Honey bee sociogenomics: A genome-scale perspective on bee social behavior and health

Apidologie

Volumn 45, Issue 3, 2014, Pages 375-395

  Dolezal, Adam G ^a   Toth, Amy L ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

behavioral maturation; caste; comparative genomics; division of labor; genome

Indexed keywords

CASTE; COMPARATIVE STUDY; GENOME; GENOMICS; HONEYBEE; LABOR DIVISION; MATURATION; PHYSIOLOGICAL RESPONSE; SOCIAL BEHAVIOR;

EID: 84899584978     PISSN: 00448435     EISSN: 12979678     Source Type: Journal    
DOI: 10.1007/s13592-013-0251-4     Document Type: Review

References (144)

1. Alaux, C.; Robinson, G.E. (2007) Alarm pheromone induces immediate-early gene expression and slow behavioral response in honey bees. J. Chem. Ecol. 33(7), 1346-1350
2. Alaux, C.; Duong, N.; Schneider, S.S.; Southey, B.R.; Rodriguez-Zas, S.; et al. (2009a) Modulatory communication signal performance is associated with a distinct neurogenomic state in honey bees. PloS ONE 4(8), e6694. doi: 10.1371/journal.pone.0006694
3. Alaux, C.; Le Conte, Y.; Adams, H.A.; Rodriguez-Zas, S.; Grozinger, C.M.; et al. (2009b) Regulation of brain gene expression in honey bees by brood pheromone. Genes Brain Behav. 8(3), 309-319
4. Alaux, C.; Sinha, S.; Hasadsri, L.; Hunt, G.J.; Guzman-Novoa, E.; et al. (2009c) Honey bee aggression supports a link between gene regulation and behavioral evolution. Proc. Natl. Acad. Sci. U. S. A. 106(36), 15400-15405
5. Alaux, C.; Dantec, C.; Parrinello, H.; Le Conte, Y. (2011) Nutrigenomics in honey bees: Digital gene expression analysis of pollen's nutritive effects on healthy and varroa-parasitized bees. BMC Genomics 12, 496. doi: 10.1186/1471-2164-12-496
6. Amdam, G.V.; Page Jr.; R.E.; Fondrk, M.K.; Brent, C.S. (2010) Hormone response to bidirectional selection on social behavior. Evol. Dev. 12(5), 428-436
7. Ament, S.A.; Corona, M.; Pollock, H.S.; Robinson, G.E. (2008) Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proc. Natl. Acad. Sci. U. S. A. 105(11), 4226-4231
8. Ament, S.A.; Wang, Y.; Robinson, G.E. (2010) Nutritional regulation of division of labor in honey bees: toward a systems biology perspective. WIREs Syst. Biol. Med. 2(5), 566-576
9. Ament, S.A.; Blatti, C.A.; Alaux, C.; Wheeler, M.M.; Toth, A.L.; et al. (2012a) New meta-analysis tools reveal common transcriptional regulatory basis for multiple determinants of behavior. Proc. Natl. Acad. Sci. U. S. A. 109(26), E1801-E1810
10. Ament, S.A.; Wang, Y.; Chen, C.C.; Blatti, C.A.; Hong, F.; et al. (2012b) The transcription factor ultraspiracle influences honey bee social behavior and behavior-related gene expression. PloS Genet. 8(3), e1002596
11. Barchuk, A.R.; Cristino, A.S.; Kucharski, R.; Costa, L.F.; Simoes, Z.L.P.; et al. (2007) Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Dev. Biol. 7, 70. doi: 10.1186/1471-213X-7-70
12. Behura, S.K.; Whitfield, C.W. (2010) Correlated expression patterns of microRNA genes with age-dependent behavioural changes in honeybee. Insect Mol. Biol. 19(4), 431-439
13. Ben-Shahar, Y. (2005) The foraging gene, behavioral plasticity, and honeybee division of labor. J. Comp. Physiol. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 191(11), 987-994
14. Bird, A. (2007) Perceptions of epigenetics. Nature 447(7143), 396-398
15. Bonasio, R.; Li, Q.; Lian, J.; Mutti, N.S.; Jin, L.; et al. (2012) Genome-wide and caste-specific DNA methylomes of the ants Camponotus floridanus and Harpegnathos saltator. Curr. Biol. 22(19), 1755-1764
16. Cardoen, D.; Wenseleers, T.; Ernst, U.R.; Danneels, E.L.; Laget, D.; et al. (2011) Genome-wide analysis of alternative reproductive phenotypes in honeybee workers. Mol. Ecol. 20(19), 4070-4084
17. Cash, A.C.; Whitfield, C.W.; Ismail, N.; Robinson, G.E. (2005) Behavior and the limits of genomic plasticity: power and replicability in microarray analysis of honeybee brains. Genes Brain Behav. 4(4), 267-271
18. Chandrasekaran, S.; Ament, S.A.; Eddy, J.A.; Rodriguez-Zas, S.L.; Schatz, B.R.; et al. (2011) Behavior-specific changes in transcriptional modules lead to distinct and predictable neurogenomic states. Proc. Natl. Acad. Sci. U. S. A. 108(44), 18020-18025
19. Chen, K.; Rajewsky, N. (2007) The evolution of gene regulation by transcription factors and microRNAs. Nat. Rev. Genet. 8(2), 93-103
20. Chen, X.; Hu, Y.; Zheng, H.Q.; Cao, L.F.; Niu, D.F.; et al. (2012) Transcriptome comparison between honey bee queen- and worker-destined larvae. Insect Biochem. Mol. 42(9), 665-673
21. Cornman, S.R.; Schatz, M.C.; Johnston, S.J.; Chen, Y.P.; Pettis, J.; et al. (2010) Genomic survey of the ectoparasitic mite Varroa destructor, a major pest of the honey bee Apis mellifera. BMC Genomics 11, 602. doi: 10.1186/1471-2164-11-602
22. Cornman, R.S.; Tarpy, D.R.; Chen, Y.P.; Jeffreys, L.; Lopez, D.; et al. (2012) Pathogen webs in collapsing honey bee colonies. PloS ONE 7(8), e43562. doi: 10.1371/journal.pone.0043562
23. Cornman, R.S.; Boncristiani, H.; Dainat, B.; Chen, Y.P.; vanEngelsdorp, D.; et al. (2013) Population-genomic variation within RNA viruses of the Western honey bee, Apis mellifera, inferred from deep sequencing. BMC Genomics 14, 154. doi: 10.1186/1471-2164-14-154
24. Cox-Foster, D.L.; Conlan, S.; Holmes, E.C.; Palacios, G.; Evans, J.D.; et al. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318(5848), 283-287
25. Crews, D. (2008) Epigenetics and its implications for behavioral neuroendocrinology. Front. Neuroendocrinol. 29(3), 344-357
26. Cristino, A.S.; Nunes, F.M.F.; Lobo, C.H.; Bitondi, M.M.G.; Simoes, Z.L.P.; et al. (2006) Caste development and reproduction: a genome-wide analysis of hallmarks of insect eusociality. Insect Mol. Biol. 15(5), 703-714
27. Daugherty, T.H.F.; Toth, A.L.; Robinson, G.E. (2011) Nutrition and division of labor: effects on foraging and brain gene expression in the paper wasp Polistes metricus. Mol. Ecol. 20(24), 5337-5347
28. Dickman, M.J.; Kucharski, R.; Maleszka, R.; Hurd, P.J. (2013) Extensive histone post-translational modification in honey bees. Insect Biochem. Mol. 43(2), 125-137
29. Dyer, F.C. (2002) The biology of the dance language. Annu.Rev. Entomol. 47, 917-949
30. Edgar, B.A. (2006) How flies get their size: genetics meets physiology. Nat. Rev. Genet. 7(12), 907-916
31. Elsik, C.G.; Mackey, A.J.; Reese, J.T.; Milshina, N.V.; Roos, D.S.; et al. (2007) Creating a honey bee consensus gene set. Genome Biol 8(1)
32. Engel, P.; Martinson, V.G.; Moran, N.A. (2012) Functional diversity within the simple gut microbiota of the honey bee. Proc. Natl. Acad. Sci. U. S. A. 109(27), 11002-11007
33. Erickson, D.L.; Fenster, C.B.; Stenoien, H.K.; Price, D. (2004) Quantitative trait locus analyses and the study of evolutionary process. Mol. Ecol. 13(9), 2505-2522
34. Evans, J.D.; Schwarz, R.S. (2011) Bees brought to their knees: microbes affecting honey bee health. Trends Microbiol. 19(12), 614-620
35. Evans, J.D.; Wheeler, D.E. (2001) Expression profiles during honeybee caste determination. Genome Biol. 2(1), research0001.1-research0001.6.
36. Evans, J.D.; Aronstein, K.; Chen, Y.P.; Hetru, C.; Imler, J.L.; et al. (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 15(5), 645-656
37. Ferreira, P.G.; Patalano, S.; Chauhan, R.; Ffrench-Constant, R.; Gabaldon, T.; et al. (2013) Transcriptome analyses of primitively eusocial wasps reveal novel insights into the evolution of sociality and the origin of alternative phenotypes. Genome Biol. 14(2), R20
38. Fischman, B.J.; Woodard, S.H.; Robinson, G.E. (2011) Molecular evolutionary analyses of insect societies. Proc. Natl. Acad. Sci. U. S. A. 108, 10847-10854
39. Flores, K.; Wolschin, F.; Corneveaux, J.J.; Allen, A.N.; Huentelman, M.J.; et al. (2012) Genome-wide association between DNA methylation and alternative splicing in an invertebrate. Bmc Genomics 13, 480. doi: 10.1186/1471-2164-13-480
40. Foret, S.; Maleszka, R. (2006) Function and evolution of a gene family encoding odorant binding-like proteins in a social insect, the honey bee (Apis mellifera). Genome Res. 16(11), 1404-1413
41. Foret, S.; Wanner, K.W.; Maleszka, R. (2007) Chemosensory proteins in the honey bee: insights from the annotated genome, comparative analyses and expressional profiling. Insect Biochem. Mol. Biol. 37(1), 19-28
42. Foret, S.; Kucharski, R.; Pellegrini, M.; Feng, S.H.; Jacobsen, S.E.; et al. (2012) DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees. Proc. Natl. Acad. Sci. U. S. A. 109(13), 4968-4973
43. Gallai, N.; Salles, J.M.; Settele, J.; Vaissiere, B.E. (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68(3), 810-821
44. Gempe, T.; Stach, S.; Bienefeld, K.; Beye, M. (2012) Mixing of honeybees with different genotypes affects individual worker behavior and transcription of genes in the neuronal substrate. PloS ONE 7(2), e31653. doi: 10.1371/journal.pone.0031653
45. Gerhold, D.; Caskey, C.T. (1996) It's the genes! EST access to human genome content. Bioessays 18(12), 973-981
46. Gotzek, D.; Ross, K.G. (2007) Genetic regulation of colony social organization in fire ants: an integrative overview. Q. Rev. Biol. 82(3), 201-226
47. Gotzek, D.; Ross, K.G. (2009) Current status of a model system: the gene Gp-9 and its association with social organization in fire ants. PloS ONE 4(11), e7713. doi: 10.1371/journal.pone.0007713
48. Graham, A.M.; Munday, M.D.; Kaftanoglu, O.; Page, R.E.; Amdam, G.V.; et al. (2011) Support for the reproductive ground plan hypothesis of social evolution and major QTL for ovary traits of Africanized worker honey bees (Apis mellifera L.). BMC Evol. Biol. 11, 95. doi: 10.1186/1471-2148-11-95
49. Greenberg, J.K.; Xia, J.; Zhou, X.; Thatcher, S.R.; Gu, X.; et al. (2012) Behavioral plasticity in honey bees is associated with differences in brain microRNA transcriptome. Genes Brain Behav. 11(6), 660-670
50. Grozinger, C.M.; Robinson, G.E. (2002) Microarray analysis of pheromone-mediated gene expression in the honey bee brain. Integr. Comp. Biol. 42(6), 1237
51. Grozinger, C.M.; Robinson, G.E. (2007) Endocrine modulation of a pheromone-responsive gene in the honey bee brain. J. Comp. Physiol. A. 193(4), 461-470
52. Grozinger, C.M.; Sharabash, N.M.; Whitfield, C.W.; Robinson, G.E. (2003) Pheromone-mediated gene expression in the honey bee brain. Proc. Natl. Acad. Sci. U. S. A. 100, 14519-14525
53. Hartfelder, K. (2000) Insect juvenile hormone: from "status quo" to high society. Braz. J. Med. Biol. Res. 33, 157-177
54. Herb, B.R.; Wolschin, F.; Hansen, K.D.; Aryee, M.J.; Langmead, B.; et al. (2012) Reversible switching between epigenetic states in honeybee behavioral subcastes. Nat. Neurosci. 15(10), 1371-1373
55. Hernandez, L.G.; Lu, B.W.; da Cruz, G.C.N.; Calabria, L.K.; Martins, N.F.; et al. (2012) Worker honeybee brain proteome. J. Proteome Res. 11(3), 1485-1493
56. Hogeweg, P. (2011) The roots of bioinformatics in theoretical biology. PloS Comput. Biol. 7(3), e1002021. doi: 10.1371/journal.pcbi.1002021
57. Hunt, G.J.; Page, R.E.; Fondrk, M.K.; Dullum, C.J. (1995) Major quantitative trait loci affecting honey-bee foraging behavior. Genetics 141(4), 1537-1545
58. Hunt, G.J.; Guzman-Novoa, E.; Fondrk, M.K.; Page, R.E. (1998) Quantitative trait loci for honey bee stinging behavior and body size. Genetics 148(3), 1203-1213
59. Hunt, G.J.; Amdam, G.V.; Schlipalius, D.; Emore, C.; Sardesai, N.; et al. (2007) Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften 94(4), 247-267
60. Hunt, B.G.; Wyder, S.; Elango, N.; Werren, J.H.; Zdobnov, E.M.; et al. (2010) Sociality is linked to rates of protein evolution in a highly social insect. Mol. Biol. Evol. 27(3), 497-500
61. Johnson, B.R.; Tsutsui, N.D. (2011) Taxonomically restricted genes are associated with the evolution of sociality in the honey bee. Bmc Genomics 12, 164. doi: 10.1186/1471-2164-12-164
62. Johnson, R.M.; Evans, J.D.; Robinson, G.E.; Berenbaum, M.R. (2009) Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera). Proc. Natl. Acad. Sci. U. S. A. 106(35), 14790-14795
63. Kamakura, M. (2011) Royalactin induces queen differentiation in honeybees. Nature 473(7348), 478-483
64. Keller, L.; Ross, K.G. (1999) Major gene effects on phenotype and fitness: the relative roles of Pgm-3 and Gp-9 in introduced populations of the fire ant Solenopsis invicta. J. Evol. Biol. 12(4), 672-680
65. Kocher, S.D.; Richard, F.J.; Tarpy, D.R.; Grozinger, C.M. (2008) Genomic analysis of post-mating changes in the honey bee queen (Apis mellifera). Bmc Genomics 9, 232. doi: 10.1186/1471-2164-9-232
66. Kocher, S.D.; Ayroles, J.F.; Stone, E.A.; Grozinger, C.M. (2010a) Individual variation in pheromone response correlates with reproductive traits and brain gene expression in worker honey bees. PloS ONE 5(2), e9116. doi: 10.1371/journal.pone.0009116
67. Kocher, S.D.; Tarpy, D.R.; Grozinger, C.M. (2010b) The effects of mating and instrumental insemination on queen honey bee flight behaviour and gene expression. Insect Mol. Biol. 19(2), 153-162
68. Kronforst, M.R.; Gilley, D.C.; Strassmann, J.E.; Queller, D.C. (2008) DNA methylation is widespread across social Hymenoptera. Current Biology 18(7): R287-R288.
69. Kucharski, R.; Maleszka, R. (2002) Evaluation of differential gene expression during behavioral development in the honeybee using microarrays and northern blots. Genome Biol. 3(2), RESEARCH0007.
70. Kucharski, R.; Maleszka, J.; Foret, S.; Maleszka, R. (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science 319(5871), 1827-1830
71. Le Conte, Y.; Hefetz, A. (2008) Primer pheromones in social hymenoptera. Annu. Rev. Entomol. 53, 523-542
72. Le Conte, Y.; Mohammedi, A.; Robinson, G.E. (2001) Primer effects of a brood pheromone on honeybee behavioural development. Proc. R. Soc. B.: Biol. Sci. 268(1463), 163-168
73. Le Conte, Y.; Alaux, C.; Martin, J.F.; Harbo, J.R.; Harris, J.W.; et al. (2011) Social immunity in honeybees (Apis mellifera): transcriptome analysis of Varroa-hygienic behaviour. Insect Mol. Biol. 20(3), 399-408
74. Liang, Z.Z.S.; Nguyen, T.; Mattila, H.R.; Rodriguez-Zas, S.L.; Seeley, T.D.; et al. (2012) Molecular determinants of scouting behavior in honey bees. Science 335(6073), 1225-1228
75. Linksvayer, T.A.; Rueppell, O.; Siegel, A.; Kaftanoglu, O.; Page, R.E.; et al. (2009) The genetic basis of transgressive ovary size in honeybee workers. Genetics 183(2), 693-707
76. Liu, F.; Peng, W.; Li, Z.; Li, W.; Li, L.; et al. (2012) Next-generation small RNA sequencing for microRNAs profiling in Apis mellifera: comparison between nurses and foragers. Insect Mol. Biol. 21(3), 297-303
77. Lobo, N.F.; Ton, L.Q.; Hill, C.A.; Emore, C.; Romero-Severson, J.; et al. (2003) Genomic analysis in the sting-2 quantitative trait locus for defensive behavior in the honey bee, Apis mellifera. Genome Res. 13(12), 2588-2593
78. Lutz, C.C.; Rodriguez-Zas, S.L.; Fahrbach, S.E.; Robinson, G.E. (2012) Transcriptional response to foraging experience in the honey bee mushroom bodies. Dev. Neurobiol. 72(2), 153-166
79. Lyko, F.; Foret, S.; Kucharski, R.; Wolf, S.; Falckenhayn, C.; et al. (2010) The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PloS Biol. 8(11), e1000506. doi: 10.1371/journal.pbio.1000506
80. McClung, C.A.; Nestler, E.J. (2008) Neuroplasticity mediated by altered gene expression. Neuropsychopharmacol: Off. Publ. Am. Coll. Neuropsychopharmacol. 33(1), 3-17
81. Mullin, C.A.; Frazier, M.; Frazier, J.L.; Ashcraft, S.; Simonds, R.; et al. (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PloS ONE 5(3), e9754. doi: 10.1371/journal.pone.0009754
82. Naug, D. (2009) Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biol. Conserv. 142(10), 2369-2372
83. Navajas, M.; Migeon, A.; Alaux, C.; Martin-Magniette, M.L.; Robinson, G.E.; et al. (2008) Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection. BMC Genomics 9, 301. doi: 10.1186/1471-2164-9-301
84. Nelson, F.C. (1927) Adaptability of young bees under adverse conditions. Am. Bee J. 67, 242-243
85. Nelson, C.M.; Ihle, K.; Amdam, G.V.; Fondrk, M.K.; Page, R.E. (2007) The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biol. 5, 673-677
86. Ometto, L.; Shoemaker, D.; Ross, K.G.; Keller, L. (2011) Evolution of gene expression in fire ants: the effects of developmental stage, caste, and species. Mol. Biol. Evol. 28(4), 1381-1392
87. Oxley, P.R.; Thompson, G.J.; Oldroyd, B.P. (2008) Four quantitative trait loci that influence worker sterility in the honeybee (Apis mellifera). Genetics 179(3), 1337-1343
88. Oxley, P.R.; Spivak, M.; Oldroyd, B.P. (2010) Six quantitative trait loci influence task thresholds for hygienic behaviour in honeybees (Apis mellifera). Mol. Ecol. 19(7), 1452-1461
89. Page, R.E.; Fondrk, M.K. (1995) The effects of colony level selection on the social-organization of honey-bee (Apis mellifera L) colonies - colony level components of pollen hoarding. Behav. Ecol. Sociobiol. 36(2), 135-144
90. Page, R.E.; Rueppell, O.; Amdam, G.V. (2012) Genetics of reproduction and regulation of honeybee (Apis mellifera L.) social behavior. Annu. Rev. Genet. 46, 97-119
91. Pankiw, T.; Huang, Z.Y.; Winston, M.L.; Robinson, G.E. (1998) Queen mandibular gland pheromone influences worker honey bee (Apis mellifera L.) foraging ontogeny and juvenile hormone titers. J. Insect Physiol. 44(7-8), 685-692
92. Pelosi, P.; Calvello, M.; Ban, L.P. (2005) Diversity of odorant-binding proteins and chemosensory proteins in insects. Chem. Senses 30, I291-I292
93. Qiu, P.; Pan, P.C.; Govind, S. (1998) A role for the Drosophila Toll/Cactus pathway in larval hematopoiesis. Development 125(10), 1909-1920
94. Rachinsky, A.; Hartfelder, K. (1990) Corpora allata activity, a prime regulating element for caste-specific juvenile hormone titre in honey bee larvae (Apis mellifera carnica). J. Insect Physiol. 36, 189-194
95. Rembold, H. (1987) Caste specific modulation of juvenile hormone titers in Apis mellifera. Insect Biochem. 17, 1003-1006
96. Rembold, H.; Czoppelt, C.; Rao, P.J. (1974) Effect of juvenile-hormone treatment on caste differentiation in honeybee, Apis mellifera. J. Insect Physiol. 20(7), 1193-1202
97. Richard, F.J.; Holt, H.L.; Grozinger, C.M. (2012) Effects of immunostimulation on social behavior, chemical communication and genome-wide gene expression in honey bee workers (Apis mellifera). BMC Genomics 13, 558
98. Robinson, G.E. (1987) Regulation of honey bee age polyethism by juvenile hormone. Behav. Ecol. Sociobiol. 20, 329-338
99. Robinson, G.E. (1992) Regulation of division of labor in insect societies. Annu. Rev. Entomol. 37, 637-665
100. Robinson, G.E. (1999) Integrative animal behaviour and sociogenomics. Trends Ecol. Evol. 14(5), 202-205
101. Robinson, G.E. (2002) Genomics and integrative analyses of division of labor in honeybee colonies. Am. Nat. 160, S160-S172
102. Robinson, G.E.; Page, R.E.; Strambi, C.; Strambi, A. (1989) Hormonal and genetic-control of behavioral integration in honey bee colonies. Science 246(4926), 109-111
103. Robinson, G.E.; Grozinger, C.M.; Whitfield, C.W. (2005) Sociogenomics: social life in molecular terms. Nat. Rev. Genet. 6(4), 257-270
104. Rosenkranz, P.; Aumeier, P.; Ziegelmann, B. (2010) Biology and control of Varroa destructor. J. Invertebr. Pathol. 103, S96-S119
105. Rothenbuhler, W.C. (1964) Behaviour genetics of nest cleaning in honey bees. I. Responses of 4 inbred lines to disease-killed brood. Anim. Behav. 12(4), 578
106. Rueppell, O. (2013) The architecture of the pollen hoarding syndrome in honey bees: implications for understanding social evolution, behavioral syndromes, and selective breeding. Apidologie. doi: 10.1007/s13592-013-0244-3 (this issue)
107. Schena, M.; Shalon, D.; Davis, R.W.; Brown, P.O. (1995) Quantitative monitoring of gene-expression patterns with a complementary-DNA microarray. Science 270(5235), 467-470
108. Schneider, S.S.; Lewis, L.A. (2004) The vibration signal, modulatory communication and the organization of labor in honey bees, Apis mellifera. Apidologie 35(2), 117-131
109. Seeley, T.D. (1985) Honeybee ecology: a study of adaptation in social life. Princeton University Press, Princeton
110. Sen Sarma, M.; Whitfield, C.W.; Robinson, G.E. (2007) Species differences in brain gene expression profiles associated with adult behavioral maturation in honey bees. BMC Genomics 8, 202.
111. Sen Sarma, M.; Rodriguez-Zas, S.L.; Hong, F.; Zhong, S.; Robinson, G.E. (2009) Transcriptomic profiling of central nervous system regions in three species of honey bee during dance communication behavior. PloS ONE 4(7)
112. Sen Sarma, M.; Rodriguez-Zas, S.L.; Gernat, T.; Nguyen, T.; Newman, T.; et al. (2010) Distance-responsive genes found in dancing honey bees. Genes Brain Behav. 9(7), 825-830
113. Sinha, S.; Ling, X.; Whitfield, C.W.; Zhai, C.X.; Robinson, G.E. (2006) Genome scan for cis-regulatory DNA motifs associated with social behavior in honey bees. Proc. Natl. Acad. Sci. U. S. A. 103(44), 16352-16357
114. Smith, C.R.; Toth, A.L.; Suarez, A.V.; Robinson, G.E. (2008) Genetic and genomic analyses of the division of labour in insect societies. Nat. Rev. Genet. 9(10), 735-748
115. Smith, C.R.; Mutti, N.S.; Jasper, W.C.; Naidu, A.; Smith, C.D.; et al. (2012) Patterns of DNA methylation in development, division of labor and hybridization in an ant with genetic caste determination. PloS ONE 7(8), e42433. doi: 10.1371/journal.pone.0042433
116. Sullivan, J.P.; Jassim, O.; Fahrbach, S.E.; Robinson, G.E. (2000) Juvenile hormone paces behavioral development in the adult worker honey bee. Hormon. Behav. 37, 1-14
117. Sumner, S.; Pereboom, J.J.M.; Jordan, W.C. (2006) Differential gene expression and phenotypic plasticity in behavioural castes of the primitively eusocial wasp, Polistes canadensis. Proc. R. Soc. B.: Biol. Sci. 273(1582), 19-26
118. Thompson, G.J.; Kucharski, R.; Maleszka, R.; Oldroyd, B.P. (2006) Towards a molecular definition of worker sterility: differential gene expression and reproductive plasticity in honey bees. Insect Mol. Biol. 15(5), 637-644
119. Thompson, G.J.; Kucharski, R.; Maleszka, R.; Oldroyd, B.P. (2008) Genome-wide analysis of genes related to ovary activation in worker honey bees. Insect Mol. Biol. 17(6), 657-665
120. Toth, A.L.; Robinson, G.E. (2005) Worker nutrition and division of labour in honeybees. Anim. Behav. 69, 427-435
121. Toth, A.L.; Robinson, G.E. (2007) Evo-devo and the evolution of social behavior. Trends Genet. 23(7), 334-341
122. Toth, A.L.; Kantarovich, S.; Meisel, A.F.; Robinson, G.E. (2005) Nutritional status influences socially regulated foraging ontogeny in honey bees. J. Exp. Biol. 208(24), 4641-4649
123. Toth, A.L.; Varala, K.; Henshaw, M.T.; Rodriguez-Zas, S.L.; Hudson, M.E.; et al. (2010) Brain transcriptomic analysis in paper wasps identifies genes associated with behaviour across social insect lineages. Proc. R. Soc. B.: Biol. Sci. 277(1691), 2139-2148
124. Tu, M.P.; Yin, C.M.; Tatar, M. (2005) Mutations in insulin signaling pathway alter juvenile hormone synthesis in Drosophila melanogaster. Gen. Comp. Endocrinol. 142(3), 347-356
125. Viljakainen, L.; Evans, J.D.; Hasselmann, M.; Rueppell, O.; Tingek, S.; et al. (2009) Rapid evolution of immune proteins in social insects. Mol. Biol. Evol. 26(8), 1791-1801
126. Wang, Z.; Gerstein, M.; Snyder, M. (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10(1), 57-63
127. Wang, Y.; Kocher, S.D.; Linksvayer, T.A.; Grozinger, C.M.; Page, R.E.; et al. (2012) Regulation of behaviorally associated gene networks in worker honey bee ovaries. J. Exp. Biol. 215(1), 124-134
128. Wang, J.; Wurm, Y.; Nipitwattanaphon, M.; Riba-Grognuz, O.; Huang, Y.C.; et al. (2013) A Y-like social chromosome causes alternative colony organization in fire ants. Nature 493(7434), 664-668
129. Weaver, D.B.; Anzola, J.M.; Evans, J.D.; Reid, J.G.; Reese, J.T.; et al. (2007) Computational and transcriptional evidence for microRNAs in the honey bee genome. Genome Biol. 8(6), R97.
130. Weiner, S.A.; Galbraith, D.A.; Adams, D.C.; Valenzuela, N.; Noll, F.B.; et al. (2013) A survey of DNA methylation across social insect species, lifestages, and castes reveals abundant and caste-associated methylation in a primitively social wasp. Naturwissenschaften 100(8), 795-799. doi: 10.1007/s00114-013-1064-z
131. Weinstock, G.M.; Robinson, G.E.; Gibbs, R.A.; Weinstock, G.M.; Weinstock, G.M.; et al. (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443(7114), 931-949
132. Wheeler, D.E.; Buck, N.; Evans, J.D. (2006) Expression of insulin pathway genes during the period of caste determination in the honey bee, Apis mellifera. Insect Mol. Biol. 15(5), 597-602
133. Whitfield, C.W.; Band, M.R.; Bonaldo, M.F.; Kumar, C.G.; Liu, L.; et al. (2002) Annotated expressed sequence tags and cDNA microarrays for studies of brain and behavior in the honey bee. Genome Res. 12(4), 555-566
134. Whitfield, C.W.; Cziko, A.M.; Robinson, G.E. (2003) Gene expression profiles in the brain predict behavior in individual honey bees. Science 302(5643), 296-299
135. Whitfield, C.W.; Ben-Shahar, Y.; Brillet, C.; Leoncini, I.; Crauser, D.; et al. (2006) Genomic dissection of behavioral maturation in the honey bee. Proc. Natl. Acad. Sci. U. S. A. 103(44), 16068-16075
136. Wilson, E.O. (1971) The insect societies. Belknap Press of Harvard University Press, Cambridge
137. Wilson-Rich, N.; Spivak, M.; Fefferman, N.H.; Starks, P.T. (2009) Genetic, individual, and group facilitation of disease resistance in insect societies. Annu. Rev. Entomol. 54, 405-423
138. Winston, M.L. (1987) The biology of the honey bee. Harvard University Press, Cambridge
139. Winston, M.L.; Slessor, K.N. (1998) Honey bee primer pheromones and colony organization: gaps in our knowledge. Apidologie 29(1-2), 81-95
140. Wolschin, F.; Amdam, G.V. (2007) Plasticity and robustness of protein patterns during reversible development in the honey bee (Apis mellifera). Anal. Bioanal. Chem. 389(4), 1095-1100
141. Woodard, S.H.; Fischman, B.J.; Venkat, A.; Hudson, M.E.; Varala, K.; et al. (2011) Genes involved in convergent evolution of eusociality in bees. Proc. Natl. Acad. Sci. U. S. A. 108(18), 7472-7477
142. Wray, G.A. (2007) The evolutionary significance of cis-regulatory mutations. Nat. Rev. Genet. 8(3), 206-216
143. Wurm, Y.; Wang, J.; Riba-Grognuz, O.; Corona, M.; Nygaard, S.; et al. (2011) The genome of the fire ant Solenopsis invicta. Proc. Natl. Acad. Sci. U. S. A. 108(14), 5679-5684
144. Zhang, Y.; Liu, X.J.; Zhang, W.Q.; Han, R.C. (2010) Differential gene expression of the honey bees Apis mellifera and A. cerana induced by Varroa destructor infection. J. Insect Physiol. 56(9), 1207-1218