Abstract

Phenotypic plasticity allows animals to modify their behavior, physiology, and morphology to adapt to environmental change. The global pest, the desert locust, shows two extreme phenotypes; a solitarious phase that is relatively harmless and a gregarious phase that forms swarms and causes extensive agricultural and economic damage. In the field, environmental conditions can drive isolated animals into crowded populations and previous studies have identified the biogenic amine serotonin as a key determinant of this transition. Here we take an integrated approach to investigate the neurochemical, physiological, and behavioral correlates defined by a laboratory based paradigm that mimics facets of swarm break down as gregarious locusts become isolated. Following isolation there was an increased propensity of locusts to avoid conspecifics, and show a reduced locomotion. Changes in choice behavior occurred within 1 h of isolation although isolation-related changes progressed with increased isolation time. Isolation was accompanied by changes in the levels of the biogenic amines dopamine, octopamine, and serotonin within the CNS within 1 h. Dopamine levels were higher in isolated animals and we focused on the role played by this transmitter in synaptic changes that may underpin solitarization. Dopamine reduced synaptic efficacy at a key central synapse between campaniform sensilla (CS) and a fast extensor tibiae motor neuron that is involved in limb movement. We also show that dopamine injection into the haemocoel was sufficient to induce solitarious-like behavior in otherwise gregarious locusts. Further, injection of a dopamine antagonist, fluphenazine, into isolated locusts induced gregarious-like behavior. This highlights that dopaminergic modulation plays an important role in the plasticity underpinning phase transition and sets a context to deepen the understanding of the complementary role that distinct neuromodulators play in polyphenism in locusts.

Highlights

  • The phenotype of an animal can be influenced and modified by cues in the external environment

  • Results showed that both groups covered approximately the same distance from the release chamber to the stimulus cage suggesting there was no significant difference in the sinuosity of their walking paths, with gregarious locusts covering 211 ± 10 mm and isolated locusts covering 234 ± 20 mm (Students T-test, P = 0.58, n = 13 gregarious and n = 11 isolated locusts)

  • These differences in walking velocity reflect the times the two groups took to cross the arena with gregarious locusts reaching the end line in significantly shorter times of 42.5 ± 11.2 s compared to 120.8 ± 28 s in isolated animals (Figure 1G)

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Summary

Introduction

The phenotype of an animal can be influenced and modified by cues in the external environment. At low population densities locusts avoid contact with conspecifics, are cryptic in appearance, fly mainly at night and do not swarm (Uvarov, 1977). They are green or brown as nymphs and pale yellow when mature. Locusts in the gregarious phase actively group together, are yellow and black as nymphs, but bright yellow as adults (Uvarov, 1977) In this phase the locusts are highly active and fly during the day and can cause immense agricultural and economic damage by their voracious feeding on crops (Bullen, 1966)

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