Ильясов Р. А., Ильясова А. Ю., Саттаров В. Н., Богуславский Д. В. Октопамин – адаптивный нейромедиатор медоносных пчел при температурном стрессе // Научная жизнь. 2024. Т. 19. Вып. 6 (138). С. 1074-1085. DOI: 10.35679/1991-9476-2024-19-6-1074-1085

Ильясов Рустем Абузарович, д-р биол. наук, вед. науч. сотр. лаборатории «Нейробиология развития», ФГБУН «Институт биологии развития им. Н. К. Кольцова РАН»: Россия, 119334. г. Москва, ул. Вавилова, 26.
Ильясова Алла Юрьевна, инженер-исследователь лаборатории «Нейробиология развития», ФГБУН «Институт биологии развития им. Н. К. Кольцова РАН»: Россия, 119334. г. Москва, ул. Вавилова, 26.
Саттаров Венер Нуруллович, д-р биол. наук, профессор, Почетный работник воспитания и просвещения Российской Федерации, зав. кафедрой «Экология, география и природопользование», ФГБОУ ВО «Башкирский государственный педагогический университет им. М. Акмуллы»: Россия, 450008, Республика Башкортостан, г. Уфа, ул. Октябрьской революции, 3а.
Богуславский Дмитрий Викторович, канд. биол. наук, ст. науч. сотр. лаборатории «Нейробиология развития», ФГБУН «Институт биологии развития им. Н. К. Кольцова РАН»: Россия, 119334. г. Москва, ул. Вавилова, 26.

Тел.: (987) 487-02-88
E-mail: wener5791@yandex.ru

В условиях изменяющегося климата роль нейрохимических факторов в адаптации медоносной пчелы (Apis mellifera) к температурным стрессам приобретает всё большее значение. Настоящая работа посвящена изучению роли октопамина - нейромедиатора, нейромодулятора, нейрогормона, связанного с проведением физиологических перестроек (мобилизация липидов), а также участвующего в сложных поведенческих реакциях в ответ на широкий спектр внешних и внутренних стрессогенных условий. Рассмотрены механизмы участия октопамина в иннервации грудных летательных мышц, которые обеспечивают термогенез в ответ на понижение температуры, а также его участие в поддержании устойчивого микроклимата гнезда через вентилирующее поведение при тепловом стрессе. В работе обобщены результаты исследований о возрастных и сезонных изменениях концентрации октопамина, а также его рецепторов, что способствует лучшему пониманию адаптивных ответов медоносной пчелы на экстремальные температурные условия. Установлено, что октопамин не только отвечает за иннервацию грудных летательных мышц, обеспечивающих активное теплообразование, но и влияет на социальное поведение пчел, включая вентилирование гнезда для поддержания микроклимата. Изменения в октопаминергической системе служат основой для понимания того, как медоносные пчелы реагируют на экстремальные температурные условия и какие нейрохимические процессы лежат в основе их поведения. Таким образом, данные представленные в данной статье имеют большое значение для дальнейшего изучения адаптивных механизмов пчел и могут быть полезны для разработки стратегий их защиты в условиях глобальных климатических изменений. Необходимы дальнейшие молекулярно-биологические исследования, направленные на более глубокое понимание функциональных ролей октопамина и других нейромедиаторов в адаптации пчел к температурным стрессам, что поможет обеспечить сохранение пчел, как важных опылителей, в экосистемах.

Список литературы:

1. Abou-Shaara H. F., Owayss A. A., Ibrahim Y. Y., Basuny N. K. A review of impacts of temperature and relative humidity on various activities of honey bees // Insectes Sociaux. ‒ 2017. ‒ V. 64, № 4. ‒ P. 455-463. https://doi.org/10.1007/s00040-017-0573-8.

2. Adamo S.A., Linn C.E., Hoy R.R. The role of neurohormonal octopamine during 'fight or flight' behaviour in the field cricket Gryllus bimaculatus // Journal of experimental Biology. ‒ 1995. ‒ V. 198, № Pt 8. ‒ P. 1691-1700. https://doi.org/10.1242/jeb.198.8.1691.
3. Barron A. B., Maleszka J., Vander Meer R. K., Robinson G. E., Maleszka R. Comparing injection, feeding and topical application methods for treatment of honeybees with octopamine // Journal of Insect Physiology. ‒ 2007. ‒ V. 53, № 2. ‒ P. 187-194. https://doi.org/10.1016/j.jinsphys.2006.11.009.
4. Becher M. A., Scharpenberg H., Moritz R. F. Pupal developmental temperature and behavioral specialization of honeybee workers (Apis mellifera L.) // Journal of Comparative Physiology A. ‒ 2009. ‒ V. 195, № 7. ‒ P. 673-679. https://doi.org/10.1007/s00359-009-0442-7 PMID - 19390855.
5. Blenau W., Wilms J. A., Balfanz S., Baumann A. AmOctalpha2R: Functional Characterization of a Honeybee Octopamine Receptor Inhibiting Adenylyl Cyclase Activity // International Journal of Molecular Sciences. ‒ 2020. ‒ V. 21, № 24. ‒ P. 9334. https://doi.org/10.3390/ijms21249334.
6. Bonoan R. E., Goldman R. R., Wong P. Y., Starks P. T. Vasculature of the hive: Heat dissipation in the honey bee (Apis mellifera) hive // Naturwissenschaften. ‒ 2014. ‒ V. 101, № 6. ‒ P. 459-465. https://doi.org/10.1007/s00114-014-1174-2 PMID - 24760416.
7. Brembs B., Christiansen F., Pflüger H. J., Duch C. Flight initiation and maintenance deficits in flies with genetically altered biogenic amine levels // Journal of Neuroscience. ‒ 2007. ‒ V. 27, № 41. ‒ P. 11122-11131. https://doi.org/10.1523/JNEUROSCI.2704-07.2007.
8. Chen Y. L., Hung Y. S., Yang E. C. Biogenic amine levels change in the brains of stressed honeybees // ARCHIVES OF INSECT BIOCHEMISTRY AND PHYSIOLOGY. ‒ 2008. ‒ V. 68, № 4. ‒ P. 241-250. https://doi.org/10.1002/arch.20259 PMID - 18618764.
9. Chown S. L., Terblanche J. S. Physiological diversity in insects: ecological and evolutionary contexts // Advances in Insect Physiology. ‒ 2006. ‒ V. 33. ‒ P. 50-152. https://doi.org/10.1016/S0065-2806(06)33002-0 PMID - 19212462.
10. Cook C. N., Breed M. D. Social context influences the initiation and threshold of thermoregulatory behaviour in honeybees // Animal Behaviour. ‒ 2013. ‒ V. 86, № 2. ‒ P. 323-329. https://doi.org/10.1016/j.anbehav.2013.05.021.
11. Cook C. N., Brent C. S., Breed M. D. Octopamine and tyramine modulate the thermoregulatory fanning response in honey bees (Apis mellifera) // Journal of experimental Biology. ‒ 2017. ‒ V. 220, № Pt 10. ‒ P. 1925-1930. https://doi.org/10.1242/jeb.149203.
12. Cook C. N., Kaspar R. E., Flaxman S. M., Breed M. D. Rapidly changing environment modulates the thermoregulatory fanning response in honeybee groups // Animal Behaviour. ‒ 2016. ‒ V. 115. ‒ P. 237-243. https://doi.org/10.1016/j.anbehav.2016.03.014.
13. Corby-Harris V., Deeter M. E., Snyder L., Meador C., Welchert A. C., Hoffman A., Obernesser B. T. Octopamine mobilizes lipids from honey bee (Apis mellifera) hypopharyngeal glands // Journal of experimental Biology. ‒ 2020. ‒ V. 223, № jeb216135. https://doi.org/10.1242/jeb.216135 PMID - 32139471.
14. Davenport A. P., Evans P. D. Stress-induced changes in the octopamine levels of insect haemolymph // Insect Biochemistry. ‒ 1984. ‒ V. 14, № 2. ‒ P. 135-143. https://doi.org/10.1016/0020-1790(84)90021-0.
15. Diakonova V. E. Behavioral functions of serotonin and octopamine: some paradoxes of comparative physiology // Uspehi Fiziologicheskih Nauk. ‒ 2007. ‒ V. 38. ‒ P. 3-20.
16. Egley R. L., Breed M. D. The fanner honey bee: behavioral variability and environmental cues in workers performing a specialized task // Journal of Insect Behavior. ‒ 2013. ‒ V. 26, № 2. ‒ P. 238-245. https://doi.org/10.1007/s10905-012-9357-1.
17. Even N., Devaud J. M., Barron A. B. General stress responses in the honey bee // Insects. ‒ 2012. ‒ V. 3, № 4. ‒ P. 1271-1298. https://doi.org/10.3390/insects3041271 PMID - 26466739 PMCID - PMC4553576.
18. Groh C., Tautz J., Rossler W. Synaptic organization in the adult honey bee brain is influenced by brood-temperature control during pupal development // Proceedings of the National Academy of Sciences USA. ‒ 2004. ‒ V. 101. ‒ P. 4268-4273. https://doi.org/10.1073/pnas.0400773101 PMID - 15024125 PMCID - PMC384730.
19. Harris J. W., Woodring J. Effects of stress, age, season, and source colony on levels of octopamine, dopamine and serotonin in the honey bee (Apis mellifera L.) brain // Journal of Insect Physiology. ‒ 1992. ‒ V. 38, № 1. ‒ P. 29-35. https://doi.org/10.1016/0022-1910(92)90019-A.
20. Heinrich B. Thermoregulation of African and European honeybees during foraging, attack, and hive exits and returns // Journal of experimental Biology. ‒ 1979. ‒ V. 80, № 1. ‒ P. 217-239. https://doi.org/10.1242/jeb.80.1.217.
21. Huang Q. T., Ma H. H., Deng X. L., Zhu H., Liu J., Zhou Y., Zhou X. M. Pharmacological characterization of a β‐adrenergic‐like octopamine receptor in Plutella xylostella // Archives of insect biochemistry and physiology. ‒ 2018. ‒ V. 98, № e21466. ‒ P. e21466. https://doi.org/10.1002/arch.21466.
22. Hung K. L. J., Kingston J. M., Albrecht M., Holway D. A., Kohn J. R. The worldwide importance of honey bees as pollinators in natural habitats // Proceedings of the Royal Society B: Biological Sciences. ‒ 2018. ‒ V. 285, № 20172140. https://doi.org/10.1098/rspb.2017.2140 PMID ‒ 29321298 PMCID ‒ PMC5784195.
23. Ilyasov R. A., Kutuev I. A., Petukhov A. V., Poskryakov A. V., Nikolenko A. G. Phylogenetic relationships of dark European honeybees Apis mellifera mellifera L. from the Russian Ural and West European populations // Journal of Apicultural Science. ‒ 2011. ‒ V. 55. ‒ P. 67-76.
24. Ilyasov R. A., Rašić S., Takahashi J., Danilenko V. N., Proshchalykin M. Y., Lelej A. S., Sattarov V. N., Thai P. H., Raffiudin R., Kwon H. W. Genetic relationships and signatures of adaptation to the climatic conditions in populations of Apis cerana based on the polymorphism of the gene Vitellogenin // Insects. ‒ 2022. ‒ V. 13, № 11. ‒ P. 1053. https://doi.org/10.3390/insects13111053 PMID - 36421957 PMCID - PMC9694869.
25. Jhawar J., Davidson J. D., Weidenmüller A., Wild B., Dormagen D. M., Landgraf T., Couzin I. D., Smith M. L. How honeybees respond to heat stress from the individual to colony level // Journal of the Royal Society Interface. ‒ 2023. ‒ V. 20, № 20230290. ‒ P. 20230290. https://doi.org/10.1098/rsif.2023.0290.
26. Kamboj P., Kaur G., Gupta G. Understanding the Impact of Heat Stress on Honeybee Populations: Insights into Thermoregulation, Colony Dynamics, and Environmental Interactions // Uttar Pradesh Journal of Zoology. ‒ 2024. ‒ V. 45, № 12. ‒ P. 1-13. https://doi.org/10.56557/upjoz/2024/v45i124098.
27. Kamhi J. F., Arganda S., Moreau C. S., Traniello J. F. Origins of aminergic regulation of behavior in complex insect social systems // Frontiers in Systems Neuroscience. ‒ 2017. ‒ V. 11, № 74. ‒ P. 74. https://doi.org/10.3389/fnsys.2017.00074 PMID - 29066958 PMCID - PMC5641352.
28. Kamioka T., Suzuki H. C., Ugajin A., Yamaguchi Y., Nishimura M., Sasaki T., Ono M., Kawata M. Genes associated with hot defensive bee ball in the Japanese honeybee, Apis cerana japonica // BMC ecology and evolution. ‒ 2022. ‒ V. 22, № 31. ‒ P. 31. https://doi.org/10.1186/s12862-022-01989-9.
29. Kaya-Zeeb S., Delac S., Wolf L., Marante A.L., Scherf-Clavel O., Thamm M. Robustness of the honeybee neuro-muscular octopaminergic system in the face of cold stress // Frontiers in Physiology. ‒ 2022b. ‒ V. 13. ‒ P. 1002740. https://doi.org/10.3389/fphys.2022.1002740.
30. Kaya-Zeeb S., Engelmayer L., Straßburger M., Bayer J., Bähre H., Seifert R., Scherf-Clavel O., Thamm M. Octopamine drives honeybee thermogenesis // Elife. ‒ 2022a. ‒ V. 11, № e74334. https://doi.org/10.7554/eLife.74334.
31. Kovalskyi I., Kovalska L., Druzhbiak A. I., Kovalchuk I., Boyko A., Zhmur V., Havdan R., МD., Perig D., Lunyk I., Fiialovych L., Petryshak O., Paskevych G., Bogdan B., Leshchyshyn I. 1. Ontogenesis of honey bees (Apis mellifera) under the influence of temperature stress // Regulatory Mechanisms in Biosystems. ‒ 2024.10.15421/022443. https://doi.org/10.15421/022443.
32. Lahondère C. Recent advances in insect thermoregulation // Journal of experimental Biology. ‒ 2023. ‒ V. 226. https://doi.org/10.1242/jeb.245751 PMID - 37699071.
33. Li G., Zhao H., Liu Z., Wang H., Xu B., Guo X. The wisdom of honeybee defenses against environmental stresses // Frontiers in Microbiology. ‒ 2018. ‒ V. 9. ‒ P. 722. https://doi.org/10.3389/fmicb.2018.00722.
34. Libersat F., Pflueger H.-J. Monoamines and the orchestration of behavior // Bioscience. ‒ 2004. ‒ V. 54, № 1. ‒ P. 17-25. https://doi.org/10.1641/0006-3568(2004)054[0017:MATOOB]2.0.CO;2.
35. Medina R.G., Paxton R.J., De Luna E., Fleites-Ayil F.A., Medina L.A., Quezada-Euán J.J.G. Developmental stability, age at onset of foraging and longevity of Africanized honey bees (Apis mellifera L.) under heat stress // Journal of Thermal Biology. ‒ 2018. ‒ V. 74. ‒ P. 214-225. https://doi.org/10.1016/j.jtherbio.2018.04.003.
36. Mezheritskiy M.I., Vorontsov D.D., Dyakonova V.E., Zakharov I.S. Behavioral functions of octopamine in adult insects under stressful conditions // Biology Bulletin Reviews. ‒ 2024. ‒ V. 14, № 5. ‒ P. 535-547. https://doi.org/10.1134/S2079086424700014.
37. Minaud É., Rebaudo F., Davidson P., Hatjina F., Hotho A., Mainardi G., Steffan-Dewenter I., Vardakas P., Verrier E., Requier F. How stressors disrupt honey bee biological traits and overwintering mechanisms // Heliyon. ‒ 2024. ‒ V. 10, № 14. ‒ P. e34390. https://doi.org/10.1016/j.heliyon.2024.e34390.
38. Peng T., Derstroff D., Maus L., Bauer T., Grüter C. Forager age and foraging state, but not cumulative foraging activity, affect biogenic amine receptor gene expression in the honeybee mushroom bodies // Genes, Brain and Behavior. ‒ 2021. ‒ V. 20, № e12722. ‒ P. e12722. https://doi.org/10.1111/gbb.12722.
39. Petz M., Stabentheiner A., Crailsheim K. Respiration of individual honeybee larvae in relation to age and ambient temperature // Journal of Comparative Physiology B. ‒ 2004. ‒ V. 174, № 7. ‒ P. 511-518. https://doi.org/10.1007/s00360-004-0439-z PMID - 15278398.
40. Pflüger H.J., Duch C. Dynamic neural control of insect muscle metabolism related to motor behavior // Physiology. ‒ 2011. ‒ V. 26, № 4. ‒ P. 293-303. https://doi.org/10.1152/physiol.00002.2011.
41. Qi Y. X., Xu G., Gu G. X., Mao F., Ye G. Y., Liu W., Huang J. A new Drosophila octopamine receptor responds to serotonin // Insect Biochemistry and Molecular Biology. ‒ 2017. ‒ V. 90. ‒ P. 61-70. https://doi.org/10.1016/j.ibmb.2017.09.010.
42. Schmaranzer S. Thermoregulation of water collecting honey bees (Apis mellifera) // Journal of Insect Physiology. ‒ 2000. ‒ V. 46, № 8. ‒ P. 1187-1194. https://doi.org/10.1016/S0022-1910(00)00039-1.
43. Selcho M., Pauls D. Linking physiological processes and feeding behaviors by octopamine // Curr Opin Insect Sci. ‒ 2019. ‒ V. 36. ‒ P. 125-130. https://doi.org/10.1016/j.cois.2019.09.002 PMID - 31606580.
44. Sheikh A. A., Rehman N. Z., Kumar R. Diverse adaptations in insects: A review // Journal of Entomology and Zoology Studies. ‒ 2017. ‒ V. 5. ‒ P. 343-350.
45. Sombati S., Hoyle G. Generation of specific behaviors in a locust by local release into neuropil of the natural neuromodulator octopamine // Journal of Neurobiology. ‒ 1984. ‒ V. 15. ‒ P. 481-506. https://doi.org/10.1002/neu.480150607 PMID - 6097645.
46. Southwick E. E., Moritz R. F. A. Social control of air ventilation in colonies of honey bees, Apis mellifera // Journal of Insect Physiology. ‒ 1987. ‒ V. 33, № 9. ‒ P. 623-626. https://doi.org/10.1016/0022-1910(87)90130-2.
47. Stabentheiner A., Kovac H., Mandl M., Käfer H. Coping with the cold and fighting the heat: thermal homeostasis of a superorganism, the honeybee colony // Journal of Comparative Physiology A. ‒ 2021. ‒ V. 207, № 3. ‒ P. 337-351. https://doi.org/10.1007/s00359-021-01464-8 PMID - 33598719 PMCID - PMC8079341.
48. Starks P. T., Gilley D. C. Heat shielding: a novel method of colonial thermoregulation in honey bees // Naturwissenschaften. ‒ 1999. ‒ V. 86, № 9. ‒ P. 438-440. https://doi.org/10.1007/s001140050648 PMID - 10501692.
49. Starks P. T., Johnson R. N., Siegel A. J., Decelle M. M. Heat shielding: a task for youngsters // Behavioral Ecology. ‒ 2005. ‒ V. 16, № 1. ‒ P. 128-132. https://doi.org/10.1093/beheco/arh124.
50. Strawbridge R., Javed R. R., Cave J., Jauhar S., Young A. H. The effects of reserpine on depression: A systematic review // Journal of Psychopharmacology. ‒ 2023. ‒ V. 37, № 3. ‒ P. 248-260. https://doi.org/10.1177/02698811221115762.
51. Sujkowski A., Ramesh D., Brockmann A., Wessells R. Octopamine drives endurance exercise adaptations in Drosophila // Cell Reports. ‒ 2017. ‒ V. 21, № 7. ‒ P. 1809-1823. https://doi.org/10.1016/j.celrep.2017.10.065.
52. Tautz J., Maier S., Groh C., Roessler W., Brockmann A. Behavioral performance in adult honey bees is influenced by the temperature experienced during their pupal development // Proceedings of the National Academy of Sciences USA. ‒ 2003. ‒ V. 100. ‒ P. 7343-7347. https://doi.org/10.1073/pnas.1232346100 PMID - 12764227 PMCID - PMC165877.
53. Wang Q., Xu X., Zhu X., Chen L., Zhou S., Huang Z.Y., Zhou B. Low-temperature stress during capped brood stage increases pupal mortality, misorientation and adult mortality in honey bees // Plos One. ‒ 2016. ‒ V. 11, № e0154547. ‒ P. e0154547. https://doi.org/10.1371/journal.pone.0154547 PMID - 27149383 PMCID - PMC4858150.
54. Wang Y., Zhang P., Chao Y., Zhu Z., Yang C., Zhou Z., Li Y., Long Y., Liu Y., Li D., Wang S., Qu Q. Transport and inhibition mechanism for VMAT2-mediated synaptic vesicle loading of monoamines // Cell Research. ‒ 2024. ‒ V. 34, № 1. ‒ P. 47-57. https://doi.org/10.1038/s41422-023-00906-z.
55. Woodring J. P., Meier O. W., Rose R. Effect of development, photoperiod, and stress on octopamine levels in the house cricket, Acheta domesticus // Journal of Insect Physiology. ‒ 1988. ‒ V. 34, № 8. ‒ P. 759-765. https://doi.org/10.1016/0022-1910(88)90149-7.
56. Zhao H., Li G., Guo D., Li H., Liu Q., Xu B., Guo X. Response mechanisms to heat stress in bees // Apidologie. ‒ 2021. ‒ V. 52, № 2. ‒ P. 388-399. https://doi.org/10.1007/s13592-020-00830-w.
57. Zhu C., Li H., Xu X., Zhou S., Zhou B., Li X., Zhu X. The mushroom body development and learning ability of adult honeybees are influenced by cold exposure during their early pupal stage // Frontiers in Physiology. ‒ 2023. ‒ V. 14, № 1173808. https://doi.org/10.3389/fphys.2023.1173808 PMID - 37153230 PMCID - PMC10157483.

OCTOPAMINE IS AN ADAPTIVE NEUROTRANSMITTER OF HONEY BEES UNDER TEMPERATURE STRESS

Ilyasov Rustem Abuzarovich, Dr. of Biol. Sci., Leading Researcher at the Laboratory of developmental neurobiology, Institute of developmental Biology name after N.K. Koltsov of the RAS, Moscow, Russia.
Ilyasova Alla Yuryevna, Engineer-Research at the Laboratory of developmental neurobiology, Institute of developmental Biology name after N.K. Koltsov of the RAS, Moscow, Russia.
Sattarov Vener Nurullovich, Dr. of Biol. Sci., Prof., Honorary worker of education and enlightenment of the Russian Federation, Head of the Depart. of ecology, geography and environmental management, Bashkir state pedagogical university named after M. Akmulla, Ufa, Russia.
Boguslavsky Dmitry Viktorovich, Cand. of Biol. Sci., Senior Researcher at the Laboratory of developmental neurobiology, Institute of developmental Biology name after N.K. Koltsov of the RAS, Moscow, Russia.

Keywords: octopamine, thermoregulation, honey bee, thermogenesis, adaptation, insects, Apis mellifera, cold stress, heat stress.

Abstract. In a changing climate, the role of neurochemical factors in the adaptation of honey bees (Apis mellifera) to temperature stress is becoming increasingly important. This work is devoted to the study of the role of octopamine, a neurotransmitter, neuromodulator, and neurohormone associated with physiological rearrangements (lipid mobilization), as well as involved in complex behavioral reactions in response to a wide range of external and internal stressful conditions. The mechanisms of octopamine involvement in the innervation of the pectoral flight muscles, which provide thermogenesis in response to a decrease in temperature, as well as its participation in maintaining a stable microclimate of the nest through ventilation behavior under thermal stress, are considered. The paper summarizes the results of studies on age-related and seasonal changes in the concentration of octopamine, as well as its receptors, which contributes to a better understanding of the adaptive responses of honey bees to extreme temperature conditions. It has been established that octopamine is not only responsible for the innervation of the pectoral flight muscles, which provide active heat generation, but also affects the social behavior of bees, including ventilation of the nest to maintain a microclimate. Changes in the octopaminergic system serve as the basis for understanding how honey bees respond to extreme temperature conditions and which neurochemical processes underlie their behavior. Thus, the data presented in this article are of great importance for further studying the adaptive mechanisms of bees and may be useful for developing strategies for their protection in the context of global climate change. Further molecular biological research is needed to better understand the functional roles of octopamine and other neurotransmitters in the adaptation of bees to temperature stress, which will help ensure the conservation of bees as important pollinators in ecosystems.