Juvenile hormone

Juvenile hormones (JHs) are a group of acyclic sesquiterpenoids that regulate many aspects of insect physiology. JHs regulate development, reproduction, diapause, and polyphenisms.^[1][2][3]

In insects, JH (formerly called neotenin) refers to a group of hormones, which ensure growth of the larva, while preventing metamorphosis. Because of their rigid exoskeleton, insects grow in their development by successively shedding their exoskeleton (a process known as molting).

Juvenile hormones are secreted by a pair of endocrine glands behind the brain called the corpora allata. JHs are also important for the production of eggs in female insects.

JH was discovered in 1965 and the molecular structure solved in 1967.

Most insect species contain only juvenile hormone (JH) III. To date JH 0, JH I, and JH II have been identified only in the Lepidoptera (butterflies and moths). The form JHB3 (JH III bisepoxide) appears to be the most important JH in the Diptera, or flies.^[4] Certain species of crustaceans have been shown to produce and secrete methyl farnesoate, which is juvenile hormone III lacking the epoxide group.^[5] Methyl farnesoate is believed to play a role similar to that of JH in crustaceans.

Control of development

The titre of JH found in the haemolymph of the developing insect controls the stage of development that the insect is in. During ecdysis the form of the old cuticle laid down before the next moult is controlled by the JH level in the insect. JH maintains a juvenile state. The level of it gradually decreases during the development of the insect, allowing it to proceed to successive instars with each molt.

This has been demonstrated in various studies, most prominently that by V. B. Wigglesworth in 1960s. In this study, two adult Rhodnius had their blood systems linked, ensuring that the JH titre in both would be equal. One was a third instar Rhodnius, the other was a fourth instar. When the corpora allata of the third instar insect were removed, the level of JH was equal in both insects to that in the fourth instar animal, and hence both proceeded to the fifth instar at the next moult. When the fourth instar Rhodnius had its corpora allata removed, both contained a third instar level of JH and hence one proceeded to instar four, and the other remained at this instar.

Generally, the removal of the corpora allata from juveniles will result in a diminutive adult at the next moult. Implantation of corpora allata into last larval instars will boost JH levels and hence produce a supernumary (extra) juvenile instar etc.

Juvenile hormones in honey bees

There is a complex interaction between JH, the hormone ecdysone and vitellogenin. In the development stage, as long as there is enough JH, the ecdysone promotes larva-to-larva molts. With lower amounts of JH, ecdysone promotes pupation. Complete absence of JH results in formation of the adult.^[6] In adult honey bees, JH and Vitellogenin titers in general show an inverse pattern.^{[7][8][9][10]}

JH titers in worker honey bees progressively increase through the first 15 or so days of the worker's life before the onset of foraging.^[11] During the first 15 days, workers perform tasks inside the hive, such as nursing larvae, constructing comb, and cleaning cells. JH titers peak around day 15; workers this age guard, remove dead bees from the colony, and fan at the colony entrance to cool the nest. Aggressiveness of guard bees is correlated with their blood JH levels. Even though guards have high JH levels, their ovaries are relatively undeveloped.^[12][13] Although, JH does not activate foraging. Rather it is involved in controlling the pace at which bees develop into foragers.^[14]

Vitellogenin titers are high at the beginning of adult life and slowly decrease.

JH has been known to be involved in the queen-worker caste differentiation during the larval stage.^[15] The unique negative relationship between JH and Vitellogenin may be important to the understanding of queen longevity.^[16]

See also Bee learning and communication

Forms

The structures of the different juvenile hormones.

• Methyl farnesoate
  • CAS methyl (2E,6E)-3,7,11-trimethyl-2,6,10-dodecatrienoate
  • Formula: C₁₆H₂₆O₂

• Juvenile hormone 0 (found in Lepidoptera)
  • CAS methyl (2E,6E)-10R,11S-(oxiranyl)-3,7-diethyl-11-methyl-2,6-tridecadienoate
  • Formula: C₁₉H₃₂O₃

• Juvenile hormone I (found in Lepidoptera)
  • CAS methyl (2E,6E)-10R,11S-(oxiranyl)-7-ethyl-3,11-dimethyl-2,6-tridecadienoate
  • Formula: C₁₈H₃₀O₃

• Juvenile hormone II (found in Lepidoptera)
  • CAS methyl (2E,6E)-10R,11S-(oxiranyl)-3,7,11-trimethyl-2,6-tridecadienoate
  • Formula: C₁₇H₂₈O₃

• Juvenile hormone III
  • CAS methyl (2E,6E)-10R-(oxiranyl)-3,7,11-trimethyl-2,6-dodecadienoate
  • Formula: C₁₆H₂₆O₃

• Juvenile hormone JHB3 (found in diptera)
  • CAS methyl (2E,6E)-6S,7S,10R-(dioxiranyl)-3,7,11-trimethyl-2-dodecaenoate
  • Formula: C₁₆H₂₆O₄

Use as an insecticide

Synthetic analogues of the juvenile hormone are used as an insecticide, preventing the larvae from developing into adult insects. JH itself is expensive to synthesize and is unstable in light. At high levels of JH, larva can still molt, but the result will only be a bigger larva, not an adult. Thus the insect's reproductive cycle is broken. One JH analogue, methoprene, is approved by the WHO for use in drinking water cisterns to control mosquito larvae.

Juvenile hormone regulation

Juvenile hormone is produced in the corpora allata of insects. JH will disperse throughout the haemolymph and act on responsive tissues. JH is principally degraded by the enzymes Juvenile-hormone esterase (JHE) or juvenile hormone epoxide hydrolase (JHEH). JHE and JHEH both lead to suppression of JH signaling and response. Tissues responsive to JH may produce one or both of these enzymes.

JH stimulates the accessory glands of adult males, promoting gland growth and the production of accessory gland secretion. Yolk production (vitellogenesis) in female ovaries is also stimulated by JH action. JH may also regulate reproductive behaviour in both sexes.

Notes

1. ^ Riddiford, L. M. (1994) Adv. Insect Physiol. 24, 213–274.
2. ^ Wyatt, G. R. & Davey, K. G. (1996) Adv. Insect Physiol. 26, 1–155
3. ^ Nijhout, H. F. (1994) Insect Hormones (Princeton Univ. Press, Princeton)
4. ^ Richard D.S., Applebaum S.W., Sliter T.J., Baker F.C., Schooley D.A., Reuter C.C., Henrich V.C., Gilbert L.I. (1989) Juvenile Hormone Bisepoxide Biosynthesis in vitro by the Ring Gland of Drosophila melanogaster: A Putative Juvenile Hormone in the Higher Diptera. Proc Natl Acad Sci USA 86: 1421-1425
5. ^ Laufer, H, Borst, D, Baker, FC, Carasco, C, Sinkus, M, Reuter, CC, Tsai, LW, and Schooley, DA. (1987) Identification of a juvenile hormone-like compound in a crustacean. Science 235: 202-205
6. ^ Kimball, John W. (2002) Insect hormones
7. ^ Hartfelder K, Engels W (1998) Curr Top Dev Biol 40:45–77
8. ^ Bloch G, Wheeler DE, Robinson GE (2002) in Hormones, Brain, and Behavior, ed Pfaff D (Academic, New York) Vol 3, 195–236
9. ^ Fluri P, Sabatini AG, Vecchi MA, Wille H (1981) J Apic Res 20:221–225
10. ^ Fahrbach SE, Giray T, Robinson GE (1995) Neurobiol Learn Mem 63:181–191
11. ^ Elekonich, M. M., Schulz, D. J., Bloch, G. and Robinson, G. E. (2001). Juvenile hormone levels in honey bee (Apis mellifera L.) foragers: foraging experience and diurnal variation. Journal for Insect Physiology 47,1119 -1125
12. ^ Pearce A.N., Huang Z.Y., Breed M.D. (2001) Juvenile hormone and aggression in honey bees, Journal for Insect Physiology 47, 1243– 1247.
13. ^ Breed, Michael D. (2002) Juvenile Hormone
14. ^ Sullivan, J. P., Jassim, O., Fahrbach, S. E. and Robinson, G. E. (2000). Juvenile hormone paces behavioral development in the adult worker honey bee. Horm. Behav. 37, 1-14
15. ^ Rachinsky A., Hartfelder K. (1990) Corpora allata activity, a primer regulating element for caste juvenile hormone titer in honey bee larvae (Apis mellifera carnica), J. Insect Physiol. 36, 189–194
16. ^ Miguel Corona, Rodrigo A. Velarde, Silvia Remolina, Adrienne Moran-Lauter, Ying Wang, Kimberly A. Hughes, and Gene E. Robinson Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity PNAS, Apr 2007; 104: 7128 - 7133

References

• Wigglesworth, VB. (1964) The hormonal regulation of growth and reproduction in insects. Adv. Insect Physiol. 2: 247-336
• Wigglesworth, VB. (1939) The Principles of Insect Physiology. Cambridge University Press. Cambridge.
• Berger and Dubrovsky (2005) Juvenile Hormone Molecular Actions and Interactions During Development of Drosophila. Vitamins and Hormones. 73:172-215