Early Manipulation of Juvenile Hormone Has Sexually Dimorphic Effects on Mature Adult Behavior in Drosophila Melanogaster

Overview

Journal Horm Behav

Specialties Endocrinology
Psychology
Social Sciences

Date 2013 Sep 10

PMID 24012944

Citations 12

Authors

Kathryn J Argue

Amber J Yun

Wendi S Neckameyer

Affiliations

Soon will be listed here.

Abstract

Hormones are critical for the development, maturation, and maintenance of physiological systems; therefore, understanding their involvement during maturation of the brain is important for the elucidation of mechanisms by which adults become behaviorally competent. Changes in exogenous and endogenous factors encountered during sexual maturation can have long lasting effects in mature adults. In this study, we investigated the role of the gonadotropic hormone, juvenile hormone (JH), in the modulation of adult behaviors in Drosophila. Here we utilized methoprene (a synthetic JH analog) and precocene (a JH synthesis inhibitor) to manipulate levels of JH in sexually immature male and female Drosophila with or without decreased synthesis of neuronal dopamine (DA). Locomotion and courtship behavior were assayed once the animals had grown to sexual maturity. The results demonstrate a sexually dimorphic role for JH in the modulation of these centrally controlled behaviors in mature animals that is dependent on the age of the animals assayed, and present DA as a candidate neuronal factor that differentially interacts with JH depending on the sex of the animal. The data also suggest that JH modulates these behaviors through an indirect mechanism. Since gonadotropic hormones and DA interact in mammals to affect brain development and later function, our results suggest that this mechanism for the development of adult behavioral competence may be evolutionarily conserved.

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References

Charles J, Iwema T, Epa V, Takaki K, Rynes J, Jindra M . Ligand-binding properties of a juvenile hormone receptor, Methoprene-tolerant. Proc Natl Acad Sci U S A. 2011; 108(52):21128-33. PMC: 3248530. DOI: 10.1073/pnas.1116123109. View

Somerville L, Jones R, Casey B . A time of change: behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues. Brain Cogn. 2009; 72(1):124-33. PMC: 2814936. DOI: 10.1016/j.bandc.2009.07.003. View

Gellissen G, Wyatt G . Production of lipophorin in the fat body of adult Locusta migratoria: comparison with vitellogenin. Can J Biochem. 1981; 59(8):648-54. DOI: 10.1139/o81-090. View

Liu Z, Li X, Prasifka J, Jurenka R, Bonning B . Overexpression of Drosophila juvenile hormone esterase binding protein results in anti-JH effects and reduced pheromone abundance. Gen Comp Endocrinol. 2008; 156(1):164-72. DOI: 10.1016/j.ygcen.2008.01.006. View

Raikhel A, Lea A . Juvenile hormone controls previtellogenic proliferation of ribosomal RNA in the mosquito fat body. Gen Comp Endocrinol. 1990; 77(3):423-34. DOI: 10.1016/0016-6480(90)90233-c. View

Argue K, Neckameyer W . Sexually dimorphic recruitment of dopamine neurons into the stress response circuitry. Behav Neurosci. 2013; 127(5):734-43. PMC: 4191714. DOI: 10.1037/a0033807. View

Smith S . Female sex steroid hormones: from receptors to networks to performance--actions on the sensorimotor system. Prog Neurobiol. 1994; 44(1):55-86. DOI: 10.1016/0301-0082(94)90057-4. View

Wilson T, Fabian J . A Drosophila melanogaster mutant resistant to a chemical analog of juvenile hormone. Dev Biol. 1986; 118(1):190-201. DOI: 10.1016/0012-1606(86)90087-4. View

Dallai R, Baldari C, Marchini D, de Filippis T, Rosetto M, Manetti A . Juvenile hormone regulates the expression of the gene encoding ceratotoxin a, an antibacterial peptide from the female reproductive accessory glands of the medfly Ceratitis capitata. J Insect Physiol. 2003; 43(12):1161-1167. DOI: 10.1016/s0022-1910(97)00052-8. View

10.

McEwen B . Steroid hormones: effect on brain development and function. Horm Res. 1992; 37 Suppl 3:1-10. DOI: 10.1159/000182393. View

11.

Romeo R . Puberty: a period of both organizational and activational effects of steroid hormones on neurobehavioural development. J Neuroendocrinol. 2003; 15(12):1185-92. DOI: 10.1111/j.1365-2826.2003.01106.x. View

12.

Neckameyer W, Weinstein J . Stress affects dopaminergic signaling pathways in Drosophila melanogaster. Stress. 2005; 8(2):117-31. DOI: 10.1080/10253890500147381. View

13.

Fahrbach S, Robinson G . Juvenile hormone, behavioral maturation, and brain structure in the honey bee. Dev Neurosci. 1996; 18(1-2):102-14. DOI: 10.1159/000111474. View

14.

Paus T . Growth of white matter in the adolescent brain: myelin or axon?. Brain Cogn. 2009; 72(1):26-35. DOI: 10.1016/j.bandc.2009.06.002. View

15.

Neckameyer W, Holt B, Paradowski T . Biochemical conservation of recombinant Drosophila tyrosine hydroxylase with its mammalian cognates. Biochem Genet. 2005; 43(7-8):425-43. DOI: 10.1007/s10528-005-6781-3. View

16.

Wong M, Eaton M, Moss R . Electrophysiological actions of luteinizing hormone-releasing hormone: intracellular studies in the rat hippocampal slice preparation. Synapse. 1990; 5(1):65-70. DOI: 10.1002/syn.890050106. View

17.

Strauss R, Heisenberg M . A higher control center of locomotor behavior in the Drosophila brain. J Neurosci. 1993; 13(5):1852-61. PMC: 6576564. View

18.

Neckameyer W, Matsuo H . Distinct neural circuits reflect sex, sexual maturity, and reproductive status in response to stress in Drosophila melanogaster. Neuroscience. 2008; 156(4):841-56. DOI: 10.1016/j.neuroscience.2008.08.020. View

19.

Neckameyer W . Dopamine modulates female sexual receptivity in Drosophila melanogaster. J Neurogenet. 1999; 12(2):101-14. DOI: 10.3109/01677069809167259. View

20.

Berger E, Goudie K, Klieger L, Berger M, DeCato R . The juvenile hormone analogue, methoprene, inhibits ecdysterone induction of small heat shock protein gene expression. Dev Biol. 1992; 151(2):410-8. DOI: 10.1016/0012-1606(92)90181-f. View