Abstract

The existence of alternative phenotypes arising from a single genotype that are expressed according to environmental conditions is of considerable evolutionary significance, but the controlling mechanisms remain elusive. One major source of environmental variability is the presence and actions of conspecifics which in some species has driven the evolution of multiple phenotypes to adapt to changing population densities. Desert locusts, Schistocerca gregaria, display a striking example of just such a density-dependent phenotypic plasticity, changing reversibly between a little seen solitarious phase and the notorious swarming gregarious phase. The two phases differ extensively in morphology and physiology, but behaviour is the key to both establishing and maintaining phase. Solitarious locusts actively avoid other locusts whilst gregarious locusts form cohesive groups, but forced crowding of solitarious locusts for just a few hours leads to a rapid reorientation towards gregarious behaviour. How this rapid behavioural transition is mediated, however is unknown. We show that serotonin, an evolutionarily conserved mediator of neuronal plasticity, performs this function. Serotonin in the CNS is correlated with the degree of gregarious behaviour; preventing endogenous serotonin synthesis or blocking its action prevents behavioural gregarization and application of serotonin or receptor agonists drives its acquisition. Our findings suggest that serotonin is both necessary for gregarization to occur and sufficient to induce it. The initial switch to gregarious behaviour is an essential pivot point; once solitarious locusts have overcome their mutual aversion sensory positive feedback drives the acquisition of further gregarious phase characteristics and possible swarm formation. This study identifies a neurochemical mechanism for the initiation of swarming and demonstrates how density-dependent sensory cues can initiate phenotypic change.