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Cytosine methylation in insects: new routes for the comprehension of insect complexity

Dipartimento di Scienze della Vita, Università di Modena e Reggio Emilia, Via Campi 213/d, 41125 Modena, Italy

Special Issues: Chromatin and Epigenetics

Cytosine methylation is one of the most studied epigenetic modifications and its occurrence has been deeply studied in mammals and plants. DNA methylation (together with other epigenetic modifications of DNA and histones) plays an important role in different processes. Indeed, several morphological and/or behavioural traits may origin as a consequence of the epigenetic modulation of genes so that identical genes can results in different “morphs”. Despite considerable progress during recent years, many questions remain since it is largely unknown how the environment triggers alterations in the epigenome. In the present review we discuss the use of aphids and honey bees as epigenetic experimental model to understand how cytosine methylation is directly or indirectly linked to environmental factors. Indeed, the epigenetic changes of DNA could be at the basis of unexpected morphological differences explaining also complex traits.
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Keywords epigenetics; cytosine methylation; transcription control; aphid; honey bees

Citation: Mauro Mandrioli, Gian Carlo Manicardi. Cytosine methylation in insects: new routes for the comprehension of insect complexity. AIMS Biophysics, 2015, 2(4): 412-422. doi: 10.3934/biophy.2015.4.412


  • 1. Adams RLP (1996) Principles of Medical Biology, vol. 5, JAI Press Inc., New York, 33-66.
  • 2. Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16: 6-21.    
  • 3. Ehrlich M, Gama-Sosa MA, Huang LH, et al. (1982) Amount and distribution of 5-methylcytosine in human DNA from different types of tissues of cells. Nucleic Acids Res 10: 2709-2721.
  • 4. Lister R, Pelizzola M, Dowen RH, et al. (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462: 315-322.    
  • 5. Jones PA (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nature Rev Genet 13: 484-492.    
  • 6. Walsh CP, Bestor TH (1999) Cytosine methylation and mammalian development. Genes Dev 13: 26-34.    
  • 7. Okano M, Bell DW, Haber DA, et al. 1999. DNA Methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99: 247-257.
  • 8. Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330: 622-627.    
  • 9. Liu K, Wang YF, Cantemir C, et al. (2003) Endogenous assays of DNA methyltransferases: evidence for differential activities of DNMT1, DNMT2, and DNMT3 in mammalian cells in vivo. Mol Cell Biol 23: 2709-2719.
  • 10. Chen Z, Riggs AD (2011) DNA methylation and demethylation in mammals. J Biol Chem 286: 18347-18353.    
  • 11. Mathieu O, Reinders J, Caikovski M, et al. (2007) Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell 130: 851-862.    
  • 12. Johannes F, Porcher E, Teixeira FK, et al. (2009). Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet 5: e1000530.
  • 13. Reinders J, Paszkowski J (2009) Unlocking the Arabidopsis epigenome. Epigenetics 4: 557-563.    
  • 14. Rando OJ, Verstrepen KJ (2007) Timescales of genetic and epigenetic inheritance. Cell 128: 655-668.    
  • 15. Morgan HD, Sutherland HG, Martin DI, et al. (1999) Epigenetic inheritance at the agouti locus in the mouse. Nature Genet 23: 314-318.    
  • 16. Richards EJ (2006) Inherited epigenetic variation-revisiting soft inheritance. Nat Rev Genet 7: 395-401.    
  • 17. Glastad KM, Hunt BG, Yi SV, et al. (2011) DNA methylation in insects: on the brink of the epigenomic era. Insect Mol Biol 20: 553-565.    
  • 18. Lyko F, Maleszka R (2011) Insects as innovative models for functional studies of DNA methylation. Trends Genet 27: 127-131.
  • 19. Esteller M (2004) DNA methylation: approaches and applications. CRC Press, Boca Raton, FL.
  • 20. Lockett GA, Kucharski R, Maleszka R (2012) DNA methylation changes elicited by social stimuli in the brains of worker honey bees. Genes Brain Behav 11: 235-242.
  • 21. Ikeda T, Furukawa S, Nakamura J, et al. (2011) CpG methylation in the hexamerin 110 gene in the European honeybee, Apis mellifera. J Insect Sci 11: 74.
  • 22. Mandrioli M (2004) Epigenetic tinkering and evolution: is there any continuity in the functional role of cytosine methylation from invertebrates to vertebrates? Cell Mol Life Sci 61: 2425-2427.    
  • 23. Field LM, Lyko F, Mandrioli M, et al. (2004) DNA methylation in insects. Insect Mol Biol 13: 109-115.    
  • 24. Luco RF, Allo M, Schor IE, et al. (2011) Epigenetics in alternative pre-mRNA splicing. Cell 144:16-26.    
  • 25. Simmen MW, Leitgeb S, Charlton J, et al. (1999) Non-methylated transposable elements and methylates genes in a chordate genome. Science 283: 1164-1167.    
  • 26. Loxdale HD (2009) What’s in a clone: the rapid evolution of aphid asexual lineages in relation to geography, host plant adaptation and resistance to pesticides. In: Schon I, Martens K van Dijk P eds, Lost sex: The Evolutionary Biology of Parthenogenesis. Springer, Heidelberg, Germany, pp. 535-557.
  • 27. Suomalainen E, Saura A, Lokki J (1987) Cytology and evolution in parthenogenesis. CRC Press, Boca Raton.
  • 28. Dixon AFG (1987) Parthenogenetic reproduction and the rate of increase in aphids. In: A. Minks and P. Harrewijn (ed), Aphids, their Biology, Natural Enemies and Control. vol. A, Elsevier, The Netherlands, 269-287.
  • 29. Janzen DH (1977) What are dandelions and aphids? Am Nat 111: 586-589.    
  • 30. Loxdale HD (2008a) Was Dan Janzen (1977) right about aphid clones being a ‘super-organism’, i.e. a single ‘evolutionary individual’? New insights from the use of molecular marker systems. Mitt DGaaE 16: 437-449
  • 31. Loxdale HD (2008b) The nature and reality of the aphid clone: genetic variation, adaptation and evolution. Agr Forest Entomol 10: 81-90.
  • 32. Pasquier C, Clément M, Dombrovsky A, et al. (2014) Environmentally selected aphid variants in clonality context display differential patterns of methylation in the genome. PLoS One 9: e115022.    
  • 33. Jenkins RL (1991) Colour and symbionts of aphids. PhD Thesis, University of East Anglia, UK.
  • 34. Terradot L, Simon JC, Leterne N, et al. (1999) Molecular characterization of clones of the Myzus persicae complex differing in their ability to transmit the potato leafroll lutovirus (PLRV). Bull Entomol Res 89: 355-363.
  • 35. Losey JE, Ives AR, Harmon J, et al. (1997) A polymorphism maintained by opposite patterns of parasitism and predation. Nature 388: 269-272.    
  • 36. Devonshire AL, Field LM, Foster SP, et al. (1999) The evolution of insecticide resistance in the peach-potato aphid, Myzus persicae. In: Denholm, I., Pickett, J.A. & Devonshire, A.L. (Eds), Insecticide resistance: from mechanisms to management. Wallingford, Oxon, CABI Publishing.
  • 37. Brisson JA (2010) Aphid wing dimorphisms: linking environmental and genetic control of trait variation. Philos Trans R Soc Lond B Biol Sci 365: 605-616.    
  • 38. Le Trionnaire G, Hardie J, Jaubert-Possamai S, et al. (2008) Shifting from clonal to sexual reproduction in aphids: physiological and developmental aspects. Biol Cell 100: 441-451.    
  • 39. Davis GK (2012) Cyclical parthenogenesis and viviparity in aphids as evolutionary novelties. J Exp Zool B Mol Dev Evol 318: 448-459.
  • 40. Aoki S (1977) Colophina clematis (Homoptera, Pemphigidae), an aphid species with soldiers. Kontyû 45: 276-282.
  • 41. Miyazaki M (1987) Forms and morphs of aphids. In: A. K. Minks and P. Harrewijin (eds), Aphids, Their Biology, Natural Enemies, and Control. Amsterdam: Elsevier), 27-50.
  • 42. Fukatsu T (2010) A fungal past to insect color. Science 328: 574-575.    
  • 43. Tsuchida T, Koga R, Horikawa M, et al. (2010) Symbiotic bacterium modifies aphid body color. Science 330: 1102-1104.    
  • 44. Braendle C, Davis GK, Brisson JA, et al. (2006) Wing dimorphism in aphids. Heredity 97: 192-199.    
  • 45. Stern DL, Foster WA (1996) The evolution of soldiers in aphids. Biol Rev Camb Philos Soc 71: 27-79.    
  • 46. Shibao H, Kutsukake M, Matsuyama S, et al. (2010) Mechanisms regulating caste differentiation in an aphid social system. Commun Integr Biol 3: 1-5.    
  • 47. Hattori M, Kishida O, Itino T (2013) Soldiers with large weapons in predator-abundant midsummer: reproductive plasticity in a eusocial aphid. Evol Ecol 27: 847-862.    
  • 48. Moran NA, Jarvik T (2010) Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328: 624-627.    
  • 49. Valmalette JC, Dombrovsky A, Brat P, et al. (2012) Light- induced electron transfer and ATP synthesis in a carotene synthesizing insect. Scientific report 2: 579.
  • 50. Dombrovsky A, Arthaud L, Ledger TN, et al. (2009) Profiling the repertoire of phenotypes influenced by environmental cues that occur during asexual reproduction. Genome Res 19: 2052-2063.    
  • 51. Hick CA, Field LM, Devonshire AL (1996) Changes in the methylation of amplified esterase DNA during loss and reselection of insecticide resistance in peach-potato aphids, Myzus persicae. Insect Biochem Mol Biol 26: 41-47.    
  • 52. Field LM, Blackman RL, Tyler-Smith C, et al. (1999) Relationship between amount of esterase and gene copy number in insecticide-resistant Myzus persicae (Sulzer). Biochem J 339: 737-742.    
  • 53. Field LM (2000) Methylation and expression of amplified esterase genes in the aphid Myzus persicae (Sulzer). Biochem J 349: 863-868.    
  • 54. Walsh TK, Brisson JA, Robertson HM, et al. (2010) A functional DNA methylation system in the pea aphid, Acyrthosiphon pisum. Insect Mol Biol 19: 215-228.    
  • 55. Daxinger L, Whitelaw E (2010) Transgenerational epigenetic inheritance: more questions than answers. Genome Res 20: 1623-1628.    
  • 56. Srinivasan DG, Brisson JA (2012) Aphids: a model for polyphenism and epigenetics. Genet Res Int 2012: 431531
  • 57. Maynard Smith J, Szathmary E (1995) The major transitions in evolution. Oxford University Press.
  • 58. Grosberg RK, Strathmann RR (2007) The evolution of multicellularity: a minor major transition? Annu Rev Ecol Evol Syst 38: 621-654.    
  • 59. Branda SS, Gonzalez-Pastor JE, Ben-Yehuda S, et al. (2001) Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci U S A 98:11621-11626.    
  • 60. Lurling M, Van Donk E (2000) Grazer-induced colony formation in Scenedesmus: are there costs to being colonial? Oikos 88: 111-118.    
  • 61. Kaiser D (2001) Building a multicellular organism. Annu Rev Genet 35:103-123.    
  • 62. Ausmees N, Jacobs-Wagner C (2003) Spatial and temporal control of differentiation and cell cycle progression in Caulobacter crescentus. Annu Rev Microbiol 57: 225-247.    
  • 63. Patalano S, Hore TA, Reik W, et al. (2012) Shifting behaviour: epigenetic reprogramming in eusocial insects. Curr Opin Cell Biol 24: 367-373    
  • 64. Foret S, Kuxcharski R, Pellegrini M, et al. (2012) DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees Proc Natl Acad Sci U S A 109: 4968-4973.
  • 65. Wang Y, Jorda M, Jones PL, et al. (2006) Functional CpG methylation system in a social insect. Science 314: 645-647.    
  • 66. Wurm Y, Wang J, Riba-Grognuz O, et al. (2011) The genome of the fire ant Solenopsis invicta. Proc Natl Acad Sci U S A 108: 5679-5684.    
  • 67. Suen G, Teiling C, Li L, et al. (2011) The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. PLoS Genet 7: e1002007.    
  • 68. Smith CR, Smith CD, Robertson HM, et al. (2011) Draft genome of the red harvester ant Pogonomyrmex barbatus. Proc Natl Acad Sci U S A 108: 5667-5672.    
  • 69. Lyko F, Foret S, Kucharski R, et al. (2010) The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol 8: e1000506.    
  • 70. Kucharski R, Maleszka J, Foret S, et al. (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science 319: 1827-1830.
  • 71. Shi YY, Huang ZY, Zeng ZJ, et al. (2011) Diet and cell size both affect queen-worker differentiation through DNA methylation in honey bees (Apis mellifera, Apidae). PLoS One 6: e18808.    
  • 72. Weaver N (1966) Physiology of caste determination. Annu Rev Entomol 11: 79-102.    
  • 73. Strassmann JE (1983) Gerontocracy in the social wasp, Polistes exclamans. Anim Behav 31: 431-438.    
  • 74. Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209: 2362-2367.    
  • 75. West-Eberhard MJ (2003) Developmental plasticity and evolution. New York: Oxford University Press.
  • 76. Wittkopp PJ, Kalay G (2012) Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nature Rev Genet 13: 59-69.    


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