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

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. DOI: http://dx.doi.org/10.7554/eLife.22526.001

eLife digest Migratory locusts are widespread throughout the Eastern Hemisphere, especially in Asia, Australia and Africa. Although usually solitary insects, locusts can also form swarms made up of millions of individuals, which can devastate crops. Swarming can be studied on a smaller scale in the laboratory by forcing locusts to crowd together. This causes the locusts to enter a so-called gregarious state in which they are more active and sociable, which in turn promotes swarming. Isolating individual locusts has the opposite effect, causing the insects to enter a solitary state in which they are less active. Chemicals in the locust brain called neuropeptides control phase transitions between solitary and gregarious behavior. Neuropeptides bind to specific proteins called receptors in the outer membranes of neurons and initiate unique signaling cascades inside cells. However, exactly how neuropeptides regulate the changes in locust behavior that affect swarming was not clear. Hou et al. now reveal the role that two related neuropeptides, NPF1a and NPF2, play in this process. Crowding causes the levels of NPF1a and NPF2 in the locust brain to decrease, whereas isolating individual locusts causes the levels of two NPF receptors to increase. Both neuropeptides reduce levels of a molecule called nitric oxide in the brain. NPF1a does this by reducing the activity of the enzyme that produces nitric oxide, whereas NPF2 reduces the production of this enzyme. The reduction in nitric oxide in turn makes the locusts less active. Similar NPF neuropeptides had previously been shown to affect activity levels in other invertebrates, such as roundworms and fruit flies. This, combined with the results now presented by Hou et al., suggests that the NPF/nitric oxide pathway may regulate activity in insects in general. Future work should investigate this possibility, as well as whether the NPF/nitric oxide pathway controls changes in other insect behaviors such as feeding and mating. DOI: http://dx.doi.org/10.7554/eLife.22526.002