Hormonal signaling cascades required for phototaxis switch in wandering Leptinotarsa decemlineata larvae

Many animals exploit several niches sequentially during their life cycles, a fitness referred to as ontogenetic niche shift (ONS). To successfully accomplish ONS, transition between development stages is often coupled with changes in one or more primitive, instinctive behaviors. Yet, the underlining molecular mechanisms remain elusive. We show here that Leptinotarsa decemlineata larvae finish their ONS at the wandering stage by leaving the plant and pupating in soil. At middle wandering phase, larvae also switch their phototactic behavior, from photophilic at foraging period to photophobic. We find that enhancement of juvenile hormone (JH) signal delays the phototactic switch, and vise verse. Moreover, RNA interference (RNAi)-aided knockdown of LdPTTH (prothoracicotropic hormone gene) or LdTorso (PTTH receptor gene) impairs avoidance response to light, a phenotype nonrescuable by 20-hydroxyecdysone. Consequently, the RNAi beetles pupate at the soil surface or in shallow layer of soil, with most of them failing to construct pupation chambers. Furthermore, a combination of depletion of LdPTTH/LdTorso and disturbance of JH signal causes no additive effects on light avoidance response and pupation site selection. Finally, we establish that TrpA1 (transient receptor potential (TRP) cation channel) is necessary for light avoidance behavior, acting downstream of PTTH. We conclude that JH/PTTH cascade concomitantly regulates metamorphosis and the phototaxis switch, to drive ONS of the wandering beetles from plant into soil to start the immobile pupal stage.许多动物在生命周期中会依次利用多个生态位，这种适合度相关特征被称为个体发育生态位转移（ontogenetic niche shift, ONS）。为顺利完成个体发育生态位转移，不同发育阶段间的转变通常伴随一种或多种先天本能行为的改变。然而，其背后的分子机制仍有待阐明。本研究显示，马铃薯甲虫（Leptinotarsa decemlineata）的幼虫会在漫游期通过离开寄主植物、入土化蛹来完成其个体发育生态位转移。在漫游中期，幼虫的趋光行为也发生转变：取食阶段的趋光性变为避光性。研究发现，增强保幼激素（juvenile hormone, JH）信号会延缓该趋光行为的转变，反之则会加速这一过程。此外，通过RNA干扰（RNA interference, RNAi）技术敲低马铃薯甲虫的LdPTTH（促前胸腺激素基因）或LdTorso（PTTH受体基因），会损害其避光反应，且该表型无法被20-羟基蜕皮酮（20-hydroxyecdysone）挽救。受RNA干扰的甲虫会在土壤表面或浅层土壤中化蛹，多数个体无法构建蛹室。进一步研究发现，同时敲低LdPTTH/LdTorso与干扰JH信号，对避光反应和化蛹位点选择无叠加效应。最后，我们证实TrpA1（瞬时受体电位（TRP）阳离子通道）是避光行为所必需的，其作用于PTTH的下游通路。综上，JH/PTTH信号通路协同调控变态发育与趋光性转变，驱动漫游期甲虫从寄主植物转移至土壤中，启动静止的蛹期发育阶段。