The evolution and adaptive potential of transcriptional variation in sticklebacks - Signatures of selection and widespread heritability

Molecular Biology and Evolution

Volumn 32, Issue 3, 2015, Pages 674-689

  Leder, Erica H ^a   McCairns, R J Scott ^b   Leinonen, Tuomas ^b   Cano, José M ^c   Viitaniemi, Heidi M ^a   Nikinmaa, Mikko ^a   Primmer, Craig R ^a   Merilä, Juha ^b  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF OVIEDO   (Spain)

Author keywords

Gasterosteus aculeatus; Gene expression; Microarray; QST; Quantitative genetics; Transcriptome

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CHROMOSOME 19; CHROMOSOME 21; COMPARATIVE STUDY; CONTROLLED STUDY; DIRECTIONAL SELECTION; EVOLUTION; FEMALE; GENE EXPRESSION; GENE MAPPING; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENETIC VARIATION; GENOTYPE; GENOTYPE ENVIRONMENT INTERACTION; HEREDITY; HERITABILITY; INHERITANCE; KARYOTYPE; LIVER; MALE; NATURAL SELECTION; NONHUMAN; QUANTITATIVE GENETICS; QUANTITATIVE TRAIT; STICKLEBACK; TRANSCRIPTOMICS; ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC SELECTION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; SMEGMAMORPHA;

FISH PROTEIN; TRANSCRIPTOME;

ANIMALS; EVOLUTION, MOLECULAR; FEMALE; FISH PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; MALE; SELECTION, GENETIC; SMEGMAMORPHA; TRANSCRIPTOME;

EID: 84982189674     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu328     Document Type: Article

References (124)

1. Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G. 2008. LOSITAN: a workbench to detect molecular adaptation based on a FST-outlier method. BMC Bioinformatics 9:323.
2. Aubin-Horth N, Renn SCP. 2009. Genomic reaction norms: using integrative biology to understand molecular mechanisms of phenotypic plasticity. Mol Ecol. 18:3763-3780.
3. Ayroles JF, CarboneMA, Stone EA, Jordan KW, Lyman RF,Magwire MM, Rollmann SM, Duncan LH, Lawrence F, Anholt RRH, et al. 2009. Systems genetics of complex traits in Drosophila melanogaster. Nat Genet. 41:299-307.
4. Bar-Even A, Paulsson J, Maheshri N, Carmi M, O'Shea E, Pilpel Y, Barkai N. 2006. Noise in protein expression scales with natural protein abundance. Nat Genet. 38:636-643.
5. Barber I, Arnott SA. 2000. Split-clutch IVF: a technique to examine indirect fitness consequences of mate preferences in sticklebacks. Behaviour 137:1129-1140.
6. Bedford T, Hartl DL. 2009. Optimization of gene expression by natural selection. Proc Natl Acad Sci U S A. 106:1133-1138.
7. Björck S. 1995. A review of the history of the Baltic Sea, 13.0-8.0 ka BP. Quat Int. 27:19-40.
8. Brawand D, Soumillon M, Necsulea A, Julien P, Csárdi G, Harrigan P, Weier M, Liechti A, Aximu-Petri A, Kircher M, et al. 2011. The evolution of gene expression levels in mammalian organs. Nature 478: 343-348.
9. Brem RB, Yvert G, Clinton R, Kruglyak L. 2002. Genetic dissection of transcriptional regulation in budding yeast. Science 296:752-755.
10. Brownstein MJ, Carpten JD, Smith JR. 1996. Modulation of nontemplated nucleotide addition by tag DNA polymerase: primer modifications that facilitate genotyping. Biotechniques 20: 1004-1006.
11. Cano JM, Mäkinen HS, Leinonen T, Freyhof J, Merilä J. 2008. Extreme neutral genetic and morphological divergence supports classification of Adriatic three-spined stickleback (Gasterosteus aculeatus) populations as distinct conservation units. Biol Conserv. 141: 1055-1066.
12. Cano JM, Matsuba C, Mäkinen H, Merilä J. 2006. The utility of QTLLinked markers to detect selective sweeps in natural populations: a case study of the EDA gene and a linked marker in threespine stickleback. Mol Ecol. 15:4613-4621.
13. Chan YF, Marks ME, Jones FC, Villarreal G, Shapiro MD, Brady SD, Southwick AM, Absher DM, Grimwood J, Schmutz J, et al. 2010. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327:302-305.
14. Chelaifa H, Chagué V, Chalabi S, Mestiri I, Arnaud D, Deffains D, Lu YH, Belcram H, Huteau V, Chiquet J, et al. 2013. Prevalence of gene expression additivity in genetically stable wheat allohexaploids. New Phytol. 197:730-736.
15. Colbourne JK, Pfrender ME, Gilbert D, Thomas WK, Tucker A, Oakley TH, Tokishita S, Aerts A, Arnold GJ, Basu MK, et al. 2011. The ecoresponsive genome of Daphnia pulex. Science 331:555-561.
16. Cui XQ, Affourtit J, Shockley KR, Woo Y, Churchill GA. 2006. Inheritance patterns of transcript levels in F1 hybrid mice. Genetics 174:627-637.
17. Davidson EH, Erwin DH. 2010. Evolutionary innovation and stability in animal gene networks. J Exp Zool B Mol Dev Evol. 314B:182-186.
18. Debes PV, Normandeau E, Fraser DJ, Bernatchez L, Hutchings JA. 2012. Differences in transcription levels among wild, domesticated, and hybrid Atlantic salmon (Salmo salar) from two environments. Mol Ecol. 21:2574-2587.
19. Denver DR, Morris K, Streelman JT, Kim SK, Lynch M, Thomas WK. 2005. The transcriptional consequences of mutation and natural selection in Caenorhabditis elegans. Nat Genet. 37:544-548.
20. Dixon AL, Liang L, Moffatt MF, Chen W, Heath S, Wong KCC, Taylor J, Burnett E, Gut I, Farrall M, et al. 2007. A genome-wide association study of global gene expression. Nat Genet. 39:1202-1207.
21. Durinck S, Moreau Y, Kasprzyk A, Davis S, De Moor B, Brazma A, Huber W. 2005. BioMart and Bioconductor: a powerful link between biological databases and microarray data analysis. Bioinformatics 21: 3439-3440.
22. Emerson JJ, Hsieh LC, Sung HM, Wang TY, Huang CJ, Lu HHS, Lu MYJ, Wu SH, LiWH. 2010. Natural selection on cis and trans regulation in yeasts. Genome Res. 20:826-836.
23. Eng KH, Bravo HC, Keles S. 2009. A phylogenetic mixture model for the evolution of gene expression. Mol Biol Evol. 26:2363-2372.
24. Erwin DH, Davidson EH. 2009. The evolution of hierarchical gene regulatory networks. Nat Rev Genet. 10:141-148.
25. Fay JC, Wittkopp PJ. 2008. Evaluating the role of natural selection in the evolution of gene regulation. Heredity 100:191-199.
26. Flint J, Mackay TFC. 2009. Genetic architecture of quantitative traits in mice, flies, and humans. Genome Res. 19:723-733.
27. Gao Y, Zhang H, Gao Q, Wang LL, Zhang FC, Siva VS, Zhou Z, Song LS, Zhang SC. 2013. Transcriptome analysis of artificial hybrid pufferfish Jiyan-1 and its parental species: implications for pufferfish heterosis. PLoS One 8:e58453.
28. Ghazalpour A, Bennett B, Petyuk VA, Orozco L, Hagopian R, Mungrue IN, Farber CR, Sinsheimer J, Kang HM, Furlotte N, et al. 2011. Comparative analysis of proteome and transcriptome variation in mouse. PLoS Genet. 7:e1001393.
29. Gibson G. 2008. The environmental contribution to gene expression profiles. Nat Rev Genet. 9:575-581.
30. Gibson G, Weir B. 2005. The quantitative genetics of transcription. Trends Genet. 21:616-623.
31. Gienapp P, Teplitsky C, Alho JS, Mills JA, Merilä J. 2008. Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol. 17:167-178.
32. Gilad Y, Oshlack A, Rifkin SA. 2006. Natural selection on gene expression. Trends Genet. 22:456-461.
33. Gilad Y, Oshlack A, Smyth GK, Speed TP, White KP. 2006. Expression profiling in primates reveals a rapid evolution of human transcription factors. Nature 440:242-245.
34. Gilad Y, Rifkin SA, Pritchard JK. 2008. Revealing the architecture of gene regulation: the promise of eQTL studies. Trends Genet. 24:408-415.
35. Greenbaum D, Colangelo C, Williams K, Gerstein M. 2003. Comparing protein abundance andmRNA expression levels on a genomic scale. Genome Biol. 4:117.
36. Greenwood AK, Cech JN, Peichel CL. 2012. Molecular and developmental contributions to divergent pigment patterns in marine and freshwater sticklebacks. Evol Dev. 14:351-362.
37. Hadfield JD. 2010. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw. 33:1-22.
38. Haig D. 2010. Does heritability hide in epistasis between linked SNPs? Eur J Hum Genet. 19:123.
39. Hanawalt PC, Spivak G. 2008. Transcription-coupled DNA repair: two decades of progress and surprises. Nat Rev Mol Cell Biol. 9: 958-970.
40. Harris MA, Clark J, Ireland A, Lomax J, AshburnerM, Foulger R, Eilbeck K, Lewis S, Marshall B, Mungall C, et al. 2004. The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res. 32:D258-D261.
41. Hendry AP, Kinnison MT. 1999. The pace of modern life: measuring rates of contemporary microevolution. Evolution 53:1637-1653.
42. Hindorff LA, Sethupathy P, Junkins HA, Ramos EM, Mehta JP, Collins FS, Manolio TA. 2009. Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc Natl Acad Sci U S A. 106:9362-9367.
43. Hines HM, Papa R, Ruiz M, Papanicolaou A, Wang C, Nijhout HF, McMillan WO, Reed RD. 2012. Transcriptome analysis reveals novel patterning and pigmentation genes underlying Heliconius butterfly wing pattern variation. BMC Genomics 13:288.
44. Hoffmann AA, Sgró CM. 2011. Climate change and evolutionary adaptation. Nature 470:479-485.
45. Hoffmann AA, Willi Y. 2008. Detecting genetic responses to environmental change. Nat Rev Genet. 9:421-432.
46. Houle D, Govindaraju DR, Omholt S. 2010. Phenomics: the next challenge. Nat Rev Genet. 11:855-866.
47. Huang DW, Sherman BT, Lempicki RA. 2009. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37:1-13.
48. Huang DW, Sherman BT, Tan Q, Collins JR, Alvord WG, Roayaei J, Stephens R, Baseler MW, Lane HC, Lempicki RA. 2007. The DAVID gene functional classification tool: a novel biological module-centric algorithm to functionally analyze large gene lists. Genome Biol. 8:R183.
49. Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E, Johnson J, Swofford R, Pirun M, Zody MC, White S, et al. 2012. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484: 55-61.
50. Kaern M, Elston TC, Blake WJ, Collins JJ. 2005. Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet. 6:451-464.
51. Khaitovich P, Enard W, Lachmann M, Pääbo S. 2006. Evolution of primate gene expression. Nat Rev Genet. 7:693-702.
52. Khaitovich P, Hellmann I, Enard W, Nowick K, Leinweber M, Franz H, Weiss G, Lachmann M, Pääbo S. 2005. Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees. Science 309:1850-1854.
53. Khaitovich P, Weiss G, Lachmann M, Hellmann I, Enard W, Muetzel B, Wirkner U, Ansorge W, Paabo S. 2004. A neutral model of transcriptome evolution. PLoS Biol. 2:682-689.
54. Kim J, Gibson G. 2010. Insights from GWAS into the quantitative genetics of transcription in humans. Genet Res. 92:361-369.
55. Kim N, Jinks-Robertson S. 2012. Transcription as a source of genome instability. Nat Rev Genet. 13:204-214.
56. Kitano J, Lema SC, Luckenbach JA, Mori S, Kawagishi Y, Kusakabe M, Swanson P, Peichel CL. 2010. Adaptive divergence in the thyroid hormone signaling pathway in the stickleback radiation. Curr Biol. 20:2124-2130.
57. Kohn MH, Shapiro J, Wu CI. 2008. Decoupled differentiation of gene expression and coding sequence among Drosophila populations. Genes Genet Syst. 83:265-273.
58. Ku CS, Loy EY, Pawitan Y, Chia KS. 2010. The pursuit of genome-wide association studies: where are we now? J Hum Genet. 55:195-206.
59. Landry CR, Lemos B, Rifkin SA, Dickinson WJ, Hartl DL. 2007. Genetic properties influencing the evolvability of gene expression. Science 317:118-121.
60. Landry CR, Oh J, Hartl DL, Cavalieri D. 2006. Genome-wide scan reveals that genetic variation for transcriptional plasticity in yeast is biased towards multi-copy and dispensable genes. Gene 366:343-351.
61. Leder EH, Cano JM, Leinonen T, O'Hara RB, Nikinmaa M, Primmer CR, Merilä J. 2010. Female-biased expression on the X chromosome as a key step in sex chromosome evolution in threespine sticklebacks. Mol Biol Evol. 27:1495-1503.
62. Leder EH, Merilä J, Primmer CR. 2009. A flexible whole-genome microarray for transcriptomics in three-spine stickleback (Gasterosteus aculeatus). BMC Genomics 10:426.
63. Leinonen T, Cano JM, Merilä J. 2011. Genetics of body shape and armour variation in threespine sticklebacks. J Evol Biol. 24:206-218.
64. Leinonen T, McCairns RJS, O'Hara RB, Merilä J. 2013. QST-FST comparisons: evolutionary and ecological insights from genomic heterogeneity. Nat Rev Genet. 14:179-190.
65. Lemos B, Araripe LO, Fontanillas P, Hartl DL. 2008. Dominance and the evolutionary accumulation of cis-and trans-effects on gene expression. Proc Natl Acad Sci U S A. 105:14471-14476.
66. Lemos B, Meiklejohn CD, Cáceres M, Hartl DL. 2005. Rates of divergence in gene expression profiles of primates, mice, and flies: stabilizing selection and variability among functional categories. Evolution 59: 126-137.
67. Leveelahti L, Leskinen P, Leder EH, Waser W, Nikinmaa M. 2011. Responses of threespine stickleback (Gasterosteus aculeatus, L) transcriptome to hypoxia. Comp Biochem Physiol Part D Genomics Proteomics. 6:370-381.
68. Li Y, Lvarez OAA, Gutteling EW, Tijsterman M, Fu JJ, Riksen JAG, Hazendonk E, Prins P, Plasterk RHA, Jansen RC, et al. 2006. Mapping determinants of gene expression plasticity by genetical genomics in C. elegans. PLoS Genet. 2:2155-2161.
69. Li B, Zhang DF, Jia GQ, Dai JR, Wang SC. 2009. Genome-wide comparisons of gene expression for yield heterosis in maize. Plant Mol Biol Rep. 27:162-176.
70. Liao BY, Weng MP, Zhang JZ. 2010. Contrasting genetic paths to morphological and physiological evolution. Proc Natl Acad Sci U S A. 107: 7353-7358.
71. Lockhart DJ, Winzeler EA. 2000. Genomics, gene expression and DNA arrays. Nature 405:827-836.
72. Lynch M. 1990. The rate of morphological evolution in mammals from the standpoint of the neutral expectation. Am Nat. 136:727-741.
73. Lynch M, Walsh B. 1998. Genetics and analysis of quantitative traits. Sunderland (MA): Sinauer.
74. MacLean RC. 2010. Predicting epistasis: an experimental test of metabolic control theory with bacterial transcription and translation. J Evol Biol. 23:488-493.
75. Maglott D, Ostell J, Pruitt KD, Tatusova T. 2005. Entrez Gene: genecentered information at NCBI. Nucleic Acids Res. 33:D54-D58.
76. Mäkinen HS, Cano JM, Merilä J. 2006. Genetic relationships among marine and freshwater populations of the European threespined stickleback (Gasterosteus aculeatus) revealed by microsatellites. Mol Ecol. 15:1519-1534.
77. Mäkinen HS, Merilä J. 2008. Mitochondrial DNA phylogeography of the three-spined stickleback (Gasterosteus aculeatus) in Europe: evidence for multiple glacial refugia. Mol Phylogenet Evol. 46:167-182.
78. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, et al. 2009. Finding the missing heritability of complex diseases. Nature 461: 747-753.
79. Martincorena I, Seshasayee ASN, Luscombe NM. 2012. Evidence of nonrandom mutation rates suggests an evolutionary risk management strategy. Nature 485:95-98.
80. McCairns RJS, Bernatchez L. 2010. Adaptive divergence between freshwater and marine sticklebacks: insights into the role of phenotypic plasticity from an integrated analysis of candidate gene expression. Evolution 64:1029-1047.
81. Mecham BH, Nelson PS, Storey JD. 2010. Supervised normalization of microarrays. Bioinformatics 26:1308-1315.
82. Monks SA, Leonardson A, Zhu H, Cundiff P, Pietrusiak P, Edwards S, Phillips JW, Sachs A, Schadt EE. 2004. Genetic inheritance of gene expression in human cell lines. Am J Hum Genet. 75:1094-1105.
83. Morrissey MB, Wilson AJ, Pemberton JM, Ferguson MM. 2007. A framework for power and sensitivity analyses for quantitative genetic studies of natural populations, and case studies in Soay sheep (Ovis aries). J Evol Biol. 20:2309-2321.
84. Nikinmaa M, McCairns RJS, Nikinmaa MW, Vuori KA, Kanerva M, Leinonen T, Primmer CR, Merilä J, Leder EH. 2013. Transcription and redox enzyme activities: comparison of equilibrium and disequilibrium levels in the three-spined stickleback. Proc R Soc B Lond Biol Sci. 280:20122974.
85. Nuzhdin SV, Wayne ML, Harmon KL, McIntyre LM. 2004. Common pattern of evolution of gene expression level and protein sequence in Drosophila. Mol Biol Evol. 21:1308-1317.
86. Ogasawara O, Okubo K. 2009. On theoretical models of gene expression evolution with random genetic drift and natural selection. PLoS One 4:e7943.
87. Oleksiak MF, Churchill GA, Crawford DL. 2002. Variation in gene expression within and among natural populations. Nat Genet. 32: 261-266.
88. Ovaskainen O, Cano JM, Merilä J. 2008. A Bayesian framework for comparative quantitative genetics. Proc R Soc Lond B Biol Sci. 275: 669-678.
89. Park C, Qian WF, Zhang JZ. 2012. Genomic evidence for elevated mutation rates in highly expressed genes. EMBO Rep. 13:1123-1129.
90. Pea G, Ferron S, Gianfranceschi L, Krajewski P, Pè ME. 2008. Gene expression non-additivity in immature ears of a heterotic F1 maize hybrid. Plant Sci. 174:17-24.
91. Petretto E, Mangion J, Dickens NJ, Cook SA, Kumaran MK, Lu H, Fischer J, Maatz H, Kren V, Pravenec M, et al. 2006. Heritability and tissue specificity of expression quantitative trait loci. PLoS Genet. 2:e172.
92. Powell JE, Henders AK, McRae AF, Kim J, Hemani G, Martin NG, Dermitzakis ET, Gibson G, Montgomery GW, Visscher PM. 2013. Congruence of additive and non-additive effects on gene expression estimated from pedigree and SNP data. PLoS Genet. 9:e1003502.
93. Price AL, Helgason A, Thorleifsson G, McCarroll SA, Kong A, Stefansson K. 2011. Single-tissue and cross-tissue heritability of gene expression via identity-by-descent in related or unrelated individuals. PLoS Genet. 7:e1001317.
94. Qi B, Huang W, Zhu B, Zhong XF, Guo JH, Zhao N, Xu CM, Zhang HK, Pang JS, Han FP, et al. 2012. Global transgenerational gene expression dynamics in two newly synthesized allohexaploid wheat (Triticum aestivum) lines. BMC Biol. 10:3.
95. Qin S, Kim J, Arafat D, Gibson G. 2013. Effect of normalization on statistical and biological interpretation of gene expression profiles. Front Genet. 3:160.
96. Richards CL, Rosas U, Banta J, Bhambhra N, Purugganan MD. 2012. Genome-wide patterns of Arabidopsis gene expression in nature. PLoS Genet. 8:482-495.
97. Riddle NC, Jiang HM, An LL, Doerge RW, Birchler JA. 2010. Gene expression analysis at the intersection of ploidy and hybridity in maize. Theor Appl Genet. 120:341-353.
98. Rifkin SA, Houle D, Kim J, White KP. 2005. A mutation accumulation assay reveals a broad capacity for rapid evolution of gene expression. Nature 438:220-223.
99. Rifkin SA, Kim J, White KP. 2003. Evolution of gene expression in the Drosophila melanogaster subgroup. Nat Genet. 33:138-144.
100. Roberge C, Guderley H, Bernatchez L. 2007. Genomewide identification of genes under directional selection: gene transcription QST scan in diverging Atlantic salmon subpopulations. Genetics 177:1011-1022.
101. Roff DA. 1997. Evolutionary quantitative genetics. New York: Springer.
102. Rosa GJM, de Leon N, Rosa AJM. 2006. Review of microarray experimental design strategies for genetical genomics studies. Physiol Genomics. 28:15-23.
103. Rottscheidt R, Harr B. 2007. Extensive additivity of gene expression differentiates subspecies of the house mouse. Genetics 177: 1553-1567.
104. Schena M, Shalon D, Davis RW, Brown PO. 1995. Quantitative monitoring of gene-expression patterns with a complementary-DNA microarray. Science 270:467-470.
105. Sherman BT, Huang DW, Tan QN, Guo YJ, Bour S, Liu D, Stephens R, Baseler MW, Lane HC, Lempicki RA. 2007. DAVID knowledgebase: a gene-centered database integrating heterogeneous gene annotation resources to facilitate high-throughput gene functional analysis. BMC Bioinformatics 8:426.
106. Smedley D, Haider S, Ballester B, Holland R, London D, Thorisson G, Kasprzyk A. 2009. BioMart - biological queries made easy. BMC Genomics 10:22.
107. Spitze K. 1993. Population-structure in Daphnia obtusa: quantitative genetic and allozymic variation. Genetics 135:367-374.
108. Stafflberg N. 1939. Lake Vättern: outlines of its natural history, especially its vegetation. Uppsala (Sweden): Acta Phytogeographica Suecica.
109. Strimmer K. 2008. fdrtool: a versatile R package for estimating local and tail area-based false discovery rates. Bioinformatics 24:1461-1462.
110. Stupar RM, Hermanson PJ, Springer NM. 2007. Nonadditive expression and parent-of-origin effects identified by microarray and allele-specific expression profiling of maize endosperm. Plant Physiol. 145: 411-425.
111. Swanson-Wagner RA, Jia Y, DeCook R, Borsuk LA, Nettleton D, Schnable PS. 2006. All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proc Natl Acad Sci U S A. 103:6805-6810.
112. Visscher PM, Hill WG,Wray NR. 2008. Heritability in the genomics era - concepts and misconceptions. Nat Rev Genet. 9:255-266.
113. Wagner A. 2005. Energy constraints on the evolution of gene expression. Mol Biol Evol. 22:1365-1374.
114. Wagner A. 2007. Energy costs constrain the evolution of gene expression. J Exp Zool B Mol Dev Evol. 308B:322-324.
115. Wayne ML, Pan YJ, Nuzhdin SV, McIntyre LM. 2004. Additivity and trans-acting effects on gene expression in male Drosophila simulans. Genetics 168:1413-1420.
116. Wayne ML, Telonis-Scott M, Bono LM, Harshman L, Kopp A, Nuzhdin SV, McIntyre LM. 2007. Simpler mode of inheritance of transcriptional variation in male Drosophila melanogaster. Proc Natl Acad Sci U S A. 104:18577-18582.
117. Whitehead A, Crawford DL. 2006a. Neutral and adaptive variation in gene expression. Proc Natl Acad Sci U S A. 103:5425-5430.
118. Whitehead A, Crawford DL. 2006b.Variation within and amongspecies in gene expression: raw material for evolution. Mol Ecol. 15:1197-1211.
119. Whitlock MC. 2008. Evolutionary inference from QST. Mol Ecol. 17: 1885-1896.
120. Wolak ME. 2012. nadiv: an R package to create relatedness matrices for estimating non-additive genetic variances in animal models. Methods Ecol Evol. 3:792-796.
121. Wray GA. 2007. The evolutionary significance of cis-regulatory mutations. Nat Rev Genet. 8:206-216.
122. Wray GA. 2013. Genomics and the evolution of phenotypic traits. Annu Rev Ecol Evol Syst. 44:51-72.
123. Zhang X, Byrnes JK, Gal TS, Li WH, Borevitz JO. 2008. Whole genome transcriptome polymorphisms in Arabidopsis thaliana. Genome Biol. 9:R165.
124. Zuk O, Hechter E, Sunyaev SR, Lander ES. 2012. The mystery of missing heritability: genetic interactions create phantom heritability. Proc Natl Acad Sci U S A. 109:1193-1198.