Mezheritskiy Maxim, Melnikova Victoria, Dyakonova Varvara, Vorontsov Dmitry
Koltzov Institute of Developmental Biology of the Russian Academy of Sciences, Moscow 119334, Russia.
Insects. 2024 Mar 9;15(3):183. doi: 10.3390/insects15030183.
We have recently shown that experience of flight remarkably enhanced subsequent terrestrial phonotaxis in females in response to the male calling song. Here, we elucidated the possible roles of octopamine and serotonin in the enhancing effect of flying on phonotactic behavior. Octopamine is known to be released into the hemolymph during flight in insects; however, the octopamine receptor antagonist epinastine did not abolish the effects of flight in our study. On the contrary, the drug significantly potentiated the influence of flying on phonotactic behavior. The octopamine receptor agonist chlordimeform, at a concentration of 2 mM, which was previously found to activate aggression in crickets, dramatically reduced the phonotactic response. However, at a 10-times-lower dose, chlordimeform produced a light but significant decrease in the time that females took to reach the source of the calling song. A similar effect was produced by octopamine itself, which hardly passes the blood-brain barrier in insects. The effect of flight was completely abolished in female crickets treated with alpha-methyl tryptophan (AMTP). AMPT suppresses the synthesis of serotonin, decreasing its content in the nervous systems of insects, including crickets. An activation of the serotonin synthesis with 5-hydroxytryptophan mimicked the effect of flight by increasing the number of visits to and the time spent in the zone near the source of the calling song. The 5-HT content in the third thoracic ganglion was significantly higher in flyers compared to the control group. In contrast, no changes in the octopamine level were observed in the third thoracic ganglion, which is known to play a crucial role in decision-making involved in intraspecific interactions. Therefore, the results suggest that although octopamine is known to be released into the hemolymph during flight, it is likely to inhibit rather than activate the central mechanisms related to phonotaxis. The weak facilitating effect of a low dose of chlordimeform can be attributed to the activation of peripheral octopaminergic receptors. Our results suggest that the serotoninergic system may contribute to the facilitation of female phonotactic behavior by flying. We suggest that both flying and serotonin enhance sexual motivation in females and, by these means, impact their behavioral response to the male calling song.
我们最近发现，飞行经历显著增强了雌性昆虫随后对雄性求偶鸣声的地面趋声行为。在此，我们阐明了章鱼胺和血清素在飞行对趋声行为的增强作用中可能发挥的作用。已知昆虫飞行时章鱼胺会释放到血淋巴中；然而，在我们的研究中，章鱼胺受体拮抗剂依匹斯汀并未消除飞行的影响。相反，该药物显著增强了飞行对趋声行为的影响。章鱼胺受体激动剂杀虫脒，浓度为2 mM，此前发现其能激发蟋蟀的攻击性，它显著降低了趋声反应。然而，剂量降低10倍时，杀虫脒使雌性昆虫到达求偶鸣声源所需的时间略有但显著减少。章鱼胺本身也产生了类似的效果，而章鱼胺在昆虫中几乎无法穿过血脑屏障。用α-甲基色氨酸（AMTP）处理的雌性蟋蟀中，飞行的影响完全消失。AMTP抑制血清素的合成，降低其在包括蟋蟀在内的昆虫神经系统中的含量。用5-羟色氨酸激活血清素合成，通过增加对求偶鸣声源附近区域的访问次数和停留时间，模拟了飞行的效果。与对照组相比，飞行组第三胸神经节中的5-羟色胺含量显著更高。相反，在第三胸神经节中未观察到章鱼胺水平的变化，而第三胸神经节在种内相互作用的决策中起着关键作用。因此，结果表明，尽管已知昆虫飞行时章鱼胺会释放到血淋巴中，但它可能抑制而非激活与趋声行为相关的中枢机制。低剂量杀虫脒的微弱促进作用可能归因于外周章鱼胺能受体的激活。我们的结果表明，血清素能系统可能有助于通过飞行促进雌性趋声行为。我们认为，飞行和血清素都能增强雌性的性动机，并通过这些方式影响它们对雄性求偶鸣声的行为反应。
