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A survey of DNA methylation across social insect species, life stages, and castes reveals abundant and caste-associated methylation in a primitively social wasp

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Abstract

DNA methylation plays an important role in the epigenetic control of developmental and behavioral plasticity, with connections to the generation of striking phenotypic differences between castes (larger, reproductive queens and smaller, non-reproductive workers) in honeybees and ants. Here, we provide the first comparative investigation of caste- and life stage-associated DNA methylation in several species of bees and vespid wasps displaying different levels of social organization. Our results reveal moderate levels of DNA methylation in most bees and wasps, with no clear relationship to the level of sociality. Strikingly, primitively social Polistes dominula paper wasps show unusually high overall DNA methylation and caste-related differences in site-specific methylation. These results suggest DNA methylation may play a role in the regulation of behavioral and physiological differences in primitively social species with more flexible caste differences.

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References

  • Bonasio R, Zhang G, Ye C, Mutti NS, Fang X, Qin N, Donahue G et al (2010) Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329:1068–1071

    Article  PubMed  CAS  Google Scholar 

  • Bonasio R, Li QY, Lian JM, Mutti NS, Jin LJ, Zhao HM, Zhang P, Wen P, Xiang H, Ding Y, Jin ZH, Shen SS, Wang ZJ, Wang W, Wang J, Berger SL, Liebig J, Zhang GJ, Reinberg D (2012) Genome-wide and caste-specific DNA methylomes of the ants Camponotus floridanus and Harpegnathos saltator. Curr Biol 22:1755–1764

    Article  PubMed  CAS  Google Scholar 

  • Chen Y, Sharma RP, Costa RH, Costa E, Grayson DR (2002) On the epigenetic regulation of the human reelin promoter. Nucleic Acids Res 30:2930–2939

    Article  PubMed  CAS  Google Scholar 

  • Crews D (2008) Epigenetics and its implications for behavioral neuroendocrinology. Front Neuroendocrinol 29:344–357

    Article  PubMed  CAS  Google Scholar 

  • Elango N, Hunt BG, Goodisman MAD, Yi SV (2009) DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera. Proc Natl Acad Sci U S A 106:11206–11211

    Article  PubMed  CAS  Google Scholar 

  • Herb BR, Wolschin F, Hansen KD, Aryee MJ, Langmead B, Irizarry R, Amdam GV, Feinberg AP (2012) Reversible switching between epigenetic states in honeybee behavioral subcastes. Nat Neurosci 15:1371–1373

    Article  PubMed  CAS  Google Scholar 

  • Hines HM, Hunt JH, O'Connor TK, Gillespie JJ, Cameron SA (2007) Multigene phylogeny reveals eusociality evolved twice in vespid wasps. Proc Natl Acad Sci U S A 104:3295–3299

    Article  PubMed  CAS  Google Scholar 

  • Jimenez-Chillaron JC, Diaz R, Martinez D, Pentinat T, Ramon-Krauel M, Ribo S, Plosch T (2012) The role of nutrition on epigenetic modifications and their implications on health. Biochimie 94:2242–2263

    Article  PubMed  CAS  Google Scholar 

  • Kronforst M, David G, Joan S, David Q (2006) DNA methylation is widespread across social hymenoptera. Curr Biol 18:R287–R288

    Article  Google Scholar 

  • Kucharski R, Maleszka J, Foret S, Maleszka R (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science 319:1827–1830

    Article  PubMed  CAS  Google Scholar 

  • Lockett, GA, Helliwell, P, Maleszka R (2010) Involvement of DNA methylation in memory processing in the honey bee. Neuroreport 12:812–816

    Google Scholar 

  • Lyko F, Foret S, Kucharski R, Wolf S, Falckenhayn C, Maleszka R (2010) The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol 8:e1000506

    Article  PubMed  Google Scholar 

  • Moczek A, Snell-Rood E (2008) The basis of bee-ing different: the role of gene silencing in plasticity. Evol Dev 10:511–513

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reik W, Dean W, Walter J (2001) Epigenetic reprogramming in mammalian development. Science 293:1089–1093

    Article  PubMed  CAS  Google Scholar 

  • Ross KG, Matthews RW (1991) The social biology of wasps. Ithaca, New York

    Google Scholar 

  • Shi YY, Wei YY, Huang ZY, Wang ZL, Wu XB, Zeng ZJ (2013) Genomewide analysis indicates that queen larvae have lower methylation levels in the honey bee (Apis mellifera). Naturwissenschaften 100:193–197

    Article  PubMed  CAS  Google Scholar 

  • Smith, CR, Smith, CD, Robertson, HM, Helmkampf, M et al. (2011) Draft genome of the red harvester ant Pogonomyrmex barbatus. Proc Natl Acad Sci USA 108:5667–5672

    Google Scholar 

  • Smith CR, Mutti NS, Jasper WC, Naidu A, Smith CD, Gadau J (2012) Patterns of DNA Methylation in development, division of labor and hybridization in an ant with genetic caste determination. PLoS One 7:e42433

    Article  PubMed  CAS  Google Scholar 

  • Szyf M, McGowan P, Meaney MJ (2008) The social environment and the epigenome. Environ Mol Mutagen 49:46–60

    Article  PubMed  CAS  Google Scholar 

  • Walsh TK, Brisson JA, Robertson HM, Gordon K, Jaubert-Possamai S, Tagu D, Edwards OR (2010) A functional DNA methylation system in the pea aphid, Acyrthosiphon pisum. Insect Mol Biol 19:215–228

    Article  PubMed  CAS  Google Scholar 

  • Weaver ICG, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7:847–854

    Article  PubMed  CAS  Google Scholar 

  • Weiner SA, Toth AL (2012) Epigenetics in social insects: a new direction for understanding the evolution of castes. Genet Res Int 2012:609810

    PubMed  Google Scholar 

  • West-Eberhard, MJ (2003) Developmental plasticity and evolution. Oxford University Press.

  • Zapala MA, Schork NJ (2006) Multivariate regression analysis of distance matrices for testing associations between gene expression patterns and related variables. Proc Natl Acad Sci U S A 103:19430–19435

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We would like to thank Shelby Fleischer and Ermita Hernandez for the bumble bees, Tom Glenn for the honeybees, Sarah Kocher, Bernardo Niño, and Elina Lastro Niño for D. maculata, John Wenzel for the helpful discussions, Naila Canevazzi for the DNA extractions, Daniel Kronforst for the AFLP methods, Ali Berens for the statistical analysis, and members of the Toth laboratory for reviewing the manuscript. This research was supported by the United States Department of Agriculture Award 2008-35302-06024 to ALT and National Science Foundation Award IOS-1051808 to ALT.

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Authors and Affiliations

  1. Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA, USA

    Susan A. Weiner, Dean C. Adams, Nicole Valenzuela & Amy L. Toth

  2. Department of Entomology, Center for Pollinator Research, Pennsylvania State University, University Park, PA, USA

    David A. Galbraith & Christina M. Grozinger

  3. Department of Statistics, Iowa State University, Ames, IA, USA

    Dean C. Adams

  4. Depto. de Zoologia e Botânica, IBILCE-UNESP, São José do Rio Preto, Brazil

    Fernando B. Noll

  5. Department of Entomology, Iowa State University, Ames, IA, USA

    Amy L. Toth

Authors
  1. Susan A. Weiner
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  2. David A. Galbraith
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  3. Dean C. Adams
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  4. Nicole Valenzuela
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  5. Fernando B. Noll
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  6. Christina M. Grozinger
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  7. Amy L. Toth
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Corresponding author

Correspondence to Amy L. Toth.

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Communicated by: Sven Thatje

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Weiner, S.A., Galbraith, D.A., Adams, D.C. et al. 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, 795–799 (2013). https://doi.org/10.1007/s00114-013-1064-z

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  • DOI: https://doi.org/10.1007/s00114-013-1064-z

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