The neuropeptide F/nitric oxide pathway is essential for shaping locomotor plasticity underlying locust phase transition.

Li Hou,Xianhui Wang,Feng Jiang,Le Kang,Qing Liu,Pengcheng Yang

doi:10.7554/elife.22526

Abstract

Behavioral plasticity is widespread in swarming animals, but little is known about its underlying neural and molecular mechanisms. Here, we report that a neuropeptide F (NPF)/nitric oxide (NO) pathway plays a critical role in the locomotor plasticity of swarming migratory locusts. The transcripts encoding two related neuropeptides, NPF1a and NPF2, show reduced levels during crowding, and the transcript levels of NPF1a and NPF2 receptors significantly increase during locust isolation. Both NPF1a and NPF2 have suppressive effects on phase-related locomotor activity. A key downstream mediator for both NPFs is nitric oxide synthase (NOS), which regulates phase-related locomotor activity by controlling NO synthesis in the locust brain. Mechanistically, NPF1a and NPF2 modify NOS activity by separately suppressing its phosphorylation and by lowering its transcript level, effects that are mediated by their respective receptors. Our results uncover a hierarchical neurochemical mechanism underlying behavioral plasticity in the swarming locust and provide insights into the NPF/NO axis.

Highlights

Swarming occurs in a wide variety of animal taxa, including insects, fish, birds, and mammals
We extend our work to explore which of these neuropeptides are closely tied to the behavioral phase transition. qPCR analysis (Figure 1 and Figure 1—figure supplement 1) revealed that the mRNA levels of four neuropeptide encoding genes, namely, AKH/Corazonin related peptide (ACP), Insulin-like peptide (ILP), NPF1a, and NPF2, significantly changed in the phase transition, that is, during solitarization or gregarization or both
The transcript levels of ILP and NPF1a significantly changed compared to those of ACP and NPF2. To assess whether these four neuropeptides are involved in the behavioral phase transition, we performed a behavioral screen in the gregarious phase (G-phase) locusts using transcript knockdown or peptide mRNA level

Summary

Introduction

Swarming occurs in a wide variety of animal taxa, including insects, fish, birds, and mammals. Accumulating evidence shows that neuropeptides serve as conserved neuronal signals that modulate animal behaviors in social contexts (Lieberwirth and Wang, 2014; Nilsen et al, 2011). These peptides exert their actions by binding to specific membrane receptors, most of which are G-protein-coupled receptors (Quartara and Maggi, 1997). It has been revealed that neuropeptides can induce plasticity in a series of behavioral processes, including sensory detection (Shankar et al, 2015), signal integration (Grammatopoulos, 2012), and behavioral

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Conclusion