1932

Abstract

As a species, we possess unique biological features that distinguish us from other primates. Here, we review recent efforts to identify changes in gene regulation that drove the evolution of novel human phenotypes. We discuss genotype-directed comparisons of human and nonhuman primate genomes to identify human-specific genetic changes that may encode new regulatory functions. We also review phenotype-directed approaches, which use comparisons of gene expression or regulatory function in homologous human and nonhuman primate cells and tissues to identify changes in expression levels or regulatory activity that may be due to genetic changes in humans. Together, these studies are beginning to reveal the landscape of regulatory innovation in human evolution and point to specific regulatory changes for further study. Finally, we highlight two novel strategies to model human-specific regulatory functions in vivo: primate induced pluripotent stem cells and the generation of humanized mice by genome editing.

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2016-08-31
2024-06-19
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Literature Cited

  1. 1. 1000 Genomes Proj. Consort 2015. A global reference for human genetic variation. Nature 526:68–74 [Google Scholar]
  2. Aiello LC, Dean C. 2.  1990. An Introduction to Human Evolutionary Anatomy New York: Academic [Google Scholar]
  3. Antón SC, Potts R, Aiello LC. 3.  2014. Evolution of early Homo: an integrated biological perspective. Science 345:1236828 [Google Scholar]
  4. Bailey JA, Eichler EE. 4.  2006. Primate segmental duplications: crucibles of evolution, diversity and disease. Nat. Rev. Genet. 7:552–64 [Google Scholar]
  5. Barbosa-Morais NL, Irimia M, Pan Q, Xiong HY, Gueroussov S. 5.  et al. 2012. The evolutionary landscape of alternative splicing in vertebrate species. Science 338:1587–93 [Google Scholar]
  6. Battle A, Khan Z, Wang SH, Mitrano A, Ford MJ. 6.  et al. 2015. Impact of regulatory variation from RNA to protein. Science 347:664–67 [Google Scholar]
  7. Bauernfeind AL, Soderblom EJ, Turner ME, Moseley MA, Ely JJ. 7.  et al. 2015. Evolutionary divergence of gene and protein expression in the brains of humans and chimpanzees. Genome Biol. Evol. 7:2276–88 [Google Scholar]
  8. Bejerano G, Pheasant M, Makunin I, Stephen S, Kent WJ. 8.  et al. 2004. Ultraconserved elements in the human genome. Science 304:1321–25 [Google Scholar]
  9. Bernard A, Lubbers LS, Tanis KQ, Luo R, Podtelezhnikov AA. 9.  et al. 2012. Transcriptional architecture of the primate neocortex. Neuron 73:1083–99 [Google Scholar]
  10. Bird CP, Stranger BE, Liu M, Thomas DJ, Ingle CE. 10.  et al. 2007. Fast-evolving noncoding sequences in the human genome. Genome Biol 8:R118 [Google Scholar]
  11. Blekhman R, Marioni JC, Zumbo P, Stephens M, Gilad Y. 11.  2010. Sex-specific and lineage-specific alternative splicing in primates. Genome Res 20:180–89 [Google Scholar]
  12. Blekhman R, Oshlack A, Chabot AE, Smyth GK, Gilad Y. 12.  2008. Gene regulation in primates evolves under tissue-specific selection pressures. PLOS Genet 4:e1000271 [Google Scholar]
  13. Boyd JL, Skove SL, Rouanet JP, Pilaz L-J, Bepler T. 13.  et al. 2015. Human-chimpanzee differences in a FZD8 enhancer alter cell-cycle dynamics in the developing neocortex. Curr. Biol. 25:772–79 [Google Scholar]
  14. Brawand D, Soumillon M, Necsulea A, Julien P, Csárdi G. 14.  et al. 2011. The evolution of gene expression levels in mammalian organs. Nature 478:343–48 [Google Scholar]
  15. Britten RJ, Davidson EH. 15.  1969. Gene regulation for higher cells: a theory. Science 165:349–57 [Google Scholar]
  16. Britten RJ, Davidson EH. 16.  1971. Repetitive and non-repetitive DNA sequences and a speculation on the origins of evolutionary novelty. Q. Rev. Biol. 46:111–38 [Google Scholar]
  17. Bronner ME, LeDouarin NM. 17.  2012. Development and evolution of the neural crest: an overview. Dev. Biol. 366:2–9 [Google Scholar]
  18. Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ. 18.  2013. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10:1213–18 [Google Scholar]
  19. Cain CE, Blekhman R, Marioni JC, Gilad Y. 19.  2011. Gene expression differences among primates are associated with changes in a histone epigenetic modification. Genetics 187:1225–34 [Google Scholar]
  20. Capra JA, Erwin GD, McKinsey G, Rubenstein JLR, Pollard KS. 20.  2013. Many human accelerated regions are developmental enhancers. Philos. Trans. R. Soc. B 368:20130025 [Google Scholar]
  21. Capra JA, Hubisz MJ, Kostka D, Pollard KS, Siepel A. 21.  2013. A model-based analysis of GC-biased gene conversion in the human and chimpanzee genomes. PLOS Genet 9:e1003684 [Google Scholar]
  22. Carroll SB. 22.  2005. Evolution at two levels: on genes and form. PLOS Biol 3:e245 [Google Scholar]
  23. Chan YF, Marks ME, Jones FC, Villarreal G, Shapiro MD. 23.  et al. 2010. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327:302–5 [Google Scholar]
  24. 24. Chimpanzee Seq. Anal. Consort 2005. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437:69–87 [Google Scholar]
  25. Cong L, Ran FA, Cox D, Lin S, Barretto R. 25.  et al. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–23 [Google Scholar]
  26. Cooper GM. 26.  2004. Characterization of evolutionary rates and constraints in three mammalian genomes. Genome Res 14:539–48 [Google Scholar]
  27. Cotney J, Leng J, Oh S, DeMare LE, Reilly SK. 27.  et al. 2012. Chromatin state signatures associated with tissue-specific gene expression and enhancer activity in the embryonic limb. Genome Res 22:1069–80 [Google Scholar]
  28. Cotney J, Leng J, Yin J, Reilly SK, DeMare LE. 28.  et al. 2013. The evolution of lineage-specific regulatory activities in the human embryonic limb. Cell 154:185–96 [Google Scholar]
  29. Davidson EH. 29.  2001. Genomic Regulatory Systems: Development and Evolution New York: Academic [Google Scholar]
  30. Degner JF, Pai AA, Pique-Regi R, Veyrieras J-B, Gaffney DJ. 30.  et al. 2013. DNase I sensitivity QTLs are a major determinant of human expression variation. Nature 482:390–94 [Google Scholar]
  31. Dekker J, Marti-Renom MA, Mirny LA. 31.  2013. Exploring the three-dimensional organization of genomes: interpreting chromatin interaction data. Nat. Rev. Genet. 14:390–403 [Google Scholar]
  32. Dennis MY, Nuttle X, Sudmant PH, Antonacci F, Graves TA. 32.  et al. 2012. Evolution of human-specific neural SRGAP2 genes by incomplete segmental duplication. Cell 149:912–22 [Google Scholar]
  33. DeRisi JL, Iyer VR, Brown PO. 33.  1997. Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278:680–86 [Google Scholar]
  34. Dermitzakis ET. 34.  2003. Evolutionary discrimination of mammalian conserved non-genic sequences (CNGs). Science 302:1033–35 [Google Scholar]
  35. Doolittle WF. 35.  2013. Is junk DNA bunk? A critique of ENCODE. PNAS 110:5294–300 [Google Scholar]
  36. Duret L, Galtier N. 36.  2009. Biased gene conversion and the evolution of mammalian genomic landscapes. Annu. Rev. Genom. Hum. Genet. 10:285–311 [Google Scholar]
  37. Enard W, Khaitovich P, Klose J, Zöllner S, Heissig F. 37.  et al. 2002. Intra- and interspecific variation in primate gene expression patterns. Science 296:340–43 [Google Scholar]
  38. 38. ENCODE Proj. Consort 2011. A user's guide to the Encyclopedia of DNA Elements (ENCODE). PLOS Biol. 9:e1001046 [Google Scholar]
  39. 39. ENCODE Proj. Consort 2013. An integrated encyclopedia of DNA elements in the human genome. Nature 488:57–74 [Google Scholar]
  40. Ernst J, Kellis M. 40.  2010. Discovery and characterization of chromatin states for systematic annotation of the human genome. Nat. Biotechnol. 28:817–25 [Google Scholar]
  41. Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD. 41.  et al. 2011. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473:43–49 [Google Scholar]
  42. Erwin GD, Oksenberg N, Truty RM, Kostka D, Murphy KK. 42.  et al. 2014. Integrating diverse datasets improves developmental enhancer prediction. PLOS Comp. Biol. 10:e1003677–20 [Google Scholar]
  43. Farnham PJ. 43.  2009. Insights from genomic profiling of transcription factors. Nat. Rev. Genet. 10:605–16 [Google Scholar]
  44. Fisher WW, Li JJ, Hammonds AS, Brown JB, Pfeiffer BD. 44.  et al. 2012. DNA regions bound at low occupancy by transcription factors do not drive patterned reporter gene expression in Drosophila. PNAS 109:21330–35 [Google Scholar]
  45. Florio M, Albert M, Taverna E, Namba T, Brandl H. 45.  et al. 2015. Human-specific gene ARHGAP11B promotes basal progenitor amplification and neocortex expansion. Science 347:1465–70 [Google Scholar]
  46. Freese JL, Pino D, Pleasure SJ. 46.  2010. Wnt signaling in development and disease. Neurobiol. Dis. 38:148–53 [Google Scholar]
  47. Furey TS. 47.  2012. ChIP-seq and beyond: new and improved methodologies to detect and characterize protein-DNA interactions. Nat. Rev. Genet. 13:840–52 [Google Scholar]
  48. Gallego Romero I, Pavlovic BJ, Hernando-Herraez I, Zhou X, Ward MC. 48.  et al. 2015. A panel of induced pluripotent stem cells from chimpanzees: a resource for comparative functional genomics. eLife 4:e07103 [Google Scholar]
  49. Galtier N, Duret L, Glémin S, Ranwez V. 49.  2009. GC-biased gene conversion promotes the fixation of deleterious amino acid changes in primates. Trends Genet 25:1–5 [Google Scholar]
  50. Garber M, Grabherr MG, Guttman M, Trapnell C. 50.  2011. Computational methods for transcriptome annotation and quantification using RNA-seq. Nat. Methods 8:469–77 [Google Scholar]
  51. Geschwind DH, Rakic P. 51.  2013. Cortical evolution: judge the brain by its cover. Neuron 80:633–47 [Google Scholar]
  52. Gilad Y, Oshlack A, Smyth GK, Speed TP, White KP. 52.  2006. Expression profiling in primates reveals a rapid evolution of human transcription factors. Nature 440:242–45 [Google Scholar]
  53. Gittelman RM, Hun E, Ay F, Madeoy J, Pennacchio L. 53.  et al. 2015. Comprehensive identification and analysis of human accelerated regulatory DNA. Genome Res 25:1245–55 [Google Scholar]
  54. Harris EE. 54.  2010. Nonadaptive processes in primate and human evolution. Yearb. Phys. Anthropol. 53:13–45 [Google Scholar]
  55. Harrison-Uy SJ, Pleasure SJ. 55.  2012. Wnt signaling and forebrain development. Cold Spring Harb. Perspect. Biol. 4:a008094 [Google Scholar]
  56. Hawkins RD, Hon GC, Ren B. 56.  2010. Next-generation genomics: an integrative approach. Nat. Rev. Genet. 11:476–86 [Google Scholar]
  57. Haygood R, Babbitt CC, Fedrigo O, Wray GA. 57.  2010. Contrasts between adaptive coding and noncoding changes during human evolution. PNAS 107:7853–57 [Google Scholar]
  58. Haygood R, Fedrigo O, Hanson B, Yokoyama K-D, Wray GA. 58.  2007. Promoter regions of many neural- and nutrition-related genes have experienced positive selection during human evolution. Nat. Genet. 39:1140–44 [Google Scholar]
  59. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A. 59.  et al. 2009. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459:108 [Google Scholar]
  60. Kamm GB, Lopez-Leal R, Lorenzo JR, Franchini LF. 60.  2013. A fast-evolving human NPAS3 enhancer gained reporter expression in the developing forebrain of transgenic mice. Philos. Trans. R. Soc. B 368:20130019 [Google Scholar]
  61. Kamm GB, Pisciottano F, Kliger R, Franchini LF. 61.  2013. The developmental brain gene NPAS3 contains the largest number of accelerated regulatory sequences in the human genome. Mol. Biol. Evol. 30:1088–102 [Google Scholar]
  62. Kang HJ, Kawasawa YI, Cheng F, Zhu Y, Xu X. 62.  et al. 2011. Spatio-temporal transcriptome of the human brain. Nature 478:483–89 [Google Scholar]
  63. Khaitovich P. 63.  2005. Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees. Science 309:1850–54 [Google Scholar]
  64. Khaitovich P, Enard W, Lachmann M, Pääbo S. 64.  2006. Evolution of primate gene expression. Nat. Rev. Genet. 7:693–702 [Google Scholar]
  65. Khaitovich P, Weiss G, Lachmann M, Hellmann I, Enard W. 65.  et al. 2004. A neutral model of transcriptome evolution. PLOS Biol 2:e132 [Google Scholar]
  66. Khan Z, Ford MJ, Cusanovich DA, Mitrano A, Pritchard JK, Gilad Y. 66.  2013. Primate transcript and protein expression levels evolve under compensatory selection pressures. Science 342:1100–4 [Google Scholar]
  67. Kim SY, Pritchard JK. 67.  2007. Adaptive evolution of conserved noncoding elements in mammals. PLOS Genet 3:e147 [Google Scholar]
  68. Kimura M. 68.  1968. Evolutionary rate at the molecular level. Nature 217:624–26 [Google Scholar]
  69. King MC, Wilson AC. 69.  1975. Evolution at two levels in humans and chimpanzees. Science 188:107–16 [Google Scholar]
  70. Konopka G, Friedrich T, Davis-Turak J, Winden K, Oldham MC. 70.  et al. 2012. Human-specific transcriptional networks in the brain. Neuron 75:601–17 [Google Scholar]
  71. Kostka D, Hubisz MJ, Siepel A, Pollard KS. 71.  2012. The role of GC-biased gene conversion in shaping the fastest evolving regions of the human genome. Mol. Biol. Evol. 29:1047–57 [Google Scholar]
  72. Kundaje A, Meuleman W, Bilenky M, Yen A, Zhang Z. 72.  et al. 2015. Integrative analysis of 111 reference human epigenomes. Nature 518:317–30 [Google Scholar]
  73. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC. 73.  et al. 2001. Initial sequencing and analysis of the human genome. Nature 409:860–921 [Google Scholar]
  74. Langer J. 74.  2006. The heterochronic evolution of primate cognitive development. Biol. Theory 1:41–43 [Google Scholar]
  75. Lemos B, Meiklejohn CD, Cáceres M, Hartl DL. 75.  2005. Rates of divergence in gene expression profiles of primates, mice, and flies: stabilizing selection and variability among functional categories. Evolution 59:126–37 [Google Scholar]
  76. Lettice LA, Heaney SJH, Purdie LA, Li L, de Beer P. 76.  et al. 2003. A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum. Mol. Genet. 12:1725–35 [Google Scholar]
  77. Lindblad-Toh K, Garber M, Zuk O, Lin MF, Parker BJ. 77.  et al. 2011. A high-resolution map of human evolutionary constraint using 29 mammals. Nature 478:476–82 [Google Scholar]
  78. Liu X, Somel M, Tang L, Yan Z, Jiang X. 78.  et al. 2012. Extension of cortical synaptic development distinguishes humans from chimpanzees and macaques. Genome Res 22:611–22 [Google Scholar]
  79. Locke DP, Hillier LW, Warren WC, Worley KC, Nazareth LV. 79.  et al. 2011. Comparative and demographic analysis of orang-utan genomes. Nature 469:529–33 [Google Scholar]
  80. Love MI, Huber W, Anders S. 80.  2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550–21 [Google Scholar]
  81. Lupiáñez DG, Kraft K, Heinrich V, Krawitz P, Brancati F. 81.  et al. 2015. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161:1012–25 [Google Scholar]
  82. Marchetto MCN, Narvaiza I, Denli AM, Benner C, Lazzarini TA. 82.  et al. 2013. Differential L1 regulation in pluripotent stem cells of humans and apes. Nature 503:525–29 [Google Scholar]
  83. Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y. 83.  2008. RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18:1509–17 [Google Scholar]
  84. Marques-Bonet T, Kidd JM, Ventura M, Graves TA, Cheng Z. 84.  et al. 2009. A burst of segmental duplications in the genome of the African great ape ancestor. Nature 457:877–81 [Google Scholar]
  85. McLean CY, Reno PL, Pollen AA, Bassan AI, Capellini TD. 85.  et al. 2011. Human-specific loss of regulatory DNA and the evolution of human-specific traits. Nature 471:216–19 [Google Scholar]
  86. McVicker G, van de Geijn B, Degner JF, Cain CE, Banovich NE. 86.  et al. 2013. Identification of genetic variants that affect histone modifications in human cells. Science 342:747–49 [Google Scholar]
  87. Melnikov A, Murugan A, Zhang X, Tesileanu T, Wang L. 87.  et al. 2012. Systematic dissection and optimization of inducible enhancers in human cells using a massively parallel reporter assay. Nat. Biotechnol. 30:271–77 [Google Scholar]
  88. Merkin J, Russell C, Chen P, Burge CB. 88.  2012. Evolutionary dynamics of gene and isoform regulation in mammalian tissues. Science 338:1593–99 [Google Scholar]
  89. 89. Mouse Genome Seq. Consort 2002. Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–62 [Google Scholar]
  90. Niu D-K, Jiang L. 90.  2013. Can ENCODE tell us how much junk DNA we carry in our genome?. Biochem. Biophys. Res. Commun. 430:1340–43 [Google Scholar]
  91. Nobrega MA, Ovcharenko I, Afzal V, Rubin EM. 91.  2003. Scanning human gene deserts for long-range enhancers. Science 302:413 [Google Scholar]
  92. O'Bleness M, Searles VB, Varki A, Gagneux P, Sikela JM. 92.  2012. Evolution of genetic and genomic features unique to the human lineage. Nat. Rev. Genet. 13:853–66 [Google Scholar]
  93. Palazzo AF, Gregory TR. 93.  2014. The case for junk DNA. PLOS Genet 10:e1004351 [Google Scholar]
  94. Park PJ. 94.  2009. ChIP-seq: advantages and challenges of a maturing technology. Nat. Rev. Genet. 10:669–80 [Google Scholar]
  95. Pennacchio LA, Ahituv N, Moses AM, Prabhakar S, Nobrega MA. 95.  et al. 2006. In vivo enhancer analysis of human conserved non-coding sequences. Nature 444:499–502 [Google Scholar]
  96. Perry GH, Melsted P, Marioni JC, Wang Y, Bainer R. 96.  et al. 2011. Comparative RNA sequencing reveals substantial genetic variation in endangered primates. Genome Res 22:602–10 [Google Scholar]
  97. Pickrell JK, Marioni JC, Pai AA, Degner JF, Engelhardt BE. 97.  et al. 2010. Understanding mechanisms underlying human gene expression variation with RNA sequencing. Nature 464:768–72 [Google Scholar]
  98. Pollard KS, Hubisz MJ, Rosenbloom KR, Siepel A. 98.  2009. Detection of non-neutral substitution rates on mammalian phylogenies. Genome Res 20:110–21 [Google Scholar]
  99. Pollard KS, Salama SR, King B, Kern AD, Dreszer T. 99.  et al. 2006. Forces shaping the fastest evolving regions in the human genome. PLOS Genet 2:e168 [Google Scholar]
  100. Pollard KS, Salama SR, Lambert N, Lambot M-A, Coppens S. 100.  et al. 2006. An RNA gene expressed during cortical development evolved rapidly in humans. Nature 443:167–72 [Google Scholar]
  101. Popesco MC, MacLaren EJ, Hopkins J, Dumas L, Cox M. 101.  et al. 2006. Human lineage–specific amplification, selection, and neuronal expression of DUF1220 domains. Science 313:1304–7 [Google Scholar]
  102. Prabhakar S, Noonan JP, Pääbo S, Rubin EM. 102.  2006. Accelerated evolution of conserved noncoding sequences in humans. Science 314:786 [Google Scholar]
  103. Prabhakar S, Visel A, Akiyama JA, Shoukry M, Lewis KD. 103.  et al. 2008. Human-specific gain of function in a developmental enhancer. Science 321:1346–50 [Google Scholar]
  104. Prescott SL, Srinivasan R, Marchetto MC, Grishina I, Narvaiza I. 104.  et al. 2015. Enhancer divergence and cis-regulatory evolution in the human and chimp neural crest. Cell 163:1–17 [Google Scholar]
  105. Rakic P. 105.  2009. Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 10:724–35 [Google Scholar]
  106. Reilly SK, Yin J, Ayoub AE, Emera D, Leng J. 106.  et al. 2015. Evolutionary changes in promoter and enhancer activity during human corticogenesis. Science 347:1155–59 [Google Scholar]
  107. 107. Rhesus Macaque Genome Seq. Anal. Consort 2007. Evolutionary and biomedical insights from the rhesus macaque genome. Science 316:222–34 [Google Scholar]
  108. Roberts A, Goff L, Pertea G, Kim D, Kelley DR. 108.  et al. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7:562–78 [Google Scholar]
  109. Robinson MD, McCarthy DJ, Smyth GK. 109.  2009. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–40 [Google Scholar]
  110. Robinton DA, Daley GQ. 110.  2012. The promise of induced pluripotent stem cells in research and therapy. Nature 481:295–305 [Google Scholar]
  111. Rockman MV, Hahn MW, Soranzo N, Zimprich F, Goldstein DB, Wray GA. 111.  2005. Ancient and recent positive selection transformed opioid cis-regulation in humans. PLOS Biol 3:e387 [Google Scholar]
  112. Romero IG, Ruvinsky I, Gilad Y. 112.  2012. Comparative studies of gene expression and the evolution of gene regulation. Nat. Rev. Genet. 13:505–16 [Google Scholar]
  113. Sagai T, Hosoya M, Mizushina Y, Tamura M, Shiroishi T. 113.  2005. Elimination of a long-range cis-regulatory module causes complete loss of limb-specific Shh expression and truncation of the mouse limb. Development 132:797–803 [Google Scholar]
  114. Scally A, Dutheil JY, Hillier LW, Jordan GE, Goodhead I. 114.  et al. 2012. Insights into hominid evolution from the gorilla genome sequence. Nature 483:169–75 [Google Scholar]
  115. Schmidt D, Wilson MD, Ballester B, Schwalie PC, Brown GD. 115.  et al. 2010. Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 328:1036–40 [Google Scholar]
  116. Shibata Y, Sheffield NC, Fedrigo O, Babbitt CC, Wortham M. 116.  et al. 2012. Extensive evolutionary changes in regulatory element activity during human origins are associated with altered gene expression and positive selection. PLOS Genet 8:e1002789 [Google Scholar]
  117. Siepel A. 117.  2005. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15:1034–50 [Google Scholar]
  118. Somel M, Franz H, Yan Z, Lorenc A, Guo S. 118.  et al. 2009. Transcriptional neoteny in the human brain. PNAS 106:5743–48 [Google Scholar]
  119. Somel M, Liu X, Khaitovich P. 119.  2013. Human brain evolution: transcripts, metabolites and their regulators. Nat. Rev. Neurosci. 14:112–27 [Google Scholar]
  120. Stergachis AB, Neph S, Sandstrom R, Haugen E, Reynolds AP. 120.  et al. 2014. Conservation of trans-acting circuitry during mammalian regulatory evolution. Nature 515:365–70 [Google Scholar]
  121. Takahashi K, Yamanaka S. 121.  2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–76 [Google Scholar]
  122. Taylor MS, Kai C, Kawai J, Carninci P, Hayashizaki Y. 122.  et al. 2006. Heterotachy in mammalian promoter evolution. PLOS Genet 2:e30 [Google Scholar]
  123. Taylor MS, Massingham T, Hayashizaki Y, Carninci P, Goldman N. 123.  et al. 2008. Rapidly evolving human promoter regions. Nat. Genet. 40:1262–63 [Google Scholar]
  124. Varjosalo M, Taipale J. 124.  2008. Hedgehog: functions and mechanisms. Genes Dev 22:2454–72 [Google Scholar]
  125. Villar D, Berthelot C, Aldridge S, Rayner TF, Lukk M. 125.  et al. 2015. Enhancer evolution across 20 mammalian species. Cell 160:554–66 [Google Scholar]
  126. Visel A, Blow MJ, Li Z, Zhang T, Akiyama JA. 126.  et al. 2009. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457:854–58 [Google Scholar]
  127. Visel A, Prabhakar S, Akiyama JA, Shoukry M, Lewis KD. 127.  et al. 2008. Ultraconservation identifies a small subset of extremely constrained developmental enhancers. Nat. Genet. 40:158–60 [Google Scholar]
  128. Visel A, Rubin EM, Pennacchio LA. 128.  2009. Genomic views of distant-acting enhancers. Nature 461:199–205 [Google Scholar]
  129. Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW. 129.  et al. 2013. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153:910–18 [Google Scholar]
  130. Wang Z, Gerstein M, Snyder M. 130.  2009. RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10:57–63 [Google Scholar]
  131. Wilson MD, Barbosa-Morais NL, Schmidt D, Conboy CM, Vanes L. 131.  et al. 2008. Species-specific transcription in mice carrying human chromosome 21. Science 322:434–38 [Google Scholar]
  132. Wittkopp PJ, Kalay G. 132.  2011. Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat. Rev. Genet. 13:59–69 [Google Scholar]
  133. Woolfe A, Goodson M, Goode DK, Snell P, Mcewen GK. 133.  et al. 2005. Highly conserved non-coding sequences are associated with vertebrate development. PLOS Biol 3:e7 [Google Scholar]
  134. Wray GA. 134.  2007. The evolutionary significance of cis-regulatory mutations. Nat. Rev. Genet. 8:206–16 [Google Scholar]
  135. Yang H, Wang H, Jaenisch R. 135.  2014. Generating genetically modified mice using CRISPR/Cas-mediated genome engineering. Nat. Protoc. 9:1956–68 [Google Scholar]
  136. Yang H, Wang H, Shivalila CS, Cheng AW, Shi L, Jaenisch R. 136.  2013. One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 154:1370–79 [Google Scholar]
  137. Young RS, Hayashizaki Y, Andersson R, Sandelin A, Kawaji H. 137.  et al. 2015. The frequent evolutionary birth and death of functional promoters in mouse and human. Genome Res 25:1546–57 [Google Scholar]
  138. Zhang X, Sun H, Danila DC, Johnson SR, Zhou Y. 138.  et al. 2002. Loss of expression of GADD45γ, a growth inhibitory gene, in human pituitary adenomas: implications for tumorigenesis. J. Clin. Endocrinol. Metab. 87:1262–67 [Google Scholar]
  139. Zhang YE, Long M. 139.  2014. New genes contribute to genetic and phenotypic novelties in human evolution. Curr. Opin. Genet. Dev. 29:90–96 [Google Scholar]
  140. Zhou VW, Goren A, Bernstein BE. 140.  2011. Charting histone modifications and the functional organization of mammalian genomes. Nat. Rev. Genet. 12:7–18 [Google Scholar]
  141. Zhou X, Cain CE, Myrthil M, Lewellen N, Michelini K. 141.  et al. 2014. Epigenetic modifications are associated with inter-species gene expression variation in primates. Genome Biol 15:547 [Google Scholar]
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