Patterns of DNA methylation in development, division of labor and hybridization in an ant with genetic caste determination

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Smith, Chris R ^a,b   Mutti, Navdeep S ^a,d   Jasper, W Cameron ^c   Naidu, Agni ^c   Smith, Christopher D ^c   Gadau, Jürgen ^a  

^a EARLHAM COLLEGE   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c SAN FRANCISCO STATE UNIVERSITY   (United States)

^d DUPONT COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BISULFITE; DINUCLEOTIDE;

ANT; ARTICLE; BIOINFORMATICS; CPG ISLAND; DNA DETERMINATION; DNA HYBRIDIZATION; DNA METHYLATION; FEMALE; GENE FREQUENCY; IN VIVO STUDY; INSECT CASTE; INSECT DEVELOPMENT; INSECT GENETICS; MALE; MATING; NONHUMAN; POGONOMYRMEX BARBATUS; POGONOMYRMEX RUGOSUS; QUEEN (INSECT); SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; ANTS; CPG ISLANDS; DNA METHYLATION; FEMALE; GENES, INSECT; HIERARCHY, SOCIAL; HYBRIDIZATION, GENETIC; MALE; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SEXUAL BEHAVIOR, ANIMAL;

APOIDEA; FORMICIDAE; POGONOMYRMEX BARBATUS;

EID: 84864552167     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042433     Document Type: Article

References (58)

1. Razin A, Shemer R, (1995) DNA methylation in early development. Hum Mol Genet 4: 1751-1755.
2. Field LM, Lyko F, Mandrioli M, Prantera G, (2004) DNA methylation in insects. Insect Mol Biol13: 109-115.
3. Goll MG, Bestor TH, (2005) Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74: 481-514.
4. Zemach A, McDaniel IE, Silva P, Zilberman D, (2010) Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328: 916-919.
5. Xiang H, Zhu J, Chen Q, Dai F, Li X, et al. (2010) Single base-resolution methylome of the silkworm reveals a sparse epigenomic map. Nat Biotechnol 28: 516-520.
6. Feng S, Cokus SJ, Zhang X, Chen PY, Bostick M, et al. (2010) Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci USA 107: 8689-8694.
7. Razin A, Riggs AD, (1980) DNA methylation and gene function. Science 210: 604-610.
8. Feil R, Fraga MF, (2012) Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet 13: 97-109.
9. Park J, Peng Z, Zeng J, Elango N, Park T, et al. (2011) Comparative analyses of DNA methylation and sequence evolution using Nasonia genomes. Mol Biol Evol 28: 3345-3354.
10. Lyko F, Foret S, Kucharski R, Wolf S, Falckenhayn C, et al. (2010) The honey bee epigenomes: differential methylatino o fbrain DNA in queens and workers. PLoS Biol 8: e1000506.
11. Sha K, (2008) A mechanistic view of genomic imprinting. Annu Rev Genom Hum Genet 9: 197-216.
12. Reik W, Walter J, (2001) Genomic imprinting: Parental influence on the genome. Nat Rev Genet 2: 21-32.
13. Wang Y, Jorda M, Jones PL, Maleszka R, Ling X, et al. (2006) Functional CpG methylation system in a social insect. Science 214: 645-647.
14. 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 USA 106: 11206-11211.
15. Kronforst MR, Gilley DC, Strassmann JE, Queller DC, (2008) DNA methylation is widespread across social hymenoptera. Cur Biol 18: R287-R288.
16. Foret S, Kucharski R, Pellegrini M, Feng S, Jacobsen SE, Robinson GE, Maleszka R, (2012) DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees. Proc Natl Acad Sci USA 109: 4968-4973.
17. Lockett GA, Kucharski R, Maleszka R, (2012) DNA methylation changes elicited by social stimuli in the brains of worker honey bees. Genes, Brain, Behavior 11: 235-242.
18. Kucharski R, Maleszka J, Foret S, Maleszka R, (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science 319: 1827-1830.
19. Bonasio R, Zhang G, Ye C, Mutti N, Fang X, et al. (2010) Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329: 1068-1071.
20. Smith CR, Smith CD, Robertson HM, Helmkampf H, Zimin A, et al. (2011) Draft genome of the red harvester ant Pogonomyrmex barbatus. Proc Natl Acad Sci USA 108: 5667-5672.
21. Wurm Y, Wang J, Riba-Grognuz O, Corona M, Nygaard S, (2011) The genome of the fire ant Solenopsis invicta. Proc Natl Acad Sci USA 108: 5679-5684.
22. Glastad KM, Hunt BG, Yi SV, Goodisman MAD, (2011) DNA methylation in insects: on the brink of the epigenomic era. Insect Mol Biol 20: 553-565.
23. Gadau J, Helmkampf M, Nygaard S, Roux J, Simola D, et al. (2012) The genomic impact of 100 million years of social evolution in seven ant species. Trends Genet 28: 14-21.
24. Suen G, Teiling C, Li L, Holt C, Abouheif E, et al. (2011) The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. PLoS Genet 7: e1002007.
25. Smith CD, Zimin A, Holt C, Abouheif E, Benton R, et al. (2011) Draft genome of the globally widespread and invasive Argentine ant (Linepithema humile). Proc Natl Acad Sci USA 108: 5673-5678.
26. Helms Cahan S, Parker JD, Rissing SW, Johnson RA, Polony TS, et al. (2002) Extreme genetic differences between queens and workers in hybridizing Pogonomyrmex harvester ants. Proc Roy Soc B 269(1503): 1871-1877.
27. Julian GE, Fewell JH, Gadau J, Johnson RA, Larrabee D, (2002) Genetic determination of the queen caste in an ant hybrid zone. Proc Natl Acad Sci USA 99(12): 8157-8160.
28. Volny VP, Gordon DM, (2002) Genetic basis for queen-worker dimorphism in a social insect. Proc Natl Acad Sci USA 99(9): 6108-6111.
29. Anderson KE, Linksvayer TA, Smith CR, (2008) The causes and consequences of genetic caste determination in ants (Hymenoptera: Formicidae). Myrmecol News 11: 119-132.
30. Smith CR, Toth AL, Suarez AV, Robinson GE, (2008) Genetic and genomic analyses of the division of labour in insect societies. Nat Rev Genet 9: 735-748.
31. Smith CR, Anderson KE, Tillberg CV, Gadau J, Suarez AV, (2008) Caste determination in a polymorphic social insect: nutritional, social, and genetic factors. Am Nat 172: 497-507.
32. Smith CR, Suarez AV, (2010) The trophic ecology of castes in harvester ant colonies. Funct Ecol 24: 122-130.
33. Anderson KE, Smith CR, Linksvayer TA, Mott BM, Gadau JG, et al. (2009) Modeling the maintenance of a dependent lineage system: The influence of positive frequency dependent selection on sex ratio. Evolution 63: 2142-2152.
34. Helms Cahan S, Julian GE, Rissing SW, Schwander T, Parker JD, et al. (2004) Loss of phenotypic plasticity generates genotype-caste association in harvester ants. Curr Biol 14(24): 2277-2282.
35. Helms Cahan S, Keller L, (2003) Complex hybrid origin of genetic caste determination in harvester ants. Nature 424(6946): 306-309.
36. Schwander T, Helms Cahan S, Suni SS, Keller L, (2008) Mechanisms of reproductive isolation between an ant species of hybrid origin and its parents. Evolution 62: 1635-1643.
37. Anderson KE, Gadau J, Mott BM, Johnson RA, Altamirano A, et al. (2006) Distribution and evolution of genetic caste determination in Pogonomyrmex seed-harvester ants. Ecology 87(9): 2171-2184.
38. Schwander T, Cahan SH, Keller L, (2007) Characterization and distribution of Pogonomyrmex harvester ant lineages with genetic caste determination. Mol Ecol 16(2): 367-387.
39. Yi SV, Goodisman MAD, (2009) Computational approaches for understanding the evolution of DNA methylation in animals. Epigenetics 4: 551-556.
40. Flores KB, Amdam GV, (2011) Deciphering a methylome: what can we read into patterns of DNA methylation? J Exp Biol 214: 3155-3163.
41. Schwander T, Humbert J-, Brent CS, Helms Cahan S, Chapuis L, et al. (2008) Maternal effect on female caste determination in a social insect. Curr Biol 18: 265-269.
42. Sirviö A, Pamilo P, Johnson RA, Page RE Jr, Gadau J, (2011) Origin and evolution of the dependent lineages of the genetic caste determination system of Pogonomyrmex ants. Evolution 65: 869-884.
43. Kim S-H, Elango N, Warden C, Vigoda E, Yi SV, (2006) Heterogeneous genomic molecular clocks in primates. PLoS Genet 2(10): e163.
44. Krauss V, Eisenhardt C, Unger T, (2009) The genome of the stick insect Medauroidea extradentata is strongly methylated within genes and repetitive DNA. PLoS ONE 4(9): e7223.
45. Ziller MJ, Müller F, Liao J, Zhang Y, Gu H, et al. (2011) Genomic Distribution and Inter-Sample Variation of Non-CpG Methylation across Human Cell Types. PLoS Genet 7(12): e1002389.
46. Hunt BG, Ometto L, Wurm Y, Shoemaker D, Yi SV, et al. (2011) Relaxed selection is a precursor to the evolution of phenotypic plasticity. Proc Natl Acad Sci USA 108: 15936-15941.
47. Lu H, Vinson SB, Pietrantonio PV, (2009) Oocyte membrane localization of vitellogenin receptor coincides with queen flying age, and receptor silencing by RNAi disrupts egg formation in fire ant virgin queens. FEBS Journal 276: 3110-3123.
48. Hahn DA, Johnson RA, Buck NA, Wheeler DE, (2004) Storage protein content as a functional marker for colony-founding strategies: A comparative study within the harvester ant genus Pogonomyrmex. Physiol Biochem Zool 77(1): 100-108.
49. Xiong LZ, Xu CG, Saghai Maroof MA, Zhang Q, (1999) Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation sensitive amplification polymorphism technique. Mol Gen Genet 261: 439-446.
50. Schutt A, Florl AR, Shi W, Hemberger M, Orth A, et al. (2003) DNA methylation in placentas of interspecies mouse hybrids. Genetics 165: 223-228.
51. Zhao Y, Yu S, Xing C, Fan S, Song M, (2008) Analysis of DNA methylation in cotton hybrids and their parents. Mol Biol 42: 169-178.
52. Li LC, Dahiya R, (2002) MethPrimer: designing primers for methylation PCRs. Bioinformatics 18(11): 1427-1431.
53. Lewis SE, Searle SMJ, Harris N, Gibson M, Iyer V, et al. (2002) Apollo: a sequence annotation editor. Genome Biology 3: research0082-0082.14.
54. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R, (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Bio Biotech 3: 294-299.
55. Evans JD, (1993) Parentage analyses in ant colonies using simple sequence repeat loci. Mol Ecol 2: 393-397.
56. Volny VP, Gordon DM, (2002) Characterization of polymorphic microsatellite loci in the red harvester ant, Pogonomyrmex barbatus. Mol Ecol Notes 2(3): 302-303.
57. Foitzik S, Haberl M, Gadau J, Heinze J, (1997) Mating frequency of Leptothorax nylanderi ant queens determined by microsatellite analysis. Insect Soc 44: 219-227.
58. Xu M, Li X, Korban SS, (2000) AFLP-based detection of DNA methylation. Plant Mol Biol Reptr 18: 361-368.