DNA methylation in social insects: how epigenetics can control behavior and longevity
Open accessAbstract
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.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Ant and bee castes have caste-specific DNA methylation and H3K27ac patterns functionally important for behavior.
“Comparisons between individuals from different castes have revealed that they have caste-specific DNA methylation and H3K27ac patterns that are functionally important for their behavior (Simola et al., 2016; Yan et al., 2015).”
From The Aging Epigenome (2016) · cites this paper as Yan et al., 2015
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The genetical evolution of social behaviour. I
Hamilton, W. D. (1964) · Journal of Theoretical Biology · doi:10.1016/0022-5193(64)90038-4 · Cited by 15,725 · see citing works
DNA methylation patterns and epigenetic memory
Bird, A. (2002) · Genes & Development · doi:10.1101/gad.947102 · Cited by 7,124 · see citing works
Jaenisch, R., & Bird, A. (2003) · Nature Genetics · doi:10.1038/ng1089 · Cited by 6,325 · see citing works
Hölldobler, B., & Wilson, E. O. (1990) · Springer eBooks · doi:10.1007/978-3-662-10306-7 · Cited by 5,531 · see citing works
Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2
Amir, R. E., Van den Veyver, I. B., Wan, M., Tran, C. Q., Francke, U., & Zoghbi, H. Y. (1999) · Nature Genetics · doi:10.1038/13810 · Cited by 4,990 · see citing works
Human DNA methylomes at base resolution show widespread epigenomic differences
Lister, R., Pelizzola, M., Dowen, R. H., Hawkins, R. D., Hon, G., Tonti-Filippini, J., Nery, J. R., Lee, L., Ye, Z., Ngo, Q.-M., et al. (2009) · Nature · doi:10.1038/nature08514 · Cited by 4,673 · see citing works
The genetical evolution of social behaviour. II
Hamilton, W. D. O. (1964) · Journal of Theoretical Biology · doi:10.1016/0022-5193(64)90039-6 · Cited by 4,158 · see citing works
Epigenetic differences arise during the lifetime of monozygotic twins
Fraga, M. F., Ballestar, E., Paz, M. F., Ropero, S., Setien, F., Ballestar, M. L., Heine-Suñer, D., Cigudosa, J. C., Urioste, M., Benitez, J., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500398102 · Cited by 3,602 · see citing works
CpG islands and the regulation of transcription
Deaton, A. M., & Bird, A. (2011) · Genes & Development · doi:10.1101/gad.2037511 · Cited by 3,187 · see citing works
DNA methylation landscapes: Provocative insights from epigenomics
Suzuki, M. M., & Bird, A. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2341 · Cited by 3,039 · see citing works
Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning
Cokus, S. J., Feng, S.-H., Zhang, X.-Y., Chen, Z., Merriman, B., Haudenschild, C., Pradhan, S., Nelson, S., Pellegrini, M., & Jacobsen, S. (2008) · Nature · doi:10.1038/nature06745 · Cited by 2,278 · see citing works
Linking DNA methylation and histone modification: patterns and paradigms
Cedar, H., & Bergman, Y. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2540 · Cited by 2,267 · see citing works
Global epigenomic reconfiguration during mammalian brain development
Lister, R., Mukamel, E. A., Nery, J. R., Urich, M., Puddifoot, C. A., Johnson, N. D., Lucero, J., Huang, Y., Dwork, A. J., Schultz, M. D., et al. (2013) · Science · doi:10.1126/science.1237905 · Cited by 1,830 · see citing works
Methylation-Induced Repression— Belts, Braces, and Chromatin
Bird, A. P., & Wolffe, A. P. (1999) · Cell · doi:10.1016/s0092-8674(00)81532-9 · Cited by 1,827 · see citing works
Genome-wide High-Resolution Mapping and Functional Analysis of DNA Methylation in Arabidopsis
Zhang, X., Yazaki, J., Sundaresan, A., Cokus, S. J., Chan, S. W.-L., Chen, H., Henderson, I. R., Shinn, P., Pellegrini, M. A., Jacobsen, S. E., et al. (2006) · Cell · doi:10.1016/j.cell.2006.08.003 · Cited by 1,818 · see citing works
Genome-Wide Evolutionary Analysis of Eukaryotic DNA Methylation
Zemach, A., McDaniel, I. E., Silva, P., & Zilberman, D. (2010) · Science · doi:10.1126/science.1186366 · Cited by 1,796 · see citing works
TALENs: A widely applicable technology for targeted genome editing
Joung, J. K., & Sander, J. D. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3486 · Cited by 1,650 · see citing works
TET enzymes, TDG and the dynamics of DNA demethylation
Kohli, R. M., & Zhang, Y. (2013) · Nature · doi:10.1038/nature12750 · Cited by 1,623 · see citing works
Zilberman, D., Gehring, M. A., Tran, R. K., Ballinger, T. J., & Henikoff, S. (2006) · Nature Genetics · doi:10.1038/ng1929 · Cited by 1,369 · see citing works
The Endocrine Regulation of Aging by Insulin-like Signals
Tatar, M., Bartke, A., & Antebi, A. (2003) · Science · doi:10.1126/science.1081447 · Cited by 1,327 · see citing works
Conservation and divergence of methylation patterning in plants and animals
Feng, S., Cokus, S. J., Zhang, X., Chen, P.-Y., Bostick, M., Goll, M. G., Hetzel, J., Jain, J., Strauss, S. H., Halpern, M. E., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002720107 · Cited by 1,285 · see citing works
The Superorganism: the beauty, elegance, and strangeness of insect societies
(2009) · Choice Reviews Online · doi:10.5860/choice.46-6805 · Cited by 1,205 · see citing works
Covalent Modification of DNA Regulates Memory Formation
Miller, C. A., & Sweatt, J. D. (2007) · Neuron · doi:10.1016/j.neuron.2007.02.022 · Cited by 1,180 · see citing works
DNA methylation and the frequency of CpG in animal DNA
Bird, A. P. (1980) · Nucleic Acids Research · doi:10.1093/nar/8.7.1499 · Cited by 1,175 · see citing works
Nutritional Control of Reproductive Status in Honeybees via DNA Methylation
Kucharski, R., Maleszka, J., Forêt, S., & Maleszka, R. (2008) · Science · doi:10.1126/science.1153069 · Cited by 1,146 · see citing works
Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells
Ball, M. P., Li, J. B., Gao, Y., Lee, J., LeProust, E. M., Park, I., Xie, B., Daley, G. Q., & Church, G. M. (2009) · Nature Biotechnology · doi:10.1038/nbt.1533 · Cited by 1,087 · see citing works
Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons
Feng, J., Zhou, Y., Campbell, S. L., Le, T., Li, E., Sweatt, J. D., Silva, A. J., & Fan, G. (2010) · Nature Neuroscience · doi:10.1038/nn.2514 · Cited by 1,019 · see citing works
Transcription Factors in Long-Term Memory and Synaptic Plasticity
Alberini, C. M. (2009) · Physiological Reviews · doi:10.1152/physrev.00017.2008 · Cited by 991 · see citing works
CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing
Shukla, S., Kavak, E., Gregory, M., Imashimizu, M., Shutinoski, B., Kashlev, M., Oberdoerffer, P., Sandberg, R., & Oberdoerffer, S. (2011) · Nature · doi:10.1038/nature10442 · Cited by 973 · see citing works
Neuronal Activity–Induced Gadd45b Promotes Epigenetic DNA Demethylation and Adult Neurogenesis
Dengke, K., Jang, M., Guo, J. U., Kitabatake, Y., Chang, M.-L., Pow-anpongkul, N., Flavell, R. A., Lu, B., Ming, G., & Song, H. (2009) · Science · doi:10.1126/science.1166859 · Cited by 929 · see citing works
Mohn, F., Weber, M., Rebhan, M., Roloff, T. C., Richter, J., Stadler, M. B., Bibel, M., & Schübeler, D. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.05.007 · Cited by 912 · see citing works
Molecular Signals of Epigenetic States
Bonasio, R., Tu, S., & Reinberg, D. (2010) · Science · doi:10.1126/science.1191078 · Cited by 912 · see citing works
Self-citationThe Transcriptional and Epigenomic Foundations of Ground State Pluripotency
Marks, H., Kalkan, T., Menafra, R., Denissov, S., Jones, K. A., Hofemeister, H., Nichols, J., Kranz, A., Stewart, A., Smith, A. G., et al. (2012) · Cell · doi:10.1016/j.cell.2012.03.026 · Cited by 881 · see citing works
The Juvenile Hormone Signaling Pathway in Insect Development
Jindra, M., Palli, S. R., & Riddiford, L. M. (2013) · Annual Review of Entomology · doi:10.1146/annurev-ento-120811-153700 · Cited by 874 · see citing works
Histones: annotating chromatin
Campos, E. I., & Reinberg, D. (2009) · Annual Review of Genetics · doi:10.1146/annurev.genet.032608.103928 · Cited by 852 · see citing works
Self-citation5-hmC–mediated epigenetic dynamics during postnatal neurodevelopment and aging
Szulwach, K. E., Li, X., Li, Y., Song, C., Wu, H., Dai, Q., Irier, H. A., Upadhyay, A. K., Gearing, M., Levey, A. I., et al. (2011) · Nature Neuroscience · doi:10.1038/nn.2959 · Cited by 818 · see citing works
Epigenetics in Alternative Pre-mRNA Splicing
Luco, R. F., Alló, M., Schor, I. E., Kornblihtt, A. R., & Misteli, T. (2011) · Cell · doi:10.1016/j.cell.2010.11.056 · Cited by 783 · see citing works
The Honey Bee Epigenomes: Differential Methylation of Brain DNA in Queens and Workers
Lyko, F., Foret, S., Kucharski, R., Wolf, S., Falckenhayn, C., & Maleszka, R. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000506 · Cited by 727 · see citing works
Harris, R. A., Wang, T., Coarfa, C., Nagarajan, R. P., Hong, C., Downey, S. L., Johnson, B., Fouse, S. D., Delaney, A. D., Zhao, Y., et al. (2010) · Nature Biotechnology · doi:10.1038/nbt.1682 · Cited by 713 · see citing works
Direct reprogramming of human neural stem cells by OCT4
Kim, J. B., Greber, B., Araúzo-Bravo, M. J., Meyer, J., Park, K. I., Zaehres, H., & Schöler, H. R. (2009) · Nature · doi:10.1038/nature08436 · Cited by 692 · see citing works
Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity
Corona, M., Velarde, R. A., Remolina, S. C., Moran-Lauter, A., Wang, Y., Hughes, K. A., & Robinson, G. E. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701909104 · Cited by 673 · see citing works
Neuronal activity modifies the DNA methylation landscape in the adult brain
Guo, J. U., Ma, D. K., Mo, H., Ball, M. P., Jang, M.-H., Bonaguidi, M. A., Balazer, J. A., Eaves, H. L., Xie, B., Ford, E., et al. (2011) · Nature Neuroscience · doi:10.1038/nn.2900 · Cited by 669 · see citing works
Royalactin induces queen differentiation in honeybees
Kamakura, M. (2011) · Nature · doi:10.1038/nature10093 · Cited by 659 · see citing works
Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens
LaPlant, Q., Vialou, V., Covington, H. E., Dumitriu, D., Feng, J., Warren, B. L., Maze, I., Dietz, D. M., Watts, E. L., Iñiguez, S. D., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2619 · Cited by 612 · see citing works
Dnmt3a-Dependent Nonpromoter DNA Methylation Facilitates Transcription of Neurogenic Genes
Wu, H., Coskun, V., Tao, J., Xie, W., Ge, W., Yoshikawa, K., Li, E., Zhang, Y., & Sun, Y. E. (2010) · Science · doi:10.1126/science.1190485 · Cited by 604 · see citing works
Widespread plasticity in CTCF occupancy linked to DNA methylation
Wang, H., Maurano, M. T., Qu, H., Varley, K. E., Gertz, J., Pauli, F., Lee, K., Canfield, T., Weaver, M., Sandstrom, R., et al. (2012) · Genome Research · doi:10.1101/gr.136101.111 · Cited by 588 · see citing works
Reproductive protein protects functionally sterile honey bee workers from oxidative stress
Seehuus, S., Norberg, K., Gimsa, U., Krekling, T., & Amdam, G. V. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502681103 · Cited by 586 · see citing works
Maunakea, A. K., Chepelev, I., Cui, K., & Zhao, K. (2013) · Cell Research · doi:10.1038/cr.2013.110 · Cited by 552 · see citing works
The Gene vitellogenin Has Multiple Coordinating Effects on Social Organization
Nelson, C. M., Ihle, K. E., Fondrk, M. K., Page, R. E., & Amdam, G. V. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050062 · Cited by 525 · see citing works
Cortical DNA methylation maintains remote memory
Miller, C. A., Gavin, C. F., White, J. A., Parrish, R. R., Honasoge, A., Yancey, C. R., Rivera, I. M., Rubio, M. D., Rumbaugh, G., & Sweatt, J. D. (2010) · Nature Neuroscience · doi:10.1038/nn.2560 · Cited by 521 · see citing works
DNMT1-interacting RNAs block gene-specific DNA methylation
Ruscio, A. D., Ebralidze, A. K., Benoukraf, T., Amabile, G., Goff, L. A., Terragni, J., Figueroa, M. E., de Figueiredo‐Pontes, L. L., Alberich-Jordà, M., Zhang, P., et al. (2013) · Nature · doi:10.1038/nature12598 · Cited by 508 · see citing works
Schmitz, K., Mayer, C., Postepska, A., & Grummt, I. (2010) · Genes & Development · doi:10.1101/gad.590910 · Cited by 505 · see citing works
DNA methylation and memory formation
Day, J. J., & Sweatt, J. D. (2010) · Nature Neuroscience · doi:10.1038/nn.2666 · Cited by 488 · see citing works
Young, J. I., Hong, E. P., Castle, J. C., Crespo-Barreto, J., Bowman, A. B., Rose, M. F., Kang, D., Richman, R., Johnson, J. M., Berget, S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507856102 · Cited by 484 · see citing works
Genomic Comparison of the Ants Camponotus floridanus and Harpegnathos saltator
Bonasio, R., Zhang, G., Ye, C., Mutti, N. S., Fang, X., Qin, N., Donahue, G., Yang, P., Li, Q., Li, C., et al. (2010) · Science · doi:10.1126/science.1192428 · Cited by 453 · see citing works
Self-citationThe Role of MeCP2 in the Brain
Guy, J., Cheval, H., Selfridge, J., & Bird, A. P. (2011) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-092910-154121 · Cited by 414 · see citing works
Juvenile Hormone and the Physiological Basis of Insect Polymorphisms
Nijhout, H. F., & Wheeler, D. E. (1982) · The Quarterly Review of Biology · doi:10.1086/412671 · Cited by 409 · see citing works
Dynamic expression of de novo DNA methyltransferases Dnmt3a and Dnmt3b in the central nervous system
Feng, J., Chang, H., Li, E., & Fan, G. (2005) · Journal of Neuroscience Research · doi:10.1002/jnr.20404 · Cited by 401 · see citing works
Bonasio, R., Li, Q., Lian, J., Mutti, N. S., Jin, L., Zhao, H., Zhang, P., Wen, P., Xiang, H., Ding, Y., et al. (2012) · Current Biology · doi:10.1016/j.cub.2012.07.042 · Cited by 398 · see citing works
Self-citationMolecular traces of alternative social organization in a termite genome
Terrapon, N., Li, C., Robertson, H. M., Ji, L., Meng, X., Booth, W., Chen, Z., Childers, C. P., Glastad, K. M., Gokhale, K., et al. (2014) · Nature Communications · doi:10.1038/ncomms4636 · Cited by 395 · see citing works
Self-citationRegulation of honey bee age polyethism by juvenile hormone
Robinson, G. E. (1987) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00300679 · Cited by 381 · see citing works
Phenotypic Plasticity of Insects
(2009) · Science Publishers eBooks · doi:10.1201/b10201 · Cited by 373 · see citing works
Single base–resolution methylome of the silkworm reveals a sparse epigenomic map
Xiang, H., Zhu, J., Chen, Q., Dai, F., Li, X., Li, M., Zhang, H., Zhang, G., Li, D., Dong, Y., et al. (2010) · Nature Biotechnology · doi:10.1038/nbt.1626 · Cited by 369 · see citing works
“Cotranscriptionality”: The Transcription Elongation Complex as a Nexus for Nuclear Transactions
Perales, R., & Bentley, D. L. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.09.018 · Cited by 355 · see citing works
The effect of queen pheromones on worker honey bee ovary development
Hoover, S. E., Keeling, C. I., Winston, M. L., & Slessor, K. N. (2003) · Die Naturwissenschaften · doi:10.1007/s00114-003-0462-z · Cited by 354 · see citing works
Conserved Class of Queen Pheromones Stops Social Insect Workers from Reproducing
Oystaeyen, A. V., Oliveira, R. C., Holman, L., et al. (2014) · Science · doi:10.1126/science.1244899 · Cited by 350 · see citing works
Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies
Ament, S. A., Corona, M., Pollock, H. S., & Robinson, G. E. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0800630105 · Cited by 349 · see citing works
DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees
Forêt, S., Kucharski, R., Pellegrini, M. A., Feng, S., Jacobsen, S. E., Robinson, G. E., & Maleszka, R. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1202392109 · Cited by 346 · see citing works
Sirtuins mediate mammalian metabolic responses to nutrient availability
Chalkiadaki, A., & Guarente, L. (2012) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2011.225 · Cited by 342 · see citing works
Reversible switching between epigenetic states in honeybee behavioral subcastes
Herb, B. R., Wolschin, F., Hansen, K. D., Aryee, M. J., Langmead, B., Irizarry, R. A., Amdam, G. V., & Feinberg, A. P. (2012) · Nature Neuroscience · doi:10.1038/nn.3218 · Cited by 335 · see citing works
Pennisi, E. (2013) · Science · doi:10.1126/science.341.6148.833 · Cited by 334 · see citing works
Alternative RNA splicing in the nervous system
Grabowski, P. J., & Black, D. L. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(01)00007-7 · Cited by 331 · see citing works
Elango, N., Hunt, B. G., Goodisman, M. A. D., & Yi, S. V. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900301106 · Cited by 327 · see citing works
The Kinship Theory of Genomic Imprinting
Haig, D. (2000) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.ecolsys.31.1.9 · Cited by 327 · see citing works
Epigenetic factors in aging and longevity
Gravina, S., & Vijg, J. (2009) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-009-0730-7 · Cited by 326 · see citing works
An elaborate pathway required for Ras-mediated epigenetic silencing
Gazin, C., Wajapeyee, N., Gobeil, S., Virbasius, C.-M. A., & Green, M. R. (2007) · Nature · doi:10.1038/nature06251 · Cited by 282 · see citing works
Liebig, J., Peeters, C., Oldham, N. J., Markstädter, C., & Hölldobler, B. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.8.4124 · Cited by 282 · see citing works
Self-citationDnmt2-dependent methylomes lack defined DNA methylation patterns
Raddatz, G., Guzzardo, P. M., Olova, N. N., Fantappíé, M. R., Rampp, M., Schaefer, M., Reik, W., Hannon, G. J., & Lyko, F. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1306723110 · Cited by 258 · see citing works
The Evolution of Invertebrate Gene Body Methylation
Sarda, S., Zeng, J., Hunt, B. G., & Yi, S. V. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss062 · Cited by 255 · see citing works
DNA methylation in insects: on the brink of the epigenomic era
Glastad, K. M., Hunt, B. G., Yi, S. V., & Goodisman, M. A. D. (2011) · Insect Molecular Biology · doi:10.1111/j.1365-2583.2011.01092.x · Cited by 248 · see citing works
Simola, D. F., Wissler, L., Donahue, G., Waterhouse, R. M., Helmkampf, M., Roux, J., Nygaard, S., Glastad, K. M., Hagen, D. E., Viljakainen, L., et al. (2013) · Genome Research · doi:10.1101/gr.155408.113 · Cited by 247 · see citing works
Self-citationLi‐Byarlay, H., Li, Y., Stroud, H., Feng, S., Newman, T. C., Kaneda, M. M., Hou, K. K., Worley, K. C., Elsik, C. G., Wickline, S. A., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1310735110 · Cited by 245 · see citing works
Zhou, X., Slone, J. D., Rokas, A., Berger, S. L., Liebig, J., Ray, A., Reinberg, D., & Zwiebel, L. J. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002930 · Cited by 241 · see citing works
Self-citationSiebold, A. P., Banerjee, R., Tie, F., Kiss, D. L., Moskowitz, J., & Harte, P. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907739107 · Cited by 216 · see citing works
Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees
Spannhoff, A., Kim, Y. K., Raynal, N. J. ‐., Gharibyan, V., Su, M., Zhou, Y., Li, J. X., Castellano, S., Sbardella, G., Issa, J. J., et al. (2011) · EMBO Reports · doi:10.1038/embor.2011.9 · Cited by 213 · see citing works
DNA methylation regulates associative reward learning
Day, J. J., Childs, D. S., Karlsson, M. G., Kibe, M., Moulden, J., Song, E. Y., Tahir, A., & Sweatt, J. D. (2013) · Nature Neuroscience · doi:10.1038/nn.3504 · Cited by 212 · see citing works
Insects as innovative models for functional studies of DNA methylation
Lyko, F., & Maleszka, R. (2011) · Trends in Genetics · doi:10.1016/j.tig.2011.01.003 · Cited by 208 · see citing works
Lineage-specific distribution of high levels of genomic
Ruzov, A. S., Tsenkina, Y., Serio, A., Dudnakova, T., Fletcher, J. M., Bai, Y., Chebotareva, T., Pells, S., Hannoun, Z., Sullivan, G. J., et al. (2011) · Cell Research · doi:10.1038/cr.2011.113 · Cited by 202 · see citing works
Evolution of Eukaryotic DNA Methylation and the Pursuit of Safer Sex
Zemach, A., & Zilberman, D. (2010) · Current Biology · doi:10.1016/j.cub.2010.07.007 · Cited by 201 · see citing works
Eusocial insects as emerging models for behavioural epigenetics
Yan, H., Simola, D. F., Bonasio, R., Liebig, J., Berger, S. L., & Reinberg, D. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3787 · Cited by 198 · see citing works
Self-citationPage, R. E., Scheiner, R., Erber, J., et al. (2006) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(06)74008-x · Cited by 191 · see citing works
Aging results in hypermethylation of ribosomal DNA in sperm and liver of male rats
Oakes, C. C., Smiraglia, D. J., Plass, C., Trasler, J. M., & Robaire, B. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0437971100 · Cited by 184 · see citing works
The making of a social insect: developmental architectures of social design
Page, R. E., & Amdam, G. V. (2007) · BioEssays · doi:10.1002/bies.20549 · Cited by 175 · see citing works
The Role of DNA Methylation in Invertebrates: Developmental Regulation or Genome Defense?
Regev, A., Lamb, M. J., & Jablonka, E. (1998) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025992 · Cited by 173 · see citing works
Function and Evolution of DNA Methylation in Nasonia vitripennis
Wang, X., Wheeler, D., Avery, A., Rago, A., Choi, J.-H., Colbourne, J. K., Clark, A. G., & Werren, J. H. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003872 · Cited by 172 · see citing works
The Road We Travelled: Discovery, Choreography, and Significance of Brain Replaceable Neurons
Nottebohm, F. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1298.027 · Cited by 170 · see citing works
Libbrecht, R., Corona, M., Wende, F., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1221781110 · Cited by 159 · see citing works
Dynamic DNA methylation: a prime candidate for genomic metaplasticity and behavioral adaptation
Baker‐Andresen, D., Ratnu, V. S., & Bredy, T. W. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.09.003 · Cited by 151 · see citing works
Hackett, J. A., Reddington, J. P., Nestor, C. E., Dunican, D. S., Branco, M. R., Reichmann, J., Reik, W., Surani, M. A., Adams, I. R., & Meehan, R. R. (2012) · Development · doi:10.1242/dev.081661 · Cited by 149 · see citing works
A chromatin link to caste identity in the carpenter ant Camponotus floridanusPreprint
Simola, D. F., Ye, C., Mutti, N. S., Dolezal, K., Bonasio, R., Liebig, J., Reinberg, D., & Berger, S. L. (2012) · Genome Research · doi:10.1101/gr.148361.112 · Cited by 145 · see citing works
Self-citationHunt, G. J. (2007) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2007.01.010 · Cited by 135 · see citing works
Soldier Determination in Ants: New Role for Juvenile Hormone
Wheeler, D. E., & Nijhout, H. F. (1981) · Science · doi:10.1126/science.213.4505.361 · Cited by 131 · see citing works
Schulte, C. E., Theilenberg, E., Müller-Borg, M., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1402341111 · Cited by 129 · see citing works
Social insects as a model to study the molecular basis of ageing
Keller, L., & Jemielity, S. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2006.04.002 · Cited by 123 · see citing works
Methylation and worker reproduction in the bumble-bee (Bombus terrestris)
Amarasinghe, H. E., Clayton, C. I., & Mallon, E. B. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.2502 · Cited by 118 · see citing works
Alternative Pre-mRNA Splicing and Neuronal Function
Black, D. L., & Grabowski, P. J. (2003) · Progress in molecular and subcellular biology · doi:10.1007/978-3-662-09728-1_7 · Cited by 114 · see citing works
Involvement of DNA methylation in memory processing in the honey bee
Lockett, G. A., Helliwell, P. G., & Maleszka, R. (2010) · Neuroreport · doi:10.1097/wnr.0b013e32833ce5be · Cited by 107 · see citing works
Theory of genomic imprinting conflict in social insects
Queller, D. C. (2003) · BMC Evolutionary Biology · doi:10.1186/1471-2148-3-15 · Cited by 106 · see citing works
Hunt, B. G., Glastad, K. M., Yi, S. V., & Goodisman, M. A. D. (2013) · Genome Biology and Evolution · doi:10.1093/gbe/evt030 · Cited by 103 · see citing works
Inano, K., Suetake, I., Ueda, T., Miyake, Y., Nakamura, M., Okada, M., & Tajima, S. (2000) · The Journal of Biochemistry · doi:10.1093/oxfordjournals.jbchem.a022755 · Cited by 99 · see citing works
Epigenetics in Social Insects: A New Direction for Understanding the Evolution of Castes
Weiner, S. A., & Toth, A. L. (2012) · Genetics Research International · doi:10.1155/2012/609810 · Cited by 97 · see citing works
The evolving functions of DNA methylation
Zilberman, D. (2008) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2008.07.004 · Cited by 94 · see citing works
Popkie, A. P., Zeidner, L. C., Albrecht, A. M., D’Ippolito, A. M., Eckardt, S., Newsom, D. E., Groden, J. L., Doble, B. W., Aronow, B. J., McLaughlin, K. J., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.170704 · Cited by 91 · see citing works
LAY EGGS, LIVE LONGER: DIVISION OF LABOR AND LIFE SPAN IN A CLONAL ANT SPECIES
Hartmann, A., & Heınze, J. (2003) · Evolution · doi:10.1111/j.0014-3820.2003.tb00254.x · Cited by 91 · see citing works
Amdam, G. V., & Page, R. E. (2005) · Ageing Research Reviews · doi:10.1016/j.arr.2005.03.007 · Cited by 90 · see citing works
Long live the queen: studying aging in social insects
Jemielity, S., Chapuisat, M., Parker, J. D., & Keller, L. (2005) · AGE · doi:10.1007/s11357-005-2916-z · Cited by 88 · see citing works
Humann, F. C., Tibério, G. J., & Hartfelder, K. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078915 · Cited by 84 · see citing works
Temperature sensing across species
McKemy, D. D. (2007) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-006-0199-6 · Cited by 84 · see citing works
The draft genome of a socially polymorphic halictid bee, Lasioglossum albipes
Kocher, S. D., Li, C., Yang, W. C., Tan, H., Yi, S. V., Yang, X., Hoekstra, H. E., Zhang, G., Pierce, N. E., & Yu, D. W. (2013) · Genome biology · doi:10.1186/gb-2013-14-12-r142 · Cited by 83 · see citing works
Loss of Imprinting of IGF2 as an Epigenetic Marker for the Risk of Human Cancer
Cui, H. (2007) · Disease Markers · doi:10.1155/2007/363464 · Cited by 82 · see citing works
Characterization of genome methylation patterns in the desert locust Schistocerca gregaria
Falckenhayn, C., Boerjan, B., Raddatz, G., Frohme, M., Schoofs, L., & Lyko, F. (2012) · Journal of Experimental Biology · doi:10.1242/jeb.080754 · Cited by 81 · see citing works
DNA methylation is widespread across social Hymenoptera
Kronforst, M. R., Gilley, D. C., Strassmann, J. E., & Queller, D. C. (2008) · Current Biology · doi:10.1016/j.cub.2008.02.015 · Cited by 80 · see citing works
Jeltsch, A. (2010) · Science · doi:10.1126/science.1190738 · Cited by 75 · see citing works
5‐Hydroxymethylcytosine: a new kid on the epigenetic block?
Matarese, F., Pau, E. C. D. S., & Stunnenberg, H. G. (2011) · Molecular Systems Biology · doi:10.1038/msb.2011.95 · Cited by 74 · see citing works
Getting rid of DNA methylation
Piccolo, F. M., & Fisher, A. G. (2013) · Trends in Cell Biology · doi:10.1016/j.tcb.2013.09.001 · Cited by 74 · see citing works
Intronic Non-CG DNA hydroxymethylation and alternative mRNA splicing in honey bees
Cingolani, P., Cao, X., Khetani, R. S., Chen, C.-C., Coon, M., Sammak, A., Bollig-Fischer, A. B., Land, S. J., Huang, Y., Hudson, M. E., et al. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-666 · Cited by 72 · see citing works
Endocrine function in naturally long-living small mammals
Buffenstein, R., & Pinto, M. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.04.021 · Cited by 71 · see citing works
Smaller Brains and Optic Lobes in Reproductive Workers of the Ant Harpegnathos
Gronenberg, W., & Liebig, J. (1999) · Die Naturwissenschaften · doi:10.1007/s001140050631 · Cited by 68 · see citing works
Self-citationLifespan and reproduction in a queenless ant
Tsuji, K., Nakata, K., & Heınze, J. (1996) · Die Naturwissenschaften · doi:10.1007/bf01141985 · Cited by 67 · see citing works
Insights into DNA hydroxymethylation in the honeybee from in-depth analyses of TET dioxygenase
Wojciechowski, M., Rafalski, D., Kucharski, R., Misztal, K., Maleszka, J., Bochtler, M., & Maleszka, R. (2014) · Open Biology · doi:10.1098/rsob.140110 · Cited by 67 · see citing works
DNA Methylation Mediates the Discriminatory Power of Associative Long-Term Memory in Honeybees
Biergans, S. D., Jones, J. C., Treiber, N., Galizia, C. G., & Szyszka, P. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039349 · Cited by 67 · see citing works
Juvenile hormone induces queen development in late-stage larvae of the ant Harpegnathos saltator
Penick, C. A., Prager, S. S., & Liebig, J. (2012) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2012.10.004 · Cited by 65 · see citing works
Self-citationPaternal Effects on the Defensive Behavior of Honeybees
Guzmán‐Novoa, E., Hunt, G. J., Page, R. E., et al. (2005) · Journal of Heredity · doi:10.1093/jhered/esi038 · Cited by 59 · see citing works
Smith, C. R., Smith, C. R., Mutti, N. S., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042433 · Cited by 55 · see citing works
Weiner, S. A., Galbraith, D. A., Adams, D. C., et al. (2013) · Die Naturwissenschaften · doi:10.1007/s00114-013-1064-z · Cited by 54 · see citing works
Kin conflict in insect societies: a new epigenetic perspective
Drewell, R. A., Lo, N. C., Oxley, P. R., & Oldroyd, B. P. (2012) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2012.02.005 · Cited by 48 · see citing works
her, M. B. U. (2008) · Obesity Facts · doi:10.1159/000145930 · Cited by 43 · see citing works
A conserved role for intragenic DNA methylation in alternative pre-mRNA splicing
Oberdoerffer, S. (2012) · Transcription · doi:10.4161/trns.19816 · Cited by 41 · see citing works
Emerging topics in epigenetics: ants, brains, and noncoding RNAs
Bonasio, R. (2012) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06363.x · Cited by 40 · see citing works
Self-citationThe role of chromatin and epigenetics in the polyphenisms of ant castes
Bonasio, R. (2014) · Briefings in Functional Genomics · doi:10.1093/bfgp/elt056 · Cited by 40 · see citing works
Self-citationGenomic imprinting and kinship in the social Hymenoptera: What are the predictions?
Kronauer, D. J. C. (2008) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2008.06.019 · Cited by 38 · see citing works
Are Ant Workers Capable of Colony Foundation?
Liebig, J., Hölldobler, B., & Peeters, C. (1998) · Die Naturwissenschaften · doi:10.1007/s001140050470 · Cited by 33 · see citing works
Self-citationGENETIC COMPATIBILITY AFFECTS DIVISION OF LABOR IN THE ARGENTINE ANTLINEPITHEMA HUMILE
Libbrecht, R., & Keller, L. (2012) · Evolution · doi:10.1111/j.1558-5646.2012.01792.x · Cited by 31 · see citing works
Fowler, H. G., & Roberts, R. B. (1980) · Journal of the Kansas Entomological Society · Cited by 29 · see citing works
Cortese, R., Lewin, J., Bäckdahl, L., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0026002 · Cited by 27 · see citing works
DNA methylation in the termite Coptotermes lacteus
Lo, N., Li, B., & Újvári, B. (2011) · Insectes Sociaux · doi:10.1007/s00040-011-0213-7 · Cited by 24 · see citing works
The draft genome of a socially polymorphic halictid bee, Lasioglossum albipes (vol 14, R142, 2013)
Sd, K., Li, C., Yang, W., et al. (2015) · Cited by 12 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- Allis CD, Jenuwein T, Reinberg D. 2007. Epigenetics. Cold Spring Harbor, NY: Cold Spring Harb. Lab. Press
- H ölldobler B, Wilson EO. 1990. The Ants. Cambridge, MA: Belknap Press of Harvard Univ. Press
Cited by
Sorted by citations
Booth, L. N., & Brunet, A. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.05.013 · Cited by 499 · see citing works
Epigenetic changes during aging and their reprogramming potential
Kane, A. E., & Sinclair, D. A. (2019) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2019.1570075 · Cited by 283 · see citing works
- Authors
- Yan, H., Bonasio, R., Simola, D. F., Liebig, J., Berger, S. L., & Reinberg, D.
- Affiliations
- Department of Biochemistry and Molecular Pharmacology and
- University of Pennsylvania (US)
- Arizona State University (US)
- Howard Hughes Medical Institute (US)
- Venue
- Annual Review of Entomology
- Publisher
- Annual Reviews
- Published
- 2015-01-07
- Volume
- 60
- Issue
- 1
- Pages
- 435-452
- ISSN
- 0066-4170 (ISSN-L)
- 1545-4487
- OpenAlex
- W2143558266
- Cited by
- 183
- References
- 147
- Citations by year
- 2026: 7 · 2025: 13 · 2024: 6 · 2023: 6 · 2022: 12 · 2021: 40 · 2020: 17 · 2019: 15 · 2018: 16 · 2017: 21 · 2016: 18 · 2015: 12
- FWCI
- 1.60
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Annual Review of Entomology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute (2009005)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Insect and Arachnid Ecology and Behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- DNA methylation, eusocial insects, epigenetics, phenotypic plasticity, social behavior, longevity, gene body methylation, gene expression regulation, caste differentiation, lifespan
- MeSH terms
- Animals, Behavior, Animal, Gene Expression Regulation, Hymenoptera, Longevity, DNA Methylation, Isoptera, Epigenesis, Genetic
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review