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Abstract

In eusocial insects, genetically identical individuals can exhibit striking differences in behavior and longevity. The molecular basis of such phenotypic plasticity is of great interest to the scientific community. DNA methylation, as well as other epigenetic signals, plays an important role in modulating gene expression and can therefore establish, sustain, and alter organism-level phenotypes, including behavior and life span. Unlike DNA methylation in mammals, DNA methylation in insects, including eusocial insects, is enriched in gene bodies of actively expressed genes. Recent investigations have revealed the important role of gene body methylation in regulating gene expression in response to intrinsic and environmental factors. In this review, we summarize recent advances in DNA methylation research and discuss its significance in our understanding of the epigenetic underpinnings of behavior and longevity.

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2015-01-07
2024-06-24
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Literature Cited

  1. Alberini CM. 1.  2009. Transcription factors in long-term memory and synaptic plasticity. Physiol. Rev. 89:121–45 [Google Scholar]
  2. Allis CD, Jenuwein T, Reinberg D. 2.  2007. Epigenetics Cold Spring Harbor, NY: Cold Spring Harb. Lab. Press [Google Scholar]
  3. Amarasinghe HE, Clayton CI, Mallon EB. 3.  2014. Methylation and worker reproduction in the bumble-bee (Bombus terrestris). Proc. Biol. Sci. 281:20132502 [Google Scholar]
  4. Amdam GV, Page RP. 4.  2005. Intergenerational transfers may have decoupled physiological and chronological age in a eusocial insect. Ageing Res. Rev. 4:398–408 [Google Scholar]
  5. Ament SA, Corona M, Pollock HS, Robinson GE. 5.  2008. Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proc. Natl. Acad. Sci. USA 105:4226–31 [Google Scholar]
  6. Amir RE, van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY. 6.  1999. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 23:185–88 [Google Scholar]
  7. Baker-Andresen D, Ratnu VS, Bredy TW. 7.  2013. Dynamic DNA methylation: a prime candidate for genomic metaplasticity and behavioral adaptation. Trends Neurosci. 36:3–13 [Google Scholar]
  8. Ball MP, Li JB, Gao Y, Lee JH, LeProust EM. 8.  et al. 2009. Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells. Nat. Biotechnol. 27:361–68 [Google Scholar]
  9. Biergans SD, Jones JC, Treiber N, Galizia CG, Szyszka P. 9.  2012. DNA methylation mediates the discriminatory power of associative long-term memory in honeybees. PLOS ONE 7:e39349 [Google Scholar]
  10. Bird A. 10.  2002. DNA methylation patterns and epigenetic memory. Genes Dev. 16:6–21 [Google Scholar]
  11. Bird AP. 11.  1980. DNA methylation and the frequency of CpG in animal DNA. Nucleic Acids Res. 8:1499–504 [Google Scholar]
  12. Bird AP, Wolffe AP. 12.  1999. Methylation-induced repression—belts, braces, and chromatin. Cell 99:451–54 [Google Scholar]
  13. Black DL, Grabowski PJ. 13.  2003. Alternative pre-mRNA splicing and neuronal function. Prog. Mol. Subcell. Biol. 31:187–216 [Google Scholar]
  14. Bluher M. 14.  2008. Fat tissue and long life. Obes. Facts 1:176–82 [Google Scholar]
  15. Bonasio R. 15.  2012. Emerging topics in epigenetics: ants, brains, and noncoding RNAs. Ann. N. Y. Acad. Sci. 1260:14–23 [Google Scholar]
  16. Bonasio R. 16.  2014. The role of chromatin and epigenetics in the polyphenisms of ant castes. Brief Funct. Genomics 13:235–45 [Google Scholar]
  17. Bonasio R, Li Q, Lian J, Mutti NS, Jin L. 17.  et al. 2012. Genome-wide and caste-specific DNA methylomes of the ants Camponotus floridanus and Harpegnathos saltator. Curr. Biol. 22:1755–64 [Google Scholar]
  18. Bonasio R, Tu S, Reinberg D. 18.  2010. Molecular signals of epigenetic states. Science 330:612–16 [Google Scholar]
  19. Bonasio R, Zhang G, Ye C, Mutti NS, Fang X. 19.  et al. 2010. Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329:1068–71 [Google Scholar]
  20. Buffenstein R, Pinto M. 20.  2009. Endocrine function in naturally long-living small mammals. Mol. Cell Endocrinol. 299:101–11 [Google Scholar]
  21. Campos EI, Reinberg D. 21.  2009. Histones: annotating chromatin. Annu. Rev. Genet. 43:559–99 [Google Scholar]
  22. Cedar H, Bergman Y. 22.  2009. Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 10:295–304 [Google Scholar]
  23. Chalkiadaki A, Guarente L. 23.  2012. Sirtuins mediate mammalian metabolic responses to nutrient availability. Nat. Rev. Endocrinol. 8:287–96 [Google Scholar]
  24. Cingolani P, Cao X, Khetani RS, Chen CC, Coon M. 24.  et al. 2013. Intronic non-CG DNA hydroxy-methylation and alternative mRNA splicing in honey bees. BMC Genomics 14:666 [Google Scholar]
  25. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B. 25.  et al. 2008. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:215–19 [Google Scholar]
  26. Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y. 26.  et al. 2007. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc. Natl. Acad. Sci. USA 104:7128–33 [Google Scholar]
  27. Cortese R, Lewin J, Backdahl L, Krispin M, Wasserkort R. 27.  et al. 2011. Genome-wide screen for differential DNA methylation associated with neural cell differentiation in mouse. PLOS ONE 6:e26002 [Google Scholar]
  28. Cui H. 28.  2007. Loss of imprinting of IGF2 as an epigenetic marker for the risk of human cancer. Dis. Markers 23:105–12 [Google Scholar]
  29. Day JJ, Childs D, Guzman-Karlsson MC, Kibe M, Moulden J. 29.  et al. 2013. DNA methylation regulates associative reward learning. Nat. Neurosci. 16:1445–52 [Google Scholar]
  30. Day JJ, Sweatt JD. 30.  2010. DNA methylation and memory formation. Nat. Neurosci. 13:1319–23 [Google Scholar]
  31. Deaton AM, Bird A. 31.  2011. CpG islands and the regulation of transcription. Genes Dev. 25:1010–22 [Google Scholar]
  32. Di Ruscio A, Ebralidze AK, Benoukraf T, Amabile G, Goff LA. 32.  et al. 2013. DNMT1-interacting RNAs block gene-specific DNA methylation. Nature 503:371–76 [Google Scholar]
  33. Drewell RA, Lo N, Oxley PR, Oldroyd BP. 33.  2012. Kin conflict in insect societies: a new epigenetic perspective. Trends Ecol. Evol. 27:367–73 [Google Scholar]
  34. Elango N, Hunt BG, Goodisman MA, Yi SV. 34.  2009. DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera. Proc. Natl. Acad. Sci. USA 106:11206–11 [Google Scholar]
  35. Falckenhayn C, Boerjan B, Raddatz G, Frohme M, Schoofs L, Lyko F. 35.  2013. Characterization of genome methylation patterns in the desert locust Schistocerca gregaria. J. Exp. Biol. 216:1423–29 [Google Scholar]
  36. Feng J, Chang H, Li E, Fan G. 36.  2005. Dynamic expression of de novo DNA methyltransferases Dnmt3a and Dnmt3b in the central nervous system. J. Neurosci. Res. 79:734–46 [Google Scholar]
  37. Feng J, Zhou Y, Campbell SL, Le T, Li E. 37.  et al. 2010. Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat. Neurosci. 13:423–30 [Google Scholar]
  38. Feng S, Cokus SJ, Zhang X, Chen PY, Bostick M. 38.  et al. 2010. Conservation and divergence of methylation patterning in plants and animals. Proc. Natl. Acad. Sci. USA 107:8689–94 [Google Scholar]
  39. Foret S, Kucharski R, Pellegrini M, Feng S, Jacobsen SE. 39.  et al. 2012. DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees. Proc. Natl. Acad. Sci. USA 109:4968–73 [Google Scholar]
  40. Fowler HG, Roberts RB. 40.  1980. Foraging behavior of the carpenter ant, Camponotus pennsylvanicus, (Hymenoptera: Formicidae) in New Jersey. J. Kans. Entomol. Soc. 53:295–304 [Google Scholar]
  41. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F. 41.  et al. 2005. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl. Acad. Sci. USA 102:10604–9 [Google Scholar]
  42. Gazin C, Wajapeyee N, Gobeil S, Virbasius CM, Green MR. 42.  2007. An elaborate pathway required for Ras-mediated epigenetic silencing. Nature 449:1073–77 [Google Scholar]
  43. Glastad KM, Hunt BG, Yi SV, Goodisman MA. 43.  2011. DNA methylation in insects: on the brink of the epigenomic era. Insect Mol. Biol. 20:553–65 [Google Scholar]
  44. Grabowski PJ, Black DL. 44.  2001. Alternative RNA splicing in the nervous system. Prog. Neurobiol. 65:289–308 [Google Scholar]
  45. Gravina S, Vijg J. 45.  2010. Epigenetic factors in aging and longevity. Pflügers Arch. 459:247–58 [Google Scholar]
  46. Gronenberg W, Liebig J. 46.  1999. Smaller brains and optic lobes in reproductive workers of the ant Harpegnathos. Naturwissenschaften 86:343–45 [Google Scholar]
  47. Guo JU, Ma DK, Mo H, Ball MP, Jang MH. 47.  et al. 2011. Neuronal activity modifies the DNA methylation landscape in the adult brain. Nat. Neurosci. 14:1345–51 [Google Scholar]
  48. Guy J, Cheval H, Selfridge J, Bird A. 48.  2011. The role of MeCP2 in the brain. Annu. Rev. Cell Dev. Biol. 27:631–52 [Google Scholar]
  49. Guzman-Novoa E, Hunt GJ, Page RE Jr, Uribe-Rubio JL, Prieto-Merlos D, Becerra-Guzman F. 49.  2005. Paternal effects on the defensive behavior of honeybees. J. Hered. 96:376–80 [Google Scholar]
  50. Hackett JA, Reddington JP, Nestor CE, Dunican DS, Branco MR. 50.  et al. 2012. Promoter DNA methylation couples genome-defence mechanisms to epigenetic reprogramming in the mouse germline. Development 139:3623–32 [Google Scholar]
  51. Haig D. 51.  2000. The kinship theory of genomic imprinting. Annu. Rev. Ecol. Syst. 31:9–32 [Google Scholar]
  52. Hamilton WD. 52.  1964. The genetical evolution of social behaviour. I. J. Theor. Biol. 7:1–16 [Google Scholar]
  53. Hamilton WD. 53.  1964. The genetical evolution of social behaviour. II. J. Theor. Biol. 7:17–52 [Google Scholar]
  54. Harris RA, Wang T, Coarfa C, Nagarajan RP, Hong C. 54.  et al. 2010. Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications. Nat. Biotechnol. 28:1097–105 [Google Scholar]
  55. Hartmann A, Heinze J. 55.  2003. Lay eggs, live longer: division of labor and life span in a clonal ant species. Evolution 57:2424–29 [Google Scholar]
  56. Herb BR, Wolschin F, Hansen KD, Aryee MJ, Langmead B. 56.  et al. 2012. Reversible switching between epigenetic states in honeybee behavioral subcastes. Nat. Neurosci. 15:1371–73 [Google Scholar]
  57. Hölldobler B, Wilson EO. 57.  1990. The Ants Cambridge, MA: Belknap Press of Harvard Univ. Press [Google Scholar]
  58. Hölldobler B, Wilson EO. 58.  2009. The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies New York: W.W. Norton [Google Scholar]
  59. Hoover SE, Keeling CI, Winston ML, Slessor KN. 59.  2003. The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 90:477–80 [Google Scholar]
  60. Humann FC, Tiberio GJ, Hartfelder K. 60.  2013. Sequence and expression characteristics of long noncoding RNAs in honey bee caste development—potential novel regulators for transgressive ovary size. PLOS ONE 8:e78915 [Google Scholar]
  61. Hunt BG, Glastad KM, Yi SV, Goodisman MA. 61.  2013. Patterning and regulatory associations of DNA methylation are mirrored by histone modifications in insects. Genome Biol. Evol. 5:591–98 [Google Scholar]
  62. Hunt GJ. 62.  2007. Flight and fight: a comparative view of the neurophysiology and genetics of honey bee defensive behavior. J. Insect Physiol. 53:399–410 [Google Scholar]
  63. Inano K, Suetake I, Ueda T, Miyake Y, Nakamura M. 63.  et al. 2000. Maintenance-type DNA methyltransferase is highly expressed in post-mitotic neurons and localized in the cytoplasmic compartment. J. Biochem. 128:315–21 [Google Scholar]
  64. Jaenisch R, Bird A. 64.  2003. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33:Suppl.245–54 [Google Scholar]
  65. Jeltsch A. 65.  2010. Phylogeny of methylomes. Science 328:837–38 [Google Scholar]
  66. Jemielity S, Chapuisat M, Parker JD, Keller L. 66.  2005. Long live the queen: studying aging in social insects. Age 27:241–48 [Google Scholar]
  67. Jindra M, Palli SR, Riddiford LM. 67.  2013. The juvenile hormone signaling pathway in insect development. Annu. Rev. Entomol. 58:181–204 [Google Scholar]
  68. Joung JK, Sander JD. 68.  2013. TALENs: a widely applicable technology for targeted genome editing. Nat. Rev. Mol. Cell Biol. 14:49–55 [Google Scholar]
  69. Kamakura M. 69.  2011. Royalactin induces queen differentiation in honeybees. Nature 473:478–83 [Google Scholar]
  70. Keller L, Jemielity S. 70.  2006. Social insects as a model to study the molecular basis of ageing. Exp. Gerontol. 41:553–56 [Google Scholar]
  71. Kim JB, Greber B, Arauzo-Bravo MJ, Meyer J, Park KI. 71.  et al. 2009. Direct reprogramming of human neural stem cells by OCT4. Nature 461:649–53 [Google Scholar]
  72. Kocher SD, Li C, Yang W, Tan H, Yi SV. 72.  et al. 2013. The draft genome of a socially polymorphic halictid bee, Lasioglossum albipes. Genome Biol. 14:R142 [Google Scholar]
  73. Kohli RM, Zhang Y. 73.  2013. TET enzymes, TDG and the dynamics of DNA demethylation. Nature 502:472–79 [Google Scholar]
  74. Kronauer DJC. 74.  2008. Genomic imprinting and kinship in the social Hymenoptera: What are the predictions?. J. Theor. Biol. 254:737–40 [Google Scholar]
  75. Kronforst MR, Gilley DC, Strassmann JE, Queller DC. 75.  2008. DNA methylation is widespread across social Hymenoptera. Curr. Biol. 18:R287–88 [Google Scholar]
  76. Kucharski R, Maleszka J, Foret S, Maleszka R. 76.  2008. Nutritional control of reproductive status in honeybees via DNA methylation. Science 319:1827–30 [Google Scholar]
  77. LaPlant Q, Vialou V, Covington HE. Dumitriu D, Feng J. 77.  3rd, et al. 2010. Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat. Neurosci. 13:1137–43 [Google Scholar]
  78. Libbrecht R, Corona M, Wende F, Azevedo DO, Serrao JE, Keller L. 78.  2013. Interplay between insulin signaling, juvenile hormone, and vitellogenin regulates maternal effects on polyphenism in ants. Proc. Natl. Acad. Sci. USA 110:11050–55 [Google Scholar]
  79. Libbrecht R, Keller L. 79.  2013. Genetic compatibility affects division of labor in the Argentine ant Linepithema humile. Evolution 67:517–24 [Google Scholar]
  80. Liebig J, Hölldobler B, Peeters C. 80.  1998. Are ant workers capable of colony foundation?. Naturwissenschaften 85:133–35 [Google Scholar]
  81. Liebig J, Peeters C, Oldham NJ, Markstadter C, Hölldobler B. 81.  2000. Are variations in cuticular hydrocarbons of queens and workers a reliable signal of fertility in the ant Harpegnathos saltator?. Proc. Natl. Acad. Sci. USA 97:4124–31 [Google Scholar]
  82. Lister R, Mukamel EA, Nery JR, Urich M, Puddifoot CA. 82.  et al. 2013. Global epigenomic reconfiguration during mammalian brain development. Science 341:1237905 [Google Scholar]
  83. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G. 83.  et al. 2009. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462:315–22 [Google Scholar]
  84. Li-Byarlay H, Li Y, Stroud H, Feng S, Newman TC. 84.  et al. 2013. RNA interference knockdown of DNA methyl-transferase 3 affects gene alternative splicing in the honey bee. Proc. Natl. Acad. Sci. USA 110:12750–55 [Google Scholar]
  85. Lo N, Li B, Ujvari B. 85.  2012. DNA methylation in the termite Coptotermes lacteus. Insectes Sociaux 59:257–61 [Google Scholar]
  86. Lockett GA, Helliwell P, Maleszka R. 86.  2010. Involvement of DNA methylation in memory processing in the honey bee. Neuroreport 21:812–16 [Google Scholar]
  87. Luco RF, Allo M, Schor IE, Kornblihtt AR, Misteli T. 87.  2011. Epigenetics in alternative pre-mRNA splicing. Cell 144:16–26 [Google Scholar]
  88. Lyko F, Foret S, Kucharski R, Wolf S, Falckenhayn C, Maleszka R. 88.  2010. The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLOS Biol. 8:e1000506 [Google Scholar]
  89. Lyko F, Maleszka R. 89.  2011. Insects as innovative models for functional studies of DNA methylation. Trends Genet. 27:127–31 [Google Scholar]
  90. Ma DK, Jang MH, Guo JU, Kitabatake Y, Chang ML. 90.  et al. 2009. Neuronal activity–induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323:1074–77 [Google Scholar]
  91. Marks H, Kalkan T, Menafra R, Denissov S, Jones K. 91.  et al. 2012. The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149:590–604 [Google Scholar]
  92. Matarese F, Carrillo-de Santa Pau E, Stunnenberg HG. 92.  2011. 5-Hydroxymethylcytosine: a new kid on the epigenetic block?. Mol. Syst. Biol. 7:562 [Google Scholar]
  93. Maunakea AK, Chepelev I, Cui K, Zhao K. 93.  2013. Intragenic DNA methylation modulates alternative splicing by recruiting MeCP2 to promote exon recognition. Cell Res. 23:1256–69 [Google Scholar]
  94. McKemy DD. 94.  2007. Temperature sensing across species. Pflügers Arch. 454:777–91 [Google Scholar]
  95. Miller CA, Gavin CF, White JA, Parrish RR, Honasoge A. 95.  et al. 2010. Cortical DNA methylation maintains remote memory. Nat. Neurosci. 13:664–66 [Google Scholar]
  96. Miller CA, Sweatt JD. 96.  2007. Covalent modification of DNA regulates memory formation. Neuron 53:857–69 [Google Scholar]
  97. Mohn F, Weber M, Rebhan M, Roloff TC, Richter J. 97.  et al. 2008. Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol. Cell 30:755–66 [Google Scholar]
  98. Nelson CM, Ihle KE, Fondrk MK, Page RE, Amdam GV. 98.  2007. The gene vitellogenin has multiple coordinating effects on social organization. PLOS Biol. 5:e62 [Google Scholar]
  99. Nijhout HF, Wheeler DE. 99.  1982. Juvenile hormone and the physiological basis of insect polymorphisms. Q. Rev. Biol. 57:109–33 [Google Scholar]
  100. Nottebohm F. 100.  2004. The road we travelled: discovery, choreography, and significance of brain replaceable neurons. Ann. N. Y. Acad. Sci. 1016:628–58 [Google Scholar]
  101. Oakes CC, Smiraglia DJ, Plass C, Trasler JM, Robaire B. 101.  2003. Aging results in hypermethylation of ribosomal DNA in sperm and liver of male rats. Proc. Natl. Acad. Sci. USA 100:1775–80 [Google Scholar]
  102. Oberdoerffer S. 102.  2012. A conserved role for intragenic DNA methylation in alternative pre-mRNA splicing. Transcription 3:106–9 [Google Scholar]
  103. Page RE Jr, Amdam GV. 103.  2007. The making of a social insect: developmental architectures of social design. Bioessays 29:334–43 [Google Scholar]
  104. Page RE Jr, Scheiner R, Erber J, Amdam GV. 104.  2006. The development and evolution of division of labor and foraging specialization in a social insect (Apis mellifera L.). Curr. Top. Dev. Biol. 74:253–86 [Google Scholar]
  105. Penick CA, Prager SS, Liebig J. 105.  2012. Juvenile hormone induces queen development in late-stage larvae of the ant Harpegnathos saltator. J. Insect Physiol. 58:1643–49 [Google Scholar]
  106. Pennisi E. 106.  2013. The CRISPR craze. Science 341:833–36 [Google Scholar]
  107. Perales R, Bentley D. 107.  2009. “Cotranscriptionality”: the transcription elongation complex as a nexus for nuclear transactions. Mol. Cell 36:178–91 [Google Scholar]
  108. Piccolo FM, Fisher AG. 108.  2014. Getting rid of DNA methylation. Trends Cell Biol. 24:136–43 [Google Scholar]
  109. Popkie AP, Zeidner LC, Albrecht AM, D'Ippolito A, Eckardt S. 109.  et al. 2010. Phosphatidylinositol 3-kinase (PI3K) signaling via glycogen synthase kinase-3 (Gsk-3) regulates DNA methylation of imprinted loci. J. Biol. Chem. 285:41337–47 [Google Scholar]
  110. Queller DC. 110.  2003. Theory of genomic imprinting conflict in social insects. BMC Evol. Biol. 3:15 [Google Scholar]
  111. Raddatz G, Guzzardo PM, Olova N, Fantappie MR, Rampp M. 111.  et al. 2013. Dnmt2-dependent methylomes lack defined DNA methylation patterns. Proc. Natl. Acad. Sci. USA 110:8627–31 [Google Scholar]
  112. Regev A, Lamb MJ, Jablonka E. 112.  1998. The role of DNA methylation in invertebrates: developmental regulation or genome defense?. Mol. Biol. Evol. 15:880–91 [Google Scholar]
  113. Robinson GE. 113.  1987. Regulation of honey bee age polyethism by juvenile hormone. Behav. Ecol. Sociobiol. 20:329–38 [Google Scholar]
  114. Ruzov A, Tsenkina Y, Serio A, Dudnakova T, Fletcher J. 114.  et al. 2011. Lineage-specific distribution of high levels of genomic 5-hydroxymethylcytosine in mammalian development. Cell Res. 21:1332–42 [Google Scholar]
  115. Sarda S, Zeng J, Hunt BG, Yi SV. 115.  2012. The evolution of invertebrate gene body methylation. Mol. Biol. Evol. 29:1907–16 [Google Scholar]
  116. Schmitz KM, Mayer C, Postepska A, Grummt I. 116.  2010. Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev. 24:2264–69 [Google Scholar]
  117. Schulte C, Theilenberg E, Muller-Borg M, Gempe T, Beye M. 117.  2014. Highly efficient integration and expression of piggyBac-derived cassettes in the honeybee (Apis mellifera). Proc. Natl. Acad. Sci. USA 111:9003–8 [Google Scholar]
  118. Seehuus SC, Norberg K, Gimsa U, Krekling T, Amdam GV. 118.  2006. Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proc. Natl. Acad. Sci. USA 103:962–67 [Google Scholar]
  119. Shukla S, Kavak E, Gregory M, Imashimizu M, Shutinoski B. 119.  et al. 2011. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 479:74–79 [Google Scholar]
  120. Siebold AP, Banerjee R, Tie F, Kiss DL, Moskowitz J, Harte PJ. 120.  2010. Polycomb Repressive Complex 2 and Trithorax modulate Drosophila longevity and stress resistance. Proc. Natl. Acad. Sci. USA 107:169–74 [Google Scholar]
  121. Simola DF, Wissler L, Donahue G, Waterhouse RM, Helmkampf M. 121.  et al. 2013. Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality. Genome Res. 23:1235–47 [Google Scholar]
  122. Simola DF, Ye C, Mutti NS, Dolezal K, Bonasio R. 122.  et al. 2013. A chromatin link to caste identity in the carpenter ant Camponotus floridanus. Genome Res. 23:486–96 [Google Scholar]
  123. Smith CR, Mutti NS, Jasper WC, Naidu A, Smith CD, Gadau J. 123.  2012. Patterns of DNA methylation in development, division of labor and hybridization in an ant with genetic caste determination. PLOS ONE 7e42433 [Google Scholar]
  124. Spannhoff A, Kim YK, Raynal NJ, Gharibyan V, Su MB. 124.  et al. 2011. Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. EMBO Rep. 12:238–43 [Google Scholar]
  125. Suzuki MM, Bird A. 125.  2008. DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet. 9:465–76 [Google Scholar]
  126. Szulwach KE, Li X, Li Y, Song CX, Wu H. 126.  et al. 2011. 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat. Neurosci. 14:1607–16 [Google Scholar]
  127. Tatar M, Bartke A, Antebi A. 127.  2003. The endocrine regulation of aging by insulin-like signals. Science 299:1346–51 [Google Scholar]
  128. Terrapon NLC, Robertson HM, Ji L, Meng X. 128.  et al. 2014. Molecular traces of alternative social organization in a termite genome. Nat. Commun. 5:3636 [Google Scholar]
  129. Tsuji K, Nakata K, Heinze J. 129.  1996. Lifespan and reproduction in a queenless ant. Naturwissenschaften 83:577–78 [Google Scholar]
  130. van Oystaeyen A, Oliveira RC, Holman L, van Zweden JS, Romero C. 130.  et al. 2014. Conserved class of queen pheromones stops social insect workers from reproducing. Science 343:287–90 [Google Scholar]
  131. Wang H, Maurano MT, Qu H, Varley KE, Gertz J. 131.  et al. 2012. Widespread plasticity in CTCF occupancy linked to DNA methylation. Genome Res. 22:1680–88 [Google Scholar]
  132. Wang X, Wheeler D, Avery A, Rago A, Choi JH. 132.  et al. 2013. Function and evolution of DNA methylation in Nasonia vitripennis. PLOS Genet. 9:e1003872 [Google Scholar]
  133. Weiner SA, Galbraith DA, Adams DC, Valenzuela N, Noll FB. 133.  et al. 2013. A survey of DNA methylation across social insect species, life stages, and castes reveals abundant and caste-associated methylation in a primitively social wasp. Naturwissenschaften 100:795–99 [Google Scholar]
  134. Weiner SA, Toth AL. 134.  2012. Epigenetics in social insects: a new direction for understanding the evolution of castes. Genet. Res. Int. 2012:609810 [Google Scholar]
  135. Wheeler DE, Nijhout HF. 135.  1981. Soldier determination in ants: new role for juvenile hormone. Science 213:361–63 [Google Scholar]
  136. Whitman D, Ananthakrishnan TN. 136.  2009. Phenotypic Plasticity of Insects: Mechanisms and Consequences Enfield, NH: Science Publ. [Google Scholar]
  137. Wojciechowski M, Rafalski D, Kucharski R, Misztal K, Maleszka J. 137.  et al. 2014. Insights into DNA hydroxymethylation in the honeybee from in-depth analyses of TET dioxygenase. Open Biol 4:140110 [Google Scholar]
  138. Wu H, Coskun V, Tao J, Xie W, Ge W. 138.  et al. 2010. Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 329:444–48 [Google Scholar]
  139. Xiang H, Zhu J, Chen Q, Dai F, Li X. 139.  et al. 2010. Single base–resolution methylome of the silkworm reveals a sparse epigenomic map. Nat. Biotechnol. 28:516–20 [Google Scholar]
  140. Yan H, Simola DF, Bonasio R, Liebig J, Berger SL, Reinberg D. 140.  2014. Eusocial insects as emerging models for behavioural epigenetics. Nat. Rev. Genet. 15:677–88 [Google Scholar]
  141. Young JI, Hong EP, Castle JC, Crespo-Barreto J, Bowman AB. 141.  et al. 2005. Regulation of RNA splicing by the methylation-dependent transcriptional repressor methyl-CpG binding protein 2. Proc. Natl. Acad. Sci. USA 102:17551–58 [Google Scholar]
  142. Zemach A, McDaniel IE, Silva P, Zilberman D. 142.  2010. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328:916–19 [Google Scholar]
  143. Zemach A, Zilberman D. 143.  2010. Evolution of eukaryotic DNA methylation and the pursuit of safer sex. Curr. Biol. 20:R780–85 [Google Scholar]
  144. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW. 144.  et al. 2006. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189–201 [Google Scholar]
  145. Zhou X, Slone JD, Rokas A, Berger SL, Liebig J. 145.  et al. 2012. Phylogenetic and transcriptomic analysis of chemosensory receptors in a pair of divergent ant species reveals sex-specific signatures of odor coding. PLoS Genet. 8e1002930 [Google Scholar]
  146. Zilberman D. 146.  2008. The evolving functions of DNA methylation. Curr. Opin. Plant Biol. 11:554–59 [Google Scholar]
  147. Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S. 147.  2007. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat. Genet. 39:61–69 [Google Scholar]
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