1932

Abstract

In this review, I discuss current knowledge and outstanding questions on the neuromodulators that influence aggressive behavior of the fruit fly . I first present evidence that exchange information during an agonistic interaction and choose appropriate actions based on this information. I then discuss the influence of several biogenic amines and neuropeptides on aggressive behavior. One striking characteristic of neuromodulation is that it can configure a neural circuit dynamically, enabling one circuit to generate multiple outcomes. I suggest a consensus effect of each neuromodulatory molecule on aggression, as well as effects of receptor proteins where relevant data are available. Lastly, I consider neuromodulation in the context of strategic action choices during agonistic interactions. Genetic components of neuromodulatory systems are highly conserved across animals, suggesting that molecular and cellular mechanisms controlling aggression can shed light on neural principles governing action choice during social interactions.

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2017-07-25
2024-03-29
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Literature Cited

  1. Adamo SA, Linn CE, Hoy RR. 1995. The role of neurohormonal octopamine during “fight or flight” behaviour in the field cricket Gryllus bimaculatus. J. Exp. Biol. 198:1691–700 [Google Scholar]
  2. Albrecht DR, Bargmann CI. 2011. High-content behavioral analysis of Caenorhabditis elegans in precise spatiotemporal chemical environments. Nat. Methods 8:599–605 [Google Scholar]
  3. Alekseyenko OV, Chan YB, Fernandez MP, Bülow T, Pankratz MJ, Kravitz EA. 2014. Single serotonergic neurons that modulate aggression in Drosophila. Curr. Biol. 24:2700–7 [Google Scholar]
  4. Alekseyenko OV, Chan YB, Li R, Kravitz EA. 2013. Single dopaminergic neurons that modulate aggression in Drosophila. PNAS 110:6151–56 [Google Scholar]
  5. Alekseyenko OV, Lee C, Kravitz EA. 2010. Targeted manipulation of serotonergic neurotransmission affects the escalation of aggression in adult male Drosophila melanogaster. PLOS ONE 5:e10806 [Google Scholar]
  6. Anderson DJ. 2012. Optogenetics, sex, and violence in the brain: implications for psychiatry. Biol. Psychiatry 71:1081–89 [Google Scholar]
  7. Anderson DJ, Adolphs R. 2014. A framework for studying emotions across species. Cell 157:187–200 [Google Scholar]
  8. Anderson DJ, Perona P. 2014. Toward a science of computational ethology. Neuron 84:18–31 [Google Scholar]
  9. Andrews JC, Fernández MP, Yu Q, Leary GP, Leung AKW. et al. 2014. Octopamine neuromodulation regulates Gr32a-linked aggression and courtship pathways in Drosophila males. PLOS Genet 10:e1004356 [Google Scholar]
  10. Arnott G, Elwood RW. 2009. Assessment of fighting ability in animal contests. Anim. Behav. 77:991–1004 [Google Scholar]
  11. Asahina K, Watanabe K, Duistermars BJ, Hoopfer E, Gonzalez CR. et al. 2014. Tachykinin-expressing neurons control male-specific aggressive arousal in Drosophila. Cell 156:221–35 [Google Scholar]
  12. Aso Y, Rubin GM. 2016. Dopaminergic neurons write and update memories with cell-type-specific rules. eLife 5:e16135 [Google Scholar]
  13. Azim E, Jiang J, Alstermark B, Jessell TM. 2014. Skilled reaching relies on a V2a propriospinal internal copy circuit. Nature 508:357–63 [Google Scholar]
  14. Baerends GP. 1976. Functional organization of behavior. Anim. Behav. 24:726–38 [Google Scholar]
  15. Baier A, Wittek B, Brembs B. 2002. Drosophila as a new model organism for the neurobiology of aggression. ? J. Exp. Biol. 205:1233–40 [Google Scholar]
  16. Bargmann CI. 2012. Beyond the connectome: how neuromodulators shape neural circuits. Bioessays 34:458–65 [Google Scholar]
  17. Berman GJ, Choi DM, Bialek W, Shaevitz JW. 2014. Mapping the stereotyped behaviour of freely moving fruit flies. J. R. Soc. Interface 11:20140672 [Google Scholar]
  18. Berridge KC. 2004. Motivation concepts in behavioral neuroscience. Physiol. Behav. 81:179–209 [Google Scholar]
  19. Billeter JC, Atallah J, Krupp JJ, Millar JG, Levine JD. 2009. Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 461:987–91 [Google Scholar]
  20. Birse RT, Johnson EC, Taghert PH, Nässel DR. 2006. Widely distributed Drosophila G-protein-coupled receptor (CG7887) is activated by endogenous tachykinin-related peptides. J. Neurobiol. 66:33–46 [Google Scholar]
  21. Blanchard DC, Blanchard RJ. 2003. What can animal aggression research tell us about human aggression. ? Horm. Behav. 44:171–77 [Google Scholar]
  22. Bosch OJ, Meddle SL, Beiderbeck DI, Douglas AJ, Neumann ID. 2005. Brain oxytocin correlates with maternal aggression: link to anxiety. J. Neurosci. 25:6807–15 [Google Scholar]
  23. Breed MD, Guzman-Novoa E, Hunt GJ. 2004. Defensive behavior of honey bees: organization, genetics, and comparisons with other bees. Annu. Rev. Entomol. 49:271–98 [Google Scholar]
  24. Briffa M, Sneddon LU. 2007. Physiological constraints on contest behaviour. Funct. Ecol. 21:627–37 [Google Scholar]
  25. Brown JL, Hunsperger RW, Rosvold HE. 1969. Defence, attack, and flight elicited by electrical stimulation of the hypothalamus of the cat. Exp. Brain Res. 8:113–29 [Google Scholar]
  26. Bubak AN, Renner KJ, Swallow JG. 2014. Heightened serotonin influences contest outcome and enhances expression of high-intensity aggressive behaviors. Behav. Brain Res. 259:137–42 [Google Scholar]
  27. Bubak AN, Rieger NS, Watt MJ, Renner KJ, Swallow JG. 2015. David vs. Goliath: Serotonin modulates opponent perception between smaller and larger rivals. Behav. Brain Res. 292:521–27 [Google Scholar]
  28. Cachero S, Ostrovsky AD, Yu JY, Dickson BJ, Jefferis GS. 2010. Sexual dimorphism in the fly brain. Curr. Biol. 20:1589–601 [Google Scholar]
  29. Certel SJ, Leung A, Lin CY, Perez P, Chiang AS, Kravitz EA. 2010. Octopamine neuromodulatory effects on a social behavior decision-making network in Drosophila males. PLOS ONE 5:e13248 [Google Scholar]
  30. Certel SJ, Savella MG, Schlegel DC, Kravitz EA. 2007. Modulation of Drosophila male behavioral choice. PNAS 104:4706–11 [Google Scholar]
  31. Chalasani SH, Kato S, Albrecht DR, Nakagawa T, Abbott LF, Bargmann CI. 2010. Neuropeptide feedback modifies odor-evoked dynamics in Caenorhabditis elegans olfactory neurons. Nat. Neurosci. 13:615–21 [Google Scholar]
  32. Chen S, Lee AY, Bowens NM, Huber R, Kravitz EA. 2002. Fighting fruit flies: a model system for the study of aggression. PNAS 99:5664–68 [Google Scholar]
  33. Chiu AY, Hunkapiller MW, Heller E, Stuart DK, Hood LE, Strumwasser F. 1979. Purification and primary structure of the neuropeptide egg-laying hormone of Aplysia californica. PNAS 76:6656–60 [Google Scholar]
  34. Clowney EJ, Iguchi S, Bussell JJ, Scheer E, Ruta V. 2015. Multimodal chemosensory circuits controlling male courtship in Drosophila. Neuron 87:1036–49 [Google Scholar]
  35. Coccaro EF, Fanning JR, Phan KL, Lee R. 2015. Serotonin and impulsive aggression. CNS Spectr 20:295–302 [Google Scholar]
  36. Cohn R, Morantte I, Ruta V. 2015. Coordinated and compartmentalized neuromodulation shapes sensory processing in Drosophila. Cell 163:1742–55 [Google Scholar]
  37. Cole SH, Carney GE, McClung CA, Willard SS, Taylor BJ, Hirsh J. 2005. Two functional but noncomplementing Drosophila tyrosine decarboxylase genes: distinct roles for neural tyramine and octopamine in female fertility. J. Biol. Chem. 280:14948–55 [Google Scholar]
  38. Dankert H, Wang L, Hoopfer ED, Anderson DJ, Perona P. 2009. Automated monitoring and analysis of social behavior in Drosophila. Nat. Methods 6:297–303 [Google Scholar]
  39. Davis SM, Thomas AL, Nomie KJ, Huang L, Dierick HA. 2014. Tailless and Atrophin control Drosophila aggression by regulating neuropeptide signalling in the pars intercerebralis. Nat. Commun. 5:3177 [Google Scholar]
  40. De Felipe C, Herrero JF, O'Brien JA, Palmer JA, Doyle CA. et al. 1998. Altered nociception, analgesia and aggression in mice lacking the receptor for substance P. Nature 392:394–97 [Google Scholar]
  41. Dell AI, Bender JA, Branson K, Couzin ID, de Polavieja GG. et al. 2014. Automated image-based tracking and its application in ecology. Trends Ecol. Evol. 29:417–28 [Google Scholar]
  42. Dierick HA. 2007. A method for quantifying aggression in male Drosophila melanogaster. Nat. Protoc. 2:2712–18 [Google Scholar]
  43. Dierick HA, Greenspan RJ. 2006. Molecular analysis of flies selected for aggressive behavior. Nat. Genet. 38:1023–31 [Google Scholar]
  44. Dierick HA, Greenspan RJ. 2007. Serotonin and neuropeptide F have opposite modulatory effects on fly aggression. Nat. Genet. 39:678–82 [Google Scholar]
  45. Dismukes RK. 1979. New concepts of molecular communication among neurons. Behav. Brain Sci. 2:409–16 [Google Scholar]
  46. Dow MA, von Schilcher F. 1975. Aggression and mating success in Drosophila melanogaster. Nature 254:511–12 [Google Scholar]
  47. Dweck HK, Ebrahim SA, Thoma M, Mohamed AA, Keesey IW. et al. 2015. Pheromones mediating copulation and attraction in Drosophila. PNAS 112:E2829–35 [Google Scholar]
  48. Edwards AC, Mackay TF. 2009. Quantitative trait loci for aggressive behavior in Drosophila melanogaster. Genetics 182:889–97 [Google Scholar]
  49. Edwards AC, Rollmann SM, Morgan TJ, Mackay TF. 2006. Quantitative genomics of aggressive behavior in Drosophila melanogaster. PLOS Genet. 2:e154 [Google Scholar]
  50. Egnor SE, Branson K. 2016. Computational analysis of behavior. Annu. Rev. Neurosci. 39:217–36 [Google Scholar]
  51. Enquist M. 1985. Communication during aggressive interactions with particular reference to variation in choice of behavior. Anim. Behav. 33:1152–61 [Google Scholar]
  52. Eyjolfsdottir E, Branson S, Burgos-Artizzu XP, Hoopfer ED, Schor J. et al. 2014. Detecting social actions of fruit flies. Comput. Vis. ECCV 2014 8690:772–87 [Google Scholar]
  53. Fan P, Manoli DS, Ahmed OM, Chen Y, Agarwal N. et al. 2013. Genetic and neural mechanisms that inhibit Drosophila from mating with other species. Cell 154:89–102 [Google Scholar]
  54. Fernández MP, Chan YB, Yew JY, Billeter JC, Dreisewerd K. et al. 2010. Pheromonal and behavioral cues trigger male-to-female aggression in Drosophila. PLOS Biol. 8:e1000541 [Google Scholar]
  55. Ferveur JF. 2005. Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav. Genet. 35:279–95 [Google Scholar]
  56. Gaudry Q, Kristan WB Jr. 2009. Behavioral choice by presynaptic inhibition of tactile sensory terminals. Nat. Neurosci. 12:1450–57 [Google Scholar]
  57. Giovenardi M, Padoin MJ, Cadore LP, Lucion AB. 1998. Hypothalamic paraventricular nucleus modulates maternal aggression in rats: effects of ibotenic acid lesion and oxytocin antisense. Physiol. Behav. 63:351–59 [Google Scholar]
  58. Gratz SJ, Ukken FP, Rubinstein CD, Thiede G, Donohue LK. et al. 2014. Highly specific and efficient CRISPR/Cas9-catalyzed homology-directed repair in Drosophila. Genetics 196:961–71 [Google Scholar]
  59. Guillemin R. 2005. Hypothalamic hormones a.k.a. hypothalamic releasing factors. J. Endocrinol. 184:11–28 [Google Scholar]
  60. Halasz J, Zelena D, Toth M, Tulogdi A, Mikics E, Haller J. 2009. Substance P neurotransmission and violent aggression: the role of tachykinin NK1 receptors in the hypothalamic attack area. Eur. J. Pharmacol. 611:35–43 [Google Scholar]
  61. Hamada FN, Rosenzweig M, Kang K, Pulver SR, Ghezzi A. et al. 2008. An internal thermal sensor controlling temperature preference in Drosophila. Nature 454:217–20 [Google Scholar]
  62. Hammels C, Pishva E, De Vry J, van den Hove DL, Prickaerts J. et al. 2015. Defeat stress in rodents: from behavior to molecules. Neurosci. Biobehav. Rev. 59:111–40 [Google Scholar]
  63. Hashikawa K, Hashikawa Y, Falkner A, Lin D. 2016. The neural circuits of mating and fighting in male mice. Curr. Opin. Neurobiol. 38:27–37 [Google Scholar]
  64. Hewes RS, Taghert PH. 2001. Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. Genome Res 11:1126–42 [Google Scholar]
  65. Hige T, Aso Y, Modi MN, Rubin GM, Turner GC. 2015. Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila. Neuron 88:985–98 [Google Scholar]
  66. Hoffmann AA. 1987a. A laboratory study of male territoriality in the sibling species Drosophila melanogaster and D. simulans. Anim. Behav. 35:807–18 [Google Scholar]
  67. Hoffmann AA. 1987b. Territorial encounters between Drosophila males of different sizes. Anim. Behav. 35:1899–901 [Google Scholar]
  68. Hoffmann AA. 1988. Heritable variation for territorial success in two Drosophila melanogaster populations. Anim. Behav. 36:1180–89 [Google Scholar]
  69. Hoffmann AA, Cacoyianni Z. 1990. Territoriality in Drosophila melanogaster as a conditional strategy. Anim. Behav. 40:526–37 [Google Scholar]
  70. Hong W, Kennedy A, Burgos-Artizzu XP, Zelikowsky M, Navonne SG. et al. 2015. Automated measurement of mouse social behaviors using depth sensing, video tracking, and machine learning. PNAS 112:E5351–60 [Google Scholar]
  71. Hoopfer ED. 2016. Neural control of aggression in Drosophila. Curr. Opin. Neurobiol. 38:109–18 [Google Scholar]
  72. Hoopfer ED, Jung Y, Inagaki HK, Rubin GM, Anderson DJ. 2015. P1 interneurons promote a persistent internal state that enhances inter-male aggression in Drosophila. eLife 4:e11346 [Google Scholar]
  73. Hoyer SC, Eckart A, Herrel A, Zars T, Fischer SA. et al. 2008. Octopamine in male aggression of Drosophila. Curr. Biol. 18:159–67 [Google Scholar]
  74. Hsu Y, Earley RL, Wolf LL. 2006. Modulation of aggressive behaviour by fighting experience: mechanisms and contest outcomes. Biol. Rev. Camb. Philos. Soc. 81:33–74 [Google Scholar]
  75. Huber R, Delago A. 1998. Serotonin alters decisions to withdraw in fighting crayfish, Astacus astacus: the motivational concept revisited. J. Comp. Physiol. A 182:573–83 [Google Scholar]
  76. Huber R, Smith K, Delago A, Isaksson K, Kravitz EA. 1997. Serotonin and aggressive motivation in crustaceans: altering the decision to retreat. PNAS 94:5939–42 [Google Scholar]
  77. Huntingford F, Turner A. 1987. Animal Conflict New York: Chapman Hall Ltd.
  78. Hussain A, Üçpunar HK, Zhang M, Loschek LF, Kadow ICG. 2016. Neuropeptides modulate female chemosensory processing upon mating in Drosophila. PLOS Biol. 14:e1002455 [Google Scholar]
  79. Im SH, Taghert PH. 2010. PDF receptor expression reveals direct interactions between circadian oscillators in Drosophila. J. Comp. Neurol. 518:1925–45 [Google Scholar]
  80. Inagaki HK, Ben-Tabou de-Leon S, Wong AM, Jagadish S, Ishimoto H. et al. 2012. Visualizing neuromodulation in vivo: TANGO-mapping of dopamine signaling reveals appetite control of sugar sensing. Cell 148:583–95 [Google Scholar]
  81. Ishikawa Y, Aonuma H, Sasaki K, Miura T. 2016. Tyraminergic and octopaminergic modulation of defensive behavior in termite soldier. PLOS ONE 11:e0154230 [Google Scholar]
  82. Ito H, Fujitani K, Usui K, Shimizu-Nishikawa K, Tanaka S, Yamamoto D. 1996. Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. PNAS 93:9687–92 [Google Scholar]
  83. Jacobs ME. 1960. Influence of light on mating of Drosophila melanogaster. Ecology 41:182–88 [Google Scholar]
  84. Jiang H, Lkhagva A, Daubnerova I, Chae HS, Simo L. et al. 2013. Natalisin, a tachykinin-like signaling system, regulates sexual activity and fecundity in insects. PNAS 110:E3526–34 [Google Scholar]
  85. Johnson EC, Bohn LM, Barak LS, Birse RT, Nässel DR. et al. 2003. Identification of Drosophila neuropeptide receptors by G protein-coupled receptors-β-arrestin2 interactions. J. Biol. Chem. 278:52172–78 [Google Scholar]
  86. Johnson O, Becnel J, Nichols CD. 2009. Serotonin 5-HT2 and 5-HT1A-like receptors differentially modulate aggressive behaviors in Drosophila melanogaster. Neuroscience 158:1292–300 [Google Scholar]
  87. Kabra M, Robie AA, Rivera-Alba M, Branson S, Branson K. 2013. JAABA: interactive machine learning for automatic annotation of animal behavior. Nat. Methods 10:64–67 [Google Scholar]
  88. Kallman BR, Kim H, Scott K. 2015. Excitation and inhibition onto central courtship neurons biases Drosophila mate choice. eLife 4:e11188 [Google Scholar]
  89. Karl T, Lin S, Schwarzer C, Sainsbury A, Couzens M. et al. 2004. Y1 receptors regulate aggressive behavior by modulating serotonin pathways. PNAS 101:12742–47 [Google Scholar]
  90. Kataoka H, Troetschler RG, Kramer SJ, Cesarin BJ, Schooley DA. 1987. Isolation and primary structure of the eclosion hormone of the tobacco hornworm. Manduca sexta. Biochem. Biophys. Res. Commun. 146:746–50 [Google Scholar]
  91. Kavaliers M, Hirst M. 1985. FMRFamide, a putative endogenous opiate antagonist: evidence from suppression of defeat-induced analgesia and feeding in mice. Neuropeptides 6:485–94 [Google Scholar]
  92. Kayser MS, Mainwaring B, Yue Z, Sehgal A. 2015. Sleep deprivation suppresses aggression in Drosophila. eLife 4:e07643 [Google Scholar]
  93. Kim WJ, Jan LY, Jan YN. 2013. A PDF/NPF neuropeptide signaling circuitry of male Drosophila melanogaster controls rival-induced prolonged mating. Neuron 80:1190–205 [Google Scholar]
  94. Ko KI, Root CM, Lindsay SA, Zaninovich OA, Shepherd AK. et al. 2015. Starvation promotes concerted modulation of appetitive olfactory behavior via parallel neuromodulatory circuits. eLife 4:e08298 [Google Scholar]
  95. Koganezawa M, Kimura K, Yamamoto D. 2016. The neural circuitry that functions as a switch for courtship versus aggression in Drosophila males. Curr. Biol. 26:1395–403 [Google Scholar]
  96. Kohl J, Ostrovsky AD, Frechter S, Jefferis GS. 2013. A bidirectional circuit switch reroutes pheromone signals in male and female brains. Cell 155:1610–23 [Google Scholar]
  97. Koolhaas JM. 1978. Hypothalamically induced intraspecific aggressive behaviour in the rat. Exp. Brain. Res. 32:365–75 [Google Scholar]
  98. Krashes MJ, DasGupta S, Vreede A, White B, Armstrong JD, Waddell S. 2009. A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139:416–27 [Google Scholar]
  99. Kravitz EA. 1988. Hormonal control of behavior: amines and the biasing of behavioral output in lobsters. Science 241:1775–81 [Google Scholar]
  100. Kravitz EA. 2000. Serotonin and aggression: insights gained from a lobster model system and speculations on the role of amine neurons in a complex behavior. J. Comp. Physiol. A 186:221–38 [Google Scholar]
  101. Kravitz EA, Fernandez MP. 2015. Aggression in Drosophila. Behav. Neurosci. 129:549–63 [Google Scholar]
  102. Kravitz EA, Huber R. 2003. Aggression in invertebrates. Curr. Opin. Neurobiol. 13:736–43 [Google Scholar]
  103. Kruk MR, Van der Poel AM, Meelis W, Hermans J, Mostert PG. et al. 1983. Discriminant analysis of the localization of aggression-inducing electrode placements in the hypothalamus of male rats. Brain Res 260:61–79 [Google Scholar]
  104. Kurtovic A, Widmer A, Dickson BJ. 2007. A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446:542–46 [Google Scholar]
  105. Lebestky T, Chang JS, Dankert H, Zelnik L, Kim YC. et al. 2009. Two different forms of arousal in Drosophila are oppositely regulated by the dopamine D1 receptor ortholog DopR via distinct neural circuits. Neuron 64:522–36 [Google Scholar]
  106. LeDoux J. 2012. Rethinking the emotional brain. Neuron 73:653–76 [Google Scholar]
  107. Lee G, Hall JC. 2000. A newly uncovered phenotype associated with the fruitless gene of Drosophila melanogaster: aggression-like head interactions between mutant males. Behav. Genet. 30:263–75 [Google Scholar]
  108. Leinwand SG, Chalasani SH. 2013. Neuropeptide signaling remodels chemosensory circuit composition in Caenorhabditis elegans. Nat. Neurosci. 16:1461–67 [Google Scholar]
  109. Lim RS, Eyjolfsdottir E, Shin E, Perona P, Anderson DJ. 2014. How food controls aggression in Drosophila. PLOS ONE 9:e105626 [Google Scholar]
  110. Liu W, Liang X, Gong J, Yang Z, Zhang YH. et al. 2011. Social regulation of aggression by pheromonal activation of Or65a olfactory neurons in Drosophila. Nat. Neurosci. 14:896–902 [Google Scholar]
  111. Livingstone MS, Harris-Warrick RM, Kravitz EA. 1980. Serotonin and octopamine produce opposite postures in lobsters. Science 208:76–79 [Google Scholar]
  112. Lorenz K. 1966. On Aggression New York: Harcourt
  113. Lu B, LaMora A, Sun Y, Welsh MJ, Ben-Shahar Y. 2012. ppk23-dependent chemosensory functions contribute to courtship behavior in Drosophila melanogaster. PLOS Genet. 8:e1002587 [Google Scholar]
  114. Manoli DS, Fan P, Fraser EJ, Shah NM. 2013. Neural control of sexually dimorphic behaviors. Curr. Opin. Neurobiol. 23:330–38 [Google Scholar]
  115. Marder E. 2012. Neuromodulation of neuronal circuits: back to the future. Neuron 76:1–11 [Google Scholar]
  116. Marder E, O'Leary T, Shruti S. 2014. Neuromodulation of circuits with variable parameters: Single neurons and small circuits reveal principles of state-dependent and robust neuromodulation. Annu. Rev. Neurosci. 37:329–46 [Google Scholar]
  117. Marti T, Takio K, Walsh KA, Terzi G, Truman JW. 1987. Microanalysis of the amino acid sequence of the eclosion hormone from the tobacco hornworm Manduca sexta. FEBS Lett. 219:415–18 [Google Scholar]
  118. Michel MC, Wieland T, Tsujimoto G. 2009. How reliable are G-protein-coupled receptor antibodies? Naunyn Schmiedeberg's Arch. Pharmacol. 379:385–88 [Google Scholar]
  119. Miyamoto T, Amrein H. 2008. Suppression of male courtship by a Drosophila pheromone receptor. Nat. Neurosci. 11:874–76 [Google Scholar]
  120. Moyer KE. 1968. Kinds of aggression and their physiological basis. Commun. Behav. Biol. 2:65–87 [Google Scholar]
  121. Nässel DR. 2009. Neuropeptide signaling near and far: How localized and timed is the action of neuropeptides in brain circuits. ? Invertebr. Neurosci. 9:57–75 [Google Scholar]
  122. Nässel DR, Wegener C. 2011. A comparative review of short and long neuropeptide F signaling in invertebrates: any similarities to vertebrate neuropeptide Y signaling. ? Peptides 32:1335–55 [Google Scholar]
  123. Nässel DR, Winther AM. 2010. Drosophila neuropeptides in regulation of physiology and behavior. Prog. Neurobiol. 92:42–104 [Google Scholar]
  124. Nelson RJ, Chiavegatto S. 2001. Molecular basis of aggression. Trends Neurosci 24:713–19 [Google Scholar]
  125. Nelson RJ, Demas GE, Huang PL, Fishman MC, Dawson VL. et al. 1995. Behavioural abnormalities in male mice lacking neuronal nitric oxide synthase. Nature 378:383–86 [Google Scholar]
  126. Nelson RJ, Trainor BC. 2007. Neural mechanisms of aggression. Nat. Rev. Neurosci. 8:536–46 [Google Scholar]
  127. Nilsen SP, Chan YB, Huber R, Kravitz EA. 2004. Gender-selective patterns of aggressive behavior in Drosophila melanogaster. PNAS 101:12342–47 [Google Scholar]
  128. Orchard I. 1982. Octopamine in insects: neurotransmitter, neurohormone, and neuromodulator. Can. J. Zool. 60:659–69 [Google Scholar]
  129. Parker GA. 1974. Assessment strategy and evolution of fighting behavior. J. Theor. Biol. 47:223–43 [Google Scholar]
  130. Parker GA, Rubenstein DI. 1981. Role assessment, reserve strategy, and acquisition of information in asymmetric animal conflicts. Anim. Behav. 29:221–40 [Google Scholar]
  131. Payne RJH, Pagel M. 1997. Why do animals repeat displays?. Anim. Behav. 54:109–19 [Google Scholar]
  132. Peeke HVS, Blank GS, Figler MH, Chang ES. 2000. Effects of exogenous serotonin on a motor behavior and shelter competition in juvenile lobsters (Homarus americanus). J. Comp. Physiol. A 186:575–82 [Google Scholar]
  133. Penn JK, Zito MF, Kravitz EA. 2010. A single social defeat reduces aggression in a highly aggressive strain of Drosophila. PNAS 107:12682–86 [Google Scholar]
  134. Poels J, Birse RT, Nachman RJ, Fichna J, Janecka A. et al. 2009. Characterization and distribution of NKD, a receptor for Drosophila tachykinin-related peptide 6. Peptides 30:545–56 [Google Scholar]
  135. Port F, Chen HM, Lee T, Bullock SL. 2014. Optimized CRISPR/Cas tools for efficient germline and somatic genome engineering in Drosophila. PNAS 111:E2967–76 [Google Scholar]
  136. Rezaval C, Nojima T, Neville MC, Lin AC, Goodwin SF. 2014. Sexually dimorphic octopaminergic neurons modulate female postmating behaviors in Drosophila. Curr. Biol. 24:725–30 [Google Scholar]
  137. Richfield EK, Penney JB, Young AB. 1989. Anatomical and affinity state comparisons between dopamine D1 and D2 receptors in the rat central nervous system. Neuroscience 30:767–77 [Google Scholar]
  138. Rillich J, Stevenson PA. 2014. A fighter's comeback: Dopamine is necessary for recovery of aggression after social defeat in crickets. Horm. Behav. 66:696–704 [Google Scholar]
  139. Root CM, Ko KI, Jafari A, Wang JW. 2011. Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search. Cell 145:133–44 [Google Scholar]
  140. Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A. et al. 1996. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87:1079–89 [Google Scholar]
  141. Salio C, Lossi L, Ferrini F, Merighi A. 2006. Neuropeptides as synaptic transmitters. Cell Tissue Res 326:583–98 [Google Scholar]
  142. Saudou F, Amlaiky N, Plassat JL, Borrelli E, Hen R. 1990. Cloning and characterization of a Drosophila tyramine receptor. EMBO J 9:3611–17 [Google Scholar]
  143. Scott JP, Fredericson E. 1951. The causes of fighting in mice and rats. Physiol. Zool. 24:273–309 [Google Scholar]
  144. Shaikh MB, Steinberg A, Siegel A. 1993. Evidence that substance P is utilized in medial amygdaloid facilitation of defensive rage behavior in the cat. Brain Res 625:283–94 [Google Scholar]
  145. Shorter J, Couch C, Huang W, Carbone MA, Peiffer J. et al. 2015. Genetic architecture of natural variation in Drosophila melanogaster aggressive behavior. PNAS 112:E3555–63 [Google Scholar]
  146. Siegel A, Pott CB. 1988. Neural substrates of aggression and flight in the cat. Prog. Neurobiol. 31:261–83 [Google Scholar]
  147. Siegel A, Roeling TA, Gregg TR, Kruk MR. 1999. Neuropharmacology of brain-stimulation-evoked aggression. Neurosci. Biobehav. Rev. 23:359–89 [Google Scholar]
  148. Smith JM. 1974. Theory of games and evolution of animal conflicts. J. Theor. Biol. 47:209–21 [Google Scholar]
  149. Smith JM, Parker GA. 1976. The logic of asymmetric contests. Anim. Behav. 24:159–75 [Google Scholar]
  150. Smith JM, Price GR. 1973. Logic of animal conflict. Nature 246:15–18 [Google Scholar]
  151. Starostina E, Liu T, Vijayan V, Zheng Z, Siwicki KK, Pikielny CW. 2012. A Drosophila DEG/ENaC subunit functions specifically in gustatory neurons required for male courtship behavior. J. Neurosci. 32:4665–74 [Google Scholar]
  152. Sternson SM. 2013. Hypothalamic survival circuits: blueprints for purposive behaviors. Neuron 77:810–24 [Google Scholar]
  153. Stevenson PA, Dyakonova V, Rillich J, Schildberger K. 2005. Octopamine and experience-dependent modulation of aggression in crickets. J. Neurosci. 25:1431–41 [Google Scholar]
  154. Stevenson PA, Hofmann HA, Schoch K, Schildberger K. 2000. The fight and flight responses of crickets depleted of biogenic amines. J. Neurobiol. 43:107–20 [Google Scholar]
  155. Stevenson PA, Rillich J. 2015. Adding up the odds—nitric oxide signaling underlies the decision to flee and post-conflict depression of aggression. Sci. Adv. 1:e1500060 [Google Scholar]
  156. Stowers L, Logan DW. 2010. Olfactory mechanisms of stereotyped behavior: on the scent of specialized circuits. Curr. Opin. Neurobiol. 20:274–80 [Google Scholar]
  157. Taghert PH, Nitabach MN. 2012. Peptide neuromodulation in invertebrate model systems. Neuron 76:82–97 [Google Scholar]
  158. Thistle R, Cameron P, Ghorayshi A, Dennison L, Scott K. 2012. Contact chemoreceptors mediate male-male repulsion and male-female attraction during Drosophila courtship. Cell 149:1140–51 [Google Scholar]
  159. Thomas AL, Davis SM, Dierick HA. 2015. Of fighting flies, mice, and men: Are some of the molecular and neuronal mechanisms of aggression universal in the animal kingdom. PLOS Genet 11:e1005416 [Google Scholar]
  160. Tinbergen N. 1951. The Study of Instinct Oxford, UK: Clarendon Press
  161. Toda H, Zhao X, Dickson BJ. 2012. The Drosophila female aphrodisiac pheromone activates ppk23+ sensory neurons to elicit male courtship behavior. Cell Rep. 1:599–607 [Google Scholar]
  162. Trannoy S, Chowdhury B, Kravitz EA. 2015. Handling alters aggression and “loser” effect formation in Drosophila melanogaster. Learn. Mem. 22:64–68 [Google Scholar]
  163. Trannoy S, Penn J, Lucey K, Popovic D, Kravitz EA. 2016. Short and long-lasting behavioral consequences of agonistic encounters between male Drosophila melanogaster. PNAS 113:4818–23 [Google Scholar]
  164. Ueda A, Kidokoro Y. 2002. Aggressive behaviours of female Drosophila melanogaster are influenced by their social experience and food resources. Physiol. Entomol. 27:21–28 [Google Scholar]
  165. Vaaga CE, Borisovska M, Westbrook GL. 2014. Dual-transmitter neurons: functional implications of co-release and co-transmission. Curr. Opin. Neurobiol. 29:25–32 [Google Scholar]
  166. van den Pol AN. 2012. Neuropeptide transmission in brain circuits. Neuron 76:98–115 [Google Scholar]
  167. van der Goes van Naters W, Carlson JR. 2007. Receptors and neurons for fly odors in Drosophila. Curr. Biol. 17:606–12 [Google Scholar]
  168. Van Swinderen B, Andretic R. 2011. Dopamine in Drosophila: setting arousal thresholds in a miniature brain. Proc. R. Soc. B 278:906–13 [Google Scholar]
  169. Vrontou E, Nilsen SP, Demir E, Kravitz EA, Dickson BJ. 2006. fruitless regulates aggression and dominance in Drosophila. Nat. Neurosci. 9:1469–71 [Google Scholar]
  170. Walker SJ, Corrales-Carvajal VM, Ribeiro C. 2015. Postmating circuitry modulates salt taste processing to increase reproductive output in Drosophila. . Curr. Biol. 25:2621–30 [Google Scholar]
  171. Wang L, Anderson DJ. 2010. Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 463:227–31 [Google Scholar]
  172. Wang L, Dankert H, Perona P, Anderson DJ. 2008. A common genetic target for environmental and heritable influences on aggressiveness in Drosophila. PNAS 105:5657–63 [Google Scholar]
  173. Wang L, Han X, Mehren J, Hiroi M, Billeter JC. et al. 2011. Hierarchical chemosensory regulation of male-male social interactions in Drosophila. Nat. Neurosci. 14:757–62 [Google Scholar]
  174. Wang Y, Pu Y, Shen P. 2013. Neuropeptide-gated perception of appetitive olfactory inputs in Drosophila larvae. Cell Rep 3:820–30 [Google Scholar]
  175. Wen T, Parrish CA, Xu D, Wu Q, Shen P. 2005. Drosophila neuropeptide F and its receptor, NPFR1, define a signaling pathway that acutely modulates alcohol sensitivity. PNAS 102:2141–46 [Google Scholar]
  176. Williams MJ, Goergen P, Phad G, Fredriksson R, Schioth HB. 2014. The Drosophila Kctd-family homologue Kctd12-like modulates male aggression and mating behaviour. Eur. J. Neurosci. 40:2513–26 [Google Scholar]
  177. Wiltschko AB, Johnson MJ, Iurilli G, Peterson RE, Katon JM. et al. 2015. Mapping sub-second structure in mouse behavior. Neuron 88:1121–35 [Google Scholar]
  178. Yapici N, Kim YJ, Ribeiro C, Dickson BJ. 2008. A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature 451:33–37 [Google Scholar]
  179. Yu JY, Kanai MI, Demir E, Jefferis GS, Dickson BJ. 2010. Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr. Biol. 20:1602–14 [Google Scholar]
  180. Yuan Q, Song Y, Yang CH, Jan LY, Jan YN. 2014. Female contact modulates male aggression via a sexually dimorphic GABAergic circuit in Drosophila. Nat. Neurosci. 17:81–88 [Google Scholar]
  181. Yurkovic A, Wang O, Basu AC, Kravitz EA. 2006. Learning and memory associated with aggression in Drosophila melanogaster. PNAS 103:17519–24 [Google Scholar]
  182. Zahrt J, Taylor JR, Mathew RG, Arnsten AF. 1997. Supranormal stimulation of D1 dopamine receptors in the rodent prefrontal cortex impairs spatial working memory performance. J. Neurosci. 17:8528–35 [Google Scholar]
  183. Zhou C, Rao Y, Rao Y. 2008. A subset of octopaminergic neurons are important for Drosophila aggression. Nat. Neurosci. 11:1059–67 [Google Scholar]
  184. Zwarts L, Magwire MM, Carbone MA, Versteven M, Herteleer L. et al. 2011. Complex genetic architecture of Drosophila aggressive behavior. PNAS 108:17070–75 [Google Scholar]
  185. Zwarts L, Versteven M, Callaerts P. 2012. Genetics and neurobiology of aggression in Drosophila. Fly 6:35–48 [Google Scholar]
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