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Avdeev N.V. About the dose-dependent effect of exogenous 20-hydroxyecdysone on the hypopharyngeal gland and behavior of adult bees Apis mellifera L. Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2024, Vol. 59, № 6, p. 1160-1168.
(how to cite this article)

doi: 10.15389/agrobiology.2024.6.1160eng

UDC: 638.1:591.1:577.171.7

Acknowledgements:
Сarried out within the framework of the state assignment for the Perm Research Institute of Agriculture - a branch of the Perm Federal Research Center, Ural Branch RAS on the topic “Search, study of genetic sources and donors of economically valuable traits of perennial forage grasses, development of scientific foundations for technologies for the cultivation and use of crops with biological activity” (No. 122030400198-6).

 

ABOUT THE DOSE-DEPENDENT EFFECT OF EXOGENOUS 20-HYDROXYECDYSONE ON THE HYPOPHARYNGEAL GLAND AND BEHAVIOR OF ADULT BEES Apis mellifera L.

N.V. Avdeev ✉

Perm Agricultural Research Institute — Branch of Perm Federal Research Center RAS, 12, ul. Kul’tury, Lobanovo village, PermDistrict, 14532 Russia, e-mail permbee@yandex.ru (✉ corresponding author)

ORCID:
Avdeev N.V. orcid.org/0000-0002-0320-9681

Final revision received March 14, 2022
Accepted July 07, 2022

20-Hydroxyecdysone (20E) is a biologically active substance that has multiple effects on both vertebrates and invertebrates. In arthropods, the steroid hormone 20E is primarily known as the molting hormone in imaginal phases; relatively recent studies indicate the activity of 20E on imago. However, the results of studies of its effects are contradictory, and an attempt to commercially use 20E preparations in beekeeping was unsuccessful, probably due to the tolerance of Apis mellifera L. to exogenous 20E due to increased metabolism or activation of the blood-brain barrier. In the present work, in a model experiment, we have shown that the biological effect of 20E on young bees is manifested in a dose-dependent effect on food storage in honeycomb cells, on the development of the pharyngeal gland, and the accumulation of proline secreted by it in honey. The aim of the study was to identify the dose of exogenous 20E that activates the compensatory reaction to its intake into the body, and peculiarities of this reaction. In a laboratory experiment, 50 newly emerged workers each were supplied with 50 % sugar syrup, an empty comb and kept in 120×105×40 mm cages in a hygrothermostat at 35.0±0.2 °С and relative air humidity 50±5 % for 7 days. The sugar syrup in the experiment contained the additive 20E at a concentration of 4×10-10 to 1×10-5 mol/l with daily dose from 0.01 to 250 pmol per bee. The lowest studied daily dose of 20E (0.01 pmol per bee) does not have a significant effect on the size of the hypopharyngeal gland acini. The maximum reduction (by 1/4, p < 0.001) in the diameter of the hypopharyngeal gland acini was noted both at the maximum studied dose (250 pmol/bee per day) and at the low dose of 20E (0.05 pmol/bee per day). The minimum length of the follicles (by 1/5, p < 0.001) is characteristic only for a low dose of 20E (0.05 pmol/bee per day), at the maximum studied dose (250 pmol/bee per day), the acini were elongated, almost reaching the values control (p < 0.05). The size of acini at an intermediate daily dose (0.5 pmol/bee) had intermediate values between the values typical for a dose of 0.05 pmol/bee per day and the control, significantly differing from them (p < 0.001). An abrupt 2-fold decrease (p < 0.05) in proline secretion and activity of bees in terms of food storage was also revealed with an increase in the 20E concentration from 4× 10-10 to 2× 10-9 mol/l (from 0.01 to 0.05 pmol/bee per day). We suggest that 20E fed at a daily dose of 0.05 pmol per bee activates oxidation of 20E, causing a decrease in the 20E accumulation in the hemolymph and a sharp change in the influence, including change to the opposite biological effects.

Keywords: Apis mellifera L., honey bee, 20-hydroxyecdysone, molting hormone, dose-response, hypopharyngeal gland, proline, nectar storage.

 

REFERENCES

  1. Prasad S., Upadhyay V.B. Influence of 20-hydroxyecdysone on the larval performance of multivoltine mulberry silkworm (Bombyx mori Linn). African Journal of Basic & Applied Sciences, 2012, 4(5): 146-154 CrossRef
  2. Barge S., Pardeshi A. Influence of phytoecdysteroids isolated from Coix aquatica on cocoon characteristics of silkworm Bombyx mori L. The Pharma Innovation Journal, 2019, 8(3): 389-393.
  3. Kakpakov V.T., Kulinich A.V. Preparat dlya stimulyatsii razmnozheniya nasekomykh. A. s. RU 2034504 C1 (RF) 23 K 1/18, 1/20, A 01 K 49/00, 53/00. Kakpakov V.T., Kulinich A.A. (RF). № 93052227/15. Zayavl. 18.11.93. Opubl. 10.05.95 [Preparation for stimulation of reproduction of insects. A. c. RU 2034504 C1 (RF) 23 K 1/18, 1/20, A 01 K 49/00, 53/00. Kakpakov V. T., Kulinich A.A. (RF). No. 93052227/15. Appl. 11/18/93. Publ. 05/10/95] (in Russ.).
  4. Shangareva G.S., Baltaev U.A., Odinokov V.N. Sposob uluchsheniya zimovki pchelinykh semey. A. s. RU2125793 C1 (RF). A 01 K 47/00, A 23 K 1/18. Institut neftekhimiii i kataliza s opytnym zavodom AN Respubliki Bashkortostan. № 97119262/13. Zayavl. 20.11.1997. Opubl. 10.02.1999 [Method for improving wintering of bee colonies. A. s. RU2125793 C1 (RF). A 01 K 47/00, A 23 K 1/18. Institute of Petrochemistry and Catalysis with a pilot plant of the Academy of Sciences of the Republic of Bashkortostan. No. 97119262/13. Appl. 11/20/1997. Publ. 02/10/1999] (in Russ.).
  5. Ishmuratova N.M., Giniyatullin M.G., Ishmuratov G.Yu. Pchelovodstvo, 2005, 4: 19-20 (in Russ.).
  6. Geddes L.H., McQuillan H.J., Aiken A., Vergoz V., Mercer A.R. Steroid hormone (20-hydroxyecdysone) modulates the acquisition of aversive olfactory memories in pollen forager honeybees. Learning & Ьemory (Cold Spring Harbor, N.Y.), 2013, 20(8): 399-409 CrossRef
  7. Trawinski A.M. Characterizing ecdysteroid titer profiles and the functional role of ecdysteroids in adult worker honey bees (Apis mellifera). Wake Forest University, 2016.
  8. Timofeev N.P. Materialy IV Mezhdunarodnoynauchno-proizvodstvennoy konferentsii «Selektsiya, ekologiya, tekhnologiya vozdelyvaniya i pererabotki netraditsionnykh rasteniy» [Proc. IV Int. Conf. «Selection, ecology, technology of cultivation and processing of non-traditional plants»]. Simferopol’, 1996: 231-232 (in Russ.).
  9. Ueno T., Takeuchi H., Kawasaki K., Kubo T. Changes in the gene expression profiles of the hypopharyngeal gland of worker honeybees in association with worker behavior and hormonal factors. Behavior and Hormonal Factors, 2015, 10(6): 1-20 CrossRef
  10. Winkler P., Sieg F., Buttstedt A. Transcriptional control of honey bee (Apis mellifera) major royal jelly proteins by 20-hydroxyecdysone. Insects, 2018, 9(3): 122 CrossRef
  11. Corby-Harris V., Snyder L., Meador C. Fat body lipolysis connects poor nutrition to hypopharyngeal gland degradation in Apis mellifera. Journal of Insect Physiology, 2019, 116: 1-9 CrossRef
  12. Wegener J., Huang Z.Y., Lorenz M.W., Bienefeld K. Regulation of hypopharyngeal gland activity and oogenesis in honey bee (Apis mellifera) workers. Journal of Insect Physiology, 2009, 55: 716-725 CrossRef
  13. Arif Y., Singh P., Bajguz A., Hayat S. Phytoecdysteroids: distribution, structural diversity, biosynthesis, activity, and crosstalk with phytohormones. International Journal of Molecular Sciences, 2022, 23: 8664 CrossRef
  14. Lafont R., Balducci C., Dinan L. Ecdysteroids. Encyclopedia, 2021, 1: 1267-1302 CrossRef
  15. Ufimtsev K.G., Shirshova T.I., Volodin V.V. Uspekhi sovremennoy biologii, 2009, 129(3): 1-15 (in Russ.).
  16. Calas D., Denis Thiéry D., Marion-Poll F. 20-Hydroxyecdysone deters oviposition and larval feeding in the European grapevine moth, Lobesia botrana. Journal of Chemical Ecology, 2006, 32: 2443-2454 CrossRef
  17. Pestov S.V., Filippov N.I., Ufimtsev K.G., Volodin V.V. Materialy XII Vserossiiskoy nauchno-prakticheskoy konferentsii «Biodiagnostika sostoyaniya prirodnykh i prirodno-tekhnogennykh sistem» [Proc. XII Russian Conf. «Biodiagnostics of the state of natural and natural-technogenic systems»]. Kirov, 2014, 1: 195-198 CrossRef (in Russ.).
  18. Volodina C.O., Volodin V.V., Gorovoy P.G., Tkachenko K.G., Novozhilova E.V., Ishmuratova M.M., Chadin I.F., Kanev V.A., Ley Sh. Turczaninowia, 2012, 15(4): 58-75 (in Russ.).
  19. Timofeev N.P. Experience of Rhaponticum carthamoides (Willd.) Iliin cultivation as a natural source of ecdysterone under the conditions of the Arkhangelsk region. Sel’skokhozyaystvennaya Biologiya [Agricultural Biology], 2023, 58(1): 114-141 CrossRef
  20. Pestov S.V., Filippov N.I., Ufimtsev K.G., Volodin V.V., Volodina S.O., Dontsov A.G., Beshley I.V. Teoreticheskaya i prikladnaya ekologiya, 2017, 3: 91-96 (in Russ.).
  21. Avdeev N.V. Materialy Mezhdunarodnoy nauchno-prakticheskoy konferentsii «Pchelovodstvo i apiterapiya: aktual’nye voprosy, dostizheniya i innovatsii» [Proc. Int. Conf. «Beekeeping and apitherapy: current issues, achievements and innovations»]. Rybnoe, 2024: 14-20 (in Russ.).
  22. Es’kov E.K. Zhurnal evolyutsionnoy biokhimii i fiziologii, 2014, 50(5): 321-335 (in Russ.).
  23. Tozetto S., Bitondi M., Dallacqua R.P., Simoes Z.L. Protein profiles of testes, seminal vesicles and accessory glands of honey bee pupae and their relation to the ecdysteroid titer. Apidologie, 2006, 38(1): 1-12 CrossRef
  24. Pinto L.Z., Hartfelder K., Gentile Bitondi M.M., Simoes Z.L. Ecdysteroid titers in pupae of highly social bees relate to distinct modes of caste development. Journal of Insect Physiology, 2002, 48(8): 783-790 CrossRef
  25. Dai Z., Sun, B., Wang Y., Zhang, Z., Sun W. Identification of genes involved in resistance to high exogenous 20-hydroxyecdysone in Spodoptera litura. Insects, 2022, 13: 297 CrossRef
  26. Guittard E., Blais C., Maria A., Parvy J.P., Pasricha S., Lumb C., Lafont R., Daborn P.J., Dauphin-Villem C. CYP18A1, a key enzyme of Drosophila steroid hormone inactivation, is essential for metamorphosis. Developmental Biology, 2011, 349(1): 35-45 CrossRef
  27. Claudianos C., Ranson H., Johnson R.M., Biswas S., Schuler M.A., Berenbaum M.R. Feyereisen R., Oakeshott J.G. A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Molecular Biology, 2006, 15(5): 615-636 CrossRef
  28. Berenbaum M.R., Johnson R.M. Xenobiotic detoxification pathways in honey bees. Current Opinion in Insect Science, 2015, 10: 51-58 CrossRef
  29. Williams D.R., Fisher M.J., Rees H.H. Characterization of ecdysteroid 26-hydroxylase: an enzyme involved in molting hormone inactivation. Archives of Biochemistry and Biophysics, 2000, 376: 389-398 CrossRef
  30. Okamoto N., Yamanaka N. Steroid hormone entry into the brain requires a membrane transporter in Drosophila. Current Biology, 2020, 30(2): 359-366 CrossRef
  31. Bosua H.J., Nicolson S.W., Archer C.R., Pirk C.W.W. Effects of cage volume and bee density on survival and nutrient intake of honeybees (Apis mellifera L.) under laboratory conditions. Apidologie, 2018, 49: 734-746 CrossRef
  32. Williams G.R., Alaux C., Costa C., Csáki T., Doublet V., Eisenhardt D., Fries I., Kuhn R., McMahon D.P., Medrzycki P., Murray T.E., Natsopoulou M.E., Neumann R., Oliver R., Paxton R.J., Pernal S.F., Shutler D., Tanner G., van der Steen J.J.M., Brodschneider R. Standard methods for maintaining adult Apis mellifera in cages under in vitro laboratory conditions. Journal of Apicultural Research, 2013, 52(1): 1-36 CrossRef
  33. Maslennikova V.I, Korolev A.V. Pchelovodstvo, 2010, 4: 16-19 (in Russ.).
  34. Amdam G.V., Page R.E.J., Fondrk M.K., Brent C.S. Hormone response to bidirectional selection on social behavior. Evolution & Development, 2010, 12: 428-436 CrossRef
  35. Hartfelder K., Bitondi M.M.G., Santana W.C., Simoes Z.L.P. Ecdysteroid titer and reproduction in queens and workers of the honey bee and of a stingless bee: loss of ecdysteroid function at increasing levels of sociality? Insect Biochemistry and Molecular Biology, 2002, 32: 211-216 CrossRef
  36. Crailsheim K. Distribution of haemolymph in the honeybee (Apis mellifica) in relation to season, age and temperature. Journal of Insect Physiology, 1985, 31: 707-713 CrossRef

 

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