Abstract

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.

Highlights

  • Movements to stage-dependent resources, i.e., ontogenetic niche shifts, occur in nearly 80% of animal taxa

  • We show that juvenile hormone (JH)/prothoracicotropic hormone (PTTH) cascade controls the phototaxis switch, through a step in photo transduction between the photoreceptor molecule and the transient receptor potential cation channel

  • We examined the relative mRNA levels of a JH biosynthesis gene LdJHAMT and two JH signaling pathway genes (LdMet and LdKr-h1), and found that the levels of these genes varied little in LdPTTH or LdTorso RNA interference (RNAi) larvae when measured 1 and 2 days post ecdysis to fourth-instar larvae (S4G and S5Q–S5S Figs)

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Summary

Introduction

Movements to stage-dependent resources, i.e., ontogenetic niche shifts (hereafter ONS), occur in nearly 80% of animal taxa. Sessile pupae are vulnerable to potentially harmful factors such as desiccation, predation, parasitism and pathogen infection. These latent mortal dangers drive a lot of Holometabolans shifting into less risky habitats for pupation [8,9,10,11,12]. For other dsRNA feeding bioassays, the newly-ecdysed third-instar larvae were used. The larvae were allowed to feed treated foliage for 3 days (replaced with freshly treated ones each day), and were transferred to untreated foliage if necessary

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