Neural and hormonal control of postecdysial behaviors in insects

Annual Review of Entomology

Volumn 59, Issue , 2014, Pages 363-381

  White, Benjamin H ^a   Ewer, John ^b  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b UNIVERSIDAD DE VALPARAÍSO   (Chile)

Author keywords

Bursicon; Drosophila; Ecdysis; Neuroendocrine; Neuroethology; Wing expansion

Indexed keywords

INSECT HORMONE;

ANIMAL; DROSOPHILA MELANOGASTER; FORELIMB; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLTING; NEUROSECRETION;

ANIMALS; DROSOPHILA MELANOGASTER; INSECT HORMONES; MOLTING; NEUROSECRETORY SYSTEMS; WING;

EID: 84891952890     PISSN: 00664170     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-ento-011613-162028     Document Type: Article

References (65)

1. Ampleford EJ, Steel CGH. 1982. The behavior of Rhodnius prolixus (Stål) during the imaginal ecdysis. Can. J. Zool. 60:168-74
2. Arakane Y, Li B,Muthukrishnan S, Beeman RW, Kramer KJ, Park Y. 2008. Functional analysis of four neuropeptides, EH, ETH, CCAP and bursicon, and their receptors in adult ecdysis behavior of the red flour beetle, Tribolium castaneum. Mech. Dev. 125:984-95
3. Baker JD, McNabb SL, Truman JW. 1999. The hormonal coordination of behavior and physiology at adult ecdysis in Drosophila melanogaster. J. Exp. Biol. 202:3037-48
4. Baker JD, Truman JW. 2002. Mutations in the Drosophila glycoprotein hormone receptor, rickets, eliminate neuropeptide-induced tanning and selectively block a stereotyped behavioral program. J. Exp. Biol. 205:2555-65
5. Carlson Jr. 1977. Imaginal ecdysis of the cricket (Teleogryllus oceanicus). 1. Organization ofmotor programs and roles of central and sensory control. J. Comp. Physiol. A 115:299-317
6. Carlson JR, Bentley D. 1977. Ecdysis: Neural orchestration of a complex behavioral performance. Science 195:1006-8
7. Carlson JR, Ogara BA. 1983. The ecdysis of the cricket, Teleogryllus oceanicus: Generation of the pharyngeal air-swallowing motor program by the isolated frontal ganglion. Comp. Biochem. Physiol. A 75:579-87
8. Chang JC, Yang RB, Adams ME, Lu KH. 2009. Receptor guanylyl cyclases in Inka cells targeted by eclosion hormone. Proc. Natl. Acad. Sci. USA 106:13371-76
9. Clark AC, Del Campo M, Ewer J. 2004. Neuroendocrine control of larval ecdysis behavior in Drosophila: Complex regulation by partially redundant neuropeptides. J. Neurosci. 24:4283-92
10. Cottrell CB. 1962. General observations on the imaginal ecdysis of blow flies. Trans. R. Entomol. Soc. Lond. 114:317-33
11. Cottrell CB. 1964. Insect ecdysis with particular emphasis on cuticular hardening and darkening. Adv. Insect Physiol. 2:175-218
12. Dai L, Dewey EM, Zitnan D, Luo CW,HoneggerHW, AdamsME. 2008. Identification, developmental expression, and functions of bursicon in the tobacco hawkmoth, Manduca sexta. J. Comp. Neurol. 506:759-74
13. Davis NT, Homberg U, Dircksen H, Levine RB, Hildebrand JG. 1993. Crustacean cardioactive peptideimmunoreactive neurons in the hawkmoth Manduca sexta and changes in their immunoreactivity during postembryonic development. J. Comp. Neurol. 338:612-27
14. Delachambre J, Delbecque JP, Provansal A, Dereggi ML, Cailla H. 1979. Induction of epidermal cyclicamp by bursicon in mealworm, Tenebrio molitor. Experientia 35:701-2
15. Denlinger DL, Zdarek J. 1994. Metamorphosis behavior of flies. Annu. Rev. Entomol. 39:243-66
16. Dewey EM, McNabb SL, Ewer J, Kuo GR, Takanishi CL, et al. 2004. Identification of the gene encoding bursicon, an insect neuropeptide responsible for cuticle sclerotization and wing spreading. Curr. Biol. 14:1208-13
17. Diao F, White BH. 2012. A novel approach for directing transgene expression in Drosophila: T2A-Gal4 in-frame fusion. Genetics 190:1139-44
18. Eidmann H. 1924. Untersuchungen über Wachstum und Häutung der Insekten. Z. Wiss. Biol. Morphol. Oekol. 2:567-610
19. Ewer J, De Vente J, Truman JW. 1994. Neuropeptide induction of cyclic GMP increases in the insect CNS: Resolution at the level of single identifiable neurons. J. Neurosci. 14:7704-12
20. Ewer J, Reynolds S. 2002. Neuropeptide control of molting in insects. In Hormones, Brain and Behavior, ed.DWPfaff, AP Arnold, SE Fahrbach, AMEtgen, RT Rubin, pp. 1-92. San Diego, CA: Academic
21. Ewer J, Truman JW. 1996. Increases in cyclic 3,5-guanosine monophosphate (cGMP) occur at ecdysis in an evolutionarily conserved crustacean cardioactive peptide-immunoreactive insect neuronal network. J. Comp. Neurol. 370:330-41
22. Fraenkel G. 1935. Observations and experiments on the blow-fly (Calliphora erythrocephala) during the first day after emergence. Proc. Zool. Soc. Lond. 105:893-904
23. Fraenkel G, Hsiao C. 1965. Bursicon, a hormone which mediates tanning of the cuticle in the adult fly and other insects. J. Insect Physiol. 11:513-56
24. Fuse M, Truman JW. 2002. Modulation of ecdysis in the moth Manduca sexta: The roles of the suboesophageal and thoracic ganglia. J. Exp. Biol. 205:1047-58
25. Gammie SC, Truman JW. 1997. Neuropeptide hierarchies and the activation of sequential motor behaviors in the hawkmoth, Manduca sexta. J. Neurosci. 17:4389-97
26. Honegger HW, Dewey EM, Ewer J. 2008. Bursicon, the tanning hormone of insects: Recent advances following the discovery of its molecular identity. J. Comp. Physiol. A 194:989-1005
27. Huang J, Zhang Y, Li M, Wang S, Liu W, et al. 2007. RNA interference-mediated silencing of the bursicon gene induces defects in wing expansion of silkworm. FEBS Lett. 581:697-701
28. Hughes TD. 1980. Imaginal ecdysis of the desert locust, Schistocerca gregaria. 1. Description of the behavior. Physiol. Entomol. 5:47-54
29. Hughes TD. 1980. Imaginal ecdysis of the desert locust, Schistocerca gregaria. 2.Motor-Activity underlying the pre-emergence and emergence behavior. Physiol. Entomol. 5:55-71
30. Kammer AE, Kinnamon SC. 1977. Patterned muscle activity during eclosion in the hawkmoth Manduca sexta. J. Comp. Physiol. 114:313-26
31. Kim YJ, Spalovska-Valachova I, Cho KH, Zitnanova I, Park Y, et al. 2004. Corazonin receptor signaling in ecdysis initiation. Proc. Natl. Acad. Sci. USA 101:6704-9
32. Kim YJ, Zitnan D, ChoKH, Schooley DA, Mizoguchi A, AdamsME. 2006. Central peptidergic ensembles associated with organization of innate behavior. Proc. Natl. Acad. Sci. USA 103:14211-16
33. Lahr E, Dean D, Ewer J. 2012. Genetic analysis of ecdysis behavior in Drosophila reveals partially overlapping functions of two unrelated neuropeptides. J. Neurosci. 32:6819-29
34. Luan H, Diao F, Peabody NC, White BH. 2012. Command and compensation in a neuromodulatory decision network. J. Neurosci. 32:880-89
35. LuanH, Lemon WC, Peabody NC, Pohl JB, Zelensky PK, et al. 2006. Functional dissection of a neuronal network required for cuticle tanning and wing expansion in Drosophila. J. Neurosci. 26:573-84
36. Luo C-W, Dewey EM, Sudo S, Ewer J, Hsu SY, et al. 2005. Bursicon, the insect cuticle hardening hormone, is a heterodimeric cystine knot protein that activates G protein-coupled receptor LGR2. Proc. Natl. Acad. Sci. USA 102:2820-25
37. McNabb SL, Baker JD, Agapite J, Steller H, Riddiford LM, Truman JW. 1997. Disruption of behavioral sequence by targeted death of peptidergic neurons in Drosophila. Neuron 19:813-23
38. Mendive FM, Van Loy T, Claeysen S, Poels J, Williamson M, et al. 2005. Drosophila molting neurohormone bursicon is a heterodimer and the natural agonist of the orphan receptor DLGR2. FEBS Lett. 579:2171-76
39. Miles CI, Booker R. 1998. The role of the frontal ganglion in the feeding and eclosion behavior of the moth Manduca sexta. J. Exp. Biol. 201:1785-98
40. Mills RR, Mathur RB, Guerra AA. 1965. Studies on the hormonal control of tanning in the American cockroach: I. Release of an activation factor from the terminal abdominal ganglion. J. Insect Physiol. 11:1047-53
41. Park JH, Schroeder AJ, Helfrich-Förster C, Jackson FR, Ewer J. 2003. Targeted ablation of CCAP neuropeptide-containing neurons of Drosophila causes specific defects in execution and circadian timing of ecdysis behavior. Development 130:2645-56
42. Peabody NC,Diao F, LuanH,WangH,Dewey EM, et al. 2008. Bursicon functions within the Drosophila CNS to modulate wing expansion behavior, hormone secretion, and cell death. J. Neurosci. 28:14379-91
43. Peabody NC, Pohl JB, Diao F, Vreede AP, Sandstrom DJ, et al. 2009. Characterization of the decision network for wing expansion in Drosophila using targeted expression of the TRPM8 channel. J. Neurosci. 29:3343-53
44. Reid SNM, Fraenkel G, Friedman S. 1987. Extrication, the primary event in eclosion, and its relationship to digging, pumping and tanning in Sarcophaga bullata. J. Insect Physiol. 33:339-48
45. Reynolds S. 1983. Bursicon. In Endocrinology of Insects, ed.GHDowner,HLaufer, pp. 235-48. New York: Alan R. Liss
46. Reynolds SE. 1976. Hormonal regulation of cuticle extensibility in newly emerged adult blow flies. J. Insect
47. Reynolds SE. 1980. Integration of behavior and physiology in ecdysis. In Advances in Insect Physiology, Vol. 15, ed. M Berridge, JE Treherne, VB Wigglesworth, pp. 476-595. London: Academic
48. Simpson JH. 2009. Mapping and manipulating neural circuits in the fly brain. Adv. Genet. 65:79-143
49. Steel CG, Vafopoulou X. 2002. Physiology of insect clocks. In Insect Clocks, ed. DS Saunders, pp. 115-88. Amsterdam: Elsevier
50. Tinbergen N. 2005. On aims and methods of ethology. Anim. Biol. 55:297-321
51. Truman JW. 1973. Physiology of insect ecdysis. 3. Relationship between hormonal control of eclosion and of tanning in tobacco hornworm, Manduca sexta. J. Exp. Biol. 58:821-29
52. Truman JW. 2005. Hormonal control of insect ecdysis: Endocrine cascades for coordinating behavior with physiology. Vitam. Horm. 73:1-30
53. Truman JW, Endo PT. 1974. Physiology of insect ecdysis: Neural and hormonal factors involved in wing-spreading behavior of moths. J. Exp. Biol. 61:47-55
54. Truman JW, Riddiford LM. 1970. Neuroendocrine control of ecdysis in silkmoths. Science 167:1624-26
55. Veenstra JA, Rombauts S, Grbic M. 2012. In silico cloning of genes encoding neuropeptides, neurohormones and their putativeG-protein-coupled receptors in a spider mite. Insect Biochem. Mol. Biol. 42:277-95
56. Venken KJ, Simpson JH, Bellen HJ. 2011. Genetic manipulation of genes and cells in the nervous system of the fruit fly. Neuron 72:202-30
57. Veverytsa L, Allan DW. 2012. Temporally tuned neuronal differentiation supports the functional remodeling of a neuronal network in Drosophila. Proc. Natl. Acad. Sci. USA 109:E748-56
58. Webster SG, Wilcockson DC, Mrinalini, Sharp JH. 2013. Bursicon and neuropeptide cascades during the ecdysis program of the shore crab, Carcinus maenas. Gen. Comp. Endocrinol. 182:54-64
59. White BH, Peabody NC. 2009. Neurotrapping: Cellular screens to identify the neural substrates of behavior in Drosophila. Front. Mol. Neurosci. 2:20
60. Zdarek J, Denlinger DL. 1987. Posteclosion behavior of the flesh fly, Sarcophaga crassipalpis: A comparison of wild-Type and unicorn mutants. Arch. Insect Biochem. Physiol. 4:101-6
61. Zilberstein Y, Ewer J, Ayali A. 2006. Neuromodulation of the locust frontal ganglion during the moult: A novel role for insect ecdysis peptides. J. Exp. Biol. 209:2911-19
62. Zitnan D, AdamsM. 2004. Neuroendocrine regulation of insect ecdysis. In ComprehensiveMolecular Insect Science, ed. L Gilbert, I Kostas, S Gill, pp. 1-60. Amsterdam/Boston: Elsevier
63. Zitnan D, Adams ME. 2000. Excitatory and inhibitory roles of central ganglia in initiation of the insect ecdysis behavioural sequence. J. Exp. Biol. 203:1329-40
64. Zitnan D, AdamsME. 2012. Neuroendocrine regulation of ecdysis. In Insect Endocrinology, ed. LI Gilbert, pp. 253-309. Amsterdam: Elsevier
65. Zitnan D, Hollar L, Spalovska II, Takac P, Zitnanova II, et al. 2002. Molecular cloning and function of ecdysis-Triggering hormones in the silkworm Bombyx mori. J. Exp. Biol. 205:3459-73