Coevolution within and between Regulatory Loci Can Preserve Promoter Function Despite Evolutionary Rate Acceleration

1. HareEE, PetersonBK, IyerVN, MeierR, EisenMB (2008) Sepsid even-skipped enhancers are functionally conserved in Drosophila despite lack of sequence conservation. PLoS Genet 4: e1000106 doi:10.1371/journal.pgen.1000106.

2. SwansonCI, EvansNC, BaroloS (2010) Structural rules and complex regulatory circuitry constrain expression of a Notch- and EGFR-regulated eye enhancer. Developmental Cell 18: 359–370.

3. LudwigMZ, PatelNH, KreitmanM (1998) Functional analysis of eve stripe 2 enhancer evolution in Drosophila: Rules governing conservation and change. Development 125: 949–958.

4. DonigerSW, FayJC (2007) Frequent gain and loss of functional transcription factor binding sites. PLoS Comput Biol 3: e99 doi:10.1371/journal.pcbi.0030099.

5. HeBZ, HollowayAK, MaerklSJ, KreitmanM (2011) Does positive selection drive transcription factor binding site turnover? A test with Drosophila cis-regulatory modules. PLoS Genet 7: e1002053 doi:10.1371/journal.pgen.1002053.

6. ShawPJ, WrattenNS, McGregorAP, DoverGA (2002) Coevolution in bicoid-dependent promoters and the inception of regulatory incompatibilities among species of higher Diptera. Evol Dev 4: 265–277.

7. BakerCR, TuchBB, JohnsonAD (2011) Extensive DNA-binding specificity divergence of a conserved transcription regulator. Proc Natl Acad Sci U S A 108: 7493–7498.

8. LandryCR, WittkoppPJ, TaubesCH, RanzJM, ClarkAG, et al. (2005) Compensatory cis-trans evolution and the dysregulation of gene expression in interspecific hybrids of Drosophila. Genetics 171: 1813–1822.

9. TsankovAM, ThompsonDA, SochaA, RegevA, RandoOJ (2010) The role of nucleosome positioning in the evolution of gene regulation. PLoS Biol 8: e1000414 doi:10.1371/journal.pbio.1000414.

10. HittingerCT, GoncalvesP, SampaioJP, DoverJ, JohnstonM, et al. (2010) Remarkably ancient balanced polymorphisms in a multi-locus gene network. Nature 464: 54–58.

11. GerkeJ, LorenzK, CohenB (2009) Genetic interactions between transcription factors cause natural variation in yeast. Science 323: 498–501.

12. GaschAP, MosesAM, ChiangDY, FraserHB, BerardiniM, et al. (2004) Conservation and evolution of cis-regulatory systems in ascomycete fungi. PLoS Biol 2: e398 doi:10.1371/journal.pbio.0020398.

13. HittingerCT, CarrollSB (2007) Gene duplication and the adaptive evolution of a classic genetic switch. Nature 449: 677–681.

14. TuchBB, GalgoczyDJ, HerndayAD, LiH, JohnsonAD (2008) The evolution of combinatorial gene regulation in fungi. PLoS Biol 6: e38 doi:10.1371/journal.pbio.0060038.

15. WangXD, ChamberlinHM (2004) Evolutionary innovation of the excretory system in Caenorhabditis elegans. Nat Genet 36: 231–232.

16. SungH, WangT, WangD, HuangY, WuJ, et al. (2009) Roles of trans and cis variation in yeast intraspecies evolution of gene expression. Mol Biol Evol 26: 2533–2538.

17. MarcelliniS, SimpsonP (2006) Two or four bristles: Functional evolution of an enhancer of scute in Drosophilidae. PLoS Biol 4: e386 doi:10.1371/journal.pbio.0040386.

18. EmersonJJ, HsiehL, SungH, WangT, HuangC, et al. (2010) Natural selection on cis and trans regulation in yeasts. Genome Res 20: 826–836.

19. GibsonG, Riley-BergerR, HarshmanL, KoppA, VachaS, et al. (2004) Extensive sex-specific nonadditivity of gene expression in Drosophila melanogaster. Genetics 167: 1791–1799.

20. ChanET, QuonGT, ChuaG, BabakT, TrochessetM, et al. (2009) Conservation of core gene expression in vertebrate tissues. Journal of Biology 8: 33–33.

21. AparicioS, MorrisonA, GouldA, GilthorpeJ, ChaudhuriC, et al. (1995) Detecting conserved regulatory elements with the model genome of the Japanese puffer fish, Fugu rubripes. Proc Natl Acad Sci U S A 92: 1684–1688.

22. BarriereA, GordonKL, RuvinskyI (2011) Distinct functional constraints partition sequence conservation in a cis-regulatory element. PLoS Genet 7: e1002095 doi:10.1371/journal.pgen.1002095.

23. DoverGA, FlavellRB (1984) Molecular coevolution: DNA divergence and the maintenance of function. Cell 38: 622–623.

24. TrueJR, HaagES (2001) Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 3: 109–119.

25. TsongAE, TuchBB, LiH, JohnsonAD (2006) Evolution of alternative transcriptional circuits with identical logic. Nature 443: 415–420.

26. ChangY, LiuFR, YuN, SungH, YangP, et al. (2008) Roles of cis- and trans-changes in the regulatory evolution of genes in the gluconeogenic pathway in yeast. Mol Biol Evol 25: 1863–1875.

27. TiroshI, ReikhavS, LevyAA, BarkaiN (2009) A yeast hybrid provides insight into the evolution of gene expression regulation. Science 324: 659–662.

28. WittkoppPJ, HaerumBK, ClarkAG (2008) Regulatory changes underlying expression differences within and between Drosophila species. Nat Genet 40: 346–350.

29. McManusCJ, CoolonJD, DuffMO, Eipper-MainsJ, GraveleyBR, et al. (2010) Regulatory divergence in Drosophila revealed by mRNA-seq. Genome Res 20: 816–825.

30. GrazeRM, McIntyreLM, MainBJ, WayneML, NuzhdinSV (2009) Regulatory divergence in Drosophila melanogaster and D. simulans, a genomewide analysis of allele-specific expression. Genetics 183: 547–561.

31. Ortiz-BarrientosD, CountermanBA, NoorMAF (2007) Gene expression divergence and the origin of hybrid dysfunctions. Genetica 129: 71–81.

32. SkellyDA, RonaldJ, AkeyJM (2009) Inherited variation in gene expression. Annual Review of Genomics and Human Genetics 10: 313–332.

33. StrangerBE, ForrestMS, ClarkAG, MinichielloMJ, DeutschS, et al. (2005) Genome-wide associations of gene expression variation in humans. PLoS Genet 1: e78 doi:10.1371/journal.pgen.0010078.

34. TishkoffSA, ReedFA, RanciaroA, VoightBF, BabbittCC, et al. (2007) Convergent adaptation of human lactase persistence in Africa and Europe. Nat Genet 39: 31–40.

35. BeallCM, CavalleriGL, DengL, ElstonRC, GaoY, et al. (2010) Natural selection on EPAS1 (HIF2 alpha) associated with low hemoglobin concentration in Tibetan highlanders. Proc Natl Acad Sci U S A 107: 11459–11464.

36. GordonKL, RuvinskyI (2012) Tempo and mode in evolution of transcriptional regulation. PLoS Genet 8: e1002432 doi:10.1371/journal.pgen.1002432.

37. GilleardJS, BarryJD, JohnstoneIL (1997) Cis regulatory requirements for hypodermal cell-specific expression of the Caenorhabditis elegans cuticle collagen gene dpy-7. Mol Cell Biol 17: 2301–2311.

38. KennedyBP, AamodtEJ, AllenFL, ChungMA, HeschlMFP, et al. (1993) The gut esterase gene (ges-1) from the nematodes Caenorhabditis elegans and Caenorhabditis briggsae. J Mol Biol 229: 890–908.

39. KirouacM, SternbergPW (2003) Cis-regulatory control of three cell fate-specific genes in vulval organogenesis of Caenorhabditis elegans and C. briggsae. Dev Biol 257: 85–103.

40. RomanoLA, WrayGA (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.

41. WenickAS, HobertO (2004) Genomic cis-regulatory architecture and trans-acting regulators of a single interneuron-specific gene battery in C. elegans. Developmental Cell 6: 757–770.

42. WangXD, ChamberlinHM (2002) Multiple regulatory changes contribute to the evolution of the Caenorhabditis lin-48 ovo gene. Genes Dev 16: 2345–2349.

43. WittkoppPJ, VaccaroK, CarrollSB (2002) Evolution of yellow gene regulation and pigmentation in Drosophila. Current Biology 12: 1547–1556.

44. KiontkeK, GavinNP, RaynesY, RoehrigC, PianoF, et al. (2004) Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc Natl Acad Sci U S A 101: 9003–9008.

45. RuvinskyI, RuvkunG (2003) Functional tests of enhancer conservation between distantly related species. Development 130: 5133–5142.

46. McintireSL, JorgensenE, KaplanJ, HorvitzHR (1993) The GABAergic nervous-system of Caenorhabditis elegans. Nature 364: 337–341.

47. GuastellaJ, JohnsonCD, StrettonAOW (1991) GABA-immunoreactive neurons in the nematode Ascaris. J Comp Neurol 307: 584–597.

48. McIntireSL, ReimerRJ, SchuskeK, EdwardsRH, JorgensenEM (1997) Identification and characterization of the vesicular GABA transporter. Nature 389: 870–876.

49. ZhaoZ, BoyleTJ, BaoZ, MurrayJI, MericleB, et al. (2008) Comparative analysis of embryonic cell lineage between Caenorhabditis briggsae and Caenorhabditis elegans. Dev Biol 314: 93–99.

50. Frokjaer-JensenC, DavisMW, HopkinsCE, NewmanBJ, ThummelJM, et al. (2008) Single-copy insertion of transgenes in Caenorhabditis elegans. Nat Genet 40: 1375–1383.

51. WangX, SommerRJ (2011) Antagonism of LIN-17/Frizzled and LIN-18/Ryk in nematode vulva induction reveals evolutionary alterations in core developmental pathways. PLoS Biol 9: e1001110 doi:10.1371/journal.pbio.1001110.

52. SwansonCI, SchwimmerDB, BaroloS (2011) Rapid evolutionary rewiring of a structurally constrained eye enhancer. Current Biology 21: 1186–1196.

53. MaheshwariS, BarbashDA (2012) Cis-by-trans regulatory divergence causes the asymmetric lethal effects of an ancestral hybrid incompatibility gene. PLoS Genet 8: e1002597 doi:10.1371/journal.pgen.1002597.

54. OrrHA, TurelliM (2001) The evolution of postzygotic isolation: Accumulating Dobzhansky-Muller Incompatibilities. Evolution 55: 1085–1094.

55. BremRB, KruglyakL (2005) The landscape of genetic complexity across 5,700 gene expression traits in yeast. Proc Natl Acad Sci U S A 102: 1572–1577.

56. RanzJM, NamgyalK, GibsonG, HartlDL (2004) Anomalies in the expression profile of interspecific hybrids of Drosophila melanogaster and Drosophila simulans. Genome Res 14: 373–379.

57. RiesebergLH, WidmerA, ArntzAM, BurkeJM (2003) The genetic architecture necessary for transgressive segregation is common in both natural and domesticated populations. Phil Trans R Soc B 358: 1141–1147.

58. EmersonJJ, LiW (2010) The genetic basis of evolutionary change in gene expression levels. Phil Trans R Soc B 365: 2581–2590.

59. Powell-CoffmanJA, BradfieldCA, WoodWB (1998) Caenorhabditis elegans orthologs of the aryl hydrocarbon receptor and its heterodimerization partner the aryl hydrocarbon receptor nuclear translocator. Proc Natl Acad Sci U S A 95: 2844–2849.

60. QinH, ZhaiZ, Powell-CoffmanJA (2006) The Caenorhabditis elegans AHR-1 transcription complex controls expression of soluble guanylate cyclase genes in the URX neurons and regulates aggregation behavior. Dev Biol 298: 606–615.

61. HuangX, Powell-CoffmanJA, JinYS (2004) The AHR-1 aryl hydrocarbon receptor and its co-factor the AHA-1 aryl hydrocarbon receptor nuclear translocator specify GABAergic neuron cell fate in C. elegans. Development 131: 819–828.

62. QinHT, Powell-CoffmanJA (2004) The Caenorhabditis elegans aryl hydrocarbon receptor, AHR-1, regulates neuronal development. Dev Biol 270: 64–75.

63. LusskaA, ShenE, WhitlockJP (1993) Protein-DNA interactions at a dioxin-responsive enhancer. Analysis of 6 bona fide DNA-binding sites for the liganded Ah receptor. J Biol Chem 268: 6575–6580.

64. GroveCA, De MasiF, BarrasaMI, NewburgerDE, AlkemaMJ, et al. (2009) A multiparameter network reveals extensive divergence between C. elegans bHLH transcription factors. Cell 138: 314–327.

65. WalhoutAJM, van der VlietPC, TimmersHTM (1998) Sequences flanking the E-box contribute to cooperative binding by c-Myc/Max heterodimers to adjacent binding sites. Biochimica Et Biophysica Acta 139: 189–201.

66. MauranoMT, WangH, KutyavinT, StamatoyannopoulosJA (2012) Widespread site-dependent buffering of human regulatory polymorphism. PLoS Genet 8: e1002599 doi:10.1371/journal.pgen.1002599.

67. LudwigMZ, BergmanC, PatelNH, KreitmanM (2000) Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 403: 564–567.

68. EmeraD, WagnerGP (2012) Transformation of a transposon into a derived prolactin promoter with function during human pregnancy. Proc Natl Acad Sci U S A 109: 11246–11251.

69. KryazhimskiyS, DushoffJ, BazykinGA, PlotkinJB (2011) Prevalence of epistasis in the evolution of influenza A surface proteins. PLoS Genet 7: e1001301 doi:10.1371/journal.pgen.1001301.

70. OrtlundEA, BridghamJT, RedinboMR, ThorntonJW (2007) Crystal structure of an ancient protein: Evolution by conformational epistasis. Science 317: 1544–1548.

71. HaagES (2007) Compensatory vs. pseudocompensatory evolution in molecular and developmental interactions. Genetica 129: 45–55.

72. BullaugheyK (2012) Multidimensional adaptive evolution of a feed forward network and the illusion of compensation. Evolution In press.

73. RockmanMV, HahnMW, SoranzoN, ZimprichF, GoldsteinDB, et al. (2005) Ancient and recent positive selection transformed opioid cis-regulation in humans. PLoS Biol 3: e387 doi:10.1371/journal.pbio.0030387.

74. FrankelN, ErezyilmazD, McGregorAP, WangS, PayreF, et al. (2011) Morphological evolution caused by many subtle-effect substitutions in regulatory DNA. Nature 474: 598–603.

75. KuoD, LiconK, BandyopadhyayS, ChuangR, LuoC, et al. (2010) Coevolution within a transcriptional network by compensatory trans and cis mutations. Genome Res 20: 1672–1678.

76. WangXD, GreenbergJF, ChamberlinHM (2004) Evolution of regulatory elements producing a conserved gene expression pattern in Caenorhabditis. Evol Dev 6: 237–245.

77. LynchVJ, TanzerA, WangY, LeungFC, GellersenB, et al. (2008) Adaptive changes in the transcription factor HoxA-11 are essential for the evolution of pregnancy in mammals. Proc Natl Acad Sci U S A 105: 14928–14933.

78. BonnetonF, ShawPJ, FazakerleyC, ShiM, DoverGA (1997) Comparison of bicoid-dependent regulation of hunchback between Musca domestica and Drosophila melanogaster. Mech Dev 66: 143–156.

79. JohnsonNA, PorterAH (2007) Evolution of branched regulatory genetic pathways: Directional selection on pleiotropic loci accelerates Developmental System Drift. Genetica 129: 57–70.

80. LudwigMZ, PalssonA, AlekseevaE, BergmanCM, NathanJ, et al. (2005) Functional evolution of a cis-regulatory module. PLoS Biol 3: e93 doi:10.1371/journal.pbio.0030093.

81. CrockerJ, TamoriY, ErivesA (2008) Evolution acts on enhancer organization to fine-tune gradient threshold readouts. PLoS Biol 6: e263 doi:10.1371/journal.pbio.0060263.

82. ZillOA, ScannellD, TeytelmanL, RineJ (2010) Co-evolution of transcriptional silencing proteins and the DNA elements specifying their assembly. PLoS Biol 8: e1000550 doi:10.1371/journal.pbio.1000550.

83. XiaoW, PelcherLE, RankGH (1991) Evidence for cis-acting and trans-acting element coevolution of the 2-microns circle genome in Saccharomyces cerevisiae. J Mol Evol 32: 145–152.

84. HershBM, CarrollSB (2005) Direct regulation of knot gene expression by ultrabithorax and the evolution of cis-regulatory elements in Drosophila. Development 132: 1567–1577.

85. TakahasiKR, MatsuoT, Takano-Shimizu-KounoT (2011) Two types of cis-trans compensation in the evolution of transcriptional regulation. Proc Natl Acad Sci U S A 108: 15276–15281.

86. McGregorAP, ShawPJ, HancockJM, BoppD, HedigerM, et al. (2001) Rapid restructuring of bicoid-dependent hunchback promoters within and between Dipteran species: Implications for molecular coevolution. Evol Dev 3: 397–407.

87. BullaugheyK (2011) Changes in selective effects over time facilitate turnover of enhancer sequences. Genetics 187: 567–U328.

88. TakahashiH, MitaniY, SatohG, SatohN (1999) Evolutionary alterations of the minimal promoter for notochord-specific brachyury expression in ascidian embryos. Development 126: 3725–3734.

89. Oda-IshiiI, BertrandV, MatsuoI, LemaireP, SaigaH (2005) Making very similar embryos with divergent genomes: Conservation of regulatory mechanisms of Otx between the ascidians Halocynthia roretzi and Ciona intestinalis. Development 132: 1663–1674.

90. RiesebergLH, ArcherMA, WayneRK (1999) Transgressive segregation, adaptation and speciation. Heredity 83: 363–372.

91. BremRB, YvertG, ClintonR, KruglyakL (2002) Genetic dissection of transcriptional regulation in budding yeast. Science 296: 752–755.

92. HaertyW, SinghRS (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.

93. PhillipsPC (2008) Epistasis—the essential role of gene interactions in the structure and evolution of genetic systems. Nature Reviews Genetics 9: 855–867.

94. BloomJD, GongLI, BaltimoreD (2010) Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science 328: 1272–1275.

95. LunzerM, GoldingGB, DeanAM (2010) Pervasive cryptic epistasis in molecular evolution. PLoS Genet 6: e1001162 doi:10.1371/journal.pgen.1001162.

96. WeinreichDM, DelaneyNF, DePristoMA, HartlDL (2006) Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312: 111–114.

97. BridghamJT, OrtlundEA, ThorntonJW (2009) An epistatic ratchet constrains the direction of glucocorticoid receptor evolution. Nature 461: 515–U78.

98. AzevedoRBR, LohausR, SrinivasanS, DangKK, BurchCL (2006) Sexual reproduction selects for robustness and negative epistasis in artificial gene networks. Nature 440: 87–90.

99. GertzJ, GerkeJP, CohenBA (2010) Epistasis in a quantitative trait captured by a molecular model of transcription factor interactions. Theor Popul Biol 77: 1–5.

100. GerkeJ, LorenzK, RamnarineS, CohenB (2010) Gene-environment interactions at nucleotide resolution. PLoS Genet 6: e1001144 doi:10.1371/journal.pgen.1001144.

101. BremRB, StoreyJD, WhittleJ, KruglyakL (2005) Genetic interactions between polymorphisms that affect gene expression in yeast. Nature 436: 701–703.

102. SteinerCC, WeberJN, HoekstraHE (2007) Adaptive variation in beach mice produced by two interacting pigmentation genes. PLoS Biol 5: e219 doi:10.1371/journal.pbio.0050219.

103. WohlbachDJ, ThompsonDA, GaschAP, RegevA (2009) From elements to modules: Regulatory evolution in Ascomycota fungi. Curr Opin Genet Dev 19: 571–578.

104. PaixaoT, AzevedoRBR (2010) Redundancy and the evolution of cis-regulatory element multiplicity. PLoS Comput Biol 6: e1000848 doi:10.1371/journal.pcbi.1000848.

105. LiH, JohnsonAD (2010) Evolution of transcription networks—lessons from yeasts. Current Biology 20: R746–R753.

106. RebeizM, JikomesN, KassnerVA, CarrollSB (2011) Evolutionary origin of a novel gene expression pattern through co-option of the latent activities of existing regulatory sequences. Proc Natl Acad Sci U S A 108: 10036–10043.

107. DraghiJA, ParsonsTL, WagnerGP, PlotkinJB (2010) Mutational robustness can facilitate adaptation. Nature 463: 353–355.

108. KimJ (2001) Macro-evolution of the hairy enhancer in Drosophila species. J Exp Zool 291: 175–185.

109. WangRL, StecA, HeyJ, LukensL, DoebleyJ (1999) The limits of selection during maize domestication. Nature 398: 236–239.

110. SellaG, PetrovDA, PrzeworskiM, AndolfattoP (2009) Pervasive natural selection in the Drosophila genome? PLoS Genet 5: e1000495 doi:10.1371/journal.pgen.1000495.

111. PrabhakarS, NoonanJP, PaeaeboS, RubinEM (2006) Accelerated evolution of conserved noncoding sequences in humans. Science 314: 786–786.

112. PollardKS, SalamaSR, KingB, KernAD, DreszerT, et al. (2006) Forces shaping the fastest evolving regions in the human genome. PLoS Genet 2: e168 doi:10.1371/journal.pgen.0020168.

113. Lindblad-TohK, GarberM, ZukO, LinMF, ParkerBJ, et al. (2011) A high-resolution map of human evolutionary constraint using 29 mammals. Nature 478: 476–482.

114. GranatoM, SchnabelH, SchnabelR (1994) pha-1, a selectable marker for gene-transfer in C. elegans. Nucleic Acids Res 22: 1762–1763.

115. Evans TC (2006) Transformation and microinjection. In: WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.108.1, http://www.wormbook.org. Accessed 2012 Aug 14.