Zhang Xufeng, Hu Han, Han Bin, Wei Qiaohong, Meng Lifeng, Wu Fan, Fang Yu, Feng Mao, Ma Chuan, Rueppell Olav, Li Jianke
Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, Beijing, China; Institute of Horticultural Research, Shanxi Academy of Agricultural Sciences, Shanxi Agricultural University, Taiyuan, China.
Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, Beijing, China.
Mol Cell Proteomics. 2020 Oct;19(10):1632-1648. doi: 10.1074/mcp.RA120.002123. Epub 2020 Jul 15.
The neuronal basis of complex social behavior is still poorly understood. In honeybees, reproductive investment decisions are made at the colony-level. Queens develop from female-destined larvae that receive alloparental care from nurse bees in the form of ad-libitum royal jelly (RJ) secretions. Typically, the number of raised new queens is limited but genetic breeding of "royal jelly bees" (RJBs) for enhanced RJ production over decades has led to a dramatic increase of reproductive investment in queens. Here, we compare RJBs to unselected Italian bees (ITBs) to investigate how their cognitive processing of larval signals in the mushroom bodies (MBs) and antennal lobes (ALs) may contribute to their behavioral differences. A cross-fostering experiment confirms that the RJB syndrome is mainly due to a shift in nurse bee alloparental care behavior. Using olfactory conditioning of the proboscis extension reflex, we show that the RJB nurses spontaneously respond more often to larval odors compared with ITB nurses but their subsequent learning occurs at similar rates. These phenotypic findings are corroborated by our demonstration that the proteome of the brain, particularly of the ALs differs between RJBs and ITBs. Notably, in the ALs of RJB newly emerged bees and nurses compared with ITBs, processes of energy and nutrient metabolism, signal transduction are up-regulated, priming the ALs for receiving and processing the brood signals from the antennae. Moreover, highly abundant major royal jelly proteins and hexamerins in RJBs compared with ITBs during early life when the nervous system still develops suggest crucial new neurobiological roles for these well-characterized proteins. Altogether, our findings reveal that RJBs have evolved a strong olfactory response to larvae, enabled by numerous neurophysiological adaptations that increase the nurse bees' alloparental care behavior.
复杂社会行为的神经元基础仍知之甚少。在蜜蜂中，繁殖投资决策是在群体层面做出的。蜂王由雌性注定的幼虫发育而来，这些幼虫从哺育蜂那里接受以随意分泌蜂王浆（RJ）形式的异亲照料。通常，培育的新蜂王数量有限，但几十年来为提高RJ产量而对“蜂王浆蜜蜂”（RJBs）进行的遗传育种导致对蜂王的繁殖投资大幅增加。在这里，我们将RJBs与未选择的意大利蜜蜂（ITBs）进行比较，以研究它们在蘑菇体（MBs）和触角叶（ALs）中对幼虫信号的认知处理如何导致它们的行为差异。一项交叉寄养实验证实，RJB综合征主要是由于哺育蜂异亲照料行为的转变。通过对喙伸反射进行嗅觉条件训练，我们发现与ITB哺育蜂相比，RJB哺育蜂对幼虫气味的自发反应更频繁，但它们随后的学习速度相似。我们证明RJB和ITB之间大脑蛋白质组，特别是ALs的蛋白质组存在差异，从而证实了这些表型发现。值得注意的是，与ITB相比，在新出现的RJB蜜蜂和哺育蜂的ALs中，能量和营养代谢、信号转导过程上调，使ALs能够接收和处理来自触角的育雏信号。此外，与ITB相比，在神经系统仍在发育的早期生活中，RJB中大量丰富的主要蜂王浆蛋白和六聚蛋白表明这些特征明确的蛋白质具有重要的新神经生物学作用。总之，我们的研究结果表明，RJB已经进化出对幼虫的强烈嗅觉反应，这是由众多神经生理适应实现的，这些适应增加了哺育蜂的异亲照料行为。
