1932

Abstract

The study of insect social behavior has offered tremendous insight into the molecular mechanisms mediating behavioral and phenotypic plasticity. Genomic applications to the study of eusocial insect species, in particular, have led to several hypotheses for the processes underlying the molecular evolution of behavior. Advances in understanding the genetic control of social organization have also been made, suggesting an important role for supergenes in the evolution of divergent behavioral phenotypes. Intensive study of social phenotypes across species has revealed that behavior and caste are controlled by an interaction between genetic and environmentally mediated effects and, further, that gene expression and regulation mediate plastic responses to environmental signals. However, several key methodological flaws that are hindering progress in the study of insect social behavior remain. After reviewing the current state of knowledge, we outline ongoing challenges in experimental design that remain to be overcome in order to advance the field.

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2017-11-27
2024-05-21
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Literature Cited

  1. Adkins-Regan E. 1.  2005. Hormones and Animal Social Behavior Princeton, NJ: Princeton Univ. Press
  2. Akçay E, Linksvayer TA, Van Cleve J. 2.  2015. Bridging social evolution theory and emerging empirical approaches to social behavior. Curr. Opin. Behav. Sci 6:59–64 [Google Scholar]
  3. Amdam GV, Csondes A, Fondrk MK, Page RE. 3.  2006. Complex social behaviour derived from maternal reproductive traits. Nature 439:76–78 [Google Scholar]
  4. Amdam GV, Norberg K, Fondrk MK, Page RE. 4.  2004. Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. PNAS 101:11350–55 [Google Scholar]
  5. Amdam GV, Page RE. 5.  2010. The developmental genetics and physiology of honeybee societies. Anim. Behav 79:973–80 [Google Scholar]
  6. Ament SA, Corona M, Pollock HS, Robinson GE. 6.  2008. Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. PNAS 105:4226–31 [Google Scholar]
  7. Ament SA, Velarde RA, Kolodkin MH, Moyse D, Robinson GE. 7.  2011. Neuropeptide Y-like signalling and nutritionally mediated gene expression and behaviour in the honey bee. Insect Mol. Biol 20:335–45 [Google Scholar]
  8. Ament SA, Wang Y, Robinson GE. 8.  2010. Nutritional regulation of division of labor in honey bees: toward a systems biology perspective. Wiley Interdiscip. Rev. Syst. Biol. Med 2:566–76 [Google Scholar]
  9. Anstey ML, Rogers SM, Ott SR, Burrows M, Simpson SJ. 9.  2009. Serotonin mediates behavioral gregarization underlying swarm formation in desert locusts. Science 323:627–30 [Google Scholar]
  10. Ashok M, Turner C, Wilson TG. 10.  1998. Insect juvenile hormone resistance gene homology with the bHLH-PAS family of transcriptional regulators. PNAS 95:2761–66 [Google Scholar]
  11. Barchuk AR, Bitondi MMG, Simões ZLP. 11.  2002. Effects of juvenile hormone and ecdysone on the timing of vitellogenin appearance in hemolymph of queen and worker pupae of Apis mellifera. J. Insect Sci 2:1 [Google Scholar]
  12. Ben-Shahar Y, Dudek NL, Robinson GE. 12.  2004. Phenotypic deconstruction reveals involvement of manganese transporter malvolio in honey bee division of labor. J. Exp. Biol 207:3281–88 [Google Scholar]
  13. Ben-Shahar Y, Leung HT, Pak WL, Sokolowski MB, Robinson GE. 13.  2003. cGMP-dependent changes in phototaxis: a possible role for the foraging gene in honey bee division of labor. J. Exp. Biol. 206:2507–15 [Google Scholar]
  14. Ben-Shahar Y, Robichon A, Sokolowski MB, Robinson GE. 14.  2002. Influence of gene action across different time scales on behavior. Science 296:741–44 [Google Scholar]
  15. Berens AJ, Hunt JH, Toth AL. 15.  2015. Comparative transcriptomics of convergent evolution: Different genes but conserved pathways underlie caste phenotypes across lineages of eusocial insects. Mol. Biol. Evol 32:690–703 [Google Scholar]
  16. Bernhard Kraus F, Gerecke E, Moritz RFA. 16.  2011. Shift work has a genetic basis in honeybee pollen foragers (Apis mellifera L.). Behav. Genet 41:323–28 [Google Scholar]
  17. Bloch G, Borst DW, Huang Z-Y, Robinson GE, Cnaani J, Hefetz A. 17.  2000. Juvenile hormone titers, juvenile hormone biosynthesis, ovarian development and social environment in Bombus terrestris. J. Insect Physiol 46:47–57 [Google Scholar]
  18. Bloch G, Shpigler H, Wheeler DE, Robinson GE. 18.  2009. Endocrine influences on the organization of insect societies. Hormones, Brain and Behavior, Vol. 1 DW Pfaff, AP Arnold, AM Etgen, SE Fahrbach, RT Rubin 1027–68 San Diego: Academic Press, 2nd ed.. [Google Scholar]
  19. Blomberg SP, Garland T, Ives AR. 19.  2003. Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution 57:717–45 [Google Scholar]
  20. Bomtorin AD, Mackert A, Rosa GCC, Moda LM, Martins JR. 20.  et al. 2014. Juvenile hormone biosynthesis gene expression in the corpora allata of honey bee (Apis mellifera L.) female castes. PLOS ONE 9:e86923 [Google Scholar]
  21. Bonasio R, Li Q, Lian J, Mutti NS, Jin L. 21.  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]
  22. Bonasio R, Zhang G, Ye C, Mutti NS, Fang X. 22.  et al. 2010. Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329:1068–71 [Google Scholar]
  23. Brian MV. 23.  1963. Studies of caste differentiation in Myrmica rubra L. Insectes Sociaux 10:91–102 [Google Scholar]
  24. Cahan SH, Parker JD, Rissing SW, Johnson RA, Polony TS. 24.  et al. 2002. Extreme genetic differences between queens and workers in hybridizing Pogonomyrmex harvester ants. Proc. R. Soc. B 269:1871–77 [Google Scholar]
  25. Cameron RC, Duncan EJ, Dearden PK. 25.  2013. Biased gene expression in early honeybee larval development. BMC Genom 14:903 [Google Scholar]
  26. Cassill DL, Tschinkel WR. 26.  2000. Behavioral and developmental homeostasis in the fire ant. Solenopsis invicta. J. Insect Physiol 46:933–39 [Google Scholar]
  27. Chandrasekaran S, Ament SA, Eddy JA, Rodriguez-Zas SL, Schatz BR. 27.  et al. 2011. Behavior-specific changes in transcriptional modules lead to distinct and predictable neurogenomic states. PNAS 108:18020–25 [Google Scholar]
  28. Chen X, Hu Y, Zheng H, Cao L, Niu D. 28.  et al. 2012. Transcriptome comparison between honey bee queen- and worker-destined larvae. Insect Biochem. Mol. Biol 42:665–73 [Google Scholar]
  29. Cnaani J, Borst DW, Huang Z-Y, Robinson GE, Hefetz A. 29.  1997. Caste determination in Bombus terrestris: differences in development and rates of JH biosynthesis between queen and worker larvae. J. Insect Physiol 43:373–81 [Google Scholar]
  30. Constant N, Santorelli LA, Lopes JFS, Hughes WOH. 30.  2012. The effects of genotype, caste, and age on foraging performance in leaf-cutting ants. Behav. Ecol 23:1284–88 [Google Scholar]
  31. Corona M, Libbrecht R, Wheeler DE. 31.  2016. Molecular mechanisms of phenotypic plasticity in social insects. Curr. Opin. Insect Sci 13:55–60 [Google Scholar]
  32. Corona M, Libbrecht R, Wurm Y, Riba-Grognuz O, Studer RA, Keller L. 32.  2013. Vitellogenin underwent subfunctionalization to acquire caste and behavioral specific expression in the harvester ant Pogonomyrmex barbatus. PLOS Genet 9:e1003730 [Google Scholar]
  33. Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y. 33.  et al. 2007. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. PNAS 104:7128–33 [Google Scholar]
  34. Costa JT. 34.  1997. Caterpillars as social insects: Largely unrecognized, the gregarious behavior of caterpillars is changing the way entomologists think about social insects. American Scientist March–April 150–59
  35. Costa JT. 35.  2006. The Other Insect Societies Cambridge, MA: Harvard Univ. Press
  36. Crespi BJ. 36.  1992. Eusociality in Australian gall thrips. Nature 359:724–26 [Google Scholar]
  37. Danforth BN. 37.  2013. Social insects: Are ants just wingless bees?. Curr. Biol 23:R1011–12 [Google Scholar]
  38. de Azevedo SV, Hartfelder K. 38.  2008. The insulin signaling pathway in honey bee (Apis mellifera) caste development—differential expression of insulin-like peptides and insulin receptors in queen and worker larvae. J. Insect Physiol 54:1064–71 [Google Scholar]
  39. Dolezal AG, Brent CS, Hölldobler B, Amdam GV. 39.  2012. Worker division of labor and endocrine physiology are associated in the harvester ant, Pogonomyrmex californicus. J. Exp. Biol 215:454–60 [Google Scholar]
  40. Dolezal AG, Johnson J, Hölldobler B, Amdam GV. 40.  2013. Division of labor is associated with age-independent changes in ovarian activity in Pogonomyrmex californicus harvester ants. J. Insect Physiol 59:519–24 [Google Scholar]
  41. Eggert A-K, Reinking M, Müller JK. 41.  1998. Parental care improves offspring survival and growth in burying beetles. Anim. Behav 55:97–107 [Google Scholar]
  42. Eyer P-A, Freyer J, Aron S. 42.  2013. Genetic polyethism in the polyandrous desert ant Cataglyphis cursor. Behav. Ecol 24:144–51 [Google Scholar]
  43. Fischer EK, O'Connell LA. 43.  2017. Modification of feeding circuits in the evolution of social behavior. J. Exp. Biol 220:92–102 [Google Scholar]
  44. Foret S, Kucharski R, Pellegrini M, Feng S, Jacobsen SE. 44.  et al. 2012. DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees. PNAS 109:4968–73 [Google Scholar]
  45. Fournier D, Estoup A, Orivel J, Foucaud J, Jourdan H. 45.  et al. 2005. Clonal reproduction by males and females in the little fire ant. Nature 435:1230–34 [Google Scholar]
  46. Glastad KM, Hunt BG, Yi SV, Goodisman MAD. 46.  2014. Epigenetic inheritance and genome regulation: Is DNA methylation linked to ploidy in haplodiploid insects?. Proc. R. Soc. B 281:20140411 [Google Scholar]
  47. Grüter C, Menezes C, Imperatriz-Fonseca VL, Ratnieks FLW. 47.  2012. A morphologically specialized soldier caste improves colony defense in a neotropical eusocial bee. PNAS 109:1182–86 [Google Scholar]
  48. Harpur BA, Kent CF, Molodtsova D, Lebon JMD, Alqarni AS. 48.  et al. 2014. Population genomics of the honey bee reveals strong signatures of positive selection on worker traits. PNAS 111:2614–19 [Google Scholar]
  49. Hecker M, Lambeck S, Toepfer S, van Someren E, Guthke R. 49.  2009. Gene regulatory network inference: data integration in dynamic models—a review. Biosystems 96:86–103 [Google Scholar]
  50. Herb BR, Wolschin F, Hansen KD, Aryee MJ, Langmead B. 50.  et al. 2012. Reversible switching between epigenetic states in honeybee behavioral subcastes. Nat. Neurosci 15:1371–73 [Google Scholar]
  51. Hofmann HA, Beery AK, Blumstein DT, Couzin ID, Earley RL. 51.  et al. 2014. An evolutionary framework for studying mechanisms of social behavior. Trends Ecol. Evol 29:581–89 [Google Scholar]
  52. Hölldobler B, Wilson EO. 52.  1990. The Ants Cambridge, MA: Belknap Press/Harvard Univ. Press
  53. Hoyer SC, Liebig J, Rössler W. 53.  2005. Biogenic amines in the ponerine ant Harpegnathos saltator: serotonin and dopamine immunoreactivity in the brain. Arthropod Struct. Dev 34:429–40 [Google Scholar]
  54. Hughes WOH, Boomsma JJ. 54.  2008. Genetic royal cheats in leaf-cutting ant societies. PNAS 105:5150–53 [Google Scholar]
  55. Hughes WOH, Sumner S, Van Borm S, Boomsma JJ. 55.  2003. Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants. PNAS 100:9394–97 [Google Scholar]
  56. Ingram KK, Gordon DM, Friedman DA, Greene M, Kahler J. 56.  et al. 2016. Context-dependent expression of the foraging gene in field colonies of ants: the interacting roles of age, environment and task. Proc. R. Soc. B 283:20160841 [Google Scholar]
  57. Ingram KK, Oefner P, Gordon DM. 57.  2005. Task-specific expression of the foraging gene in harvester ants. Mol. Ecol 14:813–18 [Google Scholar]
  58. Jasper WC, Linksvayer TA, Atallah J, Friedman D, Chiu JC, Johnson BR. 58.  2015. Large-scale coding sequence change underlies the evolution of postdevelopmental novelty in honey bees. Mol. Biol. Evol 32:334–46 [Google Scholar]
  59. Jindra M, Uhlirova M, Charles J-P, Smykal V, Hill RJ. 59.  et al. 2015. Genetic evidence for function of the bHLH-PAS protein Gce/Met as a juvenile hormone receptor. PLOS Genet 11:e1005394 [Google Scholar]
  60. Johnson BR, Jasper WC. 60.  2016. Complex patterns of differential expression in candidate master regulatory genes for social behavior in honey bees. Behav. Ecol. Sociobiol 70:1033–43 [Google Scholar]
  61. Johnson BR, Linksvayer TA. 61.  2010. Deconstructing the superorganism: social physiology, groundplans, and sociogenomics. Q. Rev. Biol 85:57–79 [Google Scholar]
  62. Kaib M, Husseneder C, Epplen C, Epplen JT, Brandl R. 62.  1996. Kin-biased foraging in a termite. Proc. R. Soc. B 263:1527–32 [Google Scholar]
  63. Kamakura M. 63.  2011. Royalactin induces queen differentiation in honeybees. Nature 473:478–83 [Google Scholar]
  64. Kapheim KM, Johnson MM. 64.  2017. Support for the reproductive ground plan hypothesis in a solitary bee: links between sucrose response and reproductive status. Proc. R. Soc. B 284:20162406 [Google Scholar]
  65. Keller L. 65.  1993. Queen Number and Sociality in Insects Oxford, UK: Oxford Univ. Press
  66. Keller L. 66.  1995. Social life: the paradox of multiple-queen colonies. Trends Ecol. Evol 10:355–60 [Google Scholar]
  67. Keller L, Passera L. 67.  1992. Mating system, optimal number of matings, and sperm transfer in the Argentine ant Iridomyrmex humilis. Behav. Ecol. Sociobiol 31:359–66 [Google Scholar]
  68. Keller L, Ross KG. 68.  1998. Selfish genes: a green beard in the red fire ant. Nature 394:573–75 [Google Scholar]
  69. Kelstrup HC, Hartfelder K, Esterhuizen N, Wossler TC. 69.  2017. Juvenile hormone titers, ovarian status and epicuticular hydrocarbons in gynes and workers of the paper wasp Belonogaster longitarsus. J. Insect Physiol 98:83–92 [Google Scholar]
  70. Kent DS, Simpson JA. 70.  1992. Eusociality in the beetle Austroplatypus incompertus (Coleoptera: Curculionidae). Naturwissenschaften 79:86–87 [Google Scholar]
  71. Kerr WE, Akahira Y, Camargo CA. 71.  1975. Sex determination in bees. IV. Genetic control of juvenile hormone production in Melipona quadrifasciata (Apidae). Genetics 81:749–56 [Google Scholar]
  72. Khalturin K, Hemmrich G, Fraune S, Augustin R, Bosch TCG. 72.  2009. More than just orphans: Are taxonomically-restricted genes important in evolution?. Trends Genet 25:404–13 [Google Scholar]
  73. Klein A, Schultner E, Lowak H, Schrader L, Heinze J. 73.  et al. 2016. Evolution of social insect polyphenism facilitated by the sex differentiation cascade. PLOS Genet 12:e1005952 [Google Scholar]
  74. Kobayashi K, Hasegawa E, Ohkawara K. 74.  2008. Clonal reproduction by males of the ant Vollenhovia emeryi (Wheeler). Entomol. Sci 11:167–72 [Google Scholar]
  75. Krieger MJB, Ross KG. 75.  2002. Identification of a major gene regulating complex social behavior. Science 295:328–32 [Google Scholar]
  76. Kucharski R, Maleszka J, Foret S, Maleszka R. 76.  2008. Nutritional control of reproductive status in honeybees via DNA methylation. Science 319:1827–30 [Google Scholar]
  77. Kunte K, Zhang W, Tenger-Trolander A, Palmer DH, Martin A. 77.  et al. 2014. doublesex is a mimicry supergene. Nature 507:229–32 [Google Scholar]
  78. Küpper C, Stocks M, Risse JE, dos Remedios N, Farrell LL. 78.  et al. 2015. A supergene determines highly divergent male reproductive morphs in the ruff. Nat. Genet 48:179–83 [Google Scholar]
  79. Kvist J, Wheat CW, Kallioniemi E, Saastamoinen M, Hanski I, Frilander MJ. 79.  2013. Temperature treatments during larval development reveal extensive heritable and plastic variation in gene expression and life history traits. Mol. Ecol 22:602–19 [Google Scholar]
  80. Li J, Cocker JM, Wright J, Webster MA, McMullan M. 80.  et al. 2016. Genetic architecture and evolution of the S locus supergene in Primula vulgaris. Nat. Plants 2:16188 [Google Scholar]
  81. Libbrecht R, Corona M, Wende F, Azevedo DO, Serrão JE, Keller L. 81.  2013. Interplay between insulin signaling, juvenile hormone, and vitellogenin regulates maternal effects on polyphenism in ants. PNAS 110:11050–55 [Google Scholar]
  82. Libbrecht R, Keller L. 82.  2013. Genetic compatibility affects division of labor in the Argentine ant Linepithema humile.. Evolution 67:517–24 [Google Scholar]
  83. Libbrecht R, Oxley PR, Keller L, Kronauer DJC. 83.  2016. Robust DNA methylation in the clonal raider ant brain. Curr. Biol 26:391–95 [Google Scholar]
  84. Libbrecht R, Oxley PR, Kronauer DJC, Keller L. 84.  2013. Ant genomics sheds light on the molecular regulation of social organization. Genome Biol 14:212 [Google Scholar]
  85. Libbrecht R, Schwander T, Keller L. 85.  2011. Genetic components to caste allocation in a multiple-queen species. Evolution 65:2907–15 [Google Scholar]
  86. Lillico-Ouachour A, Abouheif E. 86.  2017. Regulation, development, and evolution of caste ratios in the hyperdiverse ant genus Pheidole. Curr. Opin. Insect Sci 19:43–51 [Google Scholar]
  87. Linksvayer TA. 87.  2015. The molecular and evolutionary genetic implications of being truly social for the social insects. Advances in Insect Physiology: Genomics, Physiology and Behaviour of Social Insects, Vol. 48 A Zayed, CF Kent 271–92 London: Academic Press [Google Scholar]
  88. Linksvayer TA, Fewell JH, Gadau J, Laubichler MD. 88.  2012. Developmental evolution in social insects: regulatory networks from genes to societies. J. Exp. Zool. B Mol. Dev. Evol 318:159–69 [Google Scholar]
  89. Lockett GA, Almond EJ, Huggins TJ, Parker JD, Bourke AFG. 89.  2016. Gene expression differences in relation to age and social environment in queen and worker bumble bees. Exp. Gerontol 77:52–61 [Google Scholar]
  90. Lockett GA, Kucharski R, Maleszka R. 90.  2012. DNA methylation changes elicited by social stimuli in the brains of worker honey bees. Genes Brain Behav 11:235–42 [Google Scholar]
  91. Lu H-L, Pietrantonio PV. 91.  2011. Insect insulin receptors: insights from sequence and caste expression analyses of two cloned hymenopteran insulin receptor cDNAs from the fire ant. Insect Mol. Biol 20:637–49 [Google Scholar]
  92. Lucas C, Nicolas M, Keller L. 92.  2015. Expression of foraging and Gp-9 are associated with social organization in the fire ant Solenopsis invicta. Insect Mol. Biol 24:93–104 [Google Scholar]
  93. Lucas C, Sokolowski MB. 93.  2009. Molecular basis for changes in behavioral state in ant social behaviors. PNAS 106:6351–56 [Google Scholar]
  94. Lucas ER, Romiguier J, Keller L. 93a.  2017. Gene expression is more strongly influenced by age than caste in the ant Lasius niger. Mol. Ecol. 26:5058–73 [Google Scholar]
  95. Lyko F, Foret S, Kucharski R, Wolf S, Falckenhayn C, Maleszka R. 94.  2010. The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLOS Biol 8:e1000506 [Google Scholar]
  96. Ma Z, Guo W, Guo X, Wang X, Kang L. 95.  2011. Modulation of behavioral phase changes of the migratory locust by the catecholamine metabolic pathway. PNAS 108:3882–87 [Google Scholar]
  97. Manfredini F, Riba-Grognuz O, Wurm Y, Keller L, Shoemaker D, Grozinger CM. 96.  2013. Sociogenomics of cooperation and conflict during colony founding in the fire ant Solenopsis invicta. PLOS Genet 9:e1003633 [Google Scholar]
  98. Mao L, Henderson G, Liu Y, Laine RA. 97.  2005. Formosan subterranean termite (Isoptera: Rhinotermitidae) soldiers regulate juvenile hormone levels and caste differentiation in workers. Ann. Entomol. Soc. Am 98:340–45 [Google Scholar]
  99. McGary KL, Park TJ, Woods JO, Cha HJ, Wallingford JB, Marcotte EM. 98.  2010. Systematic discovery of nonobvious human disease models through orthologous phenotypes. PNAS 107:6544–49 [Google Scholar]
  100. McKenzie SK, Fetter-Pruneda I, Ruta V, Kronauer DJC. 99.  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]
  101. McQuillan HJ, Nakagawa S, Mercer AR. 100.  2012. Mushroom bodies of the honeybee brain show cell population-specific plasticity in expression of amine-receptor genes. Learn. Mem 19:151–58 [Google Scholar]
  102. Mersch DP, Crespi A, Keller L. 101.  2013. Tracking individuals shows spatial fidelity is a key regulator of ant social organization. Science 340:1090–93 [Google Scholar]
  103. Mery F, Varela SAM, Danchin É, Blanchet S, Parejo D. 102.  et al. 2009. Public versus personal information for mate copying in an invertebrate. Curr. Biol 19:730–34 [Google Scholar]
  104. Mikheyev AS, Linksvayer TA. 103.  2015. Genes associated with ant social behavior show distinct transcriptional and evolutionary patterns. eLife 4:e04775 [Google Scholar]
  105. Molet M, Wheeler DE, Peeters C. 104.  2012. Evolution of novel mosaic castes in ants: modularity, phenotypic plasticity, and colonial buffering. Am. Nat 180:328–41 [Google Scholar]
  106. Molodtsova D, Harpur BA, Kent CF, Seevananthan K, Zayed A. 105.  2014. Pleiotropy constrains the evolution of protein but not regulatory sequences in a transcription regulatory network influencing complex social behaviors. Front. Genet 5:431 [Google Scholar]
  107. Monnin T, Peeters C. 106.  1999. Dominance hierarchy and reproductive conflicts among subordinates in a monogynous queenless ant. Behav. Ecol 10:323–32 [Google Scholar]
  108. Montgomery SH, Mank JE. 107.  2016. Inferring regulatory change from gene expression: the confounding effects of tissue scaling. Mol. Ecol 25:5114–28 [Google Scholar]
  109. Moore AJ, Brodie ED III, Wolf JB. 108.  1997. Interacting phenotypes and the evolutionary process: I. Direct and indirect genetic effects of social interactions. Evolution 51:1352–62 [Google Scholar]
  110. Morandin C, Tin MMY, Abril S, Gómez C, Pontieri L. 109.  et al. 2016. Comparative transcriptomics reveals the conserved building blocks involved in parallel evolution of diverse phenotypic traits in ants. Genome Biol 17:43 [Google Scholar]
  111. Mutti NS, Dolezal AG, Wolschin F, Mutti JS, Gill KS, Amdam GV. 110.  2011. IRS and TOR nutrient-signaling pathways act via juvenile hormone to influence honey bee caste fate. J. Exp. Biol 214:3977–84 [Google Scholar]
  112. Nijhout HF. 111.  2003. The control of body size in insects. Dev. Biol 261:1–9 [Google Scholar]
  113. O'Connell LA, Hofmann HA. 112.  2012. Evolution of a vertebrate social decision-making network. Science 336:1154–57 [Google Scholar]
  114. O'Donnell S. 113.  1996. RAPD markers suggest genotypic effects on forager specialization in a eusocial wasp. Behav. Ecol. Sociobiol 38:83–88 [Google Scholar]
  115. Ohkawara K, Nakayama M, Satoh A, Trindl A, Heinze J. 114.  2006. Clonal reproduction and genetic caste differences in a queen-polymorphic ant. Vollenhovia emeryi. Biol. Lett 2:359–63 [Google Scholar]
  116. Oster GF, Wilson EO. 115.  1978. Caste and Ecology in the Social Insects Princeton, NJ: Princeton Univ. Press
  117. Oxley PR, Ji L, Fetter-Pruneda I, McKenzie SK, Li C. 116.  et al. 2014. The genome of the clonal raider ant Cerapachys biroi. Curr. Biol 24:451–58 [Google Scholar]
  118. Pamminger T, Hughes WOH. 117.  2016. Testing the reproductive groundplan hypothesis in ants (Hymenoptera: Formicidae). Evolution 71:153–59 [Google Scholar]
  119. Pandey A, Bloch G. 118.  2015. Juvenile hormone and ecdysteroids as major regulators of brain and behavior in bees. Curr. Opin. Insect Sci 12:26–37 [Google Scholar]
  120. Patalano S, Vlasova A, Wyatt C, Ewels P, Camara F. 119.  et al. 2015. Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies. PNAS 112:13970–75 [Google Scholar]
  121. Patel A, Fondrk MK, Kaftanoglu O, Emore C, Hunt G. 120.  et al. 2007. The making of a queen: TOR pathway is a key player in diphenic caste development. PLOS ONE 2:e509 [Google Scholar]
  122. Peeters C, Liebig J, Hölldobler B. 121.  2000. Sexual reproduction by both queens and workers in the ponerine ant Harpegnathos saltator. Insectes Sociaux 47:325–32 [Google Scholar]
  123. Penick CA, Brent CS, Dolezal K, Liebig J. 122.  2014. Neurohormonal changes associated with ritualized combat and the formation of a reproductive hierarchy in the ant Harpegnathos saltator. J. Exp. Biol 217:1496–503 [Google Scholar]
  124. Penick CA, Liebig J, Brent CS. 123.  2011. Reproduction, dominance, and caste: endocrine profiles of queens and workers of the ant Harpegnathos saltator. J. Comp. Physiol. A 197:1063–71 [Google Scholar]
  125. Pereira HS, Sokolowski MB. 124.  1993. Mutations in the larval foraging gene affect adult locomotory behavior after feeding in Drosophila melanogaster. PNAS 90:5044–46 [Google Scholar]
  126. Pinto LZ, Bitondi MMG, Simões ZLP. 125.  2000. Inhibition of vitellogenin synthesis in Apis mellifera workers by a juvenile hormone analogue, pyriproxyfen. J. Insect Physiol 46:153–60 [Google Scholar]
  127. Purcell J, Brelsford A, Wurm Y, Perrin N, Chapuisat M. 126.  2014. Convergent genetic architecture underlies social organization in ants. Curr. Biol 24:2728–32 [Google Scholar]
  128. Rajakumar R, San Mauro D, Dijkstra MB, Huang MH, Wheeler DE. 127.  et al. 2012. Ancestral developmental potential facilitates parallel evolution in ants. Science 335:79–82 [Google Scholar]
  129. Ravary F, Lecoutey E, Kaminski G, Châline N, Jaisson P. 128.  2007. Individual experience alone can generate lasting division of labor in ants. Curr. Biol 17:1308–12 [Google Scholar]
  130. Rehan SM, Toth AL. 129.  2015. Climbing the social ladder: the molecular evolution of sociality. Trends Ecol. Evol 30:426–33 [Google Scholar]
  131. Roberts RB, Ser JR, Kocher TD. 130.  2009. Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi cichlid fishes. Science 326:998–1001 [Google Scholar]
  132. Robinson GE, Vargo EL. 131.  1997. Juvenile hormone in adult eusocial hymenoptera: gonadotropin and behavioral pacemaker. Arch. Insect Biochem. Physiol 35:559–83 [Google Scholar]
  133. Ross KG, Keller L. 132.  1995. Ecology and evolution of social organization: insights from fire ants and other highly eusocial insects. Annu. Rev. Ecol. Syst 26:631–56 [Google Scholar]
  134. Ross KG, Keller L. 133.  1998. Genetic control of social organization in an ant. PNAS 95:14232–37 [Google Scholar]
  135. Roy-Zokan EM, Cunningham CB, Hebb LE, McKinney EC, Moore AJ. 134.  2015. Vitellogenin and vitellogenin receptor gene expression is associated with male and female parenting in a subsocial insect. Proc. R. Soc. B 282:20150787 [Google Scholar]
  136. Schneider J, Atallah J, Levine JD. 135.  2017. Social structure and indirect genetic effects: genetics of social behaviour. Biol. Rev 92:1027–38 [Google Scholar]
  137. Schulz DJ, Robinson GE. 136.  1999. Biogenic amines and division of labor in honey bee colonies: behaviorally related changes in the antennal lobes and age-related changes in the mushroom bodies. J. Comp. Physiol. A 184:481–88 [Google Scholar]
  138. Schwander T, Humbert J-Y, Brent CS, Cahan SH, Chapuis L. 137.  et al. 2008. Maternal effect on female caste determination in a social insect. Curr. Biol 18:265–69 [Google Scholar]
  139. Schwander T, Keller L. 138.  2008. Genetic compatibility affects queen and worker caste determination. Science 322:552 [Google Scholar]
  140. Schwander T, Libbrecht R, Keller L. 139.  2014. Supergenes and complex phenotypes. Curr. Biol 24:R288–94 [Google Scholar]
  141. Schwander T, Lo N, Beekman M, Oldroyd BP, Keller L. 140.  2010. Nature versus nurture in social insect caste differentiation. Trends Ecol. Evol 25:275–82 [Google Scholar]
  142. Seeley TD. 141.  1982. Adaptive significance of the age polyethism schedule in honeybee colonies. Behav. Ecol. Sociobiol 11:287–93 [Google Scholar]
  143. Sheehan MJ, Tibbetts EA. 142.  2011. Specialized face learning is associated with individual recognition in paper wasps. Science 334:1272–75 [Google Scholar]
  144. Shi Y-Y, Zheng H-J, Pan Q-Z, Wang Z-L, Zeng Z-J. 143.  2015. Differentially expressed microRNAs between queen and worker larvae of the honey bee (Apis mellifera). Apidologie 46:35–45 [Google Scholar]
  145. Simola DF, Graham RJ, Brady CM, Enzmann BL, Desplan C. 144.  et al. 2016. Epigenetic (re)programming of caste-specific behavior in the ant Camponotus floridanus. Science 351:aac6633 [Google Scholar]
  146. Simola DF, Ye C, Mutti NS, Dolezal K, Bonasio R. 145.  et al. 2013. A chromatin link to caste identity in the carpenter ant Camponotus floridanus. Genome Res 23:486–96 [Google Scholar]
  147. Smith CR, Anderson KE, Tillberg CV, Gadau J, Suarez AV. 146.  2008. Caste determination in a polymorphic social insect: nutritional, social, and genetic factors. Am. Nat 172:497–507 [Google Scholar]
  148. Sokolowski MB. 147.  2010. Social interactions in “simple” model systems. Neuron 65:780–94 [Google Scholar]
  149. Solis CR, Strassmann JE. 148.  1990. Presence of brood affects caste differentiation in the social wasp, Polistes exclamans Viereck (Hymenoptera: Vespidae). Funct. Ecol 4:531–41 [Google Scholar]
  150. Stern DL, Foster WA. 149.  1996. The evolution of soldiers in aphids. Biol. Rev 71:27–79 [Google Scholar]
  151. Stevenson PA, Rillich J. 150.  2016. Controlling the decision to fight or flee: the roles of biogenic amines and nitric oxide in the cricket. Curr. Zool 62:265–75 [Google Scholar]
  152. Sullivan JP, Jassim O, Fahrbach SE, Robinson GE. 151.  2000. Juvenile hormone paces behavioral development in the adult worker honey bee. Horm. Behav 37:1–14 [Google Scholar]
  153. Sumner S. 152.  2014. The importance of genomic novelty in social evolution. Mol. Ecol 23:26–28 [Google Scholar]
  154. Szathmáry E, Smith JM. 153.  1995. The major evolutionary transitions. Nature 374:227–32 [Google Scholar]
  155. Tarver MR, Zhou X, Scharf ME. 154.  2010. Socio-environmental and endocrine influences on developmental and caste-regulatory gene expression in the eusocial termite Reticulitermes flavipes. BMC Mol. Biol 11:28 [Google Scholar]
  156. Theraulaz G, Bonabeau E, Denuebourg J-N. 155.  1998. Response threshold reinforcements and division of labour in insect societies. Proc. R. Soc. B 265:327–32 [Google Scholar]
  157. Thomas JW, Cáceres M, Lowman JJ, Morehouse CB, Short ME. 156.  et al. 2008. The chromosomal polymorphism linked to variation in social behavior in the white-throated sparrow (Zonotrichia albicollis) is a complex rearrangement and suppressor of recombination. Genetics 179:1455–68 [Google Scholar]
  158. Tibbetts EA, Crocker KC. 157.  2014. The challenge hypothesis across taxa: social modulation of hormone titres in vertebrates and insects. Anim. Behav 92:281–90 [Google Scholar]
  159. Tilley CA, Oldroyd BP. 158.  1997. Unequal subfamily proportions among honey bee queen and worker brood. Anim. Behav 54:1483–90 [Google Scholar]
  160. Toth AL, Rehan SM. 159.  2017. Molecular evolution of insect sociality: an eco-evo-devo perspective. Annu. Rev. Entomol 62:419–42 [Google Scholar]
  161. Toth AL, Robinson GE. 160.  2007. Evo-devo and the evolution of social behavior. Trends Genet 23:334–41 [Google Scholar]
  162. Tuttle EM, Bergland AO, Korody ML, Brewer MS, Newhouse DJ. 161.  et al. 2016. Divergence and functional degradation of a sex chromosome-like supergene. Curr. Biol 26:3344–50 [Google Scholar]
  163. Volny VP, Gordon DM. 162.  2002. Genetic basis for queen–worker dimorphism in a social insect. PNAS 99:6108–11 [Google Scholar]
  164. Wang J, Wurm Y, Nipitwattanaphon M, Riba-Grognuz O, Huang Y-C. 163.  et al. 2013. A Y-like social chromosome causes alternative colony organization in fire ants. Nature 493:664–68 [Google Scholar]
  165. Wcislo WT, Danforth BN. 164.  1997. Secondarily solitary: the evolutionary loss of social behavior. Trends Ecol. Evol 12:468–74 [Google Scholar]
  166. Wedd L, Maleszka R. 165.  2016. DNA methylation and gene regulation in honeybees: from genome-wide analyses to obligatory epialleles. DNA Methyltransferases—Role and Function A Jeltsch, RZ Jurkowska 193–211 Cham, Switz.: Springer [Google Scholar]
  167. Weitekamp CA, Hofmann HA. 166.  2017. Brain systems underlying social behavior. In Evolution of Nervous Systems, Vol. 1 J Kaas 327–34 Oxford, UK: Elsevier, 2nd ed.. [Google Scholar]
  168. West-Eberhard MJ. 167.  1986. Dominance relations in Polistes canadensis (L.), a tropical social wasp. Monitore Zool. Ital 20:263–81 [Google Scholar]
  169. Wheeler DE. 168.  1991. The developmental basis of worker caste polymorphism in ants. Am. Nat 138:51218–38 [Google Scholar]
  170. Wheeler DE, Buck N, Evans JD. 169.  2006. Expression of insulin pathway genes during the period of caste determination in the honey bee, Apis mellifera. Insect Mol. Biol 15:597–602 [Google Scholar]
  171. Wheeler DE, Nijhout HF. 170.  1981. Soldier determination in ants: new role for juvenile hormone. Science 213:361–63 [Google Scholar]
  172. Wheeler MM, Robinson GE. 171.  2014. Diet-dependent gene expression in honey bees: honey vs. sucrose or high fructose corn syrup. Sci. Rep 4:5726 [Google Scholar]
  173. Wilkins AS. 172.  2013. “The genetic tool-kit”: the life-history of an important metaphor. Advances in Evolutionary Developmental Biology JT Streelman 1–14 Hoboken, NJ: John Wiley & Sons, Inc. [Google Scholar]
  174. Wissler L, Gadau J, Simola DF, Helmkampf M, Bornberg-Bauer E. 173.  2013. Mechanisms and dynamics of orphan gene emergence in insect genomes. Genome Biol. Evol 5:439–55 [Google Scholar]
  175. Wolschin F, Mutti NS, Amdam GV. 174.  2011. Insulin receptor substrate influences female caste development in honeybees. Biol. Lett 7:112–15 [Google Scholar]
  176. Wu Q, Wen T, Lee G, Park JH, Cai HN, Shen P. 175.  2003. Developmental control of foraging and social behavior by the Drosophila neuropeptide Y-like system. Neuron 39:147–61 [Google Scholar]
  177. Wurm Y, Wang J, Riba-Grognuz O, Corona M, Nygaard S. 176.  et al. 2011. The genome of the fire ant Solenopsis invicta. PNAS 108:5679–84 [Google Scholar]
  178. Yang M, Wei Y, Jiang F, Wang Y, Guo X. 177.  et al. 2014. MicroRNA-133 inhibits behavioral aggregation by controlling dopamine synthesis in locusts. PLOS Genet 10:e1004206 [Google Scholar]
  179. Zhou X, Oi FM, Scharf ME. 178.  2006. Social exploitation of hexamerin: RNAi reveals a major caste-regulatory factor in termites. PNAS 103:4499–504 [Google Scholar]
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