, and fasting on its pituitary expression. Gen. Comp. Endocrinol. 161, 162–170. CrossRefGoogle Scholar
Vargas-Chacoff, L., Astola, A., Arjona, F.J., Martín del Río, M.P.,García-Cózar, F., Mancera, J.M.,Martínez-Rodríguez, G., 2009, Pituitary gene and protein expression under experimental variation on salinity and temperature in gilthead sea bream Sparus aurata . Comp. Biochem. Physiol. B154, 303–308. CrossRefGoogle Scholar
Varsamos, S., Diaz, J.-P., Charmantier, G., Flik, G., Blasco, C., Connes,, R., 2002, Branchial chloride cells in sea bass (Dicentrarchus labrax) adapted to fresh water, seawater, and doubly concentrated seawater. J. Exp. Zool. 293, 12–26. CrossRefGoogle ScholarPubMed
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, 473–480. CrossRefGoogle ScholarPubMed
Vasemägi, A., Nilsson, J., Primmer, C.R., 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, 1067–1076. CrossRefGoogle Scholar
Volckaert F.A.M., Batargias C., Canario A., Chatziplis D., Chistiakhov D., Haley C., Libertini A., Tsigenopoulos C., 2008, European sea bass. In: Kocher T.D., Cole C. (Eds.) Genome mapping and genomics in animals. Vol. 2: Genome mapping and genomics in fishes and aquatic animal. Berlin, Springer-Verlag, pp. 117–133.
Von Schalburg, K., Yazawa, R., de Boer, J., Lubieniecki, K., Goh, B., Straub, C., Beetz-Sargent, M.R., Robb, A., Davidson, W.S., Devlin, R.H., Koop, B.F., 2008, Isolation, characterization and comparison of Atlantic and Chinook salmon growth hormone 1 and 2. BMC Genomics 9, 522. Google Scholar
Weir, B.S., 1979, Inferences about linkage disequilibrium. Biometrics 35, 235–254. CrossRefGoogle Scholar
Weir, B.S., Cockerham, C.C., 1984, Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370. Google Scholar
Wray, G., 2007, The evolutionary significance of cis-regulatory mutations. Nat. Rev. Genet. 8, 206–216. CrossRefGoogle Scholar
Zhang, D., Shao, Y., Jiang, S., Li, J., Xu, X., 2009, Nibea coibor growth hormone gene: its phylogenetic significance, microsatellite variation and expression analysis. Gen. Comp. Endocrinol. 163, 233–241. CrossRefGoogle Scholar
Zheng, C., Ovaskainen, O., Hanski, I., 2009, Modelling single nucleotide effects in phosphoglucose isomerase on dispersal in the Glanville fritillary butterfly: coupling of ecological and evolutionary dynamics. Phil. Trans. R. Soc. B364, 1519–1532. CrossRefGoogle Scholar
Zhu, Y., Thomas, P., 1998, Effects of light on plasma somatolactin levels in red drum (Sciaenops ocellatus). Gen. Comp. Endocrinol. 111, 76–82. CrossRefGoogle Scholar