Major disruption of gene expression in hybrids between young sympatric anadromous and resident populations of brook charr (Salvelinus fontinalis Mitchill)

Journal of Evolutionary Biology

Volumn 22, Issue 8, 2009, Pages 1708-1720

  Mavarez, Jesus ^a,b   Audet, Celine ^c   Bernatchez, Louis ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b INSTITUTO VENEZOLANO DE INVESTIGACIONES CIENTÍFICAS   (Venezuela)

^c INSTITUT DES SCIENCES DE LA MER DE RIMOUSKI   (Canada)

Author keywords

Ecological divergence; Fish; Genomic incompatibilities; Hybridization; Microarrays; Reproductive isolation

Indexed keywords

COMPLEMENTARY DNA;

DIVERGENCE; GENE EXPRESSION; GENETIC VARIATION; GENOMICS; HYBRID; HYBRIDIZATION; IMMUNE RESPONSE; OSMOREGULATION; PHENOTYPE; REPRODUCTIVE ISOLATION; SALMONID; SELF INCOMPATIBILITY; SYMPATRY;

ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; DNA MICROARRAY; GENE EXPRESSION; GENETICS; HYBRIDIZATION; SPECIES DIFFERENCE; TROUT;

ANALYSIS OF VARIANCE; ANIMALS; DNA, COMPLEMENTARY; GENE EXPRESSION; HYBRIDIZATION, GENETIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SPECIES SPECIFICITY; TROUT;

SALVELINUS FONTINALIS;

EID: 67650381846     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2009.01785.x     Document Type: Article

References (97)

1. Arnosti, D.N. 2003. Analysis and function of transcriptional regulatory elements: insights from Drosophila. Annu. Rev. Entomol. 48 : 579 602. (Pubitemid 37365403)
2. Barbash, D.A., Siino, D.F., Tarone, A.M. Roote, J. 2003. A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc. Natl Acad. Sci. USA 100 : 5302 5307. (Pubitemid 36542700)
3. Benjamini, Y. Hochberg, Y. 1995. Controlling the false discovery rate - a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B - (Methodological) 57 : 289 300.
4. Bertrand, M., Marcogliese, D.J. Magnan, P. 2008. Trophic polymorphism in brook charr revealed by diet, parasites and morphometrics. J. Fish Biol. 72 : 555 572. (Pubitemid 351225066)
5. Boula, D., Castric, V., Bernatchez, L. Audet, C. 2002. Physiological, endocrine, and genetic bases of anadromy in the brook charr, Salvelinus fontinalis, of the Laval River (Quebec, Canada). Environ. Biol. Fish 64 : 229 242. (Pubitemid 34791797)
6. Boursot, P., Auffray, J.-C., Britton-Davidian, J. Bonhomme, F. 1993. The evolution of house mice. Annu. Rev. Ecol. Syst. 24 : 119 152.
7. Boursot, P., Din, W., Anand, R., Darviche, D., Dod, B., VonDeimling, F., Talwar, G.P. Bonhomme, F. 1996. Origin and radiation of the house mouse: Mitochondrial DNA phylogeny. J. Evol. Biol. 9 : 391 415.
8. Brem, R.B., Yvert, G., Clinton, R. Kruglyak, L. 2002. Genetic dissection of transcriptional regulation in budding yeast. Science 296 : 752 755. (Pubitemid 34442007)
9. Brideau, N.J., Flores, H.A., Wang, J., Maheshwari, S., Wang, X. Barbash, D.A. 2006. Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314 : 1292 1295. (Pubitemid 44846401)
10. Castric, V. Bernatchez, L. 2003. The rise and fall of isolation by distance in the anadromous brook charr (Salvelinus fontinalis Mitchill). Genetics 163 : 983 996. (Pubitemid 36417940)
11. Comai, L., Madlung, A., Josefsson, C. Tyagi, A. 2003. Do the different parental 'heteromes' cause genomic shock in newly formed allopolyploids? Phil. Trans. R. Soc. Lond. B 358 : 1149 1155. (Pubitemid 36774908)
12. Coyne, J.A. Orr, H.A. 2004. Speciation. Sinauer Associates, Sunderland, MA, USA.
13. Cui, X.G., Hwang, J.T.G., Qiu, J., Blades, N.J. Churchill, G.A. 2005. Improved statistical tests for differential gene expression by shrinking variance components estimates. Biostatistics 6 : 59 75. (Pubitemid 41240370)
14. Davies, K.J.A. 2000. Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life 50 : 279 289. (Pubitemid 32289086)
15. Denver, D.R., Morris, K., Streelman, J.T., Kim, S.K., Lynch, M. Thomas, W.K. 2005. The transcriptional consequences of mutation and natural selection in Caenorhabditis elegans. Nat. Genet. 37 : 544 548. (Pubitemid 40617285)
16. Derome, N. Bernatchez, L. 2006. The transcriptomics of ecological convergence between 2 limnetic coregonine fishes (Salmonidae). Mol. Biol. Evol. 23 : 2370 2378. (Pubitemid 44737131)
17. Derome, N., Duchesne, P. Bernatchez, L. 2006. Parallelism in gene transcription among sympatric lake whitefish (Coregonus clupeaformis Mitchill) ecotypes. Mol. Ecol. 15 : 1239 1249.
18. Derome, N., Bougas, B., Rogers, SM, Whiteley, A, Labbe, A, Laroche, J Bernatchez, L. 2008. Pervasive sex-linked effects on transcription regulation as revealed by eQTLmapping in lake whitefish species pairs (Coregonus sp, Salmonidae). Genetics 179 : 1903 1917.
19. Dobzhansky, T. 1937. Genetics and the Origin of Species. Columbia University Press, New York.
20. Draghici, S. 2003. Data Analysis Tools for Microarrays. Chapman and Hall/CRC Press, Boca Raton, FL, USA.
21. Evans, B.J., Kelley, D.B., Tinsley, R.C., Melnick, D.J. Cannatella, D.C. 2004. A mitochondrial DNA phylogeny of African clawed frogs: phylogeography and implications for polyploid evolution. Mol. Phylogenet. Evol. 33 : 197 213. (Pubitemid 39138745)
22. Evans, B.J., Kelley, D.B., Melnick, D.J. Cannatella, D.C. 2005. Evolution of RAG-1 in polyploid clawed frogs. Mol. Biol. Evol. 22 : 1193 1207. (Pubitemid 40577757)
23. Gibson, G. 1996. Epistasis and pleiotropy as natural properties of transcriptional regulation. Theor. Popul. Biol. 49 : 58 89. (Pubitemid 26310419)
24. Gibson, G. Weir, B. 2005. The quantitative genetics of transcription. Trends Genet. 21 : 616 623. (Pubitemid 41429290)
25. Giger, T., Excoffier, L., Day, P.J.R., Champigneulle, A., Hansen, M.M., Powell, R. Largiader, C.R. 2006. Life history shapes gene expression in salmonids. Curr. Biol. 16 : R281 R282.
26. Giger, T., Excoffier, L., Amstutz, U., Day, P.J.R., Champigneulle, A., Hansen, M.M., Kelso, J. Largiader, C.R. 2008. Population transcriptomics of life-history variation in the genus Salmo. Mol. Ecol. 17 : 3095 3108. (Pubitemid 351861463)
27. Gilad, Y., Oshlack, A. Rifkin, S.A. 2006. Natural selection on gene expression. Trends Genet. 22 : 456 461. (Pubitemid 44093766)
28. Haerty, W. Singh, R.S. 2006. Gene regulation divergence is a major contributor to the evolution of Dobzhansky-Muller incompatibilities between species of Drosophila. Mol. Biol. Evol. 23 : 1707 1714. (Pubitemid 44309764)
29. Hedgecock, D., Lin, J., DeCola, S., Haudenschild, C.D., Meyer, E., Manahan, D.T. Bowen, B. 2007. Transcriptomic analysis of growth heterosis in larval Pacific oysters (Crassostrea gigas). Proc. Natl Acad. Sci. USA 104 : 2313 2318. (Pubitemid 46391394)
30. Inga, A., Reamon-Buettner, S.M., Borlak, J. Resnick, M.A. 2005. Functional dissection of sequence-specific NKX2-5 DNA binding domain mutations associated with human heart septation defects using a yeast-based system. Hum. Mol. Genet. 14 : 1965 1975. (Pubitemid 41418033)
31. Johnson, N.A. Porter, A.H. 2000. Rapid speciation via parallel, directional selection on regulatory genetic pathways. J. Theor. Biol. 205 : 527 542. (Pubitemid 30627568)
32. Kerr, M.K., Martin, M. Churchill, G.A. 2000. Analysis of variance for gene expression microarray data. J. Comput. Biol. 7 : 819 837.
33. Kerr, M.K., Afshari, C.A., Bennett, L., Bushel, P., Martinez, J., Walker, N.J. Churchill, G.A. 2002. Statistical analysis of a gene expression microarray experiment with replication. Stat. Sin. 12 : 203 217.
34. Landry, C.R., Wittkopp, P.J., Taubes, C.H., Ranz, J.M., Clark, A.G. Hartl, D.L. 2005. Compensatory cis-trans evolution and the dysregulation of gene expression in interspecific hybrids of Drosophila. Genetics 171 : 1813 1822.
35. Landry, C.R., Hartl, D.L. Ranz, J.M. 2007. Genome clashes in hybrids: insights from gene expression. Heredity 99 : 483 493. (Pubitemid 350006183)
36. Lefrant, A. 2006. Resistance des ombles (Salvelinus fontinalis et Salvelinus alpinus) aux infections bacteriennes opportunistes en milieu marin, M.sc. Thesis. Universite du Quebec à Rimouski, Rimouski.
37. Lemos, B., Meiklejohn, C.D., Caceres, M. Hartl, D.L. 2005. Rates of divergence in gene expression profiles of primates, mice, and flies: Stabilizing selection and variability among functional categories. Evolution 59 : 126 137. (Pubitemid 40181305)
38. Lenormand, S., Dodson, J.J. Menard, A. 2004. Seasonal and ontogenetic patterns in the migration of anadromous brook charr (Salvelinus fontinalis). Can. J. Fish. Aquat. Sci. 61 : 54 67. (Pubitemid 38554870)
39. Levine, A.J. 1997. p53, the cellular gatekeeper for growth and division. Cell 88 : 323 331. (Pubitemid 27131374)
40. Levine, M. Tjian, R. 2003. Transcription regulation and animal diversity. Nature 424 : 147 151. (Pubitemid 36858677)
41. Li, H. Yamada, H. 2002. Changes of the fatty acid composition in smolts of masu salmon (Oncorhynchus masou), associated with desmoltification and sea-water transfer. Comp. Biochem. Physiol. A 103 : 221 226.
42. Lu, G. Bernatchez, L. 1998. Experimental evidence for reduced hybrid viability between dwarf and normal ecotypes of lake whitefish (Coregonus clupeaformis Mitchill). Proc. R. Soc. Lond. Ser. B 265 : 1025 1030. (Pubitemid 28271734)
43. Ludwig, M.Z., Bergman, C., Patel, N.H. Kreitman, M. 2000. Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 403 : 564 567. (Pubitemid 30082204)
44. Ludwig, M.Z., Palsson, A., Alekseeva, E., Bergman, C.M., Nathan, J. Kreitman, M. 2005. Functional evolution of a cis-regulatory module. PLoS Biol. 3 : 588 598.
45. Lynch, M. 2007. The Origins of Genome Architecture. Sinauer Associates, Sunderland, MA, USA.
46. Magnan, P., Audet, C., Glemet, H., Legault, M., Rodriguez, M.A. Taylor, E.B. 2002. Developments in the ecology, evolution, and behaviour of the charrs, genus Salvelinus: relevance for their management and conservation. Environ. Biol. Fish 64 : 9 14. (Pubitemid 34791777)
47. Malone, J.H., Chrzanowski, T.H. Michalak, P. 2007. Sterility and gene expression in hybrid males of Xenopus laevis and X. muelleri. PLoS ONE 2 : e781.
48. Martinez-Alvarez, R.M., Morales, A.E. Sanz, A. 2005a. Antioxidant defenses in fish: biotic and abiotic factors. Rev. Fish Biol. Fisheries 15 : 75 88. (Pubitemid 43012773)
49. Martinez-Alvarez, R.M., Sanz, A., Garcia-Gallego, M., Domezain, A., Domezain, J., Carmona, R., Ostos-Garrido, M.D. Morales, A.E. 2005b. Adaptive branchial mechanisms in the sturgeon Acipenser naccarii during acclimation to saltwater. Comp. Biochem. Physiol. A 141 : 183 190. (Pubitemid 40965751)
50. McClintock, B. 1984. The significance of responses of the genome to challenge. Science 226 : 792 801. (Pubitemid 15200674)
51. Meiklejohn, C.D., Parsch, J., Ranz, J.M. Hartl, D.L. 2003. Rapid evolution of male-biased gene expression in Drosophila. Proc. Natl Acad. Sci. USA 100 : 9894 9899. (Pubitemid 37087039)
52. Michalak, P. Noor, M.A. 2003. Genome-wide patterns of expression in Drosophila pure species and hybrid males. Mol. Biol. Evol. 20 : 1070 1076. (Pubitemid 36792823)
53. Moehring, A.J., Teeter, K.C. Noor, M.A. 2007. Genome-wide patterns of expression in Drosophila pure species and hybrid males. II. Examination of multiple-species hybridizations, platforms, and life cycle stages. Mol. Biol. Evol. 24 : 137 145. (Pubitemid 46026289)
54. Morinville, G.R. Rasmussen, J.B. 2003. Early juvenile bioenergetic differences between anadromous and resident brook charr (Salvelinus fontinalis). Can. J. Fish. Aquat. Sci. 60 : 401 410. (Pubitemid 36901161)
55. Morinville, G.R. Rasmussen, J.B. 2006. Does life-history variability in salmonids affect habitat use by juveniles? A comparison among streams open and closed to anadromy. J. Anim. Ecol. 75 : 693 704. (Pubitemid 43725529)
56. Morinville, G.R. Rasmussen, J.B. 2008. Distinguishing between juvenile anadromous and resident brook charr (Salvelinus fontinalis) using morphology. Environ. Biol. Fish 81 : 171 184. (Pubitemid 350234078)
57. Muller, H.J. 1942. Isolating mechanisms, evolution, and temperature. Biol. Symp. 6 : 71 125.
58. Nolte, A.W., Renaut, S. Bernatchez, L. 2009. Divergence in gene regulation at young life history stages of whitefish (Coregonus sp.) and the emergence of genomic isolation. BMC Evol. Biol. 9 : 59.
59. Oleksiak, M.F., Churchill, G.A. Crawford, D.L. 2002. Variation in gene expression within and among natural populations. Nat. Genet. 32 : 261 266.
60. Oleksiak, M.F., Roach, J.L. Crawford, D.L. 2005. Natural variation in cardiac metabolism and gene expression in Fundulus heteroclitus. Nat. Genet. 37 : 67 72. (Pubitemid 40070941)
61. Orino, K., Lehman, L., Tsuji, Y., Ayaki, H., Torti, S.V. Torti, F.M. 2001. Ferritin and the response to oxidative stress. Biochem. J. 357 : 241 247. (Pubitemid 32642922)
62. Orr, H.A. 1997. Haldane's rule. Annu. Rev. Ecol. Syst. 28 : 195 218. (Pubitemid 28012290)
63. Orr, H.A. Presgraves, D.C. 2000. Speciation by postzygotic isolation: forces, genes and molecules. BioEssays 22 : 1085 1094. (Pubitemid 32010518)
64. Ortiz-Barrientos, D., Counterman, B.A. Noor, M.A.F. 2007. Gene expression divergence and the origin of hybrid dysfunctions. Genetica 129 : 71 81. (Pubitemid 44949617)
65. Pattanaik, S., Xie, C.H. Yuan, L. 2008. The interaction domains of the plant Myc-like bHLH transcription factors can regulate the transactivation strength. Planta 227 : 707 715.
66. Perry, G.M., Audet, C., Laplatte, B. Bernatchez, L. 2004. Shifting patterns in genetic control at the embryo-alevin boundary in brook charr. Evolution 58 : 2002 2012. (Pubitemid 39348501)
67. Perry, G.M., Audet, C. Bernatchez, L. 2005. Maternal genetic effects on adaptive divergence between anadromous and resident brook charr during early life history. J. Evol. Biol. 18 : 1348 1361. (Pubitemid 41725685)
68. Porter, A.H. Johnson, N.A. 2002. Speciation despite gene flow when developmental pathways evolve. Evolution 56 : 2103 2111. (Pubitemid 35436819)
69. Proulx, R. Magnan, P. 2004. Contribution of phenotypic plasticity and heredity to the trophic polymorphism of lacustrine brook charr (Salvelinus fontinalis M.). Evol. Ecol. Res. 6 : 503 522. (Pubitemid 38708745)
70. Ranz, J.M., Namgyal, K., Gibson, G. Hartl, D.L. 2004. Anomalies in the expression profile of interspecific hybrids of Drosophila melanogaster and Drosophila simulans. Genome Res. 14 : 373 379. (Pubitemid 38386604)
71. Rawson, P.D. Burton, R.S. 2002. Functional coadaptation between cytochrome c and cytochrome c oxidase within allopatric populations of a marine copepod. Proc. Natl Acad. Sci. USA 99 : 12955 12958.
72. Reiner, A., Yekutieli, D. Benjamini, Y. 2003. Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19 : 368 375. (Pubitemid 36284936)
73. Renaut, S., Nolte, A.W. Bernatchez, L. 2009. Transcriptomic investigation of post-zygotic isolation in lake whitefish (Coregonus clupeaformis). Mol. Biol. Evol. 26 : 925 936.
74. Ritola, O., Livingstone, D.R., Peters, L.D. Lindstrom-Seppa, P. 2002. Antioxidant processes are affected in juvenile rainbow trout (Oncorhynchus mykiss) exposed to ozone and oxygen-supersaturated water. Aquaculture 210 : 1 19. (Pubitemid 34824981)
75. Rogers, S.M.R. Bernatchez, L. 2006. The genetic basis of intrinsic and extrinsic postzygotic reproductive isolation jointly promoting speciation in the lake whitefish species complex (Coregonus clupeaformis). J. Evol. Biol. 19 : 1979 1994. (Pubitemid 44571637)
76. Romano, L.A. Wray, G.A. 2003. Conservation of Endo16 expression in sea urchins despite evolutionary divergence in both cis and trans-acting components of transcriptional regulation. Development 130 : 4187 4199. (Pubitemid 37063434)
77. Rottscheidt, R. Harr, B. 2007. Extensive additivity of gene expression differentiates subspecies of the house mouse. Genetics 177 : 1553 1567. (Pubitemid 350277052)
78. von Schalburg, K.R., Rise, M.L., Cooper, G.A., Brown, G.D., Gibbs, A.R., Nelson, C.C., Davidson, W.S. Koop, B.F. 2005. Fish and chips: various methodologies demonstrate utility of a 16,006-gene salmonid microarray. BMC Genomics 6 : 126.
79. Segal, E., Raveh-Sadka, T., Schroeder, M., Unnerstall, U. Gaul, U. 2008. Predicting expression patterns from regulatory sequence in Drosophila segmentation. Nature 451 : 535 U531.
80. Shaw, P.J., Wratten, N.S., McGregor, A.P. Dover, G.A. 2002. Coevolution in bicoid-dependent promoters and the inception of regulatory incompatibilities among species of higher Diptera. Evol. Dev. 4 : 265 277. (Pubitemid 34805363)
81. Sheridan, M.A., Woo, N.Y.S. Bern, H.A. 1985. Changes in the rates of glycogenesis, glycogenolysis, lipogenesis, and lipolysis in selected tissues of the coho salmon (Oncorhynchus kisutch) associated with parr-smolt transformation. J. Exp. Zool. 236 : 35 44. (Pubitemid 15232538)
82. Simon, D.B., Nelson-Williams, C., Bia, M.J., Ellison, D., Karet, F.E., Molina, A.M., Vaara, I., Iwata, F., Cushner, H.M., Koolen, M., Gainza, F.J., Gitelman, H.J. Lifton, R.P. 1996. Gitelman's variant of Bartter's syndrome, inherited hypokalaemic alkalosis, is caused by mutations in the thiazide-sensitive Na-Cl cotransporter. Nat. Genet. 12 : 24 30. (Pubitemid 26011315)
83. Singh, R.S. Kulathinal, R.J. 2000. Sex gene pool evolution and speciation: A new paradigm. Genes Genet. Syst. 75 : 119 130.
84. St-Cyr, J., Derome, N. Bernatchez, L. 2008. The transcriptomics of life-history trade-offs in whitefish species pairs (Coregonus sp.). Mol. Ecol. 17 : 1850 1870.
85. Stone, J.R. Wray, G.A. 2001. Rapid evolution of cis-regulatory sequences via local point mutations. Mol. Biol. Evol. 18 : 1764 1770. (Pubitemid 32776927)
86. Tamura, K., Subramanian, S. Kumar, S. 2004. Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol. Biol. Evol. 21 : 36 44. (Pubitemid 38233516)
87. Theriault, V. Dodson, J.J. 2003. Body size and the adoption of a migratory tactic in brook charr. J. Fish Biol. 63 : 1144 1159. (Pubitemid 38592219)
88. Theriault, V., Bernatchez, L. Dodson, J.J. 2007a. Mating system and individual reproductive success of sympatric anadromous and resident brook charr, Salvelinus fontinalis, under natural conditions. Behav. Ecol. Sociobiol. 62 : 51 65. (Pubitemid 47568632)
89. Theriault, V., Garant, D., Bernatchez, L. Dodson, J.J. 2007b. Heritability of life-history tactics and genetic correlation with body size in a natural population of brook charr (Salvelinus fontinalis). J. Evol. Biol. 20 : 2266 2277. (Pubitemid 47621905)
90. Thomas, P.D., Campbell, M.J., Kejariwal, A., Mi, H., Karlak, B., Daverman, R., Diemer, K., Muruganujan, A. Narechania, A. 2003. PANTHER: a library of protein families and subfamilies indexed by function. Genome Res. 13 : 2199 2141.
91. Ting, C.T., Tsaur, S.C., Wu, M.L. Wu, C.I. 1998. A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282 : 1501 1504.
92. Torti, F.M. Torti, S.V. 2002. Regulation of ferritin genes and protein. Blood 99 : 3505 3516. (Pubitemid 34534516)
93. True, J.R. Haag, E.S. 2001. Developmental system drift and flexibility in evolutionary trajectories. Evol. Dev. 3 : 109 119. (Pubitemid 32406509)
94. Wang, J.L., Tian, L., Lee, H.S., Wei, N.E., Jiang, H.M., Watson, B., Madlung, A., Osborn, T.C., Doerge, R.W., Comai, L. Chen, Z.J. 2006. Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172 : 507 517. (Pubitemid 43345511)
95. Whiteley, A.R., Derome, N., Rogers, S.M., St-Cyr, J., Laroche, J., Labbe, A., Nolte, A., Renaut, S., Jeukens, J. Bernatchez, L. 2008. The Phenomics and Expression Quantitative Trait Locus Mapping of Brain Transcriptomes Regulating Adaptive Divergence in Lake Whitefish Species Pairs (Coregonus sp.). Genetics 180 : 147 164.
96. Wray, G.A., Hahn, M.W., Abouheif, E., Balhoff, J.P., Pizer, M., Rockman, M.V. Romano, L.A. 2003. The evolution of transcriptional regulation in eukaryotes. Mol. Biol. Evol. 20 : 1377 1419. (Pubitemid 37086669)
97. Wu, C.I., Johnson, N.A. Palopoli, M.F. 1996. Haldane's rule and its legacy: Why are there so many sterile males? Trends Ecol. Evol. 11 : 281 284. (Pubitemid 126377028)