Variation in gene expression along a salinity gradient in wild populations of the euryhaline black-chinned tilapia Sarotherodon melanotheron

Journal of Fish Biology

Volumn 80, Issue 4, 2012, Pages 785-801

  Tine, M ^a,b   Guinand, B ^b   Durand, J D ^c  

^a MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^b UNIV MONTPELLIER   (France)

^c INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (Senegal)

Author keywords

Adaptation; Biomarker; Fish; Osmoregulation; Plasticity

Indexed keywords

ANIMAL; ARTICLE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PRINCIPAL COMPONENT ANALYSIS; SALINITY; TILAPIA; UPREGULATION;

ANIMALS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; PRINCIPAL COMPONENT ANALYSIS; SALINITY; TILAPIA; UP-REGULATION;

SAROTHERODON MELANOTHERON; TILAPIA;

EID: 84859421247     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2012.03220.x     Document Type: Article

References (75)

1. Albaret, J.-J., Simier, M., Darboe, F. S., Ecoutin, J.-M., Rafray, J. & de Morais, L. T. (2004). Fish diversity and distribution in the Gambia Estuary, West Africa, in relation to environmental variables. Aquatic Living Resourses 17, 35-46.
2. Ardjosoediro, I. & Ramnarine, I. W. (2002). The influence of the turbidity on growth, feed conversion and survivorship of the Jamaica red tilapia strain. Aquaculture 212, 159-165.
3. Aykanat, T., Thrower, F. P. & Heath, D. D. (2011). Rapid evolution of osmoregulatory function by modification of gene transcription in steelhead trout. Genetica 139, 233-242.
4. Bouvy, M., Briand, E., Boup, M. M., Got, P., Leboulanger, C., Bettarel, Y. & Arfi, R. (2008). Effects of sewage discharges on microbial components in tropical coastal waters (Senegal, West Africa). Marine and Freshwater Research 59, 614-626.
5. Cogels, F.-X., Thiam, A. & Gac, J.-Y. (1993). Premiers effets des barrages sur le fleuve Sénégal sur le lac de Guiers. Revue d'Hydrobiologie Tropicale 26, 105-117.
6. Colombini, M. (2004). VDAC: the channel at the interface between mitochondria and the cytosol. Molecular and Cellular Biochemistry 256/257, 107-115.
7. Cossins, A. R. & Crawford, D. L. (2005). Opinion - fish as models for environmental genomics. Nature Reviews Genetics 6, 324-333.
8. Cossins, A., Fraser, J., Hughes, M. & Gracey, A. (2006). Post-genomic approaches to understanding the mechanisms of environmentally induced phenotypic plasticity. Journal of Experimental Biology 209, 2328-2336.
9. Crawford, D. L. & Oleksiak, M. F. (2007). The biological importance of measuring individual variation. Journal of Experimental Biology 210, 1613-1621.
10. Crockett, E. L., Londraville, R. L., Wilkes, E. E. & Popesco, M. C. (1999). Enzymatic capacities for b-oxidation of fatty fuels are low in the gill of teleost fishes despite presence of fatty acid-binding protein. Journal of Experimental Zoology 284, 276-285.
11. Dalziel, A. C., Rogers, S. M. & Schulte, P. M. (2009). Linking genotypes to phenotypes and fitness: how mechanistic biology can inform molecular ecology. Molecular Ecology 18, 4997-5017.
12. Deane, E. E. & Woo, N. Y. S. (2004). Differential gene expression associated with euryhalinity in sea bream (Sparus sarba). American Journal of Physiology 287, R1054-R1063.
13. Deane, E. E., Kelly, S. P., Luk, J. C. Y. & Woo, N. Y. S. (2002). Chronic salinity adaptation modulates hepatic heat shock protein and insulin-like growth factor I expression in black sea bream. Marine Biotechnology 4, 193-205.
14. Diatchenko, L., Lau, Y.-F. C., Campbell, A. P., Chenchik, A., Moqadam, F., Huang, B., Lukyanov, S., Lukyanov, K., Gurskaya, N., Sverdlov, E. D. & Siebert, P. D. (1996). Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proceedings of the National Academy of Sciences of the United States of America 93, 6025-6030.
15. Diouf, K., Guilhaumon, F., Aliaume, C., Ndiaye, P., Do Chi, T. & Panfili, J. (2009). Effects of the environment on fish juvenile growth in West African stressful estuaries. Estuarine Coastal and Shelf Sciences 83, 115-125.
16. Douglas, S. E. (2006). Microarray studies of gene expression in fish. OMICS 10, 474-489.
17. Edmonds, B. T. & Koenig, E. (1990). Volume regulation in response to hypo-osmotic stress in goldfish retinal ganglion cell axons regenerating in vitro. Brain Research 520, 159-165.
18. Gac, J.-Y., Carn, M. & Saos, J.-L. (1986). Les invasions marines dans la basse vallée du Sénégal. Revue d'Hydrobiologie Tropicale 19, 3-17.
19. Ghalambor, C. K., McKay, J. K., Carroll, S. P. & Reznick, D. N. (2007). Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology 21, 394-407.
20. Gibson, G. (2008). The environmental contribution to gene expression profiles. Nature Reviews Genetics 9, 575-581.
21. Goetz, F. W. & MacKenzie, S. (2008). Functional genomics with microarrays in fish biology and fisheries. Fish and Fisheries 9, 378-395.
22. Gracey, A. Y., Chaney, M. L., Boomhower, J. P., Tyburczy, W. R., Connor K. & Somero, G. N. (2008). Rhythms of gene expression in a fluctuating intertidal environment. Current Biology 18, 1501-1507.
23. Henry, R. P. (2001). Environmentally mediated carbonic anhydrase induction in the gills of euryhaline crustaceans. Journal Experimental Biology 204, 991-1002.
24. Henry, R. P., Gehnrich, S., Weihrauch, D. & Towle, D. W. (2003). Salinity-mediated carbonic anhydrase induction in the gills of the euryhaline green crab, Carcinus maenas. Comparative Biochemistry and Physiology C 136, 243-258.
25. Hodgins-Davis, A. & Townsend, J. P. (2009). Evolving gene expression: from G to E to G x E. Trends in Ecology and Evolution 24, 649-658.
26. Hofmann, G. E. & Todgham, A. E. (2010). Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Annual Review of Physiology 72, 127-145.
27. Hwang, P. P. & Lee, T. H. (2007). New insights into fish ion regulation and mitochondrion-rich cells. Comparative Biochemistry and Physiology A 148, 479-497.
28. Jensen, M. 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.). Journal of Experimental Zoology 282, 290-300.
29. Jury, D. R., Kaveti, S., Duan, Z. H., Willard, B., Kinter, M. & Londraville, R. (2008). Effects of calorie restriction on the zebrafish liver proteome. Comparative Biochemistry and Physiology D 3, 275-282.
30. Kadenbach, B. (2003). Intrinsic and extrinsic uncoupling of oxidative phosphorylation. Biochimica and Biophysica Acta: Bioenergetics 1604, 77-94.
31. Kalujnaia, S., McWilliam, I. S., Zaguinaiko, V. A., Feilen, A. L., Nicholson, J., Hazon, N., Cutler, C. P., Balment, R. J., Cossins, A. R., Hughes, M. et al. (2007). Salinity adaptation and gene profiling analysis in the European eel (Anguilla anguilla) using microarray technology. General and Comparative Endocrinology 152, 274-280.
32. Kassahn, K. S. (2008). Microarrays for comparative and ecological genomics: beyond singlespecies applications of array technologies. Journal of Fish Biology 72, 2407-2434.
33. Kelly, S. P., Chow, I. N. K. & Woo, N. Y. S. (1999). Haloplasticity of black seabream (Mylio macrocephalus): hypersaline to freshwater acclimation. Journal of Experimental Biology 283, 226-241.
34. Kimbrell, T. & Holt, R. D. (2007). Canalization breakdown and evolution in a source-sink system. The American Naturalist 169, 370-382.
35. Kolditz, C. I., Pabouf, G., Borthaire, M., Esquerre, D., SanCristobal, M., Lefèvre, F. & Médale, F. (2009). Changes induced by dietary energy intake and divergent selection for muscle fat content in rainbow trout (Oncorhynchus mykiss), assessed by transcriptome and proteome analysis of the liver. BMC Genomics 9, 506.
36. Kültz, D. & Avila, K. (2001). Mitogen-activated protein kinases are in vivo transducers of osmosensory signals in fish gill cells. Comparative Biochemistry and Physiology B 129, 821-829.
37. Labonne, M., Morize, E., Scolan, P., Laë, R., Dabas, E. & Bohn, M. (2009). Impact of salinity on early life history traits of three estuarine fish species in Senegal. Estuarine Coastal and Shelf Sciences 82, 673-681.
38. Laiz-Carriòn, R., Guerreiro, P. M., Fuentes, J., Canario, A. V. M., Del Rio, M. P. M. & Mancera, J. M. (2005). Branchial osmoregulatory response to salinity in the gilthead sea bream, Sparus auratus. Journal of Experimental Zoology 303A, 563-576.
39. Lande, R. (2009). Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. Journal of Evolutionary Biology 22, 1435-1446.
40. Langdon, J. S. (1987). Active osmoregulation in the Australian bass, Macquaria novemaculeata (Steindachner), and the golden perch, Macquaria ambigua (Richardson) (Percichthyidae). Journal of Marine and Freshwater Research 38, 771-776.
41. Larsen, P. F., Schulte, P. M. & Nielsen, E. E. (2011). Gene expression analysis for the identification of selection and local adaptation in fishes. Journal of Fish Biology 78, 1-22.
42. Legendre, M. & Ecoutin, J. M. (1989). Suitability of brackish water tilapia species from the Ivory Coast for lagoon aquaculture. 1 - reproduction. Aquatic Living Resourse 2, 71-79.
43. Lin, C. H. & Lee, T. H. (2005). Sodium or potassium ions activate different kinetics of gill Na, K-ATPase in three seawater- and freshwater-acclimated euryhaline teleosts. Journal of Experimental Zoology A 303, 57-65.
44. Lin, C. H., Huang, C. L., Yang, C. H., Lee, T. H. & Hwang, P. P. (2004). Time-course changes in the expression of Na, K-ATPase and the morphometry of mitochondrion-rich cells in gills of euryhaline tilapia (Oreochromis mossambicus) during freshwater acclimation. Journal of Experimental Zoology A 301, 85-96.
45. López-Maury, L., Marguerat, S. & Bähler, J. (2008). Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nature Reviews Genetics 9, 583-593.
46. Marshall, W. S. & Bryson, S. E. (1998). Transport mechanisms of seawater teleost chloride cells: an inclusive model of a multifunctional cell. Comparative Biochemistry and Physiology A 119, 97-106.
47. Miller, K. M. & Maclean, N. (2008). Teleost microarrays: development in a broad phylogenetic range reflecting diverse applications. Journal of Fish Biology 72, 2039-2050.
48. Motais, R., Fievet, B., Borgese, F. & Garcia-Romeu, F. (1997). Association of the band 3 protein with a volume-activated, anion and amino acid channel: a molecular approach. Journal of Experimental Biology 200, 361-367.
49. Oleksiak, M. F. (2010). Genomic approaches with natural fish populations. Journal of Fish Biology 76, 1067-1093.
50. Pagès, J. & Citeau, J. (1990). Rainfall and salinity of a sahelian estuary between 1927 and 1987. Journal of Hydrology 113, 325-341.
51. Panfili, J., Mbow, A., Durand, J.-D., Diop, K., Diouf, K., Thior, D., Ndiaye, P. & Laë, R. (2004a). Influence of salinity on the life-history traits of the West African black-chinned tilapia (Sarotherodon melanotheron): comparison between the Gambia and Saloum estuaries. Aquatic Living Resources 17, 65-74.
52. Panfili, J., Durand, J.-D., Mbow, A., Guinand, B., Diop, K., Kantoussan, J., Thior, D., Thiaw, O. T., Albaret, J.-J. & Laë, R. (2004b). Influence of salinity on life history traits of the bonga shad Ethmalosa fimbriata (Pisces, Clupeidae): comparison between the Gambia and Saloum estuaries. Marine Ecology Progress Series 270, 241-257.
53. Panfili, J., Thior, D., Ecoutin, J.-M., Ndiaye, P. & Albaret, J.-J. (2006). Influence of salinity on the size at maturity for fish species reproducing in contrasting West African estuaries. Journal of Fish Biology 69, 95-113.
54. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, 2002-2007.
55. Pierce, S. K. & Warren, J. W. (2001). The taurine efflux portal used to regulate cell volume in response to hypoosmotic stress seems to be similar in many cell types: lessons to be learned from molluscan red blood cells. American Zoologist 41, 710-720.
56. Pörtner, H. O., Schulte, P. M., Wood, C. M. & Schiemer, F. (2010). Niche dimensions in fishes: an integrative view. Physiologial and Biochemical Zoology 83, 808-826.
57. Pouyaud, L., Desmarais, E., Chenuil, A., Agnèse, J.-F. & Bonhomme, F. (1999). Kin cohesiveness and possible inbreeding in the mouth brooding tilapia Sarotherodon melanotheron (Pisces Cichlidae). Molecular Ecology 8, 803-812.
58. Price, T. D., Qvarnström, A. & Irwin, D. E. (2003). The role of phenotypic plasticity in driving genetic evolution. Proceeding of the Royal Society B 270, 1433-1440.
59. Roberge, C., Einum, S., Guderley, H. & Bernatchez, L. (2006). Rapid parallel evolutionary changes of gene transcription profiles in farmed Atlantic salmon. Molecular Ecology 15, 9-20.
60. Sakamoto, T., Uchida, K. & Yokota, S. (2001). Regulation of the ion-transporting mitochondrion-rich cell during adaptation of teleost fishes to different salinities. Zoological Sciences 18, 1163-1174.
61. Scott, C. P., Williams, D. A. & Crawford, D. L. (2009). The effect of genetic and environmental variation on metabolic gene expression. Molecular Ecology 18, 2832-2843.
62. Scott, G. R., Claiborne, J. B., Edwards, S. L., Schulte, P. M. & Wood, C. M. (2005). Gene expression after freshwater transfer in gills and opercular epithelia of killifish: insight into divergent mechanisms of ion transport. Journal of Experimental Biology 208, 2719-2729.
63. Shiu, S. H. & Borevitz, J. O. (2008). The next generation of microarray research: applications in evolutionary and ecological genomics. Heredity 100, 141-149.
64. Simier, M., Blanc, L., Aliaume, C., Diouf, P. S. & Albaret, J.-J. (2004). Spatial and temporal structure of fish assemblages in an "inverse estuary", the Sine Saloum system (Senegal). Estuarine Coastal and Shelf Sciences 59, 69-86.
65. Simier, M., Laurent, C., Ecoutin, J.-M. & Albaret, J.-J. (2006). The Gambia River estuary: a reference point for estuarine fish assemblages studies in West Africa. Estuarine Coastal and Shelf Sciences 69, 615-628.
66. Stahl, A. (2004). A current review of fatty acid transport proteins (SLC27). Pflügers Archivs 447, 722-727.
67. Stahl, A., Gimeno, R. E., Tartaglia, L. A. & Lodish, H. F. (2001). Fatty acid transport proteins: a current view of a growing family. Trends in Endocrinology and Metabolism 12, 266-273.
68. Thünken, T., Bakler, T. C. M., Baldauf, S. A. & Kullmann, H. (2007). Active inbreeding in a cichlid fish and its adaptative significance. Current Biology 17, 225-229.
69. Tine, M., de Lorgeril, J., Diop, K., Bonhomme, F., Panfili, J. & Durand, J.-D. (2007). Growth hormone and Prolactin-1 gene transcription in natural populations of the black-chinned tilapia Sarotherodon melanotheron acclimatised to different salinities. Comparative Biochemistry and Physiology B 147, 541-549.
70. Tine, M., de Lorgeril, J., D'Cotta, H., Pepey, E., Bonhomme, F., Baroiller, J.-F. & Durand, J.-D. (2008). Transcriptional responses of the black-chinned tilapia Sarotherodon melanotheron to salinity extremes. Marine Genomics 1, 37-46.
71. Tine, M., Bonhomme, F., McKenzie, D. J. & Durand, J.-D. (2010). Differential expression of the heat shock protein Hsp70 in natural populations of the tilapia, Sarotherodon melanotheron, acclimatised to a range of environmental salinities. BMC Ecology 10, 11.
72. Tipsmark, C. K., Madsen, S. S. & Borski, R. J. (2004). Effect of salinity on expression of branchial ion transporters in striped bass (Morone saxatilis). Journal of Experimental Zoology 301A, 979-991.
73. Tseng, Y. C. & Hwang P.-P. (2008). Some insights into energy metabolism for osmoregulation in fish. Comparative Biochemistry and Physiology C 148, 419-429.
74. Varsamos, S., Nebel, C. & Charmantier, G. (2005). Ontogeny of osmoregulation in postembryonic fish: a review. Comparative Biochemistry and Physiology A 141, 401-429.
75. West-Eberhard, M. J. (2003). Developmental Plasticity and Evolution. Oxford: Oxford University Press.