Recent Advances in Behavioral (Epi)Genetics in Eusocial Insects

Literature Cited

1. 1.  Abouheif E, Wray GA 2002. Evolution of the gene network underlying wing polyphenism in ants. Science 297:249–52
   [Google Scholar]
2. 2.  Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY 1999. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 23:185–88
   [Google Scholar]
3. 3.  Barish S, Volkan PC 2015. Mechanisms of olfactory receptor neuron specification in Drosophila. Wiley Interdiscip. Rev. Dev. Biol. 4:609–21
   [Google Scholar]
4. 4.  Barth RH, Lester LJ, Sroka P, Kessler T, Hearn R 1975. Juvenile hormone promotes dominance behavior and ovarian development in social wasps (Polistes annularis). Experientia 31:691–92
   [Google Scholar]
5. 5.  Beites CL, Kawauchi S, Crocker CE, Calof AL 2005. Identification and molecular regulation of neural stem cells in the olfactory epithelium. Exp. Cell Res. 306:309–16
   [Google Scholar]
6. 6.  Benton R, Sachse S, Michnick SW, Vosshall LB 2006. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLOS Biol. 4:e20
   [Google Scholar]
7. 7.  Bohm MK 1972. Effects of environment and juvenile hormone on ovaries of the wasp, Polistes metricus. J. Insect Physiol. 18:1875–83
   [Google Scholar]
8. 8.  Bonasio R, Li Q, Lian J, Mutti NS, Jin L 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]
9. 9.  Bonasio R, Zhang G, Ye C, Mutti NS, Fang X et al. 2010. Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329:1068–71
   [Google Scholar]
10. 10.  Brian MV 1973. Temperature choice and its relevance to brood survival and caste determination in the ant Myrmica rubra L. Physiol. Zool. 46:245–52
    [Google Scholar]
11. 11.  Brind'Amour J, Liu S, Hudson M, Chen C, Karimi MM, Lorincz MC 2015. An ultra-low-input native ChIP-seq protocol for genome-wide profiling of rare cell populations. Nat. Commun. 6:6033
    [Google Scholar]
12. 12.  Bryant DM, Mostov KE 2008. From cells to organs: building polarized tissue. Nat. Rev. Mol. Cell Biol. 9:887–901
    [Google Scholar]
13. 13.  Buenrostro JD, Wu B, Litzenburger UM, Ruff D, Gonzales ML et al. 2015. Single-cell chromatin accessibility reveals principles of regulatory variation. Nature 523:486–90
    [Google Scholar]
14. 14.  Carlin NF, Holldobler B 1983. Nestmate and kin recognition in interspecific mixed colonies of ants. Science 222:1027–29
    [Google Scholar]
15. 15.  Chandrasekaran S, Rittschof CC, Djukovic D, Gu H, Raftery D et al. 2015. Aggression is associated with aerobic glycolysis in the honey bee brain. Genes Brain Behav. 14:158–66
    [Google Scholar]
16. 16.  Chiang A, Priya R, Ramaswami M, Vijayraghavan K, Rodrigues V 2009. Neuronal activity and Wnt signaling act through Gsk3-β to regulate axonal integrity in mature Drosophila olfactory sensory neurons. Development 136:1273–82
    [Google Scholar]
17. 17.  Clowney EJ, LeGros MA, Mosley CP, Clowney FG, Markenskoff-Papadimitriou EC et al. 2012. Nuclear aggregation of olfactory receptor genes governs their monogenic expression. Cell 151:724–37
    [Google Scholar]
18. 18.  Cnaani J, Robinson GE, Bloch G, Borst D, Hefetz A 2000. The effect of queen-worker conflict on caste determination in the bumblebee Bombus terrestris. Behav. Ecol. Sociobiol. 47:346–52
    [Google Scholar]
19. 19.  Cool-Kwait E, Topoff H 1984. Raid organization and behavioral development in the slave-making ant Polyergus lucidus Mayr. Insectes Soc. 31:361–74
    [Google Scholar]
20. 20.  Cornette R, Gotoh H, Koshikawa S, Miura T 2008. Juvenile hormone titers and caste differentiation in the damp-wood termite Hodotermopsis sjostedti (Isoptera, Termopsidae). J. Insect Physiol. 54:922–30
    [Google Scholar]
21. 21.  Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y et al. 2007. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. PNAS 104:7128–33
    [Google Scholar]
22. 22.  Crespi BJ, Yanega D 1995. The definition of eusociality. Behav. Ecol. 6:109–15
    [Google Scholar]
23. 22a.  de Oliveira Campos LA, Velthuis-Kluppell FM, Velthuis HHW 1975. Juvenile hormone and caste determination in a stingless bee. Naturwissenschaften 62:98–99
    [Google Scholar]
24. 23.  d'Ettorre P, Deisig N, Sandoz JC 2017. Decoding ants’ olfactory system sheds light on the evolution of social communication. PNAS 114:8911–13
    [Google Scholar]
25. 24.  Dalton RP, Lomvardas S 2015. Chemosensory receptor specificity and regulation. Annu. Rev. Neurosci. 38:331–49
    [Google Scholar]
26. 25.  Despland E, Simpson SJ 2005. Food choices of solitarious and gregarious locusts reflect cryptic and aposematic antipredator strategies. Anim. Behav. 69:471–79
    [Google Scholar]
27. 25a.  Dietz A, Hermann HR, Blum MS 1979. The role of exogenous JH I, JH III and anti-JH (precocene II) on queen induction of 4.5-day-old worker honey bee larvae. J. Insect Physiol. 25:503–12
    [Google Scholar]
28. 26.  Durst C, Eichmüller S, Mensel R 1994. Development and experience lead to increased volume of subcompartments of the honeybee mushroom body. Behav. Neural Biol. 62:259–63
    [Google Scholar]
29. 27.  Endo K, Karim MR, Taniguchi H, Krejci A, Kinameri E et al. 2011. Chromatin modification of Notch targets in olfactory receptor neuron diversification. Nat. Neurosci. 15:224–33
    [Google Scholar]
30. 28.  Fahrbach SE 2006. Structure of the mushroom bodies of the insect brain. Annu. Rev. Entomol. 51:209–32
    [Google Scholar]
31. 28a.  Fahrbach SE, Dobrin S 2009. The how and why of structural plasticity in the adult honeybee brain. Cognitive Ecology II R Dukas, JM Ratcliffe 27–46 Chicago: Univ. Chicago Press
    [Google Scholar]
32. 29.  Fahrbach SE, Giray T, Robinson GE 1995. Volume changes in the mushroom bodies of adult honey bee queens. Neurobiol. Learn. Mem. 63:181–91
    [Google Scholar]
33. 30.  Falibene A, Roces F, Rossler W 2015. Long-term avoidance memory formation is associated with a transient increase in mushroom body synaptic complexes in leaf-cutting ants. Front. Behav. Neurosci. 9:84
    [Google Scholar]
34. 31.  Farris SM, Robinson GE, Fahrbach SE 2001. Experience- and age-related outgrowth of intrinsic neurons in the mushroom bodies of the adult worker honeybee. J. Neurosci. 21:6395–404
    [Google Scholar]
35. 32.  Feyereisen R, Tobe SS 1981. A rapid partition assay for routine analysis of juvenile hormone release by insect corpora allata. Anal. Biochem. 111:372–75
    [Google Scholar]
36. 33.  Foret S, Kucharski R, Pellegrini M, Feng S, Jacobsen SE et al. 2012. DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees. PNAS 109:4968–73
    [Google Scholar]
37. 34.  Franklin EL, Franks NR 2012. Individual and social learning in tandem-running recruitment by ants. Anim. Behav. 84:361–68
    [Google Scholar]
38. 35.  Friedman DA, Gordon DM, Luo L 2017. The MutAnts are here. Cell 170:601–2
    [Google Scholar]
39. 36.  von Frisch K 1949. Die Polarisation des Himmelslichtes als orientierender Faktor bei den Tänzen der Bienen. Experientia 5:142–48
    [Google Scholar]
40. 37.  Gadau J, Helmkampf M, Nygaard S, Roux J, Simola DF et al. 2012. The genomic impact of 100 million years of social evolution in seven ant species. Trends Genet. 28:14–21
    [Google Scholar]
41. 38.  Ghaninia M, Haight K, Berger SL, Reinberg D, Zwiebel LJ et al. 2017. Chemosensory sensitivity reflects reproductive status in the ant Harpegnathos saltator. Sci. Rep. 7:3732
    [Google Scholar]
42. 39.  Glastad KM, Gokhale K, Liebig J, Goodisman MA 2016. The caste- and sex-specific DNA methylome of the termite Zootermopsis nevadensis. Sci. Rep. 6:37110
    [Google Scholar]
43. 40.  Gospocic J, Shields EJ, Glastad KM, Lin Y, Penick CA et al. 2017. The neuropeptide corazonin controls social behavior and caste identity in ants. Cell 170:748–59.e12
    [Google Scholar]
44. 41.  Gronenberg W, Heeren S, Hölldobler B 1996. Age-dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus. J. Exp. Biol. 199:2011–19
    [Google Scholar]
45. 42.  Gronenberg W, Liebig J 1999. Smaller brains and optic lobes in reproductive workers of the ant Harpegnathos. Naturwissenschaften 86:343–45
    [Google Scholar]
46. 43.  Hansson BS, Stensmyr MC 2011. Evolution of insect olfaction. Neuron 72:698–711
    [Google Scholar]
47. 44.  Hartfelder K, Emlen DJ 2012. Endocrine control of insect polyphenism. Insect Endocrinology LI Gilbert 464–522 New York: Academic
    [Google Scholar]
48. 45.  Hartfelder K, Makert GR, Judice CC, Pereira GAG, Santana WC et al. 2006. Physiological and genetic mechanisms underlying caste development, reproduction and division of labor in stingless bees. Apidologie 37:144–63
    [Google Scholar]
49. 46.  Hensch TK 2005. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6:877–88
    [Google Scholar]
50. 47.  Herb BR, Wolschin F, Hansen KD, Aryee MJ, Langmead B et al. 2012. Reversible switching between epigenetic states in honeybee behavioral subcastes. Nat. Neurosci. 15:1371–73
    [Google Scholar]
51. 48.  Hölldobler B, Wilson EO 1990. The Ants Cambridge, MA: Belknap
52. 49.  Hölldobler B, Wilson EO 2008. The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies New York: W.W. Norton
53. 50.  Huang Z-Y, Robinson GE 1996. Regulation of honey bee division of labor by colony age demography. Behav. Ecol. Sociobiol. 39:147–58
    [Google Scholar]
54. 51.  Ishikawa Y, Aonuma H, Miura T 2008. Soldier-specific modification of the mandibular motor neurons in termites. PLOS ONE 3:e2617
    [Google Scholar]
55. 52.  Ishikawa Y, Okada Y, Ishikawa A, Miyakawa H, Koshikawa S, Miura T 2010. Gene expression changes during caste-specific neuronal development in the damp-wood termite Hodotermopsis sjostedti. BMC Genom. 11:314
    [Google Scholar]
56. 53.  Ismail N, Robinson GE, Fahrbach SE 2006. Stimulation of muscarinic receptors mimics experience-dependent plasticity in the honey bee brain. PNAS 103:207–11
    [Google Scholar]
57. 54.  Jafari S, Alenius M 2015. Cis-regulatory mechanisms for robust olfactory sensory neuron class-restricted odorant receptor gene expression in Drosophila. PLOS Genet. 11:e1005051
    [Google Scholar]
58. 55.  Jafari S, Alkhori L, Schleiffer A, Brochtrup A, Hummel T, Alenius M 2012. Combinatorial activation and repression by seven transcription factors specify Drosophila odorant receptor expression. PLOS Biol. 10:e1001280
    [Google Scholar]
59. 56.  Joseph RM, Carlson JR 2015. Drosophila chemoreceptors: a molecular interface between the chemical world and the brain. Trends Genet. 31:683–95
    [Google Scholar]
60. 57.  Jowaed A, Schmitt I, Kaut O, Wullner U 2010. Methylation regulates alpha-synuclein expression and is decreased in Parkinson's disease patients’ brains. J. Neurosci. 30:6355–59
    [Google Scholar]
61. 58.  Kamakura M 2011. Royalactin induces queen differentiation in honeybees. Nature 473:478–83
    [Google Scholar]
62. 59.  Khamis AM, Hamilton AR, Medvedeva YA, Alam T, Alam I et al. 2015. Insights into the transcriptional architecture of behavioral plasticity in the honey bee Apis mellifera. Sci. Rep. 5:11136
    [Google Scholar]
63. 60.  Kohno H, Suenami S, Takeuchi H, Sasaki T, Kubo T 2016. Production of knockout mutants by CRISPR/Cas9 in the European honeybee, Apis mellifera L. Zool. Sci. 33:505–12
    [Google Scholar]
64. 61.  Komiyama T, Luo L 2006. Development of wiring specificity in the olfactory system. Curr. Opin. Neurobiol. 16:67–73
    [Google Scholar]
65. 62.  Konstantinides N, Kapuralin K, Fadil C, Barboza L, Satija R, Desplan C 2018. Phenotypic convergence: distinct transcription factors regulate common terminal features. Cell 174:622–35.e13
    [Google Scholar]
66. 63.  Kucharski R, Maleszka J, Foret S, Maleszka R 2008. Nutritional control of reproductive status in honeybees via DNA methylation. Science 319:1827–30
    [Google Scholar]
67. 64.  Kuhn-Buhlmann S, Wehner R 2006. Age-dependent and task-related volume changes in the mushroom bodies of visually guided desert ants, Cataglyphis bicolor. J. Neurobiol. 66:511–21
    [Google Scholar]
68. 65.  Laissue PP, Vosshall LB 2008. The olfactory sensory map in Drosophila. Adv. Exp. Med. Biol. 628:102–14
    [Google Scholar]
69. 66.  Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB 2004. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43:703–14
    [Google Scholar]
70. 67.  Lein E, Borm LE, Linnarsson S 2017. The promise of spatial transcriptomics for neuroscience in the era of molecular cell typing. Science 358:64–69
    [Google Scholar]
71. 68.  Leonhardt SD, Menzel F, Nehring V, Schmitt T 2016. Ecology and evolution of communication in social insects. Cell 164:1277–87
    [Google Scholar]
72. 69.  Li-Byarlay H, Li Y, Stroud H, Feng S, Newman TC et al. 2013. RNA interference knockdown of DNA methyl-transferase 3 affects gene alternative splicing in the honey bee. PNAS 110:12750–55
    [Google Scholar]
73. 70.  Li-Byarlay H, Rittschof CC, Massey JH, Pittendrigh BR, Robinson GE 2014. Socially responsive effects of brain oxidative metabolism on aggression. PNAS 111:12533–37
    [Google Scholar]
74. 71.  Libbrecht R, Oxley PR, Keller L, Kronauer DJ 2016. Robust DNA methylation in the clonal raider ant brain. Curr. Biol. 26:391–95
    [Google Scholar]
75. 72.  Liebig J, Peeters C, Oldham NJ, Markstädter C, Hölldobler B 2000. Are variations in cuticular hydrocarbons of queens and workers a reliable signal of fertility in the ant Harpegnathos saltator?. PNAS 97:4124–31
    [Google Scholar]
76. 73.  Lubeck E, Coskun AF, Zhiyentayev T, Ahmad M, Cai L 2014. Single-cell in situ RNA profiling by sequential hybridization. Nat. Methods 11:360–61
    [Google Scholar]
77. 74.  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
    [Google Scholar]
78. 75.  Ma L, Wu Y, Qiu Q, Scheerer H, Moran A, Yu CR 2014. A developmental switch of axon targeting in the continuously regenerating mouse olfactory system. Science 344:194–97
    [Google Scholar]
79. 76.  Macosko EZ, Basu A, Satija R, Nemesh J, Shekhar K et al. 2015. Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell 161:1202–14
    [Google Scholar]
80. 77.  Magklara A, Yen A, Colquitt BM, Clowney EJ, Allen W et al. 2011. An epigenetic signature for monoallelic olfactory receptor expression. Cell 145:555–70
    [Google Scholar]
81. 78.  Masuoka Y, Yaguchi H, Suzuki R, Maekawa K 2015. Knockdown of the juvenile hormone receptor gene inhibits soldier-specific morphogenesis in the damp-wood termite Zootermopsis nevadensis (Isoptera: Archotermopsidae). Insect Biochem. Mol. Biol. 64:25–31
    [Google Scholar]
82. 79.  McGuire SE, Le PT, Davis RL 2001. The role of Drosophila mushroom body signaling in olfactory memory. Science 293:1330–33
    [Google Scholar]
83. 80.  McKenzie SK, Fetter-Pruneda I, Ruta V, Kronauer DJ 2016. Transcriptomics and neuroanatomy of the clonal raider ant implicate an expanded clade of odorant receptors in chemical communication. PNAS 113:14091–96
    [Google Scholar]
84. 81.  Monahan K, Lomvardas S 2015. Monoallelic expression of olfactory receptors. Annu. Rev. Cell Dev. Biol. 31:721–40
    [Google Scholar]
85. 82.  Morel L, Blum MS 1988. Nestmate recognition in Camponotus floridanus callow worker ants: Are sisters or nestmates recognized?. Anim. Behav. 36:718–25
    [Google Scholar]
86. 83.  Mueller UG 1998. The evolution of agriculture in ants. Science 281:2034–38
    [Google Scholar]
87. 84.  Muscedere ML, Traniello JF 2012. Division of labor in the hyperdiverse ant genus Pheidole is associated with distinct subcaste- and age-related patterns of worker brain organization. PLOS ONE 7:e31618
    [Google Scholar]
88. 85.  Nagano T, Lubling Y, Stevens TJ, Schoenfelder S, Yaffe E et al. 2013. Single-cell Hi-C reveals cell-to-cell variability in chromosome structure. Nature 502:59–64
    [Google Scholar]
89. 86.  Nakanishi A, Nishino H, Watanabe H, Yokohari F, Nishikawa M 2009. Sex-specific antennal sensory system in the ant Camponotus japonicus: structure and distribution of sensilla on the flagellum. Cell Tissue Res. 338:79–97
    [Google Scholar]
90. 87.  Nijhout HF 1999. Control mechanisms of polyphenic development in insects. BioScience 49:181–92
    [Google Scholar]
91. 88.  Nijhout HF, Wheeler DE 1982. Juvenile hormone and the physiological basis of insect polymorphisms. Q. Rev. Biol. 57:109–33
    [Google Scholar]
92. 89.  Ott SR, Rogers SM 2010. Gregarious desert locusts have substantially larger brains with altered proportions compared with the solitarious phase. Proc. Biol. Sci. 277:3087–96
    [Google Scholar]
93. 90.  Oxley PR, Ji L, Fetter-Pruneda I, McKenzie SK, Li C et al. 2014. The genome of the clonal raider ant Cerapachys biroi. Curr. Biol. 24:451–58
    [Google Scholar]
94. 91.  Ozaki M, Wada-Katsumata A, Fujikawa K, Iwasaki M, Yokohari F et al. 2005. Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science 309:311–14
    [Google Scholar]
95. 92.  Paoli PP, Wakeling LA, Wright GA, Ford D 2014. The dietary proportion of essential amino acids and Sir2 influence lifespan in the honeybee. Age 36:9649
    [Google Scholar]
96. 93.  Pask GM, Slone JD, Millar JG, Das P, Moreira JA et al. 2017. Specialized odorant receptors in social insects that detect cuticular hydrocarbon cues and candidate pheromones. Nat. Commun. 8:297
    [Google Scholar]
97. 94.  Penick CA, Prager SS, Liebig J 2012. Juvenile hormone induces queen development in late-stage larvae of the ant Harpegnathos saltator. J. Insect Physiol. 58:1643–49
    [Google Scholar]
98. 95.  Peters RS, Krogmann L, Mayer C, Donath A, Gunkel S et al. 2017. Evolutionary history of the Hymenoptera. Curr. Biol. 27:1013–18
    [Google Scholar]
99. 96.  Rachinsky A, Strambi C, Strambi A, Hartfelder K 1990. Caste and metamorphosis: hemolymph titers of juvenile hormone and ecdysteroids in last instar honeybee larvae. Gen. Comp. Endocrinol. 79:31–38
    [Google Scholar]
100. 97.  Rajakumar R, San Mauro D, Dijkstra MB, Huang MH, Wheeler DE et al. 2012. Ancestral developmental potential facilitates parallel evolution in ants. Science 335:79–82
     [Google Scholar]
101. 98.  Ravi N, Sanchez-Guardado L, Lois C, Kelsch W 2017. Determination of the connectivity of newborn neurons in mammalian olfactory circuits. Cell. Mol. Life Sci. 74:849–67
     [Google Scholar]
102. 99.  Reid CR, Lutz MJ, Powell S, Kao AB, Couzin ID, Garnier S 2015. Army ants dynamically adjust living bridges in response to a cost-benefit trade-off. PNAS 112:15113–18
     [Google Scholar]
103. 99a.  Robeau RM, Vinson SB 1976. Effects of juvenile hormone analogues on caste differentiation in the imported fire ant, Solenopsis invicta. J. Georgia Entomol. Soc. 11:198–202
     [Google Scholar]
104. 100.  Robinson GE 1992. Regulation of division of labor in insect societies. Annu. Rev. Entomol. 37:637–65
     [Google Scholar]
105. 101.  Robinson GE, Page RE, Strambi C, Strambi A 1992. Colony integration in honey bees: mechanisms of behavioral reversion. Ethology 90:336–48
     [Google Scholar]
106. 102.  Deleted in proof
107. 103.  Rotem A, Ram O, Shoresh N, Sperling RA, Goren A et al. 2015. Single-cell ChIP-seq reveals cell subpopulations defined by chromatin state. Nat. Biotechnol. 33:1165–72
     [Google Scholar]
108. 104.  Sakano H 2010. Neural map formation in the mouse olfactory system. Neuron 67:530–42
     [Google Scholar]
109. 105.  Satoh A, Brace CS, Rensing N, Cliften P, Wozniak DF et al. 2013. Sirt1 extends life span and delays aging in mice through the regulation of Nk2 homeobox 1 in the DMH and LH. Cell Metab. 18:416–30
     [Google Scholar]
110. 106.  Schmid A, Chiba A, Doe CQ 1999. Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 126:4653–89
     [Google Scholar]
111. 107.  Schmitt DE, Esch HE 1993. Magnetic orientation of honeybees in the laboratory. Naturwissenschaften 80:41–43
     [Google Scholar]
112. 108.  Scholl C, Wang Y, Krischke M, Mueller MJ, Amdam GV, Rossler W 2014. Light exposure leads to reorganization of microglomeruli in the mushroom bodies and influences juvenile hormone levels in the honeybee. Dev. Neurobiol. 74:1141–53
     [Google Scholar]
113. 109.  Schulte C, Theilenberg E, Müller-Borg M, Gempe T, Beye M 2014. Highly efficient integration and expression of piggyBac-derived cassettes in the honeybee (Apis mellifera). PNAS 111:9003–8
     [Google Scholar]
114. 110.  Schwarz MP, Richards MH, Danforth BN 2007. Changing paradigms in insect social evolution: insights from halictine and allodapine bees. Annu. Rev. Entomol. 52:127–50
     [Google Scholar]
115. 111.  Sharma KR, Enzmann BL, Schmidt Y, Moore D, Jones GR et al. 2015. Cuticular hydrocarbon pheromones for social behavior and their coding in the ant antenna. Cell Rep. 12:1261–71
     [Google Scholar]
116. 112.  Shi NN, Tsai CC, Camino F, Bernard GD, Yu N, Wehner R 2015. Keeping cool: enhanced optical reflection and radiative heat dissipation in Saharan silver ants. Science 349:298–301
     [Google Scholar]
117. 113.  Shields EJ, Sheng L, Weiner AK, Garcia BA, Bonasio R 2018. High-quality genome assemblies reveal long non-coding RNAs expressed in ant brains. Cell Rep. 23:3078–90
     [Google Scholar]
118. 113a.  Shpigler H, Amsalem E, Huang ZY, Cohen M, Siegel AJ et al. 2014. Gonadotropic and physiological functions of juvenile hormone in bumblebee (Bombus terrestris) workers. PLOS ONE 9:e100650
     [Google Scholar]
119. 114.  Shpigler HY, Saul MC, Corona F, Block L, Ahmed AC et al. 2017. Deep evolutionary conservation of autism-related genes. PNAS 114:9653–58
     [Google Scholar]
120. 115.  Simola DF, Graham RJ, Brady CM, Enzmann BL, Desplan C et al. 2016. Epigenetic (re)programming of caste-specific behavior in the ant Camponotus floridanus. Science 351:aac6633
     [Google Scholar]
121. 116.  Simola DF, Ye C, Mutti NS, Dolezal K, Bonasio R et al. 2013. A chromatin link to caste identity in the carpenter ant Camponotus floridanus. Genome Res. 23:486–96
     [Google Scholar]
122. 117.  Skene PJ, Henikoff S 2017. An efficient targeted nuclease strategy for high-resolution mapping of DNA binding sites. eLife 6:e21856
     [Google Scholar]
123. 118.  Sledge MF, Boscaro F, Turillazzi S 2001. Cuticular hydrocarbons and reproductive status in the social wasp Polistes dominulus. Behav. Ecol. Sociobiol. 49:401–9
     [Google Scholar]
124. 119.  Slone JD, Pask GM, Ferguson ST, Millar JG, Berger SL et al. 2017. Functional characterization of odorant receptors in the ponerine ant, Harpegnathos saltator. PNAS 114:8586–91
     [Google Scholar]
125. 120.  Smith AR, Seid MA, Jimenez LC, Wcislo WT 2010. Socially induced brain development in a facultatively eusocial sweat bee Megalopta genalis (Halictidae). Proc. Biol. Sci. 277:2157–63
     [Google Scholar]
126. 121.  Spannhoff A, Kim YK, Raynal NJ, Gharibyan V, Su MB et al. 2011. Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. EMBO Rep. 12:238–43
     [Google Scholar]
127. 122.  Spindler SR, Hartenstein V 2010. The Drosophila neural lineages: a model system to study brain development and circuitry. Dev. Genes Evol. 220:1–10
     [Google Scholar]
128. 123.  Ståhl PL, Salmén F, Vickovic S, Lundmark A, Navarro JF et al. 2016. Visualization and analysis of gene expression in tissue sections by spatial transcriptomics. Science 353:78–82
     [Google Scholar]
129. 124.  Stieb SM, Hellwig A, Wehner R, Rossler W 2012. Visual experience affects both behavioral and neuronal aspects in the individual life history of the desert ant Cataglyphis fortis. Dev. Neurobiol. 72:729–42
     [Google Scholar]
130. 125.  Stieb SM, Muenz TS, Wehner R, Rössler W 2010. Visual experience and age affect synaptic organization in the mushroom bodies of the desert ant Cataglyphis fortis. Dev. Neurobiol. 70:408–23
     [Google Scholar]
131. 126.  Strausfeld NJ, Hansen L, Li Y, Gomez RS, Ito K 1998. Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn. Mem. 5:11–37
     [Google Scholar]
132. 127.  Tarver MR, Florane CB, Zhang D, Grimm C, Lax AR 2012. Methoprene and temperature effects on caste differentiation and protein composition in the Formosan subterranean termite, Coptotermes formosanus. J. Insect Sci. 12:18
     [Google Scholar]
133. 128.  Terrapon N, Li C, Robertson HM, Ji L, Meng X et al. 2014. Molecular traces of alternative social organization in a termite genome. Nat. Commun. 5:3636
     [Google Scholar]
134. 129.  Tissenbaum HA, Guarente L 2001. Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans. Nature 410:227–30
     [Google Scholar]
135. 130.  Trible W, Olivos-Cisneros L, McKenzie SK, Saragosti J, Chang NC et al. 2017. orco mutagenesis causes loss of antennal lobe glomeruli and impaired social behavior in ants. Cell 170:727–35.e10
     [Google Scholar]
136. 131.  Tsai L, Barnea G 2014. A critical period defined by axon-targeting mechanisms in the murine olfactory bulb. Science 344:197–200
     [Google Scholar]
137. 132.  Vinson SB, Robeau R 1974. Insect growth regulator effects on colonies of the imported fire ant. J. Econ. Entomol. 67:584–87
     [Google Scholar]
138. 133.  Vowles DM 1950. Sensitivity of ants to polarized light. Nature 165:282–83
     [Google Scholar]
139. 134.  Waddington CH 1957. The Strategy of the Genes London:George Allen–Unwin
140. 135.  Wang SC, Oelze B, Schumacher A 2008. Age-specific epigenetic drift in late-onset Alzheimer's disease. PLOS ONE 3:e2698
     [Google Scholar]
141. 136.  Wheeler DE 1986. Developmental and physiological determinants of caste in social Hymenoptera: evolutionary implications. Am. Nat. 128:13–34
     [Google Scholar]
142. 137.  Wheeler DE, Nijhout HF 1981. Soldier determination in ants: new role for juvenile hormone. Science 213:361–63
     [Google Scholar]
143. 138.  Wilson EO 1965. Chemical communication in the social insects. Science 149:1064–71
     [Google Scholar]
144. 139.  Wilson EO 1983. Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta). III. Ergonomic resiliency in foraging by A. cephalotes. Behav. Ecol. Sociobiol. 14:47–54
     [Google Scholar]
145. 140.  Wilson EO 1984. The relation between caste ratios and division of labor in the ant genus Pheidole (Hymenoptera, Formicidae). Behav. Ecol. Sociobiol. 16:89–98
     [Google Scholar]
146. 141.  Withers GS, Fahrbach SE, Robinson GE 1993. Selective neuroanatomical plasticity and division of labour in the honeybee. Nature 364:238–40
     [Google Scholar]
147. 142.  Yan H, Bonasio R, Simola DF, Liebig J, Berger SL, Reinberg D 2015. DNA methylation in social insects: how epigenetics can control behavior and longevity. Annu. Rev. Entomol. 60:435–52
     [Google Scholar]
148. 143.  Yan H, Opachaloemphan C, Mancini G, Yang H, Gallitto M et al. 2017. An engineered orco mutation produces aberrant social behavior and defective neural development in ants. Cell 170:736–47.e9
     [Google Scholar]
149. 144.  Yan H, Simola DF, Bonasio R, Liebig J, Berger SL, Reinberg D 2014. Eusocial insects as emerging models for behavioural epigenetics. Nat. Rev. Genet. 15:677–88
     [Google Scholar]
150. 145.  Yu CR, Power J, Barnea G, O'Donnell S, Brown HEV et al. 2004. Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42:553–66
     [Google Scholar]
151. 146.  Zheng GXY, Terry JM, Belgrader P, Ryvkin P, Bent ZW et al. 2017. Massively parallel digital transcriptional profiling of single cells. Nat. Commun. 8:14049
     [Google Scholar]
152. 147.  Zhou X, Rokas A, Berger SL, Liebig J, Ray A, Zwiebel LJ 2015. Chemoreceptor evolution in Hymenoptera and its implications for the evolution of eusociality. Genome Biol. Evol. 7:2407–16
     [Google Scholar]
153. 148.  Zhou X, Slone JD, Rokas A, Berger SL, Liebig J 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. 8:e1002930
     [Google Scholar]
154. 149.  Zube C, Rossler W 2008. Caste- and sex-specific adaptations within the olfactory pathway in the brain of the ant Camponotus floridanus. Arthropod Struct. Dev. 37:469–79
     [Google Scholar]