Journal of Comparative Physiology A

, Volume 193, Issue 2, pp 181–199 | Cite as

Influences of octopamine and juvenile hormone on locomotor behavior and period gene expression in the honeybee, Apis mellifera

Original Paper

Abstract

Octopamine (OA) and juvenile hormone (JH) are implicated in the regulation of age-based division of labor in the honeybee, Apis mellifera. We tested the hypothesis that these two neuroendocrine signals influence task-associated plasticity in circadian and diurnal rhythms, and in brain expression of the clock gene period (per). Treatment with OA, OA antagonist (epinastine), or both, did not affect the age at onset of circadian rhythmicity or the free running period in constant darkness (DD). Young bees orally treated with OA in light–dark (LD) illumination regime for 6 days followed by DD showed reduced alpha (the period between the daily onset and offset of activity) during the first 4 days in LD and the first 4 days in DD. Oral treatment with OA, epinastine, or both, but not manipulations of JH levels, caused increased average daily levels and aberrant patterns of brain per mRNA oscillation in young bees. These results suggest that OA and JH do not influence the development or function of the central pacemaker but rather that OA influences the brain expression of a clock gene and characteristics of locomotor behavior that are not thought to be under direct control of the circadian pacemaker.

Keywords

Honey bee Circadian rhythms Light Octopamine Clock gene Juvenile hormone Locomotor behavior 

Abbreviations

ANOVA

Analysis of variance

5-HT

Serotonin

CA

Corpora allata

CT

Circadian time

DA

Dopamine

DD

Constant darkness

DHBA

Dihydroxybenzylamine

EF-1α

Elongation factor-1α

Epi

Epinastine

HPLC

High-performance liquid chromatography

FRP

Free running period

JH

Juvenile hormone

LD

Light–dark

Met

Methoprene

OA

Octopamine

PCR

Polymerase chain reaction

Per

Period

RT

Reverse transcription

SCN

Suprachiasmatic nucleus

SS

Sugar syrup

ZT

Zeitgeber time

Supplementary material

359_2006_179_MOESM1_ESM.ppt (38 kb)
Supplementary material

References

  1. Barron AB, Robinson GE (2005) Selective modulation of task performance by octopamine in honey bee (Apis mellifera) division of labour. J Comp Physiol A 191:659–668CrossRefGoogle Scholar
  2. Barron AB, Schulz DJ, Robinson GE (2002) Octopamine modulates responsiveness to foraging-related stimuli in honey bees (Apis mellifera). J Comp Physiol A 188:603–610CrossRefGoogle Scholar
  3. Battelle BA (2002) Circadian efferent input to Limulus eyes: anatomy, circuitry, and impact. Microsc Res Techniq 58:345–355CrossRefGoogle Scholar
  4. Bicker G (1999) Biogenic amines in the brain of the honeybee: cellular distribution, development, and behavioral functions. Microsc Res Techniq 44:166–178CrossRefGoogle Scholar
  5. Bicker G, Menzel R (1989) Chemical codes for the control of behaviour in arthropods. Nature, 337:33–39PubMedCrossRefGoogle Scholar
  6. Bloch G, Robinson GE (2001) Reversal of honeybee behavioural rhythms. Nature 410:1048PubMedCrossRefGoogle Scholar
  7. Bloch G, Toma DP, Robinson GE (2001) Behavioral rhythmicity, age, division of labor and period expression in the honey bee brain. J Biol Rhythms 16:444–456PubMedCrossRefGoogle Scholar
  8. Bloch G, Wheeler DE, Robinson GE (2002a) Endocrine influences on the organization of insect societies. In: Pfaff D, rnold AP, Etgen AM, Fahrbach SE, Rubin RT (eds) Hormones, Brain and Behavior, vol. III, Non-mammalian hormone-behavior systems. Academic, San Diego, pp 195–235Google Scholar
  9. Bloch G, Sullivan JP, Robinson GE (2002b) Juvenile hormone and circadian locomotor activity in the honey bee Apis mellifera. J Insect Physiol 48:1123–1131CrossRefGoogle Scholar
  10. Bloch G, Solomon SM, Robinson GE, Fahrbach SE (2003) Patterns of PERIOD and pigment-dispersing hormone immunoreactivity in the brain of the European honeybee (Apis mellifera): age- and time-related plasticity. J Comp Neurol 464:269–284PubMedCrossRefGoogle Scholar
  11. Bloch G, Rubinstein CD, Robinson GE (2004) Period expression in the honey bee brain is developmentally regulated and not affected by light, flight experience, or colony type. Insect Biochem Mol Biol 34:879–891PubMedCrossRefGoogle Scholar
  12. Bloch G, Shemesh Y, Robinson GE (2006) Seasonal and task-related variation in free running activity rhythms in honey bees (Apis mellifera). Insect Soc 53:115–118CrossRefGoogle Scholar
  13. Burrell BD, Smith BH (1995) Modulation of the honey bee (Apis mellifera) sting response by octopamine. J Insect Physiol 41:671–680CrossRefGoogle Scholar
  14. Chyb S, Hevers W, Forte M, Wolfgang WJ, Selinger Z, Hardie RC (1999) Modulation of the light response by cAMP in Drosophila photoreceptors. J Neurosci 19:8799–8807PubMedGoogle Scholar
  15. Cymborowski B (1998) Serotonin modulates a photic response in circadian locomotor rhythmicity of adults of the blow fly, Calliphora vicina. Physiol Entomol 23:25–32CrossRefGoogle Scholar
  16. Degen J, Gewecke M, Roeder T (2000) Octopamine receptors in the honey bee and locust nervous system: pharmacological similarities between homologous receptors of distantly related species. Br J Pharmacol 130:587–594PubMedCrossRefGoogle Scholar
  17. Drijfhout WJ, van der Linde AG, Kooi SE, Grol CJ, Westerink BHC (1996) Norepinephrine release in the rat pineal gland: the input from the biological clock measured by in vivo microdialysis. J Neurochem 66:748–755PubMedCrossRefGoogle Scholar
  18. Dunlap JC (1999) Molecular bases for circadian clocks. Cell 96:271–290PubMedCrossRefGoogle Scholar
  19. Erber J, Kloppenburg P, Scheidler A (1993) Neuromodulation by serotonin and octopamine in the honeybee—behaviour, neuroanatomy and electrophysiology. Experientia 49:1073–1083CrossRefGoogle Scholar
  20. Franken P, Dudley CA, Estill SJ, Barakat M, Thomason R, O’Hara BF, McKnight SL (2006) NPAS2 as a transcriptional regulator of non-rapid eye movement sleep: genotype and sex interactions. Proc Nat Acad Sci USA 103:7118–7123PubMedCrossRefGoogle Scholar
  21. Fussnecker BL, Smith BH, Mustard JA (2006) Octopamine and tyramine influence the behavioral profile of locomotor activity in the honey bee (Apis mellifera). J Insect Physiol DOI 10.1016/j.jinsphys.2006.07.008 (in press)Google Scholar
  22. Gingras JL, Lawson EE, McNamara MC (1996) Developmental characteristics in the daily rhythm of norepinephrine concentration within rabbit brainstem regions. Reprod Fert Dev 8:189–194CrossRefGoogle Scholar
  23. Giray T, Huang ZY, Guzman-Novoa E, Robinson GE (1999) Physiological correlates of genetic variation for rate of behavioral development in the honeybee, Apis mellifera. Behav Ecol Sociobiol 47:17–28CrossRefGoogle Scholar
  24. Goel N, Governale MM, Jechura TJ, Lee TM (2000) Effects of intergeniculate leaflet lesions on circadian rhythms in Octodon degus. Brain Res 877:306–313PubMedCrossRefGoogle Scholar
  25. Gracioli LF, de Moraes RLMS (2002) Juvenile hormone promotes changes in the expression of hypopharyngeal gland proteins of worker Apis mellifera (Hymenoptera:Apidae). Sociobiology 40:443–448Google Scholar
  26. Hall JC (1998) Genetics of biological rhythms in Drosophila. Adv Genet 38:135–184PubMedCrossRefGoogle Scholar
  27. Huang ZY, Robinson GE, Tobe SS, Yagi KJ, Strambi C, Strambi A, Stay B (1991) Hormonal regulation of behavioural development in the honey bee is based on changes in the rate of juvenile hormone biosynthesis. J Insect Physiol 37:733–742CrossRefGoogle Scholar
  28. Kaiser W, Steiner-Kaiser J (1983) Neuronal correlates of sleep, wakefulness and arousal in a diurnal insect. Nature 301:707–709PubMedCrossRefGoogle Scholar
  29. Kaiser W (1988) Busy bees need rest, too: Behavioral and electromyographical sleep signs in honeybees. J Comp Physiol A 163:565–584CrossRefGoogle Scholar
  30. Khadilkar RV, Mytinger JR, Thomason LE, Runyon SL, Washicosky KJ, Jinks RN (2002) Central regulation of photosensitive membrane turnover in the lateral eye of Limulus. I. Octopamine primes the retina for daily transient rhabdom shedding. Vis Neurosci 19:283–297PubMedCrossRefGoogle Scholar
  31. Klarsfeld A, Leloup JC, Rouyer F (2003) Circadian rhythms of locomotor activity in Drosophila. Behav Proc 64:161–175CrossRefGoogle Scholar
  32. Kloppenburg P, Erber J (1995) The modulatory effects of serotonin and octopamine in the visual system of the honey bee (Apis mellifera l) .2. Electrophysiological analysis of motion-sensitive neurons in the lobula. J Comp Physiol A 176:119–129CrossRefGoogle Scholar
  33. Kubo T, Sasaki M, Nakamura J, Sasagawa H, Ohashi K, Takeuchi H, Natori S (1996) Change in the expression of hypopharyngeal-gland proteins of the worker honeybees (Apis mellifera L.) with age and/or role. J Biochem Tokyo 119:291–295PubMedGoogle Scholar
  34. Lamont EW, Robinson B, Stewart J, Amir S (2005) The central and basolateral nuclei of the amygdala exhibit opposite diurnal rhythms of expression of the clock protein Period2. Proc Nat Acad Sci USA 102:4180–4184PubMedCrossRefGoogle Scholar
  35. Linn CE, Roelofs WL (1986) Modulatory effects of octopamine and serotonin on male sensitivity and periodicity of response to sex pheromones in the cabbage looper moth, Trichoplusia ni. Arch Insect Biochem Physiol 3:161–171CrossRefGoogle Scholar
  36. Linn CE, Roelofs WL (1992) Role of photoperiod cues in regulating the modulatory action of octopamine on pheromone-response thresholds in the cabbage-looper moth. Arc Insect Biochem Physiol 20:285–302CrossRefGoogle Scholar
  37. Linn CE, Campbell MG, Poole KR, Wu WQ, Roelofs WL (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 42:881–891CrossRefGoogle Scholar
  38. Lohse MJ (1993) Molecular mechanisms of membrane receptor desensitization. Biochim Biophys Acta 1179:171–188PubMedCrossRefGoogle Scholar
  39. Maqueira B, Chatwin H, Evans PD (2005) Identification and characterization of a novel family of Drosophila beta-adrenergic-like octopamine G-protein coupled receptors. J Neurochem 94:547–560PubMedCrossRefGoogle Scholar
  40. Menzel R, Muller U (1996) Learning and memory in honeybees: from behavior to neural substrates. Annu Rev Neurosci 19:379–404PubMedCrossRefGoogle Scholar
  41. Meyer-Bernstein EL, Morin LP (1996) Differential serotonergic innervation of the suprachiasmatic nucleus and the intergeniculate leaflet and its role in circadian rhythm modulation. J Neurosci 16:2097–2111PubMedGoogle Scholar
  42. Meyer-Bernstein EL, Blanchard JH, Morin LP (1997) The serotonergic projection from the median raphe nucleus to the suprachiasmatic nucleus modulates activity phase onset, but not other circadian rhythm parameters. Brain Res 25:112–120CrossRefGoogle Scholar
  43. Milde JJ, Homberg U (1984) Ocellar interneurons in the honeybee - characteristics of spiking l-neurons. J Comp Physiol A 155:151–160CrossRefGoogle Scholar
  44. Meinertzhagen IA, Pyza E (1999) Neurotransmitter regulation of circadian structural changes in the fly’s visual system. Microsc Res Techniq 45:96–105CrossRefGoogle Scholar
  45. Mizunami M (1995) Functional diversity of neural organization in insect ocellar systems. Vis Res 35:443–452PubMedCrossRefGoogle Scholar
  46. Moore D (2001) Honey bee circadian clocks: behavioral control from individual workers to whole-colony rhythms. J Insect Physiol 47:843–857CrossRefGoogle Scholar
  47. Moore D, Angel JE, Cheeseman IM, Fahrbach SE, Robinson GE (1998) Timekeeping in the honey bee colony: integration of circadian rhythms and division of labor. Behav Ecol Sociobiol 43:147–160CrossRefGoogle Scholar
  48. Morin LP (1999) Serotonin and the regulation of mammalian circadian rhythmicity. Ann Med 31:12–33PubMedGoogle Scholar
  49. Moritz RFA, Sakofski F (1991) The role of the queen in circadian rhythems of honeybees (Apis mellifera L.). Behav Ecol Sociobiol 29:361–365CrossRefGoogle Scholar
  50. Nakamura TJ, Moriya T, Inoue S, Shimazoe T, Watanabe S, Ebihara S, Shinohara K (2005) Estrogen differentially regulates expression of Per1 and Per2 genes between central and peripheral clocks and between reproductive and nonreproductive tissues in female rats. J Neurosci Res 82:622–630PubMedCrossRefGoogle Scholar
  51. Ohashi K, Natori S, Kubo T (1997) Change in the mode of gene expression of the hypopharyngeal gland cells with an age-dependent role change of the worker honeybee Apis mellifera L. Eur J Biochem 249:797–802PubMedCrossRefGoogle Scholar
  52. Pankiw T, Page RE (2003) Effect of pheromones, hormones, and handling on sucrose response thresholds of honey bees (Apis mellifera L.). J Comp Physiol A 189:675–684CrossRefGoogle Scholar
  53. Peitsch D, Fietz A, Hertel H, Desouza J, Ventura DF, Menzel R (1992) The spectral input systems of hymenopteran insects and their receptor-based color-vision. J Comp Physiol A 170:23–40PubMedCrossRefGoogle Scholar
  54. Perrin JS, Segall LA, Harbour VL, Woodside B, Amir S (2006) The expression of the clock protein PER2 in the limbic forebrain is modulated by the estrous cycle. Proc Nat Acad Sci USA 103:5591–5596PubMedCrossRefGoogle Scholar
  55. Pophof B (2000) Octopamine modulates the sensitivity of silkmoth pheromone receptor neurons. J Comp Physiol A 186:307–313PubMedCrossRefGoogle Scholar
  56. Renner M (1955) Ein Transozeanversuch zum Zeitsinn der Honigbiene. Naturwissenchaften 42:540–541CrossRefGoogle Scholar
  57. Robinson GE (1985) Effects of a juvenile hormone analogue on honey bee foraging behaviour and alarm pheromone production. J Insect Physiol 31:277–282CrossRefGoogle Scholar
  58. Robinson GE (1987) Modulation of alarm pheromone perception in the honey bee: evidence for division of labor based on hormonally regulated response thresholds. J Comp Physiol A 160:613–619CrossRefGoogle Scholar
  59. Robinson GE, Heuser LM, Le Conte Y, Lenquette F, Hollingworth RM (1999) Neurochemicals aid bee nestmate recognition. Nature 399:534–535CrossRefGoogle Scholar
  60. Roeder T (1999) Octopamine in invertebrates. Prog Neurobiol 59:533–561PubMedCrossRefGoogle Scholar
  61. Roeder T (2005) Tyramine and octopamine: ruling behavior and metabolism. Annu Rev Entomol 50:447–477PubMedCrossRefGoogle Scholar
  62. Roeder T, Degen J, Gewecke M (1998) Epinastine, a highly specific antagonist of insect neural octopamine receptors. Eur J Pharmacol 349:171–177PubMedCrossRefGoogle Scholar
  63. Rubin R, Shemesh Y, Cohen M, Elgavish S. Robertson HM, Bloch G (2006) Molecular and phylogenetic analyses reveal mammalian-like clockwork in the honey bee (Apis mellifera) and shed new light on the molecular evolution of the circadian clock. Genome Res 16:1352–1365PubMedCrossRefGoogle Scholar
  64. Saifullah ASM, Tomioka K (2002) Serotonin sets the day state in the neurons that control coupling between the optic lobe circadian pacemakers in the cricket Gryllus bimaculatus. J Exp Biol 205:1305–1314PubMedGoogle Scholar
  65. Sasagawa H, Sasaki M, Okada I (1989) Hormonal-control of the division of labor in adult honeybees (Apis mellifera L). 1. Effect of methoprene on corpora allata and hypopharyngeal gland, and its alpha-glucosidase activity. Appl Entomol Zool 24:66–77Google Scholar
  66. Scheiner R, Pluckhahn S, Oney B, Blenau W, Erber J (2002) Behavioural pharmacology of octopamine, tyramine and dopamine in honey bees. Behav Brain Res 136:545–553PubMedCrossRefGoogle Scholar
  67. Schulz DJ, Robinson GE (1999) Biogenic amines and division of labor in honey bee colonies: behaviorally related changes in antennal lobes and age-related changes in the mushroom bodies. J Comp Physiol A 184:481–488PubMedCrossRefGoogle Scholar
  68. Schulz DJ, Robinson GE (2001) Octopamine influences division of labor in honey bee colonies, J Comp Physiol A 187:53–61PubMedCrossRefGoogle Scholar
  69. Schulz DJ, Barron AB, Robinson GE (2002a). A role for octopamine in honey bee division of labor. Brain Behav Evol 60:350–359CrossRefGoogle Scholar
  70. Schulz DJ, Sullivan JP, Robinson GE (2002b) Juvenile hormone and octopamine in the regulation of division of labor in honey bee colonies. Horm Behav 42:222–231CrossRefGoogle Scholar
  71. Schulz DJ, Elekonich MM, Robinson GE (2003) Biogenic amines in the antennal lobes and the initiation and maintenance of foraging behavior in honey bees. J Neurobiol 54:406–416PubMedCrossRefGoogle Scholar
  72. Shimizu I, Kawai Y, Taniguchi M, Aoki S (2001) Circadian rhythm and cDNA cloning of the clock gene period in the honeybee Apis cerana japonica. Zool Sci 18:779–789CrossRefGoogle Scholar
  73. Sinakevitch I, Niwa M, Strausfeld NJ (2005) Octopamine-like immunoreactivity in the honey bee and cockroach: comparable organization in the brain and subesophageal ganglion. J Comp Neurol 488:233–254PubMedCrossRefGoogle Scholar
  74. Spivak M, Masterman R, Ross R, Mesce KA (2003) Hygienic behavior in the honey bee (Apis mellifera L.) and the modulatory role of octopamine. J Neurobiol 55:341–354PubMedCrossRefGoogle Scholar
  75. Sokal RR, Rohlf FJ (1995) Biometry, 3 edn. W. H. Freeman and Company, New YorkGoogle Scholar
  76. Steenhard BM, Besharse JC (2000) Phase shifting the retinal circadian clock: xPer2 mRNA induction by light and dopamine. J Neurosci 20:8572–8577PubMedGoogle Scholar
  77. Stern M, Thompson KSJ, Zhou P, Watson DG, Midgley JM, Gewecke M, Bacon JP (1995) Octopaminergic neurons in the locust brain—morphological, biochemical and electrophysiological characterization of potential modulators of the visual-system. J Comp Physiol A 177:611–625CrossRefGoogle Scholar
  78. Stevenson PA, Dyakonova V, Rillich J, Schildberger K (2005) Octopamine and experience-dependent modulation of aggression in crickets. J Neurosci 25:1431–1441PubMedCrossRefGoogle Scholar
  79. Su YF, Harden TK, Perkins JP (1980) Catecholamine-specific desensitization of adenylate-cyclase—evidence for a multistep process. J Biol Chem 255:7410–7419PubMedGoogle Scholar
  80. Sullivan JP, Jassim O, Fahrbach SE, Robinson GE (2000) Juvenile hormone paces behavioral development in the adult worker honey bee. Horm Behav 37:1–14PubMedCrossRefGoogle Scholar
  81. Sullivan JP, Fahrbach SE, Harrison JF, Capaldi EA, Fewell JH, Robinson GE (2003) Juvenile hormone and division of labor in honey bee colonies: effects of allatectomy on flight behavior and metabolism. J Exp Biol 206:2287–2296PubMedCrossRefGoogle Scholar
  82. Takahashi S, Yokota S, Hara R, Kobayashi T, Akiyama M, Moriya T, Shibata S (2001) Physical and inflammatory stressors elevate circadian clock gene mPer1 mRNA levels in the paraventricular nucleus of the mouse. Endocrinology 142:4910–4917PubMedCrossRefGoogle Scholar
  83. Terazono H, Mutoh T, Yamaguchi S, Kobayashi M, Akiyama M, Udo R, Ohdo S, Okamura H, Shibata S (2003) Adrenergic regulation of clock gene expression in mouse liver. Proc Nat Acad Sci USA 100:6795–6800PubMedCrossRefGoogle Scholar
  84. Toma DP, Bloch G, Moore D, Robinson GE (2000) Changes in period mRNA levels in the brain and division of labor in honey bee colonies. Proc Nat Acad Sci USA 97:6914–6919PubMedCrossRefGoogle Scholar
  85. Unoki S, Matsumoto Y, Mizunami M (2005) Participation of octopaminergic reward system and dopaminergic punishment system in insect olfactory learning revealed by pharmacological study. Eur J Neurosci 22:1409–1416PubMedCrossRefGoogle Scholar
  86. von Frisch K (1967) The dance language and orientation of bees. Harvard University Press, CambridgeGoogle Scholar
  87. Wagener-Hulme C, Kuehn JC, Schulz DJ, Robinson GE (1999) Biogenic amines and division of labor in honey bee colonies. J Comp Physiol A 184:471–479PubMedCrossRefGoogle Scholar
  88. Williams JA, Sehgal A (2001) Molecular components of the circadian system in Drosophila. Ann Rev Physiol 63:729–755CrossRefGoogle Scholar
  89. Winer J, Jung CKS, Shackel I, Williams PM (1999) Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal Biochem 270:41–49PubMedCrossRefGoogle Scholar
  90. Withers GS, Fahrbach SE, Robinson GE (1995) Effects of experience and juvenile hormone on the organization of the mushroom bodies of honey bees. J Neurobiol 26:130–144PubMedCrossRefGoogle Scholar
  91. Wyatt GR, Davey KG (1996). Cellular and molecular actions of juvenile hormone. II. Roles of juvenile hormone in adult insects. Adv Insect Physiol 26:2–155Google Scholar
  92. Yellman C, Tao H, He B, Hirsh J (1997) Conserved and sexually dimorphic behavioral responses to biogenic amines in decapitated Drosophila. Proc Nat Acad Sci USA 94:4131–4136PubMedCrossRefGoogle Scholar
  93. Yerushalmi S, Bodenhaimer S, Bloch G (2006) Developmentally determined attenuation in circadian rhythms links chronobiology to social organization in bees. J Exp Biol 209:1044–1051PubMedCrossRefGoogle Scholar
  94. Yuan Q, Lin F, Zheng X, Sehgal A (2005) Serotonin modulates circadian entrainment in Drosophila. Neuron 47:115–127PubMedCrossRefGoogle Scholar

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© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Department of Evolution, Systematics, and Ecology, The Alexander Silberman Institute of Life SciencesThe Hebrew University of JerusalemJerusalemIsrael

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