In insects, olfaction plays a crucial role in many behavioral contexts, such as locating food, sexual partners, and oviposition sites. To successfully perform such behaviors, insects must respond to chemical stimuli at the right moment. Insects modulate their olfactory system according to their physiological state upon interaction with their environment. Here, we review the plasticity of behavioral responses to different odor types according to age, feeding state, circadian rhythm, and mating status. We also summarize what is known about the underlying neural and endocrinological mechanisms, from peripheral detection to central nervous integration, and cover neuromodulation from the molecular to the behavioral level. We describe forms of olfactory plasticity that have contributed to the evolutionary success of insects and have provided them with remarkable tools to adapt to their ever-changing environment.


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Literature Cited

  1. Abrieux A, Debernard S, Maria A, Gaertner C, Anton S. 1.  et al. 2013. Involvement of the G-protein-coupled dopamine/ecdysteroid receptor DopEcR in the behavioral response to sex pheromone in an insect. PLOS ONE 8:e72785 [Google Scholar]
  2. Abrieux A, Duportets L, Debernard S, Gadenne C, Anton S. 2.  2014. The GPCR membrane receptor, DopEcR, mediates the actions of both dopamine and ecdysone to control sex pheromone perception in an insect. Front. Behav. Neurosci. 8:312 [Google Scholar]
  3. Addesso KN, McAuslane HJ. 3.  2009. Pepper weevil attraction to volatiles from host and nonhost plants. Environ. Entomol. 38:216–24 [Google Scholar]
  4. Anderson P, Anton S. 4.  2014. Experience-based modulation of behavioural responses to plant volatiles and other sensory cues in insect herbivores. Plant Cell Environ. 37:1826–35 [Google Scholar]
  5. Anton S, Gadenne C. 5.  1999. Effect of juvenile hormone on the central nervous processing of sex pheromone in an insect. PNAS 96:5764–67Describes modulation of antennal lobe sensitivity as a function of age and juvenile hormone titer. [Google Scholar]
  6. Anton S, Homberg U. 6.  1999. Antennal lobe structure. See Ref. 53 98–125
  7. Arnold SEJ, Stevenson PC, Belmain SR. 7.  2012. Odour-mediated orientation of beetles is influenced by age, sex and morph. PLOS ONE 7:e49071 [Google Scholar]
  8. Barron AB, Schulz DJ, Robinson GE. 8.  2002. Octopamine modulates responsiveness to foraging-related stimuli in honey bees (Apis mellifera). J. Comp. Physiol. A 188:603–10 [Google Scholar]
  9. Barrozo RB, Gadenne C, Anton S. 9.  2010. Switching attraction to inhibition: mating-induced reversed role of sex pheromone in an insect. J. Exp. Biol. 213:2933–39Correlates antennal lobe sensitivity changes with a mating-induced behavioral switch in male moths. [Google Scholar]
  10. Barrozo RB, Jarriault D, Deisig N, Gemeno C, Monsempes C. 10.  et al. 2011. Mating-induced differential coding of plant odour and sex pheromone in a male moth. Eur. J. Neurosci. 33:1841–50 [Google Scholar]
  11. Barrozo RB, Jarriault D, Simeone X, Gaertner C, Gadenne C, Anton S. 11.  2010. Mating-induced transient inhibition of responses to sex pheromone in a male moth is not mediated by octopamine or serotonin. J. Exp. Biol. 213:1100–6 [Google Scholar]
  12. Barrozo RB, Lazzari C. 12.  2004. The response of the blood-sucking bug Triatoma infestans to carbon dioxide and other host odours. Chem. Senses 29:319–29 [Google Scholar]
  13. Barrozo RB, Minoli SA, Lazzari CR. 13.  2004. Circadian rhythm of behavioural responsiveness to carbon dioxide in the blood-sucking bug Triatoma infestans (Heteroptera: Reduviidae). J. Insect Physiol. 50:249–54 [Google Scholar]
  14. Bentley MD, Day JF. 14.  1989. Chemical ecology and behavioral aspects of mosquito oviposition. Annu. Rev. Entomol. 34:401–21 [Google Scholar]
  15. Bigot L, Shaik HA, Bozzolan F, Party V, Lucas P. 15.  et al. 2012. Peripheral regulation by ecdysteroids of olfactory responsiveness in male Egyptian cotton leaf worms, Spodoptera littoralis. Insect Biochem. Mol. Biol. 42:22–31 [Google Scholar]
  16. Bodin A, Barrozo RB, Couton L, Lazzari CR. 16.  2008. Temporal modulation and adaptive control of the behavioural response to odours in Rhodnius prolixus. J. Insect Physiol. 54:1343–48Reveals rhythm-dependent orientation toward host and refuge-related odors in fine synchrony with the animal's activities. [Google Scholar]
  17. Bodin A, Vinauger C, Lazzari CR. 17.  2009. Behavioural and physiological state dependency of host seeking in the blood-sucking insect Rhodnius prolixus. J. Exp. Biol. 212:2386–93 [Google Scholar]
  18. Bodin A, Vinauger C, Lazzari CR. 18.  2009. State-dependency of host-seeking in Rhodnius prolixus: the post-ecdysis time. J. Insect Physiol. 55:574–79 [Google Scholar]
  19. Bohbot JD, Durand NF, Vinyard BT, Dickens JC. 19.  2013. Functional development of the octenol response in Aedes aegypti. Front. Physiol. 4:39 [Google Scholar]
  20. Bonizzoni M, Dunn WA, Campbell CL, Olson KE, Dimon MT. 20.  et al. 2011. RNA-seq analyses of blood-induced changes in gene expression in the mosquito vector species, Aedes aegypti. BMC Genomics 12:82 [Google Scholar]
  21. Brady J, Crump AJ. 21.  1978. The control of circadian activity rhythms in tsetse flies: environment or physiological clock?. Physiol. Entomol. 3:177–90 [Google Scholar]
  22. Brevault T, Quilici S. 22.  2010. Flower and fruit volatiles assist host-plant location in the tomato fruit fly Neoceratitis cyanescens. Physiol. Entomol. 35:9–18 [Google Scholar]
  23. Brown MR, Klowden MJ, Crim JW, Young L, Shrouder LA, Lea AO. 23.  1994. Endogenous regulation of mosquito host-seeking behavior by a neuropeptide. J. Insect Physiol. 40:399–406 [Google Scholar]
  24. Busto GUG, Cervantes-Sandoval II, Davis RLR. 24.  2010. Olfactory learning in Drosophila. Annu. Rev. Physiol. 25:338–46 [Google Scholar]
  25. Castrovillo PJ, Cardé RT. 25.  1979. Environmental regulation of female calling and male pheromone responsive periodicities in the codling moth (Laspeyresia pomonella). J. Insect Physiol. 25:659–67 [Google Scholar]
  26. Crnjar R, Yin CM, Stoffolano JG, Barbarossa IT, Liscia A, Angioy AM. 26.  1990. Influence of age on the electroantennogram response of the female blowfly (Phormia regina). J. Insect Physiol. 36:917–21 [Google Scholar]
  27. Das S, Dimopoulos G. 27.  2008. Molecular analysis of light pulse stimulated blood feeding inhibition in Anopheles gambiae. Am. J. Trop. Med. Hyg. 79:333 [Google Scholar]
  28. Davis EE. 28.  1984. Development of lactic acid-receptor sensitivity and host-seeking behaviour in newly emerged female Aedes aegypti mosquitoes. J. Insect Physiol. 30:211–15 [Google Scholar]
  29. Davis EE. 29.  1984. Regulation of sensitivity in the peripheral chemoreceptor systems for host-seeking behaviour by a haemolymph-borne factor in Aedes aegypti. J. Insect Physiol. 30:179–83 [Google Scholar]
  30. de Belle JS, Kanzaki R. 30.  1999. Protocerebral olfactory processing. See Ref. 53 243–81
  31. De Cristofaro A, Ioriatti C, Pasqualini E. 31.  2004. Electrophysiological responses of Cydia pomonella to codlemone and pear ester ethyl (E, Z)-2, 4-decadienoate: peripheral interactions in their perception and evidences for cells responding to both compounds. Bull. Insectol. 57:137–44 [Google Scholar]
  32. Devaud JM, Acebes A, Ramaswami M, Ferrús A. 32.  2003. Structural and functional changes in the olfactory pathway of adult Drosophila take place at a critical age. J. Neurobiol. 56:13–23 [Google Scholar]
  33. Domingue MJ, Roelofs WL, Linn CE, Baker TC. 33.  2006. Effects of egg-to-adult development time and adult age on olfactory neuron response to semiochemicals in European corn borers. J. Insect Physiol. 52:975–83 [Google Scholar]
  34. Dukas R. 34.  2008. Evolutionary biology of insect learning. Annu. Rev. Entomol. 53:145–60 [Google Scholar]
  35. Duportets L, Barrozo RB, Bozzolan F, Gaertner C, Anton S. 35.  et al. 2010. Cloning of an octopamine/tyramine receptor and plasticity of its expression as a function of adult sexual maturation in the male moth Agrotis ipsilon. Insect Mol. Biol. 19:489–99 [Google Scholar]
  36. Duportets L, Dufour MC, Couillaud F, Gadenne C. 36.  1998. Biosynthetic activity of corpora allata, growth of sex accessory glands and mating in the male moth Agrotis ipsilon (Hufnagel). J. Exp. Biol. 201:2425–32 [Google Scholar]
  37. Duportets L, Maria A, Vitecek S, Gadenne C, Debernard S. 37.  2013. Steroid hormone signaling is involved in the age-dependent behavioral response to sex pheromone in the adult male moth Agrotis ipsilon. Gen. Comp. Endocrinol. 186:58–66 [Google Scholar]
  38. Edgecomb RS, Harth CE, Schneiderman AM. 38.  1994. Regulation of feeding behavior in adult Drosophila melanogaster varies with feeding regime and nutritional state. J. Exp. Biol. 197:215–35 [Google Scholar]
  39. Farhadian SF, Suarez-Farinas M, Cho CE, Pellegrino M, Vosshall LB. 39.  2012. Post-fasting olfactory, transcriptional, and feeding responses in Drosophila. Physiol. Behav. 105:544–53 [Google Scholar]
  40. Fernandez NM, Klowden MJ. 40.  1995. Male accessory gland substances modify the host-seeking behavior of gravid Aedes aegypti mosquitoes. J. Insect Physiol. 41:965–70 [Google Scholar]
  41. Fletcher BS, Giannakakis A. 41.  1973. Factors limiting the response of females of the Queensland fruit fly, Dacus tryoni, to the sex pheromone of the male. J. Insect Physiol. 19:1147–55 [Google Scholar]
  42. Fox AN, Pitts RJ, Robertson HM, Carlson JR, Zwiebel LJ. 42.  2001. Candidate odorant receptors from the malaria vector mosquito Anopheles gambiae and evidence of down-regulation in response to blood feeding. PNAS 98:14693–97 [Google Scholar]
  43. Gadenne C, Anton S. 43.  2000. Central processing of sex pheromone stimuli is differentially regulated by juvenile hormone in a male moth. J. Insect Physiol. 46:1195–206 [Google Scholar]
  44. Gadenne C, Dufour MC, Anton S. 44.  2001. Transient post-mating inhibition of behavioural and central nervous responses to sex pheromone in an insect. Proc. R. Soc. B 268:1631–35 [Google Scholar]
  45. Gadenne C, Renou M, Sreng L. 45.  1993. Hormonal control of sex pheromone responsiveness in the male black cutworm, Agrotis ipsilon. Experientia 49:721–24 [Google Scholar]
  46. Galizia CG, Szyszka P. 46.  2008. Olfactory coding in the insect brain: molecular receptive ranges, spatial and temporal coding. Entomol. Exp. Appl. 128:81–92 [Google Scholar]
  47. Grant AJ, O'Connell RJ. 47.  2007. Age-related changes in female mosquito carbon dioxide detection. J. Med. Entomol. 44:617–23 [Google Scholar]
  48. Greiner B, Gadenne C, Anton S. 48.  2002. Central processing of plant volatiles in Agrotis ipsilon males is age-independent in contrast to sex pheromone processing. Chem. Senses 27:45–48 [Google Scholar]
  49. Groh C, Ahrens D, Rössler W. 49.  2006. Environment- and age-dependent plasticity of synaptic complexes in the mushroom bodies of honeybee queens. Brain Behav. Evol. 68:1–14 [Google Scholar]
  50. Groh C, Lu Z, Meinertzhagen IA, Rössler W. 50.  2012. Age-related plasticity in the synaptic ultrastructure of neurons in the mushroom body calyx of the adult honeybee Apis mellifera. J. Comp. Neurol. 520:3509–27Provides evidence for age-dependent synaptic plasticity in mushroom bodies in honey bees. [Google Scholar]
  51. Gronenberg W, Heeren S, Hölldobler B. 51.  1996. Age-dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus. J. Exp. Biol. 199:2011–19 [Google Scholar]
  52. Grotewiel MS, Martin I, Bhandari P, Cook-Wiens E. 52.  2005. Functional senescence in Drosophila melanogaster. Ageing Res. Rev. 4:372–97 [Google Scholar]
  53. Hansson BS. 53.  1999. Insect Olfaction Berlin: Springer
  54. Hansson BS, Christensen TA. 54.  1999. Functional characteristics of the antennal lobe. See Ref. 53 126–64
  55. Haynes KF, Birch MC. 55.  1984. The periodicity of pheromone release and male responsiveness in the artichoke plume moth, Platyptilia carduidactyla. Physiol. Entomol. 9:287–95 [Google Scholar]
  56. Homberg U, Müller U. 56.  1999. Neuroactive substances in the antennal lobe. See Ref. 53 181–207
  57. Huetteroth W, Schachtner J. 57.  2005. Standard three-dimensional glomeruli of the Manduca sexta antennal lobe: a tool to study developmental and adult neuronal plasticity. Cell Tissue Res. 319:513–24 [Google Scholar]
  58. Ignell R, Couillaud F, Anton S. 58.  2001. Juvenile-hormone-mediated plasticity of aggregation behaviour and olfactory processing in adult desert locusts. J. Exp. Biol. 204:249–59 [Google Scholar]
  59. Jacquin-Joly E, Lucas P. 59.  2005. Pheromone reception and transduction: mammals and insects illustrate converging mechanisms across phyla. Curr. Topics Neurochem. 4:75–105 [Google Scholar]
  60. Jang EB. 60.  1995. Effects of mating and accessory gland injections on olfactory-mediated behavior in the female Mediterranean fruit fly, Ceratitis capitata. J. Insect Physiol. 41:705–10Reveals a role of sex accessory glands in postmating behavioral changes in female fruit flies. [Google Scholar]
  61. Jang EB. 61.  2002. Physiology of mating behavior in Mediterranean fruit fly (Diptera: Tephritidae): chemoreception and male accessory gland fluids in female post-mating behavior. Fla. Entomol. 85:89–93 [Google Scholar]
  62. Jarriault D, Barrozo RB, de Carvalho Pinto CJ, Greiner B, Dufour MC. 62.  et al. 2009. Age-dependent plasticity of sex pheromone response in the moth, Agrotis ipsilon: combined effects of octopamine and juvenile hormone. Horm. Behav. 56:185–91 [Google Scholar]
  63. Katsoyannos BI. 63.  1982. Male sex pheromone of Rhagoletis cerasi L. (Diptera, Tephritidae): factors affecting release and response and its role in the mating behavior. Z. Angew. Entomol. 94:187–98 [Google Scholar]
  64. Keil TA. 64.  1999. Morphology and development of the peripheral olfactory organs. See Ref. 53 5–48
  65. Klowden MJ. 65.  1990. The endogenous regulation of mosquito reproductive behavior. Experientia 46:660–70 [Google Scholar]
  66. Klowden MJ. 66.  1997. Endocrine aspects of mosquito reproduction. Arch. Insect Biochem. Physiol. 35:491–512 [Google Scholar]
  67. Klowden MJ. 67.  2001. Sexual receptivity in Anopheles gambiae mosquitoes: absence of control by male accessory gland substances. J. Insect Physiol. 47:661–66 [Google Scholar]
  68. Klowden MJ, Blackmer JL. 68.  1987. Humoral control of preoviposition behavior in the mosquito, Aedes aegypti. J. Insect Physiol. 33:689–92 [Google Scholar]
  69. Klowden MJ, Lea AO. 69.  1979. Abdominal distention terminates subsequent host-seeking behaviour of Aedes aegypti following a blood meal. J. Insect Physiol. 25:583–85 [Google Scholar]
  70. Klowden MJ, Lea AO. 70.  1979. Humoral inhibition of host-seeking in Aedes aegypti during oocyte maturation. J. Insect Physiol. 25:231–35 [Google Scholar]
  71. Krishnan B, Dryer SE, Hardin PE. 71.  1999. Circadian rhythms in olfactory responses of Drosophila melanogaster. Nature 400:375–78 [Google Scholar]
  72. Kromann SH, Saveer AM, Binyameen M, Bengtsson M, Birgersson G. 72.  et al. 2014. Concurrent modulation of neuronal and behavioural olfactory responses to sex and host plant cues in a male moth. Proc. R. Soc. B 282:20141884 [Google Scholar]
  73. Landolt PJ, Heath RR. 73.  1988. Effects of age, mating, and time of day on behavioral-responses of female papaya fruit fly, Toxotrypana curvicauda Gerstaecker (Diptera, Tephritidae), to synthetic sex pheromone. Environ. Entomol. 17:47–51 [Google Scholar]
  74. Lange A, Orchard I, Barrett FM. 74.  1989. Changes in hemolymph serotonin levels associated with feeding in the bloodsucking bug, Rhodnius prolixus. J. Insect Physiol. 35:393–99 [Google Scholar]
  75. Latorre-Estivalis JM, Omondi BA, DeSouza O, Oliveira IHR, Ignell R, Lorenzo MG. 75.  2015. Molecular basis of peripheral olfactory plasticity in Rhodnius prolixus, a Chagas disease vector. Front. Ecol. Evol. 3:74 [Google Scholar]
  76. Liang DS, Schal C. 76.  1990. Circadian rhythmicity and development of the behavioral-response to sex-pheromone in male brown-banded cockroaches, Supella longipalpa. Physiol. Entomol. 15:355–61 [Google Scholar]
  77. Lightle D, Ambrosino M, Lee JC. 77.  2010. Sugar in moderation: Sugar diets affect short-term parasitoid behaviour. Physiol. Entomol. 35:179–85 [Google Scholar]
  78. Linn CE, Campbell MG, Poole KR, Wu W-Q, Roelofs WL. 78.  1996. Effects of photoperiod on the circadian timing of pheromone response in male Trichoplusia ni: relationship to the modulatory action of octopamine. J. Insect Physiol. 42:881–91 [Google Scholar]
  79. Linn CE, Campbell MG, Roelofs WL. 79.  1992. Photoperiod cues and the modulatory action of octopamine and 5-hydroxytryptamine on locomotor and pheromone in male gypsy moths, Lymantria dispar. Arch. Insect Biochem. Physiol. 20:265–84 [Google Scholar]
  80. Liu R, Lehane S, He X, Lehane M, Hertz-Fowler C. 80.  et al. 2010. Characterisations of odorant-binding proteins in the tsetse fly Glossina morsitans morsitans. Cell. Mol. Life Sci. 67:919–29 [Google Scholar]
  81. Lorenzo MG, Lazzari CR. 81.  1998. Activity pattern in relation to refuge exploitation and feeding in Triatoma infestans (Hemiptera: Reduviidae). Acta Trop. 70:163–70 [Google Scholar]
  82. Luo S, Michaud JP, Li J, Liu X, Zhang Q. 82.  2013. Odor learning in Microplitis mediator (Hymenoptera: Braconidae) is mediated by sugar type and physiological state. Biol. Control 65:207–11 [Google Scholar]
  83. Marinotti O, Calvo E, Nguyen QK, Dissanayake S, Ribeiro JMC, James AA. 83.  2006. Genome-wide analysis of gene expression in adult Anopheles gambiae. Insect Mol. Biol. 15:1–12 [Google Scholar]
  84. Martel V, Anderson P, Hansson BS, Schlyter F. 84.  2009. Peripheral modulation of olfaction by physiological state in the Egyptian leaf worm Spodoptera littoralis (Lepidoptera: Noctuidae). J. Insect Physiol. 55:793–97 [Google Scholar]
  85. Masante-Roca I, Anton S, Delbac L, Dufour M-C, Gadenne C. 85.  2007. Attraction of the grapevine moth to host and non-host plant parts in the wind tunnel: effects of plant phenology, sex, and mating status. Entomol. Exp. Appl. 122:239–45 [Google Scholar]
  86. McQuillan HJ, Barron AB, Mercer AR. 86.  2012. Age- and behaviour-related changes in the expression of biogenic amine receptor genes in the antennae of honey bees (Apis mellifera). J. Comp. Physiol. A 198:753–61 [Google Scholar]
  87. Mechaber WL, Capaldo CT, Hildebrand JG. 87.  2002. Behavioral responses of adult female tobacco hornworms, Manduca sexta, to host plant volatiles change with age and mating status. J. Insect Sci. 2:5 [Google Scholar]
  88. Merlin C, Francois M-C, Queguiner I, Maibeche-Coisne M, Jacquin-Joly E. 88.  2006. Evidence for a putative antennal clock in Mamestra brassicae: molecular cloning and characterization of two clock genes—period and cryptochrome—in antennae. Insect Mol. Biol. 15:137–45 [Google Scholar]
  89. Merlin C, Lucas P, Rochat D, François M, Maïbèche-Coisne M, Jacquin-Joly E. 89.  2007. An antennal circadian clock and circadian rhythms in peripheral pheromone reception in the moth Spodoptera littoralis. J. Biol. Rhythms 22:502–14Shows a circadian rhythm of expression of clock genes in the moth antenna and brain. [Google Scholar]
  90. Naccarati C, Audsley N, Keen JN, Kim J-H, Howell GJ. 90.  et al. 2012. The host-seeking inhibitory peptide, Aea-HP-1, is made in the male accessory gland and transferred to the female during copulation. Peptides 34:150–57 [Google Scholar]
  91. Nässel DR. 91.  1988. Serotonin and serotonin-immunoreactive neurons in the nervous system of insects. Prog. Neurobiol. 30:1–85 [Google Scholar]
  92. Niven JE, Laughlin SB. 92.  2008. Energy limitation as a selective pressure on the evolution of sensory systems. J. Exp. Biol. 211:1792–804 [Google Scholar]
  93. Otter CJD, Tchikaya T, Schutte AM. 93.  1991. Effects of age, sex and hunger on the antennal olfactory sensitivity of tsetse flies. Physiol. Entomol. 16:173–82 [Google Scholar]
  94. Page TL, Koelling E. 94.  2003. Circadian rhythm in olfactory response in the antennae controlled by the optic lobe in the cockroach. J. Insect Physiol. 49:697–707 [Google Scholar]
  95. Payne TL, Shorey HH, Gaston LK. 95.  1970. Sex pheromones of noctuid moths: factors influencing antennal responsiveness in males of Trichoplusia ni. J. Insect Physiol. 16:1043–55 [Google Scholar]
  96. Pearson GA, Schal C. 96.  1999. Electroantennogram responses of both sexes of grape root borer (Lepidoptera: Sesiidae) to synthetic female sex pheromone. Environ. Entomol. 28:943–46 [Google Scholar]
  97. Pham-Delegue MH, Trouiller J, Caillaud CM, Roger B, Masson C. 97.  1993. Effect of queen pheromone on worker bees of different ages: behavioural and electrophysiological responses. Apidologie 24:267–81 [Google Scholar]
  98. Qiu YT, van Loon JJA, Takken W, Meijerink J, Smid HM. 98.  2006. Olfactory coding in antennal neurons of the malaria mosquito, Anopheles gambiae. Chem. Senses 31:845–63 [Google Scholar]
  99. Randlkofer B, Obermaier E, Meiners T. 99.  2007. Mother's choice of the oviposition site: balancing risk of egg parasitism and need of food supply for the progeny with an infochemical shelter?. Chemoecology 17:177–86 [Google Scholar]
  100. Reddy GVP, Guerrero A. 100.  2000. Behavioral responses of the diamondback moth, Plutella xylostella, to green leaf volatiles of Brassica oleracea subsp. capitata. J. Agric. Food Chem. 48:6025–29 [Google Scholar]
  101. Reisenman CE. 101.  2014. Hunger is the best spice: effects of starvation in the antennal responses of the blood-sucking bug Rhodnius prolixus. J. Insect Physiol. 71:8–13Shows effects of starvation and day/night conditions on bugs' antennal responses to host odors. [Google Scholar]
  102. Reisenman CE, Lee Y, Gregory T, Guerenstein PG. 102.  2013. Effects of starvation on the olfactory responses of the blood-sucking bug Rhodnius prolixus. J. Insect Physiol. 59:717–21 [Google Scholar]
  103. Rinker DC, Pitts RJ, Zhou X, Suh E, Rokas A. 103.  et al. 2013. Blood meal-induced changes to antennal transcriptome profiles reveal shifts in odor sensitivities in Anopheles gambiae. PNAS 110:8260–65 [Google Scholar]
  104. Root CM, Ko KI, Jafari A, Wang JW. 104.  2011. Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search. Cell 145:133–44 [Google Scholar]
  105. Rospars JP. 105.  1988. Structure and development of the insect antennodeutocerebral system. Int. J. Insect Morphol. Embryol. 17:243–94 [Google Scholar]
  106. Rund SSC, Bonar NA, Champion MM, Ghazi JP, Houk CM. 106.  et al. 2013. Daily rhythms in antennal protein and olfactory sensitivity in the malaria mosquito Anopheles gambiae. Sci. Rep. 3:2494 [Google Scholar]
  107. Rund SSC, Gentile JE, Duffield GE. 107.  2013. Extensive circadian and light regulation of the transcriptome in the malaria mosquito Anopheles gambiae. BMC Genomics 14:218 [Google Scholar]
  108. Rund SSC, Hou TY, Ward SM, Collins FH, Duffield GE. 108.  2011. Genome-wide profiling of diel and circadian gene expression in the malaria vector Anopheles gambiae. PNAS 108:E421–30 [Google Scholar]
  109. Ruther J, Stahl LM, Steiner S, Garbe LA, Tolasch T. 109.  2007. A male sex pheromone in a parasitic wasp and control of the behavioral response by the female's mating status. J. Exp. Biol. 210:2163–69 [Google Scholar]
  110. Saveer AM, Kromann SH, Birgersson G, Bengtsson M, Lindblom T. 110.  et al. 2012. Floral to green: Mating switches moth olfactory coding and preference. Proc. R. Soc. B 279:2314–22Demonstrates differential changes in plant odor attraction after mating in female moths. [Google Scholar]
  111. Schuckel J, Siwicki KK, Stengl M. 111.  2007. Putative circadian pacemaker cells in the antenna of the hawkmoth Manduca sexta. Cell Tissue Res. 330:271–78 [Google Scholar]
  112. Seabrook WD, Hirai K, Shorey HH, Gaston LK. 112.  1979. Maturation and senescence of an insect chemosensory response. J. Chem. Ecol. 5:587–94 [Google Scholar]
  113. Seid MA, Traniello JFA. 113.  2006. Age-related repertoire expansion and division of labor in Pheidole dentata (Hymenoptera: Formicidae): a new perspective on temporal polyethism and behavioral plasticity in ants. Behav. Ecol. Sociobiol. 60:631–44 [Google Scholar]
  114. Sengupta P. 114.  2013. The belly rules the nose: feeding state-dependent modulation of peripheral chemosensory responses. Curr. Opin. Neurobiol. 23:68–75Reviews neuromodulatory mechanisms underlying feeding state–dependent behavior and signal detection. [Google Scholar]
  115. Shorey HH, Morin KL, Gaston LK. 115.  1968. Sex pheromones of noctuid moths. XV. Timing of development of pheromone-responsiveness and other indicators of reproductive age in males of eight species. Ann. Entomol Soc. Am. 61:857–61 [Google Scholar]
  116. Siju KP, Hansson B, Ignell R. 116.  2008. Immunocytochemical localization of serotonin in the central and peripheral chemosensory system of mosquitoes. Arthropod Struct. Dev. 37:248–59 [Google Scholar]
  117. Siju KP, Hill SR, Hansson BS, Ignell R. 117.  2010. Influence of blood meal on the responsiveness of olfactory receptor neurons in antennal sensilla trichodea of the yellow fever mosquito, Aedes aegypti. J. Insect Physiol. 56:659–65 [Google Scholar]
  118. Silvegren G, Löfstedt C, Rosen WQ. 118.  2005. Circadian mating activity and effect of pheromone pre-exposure on pheromone response rhythms in the moth Spodoptera littoralis. J. Insect Physiol. 51:277–86 [Google Scholar]
  119. Takken W, van Loon J, Adam W. 119.  2001. Inhibition of host-seeking response and olfactory responsiveness in Anopheles gambiae following blood feeding. J. Insect Physiol. 47:303–10 [Google Scholar]
  120. Tanoue S, Krishnan P, Krishnan B, Dryer SE, Hardin PE. 120.  2004. Circadian clocks in antennal neurons are necessary and sufficient for olfaction rhythms in Drosophila. Curr. Biol. 14:638–49 [Google Scholar]
  121. Turgeon JJ, McNeil JN, Roelofs WL. 121.  1983. Responsiveness of Pseudaletia unipuncta males to the female sex pheromone. Physiol. Entomol. 8:339–44 [Google Scholar]
  122. Van der Goes van Naters WM, Den Otter CJ, Maes FW. 122.  1998. Olfactory sensitivity in tsetse flies: a daily rhythm. Chem. Senses 23:351–57 [Google Scholar]
  123. Vergoz V, McQuillan HJ, Geddes LH, Pullar K, Nicholson BJ. 123.  et al. 2009. Peripheral modulation of worker bee responses to queen mandibular pheromone. PNAS 106:20930–35Reveals dopamine-induced peripheral modulation of honey bee worker responses to queen mandibular pheromone. [Google Scholar]
  124. Vitecek S, Maria A, Blais C, Duportets L, Gaertner C. 124.  et al. 2013. Is the rapid post-mating inhibition of pheromone response triggered by ecdysteroids or other factors from the sex accessory glands in the male moth Agrotis ipsilon?. Horm. Behav. 63:700–8 [Google Scholar]
  125. Wang S, Zhang S, Sato K, Srinivasan MV. 125.  2005. Maturation of odor representation in the honeybee antennal lobe. J. Insect Physiol. 51:1244–54 [Google Scholar]
  126. Warnes ML, Finlayson LH. 126.  1986. Electroantennogram responses of the stable fly, Stomoxys calcitrans, to carbon dioxide and other odors. Physiol. Entomol. 11:469–73 [Google Scholar]
  127. Wilson RI, Mainen ZF. 127.  2006. Early events in olfactory processing. Annu. Rev. Neurosci. 29:163–201 [Google Scholar]
  128. Winnington AP, Napper RM, Mercer AR. 128.  1996. Structural plasticity of identified glomeruli in the antennal lobes of the adult worker honey bee. J. Comp. Neurol. 365:479–90 [Google Scholar]
  129. Worster AS, Seabrook WD. 129.  1989. Electrophysiological investigation of diel variations in the antennal sensitivity of the male spruce budworm moth Choristoneura fumiferana (Lepidoptera: Tortricidae). J. Insect Physiol. 35:1–5 [Google Scholar]
  130. Wyatt TD. 130.  2014. Pheromones and Animal Behavior Cambridge, UK: Cambridge Univ. Press
  131. Yeh C, Klowden MJ. 131.  1990. Effects of male accessory gland substances on the pre-oviposition behaviour of Aedes aegypti mosquitoes. J. Insect Physiol. 36:799–803 [Google Scholar]
  132. Zhukovskaya MI. 132.  1995. Circadian rhythm of sex pheromone perception in the male American cockroach, Periplaneta americana L. J. Insect Physiol. 41:941–46 [Google Scholar]

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