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 additional effects on light avoidance response and pupation site. 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.Author summaryMany animals occupy distinct niches and utilize diverse resources at different development stages in order to meet stage-dependent requirements and overcome stage-specific limitations. This fitness is referred to as ontogenetic niche shift (ONS). During the preparation for ONS, animals often change one or more primitive, instinctive behaviors. Holometabolous insects, with four discrete developmental periods usually in different niches, are a suitable animal group to explore the molecular modes of these behavioral switches. Here we find that Leptinotarsa decemlineata larvae, an insect defoliator of potatoes, switch their phototactic behavior, from photophilic at feeding period to photophobic during the larval-pupal transition (wandering stage). This phototactic switch facilitates the wandering larvae to accomplish the ONS from potato plant to their pupation site below ground. We show that JH/PTTH cascade controls the phototaxis switch, through a step in photo transduction between the photoreceptor molecule and the transient receptor potential cation channel.