Modulation of behavioral phase changes of the migratory locust by the catecholamine metabolic pathway

Abstract

The migratory locust, Locusta migratoria, shows a striking phenotypic plasticity. It transitions between solitary and gregarious phases in response to population density changes. However, the molecular mechanism underlying the phase-dependent behavior changes remains elusive. Here we report a genome-wide gene expression profiling of gregarious and solitary nymphs at each stadium of the migratory locust, and we identified the most differentially expressed genes in the fourth stadium of the two phases. Bioinformatics analysis indicated that the catecholamine metabolic pathway was the most significant pathway up-regulated in the gregarious phase. We found pale, henna, and vat1, involved in dopamine biosynthesis and synaptic release, were critical target genes related to behavioral phase changes in the locusts. The roles of these genes in mediating behavioral changes in the gregarious individuals were confirmed by RNAi and pharmacological intervention. A single injection of dopamine or its agonist initiated gregarious behavior. Moreover, continuous and multiple injections of a dopamine agonist coupled with crowding resulted in more pronounced gregarious behavior. Our study thus provides insights into the relationships between genes and behavior in phase transition of this important pest species.microarray | RNA interference | polyphenism P henotypic plasticity associated with locust phase polyphenism arises when extrinsic factors induce alternative phenotypes in individuals with the same genetic background (1). Solitary locusts usually live in an isolated state, with their cryptic body color blending well into the surroundings (2). Population density is a substantial source of extrinsic factors that leads to the reversible transformation between solitary and gregarious phases. Under high population density, migratory locusts (Locusta migratoria) form large, fast-flying swarms that wreak havoc on local vegetation (3, 4). Gregarious locusts have a distinctive orange body color with dark patterns as nymphs. In addition, they are attracted to one another and exhibit collective social behavior (2).Behavior is one of the most obvious traits to examine to evaluate the phase state of the migratory locust (1-6). Although the neuronal circuitry responsible for processing and integrating phase-shifting cues is not clear, several neurochemicals have been implicated (1). For instance, the biogenic amine serotonin was found to be necessary and sufficient for inducing gregarious behavior in the desert locust, Schistocerca gregaria (7).The first step in identifying the mechanisms underlying phenotypic plasticity in locusts is to understand how behavior is regulated. A void in our understanding of the mechanism of the phenomena is the interaction of gene expression and environment in regulating phase change of the migratory locust (1). Because of the inherent complexity associated with phase transition, the full complement of behavioral and physiological changes is underwritten by genetic and epigenetic factors (8,9). In previous st...

Critical role for protein kinase A in the acquisition of gregarious behavior in the desert locust

“…This indicates that, after induction, gregariousness is maintained by other means, echoing the transient role of 5-HT in classical forms of learning. Aminergic signaling has since been confirmed as central to behavioral phase change in the migratory locust (Locusta migratoria); in this insect, which is only distantly related to Schistocerca, 5-HT appears to act in synergy with dopamine (12).…”

“…Knowledge about the extensive differences in gene expression between the fully established phases has increased dramatically in recent years, but the molecular mechanisms that switch between the two extreme phenotypes have yet to be fully established (11)(12)(13). The discovery of a central role for the biogenic amine serotonin [5-hydroxytryptamine (5-HT)] in inducing behavioral gregarization (14) suggests parallels with mechanisms underlying classical forms of neuronal and behavioral plasticity (15).…”

Metabolomic analysis reveals that carnitines are key regulatory metabolites in phase transition of the locusts

“…The current study reports that a small group of intermediary metabolites appears to play a regulatory role in the expression of phase characteristics. It represents a mechanism of plasticity regulation, distinct from traditional regulators, such as developmental hormones (7) and biogenic amines (9).…”

“…Behavioral change has been regarded as a key step for the establishment of a positive-feedback loop that can drive an initially solitarious phase to the gregarious phase, which is triggered by multiple sensory inputs from other individuals (7). The neuromodulation of CNS circuits and the changes of olfactory sensitivity have been recently proposed to be involved in mediating the initiation of behavioral phase change (8)(9)(10). However, the process in which a set of varied phase traits are subsequently expressed during the development of locusts is not as well understood.…”

Exposure to static electric fields leads to changes in biogenic amine levels in the brains ofDrosophila

“…Taken together these results raise the question as to whether static electric fields could also alter the brain's neurochemistry in insects. Amines play a major role in the behaviour of insects, from underpinning extreme changes in phenotypic plasticity in locusts where dopamine and serotonin have a major role in driving the swarming form of migratory and desert locusts [16][17][18], to social interactions between nest-mates influencing brain biogenic amine homeostasis in stressed ants [19,20]. They also play a crucial role in aggressive encounters between dominant and submissive animals [21].…”