Oxidative phosphorylation gene transcription in whitefish species pairs reveals patterns of parallel and nonparallel physiological divergence

Journal of Evolutionary Biology

Volumn 25, Issue 9, 2012, Pages 1823-1834

  Evans, Melissa L ^a,b   Bernatchez, L ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

Coregonus; Gene transcription; Metabolism; Oxidative phosphorylation; Phenotypic divergence; Physiology; Speciation

Indexed keywords

ADENOSINE TRIPHOSPHATE; MITOCHONDRIAL DNA;

ADAPTATION; CLUPEOID; ENERGETICS; GENETIC VARIATION; LAKE ECOSYSTEM; METABOLISM; OXIDATION; PARALLEL EVOLUTION; PHENOTYPIC PLASTICITY; PHOSPHORUS; PHYSIOLOGICAL RESPONSE; SPECIATION (BIOLOGY);

ADAPTATION; ANIMAL; ARTICLE; CELL NUCLEUS; ECOSYSTEM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; LAKE; METABOLISM; METHODOLOGY; MITOCHONDRIAL GENE; MITOCHONDRION; NONPARAMETRIC TEST; NUCLEOTIDE SEQUENCE; OXIDATIVE PHOSPHORYLATION; PHYSIOLOGY; POPULATION GENETICS; SALMONID; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION; SYMPATRY; UNITED STATES; UPREGULATION;

ADAPTATION, BIOLOGICAL; ADENOSINE TRIPHOSPHATE; ANIMALS; BASE SEQUENCE; CELL NUCLEUS; DNA, MITOCHONDRIAL; ECOSYSTEM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENES, MITOCHONDRIAL; GENETIC SPECIATION; GENETICS, POPULATION; LAKES; MAINE; MITOCHONDRIA; OXIDATIVE PHOSPHORYLATION; SALMONIDAE; SPECIES SPECIFICITY; STATISTICS, NONPARAMETRIC; SYMPATRY; TRANSCRIPTION, GENETIC; UP-REGULATION;

MAINE; UNITED STATES;

COREGONUS; COREGONUS CLUPEAFORMIS;

EID: 84865187166     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2012.02570.x     Document Type: Article

References (67)

1. Aljanabi, S.M. & Martinez, I. 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res. 25: 4692-4693.
2. Ballard, J.W. & Melvin, R.G. 2010. Linking the mitochondrial genotype to the organismal phenotype. Mol. Ecol. 19: 1523-1539.
3. Bayona-Bafaluy, M.P., Muller, S. & Moraes, C.T. 2005. Fast adaptive coevolution of nuclear and mitochondrial subunits of ATP synthetase in orangutan. Mol. Biol. Evol. 22: 716-724.
4. Bernatchez, L. & Dodson, J.J. 1990. Allopatric origin of sympatric populations of lake whitefish (Coregonus clupeaformis) as revealed by mitochondrial-DNA restriction analysis. Evolution 44: 1263-1271.
5. Bernatchez, L. & Danzmann, R.G. 1993. Congruence in control-region sequence and restriction-site variation in mitochondrial-DNA of brook charr (Salvelinus fontinalis Mitchill). Mol. Biol. Evol. 10: 1002-1014.
6. Bernatchez, L. & Dodson, J.J. 1994. Phylogenetic relationships among palearctic and nearctic whitefish (Coregonus sp.) populations as revealed by mitochondrial DNA variation. Can. J. Fish. Aquat. Sci. 51: 240-251.
7. Bernatchez, L., Renaut, S., Whiteley, A.R., Derome, N., Jeukens, J., Landry, L. et al. 2010. On the origin of species: insights from the ecological genomics of lake whitefish. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365: 1783-1800.
8. Blier, P.U., Dufresne, F. & Burton, R.S. 2001. Natural selection and the evolution of mtDNA encoded peptides: evidence for intergenomic co-adaptation. Trends Genet. 17: 400-406.
9. Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Hugget, J., Kubista, M. et al. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55: 611-622.
10. Campbell, D. & Bernatchez, L. 2004. Generic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Mol. Biol. Evol. 21: 945-956.
11. Cheviron, Z.A., Whitehead, A. & Brumfield, R.T. 2008. Transcriptomic variation and plasticity in rufous-collared sparrows (Zonotrichia capensis) along an altitudinal gradient. Mol. Ecol. 17: 4556-4569.
12. Dalziel, A.C., Moore, S.E. & Moyes, C.D. 2005. Mitochondrial enzyme content in the muscles of high-performance fish: evolution and variation among fiber types. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288: R163-R172.
13. Dalziel, A.C., Moyes, C.D., Fredriksson, E. & Lougheed, S.C. 2006. Molecular evolution of cytochrome c oxidase in high-performance fish (Teleostei: Scombroidei). J. Mol. Evol. 62: 319-331.
14. Derome, N., Duchesne, P. & Bernatchez, L. 2006. Parallelism in gene transcription among sympatric lake whitefish (Coregonus clupeaformis Mitchill) ecotypes. Mol. Ecol. 15: 1239-1249.
15. Ellison, C.K. & Burton, R.S. 2008. Interpopulation hybrid breakdown maps to the mitochondrial genome. Evolution 62: 631-638.
16. Ellison, C.K. & Burton, R.S. 2010. Cytonuclear conflict in interpopulation hybrids: the role of RNA polymerase in mtDNA transcription and replication. J. Evol. Biol. 23: 528-538.
17. Evans, M.L., Præbel, K., Peruzzi, S. & Bernatchez, L. 2012. Parallelism in the oxygen transport system of the lake whitefish: the role of physiological divergence in ecological speciation. Mol. Ecol. (in press), doi:10.1111/j.1365-294X.2012.05682.x.
18. Fan, S., Elmer, K.R. & Meyer, A. 2012. Genomics of adaptation and speciation in cichlid fishes: recent advances and analyses in African and Neotropical lineages. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367: 385-394.
19. Faul, F., Erdfelder, E., Lang, A.G. & Buchner, A. 2007. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav. Res. Methods 39: 175-191.
20. Gagnaire, P.-A., Normandeau, E. & Bernatchez, L. 2012. Comparative genomics reveals adaptive protein evolution and a possible cytonuclear incompatibility between European and American eels. Mol. Biol. Evol. (in press), doi:10.1093/molbev/mss076.
21. Garbian, Y., Ovadia, O., Dadon, S. & Mishmar, D. 2010. Gene expression patterns of oxidative phosphorylation complex I subunits are organized in clusters. PLoS ONE 5: e9985.
22. Garvin, M.R., Bielawski, J.P. & Gharrett, A.J. 2011. Positive Darwinian selection in the piston that powers proton pumps in complex I of the mitochondria of Pacific salmon. PLoS ONE 6: e24127.
23. Gershoni, M., Templeton, A.R. & Mishmar, D. 2009. Mitochondrial bioenergetics as a major motive force of speciation. Bioessays 31: 642-650.
24. Gilbert, T.L., Brown, J.R., Ohara, P.J., Buroker, N.E., Beckenbach, A.T. & Smith, M.J. 1988. Sequence of transfer Rna-thr and transfer Rna-pro from white sturgeon (Acipenser transmontanus) mitochondria. Nucleic Acids Res. 16: 11825.
25. Good, P. 2000. Permutation Tests: A Practical Guide to Resampling Methods for Testing Hypotheses. Springer, New York.
26. Gracey, A.Y., Troll, J.V. & Somero, G.N. 2001. Hypoxia-induced gene expression profiling in the euryoxic fish Gillichthys mirabilis. Proc. Natl Acad. Sci. USA 98: 1993-1998.
27. Gracey, A.Y., Fraser, E.J., Li, W., Fang, Y., Taylor, R.R., Rogers, J. et al. 2004. Coping with cold: an integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. Proc. Natl Acad. Sci. USA 101: 16970-16975.
28. Grossman, L.I., Wildman, D.E., Schmidt, T.R. & Goodman, M. 2004. Accelerated evolution of the electron transport chain in anthropoid primates. Trends Genet. 20: 578-585.
29. Guderley, H. 2004. Locomotor performance and muscle metabolic capacities: impact of temperature and energetic status. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 139: 371-382.
30. Hardewig, I., van Dijk, P.L., Moyes, C.D. & Pörtner, H.O. 1999. Temperature-dependent expression of cytochrome-c oxidase in Antarctic and temperate fish. Am. J. Physiol. 277: R508-R516.
31. Jeukens, J., Bittner, D., Knudsen, R. & Bernatchez, L. 2009. Candidate genes and adaptive radiation: insights from transcriptional adaptation to the limnetic niche among Coregonine fishes (Coregonus spp., Salmonidae). Mol. Biol. Evol. 26: 155-166.
32. Jørgensen, S.M., Kleveland, E.J., Grimholt, U. & Gjoen, T. 2006. Validation of reference genes for real-time polymerase chain reaction studies in Atlantic salmon. Mar. Biotechnol. 8: 398-408.
33. Kadenbach, B. 2003. Intrinsic and extrinsic uncoupling of oxidative phosphorylation. Biochim. Biophys. Acta 1604: 77-94.
34. Kaeuffer, R., Peichel, C.L., Bolnick, D.I. & Hendry, A.P. 2012. Parallel and nonparallel aspects of ecological, phenotypic, and genetic divergence across replicate population pairs of lake and stream stickleback. Evolution 66: 402-418.
35. Kahilainen, K. & Lehtonen, H. 2003. Piscivory and prey selection of four predator species in a whitefish dominated subarctic lake. J. Fish Biol. 63: 659-672.
36. Kahilainen, K., Malinen, T., Tuomaala, A. & Lehtonen, H. 2004. Diel and seasonal habitat and food segregation of three sympatric Coregonus lavaretus forms in a subarctic lake. J. Fish Biol. 64: 418-434.
37. Kelly, A.K., Waters, S.M., McGee, M., Fonseca, R.G., Carberry, C. & Kenny, D.A. 2011. mRNA expression of genes regulating oxidative phosphorylation in the muscle of beef cattle divergently ranked on residual feed intake. Physiol. Genomics 43: 12-23.
38. Landry, L., Vincent, W.F. & Bernatchez, L. 2007. Parallel evolution of lake whitefish dwarf ecotypes in association with limnological features of their adaptive landscape. J. Evol. Biol. 20: 971-984.
39. Landry, L. & Bernatchez, L. 2010. Role of epibenthic resource opportunities in the parallel evolution of lake whitefish species pairs (Coregonus sp.). J. Evol. Biol. 23: 2602-2613.
40. Lenaz, G. 2001. The mitochondrial production of reactive oxygen species: mechanisms and implications in human pathology. IUBMB Life 52: 159-164.
41. Lu, G.Q. & Bernatchez, L. 1999. Correlated trophic specialization and genetic divergence in sympatric lake whitefish ecotypes (Coregonus clupeaformis): Support for the ecological speciation hypothesis. Evolution 53: 1491-1505.
42. Lu, G., Basley, D.J. & Bernatchez, L. 2001. Contrasting patterns of mitochondrial DNA and microsatellite introgressive hybridization between lineages of lake whitefish (Coregonus clupeaformis); relevance for speciation. Mol. Ecol. 10: 965-985.
43. Martinez-Fernandez, M., Bernatchez, L., Rolan-Alvarez, E. & Quesada, H. 2010. Insights into the role of differential gene expression on the ecological adaptation of the snail Littorina saxatilis. BMC Evol. Biol. 10: 356.
44. Mishmar, D., Ruiz-Pesini, E., Golik, P., Macaulay, V., Clark, A.G., Hosseini, S. et al. 2003. Natural selection shaped regional mtDNA variation in humans. Proc. Natl Acad. Sci. USA 100: 171-176.
45. Moyes, C.D. 2003. Controlling muscle mitochondrial content. J. Exp. Biol. 206: 4385-4391.
46. Olsvik, P.A., Lie, K.K., Jordal, A.E., Nilsen, T.O. & Hordvik, I. 2005. Evaluation of potential reference genes in real-time RT-PCR studies of Atlantic salmon. BMC Mol. Biol. 6: 21.
47. Pigeon, D., Chouinard, A. & Bernatchez, L. 1997. Multiple modes of speciation involved in the parallel evolution of sympatric morphotypes of lake whitefish (Coregonus clupeaformis, Salmonidae). Evolution 51: 196-205.
48. Pörtner, H.O., Schulte, P.M., Wood, C.M. & Schiemer, F. 2010. Niche dimensions in fishes: an integrative view. Physiol. Biochem. Zool. 83: 808-826.
49. 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.
50. Reinecke, F., Smeitink, J.A.M. & van der Westhuizen, F.H. 2009. OXPHOS gene expression and control in mitochondrial disorders. Biochim. Biophys. Acta 1792: 1113-1121.
51. Renaut, S., Nolte, A.W. & Bernatchez, L. 2010. Mining transcriptome sequences towards identifying adaptive single nucleotide polymorphisms in lake whitefish species pairs (Coregonus spp. Salmonidae). Mol. Ecol. 19: 115-131.
52. Renaut, S., Nolte, A.W., Rogers, S.M., Derome, N. & Bernatchez, L. 2011. SNP signatures of selection on standing genetic variation and their association with adaptive phenotypes along gradients of ecological speciation in lake whitefish species pairs (Coregonus spp.). Mol. Ecol. 20: 545-559.
53. Robinson, B.W. & Wilson, D.S. 1994. Character release and displacement in fishes - a neglected literature. Am. Nat. 144: 596-627.
54. Rogers, S.M., Gagnon, V. & Bernatchez, L. 2002. Genetically based phenotype-environment association for swimming behavior in lake whitefish ecotypes (Coregonus clupeaformis Mitchill). Evolution 56: 2322-2329.
55. Rosenblum, E.B. & Harmon, L.J. 2011. "Same same but different": replicated ecological speciation at White Sands. Evolution 65: 946-960.
56. Ruiz-Pesini, E., Mishmar, D., Brandon, M., Procaccio, V. & Wallace, D.C. 2004. Effects of purifying and adaptive selection on regional variation in human mtDNA. Science 303: 223-226.
57. Sanogo, Y.O., Hankison, S., Band, M., Obregon, A. & Bell, A.M. 2011. Brain transcriptomic response of threespine sticklebacks to cues of a predator. Brain Behav. Evol. 77: 270-285.
58. Saraste, M. 1999. Oxidative phosphorylation at the fin de siecle. Science 283: 1488-1493.
59. Scott, G.R., Schulte, P.M., Egginton, S., Scott, A.L.M., Richards, J.G. & Milsom, W.K. 2010. Molecular evolution of cytochrome c oxidase underlies high-altitude adaptation in the bar-headed goose. Mol. Biol. Evol. 28: 351-363.
60. Seebacher, F., Brand, M.D., Else, P.L., Guderley, H., Hulbert, A.J. & Moyes, C.D. 2010. Plasticity of oxidative metabolism in variable climates: molecular mechanisms. Physiol. Biochem. Zool. 83: 721-732.
61. 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.
62. Storey, K.B. 2007. Anoxia tolerance in turtles: metabolic regulation and gene expression. Comp. Biochem. Physiol., Part A Mol. Integr. Physiol. 147: 263-276.
63. Storz, J.F., Scott, G.R. & Cheviron, Z.A. 2010. Phenotypic plasticity and genetic adaptation to high-altitude hypoxia in vertebrates. J. Exp. Biol. 213: 4125-4136.
64. Trudel, M., Tremblay, A., Schetagne, R. & Rasmussen, J.B. 2001. Why are dwarf fish so small? An energetic analysis of polymorphism in lake whitefish (Coregonus clupeaformis). Can. J. Fish. Aquat. Sci. 58: 394-405.
65. van Waveren, C. & Moraes, C.T. 2008. Transcriptional co-expression and co-regulation of genes coding for components of the oxidative phosphorylation system. BMC Genomics 9: 18.
66. Whiteley, A.R., Derome, N., Rogers, S.M., St-Cyr, J., Laroche, J., Labbe, A. et al. 2008. The phenomics and expression quantitative trait locus mapping of brain transcriptomics regulating adaptive divergence in lake whitefish species pairs (Coregonus sp.). Genetics 180: 147-164.
67. Zar, J.H. 1999. Biostatistical Analysis. Prentice Hall, New Jersey.